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

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.

Structural analysis of the tongue and hyoid apparatus in a woodpecker

“…Carbon and nitrogen peaks are not labeled and excluded for quantification results due to the relatively high intensity of the carbon peak and low intensity of the nitrogen peak compared to the other elements (S, P, O, and Ca). The chemical composition (mainly P and S) is similar to that reported for the keratin in the woodpecker’s beak [11]. This, coupled with the SEM images, indicates that the lingual apex has a keratin outer sheath that surrounds the paraglossal bone, as is found in other birds [26].…”

“…7f and g). The fibers are ~194 nm in diameter and >10 μm in length, comparable to mineralized collagen fibril bundles found in the bony core of woodpecker’s beak [11]. Overall, the multilayered structure of the lingual body is similar to the lingual apex.…”

“…Strong neck muscles provide protection from injury caused by rotational forces [9]. A previous study of the relationship between structure and mechanical properties of the beak of woodpeckers revealed that the lower porosity found in the bony layer strengthens the beak for pecking [11]. In addition, the sponge-like bone structure within the upper beak and the more plate-like cranial bones (both absent in non-pecking birds) may also contribute to the energy absorption [6,9,12].…”

Bioinspired engineering of honeycomb structure – Using nature to inspire human innovation

“…The multiscale honeycomb as a storage of honey and pollen is an important clue to recognize the nestmate [433,434] and to understand the evolution of honeybees (e.g., honeybee growth and brood survivorship) [435,436]. Similarly, most biological materials exhibit inherent multifunctional integration due to porous and multiscale structures (Table 7) [437][438][439][440]. For artificially-made multifunctional honeycombs, their functional properties should be understood as their mechanical properties to better meet the requirements.…”

“…Bending fatigue Rectangular fracture shape [128] Micelle-templated silicates 35nm,80nm Compression Brittle crushing [136] Nano-structured glass fibers 3nm Simulated nanoindentation - [137] Mesoporous silica 5nm Unilateral external pressure Destroy [138] Mesoporous silicaNanoindentation Elastic modulus， hardness [139][140][141] Carbon/epoxy composite Small aircraft [221,222] Polypropylene (PP) Vehicle [223] Carbon/epoxy laminate Airfoil [224,225] Honeycomb structural support for larvae storage of honey and pollen [435,436] Bone structural support protect for body and blood cell formation minerals storage [437] Red-bellied woodpecker beak structural support amazingly efficient shock energy absorption [438] Tree trunk and root structural support anchoring nutrient transport [439] Butterfly wing structural support structural color superhydrophobicity self-cleaning properties directional adhesive functions chemical sensing capabilities [440] …”