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. 2025 Jun 21;309(5):1422–1432. doi: 10.1002/ar.70008

A proximodistal gradient in bone structure and mechanics in the wings of Seba's short‐tailed bat, Carollia perspicillata

Xiaoxiang Ma 1, Aowen Deng 2, Sabah Nobakhti 2, Sharon Swartz 3, Sandra J Shefelbine 1,2,✉
PMCID: PMC13047950  PMID: 40542556

Abstract

Bats possess the remarkable ability to fly, and with this, distinctive wing bone properties. We investigated the structural, mechanical, and compositional properties of the humerus, radius, metacarpals, and proximal and middle phalanges of Carollia perspicillata, an approximately 15 g fruit‐eating bat native to the Neotropics. We used microcomputed tomography (micro‐CT) to assess cross‐sectional properties (cross‐sectional area, second moment of area, circularity index), quantitative backscattered scanning electron microscopy (SEM) to assess mineral density in longitudinal sections, and nanoindentation to determine the elastic modulus along the length of each bone. Our findings revealed proximal to distal structural, mechanical, and mineral density gradients along the length of the wing. Proximal bones possessed larger cross‐sectional area, second moment of area, mineral density, and elastic modulus than distal bones. Proximal bones were more circular in cross‐section than the more elliptical distal bones, suggesting adaptation to torsional loading around the long axis and bending loading perpendicular to the long axis, respectively. This morphological and material properties gradient is linked to the bat's flight capabilities, reducing inertia and increasing ductility of the distal wing.

Keywords: bat, bone density, mechanics, structure, wing

1. INTRODUCTION

Bats, Order Chiroptera, comprise a minimum of 21 discernible family lineages (Simmons & Cirranello, 2023). The ancestors of bats were likely diminutive, arboreal, nocturnal insectivores (Gunnell & Simmons, 2005) but the ultimate placement of bats among eutherian mammals remains unclear (Zachos, 2020). Virtually all aspects of the morphology of the bat postcranial skeleton differ from those of their terrestrial, quadrupedal relatives, and many specializations of the bat limb skeleton are critical determinants of their flight capabilities (Norberg & Rayner, 1987; Panyutina et al., 2015; Swartz & Middleton, 2008; Vaughan, 1970).

The bone structure of bats serves as a compelling illustration of how natural selection can adapt anatomy to facilitate unique forms of locomotion, particularly flight. Bat wings exhibit a high degree of articulation, featuring numerous independent joints, in contrast to the fused digits found in birds and the single joint of the insect wing (Lindhe Norberg, 1990; Riskin et al., 2008). Pterosaur wings possessed more joints than those of other flying animals (Paul, 2022; Tokita, 2015; Unwin & Bakhurina, 1994; Wang et al., 2019), yet it is the three‐dimensional complexity of bat wing architecture that is distinctive in the biological world (Fan et al., 2022). The number of articulations varies across bat species and is dependent on feeding ecology (frugivore or insectivore) and the trade‐offs between maneuverability and energy efficiency (Bahlman et al., 2016). The bones of the wing, particularly those of the hand, are greatly elongated, and the structure of joints limits shoulder, elbow, and wrist motions compared to the full range of motion possible at the homologous joints in other mammals (Gaudioso et al., 2023; Norberg, 1972b; Swartz & Middleton, 2008; Vaughan, 1959, 1970). The wing bones are intricately integrated into the thin and specialized wing membrane skin, the patagium (Swartz et al., 1996). In many bat species, the patagium also integrates with the legs, tail, and basicranium. The elongation of wing bones, particularly the radius and metacarpals III, IV, and V, plays a crucial role in providing surface area for the wing membrane, allowing the digits to effectively stretch the membrane—an essential prerequisite for functional flight (Norberg, 1972b; Sears et al., 2006; Vaughan, 1959). The wing skeleton exhibits some traits that enhance rigidity and others that enhance flexibility (Cleland et al., 2021; Norberg, 1969; Swartz, 1997).

Beyond extreme elongation, numerous mechanical characteristics of the bat limb skeleton are influenced by the mechanics of flight. Reduction of skeletal weight and proximal concentration of the mass of the wing allow bats to maneuver with agility (Lindhe Norberg, 1990; Norberg, 1972a). The digits account for approximately 10% of the wing mass but nearly 50% of the inertial cost of flight because of their distance from the shoulder joint. The amount of mineral in the bone, determined by ash content, decreases from proximal to distal wing bones, which mitigates inertial costs of the wingbeat cycle because mass located close to the wing's center of rotation reduces inertia (Papadimitriou et al., 1996; Riskin et al., 2012; Swartz & Middleton, 2008). The geometric and mineral adaptations in bat wing bones reduce the mass moment of inertia of the distal bones, thereby reducing the energetic/inertial cost of moving the wing (Swartz, 1997).

In addition to contending with inertial costs, the humerus and radius are subjected to significant torsion during flight (Swartz et al., 1992). A large outer diameter of the cortical bone contributes to the capacity to withstand larger torques while minimizing mass. The distal bones exhibit smaller diameters and cross‐sectional areas. This pattern suggests a potential proximal–distal gradient in cross‐sectional area (Norberg, 1972b; Swartz, 1997; Swartz et al., 1992). Similarly, in each bone, the distal epiphyses are slightly narrower than the proximal epiphyses (López‐Aguirre et al., 2021; Swartz et al., 1996; Vaughan, 1959).

In this study, we aimed to determine the detailed proximal‐distal structural and material properties along the wing in one bat species, Carollia perspicillata, Seba's short‐tailed fruit bat. We used micro‐CT to assess cross‐sectional properties along the length of the bones, nanoindentation to determine elastic modulus, and quantitative backscattered electron microscopy to determine mineral density. We hypothesized that both structural (cross‐sectional area and second moment of area) and material properties (density and modulus) would decrease within a bone as well as among bones from proximal to distal.

2. MATERIALS AND METHODS

2.1. Samples

We analyzed the humerus, radius, metacarpal III, IV, and V, the proximal phalanx III and IV, and the middle phalanx III of six C. perspicillata. We selected this species for study because its flight is well‐studied (Boerma et al., 2019; Carneiro et al., 2023; Konow et al., 2015, 2017; Rummel et al., 2019; Von Busse et al., 2013, 2014), and we were able to obtain multiple skeletons for destructive sampling (Figure 1). All bats were fresh‐frozen specimens of nonlactating adults that had been housed at the Brown Center for Animal Research and Education for other studies; use and care procedures were approved by the Brown University IACUC (Protocol 1603000199).

FIGURE 1.

FIGURE 1

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The wing skeleton of the bat consists of the humerus, radius, a remnant ulna (not studied in this work), and elongated metacarpals and phalanges. Scaled three‐dimensional micro‐CT scans of each bone are shown next to the wing schematic with sample size and the mean length indicated. Unmineralized distal phalanges are not shown.

2.2. Micro‐CT

Bones were imaged with microcomputed tomography (micro‐CT) (SCANCO Medical μCT 35) at an isotropic voxel size of 10 μm using an X‐ray source power of 70 kVp, an aluminum filter of 0.5 mm, an X‐ray intensity of 114 μA and an integration time of 400 ms per slice. Cortical bone was segmented using ImageJ to remove noise, with a threshold applied to isolate the mineralized bone. The threshold varied based on each image's brightness and was determined in combination with visual inspection. On average, the threshold was around 42,500 out of a possible 65,535.

Structural properties of the cortical bone (cross‐sectional area, maximum and minimum second moment of area, I min and I max) were evaluated in cross‐sections perpendicular to the long axis every 10 μm along the length of each bone. For each bone, we determined the circularity along the middle 60% of the bone's diaphysis, excluding epiphyses. The circularity index was calculated as I min/I max, where a value of one indicates a circular cross‐section and less than one indicates an elliptical shape. We also measured mean cortical thickness in each cross‐section along the diaphyseal length. The very small marrow cavity of the middle phalanx made it challenging to detect cortical thickness. This value was not reported.

2.3. Quantitative backscatter scanning electron microscopy (SEM)

We used quantitative backscattered scanning electron microscopy (qbSEM) to determine mineral density. Calcium has the highest atomic number (Z = 20) among the constitutive elements of bone; thus, the backscattered signal in a qbSEM image reflects the bone's Ca concentration (Roschger et al., 1998).

One specimen of each bone type was processed for qbSEM. The samples were progressively dehydrated with increasing concentrations of ethanol: 70% (48 h), 80% (24 h), 90% (24 h), and 100% (72 h). Samples were then immersed in xylene (Thermo Fischer Scientific, MA) for 24 h and then in destabilized methyl methacrylate monomer (MMA, Sigma‐Aldrich, MO) for 48 h. Each sample was placed in a glass vial filled with PMMA and 2% benzoyl peroxide (Sigma‐Aldrich, MO, US), infiltrated for 48 h, and allowed to polymerize for 10 days at room temperature. After solidification, glass vials were broken to access the blocks of PMMA containing the bone.

Blocks containing specimens were sectioned parallel to the bones' longitudinal axes using a low‐speed saw (IsoMet 1000 Precision Saw, Buehler, Braunschweig, Germany) equipped with a 500‐micronthick diamond blade (Buehler, Braunschweig, Germany). The longitudinal surface of each sample was polished with successively finer grades of alumina powder (1, 0.3, and 0.05 mm) and cleaned using an ultrasound bath between the polishing steps.

To eliminate electron charging, samples were coated with carbon and connected to the edge of the sample holder at three locations with carbon adhesive. Specimens were imaged at 20 kV accelerating voltage, with saturated filament current and 1.5 nA probe current measured with a Faraday cup, at a working distance of 12 mm. Magnification settings, store resolution, and scan speed were consistent among imaging sessions. qbSEM presents mineral density values in grayscale images in the range of 0–255 gray level numbers. To calibrate the backscatter signal across multiple imaging sessions, we used a calibration phantom of carbon (Z = 6) and aluminum (Z = 13) (Micro‐Analysis, Huntingdon, UK). Reproducibility was confirmed by scanning the same sample in multiple imaging sessions and demonstrating the same degree of mineralization. Consistent imaging and calibration with phantom standards allowed for quantitative comparison of backscattered intensities. To increase the dynamic range of the bone mineralization measurements at different parts of the specimen, we adopted brightness and contrast values that set the gray level number of carbon and aluminum as close as possible to 25 and 225, respectively (Roschger et al., 2003).

2.4. Nanoindentation

Longitudinally sectioned bones (n = 1/bone type) were repolished and tested by nanoindentation to determine variation in material properties along the length of each bone. We used the Oliver‐Pharr method with a Berkovich tip to determine elastic modulus. The Oliver‐Pharr method assumes the unloading curve is purely elastic, which is not met for bone, resulting in overestimates of modulus (Ngan et al., 2005). Regardless, the use of the Berkovich tip and the Oliver‐Pharr method has been widely adopted in bone nanoindentation experiments (Faingold et al., 2012; Franzoso & Zysset, 2009; Spiesz et al., 2013; Tai et al., 2007), and we follow this approach, particularly because the relative moduli along the wing are more important to this analysis than absolute moduli values.

Nanoindentation was performed with the NanoForce indentation system (Bruker, MA, US). The dynamic test module allowed for continuous characterization of mechanical properties as a function of the indentation depth. In this configuration, the indenter was moved at a constant displacement rate 0.1 s−1 with a small oscillation (~2 nm amplitude at 100 Hz) superimposed on top of that movement. Each point was indented to 400 nm, and contact stiffness was determined at a depth of 350 nm. We performed a series of indents perpendicular to the long axis of the bone at a spacing 20 μm. Indents in PMMA were discarded, resulting in 5–15 indents in bone in each series, depending on the thickness of the cortex. Lines of indentations were 4 mm apart down the length of the bone.

We report the results of the indentation tests as a reduced modulus:

ER=Sπ2βAc

where S was the slope of the unloading curve, A c was the contact area (~24.5 hc2, h c  = contact depth) (Fischer‐Cripps, 2004) and b is a correction parameter 1.034 for the Berkovich tip. The material modulus (E s ) was then calculated by:

Es≈ER1−υs2

We assume Poisson's ratio, 𝜈s, to be 0.3 for bone (Rodriguez‐Florez et al., 2013).

3. RESULTS

3.1. Micro‐CT

The cross‐sectional area decreased within each bone and among bones from proximal to distal (Figure 2). The cross‐sectional areas of the epiphyses were larger than those of the diaphysis. The proximal epiphysis was larger in cross‐sectional area than the distal epiphysis, except for the radius, in which the distal epiphysis was larger than the proximal epiphysis.

FIGURE 2.

FIGURE 2

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CSA vs. length (%) from the humerus to middle phalanx III. Cross‐sectional area decreased from proximal to distal. Each line is a distinct specimen.

The cross‐sectional area of metacarpal III is 30% greater than that of metacarpal IV and V. Proximal phalanx III had approximately 40% greater cross‐sectional area than proximal phalanx IV (Figure 3).

FIGURE 3.

FIGURE 3

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(a) Metacarpal III, IV, and V CSA vs. % length. Metacarpal III has a larger cross‐sectional area. (b) Proximal phalanx III and IV CSA vs. % length. Proximal phalanx III has a larger CSA. Each line indicates a distinct specimen.

The second moment of area quantifies how area is distributed in a cross‐section perpendicular to the long axis. It is calculated around an axis within the cross‐section. Here we calculate the maximum second moment of area. I max decreases from proximal to distal (Figure 4).

FIGURE 4.

FIGURE 4

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(a) The maximum second moment of area is (I max) is a measure of the bones' geometric resistance to bending. (a) Imax vs. length (%) from proximal humerus to distal middle phalanx III. Each line indicates a distinct specimen. (b) The inset indicates the same data with the y‐axis adjusted so that the small moment of area is visible.

To assess bone circularity, we computed the ratio I min:I max along the length of the bone. Our analysis revealed a general decrease in circularity from the humerus to the third phalanx (Figure 5 and Figure S5).

FIGURE 5.

FIGURE 5

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Circularity from proximal humerus to distal middle phalanx III of the diaphysis (20%–80% length) for bones from four individuals. (Figure S5 has more cross sections of middle phalanx III.)

Mean cortical thickness was similar among bones in the bat wing, around 0.25 mm (Figure 6).

FIGURE 6.

FIGURE 6

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Mean thickness of the diaphysis (20%–80% length) from proximal humerus to distal proximal phalanx III. The cortical thickness of the diaphysis was constant (0.25 mm) across all bones.

3.2. qbSEM

The mineral density level, given by the mode of the histogram of gray values, decreased along the length of the bone (Figure 7). In most bones, the epiphyseal regions had lower mineral density than the diaphyseal regions.

FIGURE 7.

FIGURE 7

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Mode of the mineral density along the length of the bone. Longitudinal sections are shown with color plot of gray level (Figure S6 has enlargements of the color plots.)

3.3. Nanoindentation

Each line of indents (perpendicular to the long axis of the bone) yielded 5–10 bone indents (Figure 8). The variability within a line of indents at a particular cross section was ~10 GPa, reflecting the heterogeneous nature of the bone tissue. Despite the variability, the mean modulus decreased down the length of the wing, within and among bones.

FIGURE 8.

FIGURE 8

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Modulus vs. length (%) from proximal humerus to distal middle phalanx III.

4. DISCUSSION

We found a gradient in structural, material, and mechanical properties along the length of the bat wing bones. In this study, we found consistency across samples, although we analyzed only four bat wings. For the high‐resolution techniques (qbSEM and nanoindentation), we analyzed bones of a single representative wing and examined variation within and among bones, which we considered more important than variation between individuals. We found a decrease in cross‐sectional area and maximum second moment of area (I max) from proximal to distal within each bone as well as across bones from proximal to distal. These results are consistent with those of previous caliper‐based studies that found a proximal to distal decrease in diaphysis diameters among and within bat wing bones (Swartz, 1997; Vaughan, 1959). Compared to external morphometrics, micro‐CT achieves high spatial resolution and captures both internal and external structures. Measures of cross‐sectional area, second moment of area, circularity, and thickness rely on internal dimensions that cannot be assessed with measurements only on the external surface. Particularly when minimizing weight while maximizing strength, for example, to resist bending or torsional loads during flight, the arrangement of material around the axis of bending or torsion is critical. Micro‐CT provides the ability to assess the amount and distribution of bone.

Circularity demonstrated a decreasing trend from the proximal to distal end of the bone, from a fairly circular humerus diaphysis (circularity index = 0.9) to the elliptical phalanx (circularity index = 0.4). Because bones adapt to mechanical loading, we expect bones with torsional loads to have circular cross sections; the magnitude of torsional stresses is equivalent around the circumference of a beam‐like bone, resulting in evenly distributed periosteal bone formation. Our data indicate that the proximal bones are more circular than the distal, indicating torsional loading around the long axis of the bone in the proximal bones and bending loading perpendicular to the long axis in the distal bones, as has been hypothesized previously (López‐Aguirre et al., 2021; Swartz et al., 1997; Vaughan, 1959). The ginglymoid motion of the distal joints also suggests motions that cause bending.

It is interesting that all bones of the wing had a similar cortical thickness of 0.2–0.3 mm. The diffusion of nutrients in bone is limited to approximately 0.23 mm from a blood supply (Lozupone & Favia, 1990). This diffusion limit is thought to influence the size of osteons (Felder et al., 2017; Lozupone & Favia, 1990) and size of trabeculae (Doube et al., 2011). In larger species blood vessels at the center of osteons, called Haversian canals, provide nutrients to the osteocytes within the osteon. In smaller species, such as mice, the cortical bone does not have osteons because osteocytes in the thin cortical bone can receive nutrients from the medullary canal and the periosteum. A cortical bone thickness of 0.25 mm in C. perspicillata implies no need for an osteonal structure. It has also been suggested that osteons are typically not found in bones in which the cortical thickness does not permit osteonal remodeling without significantly compromising the structure, typically in animals less than 2 kg (Felder et al., 2017). Previous studies have shown that most small bat species do not have osteons (Hieronymus et al., 2024; Lee & Simons, 2015; Skedros & Doutré, 2019).

We used qbSEM to evaluate the mineral density within a bat wing bone. Unlike ashing, which provides a bulk measure of mineral content of a bone, qbSEM maps spatial variations in mineralization, allowing assessment of regional differences within individual bones. For example, we demonstrate higher mineral density in the midshaft of the radius compared to the proximal and distal ends of the bone. This regional change would not be evidenced by ashing the entire bone. Similar to previous studies that used ashing (Papadimitriou et al., 1996) or micro‐CT (Cleland et al., 2021), we found that mineral density decreased from proximal to distal in the wing. This reduction in mineralization reduces the mass of the distal bones and increases flexibility of the bone (Currey, 1988, 2013, 2014). This could not only aid in flight but also increase ductility of the distal wing to protect from fractures.

We used nanoindentation to assess the elastic modulus of the bones. Nanoindentation allows probing small regions of bone and can determine heterogeneities in material properties. We found a decreasing elastic modulus from the proximal to the distal end of the wing bones. Not surprisingly, this trend is similar to the patterns of mineralization. Previous studies have assessed bulk (whole‐bone) stiffness with mechanical testing and also found lower stiffness in the distal bones (Norberg, 1969). Studies using Vicker's hardness test (4 indents/bone) also found a decrease in modulus from proximal bones to distal (Cleland et al., 2021). Our values for modulus are considerably larger (35–15 GPa) than those found by Cleland (17–5.5 GPa), which is likely due to the preparation of the sample, testing protocol, and analysis method, as we have shown previously (Rodriguez‐Florez et al., 2013).

In this study, the analysis of bone properties consistently revealed a proximal‐distal gradient, which results in a flexible yet resilient structure at the wing's distal end. Future work will examine the mineralization of the wing during development and differences among species with known differences in flight ecology.

AUTHOR CONTRIBUTIONS

Xiaoxiang Ma: Writing – original draft; writing – review and editing; visualization; data curation. Aowen Deng: Methodology; investigation; formal analysis. Sabah Nobakhti: Methodology. Sharon Swartz: Conceptualization; writing – review and editing; supervision; resources. Sandra J. Shefelbine: Conceptualization; investigation; writing – review and editing; methodology; project administration; data curation; supervision; resources.

FUNDING INFORMATION

All materials and time were donated to this project. There were no external funds used.

CONFLICT OF INTEREST STATEMENT

Authors have no conflict of interest.

Supporting information

Figure S1.–S6.

AR-309-1422-s001.pdf (1.7MB, pdf)

ACKNOWLEDGMENTS

We thank Dr. Sandip Banu for his assistance in the nanoindentation of the bat bones.

DATA AVAILABILITY STATEMENT

Data including micro‐CT scans and nanoindentation data can be found on the data repository site: https://hdl.handle.net/2047/D20710532.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Figure S1.–S6.

AR-309-1422-s001.pdf (1.7MB, pdf)

Data Availability Statement

Data including micro‐CT scans and nanoindentation data can be found on the data repository site: https://hdl.handle.net/2047/D20710532.

Articles from Anatomical Record (Hoboken, N.j. : 2007) are provided here courtesy of Wiley

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