Journal of Materials Science

, Volume 55, Issue 10, pp 4524–4537 | Cite as

Asian ladybird folding and unfolding of hind wing: biomechanical properties of resilin in affecting the tensile strength of the folding area

  • Zelai Song
  • Yongwei Yan
  • Jin Tong
  • Jiyu SunEmail author
Polymers & biopolymers


The deployable hind wings of Coleoptera are a highly specialized motive system that can fold and unfold in a unique way. Resilin in the wing membrane of Asian ladybird beetle (Harmonia axyridis) hind wings plays an active role during folding and unfolding of the wing. This study investigates the tensile properties of the hind wing and the distribution of resilin through the hind wing in an adult H. axyridis (Coleoptera: Coccinellidae) and how the resilin in the membrane of the hind wing affects its mechanical characteristics. The cross sections of veins of the hind wing are investigated by inverted fluorescence microscopy. Based on those results, two three-dimensional finite element models of the hind wing with/without resilin are established. The displacements, when subjected to pressure on the ventral side, are analyzed when the membrane wings are filled with/without resilin. The resilin in the hind wing is effectively for changing the flight performance such as the condition of stress and deformation. The results in this paper reveal the multiple functions of the resilin in the hind wings and have important implications for the design of biomimetic deployable micro-air vehicles.



This work was supported by the National Natural Science Foundation of China (Grant Number 31672348), Joint Fund for Pre-research of Equipment and Weapons Industry (Grant Number 6141B012833), China-EU H2020 FabSurfWAR Project (Grant Number 644971), and 111 Project (B16020) of China.

Author contributions

ZLS and JYS designed the study; ZLS and YWY coordinated the study; ZLS, JT, and JYS conducted the research and analyzed the data; ZLS wrote the manuscript; JYS reviewed the manuscript, discussed the results, and gave the final approval for publication; Mr. Zhiqiang Zhang, ShenYang YuanJie Optics Technology Co., Ltd., offered technology supporting.

Compliance with ethical standards

Conflict of interest

The authors declare there are no conflicts of interest to disclose.

Ethical standard

This work complies with ethical guidelines at Jilin University.


  1. 1.
    Geisler T (2016) Observations and measurements of wing parameters of the selected beetle species and the design of a mechanism structure implementing a complex wing movement. Int J Appl Mech Eng 21:837–847. CrossRefGoogle Scholar
  2. 2.
    Takizawa K, Tezduyar TE, Buscher A (2015) Space–time computational analysis of MAV flapping-wing aerodynamics with wing clapping. Comput Mech 55:1131–1141. CrossRefGoogle Scholar
  3. 3.
    Phan HV, Au TKL, Park HC (2016) Clap-and-fling mechanism in a hovering insect-like two-winged flapping-wing micro air vehicle. R Soc Open Sci 3:160746. CrossRefGoogle Scholar
  4. 4.
    Phan HV, Kang T, Park HC (2017) Design and stable flight of a 21 g insect-like tailless flapping wing micro air vehicle with angular rates feedback control. Bioinspir Biomim 12:036006. CrossRefGoogle Scholar
  5. 5.
    Yan X, Qi M, Lin L (2015) Self-lifting artificial insect wings via electrostatic flapping actuators. In: 2015 28th IEEE international conference on micro electro mechanical systems (MEMS). IEEE, pp 22–25.
  6. 6.
    Nguyen Q-V, Chan WL, Debiasi M (2016) Hybrid design and performance tests of a hovering insect-inspired flapping-wing micro aerial vehicle. J Bionic Eng 13:235–248. CrossRefGoogle Scholar
  7. 7.
    Van Truong T, Nguyen Q-V, Lee H (2017) Bio-inspired flexible flapping wings with elastic deformation. Aerospace 4:37. CrossRefGoogle Scholar
  8. 8.
    Truong QT, Argyoganendro BW, Park HC (2014) Design and demonstration of insect mimicking foldable artificial wing using four-bar linkage systems. J Bionic Eng 11:449–458. CrossRefGoogle Scholar
  9. 9.
    Muhammad A, Park HC, Hwang DY et al (2009) Mimicking unfolding motion of a beetle hind wing. Chin Sci Bull 54:2416–2424. CrossRefGoogle Scholar
  10. 10.
    Jitsukawa T, Adachi H, Abe T et al (2017) Bio-inspired wing-folding mechanism of micro air vehicle (MAV). Artif Life Robot 22:203–208. CrossRefGoogle Scholar
  11. 11.
    Maes S, Massart X, Grégoire JC, De Clercq P (2014) Dispersal potential of native and exotic predatory ladybirds as measured by a computer-monitored flight mill. Biocontrol 59:415–425. CrossRefGoogle Scholar
  12. 12.
    Miller LA, Peskin CS (2009) Flexible clap and fling in tiny insect flight. J Exp Biol 212:3076–3090. CrossRefGoogle Scholar
  13. 13.
    Haas F, Beutel RG (2001) Wing folding and the functional morphology of the wing base in Coleoptera. Zoology 104:123–141. CrossRefGoogle Scholar
  14. 14.
    Saito K, Nomura S, Yamamoto S et al (2017) Investigation of hindwing folding in ladybird beetles by artificial elytron transplantation and microcomputed tomography. Proc Natl Acad Sci 114:5624–5628. CrossRefGoogle Scholar
  15. 15.
    Kwok K, Pellegrino S (2013) Folding, stowage, and deployment of viscoelastic tape springs. AIAA J 51:1908–1918. CrossRefGoogle Scholar
  16. 16.
    Schieber G, Born L, Bergmann P et al (2017) Hindwings of insects as concept generator for hingeless foldable shading systems. Bioinspir Biomim 13:016012. CrossRefGoogle Scholar
  17. 17.
    Lawrence JF (1993) Evolution of the hind wing in coleoptera. Can Entomol 125:181–258. CrossRefGoogle Scholar
  18. 18.
    Ha NS, Truong QT, Goo NS, Park HC (2013) Biomechanical properties of insect wings: the stress stiffening effects on the asymmetric bending of the Allomyrina dichotoma beetle’s hind wing. PLoS ONE. CrossRefGoogle Scholar
  19. 19.
    Saito K, Tachi T, Niiyama R, Kawahara Y (2017) Design of a beetle inspired deployable wing. In: 41st mechanisms and robotics conference. ASME, vol 5B(4), pp 1–6.
  20. 20.
    Sun J, Liu C, Bhushan B et al (2018) Effect of microtrichia on the interlocking mechanism in the Asian ladybeetle, Harmonia axyridis (Coleoptera: Coccinellidae). Beilstein J Nanotechnol 9:812–823. CrossRefGoogle Scholar
  21. 21.
    Hedrick TL, Combes SA, Miller LA (2015) Recent developments in the study of insect flight. Can J Zool 93:925–943. CrossRefGoogle Scholar
  22. 22.
    Combes SA (2010) Materials, structure, and dynamics of insect wings as bioinspiration for MAVs. In: Blockley R, Shyy W (eds) Encyclopedia of aerospace engineering. Wiley, Chichester, pp 1–10. CrossRefGoogle Scholar
  23. 23.
    Fedorenko DN (2015) Transverse folding and evolution of the hind wings in beetles (Insecta, Coleoptera). Biol Bull Rev 5:71–84. CrossRefGoogle Scholar
  24. 24.
    Saito K, Yamamoto S, Maruyama M, Okabe Y (2014) Asymmetric hindwing foldings in rove beetles. Proc Natl Acad Sci 111:16349–16352. CrossRefGoogle Scholar
  25. 25.
    Haas F (2006) Evidence from folding and functional lines of wings on inter-ordinal relationships in Pterygota. Arthropod Syst Phylogeny 64:149–158Google Scholar
  26. 26.
    Haas F, Gorb S, Blickhan R (2000) The function of resilin in beetle wings. Proc R Soc Lond Ser B Biol Sci 267:1375–1381. CrossRefGoogle Scholar
  27. 27.
    Rajabi H, Shafiei A, Darvizeh A, Gorb SN (2016) Resilin microjoints: a smart design strategy to avoid failure in dragonfly wings. Sci Rep 6:39039. CrossRefGoogle Scholar
  28. 28.
    Burrows M (2016) Development and deposition of resilin in energy stores for locust jumping. J Exp Biol 219:2449–2457. CrossRefGoogle Scholar
  29. 29.
    Su RS, Kim Y, Liu JC (2014) Resilin: protein-based elastomeric biomaterials. Acta Biomater 10:1601–1611. CrossRefGoogle Scholar
  30. 30.
    Haas F, Gorb S, Wootton R (2000) Elastic joints in dermapteran hind wings: materials and wing folding. Arthropod Struct Dev 29:137–146. CrossRefGoogle Scholar
  31. 31.
    Li L, Guo C, Li X et al (2017) Microstructure and mechanical properties of rostrum in Cyrtotrachelus longimanus (Coleoptera: Curculionidae). Anim Cells Syst (Seoul) 21:199–206. CrossRefGoogle Scholar
  32. 32.
    Andersen SO, Weis-Fogh T (1964) Resilin. A rubberlike protein in arthropod cuticle. In: Beament JWL, Treherne JE, Wigglesworth VB (eds) Advances in insect physiology. Academic Press, London, pp 1–65. CrossRefGoogle Scholar
  33. 33.
    Rajabi H, Ghoroubi N, Stamm K et al (2017) Dragonfly wing nodus: a one-way hinge contributing to the asymmetric wing deformation. Acta Biomater 60:330–338. CrossRefGoogle Scholar
  34. 34.
    Mamat-Noorhidayah, Yazawa K, Numata K, Norma-Rashid Y (2018) Morphological and mechanical properties of flexible resilin joints on damselfly wings (Rhinocypha spp.). PLoS One 13:e0193147. CrossRefGoogle Scholar
  35. 35.
    Manuscript A (2012) Recombinant exon-encoded resilins for elastomeric biomaterials. Biomaterials 32:9231–9243. CrossRefGoogle Scholar
  36. 36.
    Appel E, Heepe L, Lin CP, Gorb SN (2015) Ultrastructure of dragonfly wing veins: composite structure of fibrous material supplemented by resilin. J Anat 227:561–582. CrossRefGoogle Scholar
  37. 37.
    Sun J, Song Z, Pan C, Liu Z (2018) Analysis of light-mass and high-strength veins of hind wing from Asian Ladybird beetle. In: 2018 IEEE international conference on manipulation, manufacturing and measurement on the nanoscale (3M-NANO). IEEE, pp 142–145.
  38. 38.
    Neff D, Frazier SF, Quimby L et al (2000) Identification of resilin in the leg of cockroach, Periplaneta americana: confirmation by a simple method using pH dependence of UV fluorescence. Arthropod Struct Dev 29:75–83. CrossRefGoogle Scholar
  39. 39.
    Kreuz P, Arnold W, Kesel AB (2001) Acoustic microscopic analysis of the biological structure of insect wing membranes with emphasis on their waxy surface. Ann Biomed Eng 29:1054–1058. CrossRefGoogle Scholar
  40. 40.
    Peisker H, Michels J, Gorb SN (2013) Evidence for a material gradient in the adhesive tarsal setae of the ladybird beetle Coccinella septempunctata. Nat Commun 4:1607–1608. CrossRefGoogle Scholar
  41. 41.
    Hou D, Zhong Z, Yin Y et al (2017) The role of soft vein joints in dragonfly flight. J Bionic Eng 14:738–745. CrossRefGoogle Scholar
  42. 42.
    Saha R, Nix WD (2002) Effects of the substrate on the determination of thin film mechanical properties by nanoindentation. Acta Mater 50:23–38. CrossRefGoogle Scholar
  43. 43.
    Bell TJ, Field JS, Swain MV (1992) Elastic–plastic characterization of thin films with spherical indentation. Thin Solid Films 220:289–294. CrossRefGoogle Scholar
  44. 44.
    Betts CR (2009) The comparative morphology of the wings and axillae of selected Heteroptera. J Zool 1:255–282. CrossRefGoogle Scholar
  45. 45.
    Haas F, Wootton RJ (1996) Two basic mechanisms in insect wing folding. Proc R Soc Lond Ser B Biol Sci 263:1651–1658. CrossRefGoogle Scholar
  46. 46.
    Haas F (2000) Wing folding in insects: a natural, deployable structure.
  47. 47.
    Forbes WTM (1926) The wing folding patterns of the Coleoptera. J N Y Entomol Soc 34:91–139. CrossRefGoogle Scholar
  48. 48.
    Wootton RJ, Herbert RC, Young PG, Evans KE (2003) Approaches to the structural modelling of insect wings. Philos Trans R Soc B Biol Sci 358:1577–1587. CrossRefGoogle Scholar
  49. 49.
    Michels J, Gorb SN (2012) Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy. J Microsc 245:1–16. CrossRefGoogle Scholar
  50. 50.
    Jongerius SR, Lentink D (2010) Structural analysis of a dragonfly wing. Exp Mech 50:1323–1334. CrossRefGoogle Scholar
  51. 51.
    Kantor Y, Kardar M, Nelson DR (1987) Tethered surfaces: statics and dynamics. Phys Rev A 35:3056–3071. CrossRefGoogle Scholar
  52. 52.
    Meresman Y, Ribak G (2017) Allometry of wing twist and camber in a flower chafer during free flight: how do wing deformations scale with body size? R Soc Open Sci. CrossRefGoogle Scholar
  53. 53.
    Herbert RC, Young PG, Smith CW et al (2000) The hind wing of the desert locust (Schistocerca gregaria Forskål) II. Mechanical properties and functioning of the membrane C. J Exp Biol 203:2945–2955Google Scholar
  54. 54.
    Rothschild M, Von Euw J, Reichstein T (1972) Aristolochic acids stored by Zerynthia polyxena (Lepidoptera). Insect Biochem 2:334–343. CrossRefGoogle Scholar
  55. 55.
    Chimakurthi SK, Cesnik CES, Stanford BK (2011) Flapping-wing structural dynamics formulation based on a corotational shell finite element. AIAA J 49:128–142. CrossRefGoogle Scholar
  56. 56.
    Faber JA, Arrieta AF, Studart AR (2018) Bioinspired spring origami. Science 359:1386–1391. CrossRefGoogle Scholar
  57. 57.
    Weis-Fogh T (1961) Molecular interpretation of the elasticity of resilin, a rubber-like protein. J Mol Biol 3:648–667. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Key Laboratory of Bionic Engineering (Ministry of Education, China)Jilin UniversityChangchunPeople’s Republic of China

Personalised recommendations