Structure and mechanical properties of selected protective systems in marine organisms

Materials Science and Engineering C

Volumn 59, Issue , 2016, Pages 1143-1167

  Naleway, Steven E ^a   Taylor, Jennifer R A ^b   Porter, Michael M ^e   Meyers, Marc A ^a,c,d   McKittrick, Joanna ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e Clemson University   (United States)

Author keywords

Bioinspired design; Marine organisms; Protective mechanisms; Structural biological materials

Indexed keywords

BIOLOGY; HYDROSTATIC PRESSURE; MARINE BIOLOGY; MECHANICAL PROPERTIES;

BASIC BUILDING BLOCK; BIO-INSPIRED DESIGNS; INTERTIDAL ZONES; MANGROVE FOREST; MARINE ORGANISMS; NATIVE ENVIRONMENT; PROTECTIVE SYSTEMS; SPECIFIC ENVIRONMENTAL CONDITIONS;

BIOLOGICAL MATERIALS;

BIOPOLYMER; MINERAL;

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL SHELL; AQUATIC SPECIES; MORPHOGENESIS; PHYSIOLOGY;

ANIMAL SHELLS; ANIMALS; AQUATIC ORGANISMS; BIOPOLYMERS; BODY PATTERNING; MINERALS;

EID: 84949599508     PISSN: 09284931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.msec.2015.10.033     Document Type: Review

References (228)

1. E. Arzt Biological and artificial attachment devices: lessons for materials scientists from flies and geckos Mater. Sci. Eng. C 26 2006 1245 1250
2. M.A. Meyers, J. McKittrick, and P.-Y. Chen Structural biological materials: critical mechanics-materials connections Science 339 2013 773 779
3. M.A. Meyers, P.-Y. Chen, M.I. Lopez, Y. Seki, and A.Y.M. Lin Biological materials: a materials science approach J. Mech. Behav. Biomed. Mater. 4 2011 626 657
4. M.A. Meyers, P.-Y. Chen, A.Y.M. Lin, and Y. Seki Biological materials: structure and mechanical properties Prog. Mater. Sci. 53 2008 1 206
5. P.-Y. Chen, J. McKittrick, and M.A. Meyers Biological materials: functional adaptations and bioinspired designs Prog. Mater. Sci. 57 2012 1492 1704
6. S.E. Naleway, M.M. Porter, J. McKittrick, and M.A. Meyers Structural design elements in biological materials: application to bioinspiration Adv. Mater. 27 2015 5455 5476
7. U.G.K. Wegst, and M.F. Ashby The mechanical efficiency of natural materials Philos. Mag. 84 2004 2167 2181
8. C. Mora, D.P. Tittensor, S. Adl, A.G.B. Simpson, and B. Worm How many species are there on earth and in the ocean? PLoS One 9 2011 e1001127
9. E. Munch, M.E. Launey, D.H. Alsem, E. Saiz, A.P. Tomsia, and R.O. Ritchie Tough, bio-inspired hybrid materials Science 322 2008 1516 1520
10. W.E.G. Müller, X.H. Wang, F.Z. Cui, K.P. Jochum, W. Tremel, J. Bill, H.C. Schroder, F. Natalio, U. Schlossmacher, and M. Wiens Sponge spicules as blueprints for the biofabrication of inorganic-organic composites and biomaterials Appl. Microbiol. Biotechnol. 83 2009 397 413
11. J. Aizenberg, V.C. Sundar, A.D. Yablon, J.C. Weaver, and G. Chen Biological glass fibers: correlation between optical and structural properties Proc. Natl. Acad. Sci. 101 2004 3358 3363
12. W. Yang, S.E. Naleway, M.M. Porter, M.A. Meyers, and J. McKittrick The armored carapace of the boxfish Acta Biomater. 23 2015 1 10
13. W. Yang, I.H. Chen, B. Gludovatz, E.A. Zimmermann, R.O. Ritchie, and M.A. Meyers Natural flexible dermal armor Adv. Mater. 25 2013 31 48
14. R.O. Ritchie The conflicts between strength and toughness Nat. Mater. 10 2011 817 822
15. J.D. Currey, and K. Brear Hardness, young's modulus and yield stress in mammalian mineralized tissues J. Mater. Sci. Mater. Med. 1 1990 14 20
16. R. Parenteau-Bareil, R. Gauvin, and F. Berthod Collagen-based biomaterials for tissue engineering applications Materials 3 2010 1863 1887
17. Y. Omura, N. Urano, and S. Kimura Occurrence of fibrillar collagen with structure of (alpha(1))(2) alpha(2) in the test of sea urchin Asthenosoma ijimai Comp. Biochem. Physiol. B 115 1996 63 68
18. T. Nagai, and N. Suzuki Partial characterization of collagen from purple sea urchin (Anthocidaris crassispina) test Int. J. Food Sci. Technol. 35 2000 497 501
19. S. Kimura, Y. Takema, and M. Kubota Octopus skin collagen - isolation and characterization of collagen comprising two distinct a chains J. Biol. Chem. 256 1981 3230 3234
20. S. Kimura, Y. Omura, M. Ishida, and H. Shirai Molecular characterization of fibrillar collagen from the body wall of starfish Asterias amurenis Comp. Biochem. Physiol. B 104 1993 663 668
21. S. Kimura, S. Miura, and Y.H. Park Collagen as the major edible component of jellyfish (Stomolophus nomural) J. Food Sci. 48 1983 1758 1760
22. S. Miura, and S. Kimura Jellyfish mesogloea collagen. Characterization of molecules as α1 α2 α3 heterotrimers J. Biol. Chem. 260 1985 5352 5356
23. S. Kimura, X.P. Zhu, R. Matsui, M. Shijoh, and S. Takamizawa Characterization of fish muscle type-I collagen J. Food Sci. 53 1988 1315 1318
24. T. Nagai, Y. Araki, and N. Suzuki Collagen of the skin of ocellate puffer fish (Takifugu rubripes) Food Chem. 78 2002 173 177
25. M.A. Meyers, Y.S. Lin, E.A. Olevsky, and P.-Y. Chen Battle in the Amazon: Arapaima versus piranha Adv. Biomater. 14 2012 B88 B279
26. M.P.E. Wenger, L. Bozec, M.A. Horton, and P. Masquida Mechanical properties of collagen fibrils Biophys. J. 93 2007 1255 1263
27. J.S. Graham, A.N. Vomund, C.L. Phillips, and M. Grandbois Structural changes in human type I collagen fibrils investigated by force spectroscopy Exp. Cell Res. 299 2004 335 342
28. H. Ehrlich Chitin and collagen as universal and alternative templates in biomineralization Int. Geol. Rev. 52 2010 661 699
29. W. Yang, V.R. Sherman, B. Gludovatz, M. Mackey, E.A. Zimmermann, E.H. Chang, E. Schaible, Z. Qin, M.J. Buehler, R.O. Ritchie, and M.A. Meyers Protective role of Arapaima gigas fish scales: structure and mechanical behavior Acta Biomater. 10 2014 3599 3614
30. J. McKittrick, P.-Y. Chen, S.G. Bodde, W. Yang, E.E. Novitskaya, and M.A. Meyers The structure, functions, and mechanical properties of keratin JOM 64 2012 449 468
31. J.G. Rouse, and M.E. Van Dyke A review of keratin-based biomaterials for biomedical applications Materials 3 2010 999 1014
32. E.A. Koch, R.H. Spitzer, R.B. Pithawalla, and F.A. Castillos Hagfish biopolymer: a type I/type II homologue of epidermal keratin intermediate filaments Int. J. Biol. Macromol. 17 1995 283 292
33. M. Feughelman Structural features of keratin suggested by its mechanical properties Biochim. Biophys. Acta 32 1959 596 597
34. R.D.B. Fraser, T.P. MacRae, D.A.D. Parry, and E. Suzuki Structure of beta-keratin Polymer 10 1969 810
35. M.W. Trim, M.F. Horstemeyer, H. Rhee, H. Le Kadiri, L.N. Williams, J. Liao, K.B. Walters, J. McKittrick, and S.J. Park The effects of water and microstructure on the mechanical properties of bighorn sheep (Ovis canadensis) horn keratin Acta Biomater. 7 2011 1228 1240
36. L. Tombolato, E.E. Novitskaya, P.-Y. Chen, F.A. Sheppard, and J. McKittrick Microstructure, elastic properties and deformation mechanisms of horn keratin Acta Biomater. 6 2010 319 330
37. H. Zahn, J. Fohles, M. Nienhaus, A. Schwan, and M. Spel Wool as a biological composite structure Ind. Eng. Chem. Prod. Res. Dev. 19 1980 496 501
38. S.L. Rosen Fundamental Principles of Polymeric Materials 2nd ed. 1993 John Wiley & Sons Inc. New York
39. M.A. Kennedy, A.J. Peacock, and L. Mandelkern Tensile properties of crystalline polymers - linear polyethylene Macromolecules 27 1994 5297 5310
40. M.N.V.R. Kumar A review of chitin and chitosan applications React. Funct. Polym. 46 2000 1 27
41. M. Rinaudo Chitin and chitosan: properties and applications Prog. Polym. Sci. 31 2006 603 632
42. A. Miserez, D. Rubin, and J.H. Waite Cross-linking chemistry of squid beak J. Biol. Chem. 285 2010 38115 38124
43. K.M. Rudall, and W. Kenchington The chitin system Biol. Rev. 48 1973 597 633
44. Y. Bouligand Twisted fiberous arrangements in biological materials and cholesteric mesophases Tissue Cell 4 1972 189 217
45. M.M. Giraud-Guille Fine structure of the chitin protein system in the crab cuticle Tissue Cell 16 1984 75 92
46. M.M. Giraud-Guille, H. Chanzy, and R. Vuong Chitin crystals in arthropod cuticles revealed by diffraction contrast transmission electron-microscopy J. Struct. Biol. 103 1990 232 240
47. M.M. Giraud-Guille Plywood structures in nature Curr. Opin. Solid State Mater. Sci. 3 1998 221 227
48. H. Ehrlich Biological Materials of Marine Origin: Springer 2015
49. M.N. Dean, and A.P. Summers Mineralized cartilage in the skeleton of chondrichthyan fishes Zoology 109 2006 164 168
50. A.G. Cole, and B.K. Hall Cartilage differentiation in cephalopod molluscs Zoology 112 2009 2 15
51. A.G. Cole, and B.K. Hall The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa Zoology 107 2004 261 273
52. P.-Y. Chen, D. Toroian, P.A. Price, and J. McKittrick Minerals form a continuum phase in mature cancellous bone Calcif. Tissue Int. 88 2011 351 361
53. S.V. Dorozhkin Calcium orthophosphates in nature, biology and medicine Materials 2 2009 399 498
54. S. Weiner, and H.D. Wangner The material bone: structure mechanical function relations Annu. Rev. Mater. Sci. 28 1998 271 298
55. E.E. Novitskaya, P.-Y. Chen, S. Lee, A.B. Castro-Cesena, G.A. Hirata, V.A. Lubarda, and J. McKittrick Anisotropy in the compressive mechanical properties of bovine cortical bone and the mineral and protein constituents Acta Biomater. 7 2011 3170 3177
56. W. Yang, I.H. Chen, J. McKittrick, and M.A. Meyers Flexible dermal armor in nature JOM 64 2012 475 485
57. M.M. Porter, J. McKittrick, and M.A. Meyers Biomimetic materials by freeze casting JOM 65 2013 720 727
58. M. Vallet-Regi, and J.M. Gonzalez-Calbet Calcium phosphates as substitution of bone tissues Prog. Solid State Chem. 32 2004 1 31
59. L.L. Hench Bioceramics - from concept to clinic J. Am. Ceram. Soc. 74 1991 1487 1510
60. L.L. Hench Bioceramics J. Am. Ceram. Soc. 81 1998 1705 1728
61. S. Deville, E. Saiz, R.K. Nalla, and A.P. Tomsia Freezing as a path to build complex composites Science 311 2006 515 518
62. M.J. Olszta, X.G. Cheng, S.S. Jee, R. Kumar, Y.Y. Kim, M.J. Kaufman, E.P. Douglas, and L.B. Gower Bone structure and formation: a new perspective Mater. Sci. Eng. R 58 2007 77 116
63. F. Nudelman, K. Pieterse, A. George, P.H.H. Bomans, H. Friedrich, L.J. Brylka, P.A.J. Hilbers, G. de With, and N.A.J.M. Sommerdijk The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors Nat. Mater. 9 2010 1004 1009
64. T. Ikoma, H. Kobayashi, J. Tanaka, D. Walsh, and S. Mann Microstructure, mechanical, and biomimetic properties of fish scales from Pagrus major J. Struct. Biol. 142 2003 327 333
65. P. Ducheyne, and Q. Qiu Bioactive ceramics: the effect of surface reactivity on bone formation and bone cell function Biomaterials 20 1999 2287 2303
66. G. Mayer Rigid biological systems as models for synthetic composites Science 310 2005 1144 1147
67. S. Blank, M. Arnoldi, S. Khoshnavaz, L. Treccani, M. Kuntz, K. Mann, G. Grathwohl, and M. Fritz The nacre protein perlucin nucleates growth of calcium carbonate crystals J. Microsc. (Oxford) 212 2003 280 291
68. F.C. Meldrum, and H. Colfen Controlling mineral morphologies and structures in biological and synthetic systems Chem. Rev. 108 2008 4332 4432
69. G. Wolf, E. Konigsberger, H.G. Schmidt, L.C. Konigsberger, and H. Gamsjager Thermodynamic aspects of the vaterite-calcite phase transition J. Therm. Anal. Calorim. 60 2000 463 472
70. G. Falini, S. Albeck, S. Weiner, and L. Addadi Control of aragonite or calcite polymorphism by mollusk shell macromolecules Science 271 1996 67 69
71. A.M. Belcher, X.H. Wu, R.J. Christensen, P.K. Hansma, G.D. Stucky, and D.E. Morse Control of crystal phase switching and orientation by soluble mollusc-shell proteins Nature 381 1996 56 58
72. X. Long, Y.R. Ma, and L.M. Qi Biogenic and synthetic high magnesium calcite - a review J. Struct. Biol. 185 2014 1 14
73. G. Falini, S. Fermani, M. Gazzano, and A. Ripamonti Biomimetic crystallization of calcium carbonate polymorphs by means of collagenous matrices Chem. Eur. J. 3 1997 1807 1814
74. R.M.S. Schofield, J.C. Niedbala, M.H. Nesson, Y. Tao, J.E. Shokes, R.A. Scott, and M.J. Latimer Br-rich tips of calcified crab claws are less hard but more fracture resistant: a comparison of mineralized and heavy-element biological materials J. Struct. Biol. 166 2009 272 287
75. B.W. Cribb, A. Rathmell, R. Charters, R. Rasch, H. Huang, and I.R. Tibbetts Structure, composition and properties of naturally occurring non-calcified crustacean cuticle Arthropod Struct. Dev. 38 2009 173 178
76. C.C. Perry, and T. Keeling-Tucker Biosilicification: the role of the organic matrix in structure control J. Biol. Inorg. Chem. 5 2000 537 550
77. E. Epstein Silicon: its manifold roles in plants Ann. Appl. Biol. 155 2009 155 160
78. P.W. Lucas, I.M. Turner, N.J. Dominy, and N. Yamashita Mechanical defences to herbivory Ann. Bot. 86 2000 913 920
79. I.C. Gebeshuber, J.H. Kindt, J.B. Thompson, Y. Del Amo, H. Stachelberger, M.A. Brzezinski, G.D. Stucky, D.E. Morse, and P.K. Hansma Atomic force microscopy study of living diatoms in ambient conditions J. Microsc. (Oxford) 212 2003 292 299
80. A.P. Garcia, N. Pugno, and M.J. Buehler Superductile, wavy silica nanostructures inspired by diatom algae Adv. Eng. Mater. 13 2011 B14 B405
81. E. Epstein Silicon Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 1999 641 664
82. K. Shimizu, J. Cha, G.D. Stucky, and D.E. Morse Silicatein alpha: cathepsin L-like protein in sponge biosilica Proc. Natl. Acad. Sci. U. S. A. 95 1998 6234 6238
83. L. Xia, Y. Liu, and Z.B. Li Biosilicification templated by amphiphilic block copolypeptide assemblies Macromol. Biosci. 10 2010 1566 1575
84. D. Schuler, and R.B. Frankel Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications Appl. Microbiol. Biotechnol. 52 1999 464 473
85. C.T. Lefevre, N. Viloria, M.L. Schmidt, M. Posfai, R.B. Frankel, and D.A. Bazylinski Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria ISME J. 6 2012 440 450
86. K.J. Lohmann Magnetic orientation by hatchling loggerheasd sea-turtles (Caretta caretta) J. Exp. Biol. 155 1991 37 49
87. K.J. Lohmann, and C.M.F. Lohmann Detection of magnetic field intensity by sea turtles Nature 380 1996 59 61
88. L.C. Boles, and K.J. Lohmann True navigation and magnetic maps in spiny lobsters Nature 421 2003 60 63
89. Q.Q. Wang, M. Nemoto, D.S. Li, J.C. Weaver, B. Weden, J. Stegemeier, K.N. Bozhilov, L.R. Wood, G.W. Milliron, C.S. Kim, E. DiMasi, and D. Kisailus Phase transformations and structural developments in the radular teeth of Cryptochiton stelleri Adv. Funct. Mater. 23 2013 2908 2917
90. S.E. Greene, and A. Komeili Biogenesis and subcellular organization of the magnetosome organelles of magnetotactic bacteria Curr. Opin. Cell Biol. 24 2012 490 495
91. G.W. Luther, T.F. Rozan, M. Taillefert, D.B. Nuzzio, C. Di Meo, T.M. Shank, R.A. Lutz, and S.C. Cary Chemical speciation drives hydrothermal vent ecology Nature 410 2001 813 816
92. Y. Suzuki, R.E. Kopp, T. Kogure, A. Suga, K. Takai, S. Tsuchida, N. Ozaki, K. Endo, J. Hashimoto, Y. Kato, C. Mizota, T. Hirata, H. Chiba, K.H. Nealson, K. Horikoshi, and J.L. Kirschvink Sclerite formation in the hydrothermal-vent "scaly-foot" gastropod - possible control of iron sulfide biomineralization by the animal Earth Planet. Sci. Lett. 242 2006 39 50
93. F. Barthelat, H. Tang, P.D. Zavattieri, C.M. Li, and H.D. Espinosa On the mechanics of mother-of-pearl: a key feature in the material hierarchical structure J. Mech. Phys. Solids 55 2007 306 337
94. H.D. Espinosa, A.L. Juster, F.J. Latourte, O.Y. Loh, D. Gregoire, and P.D. Zavattieri Tablet-level origin of toughening in abalone shells and translation to synthetic composite materials Nat. Commun. 2 2011
95. L. Addadi, D. Joester, F. Nudelman, and S. Weiner Mollusk shell formation: a source of new concepts for understanding biomineralization processes Chemistry 12 2006 980 987
96. A.Y.M. Lin, M.A. Meyers, and K.S. Vecchio Mechanical properties and structure of Strombus gigas, Tridacna gigas, and Haliotis rufescens sea shells: a comparative study Mater. Sci. Eng. C 26 2006 1380 1389
97. A.Y.M. Lin, P.-Y. Chen, and M.A. Meyers The growth of nacre in the abalone shell Acta Biomater. 4 2008 131 138
98. A. Lin, and M.A. Meyers Growth and structure in abalone shell Mater. Sci. Eng. A 390 2005 27 41
99. M.A. Meyers, C.T. Lim, A. Li, B.R.H. Nizam, E.P.S. Tan, Y. Seki, and J. McKittrick The role of organic intertile layer in abalone nacre Mater. Sci. Eng. C 29 2009 2398 2410
100. M.I. Lopez, P.E.M. Martinez, and M.A. Meyers Organic interlamellar layers, mesolayers and mineral nanobridges: contribution to strength in abalone (Haliotis rufescence) nacre Acta Biomater. 10 2014 2056 2064
101. M.I. Lopez, P.-Y. Chen, J. McKittrick, and M.A. Meyers Growth of nacre in abalone: seasonal and feeding effects Mater. Sci. Eng. C 31 2011 238 245
102. R. Menig, M.H. Meyers, M.A. Meyers, and K.S. Vecchio Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells Acta Mater. 48 2000 2383 2393
103. C. Salinas, and D. Kisailus Fracture mitigation strategies in gastropod shells JOM 65 2013 473 480
104. R. Menig, M.H. Meyers, M.A. Meyers, and K.S. Vecchio Quasi-static and dynamic mechanical response of Strombus gigas (conch) shells Mater. Sci. Eng. A 297 2001 203 211
105. S. Kamat, X. Su, R. Ballarini, and A.H. Heuer Structural basis for the fracture toughness of the shell of the conch Strombus gigas Nature 405 2000 1036 1040
106. R.O. Ritchie Mechanisms of fatigue crack-propagation in metals, ceramics and composites - role of crack tip sheilding Mater. Sci. Eng. A 103 1988 15 28
107. R.O. Ritchie Mechanisms of fatigue-crack propagation in ductile and brittle solids Int. J. Fract. 100 1999 55 83
108. F. Bouville, E. Maire, S. Meille, B. Van de Moortele, A.J. Stevenson, and S. Deville Strong, tough and stiff bioinspired ceramics from brittle constituents Nat. Mater. 13 2014 508 514
109. H.M. Yao, M. Dao, T. Imholt, J.M. Huang, K. Wheeler, A. Bonilla, S. Suresh, and C. Ortiz Protection mechanisms of the iron-plated armor of a deep-sea hydrothermal vent gastropod PNAS 107 2010 987 992
110. A. Waren, S. Bengtson, S.K. Goffredi, and C.L. Van Dover A hot-vent gastropod with iron sulfide dermal sclerites Science 302 2003 1007
111. M.J. Vendrasco, T.E. Wood, and B.N. Runnegar Articulated Palaeozoic fossil with 17 plates greatly expands disparity of early chitons Nature 429 2004 288 291
112. K. Treves, W. Traub, S. Weiner, and L. Addadi Aragonite formation in the chiton (Mollusca) girdle Helv. Chim. Acta 86 2003 1101 1112
113. M.J. Connors, H. Ehrlich, M. Hog, C. Godeffroy, S. Araya, I. Kallai, D. Gazit, M. Boyce, and C. Ortiz Three-dimensional structure of the shell plate assembly of the chiton Tonicella marmorea and its biomechanical consequences J. Struct. Biol. 177 2012 314
114. M. Nemoto, Q.Q. Wang, D.S. Li, S.Q. Pan, T. Matsunaga, and D. Kisailus Proteomic analysis from the mineralized radular teeth of the giant Pacific chiton, Cryptochiton stelleri (Mollusca) Proteomics 12 2012 2890 2894
115. K.M. Towe, and H.A. Lowensta Ultrastructure and development of iron mineralization in radular teeth of Cryptochiton stelleri (Mollusca) J. Ultrastruct. Res. 17 1967 1 13
116. L.M. Gordon, J.K. Roman, R.M. Everly, M.J. Cohen, J.J. Wilker, and D. Joester Selective formation of metastable ferrihydrite in the chiton tooth Angew. Chem. 53 2014 11506 11509
117. V. Martin-Jezequel, M. Hildebrand, and M.A. Brzezinski Silicon metabolism in diatoms: implications for growth J. Phycol. 36 2000 821 840
118. M. Hildebrand Diatoms, biomineralization processes, and genomics Chem. Rev. 108 2008 4855 4874
119. G. Sarthou, K.R. Timmermans, S. Blain, and P. Treguer Growth physiology and fate of diatoms in the ocean: a review J. Sea Res. 53 2005 25 42
120. P. Treguer, D.M. Nelson, A.J. Van Beenekom, D.J. DeMaster, A. Leynaert, and B. Queguiner The silica balance in the world ocean: a reestimate Science 268 1995 375 379
121. C.E. Hamm, R. Merkel, O. Springer, P. Jurkojc, C. Maier, K. Prechtel, and V. Smetacek Architecture and material properties of diatom shells provide effective mechanical protection Nature 421 2003 841 843
122. H. Hildebrand, C.D. Durselen, D. Kirschtel, U. Pollingher, and T. Zohary Biovolume calculation for pelagic and benthic microalgae J. Phycol. 35 1999 403 424
123. D. Losic, K. Short, J.G. Mitchell, R. Lal, and N.H. Voelcker AFM nanoindentations of diatom biosilica surfaces Langmuir 23 2007 5014 5021
124. N. Almqvist, Y. Delamo, B.L. Smith, N.H. Thomson, A. Bartholdson, R. Lal, M. Brzezinski, and P.K. Hansma Micromechanical and structural properties of a pennate diatom investigated by atomic force microscopy J. Microsc. 202 2001 518 532
125. G. Francius, B. Tesson, E. Dague, V. Martin-Jezequel, and Y.F. Dufrene Nanostructure and nanomechanics of live Phaeodactylum tricornutum morphotypes Environ. Microbiol. 10 2008 1344 1356
126. N. Kroger, R. Deutzmann, C. Bergsdorf, and M. Sumper Species-specific polyamines from diatoms control silica morphology PNAS 97 2000 14133 14138
127. N. Kroger, R. Deutzmann, and M. Sumper Polycationic peptides from diatom biosilica that direct silica nanosphere formation Science 286 1999 1129 1132
128. M. Sumper A phase separation model for the nanopatterning of diatom biosilica Science 295 2002 2430 2433
129. J.R. Young Functions of coccoliths W.G. Siesser, A. Winter, Coccolithophores 1994 Cambridge University Press Cambridge, UK 63 82
130. B.L. Smith, G.T. Paloczi, P.K. Hansma, and R.P. Levine Discerning nature's mechanism for making complex biocomposite crystals J. Cryst. Growth 211 2000 116 121
131. S. Mann, and N.H.C. Sparks Single crystal nature of coccolith elements of the marine alga Emiliania huxleyi as determined by electron diffraction and high resolution electron microscopy Proc. R. Soc. B 234 1988 441 453
132. 3 formation in coccolithophores Comp. Biochem. Physiol. B 136 2003 743 754
133. P.-Y. Chen, A.Y.M. Lin, J. McKittrick, and M.A. Meyers Structure and mechanical properties of crab exoskeletons Acta Biomater. 4 2008 587 596
134. D.F. Travis The molting cycle of the spiny lobster, Panulirus argus-Latreille. II. Pre-ecdysial histological and histochemical changes in the hepatopancreas and integumental tissues Biol. Bull. 108 1955 88 112
135. Y. Bouligand Aspects ultrastructuraux de la calcification chez les Crabes 1970 Septieme Congres Internationale de Microscopie Electronique Gernoble, France 105 106
136. H.O. Fabritius, C. Sachs, P.R. Triguero, and D. Raabe Influence of structural principles on the mechanics of a biological fiber-based composite material with hierarchical organization: the exoskeleton of the lobster Homarus americanus Adv. Mater. 21 2009 391 400
137. D. Raabe, C. Sachs, and P. Romano The crustacean exoskeleton as an example of a structurally and mechanically graded biological nanocomposite material Acta Mater. 53 2005 4281 4292
138. R. Dillaman, S. Hequembourg, and M. Gay Early pattern of calcification in the dorsal carapace of the blue crab, Callinectes sapidus J. Microsc. 263 2005 356 374
139. H.O. Fabritius, E.S. Karsten, K. Balasundaram, S. Hild, K. Huemer, and D. Raabe Correlation of structure, composition and local mechanical properties in the dorsal carapace of the edible crab Cancer pagurus Z. Krist. Cryst. Mater. 227 2012 766 776
140. D. Raabe, P. Romano, C. Sachs, H. Fabritius, A. Al-Sawalmih, S. Yi, G. Servos, and H.G. Hartwig Microstructure and crystallographic texture of the chitin-protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus Mater. Sci. Eng. A 421 2006 143 153
141. L. Cheng, L.Y. Wang, and A.M. Karlsson Image analyses of two crustacean exoskeletons and implications of the exoskeletal microstructure on the mechanical behavior J. Mater. Res. 23 2008 2854 2872
142. C. Sachs, H. Fabritius, and D. Raabe Experimental investigation of the elastic-plastic deformation of mineralized lobster cuticle by digital image correlation J. Struct. Biol. 155 2006 409 425
143. H.R. Hepburn, I. Joffe, N. Green, and K.J. Nelson Mechanical-properties of a crab shell Comp. Biochem. Physiol. 50 1975 551 554
144. I. Joffe, H.R. Hepburn, K.J. Nelson, and N. Green Mechanical-properties of a crustacean exoskelton Comp. Biochem. Physiol. 50 1975 545 549
145. C.L. Williams, R.M. Dillaman, E.A. Elliott, and D.M. Gay Formation of the arthrodial membrane in the blue crab, Callinectes sapidus J. Morphol. 256 2003 260 269
146. C.A. Melnick, Z. Chen, and J.J. Mecholsky Hardness and toughness of exoskeleton material in the stone crab, Menippe mercenaria J. Mater. Res. 11 1996 2903 2907
147. S.J. Foster, and A.C.J. Vincent Life history and ecology of seahorses: implications for conservation and management J. Fish Biol. 65 2004 1 61
148. T.R. Consi, P.A. Seifert, M.S. Triantafyllou, and E.R. Edelman The dorsal fin engine of the seahorse Hippocampus 248 2001 1
149. M.A. Ashley-Ross Mechanical properties of the dorsal fin muscle of seahorse (Hippocampus) and pipefish (Syngnathus) J. Exp. Zool. 293 2002 561 577
150. M.M. Porter, E.E. Novitskaya, A.B. Castro-Cesena, M.A. Meyers, and J. McKittrick Highly deformable bones: unusual deformation mechanisms of seahorse armor Acta Biomater. 9 2013 6763 6770
151. M.E. Hale Functional morphology of ventral tail bending and prehensile abilities of the seahorse, Hippocampus kuda J. Morphol. 227 1996 51 65
152. T. Praet, D. Adriaens, S. Van Cauter, B. Masschaele, M. De Beule, and B. Verhegghe Inspiration from nature: dynamic modelling of the musculoskeletal structure of the seahorse tail Int. J. Numer. Methods Biomed. Eng. 28 2012 1028 1042
153. C. Neutens, D. Adriaens, J. Christiaens, B. De Kegel, M. Dierick, R. Boistel, and L. Van Hoorebeke Grasping convergent evolution in syngnathids: a unique tale of tails J. Anat. 224 2014 710 723
154. M.M. Porter, D. Adriaens, R.L. Hatton, M.A. Meyers, and J. McKittrick Why the seahorse tail is square Science 349 2015 6683 (aaa)
155. D. Kleiber, L.K. Blight, I.R. Caldwell, and A.C.J. Vincent The importance of seahorses and pipefishes in the diet of marine animals Rev. Fish Biol. Fish. 21 2011 205 223
156. W.E.G. Müller, X.H. Wang, K. Kropf, H. Ushijima, W. Geurtsen, C. Eckert, M.N. Tahir, W. Tremel, A. Boreiko, U. Schloßmacher, J.H. Li, and H.C. Schröder Bioorganic/inorganic hybrid composition of sponge spicules: matrix of the giant spicules and of the comitalia of the deep sea hexactinellid Monorhaphis J. Struct. Biol. 161 2008 188 203
157. J.C. Weaver, J. Aizenberg, G.E. Fantner, D. Kisailus, A. Woesz, P. Allen, K. Fields, M.J. Porter, F.W. Zok, P.K. Hansma, P. Fratzl, and D.E. Morse Hierarchical assembly of the siliceous skeletal lattice of the hexactinellid sponge Euplectella aspergillum J. Struct. Biol. 158 2007 93 106
158. J. Aizenberg, J.C. Weaver, M.S. Thanawala, V.C. Sundar, D.E. Morse, and P. Fratzl Skeleton of Euplectella sp.: structural hierarchy from the nanoscale to the macroscale Science 309 2005 275 278
159. G. Imsiecke, R.T. Steffen, M. Custodio, R. Borojevic, and W. Muller Formation of spicules by sclerocytes from the freshwater sponge Ephydatia muelleri in short-term cultures in vitro In Vitro Cell. Dev. Biol. Anim. 31 1995 528 535
160. J.N. Cha, K. Shimizu, Y. Zhou, S.C. Christiansen, B.F. Chmelka, G.D. Stucky, and D.E. Morse Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro Proc. Natl. Acad. Sci. U. S. A. 96 1999 361 365
161. A. Woesz, J.C. Weaver, M. Kazanci, Y. Dauphin, J. Aizenberg, D.E. Morse, and P. Fratzl Micromechanical properties of biological silica in skeletons of deep-sea sponges J. Mater. Res. 21 2006 2068 2078
162. M.M. Porter, L. Meraz, A. Calderon, H. Choi, A. Chouhan, L. Wang, M.A. Meyers, and J. McKittrick Torsional properties of helix-reinforced composites fabricated by magnetic freeze casting Compos. Struct. 119 2015 174 184
163. V. Presser, S. Schultheiss, C. Berthold, and K.G. Nickel Sea urchin spines as a model-system for permeable, light-weight ceramics with graceful failure behavior. Part I. Mechanical behavior of sea urchin spines under compression J. Bionic Eng. 6 2009 203 213
164. J. Seto, Y.R. Ma, S.A. Davis, F. Meldrum, A. Gourrier, Y.Y. Kim, U. Schilde, M. Sztucki, M. Burghammer, S. Maltsev, C. Jager, and H. Colfen Structure-property relationships of a biological mesocrystal in the adult sea urchin spine PNAS 109 2012 3699 3704
165. Y. Oaki, and H. Imai Nanoengineering in echinoderms: the emergence of morphology from nanobricks Small 2 2006 66 70
166. J. Aizenberg, J. Hanson, T.F. Koetzle, S. Weiner, and L. Addadi Control of macromolecule distribution within synthetic and biogenic single calcite crystals J. Am. Chem. Soc. 119 1997 881 886
167. Y. Politi, T. Arad, E. Klein, S. Weiner, and L. Addadi Sea urchin spine calcite forms via a transient amorphous calcium carbonate phase Science 306 2004 1161 1164
168. C. Moureaux, A. Perez-Huerta, P. Compere, W. Zhu, T. Leloup, M. Cusack, and P. Dubois Structure, composition and mechanical relations to function in sea urchin spine J. Struct. Biol. 170 2010 41 49
169. P.B. Edwards, and T.A. Ebert Plastic responses to limited food availability and spine damage in the sea urchin Strongylocentrotus purpuratus (Stimpson) J. Exp. Mar. Biol. Ecol. 145 1991 205 220
170. P. Dubois, and L. Ameye Regeneration of spines and pedicellariae in echinoderms: a review Microsc. Res. Tech. 55 2001 427 437
171. L.J. Gibson, and M.F. Ashby Cellular Solids: Structure and Properties 1999 Cambridge University Press
172. X. Su, S. Kamat, and A.H. Heuer The structure of sea urchin spines, large biogenic single crystals of calcite J. Mater. Sci. 35 2000 5545 5551
173. J. Weber, R. Greer, B. Voight, E. White, and R. Roy Unusual strength properties of echinoderm calcite J. Ultrastruct. Res. 26 1969 355 366
174. Y. Ma, B. Aichmayer, O. Paris, P. Fratzl, A. Meibom, R.A. Metzler, Y. Politi, L. Addadi, P.U.P.A. Gilbert, and S. Weiner The grinding tip of the sea urchin tooth exhibits exquisite control over calcite crystal orientation and Mg distribution PNAS 106 2009 6048 6053
175. Y. Ma, S.R. Cohen, L. Addadi, and S. Weiner Sea urchin tooth design: an "all-calcite" polycrystalline reinforced fiber composite for grinding rocks Adv. Mater. 20 2008 1555 1559
176. C.E. Killian, R.A. Metzler, Y. Gong, T.H. Churchill, I.C. Olson, V. Trubetskoy, M.B. Christensen, J.H. Fournelle, F. De Carlo, S. Cohen, J. Mahamid, A. Scholl, A. Young, A. Doran, F.H. Wilt, S.N. Coppersmith, and P.U.P.A. Gilbert Self-sharpening mechanism of the sea urchin tooth Adv. Funct. Mater. 21 2011 682 690
177. J.C. Tyler, and F. Santini Review and reconstructions of the tetraodonitform fishes from the Eocene of Monte Bolca, Italy, with comments on related tertiary taxa Studi e Ricerche sui Giacimenti Terziari di Bolca Museo Civico di Storia Naturale di Verona 9 2002 47 119
178. E.L. Brainerd Puffer inflation: functional morphology of postcranial structures in Diodon holocanthus (Tetraodontiformes) J. Morphol. 220 1994 243 261
179. T. Ikoma, H. Kobayashi, J. Tanaka, D. Walsh, and S. Mann Physical properties of type I collagen extracted from fish scales of Pagrus major and Oreochromis niloticas Int. J. Biol. Macromol. 32 2003 199 204
180. D. Zhu, C.F. Ortega, R. Motamedi, L. Szewciw, F. Vernerey, and F. Barthelat Structure and mechanical performance of a "modern" fish scale Adv. Eng. Mater. 14 2012 B94 B185
181. B.J.F. Bruet, J.H. Song, M.C. Boyce, and C. Ortiz Materials design principles of ancient fish armour Nat. Mater. 7 2008 748 756
182. J.H. Song, C. Ortiz, and M.C. Boyce Threat-protection mechanics of an armored fish J. Mech. Behav. Biomed. Mater. 4 2011 699 712
183. E.A. Zimmermann, B. Gludovatz, E. Schaible, N.K.N. Dave, W. Yang, M.A. Meyers, and R.O. Ritchie Mechanical adaptability of the Bouligand-type structure in natural dermal armour Nat. Commun. 4 2013 2634
184. J.H. Long, M.E. Hale, M.J. McHenry, and M.W. Westneat Functions of fish skin: flexural stiffness and steady swimming of longnose gar Lepisosteus osseus J. Exp. Biol. 199 1996 2139 2151
185. J.H. Long, B. Adcock, and R.G. Root Force transmission via axial tendons in undulating fish: a dynamic analysis Comp. Biochem. Physiol. A Physiol. 133 2002 911 929
186. J.H. Long, T.J. Koob, K. Irving, K. Combie, V. Engel, N. Livingston, A. Lammert, and J. Schumacher Biomimetic evolutionary analysis: testing the adaptive value of vertebrate tail stiffness in autonomous swimming robots J. Exp. Biol. 209 2006 4732 4746
187. W. Yang, B. Gludovatz, E.A. Zimmermann, H.A. Bale, R.O. Ritchie, and M.A. Meyers Structure and fracture resistance of alligator gar (Atractosteus spatula) armored fish scales Acta Biomater. 9 2013 5876 5889
188. J.Y. Sire, and A. Huysseune Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach Biol. Rev. 78 2003 219 249
189. E.S. Goodrich On the scales of fish living and extinct, and then importance in classification Proc. Zool. Soc. London 77 1907 751 774
190. F.J. Vernerey, and F. Barthelat Skin and scales of teleost fish: simple structure but high performance and multiple functions J. Mech. Phys. Solids 68 2014 66 76
191. D.J. Zhu, L. Szewciw, F. Vernerey, and F. Barthelat Puncture resistance of the scaled skin from striped bass: collective mechanisms and inspiration for new flexible armor designs J. Mech. Behav. Biomed. Mater. 24 2013 30 40
192. M.M. Smith, M.H. Hobdell, and W.A. Miller Structure of scales of Latimeria chalumnae J. Zool. 167 1972 501 509
193. T.O.R. Orvig Paleohistological notes I. On the structure of the bone tissue in the scales of certain Palaeonisciformes Arkiv Zool. 10 1957 481 490
194. G.H. Roux The microscopic anatomy of the Latimeria scale S. Afr. J. Med. Sci. 7 1942 1 18
195. E. Jarvik On some osteolepiform crossopterygians from the Upper Old Red Sandstone of Scotland K. Svenska Vetenskapsakad. Handl. 2 1950 1 35
196. V.R. Sherman, W. Yang, and M.A. Meyers The materials science of collagen J. Mech. Behav. Biomed. Mater. 2015 (in press)
197. J.R. Grubich, S. Huskey, S. Crofts, G. Orti, and J. Porto Mega-bites: extreme jaw forces of living and extinct piranhas (Serrasalmidae) Sci. Report. 2012
198. P.-Y. Chen, J. Schirer, A. Simpson, R. Nay, Y.-S. Lin, W. Yang, M.I. Lopez, J. Li, E.A. Olevsky, and M.A. Meyers Predation versus protection: fish teeth and scales evaluated by nanoindentation J. Mater. Res. 27 2012 100 112
199. A.K. Dastjerdi, and F. Barthelat Teleost fish scales amongst the toughest collagenous materials J. Mech. Behav. Biomed. Mater. 2015 (in press)
200. I.H. Chen, W. Yang, and M.A. Meyers Leatherback sea turtle shell: a tough and flexible biological design Acta Biomater. 2015 (in press)
201. J.D.R. Houghton, T.K. Doyle, J. Davenport, R.P. Wilson, and G.C. Hays The role of infrequent and extraordinary deep dives in leatherback turtles (Dermochelys coriacea) J. Exp. Biol. 211 2008 2566 2575
202. L. Besseau, and Y. Bouligand The twisted collagen network of the box-fish scutes Tissue Cell 30 1998 251 260
203. C.-Y. Sun, and P.-Y. Chen Structural design and mechanical behavior of alligator (Alligator mississippiensis) osteoderms Acta Biomater. 9 2013 9049 9064
204. S. Amini, A. Masic, L. Bertinetti, J.S. Teguh, J.S. Herrin, X. Zhu, H.B. Su, and A. Miserez Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages Nat. Commun. 5 2014
205. 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 The stomatopod dactyl club: a formidable damage-tolerant biological hammer Science 336 2012 1275 1280
206. J.D. Currey, A. Nash, and W. Bonfield Calcified cuticle in the stomatopod smashing limb J. Mater. Sci. 17 1982 1939 1944
207. N. Guarín-Zapata, J. Gomez, N. Yaraghi, D. Kisailus, and P.D. Zavattieri Shear wave filtering in naturally-occurring Bouligand structures Acta Biomater. 23 2015 11 20
208. L.K. Grunenfelder, N. Suksangpanya, C. Salinas, G. Milliron, N. Yaraghi, S. Herrera, K. Evans-Lutterodt, S.R. Nutt, P. Zavattieri, and D. Kisailus Bio-inspired impact-resistant composites Acta Biomater. 10 2014 3997 4008
209. D.A.D. Parry, and A.C.T. North Hard alpha-keratin intermediate filament chains: substructure of the N- and C-terminal domains and the predicted structure and function of the C-terminal domains of Type I and Type II chains J. Struct. Biol. 122 1998 67 75
210. J. McKittrick, P.-Y. Chen, L. Tombolato, E.E. Novitskaya, M.W. Trim, G.A. Hirata, E.A. Olevsky, M.F. Horstemeyer, and M.A. Meyers Energy absorbent natural materials and bioinspired design strategies: a review Mater. Sci. Eng. C 30 2010 331 342
211. D. Raabe, A. Al-Sawalmih, S.B. Yi, and H. Fabritius Preferred crystallographic texture of alpha-chitin as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus americanus Acta Biomater. 3 2007 882 895
212. 3 prepared by a bubbling method J. Eur. Ceram. Soc. 26 2006 843 847
213. M.I. Lopez, and M.A. Meyers The organic interlamellar layer in abalone nacre: formation and mechanical response Mater. Sci. Eng. C 58 2015 7 13
214. J.R. Young, M. Geisen, L. Cros, A. Kleijne, I. Probert, and J.B. Ostergaard A guide to extant coccolithophore taxonomy J. Nanoplankton Res. 1 2003 1 132
215. G. Mayer, and M. Sarikaya Rigid biological composite materials: structural examples for biomimetic design Exp. Mech. 42 2002 395 403
216. S. Weiner, and L. Addadi Design strategies in mineralized biological materials J. Mater. Chem. 7 1997 689 702
217. B.H. Ji, and H.J. Gao Mechanical properties of nanostructure of biological materials J. Mech. Phys. Solids 52 2004 1963 1990
218. I. Jager, and P. Fratzl Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles Biophys. J. 79 2000 1737 1746
219. J.F.V. Vincent, and U.G.K. Wegst Design and mechanical properties of insect cuticle Arthropod Struct. Dev. 33 2004 187 199
220. G. De With, H.J.A. Van Dijk, N. Hattu, and K. Prijs Preparation, microstructure and mechanical properties of dense polycrystalline hydroxy apatite J. Mater. Sci. 16 1981 1592 1598
221. C. Levi, J.L. Barton, C. Guillemet, E. Lebras, and P. Lehuede A remarkably strong natural glassy rod - the anchoring spicule of the monorhaphis sponge J. Mater. Sci. Lett. 8 1989 337 339
222. M. Sarikaya, H. Fong, N. Sunderland, B.D. Flinn, G. Mayer, A. Mescher, and E. Gaino Biomimetic model of a sponge-spicular optical fiber - mechanical properties and structure J. Mater. Res. 16 2001 1420 1428
223. P.-Y. Chen, A.Y.M. Lin, A.G. Stokes, Y. Seki, S.G. Bodde, J. McKittrick, and M.A. Meyers Structural biological materials: overview of current research JOM 60 2008 23 32
224. A.P. Jackson, J.F.V. Vincent, and R.M. Turner The mechanical design of nacre Proc. R. Soc. B 234 1988
225. D.S. Fudge, and J.M. Gosline Molecular design of the alpha-keratin composite: insights from a matrix-free model, hagfish slime threads Proc. R. Soc. B 271 2004 291 299
226. D.K. Hayes, and W.D. Armstrong Distribution of mineral material in calcified carapace and claw shell of the American lobster, Homarus americanus, evaluated by means of microroentgenograms Biol. Bull. 121 1961 307 315
227. L.D. Mkukuma, J.M.S. Skakle, I.R. Gibson, C.T. Imrie, R.M. Aspden, and D.W.L. Hukins Effect of the proportion of organic material in bone on thermal decomposition of bone mineral: an investigation of a variety of bones from different species using thermogravimetric analysis coupled to mass spectrometry, high-temperature X-ray diffraction, and Fourier transform infrared spectroscopy Calcif. Tissue Int. 75 2004 321 328
228. S. Sankar, S. Sekar, R. Mohan, S. Rani, J. Sundaraseelan, and T.R. Sastry Preparation and partial characterization of collagen sheet from fish (Lates calcarifer) scales Int. J. Biol. Macromol. 42 2008 6 9