Limits...
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

Interspecific scaling of mass-specific field metabolic rate (FMR) in bats and birds.Bat and bird data points are omitted for clarity. Shaded regions are 95% confidence bands. Representative views of histology from avian ((A) Phalaenoptilus nuttallii, (B) Nothura darwinii, (C) Tinamus major) and chiropteran ((D) Phyllostomus discolor, (E) Rousettus leschenaultii, (F) Pteropus vampyrus) humeri suggest that the vascular dichotomy between bats and birds is not related to mass-specific FMR.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4359045&req=5

fig-4: Interspecific scaling of mass-specific field metabolic rate (FMR) in bats and birds.Bat and bird data points are omitted for clarity. Shaded regions are 95% confidence bands. Representative views of histology from avian ((A) Phalaenoptilus nuttallii, (B) Nothura darwinii, (C) Tinamus major) and chiropteran ((D) Phyllostomus discolor, (E) Rousettus leschenaultii, (F) Pteropus vampyrus) humeri suggest that the vascular dichotomy between bats and birds is not related to mass-specific FMR.

Mentions: Across amniotes, maximum somatic growth rates (Case, 1978) and field metabolic rates (Nagy, 2005) are strongly dependent on body mass. Consequently, the increased bone vascularity in large-bodied bats compared to small-bodied bats may reflect rapid somatic growth rate, elevated field metabolic rate, or large size. When the confounding influence of size on somatic growth and field metabolic rate is accounted for (i.e., a relative growth rate and mass-specific field metabolic rate, respectively), large-bodied bats have relatively low growth and field metabolic rates compared to small-bodied ones (Figs. 4 and 5). In both growth and metabolic datasets, significant negative scaling trends are revealed by OLS and PGLS regressions (Tables 2 and 3). Moreover, scaling relationships recovered by OLS and PGLS regressions in the growth and metabolic datasets, respectively, are statistically indistinguishable. Consilience from several models of evolution suggests that neither growth rate nor field metabolic rate alone explains the increased bone vascularity (humerus or otherwise) in large-bodied bats. Instead, there appears to be a threshold of adult size at ∼100–200 g above which bats show vascularized humeri (Fig. 2F), radii (Bennett & Forwood, 2010) and femora (Foote, 1916). Other clades of amniotes also show a size threshold in bone vascularity, although the precise threshold varies with the clade (de Margerie et al., 2005; de Buffrénil, Houssaye & Böhme, 2008; Werning, 2013). Large size in bats and other amniotes may necessitate vascularized cortical bone to provide additional capacity for nutrient and waste exchange beyond that supplied by canaliculi (de Ricqlès et al., 1991).


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

Lee AH, Simons EL - PeerJ (2015)

Interspecific scaling of mass-specific field metabolic rate (FMR) in bats and birds.Bat and bird data points are omitted for clarity. Shaded regions are 95% confidence bands. Representative views of histology from avian ((A) Phalaenoptilus nuttallii, (B) Nothura darwinii, (C) Tinamus major) and chiropteran ((D) Phyllostomus discolor, (E) Rousettus leschenaultii, (F) Pteropus vampyrus) humeri suggest that the vascular dichotomy between bats and birds is not related to mass-specific FMR.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-4: Interspecific scaling of mass-specific field metabolic rate (FMR) in bats and birds.Bat and bird data points are omitted for clarity. Shaded regions are 95% confidence bands. Representative views of histology from avian ((A) Phalaenoptilus nuttallii, (B) Nothura darwinii, (C) Tinamus major) and chiropteran ((D) Phyllostomus discolor, (E) Rousettus leschenaultii, (F) Pteropus vampyrus) humeri suggest that the vascular dichotomy between bats and birds is not related to mass-specific FMR.
Mentions: Across amniotes, maximum somatic growth rates (Case, 1978) and field metabolic rates (Nagy, 2005) are strongly dependent on body mass. Consequently, the increased bone vascularity in large-bodied bats compared to small-bodied bats may reflect rapid somatic growth rate, elevated field metabolic rate, or large size. When the confounding influence of size on somatic growth and field metabolic rate is accounted for (i.e., a relative growth rate and mass-specific field metabolic rate, respectively), large-bodied bats have relatively low growth and field metabolic rates compared to small-bodied ones (Figs. 4 and 5). In both growth and metabolic datasets, significant negative scaling trends are revealed by OLS and PGLS regressions (Tables 2 and 3). Moreover, scaling relationships recovered by OLS and PGLS regressions in the growth and metabolic datasets, respectively, are statistically indistinguishable. Consilience from several models of evolution suggests that neither growth rate nor field metabolic rate alone explains the increased bone vascularity (humerus or otherwise) in large-bodied bats. Instead, there appears to be a threshold of adult size at ∼100–200 g above which bats show vascularized humeri (Fig. 2F), radii (Bennett & Forwood, 2010) and femora (Foote, 1916). Other clades of amniotes also show a size threshold in bone vascularity, although the precise threshold varies with the clade (de Margerie et al., 2005; de Buffrénil, Houssaye & Böhme, 2008; Werning, 2013). Large size in bats and other amniotes may necessitate vascularized cortical bone to provide additional capacity for nutrient and waste exchange beyond that supplied by canaliculi (de Ricqlès et al., 1991).

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