Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Materials design principles of ancient fish armour

Abstract

Knowledge of the structure–property–function relationships of dermal scales of armoured fish could enable pathways to improved bioinspired human body armour, and may provide clues to the evolutionary origins of mineralized tissues. Here, we present a multiscale experimental and computational approach that reveals the materials design principles present within individual ganoid scales from the ‘living fossil’ Polypterus senegalus. This fish belongs to the ancient family Polypteridae, which first appeared 96 million years ago during the Cretaceous period and still retains many of their characteristics. The mechanistic origins of penetration resistance (approximating a biting attack) were investigated and found to include the juxtaposition of multiple distinct reinforcing composite layers that each undergo their own unique deformation mechanisms, a unique spatial functional form of mechanical properties with regions of differing levels of gradation within and between material layers, and layers with an undetectable gradation, load-dependent effective material properties, circumferential surface cracking, orthogonal microcracking in laminated sublayers and geometrically corrugated junctions between layers.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structure of Polypterus senegalus scale.
Figure 2: Mechanical properties derived from nanoindentation experiments across the cross-section of the different material layers of an individual P. senegalus scale.
Figure 3: Predictions of effective microindentation mechanical properties of P. senegalus scale via multilayered FEA simulations.
Figure 4: Simulation contours of stress, plastic strain and pressure fields of a P. senegalus scale via multilayered FEA simulations.
Figure 5: Topographic profiles, residual impressions of microindentation and fracture of an individual P. senegalus scale.

Similar content being viewed by others

References

  1. Hoedeman, J. J. Naturalists Guide to Fresh Water Aquarium Fish (Sterling Publishing Co., Oak Tree Press Co., New York, London, and Sydney, 1974).

    Google Scholar 

  2. Colbert, E. H. Evolution of the Vertebrates: A History of Backboned Animals Through Time (Wiley, New York, 1955).

    Google Scholar 

  3. Miller, H. The Cruise of the Betsy or Summer Holiday in the Hebrides with Rambles of a Geologist or Ten Thousand Miles of Fossiliferous Deposits of Scotland (Gould and Lincoln, Boston, 1857).

    Google Scholar 

  4. Romer, A. S. Eurypterid influence on vertebrate history. Science 78, 114–117 (1933).

    Article  CAS  Google Scholar 

  5. Ørvig, T. in Proc. 4th Nobel Symp. (ed. Ørvig, T.) 373–397 (Almqvist and Wiskell, Stockholm, 1968).

    Google Scholar 

  6. Long, J. H. & Nipper, K. S. The importance of body stiffness in undulatory propulsion. Am. Zool. 36, 678–694 (1996).

    Article  Google Scholar 

  7. Raschi, W. & Tabit, C. Functional aspects of placoid scales: A review and update. Aust. J. Mar. Freshw. Res. 43, 123–147 (1992).

    Article  Google Scholar 

  8. Anderson, P. S. L. & Westneat, M. W. Feeding mechanics and bite force modelling of the skull of Dunkleosteus terrelli, an ancient apex predator. Biol. Lett. 22, 76–79 (2007).

    Google Scholar 

  9. Arciszewski, T. & Cornell, J. in Bio-Inspiration: Learning Creative Design Principia (ed. Smith, I. F. C.) (Springer, Berlin, 2006).

    Google Scholar 

  10. Weiner, S. & Addadi, L. Design strategies in mineralized biological materials. J. Mater. Chem. 7, 689–702 (1997).

    Article  CAS  Google Scholar 

  11. Gao, H., Ji, B., Jager, I. L., Arzt, E. & Fratzl, P. Materials become insensitive to flaws at nanoscale: Lessons from nature. Proc. Natl Acad. Sci. USA 100, 5597–5600 (2003).

    Article  CAS  Google Scholar 

  12. Buehler, M. J. Molecular nanomechanics of nascent bone: Fibrillar toughening by mineralization. Nanotechnology 18, 1–9 (2007).

    Article  Google Scholar 

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

    CAS  Google Scholar 

  14. Fantner, G. E. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Mater. 4, 612–616 (2005).

    Article  CAS  Google Scholar 

  15. Tai, K., Dao, M., Suresh, S., Palazoglu, A. & Ortiz, C. Nanoscale heterogeneity promotes energy dissipation in bone. Nature Mater. 6, 454–462 (2007).

    Article  CAS  Google Scholar 

  16. Balooch, G. et al. Evaluation of a new modulus mapping technique to investigate microstructural features of human teeth. J. Biomech. 37, 1223–1232 (2004).

    Article  CAS  Google Scholar 

  17. Bruet, B. J. F. et al. Nanoscale morphology and indentation of individual nacre tablets from the gastropod mollusc Trochus niloticus. J. Mater. Res. 20, 2400–2419 (2005).

    Article  CAS  Google Scholar 

  18. Raabe, D., Sachs, C. & Romano, P. The crustacean exoskeleton as an example of a structurally and mechanically graded biological nanocomposite material. Acta Mater. 53, 4281–4292 (2005).

    Article  CAS  Google Scholar 

  19. Barbakadze, N., Enders, S., Gorb, S. & Arzt, E. Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J. Exp. Biol. 209, 722–730 (2006).

    Article  CAS  Google Scholar 

  20. Ortiz, C. & Boyce, M. C. Bioinspired structural materials. Science 319, 1053–1054 (2008).

    Article  CAS  Google Scholar 

  21. Daget, J., Gayet, M., Meunier, F. J. & Sire, J.-Y. Major discoveries on the dermal skeleton of fossil and recent polypteriforms: A review. Fish Fisheries 2, 113–124 (2001).

    Article  Google Scholar 

  22. Kodera, H. et al. Jurassic Fishes: Selection, Care, Behavior (T. F. H. Publications, New Jersey, 1994).

    Google Scholar 

  23. Carroll, R. L. Vertebrate Paleontology and Evolution (W. H. Freeman and Company, New York, 1988).

    Google Scholar 

  24. Oliver, W. C. & Pharr, G. M. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564–1583 (1992).

    Article  CAS  Google Scholar 

  25. Ørvig, T. in Structural and Chemical Organization of Teeth (ed. Miles, A. E.) Ch. 2, 45–110 (Academic, New York, 1967).

    Google Scholar 

  26. Meunier, F. J. Recherches histologiques sur le squelette dermique des Polypteridae. Archives de Zoologie Expérimentale et Générale 122, 279–295 (1980).

    Google Scholar 

  27. Meunier, F. J. Os cellulaire, os acellulaire et tissus dérivés chez les Ostéichthyens: Les phénomènes de l’acellularisation et de la perte de minéralisation. L’Année Biologique 26, 201–233 (1987).

    CAS  Google Scholar 

  28. Sire, J.-Y. From ganoid to elasmoid scales in the Actinopterygian fishes. Neth. J. Zool. 40, 75–92 (1990).

    Article  Google Scholar 

  29. Jayachandran, R., Boyce, M. C. & Argon, A. S. Design of multilayer polymeric coatings for indentation resistance. J. Comput.-Aided Mater. Design 2, 151–166 (1995).

    Article  CAS  Google Scholar 

  30. Markey, M. J., Main, R. P. & Marshall, C. R. In vivo cranial suture function and suture morphology in the extant fish Polypterus: Implications for inferring skull function in living and fossil fish. J. Exp. Biol. 209, 2085–2102 (2006).

    Article  Google Scholar 

  31. Lauder, G. V. Evolution of the feeding mechanism in primitive actinopterygian fishes; a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. J. Morphol. 163, 283–317 (1980).

    Article  Google Scholar 

  32. Gemballa, S. & Bartsch, P. Architecture of the integument in lower Teleostomes: Functional morphology and evolutionary implications. J. Morphol. 253, 290–309 (2002).

    Article  Google Scholar 

  33. Tai, K., Ulm, F.-J. & Ortiz, C. Nanogranular origins of the strength of bone. Nano Lett. 6, 2520–2525 (2006).

    Article  CAS  Google Scholar 

  34. Gupta, H. S. et al. Nanoscale deformation mechanisms in bone. Nano Lett. 5, 2108–2111 (2005).

    Article  CAS  Google Scholar 

  35. Tai, K., Qi, H.-J. & Ortiz, C. Effect of mineral content on the nanoindentation properties and nanoscale deformation mechanisms of bovine tibial cortical bone. J. Mater. Sci.: Mater. Med. 16, 947–959 (2005).

    CAS  Google Scholar 

  36. Nalla, R. K., Kinney, J. H. & Ritchie, R. O. Mechanistic fracture criteria for the failure of human cortical bone. Nature Mater. 2, 164–168 (2003).

    Article  CAS  Google Scholar 

  37. Imbeni, V., Kruzic, J. J., Marshall, G. W. & Ritchie, R. O. The dentin–enamel junction and the fracture of human teeth. Nature Mater. 4, 229–232 (2005).

    Article  CAS  Google Scholar 

  38. Suresh, S. Graded materials for resistance to contact deformation and damage. Science 292, 2447–2451 (2001).

    Article  CAS  Google Scholar 

  39. Shimizu, D. & Macho, G. A. Functional significance of the microstructural detail of the primate dentino-enamel junction: A possible example of exaption. J. Human Evolut. 52, 103–111 (2007).

    Article  Google Scholar 

  40. Humphries, J. Polypterus senegalus, online digital morphology. Accessed June 1, 2007 at <http://digimorph.Org/specimens/polypterus_senegalus/whole/> (Michigan Museum of Zoology) (ummz 195008). (2003).

Download references

Acknowledgements

The authors thank the MIT Department of Materials Science and Engineering Nanomechanical Testing Facility, the National Science Foundation MIT Center for Materials Science and Engineering, the Centre de Recherche de la Matière Condensée et des Nanosciences (CRMC-N) at Université de Marseille-Luminy, France, the MIT International Science and Technology Initiatives—France Seed Fund and the US Army through the MIT Institute for Soldier Nanotechnologies (contract number DAAD-19-02-D0002), as well as R. Jensen and T. Weerasooriya from the US Army Research Laboratory and T. Imholt from Raytheon for discussions. The content does not necessarily reflect the position of the government and no official endorsement should be inferred. The authors would also like to thank E. Chen, J. H. Choi, J. Kim, J. Y. Mao, M. D. Mascaro and E. R. Pfeiffer for assisting with initial sample preparation and preliminary data, A. Baronnet for assistance with electron microscopy and G. Lauder (Harvard University) for carrying out the scale-removal surgery.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christine Ortiz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bruet, B., Song, J., Boyce, M. et al. Materials design principles of ancient fish armour. Nature Mater 7, 748–756 (2008). https://doi.org/10.1038/nmat2231

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nmat2231

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing