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A natural impact-resistant bicontinuous composite nanoparticle coating

Nature Materials volume 19, pages 1236–1243 (2020)Cite this article

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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.

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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.

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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.

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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

Authors and Affiliations

  1. Department of Chemical and Environmental Engineering, University of California, Riverside, CA, USA

    Wei Huang & David Kisailus

  2. Department of Materials Science and Engineering, University of California, Irvine, CA, USA

    Wei Huang & David Kisailus

  3. Lyles School of Civil Engineering, Purdue University, West Lafayette, IN, USA

    Mehdi Shishehbor, Nicolás Guarín-Zapata & Pablo Zavattieri

  4. Oxford Instruments Asylum Research, Goleta, CA, USA

    Nathan D. Kirchhofer & Jason Li

  5. Materials Science and Engineering Program, University of California, Riverside, CA, USA

    Luz Cruz, Taifeng Wang & David Kisailus

  6. Bruker, Minneapolis, MN, USA

    Sanjit Bhowmick, Douglas Stauffer & Praveena Manimunda

  7. Central Facility for Advanced Microscopy and Microanalysis, University of California, Riverside, CA, USA

    Krassimir N. Bozhilov

  8. Department of Integrative Biology, University of California, Berkeley, CA, USA

    Roy Caldwell

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  1. Wei Huang
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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.

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Correspondence to David Kisailus.

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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 (a–e) 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 (a–f) 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, c–f, 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 (c–i) were observed.

Source data

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

In situ compression tests of single HAP nanoparticles. a–d, 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.

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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

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