Aerial locomotion in flies and robots: Kinematic control and aerodynamics of oscillating wings

Arthropod Structure and Development

Volumn 33, Issue 3, 2004, Pages 331-345

  Lehmann, Fritz Olaf ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

Drosophila melanogaster; Flight behavior; Fruit fly; Muscle mechanical power; Unsteady aerodynamics

Indexed keywords

BIOMIMETICS; DROSOPHILA; DYNAMICS; FEEDBACK SYSTEM; FLIGHT MUSCLE; FORELIMB; KINEMATICS; LOCOMOTION; MOTION; MOTOR CONTROL; MUSCLE STRENGTH; NEUROMUSCULAR SYSTEM; NONHUMAN; OSCILLATION; REVIEW; ROBOTICS;

ANIMALIA; DROSOPHILA MELANOGASTER; INSECTA; MELANOGASTER;

EID: 3242765412     PISSN: 14678039     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.asd.2004.05.003     Document Type: Article

References (130)

1. Ahn A.N., Full R.J. A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect. Journal of Experimental Biology. 205:2002;379-389
2. Alexander D.E. Wind tunnel studies of turns by flying dragonflies. Journal of Experimental Biology. 122:1986;81-98
3. Azuma A., Watanabe T. Flight performance of a dragonfly. Journal of Experimental Biology. 137:1988;221-252
4. Balint C.N., Dickinson M.H. The correlation between wing kinematics and steering muscle activity in the blowfly Calliphora vicina. Journal of Experimental Biology. 204:2001;4213-4226
5. Bennett L. Clap and fling aerodynamics - an experimental evaluation. Journal of Experimental Biology. 69:1977;261-272
6. Birch J.M., Dickinson M.H. Spanwise flow and the attachment of the leading-edge vortex on insect wings. Nature. 412:2001;729-733
7. Borst A., Bahde S. Comparison between the movement detection systems underlying the optomotor and the landing response in the housefly. Biological Cybernetics. 56:1987;217-224
8. Borst A., Bahde S. Visual information processing in the fly's landing system. Journal of Comparative Physiology A. 163:1988;167-173
9. Braitenberg V. Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Experimental Brain Research. 3:1967;271-298
10. Bülthoff H., Poggio T., Wehrhahn C. 3-D-analysis of the flight trajectories of flies (Drosophila melanogaster). Zeitschrift für Naturforschung 35c. 1980;811-815
11. Casey T.M., Ellington C.P. Energetics of insect flight. Wieser W., Gnaiger E. Energy Transformations in Cells and Organisms. 1989;200-210 Thieme, Stuttgart
12. Collett T.S., Land M.F. Visual control of flight behavior in the hoverfly, Syritta pipiens L. Journal of Comparative Physiology A. 99:1975;1-66
13. Crompton B., Thomason J.C., Mclachlan A. Mating in a viscous universe: the race is to the agile, not to the swift. Proceedings of the Royal Society of London B: Biological Sciences. 270:2003;1991-1995
14. Dalton S. Borne on the Wind. 1975;Reader's Digest Press, New York
15. David C.T. The relationship between body angle and flight speed in free flying Drosophila. Physiological Entomology. 3:1978;191-195
16. De-Laurier J.D. An aerodynamic model for flapping-wing flight. Aeronautical Journal. 1993;125-130
17. Dickinson M.H., Götz K.G. Unsteady aerodynamic performance of model wings at low Reynolds numbers. Journal of Experimental Biology. 174:1993;45-64
18. Dickinson M.H., Götz K.G. The wake dynamics and flight forces of the fruit fly, Drosophila melanogaster. Journal of Experimental Biology. 199:1996;2085-2104
19. Dickinson M.H., Tu M.S. The function of Dipteran flight muscle. Comparative Biochemistry and Physiology A. 116:1997;223-238
20. Dickinson M.H., Lehmann F.-O., Götz K.G. The active control of wing rotation by Drosophila. Journal of Experimental Biology. 182:1993;173-189
21. Dickinson M.H., Hyatt C.J., Lehmann F.-O., Moore J.R., Reedy M.C., Simcox A., Tohotong R., Vigoreaux J.O., Yamashita H., Maughan D.W. Phosphorylation-dependent power output of transgenic flies: an integrated study. Biophysical Journal. 7:1997;3122-3134
22. Dickinson M.H., Lehmann F.-O., Chan W.P. The control of mechanical power in insect flight. American Zoologist. 38:1998;718-728
23. Dickinson M.H., Lehmann F.-O., Sane S. Wing rotation and the aerodynamic basis of insect flight. Science. 284:1999;1954-1960
24. Dudley R. The biomechanics of insect flight. 2002;Princeton University Press, Princeton
25. Dudley R., Ellington C.P. Mechanics of forward flight in bumblebees. II. Quasi-steady lift and power requirements. Journal of Experimental Biology. 148:1990;53-88
26. Eckert H. Optomotorische Untersuchungen am visuellen System der Stubenfliege Musca domestica L. Kybernetik. 14:1973;1-23
27. Egelhaaf M. Visual afferences to flight steering muscles controlling optomotor responses of the fly. Journal of Comparative Physiology A. 165:1989;719-730
28. Egelhaaf M., Borst A. Bewegungswahrnehmung und visuelle Orientierung bei Fliegen. Naturwissenschaften. 77:1990;366-377
29. Egelhaaf M., Borst A. Motion computation and visual orientation in flies. Comparative Biochemical Physiology. 104A:1993;659-673
30. Ellington C.P. The aerodynamics of hovering insect flight. I. The quasi-steady analysis. Philosophical Transactions of the Royal Society London B. 305:1984;1-15
31. Ellington C.P. The aerodynamics of insect flight. VI. Lift and power requirements. Philosophical Transactions of the Royal Society London B. 305:1984;145-181
32. Ellington C.P. The novel aerodynamics of insect flight: applications to micro-air vehicles. Journal of Experimental Biology. 202:1999;3439-3448
33. Ellington C.P., van den Berg C., Willmott A.P., Thomas A.L.R. Leading-edge vortices in insect flight. Nature. 384:1996;626-630
34. Ennos A.R. Inertial and aerodynamic torques on the wings of Diptera in flight. Journal of Experimental Biology. 142:1989;87-95
35. Ennos A.R. The kinematics and aerodynamics of the free flight of some Diptera. Journal of Experimental Biology. 142:1989;49-85
36. Fry S.N., Sayaman R., Dickinson M.H. The aerodynamics of free-flight maneuvers in Drosophila. Science. 300:2003;495-498
37. Götz K.G. Behavioral analysis of the visual system of the fruit fly Drosophila. Götz K.G. Symposium on the information processing in sight sensory systems. 1965;85-100 MIT, Pasadena
38. Götz K.G. Flight control in Drosophila by visual perception of motion. Biological Cybernetics. 4:1968;199-208
39. Götz K.G. Frank G.M., Kayashin L.P. Visual control of locomotion in the fruit fly Drosophila. IUPAB Symposial papers. vol. 3:1974;491-507 Academy of Sciences of the USSR, Mill Valley
40. Götz K.G. Bewegungssehen und Flugsteuerung bei der Fliege Drosophila. Nachtigall W. BIONA-report 2. 1983;21-34 Fischer, Stuttgart
41. Götz K.G. Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. Journal of Experimental Biology. 128:1987;35-46
42. Götz K.G., Wandel U. Optomotor control of the force of flight in Drosophila and Musca II. Covariance of lift and thrust in still air. Biological Cybernetics. 51:1984;135-139
43. Götz K.G., Wehrhan C. Optomotor control of the force of flight in Drosophila and Musca. I. Homology of wingbeat-inhibiting movement detectors. Biological Cybernetics. 51:1984;129-134
44. Götz K.G., Hengstenberg B., Biesinger R. Optomotor control of wing beat and body posture in Drosophila. Biological Cybernetics. 35:1979;101-112
45. Heide G. Die Funktion der nicht-fibrillären Flugmuskeln bei der Schmeiβfliege Calliphora. Teil I: Lage, Insertionsstellen und Innervierungsmuster der Muskeln. Zoologische Jahrbücher. Abteilung Allgemeine Zoologie und Physiologie der Tiere. 76:1971;87-98
46. Heide G. Die Funktion der nicht-fibrillären Flugmuskeln bei der Schmeiβfliege Calliphora. Teil II: Muskuläre Mechanismen der Flugssteuerung und ihre nervöse Kontrolle. Zoologische Jahrbücher. Abteilung Allgemeine Zoologie und Physiologie der Tiere. 76:1971;99-137
47. Heide G. Properties of a motor output system involved in the optomotor response in flies. Biological Cybernetics. 20:1975;99-112
48. Heide G., Götz K.G. Optomotor control of course and altitude in Drosophila is achieved by at least three pairs of flight steering muscles. Journal of Experimental Biology. 199:1996;1711-1726
49. Heide G., Spüler M., Götz K.G., Kamper K. Neural control of asynchronous flight muscles in flies during induced flight manoeuvers. Wendler G. Insect Locomotion. 1985;215-222 Parey, Berlin
50. Heisenberg M., Wolf R. On the fine structure of yaw torque in visual flight orientation of Drosophila melanogaster. Journal of Comparative Physiology A. 130:1979;113-130
51. Heisenberg M., Wolf R. Vision in Drosophila. 1984;Springer, Berlin
52. Heisenberg M., Wolf R. Reafferent control of optomotor yaw torque in Drosophila melanogaster. Journal of Comparative Physiology A. 163:1988;373-388
53. Heisenberg M., Wolf R. The sensory-motor link in motion-dependent flight control of flies. Miles F.A., Wallman J. Visual Motion and its Role in the Stabilization of Gaze. 1993;265-283 Elsevier, Amsterdam
54. Hengstenberg R. Controlling the fly's gyroscope. Nature. 392:1998;757
55. Hollick F.S.J. The flight of the dipterous fly Muscina sabulans Fallén. Philosophical Transactions of the Royal Society London B. 230:1940;357-390
56. Homsher E., Kean C.J. Skeletal muscle energetics and metabolism. Annual Review of Physiology. 40:1978;93-131
57. Jensen M. Biology and physics of locust flight. III. The aerodynamics of locust flight. Philosophical Transactions of the Royal Society London B. 239:1956;511-552
58. Kamakoti R., Shyy W. Moving grid computations for turbulent, aeroelastic flows. AIAA Journal. 33:2003;1-13
59. Kirschfeld K. Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Experimental Brain Research. 3:1967;248-270
60. Kirschfeld K. An optomotor control system with automatic compensation for contrast and texture. Proceedings of the Royal Society of London B. 246:1991;261-268
61. Kliss M., Somps C., Luttges M.W. Stable vortex structures: a flat plate model of dragonfly hovering. Journal of Theoretical Biology. 136:1989;209-228
62. Kutsch W., Hug W. Dipteran flight motor pattern: invariabilities and changes during postlarval development. Journal of Neurobiology. 12:1981;1-14
63. Lan C.E. The unsteady quasi-vortex-lattice method with applications to animal propulsion. Journal of Fluid Mechanics. 93:1979;747-765
64. Lan S., Sun M. Aerodynamic force and flow structures of two airfoils in flapping motions. Acta Mechanica Sinica (English Series). 17:2001;310-331
65. Lan S., Sun M. Aerodynamic properties of a wing performing unsteady rotational motions at low Reynolds Number. Acta Mechanica. 149:2001;145-147
66. Land M.F., Collett T.S. Chasing behaviour of houseflies (Fannia canicularis). Journal of Comparative Physiology A. 89:1974;331-357
67. Lehmann, F.-O., 1994. Aerodynamische, kinematische und electrophysiologische Aspekte der Flugkrafterzeugung und Flugkraftsteuerung bei der Taufliege Drosophila melanogaster. Thesis, Max-Planck-Institute for biological Cybernetics, Tübingen.
68. Lehmann F.-O. Ambient temperature affects free-flight performance in the fruit fly Drosophila melanogaster. Journal of Comparative Physiology B. 169:1999;165-171
69. Lehmann F.-O. The efficiency of aerodynamic force production in Drosophila. Comparative Biochemistry and Physiology A. 131:2001;77-88
70. Lehmann F.-O. The mechanisms of lift enhancement in insect flight. Naturwissenschaften. 91:2004;101-122
71. Lehmann F.-O., Dickinson M.H. The changes in power requirements and muscle efficiency during elevated force production in the fruit fly, Drosophila melanogaster. Journal of Experimental Biology. 200:1997;1133-1143
72. Lehmann F.-O., Dickinson M.H. The control of wing kinematics and flight forces in fruit flies (Drosophila spp.). Journal of Experimental Biology. 201:1998;385-401
73. Lehmann F.-O., Dickinson M.H. The production of elevated flight force compromises flight stability in the fruit fly Drosophila. Journal of Experimental Biology. 204:2001;627-635
74. Lehmann F.-O., Götz K.G. Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster. Journal of Comparative Physiology A. 179:1996;311-322
75. Liu H. Computational biological fluid dynamics: digitizing and visualizing animal swimming and flying. Integrative and Comparative Biology. 42:2002;1050-1059
76. Liu H., Ellington C.P., Kawachi K., van den Berg C., Willmott A.P. A computational fluid dynamic study of hawkmoth hovering. Journal of Experimental Biology. 201:1998;461-477
77. Marden J.H. Bodybuilding dragonflies: costs and benefits of maximizing flight muscle. Physiological Zoology. 62:1989;505-521
78. Maxworthy T. Experiments on the Weis-Fogh mechanism of lift generation by insects in hovering flight. Part 1. Dynamics of the fling. Journal of Fluid Mechanics. 93:1979;47-63
79. Mayer M., Vogtmann K., Bausenwein B., Wolf R., Heisenberg M. Flight control during free yaw turns in Drosophila melanogaster. Journal of Comparative Physiology A. 163:1988;389-399
80. Nachtigall W. Insects in Flight. 1974;McGraw-Hill, New York
81. Nachtigall W. Die aerodynamische Polare des Tipula-Flügels und eine Einrichtung zur halbautomatischen Polarenaufbahme. Nachtigall W. Physiology of Movement; Biomechanics. 1977;347-352 Fischer, Stuttgart
82. Nachtigall W., Wilson D.M. Neuro-muscular control of dipteran flight. Journal of Experimental Biology. 47:1967;77-97
83. Nalbach G. Extremely non-orthogonal axes in a sense organ for rotation: behavioral analysis of the dipteran haltere system. Neuroscience. 61:1994;149-163
84. Norberg U.M. Structure, form, and function of flight in engineering and the living world. Journal of Morphology. 252:2002;52-81
85. Pfau H.K. Funktion einiger direkter tonischer Flügelmuskeln von Calliphora erythrocephala Meigen. Verhandlungen der Deutschen Zoologischen Gesellschaft. 70:1977;275
86. Pringle J.W.S. The gyroscopic mechanism of the halteres of Diptera. Philosophical Transactions of the Royal Society London B. 233:1948;347-384
87. Ramamurti R., Sandberg W.C. Computational study of 3-D flapping foil flows. AIAA PAPER 2001-0605. 2001
88. Reichardt W., Poggio T. A theory of the pattern induced flight orientation of the fly Musca domestica II. Biological Cybernetics. 18:1975;69-80
89. Reichardt W., Poggio T. Visual control of orientation behavior in the fly. Part I. A quantitative analysis. Quarterly Reviews of Biophysics. 9:1976;311-375
90. Saharon D., Luttges M.W. Visualization of unsteady separated flow produces by mechanically driven dragonfly wing kinematics model. AIAA PAPER 88-0569. 1988
91. Salkoff L., Wyman R.J. Ionic currents in Drosophila flight muscle. Journal of Physiology. 337:1983;687-709
92. Sane S., Dickinson M.H. The control of flight force by a flapping wing: lift and drag production. Journal of Experimental Biology. 204:2001;2607-2626
93. Sane S.P., Dickinson M.H. The aerodynamic effects of wing rotation and a revised quasi-steady model of flapping flight. Journal of Experimental Biology. 205:2002;1087-1096
94. Savage S.B., Newman B.G., Wong D.T.-M. The role of vortices and unsteady effects during the hovering flight of dragonflies. Journal of Experimental Biology. 83:1979;59-77
95. Schenato L., Deng X., Sastry S. Flight control system for a micromechanical flying insect: architecture and implementation. In: IEEE International Conference on Robotics and Automation, Seoul, Korea. 2001
96. Sherman A., Dickinson M.H. A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster. Journal of Experimental Biology. 206:2003;295-302
97. Sherman A., Dickinson M.H. Summation of visual and mechanosensory feedback in Drosophila flight control. Journal of Experimental Biology. 207:2004;133-142
98. Shyy W., Berg M., Ljungqvist D. Flapping and flexible wings for biological and micro air vehicles. Progress in Aerospace Sciences. 35:1999;455-505
99. Spedding G.R., Maxworthy T. The generation of circulation and lift in a rigid two-dimensional fling. Journal of Fluid Mechanics. 165:1986;247-272
100. Spüler M., Heide G. Simultaneous recordings of torque, thrust and muscle spikes from the fly Musca domestica during optomotor responses. Zeitschrift für Naturforschung. 33c:1978;455-457
101. Srygley R.B., Dudley R. Correlations of the position of center of body mass with butterfly escape tactics. Journal of Experimental Biology. 174:1993;155-166
102. Sun M., Hamdani H. A study on the mechanism of high-lift generation by an airfoil in unsteady motion at low Reynolds Number. Acta Mechanica Sinica (English Series). 17:2001;97-114
103. Sunada S. Fundamental analysis of three-dimensional near fling. Journal of Experimental Biology. 183:1993;217-248
104. Tammero L.F., Dickinson M.H. Journal of Experimental Biology. 205:2002;327-343
105. Taylor G.K. Mechanics and aerodynamics of insect flight control. Biological Review. 76:2001;449-471
106. Tu M.S. Physiological and biomechanical analysis of flight control by two specialized steering muscles in the blowfly, Calliphora vicina. In: Organismal Biology and Anatomy. 1995;University of Chicago, Chicago
107. Tu M.S., Dickinson M.H. Modulation of negative work output from a steering muscle of the blowfly Calliphora vicina. Journal of Experimental Biology. 192:1994;207-224
108. Tu M.S., Dickinson M.H. The control of wing kinematics by two steering muscles of the blowfly, Calliphora vicina. Journal of Comparative Physiology A. 178:1996;813-830
109. Usherwood J.R., Ellington C.P. The aerodynamic of revolving wings. I. model hawkmoth wings. Journal of Experimental Biology. 205:2002;1547-1564
110. Vogel S. Flight in Drosophila III. Aerodynamic characteristics of fly wings and wing models. Journal of Experimental Biology. 46:1967;431-443
111. Wagner H. Aspects of the free flight behaviour of houseflies (Musca domestica). Gewecke M., Wendler G. Insect Locomotion. 1985;223-232 Parey, Hamburg
112. Wagner H. Flight performance and visual control of flight of the free-flying housefly (Musca domestica L.) II. Pursuit of targets. Philosophical Transactions of the Royal Society London B. 312:1986;553-579
113. Walker J.A. Functional morphology and virtual models: physical constraints on the design of oscillating wings, fins, legs and feet at intermediate Reynolds numbers. Integrative and Comparative Biology. 42:2002;232-242
114. Walker J.A. Rotational lift: something different or more of the same? Journal of Experimental Biology. 205:2002;3783-3792
115. Wang H., Zeng L., Liu H., Chunyong Y. Measuring wing kinematics, flight trajectory and body attitude during forward flight and turning maneuvers in dragonflies. Journal of Experimental Biology. 206:2003;745-757
116. Wang Z.J., Birch J.M., Dickinson M.H. Unsteady forces and flows in low Reynolds number hovering flight: two dimensional computation vs. robotic wing experiments. Journal of Experimental Biology. 207:2003;449-460
117. Wehrhahn C., Poggio T., Bülthoff H. Tracking and chasing in house flies (Musca). An analysis of 3-D flight trajectories. Biological Cybernetics. 45:1982;123-130
118. Wehrhahn C., Rapf D. ON- and OFF-pathways form separate neural substrates for motion perception: psychophysical evidence. Journal of Neuroscience. 12:1992;2247-2250
119. Weis-Fogh T. Quick estimates of flight fitness in hovering animals, including novel mechanisms for lift production. Journal of Experimental Biology. 59:1973;169-230
120. Willmott A.P., Ellington C.P., Thomas A.L.R. Flow visualization and unsteady aerodynamics in the flight of the hawkmoth Manduca sexta. Philosophical Transactions of the Royal Society London B. 352:1996;303-316
121. Wisser A. Mechanisms of wing rotating regulation in Calliphora erythrocephala (Insecta, Diptera). Zoomorphology. 106:1987;261-268
122. Wisser A., Nachtigall W. Functional-morphological investigations on the flight muscles and their insertion points in the blowfly Calliphora erythrocephala (Insecta, Diptera). Zoomorphology. 104:1984;188-195
123. Wolf R., Heisenberg M. Visual control of straight flight in Drosophila melanogaster. Journal of Comparative Physiology A. 167:1990;269-283
124. Zanker J.M. The wing beat of Drosophila melanogaster I. Kinematics. Philosophical Transactions of the Royal Society London B. 327:1990;1-18
125. Zanker J.M. The wing beat of Drosophila melanogaster III. Control. Philosophical Transactions of the Royal Society London B. 327:1990;45-64
126. Zanker J.M. On the coordination of motor output during visual flight control in flies. Journal of Comparative Physiology A. 169:1991;127-134
127. Zanker J.M., Götz K.G. The wing beat of Drosophila melanogaster II. Dynamics. Philosophical Transactions of the Royal Society London B. 327:1990;19-44
128. Zbikowski R. On aerodynamic modelling of an insect-like flapping wing in hover for micro air vehicles. Philosophical Transactions of the Royal Society London A. 360:2002;273-290
129. Zeil J. Sexual dimorphism in the visual system of flies: the free flight behavior of male Bibionidae (Diptera). Journal of Comparative Physiology A. 150:1983;395-412
130. Zeil J. Sexual dimorphism in the visual system of flies: the compound eyes and neural superposition in Bibionidae (diptera). Journal of Comparative Physiology A. 150:1983;379-393