Comparative Physiology of the Flight Motor

Comparative Physiology of the Flight Motor J. W. S. PRINGLE Department of Zoology, University of Oxford, England I. Introduction

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IC. The Generation of Lift and Thrust .

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General The flight of Coleoptera . Gliding flight of Lepidoptera . The flight of small Diptera . Kinematics of Wing Motion . A. Diptera B. Apis mellifera . IV. Stability in Flight . A. Diptera . B. Other insects . V. The Motor Mechanism of Flight Reflexes . A. List of reflexes . B. Initiation, maintenance and termination of flight C. Control of amplitude, frequency and power . D. Control of velocity E. Control of lift . F. Control of attitude VI. Comparative Studies . A. Axioms B. Differentiation of the flight muscles . References . A.

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1. I N T R O D U C T I O N The study of flight has now thrown light on such diverse aspects of insect physiology that it is impossible to discuss the whole of the subject in a single article. This review will be concerned largely with mechanical phenomena and it has as its objective an understanding of the effector mechanism responsible for motion in the air. Part of the problem is the elucidation of the lines of evolution of the flight system in the various orders. The review will not be concerned with energetics (Weis-Fogh, 1961), with the biochemistry of flight muscle (Maruyama, 1965; Sacktor, 1965) or the control of metabolism (Harvey and Haskell, 1966), nor with central nervous organization responsible for the control 163

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of flight, which is dealt with in a separate article in this volume (Wilson, 1968); these topics have been adequately treated elsewhere. The work to be summarized will be that done recently on the kinematics and aerodynamics of the wing motion, the reflex regulation of that motion and the arrangement and physiology of the power-producing and controlling muscles. The peculiarities of the contractile mechanism of fibrillar flight muscle have recently been considered from a biophysical and biochemical point of view (Pringle, 1967) and will here be treated functionally; that is, in relation to the design of the flight system as a whole. The self-oscillatory property of fibrillar muscle profoundly affects both the nervous and skeletal organization of those insects that possess it and the evolution of this property in several distinct lines within the Insecta must have involved parallel modifications of all parts of the flight machinery. It is at present by no means clear how efficient flight was possible during some of the stages through which these insects must have passed. Since it may be assumed, however, that such functional continuity was achieved in each case, useful clues to the nature of the constituent physiological mechanisms may be obtained from functional arguments. 11. THEG E N E R A T I O OFNL I F TA N D THRUST A. GENERAL

The ultimate requirement for the flight motor is that it should generate sufficient lift to support the weight of the insect and sufficient thrust to pull it through the air. Tn the absence of independently movable tail surfaces, as in birds and aeroplanes, there is a further requirement that the lift and thrust must be controllable in such a way as to enable the insect to balance and to turn and move in the required direction. Since lift and thrust are produced by the interaction between the air and the moving wings, aerodynamics must come first in any discussion of the design of the flight system. In their comprehensive review of earlier theories about the aerodynamics of insect flight, Weis-Fogh and Jensen (1956) emphasized the dangers of simplifying the problem. As they remarked, natural flapping flight is a complicated type of locomotion, and a misleading picture can easily be obtained if the kinematics of the wing motion are not known in detail. Weis-Fogh’s (1956a) analysis of the kinematics of normal locust flight enabled Jensen (1956) to make the first accurate study of the aerodynamics of an insect, and, as a result, it can be stated with some certainty that for an insect of the size and shape of Schistocercu grcguriu,

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beating its wings at about 17 beats per second, classical steady-state aerodynamic theory provides a quantitative explanation of the forces generated by the wing motion (summary in Pringle, 1957). In order to appreciate the researches that have been made since then, it is important to understand why this does not solve the problem for other insects. The complications that arise are matters of scale. Small insects move through the air at low speeds, but if the wing beat frequency is high, the movement involves high accelerations. Vogel(l964) points out that size and speed of the air-flow are complementary factors, since the Reynolds number, the relevant index to the flow rigime, involves a product of length and velocity. [(Re) = (pVd)/q, where p is the density of the air and q is its viscosity.] For the flight of Schistocerca gregaria, (Re) is approximately 2000 (Jensen, 1956). At such values and above, turbulent motion can occur in the air and high values of the lift coefficient C, are obtained from well-designed aerofoils at optimum angles of attack. As (Re) falls to a value of about 100 the maximum lift coefficient gets less and is obtained at higher angles of attack (45-50"; Thom and Swart, 1940; Vogel, 1966, 1967b); the drag coefficient increases and becomes less dependent on the angle of attack. Finally at values of (Re) less than about 20, vortices cannot form and the drag coefficient remains greater than the lift coefficient at all angles of attack; the drag is now almost entirely due to skin friction and is independent of the shape and orientation of the object, being merely proportional to its surface area. Horridge (1956) has argued that very small insects must fly by so changing the surface area of the wings that the drag is different on the down- and upstrokes. Insects with a wing length of less than 0.1 mm tend to have the wing reduced to a central rod with fringes of hairs (Pringle, 1957) and this may facilitate such a change in surface area. Even before the scale of size is reached at which drag rather than lift forces become the dominant feature of the aerodynamics, complications may be introduced by the accelerations implicit in the high frequency of beat in small insects. It is known that higher lift coefficients can occur if the incidence is changing rapidly and if the air is accelerating over the wing surface (Moore, 1956). If an appreciable quantity of air is entrained by the wing motion, the actual angle of attack on the air may not be that deducible from the inclination of the wing and the direction of overall movement. Particularly at low Reynolds numbers, the air mass contained in the boundary layer or an even larger induced mass may be accelerated by the wing motion and contribute to the aerodynamic forces. The reality of this last effect was established by Vogel (1962), who showed that the inertia of the boundary layer could make a signi-

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ficant contribution to the total mass in the mechanically-resonant wingthorax system. In insects where the index P . f-liz.M;’ is large ( I = wing length, f = frequency, M , = wing mass) the inertia of the boundary layer contributes appreciably to the total. Vogel computed this index for those species in which Sotavalta (1952) had shown an effect of air density on the wing-beat frequency and found values between 40 and 190; for those species where beat frequency was independent of air density, the index was between 8 and 20. The extent to which these factors are important can only be decided by detailed examination of the flight of each type of insect. This is now widely appreciated by biologists, but aeronautical engineers are still occasionally tempted into thinking that a n answer can be found by theoretical or practical study of a simplified situation. In the years preceding Weis-Fogh and Jensen’s study of the locust, the most elaborate of these theoretical exercises was that of Osborne (1951), who derived formulae for computing the lift and drag coefficients and the total power of an insect from structural measurements and then applied the formulae to the data of Magnan (1934). The results, in several cases, produced values for the lift coefficient which would be impossible under steadystate conditions with slightly cambered aerofoils, and Osborne concluded that aerodynamic inertial forces due to wing acceleration must play a significant r61e. Weis-Fogh and Jensen (1956) criticized this conclusion on the grounds that the data of Magnan (1934) were not all obtained under the same conditions; they showed that Osborne’s formulae did not give unusually large values of the lift coefficient when used with their own, more reliable measurements of the flight of Schistocerca nor with their reasonably postulated flight data for a “horse-fly ” or a “mosquito”. The Reynolds numbers for these idealized types of “small” insect would be about 5000 and 800, respectively, at which the flow rCgime is nearly normal.

B. T H E F L I G H T O F C O L E O P T E R A

1. Wings

Recently Bennett (1966) has revived the discussion on the basis of an experimental study of a model of the wing of MeIoIontha vulgaris, one of the insects for which Osborne’s analysis of Magnan’s data produced the high value of 2.0 for the mean lift coefficient on the downstroke. The model was made from cellophane stretched over a wire frame and

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was dtiven in such a way that its angle of attack* changed sharply at the top and bottom of the stroke (Fig. 1). The resulting motion was compared with that of the insect in flight, as analysed frame by frame from high-speed motion pictures and was said to differ in three respects: (1) the effect of the elytra was omitted; (2) the rate of change of angle CELLOPHANE TAPE M

TYPICAL WING SECTION

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LATERAL SECTION FIG.1. Mechanism simulating wing movement of Melolonthu. (Bennett, 1966).

of attack was much less, requiring 20 degrees of stroke for completion in the model compared with only 5 degrees in the insect; (3) no attempt was made to simulate wing twist or section camber. The interaction between the two wings was simulated by placing a fixed surface as an image plane in the insect’s vertical plane of symmetry; forward motion * “Angle of attack”, in this review means the inclination of the wing surface to an axis

in space or the longitudinal axis of the body. The term “incidence” refers to the angle of the wing surface to the true wind direction.

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was reproduced with a wind-tunnel. With the model in flapping motion, instantaneous induced air velocities were sampled with a hot-wire anemometer of short time constant placed upstream and downstream of the flapping plane around an azimuthal arc at 0.7 of the wing span; the magnitude and direction of the air-flow were thus determined. By analysis of the oscillograms, a measure was obtained of the vertical and horizontal components of the time-averaged induced velocity upstream and downstream. Propeller theory was then used to derive a value of 1.06g for the vertical force; the difference of this from the weight of the insect, 0.96g, is said to represent errors in modelling, in experiment and in calculation. Since the Reynolds number for this model was 3100, the conclusion that the lifting process results from increase in the downward momentum of the air passing through the flapping plane (i.e. from a normal type of lift coefficient), rather than from a high drag coefficient during the downstroke, is hardly unexpected. More controversial is the claim that unsteady effects dominate the simulated performance. The vertical impulse experienced by the air moving through a unit area located at the mid-downstroke azimuth position in the course of a single stroke was computed by integrating the instantaneous vertical force with respect to time; the value obtained was 3.32 x g sec/cm2. Near steady-state conditions were then set up by allowing the model wing to perform a complete rotation (instead of a flapping motion) at the same incidence and with the same tangential velocity; the value was now 1.67 x g sec/cm2. Finally true steady-state conditions were established by setting the wind-tunnel axis normal to the propeller disc g sec/cm2. and adjusting the air speed; the value was now 1-19x Bennett concluded that these experiments do not support Jensen’s (1956) conclusion that insect flight may be treated as a sequence of stationary flow situations. Apart from the possibility that there were undetected differences in the radial component of the air-flow under the three conditions (these would not have been detected by the experimental set-up), it does appear to have been established that unsteady flow effects dominated the performance of the model tested. The author states that it cannot yet be decided whether these were due to vigorous “destalling” (effects due to wing acceleration) or to virtual mass forces (effects due to the inertia of the boundary layer and other air in induced motion). He should also have said that it cannot yet be decided whether the conclusions apply to the actual flight of the insect, since errors in modelling might produce a larger effect than was assumed. The differences between the performance of the model and that of the insect were considerable. Sotavalta (1952) states that the amplitude of the wing

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stroke in Melolontha is 180", not 150" as in the model; he gives the beat frequency as 62/sec, not 46/sec. The interaction between the two wings may not have been correctly simulated by the image plane, and there were certainly important errors in the angles of attack at the top and bottom of the stroke. Changes in camber and twist during the stroke were not simulated. Against Bennett's conclusion is the fact that Melolontha vulgaris is not an insect in which the inertia of the boundary layer would be expected to be significant. Sotavalta (1952) did not study the effect of air density on the wing-beat frequency of this species, but application of Vogel's (1962) index to Sotavalta's structural data gives a value of 11.2; this is well within the range over which the inertia of the boundary layer is negligible. 2. Elytra Bennett (1966) considered that the contribution of the elytra to the total vertical force would be small, owing to their low flapping speed. It has usually been assumed that the elytra, which except in Cetoniidae are held extended at a pronounced dihedral angle, contribute at least to the stability of flight. Stellwaag (1914) found that, although slow flight was possible after unilateral extirpation of an elytron, the insect flew forward in a wide curve. The aerodynamics of the elytra have now been studied experimentally in Oryctes boas by Burton and Sandeman (1961) and in Melolontha by NachtigaIl(l964). Burton and Sandeman (1961) showed by stroboscopic illumination that the elytra were not stationary but moved through an angle of 20" in phase with the wings; their angle of incidence changed from 20" at the top of the stroke to 34" at the bottom. Measurements were made of the lift generated by an insect with its two elytra fixed in their middle position and mounted in a simple wind-tunnel at various angles of attack; similar measurements with elytra removed made it possible to calculate the contribution of the elytra. The results given appear not to be very exact and the lift is only approximately proportional to the square of the velocity above 10" incidence. The data have been plotted in Fig. 2 as L / V 2 ( L = lift produced by the elytra as a percentage of body weight; V = wind speed) and values of the lift coefficient C, have been calculated for a body weight of 5.2 g and a n elytral surface area of 7.2 cm2 (values measured from a large specimen of Oryctes rhinoceros, which is similar to 0. boas). A curve can be drawn through the experimental points which is of the type expected for a highly cambered aerofoil. There is a distinct stall at about 25" incidence and the value of C,,,, of 1.2 is reasonable. Burton and Sandeman

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state that in their wind-tunnel the preferred flying speed at which the net drag was zero was about 4m/sec and that under these conditions the angle of attack of the elytra, at their mid-stroke position, was 26"; they are then producing lift equal to 21% of the body weight. In the more exact study of Melolontha by Nachtigall(1964), measurements of lift and drag were made at a single air speed of 2.25 m/sec at a Reynolds number of lo00 (Fig. 3). The derived curve for the lift of the elytra again shows a pronounced stall at about 30"incidence. Their drag

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FIG.2. Lift produced by the elytra of Oryctes boas at different angles of attack. (Data of Burton and Sandeman, 1961, replotted as described in the text).

is high but the lift exceeds the drag by a small amount over a range of incidences from 8-28'. In the combination of body plus elytra, the drag is always greater than the lift, but the presence of the elytra does improve the lift/drag ratio and under optimum conditions they can carry perhaps 10% of the body weight. They are not held in flight in the position that would give the maximum lifting effect, but at a pronounced dihedral angle; for this reason and because of large errors introduced by small uncertainties in the air velocity, Nachtigall does not consider that it is justifiable to compute values of C, and C , (personal communication). He quotes Demo11 (1918) and his own unpublished observations that Melolontha cannot fly when its elytra have been removed and sug-

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gests that this is due to upset to the resonance of the whole thoracic system rather than to loss of the small contribution that the elytra make to the aerodynamic forces. A further uossible r81e in conferring lateral stability is discussed later.

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FIG.3. Lift L , + , and drag D B f Eof the body with elytra of Melolonrha at different angles of attack. Curves L E and DE are derived curves of lift and drag for the elytra alone. (Redrawn from Nachtigall, 1964, with ordinate values corrected). C. G L I D I N G F L I G H T OF L E P I D O P T E R A

Nachtigall (1967) has made accurate measurements in the windtunnel of the lift and drag of six species of Lepidoptera when the wings were fixed in their gliding attitude. No great differences were found between the different species. Figure 4 shows a polar plot of the lift and drag for a mounted specimen of Agupetes gulutheu. This plot is convenient for showing a number of features of the aerodynamics: (1) For a very slightly cambered wing, the maximum lift occurs at the high angle of attack of 30-40". Jensen (1956) found a maximum at about 15" for the fore-wing of the locust and 25" for the hind-wings. The maximum value of C, works out at about 0.85 (estimated wing area, 8.5 cm2) as compared with 1.3 for the fore-wings and 1.1 for the hindwings of Schistocercu. Both effects may be related to the flexibility of

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the butterfly wings; Jensen points out that flexibility of the locust hindwing can make a difference of 15" in angle of attack between the tip and the base. (2) The stall is very gradual, so that there will be little loss of control if the incidence for maximum lift is exceeded. (3) On this plot, the maximum ratio of lift to drag is given at the point at which a line through the origin touches the curve at a tangent. The angle that this line makes with the lift axis gives the best gliding angle, which is 15-24' in different specimens.

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FIG.4. Aguperes guluthru (Lepidoptera). polar plot of lift and drag of a mounted insect in 2.0 m/sec air-flow. Angle of attack indicated on curve. (Redrawn from Nachtigall, 1967).

(4) Both lift and drag depend on the square of the air speed; the shape of the polar therefore changes with air speed. Without knowing the weight of the live insect (Nachtigall did not have fresh specimens available) it is not possible to determine the minimum flying speed needed to produce lift sufficient for support. There is also insufficient information in this paper to justify the statement that the flatness of the polar near the region of maximum lift results in absolute flight stability. Stability in flight depends on the direction of chord-wise travel of the centre of aerodynamic pressure when the incidence changes. It will be

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helped by the smooth stall and the span-wise twist (“wash-out”) which is stated to be present, but these are secondary influences. The influence of the wing hairs and the wing scales was also studied (see also Nachtigall, 1965). Removing the hairs slightly improved the aerodynamic performance, but removing the scales definitely worsened it, particularly near the region of maximum lift where the reduction varied between 10 and 35%. The scales must act in a manner not fully understood to delay the turbulent break-away of the air-flow on the top surface as the wing approaches stalling incidence. D. T H E F L I G H T O F S M A L L D I P T E R A

Owing to the absence of complications due to the second pair of wings, flies have always been favourite insects for study of the aerodynamics of flight. Apart from some of the larger Nematocera, the wingbeat frequencies are high (Sotavalta, 1947) and at some point in the scale of size covered by the Diptera departures from steady-state aerodynamics are to be expected. Although it cannot yet be said that this point has been determined, several notable advances have been made since 1957. A great gap in knowledge has been filled by Nachtigall’s (1966) detailed account of the kinematics of wing motion in Phormia regina, but since this does not include actual measurements of lift and drag it will be discussed in the next section. A brief note by Baird (1965) reports some strain gauge measurements of lift and drag in Sarcophaga bullara and their correlation with wing position as determined photographically. Unusually high peak values of lift were obtained during brief periods in the cycle, and it is suggested that useful forces are obtained on the upstroke. The full report of this work will be of interest. The first experimental stljciy of a small insect is described by Vogel ( 1966), who established the flight performance of Drosophila uirilis at a Reynolds number of about 100. The lift required to support the body weight (2.0 dynes) was produced at a forward speed of 200 cm/sec with a body angle (upward tilt of the longitudinal axis) of 10”(Fig. 5); during this “standard performance” the beat frequency was 195/sec, the stroke angle 146” and the stroke plane angle +65”. The effect of the low Reynolds number was shown in the slight dependence of the parasitic drag on the body angle; perhaps because of this, there was one notable simplification of the flight control mechanism from that found in the locust. All the stroke parameters measured were found to be independent of the body angle; tilting the fly thus caused the lift and “preferred flying speed” (the speed of air movement at which the net drag was

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zero) to vary with the body angle over the range from - 10 to + 40". I n the locust, experimental change of the body angle brings into play the lift control reaction (see page 209), through the operation of which the lift tends to remain constant; because of this, it is impossible to influence the lift significantly by changing the body angle between 0" and 15-20" (Weis-Fogh, I956a, b). Vogel went to some pains to establish that the performance achieved by his tethered flies was comparable to that in free flight. He found that in free flight the forward velocity was usually less than 200 cm/sec, but that the freely flying animals were climbing along paths 15" to 20" above I

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FIG.5. Flight performance of a specimen of Drosophi/u uirilis. <-), lift; 0 , "preferred flying speed". Dashed lines mark values of body angle and flying speed at 100% lift. (From Vogel, 1966).

horizontal. The speed achieved by tethered flies in the wind-tunnel at 100% lift (equal to the body weight) was near to the maximum possible and occurred with the stroke plane nearly vertical ; under these conditions the forward distance travelled during one full wing cycle was just over twice the total span of both wings, which is a reasonable maximum by conventional standards of propeller performance. The conclusion from this part of the investigation was that the direction of the aerodynamic output force is primarily determined by the body angle and that variations in lift and flying speed can be explained

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in terms of a simple actuator disc with variable inclination, and not by changes in the form of the beat or of the angle of attack. This does not, however, imply that other parameters cannot be changed for short periods; and, in a further paper, Vogel (1967a) describes observations of those flight performances which, though not “successful” in the sense that steady values of lift and preferred flying speed were maintained for the prescribed period, provided useful information about the methods used for “voluntary” control. Body angle was now experimentally fixed at a single value for all measurements on each individual fly and performances were selected in which lift and air speed varied erratically. Flash photographs of 1 psec duration were taken at random times from a position in front of and 40” above the specimen, and from examination of these exposures it was possible to get an indication of changes in the stroke parameters accompanying particular performances. The main results were: (1) Wing-beat frequency changed very little under any conditions. In no case was the frequency more than k 10% of the average value and there was no correlation between frequency and other parameters. A slight decline in frequency was sometimes noted during the course of experiments on a particular fly; lift and thrust were then proportional to the square of the frequency, as in propellers. Since in a flight system powered by fibrillar muscle the frequency is largely determined by mechanical resonance, this parameter is effectively eliminated from those available for control. Vogel points out that, in an insect in which the inertia of the boundary layer has been shown to be a significant fraction of the total wing mass, there should be some influence on frequency of increase in stroke angle or flying speed, since these should reduce the moment of inertia of the boundary layer, but the effect is evidently too small to be detected. (2) Stroke angle (=amplitude of beat) and stroke plane were found to be fully interdependent parameters. The position of the wing at the top of the stroke did not change; increase in stroke angle from 90” to 150” was accompanied by a forward shift in the position of the bottom of the stroke, with only a slight change in its vertical position relative to the body axis (Fig. 6). There was a corresponding change in lift and thrust, and thus of total power. (3) In relation to the insect the angle of attack of the wing surface changed during the beat but was constant over the whole length of the wing, so that the movement was one of rotation from the base, rather than twist along the span. The angle was nearly constant during the whole of the downstroke and was not affected by the flying speed; the

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wing motion thus appeared similar in still air, when the middle of the wing was moving at 200 cm/sec, and in a 200 cm/sec air-flow. Since the incidence to the relative wind must have been very different under these two conditions, this means that there is no regulation of this parameter. Furthermore, since the wing performs an angular movement, an angle of attack which is constant over the span implies a variation in incidence along the length of the wing when there is any appreciable translational movement of the air relative to the fly.

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(4) The wing profile was flat during the upstroke, but a slight camber appeared during the lower two-thirds of the downstroke. Lengthwise bending was observed near the wing base. Both these effects were in the opposite direction from that expected from passive deformation caused by the air-flow and must be actively produced. Alteration of air speed did not change the surface contour of the wing but produced a slight backward shift of the stroke plane.

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The main conclusion from this work was that lift and thrust are increased by Drosophila primarily by increase of the stroke angle, which also changes the stroke plane by moving forward the bottom part of the stroke. No measurements were made of the pitching moment (torque about the transverse axis of the fly) which this might produce, but Vogel points out that there should be a forward movement of the line of action of the total aerodynamic force tending to increase the body angle. Since the earlier study showed that increasing the body angle increases the lift and decreases the preferred flying speed without change in the stroke parameters, the overall result of an increase in stroke angle in free flight will be to make the fly climb more steeply with lower forward velocity. I t is, however, unlikely that this is the only means of control, since there would then be an invariable coupling between power output and the direction of flight. Some control may be exercised by the hind-legs, which are not held tightly against the body as are the proand mesothoracic legs, but control of some other unidentified parameter is also probable. In a third paper Vogel (1967b) has described the aerodynamic characteristics of the Drosophila wing and compared them with those of flat models in the same dimensional range. The most notable features were : (1) the greater L / D ratio at positive angles of incidence of the cambered as compared with the flat wing and the slightly better performance of the flat wing at negative incidence, such as is found during the upstroke. Camber was more effective in the wing than in the models. (2) near constancy of the lift coefficient of the wing over an incidence range from 20-50" (Fig. 7), compared to the distinct stall of the models. Vogel showed by use of the wind-tunnel balance and by means of visualized flow patterns how the stall of the models occurs at higher angles of incidence as (Re) is reduced from 200 to 60; this is the critical range for change of the flow pattern. The stall is further prevented in the natural wing by the microtrichia on the wing surface, which must influence the flow even though they lie within the boundary layer; their function may be to prevent backflow along the top surface, the occurrence of which is known to promote vortices and stalling. It is pointed out that hairs are retained only over the critical parts of the surface (the distal and posterior parts) in partly glabrous wings and that hairiness correlates inversely with aspect ratio (span/chord) in biting midges ; a broad wing is more liable to stall than a narrow one and the hairs may compensate for this.

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The polar curves for a conventional aerofoil, Schistocerco and Drosophilu, are compared in Fig. 7. The constancy of the lift coefficient over a wide range of angles helps to explain the absence of twist in the wing during flight. Due to the angular motion, there must be a very different incidence to the relative wind at tip and base during forward flight, but no part of the wing will stall. Owing to the low Reynolds number, the maximum LID ratio is small, but it does not necessarily follow that flight is energetically inefficient. In this dimensional range, C, is still 1

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FIG.7. Polar diagrams of three different airfoils. A. Conventional profile, NACA 2409, aspect ratio of 6, ( R e ) == 5 x lo8. B. Schistocerca hind-wing, (Re) == 4 x lo3. C. Drosophilu wing, ( R e ) 2 x lo2. On each curve the point of maximum LID is marked, with its value underlined. (From Vogel, 1967b).

greater at high than at low angles of incidence and the fly may obtain some effective lift and thrust forces from the wing drag during the downstoke, which under some circumstances may be inclined downwards and backwards instead of downwards and forwards as in larger insects (Fig. 6). It is not clear whether Vogel took this factor into account in his approximate computation of the expected overall performance from the kinematics of wing motion and the aerodynamic measurements on the

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wings. He found values for the total integrated forces that were only half those needed to sustain flight, but he cautions that the conclusion should not be drawn from this that stall hysteresis and other non-steadystate factors must be important in Drosophila. 111. T H EK I N E M A T I COSF W I N G M O T I O N

It will be apparent that a proper understanding of the aerodynamics of insect flight can only be achieved when full information is available about the precise form of the wing motion. If the beat frequency is sufficiently constant, such information can be obtained stroboscopically; that is, by illumination with brief flashes of light phased to known instants in the stroke cycle. More satisfactory, if the equipment is available, is continuous cinematography at really high speed, since one can then analyse single wing strokes. There remains, however, the problem of describing in a manner which can be appreciated by the reader the vast amount of information so obtained. A. D I P T E R A

Nachtigall (1966) has now used high-speed cinematography to make a detailed study of the form of the wing movements of the large fly Phorniia regina under two well-defined conditions. “Free flight” is defined as the flight of a fly suspended by the tip of the abdomen in an air-flow just sufficient to keep it stationary in space and mounted in a way that permits the fly to take up its preferred orientation; “flight in still air” is the condition when the fly is fixed in space with no air-flow. The wing movements are very different under these two conditions. For a complete description of the results it is necessary to define several reference systems. The system with axes related to the longitudinal axis of the body is defined as the t-system. That with axes related to the direction of the air-flow is the e-system, and that with axes related to the geoclinic vertical is the g-system. In each system, the vertical (or near-vertical) axis is the z-axis, the transverse axis is the y-axis and the longitudinal axis is the x-axis. Suffixes denote the system of reference in use. Thus, since in this investigation bilateral symmetry was always preserved, y, = y e . The body was, however, sometimes tilted up by the body angle, so xt # x, and zt # 2,. Under the conditions studied so far, the e-system and the g-system were coincident. The wing-tip moves on a great circle and various forms of description are possible in two-dimensional graphs. Figure 8 shows the wing-tip path of three different strokes as a projection of the surface of a globe.

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J . W . S. PRINGLE

FIG.8. Path of the wing-tip of Phornzio reginn in "free flight", plotted on the surface of a sphere centred on the wing base; ends of strokes shown separately. (From Nachtigall, 1966).

Figure 9 shows the time course of angular movement in the three planes of the t-system. Both these figures related to a fly in fast, forward flight. Figure 10 shows silhouettes from the three axes of the t-system during one complete stroke. The pro-jections of Figs I 1 and 12 are more complicated. The stroke plane is defined as the plane of the great circle which most nearly coincides with the wing-tip path; if this circle is developed

FIG.9. Time course of angular movement of the wing of Phormia regina in fast, free flight, plotted in the three planes defined by the body axes (t-system). Points are individual frames at 1/6400 sec interval. (From Nachtigall, 1966).

FIG.10. Silhouettes of fly from direction of the three body axes during one complete wing beat. (From Nachtigall, 1966).

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into a line by unrolling the left or right half-cylinder on whose surface it lies and whose axis is the longitudinal axis of the fly, the path of the wing-tip is described by the two-dimensional plot of Fig. 11. Unrolling the half-cylinder whose axis is the direction of the air-flow produces the

FIG.1 1 . Path of the wing-tip and angle of attack in relation to the body as plotted on a developed cylindrical surface (see text). The triangles mark the upper leading edge of the wing and are drawn solid for the downstroke. y , is the best great circle defining the stroke plane. (From Nachtigall, 1966).

plot on the right of Fig. 12. On these developed plots, the lines y, and correspond to the stroke plane and the axes 5, and 5, are drawn at the level of the wing-base. It is important to remember that Figs 11 and 12 are obtained by unrolling a cylindrical surface and not by projection of the spherical surface on to a plane; particularly at the top of the stroke there is a large component of wing-tip movement in a lateral direction. The projection of Fig. 12 is the same as that used by Jensen (1956) (his Figs 111.6 and 111.8) to illustrate the motion of the locust wing. yt

C O M P A R A T I V E P H Y S I O L O G Y O F T H E F L I G H T MOTOR

183

When considering the thoracic mechanisms by means of which the wing movements are produced, the plot of Fig. 11 and the silhouettes of Fig. 10 are the most useful. When considering the probable aerodynamic effect of the movements, Fig. 12 is of greater interest, since a translational movement can be added geometrically to give the path of the wing in space during free flight. The most accurate information about the time course of the movement is given by Fig. 9, on which measurements from individual photographic frames are plotted.

FIG. 12. Path of the wing-tip in relation to the air-flow, together with the path of the wing-tip in space and the incidence of the wing, as plotted on a developed cylindrical surface (see text). Triangles as in Fig. 1 1 . (From Nachtigall, 1966).

Nachtigall derived from the curves of Fig. 9 a plot of the time course of movement and then by successive differentiation could compute the changes of velocity and of acceleration; these have not been reproduced here since they are not directly relevant to the discussion. The other plots are all necessary for a full description of the kinematics. The time course of the stroke will now be described together with some qualitative features of the aerodynamics. It is convenient to distinguish four phases; downstroke, lower reversal movement, upstroke, upper reversal movement. 1. Downstroke (Nos. 3-14 of Fig. 10; Nos. 1-22 of Figs 11 and 12). The wing moves downwards and forwards with a steadily changing

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J . W. S. PRINCLE

angle of attack, but Fig. 12 shows that it maintains a positive angle of incidence to the relative wind throughout this phase. During most of the downstroke the velocity of movement is constant and relatively slow. The surface remains flat and shows little passive flexion or bowing between the veins. This is aerodynamically the most important part of the stroke and generates the main lift; only in the middle of the downstroke is there any thrust. 2 . Lower reversal rnooernent. During this phase there is a rapid turnover of the wing, produced actively from the base, so that by the beginning of the upstroke the morphologically upper surface of the wing is the aerodynamic lower surface. The axis of turning lies behind the wing-tip, so that the tip executes a complicated downward and backward path during a period of about I/3 msec while the wing is almost stationary. The surface thus becomes nearly vertical and the reversal finishes with a flick of the wing-tip which is probably passive due to the aerodynamic force acting on it. 3. Upstroke. Much thrust is generated during the first half of the upstroke, when the wing surface is morphologically inverted. Half-way through this phase (No. 45 on Fig. 12) the aerodynamic incidence becomes zero and from then on the upstroke seems to be aerodynamically inefficient. The upstroke is kinematically complicated by the fact that the wing is not a rigid plate but can twist, due to interaction between the torque at its base and the aerodynamic forces. Nachtigall argues, however, that the twist can be almost discounted since it is greatest at those phases of the stroke that are aerodynamically ineffective, namely the reversal movements. During the middle of the downstroke there is almost no twist; during the first part of the upstroke when the twist is maximal (No. 19 on Fig. 10) the angle of attack is constant over the outer two-thirds of the span. The inner third of the fly’s wing has a smaller chord and since it moves at lower velocity owing to the angular nature of the motion, the harmful effect of its twist is minimized. 4. Upper reversal movement. At the end of the upstroke the path of the wing-tip bends round so that it is moving forwards through the air with its lower surface to the front and almost perpendicular to its direction of movement. At the top of the stroke the wing rotates rapidly from this aerodynamically unfavourable orientation, the active torque being helped by passive forces. The downstroke starts at once, at high incidence. These complicated movements are best appreciated by examination of the figures, which display them more adequately than any verbal description. The resulting motion of the wings is not harmonic since

185 the upstroke velocity is higher and its duration shorter than the downstroke. Velocities and accelerations of the wing, computed from the observed motion, are highly irregular; the bending due to aerodynamic forces evidently makes it impossible to deduce anything from these curves about the timing of the muscular contractions. At the start of flight, stroke amplitude builds up steadily, over several cycles at constant frequency, and there is a similar gradual decline in amplitude before motion stops. Figures 13 and 14 illustrate the different form of the wing stroke when the insect is flying in still air. The chief difference is that the planes of the upstroke and downstroke are now the same. The two parts of the stroke have the same duration and the velocities of movement are constant and nearly equal throughout the strokes. It appears that in free flight C O M P A R A T I V E P H Y S I O L O G Y O F T H E F L I G H T MOTOR

FIG.13. Path of the wing-tip in still air, plotted as in Fig. 8. (From Nachtigall, 1966).

the air-flow slows the downstroke and accelerates the upstroke, perhaps partly through a direct influence of the aerodynamic forces acting on the wings. Changes in the angle of attack during the stroke are very similar to those of free flight, showing the active nature of the twisting; at the middle of the downstroke the pronation is slightly greater and at the beginning of the upstroke the supination is greater and occurs earlier. It is impossible from kinematic studies alone to say whether these differences are the passive result of the air-flow or represent active compensatory movements. This detailed study of the wing motion of a fly confirms and extends earlier studies and it raises a large number of interesting questions. Without accompanying dynamic measurements, it does not help to decide whether steady-state aerodynamics can account for the generation of lift and thrust in an insect of this size and wing-beat frequency,

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J . W . S . PRINGLE

but it does form an essential preliminary to such a study. It is of immediate relevance to the problem of the mechanics of the thorax and the functional r61e of the various muscles, which will be considered later. It also provides an essential background for discussion of the nature of the compensatory control movements in Diptera.

7Y -

37 L-

--

5-

FIG.14. Path of the wing-tip and angle of attack in relation to the body during flight in still air. Plot as in Fig. 11. (From Nachtigall, 1966). B. APlS MELLIFERA

The most quoted observations of the wing motion of the bee are those of Stellwaag (1916). Recently, accurate studies of the kinematics have been made by Neuhaus and Wohlgemuth ( I 960), Wohlgemuth (1962) and Herbst and Freund (1962). These authors used high-speed

COMPARATIVE PHYSIOLOGY OF THE FLIGHT MOTOR

187

cinematography to record the form of the beat during ventilating movements and compared this pattern of behaviour to that observed during tethered flight in an air-flow and in free flight. Unlike the fly, the up- and downstroke of the wing beat in a bee lie close to each other under nearly all circumstances, so that the wing-tip path is never a wide loop or figure eight (Fig. 15). When not turning, the stroke plane remains inclined at about 120" to the longitudinal body axis, but its orientation in space naturally depends on the body angle. Apart from flight, bees use their wings to maintain the aeration of the hive (Fucheln) and also to distribute the secretion from abdominal

FIG.IS. Apis niellifern. Body attitude and path of the wing-tip during A, flight at 3 m/sec airflow; B, "Sterzeh". (Redrawn from Wohlgemuth, 1962).

scent glands (Sterzeht). The insect clings firmly with its legs and raises its abdomen at an angle of 25-30', bringing the stroke plane nearly vertical (Fig. 15B). Wohlgemuth (1962) has shown that there is a smooth gradation of behaviour from that observed in fanning to that characteristic of flight. At one extreme, the wings throughout the stroke remain inclined backward at about 30" to the transverse axis of the body; the beat frequency in this position averages 120/sec and the angle of attack changes during the stroke as shown in Fig. 16B. At the other extreme is the flight pattern in a 3 m/sec air-flow, when the whole stroke is rotated forwards; the beat frequency is now 200-225/sec, and the angle of attack changes as shown in Fig. 16A. The stroke angle (amplitude) is not correlated with fore-and-aft positioning of the stroke, nor with beat frequency; in either the fanning or flight attitudes, or in

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J . W. S. P R I N G L E

the intermediate attitudes adopted during Sterzeln, it is 65-120”, depending on the intensity of the behaviour. Addition of the air-flow vector to the wing motion shows that the angle of incidence to the relative wind at the widest part of the wing is about 15” during flight for almost the whole of the downstroke. For nearly two-thirds of the upstroke, the wing incidence to the relative wind is approximately zero; in contrast to the fly, the upstroke during flight therefore generates no useful aerodynamic forces. This conclusion is reinforced by examination of the form of the wing-tip path and by the changes in wing-tip velocity during the stroke (Fig. 17A). During

FIG.16. Apis mellifera. Path of the wing-tip and angle of attack of the widest part of the wing during A, flight at 3 m/sec airflow; B, fanning. (From Neuhaus and Wohlgemuth, 1960.)

the downstroke, the path of the tip is variable, suggesting a high aerodynamic loading and some wing flexibility (Figs 15, 16); during the upstroke it is straight and constant. Fig. 17A shows that the downstroke lasts longer than the upstroke and that for 30% of the downstroke the velocity is constant at a moderate value, indicating that the muscles are heavily loaded; the upstroke shows no such pause but sometimes a slight acceleration. The curvature of the wing-tip path (Fig. 16B) and the changes in tip velocity (Fig. 17B) suggest that during fanning the loading is high during both strokes, and this is borne out by calculation that during much of both strokes the wings are at a high incidence to the relative wind. The whole body of the insect actually oscillates up and down during strong fanning movements. The “Sterzeln” pattern spans this range of behaviour. Low-frequency movements with the wings

C O M P A R A T I V E P H Y S I O L O G Y O F T H E F L I G H T MOTOR

189

drawn back are similar to fanning except that the incidence to the relative wind is lower and the motion more nearly sinusoidal; this pattern is also seen at the start of ventilating activity. High-frequency “Sterzeln” movements with the wings drawn forwards are similar to those of flight. Neuhaus and Wohlgemuth (1960) state that the stroke pattern seen in tethered flight at 3 m/sec air-flow closely resembles that found in freeflight cinematographs of bees leaving the hive, but that when a returning bee nears the hive the body angle increases and the stroke plane is tilted backwards. They did not investigate other air-flow velocities or body attitudes. Herbst and Freund report similar observations of the range of ventilating behaviour, but include some accurate graphs of the angle of beat and angle of attack during the stroke cycle. They show that the

A

8

B

4 0

Downstroke

Upstroke t

FIG.17. Apis rnellifru. Velocity of the wing-tip in lateral projection during A, flight at 3 m/sec airflow; B, fanning. (From Neuhaus and Wohlgemuth, 1960).

rates of the reversal movements at the top and bottom of the stroke are variable, that the full range of beat frequencies is 85 to 240/sec and that the beat interval may vary by 10% over the space of a few cycles. Since the bee’s flight mechanism is powered by self-oscillating, fibrillar muscle, the last two observations suggest that the aerodynamic damping of the mechanical resonance must be very high and that there must also be some control of the elastic compliance of the thorax and muscles. One may conclude from these studies that the flight system of Apis differs from that of Phormiu in that the wing is more flexible and that,

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J . W . S. PRINGLE

at any rate under the flight condition studied (3 m/sec air-flow), the upstroke contributes little to the aerodynamic force. The following parameters are under active control : (1) the fore-and-aft position of the stroke, which appears also to influence beat frequency. (2) the stroke amplitude. (3) the angle of attack during the downstroke, possibly with independent control of the angle of attack in different parts of the stroke. (4) the angle of attack during the upstroke (evidence so far only from ventilating behaviour).

To these must be added the old observations by Stellwaag (1916) of control of ( 5 ) the stroke planc, which will be discussed in the section dealing with flight reflexes.

IV. ST A BI L I T IYN FLIGHT A. D I P T E R A

As was first pointed out in the context of insect flight by Hollick (1940), control is required both of the magnitude of the lift and thrust (in order to vary the vertical and horizontal motion) and also of the line of action of the aerodynamic resultant in relation to the centre of gravity. In an animal which does not possess secondary stabilizing surfaces such as the tail of a bird or aeroplane, turning couples (torques) in one or more of the three planes of space will be generated if the resultant of the total aerodynamic forces does not pass through the centre of gravity. Furthermore, stability (that is, a tendency to return to the original attitude when displaced) will only be present if the line of action of this resultant moves, on angular displacement of the insect, in such a sense as to produce a restoring torque. No further experimental measurements of the torque acting on a flying Dipteran have been made since Hollick (1940), but some deductions are possible from the more accurate kinematic studies that have been made since then. Stability in a flying machine may be passive or active; that is, it may be inherent in the aerodynamic properties of the structure or it may involve active movement of the control surfaces. In a flying insect, the question is whether or not reflexes are always involved. Stability can be studied in flies in the probable absence of reflexes by using the phe-

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191

nomenon of “anaesthetic flight” (RuuschJlug), the activity which occurs during recovery from certain anaesthetics due to maintained motor activation of the self-oscillatory indirect flight muscles (Pringle, 1949). Hollick showed that free flight in this condition is stable if the wings are undamaged, but that there is not the usual compensation for bilateral asymmetry which is provided by reflexes from the halteres (Schneider, 1953; Faust, 1952; discussion in Pringle, 1957). Anaesthetic flight in calm air is, in fact, just stable in all three planes of space and we may consider for each plane in turn how this stability is achieved through the design of the flight system. Factors which make for inherent lateral (i.e. rolling) stability in a flying machine are location of the wings above the centre of gravity, mounting the wings at a dihedral angle and having the angle of incidence greater at the base than at the wing-tip (“wash-out”). In Phormia the angle of attack of the wing giving the maximum lift occurs in the middle of the stroke (points 12-15 on Fig. 12), when the wing is still above the horizontal. This suggests that the first two of the above factors may be operative. A difference in angle of incidence along the span is said by Nachtigall to be absent during the parts of the stroke that are most effective aerodynamically and this factor could only operate, if at all, during the lower reversal movement. Inherent stability in yaw (i.e. turning about a vertical axis) demands that the thrust be delivered by the wings at a point in front of the centre of drag of the body. The position of the latter has not been determined, but it may be assumed to be about one-third of the way along the body which, in a fly, is very near to the wing base. Nachtigall (1966) shows that the main thrust comes from the beginning of the upstroke. The thrust is, therefore, delivered well forward of the wing base and some inherent stability in yaw may be expected. Stability is most important in the pitching plane, and this was the plane considered by Hollick (1940), who first described both the inherent and the reflex mechanisms in Muscina stabuluns. His observations may be summarized as follows : (1) In still air, the magnitude, direction and line of action of the aerodynamic resultant are independent of the body angle. There is no inherent or reflex regulation by gravity. (2) In still air, spontaneous variability during different periods of flight showed that there is a close correlation between the amplitude of beat (stroke angle) and the line of action of the resultant (Fig. 18). A large majority of the flies tested in still air flew in the condition in

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J . W . S. P R I N G L E

Fig. 18B.Although the magnitude of the aerodynamic force was sufficient or more than sufficient to support their weight, when released they immediately plunged forward due to the large pitching torque. (3) Exposure to an air-flow reduced the amplitude of beat and increase in body angle now produced a further considerable reduction

120

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FIG. 18. Muscina stabulans. A. Relationship between stroke amplitude and the horizontal distance from the centre of gravity to the line of action of the aerodynamic resultant. The outlines show stroke amplitude as viewed at right angles to the stroke plane. B. Diagram showing the modal magnitude and line of action of the resultant in still air. (From Pringle, 1957, after Hollick, 1940).

(Fig. 19). An effect of body angle on stroke angle was also seen after amputation of the antennae, (4) Increasing air flow also changed the path of the wing-tip as shown in Fig. 20A. In intact flies the change was primarily a moving forward of the path of the downstroke. After removal of the antennae, air-flow

COMPARATIVE PHYSIOLOGY OF THE FLIGHT MOTOR

193

merely reduced the forward travel of the wing at the bottom of the stroke and moved backward the last part of the upstroke (Fig. 20B). Hollick concluded that these effects conferred two types of longitudinal stability : (a) Inherent stability dug to the fact that, in an air-flow, increasing body angle decreased the stroke amplitude and thus moved the line of 140' c

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FIG.19. Muscina stabulans. Average angle between the wings at the bottom of the stroke at different body angles in still air and in an air-flow of different velocities. (From Hollick, 1940).

action of the resultant backward. This must produce a restoring torque. Since this is a direct influence of the aerodynamic forces on the wing motion, the restoring torque will be greater at higher forward speeds, exactly as in a conventional flying machine with auxiliary tail surfaces. (b) Reflex stability due to the change in the path of the wing-tip (longitudinal position of the downstroke) when the air-flow stimulates

194

J . W . S . PRINGLE

the antennae. This reflex will produce a zero pitching moment only at a certain air speed; the direction of the torque at lower or higher speeds is such as to make the insect dive or climb until the optimum speed is reached. These suggestions are entirely consistent with the accurate kinematic studies of Nachtigall (1966), in spite of the different species of muscid Dipteran used. Caution is needed in comparing Fig. 20 with Figs 1 1 , 12 and 14, since the former is a projection of the spherical surface on which the wing-tip moves and Figs 11, 12 and 14 are developments of a cylindrical surface. The following features of the wing motion of Phormia are significant in the comparison : (1) In an air-flow the downstroke path moves forward from its position in still air (Figs 1 1 and 14). This is evidently the reflex effect described by Hollick (1940).

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FIG.20. Musca dontcsticn. Lateral view of the path of the wing-tip at different air speeds in intact insect and after removal of the antennae. (From Hollick, 1940.)

(2) The wing surface is at right angles to its direction of motion at the top and bottom of the stroke. It is thus at these instants that air-flow may be expected to produce the greatest longitudinal displacement of the wing-tip path due to the direct influence of the aerodynamic forces (Fig. 20B). (3) Hollick found that the passive reduction in stroke amplitude in an air-flow was greatest at large body angles and that it arises from a curtailment of the beat at the bottom of the stroke (Fig. 19). Figures 1 1 and 12 show that increase in body angle will cause the wing to be moving at above-optimum incidence earlier in the downstroke; its

C O M P A R A T I V E PHYSIOLOGY O F T H E F L I G H T MOTOR

195

movement will thus be more resisted by the increased drag and the stroke angle will decrease. There are thus good reasons for thinking that the form of the wing motion shown by a fly in an air-flow automatically confers inherent stability in the pitching plane, in spite of the absence of fixed auxiliary surfaces. The stable movement of the line of action of the resultant arises from two features of the mechanism, (a) the plane of the wing-beat, such that at the bottom of the stroke the wing is in front of the centre of gravity: (b) the gradual supination at the end of the downstroke, so that, when increase of body angle increases the incidence above the optimum, this part of the stroke is curtailed and its contribution to the lift reduced. Decrease of body angle will have the opposite effect, increasing the stroke amplitude at the bottom and increasing the component of lift acting in front of the centre of gravity. We have already seen how inherent stability in yaw may be produced by the fact that the main thrust comes early in the upstroke when the wing is in front of the centre of gravity, and how inherent stability in roll may result from the twist at the lower reversal movement and from the fact that the lift is mainly produced when the wing is above the centre of gravity. If further studies show this to be correct the remarkable conclusion will be reached that by virtue solely of the kinematics of the wing motion, a fly has slight inherent stability in all three planes of space. R . OTHER INSECTS

In the course of his study of the reflex control of velocity of flight in the honey-bee, Heran (1959) made some observations of this insect in tethered, anaesthetic flight and was able to show that, as in the fly, reflexes are absent. He found a small but significant influence of the air-flow on the amplitude of beat, but he did not study how this may be influenced by body angle nor did he consider the question of longitudinal stability. Anaesthetic flight in the honey-bee is not so stable as in the fly, and it is possible that this species relies more completely on reflex stabilization. Faust (1952) performed experiments on a variety of insects in free flight in total darkness to determine stability in the absence of an orienting light stimulus. He found that Diptera and Odonata flew normally and that slow-flying Lepidoptera preserved a normal flight attitude, though they did not move far in flight. The other insects showed varying degrees of disorientation. Coleoptera often showed long periods

196

J . W. S. PRINGLE

of rather unsteady flight, usually in a wide spiral; the moths Plusia and Agrotis and the honey-bee, though maintaining normal attitude, flew down in a steep spiral; most of the Hymenoptera, Sphinx (Lepidoptera) and Cetonia (Coleoptera) were completely disoriented. These experiments did not, of course, eliminate the influence of proprioceptive reflexes, but they suggest that, in all except the last group, some measure of inherent stability must be present, especially in the pitching plane; stability in roll appears to be better in most Coleoptera than in the other Orders. Haskell (1960) added the locust to the species tested. Completely blinded insects were sometimes able to fly as far as loom, but the

FIG.21. A. Movement of the wing-tips of Schistocerca gregaria in relation to the air during standard flight conditions. B. Lift generated in different parts of the stroke. (Replotted from Jensen, 1956).

majority were unstable in roll and eventually went into a spin. Goodman (1965) made a laboratory study of visual stabilization in Schistocerca by mounting the insect in front of a wind-tunnel in a framework that was free to rotate about the longitudinal axis, but this arrangement would not have detected inherent lateral stability; it was intended to demonstrate rolling reflexes. Gettrup (1966) found instability around the three main body axes in Schistocerca after destruction of all companiform sensilla on the wings and stressed the importance of reflex control. The locust is the only one of these insects for which sufficiently accurate data are available to permit an analysis of the expected stability

COMPARATIVE PHYSIOLOGY OF THE FLIGHT MOTOR

197

of the aerodynamic mechanism. Figure 21 shows the movement in space of the fore- and hind-wing-tips during steady flight, together with the instantaneous values of the lift generated. An approximate estimate of the lateral stability to be expected from the contribution of each pair of wings can be obtained by summing over the whole cycle the product of the instantaneous lift and the vertical distance of the wing-tip above or below the wing base. For the curves of Fig. 21 this gives values (arbitrary units) of + 2240 for the fore-wings and - 940 for the hind-wings. The hind-wings contribute 71% of the total lift (Jensen, 1956), but by themselves would create a system which is unstable in the rolling plane owing to the fact that the lift is mainly delivered when they are below the horizontal. The smaller lift contribution from the fore-wings greatly increases lateral stability. Overall, these data suggest that the insect should just be stable, but no account has been taken of wing interaction, wing twisting and several other factors which may complicate the situation. An interesting feature of this analysis for the locust is that it suggests a possible evolutionary origin for the state of affairs found in the Coleoptera. Here the hind-wings nearly meet in the mid-ventral line at the bottom of the stroke (Magnan, 1934), and it seems likely that their contribution to the lift is an even more unstable one than in the locust; the elytra, on the other hand, are held in flight at a pronounced dihedral angle and the appreciable lift that they are now known to produce should compensate for this instability, particularly during fast, forward motion. Faust’s (1952) demonstration that Cetonia is noticeably less stable in roll in the absence of visual stimuli is significant, since this family, alone in the Coleoptera, flies with its elytra folded. Stability in yaw will not be a problem in insects with a long abdomen, since this will act like a rudder to maintain the direction of movement in the air. In the locust the main thrust is delivered by both wings in the middle of the downstroke and by the hind-wings only rather late in the upstroke; for this reason and because the whole of the beat of the hindwings takes place with the wing behind the transverse (y,z,) plane, stability in yaw might be expected to be poor if the centre of drag of the body were located at the wing base. A long abdomen will also contribute to stability in pitch, and it may be for this reason that the Odonata are able to fly stably in complete darkness. The extreme development of this mechanism is found in the genus Petalura, where the anal appendages are expanded into flat surfaces which must function like a conventional tailplane (Tillyard, 1908). The passive mechanism found in flies could hardly operate in an insect

198

J . W . S. P R l N G L E

like a locust where there is not the same close correlation between the stroke plane and the stroke amplitude. It may be that the shortening of the abdomen, found in flies and bees and necessary if the insect is to perform rapid turning movements, is only acceptable aerodynamically in insects with a high-frequency wing-beat, because of its inevitable effect on stability in the pitching plane. It also demands a more elaborate and accurate system of reflex control of flight, which is superimposed on the necessary minimum of inherent stability.

v. T H E MOTORMECHANISM OF

FLIGHT REFLEXES

A . LIST O F R E F L E X E S

In this section we shall be concerned only with those reflexes that arc known to produce a rapid change in the spatial or temporal pattern of wing movements. Many other types of afferent stimulus affect features of insect behaviour that involve flight, but these will not be discussed unless it is known how their efferent effect is produced. The following reflexes have been described : (1) A reflex from a stretch receptor at the base of both pairs of wings, affecting the frequency of the neurogenic rhythm (Schistocerca : Wilson, 1961; Gettrup, 1962, 1963; Wilson and Gettrup, 1963). Study of this reflex gives no information about the effector mechanism of the flight motor and it will not be further discussed. (2) Reflexes from campaniform sensilla on the ventral surface of the costa and subcosta controlling aerodynamic lift and various features of the wing movement (Scltistocercu: Gettrup, 1965a, b, 1966). (3) A reflex from Johnston’s organ in the antennae, affecting (a) the path of the wing-tip during the downstroke (muscid Diptera: Hollick, 1940; Nachtigall, 1966). (b) the stroke amplitude and the velocity of forward flight (Calkphora: Burkhardt and Schneider, 1957; Apis: Heran, 1959). (4) Reflexes from the halteres, counteracting rotation in each of the three planes of space (Diptera: Fraenkel and Pringle, 1938; Fraenkel, 1939; Pringle, 1948; Faust, 1952). (5) A reflex from neck receptors (probably hair plates) controlling stability in the rolling plane by differential wing twisting (Odonata: Mittelstaedt, 1950). (6) A reflex from hairs on the front of the head, regulating the yawing torque in relation to the direction of the air-flow (Schistocerca and Locusta: Weis-Fogh, 1949, 1950; Guthrie, 1966).

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(7) A reflex initiating the motor discharge to the flight muscles on loss of contact by the legs (nearly all insects except Coleoptera: Fraenkel, 1932). Further stimuli may be needed to maintain flight (Calliphora: Hollick, 1940; Schistocerca : Weis-Fogh, 1956b). (8) Visual control of stability in roll (Schistocerca: Goodman, 1965; Odonata: Mittelstaedt, 1950) and yaw (Schistocerca: Dugard, 1967). A dorsal light reaction and a reaction to the position of the horizon in the visual field are distinct sensory influences. These reflexes are integrated with the neck proprioceptive reflexes (5, above). (9) Dynamic visual (optomotor) reflexes, regulating the orientation and velocity of flight in relation to movement of the visual field (Apis: Schaller, 1960; Kunze, 1961; Heran, 1955; Heran and Lindauer, 1963. Muscid Diptera: Smyth and Yurkiewicz, 1966; Nachtigall and Wilson, 1967. Oryctes (Coleoptera) : Burton, 1964). B.

INITIATION,

M A I N T E N A N C E A N D T E R M I N A T I O N OF FLIGHT

Both in insects with synchronous and with asynchronous motor control, flight is normally initiated by starting the discharge of impulses in the nerves to the indirect flight muscles. In Schistocerca (Wilson, 1961) the motor discharge is synchronous with the frequency of beat from the first cycle of activity; at the beginning and end of flight, elevator muscles activity predominates over depressor activity. In muscid Diptera (Pringle, 1949; Nachtigall and Wilson, 1967) and in the beetle Oryctes (Darwin and Pringle, 1959) there is a high-frequency burst of motor nerve impulses to the indirect muscles at the start of flight and the frequency then falls to the low value characteristic of steady activity. However, in the water-bug Lethoceros, where flight is always preceded by a period of warming up, no change may be observable in the motor discharge to the indirect flight muscles at the instant that wing movements commence (Barber and Pringle, 1966). Motor excitation of the indirect muscles is also involved in the warming-up process before flight in the water-beetle Acilius, though mechanical activity during this process is limited to movements of minute amplitude at the wing base (Leston et al., 1965). Nervous excitation and minute thoracic oscillations at about twice the normal wing-beat frequency occur in muscid Diptera shortly before the wings are drawn forward into the flight position (Nachtigall and Wilson, 1967). Spontaneous termination of flight in Vespa and in flies is usually signalled by cessation of motor nerve impulses followed by a gradual

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decline in the amplitude of wing beat (Roeder, 1951), but wing movement in flies may be stopped abruptly on one or both sides of the body without change in motor activity to the indirect muscles (Boettiger, 1957; Nachtigall and Wilson, 1967). It is thus clear that activity in muscles other than the power-producing indirect muscles may be involved in initiation and termination of flight in insects with fibrillar muscles. Nachtigall and Wilson (1967) have confirmed by electrical recording that the non-fibrillar tergotrochanteral muscles of muscid Diptera are excited by a volley of 1 , 2 or 3 impulses (and that there is a strong jumping thrust from the mesothoracic legs) about 12 msec before the start of wing movements. This special adaptation for rapid take-off by initial elevation of the wings is not, however, present in all Diptera (Smart, 1958, 1959) nor in bees or beetles. Flight can start even in muscids after the lower insertion has been cut by removal of the legs; the tergotrochanteral muscle is therefore not necessary for the start of the auto-rhythmic activity. The main requirement if power is to be drawn from the activated fibrillar muscles is that the wing position and thoracic elasticity should be such that a mechanical resonance is created in a frequency range that is matched to the properties of the muscles. The mechanism by which this is achieved and the means of control of the power take-off involves other sets of muscles. On the sensory side, flight is initiated in most insects (not Coleoptera and only under some conditions in aquatic Hemiptera; Dingle, 1961) by loss of contact by the legs (reflex 7). In Drosophila, Muscina and some other insects it may then continue for long periods in still air, but in Schistocercu, Apis and most muscid Dipteru further stimuli are needed to maintain activity. These include wind-sensitive receptors on the head (Schistocercu: Weis-Fogh, 1956b) or antennae (Hollick, 1940), moving visual field (Schaller, 1960) or “wind on the moving wings” (WeisFogh, 1956b), which Gettrup (1966) has shown to mean the campaniform sensilla on the lower surface of the fore-wings. The central nervous organization by which these stimuli maintain excitation to the flight muscles is unknown. C . CONTROL O F AMPLITUDE, FREQUENCY A N D POWER

Insects require to control the mechanical power output in flight in order to move forwards or upwards at different velocities and to lift a variable body weight. This cannot be done, as with a rotating propeller, simply by increasing the angular velocity. Weis-Fogh (1965) has emphasized that energetic efficiency in a flapping-wing system like an

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insect is only achievable if there is considerable storage of kinetic energy in elastic structures. This implies that the thorax, muscles and wings must together form a mechanically resonant system, and it imposes limitations on the parameters which are available for the control of power output. They are, essentially, three: (a) The amplitude of beat, implying a change in the distance through which the muscles shorten. (b) The frequency of beat, implying a change in the elastic properties of the thorax (since the inertia cannot change) and of the velocity of shortening of the muscles. (c) The aerodynamic incidence of the wings, implying a change in the loading of the muscles. It is now possible to outline how these parameters are used by various types of insect for the control of power output. 1. Indirect muscles

In the locust with synchronous power-producing muscles, neither the stroke angle (amplitude of beat) nor the beat frequency vary enough to account for the variation of power (Weis-Fogh, 1956a); the main controlled variable is the aerodynamic incidence of the fore-wings, and therefore the loading of the muscles. In order that the same velocity of shortening be achieved, the excitation must therefore increase. Wilson and Weis-Fogh (1962) found by electrical recording that there was an increase both in the number of active motor units and in the number of impulses in the volleys in the indirect muscles when power output was higher. The total number of nerve impulses reaching the powerproducing musculature per second thus increased, though the volleys still occurred at the frequency of wing beat. Changes in the timing of the volleys as the number of active motor units increased were correlated with a slight increase in beat frequency, assisting the increase in power. In insects with asynchronous power-producing muscles, the wing-beat frequency is directly determined by and not merely related to the mechanical resonant frequency of the thorax/wing system. Apart from a small change in the effective elasticity of the fibrillar muscles produced by increase of their excitation, beat frequency can therefore only be changed through auxiliary mechanisms. Increased excitation of the fibrillar muscles will produce an increase in stroke angle if the incidence and loading do not change, and increased excitation is required in order to maintain the same amplitude of beat under conditions of increased loading.

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Nachtigall and Wilson (1967) measured not the power output but the aerodynamic lift at constant thrust of several species of large fly and found, during spontaneous variations in performance, a high correlation between lift and the frequency of motor nerve impulses to all the indirect flight muscles. This is an indication that power is controlled by adjustment of the power generator. Smyth and Yurkiewicz (1966) recorded a reduction in impulse frequency in dorsoventral and dorsal longitudinal muscles of a blow-fly when a pattern of stripes was moved from front to rear in the visual field (reflex 9), indicating that there is reflex regulation of this parameter. All authors agree, however, that there is not a large change in stroke amplitude (amplitude of beat) in flies when power output changes, except at the very beginning and end of a period of flying. Correlated increase in aerodynamic loading due to changes in angle of attack and also an increase in wing-beat frequency due to a change in thoracic elasticity must absorb most of the additional mechanical power generated. Evidence for a mechanism of this sort was provided by Chadwick (1951), who showed in Drosophila that change of air density did not produce the change in stroke angle expected in the absence of other compensatory effects (see also Chadwick, 1953). Large changes in stroke angle and of the amplitude of muscular contractions occur only at large body angles (Fig. 19), which would be unlikely to occur in life except as transient attitudes. Increases in motor nerve impulse frequency to the indirect fibrillar muscles have also been reported by Burton (1964) in the beetle Oryctes boas and correlated with increase in the amplitude of beat. Since these increased excitation frequencies were only observed unilaterally in the experiments described, one cannot conclude with certainty that stroke angle is a variable parameter in changes of output power in beetles, but the possibility is clearly indicated. No measurements appear to have been made of the frequency of excitation of the indirect muscles in the honey-bee, where large changes of stroke angle are involved in control of the velocity of flight (Heran, 1956; see later). 2. Direct inuscles

Changes in the angle of attack of the wings during the stroke are produced in the locust by the timing and force of contraction of the direct (basalar and subalar) muscles (Wilson and Weis-Fogh, 1962; Wilson, 1962). It is mainly the supination-producing subalar muscle whose degree of excitation is under reflex control and, since supination increases the aerodynamic loading during the downstroke, there is an

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automatic correlation between loading and total power production during the operation of this reflex. A similar situation is found in Odonata, where Neville (1960) showed that the angle of attack during the middle of the downstroke (Fig. 22) is controlled by the balance of excitation to the large second basalar and second subalar muscles, both of which contract at wing-beat frequency and are synergic so far as depression of the wing is concerned.

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FIG.22. Diagrams showing the angle of attack of the fore-wings of Aeshizu at different instants in the stroke and the effect of cutting various muscles. The leading edge is shown by a dot. Series (i) are downstroke and series (ii) upstroke. (a) normal stroke, (b) without anterior coxoalar, (c) without anterior coxoalar and third subalar, (d) without third subalar, (e) without first and second basalars and third subalars, (f) without second subalar. (From Neville, 1960).

He found that supination for short periods at the bottom of the downstroke and the latter part of the upstroke was also produced by contraction, respectively, of the anterior coxoalar and third subalar muscles, the latter of which operates tonically and transmits its force through a long elastic ligament. The size of these muscles shows, however, that they can contribute little to the control of power and they must be involved in attitude or directional control.

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Among well-studied types of insect with asynchronous flight mechanisms, Coleoptera and Hemiptera have several fibrillar muscles other than the indirect dorsal longitudinal afid dorsoventral. In both these Orders, the main basalar inuscle is fibrillar and also the indirect oblique dorsal which tends to supinate the wing. In beetles but not in Belostomatid bugs, the subalar is also of this type (Pringle, 1957; Barber and Pringle, 1966). Simultaneous increase in frequency of excitation to all the power producing muscles, direct and indirect, as found by Burton (1964), might therefore be expected to produce an increase in stroke angle, since there is no obvious provision for change in relative phasing of the cycles of mechanical activity of different muscles such as is found in the synchronous locust and therefore no simple way of achieving simultaneously a change in angle of attack during the downstroke and an increase in muscle loading. Such a mechanism would require that the basic time constants of “delayed tension” in the direct fibrillar muscles be different from that of the indirect muscles (Pringle, 1967), and would be sensitive to small changes in beat frequency, making it unreliable as a means of control. It is interesting that direct fibrillar muscles are found in some of the lower Hymenoptera (Daly, 1963) and in Diptera Nematocera (Smart, 1957, 1959). The highly simplified condition of the fibrillar musculature found in the Apoidea, Vespoidea and the muscid Diptera is evidently a late evolutionary development, but its independent evolution in these two lines may indicate that there is some inherent disadvantage, such as that suggested above, in the control of angle of attack by an autorhythmic mechanism. As explained earlier, power can only be drawn from the fibrillar muscles if the wing is coupled to them so as to generate the correct mechanical resonance, and a possible mechanism for the control of power exists in flies and other insects through the folding of the wings, which decouples them from their normal basal articulations. Folding is generally produced by the “adductor” muscle (terminology of Ritter, 1911 ; 3rd axillary muscle in many insects, Pringle, 1957), unfolding either by tonic contraction of the indirect muscles (honey-bee, Pringle, 1961) or, in muscid Diptera, by the “abductor” muscle (“anterior episternal basalar”, Smart, 1959). Nachtigall and Wilson (1967) show that the abductor muscles of flies are involved in drawing forward the wings at the start of flight and that full amplitude and power are not reached until this movement has occurred. When the wings are folded, minute vibrations of the pleural wall occur at approximately twice the normal beat frequency. They find, however, that neither the abductor nor the

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adductor muscles are excited during steady, straight flight, and this seems to exclude the promotion and remotion of the wing as a parameter that is used in flies for the control of total output power. Differential effects in this system during turning will be discussed later. There is no other evidence that a wing opening and folding mechanism is used for control during normal flight. 3. Accessory indirect muscles Muscles of this tonically contracting group change the structural characteristics of the thoracic box (Bonhag, 1949; Pringle, 1957). The mode of action of only two of them is known. It was first shown by Boettiger and Furshpan (1952) that tonic contraction of the pleurosternal muscle in Sarcophaga under the influence of CCl, moves inwards the mesopleural wing articulation and introduces a click action into the mechanical coupling between thorax and wings. During flight, this means that the velocity of wing movement on the up- and downstrokes is faster than it would be in a harmonic motion; with the wings folded, it provides a mechanical load with the right characteristics to permit oscillations to occur when the wing inertia is not coupled into the resonant system. Nachtigall and Wilson (1967) proved by electrical recording from the pleurosternal muscle in flies that it is indeed brought into action at the start of flight before any oscillations begin, and also before the movement forward of the wings couples them to the source of power in the indirect muscles. Non-linearity in the wing-thorax coupling appears to be widespread in the Pterygota, but in other Orders it has not been proved to be controlled by the pleurosternal muscle. A click action of the articulation has been demonstrated in Coleoptera (Pringle, 1957; Leston, Pringle and White, 1965), and in the metathorax of Schistocerca (T. Weis-Fogh, unpublished, quoted by Pringle, 1957), but is apparently absent in bees (J. W. S. Pringle, unpublished). The pleurosternal muscle tends to be replaced by skeletal or ligamentous internal bracing in many Lepidoptera (Chadwick, 1959); in scarabeid Coleoptera and in the Apoidea, its location is such that it is hard to see how it could greatly influence the thoracic elasticity, and its function may have been taken over by small tergopleural 01 other muscles. The great development of the click mechanism in Diptera may perhaps be correlated with the peculiar ability of these insects to start into flight without the preliminary warming up that is characteristic of many of the higher Orders. The oscillation frequency at which fibrillar muscles deliver their maximum power is greatly influenced by temperature (Machin, Pringle and Tamasige,

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1962), whereas the mechanical resonance of the wing-thorax system is almost temperature-invariant ; a proper matching of the two will therefore normally be achieved only at a certain temperature. In flies, however, the click mechanism ensures that shortening does not occur until tension has been developed; power output is thus much less sensitive to proper matching of the properties of the thorax and the muscles and therefore to the temperature. The second accessory indirect muscle whose action can be partially understood is the muscle of the axillary lever in bees. This slender tonic muscle operates the mechanism of the axillary lever (Fig. 23) and its contraction moves backward the 4th axillary and alters the relative positions of notum and pleuron through the axillary arm. Pringle (1961, 1965) has suggested that this gives a control of power through increase in the maintained stretch imposed on the indirect muscles. If this is proved to be correct, it will represent a distinct means of control from that found in other insects. An additional function for the axillary lever system is outlined in Section E.2. D. CONTROL OF VELOCITY

I . Apis inellifera It has long been known from field observations that a foraging worker-bee regulates its speed of flight according to the velocity of the wind with or against which it is flying. Heran (1955, 1956) showed that this involves sensory indication both of the velocity of movement through the air and of the velocity of movement over the ground. The former is obtained by means of the antennae (reflex 3b) and the latter using the eyes (reflex 9). The effector coordination is apparently similar in the two cases, though Heran (1959) made measurements of only one parameter, the amplitude of beat as viewed from a fixed direction in front of the insect; this may not give reliable values of the stroke angle if the stroke plane alters, He states that, in fixed bees, the normal stroke angle of about 120" was reduced to about 80" in an air-flow of 6-7 m/sec, with some change in the path of the wing-tip. This reflex was lost after amputation or fixation of the antennae. It is evidently a natural response, since bees fly to a good food source at about 8 m/sec and can exceed 10 m/sec through the air in a head-wind. The optomotor control was studied by Heran (1955), using a striped drum rotating about the transverse axis and placed below the bee so that it subtended an angle of 70". At a visual speed of 2.5 m/sec, the stroke amplitude was reduced by 12", and at 4*6m/sec by 23"; the

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magnitude of the effect was not changed when an air-flow was present. The reduction in stroke angle occurred mainly in the lower part of the beat. At a visual speed of 10.6 m/sec the reduction in stroke angle was less, and at about 20 m/sec it was hardly apparent; at these speeds of drum rotation the stripes are probably passing a point in the visual field above the flicker fusion frequency of the eye. Rotation of the drum also produced a change in the stroke plane, but this was not measured. A different response to optomotor stimulation was reported by Schaller (1960), who used two moving bands of vertical stripes, one on each side of the suspended bee; stroboscopic illumination was used to observe the wing positions. Schaller states that when the stripes moved from head to tail at the same speed of 35 cm/sec on each side, the stroke angle was increased from an initial value of less than 90" to a higher value, with an increase in the inclination of the stroke plane. As viewed from the front the pronation during the downstroke was reduced from 30" to 10" and the supination during the upstroke increased from an average of 40" to about 85". Both lift and thrust forces were increased and the duration of flight greatly prolonged. It seems probable that in these experiments the level of illumination was too low to produce the full amplitude of wing-beat in the absence of further excitation and that the stimulus of stripes moving at slow speed supplied this. The largeamplitude condition observed by Schaller was therefore the initial condition in Heran's experiments. In still air with a stationary and dimly lit visual field, the wing motion of a suspended bee is more similar to that used for fanning than for flight. Heran's observations are therefore indicative of the free-flight situation and they suggest that in bees the stroke angle is reduced as air speed and ground speed increase, thus regulating the velocity of flight in the way observed in the field. If other stroke parameters do not change much, this will be automatically correlated with a reduction of output power, and it is presumably achieved on the motor side by reduction in excitation to the indirect flight muscles. 2. Diptera Mention has already been made of the experiments of Hollick (1940) in which it was shown that the chief effect of increased air-flow in Muscina was a change in the path of the downstroke (Fig. 18). This, by, itself, will not regulate the aerodynamic thrust and the velocity of flight; the regulation is of the pitching moment, which leads to a change in velocity only when the fly has gained speed through a short dive or

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lost it through a short climb. The small influence of air-flow on stroke angle at small body angles was probably a direct effect and indicated the absence rather than the presence of a velocity regulating reflex. The antennal reflex was further studied by Burkhardt and Schneider (1957), who found in free-flight experiments that under strong lighting conditions removal of the antennae had little effect on forward velocity. In dim light, however, when an intact CuZliphoru normally either hovers or moves forward very slowly, an insect without antennae flew fast round the room and frequently collided with the walls. This does not, however, prove that the control of velocity by a visual reflex in bright light and by the antennae in dim light is done directly as in the bee; the control could be indirect through a change in pitching attitude. Further proof that the intensity of illumination has an important influence on the behaviour of a fly was given by Goodman (1960), who described the leg and wing movements involved in the landing response of LuciIiu sericutu and showed that they could be evoked merely by a reduction in light intensity. At the same time as the legs were lowered, the beat frequency was reduced and the stroke plane changed from its normal inclined position into a mere vertical orientation. From what is known from other studies, this was probably simply a sign of reduced power output from the flight motor as flight terminates, since it is the effect to be expected from relaxation of the pleurosternal muscle and reduction of excitation of the indirect muscles. The evidence, though inconclusive, suggests that although antennal and optomotor stimuli produce qualitatively similar effects on the speed of flight in large flies and in bees, the effector mechanisms may be different. A fly appears not to have (or to need) such an accurate control of velocity and it may achieve control largely by change in body angle. Vogel(l966) states that this is the chief means of control in Drosophilu and that no change in the angle of attack of the wings during the downstroke occurs when the air-flow is increased from 0 to 2m/sec. The automatic coupling between stroke angle and stroke plane and the movement of the line of action of the aerodynamic resultant in muscids will tend, in free flight, to produce an automatic relation between power output and lift, rather than between power output and forward velocity. The bee, on the other hand, appears not to vary the path of the wing on the downstroke to the extent seen in muscids and seems able to change the direction of the aerodynamic resultant without change of body angle. This gives it a wider control of forward velocity and enables it to maintain a constancy of the orientation of the body in space that may be needed in an animal that relies so much on accurate visual stimuli.

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E . CONTROL OF LIFT

It is convenient to discuss the locust first under this heading since only here has the mechanism of a lift-control reaction been fully elucidated; in this insect it appears to be the regulated parameter, while the forward velocity was found by Weis-Fogh (1956a) to vary from a maximum of 5.5 m/sec at the start of flight to a minimum of 3.5 m/sec, below which the insect cannot maintain itself in the air. The lift-control reaction (Weis-Fogh, 1956b; Gettrup and Wilson, 1964) was first identified when it was discovered that the lift produced by a locust flying in front of the wind-tunnel remained almost constant when the body angle was increased from 0 to 15". Since neither the beat frequency, the stroke angle nor the stroke plane changed enough to account for this, it was concluded that the controlled parameter was the angle of attack during the downstroke. Gettrup and Wilson (1964) established that the angle of attack of the hind-wings did not change and that therefore there is a compensatory change of pitching moment as well as a regulation of the total aerodynamic lift. Wilson and Weis-Fogh (1962) showed by electrophysiological recording that the effector action is chiefly mediated through variable excitation to the subalar muscle, and Gettrup (1965a, b; 1966) showed that it is chiefly the campaniform sensilla on the lower surface of the hind-wings that monitor the lift during their downstroke and form the sensory element in the reflex. Of all the reflexes involved in the control of insect flight, this is probably the most fully worked out. 2. Other insects In other insects, measurements of the lift have not been dissociated from measurements of total aerodynamic power, and it is therefore not possible to conclude that this parameter is under specific control. Thus Vogel's (1 967a) demonstration of a correlation in Drosophila between lift and stroke angle may merely show spontaneous variability in the excitation of the indirect flight muscles. In this species the lift control reaction is definitely absent (Vogel, 1966). Hollick (1940) does not state how lift varies with body angle in Muscina and one cannot therefore decide on present evidence whether the absence of the reflex in Drosophila is characteristic of flies in general or of small insects. The former would be consistent with the conclusion that velocity of flight in muscid Diptera is controlled indirectly by change of attitude. The control of lift presents special problems in insects that can hover or fly backwards, that is, that can remain airborne without forward

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velocity. The wing kinematics required for hovering have not been fully elucidated, but in some insects it seems to be achieved (as in humming birds, Greenewalt, 1960) by bringing the stroke plane nearly horizontal. The simplest method of doing this is by an increase in body angle. Vogel (1966) showed for tethered Drosophila that lift equal to 100% body weight was produced at a body angle of +65" at zero forward velocity. Demo11 (1918) showed in MeZoZontha in free flight that reducing the area of the wings led to flight at a higher body angle and at slower forward speed, but that the insect could remain airborne; this

FIG. 23. Semi-diagrammatic internal view of some lateral mesothoracic muscles of Xylophaga (Apidae). (Original).

suggests that lift is the controlled parameter and that regulation, as in muscids, is by change of body angle. In contrast to this, the honey-bee hovers with little change of the attitude of the body and must either change the stroke plane in relation to the body (Stellwaag, 1916; Heran, 1959) or change the kinematics in a way not understood. Syrphid Diptera hover with the stroke plane vertical (Magnan, 1934). Mention has already been made of the mechanism of the axillary lever in the Apoidea (Fig. 23). This peculiar development of the posterior

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notal wing articulation must be correlated with some special control mechanism in bees. Contraction of the muscle acts through a large leverage to change the relative position of notum and pleuron, the force being transmitted through the axillary arm and the 4th axillary sclerite. In addition to increasing the mean length of both dorsoventral and dorsal longitudinal muscles, so that more power will be drawn from them, it also appears to rotate the stroke plane into a more horizontal position. Unfortunately the muscle is very inaccessible in the flying insect, and this anatomical deduction cannot be checked experimentally. There has been no modern account of the flight muscles of Syrphidae, but Bonhag (1949) gives a detailed description of Tabanus sulcifrons, which can also hover. There is no movable portion of the postphragma in any way resembling the axillary lever. F. CONTROL OF ATTITUDE

1. Pitch

We have now to consider in turn the reflexes that enable a flying insect to maintain its orientation in space. The question of inherent stability, due to a direct influence of the aerodynamic forces on the wing motion, was discussed in Section IV; here we are concerned with the active contraction of direct flight muscles. Reflex stabilizing mechanisms in the pitching plane have already been described in the antenna1 reflex of Muscina (Hollick, 1940) and in the lift control reaction of Sclzistocerca (Gettrup and Wilson, 1964). In Schistocerca a reduction in the angle of attack of the fore-wings during the downstroke, and the absence of a similar change in the hind-wing, leads to a forward pitching moment when the body angle is increased; in Muscina, a forward pitching moment is produced by backward displacement of the path of the downstroke when the air-flow on the antennae is reduced. In Schistocerca, the compensation for change of attitude is accompanied by a regulation of total lift; in Muscina, with only a single pair of wings, the magnitude and the line of action of the aerodynamic resultant are independently controlled. The change in wing motion in Calliphora during operation of the dynamic reflexes from the halteres (reflex 4) was described by Faust (1952). Figure 24C shows that forward rotation (when one would expect there to be a compensatory backward pitching moment) leads to an increase in angle of attack during the downstroke, especially at the beginning and end of the stroke. If one compares these outline tracings with the silhouettes of Fig. 10 and with the angles of attack shown on

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A

FIG. 24. Tracings from high-speed photographs of the downstroke of Calliphora. A, during backward pitching rotation at 2.5 rotations/sec; B, during normal flight in still air; C,during forward pitching rotation at 2.5 rotations/sec. (From Faust, 1952).

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the developed cylindrical plot of Fig. 11, it is clear that the drag at the top of the stroke and the lift at the bottom of the stroke should both be greater with the motion shown in Fig. 24C; both these will produce a torque tending to resist the forward rotation. Faust did not observe his flies from the side and so would not have detected any change in the path of the wing-tip; it is therefore possible that the path of the downstroke moved forward in Fig. 24C and that is a similar effector response as that observed by Hollick in Muscina. 2. Roll Reflex stabilization in roll has been studied in Schistocerca by Goodman (1965) and Gettrup (1966), in Anax by Mittelstaedt (1950) and in Calliphoru by Faust (1952) and Schneider (1956). The sense organs involved include the eyes, the neck proprioceptors, the campaniform sensilla at the base of the fore-wings and the halteres. In all cases where it has been investigated, the effector movement is a small differential change in the angle of attack in the middle of the downstroke. The movement is particularly clear in Odonata, where it can be elicited when the wings are not beating; in this Order, where the mechanisms of the fore- and hind-wings are entirely independent, all four wings twist (Mittelstaedt, 1950). Mittelstaedt did not determine which muscles are used to produce this motion, but from the work of Neville (1960) it seems probable that it is due to antagonistic action of one or more muscles of the basalar and subalar complexes. Control through a subalar muscle is probable since this will lead to a more powerful downstroke of the wing with the greater angle of attack. There is no reason to doubt that this is the general mechanism of control in roll but a complication arises in those insects in which the fore- and hind-wings are coupled together; here the angle of attack of the forewings cannot be changed without change in the azimuthal position of the hind-wings. The difficultyis resolved in the case of the Apidae by the fact that the direct basalar and subalar muscles of the metathorax are the only muscles producing downward torque on the hind-wings ; both are tonic, non-fibrillar muscles acting through elastic apodemes, and if control is exercised mainly through the larger subalar muscle, then increased angle of attack and relative downward displacement of the hind-wing will be produced simultaneously.

3. Yaw Turning need not be linked to banking in a flying machine that lacks a rudder and tail surfaces. Insects therefore require reflex control in both

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roll and yaw, though the two may be linked; if there is forward motion through the air, a banked turn is aerodynamically more efficient, but in hovering flight banking is unnecessary. Control of directional change has been studied in Schistocercu by Weis-Fogh (1956b) and Dugard (1967), in muscid Diptera by Faust (1952), Smyth and Yurkevicz (1966), Nachtigall (1967) and Nachtigall and Wilson (1967), in Apis by Stellwaag (1916), Schaller (1960), Kunze (1961), Heran and Lindauer (1963) and in Oryctes by Burton (1964). There seems to be a real difference between different insects in the way turning movements are brought about. In Sclzisfocercu flying in front of a wind-tunnel and induced to turn by greater illumination of one-half of the visual field, the chief effector action was a greater and earlier pronation of the left fore-wing during a left turn ; the left wing also moved more rapidly than the right wing in its downstroke (Dugard, 1967). The change was produced by earlier and double firing of the first basalar muscle and by bringing into action one or both of the motor units in the second basalar muscle; the motor discharge to the subalar muscle was constant. The basalars on the outer side of the turn had some activity, even during rapid turns. There was no change in the pattern of movement of the hind-wings or of the motor impulses to metathoracic flight muscles, but legs and abdomen were extended towards the inside of the turn, the former through excitation of the second coxal abductors and anterior rotators at flight frequency and synchronized, respectively, with the up- and downstrokes. In the locust, control in yaw is therefore exercised by variation in angle of attack during the downstroke, but different muscles are used from those involved in the lift-control reaction and in adjustment of pitch. No difference in the frequency of motor excitation to the indirect muscles on the two sides during a turn has been reported in Schistocercu, but in Oryctes Burton (1964) states that the motor nerve impulse frequency to all six pairs of fibrillar flight muscles is increased unilaterally on the side away from which the insect is turning during asymmetrical visual stimulation. In muscid Diptera, Smyth and Yurkiewicz (1966) state that there is no difference between the left and right sides, and Nachtigall and Wilson (1967) confirm this in the extreme case when one wing is folded and not beating. This feature may be peculiar to Coleoptera. In Oryctes the amplitude of beat (stroke angle) is increased on the outer side during a turn, producing both a yawing and a rolling moment owing to the fact that the aerodynamic resultant is directed downwards and backwards in forward flight; the result must be a banked turn. In Diptera the power does not appear to be a controlled variable in

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regulation of yaw, which must be done by change of other parameters under the control of tonic muscles; yaw and roll can thus be dissociated in the way that would be expected in insects that can hover or fly forward very slowly. There is disagreement in the literature about the nature of the control movement. Nachtigall and Wilson (1967) observed spontaneous asymmetries of wing movement in tethered flies in still air. They found that asymmetrical beating was accompanied by excitation of the direct abductor or adductor muscles. When only the left wing was beating, the right adductor and the left abductor muscles were active; when only the right wing was beating, the reverse pattern was observed. During symmetrical wing movements, both muscles were usually silent, but were sometimes observed to fire at lower frequency when there was not a visually obvious turn in progress. That this is a normal mechanism of producing yawing torques is inferred from an observation by Magnan (1934) of similar asymmetries in free flight and small fore-and-aft displacements seen in high-speed photographs. Compensatory movements quite different from this were described by Faust (1952) during yawing rotations of Culliphora with intact halteres (Fig. 25). During neither direction of rotation was there any change of stroke angle, nor any modification of the upstroke, but during the downstroke the angles of attack were extremely unequal on the two sides. Examination of these tracings together with the wing-tip trajectory of Fig. 14 shows that, for example, the wing motion of Fig. 25A must produce greatly increased drag from the right wing and some increase in lift from the left. These are exactly the torques required to produce the most rapid compensation for a yaw to the left in free flight. It must therefore be doubted whether the large differences in foreand-aft wing position and in stroke angle seen in the experiments of Nachtigall and Wilson (1967) represent a normal effector pattern for regulation in the yawing plane. Their experiments were done in still air in which the flight of many muscid Diptera is intermittent. The drawing back of the wing by the muscles of the third axillary sclerite normally accompanies the termination of flight in all insects except the Odonata and is evidently used by Diptera for quick stops (Boettiger, 1957). The large size of the tergal muscle of the basalar (abductor of Ritter, 1911) is also a peculiar feature of the Diptera and could be correlated with their ability to start flight very rapidly; it is small or absent in Apidae and Oryctes, where the wings are brought forward and held forward in flight largely through the tonic contraction of both sets of indirect muscles (Pringle, I961 and unpublished observations). The observation by Nachtigall and Wilson (1967) that neither abductor nor adductor

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muscles were excited during steady flight is also consistent with the view that this antagonistic pair of muscles is concerned with starting and stopping and not with control in yaw. In the honey-bee, Stellwaag (1916) figured and described briefly a quite distinct mechanism of control, a differential change in stroke plane

B

C

FIG. 25. Tracings from high-speed photographs of the downstroke of Cafliphora. A, during yawing to the left at 2.2 rotations/sec; B, during normal flight in still air; C, during yawing to the right at 1.5 rotations/sec. (From Faust, 1952).

on the two sides. We have already seen that the ability to change the plane of the wing beat is a peculiar feature of the wing mechanism of the bee, and it has been suggested that it is achieved by the axillary lever and used for the control of lift. Anatomically, the axillary lever

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mechanisms of the left and right sides are entirely distinct and could be used differentially. The result would be a banked turn. Schaller (1960), on the basis of some not very convincing flash photographs, states that there is yet another mechanism of control in yaw and one which, unlike all other cases described in insects, involves a change in the form of the upstroke. Schaller induced turning by moving a pattern of vertical stripes past a tethered bee in opposite fore-and-aft directions on the two sides. His photographs show asymmetrical positions of legs and abdomen and large differences in the angle of attack of the wings on the two sides in the same way as was described by Faust for flies (Fig. 25), but he interprets them as showing changes in the angle of attack during the upstroke. Since an increased angle of attack on the side to which the bee is trying to turn correlates with a slight reduction in stroke amplitude, this does not make sense, since a large angle of attack during the upstroke would produce a smaller aerodynamic loading. Kunze (1961) measured torques of up to g cm with the bee in a very similar attitude, and we may conclude that Schaller’s interpretation of his results was wrong and that the same compensatory movements are made by the honey-bee during optomotor yawing reflexes as by the fly during yaw detected by the halteres. V I . COMPARATIVE STUDIES A . AXIOMS

A physiologist is interested in comparative studies primarily because a knowledge of variety may make it easier to understand basic mechanisms. It is axiomatic in the study of insect flight that the basic organization arose only once and that the anatomical and physiological patterns that are now to be found in the different Orders have evolved by differentiation in different ways from a common plan. It follows that homologies can be traced in the flight muscles and in the nerves and sense organs that are involved in flight reflexes. More important, these reflexes themselves should have a common pattern, so that it would be surprising (though never, of course, impossible) that an entirely different control movement should be used in one insect from that common to the others. At the extremes of evolutionary specialization, these homologies may be difficult to unravel, but the assumption that they are there to be unravelled provides the stimulus for this sort of essay. Kinematic and aerodynamic principles provide a further unifying

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influence. The insect wing moves essentially about a pivot, formed by complex folding of the cuticle at its base and local thickening with elastic or hard pads to form the axillary sclerites. It has three degrees of freedom in space and one in time. Thus, it can show elevation and depression, promotion and remotion, pronation and supination, and each of these motions can occur at different velocities. Furthermore, the wing is not a rigid structure, but can sometimes twist about its long axis, change section or even fold. There are, however, only certain combinations of these movements which generate lift and thrust, and once these are understood in a few insects in different size ranges, it begins to be possible to appreciate the common themes. Differences in shape between different insects arise mainly because of differential growth of the epidermal cells which lay down the cuticle. Since the muscle fibres insert directly into the cuticle, such differential growth can give rise to apparent migration of the insertions of muscles on to adjacent sclerites. By differentiation of the amount and type of cuticle laid down in different places, apparently new cuticular structures can form or old ones can change their shape. In extreme cases of this process, the nature of the reflex patterns of which certain muscles form a part may be the best clue to homology. There are few flight muscles in any insect that cannot reasonably be derived from one of the ten basic muscles shown in Fig. 26. It is the

A

B

FIG.26. Diagrammatic views of the ten muscles in the right half of a pterothoracic segment. A, more medial muscles; B, more lateral muscles. dlm, dorsal longitudinal; odm, oblique dorsal; dvm, dorsoventral; fin, wing-folding muscle of 3rd axillary;pm, pleurosternal; hi,basalar; sm, subalar; tpnil, anterior tergo-pleural; isw, intersegmental ; @ma, posterior tergo-pleural. (From Pringle, 1957).

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thesis of this review that not only was the anatomical pattern laid down early in insect evolution, but that the pattern of nervous organization was also defined at an early stage, so that it is, in principle, possible to trace continuity of function for each of these ten muscles and for the reflexes of which they form the effector machinery. This means that though the muscle may change its size and the insertions of different parts of it may move owing to differential cuticular growth, the contribution the muscle makes to the movements of the whole insect in the air either remains unchanged or changes by slow degrees so that at all stages of the process it is of advantage to the insect. It is argued that this continuity of function is preserved for each individual muscle even as it changes its physiological properties in a way that would make it seem, at first sight, inevitable that it must play a different r81e in the flight machinery. B. D I F F E R E N T I A T I O N O F T H E F L I G H T MUSCLES

Histologically and physiologically it is possible to distinguish three types of muscle in the flight system: tubular, comprising all the tonic muscles and the twitching, power-producing muscles of Odonata and cockroaches; close-packed, forming the power-producing muscles of Orthoptera, Lepidoptera and the other “synchronous” insects ;fibrillur, forming the self-oscillatory muscles of Hymenoptera, Diptera, Coleoptera and Hemiptera (Pringle, 1957). It used to be thought that within any one Order the distribution of these types of muscle was constant, but recent work has revealed considerable diversity and generalization is now dangerous. As a final summary an outline will be given of the functions and patterns of differentiation shown by the ten muscles, emphasizing newly discovered facts. The information about Hymenoptera comes from Daly (1963) unless otherwise stated. 1. Dorsal longitudinal (dlm) Probably always an important power-producing downstroke muscle. Reduced in Odonata. Close-packed in Orthoptera, mesothorax of Lepidoptera, Cicadidae, Sirex and Cephus (Hymenoptera). Fibrillar in metathorax of Coleoptera and Xyelu (Hymenoptera), mesothorax of Diptera and all other Hymenoptera, Hemiptera and Homoptera. The rnetathoracic dlwi of Apis and nearly all Hymenoptera is tubular and serves to control the transmission of energy from the mesothorax to the hind-wings, thereby preserving its original function (Pringle, 1961).

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2. Oblique dorsal (odm)

This indirect muscle appears to act, where it is present, as an upstroke supinatar, thus resembling the direct basalar and subalar muscles of some insects in providing both power and control of angle of attack. Absent or tubular and reduced in Orthoptera, Odonata and Lepidoptera. Close-packed in mesothorax of Cicadidae. Fibrillar in metathorax of Coleoptera, both segments of Xyela, mesothorax of Diptera (large except in Ptychoptera, Smart, 1959), other Hemiptera and Homoptera (Barber and Pringle, 1966), and some Hymenoptera but not Apis or Vespa. One may speculate that possession of this muscle, in either closepacked or fibrillar form, enables insects to achieve a greater degree of supination of the wing during the upstroke. All species known to possess it can hover; the honey-bee, which can hover, does not possess it, but can rotate the stroke plane by means of the axillary lever. 3. Dorsoveiztral (dvm) A complex of muscles in most insects, inserting dorsally on the tergum but ventrally on sternum, coxa or trochanter. The main powerproducing upstroke muscle, following the durn closely in its histological type. Part of it differentiates into the close-packed tergo-trochanteral muscle in many Diptera, where the rest of the muscle is fibrillar (Smart, 1959). Absent in Leptomastix (Chalcidae), which thus has no muscular antagonist to the fibrillar dlm, but instead an apodemal ligament. Absent in metathorax of Apis and Vespa but fibrillar in the metathorax of some Hymenoptera Apocrita, where this portion attaches to a detached notal sclerite. Neville (1960) describes a similar situation in Odonata, where the close-packed anterior coxoalar muscle produces supination at the end of the downstroke and throughout the upstroke by separate movement of the lateroprescutum. 4. Third axillary muscle

Present and tubular in all insects that can fold their wings. One of the most constant functional r8les of all the flight muscles.

5. Pleurosternal Tubular in all insects. Its location in Oryctes and Apidae makes it hard to see how it can influence the lateral stiffness of the thoracic box, but elsewhere, especially in Diptera, it evidently has this function. Replaced by a skeletal bridge in some Lepidoptera (Chadwick, 1959).

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6. Basalar Dorsal insertion on basafar sclerite of pleuron, if this is differentiated; ventral insertion on sternum, coxa, or pleuron. Produces downstroke pronation. Close-packed in both segments in Schistocerca, Odonata, Sirex and Cephus. Fibrillar in metathorax of Coleoptera and some Hymenoptera (pleural portion), in mesothorax of Belostomatidae (Barber and Pringle, 1966) and some Hymenoptera including Ichneumonidae. Tubular in Apis, Vespa and Diptera. The basalar complex may contain up to three distinct muscles. In Schistocerca contraction of the first basalar is required for proper pronation, and the excitation of its single motor unit is normally a pair of impulses; the second basalar has more variable excitation but produces less supination (Wilson and Weis-Fogh, 1962). The second basalar is the larger muscle in Odonata (Clark, 1940). The first basalar becomes a tubular tonic muscle in Ichneumonidae and some other Hymenoptera in which the second basalar is fibrillar, but the whole muscle is tubular and tonic in Apis and Vespa, where pronation is produced primarily by closure of the scutal cleft under the influence of the indirect muscles and only small adjustments are required by the direct muscles (Pringle, 1965). The tubular pleural musculature of the 1st axillary sclerite in Diptera may represent part of the basalar complex.

7 . Subalar Dorsal insertion on the subalar sclerite, if differentiated; ventral insertion on sternum, coxa or pleuron. Close-packed in both segments in Schistocerca. Fibrillar in metathorax of Coleoptera. Coxal portion fibrillar in mesothorax of Xyela (Hymenoptera) and Diptera Nematocera (Smart, 1959); tubular in other Hymenoptera. First and second subalars close-packed in Odonata, third subalar tubular with a long resilin ligament (Weis-Fogh, 1960); Neville (1960) shows how the third subalar of dragon-flies comes into action near the top of the upstroke, producing a phased supination in spite of the fact that it can only contract tonically (Fig. 22a, d). In Apidae the subalar sclerite is connected to the posterior part of the 2nd axillary sclerite by a ligament, so that tonic contraction of the subalar muscle will partially oppose the natural pronation movement of the wing. In the mesothorax of higher Diptera, where there is no subalar sclerite, the tubular pleural muscles of the 4th axillary probably represent the subalar complex. It is reasonable to suppose that the lift-control reaction of insects other than Schistocerca is also mediated through the subalar muscles.

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Extra power can be added when these muscles are close-packed or fibrillar and extra power can be drawn from the indirect muscles by tonically-controlled supination in other cases. This is a good example of the way reflex functioning may be preserved by a particular muscle even though its physiological type changes in the course of evolution.

8. Anterior tergopleural Dorsal insertion on the prealar arm of the tergum; ventral insertion on or near pleural ridge or basalar sclerite. Probably always tubular and usually small, but large in Diptera, where it forms the main abductor muscle of the wing (Bonhag, 1949; Nachtigall and Wilson, 1967). Part forms the remotor muscle in the metathorax of Coleoptera, where it could exercise an opposing tension to the oscillatory basalar (Darwin and Pringle, 1959). 9. Intersegtnental muscle Ventral insertion on sternal apophysis ;posterior, dorsal insertion on lateral part of post-phragma. The involvement of this muscle in the flight machinery has been doubtful and Neville (1960) has now shown that in Odonata it produces elevation of the abdomen. It is important in this review only because the axillary lever muscle of the Apidae has been homologized with it on morphological grounds (Daly, 1964); this seems improbable in view of Neville’s discovery, an‘d the axillary lever muscle will here be assumed to be a differentiation of part of the posterior tergopleural complex. 10. Posterior tergopleural Dorsal insertion on postero-lateral part of tergum near posterior notal wing process; ventral insertion on pleuron. Always tubular. Small in Orthoptera and Odonata, but one of the largest controlling systems in Hymenoptera and Diptera, where it becomes complex. Pringle (1961) suggested from an examination of the anatomy of bees that one of these muscles (which he called the scutellar muscle, no. 75 of Snodgrass, 1942) might be responsible for control of the pitching moment. Pronation at the start of the downstroke in a bee is produced by closure of the scutal cleft under the pull of the large, fibrillar dorsal longitudinal muscle acting through the lateral arm of the postphragma (Fig. 23) and does not require the phasic contraction of the direct muscles, as in Schistocerca and Odonata; all of these, being tubular in nature, would be unable to follow the frequency of wing beat. Tonic contraction of the “scutellar” muscle resists closure of the scutal cleft and might delay

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pronation at the start of the stroke. Some of the pleural muscles of the posterior notal process in Diptera (Bonhag, 1949) are so placed as to have a similar action. As stated above, the muscle of the axillary lever in bees must now be assumed to be part of the posterior tergopleural complex, so that control of power and of the stroke plane must be added to the possible functions of the tergo-pleural complex. It will require much difficult experimental work to sort out the separate controlling actions of these small tubular muscles and deductions from comparative studies are thus permissible in the absence of better evidence. REFERENCES Baird, J. L. (1965). Aerodynamic behavior of the flesh fly Sarcoplraga bullata (Diptera). Am. 2001.5, 706. Barber, S. B. and Pringle, J. W. S. (1966). Functional aspects of flight in Belostomatid bugs (Heteroptera). Proc. R. SOC.B. 164, 21. Bennett, L. (1966). Insect aerodynamics : vertical sustaining force in near-hovering flight. Science, N . Y. 152, 1263-1266. Boettiger, E. G. (1957). The machinery of insect flight. In “Recent Advances in Invertebrate Physiology” (B. T. Scheer, ed.), pp. 117-142. University of Oregon Publications. Boettiger, E. G. and Furshpan, E. (1952). The mechanics of flight movements in Diptera. Biol. Bull. Woods Hole 102, 200-21 1. Bonhag, P. F. (1949). The thoracic mechanism of the adult horsefly (Diptera: Tabanidae). Mem. Cornell agric. Exp. Sta. no. 285. Burkhardt, D. and Schneider, G. (1957). Die Antennen von Calliphora als Anzeiger der Fliiggeswindigkeit. Z. Naturf. 126, 139-143. Burton, A. J. (1964). Nervous control of flight orientation in a beetle. Nature, Lond. 204, 1333.

Burton, A. J. and Sandeman, D. C. (1961). The lift provided by the elytra of the rhinoceros beetle, Oryctes boas. S. Afr. J. Sci. 57, 107-109. Chadwick, L. E. (1951). Stroke amplitude as a function of air density in the flight of Drosophila. Biol. Bull. Woo& Hole 100, 15-27. Chadwick, L. E. (1953). The motion of the wings. In “Insect Physiology” (K. D. Roeder, ed.). John Wiley and Sons, New York and Chichester. Chadwick, L. E. (1959). The furcopleural muscles of Lepidoptera. Ann. m t . SOC. Am. 52, 665-668. Clark, H. W. (1940). The adult musculature of the Anisopterous dragonfly thorax (Odonata, Anisoptera). J. Morph. 67, 523-565. Daly, H. V. (1963). Close-packed and fibrillar muscles in the Hymenoptera. Ann. ent. SOC.Am. 56,295-306. Daly, H. V. (1964). Skeleto-muscular morphogenesis of the thorax and wings of the honey bee Apis mellifea (Hymenoptera: Apidae). U.Cal. Publ. Ent. 39, 1-77. Darwin, F. W. and Pringle, J. W. S. (1959). The physiology of insect fibrillar muscle. I. Anatomy and innervation of the basalar muscle of lamellicorn beetles. Proc. R. SOC.B, 151, 194-203.

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Demoll, R. (1918). “Der Flug der Insekten und der Vogel.” Gustav Fischer, Jena. Dingle, H. (1961). Flight and swimming reflexes in giant water bugs. Biol. Bull. Woods Hole 121, 117-128. Dugard, J. J. (1967). Directional change in flying locusts. J. Insect Physiol. 13, 1055-1 063. Faust, R. (1952). Untersuchungen zum Halterenproblem. 2001.Jb., Allg. 2001. Physiol. 63, 325-366. Fraenkel, G. (1932). Untersuchungen uber die Koordination von Reflexen und automatisch-nervosen Rhythmen bei Insekten. I. Die Flugreflexe der Insekten und ihre Koordination. Z. vergl. Physiol. 16, 371-393. Fraenkel, G. (1939). The function of the halteres of flies (Diptera). Proc. zool. Sor. Lond. A, 109, 69-78. Fraenkel, G. and Pringle, J. W. S. (1938). Halteres of flies as gyroscopic organs of equilibrium. Nature, Lond. 141, 919-921. Gettmp, E. (1962). Thoracic proprioceptors in the flight system of locusts. Nature, Lond. 193,498499. Gettrup, E. (1963). Phasic stimulation of a thoracic stretch receptor in locusts. J. exp. Biol. 40,323-333. Gettrup, E. (1965a). Control of fore-wing twisting by hindwing receptors in flying locusts. Proc. XIIth int. Congr. Ent., London 1964, 190-192. Gettrup, E. (1965b). Sensory mechanisms in locomotion : the campaniform sensilla of the insect wing and their function during flight. Cold Spr. Harb. Symp. quant. Biol. 30,615-622. Gettrup, E. (1966). Sensory regulation of wing twisting in locusts. J. exp. Biol. 44, 1-16. Gettrup, E. and Wilson, D. M. (1964). The lift-control reaction of flying locusts. J. exp. Biol. 41, 183-190. Goodman, L. J. (1960). The landing responses of insects. I. The landing response of the fly, Lucilia sericata, and other Calliphorinae. J. exp. Biol. 37, 854-878. Goodman, L. J. (1965). The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locust, Schistocerca gregaria. J. exp. Biol. 42, 385-407. Greenewalt, C. H. (1960). “Hummingbirds.” Doubleday & Co., New York. Guthrie, D. M. (1966). The function and line structure of the cephalic airflow receptor in Schistocerca gregaria. J. Cell Sci. 1, 463-470. Harvey, W. R. and Haskell, J. A. (1966). Metabolic control mechanisms in insects. Adv. Insect Physiol. 3, 133-205. Haskell, P. T. (1960). Sensory specialization in response to environmental demands. Symp. zool. SOC.Lond. 3, 1-23. Heran, H. (1955). Versuche uber die Windkompensation der Bienen. Naturwissenschaften 42, 132. Heran, H. (1956). Ein Beitrag zur Frage nach der Wahrnehmungsgrundlage der Entfernungsweise der Bienen. Z. vergl. Physiol. 38, 168-21 8. Heran, H. (1959). Wahrnehmung und Regelung der Flugeigengeschwindigkeit bei Apis mellijica L. 2.vergl. Physiol. 42, 103-163. Heran, H. and Lindauer, M. (1963). Windkompensation und Seitenwindkorrectur der Bienen beim Flug uber Wasser. Z. vergl. Physiol. 47, 39-55. Herbst, H. G. and Freund, K. (1962). Kinematik der Flugel bei ventilierenden Honigbienen. Deufsch. ent. Z. N.F. 9, Hft. I/II, 1-29.

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