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Inspired by the dynamic wet adhesive systems in nature, various artificial adhesive surfaces have been developed but still face different challenges. Crucially, the theoretical mechanics of wet adhesives has never been sufficiently revealed. Here, we develop a novel adhesive mechanism for governing wet adhesion and investigate the biological models of honeybee arolium for reproducing the natural wet adhesive systems. Micro-nano structures of honeybee arolium and arolium-prints were observed by Cryogenic scanning electron microscopy (Cryo-SEM), and the air pockets were found in the contact interface notably. Subsequently, the adhesive models with a three-phase composite interface (including air pockets, liquid secretion, and hexagonal frames of arolium), were formed to analyze the wet adhesion of honeybee arolium. The results of theoretical calculations and experiments indicated an enhanced adhesive mechanism of the honeybee by liquid self-sucking effects and air-embolism effects. Under these effects, normal and shear adhesion can be adjusted by controlling the proportion of liquid secretion and air pockets in the contact zone. Notably, the air-embolism effects contribute to the optimal coupling of smaller normal adhesion with greater shear adhesion, which is beneficial for the high stride frequency of honeybees. These works can provide a fresh perspective on the development of bio-inspired wet adhesive surfaces.


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Development of wet adhesion of honeybee arolium incorporated polygonal structure with three-phase composite interfaces

Show Author's information Lulu LIANG1Jieliang ZHAO1( )Qun NIU1Li YU1Xiangbing WU1Wenzhong WANG1( )Shaoze YAN2Zhenglei YU3
School of Mechanical Engineering, Beijing Institute of Technology, Beijing 100081, China
Division of Intelligent and Biomechanical Systems, State Key Laboratory of Tribology, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, China
Key of Bionic Engineering, Ministry of Education, Jilin University, Changchun 130022, China

Abstract

Inspired by the dynamic wet adhesive systems in nature, various artificial adhesive surfaces have been developed but still face different challenges. Crucially, the theoretical mechanics of wet adhesives has never been sufficiently revealed. Here, we develop a novel adhesive mechanism for governing wet adhesion and investigate the biological models of honeybee arolium for reproducing the natural wet adhesive systems. Micro-nano structures of honeybee arolium and arolium-prints were observed by Cryogenic scanning electron microscopy (Cryo-SEM), and the air pockets were found in the contact interface notably. Subsequently, the adhesive models with a three-phase composite interface (including air pockets, liquid secretion, and hexagonal frames of arolium), were formed to analyze the wet adhesion of honeybee arolium. The results of theoretical calculations and experiments indicated an enhanced adhesive mechanism of the honeybee by liquid self-sucking effects and air-embolism effects. Under these effects, normal and shear adhesion can be adjusted by controlling the proportion of liquid secretion and air pockets in the contact zone. Notably, the air-embolism effects contribute to the optimal coupling of smaller normal adhesion with greater shear adhesion, which is beneficial for the high stride frequency of honeybees. These works can provide a fresh perspective on the development of bio-inspired wet adhesive surfaces.

Keywords: honeybee arolium, air pockets, wet adhesion, a three-phase interface, self-sucking effects, air-embolism effects

References(54)

[1]
Baik S, Kim D W, Park Y, Lee T, Ho Bhang S, Pang C. A wet-tolerant adhesive patch inspired by protuberances in suction cups of octopi. Nature 546(7658): 396–400 (2017)
[2]
Xue L, Sanz B, Luo A, Turner K T, Wang X, Tan D, Zhang R, Du H, Steinhart M, Mijangos C, Guttmann M, Kappl M, Del Campo A. Hybrid surface patterns mimicking the design of the adhesive toe pad of tree frog. ACS Nano 11(10): 9711–9719 (2017)
[3]
Wang X, Yang B, Tan D, Li Q, Song B, Wu Z, Del Campo A, Kappl M, Wang Z, Gorb S N, Liu S, Xue L. Bioinspired footed soft robot with unidirectional all-terrain mobility. Mater Today 35(42–49) (2020)
[4]
Yang Y, Xu T, Bei H P, Zhao Y, Zhao X. Sculpting bio-inspired surface textures: An adhesive janus periosteum. Adv Funct Mater 31(37): 2104636 (2021)
[5]
Hwang G W, Lee H J, Kim D W, Yang T H, Pang C. Soft microdenticles on artificial octopus sucker enable extraordinary adaptability and wet adhesion on diverse nonflat surfaces. Adv Sci 9(31): 2202978 (2022)
[6]
Lee J, Lee B S, Baik S, Kim D, Park N J, Lee J W, Bong S K, Lee S H, Kim S N, Song J H, et al. Ultra-intimate hydrogel hybrid skin patch with asymmetric elastomeric spatula-like cylinders. Chem Eng J 444: 136581 (2022)
[7]
Baik S, Lee J, Jeon E J, Park B Y, Kim D W, Song J H, Lee H J, Han S Y, Cho S W, Pang C. Diving beetle-like miniaturized plungers with reversible, rapid biofluid capturing for machine learning-based care of skin disease. Sci Adv 7(25): 5695 (2021)
[8]
Xue B, Gu J, Li L, Yu W, Yin S, Qin M, Jiang Q, Wang W, Cao Y. Hydrogel tapes for fault-tolerant strong wet adhesion. Nat Commun 12(1): 7156 (2021)
[9]
Baik S, Hwang G W, Jang S, Jeong S, Kim K H, Yang T, Pang C. Bioinspired microsphere-embedded adhesive architectures for an electrothermally actuating transport device of dry/wet pliable surfaces. ACS Appl Mater Inter 13(5): 6930–6940 (2021)
[10]
Choi D S, Bae J W, Lee S H, Song J H, Choi S, Pang C, Kim S Y. Emotion-interactive empathetic transparent skin cushion with tailored frequency-dependent hydrogel–plasticized nonionic polyvinyl chloride interconnections. Chem Eng J 442:136142 (2022)
[11]
Min H, Baik S, Lee J, Song J H, Kim K H, Kim M S, Pang C. Enhanced biocompatibility and multidirectional wet adhesion of insect-like synergistic wrinkled pillars with microcavities. Chem Eng J 429: 132467 (2022)
[12]
Lee H, Um D, Lee Y, Lim S, Kim H, Ko H. Octopus-inspired smart adhesive pads for transfer printing of semiconducting nanomembranes. Adv Mater 28(34): 7457–7465 (2016)
[13]
Liu Q, Meng F, Wang X, Yang B, Tan D, Li Q, Shi Z, Shi K, Chen W, Liu S, Lei Y, Xue L. Tree frog-inspired micropillar arrays with nanopits on the surface for enhanced adhesion under wet conditions. ACS Appl Mater Inter 12(16): 19116–19122 (2020)
[14]
Zhao Y, Wu Y, Wang L, Zhang M, Chen X, Liu M, Fan J, Liu J, Zhou F, Wang Z. Bio-inspired reversible underwater adhesive. Nat Commun 8(1): 2218 (2017)
[15]
Federle W, Labonte D. Dynamic biological adhesion: Mechanisms for controlling attachment during locomotion. Phil Trans R Soc B 374(1784): 20190199 (2019).
[16]
Shin D, Choi W T, Lin H, Qu Z, Breedveld V, Meredith J C. Humidity-tolerant rate-dependent capillary viscous adhesion of bee-collected pollen fluids. Nat Commun 10(1): 1379 (2019)
[17]
Cai S, Bhushan B. Meniscus and viscous forces during separation of hydrophilic and hydrophobic smooth/rough surfaces with symmetric and asymmetric contact angles. Philos Trans A Math Phys Eng Sci 366(1870): 1627–1647 (2008)
[18]
Gu Z, Li S, Zhang F, Wang S. Understanding surface adhesion in nature: A peeling model. Adv Sci 3(7): 1500327 (2016)
[19]
Chen Y, Meng J, Gu Z, Wan X, Jiang L, Wang S. Bioinspired multiscale wet adhesive surfaces: Structures and controlled adhesion. Adv Funct Mater 30(5): 1905287 (2019)
[20]
Labonte D, Federle W. Rate-dependence of 'wet' biological adhesives and the function of the pad secretion in insects. Soft Matter 11(44): 8661–8673 (2015)
[21]
Gorb S N. Smooth attachment devices in insects: Functional morphology and biomechanics. Adv in Insect Physiol 34: 81–115 (2007)
[22]
Gilet T, Heepe L, Lambert P, Compère P, Gorb S N. Liquid secretion and setal compliance: The beetle's winning combination for a robust and reversible adhesion. Curr Opin Insect Sci 30: 19–25 (2018)
[23]
Stork N E, Experimental analysis of adhesion of chrysolina polita (Chrysomelidae: Coleoptera) on a variety of surfaces. J Exp Bio 88(1): 91–108 (1980)
[24]
Gernay S, Federle W, Lambert P, Gilet T. Elasto-capillarity in insect fibrillar adhesion. J R Soc Interface 13(121): 20160371 (2016)
[25]
Gorb S N. The design of the fly adhesive pad: Distal tenent setae are adapted to the delivery of an adhesive secretion. Proc R Soc B 265(1398): 747–752 (1998)
[26]
Dirks J H, Federle W. Fluid-based adhesion in insects–principles and challenges. Soft Matter 7(23): 11047–11053 (2011)
[27]
Scholz I, Baumgartner W, Federle W. Micromechanics of smooth adhesive organs in stick insects: pads are mechanically anisotropic and softer towards the adhesive surface. J Comp Physiol A 194(4): 373–384 (2008)
[28]
Labonte D, Struecker M Y, Birn-Jeffery A V, Federle W. Shear-sensitive adhesion enables size-independent adhesive performance in stick insects. Proc R Soc B 286(1913): 20191327(2019)
[29]
Dirks J, Federle W. Mechanisms of fluid production in smooth adhesive pads of insects. J R Soc Interface 8(60): 952–960 (2011)
[30]
Peng Z, Wang C, Chen S. The microstructure morphology on ant footpads and its effect on ant adhesion. Acta Mechanica 227(7): 2025–2037 (2016)
[31]
Federle W, Riehle M, Curtis A S G, Full R J. An integrative study of insect adhesion: mechanics and wet adhesion of pretarsal pads in ants. Inte Comp Bio 42(6): 1100–1106 (2002)
[32]
Persson B N J. Wet adhesion with application to tree frog adhesive toe pads and tires. J Phys Condens Matter 19(37): 376110 (2007)
[33]
Kappl M, Kaveh F, Barnes W J P. Nanoscale friction and adhesion of tree frog toe pads. Bioinspiration and Biomimetics 11(3): 035003(2016)
[34]
Zhang L, Chen H, Guo Y, Wang Y, Jiang Y, Zhang D, Ma L, Luo J, Jiang L. Micro-nano hierarchical structure enhanced strong wet friction surface inspired by tree frogs. Adv Sci 7(20): 2001125 (2020)
[35]
Li M, Shi L, Wang X. Physical mechanisms behind the wet adhesion: From amphibian toe-pad to biomimetics. Colloids Surf B 199: 111531 (2021)
[36]
Xiao Z, Zhao Q, Niu Y, Zhao D. Adhesion advances: From nanomaterials to biomimetic adhesion and applications. Soft Matter 18(18): 3447–3464 (2022)
[37]
Barnes W J P, Baum M, Peisker H, Gorb S N. Comparative Cryo-SEM and AFM studies of hylid and rhacophorid tree frog toe pads. J Morphol 274(12): 1384–1396 (2013)
[38]
Wang M, Chen W, Zhao J, Yu L, Yan S. Hairy-layer friction reduction mechanism in the honeybee abdomen. ACS Appl Mater Inter 13(21): 24524–24531 (2021)
[39]
Sample C S, Xu A K, Swartz S M, Gibson L J. Nanomechanical properties of wing membrane layers in the house cricket (Acheta domesticus Linnaeus). J Insect Physiol 74: 10–15 (2015)
[40]
Bennemann M, Backhaus S, Scholz I, Park D, Mayer J, Baumgartner W. Determination of the Young's modulus of the epicuticle of the smooth adhesive organs of carausius morosus using tensile testing. J Exp Biol 217(20): 3677–3687(2014)
[41]
Federle W, Brainerd E L, McMahon T A, Holldobler B. Biomechanics of the movable pretarsal adhesive organ in ants and bees. Proc Natl Acad Sci U S A 98(11): 6215–6220 (2001)
[42]
Kendall K. Thin-film peeling-the elastic term. J Phys D: Appl Phys 8(13): 1449–1452 (1975)
[43]
Thomas T, Tiwari G. Crushing behavior of honeycomb structure: A review. Int J Crashworthiness 24(5): 555–579 (2019)
[44]
Dirks J, Clemente C J, Federle W. Insect tricks: Two-phasic foot pad secretion prevents slipping. J R Soc Interface 7(45): 587–593 (2010)
[45]
Barr V A, Bunnell S C. Interference reflection microscopy. Current Protocols in Cell Biology 45(1): 4–23 (2009)
[46]
Liu B, Sheng G, Lim S T. Meniscus force modeling and study on the fluctuation of stiction/friction force in CSS test process. IEEE Trans Magn 33(5): 3121–3123 (1997)
[47]
Timoshenko S, Woinowsky-Krieger S. Theory of Plates and Shells. New York (USA): McGraw-hill, 1959.
[48]
Gennes P, Brochard-Wyart F, Quéré D, Reisinger A, Widom B. Capillarity and Wetting Phenomena: Bubbles, pearls, waves. New York (USA): Springer, 2004.
DOI
[49]
Greenwood J A, Williamson J B P. Contact of nominally flat surfaces. Proc R Soc Lond A 295 (1442): 300–319 (1966)
[50]
De Souza E J, Brinkmann M, Mohrdieck C, Crosby A, Arzt E. Capillary forces between chemically different substrates. Langmuir 24(18): 10161–10168 (2008)
[51]
Lorenz B, Oh Y R, Nam S K, Jeon S H, Persson B N J. Rubber friction on road surfaces: Experiment and theory for low sliding speeds. J Chem Phys 142(19): 194701 (2015)
[52]
Xue L, Kovalev A, Eichler-Volf A, Steinhart M, Gorb S N. Humidity-enhanced wet adhesion on insect-inspired fibrillar adhesive pads. Nat Commun 6(1): 6621 (2015)
[53]
Chen Y, Zhao H, Mao J, Chirarattananon P, Helbling E F, Hyun N P, Clarke D R, Wood R J. Controlled flight of a microrobot powered by soft artificial muscles. Nature 575(7782): 324–329 (2019)
[54]
Bao Y W, Wang W, Zhou Y C. Investigation of the relationship between elastic modulus and hardness based on depth-sensing indentation measurements. Acta Mater 52(18): 5397–5404 (2004)
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Received: 31 July 2022
Revised: 25 November 2022
Accepted: 23 January 2023
Published: 29 November 2023
Issue date: February 2024

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© The author(s) 2023.

Acknowledgements

This work was supported by the National Key R&D Program of China (2021YFB3400200), the Beijing Natural Science Foundation (3212012), the National Natural Science Foundation of China (52075038), the Opening Project of the Key Laboratory of Bionic Engineering (Ministry of Education), Jilin University (KF20200001), and the Opening Project of State Key Laboratory of Tribology, Tsinghua University (SKLTKF20B06). The authors thank Donglin Li for providing the picture of a honeybee adhering to the flower petals during pollen collection.

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