Skip to main content

Advertisement

SpringerLink
Log in

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

  • Polymers & biopolymers
  • Published:
Journal of Materials Science Aims and scope Submit manuscript

Abstract

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 is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9

Similar content being viewed by others

References

  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. https://doi.org/10.1515/ijame-2016-0049

    Article  Google Scholar 

  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. https://doi.org/10.1007/s00466-014-1095-0

    Article  Google Scholar 

  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. https://doi.org/10.1098/rsos.160746

    Article  Google Scholar 

  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. https://doi.org/10.1088/1748-3190/aa65db

    Article  Google Scholar 

  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. https://doi.org/10.1109/memsys.2015.7050876

  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. https://doi.org/10.1016/S1672-6529(16)60297-4

    Article  Google Scholar 

  7. Van Truong T, Nguyen Q-V, Lee H (2017) Bio-inspired flexible flapping wings with elastic deformation. Aerospace 4:37. https://doi.org/10.3390/aerospace4030037

    Article  Google Scholar 

  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. https://doi.org/10.1016/S1672-6529(14)60057-3

    Article  Google Scholar 

  9. Muhammad A, Park HC, Hwang DY et al (2009) Mimicking unfolding motion of a beetle hind wing. Chin Sci Bull 54:2416–2424. https://doi.org/10.1007/s11434-009-0242-z

    Article  Google Scholar 

  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. https://doi.org/10.1007/s10015-016-0339-9

    Article  Google Scholar 

  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. https://doi.org/10.1007/s10526-014-9576-9

    Article  Google Scholar 

  12. Miller LA, Peskin CS (2009) Flexible clap and fling in tiny insect flight. J Exp Biol 212:3076–3090. https://doi.org/10.1242/jeb.028662

    Article  Google Scholar 

  13. Haas F, Beutel RG (2001) Wing folding and the functional morphology of the wing base in Coleoptera. Zoology 104:123–141. https://doi.org/10.1078/0944-2006-00017

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1073/pnas.1620612114

    Article  CAS  Google Scholar 

  15. Kwok K, Pellegrino S (2013) Folding, stowage, and deployment of viscoelastic tape springs. AIAA J 51:1908–1918. https://doi.org/10.2514/1.J052269

    Article  Google Scholar 

  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. https://doi.org/10.1088/1748-3190/aa979c

    Article  CAS  Google Scholar 

  17. Lawrence JF (1993) Evolution of the hind wing in coleoptera. Can Entomol 125:181–258. https://doi.org/10.4039/Ent125181-2

    Article  Google Scholar 

  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. https://doi.org/10.1371/journal.pone.0080689

    Article  Google Scholar 

  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. https://doi.org/10.1115/detc2017-67697

  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. https://doi.org/10.3762/bjnano.9.75

    Article  CAS  Google Scholar 

  21. Hedrick TL, Combes SA, Miller LA (2015) Recent developments in the study of insect flight. Can J Zool 93:925–943. https://doi.org/10.1139/cjz-2013-0196

    Article  Google Scholar 

  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. https://doi.org/10.1002/9780470686652.eae404

    Chapter  Google Scholar 

  23. Fedorenko DN (2015) Transverse folding and evolution of the hind wings in beetles (Insecta, Coleoptera). Biol Bull Rev 5:71–84. https://doi.org/10.1134/S2079086415010028

    Article  Google Scholar 

  24. Saito K, Yamamoto S, Maruyama M, Okabe Y (2014) Asymmetric hindwing foldings in rove beetles. Proc Natl Acad Sci 111:16349–16352. https://doi.org/10.1073/pnas.1409468111

    Article  CAS  Google Scholar 

  25. Haas F (2006) Evidence from folding and functional lines of wings on inter-ordinal relationships in Pterygota. Arthropod Syst Phylogeny 64:149–158

    Google Scholar 

  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. https://doi.org/10.1098/rspb.2000.1153

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1038/srep39039

    Article  CAS  Google Scholar 

  28. Burrows M (2016) Development and deposition of resilin in energy stores for locust jumping. J Exp Biol 219:2449–2457. https://doi.org/10.1242/jeb.138941

    Article  Google Scholar 

  29. Su RS, Kim Y, Liu JC (2014) Resilin: protein-based elastomeric biomaterials. Acta Biomater 10:1601–1611. https://doi.org/10.1016/j.actbio.2013.06.038

    Article  CAS  Google Scholar 

  30. Haas F, Gorb S, Wootton R (2000) Elastic joints in dermapteran hind wings: materials and wing folding. Arthropod Struct Dev 29:137–146. https://doi.org/10.1016/S1467-8039(00)00025-6

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1080/19768354.2017.1330764

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1016/s0065-2806(08)60071-5

    Chapter  Google Scholar 

  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. https://doi.org/10.1016/j.actbio.2017.07.034

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1371/journal.pone.0193147

    Article  CAS  Google Scholar 

  35. Manuscript A (2012) Recombinant exon-encoded resilins for elastomeric biomaterials. Biomaterials 32:9231–9243. https://doi.org/10.1016/j.biomaterials.2011.06.010.Recombinant

    Article  Google Scholar 

  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. https://doi.org/10.1111/joa.12362

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1109/3m-nano.2018.8552182

  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. https://doi.org/10.1016/S1467-8039(00)00014-1

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1114/1.1424921

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1038/ncomms2576

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1016/S1672-6529(16)60439-0

    Article  Google Scholar 

  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. https://doi.org/10.1016/S1359-6454(01)00328-7

    Article  CAS  Google Scholar 

  43. Bell TJ, Field JS, Swain MV (1992) Elastic–plastic characterization of thin films with spherical indentation. Thin Solid Films 220:289–294. https://doi.org/10.1016/0040-6090(92)90587-2

    Article  Google Scholar 

  44. Betts CR (2009) The comparative morphology of the wings and axillae of selected Heteroptera. J Zool 1:255–282. https://doi.org/10.1111/j.1096-3642.1986.tb00639.x

    Article  Google Scholar 

  45. Haas F, Wootton RJ (1996) Two basic mechanisms in insect wing folding. Proc R Soc Lond Ser B Biol Sci 263:1651–1658. https://doi.org/10.1098/rspb.1996.0241

    Article  Google Scholar 

  46. Haas F (2000) Wing folding in insects: a natural, deployable structure. https://doi.org/10.1007/978-94-015-9514-8_15

  47. Forbes WTM (1926) The wing folding patterns of the Coleoptera. J N Y Entomol Soc 34:91–139. https://doi.org/10.2307/25004114

    Article  Google Scholar 

  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. https://doi.org/10.1098/rstb.2003.1351

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1111/j.1365-2818.2011.03523.x

    Article  CAS  Google Scholar 

  50. Jongerius SR, Lentink D (2010) Structural analysis of a dragonfly wing. Exp Mech 50:1323–1334. https://doi.org/10.1007/s11340-010-9411-x

    Article  Google Scholar 

  51. Kantor Y, Kardar M, Nelson DR (1987) Tethered surfaces: statics and dynamics. Phys Rev A 35:3056–3071. https://doi.org/10.1103/PhysRevA.35.3056

    Article  CAS  Google Scholar 

  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. https://doi.org/10.1098/rsos.171152

    Article  Google Scholar 

  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 203:2945–2955

    CAS  Google Scholar 

  54. Rothschild M, Von Euw J, Reichstein T (1972) Aristolochic acids stored by Zerynthia polyxena (Lepidoptera). Insect Biochem 2:334–343. https://doi.org/10.1016/0020-1790(72)90038-8

    Article  CAS  Google Scholar 

  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. https://doi.org/10.2514/1.J050494

    Article  Google Scholar 

  56. Faber JA, Arrieta AF, Studart AR (2018) Bioinspired spring origami. Science 359:1386–1391. https://doi.org/10.1126/science.aap7753

    Article  CAS  Google Scholar 

  57. Weis-Fogh T (1961) Molecular interpretation of the elasticity of resilin, a rubber-like protein. J Mol Biol 3:648–667. https://doi.org/10.1016/S0022-2836(61)80028-4

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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 information

Authors and Affiliations

  1. Key Laboratory of Bionic Engineering (Ministry of Education, China), Jilin University, Changchun, 130022, People’s Republic of China

    Zelai Song, Yongwei Yan, Jin Tong & Jiyu Sun

Authors
  1. Zelai Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongwei Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiyu Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Jiyu Sun.

Ethics declarations

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.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, Z., Yan, Y., Tong, J. et al. Asian ladybird folding and unfolding of hind wing: biomechanical properties of resilin in affecting the tensile strength of the folding area. J Mater Sci 55, 4524–4537 (2020). https://doi.org/10.1007/s10853-019-04326-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10853-019-04326-6

Search

Navigation