Taylor 2001

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

(2) Lateral control .................................................................................................................. 460
VI. Flight control in other insects .................................................................................................. 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

(see Kammer, 1985 for a review of this type), I have
Insect flight control has been studied extensively chosen to concentrate in detail upon the aero-
from a physiological perspective, but its mechanics dynamics and kinematics of flight control. This
are less well known. Even where the kinematic approach is similar to that of most texts on aircraft
changes elicited by a given stimulus have been flight mechanics (e.g. Nelson, 1989 ; Etkin & Reid,
defined, their consequences for aerodynamic force 1996 ; Cook, 1997 ; Vinh, 1993) in that it does not
production often remain obscure. Earlier work on complicate the discussion of flight dynamics with
flight control was firmly rooted in the assumptions of details of the engineering mechanism that adjusts an
quasi-steady aerodynamics. However, since detailed aircraft’s elevators or varies an insect’s wingbeat
quasi-steady analyses and direct force measurements frequency. Instead, I will concentrate upon how
(e.g. Weis-Fogh, 1973 ; Norberg, 1975 ; Cloupeau, different kinematic inputs affect the dependent
Devillers & Devezeaux, 1979 ; Ellington, 1984 c ; variables of position and velocity, as illustrated
Ennos, 1989 ; Dudley & Ellington, 1990 b ; Wilkin, schematically in Fig. 1. The more general question of
1990 ; Zanker & Go$ tz, 1990 ; Wilkin & Williams, how many degrees of freedom insects can control is
1993) indicate that aerodynamic force production in one of the central issues of insect flight control and
insects generally relies upon unsteady mechanisms will form the theme of this review.
(Willmott, Ellington & Thomas, 1997 ; Dickinson, The ‘ black box ’ between the inputs and outputs
Lehmann & Sane, 1999), our understanding of of Fig. 1 is properly replaced by the equations of
insect flight control must necessarily incorporate motion for a flying body together with a system of
unsteady effects. Although our understanding of
unsteady mechanisms is still very limited, more
recent experimental studies (Go$ tz, 1987 ; Dickinson, control inputs
e.g. stroke amplitude,
Lehmann & Go$ tz, 1993 ; Dickinson, 1999 ; Dickinson wingbeat frequency
et al., 1999) have begun to investigate their role in
insect flight control.
An experimental approach integrating physio- position position
logical and mechanical observations is clearly de-
attitude acceleration attitude
sirable. For example, although electromyographic
studies have demonstrated that migratory locusts angular acceleration
velocity velocity
Locusta migratoria generate different motor patterns in
response to roll and yaw stimuli (Zarnack & Mo$ hl, angular angular
1977), they cannot tell us whether this is sufficient to velocity velocity
allow roll and yaw rotations to be produced Fig. 1. Block diagram illustrating the overall approach of
separately. This can only be resolved by directly this review. The black box represents the equations of
measuring the torques and forces that the insects motion for a flying body, together with a system of
produce, or by analysing high-speed film of the transfer functions providing the mathematical relation-
insects in flight. Although the current literature does ship between control inputs and their effects upon the
permit some synthesis of aerodynamics and kin- dependent variables.
Mechanics of insect flight control 451
transfer functions providing the mathematical re- experimental approach is clearly required before we
lationship between the control inputs and their will make any further inroads towards a quantitative
effects upon the dependent variables. I shall only be analysis of insect flight control.
discussing the mechanics of insect flight control in As a final caveat, it is worth emphasising that the
qualitative terms, however, as the current literature picture of insect flight mechanics portrayed in this
does not allow for even a formal static, let alone review is far from complete. For example, although
dynamic, quantitative framework to be applied. The the open-loop conditions that are normally imposed
reasons for this are best seen by considering the two by tethering often lead to exaggerated turning
possible approaches to the quantitative analysis of responses (Robert & Rowell, 1992 a), laboratory
insect flight control. The first is to correlate free- experiments may not reveal the full gamut of control
flight manoeuvres with observed changes in wing responses used by insects flying under natural
kinematics. For example, Wakeling & Ellington conditions. Only where we can identify clear
(1997) correlated velocity and flight force with physiological limits upon performance can we be
several basic kinematic parameters measured from sure that we have correctly identified the boundary
high-speed film of free-flying dragonflies. However, of the flight envelope. As the quantity and detail of
the purpose of fitting regression lines in that study experimental work on insect flight control improves,
was ‘ only to identify trends and not to estimate a our knowledge of insects’ flight envelopes looks
functional relationship ’ (Wakeling & Ellington, certain to expand.
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, II. MANOEUVRE CONTROL VERSUS REFLEX
accurately determining the three-dimensional wing STABILISATION
kinematics of even a stationary insect presents
formidable technical difficulties, and to do so during Insect control systems serve two discrete functions :
free-flight manoeuvres is very difficult indeed. to allow controlled manoeuvres and to augment or
An alternative approach is to measure directly the provide stability in the face of external (or possibly
forces and moments on tethered insects and to internal) perturbations. Since stability will tend to
correlate these with the observed changes in wing oppose both accidental and deliberate deviations
kinematics. Unfortunately, although many studies from steady flight, these two functions are expected
have measured selected forces and torques generated to be in direct conflict unless some mechanism is
by tethered insects, the resulting force systems are present to bypass or desensitise the reflex stabilisation
rarely complete, in the sense of defining the point of system during manoeuvres. In the absence of such a
action, as well as the magnitude and direction, of the mechanism, the command to elicit a manoeuvre
resultant flight force. Only two published studies would need to override any signals from the reflex
(Hollick, 1940 ; Blondeau, 1981) appear to have stabilisation system, presumably with a consequent
made the necessary measurements to determine the drop in nervous, if not also mechanical, efficiency.
point of action of the resultant flight force, yet this is From the viewpoint of enhancing manoeuvrability,
essential in determining the effect of a force, as any the potential temporarily to disable a reflex stabil-
child who has ever played on a see-saw will know. isation system makes active control of stability
The position of the centre of gravity has likewise preferable to passive stability, which cannot gen-
rarely been recorded, but is critical in determining erally be ‘ switched off ’. The impressive flight
both the animal’s responsiveness to control inputs envelopes of flies and other highly manoeuvrable
and its characteristics of stability and equilibrium. insects must reflect in large part a strong reliance
Its role in flight dynamics is analogous to that of the upon active, rather than passive, maintenance of
fulcrum in a game of see-saw. For a full dynamic stability.
analysis of insect flight control, it will be necessary On the other hand, since active control may
also to determine the insect’s moments of inertia. augment, rather than completely replace, passive
The importance of the distribution of mass in stability, a brief discussion of the latter may be useful
determining the envelope of insect flight control has in setting corrective flight control in context. The
been emphasised by recent experimental work on first point to note is that hovering insects, like
the flight performance of neotropical butterflies hovering helicopters (Gessow & Amer, 1949 ;
(Srygley & Dudley, 1993 ; Srygley, 1994, 1999 ; Johnson, 1980 ; Padfield, 1996), possess no first-order
Srygley & Kingsolver, 2000). A more rigorous passive stability about any axis. This is because the
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.
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 Fig. 3. Conventional aircraft use mechanically separate
the insect use? How many degrees of freedom does control surfaces (shaded) to separate control of the three
this allow the insect to control? Independent control moments. In the simple system shown here, the tail
of all six of an insect’s degrees of freedom (Fig. 2) elevators are used to control pitch, the ailerons to control
would require a minimum of six independent control roll, and the rudder to control yaw. Insects lack separate
control surfaces and must instead use different rotations of
inputs. Full six-degree-of-freedom control is super-
the wings to separate the moments.
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 Early experiments in wing warping aside, the
position in space, independent modulation of pitch, conventional aircraft design paradigm has long been
heading and longitudinal acceleration will suffice, to use separate control surfaces to isolate pitch, roll
requiring just three independent control inputs. and yaw (Fig. 3). This differs markedly from the
Two-axis control systems like these are a feature of control systems of insects in which the same
some high-performance model sailplanes and could kinematic parameters are varied symmetrically for
be used by insects with no great need for manoeuvra- control of the longitudinal forces and moments, and
bility. asymmetrically for control of the lateral forces and
Three-axis control systems permit independent moments. For example, in locusts, pronation (nose-
modulation of pitch, roll and yaw and thus enable a down rotation of the wing at the top of the stroke) is
far wider range of manoeuvres. Depending upon increased symmetrically between the forewings in
whether the direction as well as the magnitude of response to a nose-up pitching disturbance, but is
longitudinal acceleration can be varied independent only increased on the inside forewing during turns
of pitch, three-axis control systems require a mini- (Gettrup & Wilson, 1964). The result is an effective
mum of either four or five independent control doubling of the number of control inputs and a
inputs. In fixed-wing aircraft and helicopters, the remarkable economy of control. It follows that
direction of longitudinal acceleration is normally insects that modulate the direction of longitudinal
dependent upon pitch, although flaps may be used acceleration by symmetrically varying the balance of
to steepen a descent without upsetting pitch equi- lift and thrust on their wings should also be able to
librium. Amongst operational aircraft, perhaps only separate roll and yaw by varying the same kinematic
the Harrier jump jet can be considered to possess parameters asymmetrically. Conversely, insects that
complete five-degree-of-freedom control in the sense modulate roll via asymmetric lift production, and
of being able to accelerate at any angle to the ground yaw via asymmetric thrust production, should also
without varying pitch. However, whereas five- be able to modulate the direction of longitudinal
degree-of-freedom control is the exception in aircraft acceleration to some degree. Hence, we would expect
and four-degree-of-freedom control the rule, the many insects using three-axis control to modulate
opposite may be the case in insects with three-axis motions in five, rather than four, of their six degrees
control because of important differences in the of freedom, although this is not to say that all
mechanisms by which control inputs are produced. combinations of these motions will be possible.
Having considered some general principles of A B

control, I will now go on to apply these specifically stroke plane
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. stroke plane
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 Fig. 4. (A, B). Stroke amplitude is the planar angle of the
control should be amongst the simplest to under- arc described by the wing leading edge between the top
stand. Specifically, there can be no question of and bottom of the stroke (dotted line in column A).
interference between the fore- and hindwings, or of a Column B shows the corresponding points of action of the
mean flight force. Decreasing the stroke amplitude
changing balance of forces between the two. Flies
(bottom row) causes the flight force to shift back,
exhibit two main classes of manoeuvre : fast, vol- generating a nose-down pitching moment about the
untary, turns, known as saccades because of their centre of gravity (part-filled circle).
kinematic resemblance to the tracking movements of
vertebrate eyes, and slower, often corrective, turns
under the influence of the optomotor control system. 4A) – is normally considered the main control
Other classes of turn have been also recorded, often parameter determining aerodynamic power output
as pursuit responses by courting males. For example, in fruit flies Drosophila spp. Stroke amplitude shows a
dolichopodid flies Poecilobothrus nobilitatus have been strong positive correlation with aerodynamic force
filmed executing 180m yaw turns in less than 40 ms production (Vogel, 1967 ; Go$ tz, 1968 ; Lehman &
during courtship (Land, 1993). Hovering male Dickinson, 1997 ; Dickinson, Lehmann & Chan,
tabanid flies Hybomitra hinei have even been recorded 1998) and is referred to as stroke angle in some
using a modified form of the Immelmann turn – a studies. Wingbeat frequency is the other principal
classic aerobatic manoeuvre consisting of a half-loop determinant of aerodynamic power output, and
followed by a half-roll, used to effect rapid reversals appears to be an important control parameter in flies
of flight direction (Wilkerson & Butler, 1984). (Dickinson et al., 1998). For example, Drosophila
Throughout this review I will be presenting results melanogaster increase their wingbeat frequency in
relating to both voluntary and corrective control, response to an increase in the speed of optic flow
and it should be borne in mind that control inputs simulating forward flight (Friedrich, Spatz &
that are suitable for one type of control may not be Bausenwein, 1994).
suitable for the other, especially where the speed of In Drosophila melanogaster, wingbeat frequency is
the motion is very different. positively correlated with aerodynamic force below
approximately the force required to support body
weight, but is negatively correlated with aerody-
(1) Longitudinal control
namic force at peak outputs (Lehmann & Dickinson,
Stroke amplitude – the angle of the planar arc or 1997). Decreases in wingbeat frequency appear to be
great circle described by the wing leading edge compensated by steeper increases in stroke am-
between the top and bottom of the stroke (Fig. plitude, however, and the product of frequency and
amplitude (which determines the translational vel- stroke amplitude, which should increase lift and
ocity of the wing) rises linearly with increasing force thrust production dorsally, inducing a restoring
production (Lehmann & Dickinson, 1997). The nose-up torque in response to nose-down stimuli
drop in wingbeat frequency at peak force production (Zanker, 1990).
may result from physiological constraints, so stroke Drosophila melanogaster are also able to vary the
amplitude and wingbeat frequency are probably not longitudinal position of the stroke plane independent
strictly independent control inputs, even though of amplitude (Zanker, 1988 b), which should allow
they are not coupled in a straightforward fashion. At pitch to be modulated independent of aerodynamic
peak levels of force production, D. melanogaster force output. Similar shifts in stroke plane position
appear to be limited to a unique combination of have also been observed in the hoverflies Eristalis
stroke amplitude, wingbeat frequency and flight tenax and Episyrphus balteatus (Ellington, 1984 a).
force coefficient, and this in turn constrains their Stroke plane inclination varies too during pitching
ability to generate the asymmetries in force pro- responses in Drosophila spp., but this is tightly
duction necessary for lateral control (Lehmann & correlated with changes in amplitude, which cause
Dickinson, 2001). An analogous degradation of the lower turning point to move almost horizontally,
turning ability with increasing flight speed was rather than parallel to the stroke plane, thereby
found by Buelthoff, Poggio & Werhahn (1980), who altering stroke inclination (Vogel, 1967 ; Zanker,
found the maximum angular velocity attained by 1988 b). Drosophila spp. do not seem to vary the angle
free-flying D. melanogaster to decrease with increasing of attack of the wings for longitudinal control (Vogel,
forward velocity, although in this case the effect is 1967), although the constancy of the angle of attack
likely to result from aerodynamic, rather than suggests that they might actively stabilise it at
physiological, constraints. different speeds (Zanker, 1990). The speed and
In larger calypterate flies (blowflies, houseflies, timing of wing rotation do appear to be important
etc.), frequency and amplitude are both positively lateral control parameters in D. melanogaster (Zanker,
correlated with aerodynamic force, but since the two 1990 ; Dickinson et al., 1993), but have not been
parameters are likely to be mechanically linked, it is investigated in the context of longitudinal control.
not necessarily easy to separate cause from effect In addition to varying their wing kinematics, flies
(Nachtigall & Wilson, 1967). Symmetrical changes may control pitch by varying their posture, much
in stroke amplitude are also correlated with cor- like a hang-glider pilot. Drosophila melanogaster elevate
rective pitch control in larger flies such as Muscina their abdomen in response to nose-down disturb-
stabulans and Calliphora erythrocephala, which decrease ances (Zanker, 1988 a, b), displacing the centre of
the amplitude of both wings in response to an gravity dorsal to the line of thrust, which therefore
increase in body angle (Hollick, 1940 ; Nalbach & generates a restoring nose-up moment with the fly’s
Hengstenberg, 1994). Changes in amplitude are inertia. The concurrent increase in drag on the
effected by adjusting the lower turning point of the dorsal side will further add to this torque (Zanker,
wings, which shifts back with a decrease in amplitude 1988 b). Similar postural changes have been observed
as the wings sweep less far forward on the down- in Calliphora erythrocephala (Nalbach & Hengstenberg,
stroke. This causes the point of action of the mean 1994), so abdominal deflection may be a widespread
flight force to shift back (Fig. 4B), generating a mechanism of pitch control in flies. Drosophila virilis
pitching moment with the fly’s weight of appropriate have also been observed to elevate their hindlegs
direction to restore it to equilibrium (Hollick, 1940). following a nose-down disturbance, which should
Similar, albeit smaller, changes in stroke amplitude increase drag dorsally and generate a nose-up
are observed during pitching responses in Drosophila pitching moment (Vogel, 1967). The raised hindlegs
spp. (Zanker, 1988 b, 1990), which may use a similar can hardly fail to meet with interference from the
mechanism for pitch control (Vogel, 1967). How- wake of the wings, and this could enhance their
ever, the smaller magnitude of the response is turning effect in much the same way that a ship’s
suggestive of a slightly different mechanism. A rudder is more effective if placed in the wake of the
prominent feature of unsteady lift-production in propeller (Vogel, 1967).
Drosophila spp., at least in tethered flight, is the clap- The various kinematic and postural changes
and-peel process in which the opening wings draw described above are only sufficient to provide two
additional air into the circulation at the start of the degrees of freedom for longitudinal control, since
downstroke (see Ellington, 1984 a, b). The extent of none of them permits control of the direction of the
contact between the wings increases with increasing resultant flight force relative to the body axes. This
would result in essentially the same situation as in vortices shed at the end of the previous half-stroke
helicopters, in which the direction of the rotor force (see Dickinson et al., 1999). This is one potential
is fixed with respect to the body. Hence, although a mechanism by which larger flies could vary the
hovering helicopter’s vertical displacement can be direction of the flight force. Changes in stroke plane
controlled directly by varying the aerodynamic force inclination observed in Drosophila melanogaster are
on the blades, it can only be given horizontal probably too small to be used for control purposes
velocity by changing the body angle to redirect the ( 0n5m ; Zanker, 1988 b), and being linked to
flight force forward (e.g. Johnson, 1980). This does changes in stroke amplitude should probably not be
in fact appear to be the mechanism by which counted as a separate control input anyway. Other
Drosophila spp. normally control their trajectory kinematic parameters have not been investigated in
(Vogel, 1966 ; David, 1985 ; Zanker, 1988 b), since the context of longitudinal control, but since longi-
the elevation of the aerodynamic force is apparently tudinal forces and moments can be produced by
kept fixed relative to the body axes (Vogel, 1966 ; symmetrically adjusting parameters used for lateral
Go$ tz, 1968 ; David, 1978 ; Go$ tz & Wandel, 1984 ; control, we will consider other potential candidates
but see Ennos, 1989). The relative proportions of lift in the context of lateral control.
and thrust are thus varied primarily by adjusting the
body angle (David, 1985 ; Zanker, 1988 b), which is
(2) Lateral control
negatively correlated with flight speed (Vogel, 1966 ;
David, 1978) to allow level flight to be maintained as Although changes in wing kinematics are likely to be
aerodynamic power output is increased. However, more important for fast flight manoeuvres, postural
the fact that Drosophila spp. normally modulate lift adjustments are commonly associated with slow
and thrust together need not imply that they are optomotor steering responses in flies (Zanker,
strictly coupled as in helicopters, and the helicopter 1988 a). Typically, the abdomen is deflected into a
model may perhaps be better thought of as a turn (Go$ tz, Hengstenberg & Biesinger, 1979 ;
facultative strategy for flight control rather than as a Zanker, 1988 a ; Zanker, Egelhaaf & Warzecha,
fixed constraint. 1991), often together with the inside hindleg
Similar results have been reported for tethered (Hollick, 1940 ; Faust, 1952 ; Nachtigall & Roth,
houseflies Musca domestica flying in still air (Go$ tz & 1983 ; Nalbach, 1989). Occasionally both hindlegs
Wandel, 1984), but the generality of this result is are extended together into the turn (Go$ tz et al.,
questionable because M. domestica does not hover 1979). Similar adjustments in locusts have been
(Wagner, 1986) and a flow of air over the antennae interpreted as producing drag-based yaw torques
is necessary for a normal stroke path in Muscina like a ship’s rudder (Camhi, 1970) and most workers
stabulans (Hollick, 1940). Free-flying M. domestica do have followed the same interpretation for flies (e.g.
appear to be able to vary the direction of the flight Go$ tz et al., 1979). Postural adjustments in other
force vector, but only within a limited range insects have been suggested to produce lateral
(Wagner, 1986). Force measurements in tethered moments by a different mechanism, shifting the
Calliphora spp. have confirmed that they also are able centre of gravity sideways from the centre of pressure
to modulate thrust independent of lift within a (Govind & Burton, 1970 ; May & Hoy, 1990 a). This
certain range (Blondeau, 1981, Nachtigall & Roth, would normally be expected to generate a roll rather
1983), although the relation may be asymmetric than a yaw torque, but abdominal deflections in
because lift appears never to be modulated in- Drosophila melanogaster do appear to generate yaw
dependent of thrust (Blondeau, 1981). torques gravimetrically (Zanker, 1988 a). This is
Any ability to alter the direction of the flight force because the axis about which yawing occurs is tilted
independent of its magnitude implies that some back approximately 30m from the vertical such that
other kinematic parameter must be varied inde- a significant component of the animal’s weight acts
pendent of stroke amplitude and wingbeat fre- normal to the yaw axis and can therefore produce a
quency, which together provide control of only the yaw couple with the flight force.
magnitude of the flight force, albeit with an element Until recently, stroke amplitude was thought to be
of redundancy. Changes in stroke plane inclination the only kinematic parameter consistently correlated
will certainly alter the direction of the resultant with roll and yaw responses in flies (Drosophila spp. :
flight force, and would almost certainly affect the Vogel, 1967 ; Go$ tz, 1968 ; Go$ tz et al., 1979, Musca
forces generated by wake capture mechanisms in domestica : Srinivasan, 1977, Calliphora spp. : Heide,
which the wings gain an additional ‘ kick ’ from 1971 ; Nachtigall & Roth, 1983 ; Hengstenberg,
Sandeman & Hengstenberg, 1986 ; Nalbach, 1989 ; 1999), the view that they are strictly coupled has
Nalbach & Hengstenberg, 1994). According to the begun to be challenged (Go$ tz, 1987 ; Ennos, 1989 ;
classical interpretation, the amplitude of the inside Zanker, 1990 ; Dickinson et al., 1993). In any case,
wing is lowered to reduce the aerodynamic force by varying the relative proportions of lift and thrust
shortening the stroke, with opposite changes oc- independently on each wing is not the only way to
curring on the outside wing. This will generate generate a yaw torque. For example, the clap-and-
rolling moments directly through asymmetric lift peel process does not occur parallel to the sagittal
production and should also generate yaw moments plane during fictive turns in Drosophila melanogaster,
directly through asymmetric thrust production. and the jet of air produced is in the appropriate
Since flying insects usually produce much less thrust direction to contribute to steering (Go$ tz, 1987 ;
than lift (typically an order of magnitude less in Zanker, 1990). This could allow yaw moments to be
Drosophila virilis ; Vogel, 1966), the resulting torques generated independent of roll, although the torques
about the yaw axis would normally be expected to generated in this way may still be rather small
be correspondingly small compared to those in roll. (Dickinson et al., 1993 ; Dickinson, 1999).
Although this classical view was originally rooted Larger flies such as Calliphora spp. (Blondeau,
in the assumptions of quasi-steady aerodynamics, the 1981 ; Schilstra & Van Hateren, 1999) and Musca
outcome could be the same for an unsteady domestica (Wagner, 1986) can certainly generate roll
translational mechanism such as delayed stall, in and yaw torques separately, though the two are
which flow remains attached to the wing at higher usually modulated together to produce a banked
angles of attack than would be possible under steady turn (Blondeau, 1981). This presumably increases
conditions. Hence, although control torques meas- manoeuvrability in the same way as in a turning
ured in Drosophila melanogaster are generally greater aircraft, by minimising sideslip and directing the
than those calculated from blade-element theory, nose into the turn. Sometimes, it may be useful to
which assumes quasi-steady aerodynamics (Zanker, swing sideways without changing heading. Heli-
1990 ; Zanker & Go$ tz, 1990), stroke amplitude could copters achieve this by banking to one side to
still play a direct role in dipteran flight control if redirect a component of the flight force sideways.
unsteady translational mechanisms were important. This is probably also the mechanism behind Collett
Dickinson et al.’s (1993) comment that changes in & Land’s (1975) observation that the hoverfly Syritta
amplitude may not be directly responsible for pipiens can fly sideways without changing its heading.
turning in D. melanogaster (on the grounds that This implies that hoverflies must also possess in-
correlated changes in the timing of stroke reversal dependent control of roll and yaw. At least one other
will be more important than stroke length per se if kinematic parameter must be varied in addition to
unsteady rotational mechanisms overwhelm quasi- stroke amplitude for roll and yaw to be controlled
steady lift production) implicitly assumes that separately, because abdominal deflection occurs too
unsteady translational mechanisms (which also have slowly to account for the rapid turns observed in
the potential to overwhelm quasi-steady lift pro- flies. For example, in Drosophila melanogaster the
duction) are insignificant. abdomen only responds strongly to oscillating visual
Changes in amplitude do not permit the direction stimuli at frequencies below 5 Hz, and the response
of the flight force to be varied directly, unless the is much stronger at lower frequencies (Zanker,
part of the stroke that is curtailed generates a force 1988 a). Peak deflection is only attained at 0n05 Hz,
in a different direction to the remainder of the suggesting that the response may be used to correct
stroke. In general, since rolling moments are nor- for inherent asymmetries in the wings or flight
mally generated by asymmetric lift and yawing motor, rather than discrete disturbances (Zanker,
moments by asymmetric thrust, separate control of 1988 a).
lift and thrust will usually be required for roll and Wingbeat frequency can immediately be ruled out
yaw to be varied independently. Roll and yaw have as a lateral control parameter because the con-
therefore been suggested to be unavoidably coupled struction of the dipteran flight motor makes it im-
in Drosophila spp. (Srinivasan, 1977), which normally possible for the wings to operate at different
modulate lift and thrust together. To conclude that frequencies (Hollick, 1940). Stroke plane inclination
Drosophila spp. are unable to uncouple lift and thrust also appears not to offer an independent control
would seem premature, however, and although input because it is closely linked to amplitude in
direct evidence that Drosophila spp. modulate roll most studies in which both have been measured
and yaw independently is still lacking (Dickinson, (Vogel, 1967 ; Nachtigall & Roth, 1983 ; Zanker,
1988 b, see also Chadwick, 1951). For example, in stroke reversal, whereas negative forces are registered
Calliphora vicina the action of the basalar muscles has if supination is delayed (Dickinson et al., 1999).
been shown explicitly to determine both stroke plane By asymmetrically varying force production in
inclination and amplitude (Tu & Dickinson, 1996). this way, flies could readily produce turning
However, the precise three-dimensional trajectory of moments for control. For example, the results of
the wingtip can be varied independently of am- Dickinson et al. (1999) indicate that the instan-
plitude in Muscina stabulans (Hollick, 1940) and C. taneous drag force may be extremely high on a wing
vicina (Tu & Dickinson, 1996), and this might be using rotational circulation and wake capture, and
used to produce control moments, perhaps by well in excess of the instantaneous lift. Hence,
altering the properties of wake capture. One wing though the instantaneous drag forces largely cancel
may even be completely folded over the body during over the course of a normal stroke, asymmetric drag
extremely fast turns (Nachtigall & Wilson, 1967), production offers a potent means of generating roll
although this is unlikely to play any role in or yaw torques in insects using rotational circulation
correctional steering. and wake capture. The direction of the axis about
Increased pronation of the inside wing has been which the resulting torque is generated will depend
observed during roll and yaw responses in Calliphora upon both the direction of the stroke and the
erythrocephala (Faust, 1952 ; Hengstenberg et al., orientation of the wing chord. For example, in
1986). Similar changes in pronation have been noted insects with a horizontal stroke plane, such as
in the cranefly Tipula oleracea (Faust, 1952) and the hoverflies, the potential to vary the horizontal force
blowfly Lucilia serricata (Sandeman, 1980). Unfortun- component may be far greater than the potential to
ately, the stage of wingbeat recorded was almost vary the vertical lift. Asymmetric variation of the
certainly wrongly described in the latter study (D. C. forces produced by rotational circulation and wake
Sandeman, pers. comm., cited in Kammer, 1985) capture would then tend to generate a yaw torque,
and it is not clear whether the magnitude or only the and this may account for the remarkable ability of
timing of rotation was varied. Angle of attack hoverflies to turn full circle whilst otherwise re-
asymmetries are taken to an extreme in the doli- maining stationary.
chopodid fly Poecilobothrus nobilitatus, which is able to In Calliphora erythrocephala (Nalbach, 1989) and
execute extraordinarily rapid 180m turns by holding Drosophila melanogaster (Dickinson et al., 1993), su-
the inside wing normal to the flow to act as an pination is delayed on the inside wing and advanced
airbrake (Land, 1993). on the outside wing during fictive turns. Parallel
In light of current views of insect flight control changes in the timing of pronation have also been
implicating unsteady aerodynamic mechanisms as observed (Nalbach, 1989). Unfortunately, it has not
the main source of control moments (Zanker, 1990), been possible to resolve changes in the timing of
the speed and timing of wing rotation are likely to be stroke reversal, so the phase of supination and stroke
at least as important as the degree of pronation reversal remains unknown. However, assuming that
(Ennos, 1989 ; Dickinson et al., 1993, 1999 ; an absolute delay in supination on the inside of a
Dickinson, 1994, 1999). Supination (nose-up ro- turn indicates that supination is also delayed relative
tation of the wings towards the bottom of the stroke) to stroke reversal, then the results of Dickinson et al.
occurs extremely rapidly in flies (Ennos, 1989). Flow (1999) imply that the flight force will be reduced or
visualisation of tethered Drosophila melanogaster reversed on the inside of a turn. Earlier supination is
(Dickinson & Go$ tz, 1996) appears to show the also correlated with increased rotational velocity in
vorticity produced by the so-called ‘ ventral flip ’ D. melanogaster (Dickinson et al., 1993, see also
(Dickinson et al., 1993) fusing with the stopping Zanker, 1990), which should increase aerodynamic
vortices shed at the end of the downstroke, so rapid force production on the outside of a turn. Both effects
wing rotation might be used for aerodynamic force should combine synergistically to produce a torque
production. Experiments with model wings (Dickin- in the correct direction to steer into the turn.
son, 1994 ; Dickinson et al., 1999) have demonstrated The timing of supination seems to be independent
that the timing of supination relative to stroke of stroke amplitude in Drosophila melanogaster, even
reversal (the point at which wing translation reverses though the two are usually modulated together
direction) is critical in determining the magnitude of (Dickinson et al., 1993). Changes in stroke amplitude
the forces produced. Large positive forces (attribu- and the timing of supination could therefore provide
table to both rotational mechanisms and wake the two inputs necessary to separate control of roll
capture) are generated when supination precedes and yaw. Alternatively, changes in stroke amplitude
might not effect steering directly, but could instead (Baker, Gewecke & Cooter, 1981). Moreover, stroke
effect steering indirectly through correlated changes amplitude and wingbeat frequency are negatively
in the timing of stroke reversal (Dickinson et al., correlated in tethered L. migratoria stimulated by air
1993). However, since it is the relative timing of currents of fixed speeds (Gewecke, 1970, 1972), so
supination and stroke reversal that primarily deter- the two must also be able to be varied independently.
mines aerodynamic force output, changes in stroke Locusts appear to regulate lift independent of
amplitude and the timing of supination would then thrust and have also been claimed to exhibit a
combine together to provide a single composite ‘ constant-lift reaction ’ (Wilson & Weis-Fogh, 1962)
variable, which would make changes in stroke in which the vertical component of force is kept more
amplitude redundant. In this case, some other or less constant following imposed changes of body
independent control input (e.g. the speed of wing angle of up to 20m (Weis-Fogh, 1956 a, b ; Gewecke,
rotation) would still be required to separate control 1975). Electrophysiological (Wilson & Weis-Fogh,
of roll and yaw. It therefore seems likely that stroke 1962 ; Gettrup, 1966 ; Zarnack & Mo$ hl, 1977) and
length per se could be an important control par- kinematic studies (Gettrup & Wilson, 1964 ; Gettrup,
ameter, at least in larger flies in which roll and yaw 1966 ; Wortmann & Zarnack, 1993) have clearly
are known to be controlled separately. demonstrated that tethered locusts increase forewing
Returning briefly to longitudinal control, sym- pronation to compensate for the increase in their
metric changes in the speed or timing of supination angle of attack that would otherwise occur following
could be used to vary the magnitude of the resultant a nose-up disturbance. The same reaction also
flight force (Dickinson et al., 1999). Changes in the appears to occur in free flight, since climbing flight is
timing of wing rotation might also provide the associated with both increased forewing pronation
additional control input required to separate control and increased body angle (Fischer & Kutsch, 2000).
of lift and thrust. Symmetric adjustment of the Hindwing pronation is largely independent of body
ventral flip could certainly enhance the pitching angle (Gettrup & Wilson, 1964 ; Wortmann &
responses discussed in the previous section, because Zarnack, 1993), however, so whereas the forewing
the lever arm at the end of the downstroke will lift coefficients should remain approximately con-
usually be such that even small changes in the stant, the hindwing lift should increase with in-
rotational forces will generate a large pitching creasing body angle, because the lift on a wing
moment. Finally, some control over the direction of generally increases with increasing angle of attack.
vortex shedding would permit an even greater degree According to Gettrup & Wilson’s (1964) model of
of control of the direction of the resultant flight force the constant-lift reaction, the drop in flight speed
(Ellington, 1984 b ; Dickinson et al., 1993). 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.
V. FLIGHT CONTROL IN ORTHOPTERA
The constant-lift reaction has been an influential
(LOCUSTS AND CRICKETS)
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
Flight control in locusts is likely to be complicated by from the objection that the quasi-steady aerody-
the interaction of flow over the fore- and hindwings, namics implicit in Gettrup & Wilson’s (1964) model
though some common principles remain. As in flies, have been shown not to apply in locusts (Cloupeau
stroke amplitude and wingbeat frequency are posi- et al., 1979 ; Wilkin, 1990), it is not clear why free-
tively correlated with aerodynamic force and flying flying locusts should possess a reflex maintaining
speed in tethered Locusta migratoria able to control constant lift at widely different body angles. A
their own speed relative to the surrounding air stabilising pitch reflex would seem to be of far
(Gewecke, 1975 ; Kutsch & Gewecke, 1979). Teth- greater utility. Studies of free-flying locusts (Baker et
ered L. migratoria also increase their wingbeat al., 1981) are consistent with the existence of a
frequency in response to an increase in the speed of stabilising pitch reaction, showing no evidence of the
optic flow simulating forward flight (Baader, Scha$ fer negative correlation between body angle and flight
& Rowell, 1992) and the same qualitative re- speed that forms an essential part of Gettrup &
lationship between wingbeat frequency and flight Wilson’s (1964) original scheme. Moreover, later
speed has been shown in free-flying L. migratoria studies (Zarnack & Wortmann, 1989 ; Wortmann &
Zarnack, 1993) have cast doubt on the existence of a and the cricket Teleogryllus oceanicus during acoustic
constant-lift reaction per se, finding no reliable avoidance responses (Moiseff, Pollack & Hoy, 1978 ;
evidence that individual locusts consistently main- Pollack & Hoy, 1981 ; Pollack, Huber & Weber,
tain constant lift at different body angles. Although 1984 ; Miles et al., 1992), although abdominal
constant lift may occasionally be maintained, there deflection alone is apparently insufficient to produce
is usually considerable temporal variation in lift yawing in T. oceanicus (May & Hoy, 1990 b). As well
production (Zarnack & Wortmann, 1989). Weis- as increasing drag on the inside of a turn, hindleg
Fogh’s (1956 a, b) original studies neglected temporal extension may effect a turn by impeding the motion
variation in lift and were based upon data averaged of the inside hindwing (Camhi, 1970 ; May & Hoy,
across individuals, so the apparent constancy of lift 1990 a). This mechanism would be expected to cause
in his figures would certainly have been exaggerated significant wear to the wing and may therefore be
by the averaging process. reserved for extreme avoidance manoeuvres.
On the other hand, given that the angle of attack Lateral movements of the hindlegs and abdomen
of the hindwings increases following an increase in have also been observed in response to visual roll
body angle, whilst the angle of attack of the forewings stimuli in locusts (Taylor, 1981 a, b), but are incon-
remains approximately constant, the changing bal- sistently correlated with rolling (Thu$ ring, 1986) and
ance of lift between fore- and hindwings should said to be neither necessary nor sufficient to effect a
produce a restoring nose-down pitching moment. correctional roll response (Schmidt & Zarnack,
Such a torque was in fact detected by Gettrup & 1987 ; Waldmann & Zarnack, 1988). However,
Wilson (1964), but was considered to be an Zanker’s (1988 a) careful study of abdominal de-
‘ unpredicted outcome ’ (Gettrup & Wilson, 1964, p. flection in Drosophila melanogaster highlights the need
189) of the constant-lift reaction. This interpretation to ensure that the rotational axis of a roll stimulus is
almost certainly reverses cause and effect, since a exactly normal to the axis about which yawing
stabilising pitch response would negate any re- occurs. If this is not the case, then a supposed roll
quirement to maintain constant lift across a range of stimulus will induce a combined roll and yaw
body angles by restoring the animal to equilibrium. response because the subject will perceive the
Indeed, loss of the sensory input supposed to mediate stimulus to contain some component of yaw. This
pronation in the constant-lift reaction leads to a probably explains why postural changes normally
complete loss of stability (Gettrup, 1966), confirming associated with yaw turns are observed in response to
that the reflex changes in pronation described above roll stimuli, although we cannot discount the
are used to maintain pitch stability. Constant lift possibility that abdominal deflection might be used
may occasionally be maintained in tethered locusts to generate roll moments by shifting the centre of
according to Gettrup & Wilson’s (1964) original gravity. Alternatively, if roll and yaw are modulated
scheme, but probably as an epiphenomenon of together in free flight, then responses to roll and yaw
changes adapted to restore pitch equilibrium in free stimuli might be reflexly coupled to effect a tighter
flight. banked turn.
Asymmetries in stroke amplitude do not appear to
be strongly correlated with turning in locusts (Baker,
(2) Lateral control
1979 ; Thu$ ring, 1986 ; Waldmann & Zarnack, 1988 ;
Locusts swing their abdomen laterally and extend Zarnack, 1988) or crickets (Wang & Robertson,
one or both hindlegs like a rudder during yaw turns 1988 ; but see May, Brodfuehrer & Hoy, 1988),
(Gettrup & Wilson, 1964 ; Dugard, 1967 ; Camhi, except during very sharp turns (Robertson & Reye,
1970 ; Cooter, 1979 ; Arbas, 1986 ; Baader, 1990 ; 1992 ; Dawson et al., 1997). Likewise, there is no
Preiss & Gewecke, 1991 ; Robert & Rowell, 1992 a, b ; evidence that differences in stroke path are cor-
Robertson & Reye, 1992 ; Preiss & Spork, 1993 ; related with turning in locusts (Zarnack, 1988),
Robertson & Johnson, 1993 ; Lorez, 1995 ; Robert- although changes in hindwing elevation may be
son, Kuhnert & Dawson, 1996 ; Dawson et al., 1997). important for steering in crickets (Wang & Robert-
Such postural changes are not always observed son, 1988 ; May et al., 1988) which also bank their
during correctional responses, however, and may be forewings relative to the body axes during turning
more important during voluntary turns (Zarnack & (May et al., 1988).
Mo$ hl, 1977 ; Gewecke & Philippen, 1978). Similar Locusts (Gettrup & Wilson, 1964) and crickets
postural changes have been observed in the bush- (Pollack & Hoy, 1981) reliably increase pronation of
cricket Tettigonia viridissima (Schulze & Schul, 2001) the inside forewing during turning responses. In
locusts, this is usually correlated with early pronation made and it remains an open question whether
of the inside wing (Dugard, 1967 ; Baker, 1979 ; differences in motor pattern will prove sufficient to
Zarnack, 1988 ; Robertson & Reye, 1992 ; Dawson et separate roll and yaw control in locusts.
al., 1997). Muscle recordings from crickets are Bulk phase shifts between contralateral wings are
suggestive of an analogous change in the timing of bound to induce lateral asymmetries in the phase of
the hindwing elevators and depressors (Wang & the fore- and hindwings during roll responses,
Robertson, 1988). These changes should reduce lift because the timing of the hindwings changes less
and thrust on the inside wing by decreasing its than that of the forewings (Schmidt & Zarnack,
effective incidence and might allow it to act as a sort 1987) and may even change in the opposite direction
of brake (Zarnack & Mo$ hl, 1977). Antisymmetric (Thu$ ring, 1986). Lateral asymmetries in the relative
changes in pronation on the outside wing, possibly positions of the fore- and hindwings are certainly
combined with increased supination on the upstroke correlated with yaw responses in locusts (Dugard,
(Zarnack, 1988), should increase lift and thrust on 1967 ; Baker, 1979 ; Cooter, 1979 ; Robertson &
the outside of the turn. The net result will be a Reye, 1992 ; Robertson & Johnson, 1993) and will
combined roll and yaw torque, leading directly into inevitably alter the aerodynamic coupling of the
a banked turn. wings (Zarnack, 1982, 1983 ; Schwenne & Zarnack,
Intriguingly, opposite changes in the timing of the 1987 ; Schmidt & Zarnack, 1987 ; Waldmann &
forewing downstroke muscles have been recorded in Zarnack, 1988 ; Robertson & Reye, 1992). Whilst
tethered locusts during presumed correctional re- there is now little doubt that ipsilateral phase shifts
sponses to imposed yaw angles (Mo$ hl & Zarnack, are important in locust flight control (Rowell, 1988),
1975, 1977 ; Zarnack & Mo$ hl, 1977). These dif- the aerodynamic changes involved are unknown.
ferences seem to be real and may result from Contralateral interference remains unquantified in
differences in the turning stimuli used (Kammer, locusts, and it is not known whether interference
1985), although the oscillating yaw stimulus used by between contralateral wings has any direct effect
Zarnack (1988) was qualitatively the same as that upon steering.
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
VI. FLIGHT CONTROL IN OTHER INSECTS
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 Studies of flight control in other insects have been
motor pattern used (Thu$ ring, 1986), so different rather limited. Negative correlations between body
motor patterns must either produce the same angle and flight velocity similar to those observed in
kinematics, which seems unlikely, or they must cause Drosophila spp. have been observed in dragonflies
the forces and moments about the other axes to vary (Wakeling & Ellington, 1997), heteropteran bugs
(Kammer, 1985 ; Thu$ ring, 1986). (Betts, 1986), bumblebees (Dudley & Ellington,
This second explanation seems quite likely. For 1990 a), honeybees (Nachtigall, Widmann &
example, whereas all of the inside forewing de- Renner, 1971 ; Esch, Nachtigall & Kogge, 1975) and
pressors contract early relative to some constant moths (Dudley & DeVries, 1990 ; Willmott &
reference during a typical roll response (Mo$ hl & Ellington, 1997). Butterflies exhibit considerable
Zarnack, 1977 ; Zarnack & Mo$ hl, 1977 ; Thu$ ring, variation in the way in which body angle varies with
1986 ; Schmidt & Zarnack, 1987 ; Waldmann & flight speed, although this is perhaps not surprising
Zarnack, 1988), individual depressors may be time- given the extent to which butterflies ’ bodies pitch up
shifted in opposite directions during yaw responses and down through the course of the wingbeat cycle
(Mo$ hl & Zarnack, 1975 ; Zarnack & Mo$ hl, 1977). (Betts & Wootton, 1988 ; Brackenbury, 1995). For
In any case, Baker’s comment that roll and yaw example, whereas free-flying Papilio rumanzovia adopt
turns in locusts are ‘ just two ways of looking at the higher body angles and shallower stroke planes
same phenomenon ’ (Baker, 1979, p. 57) is certainly during fast flight, free-flying Troides rhadamantus
an over-simplification. Although independent modu- appear to show the opposite trend (Betts & Wootton,
lation of roll and yaw has never been observed in 1988). Such variation is presumably indicative of
locusts (Hensler & Robert, 1990), simultaneous differences in the aerodynamic mechanisms being
measurements of roll and yaw torques have not been used.
It is important to realise that a negative cor- appears to decrease slightly with increasing speed
relation between flight speed and body angle need (Willmott & Ellington, 1997). This is due to a less
not imply a helicopter-like mode of flight control, in ventral excursion of the wings on the downstroke,
which the direction of the flight force is fixed with which would tend to shift the resultant flight force
respect to the body axes. Such a model may apply in rearward as in flies and presumably provides the
honeybees Apis mellifica, in which the partitioning of nose-down pitching moment required to decrease
lift and thrust seems to depend directly upon body the body angle for fast flight.
angle (Esch et al., 1975), but in heteropteran bugs, Opposite trends have been noted in the dragonfly
for example, the inclination of the stroke plane to the Sympetrum sanguinem and the damselfly Calopteryx
body may be varied by as much as 20m (Betts, 1986). splendens. In these species, hindwing stroke amplitude
Likewise in hawkmoths Manduca sexta the stroke increases with increasing speed (Wakeling & Elling-
becomes steeper relative to the body at higher speeds ton, 1997), although the regressions were not
(Willmott & Ellington, 1997) and the same trend significant at the 95 % confidence level and there
has been observed in the dragonfly Anax parthenope was no apparent change in the mean positional
(Azuma & Watanabe, 1988). No such trend was angle of the wings. This does not appear to reflect a
detected in the dragonfly Sympetrum sanguinem in general trend in dragonflies. For example, whereas
which the stroke plane was apparently kept fixed no correlation was found between stroke amplitude
with respect to the body (Wakeling & Ellington, and flight speed in free-flying Anax parthenope (Azuma
1997). Nevertheless, the direction of the flight force & Watanabe, 1988), a strong negative correlation
does not correlate closely with the orientation of was observed in tethered Orthetrum cancellatum
either the body or the stroke plane in this or other (Gewecke, Heinzel & Philippen, 1974). Decreased
dragonflies (Wakeling & Ellington, 1997), and the stroke amplitudes in the latter were associated with
orientation of the stroke plane with respect to flight reductions in only the dorsal excursions of the wings,
direction is generally rather variable (Ru$ ppell, which would tend to shift the resultant flight force
1989). The correlation of body angle with flight forward, rather than rearward as in flies and
speed and direction in dragonflies has therefore been hawkmoths. If nothing else, these results caution
suggested to be an adaptation more to minimise against extrapolating control mechanisms from one
body drag than to redirect the flight force (Wakeling group of insects, or even one species, to another.
& Ellington, 1997). Wingbeat frequency appears not to be an im-
In bumblebees Bombus terrestris, the angle of attack portant longitudinal control parameter in either
the wings is increased relative to the stroke plane as hawkmoths (Willmott & Ellington, 1997) or dragon-
the body angle is decreased (Dudley & Ellington, flies (Azuma & Watanabe, 1988 ; Wakeling &
1990 a), with the result that the effective angle of Ellington, 1997), and has also been found to be
incidence of the wings remains more or less un- uncorrelated with flight speed in damselflies (Sato &
changed (Dudley & Ellington, 1990 b). In contrast Azuma, 1997 ; Wakeling & Ellington, 1997), and
to Drosophila spp., however, the position and am- bumblebees (Dudley & Ellington, 1990 a). Wakeling
plitude of the wingbeat do not appear to vary with & Ellington (1997) did, however, note a trend for
airspeed, and it is not known how changes in body wingbeat frequency to increase with increasing force
angle are brought about (Dudley & Ellington, production in the damselfly Calopteryx splendens
1990 a). Stroke amplitude does appear to be an (P 0n1). Although trends at the 90 % significance
important longitudinal control parameter in heter- level were deemed ‘ good ’ in that study (Wakeling &
opteran bugs, which display decreased stroke ampli- Ellington, 1997, p. 566), the significance of trends
tudes during climbing flight, together with an reaching even the 95 % level should be viewed with
increase in the speed of stroke reversal and a decrease caution given that some 52 independent regressions
in the wingbeat frequency (Betts, 1986). No clear were performed, grossly inflating the risk of making
trend has been found with respect to flight speed or a Type I error. Wingbeat frequency is decreased
direction and stroke amplitude in butterflies. For during rising flight in heteropteran bugs (Betts,
example, whereas free-flying Papilio rumanzovia and 1986), and there is reasonably strong evidence that
Graphium sarpedon have been observed to increase wingbeat frequency is positively correlated with
stroke amplitude during slow flight, free-flying Precis flight speed in butterflies (Betts & Wootton, 1988).
iphita adopt sharply increased stroke amplitudes However, given the high degree of interspecific
during bursts of fast flight (Betts & Wootton, 1988). variation revealed by the latter study in the
In hawkmoths Manduca sexta, stroke amplitude correlations between other kinematic parameters
and flight velocity, it would seem premature to in free-flight manoeuvres in dragonflies (Alexander,
interpret data from a few species as indicative of a 1984, 1986 ; Ru$ ppell, 1989) and hawkmoths (A. L. R.
more general trend. Thomas, personal communication). In hawkmoths,
the wings (which are normally physically coupled)
may be completely uncoupled so as to operate in
(2) Lateral control
antiphase. Such phase shifts are likely to be a com-
Postural adjustments like those observed in flies and mon feature of flight control in four-winged insects
locusts appear to be ubiquitous steering responses in and need not necessarily be restricted to insects
insects, having also been observed in mantids in which the wings are normally uncoupled.
(Brackenbury, 1995), heteropteran bugs (Govind &
Burton, 1970 ; Govind, 1972), strepsipterans (Pix,
VII. DISCUSSION
Nalbach & Zeil, 1993) and moths (Roeder, 1967 ;
Kammer, 1971 ; Kammer & Nachtigall, 1973).
(1) How many degrees of freedom do insects
Asymmetries in stroke amplitude like those observed
control?
in turning flies have also been observed in dragonflies
(Alexander, 1986), beetles (Burton, 1964, 1971 ; To date, three-axis control of the moments has only
Schneider & Kramer, 1974), moths (Kammer, 1971) been proven in larger flies and dragonflies. Exper-
and heteropteran bugs (Govind & Burton, 1970 ; iments to determine whether other insects can
Govind, 1972). In bugs, the stroke path of the modulate roll and yaw separately have simply not
outside wing may also be shifted dorsal to the inside been performed. However, since the most common
wing (Govind & Burton, 1970), which is similar to a mode of turning is the banked turn, in which roll and
steering mechanism identified by Stellwaag (1916) yaw are advantageously coupled to reduce the
in bees and similar to an atypical steering pattern turning circle, two-axis control of the lateral and
observed during yaw turns in locusts (Cooter, 1979). longitudinal moments could also suffice (Dickinson,
In moths and butterflies, the wings on the inside of 1999). Roll and yaw would then be modulated
a turn are typically held more posteriorly than the together about an axis lying somewhere between the
outside wings, and may be slightly flexed (Roeder, morphological roll and yaw axes. Tables 1 and 2
1967). These changes probably correlate with provide a summary of the various kinematic par-
changes in the timing of muscle firing (Kammer, ameters available for lateral and longitudinal control
1971, 1985 ; Kammer & Nachtigall, 1973 ; Obara, in flying insects. In the case of locusts, it is not
1975) and presumably reduce lift and thrust on the obvious whether independent control of forewing
inside wing. pronation and ipsilateral coupling would permit
In dragonflies, amplitude asymmetries lead to separate control of roll and yaw, or whether the
banking with a strong component of sideslip within different motor patterns observed during roll and
one or two strokes, usually followed by a component yaw responses result in further kinematic changes
of yaw (Alexander, 1986). This time lag suggests that have so far gone undetected. In Drosophila spp.,
that yawing may arise indirectly through aero- on the other hand, there are more than enough
dynamic coupling of the moments, rather than independent kinematic inputs to permit separate
directly through asymmetric thrust production. control of roll and yaw, although it is equally
Specifically, the component of sideslip resulting from possible that one or more of these inputs is redundant
banking means that the oncoming flow is no longer and is simply used to provide finer control of the
parallel to the longitudinal axis, which could lead to moments. For example, Zanker (1988 a) has found
the production of a coupled yaw moment. The inside that abdominal deflection and changes in stroke
wing may also be more strongly pronated than the amplitude are modulated together in Drosophila
outside wing during banked turns, although this is melanogaster to produce a common torque about the
usually secondary to changes in amplitude and may yaw axis. Three-axis control must therefore be
only be used to fine-tune the response (Alexander, considered an unproven possibility in Drosophila spp.
1986). Very sharp yaw turns involving much more Even where three-axis control of the moments can
extreme rotation of the wings have also been be proven, this does not imply that the control axes
observed in dragonflies (Alexander, 1986), sug- must be identical with the main body axes or indeed
gesting three-axis control of the moments. Phase that the control axes must be strictly orthogonal
shifts between the fore- and hindwings analogous to (that is, perpendicular to one another). For example,
those observed in locusts have also been implicated 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
dorso-ventral body axis in Drosophila melanogaster wings would already have been articulated and
(Zanker, 1988 a), though whether an independent muscularised at their base. However, they would
roll axis exists or whether this represents a combined probably not have possessed the degree of control
roll-yaw axis in a two-axis system is unknown. required for successful modulation of the flapping
Orthogonality of the lateral control axes is not cycle, unless their gill-like precursors were used for
essential for three-axis control, but any non-ortho- swimming. Hence, the evolution of improved wing
gonality that may exist will complicate the neural control – whether for gliding or for some other
processing required to separate the various motions. putative intermediate stage such as surface-skim-
As a useful but rather imperfect analogy, consider ming (Marden & Kramer, 1994 ; Marden et al.,
how difficult it is to predict the path of a bouncing 2000) – would almost certainly have been prerequi-
rugby ball compared to a bouncing football (it is site for the evolution of flapping flight. Indeed, a
difficult to find a better analogy, precisely because wing that has evolved rotations about three axes for
manmade control systems are usually designed to act control already has at least a rudimentary version of
orthogonally). The lack of separate control surfaces each of the fundamental motions of the stroke cycle,
to isolate the three moments actually makes it rather offering one possible route to the evolution of the
likely that insect control systems will be non- stroke cycle (Hinton, 1963 ; Wigglesworth, 1963,
orthogonal. For example, there is no particular 1976 ; Wootton, 1976).
reason to suppose that changes in stroke amplitude It is difficult to draw any firm conclusions as to the
will result in a torque about an axis orthogonal to stage of evolution at which different kinematic
that due to asymmetric changes in the degree of control mechanisms would have been acquired. It
pronation or supination. Hence, although the con- seems likely that the earliest flapping insects would
trol inputs of aircraft are not always strictly have had some control of stroke amplitude, allowing
orthogonal, non-orthogonality is likely to be much direct modulation of the aerodynamic power output
more pronounced in insects and this will tend to and at least a rudimentary degree of lateral control.
complicate their flight control. This is likely to be Changes in the degree of wing pronation are also
one of the most significant differences between the likely to have been important from the outset, being
flight control systems of insects and conventional a fundamental motion of any flapping wing. Changes
aircraft. The evolved interface between mechanics in stroke amplitude or the degree of wing pronation
and processing in a non-orthogonal control system would be expected to affect both steady and
should prove an especially fruitful field for inter- unsteady mechanisms of force production, though
disciplinary research. their effects could be qualitatively different de-
pending upon the mechanism used. For example,
increasing the stroke amplitude on one wing should
(2) Evolution of insect flight control systems
increase quasi-steady lift production, but might also
The ubiquity of postural flight control suggests that lower unsteady lift production by destabilising the
it may be a primitive character amongst pterygote leading edge vortex associated with delayed stall
insects. The necessary neuromuscular mechanisms (C. P. Ellington, personal communication, cited in
for postural control would have been in place long Betts, 1986).
before the evolution of the stroke cycle, so it would Many of the other control inputs that insects use
not be surprising if this were the main means of can only be understood in the context of unsteady
control during the early evolution of flight. Indeed, aerodynamics. This is especially true of those relating
if flapping flight evolved via an intermediate gliding to the speed and timing of wing rotation or to the
stage, then postural control could even have been phase of the fore- and hindwings. To a large degree,
used to stabilise the descent of smaller insects prior to then, the evolution of flight control in insects must
the evolution of wings (Flower, 1964). Current parallel their evolutionary refinement of unsteady
developmental, neurological and morphological evi- aerodynamic mechanisms, and differences in the
dence suggests that the wings themselves evolved kinematics of flight control between insect orders will
from gills or associated epipodal structures on the therefore reflect differences in the unsteady mech-
limbs of an aquatic ancestor (Wigglesworth, 1973, anisms used. For example, the reason that changes in
1976 ; Kukalova! -Peck, 1978, 1983 ; Wootton, 1981 ; the speed and timing of supination are an important
Robertson, Pearson & Reichert, 1982 ; Kingsolver & control input in Drosophila spp., whereas changes in
Koehl, 1994 ; Thomas & Norberg, 1996 ; Averof & the degree of pronation are not, is presumably that
Cohen, 1997). Under this scenario, the incipient rotational and wake-capture mechanisms are the
major source of unsteady force production in than as a fixed constraint. On the other hand, the so-
Drosophila spp. On the other hand, changes in the called ‘ constant-lift reaction ’ of locusts (Wilson &
degree of pronation do appear to be important in Weis-Fogh, 1962) appears not to be a reflex for
locusts, which presumably reflects the importance to maintaining constant lift at varying angles of attack,
locusts of translational mechanisms of aerodynamic but rather a mechanism to restore the insect to pitch
force production. equilibrium following a disturbance.
A corollary of this is that as our knowledge of (3) The number of degrees of freedom that insects
unsteady mechanisms and their relationship to wing are able to control cannot exceed the number of
kinematics improves, it may become possible to independent control inputs. Since the latter is usually
recognise the aerodynamic mechanisms being used quite high, it seems likely that some of the control
by a given insect on the basis of how the insect varies inputs will be redundant, providing finer control of
its wing kinematics during real or fictive man- the various degrees of freedom.
oeuvres. This is potentially more powerful than (4) Although most insects are likely to generate
looking merely at the kinematics of steady flight, control moments about all three axes, full three-axis
since it will always be difficult to assess the control has only been proven for larger flies and
importance of translational mechanisms such as dragonflies.
delayed stall, which, in contrast to rotational (5) Control inputs are unlikely to operate even
mechanisms, may have no clear kinematic mani- approximately orthogonally in insects. This will tend
festation. For example, the counter-intuitive re- to complicate the neural processing required to
duction in stroke amplitude that accompanies separate out the various motions.
elevated force production in heteropteran bugs (6) Taxonomic differences in insect flight control
(Betts, 1986) and hawkmoths (Willmott & Ellington, kinematics probably reflect differences in the un-
1997) may indicate that delayed stall accounts for a steady aerodynamic mechanisms being used. The
significant portion of peak force production, es- evolution of insect flight control is therefore likely to
pecially if the wingbeat frequency is reduced have paralleled the evolutionary refinement of
simultaneously as in bugs. Future studies of the unsteady aerodynamic mechanisms.
mechanics of insect flight control will have to take (7) Classification of an insect’s control kinematics
unsteady aerodynamics explicitly into account. during real or fictive turns could provide a relatively
Experiments correlating changes in the wing kin- simple assay for determining the dominant unsteady
ematics with instantaneous force measurements and aerodynamic mechanisms being used.
flow visualisation offer one way in which this might
be achieved.
IX. ACKNOWLEDGEMENTS
VIII. CONCLUSIONS I am grateful to Adrian Thomas and Robert Nudds

for their comments upon the manuscript and thank
(1) The current literature does not permit a Bob Srygley for the image of the hawkmoth. The
formal, quantitative analysis of insect flight control, comments of an anonymous referee were extremely
because the aerodynamic force systems that biol- helpful in improving the manuscript. This work was
ogists have measured have rarely been complete, funded by a Christopher Welch Scholarship from
and because the position of the centre of gravity has the University of Oxford.
rarely been recorded in studies of insect flight
control. Future experimental studies will need to pay
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Biol. Rev. (2001), 76, pp.

449–471 " Cambridge Philosophical Society 449

Mechanics and aerodynamics of insect flight

(Received 7 November 2000 ; revised 14 June 2001

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

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

I. INTRODUCTION ematics with neurobiology and muscle mechanics

inputs. This is the first and most fundamental

Having considered some general principles of A B

IV. FLIGHT CONTROL IN DIPTERA (TRUE

Flies are the most aerobatic of insects, able to turn on

Diptera : Independent Amplitude Could be used ? Independent Independent Not

Diptera : Independent Amplitude ? Supination delayed Pronation Not applicable

VIII. CONCLUSIONS I am grateful to Adrian Thomas and Robert Nudds

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