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The Multiscale Architectures of Fish Bone and Tessellated Cartilage and Their Relation to Function

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Book cover Architectured Materials in Nature and Engineering

Part of the book series: Springer Series in Materials Science ((SSMATERIALS,volume 282))

Abstract

When describing the architecture and ultrastructure of animal skeletons , introductory biology, anatomy and histology textbooks typically focus on the few bone and cartilage types prevalent in humans. In reality, cartilage and bone are far more diverse in the animal kingdom, particularly within fishes, where cartilage and bone types exist that are characterized by features that are anomalous or even pathological in human skeletons. Here, we discuss the curious and complex architectures of fish bone and shark and ray cartilage, highlighting similarities and differences with their mammalian skeletal tissue counterparts. By synthesizing older anatomical literature with recent high-resolution structural and materials characterization work, we frame emerging pictures of form-function relationships in these tissues and of the evolution and true diversity of cartilage and bone.

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References

  1. P.C.J. Donoghue, I.J. Sansom, Origin and early evolution of vertebrate skeletonization. Microsc. Res. Tech. 59, 352–372 (2002)

    Article  Google Scholar 

  2. P.C.J. Donoghue, I.J. Sansom, J.P. Downs, Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. J. Exp. Zool. Part B Mol. Dev. Evol. 306B, 278–294 (2006)

    Article  Google Scholar 

  3. K. Kawasaki, T. Suzuki, K.M. Weiss, Genetic basis for the evolution of vertebrate mineralized tissue. Proc. Natl. Acad. Sci. U. S. A. 101, 11356–11361 (2004)

    Article  CAS  Google Scholar 

  4. R. Seidel, K. Lyons, M. Blumer, P. Zaslansky, P. Fratzl, J.C. Weaver, M.N. Dean, Ultrastructural and developmental features of the tessellated endoskeleton of elasmobranchs (sharks and rays). J. Anat. 229, 681–702 (2016)

    Article  Google Scholar 

  5. J.-Y. Sire, A. Huysseune, Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach. Biol. Rev. Camb. Philos. Soc. 78, 219–249 (2003)

    Article  Google Scholar 

  6. J.D. Currey, Collagen and the mechanical properties of bone and calcified cartilage, in Collagen: Structure and Mechanics, An Introduction, ed. by P. Fratzl (Springer US, Boston, MA, 2008), pp. 397–420

    Chapter  Google Scholar 

  7. E. Degtyar, M.J. Harrington, Y. Politi, P. Fratzl, The mechanical role of metal ions in biogenic protein-based materials. Angew. Chem. Int. Ed. 53, 12026–12044 (2014)

    Article  CAS  Google Scholar 

  8. J.D. Currey, The design of mineralised hard tissues for their mechanical functions. J. Exp. Biol. 202, 3285–3294 (1999)

    CAS  Google Scholar 

  9. J.D. Currey, The structure and mechanics of bone. J. Mater. Sci. 47, 41–54 (2011)

    Article  Google Scholar 

  10. J.D. Currey, M.N. Dean, R. Shahar, Revisiting the links between bone remodelling and osteocytes: insights from across phyla. Biol. Rev. Camb. Philos. Soc. 92, 1702–1719 (2017)

    Article  Google Scholar 

  11. M.L. Moss, A.S. Posner, X-ray diffraction study of acellular teleost bone. Nature 188, 1037–1038 (1960)

    Article  CAS  Google Scholar 

  12. M.R. Urist, Calcium and phosphorus in the blood and skeleton of the Elasmobranchii, 1–24 (1961)

    Google Scholar 

  13. J.W. Smith, Collagen fibre patterns in mammalian bone. J. Anat. 94, 329–344 (1960)

    CAS  Google Scholar 

  14. L.F. Bonewald, The amazing osteocyte. J. Bone Miner. Res. 26, 229–238 (2011)

    Article  CAS  Google Scholar 

  15. S.L. Dallas, M. Prideaux, L.F. Bonewald, The osteocyte: an endocrine cell … and more. Endocr. Rev. 34, 658–690 (2013)

    Article  CAS  Google Scholar 

  16. P.E. Witten, A. Huysseune, T. Franz-Odendaal, T. Fedak, M. Vickaryous, A. Cole, B.K. Hall, Acellular teleost bone: primitive or derived, dead or alive? Palaeontol. Assoc. Newsl. 55, 37–41 (2004)

    Google Scholar 

  17. L. Cohen, M. Dean, A. Shipov, A. Atkins, E. Monsonego-Ornan, R. Shahar, Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish. J. Exp. Biol. 215, 1983–1993 (2012)

    Article  Google Scholar 

  18. A. Atkins, M.N. Dean, M.L. Habegger, P.J. Motta, L. Ofer, F. Repp, A. Shipov, S. Weiner, J.D. Currey, R. Shahar, Remodeling in bone without osteocytes: billfish challenge bone structure-function paradigms. Proc. Natl. Acad. Sci. U. S. A. 111, 16047–16052 (2014)

    Article  CAS  Google Scholar 

  19. G.S. Helfman, B.B. Collette, D.E. Facey, B.W. Bowen, The Diversity of Fishes: Biology (Wiley-Blackwell, 2009)

    Google Scholar 

  20. R. Shahar, C. Lukas, S. Papo, J.W.C. Dunlop, R. Weinkamer, Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones. Anat. Rec. 294, 1093–1102 (2011)

    Article  Google Scholar 

  21. A. Atkins, N. Reznikov, L. Ofer, A. Masic, S. Weiner, R. Shahar, The three-dimensional structure of anosteocytic lamellated bone of fish. Acta Biomater. 13, 311–323 (2015)

    Article  CAS  Google Scholar 

  22. N. Reznikov, R. Shahar, S. Weiner, Bone hierarchical structure in three dimensions. Acta Biomater. 10, 3815–3826 (2014)

    Article  Google Scholar 

  23. L.B. Halstead, Calcified tissues in the earliest vertebrates. Calcif. Tissue Int. 3, 107–124 (1969)

    Article  CAS  Google Scholar 

  24. D.R. Hughes, J.R. Bassett, L.A. Moffat, Histological identification of osteocytes in the allegedly acellular bone of the sea breams Acanthopagrus australis, Pagrus auratus and Rhabdosargus sarba (Sparidae, Perciformes, Teleostei). Anat. Embryol. 190, 163–179 (1994)

    Article  CAS  Google Scholar 

  25. A. Kölliker, On the different types in the microscopic structure of the skeleton of osseous fishes (1857)

    Google Scholar 

  26. M.L. Moss, Studies of the acellular bone of teleost fish. Cells Tissues Organs 46, 343–362 (1961)

    Article  CAS  Google Scholar 

  27. J.Y. Sire, F.J. Meunier, The canaliculi of Williamson in holostean bone (Osteichthyes, Actinopterygii): a structural and ultrastructural study. Acta Zool. 75, 235–247 (1994)

    Article  Google Scholar 

  28. T. Ørvig, Histologic studies of placoderms and fossil elasmobranchs, 1–152 (1950)

    Google Scholar 

  29. D.E. Ashhurst, The cartilaginous skeleton of an elasmobranch fish does not heal. Matrix Biol. 23, 15–22 (2004)

    Article  CAS  Google Scholar 

  30. B.K. Hall, Bones and Cartilage, 2nd edn. (Academic Press, 2014)

    Google Scholar 

  31. M.N. Dean, C.G. Mull, S.N. Gorb, A.P. Summers, Ontogeny of the tessellated skeleton: insight from the skeletal growth of the round stingray Urobatis halleri. J. Anat. 215, 227–239 (2009)

    Article  Google Scholar 

  32. N.E. Kemp, S.K. Westin, Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks. J. Morphol. 160, 75–101 (1979)

    Article  CAS  Google Scholar 

  33. R. Seidel, M.J.F. Blumer, E.J. Pechriggl, K. Lyons, B.K. Hall, P. Fratzl, J.C. Weaver, M.N. Dean, Calcified cartilage or bone? Collagens in the tessellated endoskeletons of cartilaginous fish (sharks and rays). J. Struct. Biol. (2017)

    Google Scholar 

  34. J.G. Maisey, The diversity of tessellated calcification in modern and extinct chondrichthyans. Rev. Paléobiol. Genève 32, 355–371 (2013)

    Google Scholar 

  35. L.J. Macesic, A.P. Summers, Flexural stiffness and composition of the batoid propterygium as predictors of punting ability. J. Exp. Biol. 215, 2003–2012 (2012)

    Article  Google Scholar 

  36. J.G. Clement, Re-examination of the fine structure of endoskeletal mineralization in chondrichthyans: implications for growth, ageing and calcium homeostasis. Aust. J. Mar. Freshw. Res. 43, 157–181 (1992)

    Article  Google Scholar 

  37. S. Enault, D.N. Muñoz, W.T.A.F. Silva, V. Borday-Birraux, M. Bonade, S. Oulion, S. Ventéo, S. Marcellini, M. Debiais-Thibaud, Molecular footprinting of skeletal tissues in the catshark Scyliorhinus canicula and the clawed frog Xenopus tropicalis identifies conserved and derived features of vertebrate calcification. Front. Genet. 6, 3133–3144 (2015)

    Article  Google Scholar 

  38. R. Seidel, M. Blumer, P. Zaslansky, D. Knötel, D.R. Huber, J.C. Weaver, P. Fratzl, S. Omelon, L. Bertinetti, M.N. Dean, Ultrastructural, material and crystallographic description of endophytic masses; a possible damage response in shark and ray tessellated calcified cartilage. J. Struct. Biol. 198, 5–18 (2017)

    Article  CAS  Google Scholar 

  39. A.K. Jayasankar, R. Seidel, J. Naumann, L. Guiducci, A. Hosny, P. Fratzl, J.C. Weaver, J.W.C. Dunlop, M.N. Dean, Mechanical behavior of idealized, stingray-skeleton-inspired tiled composites as a function of geometry and material properties. J. Mech. Behav. Biomed. Mater. 73, 1–35 (2017)

    Article  Google Scholar 

  40. M.N. Dean, R. Seidel, D. Knoetel, K. Lyons, D. Baum, J.C. Weaver, P. Fratzl, To build a shark-3D tiling laws of tessellated cartilage. Integr. Comp. Biol. 56, E50 (2016)

    Google Scholar 

  41. T.L. Ferrara, P. Clausen, D.R. Huber, C.R. McHenry, V. Peddemors, S. Wroe, Mechanics of biting in great white and sandtiger sharks. J. Biomech. 44, 430–435 (2011)

    Article  CAS  Google Scholar 

  42. X. Liu, M.N. Dean, H. Youssefpour, A.P. Summers, J.C. Earthman, Stress relaxation behavior of tessellated cartilage from the jaws of blue sharks. J. Mech. Behav. Biomed. Mater. 29, 68–80 (2014)

    Article  CAS  Google Scholar 

  43. M.E. Porter, J.L. Beltran, S.M. Kajiura, T.J. Koob, A.P. Summers, Stiffness without mineral: material properties and biochemical components of jaws and chondrocrania in the Elasmobranchii (sharks, skates, and rays). PeerJ 1, e47v1 (2013)

    Google Scholar 

  44. R. Martini, Y. Balit, F. Barthelat, A comparative study of bio-inspired protective scales using 3D printing and mechanical testing. Acta Biomater. 55, 360–372 (2017)

    Article  CAS  Google Scholar 

  45. S.R. Fahle, J.C. Thomason, Measurement of jaw viscoelasticity in newborn and adult lesser spotted dogfish Scyliorhinus canicula (L., 1758). J. Fish Biol. 72, 1553–1557 (2008)

    Article  Google Scholar 

  46. M. Egerbacher, M. Helmreich, E. Mayrhofer, P. Böck, Mineralisation of the hyaline cartilage in the small-spotted dogfish Scyliorhinus canicula L. Scripta Medica (BRNO) (2006)

    Google Scholar 

  47. T.L. Ferrara, P. Boughton, E. Slavich, S. Wroe, A novel method for single sample multi-axial nanoindentation of hydrated heterogeneous tissues based on testing great white shark jaws. PLoS ONE 8, e81196 (2013)

    Article  Google Scholar 

  48. S. Applegate, A survey of shark hard parts. In Sharks, Skates and Rays (1967), pp. 37–67

    Google Scholar 

  49. S. Wroe, D.R. Huber, M. Lowry, C. McHenry, K. Moreno, P. Clausen, T.L. Ferrara, E. Cunningham, M.N. Dean, A.P. Summers, Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? J. Zool. 276, 336–342 (2008)

    Article  Google Scholar 

  50. M.N. Dean, A.P. Summers, Mineralized cartilage in the skeleton of chondrichthyan fishes. Zoology 109, 164–168 (2006)

    Article  Google Scholar 

  51. A.P. Summers, Stiffening the stingray skeleton—an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). J. Morphol. 243, 113–126 (2000)

    Article  CAS  Google Scholar 

  52. A.P. Summers, R.A. Ketcham, T. Rowe, Structure and function of the horn shark (Heterodontus francisci) cranium through ontogeny: development of a hard prey specialist. J. Morphol. 260, 1–12 (2004)

    Article  Google Scholar 

  53. M.N. Dean, D.R. Huber, H.A. Nance, Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea. J. Morphol. 267, 1137–1146 (2006)

    Article  Google Scholar 

  54. M.A. Kolmann, S.B. Crofts, M.N. Dean, A.P. Summers, N.R. Lovejoy, Morphology does not predict performance: jaw curvature and prey crushing in durophagous stingrays. J. Exp. Biol. 218, 3941–3949 (2015)

    Article  Google Scholar 

  55. R. Seidel, M. Blumer, E.-J. Pechriggl, K. Lyons, B.K. Hall, P. Fratzl, J.C. Weaver, M.N. Dean, Calcified cartilage or bone? Collagens in the tessellated endoskeletons of cartilaginous fish (sharks and rays). J. Struct. Biol. 200, 1–35 (2017)

    Article  Google Scholar 

  56. J.P. Balaban, A.P. Summers, C.A. Wilga, Mechanical properties of the hyomandibula in four shark species. J. Exp. Zool. Part A Ecol. Genet. Physiol. 323, 1–9 (2014)

    Article  Google Scholar 

  57. M.N. Dean, J.J. Bizzarro, B. Clark, C.J. Underwood, Z. Johanson, Large batoid fishes frequently consume stingrays despite skeletal damage. R. Soc. Open Sci. 4, 170674–11 (2017)

    Google Scholar 

  58. C.A.D. Wilga, S.E. Diniz, P.R. Steele, J. Sudario-Cook, E.R. Dumont, L.A. Ferry, Ontogeny of feeding mechanics in smoothhound sharks: morphology and cartilage stiffness. Integr. Comp. Biol. 56, 442–448 (2016)

    Article  Google Scholar 

  59. G. Dingerkus, B. Seret, Multiple prismatic calcium phosphate layers in the jaws of present-day sharks (Chondrichthyes; Selachii). Experientia 47, 38–40 (1991)

    Article  CAS  Google Scholar 

  60. W. Huang, W. Hongjamrassilp, J.-Y. Jung, P.A. Hastings, V.A. Lubarda, J. McKittrick, Structure and mechanical implications of the pectoral fin skeleton in the Longnose Skate (Chondrichthyes, Batoidea). Acta Biomater. 51, 393–407 (2017)

    Article  Google Scholar 

  61. P. Fratzl, O. Kolednik, F.D. Fischer, M.N. Dean, The mechanics of tessellations—bioinspired strategies for fracture resistance. Chemical Society Reviews 45, 252–267 (2016)

    Article  CAS  Google Scholar 

  62. X. Liu, M.N. Dean, A.P. Summers, J.C. Earthman, Composite model of the shark’s skeleton in bending: a novel architecture for biomimetic design of functional compression bias. Mater. Sci. Eng. C 30, 1077–1084 (2010)

    Article  CAS  Google Scholar 

  63. M.N. Dean, J.T. Schaefer, Patterns of growth and mineralization in elasmobranch cartilage. Faseb J. 19, A247–A247 (2005)

    Google Scholar 

  64. L.A. Jawad, Hyperostosis in three fish species collected from the Sea of Oman. Anat. Rec. 296, 1145–1147 (2013)

    Article  Google Scholar 

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Seidel, R., Jayasankar, A.K., Shahar, R., Dean, M.N. (2019). The Multiscale Architectures of Fish Bone and Tessellated Cartilage and Their Relation to Function. In: Estrin, Y., Bréchet, Y., Dunlop, J., Fratzl, P. (eds) Architectured Materials in Nature and Engineering. Springer Series in Materials Science, vol 282. Springer, Cham. https://doi.org/10.1007/978-3-030-11942-3_11

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