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Yi Zhang2 Paolino De Falco3 1 Yanhong Wang1 Ettore Barbieri4 1 Oskar Paris5 Nick Terrill6 Gerald Falkenberg2 Nicola Pugno7 1 8 Himadri Gupta1

2, Deutsches Elektronen-Synchrotron DESY, Hamburg, , Germany
3, Max Planck Institute of Colloids and Interfaces, Potsdam-Golm, , Germany
1, Queen Mary University of London, London, , United Kingdom
4, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokohama, , Germany
5, Montanuniversitaet Leoben, Leoben, , Germany
6, Harwell Science and Innovation Campus, Harwell, , United Kingdom
7, University of Trento, Trento, , Italy
8, Italian Space Agency, Rome, , Italy

Determining the in situ nano- and microscale mechanics of hierarchical nanocomposites, whether natural or synthetic, can be technically challenging due to the necessity to experimentally decouple deformation at multiple length scales. Doing so is critically important, as it can illuminate the mechanisms enabling multiple functional optimization in biological composites, as well as test the functionality of bioinspired materials [1]. The cuticle of arthropods (like the mantis shrimp [2]) are materials adapted for high dynamic mechanical resistance [2-3]. Cuticle consists - at the nanometre scale - of mineralized semicrystalline chitin nanofibres embedded in a more amorphous matrix of mineral (calcium carbonate) and protein, which in turn are assembled into parallel layers of fibres arranged in a twisted plywood (Bouligand) motif [2-3]. At the microscale, these plywood layers run parallel to the shell surface, and are interpenetrated by transversely-running pore-canals [2]. Here, we develop and present a novel 3D nanofibrillar orientation-cum-mechanics reconstruction method to determine deformation mechanisms at the nano- and microscale in stomatopod cuticle, which combines synchrotron microbeam X-ray diffraction with in situ deformation and fibre-composite theory [4-5]. The X-ray reconstruction method is solely based on fibre symmetry at the molecular level and hence can have wider applications beyond hierarchical biological composites. We apply the model to measure angularly-resolved deformation and reorientation of chitin nanofibers – embedded in a mineralized protein matrix – in the tergite (exoskeletal segment) of mantis shrimp, using microfocus wide-angle X-ray diffraction combined with scanning and in situ tensile loading. In combination with lamination theory, the method quantifies the internal, anisotropic strain fields inside Bouligand lamellae, is able to decouple internal fibrillar reorientation from whole-body movement, and resolves spatial gradients in fibre strain during physiological bending [4-5]. Our reconstruction technique can be applied more generally to determine the in situ and spatially-resolved dynamics of both natural and synthetic hierarchical nanocomposites.

References:
[1] S. E. Naleway, M. M. Porter, J. McKittrick and M. A. Meyers, Advanced Materials (2015), 27:5455–5476.
[2] J. C. Weaver, G. W. Milliron, A. Miserez, K. Evans-Lutterodt, S. Herrera, I. Gallana, W. J. Mershon, B. Swanson, P. Zavattieri, E. DiMasi and D. Kisailus, Science (2012), 336:1275–1280.
[3] P. Romano, H. Fabritius and D. Raabe, Acta Biomaterialia (2007) 3:301-309.
[4] Y. Zhang, P. De Falco, Y.Wang, E. Barbieri, O. Paris, N. J. Terrill, G. Falkenberg, N. M. Pugno and H. S. Gupta, Nanoscale (2017), 9:11249
[5] Y. Zhang, O. Paris, N. J. Terrill and H. S. Gupta, Scientific Reports (2016), 6:26249.

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