journal article·2020-07

Biomechanical strategies underlying the durability of a wing-to-wing coupling mechanism

Arman Toofani, Sepehr H. Eraghi, Mohammad Khorsandi, Ali Khaheshi, Abolfazl Darvizeh, Stanislav Gorb, Hamed Rajabi

Acta Biomaterialia· Volume 110
Publisher page

Abstract

Insects thrived soon after they acquired the ability to fly. Beyond the reach of the non-flying competitors, flying insects colonized a wide variety of habitats. Although flight is an efficient way to disperse and escape predators, it is energetically costly. Hence, various strategies are served to enhance flight efficiency as much as possible. A striking example is the development of wing-to-wing coupling mechanisms in many neopterous insects to minimize the aerodynamic interference of fore and hind wings. However, it remains unclear how the seemingly delicate coupling mechanisms can withstand excessive mechanical stresses encountered during flight. Here we studied the complicated coupling mechanism of drone honey bees, which consists of a set of tiny hooks and a thickened membrane. We found that the durability of the coupling mechanism results from two complementary strategies. First, the angles at which hooks and membrane are coupled and uncoupled may be adjusted, so that the resulting stresses are minimized. Second, the out-of-plane structure, soft base and pronounced tip reduce the stress developed in the hooks, yet maintaining the coupling strength. We anticipate our study, which presents the first numerical model of insect wing coupling mechanisms, to be a starting point for the development of more sophisticated models in the future. Such models are particularly useful for comparative analysis of the influence of different morphological features on the functionality of complex coupling mechanisms. STATEMENT OF SIGNIFICANCE: Hamuli, or 'tiny hooks', is the Greek term for hook-like structures on the anterior margin of honey bee hind wings. By fitting into the fold posterior margin of fore wings, the hooks couple the two wings to each other. Despite their seemingly fragile structure, the hooks withstand substantial mechanical stresses. We show that the out-of-plane structure, soft base and pronounced tip are morphological features that enhance the durability of the hooks, without compromising their function.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Insect and Arachnid Ecology and Behavior · Biomimetic flight and propulsion mechanisms · Neurobiology and Insect Physiology Research

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (35)

Show source-provided references
1. Hotspots-preserving pieces of fragile biosphere
2. Daly · 1978
3. The earliest late Carboniferous winged insect (Insecta, Protodonata) from Argentina: geographical and stratigraphical location
4. To be or not to be: postcubital vein in insects revealed by microtomography
5. Wing coupling
6. Munk · 1923
7. Unusual phase relationships between the forewings and hindwings in flying dragonflies10.1242/jeb.109.1.379 ↗
8. Hamuli in the Hymenoptera (Insecta) and their phylogenetic implications10.1080/00222939700770831 ↗
9. Flight of the honey bee. VIII. Functional elements and mechanics of the “flight motor” and the wing joint–one of the most complicated gear-mechanisms in the animal kingdom10.1007/s003600050152 ↗
10. Wing-locking mechanisms in aquatic Heteroptera10.1002/jmor.10070 ↗
11. Structure, properties and functions of the forewing-hindwing coupling of honeybees10.1016/j.jinsphys.2019.103936 ↗
12. Effects of load type (pollen or nectar) and load mass on hovering metabolic rate and mechanical power output in the honey bee Apis mellifera10.1242/jeb.00347 ↗
13. Short-amplitude high-frequency wing strokes determine the aerodynamics of honeybee flight10.1073/pnas.0506590102 ↗
14. Coping with nonrepairable body damage: effects of wing damage on foraging performance in bees10.1016/j.anbehav.2010.12.011 ↗
15. Experimental wing damage affects foraging effort and foraging distance in honeybees Apis mellifera10.1155/2011/419793 ↗
16. Observations of mating behaviour in the honeybee10.1080/00218839.1963.11100050 ↗
17. Sperm competition, kinship, and sociality in the aculeate Hymenoptera
18. Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy10.1111/j.1365-2818.2011.03523.x ↗
19. A simple, high-resolution, non-destructive method for determining the spatial gradient of the elastic modulus of insect cuticle10.1098/rsif.2018.0312 ↗
20. Stiffness distribution in insect cuticle: a continuous or a discontinuous profile?10.1098/rsif.2017.0310 ↗
21. Design and mechanical properties of insect cuticle10.1016/j.asd.2004.05.006 ↗
22. Dhondt, G. (2017). CalculiX CrunchiX User's Manual Version 2.12. Munich, Germany, accessed Dec. 31, 2019.
23. Frictional properties of contacting surfaces in the hemelytra-hindwing locking mechanism in the bug Coreus marginatus (Heteroptera, Coreidae)
24. When less is more: experimental evidence for tenacity enhancement by division of contact area10.1080/00218460490430199 ↗
25. Duration of flight and of interflight time of drone honey bees, Apis mellifera10.1093/aesa/64.3.609 ↗
26. Wing beat frequencies of Apis cerana indica and Apis mellifera10.1080/00218839.1977.11099859 ↗
27. Biomechanics of fore wing to hind wing coupling in the southern green stink bug Nezara viridula (Pentatomidae)10.1016/j.actbio.2019.09.027 ↗
28. How does a slender tibia resist buckling? Effect of material, structural and geometric characteristics on buckling behaviour of the hindleg tibia in stick insect postembryonic development
29. Cuticle sclerotization determines the difference between the elastic moduli of locust tibiae
30. Insect cuticle sclerotization10.1146/annurev.en.37.010192.001421 ↗
31. Spider mechanoreceptors10.1016/j.conb.2004.07.005 ↗
32. Natural hook-and-loop fasteners: anatomy, mechanical properties, and attachment force of the jointed hooks of the Galium aparine fruit
33. The wing coupling apparatus and the morphometric analysis of honeybee populations
34. Differences in drone and worker physiology in honeybees (Apis mellifera)10.1051/apido:2005015 ↗
35. Attachment ability of the southern green stink bug Nezara viridula (Heteroptera: Pentatomidae)10.1007/s00359-017-1177-5 ↗