Leading-edge vortices elevate lift of autorotating plant seeds.

As they descend, the autorotating seeds of maples and some other trees generate unexpectedly high lift, but how they attain this elevated performance is unknown. To elucidate the mechanisms responsible, we measured the three-dimensional flow around dynamically scaled models of maple and hornbeam seeds. Our results indicate that these seeds attain high lift by generating a stable leading-edge vortex (LEV) as they descend. The compact LEV, which we verified on real specimens, allows maple seeds to remain in the air more effectively than do a variety of nonautorotating seeds. LEVs also explain the high lift generated by hovering insects, bats, and possibly birds, suggesting that the use of LEVs represents a convergent aerodynamic solution in the evolution of flight performance in both animals and plants.

Fly flight: a model for the neural control of complex behavior.

Flies exhibit a repertoire of aerial acrobatics unmatched in robustness and aerodynamic sophistication. The exquisite control of this complex behavior emerges from encoding intricate patterns of optic flow, and the translation of these visual signals into the mechanical language of the motor system. Recent advances in experimental design toward more naturalistic visual and mechanosensory stimuli have served to reinforce fly flight as a key model system for understanding how feedback from multiple sensory modalities is integrated to control complex and robust motor behaviors across taxa.

The control of flight force by a flapping wing: lift and drag production.

We used a dynamically scaled mechanical model of the fruit fly Drosophila melanogaster to study how changes in wing kinematics influence the production of unsteady aerodynamic forces in insect flight. We examined 191 separate sets of kinematic patterns that differed with respect to stroke amplitude, angle of attack, flip timing, flip duration and the shape and magnitude of stroke deviation. Instantaneous aerodynamic forces were measured using a two-dimensional force sensor mounted at the base of the wing. The influence of unsteady rotational effects was assessed by comparing the time course of measured forces with that of corresponding translational quasi-steady estimates. For each pattern, we also calculated mean stroke-averaged values of the force coefficients and an estimate of profile power. The results of this analysis may be divided into four main points. (i) For a short, symmetrical wing flip, mean lift was optimized by a stroke amplitude of 180 degrees and an angle of attack of 50 degrees. At all stroke amplitudes, mean drag increased monotonically with increasing angle of attack. Translational quasi-steady predictions better matched the measured values at high stroke amplitude than at low stroke amplitude. This discrepancy was due to the increasing importance of rotational mechanisms in kinematic patterns with low stroke amplitude. (ii) For a 180 degrees stroke amplitude and a 45 degrees angle of attack, lift was maximized by short-duration flips occurring just slightly in advance of stroke reversal. Symmetrical rotations produced similarly high performance. Wing rotation that occurred after stroke reversal, however, produced very low mean lift. (iii) The production of aerodynamic forces was sensitive to changes in the magnitude of the wing's deviation from the mean stroke plane (stroke deviation) as well as to the actual shape of the wing tip trajectory. However, in all examples, stroke deviation lowered aerodynamic performance relative to the no deviation case. This attenuation was due, in part, to a trade-off between lift and a radially directed component of total aerodynamic force. Thus, while we found no evidence that stroke deviation can augment lift, it nevertheless may be used to modulate forces on the two wings. Thus, insects might use such changes in wing kinematics during steering maneuvers to generate appropriate force moments. (iv) While quasi-steady estimates failed to capture the time course of measured lift for nearly all kinematic patterns, they did predict with reasonable accuracy stroke-averaged values for the mean lift coefficient. However, quasi-steady estimates grossly underestimated the magnitude of the mean drag coefficient under all conditions. This discrepancy was due to the contribution of rotational effects that steady-state estimates do not capture. This result suggests that many prior estimates of mechanical power based on wing kinematics may have been grossly underestimated.

Spanwise flow and the attachment of the leading-edge vortex on insect wings.

The flow structure that is largely responsible for the good performance of insect wings has recently been identified as a leading-edge vortex. But because such vortices become detached from a wing in two-dimensional flow, an unknown mechanism must keep them attached to (three-dimensional) flapping wings. The current explanation, analogous to a mechanism operating on delta-wing aircraft, is that spanwise flow through a spiral vortex drains energy from the vortex core. We have tested this hypothesis by systematically mapping the flow generated by a dynamically scaled model insect while simultaneously measuring the resulting aerodynamic forces. Here we report that, at the Reynolds numbers matching the flows relevant for most insects, flapping wings do not generate a spiral vortex akin to that produced by delta-wing aircraft. We also find that limiting spanwise flow with fences and edge baffles does not cause detachment of the leading-edge vortex. The data support an alternative hypothesis-that downward flow induced by tip vortices limits the growth of the leading-edge vortex.

The production of elevated flight force compromises manoeuvrability in the fruit fly Drosophila melanogaster.

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

The correlation between wing kinematics and steering muscle activity in the blowfly Calliphora vicina.

Determining how the motor patterns of the nervous system are converted into the mechanical and behavioral output of the body is a central goal in the study of locomotion. In the case of dipteran flight, a population of small steering muscles controls many of the subtle changes in wing kinematics that allow flies to maneuver rapidly. We filmed the wing motion of tethered Calliphora vicina at high speed and simultaneously recorded multi-channel electromyographic signals from some of the prominent steering muscles in order to correlate kinematics with muscle activity. Using this analysis, we found that the timing of each spike in the basalare muscles was strongly correlated with changes in the deviation of the stroke plane during the downstroke. The relationship was non-linear such that the magnitude of the kinematic response to each muscle spike decreased with increasing levels of stroke deviation. This result suggests that downstroke deviation is controlled in part via the mechanical summation of basalare activity. We also found that interactions among the basalares and muscles III2-III4 determine the maximum forward amplitude of the wingstroke. In addition, activity in muscle I1 appears to participate in a wingbeat gearing mechanism, as previously proposed. Using these results, we have been able to correlate changes in wing kinematics with alteration in the spike rate, firing phase and combinatorial activity of identified steering muscles.

The scaling of carbon dioxide release and respiratory water loss in flying fruit flies (Drosophila spp.).

By simultaneously measuring carbon dioxide release, water loss and flight force in several species of fruit flies in the genus Drosophila, we have investigated respiration and respiratory transpiration during elevated locomotor activity. We presented tethered flying flies with moving visual stimuli in a virtual flight arena, which induced them to vary both flight force and energetic output. In response to the visual motion, the flies altered their energetic output as measured by changes in carbon dioxide release and concomitant changes in respiratory water loss. We examined the effect of absolute body size on respiration and transpiration by studying four different-sized species of fruit flies. In resting flies, body-mass-specific CO(2) release and water loss tend to decrease more rapidly with size than predicted according to simple allometric relationships. During flight, the mass-specific metabolic rate decreases with increasing body size with an allometric exponent of -0.22, which is slightly lower than the scaling exponents found in other flying insects. In contrast, the mass-specific rate of water loss appears to be proportionately greater in small animals than can be explained by a simple allometric model for spiracular transpiration. Because fractional water content does not change significantly with increasing body size, the smallest species face not only larger mass-specific energetic expenditures during flight but also a higher risk of desiccation than their larger relatives. Fruit flies lower their desiccation risk by replenishing up to 75 % of the lost bulk water by metabolic water production, which significantly lowers the risk of desiccation for animals flying under xeric environmental conditions.

The effect of removing the N-terminal extension of the Drosophila myosin regulatory light chain upon flight ability and the contractile dynamics of indirect flight muscle.

The Drosophila myosin regulatory light chain (DMLC2) is homologous to MLC2s of vertebrate organisms, except for the presence of a unique 46-amino acid N-terminal extension. To study the role of the DMLC2 N-terminal extension in Drosophila flight muscle, we constructed a truncated form of the Dmlc2 gene lacking amino acids 2-46 (Dmlc2(Delta2-46)). The mutant gene was expressed in vivo, with no wild-type Dmlc2 gene expression, via P-element-mediated germline transformation. Expression of the truncated DMLC2 rescues the recessive lethality and dominant flightless phenotype of the Dmlc2 null, with no discernible effect on indirect flight muscle (IFM) sarcomere assembly. Homozygous Dmlc2(Delta2-46) flies have reduced IFM dynamic stiffness and elastic modulus at the frequency of maximum power output. The viscous modulus, a measure of the fly's ability to perform oscillatory work, was not significantly affected in Dmlc2(Delta2-46) IFM. In vivo flight performance measurements of Dmlc2(Delta2-46) flies using a visual closed-loop flight arena show deficits in maximum metabolic power (P(*)(CO(2))), mechanical power (P(*)(mech)), and flight force. However, mutant flies were capable of generating flight force levels comparable to body weight, thus enabling them to fly, albeit with diminished performance. The reduction in elastic modulus in Dmlc2(Delta2-46) skinned fibers is consistent with the N-terminal extension being a link between the thick and thin filaments that is parallel to the cross-bridges. Removal of this parallel link causes an unfavorable shift in the resonant properties of the flight system, thus leading to attenuated flight performance.

How animals move: an integrative view.

Recent advances in integrative studies of locomotion have revealed several general principles. Energy storage and exchange mechanisms discovered in walking and running bipeds apply to multilegged locomotion and even to flying and swimming. Nonpropulsive lateral forces can be sizable, but they may benefit stability, maneuverability, or other criteria that become apparent in natural environments. Locomotor control systems combine rapid mechanical preflexes with multimodal sensory feedback and feedforward commands. Muscles have a surprising variety of functions in locomotion, serving as motors, brakes, springs, and struts. Integrative approaches reveal not only how each component within a locomotor system operates but how they function as a collective whole.

Convergent mechanosensory input structures the firing phase of a steering motor neuron in the blowfly, Calliphora.

The first basalar muscle (B1) is 1 of 17 small steering muscles in flies that control changes in wing stroke kinematics during flight. The B1 is often tonically active, firing a single phase-locked action potential in each and every wingbeat cycle. Changes in activation phase alter the biomechanical properties of B1, which in turn cause aerodynamically relevant changes in wing motion. The phase-locked firing of the B1 motor neuron (MNB1), is thought to arise from an interaction of wingbeat-synchronous inputs from the wings and from specialized equilibrium organs called halteres that beat antiphase to the wings and function to detect angular rotation of the body during flight. We investigated how the wing and haltere inputs interact to determine the firing phase of MNB1. Our results indicate that both wing and haltere afferents make strong monosynaptic connections with MNB1, consisting of fast electrical and slow Ca(2+)-sensitive components. Although both the wing and haltere-evoked excitatory postsynaptic potentials (EPSPs) display the two components, their relative contribution is different for the two inputs. Whereas the haltere-evoked EPSP is dominated by the fast electrical component, the wing-evoked EPSP is dominated by a large chemically mediated component and displays an additional prolonged Ca(2+)-dependent component that is absent in the haltere-evoked EPSP. Both inputs display an activity-dependent fatigue affecting both electrical and Ca(2+)-sensitive components, from which the haltere synapse recovers more rapidly. The net result of these synaptic differences is that the two pathways differ significantly in their relative ability to evoke action potentials in MNB1. Although the haltere pathway displays greater temporal precision, the wing pathway is stronger, judged by its ability to entrain MNB1 within a background of haltere stimulation. We propose a model by which these physiological differences play a functional role in tuning the firing phase of MNB1 during flight. The wing input may serve primarily to set the background firing phase of MNB1, whereas the haltere input serves to transiently advance the firing phase during equilibrium reflexes.

Wing rotation and the aerodynamic basis of insect flight.

The enhanced aerodynamic performance of insects results from an interaction of three distinct yet interactive mechanisms: delayed stall, rotational circulation, and wake capture. Delayed stall functions during the translational portions of the stroke, when the wings sweep through the air with a large angle of attack. In contrast, rotational circulation and wake capture generate aerodynamic forces during stroke reversals, when the wings rapidly rotate and change direction. In addition to contributing to the lift required to keep an insect aloft, these two rotational mechanisms provide a potent means by which the animal can modulate the direction and magnitude of flight forces during steering maneuvers. A comprehensive theory incorporating both translational and rotational mechanisms may explain the diverse patterns of wing motion displayed by different species of insects.

Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.

Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is mediated in part by motion-sensitive visual interneurons that project to steering motor circuitry within the thorax. Flies, however, possess a unique flight control equilibrium sense that is encoded by mechanoreceptors at the base of the halteres, small dumb-bell-shaped organs derived through evolutionary transformation of the hind wings. To study the input of the haltere system onto the flight control system, I constructed a mechanically oscillating flight arena consisting of a cylindrical array of light-emitting diodes that generated the moving image of a 30 degrees vertical stripe. The arena provided closed-loop visual feedback to elicit fixation behaviour, an orientation response in which flies maintain the position of the stripe in the front portion of their visual field by actively adjusting their wing kinematics. While flies orientate towards the stripe, the entire arena was swung back and forth while an optoelectronic device recorded the compensatory changes in wing stroke amplitude and frequency. In order to reduce the background changes in stroke kinematics resulting from the animal's closed-loop visual fixation behaviour, the responses to eight identical mechanical rotations were averaged in each trial. The results indicate that flies possess a robust equilibrium reflex in which angular rotations of the body elicit compensatory changes in both the amplitude and stroke frequency of the wings. The results of uni- and bilateral ablation experiments demonstrate that the halteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Coriolis forces that result from the linear motion of the haltere within the rotating frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directional tuning map of the haltere-mediated reflexes. The directional tuning of the reflex is quite linear such that the kinematic responses vary as simple trigonometric functions of stimulus orientation. The reflexes function primarily to stabilize pitch and yaw within the horizontal plane.

Visual input to the efferent control system of a fly's "gyroscope".

Dipterous insects (the true flies) have a sophisticated pair of equilibrium organs called halteres that evolved from hind wings. The halteres are sensitive to Coriolis forces that result from angular rotations of the body and mediate corrective reflexes during flight. Like the aerodynamically functional fore wings, the halteres beat during flight and are equipped with their own set of control muscles. It is shown that motoneurons innervating muscles of the haltere receive strong excitatory input from directionally sensitive visual interneurons. Visually guided flight maneuvers of flies may be mediated in part by efferent modulation of hard-wired equilibrium reflexes.

Phosphorylation-dependent power output of transgenic flies: an integrated study.

We examine how the structure and function of indirect flight muscle (IFM) and the entire flight system of Drosophila melanogaster are affected by phosphorylation of the myosin regulatory light chain (MLC2). This integrated study uses site-directed mutagenesis to examine the relationship between removal of the myosin light chain kinase (MLCK) phosphorylation site, in vivo function of the flight system (flight tests, wing kinematics, metabolism, power output), isolated IFM fiber mechanics, MLC2 isoform pattern, and sarcomeric ultrastructure. The MLC2 mutants exhibit graded impairment of flight ability that correlates with a reduction in both IFM and flight system power output and a reduction in the constitutive level of MLC2 phosphorylation. The MLC2 mutants have wild-type IFM sarcomere and cross-bridge structures, ruling out obvious changes in the ultrastructure as the cause of the reduced performance. We describe a viscoelastic model of cross-bridge dynamics based on sinusoidal length perturbation analysis (Nyquist plots) of skinned IFM fibers. The sinusoidal analysis suggests the high power output of Drosophila IFM required for flight results from a phosphorylation-dependent recruitment of power-generating cross-bridges rather than a change in kinetics of the power generating step. The reduction in cross-bridge number appears to affect the way mutant flies generate flight forces of sufficient magnitude to keep them airborne. In two MLC2 mutant strains that exhibit a reduced IFM power output, flies appear to compensate by lowering wingbeat frequency and by elevating wingstroke amplitude (and presumably muscle strain). This behavioral alteration is not seen in another mutant strain in which the power output and estimated number of recruited cross-bridges is similar to that of wild type.

The evolution of insect wings and their sensory apparatus.

The development of wings has undoubtedly played a major role in the enormous diversification of insects. New insights into the evolutionary history of insect wings are available from paleontological, physiological and biomechanical studies. A recent hypothesis, derived primarily from paleontological evidence, is that wings arose from leg exites, small flaps associated with proximal leg segments. We present data from studies on physical models that are consistent with this hypothesis. The exites would have been moveable, and measurements on scaled models show that they would have generated aerodynamic lift by unsteady mechanisms associated with vortex shedding. An examination of the sensory structures found on insect wings is also consistent with the interpretation of protowings as leg exites. In addition to mechanosensory bristles, such as are found all over the body, the wings of modern insects carry campaniform sensilla sensitive to cuticular deformation and contact chemoreceptors whose stimulation elicits a feeding response. Both classes of receptors are also found on the legs of modern insects but not on the thorax, favoring the leg exite theory.

The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster.

The limits of flight performance have been estimated in tethered Drosophila melanogaster by modulating power requirements in a 'virtual reality' flight arena. At peak capacity, the flight muscles can sustain a mechanical power output of nearly 80 W kg-1 muscle mass at 24 degrees C, which is sufficient to generate forces of approximately 150% of the animal's weight. The increase in flight force above that required to support body weight is accompanied by a rise in wing velocity, brought about by an increase in stroke amplitude and a decrease in stroke frequency. Inertial costs, although greater than either profile or induced power, would be minimal with even modest amounts of elastic storage, and total mechanical power energy should be equivalent to aerodynamic power alone. Because of the large profile drag expected at low Reynolds numbers, the profile power was approximately twice the induced power at all levels of force generation. Thus, it is the cost of overcoming drag, and not the production of lift, that is the primary requirement for flight in Drosophila melanogaster. By comparing the estimated mechanical power output with respirometrically measured total power input, we determined that muscle efficiency rises with increasing force production to a maximum of 10%. This change in efficiency may reflect either increased crossbridge activation or a favorable strain regime during the production of peak forces.

In vivo length oscillations of indirect flight muscles in the fruit fly Drosophila virilis.

We have used high-speed video microscopy to measure in vivo length oscillations of the indirect flight muscles of the fruit fly Drosophila virilis during tethered flight. The changes in muscle strain were measured by tracking the deformation of the thoracic exoskeleton at the origin and insertion of both the dorsal longitudinal (DLM) and the dorsal ventral (DVM) muscles. The mean peak-to-peak strain amplitudes were found to be 3.5% for the DLMs and 3.3% for the DVMs, although the strain amplitude within individual cycles ranged from 2 to 5%. These values are consistent with the small number of previous measurements of indirect flight muscle strain in other insects, but almost an order of magnitude greater than the strain amplitudes used in most biophysical studies of skinned Drosophila fibers. The results suggest that serial compliance within this sarcomere would need to relieve approximately 70% of the total strain in order for individual crossbridges to remain attached throughout a complete contraction-extension cycle.

The wake dynamics and flight forces of the fruit fly Drosophila melanogaster.

We have used flow visualizations and instantaneous force measurements of tethered fruit flies (Drosophila melanogaster) to study the dynamics of force generation during flight. During each complete stroke cycle, the flies generate one single vortex loop consisting of vorticity shed during the downstroke and ventral flip. This gross pattern of wake structure in Drosophila is similar to those described for hovering birds and some other insects. The wake structure differed from those previously described, however, in that the vortex filaments shed during ventral stroke reversal did not fuse to complete a circular ring, but rather attached temporarily to the body to complete an inverted heart-shaped vortex loop. The attached ventral filaments of the loop subsequently slide along the length of the body and eventually fuse at the tip of the abdomen. We found no evidence for the shedding of wing-tip vorticity during the upstroke, and argue that this is due to an extreme form of the Wagner effect acting at that time. The flow visualizations predicted that maximum flight forces would be generated during the downstroke and ventral reversal, with little or no force generated during the upstroke. The instantaneous force measurements using laser-interferometry verified the periodic nature of force generation. Within each stroke cycle, there was one plateau of high force generation followed by a period of low force, which roughly correlated with the upstroke and downstroke periods. However, the fluctuations in force lagged behind their expected occurrence within the wing-stroke cycle by approximately 1 ms or one-fifth of the complete stroke cycle. This temporal discrepancy exceeds the range of expected inaccuracies and artifacts in the measurements, and we tentatively discuss the potential retarding effects within the underlying fluid mechanics.

Haltere afferents provide direct, electrotonic input to a steering motor neuron in the blowfly, Calliphora.

The first basalar muscle (b1) is one of 17 small muscles in flies that control changes in wing stroke kinematics during steering maneuvers. The b1 is unique, however, in that it fires a single phase-locked spike during each wingbeat cycle. The phaselocked firing of the b1's motor neuron (mnb1) is thought to result from wingbeat-synchronous mechanosensory input, such as that originating from the campaniform sensilla at the base of the halteres. Halteres are sophisticated equilibrium organs of flies that function to detect angular rotations of the body during flight. We have developed a new preparation to determine whether the campaniform sensilla at the base of the halteres are responsible for the phasic activity of b1. Using intracellular recording and mechanical stimulation, we have found one identified haltere campaniform field (dF2) that provides strong synaptic input to the mnb1. This haltere to mnb1 connection consists of a fast and a slow component. The fast component is monosynaptic, mediated by an electrical synapse, and thus can follow haltere stimulation at high frequencies. The slow component is possibly polysynaptic, mediated by a chemical synapse, and fatigues at high stimulus frequencies. Thus, the fast monosynaptic electrical pathway between haltere afferents and mnb1 may be responsible in part for the phase-locked firing of b1 during flight.