1932

Abstract

Nature assembles weak organic and inorganic constituents into sophisticated hierarchical structures, forming structural composites that demonstrate impressive combinations of strength and toughness. Two such composites are the nacre structure forming the inner layer of many mollusk shells, whose brick-and-mortar architecture has been the gold standard for biomimetic composites, and the cuticle forming the arthropod exoskeleton, whose helicoidal fiber-reinforced architecture has only recently attracted interest for structural biomimetics. In this review, we detail recent biomimetic efforts for the fabrication of strong and tough composite materials possessing the brick-and-mortar and helicoidal architectures. Techniques discussed for the fabrication of nacre- and cuticle-mimetic structures include freeze casting, layer-by-layer deposition, spray deposition, magnetically assisted slip casting, fiber-reinforced composite processing, additive manufacturing, and cholesteric self-assembly. Advantages and limitations to these processes are discussed, as well as the future outlook on the biomimetic landscape for structural composite materials.

Keyword(s): biomimeticcompositecuticlehelicoidnacre
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2018-04-20
2024-04-19
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Literature Cited

  1. Roco MC. 1.  2011. The long view of nanotechnology development: the National Nanotechnology Initiative at 10 years. J. Nanopart. Res. 13:427–45 [Google Scholar]
  2. Holdren JP. 2.  2011. Materials genome initiative for global competitiveness Rep., Nat. Sci. Technol. Counc., Off. Sci. Technol. Policy Washington, DC:
  3. Meng J, Zhang P, Wang S. 3.  2015. Recent progress of abrasion-resistant materials: learning from nature. Chem. Soc. Rev. 45:237–51 [Google Scholar]
  4. De Yoreo JJ. 4.  2014. Mimicking biomineral systems: What have we achieved and where do we go from here?. Bio-Inspired Nanotechnology MR Knecht, TR Walsh 291–314 New York: Springer [Google Scholar]
  5. Wang J, Cheng Q, Tang Z. 5.  2012. Layered nanocomposites inspired by the structure and mechanical properties of nacre. Chem. Soc. Rev. 41:1111–29Wang et al. survey biomimetic efforts to fabricate layered nanocomposites inspired by nacre and discuss advantages and disadvantages of such strategies. [Google Scholar]
  6. Yao H-B, Fang H-Y, Wang X-H, Yu S-H. 6.  2011. Hierarchical assembly of micro-/nano-building blocks: bio-inspired rigid structural functional materials. Chem. Soc. Rev. 40:3764–85Yao et al. discuss hierarchical biological structures and review assembly techniques for fabricating bio-inspired rigid functional materials. [Google Scholar]
  7. Deville S. 7.  2008. Freeze-casting of porous ceramics: a review of current achievements and issues. Adv. Eng. Mater. 10:155–69 [Google Scholar]
  8. Addadi L, Gal A, Faivre D, Scheffel A, Weiner S. 8.  2015. Control of biogenic nanocrystal formation in biomineralization. Isr. J. Chem. 56:227–41 [Google Scholar]
  9. Studart AR. 9.  2016. Additive manufacturing of biologically-inspired materials. Chem. Soc. Rev. 45:359–76 [Google Scholar]
  10. Wegst UG, Bai H, Saiz E, Tomsia AP, Ritchie RO. 10.  2015. Bioinspired structural materials. Nat. Mater. 14:23–36 [Google Scholar]
  11. Naleway SE, Porter MM, McKittrick J, Meyers MA. 11.  2015. Structural design elements in biological materials: application to bioinspiration. Adv. Mater. 27:5455–76 [Google Scholar]
  12. Meyers MA, McKittrick J, Chen P-Y. 12.  2013. Structural biological materials: critical mechanics–materials connections. Science 339:773–79 [Google Scholar]
  13. Chen P-Y, McKittrick J, Meyers MA. 13.  2012. Biological materials: functional adaptations and bioinspired designs. Prog. Mater. Sci. 57:1492–704 [Google Scholar]
  14. Meyers MA, Chen P-Y, Lin AY-M, Seki Y. 14.  2008. Biological materials: structure and mechanical properties. Prog. Mater. Sci. 53:1–206 [Google Scholar]
  15. Fratzl P, Weinkamer R. 15.  2007. Nature's hierarchical materials. Prog. Mater. Sci. 52:1263–334 [Google Scholar]
  16. Kisailus D, Truong Q, Amemiya Y, Weaver JC, Morse DE. 16.  2006. Self-assembled bifunctional surface mimics an enzymatic and templating protein for the synthesis of a metal oxide semiconductor. PNAS 103:5652–57 [Google Scholar]
  17. Kisailus D, Najarian M, Weaver JC, Morse DE. 17.  2005. Functionalized gold nanoparticles mimic catalytic activity of a polysiloxane‐synthesizing enzyme. Adv. Mater. 17:1234–39 [Google Scholar]
  18. Johnson JM, Kinsinger N, Sun C, Li D, Kisailus D. 18.  2012. Urease-mediated room-temperature synthesis of nanocrystalline titanium dioxide. J. Am. Chem. Soc. 134:13974–77 [Google Scholar]
  19. Kisailus D, Choi JH, Weaver JC, Yang W, Morse DE. 19.  2005. Enzymatic synthesis and nanostructural control of gallium oxide at low temperature. Adv. Mater. 17:314–18 [Google Scholar]
  20. Sumerel JL, Yang W, Kisailus D, Weaver JC, Choi JH, Morse DE. 20.  2003. Biocatalytically templated synthesis of titanium dioxide. Chem. Mater. 15:4804–9 [Google Scholar]
  21. Yao H-B, Ge J, Mao L-B, Yan Y-X, Yu S-H. 21.  2014. Artificial carbonate nanocrystals and layered structural nanocomposites inspired by nacre: synthesis, fabrication and applications. Adv. Mater. 26:163–88Yao et al. discuss routes to fabricate and applications of artificial carbonate nanocrystals and layered structural nanocomposites inspired by nacre. [Google Scholar]
  22. Espinosa HD, Rim JE, Barthelat F, Buehler MJ. 22.  2009. Merger of structure and material in nacre and bone—perspectives on de novo biomimetic materials. Prog. Mater. Sci. 54:1059–100 [Google Scholar]
  23. Weaver JC, Milliron GW, Miserez A, Evans-Lutterodt K, Herrera S. 23.  et al. 2012. The stomatopod dactyl club: a formidable damage-tolerant biological hammer. Science 336:1275–80 [Google Scholar]
  24. Nudelman F. 24.  2015. Nacre biomineralisation: a review on the mechanisms of crystal nucleation. Semin. Cell Dev. Biol. 46:2–10 [Google Scholar]
  25. Jackson AP, Vincent JFV, Turner RM. 25.  1988. The mechanical design of nacre. Proc. R. Soc. B 234:415–40 [Google Scholar]
  26. Currey JD, Taylor JD. 26.  1974. The mechanical behaviour of some molluscan hard tissues. J. Zool. 173:395–406 [Google Scholar]
  27. Song F, Soh AK, Bai YL. 27.  2003. Structural and mechanical properties of the organic matrix layers of nacre. Biomaterials 24:3623–31 [Google Scholar]
  28. Wang RZ, Suo Z, Evans AG, Yao N, Aksay IA. 28.  2001. Deformation mechanisms in nacre. J. Mater. Res. 16:2485–93 [Google Scholar]
  29. Wang RZ, Wen HB, Cui FZ, Zhang HB, Li HD. 29.  1995. Observations of damage morphologies in nacre during deformation and fracture. J. Mater. Sci. 30:2299–304 [Google Scholar]
  30. Meyers MA, Lin AY-M, Chen P-Y, Muyco J. 30.  2008. Mechanical strength of abalone nacre: role of the soft organic layer. J. Mech. Behav. Biomed. Mater. 1:76–85 [Google Scholar]
  31. Barthelat F, Espinosa HD. 31.  2007. An experimental investigation of deformation and fracture of nacre–mother of pearl. Exp. Mech. 47:311–24 [Google Scholar]
  32. Wang R, Gupta HS. 32.  2011. Deformation and fracture mechanisms of bone and nacre. Annu. Rev. Mater. Res. 41:41–73 [Google Scholar]
  33. Espinosa HD, Juster AL, Latourte FJ, Loh OY, Gregoire D, Zavattieri PD. 33.  2011. Tablet-level origin of toughening in abalone shells and translation to synthetic composite materials. Nat. Commun. 2:173 [Google Scholar]
  34. Barthelat F, Li C-M, Comi C, Espinosa HD. 34.  2006. Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21:1977–86 [Google Scholar]
  35. Sarikaya M, Gunnison K, Yasrebi M, Aksay I. 35.  1989. Mechanical property-microstructural relationships in abalone shell. MRS Proc 174:109 [Google Scholar]
  36. Jackson AP, Vincent JFV, Turner RM. 36.  1988. The mechanical design of nacre. Proc. R. Soc. B 234:415–40 [Google Scholar]
  37. Nudelman F, Gotliv BA, Addadi L, Weiner S. 37.  2006. Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. J. Struct. Biol. 153:176–87 [Google Scholar]
  38. Checa AG, Cartwright JH, Willinger M-G. 38.  2011. Mineral bridges in nacre. J. Struct. Biol. 176:330–39 [Google Scholar]
  39. Olson IC, Gilbert PUPA. 39.  2012. Aragonite crystal orientation in mollusk shell nacre may depend on temperature. The angle spread of crystalline aragonite tablets records the water temperature at which nacre was deposited by Pinctada margaritifera. . Faraday Discuss 159:421–32 [Google Scholar]
  40. Gilbert PUPA, Metzler RA, Zhou D, Scholl A, Doran A. 40.  et al. 2008. Gradual ordering in red abalone nacre. J. Am. Chem. Soc. 130:17519–27 [Google Scholar]
  41. Lin AY-M, Chen P-Y, Meyers MA. 41.  2008. The growth of nacre in the abalone shell. Acta Biomater 4:131–38 [Google Scholar]
  42. Cartwright JH, Checa AG. 42.  2007. The dynamics of nacre self-assembly. J. R. Soc. Interface 4:491–504 [Google Scholar]
  43. Addadi L, Joester D, Nudelman F, Weiner S. 43.  2006. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chem. Eur. J. 12:980–87 [Google Scholar]
  44. Heinemann F, Launspach M, Gries K, Fritz M. 44.  2011. Gastropod nacre: structure, properties and growth—biological, chemical and physical basics. Biophys. Chem. 153:126–53 [Google Scholar]
  45. Cheng Q, Jiang L, Tang Z. 45.  2014. Bioinspired layered materials with superior mechanical performance. Acc. Chem. Res. 47:1256–66Cheng et al. review recent efforts to fabricate nacre-inspired layered composites with superior mechanical performance, with a focus on nanoscale carbon materials. [Google Scholar]
  46. Deville S, Saiz E, Nalla RK, Tomsia AP. 46.  2006. Freezing as a path to build complex composites. Science 311:515–18 [Google Scholar]
  47. Worster M, Wettlaufer J. 47.  1997. Natural convection, solute trapping, and channel formation during solidification of saltwater. J. Phys. Chem. B 101:6132–36 [Google Scholar]
  48. Munch E, Launey ME, Alsem DH, Saiz E, Tomsia AP, Ritchie RO. 48.  2008. Tough, bio-inspired hybrid materials. Science 322:1516–20 [Google Scholar]
  49. Bouville F, Maire E, Meille S, Van de Moortèle B, Stevenson AJ, Deville S. 49.  2014. Strong, tough and stiff bioinspired ceramics from brittle constituents. Nat. Mater. 13:508–14 [Google Scholar]
  50. Bai H, Chen Y, Delattre B, Tomsia AP, Ritchie RO. 50.  2015. Bioinspired large-scale aligned porous materials assembled with dual temperature gradients. Sci. Adv. 1:e1500849 [Google Scholar]
  51. Bai H, Walsh F, Gludovatz B, Delattre B, Huang C. 51.  et al. 2016. Bioinspired hydroxyapatite/poly(methyl methacrylate) composite with a nacre-mimetic architecture by a bidirectional freezing method. Adv. Mater. 28:50–56 [Google Scholar]
  52. Podsiadlo P, Kaushik AK, Arruda EM, Waas AM, Shim BS. 52.  et al. 2007. Ultrastrong and stiff layered polymer nanocomposites. Science 318:80–83 [Google Scholar]
  53. Wang J, Qiao J, Wang J, Zhu Y, Jiang L. 53.  2015. Bioinspired hierarchical alumina–graphene oxide–poly(vinyl alcohol) artificial nacre with optimized strength and toughness. ACS Appl. Mater. Interfaces 7:9281–86 [Google Scholar]
  54. Behr S, Vainio U, Müller M, Schreyer A, Schneider GA. 54.  2015. Large-scale parallel alignment of platelet-shaped particles through gravitational sedimentation. Sci. Rep. 5:9984 [Google Scholar]
  55. Dwivedi G, Flynn K, Resnick M, Sampath S, Gouldstone A. 55.  2015. Bioinspired hybrid materials from spray-formed ceramic templates. Adv. Mater. 27:3073–78 [Google Scholar]
  56. Grunenfelder LK, de Obaldia EE, Wang Q, Li D, Weden B. 56.  et al. 2014. Stress and damage mitigation from oriented nanostructures within the radular teeth of Cryptochiton stelleri. . Adv. Funct. Mater. 24:6093–104 [Google Scholar]
  57. Wang Q, Nemoto M, Li D, Weaver JC, Weden B. 57.  et al. 2013. Phase transformations and structural developments in the radular teeth of Cryptochiton stelleri. . Adv. Funct. Mater. 23:2908–17 [Google Scholar]
  58. Yaraghi NA, Guarín-Zapata N, Grunenfelder LK, Hintsala E, Bhowmick S. 58.  et al. 2016. A sinusoidally architected helicoidal biocomposite. Adv. Mater. 28:6835–44 [Google Scholar]
  59. Amini S, Tadayon M, Idapalapati S, Miserez A. 59.  2015. The role of quasi-plasticity in the extreme contact damage tolerance of the stomatopod dactyl club. Nat. Mater. 14:943–50 [Google Scholar]
  60. Le Ferrand H, Bouville F, Niebel TP, Studart AR. 60.  2015. Magnetically assisted slip casting of bioinspired heterogeneous composites. Nat. Mater. 14:1172–79 [Google Scholar]
  61. Niebel TP, Bouville F, Kokkinis D, Studart AR. 61.  2016. Role of the polymer phase in the mechanics of nacre-like composites. J. Mech. Phys. Solids 96:133–46 [Google Scholar]
  62. Finnemore A, Cunha P, Shean T, Vignolini S, Guldin S. 62.  et al. 2012. Biomimetic layer-by-layer assembly of artificial nacre. Nat. Commun. 3:966 [Google Scholar]
  63. Gower LB, Odom DJ. 63.  2000. Deposition of calcium carbonate films by a polymer-induced liquid-precursor (PILP) process. J. Cryst. Growth 210:719–34 [Google Scholar]
  64. Gower LB. 64.  2008. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108:4551–627 [Google Scholar]
  65. Olszta MJ, Odom DJ, Douglas EP, Gower LB. 65.  2009. A new paradigm for biomineral formation: mineralization via an amorphous liquid-phase precursor. Connect. Tissue Res. 44:Suppl. 1326–34 [Google Scholar]
  66. Mao LB, Gao HL, Yao HB, Liu L, Colfen H. 66.  et al. 2016. Synthetic nacre by predesigned matrix-directed mineralization. Science 354:107–10 [Google Scholar]
  67. Raabe D, Sachs C, Romano P. 67.  2005. The crustacean exoskeleton as an example of a structurally and mechanically graded biological nanocomposite material. Acta Mater 53:4281–92 [Google Scholar]
  68. Bouligand Y. 68.  1972. Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell 4:189–217 [Google Scholar]
  69. Chen P-Y, Lin AY-M, McKittrick J, Meyers MA. 69.  2008. Structure and mechanical properties of crab exoskeletons. Acta Biomater 4:587–96 [Google Scholar]
  70. Paris O, Hartmann MA, Fritz-Popovski G. 70.  2013. The mineralized crustacean cuticle: hierarchical structure and mechanical properties. Materials Design Inspired by Nature: Function Through Inner Architecture P Fratzl, JWC Dunlop, R Weinkamer 180–96 Cambridge, UK: R. Soc. Chem. [Google Scholar]
  71. Fabritius H, Sachs C, Raabe D, Nikolov S, Friák M, Neugebauer J. 71.  2011. Chitin in the exoskeletons of arthropoda: from ancient design to novel materials science. Chitin: Formation and Diagenesis NS Gupta 35–60 Dordrecht, Neth.: Springer [Google Scholar]
  72. Bentov S, Abehsera S, Sagi A. 72.  2016. The mineralized exoskeletons of crustaceans. Extracellular Composite Matrices in Arthropods E Cohen, B Moussian 137–63 Cham, Switz.: Springer [Google Scholar]
  73. Luquet G. 73.  2012. Biomineralizations: insights and prospects from crustaceans. ZooKeys 176:103–21 [Google Scholar]
  74. Grunenfelder LK, Herrera S, Kisailus D. 74.  2014. Crustacean-derived biomimetic components and nanostructured composites. Small 10:3207–32 [Google Scholar]
  75. Sachs C, Fabritius H, Raabe D. 75.  2008. Influence of microstructure on deformation anisotropy of mineralized cuticle from the lobster Homarus americanus. . J. Struct. Biol. 161:120–32 [Google Scholar]
  76. Zimmermann EA, Ritchie RO. 76.  2015. Bone as a structural material. Adv. Healthc. Mater. 4:1286 [Google Scholar]
  77. Zimmermann EA, Gludovatz B, Schaible E, Dave NK, Yang W. 77.  et al. 2013. Mechanical adaptability of the Bouligand-type structure in natural dermal armour. Nat. Commun. 4:2634 [Google Scholar]
  78. Lichtenegger H, Müller M, Paris O, Riekel C, Fratzl P. 78.  1999. Imaging of the helical arrangement of cellulose fibrils in wood by synchrotron X-ray microdiffraction. J. Appl. Crystallogr. 32:1127–33 [Google Scholar]
  79. Wagermaier W, Gupta HS, Gourrier A, Burghammer M, Roschger P, Fratzl P. 79.  2006. Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1:1–5 [Google Scholar]
  80. Weinkamer R, Fratzl P. 80.  2011. Mechanical adaptation of biological materials—the examples of bone and wood. Mater. Sci. Eng. C 31:1164–73 [Google Scholar]
  81. Nikolov S, Petrov M, Lymperakis L, Friák M, Sachs C. 81.  et al. 2010. Revealing the design principles of high-performance biological composites using ab initio and multiscale simulations: the example of lobster cuticle. Adv. Mater. 22:519–26 [Google Scholar]
  82. Gupta H, Stachewicz U, Wagermaier W, Roschger P, Wagner H, Fratzl P. 82.  2006. Mechanical modulation at the lamellar level in osteonal bone. J. Mater. Res. 21:1913–21 [Google Scholar]
  83. Fratzl P, Gupta HS, Fischer FD, Kolednik O. 83.  2007. Hindered crack propagation in materials with periodically varying Young's modulus—lessons from biological materials. Adv. Mater. 19:2657–61 [Google Scholar]
  84. Kolednik O, Predan J, Fischer FD, Fratzl P. 84.  2011. Bioinspired design criteria for damage-resistant materials with periodically varying microstructure. Adv. Funct. Mater. 21:3634–41 [Google Scholar]
  85. Launey ME, Buehler MJ, Ritchie RO. 85.  2010. On the mechanistic origins of toughness in bone. Annu. Rev. Mater. Res. 40:25–53 [Google Scholar]
  86. Mouritz AP. 86.  2007. Review of Z-pinned composite laminates. Composites A 38:2383–97 [Google Scholar]
  87. Guarín-Zapata N, Gomez J, Yaraghi N, Kisailus D, Zavattieri PD. 87.  2015. Shear wave filtering in naturally-occurring Bouligand structures. Acta Biomater 23:11–20 [Google Scholar]
  88. Roer R, Dillaman R. 88.  1984. The structure and calcification of the crustacean cuticle. Am. Zool. 24:893–909 [Google Scholar]
  89. Chockalingam S. 89.  1971. Studies on enzymes associated with calcification of the cuticle of the hermit crab Clibanarius olivaceous. . Mar. Biol. 10:169–82 [Google Scholar]
  90. Luquet G, Dauphin Y, Percot A, Salomé M, Ziegler A. 90.  et al. 2016. Calcium deposits in the crayfish, Cherax quadricarinatus: microstructure versus elemental distribution. Microsc. Microanal. 22:22–38 [Google Scholar]
  91. Sachs C, Fabritius H, Raabe D. 91.  2006. Hardness and elastic properties of dehydrated cuticle from the lobster Homarus americanus obtained by nanoindentation. J. Mater. Res. 21:1987–95 [Google Scholar]
  92. Fabritius H, Karsten ES, Balasundaram K, Hild S, Huemer K, Raabe D. 92.  2012. Correlation of structure, composition and local mechanical properties in the dorsal carapace of the edible crab Cancer pagurus. . Z. Kristall. 227:766–76 [Google Scholar]
  93. Aizenberg J, Addadi L, Weiner S, Lambert G. 93.  1996. Stabilization of amorphous calcium carbonate by specialized macromolecules in biological and synthetic precipitates. Adv. Mater. 8:222–26 [Google Scholar]
  94. Loste E, Wilson RM, Seshadri R, Meldrum FC. 94.  2003. The role of magnesium in stabilising amorphous calcium carbonate and controlling calcite morphologies. J. Cryst. Growth 254:206–18 [Google Scholar]
  95. Politi Y, Batchelor DR, Zaslansky P, Chmelka BF, Weaver JC. 95.  et al. 2009. Role of magnesium ion in the stabilization of biogenic amorphous calcium carbonate: a structure–function investigation. Chem. Mater. 22:161–66 [Google Scholar]
  96. Bentov S, Zaslansky P, Al-Sawalmih A, Masic A, Fratzl P. 96.  et al. 2012. Enamel-like apatite crown covering amorphous mineral in a crayfish mandible. Nat. Commun. 3:839 [Google Scholar]
  97. Amini S, Masic A, Bertinetti L, Teguh JS, Herrin JS. 97.  et al. 2014. Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages. Nat. Commun. 5:3187 [Google Scholar]
  98. Moreno EC, Kresak M, Zahradnik RT. 98.  1974. Fluoridated hydroxyapatite solubility and caries formation. Nature 247:64–65 [Google Scholar]
  99. Okazaki M, Tohda H, Yanagisawa T, Taira M, Takahashi J. 99.  1998. Differences in solubility of two types of heterogeneous fluoridated hydroxyapatites. Biomaterials 19:611–16 [Google Scholar]
  100. Menéndez-Proupin E, Cervantes-Rodríguez S, Osorio-Pulgar R, Franco-Cisterna M, Camacho-Montes H, Fuentes ME. 100.  2011. Computer simulation of elastic constants of hydroxyapatite and fluorapatite. J. Mech. Behav. Biomed. Mater. 4:1011–20 [Google Scholar]
  101. Politi Y, Priewasser M, Pippel E, Zaslansky P, Hartmann J. 101.  et al. 2012. A spider's fang: how to design an injection needle using chitin-based composite material. Adv. Funct. Mater. 22:2519–28 [Google Scholar]
  102. Schofield RMS, Nesson MH, Richardson KA, Wyeth P. 102.  2003. Zinc is incorporated into cuticular “tools” after ecdysis: the time course of the zinc distribution in “tools” and whole bodies of an ant and a scorpion. J. Insect Physiol. 49:31–44 [Google Scholar]
  103. Schofield RMS, Nesson MH, Richardson KA. 103.  2002. Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Naturwissenschaften 89:579–83 [Google Scholar]
  104. Cribb BW, Stewart A, Huang H, Truss R, Noller B. 104.  et al. 2008. Insect mandibles—comparative mechanical properties and links with metal incorporation. Naturwissenschaften 95:17–23 [Google Scholar]
  105. Schofield RM, Lefevre HW. 105.  1992. PIXE-STIM microtomography: zinc and manganese concentrations in a scorpion stinger. Nucl. Instrum. Methods Phys. Res. 72:104–10 [Google Scholar]
  106. Cheng L, Thomas A, Glancey JL, Karlsson AM. 106.  2011. Mechanical behavior of bio-inspired laminated composites. Composites A 42:211–20 [Google Scholar]
  107. Grunenfelder LK, Suksangpanya N, Salinas C, Milliron G, Yaraghi N. 107.  et al. 2014. Bio-inspired impact-resistant composites. Acta Biomater 10:3997–4008 [Google Scholar]
  108. Ladani RB, Ravindran AR, Wu S, Pingkarawat K, Kinloch AJ. 108.  et al. 2016. Multi-scale toughening of fibre composites using carbon nanofibres and Z-pins. Compos. Sci. Technol. 131:98–109 [Google Scholar]
  109. Gao W, Zhang Y, Ramanujan D, Ramani K, Chen Y. 109.  et al. 2015. The status, challenges, and future of additive manufacturing in engineering. Comput.-Aided Des. 69:65–89 [Google Scholar]
  110. Ang TH, Sultana FSA, Hutmacher DW, Wong YS, Fuh JYH. 110.  et al. 2002. Fabrication of 3D chitosan–hydroxyapatite scaffolds using a robotic dispensing system. Mater. Sci. Eng. C 20:35–42 [Google Scholar]
  111. Geng L, Feng W, Hutmacher DW, Wong YS, Loh HT, Fuh JY. 111.  2005. Direct writing of chitosan scaffolds using a robotic system. Rapid Prototyp. J. 11:90–97 [Google Scholar]
  112. Dellinger JG, Cesarano J, Jamison RD. 112.  2007. Robotic deposition of model hydroxyapatite scaffolds with multiple architectures and multiscale porosity for bone tissue engineering. J. Biomed. Mater. Res. A 82A:383–94 [Google Scholar]
  113. Almeida CR, Serra T, Oliveira MI, Planell JA, Barbosa MA, Navarro M. 113.  2014. Impact of 3-D printed PLA-and chitosan-based scaffolds on human monocyte/macrophage responses: unraveling the effect of 3-D structures on inflammation. Acta Biomater 10:613–22 [Google Scholar]
  114. Ribbans B, Li Y, Tan T. 114.  2016. A bioinspired study on the interlaminar shear resistance of helicoidal fiber structures. J. Mech. Behav. Biomed. Mater. 56:57–67 [Google Scholar]
  115. Milliron GW. 115.  2012. Lightweight impact-resistant composite materials: lessons from mantis shrimp PhD Thesis Univ. Calif. Riverside:
  116. Shopsowitz KE, Qi H, Hamad WY, MacLachlan MJ. 116.  2010. Free-standing mesoporous silica films with tunable chiral nematic structures. Nature 468:422–25 [Google Scholar]
  117. Majoinen J, Kontturi E, Ikkala O, Gray DG. 117.  2012. SEM imaging of chiral nematic films cast from cellulose nanocrystal suspensions. Cellulose 19:1599–605 [Google Scholar]
  118. Wang B, Walther A. 118.  2015. Self-assembled, iridescent, crustacean-mimetic nanocomposites with tailored periodicity and layered cuticular structure. ACS Nano 9:10637–46 [Google Scholar]
  119. Matsumura S, Kajiyama S, Nishimura T, Kato T. 119.  2015. Formation of helically structured chitin/CaCO3 hybrids through an approach inspired by the biomineralization processes of crustacean cuticles. Small 11:5127–33 [Google Scholar]
  120. Nan F, Chen Q, Liu P, Nagarajan S, Duan Y, Zhang J. 120.  2016. Iridescent graphene/cellulose nanocrystal film with water response and highly electrical conductivity. RSC Adv 6:93673–79 [Google Scholar]
  121. Nguyen T-D, Peres BU, Carvalho RM, MacLachlan MJ. 121.  2016. Photonic hydrogels from chiral nematic mesoporous chitosan nanofibril assemblies. Adv. Funct. Mater. 26:2875–81 [Google Scholar]
  122. Oh DX, Cha YJ, Nguyen H-L, Je HH, Jho YS. 122.  et al. 2016. Chiral nematic self-assembly of minimally surface damaged chitin nanofibrils and its load bearing functions. Sci. Rep. 6:23245 [Google Scholar]
  123. Zhu B, Merindol R, Benitez AJ, Wang B, Walther A. 123.  2016. Supramolecular engineering of hierarchically self-assembled, bioinspired, cholesteric nanocomposites formed by cellulose nanocrystals and polymers. ACS Appl. Mater. Interfaces 8:11031–40 [Google Scholar]
  124. Al-Sawalmih A, Li C, Siegel S, Fabritius H, Yi S. 124.  et al. 2008. Microtexture and chitin/calcite orientation relationship in the mineralized exoskeleton of the American lobster. Adv. Funct. Mater. 18:3307–14 [Google Scholar]
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