Microstructural design for mechanical–optical multifunctionality in the exoskeleton of the flower beetle Torynorrhina flammea

Abstract

Biological systems have a remarkable capability of synthesizing multifunctional materials that are adapted for specific physiological and ecological needs. When exploring structure–function relationships related to multifunctionality in nature, it can be a challenging task to address performance synergies, trade-offs, and the relative importance of different functions in biological materials, which, in turn, can hinder our ability to successfully develop their synthetic bioinspired counterparts. Here, we investigate such relationships between the mechanical and optical properties in a multifunctional biological material found in the highly protective yet conspicuously colored exoskeleton of the flower beetle, Torynorrhina flammea. Combining experimental, computational, and theoretical approaches, we demonstrate that a micropillar-reinforced photonic multilayer in the beetle’s exoskeleton simultaneously enhances mechanical robustness and optical appearance, giving rise to optical damage tolerance. Compared with plain multilayer structures, stiffer vertical micropillars increase stiffness and elastic recovery, restrain the formation of shear bands, and enhance delamination resistance. The micropillars also scatter the reflected light at larger polar angles, enhancing the first optical diffraction order, which makes the reflected color visible from a wider range of viewing angles. The synergistic effect of the improved angular reflectivity and damage localization capability contributes to the optical damage tolerance. Our systematic structural analysis of T. flammea’s different color polymorphs and parametric optical and mechanical modeling further suggest that the beetle’s microarchitecture is optimized toward maximizing the first-order optical diffraction rather than its mechanical stiffness. These findings shed light on material-level design strategies utilized in biological systems for achieving multifunctionality and could thus inform bioinspired material innovations.

Biomineralized Materials as Model Systems for Structural Composites: 3D Architecture

“…In sharp contrast to engineering designs, unfortunately, the objective function is typically unknown in biological materials, especially considering that they are multifunctional. [ 84 ] In many cases, optical, sensing, and energy consumption are all important constraints for biological materials. [ 39,84 ] As the objective function is unknown, parameters that represent the comprehensive mechanical performance of a microstructure can be used alternatively.…”

“…[ 84 ] In many cases, optical, sensing, and energy consumption are all important constraints for biological materials. [ 39,84 ] As the objective function is unknown, parameters that represent the comprehensive mechanical performance of a microstructure can be used alternatively. One suitable choice is the area of the enclosed polygon with different weightings (Figure 20a,d).…”

“…[ 80,81 ] 2) Fibers arranged parallel to the surface. The most common case is the rotating plywood structure (Bouligand structure) which is abundant in crustacean exoskeletons (like stomatopod dactyl club), [ 82 ] insect exoskeletons, [ 83,84 ] and bone osteon rings (Figure 5k). [ 12,85 ] Mechanically, the prismatic array is optimized for stiffness and strength along the fiber direction, [ 81 ] while the rotating plywood structure is advantageous to resist crack propagation.…”

“…The multilayer‐rotating plywood structure (Figure 9a) is broadly found in insect cuticles, [ 84 ] crustacean exoskeletons, [ 128,129 ] elasmoid fish scales, [ 128 ] and turtle carapace. [ 130 ] These biological structures function as the external armor to protect the organism and thus have strict requirements on strength, penetration resistance, and also impact resistance.…”

Microfabrication of peptide self-assemblies: inspired by nature towards applications

“…29 Over ages of evolution, diverse hierarchically aligned supramolecular structures with unique physicochemical properties for various biological activities, assembled by (poly) peptides or proteins, were naturally screened. [30][31][32] For example, the hair protein fibrillar arrays-coated skins of Saharan Silver Ants (Cataglyphis bombycina) can improve sunlight reflection and decrease their body temperature, thus protecting the insects from sunburn and overheating (Fig. 2a).…”