Advertisement

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

  • Ronald Seidel
  • Aravind K. Jayasankar
  • Ron Shahar
  • Mason N. DeanEmail author
Chapter
Part of the Springer Series in Materials Science book series (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.

References

  1. 1.
    P.C.J. Donoghue, I.J. Sansom, Origin and early evolution of vertebrate skeletonization. Microsc. Res. Tech. 59, 352–372 (2002)CrossRefGoogle Scholar
  2. 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)CrossRefGoogle Scholar
  3. 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)CrossRefGoogle Scholar
  4. 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)CrossRefGoogle Scholar
  5. 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)CrossRefGoogle Scholar
  6. 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. 397–420CrossRefGoogle Scholar
  7. 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)CrossRefGoogle Scholar
  8. 8.
    J.D. Currey, The design of mineralised hard tissues for their mechanical functions. J. Exp. Biol. 202, 3285–3294 (1999)Google Scholar
  9. 9.
    J.D. Currey, The structure and mechanics of bone. J. Mater. Sci. 47, 41–54 (2011)CrossRefGoogle Scholar
  10. 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)CrossRefGoogle Scholar
  11. 11.
    M.L. Moss, A.S. Posner, X-ray diffraction study of acellular teleost bone. Nature 188, 1037–1038 (1960)CrossRefGoogle Scholar
  12. 12.
    M.R. Urist, Calcium and phosphorus in the blood and skeleton of the Elasmobranchii, 1–24 (1961)Google Scholar
  13. 13.
    J.W. Smith, Collagen fibre patterns in mammalian bone. J. Anat. 94, 329–344 (1960)Google Scholar
  14. 14.
    L.F. Bonewald, The amazing osteocyte. J. Bone Miner. Res. 26, 229–238 (2011)CrossRefGoogle Scholar
  15. 15.
    S.L. Dallas, M. Prideaux, L.F. Bonewald, The osteocyte: an endocrine cell … and more. Endocr. Rev. 34, 658–690 (2013)CrossRefGoogle Scholar
  16. 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. 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)CrossRefGoogle Scholar
  18. 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)CrossRefGoogle Scholar
  19. 19.
    G.S. Helfman, B.B. Collette, D.E. Facey, B.W. Bowen, The Diversity of Fishes: Biology (Wiley-Blackwell, 2009)Google Scholar
  20. 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)CrossRefGoogle Scholar
  21. 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)CrossRefGoogle Scholar
  22. 22.
    N. Reznikov, R. Shahar, S. Weiner, Bone hierarchical structure in three dimensions. Acta Biomater. 10, 3815–3826 (2014)CrossRefGoogle Scholar
  23. 23.
    L.B. Halstead, Calcified tissues in the earliest vertebrates. Calcif. Tissue Int. 3, 107–124 (1969)CrossRefGoogle Scholar
  24. 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)CrossRefGoogle Scholar
  25. 25.
    A. Kölliker, On the different types in the microscopic structure of the skeleton of osseous fishes (1857)Google Scholar
  26. 26.
    M.L. Moss, Studies of the acellular bone of teleost fish. Cells Tissues Organs 46, 343–362 (1961)CrossRefGoogle Scholar
  27. 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)CrossRefGoogle Scholar
  28. 28.
    T. Ørvig, Histologic studies of placoderms and fossil elasmobranchs, 1–152 (1950)Google Scholar
  29. 29.
    D.E. Ashhurst, The cartilaginous skeleton of an elasmobranch fish does not heal. Matrix Biol. 23, 15–22 (2004)CrossRefGoogle Scholar
  30. 30.
    B.K. Hall, Bones and Cartilage, 2nd edn. (Academic Press, 2014)Google Scholar
  31. 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)CrossRefGoogle Scholar
  32. 32.
    N.E. Kemp, S.K. Westin, Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks. J. Morphol. 160, 75–101 (1979)CrossRefGoogle Scholar
  33. 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. 34.
    J.G. Maisey, The diversity of tessellated calcification in modern and extinct chondrichthyans. Rev. Paléobiol. Genève 32, 355–371 (2013)Google Scholar
  35. 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)CrossRefGoogle Scholar
  36. 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)CrossRefGoogle Scholar
  37. 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)CrossRefGoogle Scholar
  38. 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)CrossRefGoogle Scholar
  39. 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)CrossRefGoogle Scholar
  40. 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. 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)CrossRefGoogle Scholar
  42. 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)CrossRefGoogle Scholar
  43. 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. 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)CrossRefGoogle Scholar
  45. 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)CrossRefGoogle Scholar
  46. 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. 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)CrossRefGoogle Scholar
  48. 48.
    S. Applegate, A survey of shark hard parts. In Sharks, Skates and Rays (1967), pp. 37–67Google Scholar
  49. 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)CrossRefGoogle Scholar
  50. 50.
    M.N. Dean, A.P. Summers, Mineralized cartilage in the skeleton of chondrichthyan fishes. Zoology 109, 164–168 (2006)CrossRefGoogle Scholar
  51. 51.
    A.P. Summers, Stiffening the stingray skeleton—an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). J. Morphol. 243, 113–126 (2000)CrossRefGoogle Scholar
  52. 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)CrossRefGoogle Scholar
  53. 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)CrossRefGoogle Scholar
  54. 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)CrossRefGoogle Scholar
  55. 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)CrossRefGoogle Scholar
  56. 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)CrossRefGoogle Scholar
  57. 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. 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)CrossRefGoogle Scholar
  59. 59.
    G. Dingerkus, B. Seret, Multiple prismatic calcium phosphate layers in the jaws of present-day sharks (Chondrichthyes; Selachii). Experientia 47, 38–40 (1991)CrossRefGoogle Scholar
  60. 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)CrossRefGoogle Scholar
  61. 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)CrossRefGoogle Scholar
  62. 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)CrossRefGoogle Scholar
  63. 63.
    M.N. Dean, J.T. Schaefer, Patterns of growth and mineralization in elasmobranch cartilage. Faseb J. 19, A247–A247 (2005)Google Scholar
  64. 64.
    L.A. Jawad, Hyperostosis in three fish species collected from the Sea of Oman. Anat. Rec. 296, 1145–1147 (2013)CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ronald Seidel
    • 1
  • Aravind K. Jayasankar
    • 1
  • Ron Shahar
    • 2
  • Mason N. Dean
    • 1
    Email author
  1. 1.Department of BiomaterialsMax Planck Institute of Colloids and InterfacesPotsdamGermany
  2. 2.The Robert H. Smith Faculty of Agriculture, Food and Environmental Sciences, Koret School of Veterinary MedicineThe Hebrew University of JerusalemRehovotIsrael

Personalised recommendations