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Nanostructure and Nanomechanics of Stomatopod Cuticle Nanostructure and nanomechanics of stomatopod cuticle Yi Zhang A thesis submitted for the degree of Doctor of Philosophy School of Engineering and Materials Science Queen Mary University of London October 2015 Declaration I, Yi Zhang, confirm that the research included within this thesis is my own work or that where it has been carried out in collaboration with, or supported by others, that this is duly acknowledged below and my contribution indicated. Previously published material is also acknowledged below. I attest that I have exercised reasonable care to ensure that the work is original, and does not to the best of my knowledge break any UK law, infringe any third party’s copyright or other Intellectual Property Right, or contain any confidential material. I accept that the College has the right to use plagiarism detection software to check the electronic version of the thesis. I confirm that this thesis has not been previously submitted for the award of a degree by this or any other university. The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without the prior written consent of the author. Signature: Date: 2 Abstract Crustacean cuticle has attracted extensive attention for biomimetic purposes due to its outstanding mechanical properties including high toughness and stiffness. The mantis shrimp (stomatopod) telson is an extreme example, structurally optimized for dynamic loading at high impact forces. Alpha-chitin fibrillar building blocks play a key role in determining the overall mechanical properties due to its hierarchical design across all length scales. Synchrotron X-ray diffraction combined with in-situ mechanical testing was employed to investigate the structural and mechanical responses in telson cuticle at different hierarchical levels. The stomatopod tergite was used as a reference to learn how the structural and mechanical design will be correlated to the morphological changes in telson. In the thesis, we developed a novel three dimensional fibre orientation reconstruction method using mathematical models. The method was used to determine the orientation and intensity distributions of both the in-plane and out-of- plane mineralised chitin fibres from the two dimensional synchrotron X-ray diffraction scans collected from telson and tergite samples. Subsequently, in-situ tensile tests were performed on tergite cuticle to study the deformation and reorientation mechanisms of chitin fibres in the Bouligand layers comprising the bulk of the tergite, by tracing the variation of lattice spacing of the (002) peaks (along fibril direction) and (110) peaks (perpendicular to the fibril) found in the X-ray diffraction spectrum of α-Chitin. Finally, in-situ four-point bending tests were conducted to study how morphological changes contribute to the nanomechanical properties of telson across the entire tissue cross-section. Pre-strains were identified in the cuticle in static states, and vary according to the morphological position. Under loading, fibrils near physiological impact site deformed more than those in adjacent region, demonstrating different roles in energy dissipation in telson. These above findings provide useful guidelines for designing synthetic composite materials that resist repetitive impact loading. 4 Acknowledgements First and foremost, I would like to express my sincere gratitude to my supervisor Dr. Himadri Gupta for his unconditional support and assistance in bringing this project to fruition. By giving me the chance to be involved in such a fascinating project, I have gained invaluable knowledge on multiple scientific areas from him. Without his encouragement and guidance throughout the last four years I would not have been able to complete the project. I would also like to thank the School of Engineering and Materials Science (SEMS) at Queen Mary University of London (QMUL) and the Chinese Scholarship Council (CSC) for providing financial support for the PhD project. I could not have completed the project without the kind assistance of all the synchrotron scientists in I22 beamline of Diamond Light Source (UK), ESRF (France) and BESSY (Germany). Their technique supports were an essential ingredient for my thesis. My gratitude is also extended to Professor Nicola Pugno, Dr Ettore Barbieri, and Paolino De Falco for their help on the modelling work, and Professor Asa Barber, Dr Graham Davis, Professor Gleb Sukhorukov and Dr Nick Terrill for the cooperation in different stages of my project. I must also acknowledge the technicians at the SEMS workshop – Dougie Thomson, Dennis Ife and Vince Ford – who all offered help in designing and manufacturing the mechanical testers, and Jun Ma who has been extremely helpful in designing the mechanical testing programmes and the image correlation software. My appreciation must also go to the administration team in the SEMS office. You have 5 done such a good job in providing administrative support, so we could focus on our research. I am also grateful to all my colleagues in the research group, including Li, Jingyi, Sheetal, Angelo, Liisa, and Yiran. Without their kind friendship and help I could not have achieved this goal. My journey would not have been made so enjoyable without my friends, including Menglong, Chen, Mark, Shaz and Fabio; especially my roommate Simon, who has helped me so much during my time in London. Last, but certainly not least, I must give tremendous and deep thanks to my family. They have always been there whenever I needed support and company. My achievement means nothing without them. 6 Publications, Poster presentations Following papers were published or presented at scientific meetings based the work presented in this thesis: Publications Y Zhang, O Paris, NJ Terrill, and HS Gupta. The three- dimensional gradients in fibrillar orientation in an impact- resistant biological armour. Scientific Reports. 2016, doi:10.1038/srep26249. Y Zhang, E Barbieri, O Paris, AH Barber, GB Sukhorukov, NJ Terrill, NM Pugno, and HS Gupta. Angle dependent fibrillar strain and reorientation in the lamellae of a biological composite: the case of stomatopod cuticle. 2016 (in preparation) Y Zhang, E Barbieri, O Paris, AH Barber, GB Sukhorukov, NJ Terrill, NM Pugno, and HS Gupta. Morphologically correlated prestrain distribution optimized for high energy dissipation in the stomatopod telson. 2016 (in preparation) Poster presentation (including accepted abstracts) Y Zhang, O Paris, AH Barber, GB Sukhorukov, NJ Terrill, and HS Gupta. Nanostructure of Biocomposites optimized for Dynamic Mechanical Loading: Mechanisms and Emulation. Poster presented at the SEMS Research Graduate Poster Show/Industrial Liaison Forum. 14/11/2012, London,UK Y Zhang, E Barbieri, O Paris, AH Barber, GB Sukhorukov, NJ Terrill, NM Pugno, and HS Gupta. Microscale fibre orientation and mechanics in a natural biological mechanical shield: synchrotron X-ray mapping of the mantis shrimp telson. Poster presented at the 5th International Conference on the Mechanics of Biomaterials and Tissues, 08-13/December/2013, Sitges, Spain. Y Zhang, E Barbieri, O Paris, AH Barber, GB Sukhorukov, NJ Terrill, NM Pugno, and HS Gupta. 3D chitin fibre orientation reconstruction from 2D WAXD pattern. Poster presented at Synchrotron User Meeting at Diamond Light Source, September 04-05/2013, Harwell, UK. Y Zhang, E Barbieri, O Paris, AH Barber, GB Sukhorukov, NJ Terrill, NM Pugno, and HS Gupta. 3D chitin fibre reconstruction from 2D WAXD pattern. Poster will be presented at 2015 MRS Fall Meeting & Exhibit, December 01-06/2015, Boston, USA. 8 List of Abbreviations SEM Scanning electron microscopy TEM Transmission electron microscopy Micro-CT X-ray microtomography measurements SAXS Small Angle X-ray Scattering WAXD Wide Angle X-ray diffraction FWHM Full width at half maximum IR Infra-red spectroscopy LINAC Linear accelerator FESEM Field-emission scanning electron microscopy IP In-plane OP Out-of-plane DIC Digital image correlation 3D Three dimensional 2D Two dimensional 13 C NMR Carbon-13 nuclear magnetic resonance ACC Amorphous calcium carbonate ACP Amorphous calcium phosphate FAP Fluoroapatite (FAP) HAP Hydroxyl apatite 9 CAS Calcium sulphate DOC Dactyl club outer layer DIC Dactyl club inner layer SEMS School of Engineering and Materials Science QMUL Queen Mary University of London BESSY Berliner Elektronenspeicherring-Gesellschaft für Synchrotronstrahlung ESRF European Synchrotron Radiation Facility XRF X-ray fluorescence 10 List of figures Figure 1. 1. Image of mantis shrimp from website................................................26 Figure 1. 2. An overview of thesis structure and timeline of my PhD project. The blue arrows in the left indicate synchrotron beam times…………………………30 Figure 2.1. Hierarchical microstructure of the cuticle of the lobster………….. ..36 Figure 2.2. Chemical structures of chitin (a) and cellulose (b), and examples for cubic(c), orthorhombic(d) and monoclinic (e) crystal system…………………...37 Figure 2.3. Crystal structure and unit cell of α-chitin viewed normal to the bc- plane (top) and the ab-plane (bottom). The hydrogen bonds were indicated by dotted lines……………………………………………………………………………..…39 Figure 2.4. Synchrotron X-ray fibre diffraction diagram of the tendon of C. opilio recorded.The reflections which are usually used to measure the deformation of crystal lattice were indicated by red dashed rectangles………………………….40 Figure 2.5. Arrangement of the protein subunits around the chitin core from two viewing
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