Abstract
Natural surfaces that repel foreign matter are ubiquitous and crucial for living organisms. Despite remarkable liquid repellency driven by surface energy in many organisms, repelling tiny solid particles from surfaces is rare. The main challenge lies in the unfavourable scaling of inertia versus adhesion in the microscale and the inability of solids to release surface energy. Here we report a previously unexplored solid repellency on a honeybee’s comb: a catapult-like effect to immediately eject pollen after grooming dirty antennae for self-cleaning. Nanoindentation tests revealed the 38-μm-long comb features a stiffness gradient spanning nearly two orders of magnitude from ~25 MPa at the tip to ~645 MPa at the base. This significantly augments the elastic energy storage and accelerates the subsequent conversion into kinetic energy. The reinforcement in energy storage and conversion allows the particle’s otherwise weak inertia to outweigh its adhesion, thereby suppressing the unfavourable scaling effect and realizing solid repellency that is impossible in conventional uniform designs. We capitalize on this to build an elastomeric bioinspired stiffness-gradient catapult and demonstrate its generality and practicality. Our findings advance the fundamental understanding of natural catapult phenomena with the potential to develop bioinspired stiffness-gradient materials, catapult-based actuators and robotic cleaners.
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Data availability
Source data are provided with this paper.
Code availability
The custom-made code is publicly available at https://github.com/WinnJiang/Bee-code.
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Acknowledgements
We acknowledge financial support from the Research Grants Council of Hong Kong (C1006-20W, Z.W.; SRFS2223-1S01, Z.W.; 11215523, Z.W.), the Shenzhen Science and Technology Innovation Council (JCYJ20170413141208098, Z.W.), the Innovation Technology Fund (GHP/021/19SZ, Z.W.), the New Cornerstone Science Foundation through the XPLORER PRIZE (Z.W.), the Meituan Green Tech Award (Z.W.), the National Natural Science Foundation of China (52005075, Z.W.; 52075528, B.W.), and the Shenzhen Science and Technology Program (20220817165030002, J.W.).
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Z.W., J.W. and W.Z. conceived the research. W.Z., C.Z., H.Z. and X.Q. designed the experiments. W.Z., W.J. and C.Z. prepared the samples. W.Z., W.J., C.Z., W.X. and M.C. carried out the experiments. W.Z. and W.J. conducted the dynamics simulation. All authors analysed the data. W.Z., C.Z., Z.W., B.W. and J.W. wrote the paper.
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Extended data
Extended Data Fig. 1 Occurrence rate of comb cleaning behaviours.
a, Occurrence rate of two immediate behaviours after antennal grooming for honeybees, including comb cleaning and no comb cleaning behaviours. We observed 104 trials of antennal grooming from 10 living honeybee samples. We found that only 26 trials show immediate comb cleaning behaviour, while 78 trials show other subsequent behaviours such as flight, walking, or foraging. Therefore, the average occurrence rate of comb cleaning after antennal grooming for honeybees is 25%. b, Comparison of the occurrence rate of immediate comb cleaning immediately after antennal grooming for four different insects, including honeybees, southern green stink bugs, ants, and cockroaches. The occurrence rate for the honeybees is much lower than the other three insects, indicating that they may possess an unknown ability to keep their comb uncontaminated when grooming dirty antennae.
Extended Data Fig. 2 Scanning electron microscope (SEM) image of the surface of a honeybee’s comb that just performed antennal grooming in natural environments.
Most contaminants, including pollen and dusts, distribute on the middle-to-base part of the comb, leaving the middle-to-tip part almost uncontaminated.
Extended Data Fig. 3 Fraction and distribution of the residual particles of different diameter dp on the comb surface.
a, SEM image of the comb that just groomed the antennae covered with 1-30 μm silica particles. b, Plot of fraction versus \({d}_{{\rm{p}}}\) showing that most residual particles have sizes smaller than 5 μm. c, Plot of \({d}_{{\rm{p}}}\) versus normalized distance \(l/{l}_{0}\) showing that the sizes of particles gradually get larger from the tip to the base of the comb, indicating a location-dependent solid repellency performance. Here \(l/{l}_{0}=0\) denotes the tip and \(l/{l}_{0}=1\) denotes the base of the comb. Data are presented as mean ± s.d. (n = 3).
Extended Data Fig. 4 SEM image of the antennae of a honeybee.
The antennae consist of three parts: scape, pedicel, and flagellum. Note that only the flagellum part is cleaned during the antennal grooming process, and its average diameter is ~209 μm, 32 μm larger than that of the comb.
Extended Data Fig. 5 Measurement of the adhesive force.
a, Typical curves of pull-off adhesive forces on the comb surfaces using silica particles of 5, 10, 15, and 25 μm. The adhesive force can be calculated by the difference in magnitude between the lowest point and the baseline of each curve. It can be found that the adhesive force increases as the particle size gets larger. b, The influence of contact duration on the adhesive force. The adhesive forces for different contact durations are comparable with the maximum difference of 0.3%, indicating the ignorable influence of conduct duration on the adhesive force in the millisecond timescale. Data are presented as mean ± s.d. (n = 5).
Extended Data Fig. 6 Time-dependent acceleration and force analysis for a 10-μm particle adhered to the tip of the comb hair.
a, Comparison between the stiffness gradient comb hair of honeybees (\(\delta =3\)) and the uniform counterpart (\(\delta =0\)) in the deceleration phase. For \(\delta =0\), the acceleration a is relatively small, and the corresponding inertial force \({F}_{{\rm{i}}}\) of the adhered particle is insufficient to overcome \({F}_{{\rm{a}}}\). By contrast, for \(\delta =\)3, the magnitude of a sharply increases, as exemplified by the evident difference in the maximum reverse acceleration, enabling \({F}_{{\rm{i}}}-{F}_{{\rm{a}}}\) to exceed the level of 0 and triggering particle catapult. b, The dynamics of the uniform counterpart. The uniform beam exhibits 2nd order dynamics with time-varying accelerations.
Extended Data Fig. 7 Theoretical calculations.
a, Variation of normalized energy conversion duration with stiffness gradient under three different recovery rates. The good alignment between the three curves suggests that the normalized duration is independent of the recovery rate. b, Location-dependent maximum acceleration of the honeybee’s comb hair. The maximum a rapidly decreases with increasing normalized distance \(l/{l}_{0}\), suggesting that the solid repellency performance degrades from the tip to the base of the honeybee’s comb hair. c, Critical \({d}_{p}\) along the comb hair for three different stiffness gradient coefficients \(\delta\). It can be found that increasing \(\delta\) from 3 (honeybee’s case) to 4 would not give rise to notable enhancement in solid repellency performance relative to the uniform counterpart (\(\delta =0\)), especially for the part of \(l/{l}_{0}\). d, Variation of the contact force between the comb and antennae as a function of \(\delta\). For comparison, the magnitude of the contact force is normalized with respect to that for \(\delta =0\). The normalized contact force shows an exponential growth with increasing \(\delta\), resulting in a sharp increase when \(\delta\) increases from 3 to 4. The increased contact force may damage the antennal function during repeated grooming, which is unfavourable for honeybees.
Extended Data Fig. 8 Comparison of solid repellency performance between (a) the bioinspired SGC-based robot and (b) the control.
Upon sweeping and detaching surfaces covered with 25-μm particles, the SGC-based robot repels considerable amounts of particles adhered to its surface and keeps its surface clean. In contrast, the control fails to repel particles and its surface is heavily contaminated by particles. Scale bars, 10 mm.
Extended Data Fig. 9 Optical images of the self-cleaning solar power system after 12 consecutive cycles of contamination tests.
a, Optical images of surfaces of the SGC-based robot and the contaminated solar panel it cleaned. b, Optical images of surfaces of the control counterparts. In each cycle, we contaminated the solar panel with dust and subsequently actuated the cleaning robots to sweep the solar panel. There is no additional cleaning on the cleaning robots between cycles. Over 12 consecutive cycles, the surface of the SGC-based robot remains clean owing to its superior solid repellency ability and sustains a high cleaning capability to keep the solar panel clean. In striking contrast, the control with poor solid repellency ability is heavily contaminated by dust and unable to efficiently clean the solar panel surface, leaving behind a relatively dirty solar panel. Scale bars, 10 mm.
Extended Data Fig. 10 Optical images of the contact status between the plates and the solar panel surfaces from side view.
a, Optical images of the SGC-based robot at cycle 1 and cycle 12. b, Optical images of the control at cycle 1 and cycle 12. Scale bars, 10 mm.
Supplementary information
Supplementary Video 1
Natural antennal grooming behaviour of a honeybee when visiting flowers.
Supplementary Video 2
High-speed video of the solid repellency phenomenon in honeybee during its antennal grooming behaviour. The video was recorded at 1,000 f.p.s. and is shown at 30 f.p.s.
Supplementary Video 3
Application demonstration of the SGC-based robot.
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Zhang, W., Jiang, W., Zhang, C. et al. Honeybee comb-inspired stiffness gradient-amplified catapult for solid particle repellency. Nat. Nanotechnol. 19, 219–225 (2024). https://doi.org/10.1038/s41565-023-01524-x
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DOI: https://doi.org/10.1038/s41565-023-01524-x
