Biol. Rev. (2001), 76, pp.

449–471 " Cambridge Philosophical Society 449

DOI : 10.1017\S1464793101005759 Printed in the United Kingdom

Mechanics and aerodynamics of insect flight

control
GRAHAM K. TAYLOR
Department of Zoology, Oxford University, South Parks Road, Oxford, OX1 3PS, UK
(E-mail : graham.taylor!zoo.ox.ac.uk)

(Received 7 November 2000 ; revised 14 June 2001

ABSTRACT

Insects have evolved sophisticated flight control mechanisms permitting a remarkable range of manoeuvres.
Here, I present a qualitative analysis of insect flight control from the perspective of flight mechanics, drawing
upon both the neurophysiology and biomechanics literatures. The current literature does not permit a
formal, quantitative analysis of flight control, because the aerodynamic force systems that biologists have
measured have rarely been complete and the position of the centre of gravity has only been recorded in a
few studies. Treating the two best-known insect orders (Diptera and Orthoptera) separately from other
insects, I discuss the control mechanisms of different insects in detail. Recent experimental studies suggest
that the helicopter model of flight control proposed for Drosophila spp. may be better thought of as a
facultative strategy for flight control, rather than the fixed (albeit selected) constraint that it is usually
interpreted to be. On the other hand, the so-called ‘constant-lift reaction’ of locusts appears not to be a reflex
for maintaining constant lift at varying angles of attack, as is usually assumed, but rather a mechanism to
restore the insect to pitch equilibrium following a disturbance. Differences in the kinematic control
mechanisms used by the various insect orders are related to differences in the arrangement of the wings, the
construction of the flight motor and the unsteady mechanisms of lift production that are used. Since the
evolution of insect flight control is likely to have paralleled the evolutionary refinement of these unsteady
aerodynamic mechanisms, taxonomic differences in the kinematics of control could provide an assay of the
relative importance of different unsteady mechanisms. Although the control kinematics vary widely between
orders, the number of degrees of freedom that different insects can control will always be limited by the
number of independent control inputs that they use. Control of the moments about all three axes (as used
by most conventional aircraft) has only been proven for larger flies and dragonflies, but is likely to be
widespread in insects given the number of independent control inputs available to them. Unlike in
conventional aircraft, however, insects’ control inputs are likely to be highly non-orthogonal, and this will
tend to complicate the neural processing required to separate the various motions.

Key words : Insect flight control, steering, unsteady aerodynamics, kinematics, constant-lift reaction, turning,
manoeuvre.

CONTENTS

I. Introduction ............................................................................................................................ 450

II. Manoeuvre control versus reflex stabilisation ........................................................................... 451
III. General principles of control ................................................................................................... 452
IV. Flight control in Diptera (true flies)........................................................................................ 454
(1) Longitudinal control ......................................................................................................... 454
(2) Lateral control .................................................................................................................. 456
450 Graham K. Taylor

V. Flight control in Orthoptera (locusts and crickets) ................................................................. 459

(1) Longitudinal control ......................................................................................................... 459
(2) Lateral control .................................................................................................................. 460
VI. Flight control in other insects .................................................................................................. 461
(1) Longitudinal control ......................................................................................................... 461
(2) Lateral control .................................................................................................................. 463
VII. Discussion ................................................................................................................................ 463
(1) How many degrees of freedom do insects control?............................................................ 463
(2) Evolution of insect flight control systems .......................................................................... 466
VIII. Conclusions .............................................................................................................................. 467
IX. Acknowledgements .................................................................................................................. 467
X. References................................................................................................................................ 467

I. INTRODUCTION ematics with neurobiology and muscle mechanics

Insect flight control has been studied extensively
from a physiological perspective, but its mechanics
are less well known. Even where the kinematic
changes elicited by a given stimulus have been
defined, their consequences for aerodynamic force
production often remain obscure. Earlier work on
flight control was firmly rooted in the assumptions of
quasi-steady aerodynamics. However, since detailed
quasi-steady analyses and direct force measurements
(e.g. Weis-Fogh, 1973 ; Norberg, 1975 ; Cloupeau,
Devillers & Devezeaux, 1979 ; Ellington, 1984 c ;
Ennos, 1989 ; Dudley & Ellington, 1990 b ; Wilkin,
1990 ; Zanker & Go$ tz, 1990 ; Wilkin & Williams,
1993) indicate that aerodynamic force production in
insects generally relies upon unsteady mechanisms
(Willmott, Ellington & Thomas, 1997 ; Dickinson,
Lehmann & Sane, 1999), our understanding of
insect flight control must necessarily incorporate
unsteady effects. Although our understanding of
unsteady mechanisms is still very limited, more
recent experimental studies (Go$ tz, 1987 ; Dickinson,
Lehmann & Go$ tz, 1993 ; Dickinson, 1999 ; Dickinson
et al., 1999) have begun to investigate their role in
insect flight control.
An experimental approach integrating physio-
logical and mechanical observations is clearly de-
sirable. For example, although electromyographic
studies have demonstrated that migratory locusts
Locusta migratoria generate different motor patterns in
response to roll and yaw stimuli (Zarnack & Mo$ hl,
1977), they cannot tell us whether this is sufficient to
allow roll and yaw rotations to be produced
separately. This can only be resolved by directly
measuring the torques and forces that the insects
produce, or by analysing high-speed film of the
insects in flight. Although the current literature does
permit some synthesis of aerodynamics and kin-
(see Kammer, 1985 for a review of this type), I have
chosen to concentrate in detail upon the aero-
dynamics and kinematics of flight control. This
approach is similar to that of most texts on aircraft
flight mechanics (e.g. Nelson, 1989 ; Etkin & Reid,
1996 ; Cook, 1997 ; Vinh, 1993) in that it does not
complicate the discussion of flight dynamics with
details of the engineering mechanism that adjusts an
aircraft’s elevators or varies an insect’s wingbeat
frequency. Instead, I will concentrate upon how
different kinematic inputs affect the dependent
variables of position and velocity, as illustrated
schematically in Fig. 1. The more general question of
how many degrees of freedom insects can control is
one of the central issues of insect flight control and
will form the theme of this review.
The ‘ black box ’ between the inputs and outputs
of Fig. 1 is properly replaced by the equations of
motion for a flying body together with a system of
control inputs
e.g. stroke amplitude,
wingbeat frequency
position position
attitude acceleration attitude
angular acceleration
velocity velocity
angular angular
velocity velocity
Fig. 1. Block diagram illustrating the overall approach of
this review. The black box represents the equations of
motion for a flying body, together with a system of
transfer functions providing the mathematical relation-
ship between control inputs and their effects upon the
dependent variables.
Mechanics of insect flight control
transfer functions providing the mathematical re-
lationship between the control inputs and their
effects upon the dependent variables. I shall only be
discussing the mechanics of insect flight control in
qualitative terms, however, as the current literature
does not allow for even a formal static, let alone
dynamic, quantitative framework to be applied. The
reasons for this are best seen by considering the two
possible approaches to the quantitative analysis of
insect flight control. The first is to correlate free-
flight manoeuvres with observed changes in wing
kinematics. For example, Wakeling & Ellington
(1997) correlated velocity and flight force with
several basic kinematic parameters measured from
high-speed film of free-flying dragonflies. However,
the purpose of fitting regression lines in that study
was ‘ only to identify trends and not to estimate a
functional relationship ’ (Wakeling & Ellington,
1997, p. 566) and since the equations for the
regressions were not recorded, it is difficult to draw
any further quantitative conclusions. In any case,
accurately determining the three-dimensional wing
kinematics of even a stationary insect presents
formidable technical difficulties, and to do so during
free-flight manoeuvres is very difficult indeed.
An alternative approach is to measure directly the
forces and moments on tethered insects and to
correlate these with the observed changes in wing
kinematics. Unfortunately, although many studies
have measured selected forces and torques generated
by tethered insects, the resulting force systems are
rarely complete, in the sense of defining the point of
action, as well as the magnitude and direction, of the
resultant flight force. Only two published studies
(Hollick, 1940 ; Blondeau, 1981) appear to have
made the necessary measurements to determine the
point of action of the resultant flight force, yet this is
essential in determining the effect of a force, as any
child who has ever played on a see-saw will know.
The position of the centre of gravity has likewise
rarely been recorded, but is critical in determining
both the animal’s responsiveness to control inputs
and its characteristics of stability and equilibrium.
Its role in flight dynamics is analogous to that of the
fulcrum in a game of see-saw. For a full dynamic
analysis of insect flight control, it will be necessary
also to determine the insect’s moments of inertia.
The importance of the distribution of mass in
determining the envelope of insect flight control has
been emphasised by recent experimental work on
the flight performance of neotropical butterflies
(Srygley & Dudley, 1993 ; Srygley, 1994, 1999 ;
Srygley & Kingsolver, 2000). A more rigorous
451
experimental approach is clearly required before we
will make any further inroads towards a quantitative
analysis of insect flight control.
As a final caveat, it is worth emphasising that the
picture of insect flight mechanics portrayed in this
review is far from complete. For example, although
the open-loop conditions that are normally imposed
by tethering often lead to exaggerated turning
responses (Robert & Rowell, 1992 a), laboratory
experiments may not reveal the full gamut of control
responses used by insects flying under natural
conditions. Only where we can identify clear
physiological limits upon performance can we be
sure that we have correctly identified the boundary
of the flight envelope. As the quantity and detail of
experimental work on insect flight control improves,
our knowledge of insects’ flight envelopes looks
certain to expand.
II. MANOEUVRE CONTROL VERSUS REFLEX
STABILISATION
Insect control systems serve two discrete functions :
to allow controlled manoeuvres and to augment or
provide stability in the face of external (or possibly
internal) perturbations. Since stability will tend to
oppose both accidental and deliberate deviations
from steady flight, these two functions are expected
to be in direct conflict unless some mechanism is
present to bypass or desensitise the reflex stabilisation
system during manoeuvres. In the absence of such a
mechanism, the command to elicit a manoeuvre
would need to override any signals from the reflex
stabilisation system, presumably with a consequent
drop in nervous, if not also mechanical, efficiency.
From the viewpoint of enhancing manoeuvrability,
the potential temporarily to disable a reflex stabil-
isation system makes active control of stability
preferable to passive stability, which cannot gen-
erally be ‘ switched off ’. The impressive flight
envelopes of flies and other highly manoeuvrable
insects must reflect in large part a strong reliance
upon active, rather than passive, maintenance of
stability.
On the other hand, since active control may
augment, rather than completely replace, passive
stability, a brief discussion of the latter may be useful
in setting corrective flight control in context. The
first point to note is that hovering insects, like
hovering helicopters (Gessow & Amer, 1949 ;
Johnson, 1980 ; Padfield, 1996), possess no first-order
passive stability about any axis. This is because the
452 Graham K. Taylor

resultant flight force vector passes through the centre to maintain an acceptable level of dynamic stability.
of gravity at equilibrium and remains fixed in The same may be expected to be broadly true of
magnitude, position and direction with respect to flying insects. With these considerations in mind, I
the body axes as the insect’s orientation changes. will go on to consider some more general principles
The net turning moment on the insect is therefore of control.
always zero and a stabilising moment can only arise
through second-order changes in the aerodynamic
forces caused by translation of the insect as the flight
force is redirected with respect to gravity. This is the III. GENERAL PRINCIPLES OF CONTROL
means by which the dihedral of a fixed wing aircraft
provides roll stability, and it is possible that the We will begin by analogy with a more familiar
mean upward-canted coning angle of the wings of a control system. A car on a skidpan has three degrees
flapping insect could provide both pitch and roll of freedom. This is equivalent to saying that we need
stability in a similar way (Dudley, 2000). three pieces of information to completely describe its
The situation may be very different in forward position and orientation in space (for example, an x
flight, where a nose-up pitching disturbance will coordinate and a y coordinate for its position, and a
increase the angle of incidence of the wings, thereby compass bearing for its heading). To describe
increasing quasi-steady lift production. Provided this completely the motion of the system we would, of
additional lift acts behind the centre of gravity, this course, need also the first-order and second-order
will tend to generate a stabilising nose-down moment derivatives of the three positional degrees of freedom,
about the centre of gravity. Alternatively, if the but for simplicity we will only consider terms
mean flight force acts well above the centre of referring to position and orientation. By Newton’s
gravity, the insect will gain stability much like that second law, the application of a force or moment to
of a ship through a ‘ pendulum effect ’ (Lighthill, a mechanical system produces an acceleration or
1974). It is harder to predict how unsteady mech- angular acceleration of equivalent sense or direction
anisms of force production will affect stability. Some, that can be used to control position or orientation.
like Weis-Fogh’s (1973) ‘ clap-and-fling ’ and its Hence, the number of controlled degrees of freedom
derivatives (Ellington, 1984 b) or generation of a cannot exceed the number of independent control
circulation via wing rotation (Ellington, 1984 b ;
Dickinson et al., 1999), are unlikely to be greatly
roll pitch
affected by changes in the insect’s orientation, and
are therefore unlikely to provide any passive stab-
ility. On the other hand, translational mechanisms,
such as the maintenance of a leading edge vortex
(Ellington, 1984 b ; Dickinson, and Go$ tz, 1993 ;
Ellington et al., 1996 ; Willmott et al., 1997),
effectively magnify the wing lift coefficients and will
therefore tend to enhance any passive stability or
instability that would be present if the flow were
quasi-steady (G. K. Taylor & A. L. R. Thomas, in
preparation).
In the absence of detailed empirical data on the
passive stability of insects, it is difficult to make any
reliable predictions about how reflex stabilisation
yaw
and passive control will interact. Suffice it to say that
active control may be required to provide not just
static stability, in the sense of returning the insect
towards equilibrium immediately following a dis- Fig. 2. A flying insect, like this hummingbird hawkmoth
turbance, but also dynamic stability, in the sense of Macroglossum stellatarum, has six degrees of freedom. The
damping out any oscillatory modes that may be insect is free to move in translation along or rotate about
excited by a disturbance. For example, most aircraft three orthogonal axes, centred upon the centre of gravity
possess some degree of passive static stability, but (part-filled circle). Rotations about these axes are termed
pilot or computer control input is generally required pitch, roll and yaw.
Mechanics of insect flight control
inputs. This is the first and most fundamental
principle of control.
Our second principle is that it is often unnecessary
(or even undesirable) to control all of the possible
degrees of freedom. For example, a car gives its
driver control of just two of its three degrees of
freedom, making it easier to keep on the road, but
somewhat harder to parallel park. Our third
principle is that one or more redundant control
inputs can often be used to provide enhanced control
of a given degree of freedom. For example, easing off
a car’s accelerator has the same qualitative effect as
braking, but most of us would find it difficult to stop
at traffic lights without the aid of brakes.
Such considerations allow us to frame two over-
arching questions that we may ask of insect flight
control. How many independent control inputs does
the insect use? How many degrees of freedom does
this allow the insect to control? Independent control
of all six of an insect’s degrees of freedom (Fig. 2)
would require a minimum of six independent control
inputs. Full six-degree-of-freedom control is super-
fluous in most aerial applications and appears not to
be used by insects, which lack the ability to fly
sideways without banking. In fact, for control of
position in space, independent modulation of pitch,
heading and longitudinal acceleration will suffice,
requiring just three independent control inputs.
Two-axis control systems like these are a feature of
some high-performance model sailplanes and could
be used by insects with no great need for manoeuvra-
bility.
Three-axis control systems permit independent
modulation of pitch, roll and yaw and thus enable a
far wider range of manoeuvres. Depending upon
whether the direction as well as the magnitude of
longitudinal acceleration can be varied independent
of pitch, three-axis control systems require a mini-
mum of either four or five independent control
inputs. In fixed-wing aircraft and helicopters, the
direction of longitudinal acceleration is normally
dependent upon pitch, although flaps may be used
to steepen a descent without upsetting pitch equi-
librium. Amongst operational aircraft, perhaps only
the Harrier jump jet can be considered to possess
complete five-degree-of-freedom control in the sense
of being able to accelerate at any angle to the ground
without varying pitch. However, whereas five-
degree-of-freedom control is the exception in aircraft
and four-degree-of-freedom control the rule, the
opposite may be the case in insects with three-axis
control because of important differences in the
mechanisms by which control inputs are produced.
453
Fig. 3. Conventional aircraft use mechanically separate
control surfaces (shaded) to separate control of the three
moments. In the simple system shown here, the tail
elevators are used to control pitch, the ailerons to control
roll, and the rudder to control yaw. Insects lack separate
control surfaces and must instead use different rotations of
the wings to separate the moments.
Early experiments in wing warping aside, the
conventional aircraft design paradigm has long been
to use separate control surfaces to isolate pitch, roll
and yaw (Fig. 3). This differs markedly from the
control systems of insects in which the same
kinematic parameters are varied symmetrically for
control of the longitudinal forces and moments, and
asymmetrically for control of the lateral forces and
moments. For example, in locusts, pronation (nose-
down rotation of the wing at the top of the stroke) is
increased symmetrically between the forewings in
response to a nose-up pitching disturbance, but is
only increased on the inside forewing during turns
(Gettrup & Wilson, 1964). The result is an effective
doubling of the number of control inputs and a
remarkable economy of control. It follows that
insects that modulate the direction of longitudinal
acceleration by symmetrically varying the balance of
lift and thrust on their wings should also be able to
separate roll and yaw by varying the same kinematic
parameters asymmetrically. Conversely, insects that
modulate roll via asymmetric lift production, and
yaw via asymmetric thrust production, should also
be able to modulate the direction of longitudinal
acceleration to some degree. Hence, we would expect
many insects using three-axis control to modulate
motions in five, rather than four, of their six degrees
of freedom, although this is not to say that all
combinations of these motions will be possible.
454
Having considered some general principles of
control, I will now go on to apply these specifically
to insects. Although insect flight control has only
been studied in detail in two orders (Diptera and
Orthoptera), there are major systematic differences
in the mechanics of control. These relate primarily to
differences in the construction of the flight motor
and the arrangement of the wings and to probable
differences in the unsteady mechanisms of aero-
dynamic force production used. I will therefore
consider each of the different orders in turn, treating
lateral and longitudinal control separately.
IV. FLIGHT CONTROL IN DIPTERA (TRUE
FLIES)
Flies are the most aerobatic of insects, able to turn on
a pinpoint, fly sideways and even land upside-down
on a ceiling (Kammer, 1985), but since they possess
just one pair of wings the mechanics of their flight
control should be amongst the simplest to under-
stand. Specifically, there can be no question of
interference between the fore- and hindwings, or of a
changing balance of forces between the two. Flies
exhibit two main classes of manoeuvre : fast, vol-
untary, turns, known as saccades because of their
kinematic resemblance to the tracking movements of
vertebrate eyes, and slower, often corrective, turns
under the influence of the optomotor control system.
Other classes of turn have been also recorded, often
as pursuit responses by courting males. For example,
dolichopodid flies Poecilobothrus nobilitatus have been
filmed executing 180m yaw turns in less than 40 ms
during courtship (Land, 1993). Hovering male
tabanid flies Hybomitra hinei have even been recorded
using a modified form of the Immelmann turn – a
classic aerobatic manoeuvre consisting of a half-loop
followed by a half-roll, used to effect rapid reversals
of flight direction (Wilkerson & Butler, 1984).
Throughout this review I will be presenting results
relating to both voluntary and corrective control,
and it should be borne in mind that control inputs
that are suitable for one type of control may not be
suitable for the other, especially where the speed of
the motion is very different.
(1) Longitudinal control
Stroke amplitude – the angle of the planar arc or
great circle described by the wing leading edge
between the top and bottom of the stroke (Fig.
Graham K. Taylor
A B
stroke plane
stroke plane
Fig. 4. (A, B). Stroke amplitude is the planar angle of the
arc described by the wing leading edge between the top
and bottom of the stroke (dotted line in column A).
Column B shows the corresponding points of action of the
mean flight force. Decreasing the stroke amplitude
(bottom row) causes the flight force to shift back,
generating a nose-down pitching moment about the
centre of gravity (part-filled circle).
4A) – is normally considered the main control
parameter determining aerodynamic power output
in fruit flies Drosophila spp. Stroke amplitude shows a
strong positive correlation with aerodynamic force
production (Vogel, 1967 ; Go$ tz, 1968 ; Lehman &
Dickinson, 1997 ; Dickinson, Lehmann & Chan,
1998) and is referred to as stroke angle in some
studies. Wingbeat frequency is the other principal
determinant of aerodynamic power output, and
appears to be an important control parameter in flies
(Dickinson et al., 1998). For example, Drosophila
melanogaster increase their wingbeat frequency in
response to an increase in the speed of optic flow
simulating forward flight (Friedrich, Spatz &
Bausenwein, 1994).
In Drosophila melanogaster, wingbeat frequency is
positively correlated with aerodynamic force below
approximately the force required to support body
weight, but is negatively correlated with aerody-
namic force at peak outputs (Lehmann & Dickinson,
1997). Decreases in wingbeat frequency appear to be
compensated by steeper increases in stroke am-
plitude, however, and the product of frequency and
Mechanics of insect flight control
amplitude (which determines the translational vel-
ocity of the wing) rises linearly with increasing force
production (Lehmann & Dickinson, 1997). The
drop in wingbeat frequency at peak force production
may result from physiological constraints, so stroke
amplitude and wingbeat frequency are probably not
strictly independent control inputs, even though
they are not coupled in a straightforward fashion. At
peak levels of force production, D. melanogaster
appear to be limited to a unique combination of
stroke amplitude, wingbeat frequency and flight
force coefficient, and this in turn constrains their
ability to generate the asymmetries in force pro-
duction necessary for lateral control (Lehmann &
Dickinson, 2001). An analogous degradation of
turning ability with increasing flight speed was
found by Buelthoff, Poggio & Werhahn (1980), who
found the maximum angular velocity attained by
free-flying D. melanogaster to decrease with increasing
forward velocity, although in this case the effect is
likely to result from aerodynamic, rather than
physiological, constraints.
In larger calypterate flies (blowflies, houseflies,
etc.), frequency and amplitude are both positively
correlated with aerodynamic force, but since the two
parameters are likely to be mechanically linked, it is
not necessarily easy to separate cause from effect
(Nachtigall & Wilson, 1967). Symmetrical changes
in stroke amplitude are also correlated with cor-
rective pitch control in larger flies such as Muscina
stabulans and Calliphora erythrocephala, which decrease
the amplitude of both wings in response to an
increase in body angle (Hollick, 1940 ; Nalbach &
Hengstenberg, 1994). Changes in amplitude are
effected by adjusting the lower turning point of the
wings, which shifts back with a decrease in amplitude
as the wings sweep less far forward on the down-
stroke. This causes the point of action of the mean
flight force to shift back (Fig. 4B), generating a
pitching moment with the fly’s weight of appropriate
direction to restore it to equilibrium (Hollick, 1940).
Similar, albeit smaller, changes in stroke amplitude
are observed during pitching responses in Drosophila
spp. (Zanker, 1988 b, 1990), which may use a similar
mechanism for pitch control (Vogel, 1967). How-
ever, the smaller magnitude of the response is
suggestive of a slightly different mechanism. A
prominent feature of unsteady lift-production in
Drosophila spp., at least in tethered flight, is the clap-
and-peel process in which the opening wings draw
additional air into the circulation at the start of the
downstroke (see Ellington, 1984 a, b). The extent of
contact between the wings increases with increasing
455
stroke amplitude, which should increase lift and
thrust production dorsally, inducing a restoring
nose-up torque in response to nose-down stimuli
(Zanker, 1990).
Drosophila melanogaster are also able to vary the
longitudinal position of the stroke plane independent
of amplitude (Zanker, 1988 b), which should allow
pitch to be modulated independent of aerodynamic
force output. Similar shifts in stroke plane position
have also been observed in the hoverflies Eristalis
tenax and Episyrphus balteatus (Ellington, 1984 a).
Stroke plane inclination varies too during pitching
responses in Drosophila spp., but this is tightly
correlated with changes in amplitude, which cause
the lower turning point to move almost horizontally,
rather than parallel to the stroke plane, thereby
altering stroke inclination (Vogel, 1967 ; Zanker,
1988 b). Drosophila spp. do not seem to vary the angle
of attack of the wings for longitudinal control (Vogel,
1967), although the constancy of the angle of attack
suggests that they might actively stabilise it at
different speeds (Zanker, 1990). The speed and
timing of wing rotation do appear to be important
lateral control parameters in D. melanogaster (Zanker,
1990 ; Dickinson et al., 1993), but have not been
investigated in the context of longitudinal control.
In addition to varying their wing kinematics, flies
may control pitch by varying their posture, much
like a hang-glider pilot. Drosophila melanogaster elevate
their abdomen in response to nose-down disturb-
ances (Zanker, 1988 a, b), displacing the centre of
gravity dorsal to the line of thrust, which therefore
generates a restoring nose-up moment with the fly’s
inertia. The concurrent increase in drag on the
dorsal side will further add to this torque (Zanker,
1988 b). Similar postural changes have been observed
in Calliphora erythrocephala (Nalbach & Hengstenberg,
1994), so abdominal deflection may be a widespread
mechanism of pitch control in flies. Drosophila virilis
have also been observed to elevate their hindlegs
following a nose-down disturbance, which should
increase drag dorsally and generate a nose-up
pitching moment (Vogel, 1967). The raised hindlegs
can hardly fail to meet with interference from the
wake of the wings, and this could enhance their
turning effect in much the same way that a ship’s
rudder is more effective if placed in the wake of the
propeller (Vogel, 1967).
The various kinematic and postural changes
described above are only sufficient to provide two
degrees of freedom for longitudinal control, since
none of them permits control of the direction of the
resultant flight force relative to the body axes. This
456
would result in essentially the same situation as in
helicopters, in which the direction of the rotor force
is fixed with respect to the body. Hence, although a
hovering helicopter’s vertical displacement can be
controlled directly by varying the aerodynamic force
on the blades, it can only be given horizontal
velocity by changing the body angle to redirect the
flight force forward (e.g. Johnson, 1980). This does
in fact appear to be the mechanism by which
Drosophila spp. normally control their trajectory
(Vogel, 1966 ; David, 1985 ; Zanker, 1988 b), since
the elevation of the aerodynamic force is apparently
kept fixed relative to the body axes (Vogel, 1966 ;
Go$ tz, 1968 ; David, 1978 ; Go$ tz & Wandel, 1984 ;
but see Ennos, 1989). The relative proportions of lift
and thrust are thus varied primarily by adjusting the
body angle (David, 1985 ; Zanker, 1988 b), which is
negatively correlated with flight speed (Vogel, 1966 ;
David, 1978) to allow level flight to be maintained as
aerodynamic power output is increased. However,
the fact that Drosophila spp. normally modulate lift
and thrust together need not imply that they are
strictly coupled as in helicopters, and the helicopter
model may perhaps be better thought of as a
facultative strategy for flight control rather than as a
fixed constraint.
Similar results have been reported for tethered
houseflies Musca domestica flying in still air (Go$ tz &
Wandel, 1984), but the generality of this result is
questionable because M. domestica does not hover
(Wagner, 1986) and a flow of air over the antennae
is necessary for a normal stroke path in Muscina
stabulans (Hollick, 1940). Free-flying M. domestica do
appear to be able to vary the direction of the flight
force vector, but only within a limited range
(Wagner, 1986). Force measurements in tethered
Calliphora spp. have confirmed that they also are able
to modulate thrust independent of lift within a
certain range (Blondeau, 1981, Nachtigall & Roth,
1983), although the relation may be asymmetric
because lift appears never to be modulated in-
dependent of thrust (Blondeau, 1981).
Any ability to alter the direction of the flight force
independent of its magnitude implies that some
other kinematic parameter must be varied inde-
pendent of stroke amplitude and wingbeat fre-
quency, which together provide control of only the
magnitude of the flight force, albeit with an element
of redundancy. Changes in stroke plane inclination
will certainly alter the direction of the resultant
flight force, and would almost certainly affect the
forces generated by wake capture mechanisms in
which the wings gain an additional ‘ kick ’ from
Graham K. Taylor
vortices shed at the end of the previous half-stroke
(see Dickinson et al., 1999). This is one potential
mechanism by which larger flies could vary the
direction of the flight force. Changes in stroke plane
inclination observed in Drosophila melanogaster are
probably too small to be used for control purposes
( 0n5m ; Zanker, 1988 b), and being linked to
changes in stroke amplitude should probably not be
counted as a separate control input anyway. Other
kinematic parameters have not been investigated in
the context of longitudinal control, but since longi-
tudinal forces and moments can be produced by
symmetrically adjusting parameters used for lateral
control, we will consider other potential candidates
in the context of lateral control.
(2) Lateral control
Although changes in wing kinematics are likely to be
more important for fast flight manoeuvres, postural
adjustments are commonly associated with slow
optomotor steering responses in flies (Zanker,
1988 a). Typically, the abdomen is deflected into a
turn (Go$ tz, Hengstenberg & Biesinger, 1979 ;
Zanker, 1988 a ; Zanker, Egelhaaf & Warzecha,
1991), often together with the inside hindleg
(Hollick, 1940 ; Faust, 1952 ; Nachtigall & Roth,
1983 ; Nalbach, 1989). Occasionally both hindlegs
are extended together into the turn (Go$ tz et al.,
1979). Similar adjustments in locusts have been
interpreted as producing drag-based yaw torques
like a ship’s rudder (Camhi, 1970) and most workers
have followed the same interpretation for flies (e.g.
Go$ tz et al., 1979). Postural adjustments in other
insects have been suggested to produce lateral
moments by a different mechanism, shifting the
centre of gravity sideways from the centre of pressure
(Govind & Burton, 1970 ; May & Hoy, 1990 a). This
would normally be expected to generate a roll rather
than a yaw torque, but abdominal deflections in
Drosophila melanogaster do appear to generate yaw
torques gravimetrically (Zanker, 1988 a). This is
because the axis about which yawing occurs is tilted
back approximately 30m from the vertical such that
a significant component of the animal’s weight acts
normal to the yaw axis and can therefore produce a
yaw couple with the flight force.
Until recently, stroke amplitude was thought to be
the only kinematic parameter consistently correlated
with roll and yaw responses in flies (Drosophila spp. :
Vogel, 1967 ; Go$ tz, 1968 ; Go$ tz et al., 1979, Musca
domestica : Srinivasan, 1977, Calliphora spp. : Heide,
1971 ; Nachtigall & Roth, 1983 ; Hengstenberg,
Mechanics of insect flight control
Sandeman & Hengstenberg, 1986 ; Nalbach, 1989 ;
Nalbach & Hengstenberg, 1994). According to the
classical interpretation, the amplitude of the inside
wing is lowered to reduce the aerodynamic force by
shortening the stroke, with opposite changes oc-
curring on the outside wing. This will generate
rolling moments directly through asymmetric lift
production and should also generate yaw moments
directly through asymmetric thrust production.
Since flying insects usually produce much less thrust
than lift (typically an order of magnitude less in
Drosophila virilis ; Vogel, 1966), the resulting torques
about the yaw axis would normally be expected to
be correspondingly small compared to those in roll.
Although this classical view was originally rooted
in the assumptions of quasi-steady aerodynamics, the
outcome could be the same for an unsteady
translational mechanism such as delayed stall, in
which flow remains attached to the wing at higher
angles of attack than would be possible under steady
conditions. Hence, although control torques meas-
ured in Drosophila melanogaster are generally greater
than those calculated from blade-element theory,
which assumes quasi-steady aerodynamics (Zanker,
1990 ; Zanker & Go$ tz, 1990), stroke amplitude could
still play a direct role in dipteran flight control if
unsteady translational mechanisms were important.
Dickinson et al.’s (1993) comment that changes in
amplitude may not be directly responsible for
turning in D. melanogaster (on the grounds that
correlated changes in the timing of stroke reversal
will be more important than stroke length per se if
unsteady rotational mechanisms overwhelm quasi-
steady lift production) implicitly assumes that
unsteady translational mechanisms (which also have
the potential to overwhelm quasi-steady lift pro-
duction) are insignificant.
Changes in amplitude do not permit the direction
of the flight force to be varied directly, unless the
part of the stroke that is curtailed generates a force
in a different direction to the remainder of the
stroke. In general, since rolling moments are nor-
mally generated by asymmetric lift and yawing
moments by asymmetric thrust, separate control of
lift and thrust will usually be required for roll and
yaw to be varied independently. Roll and yaw have
therefore been suggested to be unavoidably coupled
in Drosophila spp. (Srinivasan, 1977), which normally
modulate lift and thrust together. To conclude that
Drosophila spp. are unable to uncouple lift and thrust
would seem premature, however, and although
direct evidence that Drosophila spp. modulate roll
and yaw independently is still lacking (Dickinson,
457
1999), the view that they are strictly coupled has
begun to be challenged (Go$ tz, 1987 ; Ennos, 1989 ;
Zanker, 1990 ; Dickinson et al., 1993). In any case,
varying the relative proportions of lift and thrust
independently on each wing is not the only way to
generate a yaw torque. For example, the clap-and-
peel process does not occur parallel to the sagittal
plane during fictive turns in Drosophila melanogaster,
and the jet of air produced is in the appropriate
direction to contribute to steering (Go$ tz, 1987 ;
Zanker, 1990). This could allow yaw moments to be
generated independent of roll, although the torques
generated in this way may still be rather small
(Dickinson et al., 1993 ; Dickinson, 1999).
Larger flies such as Calliphora spp. (Blondeau,
1981 ; Schilstra & Van Hateren, 1999) and Musca
domestica (Wagner, 1986) can certainly generate roll
and yaw torques separately, though the two are
usually modulated together to produce a banked
turn (Blondeau, 1981). This presumably increases
manoeuvrability in the same way as in a turning
aircraft, by minimising sideslip and directing the
nose into the turn. Sometimes, it may be useful to
swing sideways without changing heading. Heli-
copters achieve this by banking to one side to
redirect a component of the flight force sideways.
This is probably also the mechanism behind Collett
& Land’s (1975) observation that the hoverfly Syritta
pipiens can fly sideways without changing its heading.
This implies that hoverflies must also possess in-
dependent control of roll and yaw. At least one other
kinematic parameter must be varied in addition to
stroke amplitude for roll and yaw to be controlled
separately, because abdominal deflection occurs too
slowly to account for the rapid turns observed in
flies. For example, in Drosophila melanogaster the
abdomen only responds strongly to oscillating visual
stimuli at frequencies below 5 Hz, and the response
is much stronger at lower frequencies (Zanker,
1988 a). Peak deflection is only attained at 0n05 Hz,
suggesting that the response may be used to correct
for inherent asymmetries in the wings or flight
motor, rather than discrete disturbances (Zanker,
1988 a).
Wingbeat frequency can immediately be ruled out
as a lateral control parameter because the con-
struction of the dipteran flight motor makes it im-
possible for the wings to operate at different
frequencies (Hollick, 1940). Stroke plane inclination
also appears not to offer an independent control
input because it is closely linked to amplitude in
most studies in which both have been measured
(Vogel, 1967 ; Nachtigall & Roth, 1983 ; Zanker,
458
1988 b, see also Chadwick, 1951). For example, in
Calliphora vicina the action of the basalar muscles has
been shown explicitly to determine both stroke plane
inclination and amplitude (Tu & Dickinson, 1996).
However, the precise three-dimensional trajectory of
the wingtip can be varied independently of am-
plitude in Muscina stabulans (Hollick, 1940) and C.
vicina (Tu & Dickinson, 1996), and this might be
used to produce control moments, perhaps by
altering the properties of wake capture. One wing
may even be completely folded over the body during
extremely fast turns (Nachtigall & Wilson, 1967),
although this is unlikely to play any role in
correctional steering.
Increased pronation of the inside wing has been
observed during roll and yaw responses in Calliphora
erythrocephala (Faust, 1952 ; Hengstenberg et al.,
1986). Similar changes in pronation have been noted
in the cranefly Tipula oleracea (Faust, 1952) and the
blowfly Lucilia serricata (Sandeman, 1980). Unfortun-
ately, the stage of wingbeat recorded was almost
certainly wrongly described in the latter study (D. C.
Sandeman, pers. comm., cited in Kammer, 1985)
and it is not clear whether the magnitude or only the
timing of rotation was varied. Angle of attack
asymmetries are taken to an extreme in the doli-
chopodid fly Poecilobothrus nobilitatus, which is able to
execute extraordinarily rapid 180m turns by holding
the inside wing normal to the flow to act as an
airbrake (Land, 1993).
In light of current views of insect flight control
implicating unsteady aerodynamic mechanisms as
the main source of control moments (Zanker, 1990),
the speed and timing of wing rotation are likely to be
at least as important as the degree of pronation
(Ennos, 1989 ; Dickinson et al., 1993, 1999 ;
Dickinson, 1994, 1999). Supination (nose-up ro-
tation of the wings towards the bottom of the stroke)
occurs extremely rapidly in flies (Ennos, 1989). Flow
visualisation of tethered Drosophila melanogaster
(Dickinson & Go$ tz, 1996) appears to show the
vorticity produced by the so-called ‘ ventral flip ’
(Dickinson et al., 1993) fusing with the stopping
vortices shed at the end of the downstroke, so rapid
wing rotation might be used for aerodynamic force
production. Experiments with model wings (Dickin-
son, 1994 ; Dickinson et al., 1999) have demonstrated
that the timing of supination relative to stroke
reversal (the point at which wing translation reverses
direction) is critical in determining the magnitude of
the forces produced. Large positive forces (attribu-
table to both rotational mechanisms and wake
capture) are generated when supination precedes
Graham K. Taylor
stroke reversal, whereas negative forces are registered
if supination is delayed (Dickinson et al., 1999).
By asymmetrically varying force production in
this way, flies could readily produce turning
moments for control. For example, the results of
Dickinson et al. (1999) indicate that the instan-
taneous drag force may be extremely high on a wing
using rotational circulation and wake capture, and
well in excess of the instantaneous lift. Hence,
though the instantaneous drag forces largely cancel
over the course of a normal stroke, asymmetric drag
production offers a potent means of generating roll
or yaw torques in insects using rotational circulation
and wake capture. The direction of the axis about
which the resulting torque is generated will depend
upon both the direction of the stroke and the
orientation of the wing chord. For example, in
insects with a horizontal stroke plane, such as
hoverflies, the potential to vary the horizontal force
component may be far greater than the potential to
vary the vertical lift. Asymmetric variation of the
forces produced by rotational circulation and wake
capture would then tend to generate a yaw torque,
and this may account for the remarkable ability of
hoverflies to turn full circle whilst otherwise re-
maining stationary.
In Calliphora erythrocephala (Nalbach, 1989) and
Drosophila melanogaster (Dickinson et al., 1993), su-
pination is delayed on the inside wing and advanced
on the outside wing during fictive turns. Parallel
changes in the timing of pronation have also been
observed (Nalbach, 1989). Unfortunately, it has not
been possible to resolve changes in the timing of
stroke reversal, so the phase of supination and stroke
reversal remains unknown. However, assuming that
an absolute delay in supination on the inside of a
turn indicates that supination is also delayed relative
to stroke reversal, then the results of Dickinson et al.
(1999) imply that the flight force will be reduced or
reversed on the inside of a turn. Earlier supination is
also correlated with increased rotational velocity in
D. melanogaster (Dickinson et al., 1993, see also
Zanker, 1990), which should increase aerodynamic
force production on the outside of a turn. Both effects
should combine synergistically to produce a torque
in the correct direction to steer into the turn.
The timing of supination seems to be independent
of stroke amplitude in Drosophila melanogaster, even
though the two are usually modulated together
(Dickinson et al., 1993). Changes in stroke amplitude
and the timing of supination could therefore provide
the two inputs necessary to separate control of roll
and yaw. Alternatively, changes in stroke amplitude
Mechanics of insect flight control
might not effect steering directly, but could instead
effect steering indirectly through correlated changes
in the timing of stroke reversal (Dickinson et al.,
1993). However, since it is the relative timing of
supination and stroke reversal that primarily deter-
mines aerodynamic force output, changes in stroke
amplitude and the timing of supination would then
combine together to provide a single composite
variable, which would make changes in stroke
amplitude redundant. In this case, some other
independent control input (e.g. the speed of wing
rotation) would still be required to separate control
of roll and yaw. It therefore seems likely that stroke
length per se could be an important control par-
ameter, at least in larger flies in which roll and yaw
are known to be controlled separately.
Returning briefly to longitudinal control, sym-
metric changes in the speed or timing of supination
could be used to vary the magnitude of the resultant
flight force (Dickinson et al., 1999). Changes in the
timing of wing rotation might also provide the
additional control input required to separate control
of lift and thrust. Symmetric adjustment of the
ventral flip could certainly enhance the pitching
responses discussed in the previous section, because
the lever arm at the end of the downstroke will
usually be such that even small changes in the
rotational forces will generate a large pitching
moment. Finally, some control over the direction of
vortex shedding would permit an even greater degree
of control of the direction of the resultant flight force
(Ellington, 1984 b ; Dickinson et al., 1993).
V. FLIGHT CONTROL IN ORTHOPTERA
(LOCUSTS AND CRICKETS)
(1) Longitudinal control
Flight control in locusts is likely to be complicated by
the interaction of flow over the fore- and hindwings,
though some common principles remain. As in flies,
stroke amplitude and wingbeat frequency are posi-
tively correlated with aerodynamic force and flying
speed in tethered Locusta migratoria able to control
their own speed relative to the surrounding air
(Gewecke, 1975 ; Kutsch & Gewecke, 1979). Teth-
ered L. migratoria also increase their wingbeat
frequency in response to an increase in the speed of
optic flow simulating forward flight (Baader, Scha$ fer
& Rowell, 1992) and the same qualitative re-
lationship between wingbeat frequency and flight
speed has been shown in free-flying L. migratoria
459
(Baker, Gewecke & Cooter, 1981). Moreover, stroke
amplitude and wingbeat frequency are negatively
correlated in tethered L. migratoria stimulated by air
currents of fixed speeds (Gewecke, 1970, 1972), so
the two must also be able to be varied independently.
Locusts appear to regulate lift independent of
thrust and have also been claimed to exhibit a
‘ constant-lift reaction ’ (Wilson & Weis-Fogh, 1962)
in which the vertical component of force is kept more
or less constant following imposed changes of body
angle of up to 20m (Weis-Fogh, 1956 a, b ; Gewecke,
1975). Electrophysiological (Wilson & Weis-Fogh,
1962 ; Gettrup, 1966 ; Zarnack & Mo$ hl, 1977) and
kinematic studies (Gettrup & Wilson, 1964 ; Gettrup,
1966 ; Wortmann & Zarnack, 1993) have clearly
demonstrated that tethered locusts increase forewing
pronation to compensate for the increase in their
angle of attack that would otherwise occur following
a nose-up disturbance. The same reaction also
appears to occur in free flight, since climbing flight is
associated with both increased forewing pronation
and increased body angle (Fischer & Kutsch, 2000).
Hindwing pronation is largely independent of body
angle (Gettrup & Wilson, 1964 ; Wortmann &
Zarnack, 1993), however, so whereas the forewing
lift coefficients should remain approximately con-
stant, the hindwing lift should increase with in-
creasing body angle, because the lift on a wing
generally increases with increasing angle of attack.
According to Gettrup & Wilson’s (1964) model of
the constant-lift reaction, the drop in flight speed
that accompanies an increase in body angle in
tethered locusts (Weis-Fogh, 1956 a ; Gewecke, 1975)
combines with these changes to keep the total lift
approximately constant.
The constant-lift reaction has been an influential
paradigm in the insect flight literature, and is still
referred to frequently in discussions of insect flight
control (e.g. Zanker, 1990). However, quite apart
from the objection that the quasi-steady aerody-
namics implicit in Gettrup & Wilson’s (1964) model
have been shown not to apply in locusts (Cloupeau
et al., 1979 ; Wilkin, 1990), it is not clear why free-
flying locusts should possess a reflex maintaining
constant lift at widely different body angles. A
stabilising pitch reflex would seem to be of far
greater utility. Studies of free-flying locusts (Baker et
al., 1981) are consistent with the existence of a
stabilising pitch reaction, showing no evidence of the
negative correlation between body angle and flight
speed that forms an essential part of Gettrup &
Wilson’s (1964) original scheme. Moreover, later
studies (Zarnack & Wortmann, 1989 ; Wortmann &
460
Zarnack, 1993) have cast doubt on the existence of a
constant-lift reaction per se, finding no reliable
evidence that individual locusts consistently main-
tain constant lift at different body angles. Although
constant lift may occasionally be maintained, there
is usually considerable temporal variation in lift
production (Zarnack & Wortmann, 1989). Weis-
Fogh’s (1956 a, b) original studies neglected temporal
variation in lift and were based upon data averaged
across individuals, so the apparent constancy of lift
in his figures would certainly have been exaggerated
by the averaging process.
On the other hand, given that the angle of attack
of the hindwings increases following an increase in
body angle, whilst the angle of attack of the forewings
remains approximately constant, the changing bal-
ance of lift between fore- and hindwings should
produce a restoring nose-down pitching moment.
Such a torque was in fact detected by Gettrup &
Wilson (1964), but was considered to be an
‘ unpredicted outcome ’ (Gettrup & Wilson, 1964, p.
189) of the constant-lift reaction. This interpretation
almost certainly reverses cause and effect, since a
stabilising pitch response would negate any re-
quirement to maintain constant lift across a range of
body angles by restoring the animal to equilibrium.
Indeed, loss of the sensory input supposed to mediate
pronation in the constant-lift reaction leads to a
complete loss of stability (Gettrup, 1966), confirming
that the reflex changes in pronation described above
are used to maintain pitch stability. Constant lift
may occasionally be maintained in tethered locusts
according to Gettrup & Wilson’s (1964) original
scheme, but probably as an epiphenomenon of
changes adapted to restore pitch equilibrium in free
flight.
(2) Lateral control
Locusts swing their abdomen laterally and extend
one or both hindlegs like a rudder during yaw turns
(Gettrup & Wilson, 1964 ; Dugard, 1967 ; Camhi,
1970 ; Cooter, 1979 ; Arbas, 1986 ; Baader, 1990 ;
Preiss & Gewecke, 1991 ; Robert & Rowell, 1992 a, b ;
Robertson & Reye, 1992 ; Preiss & Spork, 1993 ;
Robertson & Johnson, 1993 ; Lorez, 1995 ; Robert-
son, Kuhnert & Dawson, 1996 ; Dawson et al., 1997).
Such postural changes are not always observed
during correctional responses, however, and may be
more important during voluntary turns (Zarnack &
Mo$ hl, 1977 ; Gewecke & Philippen, 1978). Similar
postural changes have been observed in the bush-
cricket Tettigonia viridissima (Schulze & Schul, 2001)
Graham K. Taylor
and the cricket Teleogryllus oceanicus during acoustic
avoidance responses (Moiseff, Pollack & Hoy, 1978 ;
Pollack & Hoy, 1981 ; Pollack, Huber & Weber,
1984 ; Miles et al., 1992), although abdominal
deflection alone is apparently insufficient to produce
yawing in T. oceanicus (May & Hoy, 1990 b). As well
as increasing drag on the inside of a turn, hindleg
extension may effect a turn by impeding the motion
of the inside hindwing (Camhi, 1970 ; May & Hoy,
1990 a). This mechanism would be expected to cause
significant wear to the wing and may therefore be
reserved for extreme avoidance manoeuvres.
Lateral movements of the hindlegs and abdomen
have also been observed in response to visual roll
stimuli in locusts (Taylor, 1981 a, b), but are incon-
sistently correlated with rolling (Thu$ ring, 1986) and
said to be neither necessary nor sufficient to effect a
correctional roll response (Schmidt & Zarnack,
1987 ; Waldmann & Zarnack, 1988). However,
Zanker’s (1988 a) careful study of abdominal de-
flection in Drosophila melanogaster highlights the need
to ensure that the rotational axis of a roll stimulus is
exactly normal to the axis about which yawing
occurs. If this is not the case, then a supposed roll
stimulus will induce a combined roll and yaw
response because the subject will perceive the
stimulus to contain some component of yaw. This
probably explains why postural changes normally
associated with yaw turns are observed in response to
roll stimuli, although we cannot discount the
possibility that abdominal deflection might be used
to generate roll moments by shifting the centre of
gravity. Alternatively, if roll and yaw are modulated
together in free flight, then responses to roll and yaw
stimuli might be reflexly coupled to effect a tighter
banked turn.
Asymmetries in stroke amplitude do not appear to
be strongly correlated with turning in locusts (Baker,
1979 ; Thu$ ring, 1986 ; Waldmann & Zarnack, 1988 ;
Zarnack, 1988) or crickets (Wang & Robertson,
1988 ; but see May, Brodfuehrer & Hoy, 1988),
except during very sharp turns (Robertson & Reye,
1992 ; Dawson et al., 1997). Likewise, there is no
evidence that differences in stroke path are cor-
related with turning in locusts (Zarnack, 1988),
although changes in hindwing elevation may be
important for steering in crickets (Wang & Robert-
son, 1988 ; May et al., 1988) which also bank their
forewings relative to the body axes during turning
(May et al., 1988).
Locusts (Gettrup & Wilson, 1964) and crickets
(Pollack & Hoy, 1981) reliably increase pronation of
the inside forewing during turning responses. In
Mechanics of insect flight control
locusts, this is usually correlated with early pronation
of the inside wing (Dugard, 1967 ; Baker, 1979 ;
Zarnack, 1988 ; Robertson & Reye, 1992 ; Dawson et
al., 1997). Muscle recordings from crickets are
suggestive of an analogous change in the timing of
the hindwing elevators and depressors (Wang &
Robertson, 1988). These changes should reduce lift
and thrust on the inside wing by decreasing its
effective incidence and might allow it to act as a sort
of brake (Zarnack & Mo$ hl, 1977). Antisymmetric
changes in pronation on the outside wing, possibly
combined with increased supination on the upstroke
(Zarnack, 1988), should increase lift and thrust on
the outside of the turn. The net result will be a
combined roll and yaw torque, leading directly into
a banked turn.
Intriguingly, opposite changes in the timing of the
forewing downstroke muscles have been recorded in
tethered locusts during presumed correctional re-
sponses to imposed yaw angles (Mo$ hl & Zarnack,
1975, 1977 ; Zarnack & Mo$ hl, 1977). These dif-
ferences seem to be real and may result from
differences in the turning stimuli used (Kammer,
1985), although the oscillating yaw stimulus used by
Zarnack (1988) was qualitatively the same as that
used in the three studies for which atypical time
shifts were observed. Individual locusts may also use
different patterns of muscle burst length in response
to the same roll stimulus (Waldron, 1967), so
different motor patterns may be common when only
one degree of freedom is considered. The magnitude
of a roll torque does not necessarily depend upon the
motor pattern used (Thu$ ring, 1986), so different
motor patterns must either produce the same
kinematics, which seems unlikely, or they must cause
the forces and moments about the other axes to vary
(Kammer, 1985 ; Thu$ ring, 1986).
This second explanation seems quite likely. For
example, whereas all of the inside forewing de-
pressors contract early relative to some constant
reference during a typical roll response (Mo$ hl &
Zarnack, 1977 ; Zarnack & Mo$ hl, 1977 ; Thu$ ring,
1986 ; Schmidt & Zarnack, 1987 ; Waldmann &
Zarnack, 1988), individual depressors may be time-
shifted in opposite directions during yaw responses
(Mo$ hl & Zarnack, 1975 ; Zarnack & Mo$ hl, 1977).
In any case, Baker’s comment that roll and yaw
turns in locusts are ‘ just two ways of looking at the
same phenomenon ’ (Baker, 1979, p. 57) is certainly
an over-simplification. Although independent modu-
lation of roll and yaw has never been observed in
locusts (Hensler & Robert, 1990), simultaneous
measurements of roll and yaw torques have not been
461
made and it remains an open question whether
differences in motor pattern will prove sufficient to
separate roll and yaw control in locusts.
Bulk phase shifts between contralateral wings are
bound to induce lateral asymmetries in the phase of
the fore- and hindwings during roll responses,
because the timing of the hindwings changes less
than that of the forewings (Schmidt & Zarnack,
1987) and may even change in the opposite direction
(Thu$ ring, 1986). Lateral asymmetries in the relative
positions of the fore- and hindwings are certainly
correlated with yaw responses in locusts (Dugard,
1967 ; Baker, 1979 ; Cooter, 1979 ; Robertson &
Reye, 1992 ; Robertson & Johnson, 1993) and will
inevitably alter the aerodynamic coupling of the
wings (Zarnack, 1982, 1983 ; Schwenne & Zarnack,
1987 ; Schmidt & Zarnack, 1987 ; Waldmann &
Zarnack, 1988 ; Robertson & Reye, 1992). Whilst
there is now little doubt that ipsilateral phase shifts
are important in locust flight control (Rowell, 1988),
the aerodynamic changes involved are unknown.
Contralateral interference remains unquantified in
locusts, and it is not known whether interference
between contralateral wings has any direct effect
upon steering.
VI. FLIGHT CONTROL IN OTHER INSECTS
(1) Longitudinal control
Studies of flight control in other insects have been
rather limited. Negative correlations between body
angle and flight velocity similar to those observed in
Drosophila spp. have been observed in dragonflies
(Wakeling & Ellington, 1997), heteropteran bugs
(Betts, 1986), bumblebees (Dudley & Ellington,
1990 a), honeybees (Nachtigall, Widmann &
Renner, 1971 ; Esch, Nachtigall & Kogge, 1975) and
moths (Dudley & DeVries, 1990 ; Willmott &
Ellington, 1997). Butterflies exhibit considerable
variation in the way in which body angle varies with
flight speed, although this is perhaps not surprising
given the extent to which butterflies ’ bodies pitch up
and down through the course of the wingbeat cycle
(Betts & Wootton, 1988 ; Brackenbury, 1995). For
example, whereas free-flying Papilio rumanzovia adopt
higher body angles and shallower stroke planes
during fast flight, free-flying Troides rhadamantus
appear to show the opposite trend (Betts & Wootton,
1988). Such variation is presumably indicative of
differences in the aerodynamic mechanisms being
used.
462
It is important to realise that a negative cor-
relation between flight speed and body angle need
not imply a helicopter-like mode of flight control, in
which the direction of the flight force is fixed with
respect to the body axes. Such a model may apply in
honeybees Apis mellifica, in which the partitioning of
lift and thrust seems to depend directly upon body
angle (Esch et al., 1975), but in heteropteran bugs,
for example, the inclination of the stroke plane to the
body may be varied by as much as 20m (Betts, 1986).
Likewise in hawkmoths Manduca sexta the stroke
becomes steeper relative to the body at higher speeds
(Willmott & Ellington, 1997) and the same trend
has been observed in the dragonfly Anax parthenope
(Azuma & Watanabe, 1988). No such trend was
detected in the dragonfly Sympetrum sanguinem in
which the stroke plane was apparently kept fixed
with respect to the body (Wakeling & Ellington,
1997). Nevertheless, the direction of the flight force
does not correlate closely with the orientation of
either the body or the stroke plane in this or other
dragonflies (Wakeling & Ellington, 1997), and the
orientation of the stroke plane with respect to flight
direction is generally rather variable (Ru$ ppell,
1989). The correlation of body angle with flight
speed and direction in dragonflies has therefore been
suggested to be an adaptation more to minimise
body drag than to redirect the flight force (Wakeling
& Ellington, 1997).
In bumblebees Bombus terrestris, the angle of attack
the wings is increased relative to the stroke plane as
the body angle is decreased (Dudley & Ellington,
1990 a), with the result that the effective angle of
incidence of the wings remains more or less un-
changed (Dudley & Ellington, 1990 b). In contrast
to Drosophila spp., however, the position and am-
plitude of the wingbeat do not appear to vary with
airspeed, and it is not known how changes in body
angle are brought about (Dudley & Ellington,
1990 a). Stroke amplitude does appear to be an
important longitudinal control parameter in heter-
opteran bugs, which display decreased stroke ampli-
tudes during climbing flight, together with an
increase in the speed of stroke reversal and a decrease
in the wingbeat frequency (Betts, 1986). No clear
trend has been found with respect to flight speed or
direction and stroke amplitude in butterflies. For
example, whereas free-flying Papilio rumanzovia and
Graphium sarpedon have been observed to increase
stroke amplitude during slow flight, free-flying Precis
iphita adopt sharply increased stroke amplitudes
during bursts of fast flight (Betts & Wootton, 1988).
In hawkmoths Manduca sexta, stroke amplitude
Graham K. Taylor
appears to decrease slightly with increasing speed
(Willmott & Ellington, 1997). This is due to a less
ventral excursion of the wings on the downstroke,
which would tend to shift the resultant flight force
rearward as in flies and presumably provides the
nose-down pitching moment required to decrease
the body angle for fast flight.
Opposite trends have been noted in the dragonfly
Sympetrum sanguinem and the damselfly Calopteryx
splendens. In these species, hindwing stroke amplitude
increases with increasing speed (Wakeling & Elling-
ton, 1997), although the regressions were not
significant at the 95 % confidence level and there
was no apparent change in the mean positional
angle of the wings. This does not appear to reflect a
general trend in dragonflies. For example, whereas
no correlation was found between stroke amplitude
and flight speed in free-flying Anax parthenope (Azuma
& Watanabe, 1988), a strong negative correlation
was observed in tethered Orthetrum cancellatum
(Gewecke, Heinzel & Philippen, 1974). Decreased
stroke amplitudes in the latter were associated with
reductions in only the dorsal excursions of the wings,
which would tend to shift the resultant flight force
forward, rather than rearward as in flies and
hawkmoths. If nothing else, these results caution
against extrapolating control mechanisms from one
group of insects, or even one species, to another.
Wingbeat frequency appears not to be an im-
portant longitudinal control parameter in either
hawkmoths (Willmott & Ellington, 1997) or dragon-
flies (Azuma & Watanabe, 1988 ; Wakeling &
Ellington, 1997), and has also been found to be
uncorrelated with flight speed in damselflies (Sato &
Azuma, 1997 ; Wakeling & Ellington, 1997), and
bumblebees (Dudley & Ellington, 1990 a). Wakeling
& Ellington (1997) did, however, note a trend for
wingbeat frequency to increase with increasing force
production in the damselfly Calopteryx splendens
(P 0n1). Although trends at the 90 % significance
level were deemed ‘ good ’ in that study (Wakeling &
Ellington, 1997, p. 566), the significance of trends
reaching even the 95 % level should be viewed with
caution given that some 52 independent regressions
were performed, grossly inflating the risk of making
a Type I error. Wingbeat frequency is decreased
during rising flight in heteropteran bugs (Betts,
1986), and there is reasonably strong evidence that
wingbeat frequency is positively correlated with
flight speed in butterflies (Betts & Wootton, 1988).
However, given the high degree of interspecific
variation revealed by the latter study in the
correlations between other kinematic parameters
Mechanics of insect flight control
and flight velocity, it would seem premature to
interpret data from a few species as indicative of a
more general trend.
(2) Lateral control
Postural adjustments like those observed in flies and
locusts appear to be ubiquitous steering responses in
insects, having also been observed in mantids
(Brackenbury, 1995), heteropteran bugs (Govind &
Burton, 1970 ; Govind, 1972), strepsipterans (Pix,
Nalbach & Zeil, 1993) and moths (Roeder, 1967 ;
Kammer, 1971 ; Kammer & Nachtigall, 1973).
Asymmetries in stroke amplitude like those observed
in turning flies have also been observed in dragonflies
(Alexander, 1986), beetles (Burton, 1964, 1971 ;
Schneider & Kramer, 1974), moths (Kammer, 1971)
and heteropteran bugs (Govind & Burton, 1970 ;
Govind, 1972). In bugs, the stroke path of the
outside wing may also be shifted dorsal to the inside
wing (Govind & Burton, 1970), which is similar to a
steering mechanism identified by Stellwaag (1916)
in bees and similar to an atypical steering pattern
observed during yaw turns in locusts (Cooter, 1979).
In moths and butterflies, the wings on the inside of
a turn are typically held more posteriorly than the
outside wings, and may be slightly flexed (Roeder,
1967). These changes probably correlate with
changes in the timing of muscle firing (Kammer,
1971, 1985 ; Kammer & Nachtigall, 1973 ; Obara,
1975) and presumably reduce lift and thrust on the
inside wing.
In dragonflies, amplitude asymmetries lead to
banking with a strong component of sideslip within
one or two strokes, usually followed by a component
of yaw (Alexander, 1986). This time lag suggests
that yawing may arise indirectly through aero-
dynamic coupling of the moments, rather than
directly through asymmetric thrust production.
Specifically, the component of sideslip resulting from
banking means that the oncoming flow is no longer
parallel to the longitudinal axis, which could lead to
the production of a coupled yaw moment. The inside
wing may also be more strongly pronated than the
outside wing during banked turns, although this is
usually secondary to changes in amplitude and may
only be used to fine-tune the response (Alexander,
1986). Very sharp yaw turns involving much more
extreme rotation of the wings have also been
observed in dragonflies (Alexander, 1986), sug-
gesting three-axis control of the moments. Phase
shifts between the fore- and hindwings analogous to
those observed in locusts have also been implicated
463
in free-flight manoeuvres in dragonflies (Alexander,
1984, 1986 ; Ru$ ppell, 1989) and hawkmoths (A. L. R.
Thomas, personal communication). In hawkmoths,
the wings (which are normally physically coupled)
may be completely uncoupled so as to operate in
antiphase. Such phase shifts are likely to be a com-
mon feature of flight control in four-winged insects
and need not necessarily be restricted to insects
in which the wings are normally uncoupled.
VII. DISCUSSION
(1) How many degrees of freedom do insects
control?
To date, three-axis control of the moments has only
been proven in larger flies and dragonflies. Exper-
iments to determine whether other insects can
modulate roll and yaw separately have simply not
been performed. However, since the most common
mode of turning is the banked turn, in which roll and
yaw are advantageously coupled to reduce the
turning circle, two-axis control of the lateral and
longitudinal moments could also suffice (Dickinson,
1999). Roll and yaw would then be modulated
together about an axis lying somewhere between the
morphological roll and yaw axes. Tables 1 and 2
provide a summary of the various kinematic par-
ameters available for lateral and longitudinal control
in flying insects. In the case of locusts, it is not
obvious whether independent control of forewing
pronation and ipsilateral coupling would permit
separate control of roll and yaw, or whether the
different motor patterns observed during roll and
yaw responses result in further kinematic changes
that have so far gone undetected. In Drosophila spp.,
on the other hand, there are more than enough
independent kinematic inputs to permit separate
control of roll and yaw, although it is equally
possible that one or more of these inputs is redundant
and is simply used to provide finer control of the
moments. For example, Zanker (1988 a) has found
that abdominal deflection and changes in stroke
amplitude are modulated together in Drosophila
melanogaster to produce a common torque about the
yaw axis. Three-axis control must therefore be
considered an unproven possibility in Drosophila spp.
Even where three-axis control of the moments can
be proven, this does not imply that the control axes
must be identical with the main body axes or indeed
that the control axes must be strictly orthogonal
(that is, perpendicular to one another). For example,
the nominal yaw axis is tilted some 30m back from the
 464
Table 1. Independent kinematic parameters (bold) available for longitudinal control in different insects

Supination : Phase of
speed and ipsilateral
Stroke Stroke Wingbeat Clap-and-peel timing of Degree of fore- and
trajectory amplitude frequency or clap-and fling rotation pronation hindwings

Diptera : Independent Amplitude Could be used ? Independent Independent Not

calypterate parameter ; decreased in for longitudinal parameter ; parameter ; applicable
flies could be used response to control, but could be could be
for nose-up likely to be used for used for
longitudinal disturbances tightly linked to longitudinal longitudinal
control amplitude control control
Diptera : Longitudinal Amplitude Frequency Wings Independent Degree of Not
drosophilid position of decreased in increases with approach parameter ; pronation applicable
flies stroke plane response to increasing force more closely could be appears not to
shifted nose-up production, but in response to used for be varied
independent disturbances ; decreases again nose-up longitudinal
of amplitude ; amplitude at peak outputs, disturbances ; control
stroke increases with probably may be
inclination increasing because of directly
apparently force physiological linked to
linked to production constraints amplitude?
amplitude
Orthoptera : Probably not an Amplitude Frequency Generally not Probably not an Pronation Likely to be
locusts important increases with normally applicable important increased in important ;
control increasing increases with control response to effects
parameter force increasing parameter nose-up unknown
production force disturbances
production,
but may be
varied in the

Graham K. Taylor
opposite
direction
under
open-loop
conditions
 Mechanics of insect flight control
Table 2. Independent kinematic parameters (bold) available for lateral control in different insects

Supination : speed
Clap-and-peel or and timing of Degree of Phase of ipsilateral
Stroke trajectory Stroke amplitude clap-and fling rotation pronation fore- and hindwings

Diptera : Independent Amplitude ? Supination delayed Pronation Not applicable

calypterate parameter ; could decreased on on inside wing sometimes
flies be used for lateral inside wing increased on
control. inside wing
Diptera : Independent Amplitude Wings meet at an Supination delayed Degree of pronation Not applicable
drosophilid parameter ; could decreased on angle to the on inside wing ; probably not an
flies be used for lateral inside wing sagittal plane speed of important control
control ; stroke during turns supination parameter
inclination increased on
apparently linked outside wing
to amplitude
Orthoptera : Probably not an Probably not an Not usually Probably not an Pronation Likely to be
locusts important control important control applicable important control increased on important. Effects
parameter parameter parameter inside wing unknown
Odonata : ? Amplitude Not applicable to ? Pronation Likely to be
dragonflies decreased on dragonflies increased on important ; effects
inside wing inside wing, unknown
during banked especially during
turns yaw turns

465
466
dorso-ventral body axis in Drosophila melanogaster
(Zanker, 1988 a), though whether an independent
roll axis exists or whether this represents a combined
roll-yaw axis in a two-axis system is unknown.
Orthogonality of the lateral control axes is not
essential for three-axis control, but any non-ortho-
gonality that may exist will complicate the neural
processing required to separate the various motions.
As a useful but rather imperfect analogy, consider
how difficult it is to predict the path of a bouncing
rugby ball compared to a bouncing football (it is
difficult to find a better analogy, precisely because
manmade control systems are usually designed to act
orthogonally). The lack of separate control surfaces
to isolate the three moments actually makes it rather
likely that insect control systems will be non-
orthogonal. For example, there is no particular
reason to suppose that changes in stroke amplitude
will result in a torque about an axis orthogonal to
that due to asymmetric changes in the degree of
pronation or supination. Hence, although the con-
trol inputs of aircraft are not always strictly
orthogonal, non-orthogonality is likely to be much
more pronounced in insects and this will tend to
complicate their flight control. This is likely to be
one of the most significant differences between the
flight control systems of insects and conventional
aircraft. The evolved interface between mechanics
and processing in a non-orthogonal control system
should prove an especially fruitful field for inter-
disciplinary research.
(2) Evolution of insect flight control systems
The ubiquity of postural flight control suggests that
it may be a primitive character amongst pterygote
insects. The necessary neuromuscular mechanisms
for postural control would have been in place long
before the evolution of the stroke cycle, so it would
not be surprising if this were the main means of
control during the early evolution of flight. Indeed,
if flapping flight evolved via an intermediate gliding
stage, then postural control could even have been
used to stabilise the descent of smaller insects prior to
the evolution of wings (Flower, 1964). Current
developmental, neurological and morphological evi-
dence suggests that the wings themselves evolved
from gills or associated epipodal structures on the
limbs of an aquatic ancestor (Wigglesworth, 1973,
1976 ; Kukalova! -Peck, 1978, 1983 ; Wootton, 1981 ;
Robertson, Pearson & Reichert, 1982 ; Kingsolver &
Koehl, 1994 ; Thomas & Norberg, 1996 ; Averof &
Cohen, 1997). Under this scenario, the incipient
Graham K. Taylor
wings would already have been articulated and
muscularised at their base. However, they would
probably not have possessed the degree of control
required for successful modulation of the flapping
cycle, unless their gill-like precursors were used for
swimming. Hence, the evolution of improved wing
control – whether for gliding or for some other
putative intermediate stage such as surface-skim-
ming (Marden & Kramer, 1994 ; Marden et al.,
2000) – would almost certainly have been prerequi-
site for the evolution of flapping flight. Indeed, a
wing that has evolved rotations about three axes for
control already has at least a rudimentary version of
each of the fundamental motions of the stroke cycle,
offering one possible route to the evolution of the
stroke cycle (Hinton, 1963 ; Wigglesworth, 1963,
1976 ; Wootton, 1976).
It is difficult to draw any firm conclusions as to the
stage of evolution at which different kinematic
control mechanisms would have been acquired. It
seems likely that the earliest flapping insects would
have had some control of stroke amplitude, allowing
direct modulation of the aerodynamic power output
and at least a rudimentary degree of lateral control.
Changes in the degree of wing pronation are also
likely to have been important from the outset, being
a fundamental motion of any flapping wing. Changes
in stroke amplitude or the degree of wing pronation
would be expected to affect both steady and
unsteady mechanisms of force production, though
their effects could be qualitatively different de-
pending upon the mechanism used. For example,
increasing the stroke amplitude on one wing should
increase quasi-steady lift production, but might also
lower unsteady lift production by destabilising the
leading edge vortex associated with delayed stall
(C. P. Ellington, personal communication, cited in
Betts, 1986).
Many of the other control inputs that insects use
can only be understood in the context of unsteady
aerodynamics. This is especially true of those relating
to the speed and timing of wing rotation or to the
phase of the fore- and hindwings. To a large degree,
then, the evolution of flight control in insects must
parallel their evolutionary refinement of unsteady
aerodynamic mechanisms, and differences in the
kinematics of flight control between insect orders will
therefore reflect differences in the unsteady mech-
anisms used. For example, the reason that changes in
the speed and timing of supination are an important
control input in Drosophila spp., whereas changes in
the degree of pronation are not, is presumably that
rotational and wake-capture mechanisms are the
Mechanics of insect flight control
major source of unsteady force production in
Drosophila spp. On the other hand, changes in the
degree of pronation do appear to be important in
locusts, which presumably reflects the importance to
locusts of translational mechanisms of aerodynamic
force production.
A corollary of this is that as our knowledge of
unsteady mechanisms and their relationship to wing
kinematics improves, it may become possible to
recognise the aerodynamic mechanisms being used
by a given insect on the basis of how the insect varies
its wing kinematics during real or fictive man-
oeuvres. This is potentially more powerful than
looking merely at the kinematics of steady flight,
since it will always be difficult to assess the
importance of translational mechanisms such as
delayed stall, which, in contrast to rotational
mechanisms, may have no clear kinematic mani-
festation. For example, the counter-intuitive re-
duction in stroke amplitude that accompanies
elevated force production in heteropteran bugs
(Betts, 1986) and hawkmoths (Willmott & Ellington,
1997) may indicate that delayed stall accounts for a
significant portion of peak force production, es-
pecially if the wingbeat frequency is reduced
simultaneously as in bugs. Future studies of the
mechanics of insect flight control will have to take
unsteady aerodynamics explicitly into account.
Experiments correlating changes in the wing kin-
ematics with instantaneous force measurements and
flow visualisation offer one way in which this might
be achieved.
VIII. CONCLUSIONS
(1) The current literature does not permit a
formal, quantitative analysis of insect flight control,
because the aerodynamic force systems that biol-
ogists have measured have rarely been complete,
and because the position of the centre of gravity has
rarely been recorded in studies of insect flight
control. Future experimental studies will need to pay
close attention to both these points. For a full
dynamic analysis, it will be necessary also to
determine the insect’s moments of inertia.
(2) Two influential paradigms in the insect flight
control literature appear either to have been widely
misinterpreted or to be a misinterpretation of the
empirical data. Specifically, although Drosophila spp.
normally modulate lift and thrust together, the
helicopter model of their flight control is probably
better thought of as a facultative strategy, rather
467
than as a fixed constraint. On the other hand, the so-
called ‘ constant-lift reaction ’ of locusts (Wilson &
Weis-Fogh, 1962) appears not to be a reflex for
maintaining constant lift at varying angles of attack,
but rather a mechanism to restore the insect to pitch
equilibrium following a disturbance.
(3) The number of degrees of freedom that insects
are able to control cannot exceed the number of
independent control inputs. Since the latter is usually
quite high, it seems likely that some of the control
inputs will be redundant, providing finer control of
the various degrees of freedom.
(4) Although most insects are likely to generate
control moments about all three axes, full three-axis
control has only been proven for larger flies and
dragonflies.
(5) Control inputs are unlikely to operate even
approximately orthogonally in insects. This will tend
to complicate the neural processing required to
separate out the various motions.
(6) Taxonomic differences in insect flight control
kinematics probably reflect differences in the un-
steady aerodynamic mechanisms being used. The
evolution of insect flight control is therefore likely to
have paralleled the evolutionary refinement of
unsteady aerodynamic mechanisms.
(7) Classification of an insect’s control kinematics
during real or fictive turns could provide a relatively
simple assay for determining the dominant unsteady
aerodynamic mechanisms being used.
IX. ACKNOWLEDGEMENTS
I am grateful to Adrian Thomas and Robert Nudds
for their comments upon the manuscript and thank
Bob Srygley for the image of the hawkmoth. The
comments of an anonymous referee were extremely
helpful in improving the manuscript. This work was
funded by a Christopher Welch Scholarship from
the University of Oxford.
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