Bumblebee Flight in Heavy Turbulence.

High-resolution numerical simulations of a tethered model bumblebee in forward flight are performed superimposing homogeneous isotropic turbulent fluctuations to the uniform inflow. Despite tremendous variation in turbulence intensity, between 17% and 99% with respect to the mean flow, we do not find significant changes in cycle-averaged aerodynamic forces, moments, or flight power when averaged over realizations, compared to laminar inflow conditions. The variance of aerodynamic measures, however, significantly increases with increasing turbulence intensity, which may explain flight instabilities observed in freely flying bees.

Matching spiracle opening to metabolic need during flight in Drosophila.

The respiratory exchange system of insects must maximize the flux of respiratory gases through the spiracles of the tracheal system while minimizing water loss. This trade-off between gas exchange and water loss becomes crucial when locomotor activity is increased during flight and metabolic needs are greatest. Insects that keep their spiracles mostly closed during flight reduce water loss but limit the flux of oxygen and carbon dioxide into and out of the tracheal system and thus attenuate locomotor performance. Insects that keep their spiracles completely open allow maximum gas exchange but face desiccation stress more quickly. Experiments in which water vapor was used as a tracer gas to track changes in the conductance of the respiratory system indicated that flying fruit flies minimize potential water loss by matching the area of the open spiracles to their gas exchange required for metabolic needs. This behavior maintained approximately constant pressure for carbon dioxide (1.35 kilopascals) and oxygen (19.9 kilopascals) within the tracheal system while reducing respirometric water loss by up to 23% compared with a strategy in which the spiracles are held wide open during flight. The adaptive spiracle-closing behavior in fruit flies has general implications for the ecology of flying insects because it shows how these animals may cope with environmental challenges during high locomotor performance.

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.

The efficiency of aerodynamic force production in Drosophila.

Total efficiency of aerodynamic force production in insect flight depends on both the efficiency with which flight muscles turn metabolic energy into muscle mechanical power and the efficiency with which this power is converted into aerodynamic flight force by the flapping wings. Total efficiency has been estimated in tethered flying fruit flies Drosophila by modulating their power expenditures in a virtual reality flight simulator while simultaneously measuring stroke kinematics, locomotor performance and metabolic costs. During flight, muscle efficiency increases with increasing flight force production, whereas aerodynamic efficiency of lift production decreases with increasing forces. As a consequence of these opposite trends, total flight efficiency in Drosophila remains approximately constant within the kinematic working range of the flight motor. Total efficiency is broadly independent of different profile power estimates and typically amounts to 2-3%. The animal achieves maximum total efficiency near hovering flight conditions, when the beating wings produce flight forces that are equal to the body weight of the insect. It remains uncertain whether this small advantage in total efficiency during hovering flight was shaped by evolutionary factors or results from functional constraints on both the production of mechanical power by the indirect flight muscles and the unsteady aerodynamic mechanisms in flapping flight.

Ambient temperature affects free-flight performance in the fruit fly Drosophila melanogaster.

To gain insight into how temperature affects locomotor performance in insects, the limits of flight performance have been estimated in freely flying fruit flies Drosophila melanogaster by determining the maximum load that a fly could carry following take-off. At a low ambient temperature of 15 degrees C, muscle mechanical power output matches the minimum power requirements for hovering flight. Aerodynamic force production rises with increasing temperature and eventually saturates at a flight force that is roughly equal to 2.1 times the body mass. Within the two-fold range of different body sizes, maximum flight force production during free flight does not decrease with decreasing body size as suggested by standard aerodynamic theories. Estimations of flight muscle mechanical power output yields a peak performance of 110 W kg-1 muscle tissue for short-burst flight that was measured at an ambient temperature of 30 degrees C. With respect to the uncertainties in estimating muscle mechanical power during free flight, the estimated values are similar to those that were published for flight under tethered flight conditions.

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.

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.

Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster.

During tethered flight in Drosophila melanogaster, spike activity of the second basalar flight-control muscle (M.b2) is correlated with an increase in both the ipsilateral wing beat amplitude and the ipsilateral flight force. The frequency of muscle spikes within a burst is about 100 Hz, or 1 spike for every two wing beat cycles. When M.b2 is active, its spikes tend to occur within a comparatively narrow phase band of the wing beat cycle. To understand the functional role of this phase-lock of firing in the control of flight forces, we stimulated M.b2 in selected phases of the wing beat cycle and recorded the effect on the ipsilateral wing beat amplitude. Varying the phase timing of the stimulus had a significant effect on the wing beat amplitude. A maximum increase of wing beat amplitude was obtained by stimulating M.b2 at the beginning of the upstroke or about 1 ms prior to the narrow phase band in which the muscle spikes typically occur during flight. Assuming a delay of 1 ms between the stimulation of the motor nerve and muscle activation, these results indicate that M.b2 is activated at an instant of the stroke cycle that produces the greatest effect on wing beat amplitude.

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 active control of wing rotation by Drosophila.

This paper investigates the temporal control of a fast wing rotation in flies, the ventral flip, which occurs during the transition from downstroke to upstroke. Tethered flying Drosophila actively modulate the timing of these rapid supinations during yaw responses evoked by an oscillating visual stimulus. The time difference between the two wings is controlled such that the wing on the outside of a fictive turn rotates in advance of its contralateral partner. This modulation of ventral-flip timing between the two wings is strongly coupled with changes in wing-stroke amplitude. Typically, an increase in the stroke amplitude of one wing is correlated with an advance in the timing of the ventral flip of the same wing. However, flies do display a limited ability to control these two behaviors independently, as shown by flight records in which the correlation between ventral-flip timing and stroke amplitude transiently reverses. The control of ventral-flip timing may be part of an unsteady aerodynamic mechanism that enables the fly to alter the magnitude and direction of flight forces during turning maneuvers.

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.