Wing flexibility enhances load-lifting capacity in bumblebees

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1759, 2013, Pages

  Mountcastle, Andrew M ^a   Combes, Stacey A ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Aerodynamics; Insect flight; Load lifting; Resilin; Wing deformation; Wing flexibility

Indexed keywords

AERODYNAMICS; BEE; COMPUTER SIMULATION; FLIGHT; LOCOMOTION; WING MORPHOLOGY;

EID: 84878248801     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.0531     Document Type: Article

References (57)

1. Ellington CP, van den Berg C, Willmott AP, Thomas ALR. 1996 Leading-edge vortices in insect flight. Nature 384, 626-630. (doi:10.1038/384626a0)
2. Dickinson MH, Lehmann FO, Sane SP. 1999 Wing rotation and the aerodynamic basis of insect flight. Science 284, 1954-1960. (doi:10.1126/science.284. 5422.1954)
3. Sane SP, Dickinson MH. 2002 The aerodynamic effects of wing rotation and a revised quasi-steady model of flapping flight. J. Exp. Biol. 205, 1087-1096.
4. Young J, Walker SM, Bomphrey RJ, Taylor GK, Thomas ALR. 2009 Details of insect wing design and deformation enhance aerodynamic function and flight efficiency. Science 325, 1549-1552. (doi:10. 1126/science.1175928)
5. Du G, Sun M. 2010 Effects of wing deformation on aerodynamic forces in hovering hoverflies. J. Exp. Biol. 213, 2273-2283. (doi:10.1242/jeb.040295)
6. Nakata T, Liu H. 2011 Aerodynamic performance of a hovering hawkmoth with flexible wings, a computational approach. Proc. R. Soc. B 279, 722-731. (doi:10.1098/rspb.2011.1023)
7. Vanella M, Fitzgerald T, Preidikman S, Balaras E, Balachandran B. 2009 Influence of flexibility on the aerodynamic performance of a hovering wing. J. Exp. Biol. 212, 95-105. (doi:10.1242/jeb.016428)
8. Mountcastle AM, Daniel TL. 2010 Vortexlet models of flapping flexible wings show tuning for force production and control. Bioinspir. Biomim. 5, 045005. (doi:10.1088/1748-3182/5/4/045005)
9. Mountcastle AM, Daniel TL. 2009 Aerodynamic and functional consequences of wing compliance. Exp. Fluids 46, 873-882. (doi:10.1007/s00348-008-0607-0)
10. Zhao L, Huang QF, Deng XY, Sane SP. 2010 Aerodynamic effects of flexibility in flapping wings. J. R. Soc. Interface 7, 485-497. (doi:10.1098/rsif. 2009.0200)
11. Tanaka H, Whitney JP, Wood RJ. 2011 Effect of flexural and torsional wing flexibility on lift generation in hoverfly flight. Integr. Comp. Biol. 51, 142-150. (doi:10.1093/icb/icr051)
12. Wootton RJ, Evans KE, Herbert R, Smith CW. 2000 The hind wing of the desert locust (Schistocerca gregaria Forskal) I. Functional morphology and mode of operation. J. Exp. Biol. 203, 2921-2931.
13. Haas F, Gorb S, Wootton RJ. 2000 Elastic joints in dermapteran hind wings, materials and wing folding. Arthropod. Struct. Dev. 29, 137-146. (doi:10.1016/S1467-8039(00)00025-6)
14. Haas F, Gorb S, Blickhan R. 2000 The function of resilin in beetle wings. Proc. R. Soc. Lond. B 267, 1375-1381. (doi:10.1098/rspb.2000.1153)
15. Donoughe S, Crall JD, Merz RA, Combes SA. 2011 Resilin in dragonfly and damselfly wings and its implications for wing flexibility. J. Morphol. 272, 1409-1421. (doi:10.1002/jmor.10992)
16. Weis-Fogh T. 1960 A rubber-like protein in insect cuticle. J. Exp. Biol. 37, 889-907.
17. Young D, Bennetclark HC. 1995 The role of the timbal in cicada sound production. J. Exp. Biol. 198, 1001-1019.
18. Neff D, Frazier SF, Quimby L, Wang RT, Zill S. 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. (doi:10.1016/ S1467-8039(00)00014-1)
19. Gorb SN. 1999 Serial elastic elements in the damselfly wing, mobile vein joints contain resilin. Naturwissenschaften 86, 552-555. (doi:10.1007/ s001140050674)
20. Lehmann FO, Gorb S, Nasir N, Schutzner P. 2011 Elastic deformation and energy loss of flapping fly wings. J. Exp. Biol. 214, 2949-2961. (doi:10.1242/ jeb.045351)
21. Ellington CP. 1984 The aerodynamics of hovering insect flight. II. Morphological parameters. Phil. Trans. R. Soc. Lond. B 305, 17-40. (doi:10.1098/ rstb.1984.0050)
22. Lehmann FO. 1999 Ambient temperature affects free-flight performance in the fruit fly Drosophila melanogaster. J. Comp. Physiol. B 169, 165-171. (doi:10.1007/s003600050207)
23. Buchwald R, Dudley R. 2010 Limits to vertical force and power production in bumblebees (Hymenoptera, Bombus impatiens). J. Exp. Biol. 213, 426-432. (doi:10.1242/jeb.033563)
24. Dillon ME, Dudley R. 2004 Allometry of maximum vertical force production during hovering flight of neotropical orchid bees (Apidae, Euglossini). J. Exp. Biol. 207, 417-425. (doi:10.1242/jeb.00777)
25. Marden JH. 1987 Maximum lift production during takeoff in flying animals. J. Exp. Biol. 130, 235-258.
26. Chai P, Chen JSC, Dudley R. 1997 Transient hovering performance of hummingbirds under conditions of maximal loading. J. Exp. Biol. 200, 921-929.
27. Chai P, Millard D. 1997 Flight and size constraints, hovering performance of large hummingbirds under maximal loading. J. Exp. Biol. 200, 2757-2763.
28. Marden JH. 1989 Effects of load-lifting constraints on the mating system of a dance fly. Ecology 70, 496-502. (doi:10.2307/1937553)
29. Coelho JR, Hoagland J. 1995 Load-lifting capacities of three species of yellowjackets (Vespula) foraging on honey-bee corpses. Funct. Ecol. 9, 171-174. (doi:10.2307/2390561)
30. Altshuler DL, Dudley R. 2003 Kinematics of hovering hummingbird flight along simulated and natural elevational gradients. J. Exp. Biol. 206, 3139-3147. (doi:10.1242/jeb.00540)
31. Michener CD. 1944 Comparative external morphology, phylogeny, and a classification of the bees (Hymenoptera). Bull. Am. Mus. Nat. Hist. 82, 152-317.
32. Combes SA, Daniel TL. 2003 Flexural stiffness in insect wings I. Scaling and the influence of wing venation. J. Exp. Biol. 206, 2979-2987. (doi:10. 1242/jeb.00523)
33. Mengesha TE, Vallance RR, Mittal R. 2011 Stiffness of desiccating insect wings. Bioinspir. Biomim. 6, 014001. (doi:10.1088/1748-3182/6/1/014001)
34. Feuerbacher E, Fewell JH, Roberts SP, Smith EF, Harrison JF. 2003 Effects of load type (pollen or nectar) and load mass on hovering metabolic rate and mechanical power output in the honey bee Apis mellifera. J. Exp. Biol. 206, 1855-1865. (doi:10. 1242/jeb.00347)
35. Peitsch D, Fietz A, Hertel H, Souza J, Ventura DF, Menzel R. 1992 The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A 170, 23-40.
36. Bertsch A. 1984 Foraging in male bumblebees (Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 62, 325-336. (doi:10.1007/BF00384264)
37. Dudley R, Ellington CP. 1990 Mechanics of forward flight in bumblebees. I. Kinematics and morphology. J. Exp. Biol. 148, 19-52.
38. Ellington CP. 1984 The aerodynamics of hovering insect flight III. Kinematics. Phil. Trans. R. Soc. Lond. B 305, 41-78. (doi:10.1098/rstb.1984.0051)
39. Hedrick TL. 2008 Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir. Biomim. 3, 034001. (doi:10.1088/1748-3182/3/ 3/034001)
40. Weis-Fogh T. 1961 Molecular interpretation of the elasticity of resilin, a rubber-like protein. J. Mol. Biol. 3, 648-667. (doi:10.1016/S0022-2836(61) 80028-4)
41. Altshuler DL, Dickson WB, Vance JT, Roberts SP, Dickinson MH. 2005 Short-amplitude high-frequency wing strokes determine the aerodynamics of honeybee flight. Proc. Natl Acad. Sci. USA 102, 18213-18218. (doi:10.1073/pnas.0506590102)
42. Hedenstrom A, Ellington CP, Wolf TJ. 2001 Wing wear, aerodynamics and flight energetics in bumblebees (Bombus terrestris): an experimental study. Funct. Ecol. 15, 417-422. (doi:10.1046/j. 0269-8463.2001.00531.x)
43. Bomphrey R, Taylor G, Thomas A. 2009 Smoke visualization of free-flying bumblebees indicates independent leading-edge vortices on each wing pair. Exp. Fluids 46, 811-821. (doi:10.1007/ s00348-009-0631-8)
44. Srygley RB, Thomas ALR. 2002 Unconventional lift-generating mechanisms in free-flying butterflies. Nature 420, 660-664. (doi:10.1038/nature01223)
45. Bomphrey RJ, Lawson NJ, Harding NJ, Taylor GK, Thomas ALR. 2005 The aerodynamics of Manduca sexta: digital particle image velocimetry analysis of the leading-edge vortex. J. Exp. Biol. 208, 1079-1094. (doi:10.1242/jeb.01471)
46. Maxworthy T. 1979 Experiments on the Weis-Fogh mechanism of lift generation by insects in hovering flight. I. Dynamics of the 'fling'. J. Fluid Mech. 93, 47-63. (doi:10.1017/S0022 112079001774)
47. Sane SP. 2003 The aerodynamics of insect flight. J. Exp. Biol. 206, 4191-4208. (doi:10.1242/ jeb.00663)
48. Walker SM, Thomas ALR, Taylor GK. 2010 Deformable wing kinematics in free-flying hoverflies. J. R. Soc. Interface 7, 131-142. (doi:10. 1098/rsif.2009.0120)
49. Wu JC. 1981 Theory for aerodynamic force and moment in viscous flows. AIAA J. 19, 432-441. (doi:10.2514/3.50966)
50. Combes SA, Crall JD, Mukherjee S. 2010 Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success. Biol. Lett. 6, 426-429. (doi:10.1098/rsbl.2009.0915)
51. Marden JH. 1989 Bodybuilding dragonflies: costs and benefits of maximizing flight muscle. Physiol. Zool. 62, 505-521.
52. Jantzen B, Eisner T. 2008 Hindwings are unnecessary for flight but essential for execution of normal evasive flight in Lepidoptera. Proc. Natl Acad. Sci. USA 105, 16636-16640. (doi:10.1073/ pnas.0807223105)
53. Marden JH, Chai P. 1991 Aerial predation and butterfly design: how palatability, mimicry, and the need for evasive flight constrain mass allocation. Am. Nat. 138, 15-36. (doi:10.1086/285202)
54. Haas CA, Cartar RV. 2008 Robust flight performance of bumble bees with artificially induced wing wear. Can. J. Zool. 86, 668-675. (doi:10.1139/ Z08-034)
55. Cartar RV. 1992 Morphological senescence and longevity: an experiment relating wing wear and life span in foraging wild bumble bees. J. Anim. Ecol. 61, 225-231. (doi:10.2307/5525)
56. Dukas R, Dukas L. 2011 Coping with nonrepairable body damage: effects of wing damage on foraging performance in bees. Anim. Behav. 81, 635-638. (doi:10.1016/j.anbehav.2010.12.011)
57. Heinrich B. 2004 Bumblebee economics. Cambridge, MA: Harvard University Press.