Royal Society Publishing

Hierarchical multiscale structure–property relationships of the red-bellied woodpecker (Melanerpes carolinus) beak

Nayeon Lee, M. F. Horstemeyer, Hongjoo Rhee, Ben Nabors, Jun Liao, Lakiesha N. Williams

Abstract

We experimentally studied beaks of the red-bellied woodpecker to elucidate the hierarchical multiscale structure–property relationships. At the macroscale, the beak comprises three structural layers: an outer rhamphotheca layer (keratin sheath), a middle foam layer and an inner bony layer. The area fraction of each layer changes along the length of the beak giving rise to a varying constitutive behaviour similar to functionally graded materials. At the microscale, the rhamphotheca comprises keratin scales that are placed in an overlapping pattern; the middle foam layer has a porous structure; and the bony layer has a big centre cavity. At the nanoscale, a wavy gap between the keratin scales similar to a suture line was evidenced in the rhamphotheca; the middle foam layer joins two dissimilar materials; and mineralized collagen fibres were revealed in the inner bony layer. The nano- and micro-indentation tests revealed that the hardness (associated with the strength, modulus and stiffness) of the rhamphotheca layer (approx. 470 MPa for nano and approx. 320 MPa for micro) was two to three times less than that of the bony layer (approx. 1200 MPa for nano and approx. 630 MPa for micro). When compared to other birds (chicken, finch and toucan), the woodpecker's beak has more elongated keratin scales that can slide over each other thus admitting dissipation via shearing; has much less porosity in the bony layer thus strengthening the beak and focusing the stress wave; and has a wavy suture that admits local shearing at the nanoscale. The analysis of the woodpeckers' beaks provides some understanding of biological structural materials' mechanisms for energy absorption.

1. Introduction

Woodpeckers show amazingly efficient shock absorption capabilities without any recorded damage to their beaks or brains while pecking trees. When a woodpecker makes a blow into the tree trunk, its beak repeatedly strikes at a speed of 6–7 m s−1, and the impact deceleration is of the order of 1000 g [1]. The yellow-bellied sapsucker (a type of woodpecker) can strike 100–300 times per minute on the tree, and they may spend many hours pecking for food or constructing cavities [2]. The woodpecker's capability of withstanding high impact has been studied by several researchers. Unique anatomical features of woodpeckers have been reported such as stiff tail feathers to resist gravity for working on vertical trees, wider ribs to relieve neck stress, zygodactyl feet to climb trees and an ocular system to protect their eyes [26]. The physical characteristics of the head include spongy bone on the upper beak, an extended hyoid bone, a tightly enclosed small brain within the skull and a plate-like high-strength cranial bone [711]. Also, numerical studies of the woodpecker's head reported by Wang et al. [12,13] and Zhu et al. [14] showed that the cranial bone and beak play an important role in energy dissipation. Yoon et al. [15,16] used physiological arguments from woodpeckers to develop shock absorbers for microdevices, which can resist high-frequency excitation and high-g forces by absorbing energy. Some additional examples of specific biomimetic applications include employment of spiral and wavy structures found in nature, and possibly using the woodpecker's geometrical advantages in car bumpers and athletic helmets [17].

Although some physiological and numerical studies have been conducted on woodpeckers, many studies have not focused on woodpeckers' beaks from the perspective as a biological material. Avian beaks are structural biocomposite materials. Generally, structural biological materials comprise a brittle mineral and ductile protein interacting in a complex structure that is organized in a hierarchical manner [1820]. Likewise, birds' beaks are mainly composed of β-keratin layer, which is called the rhamphotheca, bony core and cellular interface between rhamphotheca and bony core [2124]. At the microscale, the rhamphotheca comprises keratin scales with a diameter of approximately 50 μm with the core part of the beak being a closed-cell trabecular-like bone [2528]. At the nanoscale level, keratin scales comprise β-keratin filaments and have a small gap between them [26]. For the multiscale mechanical properties, Young's modulus of the rhamphotheca was reported as approximately 1 GPa for toucans and hornbills with its anisotropy depending on the geometry of the keratin scales [26]. Under compression, the stress plateau occurs at 0.3 MPa for the toucan beak and at 2 MPa for the hornbill beak [26]. At the microscale, the reported value of microhardness for the rhamphotheca was approximately 200 MPa for the toucan, hornbill and European starling [26,29]. Contrary to the rhamphotheca layer, the core part of the beak had a wide range of microhardness values with respect to the species; 0.27 GPa for toucan beaks and 0.39 GPa for hornbill beaks [26]. Seki et al. [26] also reported the nanohardnesses of the toucan beaks were 0.5 and 0.55 GPa for the rhamphotheca and the foam trabecular, respectively. The nanohardnesses of the hornbill beaks were 0.85 and 0.94 GPa for the rhamphotheca and the trabecular, respectively (table 1). Also, the elastic moduli of the woodpecker, toucan, hornbill and Java finch are represented in table 1. The elastic moduli of the beaks of woodpeckers, toucans and hornbills were obtained from nanoindentation testing while that of Java finch was obtained from a double indentation technique. The different mechanical properties of the birds reveal different functions and uses of each beak.

View this table:
Table 1.

Summary of the micro/nanohardness and elastic modulus of beaks of birds for comparison: woodpecker (n = 6), toucan [26], hornbill [26] and Java finch [30].

Our study focuses on the multiscale structure–property relationships of the woodpeckers' beaks. By studying woodpeckers' beaks, we can learn clues in solving human engineering problems related to energy absorption and shock mitigation.

2. Material and methods

The beak of an adult red-bellied woodpecker (Melanerpes carolinus), which is a medium-sized bird living in the southern USA, was studied using various microscopy techniques and mechanical testing methods. One non-living red-bellied woodpecker was obtained from the Department of Wildlife, Fisheries and Aquaculture (Mississippi State University), and two others were obtained from road-kill. The woodpeckers obtained had body lengths of 24–25 cm. The upper and lower beaks were separated from the body as shown in figure 1b, and all tests were carried out at ambient conditions.

Figure 1.

(a) A male red-bellied woodpecker (Photo courtesy of Ken Thomas, http://kenthomas.us/?page_id=140&px=%2FRed-bellied_Woodpecker-male.jpg), (b) upper and lower beaks of the woodpecker, and (c) a schematic of the cross-sectional view of the woodpecker beaks comprising three layers: outer rhamphotheca, middle foam and inner bony layers. (Online version in colour.)

The structure of the woodpeckers' beaks was characterized by scanning electron microscopy (SEM) and transmission electron microscopy (TEM). In order to observe the polished cross section of the beak, samples of the upper and lower beaks were cut into four parts from the tip to the root with length of 5 mm using a diamond saw. Each sample was mounted into epoxy using a cold mount technique and then thoroughly polished. For preparing the fractured sample and TEM sample, the beaks were fixed in 2.5% glutaraldehyde and post fixed in 2% osmium tetraoxide. Samples were then rinsed and dehydrated in a graded ethanol series. Following processing the upper beak microstructure was observed by preparing fractured surface samples using a cryofracture technique then sputter coating with gold palladium. SEM micrographs were taken using a JEOL JSM-6500F field emission gun (FEG)-SEM. The energy dispersive X-ray spectroscopy (EDS) on the FEG-SEM was also used to carry out chemical analysis of the beaks. In preparation for TEM, samples of the lower beak were taken from the beak, fixed and then embedded in Spurr's resin. Thin sections (60–80 nm) were cut on a Reichert-Jung Ultra cut E ultramicrotome and stained with uranyl acetate and lead citrate. Stained sections were examined by using a JEOL JEM-100CX II TEM at an acceleration voltage of 80 kV. The porosity and area fraction in the beak were measured via analysing two-dimensional images using Image J software (National Institutes of Health, Bethesda, MD, USA).

Microindentation and nanoindentation tests were conducted on the lower beak in order to evaluate the mechanical properties. A Vickers hardness tester (LECO Corporation, St Joseph, MI, USA) with a pyramidal diamond tip was used to examine the beak microhardness. The applied maximum load was 100 gram-force. Nanoindentation tests were carried out on the beaks mounted into epoxy by a Hysitron triboindenter with a Berkovich-type diamond tip. The loading condition was controlled as follows: 9000 μN maximum load with a 20 s loading segment and a 40 s unloading segment. This procedure was employed due to the creep behaviour of viscoelastic materials. The hardness was defined by the following equation:Embedded Image 2.1where P is the maximum applied load (N) and A the resultant projected contact area. For a Berkovich tip, A is calculated from the ideal tip area function, 25.4h2, and h is the maximum displacement. The reduced elastic modulus was derived from the initial unloading contact stiffnessEmbedded Image 2.2where the reduced modulus, Er, is derived from the displacement from both the specimen and the indenter. The reduced elastic modulus is given byEmbedded Image 2.3where E and ν are the elastic modulus and Poisson's ratio of the specimen and the indenter, respectively.

3. Results

3.1. Structure of the woodpeckers' beaks

3.1.1. Macrostructure

One of the notable characteristics of biological materials is the hierarchical structure [20]. Woodpeckers' beaks also have a unique hierarchical structure from the macroscale down to nanoscale. At the macroscale, the full length of the beak is about 4 cm, and the cross section of the woodpecker beak is composed of the outer rhamphotheca layer, the middle foam layer and the inner bony layer as the schematic of figure 1c illustrates. The upper beak has a cavity in the centre of the beak, which decreases the weight while still keeping the bending resistance fairly high. The curvature of the tip of the upper beak was measured at 19.07 mm−1, and that of the lower beak was approximately 12.01 mm−1. The density of the upper beak was 1.1 g cm−3, and that of the lower beak was 1.348 g cm−3 measured using the Archimedes method [31]. The lower density of the upper beak is due to the cavity and more porous area at the root part of the upper beak [2].

Figure 2a provides a series of cross-sectional views of the lower beak from the tip to the root. Along the beak, the geometry of the cross section changed as well as the area fraction of each layer. Figure 2b shows that the area fraction of the rhamphotheca decreased while that of the bony part increased from the tip to the root of the beak.

Figure 2.

(a) Cross-sectional views throughout the length of the woodpeckers' beaks taken by a scanning electron microscope illustrating the change in the geometries with differing ratio of each layer. (b) The area fraction of the rhamphotheca, the foam, and the bony layers along the length of the lower woodpeckers' beaks. (Online version in colour.)

3.1.2. Microstructure

The SEM images of the fractured surface of the woodpeckers' beaks reveal the microstructure of each layer (figure 3). Figure 3a shows the entire fractured surface of the upper beak having a big cavity in the centre. Figure 3b shows that the rhamphotheca layer has a thickness of 500 μm, consisting of overlapping scales. The size of the scales varies with respect to the location on the beak. At the ventral surface of the beak (mouth), the scales are more equiaxed and thicker with a dimension of 25 × 10 × 1 μm, whereas at the outside of beak the scales are more elongated and thinner with a dimension of 55 × 15 × 0.2 μm. Figure 3c shows the rough surface of the keratin scales.

Figure 3.

Microstructure of the woodpeckers' beaks garnered from scanning electron microscopy showing (a) the fractured cross section of the upper beak with the three distinctive structural layers, (b) the outer rhamphotheca layer containing overlapping scale-like features indicated by the dotted box, (c) rough surface of keratin scales, (d) the middle foam layer with a porous structure having a porosity of 30–65%, (e) the thickness of the cell wall is 0.1–2 µm, (f) the inner bony layer and (g) bundles of the fibres in the matrix.

The foam layer located between the rhamphotheca and the innermost bony layer is closed-cell type foam with a thickness of 100 μm and is graded between the rhamphotheca and bony layer. The foam layer is composed of dermis and epidermis. The dermis includes keratin filaments to provide mechanical resilience, and the epidermis includes dense bundles of collagen fibres to anchor to the inner bony layer [32,33]. Our results agree with the literature as bundles of fibres were observed in the microscopic images of the woodpecker beak. At the interface, which is particularly important due to high stresses and contact failure, the foam layer joins the dissimilar materials of keratin and bone. Figure 3d depicts the middle foam layer exhibiting a porous structure having a porosity of 27–30% near the rhamphotheca or the bony layer and 50–65% at the middle of the foam layer. At the contact region, the foam material provides flexibility. As shown in figure 3e, the thickness of the cell wall is 0.1–2 μm and the fibrils comprise the interior structure of the foam layer.

The bony layer located in the inner part of the beak has randomly distributed various-sized voids and a large cavity. Figure 3f shows that the bony layer of the woodpecker beak is not spongy-like trabecular bone and also shows that the composite bony layer comprises fibres in the longitudinal direction, which is a common structure of bone [34].

3.1.3. Nanostructure

The nanostructure of each layer of woodpeckers' beaks was investigated by TEM. Cross-sectional and lateral perspective images in figure 4 show the nanostructure of the rhamphotheca. The cross-sectional view revealed that the keratin scales are tightly packed (figure 4a), and the size of the keratin grain varies from 10 to 15 μm across the diameter. By increasing the magnification, it is shown that the grain boundary has a wavy structure (figure 4b). The waviness of the keratin grain boundary (i.e. the ratio of height to width) was calculated with the mean value being 1.0 ± 0.32. Also, figure 4c shows that there is a narrow gap along the wavy line measured as 44.2 ± 19.2 nm. Figure 4d–f depicts the lateral views of the rhamphotheca. One can observe the side view of the keratin scales in figure 4d and the boundary where two keratin scales meet in figure 4e. The fibres run parallel to the transverse orientation and zooming in on the contact surface of the two scales, figure 4f shows the gap within the wavy line.

Figure 4.

Transmission electron microscopic images of the rhamphotheca of woodpeckers' beaks show the nanostructure: (a) a cross-sectional view reveals the keratin grains in the rhamphotheca; (b) a cross-sectional view that shows the wavy ‘suture’ lines at the grain boundary; (c) a cross-sectional view that depicts a small gap in the wavy line; (d) a longitudinal view in the rhamphotheca; (e) a longitudinal view with the arrows indicating the running direction of the fibre; and (f) a longitudinal view showing the wavy line and gap. (Online version in colour.)

Figure 5, depicting SEM images, shows the nanostructure of the foam layer. Figure 5a shows the cell wall of the foam layer, in which part of it is composed of fibres as shown in figure 5b. From the image of figure 5c, the length the D-period in the fibres was measured to be in the range of 60–70 nm. The measured period falls into the range of collagen fibril D-period although it is not the exact 67–69 nm band that is often reported in soft connective tissues [35]. The stereological effect might explain this variation of D-period estimation (e.g. a slight tilt can change the period estimation). The morphology of the banded fibres under SEM and the periodic length all point to the likelihood that the fibres contained in the foam layer are collagen fibres.

Figure 5.

Nanostructure of the foam layer taken by a scanning electron microscope shows (a) the cell wall of the foam layer, (b) part of the cell wall is composed of fibres, and (c) the fibres have a D-period indicating that they are collagen.

Figure 6, depicting TEM images, shows the nanostructure of the bony layer. The bony layer contains round-shaped cells and fibres with an area fraction of the bone cells being approximately 37% (figure 6a). Figure 6b shows that the running directions of the fibres are not uniform as both longitudinal (L1 and L2) and transverse (T) directions of the fibrils are observed within the same plane. Figure 6c shows the D-period of the fibres, which is an indication of collagen. The length of the D-period in figure 6c ranged from 50 to 70 nm. From these different analyses, it is apparent that the core part of bird beak is bone, which consists of collagen and mineral.

Figure 6.

Images taken by a transmission electron microscope illustrate the nanostructure of the bony layer of the woodpeckers' beaks: (a) the distribution of the bone cells having round shapes and short fibrils (grey); (b) the fibrils are running in both longitudinal (L1 and L2) and transverse directions (T); and (c) the fibres have a D-period that is indicative of collagen. (Online version in colour.)

3.2. Chemical composition

The chemical compositions of the rhamphotheca, foam and bony layers were analysed by the EDS technique. Figure 7a shows that the main constituents of the rhamphotheca are carbon (C), nitrogen (N), oxygen (O) and a small amount of sulfur (S), which are the main components of keratin in general. The chemical components of the foam layer are C, N, O, S and a small amount of calcium (Ca) as shown in figure 7b. The chemical composition of the foam layer confirms that it is a graded material between the rhamphotheca and bony layer comprising protein and mineral. The chemical elements in the bony layer shown in figure 7c are C, N, O and various minerals such as Ca, sodium (Na) and magnesium (Mg), which are the main components of bone, thus confirming the mineralized collagen fibres observed within the bony layer as shown in figure 3f.

Figure 7.

The results of energy dispersive spectroscopy analysis for (a) the outer rhamphotheca layer composed of carbon, nitrogen, oxygen and sulfur; (b) middle foam layer composed of carbon, nitrogen, oxygen, sulfur and calcium; and (c) inner bony layer composed of carbon, nitrogen, oxygen and several minerals, such as calcium, sodium, magnesium and phosphate. (Online version in colour.)

3.3. Mechanical properties of the woodpeckers' beaks

The multiscale mechanical responses of the woodpeckers' beaks were also studied at the microscale and nanoscale under microindentation and nanoindentation tests, respectively.

Microindentation tests were performed to garner micromechanical properties. Indentation tests were conducted only on the rhamphotheca and bony layers, because the area of the foam layer was not large enough to conduct the tests. The average value of the microhardness was 0.32 ± 0.01 GPa for the rhamphotheca layer and 0.64 ± 0.07 GPa for the bony layer (table 1).

The nanomechanical properties obtained from the nanoindentation tests were the nanohardness and the reduced elastic modulus. To examine the gradient of the nanomechanical properties, experiments were performed on four different beak locations from the tip to the root, and the results are depicted in figure 8. The results show a decrease in the hardness as the location changes from the tip to the root of the beak for the rhamphotheca. The bony layer did not show a change with respect to location. The nanohardness was measured as 0.40 ± 0.08 GPa for the rhamphotheca, 0.24 ± 0.14 GPa for the foam layer and 1.16 ± 0.19 GPa for the bony layer (table 1). The relatively high mineral content of the bony layer was responsible for it being three times harder than the keratin part (rhamphotheca). The average measured values of reduced elastic moduli were 8.7 ± 1.1 GPa at the rhamphotheca, 6.5 ± 2.5 GPa at the foam layer and 30.2 ± 3.6 GPa at the bony layer (table 1).

Figure 8.

Nanomechanical properties of the rhamphotheca, foam and bony layers obtained from nanoindentation tests: (a) nanohardness and (b) reduced elastic modulus. (Online version in colour.)

4. Discussion

4.1. Macrostructure–mechanical property relationships

The woodpeckers' beaks are functionally graded materials through the length of the beak from three perspectives: (i) the geometry of the cross section of the beak changes as shown in figure 2a, (ii) the area fractions of the rhamphotheca, foam and bony portion change as shown in figure 2b, and (iii) the associated mechanical properties of the rhamphotheca, foam and bony portion are different. According to the rule of mixtures, which was developed for composite materials and can be applied for layered materials, one can estimate the modulus and hardness at each point along the beak with the correlating area fractions and strength/hardness of each sample:Embedded Image 4.1aandEmbedded Image 4.1bwhere A represents the area fraction, E represents elastic modulus and H is the hardness value. The total strength of the composite increased from the beak tip to the root. This strength gradient arises because the modulus of the bony region (Ebony) was greater than that of the rhamphotheca region (Erhamhotheca), and the area fraction of the bony layer increased from the beak tip to the root, whereas the area fraction of the rhamphotheca decreased from the beak tip to the root. Table 2 organizes the geometrical, microstructural and mechanical property information. With regard to the location on the beak, the geometry of the cross section changes similar to that of a shape of ∇ → V → U → ( ). The changed geometry of the cross section results in a change in moment of inertia, and the changing moment of inertia allows for a changing flexural stiffness over the beak. Table 2 shows that the flexural stiffness from the tip to the root of the beak increases. This implies that the beak becomes stiffer and has a greater bending resistance when traversing from the tip to the root. Another important observation is that the overall aggregate modulus increases from the tip to the root according to the rule-of-mixtures. This not only increases the stiffness but also increases the speed of the stress wave, as the shock wave velocity is proportional to the modulus over the density.

View this table:
Table 2.

Summary of the structure–property relationships of the woodpeckers' beaks, including area fraction, mechanical properties, aggregate modulus/hardness and moment of inertia at each location along the beak.

4.2. Microstructure–mechanical property relationships

The microstructural observations revealed that the rhamphotheca layer is composed of overlapping scales. Overlapping keratin scales are a common structure observed in structural materials made of keratin such as the exterior of skin, nail or avian beaks [36]. The keratin scales create friction upon movement by their stacking morphology, thus functioning as a dissipating agent. In particular, the layout of keratin scales in woodpeckers' beaks is designed to maximize friction. The keratin scales' increasing number density within the beak creates more frictional area for shearing (figure 3b). The keratin scales in the woodpecker rhamphotheca are thinner than those of the toucan and hornbill. The thickness of a single keratin scale of the woodpecker beak is 0.2–1 μm, whereas that of the toucan beak is 2–10 μm [26]. Owing to the similar overall thicknesses of rhamphotheca (approx. 500 μm), the number of keratin scales in the woodpecker beak is much greater than that of the toucan. As such, more keratin scales admit more frictional area thus inducing greater frictional dissipation via the shearing mechanism. In addition to the greater frictional shearing area, the rough surface area between the scales also assists with energy mitigation (figure 3c). The way that the keratin scales are arranged is also efficient to block crack propagation. Figure 9 shows the transverse plane of the woodpecker rhamphotheca illustrating the overlapping pattern of the keratin scales. A similar overlapping structure has also been observed in some structural biological materials, including nacre, bone and dentine [37]. The overlapping structure induces a physical restraint against free movement of the blocks, and hence it does not allow crack propagation, thus providing a greater fracture toughness and robustness to biological materials [3739]. As such, an overlapping arrangement of keratin scales in the rhamphotheca also provides a greater fracture toughness to resist fracture during high-speed pecking.

Figure 9.

The scanning electron microscopic image of the polished rhamphotheca of the woodpecker's beak at the transverse plane shows the overlapping pattern of the keratin scales, which provide resistance to crack propagation in the direction of the arrow.

Micromechanically, the microhardness of the rhamphotheca of the woodpecker is about 50% greater than those of other birds, such as the toucan, hornbill and starling. It is reported that dark-coloured beaks have a greater hardness than light-coloured beaks, so the dark beaks are less susceptible to wear [29]. As the colour of woodpeckers' beaks is predominantly black, then one would expect a greater hardness if the European starlings study [29] is consistent with woodpeckers' beaks. Our study also shows that the microhardness of the core part of the woodpeckers' beaks is indeed two to three times greater than those of the toucan and hornbill beaks (table 1). Clearly, in terms of the structure–function relationship, hardness differences would be expected in the woodpeckers' beaks versus the toucan and hornbill because the high rate shocks would be much greater for the woodpecker.

4.3. Nanostructure–mechanical property relationships

From the nanostructure of the woodpeckers' beaks as shown in figure 4e, one can observe that mechanical anisotropy arises, because the fibres are oriented parallel to the pecking direction. Bonser et al. [40,41] reported that ostrich claw and feather, composed of β-keratin, display anisotropy in which Young's modulus in the longitudinal direction of the claw was 28% greater than in the transverse direction, and the toughness of the feather also showed anisotropy according to the fibre direction. Likewise, the fibres in the rhamphotheca provide strong mechanical properties in the longitudinal direction. As the mechanical stress exhibited in the woodpeckers' beaks is mostly realized along the longitudinal axis, this may provide an advantage to the functioning of the beaks.

Additionally, the results of nanoindentation tests and nanostructural analysis show that data from the bony part have a large standard deviation as shown in figure 8. This is indicative of the heterogeneous nature of the bony layer, which comprises fibres and a mineral matrix. Various values were measured across the span of the bony layer. The hardness and reduced elastic modulus were greater at the location where there was mostly a mineral matrix, and they were lower where there was a greater fibre density but lower mineral content.

4.4. Comparison to other birds' beaks

The structure of the woodpeckers' beak is different from other birds' beaks such as the chicken and toucan. The micro- and nanostructure of chickens' beaks is compared here to the woodpeckers' beaks along with literature data on the structure of a toucan's beak. While the woodpeckers' beaks are used for penetrating and grabbing food deep within a tree, chickens' beaks are used for grabbing food from more shallow sources and toucans' beaks are used for crushing fruits. The difference in function is related to the difference in multiscale structure and mechanical properties.

Woodpeckers' beaks show some meaningful multiscale structural differences compared with other birds' beaks such as those from chickens or toucans. First, keratin scales of the woodpeckers' rhamphotheca are more elongated than the two other birds' beaks as shown in figure 10. The dimension of the keratin scales from the woodpecker is 55 × 15 × 0.2 μm, and the aspect ratio of the width over the height is about 3.67. The dimension of the chicken's keratin scale is 30 × 10 × 1 μm with an aspect ratio of the width over the height being about 3. The dimension of the toucan's keratin scale is 45 × 45 × 1 μm having an aspect ratio of about 1 [27]. The keratin scales dissipate mechanical load by friction as one scale slides against another scale. Adams et al. [42] reported that the geometry of the scales generates anisotropy, and the elongated direction of the scale can dissipate more energy than the shorter direction. This is called the differential friction effect. With respect to the differential friction effect, the large anisotropy in the longitudinal direction in the woodpeckers' beaks provides high friction to withstand the impact loading in the longitudinal direction.

Figure 10.

The dimensions and aspect ratios of the height over the width of a keratin scale from each bird are different according to their functions. Dimensions and aspect ratio of the width over the height of each bird's beak are (a) 55 × 15 × 0.2 μm and 3.67 for woodpeckers, (b) 30 × 10 × 1 μm and 3 for chickens and (c) 45 × 45 × 1 μm and 1 for toucans [27], respectively. (d) The geometry of keratin scales affects anisotropy of beaks. Black arrows indicate longitudinal direction, and grey arrows indicate transverse direction. Woodpecker image courtesy of Ken Thomas (http://kenthomas.us/?page_id=140&px=%2FRed-bellied_Woodpecker-male.jpg) and Toucan image from https://www.flickr.com/photos/15177523@N00/401000107. (Online version in colour.)

Secondly, the porosity of the woodpeckers' beaks is different from that of the chicken and toucan (figure 11). While the bony layers of the beaks from the chicken and the toucan have a closed-cell type foam with a membrane, the bony layer of the woodpecker's beak is not a foam material. The porosity of the woodpecker's bony layer is 9.9 ± 3.0%, and the porosity levels of the bony layer of the chicken and the toucan are 42.3 ± 1.3% and 61.5 ± 2.0%, respectively. As the porosity increases, the bulk modulus and the density of a material decrease. Therefore, the bulk modulus of the woodpecker's bony layer is greater than the chicken and toucan bony layer if the moduli from the nanoscale are similar. This in turn has an effect on the stress wave moving through the beak as the wave speed increases as the moduli per density increases. Hence, the woodpeckers' beaks would propagate the shock wave faster than the two other birds' beaks and in doing so, guides the wave to the hyoid bone. Also in this context, Genbrugge et al. [24] showed a large difference when comparing the trabecular porosity in the beaks of Java and Darwin's finches thus relating their structure to their different feeding habits. When considering these different birds' beaks, one can assess that the porosity directly affects the lightweightedness of the beak, the wave speed, the strength, and the directionality and means of each bird's eating function.

Figure 11.

The inner layers of the beaks show various porosities according to their function. (a) Woodpecker's bony layer having porosity of 9.9 ± 3.0%, (b) chicken's beak having porosity of 42.3 ± 1.3% and (c) toucan's beak having porosity of 61.5 ± 2.0% [27]. Woodpecker image courtesy of Ken Thomas (http://kenthomas.us/?page_id=140&px=%2FRed-bellied_Woodpecker-male.jpg) and toucan image from https://www.flickr.com/photos/15177523@N00/401000107. (Online version in colour.)

The next unique feature of the woodpeckers' beaks is the wavy structure (suture lines) as shown in figure 12. The TEM images of the rhamphotheca of the woodpecker, chicken and toucan show the wavy structure. Although the beaks of the chicken and the toucan also show the wavy structure, the waviness (i.e. the ratio of height to width) of those birds' beaks is less than that of woodpecker's beak. The waviness of the woodpecker's beak is approximately 1, while that of the chicken's beak is approximately 0.3, and that of the toucan's beak is approximately 0.05. The geometry of the wavy structure also can be found in other biological materials such as a human skull and turtle shell, which both resist compressive loads [4345]. Typically, the suture lines have a space between them comprised of collagen. When a load is imposed on the suture line, shearing will result in which the collagen is compressed and frictional forces will result thus helping to dissipate the load. Li et al. [46,47] also reported that the wavy structure's role is to provide extra stiffness and strength based on its geometry. Similarly, the wavy line in the woodpeckers' beaks is assumed to have the capability of withstanding compressive load.

Figure 12.

The wavy structure shown in the rhamphotheca of (a) woodpecker having waviness of 1, (b) chicken having waviness of 0.3 and (c) toucan having waviness of 0.05 [26]. Woodpecker image courtesy of Ken Thomas (http://kenthomas.us/?page_id=140&px=%2FRed-bellied_Woodpecker-male.jpg) and Toucan image from https://www.flickr.com/photos/15177523@N00/401000107. (Online version in colour.)

5. Conclusion

In this study, we examined the complicated, multiscale heterogeneous structure and mechanical properties of red-bellied woodpecker (M. carolinus) beaks. The woodpecker beak is a structural biocomposite having three layers: rhamphotheca (outer keratin shell), middle foam layer and inner bony layer. Along the beak from posterior to anterior, the area fraction of these three layers gradually changes, so the aggregate modulus and aggregate hardness are gradients. The rhamphotheca is made up of elongated keratin scales, and the microhardness of the rhamphotheca was measured to be approximately 323 MPa and the nanohardness approximately 470 MPa. The foam layer is a continuous unification of the rhamphotheca and bony layer, and the nanohardness of the foam layer was approximately 243 MPa. The bony layer consists of mineralized collagen with a big cavity, and the microhardness of the bony layer was measured to be approximately 636 MPa and the nanohardness approximately 2 GPa.

In summary, the three structures found in the woodpecker beak could be used as design guidelines to lower the directional stress levels in structures, because of their geometric and material integration: an elongated geometry of keratin scales that can slide over each other, lower porosity and a wavy structure with a small gap to admit local shearing. The results from this paper, in revealing the structure–property relationships of woodpeckers' beaks, can provide promising features for energy absorption in designing man-made devices.

Funding statement

This paper is based upon work supported by the Department of Energy under award no. DE-FC26-06NT42755. The authors would like to thank Center for Advanced Vehicular Systems (CAVS), Department of Defense, the DOE Southern Regional Center for Lightweight Innovative Designs (SRCLID), Amanda Lawrence, Richard Kulklinski, the MSU Electron Microscope Center and our Department of Agricultural and Biological Engineering.

  • Received March 14, 2014.
  • Accepted April 15, 2014.

References

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