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Toughening mechanisms of the elytra of the diabolical ironclad beetle

A Publisher Correction to this article was published on 19 January 2021

This article has been updated

Abstract

Joining dissimilar materials such as plastics and metals in engineered structures remains a challenge1. Mechanical fastening, conventional welding and adhesive bonding are examples of techniques currently used for this purpose, but each of these methods presents its own set of problems2 such as formation of stress concentrators or degradation under environmental exposure, reducing strength and causing premature failure. In the biological tissues of numerous animal and plant species, efficient strategies have evolved to synthesize, construct and integrate composites that have exceptional mechanical properties3. One impressive example is found in the exoskeletal forewings (elytra) of the diabolical ironclad beetle, Phloeodes diabolicus. Lacking the ability to fly away from predators, this desert insect has extremely impact-resistant and crush-resistant elytra, produced by complex and graded interfaces. Here, using advanced microscopy, spectroscopy and in situ mechanical testing, we identify multiscale architectural designs within the exoskeleton of this beetle, and examine the resulting mechanical response and toughening mechanisms. We highlight a series of interdigitated sutures, the ellipsoidal geometry and laminated microstructure of which provide mechanical interlocking and toughening at critical strains, while avoiding catastrophic failure. These observations could be applied in developing tough, impact- and crush-resistant materials for joining dissimilar materials. We demonstrate this by creating interlocking sutures from biomimetic composites that show a considerable increase in toughness compared with a frequently used engineering joint.

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Fig. 1: Mechanical properties of terrestrial beetles and architectural features of DIB (P. diabolicus).
Fig. 2: Role of regio-specific and graded lateral supports in the compression resistance of P. diabolicus.
Fig. 3: Role of suture blade geometry on mechanical performance.
Fig. 4: Role of microstructure in toughening of the medial suture.

Data availability

The data that support the findings of this study are available from the corresponding author on reasonable request. Source data are provided with this paper.

Change history

  • 19 January 2021

    A Correction to this paper has been published: https://doi.org/10.1038/s41586-020-03106-6

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Acknowledgements

This research was supported by grants from AFOSR, Multi-University Research Initiative, award FA9550-15-1-0009 (D.K.) Electron microscopy was conducted at the Central Facility for Advanced Microscopy and Microanalysis (CFAMM). D.K. thanks the Army Research Office DURIP grant (W911NF-16-1-0208) for the MIRA SEM. P.Z. thanks the AFOSR DURIP grant (FA2386-12-1-3020) for the 3D printer. A.A. and D.K. thank the Institute of Global Innovation Research (GIR) at TUAT for their support. This research used resources of the Advanced Light Source, which is a DOE Office of Science User Facility under contract no. DE-AC02-05CH11231. We also acknowledge M. Cooper for helping with CAD drawings of laminated blades.

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Authors

Contributions

J.R. conducted mechanical and ultrastructural characterization of the beetle cuticles. J.R. and D.K. analysed ultrastructural and mechanical characterization results. J.R. and M.S.H. prepared 3D-printed samples. M.S.H., D.R. and P.Z. carried out the FE simulations and assisted with data analysis. J.R., S.M. and A.A. performed chemical analysis of the beetle cuticles. D.Y.P. and H.S.B. provided assistance in acquiring CT scans. D.V. assisted in the fabrication of the laminated composite blades. D.K. planned and coordinated project and experimental tasks. All authors contributed to the writing of the manuscript.

Corresponding author

Correspondence to David Kisailus.

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The authors declare no competing interests.

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Peer review information Nature thanks Po-Yu Chen, Patrick Fairclough and Richard Johnston for their contribution to the peer review of this work.

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

Extended data figures and tables

Extended Data Fig. 1 Compression results for beetles tested.

a, Force versus displacement curves for all samples tested in compression, N = 5. Inset, image of compression test apparatus, with recently deceased sample mounted between two parallel steel plates. Scale bar, 5 mm. b, False-coloured SEM micrograph of fractured cross-section of the elytra, highlighting leaf-like setae (Se, green), epicuticle (red), exocuticle (Ex, yellow), endocuticle (En, blue), trabecula (Tr, orange) and haemolymph space (HS, violet). c, SEM micrograph of fractured exocuticle (yellow box in a), showing through-ply thickness fibres. d, SEM micrograph of endocuticle (purple box in a), revealing pseudo-helicoidal fibre orientation. e, Micro-CT reconstruction of elytra revealing internal pore canal network that leads to internal network of haemolymph space (highlighted in purple). Source data

Extended Data Fig. 2 Indentation analysis of the endocuticle of P. diabolicus.

a, Cross-section of P. diabolicus highlighting the exo- and endocuticle of the elytra. b, High-resolution surface map of exo- and endocuticle obtained with a Berkovich tip, indicating the reduced elastic modulus and hardness results from the elytra. c, d, Plots showing the variation between the reduced elastic modulus (c) and hardness (d) of the exo- and endocuticle.

Extended Data Fig. 3 Variations in macro- and microstructures in desert beetles and a flying beetle.

au, Column 1: overview of insect; column 2: elytra of organism; column 3: cross-sections (scale bars, 1 mm); column 4: suture that binds the two elytra (scale bars, 100 μm); column 5: lateral support interfacing elytra to the ventral cuticle (scale bars, 100 μm). Rows (top to bottom): ae, P. diabolicus, fj, A. verrucosus, ko, C. muricata, pt, E. grandicollis, ux, T. dichotomus (scale bars in columns 1 and 2, 5 mm). Source data

Extended Data Fig. 4 FE models of elytra under compression.

a, Model of the elytra and abdomen. b, Initial displacement of the elytra showing principal stresses at contact location. c, Increased displacement of elytra showing the distribution of principal stresses. dh, Cross sections of c highlight principal stresses at first lateral support (d), second lateral support (e, f), third lateral support (g) and repetition of second support at the posterior of the abdomen to prevent collapse of the elytra (h). i, FE model of cross-section under compression. j, FE model of suture region, indicating the dominance of tensile forces while under load. Applied compressive displacement of 0.5 mm.

Extended Data Fig. 5 Frictional microtrichia located at the interfaces between the elytra and ventral cuticle.

a, CT scans, highlighting three distinct internal regions. b, c, CT scan cross-section of the second support (b), with magnification (c) indicating the interface between the elytra and ventral cuticle. dg, SEM micrograph (d) of the elytra interface, indicating microtrichia (e) that provide frictional contact between d and f, the ventral cuticle with its surface (g) also coated with microtrichia. Source data

Extended Data Fig. 6 Mechanical response on increasing the number of blades.

a, Parametric tensile samples, inspired by the natural system, with one to five blades. b, Comparison between normalized peak load, stiffness and toughness from 3D-printed tensile experiments and simulations. c, FE tensile simulations of sutural quantity variation, showing stress distribution based on number of elements. d, FE models showing maximum strain in blades subjected to tensile loads.

Extended Data Fig. 7 Mechanical response of suture with increasing number of blades but constant contact area between elements.

a, Printed samples produced for mechanical testing. b, FE models showing maximum strain in blades subjected to tensile loads. c, Representative load versus displacement curves for tested samples.

Extended Data Fig. 8 Tensile and compressive stresses as a function of number of blades.

ae, First row: maximum principal stress contours for one (a), two (b), three (c), four (d) and five (e) blades at the point of maximum load. Second row: highlighted stress within the central blade for each set of experiments in the top row. Third row: distribution of the principal directions associated with the maximum principal stress. fj, First row: minimum principal stress contours for one (f), two (g), three (h), four (i) and five (j) blades at the point of maximum load. Second row: highlighted stress within the central blade for each set of experiments in the row above. Third row: distribution of the principal directions associated with the minimum principal stress.

Extended Data Fig. 9 Additive manufactured laminated blades.

a, Three different jigsaw geometries developed by varying θ to 15°, 25° and 50°. b, Multi-material additively manufactured jigsaw blades containing 1.2-mm-thick VeroWhite layers bonded together with 0.6-mm-thick TangoBlack Plus. Inset shows the architecture inside each blade. c, Tensile tests of 3D-printed specimens with DIC, indicating localized strain that leads to failure mechanisms including pull-out, delamination and fracture.

Extended Data Fig. 10 Tensile test of composite blades and engineering fasteners.

ad, Images of sample (left); DIC of strained sample (centre); and DIC of fractured sample (right). a, Composite blade composed of circumferentially laminated pre-impregnated carbon fibre with a core made of chopped graphite fibre plus epoxy. b, Composite blade composed of unoriented chopped-strand graphite fibres in an epoxy matrix. c, Epoxy blade. d, Titanium Hi-Lok fastener binding a plane-weave carbon fibre epoxy panel to a 6061-aluminium plate. e, Stress versus displacement curves indicating the tensile response of the laminated blades (from a) and engineering fastener (from d). f, Energy absorbed by each composite before failure. Source data

Supplementary information

Supplementary Information

This file contains information about: 1. The role of structural features, composition (including protein profiles) and surface topography on mechanical properties of elytra; 2. Discussion of nanoindentation maps; 3. Mechanics of lateral supports using FE models; 4. Microstructural effects on the mechanics of the medial suture; 5. References.

Video 1

Medial suture of P. diabolicus connecting the two elytron running along the length of the abdomen.

Video 2

Variations of lateral interfaces connecting the elytra to the ventral cuticle in P. diabolicus.

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Rivera, J., Hosseini, M.S., Restrepo, D. et al. Toughening mechanisms of the elytra of the diabolical ironclad beetle. Nature 586, 543–548 (2020). https://doi.org/10.1038/s41586-020-2813-8

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