Towards in situ determination of 3D strain and reorientation in the interpenetrating nanofibre networks of cuticle

Abstract

Determining the in situ 3D nano- and microscale strain and reorientation fields in hierarchical nanocomposite materials is technically very challenging. Such a determination is important to understand the mechanisms enabling their functional optimization. An example of functional specialization to high dynamic mechanical resistance is the crustacean stomatopod cuticle. Here we develop a new 3D X-ray nanostrain reconstruction method combining analytical modelling of the diffraction signal, fibre-composite theory and in situ deformation, to determine the hitherto unknown nano- and microscale deformation mechanisms in stomatopod tergite cuticle. Stomatopod cuticle at the nanoscale consists of mineralized chitin fibres and calcified protein matrix, which form (at the microscale) plywood (Bouligand) layers with interpenetrating pore-canal fibres. We uncover anisotropic deformation patterns inside Bouligand lamellae, accompanied by load-induced fibre reorientation and pore-canal fibre compression. Lamination theory was used to decouple in-plane fibre reorientation from diffraction intensity changes induced by 3D lamellae tilting. Our method enables separation of deformation dynamics at multiple hierarchical levels, a critical consideration in the cooperative mechanics characteristic of biological and bioinspired materials. The nanostrain reconstruction technique is general, depending only on molecular-level fibre symmetry and can be applied to the in situ dynamics of advanced nanostructured materials with 3D hierarchical design.

Multiscale Toughening Mechanisms in Biological Materials and Bioinspired Designs

“…Similar toughening mechanisms related to fiber rotation was also found in arthropod cuticles consisting of chitin fibers . Figure f shows the Bouligand or helicoidal architecture (in‐plane) of chitin fibrils in the stomatopod cuticle surface.…”

“…h) Fibril rotation angle as a function of lamellar orientation. f–h) Adapted with permission . Copyright 2017, Royal Society of Chemistry.…”

“…It was verified that as a tensile stress was applied to the cuticle samples, the out‐of‐plane fibrils underwent compressive strains, which could explain the resistance to rotation of in‐plane fibrils. As a result, the toughness in chitin microfibrils is contributed by the deformation of both the in‐plane and the out‐of‐plane fibrils …”

Proteoglycan degradation mimics static compression by altering the natural gradients in fibrillar organisation in cartilage

“…While we therefore do not believe out-of-plane tilting is playing an important role in this static compression case, SAXS tensor tomography [62], [63], [64] is a powerful new technique which can be used to resolve 3D fibril orientation in biocomposites, and in combination with in situ methods, may resolve these issues in the future especially for biocomposites where fibre orientation has more complex geometries than the quasi-1D vertical variation seen in the cylindrical samples used in the current study. Related to this, the analysis methodology used here could be refined to include angle-dependent variation of fibrillar parameters, to link to the 3D fibre-matrix models of cartilage developed previously [26], [27], [43], similar to our prior work in 3D diffraction modelling of cuticle [65]. Secondly, the biological matrix modification (partial removal of chondroitin sulphate) is a synthetic attempt to mimic the natural changes in proteoglycan composition that occur in ageing; in future, more biologically relevant analysis would include use of naturally aged tissue, together with the use of human cartilage – which can be analysed using SAXS as shown previously [20].…”

Formation and fracture mechanics of tough apatite structures in the stomatopod hammer

“…studies to characterize many biological materials including, bone [148]- [150], nacre [151], enamel [152], sponge glass spicules [153], parrotfish teeth [154], pistol shrimp claw [155] and the stomatopod dactyl club [34], [156]. A variety of X-ray techniques were used like ptychographic X-ray computed tomography (PXCT), combined microsmall angle X-ray scattering and wide-angle X-ray scattering (μSAXS-WAXS) and μXRF which allowed for high resolution 2D and 3D mapping of the microstructure, composition gradient and crystallography at the microscale and in some cases even nanoscale.…”