A natural impact-resistant bicontinuous composite nanoparticle coating

Abstract

Nature utilizes the available resources to construct lightweight, strong and tough materials under constrained environmental conditions. The impact surface of the fast-striking dactyl club from the mantis shrimp is an example of one such composite material; the shrimp has evolved the capability to localize damage and avoid catastrophic failure from high-speed collisions during its feeding activities. Here we report that the dactyl club of mantis shrimps contains an impact-resistant coating composed of densely packed (about 88 per cent by volume) ~65-nm bicontinuous nanoparticles of hydroxyapatite integrated within an organic matrix. These mesocrystalline hydroxyapatite nanoparticles are assembled from small, highly aligned nanocrystals. Under impacts of high strain rates (around 104 s−1), particles rotate and translate, whereas the nanocrystalline networks fracture at low-angle grain boundaries, form dislocations and undergo amorphization. The interpenetrating organic network provides additional toughening, as well as substantial damping, with a loss coefficient of around 0.02. An unusual combination of stiffness and damping is therefore achieved, outperforming many engineered materials.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Impact surface of the dactyl club of the mantis shrimp.
Fig. 2: Nanoarchitectural design features of particles within the impact surface of the dactyl club.
Fig. 3: Effects of high-strain-rate microimpact tests, damping behaviour and energy dissipation of the impact surface of the dactyl club.
Fig. 4: Ashby plot of loss coefficient and Young’s modulus of synthetic and natural materials.
Fig. 5: Nanoscale energy dissipation mechanisms of the impact surface of the dactyl club.
Fig. 6: Molecular dynamic simulations of the energy dissipation in the bicontinuous HAP nanoparticles.

Data availability

All the data that support the findings of this study are provided in the Supplementary Information and source data. Source data are provided with this paper.

References

  1. 1.

    Bhatnagar, A. Lightweight Ballistic Composites: Military and Law-Enforcement Applications (Woodhead, 2016).

  2. 2.

    Dalili, N., Edrisy, A. & Carriveau, R. A review of surface engineering issues critical to wind turbine performance. Renew. Sustain. Energy Rev. 13, 428–438 (2009).

    Google Scholar 

  3. 3.

    Munch, E. et al. Tough, bio-inspired hybrid materials. Science 322, 1516–1520 (2008).

    CAS  Google Scholar 

  4. 4.

    Grunenfelder, L. et al. Bio-inspired impact-resistant composites. Acta Biomater 10, 3997–4008 (2014).

    CAS  Google Scholar 

  5. 5.

    Yaraghi, N. A. & Kisailus, D. Biomimetic structural materials: inspiration from design and assembly. Annu Rev. Phys. Chem. 69, 23–57 (2018).

    CAS  Google Scholar 

  6. 6.

    Chen, P. Y., McKittrick, J. & Meyers, M. A. Biological materials: functional adaptations and bioinspired designs. Prog. Mater. Sci. 57, 1492–1704 (2012).

    CAS  Google Scholar 

  7. 7.

    Yin, Z., Hannard, F. & Barthelat, F. Impact-resistant nacre-like transparent materials. Science 364, 1260–1263 (2019).

    CAS  Google Scholar 

  8. 8.

    Gu, G. X., Takaffoli, M. & Buehler, M. J. Hierarchically enhanced impact resistance of bioinspired composites. Adv. Mater. 29, 1700060 (2017).

    Google Scholar 

  9. 9.

    Huang, W., Zaheri, A., Jung, J.-Y., Espinosa, H. D. & Mckittrick, J. Hierarchical structure and compressive deformation mechanisms of bighorn sheep (Ovis canadensis) horn. Acta Biomater. 64, 1–14 (2017).

    Google Scholar 

  10. 10.

    Wegst, U. G. K., Bai, H., Saiz, E., Tomsia, A. P. & Ritchie, R. O. Bioinspired structural materials. Nat. Mater. 14, 23–36 (2015).

    CAS  Google Scholar 

  11. 11.

    Huang, W. et al. Multiscale toughening mechanisms in biological materials and bioinspired designs. Adv. Mater. 31, 1901561 (2019).

    CAS  Google Scholar 

  12. 12.

    Schaffler, M., Radin, E. & Burr, D. Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone 10, 207–214 (1989).

    CAS  Google Scholar 

  13. 13.

    Launey, M. E., Chen, P.-Y., McKittrick, J. & Ritchie, R. Mechanistic aspects of the fracture toughness of elk antler bone. Acta Biomater. 6, 1505–1514 (2010).

    CAS  Google Scholar 

  14. 14.

    Li, L. & Ortiz, C. Pervasive nanoscale deformation twinning as a catalyst for efficient energy dissipation in a bioceramic armour. Nat. Mater. 13, 501–507 (2014).

    CAS  Google Scholar 

  15. 15.

    Shin, Y. A. et al. Nanotwin-governed toughening mechanism in hierarchically structured biological materials. Nat. Commun. 7, 10772 (2016).

    CAS  Google Scholar 

  16. 16.

    Pellman, E. J., Viano, D. C., Tucker, A. M., Casson, I. R. & Waeckerle, J. F. Concussion in professional football: reconstruction of game impacts and injuries. Neurosurgery 53, 799–814 (2003).

    Google Scholar 

  17. 17.

    Weaver, J. C. et al. The stomatopod dactyl club: a formidable damage-tolerant biological hammer. Science 336, 1275–1280 (2012).

    CAS  Google Scholar 

  18. 18.

    Caldwell, R. L. & Dingle, H. Stomatopods. Sci. Am. 234, 80–89 (1976).

    Google Scholar 

  19. 19.

    Yaraghi, N. A. et al. A sinusoidally architected helicoidal biocomposite. Adv. Mater. 28, 6835–6844 (2016).

    CAS  Google Scholar 

  20. 20.

    Amini, S., Tadayon, M., Idapalapati, S. & Miserez, A. The role of quasi-plasticity in the extreme contact damage tolerance of the stomatopod dactyl club. Nat. Mater. 14, 943–950 (2015).

    CAS  Google Scholar 

  21. 21.

    Grunenfelder, L. K. et al. Ecologically driven ultrastructural and hydrodynamic designs in stomatopod cuticles. Adv. Mater. 30, 1705295 (2018).

    Google Scholar 

  22. 22.

    Suksangpanya, N., Yaraghi, N. A., Kisailus, D. & Zavattieri, P. Twisting cracks in Bouligand structures. J. Mech. Behav. Biomed. 76, 38–57 (2017).

    Google Scholar 

  23. 23.

    Cölfen, H. & Mann, S. Higher‐order organization by mesoscale self‐assembly and transformation of hybrid nanostructures. Angew. Chem. Int. Ed. 42, 2350–2365 (2003).

    Google Scholar 

  24. 24.

    De Yoreo, J. J. et al. Crystallization by particle attachment in synthetic, biogenic, and geologic environments. Science 349, aaa6760 (2015).

    Google Scholar 

  25. 25.

    Rinaudo, M. Chitin and chitosan: properties and applications. Prog. Polym. Sci. 31, 603–632 (2006).

    CAS  Google Scholar 

  26. 26.

    Neville, A. & Luke, B. A two-system model for chitin–protein complexes in insect cuticles. Tissue Cell 1, 689–707 (1969).

    CAS  Google Scholar 

  27. 27.

    Watson, M. L. Staining of tissue sections for electron microscopy with heavy metals. J. Cell Biol. 4, 475–478 (1958).

    CAS  Google Scholar 

  28. 28.

    Gordon, L. M. & Joester, D. Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth. Nature 469, 194–197 (2011).

    CAS  Google Scholar 

  29. 29.

    Li, H., Xin, H. L., Muller, D. A. & Estroff, L. A. Visualizing the 3D internal structure of calcite single crystals grown in agarose hydrogels. Science 326, 1244–1247 (2009).

    CAS  Google Scholar 

  30. 30.

    Kim, Y.-Y. et al. Tuning hardness in calcite by incorporation of amino acids. Nat. Mater. 15, 903 (2016).

    CAS  Google Scholar 

  31. 31.

    McKenzie, B. E. et al. Controlling internal pore sizes in bicontinuous polymeric nanospheres. Angew. Chem. Int. Ed. 54, 2457–2461 (2015).

    CAS  Google Scholar 

  32. 32.

    Zhang, Q., Liu, S.-J. & Yu, S.-H. Recent advances in oriented attachment growth and synthesis of functional materials: concept, evidence, mechanism, and future. J. Mater. Chem. 19, 191–207 (2009).

    CAS  Google Scholar 

  33. 33.

    Cöelfen, H. & Antonietti, M. Mesocrystals and Nonclassical Crystallization (John Wiley & Sons, 2008).

  34. 34.

    Nudelman, F. et al. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 9, 1004–1009 (2010).

    CAS  Google Scholar 

  35. 35.

    Song, R. Q. & Cölfen, H. Mesocrystals—ordered nanoparticle superstructures. Adv. Mater. 22, 1301–1330 (2010).

    CAS  Google Scholar 

  36. 36.

    Nielsen, J. H. Remaining stress-state and strain-energy in tempered glass fragments. Glass Struct. Eng. 2, 45–56 (2017).

    Google Scholar 

  37. 37.

    Cho, K. R. et al. Direct observation of mineral–organic composite formation reveals occlusion mechanism. Nat. Commun. 7, 10187 (2016).

    Google Scholar 

  38. 38.

    Kim, Y.-Y. et al. An artificial biomineral formed by incorporation of copolymer micelles in calcite crystals. Nat. Mater. 10, 890–896 (2011).

    CAS  Google Scholar 

  39. 39.

    Sato, M., Schwarz, W. H. & Pollard, T. D. Dependence of the mechanical properties of actin/α-actinin gels on deformation rate. Nature 325, 828–830 (1987).

    CAS  Google Scholar 

  40. 40.

    Jin, K., Feng, X. & Xu, Z. Mechanical properties of chitin–protein interfaces: a molecular dynamics study. BioNanoScience 3, 312–320 (2013).

    Google Scholar 

  41. 41.

    Ashby, M. F. Materials Selection in Mechanical Design (Butterworth-Heinemann, 2011).

  42. 42.

    Unwin, A. P. et al. Escaping the Ashby limit for mechanical damping/stiffness trade-off using a constrained high internal friction interfacial layer. Sci. Rep. 8, 2454 (2018).

    CAS  Google Scholar 

  43. 43.

    Chung, D. Materials for vibration damping. J. Mater. Sci. 36, 5733–5737 (2001).

    CAS  Google Scholar 

  44. 44.

    Huang, Z. W. et al. Uncovering high-strain rate protection mechanism in nacre. Sci. Rep. 1, 148 (2011).

    CAS  Google Scholar 

  45. 45.

    Chen, M., McCauley, J. W. & Hemker, K. J. Shock-induced localized amorphization in boron carbide. Science 299, 1563–1566 (2003).

    CAS  Google Scholar 

  46. 46.

    Huang, W. et al. How water can affect keratin: hydration‐driven recovery of bighorn sheep (Ovis canadensis) horns. Adv. Funct. Mater. 29, 1901077 (2019).

    Google Scholar 

  47. 47.

    Cho, H. et al. Engineering the mechanics of heterogeneous soft crystals. Adv. Funct. Mater. 26, 6938–6949 (2016).

    CAS  Google Scholar 

  48. 48.

    Lee, J.-H., Wang, L., Boyce, M. C. & Thomas, E. L. Periodic bicontinuous composites for high specific energy absorption. Nano Lett. 12, 4392–4396 (2012).

    CAS  Google Scholar 

  49. 49.

    Gutierrez, J., Tercjak, A. & Mondragon, I. Conductive behavior of high TiO2 nanoparticle content of inorganic/organic nanostructured composites. J. Am. Chem. Soc. 132, 873–878 (2010).

    CAS  Google Scholar 

  50. 50.

    Moore, D. G., Barbera, L., Masania, K. & Studart, A. R. Three-dimensional printing of multicomponent glasses using phase-separating resins. Nat. Mater. 19, 212–217 (2020).

    CAS  Google Scholar 

  51. 51.

    Labuda, A., Kocuń, M., Meinhold, W., Walters, D. & Proksch, R. Generalized hertz model for bimodal nanomechanical mapping. Beilstein J. Nanotechnol. 7, 970–982 (2016).

    CAS  Google Scholar 

  52. 52.

    Kocun, M., Labuda, A., Meinhold, W., Revenko, I. N. & Proksch, R. Fast, high resolution, and wide modulus range nanomechanical mapping with bimodal tapping mode. ACS Nano 11, 10097–10105 (2017).

    CAS  Google Scholar 

  53. 53.

    Benaglia, S., Amo, C. A. & Garcia, R. Fast, quantitative and high resolution mapping of viscoelastic properties with bimodal AFM. Nanoscale 11, 15289–15297 (2019).

    CAS  Google Scholar 

  54. 54.

    Asif, S. S., Wahl, K. & Colton, R. Nanoindentation and contact stiffness measurement using force modulation with a capacitive load-displacement transducer. Rev. Sci. Instrum. 70, 2408–2413 (1999).

    CAS  Google Scholar 

  55. 55.

    Syed Asif, S., Wahl, K., Colton, R. & Warren, O. Quantitative imaging of nanoscale mechanical properties using hybrid nanoindentation and force modulation. J. Appl. Phys. 90, 1192–1200 (2001).

    CAS  Google Scholar 

  56. 56.

    Plimpton, S. Fast parallel algorithms for short-range molecular dynamics. J. Comput. Phys. 117, 1–19 (1995).

    CAS  Google Scholar 

  57. 57.

    Lin, T.-J. & Heinz, H. Accurate force field parameters and pH resolved surface models for hydroxyapatite to understand structure, mechanics, hydration, and biological interfaces. J. Phys. Chem. C 120, 4975–4992 (2016).

    CAS  Google Scholar 

  58. 58.

    Ching, W., Rulis, P. & Misra, A. Ab initio elastic properties and tensile strength of crystalline hydroxyapatite. Acta Biomater. 5, 3067–3075 (2009).

    CAS  Google Scholar 

  59. 59.

    Espanol, M., Portillo, J., Manero, J.-M. & Ginebra, M.-P. Investigation of the hydroxyapatite obtained as hydrolysis product of α-tricalcium phosphate by transmission electron microscopy. CrystEngComm 12, 3318–3326 (2010).

    CAS  Google Scholar 

  60. 60.

    Zhao, S. et al. Shock-induced amorphization in silicon carbide. Acta Mater. 158, 206–213 (2018).

    CAS  Google Scholar 

  61. 61.

    Lin, S., Cai, Z., Wang, Y., Zhao, L. & Zhai, C. Tailored morphology and highly enhanced phonon transport in polymer fibers: a multiscale computational framework. npj Comput. Mater. 5, 126 (2019).

    CAS  Google Scholar 

  62. 62.

    Ramachandramoorthy, R., Gao, W., Bernal, R. & Espinosa, H. High strain rate tensile testing of silver nanowires: rate-dependent brittle-to-ductile transition. Nano Lett. 16, 255–263 (2016).

    CAS  Google Scholar 

  63. 63.

    Fang, Q., Tian, Y., Wu, H. & Li, J. Revealing the deformation mechanism of amorphous polyethylene subjected to cycle loading via molecular dynamics simulations. RSC Adv. 8, 32377–32386 (2018).

    CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge N. A. Yaraghi for his work and support in the initial stage of the project. We also acknowledge L. G. Hector for his support and discussions on the application of these designs. We acknowledge funding from the Air Force Office of Scientific Research Multi-University Research Initiative (MURI AFOSR-FA9550-15-1-0009); D.K. also acknowledges funding from the Air Force Office of Scientific Research (AFOSR-FA9550-10-1-0322, AFOSR-FA9550-17-1-0449 and AFOSR-FA9550-18-1-0424) and the Army Research Office (ARO-W911NF-16-1-0208).

Author information

Affiliations

Authors

Contributions

D.K. initiated and planned the project. W.H. performed the sample preparation, characterization and mechanical experiments. M.S., N.G.-Z. and P.Z. performed the computational simulations and provided analyses and writing on simulations. N.D.K. and J.L. did the AFM tests and data analysis. L.C. performed TGA and DSC, T.W. performed the TEM sample staining and EDX, S.B. and W.H. performed the in situ TEM mechanical tests. D.S. and P.M. performed the nanoindentation and nanoDMA tests and data analysis. K.N.B. provided support on the TEM experiments as well as data analysis. R.C. provided discussion on the evolutionary and biological aspects of the manuscript. W.H. and D.K. wrote the manuscript. All the authors made edits and revisions on the final draft.

Corresponding author

Correspondence to David Kisailus.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 TEM and HRTEM micrographs of hydroxyapatite (HAP) composite nanoparticles within the impact surface.

TEM and HRTEM micrographs of hydroxyapatite (HAP) composite nanoparticles within the impact surface. a, Secondary HAP nanoparticles marked with red outlines. The yellow dashed lines show the alignment of primary particles within a single secondary HAP particle. b, SAED pattern from the TEM image in (a). The small arcs indicate slight mis-alignments of nanocrystals within the secondary particle. c, HRTEM image of a single HAP particle, with brighter contrast regions suggesting the presence of a secondary phase. d, FFT of the particle in (c). (e) HRTEM of the (100) lattice in the HAP nanocrystals. Insets: Stacking faults are observed within primary particles. Three independent dactyl clubs from 3 different mantis shrimps were examined in TEM. Similar results as shown in (ae) were observed.

Extended Data Fig. 2 HRTEM of uranyl acetate and lead citrate stained HAP nanoparticles on the impact surface.

HRTEM of uranyl acetate and lead citrate stained HAP nanoparticles on the impact surface. The reduced ordering in protein complexes provide a higher permeability for the heavy metal staining solution, resulting in greater contrast in the TEM micrograph. a, HRTEM of a HAP nanoparticle, showing chitin macromolecules wrapping around the HAP crystal. b, FFT of the HAP crystal lattice indicated with a purple box in (a). Both diffraction spots and rings are observed in the FFT pattern. Inverse Fast Fourier Transform (IFFT) is performed on the diffraction spots and rings, separately. The yellow box (upper, right inset) shows the HAP lattice after IFFT, while red box (lower, left) shows the location of chitin macromolecules. c, HRTEM of a HAP nanoparticle. d, FFT of the HAP nanoparticle in (c). The (201) reflection from HAP is indicated with a yellow arrow, whereas the (003) planes of chitin (diffraction ring) are highlighted by the green arrow. e, f, HRTEM showing the interface between chitin macromolecules and a HAP nanocrystal. The (201) crystal planes of HAP appear adjacent with (003) planes of chitin, suggesting a potential epitaxial growth of HAP on chitin macromolecules. Three independent dactyl clubs from 3 different mantis shrimps were examined in HRTEM. Similar results as shown in (af) were observed.

Extended Data Fig. 3 Strain-rate-dependent behaviour in the impact surface of dactyl club.

Strain-rate-dependent behaviour in the impact surface of dactyl club. Load–displacement curves of quasi-static nanoindentation on the impact surface with a sharp cube corner a, and a blunt spherical indenter head b, cf, SEM micrographs of the damage modes in quasi-static nanoindentation and impacts with sharp and blunt indenter heads. g, SEM images showing particle pile up and crack initiation and propagation. h, i, TEM images of HAP nanoparticles after indentation. The secondary HAP particles remain intact after quasi-static nanoindentation. Quasi-static indentation tests on five independent locations within two different dactyl clubs were performed and examined. Similar damage modes shown in (ci) were observed. Source data

Extended Data Fig. 4 In situ compression tests of single HAP nanoparticles.

In situ compression tests of single HAP nanoparticles. ad, HAP nanoparticle before and after compression tests, indicating particle breakage. Five different nanoparticles were tested. Similar particle breakage was noticed. e, Load versus displacement curves of different tests. The breakage of particles and energy dissipation events are marked with back arrows. The total energy dissipation during compression is calculated from the integration of the force-displacement curves. Source data

Supplementary information

Supplementary Information

Supplementary Figs. 1–8 and discussion.

Reporting Summary

Supplementary Video 1

HAP nanoparticles at different tilt angles in TEM.

Supplementary Video 2 In situ compression of a HAP nanoparticle.

Source data

Source Data Fig. 3

Source data for Fig. 3h–j.

Source Data Fig. 5

Source data for Fig. 5j.

Source Data Fig. 6

Source data for Fig. 6e, f.

Source Data Extended Data Fig. 3

Source data for Extended Data Fig. 3a,b.

Source Data Extended Data Fig. 4

Source data for Extended Data Fig. 4e.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Huang, W., Shishehbor, M., Guarín-Zapata, N. et al. A natural impact-resistant bicontinuous composite nanoparticle coating. Nat. Mater. 19, 1236–1243 (2020). https://doi.org/10.1038/s41563-020-0768-7

Download citation

Search

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