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Table 2. Independent kinematic parameters (bold) available for lateral control in dierent insects
Stroke trajectory Stroke amplitude
Clap-and-peel or
clap-and ing
Supination: speed
and timing of
rotation
Degree of
pronation
Phase of ipsilateral
fore- and hindwings
Diptera:
calypterate
ies
Independent
parameter; could
be used for lateral
control.
Amplitude
decreased on
inside wing
? Supination delayed
on inside wing
Pronation
sometimes
increased on
inside wing
Not applicable
Diptera:
drosophilid
ies
Independent
parameter; could
be used for lateral
control ; stroke
inclination
apparently linked
to amplitude
Amplitude
decreased on
inside wing
Wings meet at an
angle to the
sagittal plane
during turns
Supination delayed
on inside wing;
speed of
supination
increased on
outside wing
Degree of pronation
probably not an
important control
parameter
Not applicable
Orthoptera:
locusts
Probably not an
important control
parameter
Probably not an
important control
parameter
Not usually
applicable
Probably not an
important control
parameter
Pronation
increased on
inside wing
Likely to be
important. Eects
unknown
Odonata:
dragonies
? Amplitude
decreased on
inside wing
during banked
turns
Not applicable to
dragonies
? Pronation
increased on
inside wing,
especially during
yaw turns
Likely to be
important; eects
unknown
466 Graham K. Taylor
dorso-ventral body axis in Drosophila melanogaster
(Zanker, 1988a), 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 dicult it is to predict the path of a bouncing
rugby ball compared to a bouncing football (it is
dicult to nd 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 ight control. This is likely to be
one of the most signicant dierences between the
ight 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 eld for inter-
disciplinary research.
(2) Evolution of insect ight control systems
The ubiquity of postural ight 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 ight. Indeed,
if apping ight 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
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 apping
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 apping ight. 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,
oering one possible route to the evolution of the
stroke cycle (Hinton, 1963; Wigglesworth, 1963,
1976; Wootton, 1976).
It is dicult to draw any rm conclusions as to the
stage of evolution at which dierent kinematic
control mechanisms would have been acquired. It
seems likely that the earliest apping 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 apping wing. Changes
in stroke amplitude or the degree of wing pronation
would be expected to aect both steady and
unsteady mechanisms of force production, though
their eects could be qualitatively dierent 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 ight control in insects must
parallel their evolutionary renement of unsteady
aerodynamic mechanisms, and dierences in the
kinematics of ight control between insect orders will
therefore reect dierences 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
467 Mechanics of insect ight 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 reects 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 ctive man-
oeuvres. This is potentially more powerful than
looking merely at the kinematics of steady ight,
since it will always be dicult 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
signicant portion of peak force production, es-
pecially if the wingbeat frequency is reduced
simultaneously as in bugs. Future studies of the
mechanics of insect ight control will have to take
unsteady aerodynamics explicitly into account.
Experiments correlating changes in the wing kin-
ematics with instantaneous force measurements and
ow visualisation oer one way in which this might
be achieved.
VIII. CONCLUSIONS
(1) The current literature does not permit a
formal, quantitative analysis of insect ight 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 ight
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 insects moments of inertia.
(2) Two inuential paradigms in the insect ight
control literature appear either to have been widely
misinterpreted or to be a misinterpretation of the
empirical data. Specically, although Drosophila spp.
normally modulate lift and thrust together, the
helicopter model of their ight control is probably
better thought of as a facultative strategy, rather
than as a xed constraint. On the other hand, the so-
called constant-lift reaction of locusts (Wilson &
Weis-Fogh, 1962) appears not to be a reex 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 ner 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 ies and
dragonies.
(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 dierences in insect ight control
kinematics probably reect dierences in the un-
steady aerodynamic mechanisms being used. The
evolution of insect ight control is therefore likely to
have paralleled the evolutionary renement of
unsteady aerodynamic mechanisms.
(7) Classication of an insects control kinematics
during real or ctive 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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