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This research aims to further the understanding of the structure and mechanical properties of the dermal armor of the boxfish (Lactoria cornuta). Structural differences between collagen regions underlying the hexagonal scutes were observed with confocal microscopy and microcomputed tomography (μ-CT). μ-CT revealed a tapering of the mineral plate from the center of the scute to the interface between scutes, suggesting the structure allows for more flexibility at the interface. High-resolution μ-CT revealed, for the first time, a 3D image of the dermal armor’s complex collagen structure. Helical interfibrillar gaps in the collagen base were found that are similar to the Bouligand-type structure of the lobster, Homarus americanus, thereby suggesting that the collagen in the boxfish is also of a Bouligand-type structure. In situ scanning electron microscopy tests were performed in shear and tension between two connected scutes and suggest that the interfacial collagen is structurally designed to preferentially absorb energy during deformation to protect the internal collagen. Similarly, in situ small-angle x-ray scattering was performed in shear and tension and further corroborated the complex collagen structure. Lastly, these experimental results are coupled with finite element simulations that characterize the interfacial collagen and corroborate the non-linear deformation response seen during in situ testing. Overall, these findings further the understanding of the structure and mechanics of the dermal armor of the boxfish which may help provide a basis to synthesize bioinspired composites for impact-resistant materials, specifically with bioinspired Bouligand-type structures to create novel fiber-reinforced composites.

The Bouligand structure has been observed in a variety of biological materials, such as lamellar bone and exoskeleton of lobsters. It is a hierarchical and non-homogeneous architecture that exhibits excellent damage-resistant performance. This paper presents a multiscale fracture model considering the material inhomogeneity, the multiscale property, and the anisotropy to reveal the toughening mechanisms in the Bouligand structure. Firstly, the macro and micro constitutive properties of this composite are derived. Then, a multiscale fracture model is developed to characterize the local stress intensity factors and the energy release rates at the crack front of twisted cracks. Our results demonstrate that the decrease in the local energy release rate can be attributed to two-step mechanisms. The first mechanism is that the multiscale structure and the material inhomogeneity cause a release of stress near the initial crack tip. The second mechanism is that the twisted crack leads to the transformation from single-mode loading to mixed-mode loading, which enhances the fracture toughness. These results can not only reveal the toughening mechanism of the Bouligand structure but also provide guidelines for the design of high-performance composites. STATEMENT OF SIGNIFICANCE: Biological materials in nature often possess excellent mechanical properties that have not been achieved by synthetic materials. Bioinspired Bouligand structures provide prototypes for designing high-performance materials. In this study, we propose a multiscale theoretical fracture model to investigate the fracture properties of Bouligand structures with twisted cracks. We systematically consider the roles of material inhomogeneity, anisotropy, and multiscale properties. Our analysis demonstrates that the remarkable toughness of Bouligand structures results from the combined effects of material inhomogeneity and twisted cracks. This research contributes to unveiling the secret behind the outstanding toughness of Bouligand structures and provides inspiration for the development of novel designs for man-made composites., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2024 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.)

Summary: Exoskeletons of Odontodactylus japonicas, the “smasher-type” mantis shrimp, feature a raptorial appendage comprising a Bouligand architecture of chitin nanofibrils with newly observed voids or defects between the polysaccharide α-chitin and protein interfaces. Here, we use a continuous-fiber 3D printing technology to simulate such materials in carbon fiber-reinforced (helicoidal) composites, complete with the presence of voids due to imperfect printing. The specific impact energies of the 3D printed helicoidal composites are clearly superior and further enhanced by the presence of the voids. To explain the role of the Bouligand architecture, interlaminar stresses are computed and found to yield anti-delamination characteristics, and a theoretical model is derived to evaluate the optimal helicoidal architecture. Finite element modeling indicates that the voids tend to deform and coalesce on loading and appear to guide the fracture into the formation of an ideally twisted crack in the printed helicoidal composites, thereby contributing to the impact toughness.