Controlling roll perturbations in fruit flies

Journal of the Royal Society Interface

Volumn 12, Issue 105, 2015, Pages

  Beatus, Tsevi ^a   Guckenheimer, John M ^b   Cohen, Itai ^a  

^a School of Operations Research and Industrial Engineering   (United States)

^b NONE   (United States)

Author keywords

Biolocomotion; Flight control; Fruit fly; Insect flight

Indexed keywords

CONTROLLERS; DEGREES OF FREEDOM (MECHANICS); FRUITS; TWO TERM CONTROL SYSTEMS;

AERODYNAMIC INSTABILITY; BIOLOCOMOTION; CORRECTIVE ACTIONS; FLIGHT CONTROL; FRUIT FLIES; HIERARCHICAL CONTROL; INSECT FLIGHT; LINEAR PROPORTIONAL-INTEGRAL CONTROLLER;

FLIGHT CONTROL SYSTEMS;

ACCELERATION; ARTICLE; BIOMECHANICS; BODY KINEMATICS; CONTROLLED STUDY; DECELERATION; DROSOPHILA MELANOGASTER; EULER EQUATION; FLIGHT; FORELIMB; KINEMATICS; MAGNET; MAGNETIC FIELD; MATHEMATICAL PARAMETERS; NEGATIVE FEEDBACK; NONHUMAN; PITCH; ROLL PERTURBATION; ROLL VELOCITY; ROTATION; STEADY STATE; STROKE AMPLITUDE ASYMMETRY; TORQUE; VIDEORECORDING; ANIMAL; FLYING; PHYSIOLOGY; TIME FACTOR; WING;

ANIMALIA; HEXAPODA;

ANIMALS; BIOMECHANICAL PHENOMENA; DROSOPHILA MELANOGASTER; FLIGHT, ANIMAL; TIME FACTORS; VIDEO RECORDING; WINGS, ANIMAL;

EID: 85003881194     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2015.0075     Document Type: Article

References (66)

1. Combes SA, Dudley R. 2009 Turbulence-driven instabilities limit insect flight performance. Proc. Natl Acad. Sci. USA 106, 9105-9108. (doi:10.1073/pnas.0902186106)
2. Ravi S, Crall JD, Fisher A, Combes SA. 2013 Rolling with the flow: bumblebees flying in unsteady wakes. J. Exp. Biol. 216, 4299-4309. (doi:10.1242/jeb.090845)
3. Ortega-Jimenez VM, Greeter JS, Mittal R, Hedrick TL. 2013 Hawkmoth flight stability in turbulent vortex streets. J. Exp. Biol. 216, 4567-4579. (doi:10.1242/jeb.089672)
4. Vance J, Faruque I, Humbert J. 2013 Kinematic strategies for mitigating gust perturbations in insects. Bioinspir. Biomim. 8, 016004. (doi:10.1088/1748-3182/8/1/016004)
5. Sane SP. 2003 The aerodynamics of insect flight. J. Exp. Biol. 206, 4191-4208. (doi:10.1242/jeb.00663)
6. Wang ZJ. 2005 Dissecting insect flight. Annu. Rev. Fluid Mech. 37, 183-210. (doi:10.1146/annurev.fluid.36.050802.121940)
7. Taylor GK, Thomas AL. 2003 Dynamic flight stability in the desert locust Schistocerca gregaria. J. Exp. Biol. 206, 2803-2829. (doi:10.1242/jeb.00501)
8. Sun M, Xiong Y. 2005 Dynamic flight stability of a hovering bumblebee. J. Exp. Biol. 208, 447-459. (doi:10.1242/jeb.01407)
9. Taylor GK, Żbikowski R. 2005 Nonlinear timeperiodic models of the longitudinal flight dynamics of desert locusts Schistocerca gregaria. J. R. Soc. Interface 2, 197-221. (doi:10.1098/rsif.2005.0036)
10. Sun M, Wang J, Xiong Y. 2007 Dynamic flight stability of hovering insects. Acta Mech. Sin. 23, 231-246. (doi:10.1007/s10409-007-0068-3)
11. Liu H, Nakata T, Gao N, Maeda M, Aono H, Shyy W. 2010 Micro air vehicle-motivated computational biomechanics in bio-flights: aerodynamics, flight dynamics and maneuvering stability. Acta Mech. Sin. 26, 863-879. (doi:10.1007/s10409-010-0389-5)
12. Faruque I, Humbert JS. 2010 Dipteran insect flight dynamics. Part 1 Longitudinal motion about hover. J. Theor. Biol. 264, 538-552. (doi:10.1016/j.jtbi.2010.02.018)
13. Ristroph L, Ristroph G, Morozova S, Bergou AJ, Chang S, Guckenheimer J, Wang ZJ, Cohen I. 2013 Active and passive stabilization of body pitch in insect flight. J. R. Soc. Interface 10, 20130237. (doi:10.1098/rsif.2013.0237)
14. Gao N, Aono H, Liu H. 2011 Perturbation analysis of 6DoF flight dynamics and passive dynamic stability of hovering fruit fly Drosophila melanogaster. J. Theor. Biol. 270, 98-111. (doi:10.1016/j.jtbi.2010.11.022)
15. Liang B, Sun M. 2013 Nonlinear flight dynamics and stability of hovering model insects. J. R. Soc. Interface 10, 20130269. (doi:10.1098/rsif.2013.0269)
16. Xu N, Sun M. 2013 Lateral dynamic flight stability of a model bumblebee in hovering and forward flight. J. Theor. Biol. 319, 102-115. (doi:10.1016/j.jtbi.2012.11.033)
17. Zhang Y, Sun M. 2010 Dynamic flight stability of a hovering model insect: lateral motion. Acta Mech. Sin. 26, 175-190. (doi:10.1007/s10409-009-0303-1)
18. Sun M. 2014 Insect flight dynamics: stability and control. Rev. Mod. Phys. 86, 615-646. (doi:10.1103/RevModPhys.86.615)
19. Prez-Arancibia NO, Ma KY, Galloway KC, Greenberg JD, Wood JR. 2011 First controlled vertical flight of a biologically inspired microrobot. Bioinspir. Biomim. 6, 036009. (doi:10.1088/1748-3182/6/3/036009)
20. Nalbach G. 1994 Extremely non-orthogonal axes in a sense organ for rotation: behavioural analysis of the dipteran haltere system. Neuroscience 61, 149-163. (doi:10.1016/0306-4522(94)90068-X)
21. Dickinson MH. 1999 Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster. Phil. Trans. R. Soc. Lond. B 354, 903-916. (doi:10.1098/rstb.1999.0442)
22. Sherman A, Dickinson MH. 2004 Summation of visual and mechanosensory feedback in Drosophila flight control. J. Exp. Biol. 207, 133-142. (doi:10.1242/jeb.00731)
23. Sherman A, Dickinson MH. 2003 A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster. J. Exp. Biol. 206, 295-302. (doi:10.1242/jeb.00075)
24. Sugiura H, Dickinson MH. 2009 The generation of forces and moments during visual-evoked steering maneuvers in flying Drosophila. PLoS ONE 4, e4883. (doi:10.1371/journal.pone.0004883)
25. Hengstenberg R, Sandeman D, Hengstenberg B. 1986 Compensatory head roll in the blowfly Calliphora during flight. Proc. R. Soc. Lond. B 227, 455-482. (doi:10.1098/rspb.1986.0034)
26. Srinivasan MV. 1977 A visually-evoked roll response in the housefly. J. Comp. Physiol. 119, 1-14. (doi:10.1007/BF00655868)
27. Waldmann B, Zarnack W. 1988 Forewing movements and motor activity during roll manoeuvers in flying desert locusts. Biol. Cybern. 59, 325-335. (doi:10.1007/BF00332923)
28. Lehmann F-O and Dickinson M.H. 1998 The control of wing kinematics and flight forces in fruit flies (Drosophila spp). J. Exp. Biol. 201, 385-401.
29. Zanker J. 1990 The wing beat of Drosophila melanogaster. III. Control. Phil. Trans. R. Soc. Lond. B 327, 45-64. (doi:10.1098/rstb.1990.0042)
30. Windsor SP, Bomphrey RJ, Taylor GK. 2014 Visionbased flight control in the hawkmoth Hyles lineata. J. R. Soc. Interface 11, 20130921. (doi:10.1098/rsif.2013.0921)
31. Fry SN, Sayaman R, Dickinson MH. 2005 The aerodynamics of hovering flight in Drosophila. J. Exp. Biol. 208, 2303-2318. (doi:10.1242/jeb.01612)
32. Bender JA, Dickinson MH. 2006 Visual stimulation of saccades in magnetically tethered Drosophila. J. Exp. Biol. 209, 3170-3182. (doi:10.1242/jeb.02369)
33. Hengstenberg R. 1988 Mechanosensory control of compensatory head roll during flight in the blowfly Calliphora erythrocephala Meig. J. Comp. Physiol. A 163, 151-165. (doi:10.1007/BF00612425)
34. Hensler K, Robert D. 1990 Compensatory head rolling during corrective flight steering in locusts. J. Comp. Physiol. A 166, 685-693. (doi:10.1007/BF00240018)
35. Schilstra C, Van Hateren J. 1998 Stabilizing gaze in flying blowflies. Nature 395, 654. (doi:10.1038/27114)
36. Hateren J, Schilstra C. 1999 Blowfly flight and optic flow. II. Head movements during flight. J. Exp. Biol. 202, 1491-1500.
37. Boeddeker N, Hemmi JM. 2010 Visual gaze control during peering flight manoeuvres in honeybees. Proc. R. Soc. B 277, 1209-1217. (doi:10.1098/rspb.2009.1928)
38. Viollet S, Zeil J. 2013 Feed-forward and visual feedback control of head roll orientation in wasps (Polistes humilis, Vespidae, Hymenoptera). J. Exp. Biol. 216, 1280-1291. (doi:10.1242/jeb.074773)
39. Ristroph L, Bergou AJ, Ristroph G, Coumes K, Berman GJ, Guckenheimer J, Wang ZJ, Cohen I. 2010 Discovering the flight autostabilizer of fruit flies by inducing aerial stumbles. Proc. Natl Acad. Sci. USA 107, 4820-4824. (doi:10.1073/pnas.1000615107)
40. Tanaka K, Kawachi K. 2006 Response characteristics of visual altitude control system in Bombus terrestris. J. Exp. Biol. 209, 4533-4545. (doi:10.1242/jeb.02552)
41. Graetzel CF, Nelson BJ, Fry SN. 2010 Frequency response of lift control in Drosophila. J. R. Soc. Interface 7, 1603-1616. (doi:10.1098/rsif.2010.0040)
42. Hyslop A, Krapp HG, Humbert JS. 2010 Control theoretic interpretation of directional motion preferences in optic flow processing interneurons. Biol. Cybern. 103, 353-364. (doi:10.1007/s00422-010-0404-8)
43. Rohrseitz N, Fry SN. 2011 Behavioural system identification of visual flight speed control in Drosophila melanogaster. J. R. Soc. Interface 8, 171-185. (doi:10.1098/rsif.2010.0225)
44. Cheng B, Deng X, Hedrick TL. 2011 The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta). J. Exp. Biol. 214, 4092-4106. (doi:10.1242/jeb.062760)
45. Schnell B, Weir PT, Roth E, Fairhall AL, Dickinson MH. 2014 Cellular mechanisms for integral feedback in visually guided behavior. Proc. Natl Acad. Sci. USA 111, 5700-5705. (doi:10.1073/pnas.1400698111)
46. Ristroph L, Berman GJ, Bergou AJ, Wang ZJ, Cohen I. 2009 Automated hull reconstruction motion tracking (HRMT) applied to sideways maneuvers of free-flying insects. J. Exp. Biol. 212, 1324-1335. (doi:10.1242/jeb.025502)
47. Eaton RC. 1984 Neural mechanisms of startle behavior. Berlin, Germany: Springer.
48. Cheng B, Fry SN, Huang Q, Dickson WB, Dickinson MH, Deng X. 2009 Turning dynamics and passive damping in flapping flight. In IEEE Int. Conf. on Robotics and Automation, pp. 1889-1896. (doi:10.1109/ROBOT.2009.5152826)
49. Bertholf LM. 1932 The extent of the spectrum of Drosophila and the distribution of stimulative efficiencey in it. Zeitschrift für vergleichende Physiologie 18, 32-64.
50. Young J, Walker SM, Bomphrey RJ, Taylor GK, Thomas AL. 2009 Details of insect wing design and deformation enhance aerodynamic function and flight efficiency. Science 325, 1549-1552. (doi:10.1126/science.1175928)
51. 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)
52. Goodman LJ. 1960 The landing responses of insects. I. The landing response of the fly, Lucilia sericata, and other Calliphorinae. J. Exp. Biol. 37, 854-878.
53. Borst A. 1986 Time course of the houseflies' landing response. Biol. Cybern. 54, 379-383. (doi:10.1007/BF00355543)
54. Van Breugel F, Dickinson MH. 2012 The visual control of landing and obstacle avoidance in the fruit fly Drosophila melanogaster. J. Exp. Biol. 215, 1783-1798. (doi:10.1242/jeb.066498)
55. Ma KY, Chirarattananon P, Fuller SB, Wood RJ. 2013 Controlled flight of a biologically inspired, insectscale robot. Science 340, 603-607. (doi:10.1126/science.1231806)
56. 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.
57. Berman GJ, Wang JZ. 2007 Energy-minimizing kinematics in hovering insect flight. J. Fluid Mech. 582, 153-167. (doi:10.1017/S0022112007006209)
58. Pringle J. 1948 The gyroscopic mechanism of the halteres of diptera. Phil Trans. R. Soc. Lond. B 233, 347-384. (doi:10.1098/rstb.1948.0007)
59. Nalbach G. 1993 The halteres of the blowfly Calliphora. J. Comp. Physiol. A 173, 293-300. (doi:10.1007/BF00212693)
60. Weis-Fogh T. 1973 Quick estimates of flight fitness in hovering animals, including novel mechanisms for lift production. J. Exp. Biol. 59, 169-230.
61. Fotowat H, Fayyazuddin A, Bellen HJ, Gabbiani F. 2009 A novel neuronal pathway for visually guided escape in Drosophila melanogaster. J. Neurophysiol. 102, 875-885. (doi:10.1152/jn.00073.2009)
62. Eaton RC, Bombardieri RA, Meyer DL. 1977 The Mauthner-initiated startle response in teleost fish. J. Exp. Biol. 66, 65-81.
63. Gronenberg W. 1995 The fast mandible strike in the trap-jaw ant Odontomachus. 1. Temporal properties and morphological characteristics. J. Comp. Physiol. A 176, 391-398. (doi:10.1007/BF00219064)
64. Camhi JM, Nolen TG. 1981 Properties of the escape system of cockroaches during walking. J. Comp. Physiol. 142, 339-346. (doi:10.1007/BF00605446)
65. Jindrich DL, Full RJ. 2002 Dynamic stabilization of rapid hexapedal locomotion. J. Exp. Biol. 205, 2803-2823.
66. Hedrick TL, Cheng B, Deng X. 2009 Wingbeat time and the scaling of passive rotational damping in flapping flight. Science 324, 252-255. (doi:10.1126/science.1168431)