In this study, we have investigated how enhanced total flight force production compromises steering performance in tethered flying fruit flies, Drosophila melanogaster. The animals were flown in a closed-loop virtual-reality flight arena in which they modulated total flight force production in response to vertically oscillating visual patterns. By simultaneously measuring stroke amplitude and stroke frequency, we recorded the ability of each fly to modulate its wing kinematics at different levels of aerodynamic force production. At a flight force that exactly compensates body weight, the temporal deviations with which fruit flies vary their stroke amplitude and frequency are approximately 2.7 degrees and 4.8 Hz of their mean value, respectively. This variance in wing kinematics decreases with increasing flight force production, and at maximum force production fruit flies are restricted to a unique combination of stroke amplitude, stroke frequency and mean force coefficient. This collapse in the kinematic envelope during peak force production could greatly attenuate the manoeuvrability and stability of animals in free flight.

Bulthoff
H.
,
Poggio
T.
,
Wehrhahn
C.
(
1980
).
3-D-analysis of the flight trajectories of flies (Drosophila melanogaster).
Z. Naturforsch
35
,
811
–.
Dickinson
M.
(
1999
).
Haltere mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.
Phil. Trans. R. Soc. Lond
354
,
903
–.
Dickinson
M. H.
,
Lehmann
F.-O.
,
Götz
K. G.
(
1993
).
The active control of wing rotation by Drosophila.
J. Exp. Biol
182
,
173
–.
Dickinson
M. H.
,
Lehmann
F.-O.
,
Sane
S.
(
1999
).
Wing rotation and the aerodynamic basis of insect flight.
Science
284
,
1881
–.
Dudley
R.
(
1995
).
Extraordinary flight performance of orchid bees (Apidae: Euglossini) hovering in heliox (80% He/20% O2).
J. Exp. Biol
198
,
1065
–.
Ellington
C. P.
(
1984
).
The aerodynamics of insect flight. II. Morphological parameters.
Phil. Trans. R. Soc. Lond. B
305
,
17
–.
Ennos
A. R.
(
1989
).
The kinematics and aerodynamics of the free flight of some Diptera.
J. Exp. Biol
142
,
49
–.
Götz
K. G.
(
1968
).
Flight control in Drosophila by visual perception of motion.
Kybernetik
4
,
199
–.
Götz
K. G.
(
1987
).
Course control, metabolism and wingF.-O. LEHMANNANDM. H. DICKINSON635 Manoeuvrability in fruit flies interference during ultralong tethered flight in Drosophila melanogaster.
J. Exp. Biol
128
,
35
–.
Götz
K. G.
,
Hengstenberg
B.
,
Biesinger
R.
(
1979
).
Optomotor control of wing beat and body posture in Drosophila.
Biol. Cybernetics
35
,
101
–.
Heide
G.
,
Götz
K. G.
(
1996
).
Optomotor control of course and altitude in Drosophila is achieved by at least three pairs of flight steering muscles.
J. Exp. Biol
199
,
1711
–.
Hengstenberg
R.
(
1998
).
Controlling the fly's gyroscope.
Nature
392
,
757
–.
Hollick
F. S. J.
(
1940
).
The flight of the dipterous fly Muscina sabulans Fallen.
Phil. Trans. R. Soc. Lond. B
230
,
357
–.
Kirschfeld
K.
(
1967
).
Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca.
Exp. Brain Res
3
,
248
–.
Lehmann
F.-O.
,
Dickinson
M. H.
(
1998
).
The control of wing kinematics and flight forces in fruit flies (Drosophila spp .).
J. Exp. Biol
201
,
385
–.
Lehmann
F.-O.
,
Götz
K. G.
(
1996
).
Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster.
J. Comp. Physiol
179
,
311
–.
Marden
J.
(
1987
).
Maximum lift production during take-off in flying animals.
J. Exp. Biol
130
,
235
–.
Marden
J. H.
(
1989
).
Effects of load-lifting constraints on the mating system of a dance fly.
Ecology
70
,
496
–.
Marden
J. H.
,
Fitzhugh
G. H.
,
Wolf
M. R.
(
1998
).
From molecules to mating success: Integrative biology of muscle maturation in a dragonfly.
Am. Zool
38
,
528
–.
Nalbach
G.
(
1994
).
Extremely non-orthogonal axes in a sense organ for rotation: behavioral analysis of the dipteran haltere system.
Neuroscience
61
,
149
–.
Pringle
J. W. S.
(
1948
).
The gyroscopic mechanism of the halteres of Diptera.
Phil. Trans. R. Soc. Lond. B
233
,
347
–.
Roeder
K. D.
,
Treat
A. E.
(
1961
).
The detection and evasion of bats by moths.
Am. Sci
49
,
135
–.
Simon-Thomas
R. T.
,
Poorter
E. P. R.
(
1972
).
Notes on the behavior of males of Philanthus triangulum (F.) (Hymenoptera, Sphecidae).
Tijdschr. Ent
115
,
141
–.
Strohm
E.
,
Lechner
K.
(
2000
).
Male size does not affect territorial behaviour and life history traits in a sphecid wasp.
Anim. Behav
59
,
183
–.
Wagner
H.
(
1986
).
Flight performance and visual control of flight of the free-flying housefly (Musca domestica L.). II. Pursuit of targets.
Phil. Trans. R. Soc. Lond. B
312
,
553
–.
Wehrhahn
C.
,
Poggio
T.
,
Bulthoff
H.
(
1982
).
Tracking and chasing in house flies (Musca). An analysis of 3-D flight trajectories.
Biol. Cybernetics
45
,
123
–.
Zanker
J. M.
(
1990
).
The wing beat of Drosophila melanogaster. III. Control.
Phil. Trans. R. Soc. Lond. B
327
,
45
–.
Zanker
J. M.
,
Götz
K. G.
(
1990
).
The wing beat of Drosophila melanogaster. II. Dynamics.
Phil. Trans. R. Soc. Lond. B
327
,
19
–.
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