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Structural Analysis of the Tongue and Hyoid Apparatus in a Woodpecker

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Structural Analysis of the Tongue and Hyoid Apparatus in a Woodpecker

Jae-Young Jung et al. Acta Biomater.

Abstract

Woodpeckers avoid brain injury while they peck at trees up to 20Hz with speeds up to 7m/s, undergoing decelerations up to 1200g. Along with the head, beak and neck, the hyoid apparatus (tongue bone and associated soft tissues) is subjected to these high impact forces. The shape of the hyoid apparatus is unusual in woodpeckers and its structure and mechanical properties have not been reported in detail. High-resolution X-ray micro-computed tomography and scanning electron microscopy with energy dispersive X-ray spectroscopy were performed and correlated with nanoindentation mapping. The hyoid apparatus has four distinct bone sections, with three joints between these sections. Nanoindentation results on cross-sectional regions of each bone reveal a previously unreported structure consisting of a stiff core and outer, more compliant shell with moduli of up to 27.4GPa and 8.5GPa, respectively. The bending resistance is low at the posterior section of the hyoid bones, indicating that this region has a high degree of flexibility to absorb impact. These new structural findings can be applied to further studies on the energy dissipation of the woodpecker during its drumming behavior, and may have implications for the design of engineered impact-absorbing structures.

Statement of significance: Woodpeckers avoid brain injury while they peck at trees, which results in extreme impact conditions. One common adaptation in woodpeckers is the unusual shape of the elongated tongue, also called the hyoid apparatus. The relationship between the structure and mechanical properties of the bony part of the hyoid apparatus has not been previously reported. A three dimensional model of the bony tongue was developed, and the hardness and stiffness were evaluated. A new type of bone structure, which is opposite of typical skeletal bone structure was found. The combined microstructural and mechanical property analysis indicate possible energy absorption routes for the hyoid apparatus and are applicable to the design of engineered structures.

Keywords: Hyoid bone; Nanoindentation; Tongue; Woodpecker; X-ray micro-computed tomography.

Figures

Fig. 1
Fig. 1
Bones in chicken and woodpecker hyoid apparatus. (a) Photograph (dorsal view) of the hyoid bones of a domestic chicken (Gallus gallus). Taken from [51]. (b) Schematic diagram of the dorsal view showing the paraglossal, the basihyal, the urohyal bone, and the paired ceratobranchial and epibranchial bones in a domestic chicken. Adapted from [3]. (c) Lateral view of the hyoid bones of a chicken. Adapted from [3]. (d) Lateral view of a golden-fronted woodpecker (Melanerpes aurifrons) skull with the hyoid apparatus colored in red. Taken from [52]. (e) Lateral view of the hyoid bones of a red-bellied woodpecker (Melanerpes carolinus) that highlights the bones and joints. The change in cross-section of the bones along the length is indicated. Adapted from [5]. Note: the epibranchial bone is ~1/3 of the total length of the hyoid bone in chickens, but is ~2/3 of the total length in woodpeckers. Scale bars were not provided in the references for (c) and (e). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
(a) Photograph of an acorn woodpecker. (b) The dissected hyoid apparatus. (c) The dried and sectioned samples of the hyoid apparatus in transverse and longitudinal planes. Magnified photographs of the three joint locations in the hyoid apparatus between (d) the lingual apex and body, (e) the lingual body and root, and (f) the lingual root and the hyoid horn.
Fig. 3
Fig. 3
Micro-computed tomography images of the head structure of an acorn woodpecker at different orientations. (a) Left lateral view, (b) dorsal view, (c) ventral view, and (d) lateral view of the hyoid bones. A color scale is shown to indicate the gradient in color (that is associated with mineral density) from the highest density in red to lowest density in dark blue. This shows that the hyoid bones are relatively denser than the skull. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 4
Fig. 4
Micro-computed tomography images of the hyoid apparatus of an acorn woodpecker, colored for clarity. (a) Left lateral view segmented 3D models. A: paraglossal bone (yellow), B: basihyal bone (blue), C: ceratobranchial bone (green), D: epibranchial bone (red), E: Saddle-shaped joint, F: Y-shaped joint, and G: Circular joint. (b) Expanded view (dorsal, lateral and ventral) of the three joints showing that each has a distinct structure associated with different articulations and functions. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 5
Fig. 5
(a) Orthoslice images of the hyoid bone with reconstructed 3D models from micro-computed tomography data. (b) Plot of the measured cross-sectional area at each location. (c) Transverse cross-sectional images at each location showing the shape of hyoid bone along its length. Scale bar: 500 μm.
Fig. 6
Fig. 6
(a) Photograph of dissected hyoid apparatus highlighting the imaged locations on the lingual apex. Scanning electron micrographs on the dorsal surface, (b) low magnification and (c) high magnification with the outline of two keratin scales (white dotted lines), and (d) energy dispersive X-ray spectroscopy results. Scanning electron micrographs on the cross-section, (e) low magnification and (f) high magnification. (g) Fourier transform infrared spectrum of the polished sample near the region shown in (f). PG: paraglossal bone, K: keratin scales.
Fig. 7
Fig. 7
(a) Photograph of dissected hyoid apparatus highlighting the imaged locations on the lingual body. (bc) Scanning electron micrographs and (d) energy dispersive X-ray spectroscopy result of the dorsal surface. Scanning electron micrographs (eg) on the longitudinal-section and (h) on the cross-section displaying four different muscles (M) surrounding the basihyal bone (BH). (ij) Energy dispersive X-ray spectroscopy results of the center of the BH bone and the muscles, respectively. CT: connective tissue, D: dermis.
Fig. 8
Fig. 8
Cross-sectional images of the basihyal (BH), ceratobranchial (CB), epibranchial (EB) bones: (a, c, e) Optical micrographs (OM) of each bone, (b, d, f) back-scattered electron (BSE) micrographs with (g, h) the magnified images of the CB bone, and (i, j, k), nanoindentation (Young’s modulus, E) maps overlaid on schematic illustrations of bone regions. The indentation sites for each hyoid bone are shown in Fig. 5a (BH: #4, CB: #6, and EB: #12). A color scale shows the gradient in E from the highest value (35 GPa) in red to the lowest value in blue (0 GPa). In the schematic illustrations (i, j, k), gray denotes the area of soft tissue/epoxy resin, white regions are the stiffer bone and the dash-filled regions are the more compliant bone. The optical micrographs were acquired prior to nanoindentation tests while the BSE micrographs (b, d, f) were obtained after the indentation tests. Note that BSE micrographs are not sensitive enough to image small nanoindentation topography features (~400 nm). The cracks appeared under the high vacuum condition in the scanning electron microscope and were not present during nanoindentation. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 9
Fig. 9
Bar charts of (a) the Young’s modulus and (b) hardness of each bone. The solid-filled bars represent the average value of the stiff bone region and the dash-filled bars represent the average value of the compliant bone region. PG: paraglossal bone (yellow). BH: basihyal bone (blue). CB: ceratobranchial bone (green). EB-1 to EB-3: epibranchial bone (red). The indentation sites for each hyoid bone are shown in Fig. 5a (PG: #1, BH: #4, CB: #6, EB-1: #8, EB-2: #10, and EB-3: #12). For both the one-way ANOVA and t-tests, comparisons where no statistically significant difference was found are marked with an “ns” symbol. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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