The Control of Mechanical Power in Insect Flight

SYNOPSIS. The cost of locomotion is rarely constant, but rathervaries as an animal changes speed and direction. Ultimately,the locomotory muscles of an animal must compensate for thesechanging requirements by varying the amount of mechanical powerthat they produce. In this paper, we consider the mechanismsby which the mechanical power generated by the asynchronousflight muscles of the fruit fly, Drosophila melanogaster, isregulated to match the changing requirements during flight controlbehaviors. Our data come from individual flies flown in a flightarena under conditions in which stroke kinematics, total metaboliccost, and flight force are simultaneously measured. In orderto increase force production, flies must increase wing beatfrequency and wing stroke amplitude. Theory predicts that thesekinematics changes should result in a roughly cubic increasein the mechanical power requirements for flight. However, themechanical energy generated by muscle should increase only linearlywith stroke amplitude and frequency. This discrepancy impliesthat flight muscles must either recruit myofibrils or increaseactivation in order to generate sufficient mechanical powerto sustain elevated force production. By comparing respirometricallymeasured total metabolic power with kinematically estimatedmechanical power, we have calculated that the stress in theflight muscles of Drosophila must increase by 50% to accommodatea doubling of flight force. Electrophysiological evidence suggeststhat this change in stress may be accomplished by an increasedneural drive to the asynchronous muscles, which in turn mayact to recruit additional cross bridges through an increasein cytosolic calcium.     

New models for the wing extension in pterosaurs

All powered flying animals have to face the same energetic problems: operating the wings during steady flight with muscles that require constant energy input and neural control to work. Accordingly the extant flying vertebrates have apparently found very similar solutions to parts of these issues – the biomechanical automatism built in their skeletal, muscular and connective tissue system. Based on these extant analogues (birds and bats) two new models are presented here for the mechanism of the distal wing extension in pterosaurs, an extinct group of flying vertebrates. The elongate fourth finger which solely supported their extensive flight membrane was a long lever arm that experienced significant loads and for which a reduction in muscle mass through automatisation would have been strongly beneficial. In the first model we hypothesize the presence of a propatagial ligament or ligamentous system which, as a result of the elbow extension, automatically performs and maintains the extension of the wing finger during flight and prohibits the hyperextension of the elbow. The second model has a co-operating bird-like propatagial ligamentous system and bat-like tendinous extensor muscle system on the forearm of the hypothetical pterosaur. Both models provide strong benefits to an animal with powered flight: (1) reduction of muscles and weight in the distal wing; (2) prevention of hyper extension of the elbow against drag; (3) automating wing extension and thereby reducing metabolic costs required to operate the pterosaurian locomotor apparatus. These models, although hypothetical, fit with the existing fossil evidence and lay down a basis for further biomechanical and/or aerodynamical investigations.     

The Function of Dipteran Flight Muscle

The flight muscles of flies are separated into two physiologically, anatomically, and functionally distinct classes: power muscles and control muscles. The large indirect power muscles sustain the high level of mechanical energy required to flap the wings up and down during flight. The contractions in the asynchronous power muscles are initiated by stretch, and their slow presynaptic motor drive serves only to maintain a tonic level of cytosolic calcium. Although providing the mechanical energy for flight, the power muscles are not directly attached to the wings. Instead, their mechanical energy is transmitted to the base of the wings through the complex linkage system of the wing hinge. In contrast, the small control muscles insert directly onto the skeletal elements at the base of the wing. Through their mechanical effects on the hinge, the control muscles act collectively as a transmission system that determines how the mechanical energy produced by the power muscles is transformed into wing motion. The control muscles are activated by motor spikes in the conventional one-for-one fashion. Thus, although the control muscles can generate little mechanical power, they provide the means by which the nervous system can rapidly alter wing kinematics during sophisticated aerial maneuvers.     

In Vivo Time-Resolved Microtomography Reveals the Mechanics of the Blowfly Flight Motor

Dipteran flies are amongst the smallest and most agile of flying animals. Their wings are driven indirectly by large power muscles, which cause cyclical deformations of the thorax that are amplified through the intricate wing hinge. Asymmetric flight manoeuvres are controlled by 13 pairs of steering muscles acting directly on the wing articulations. Collectively the steering muscles account for <3% of total flight muscle mass, raising the question of how they can modulate the vastly greater output of the power muscles during manoeuvres. Here we present the results of a synchrotron-based study performing micrometre-resolution, time-resolved microtomography on the 145 Hz wingbeat of blowflies. These data represent the first four-dimensional visualizations of an organism''s internal movements on sub-millisecond and micrometre scales. This technique allows us to visualize and measure the three-dimensional movements of five of the largest steering muscles, and to place these in the context of the deforming thoracic mechanism that the muscles actuate. Our visualizations show that the steering muscles operate through a diverse range of nonlinear mechanisms, revealing several unexpected features that could not have been identified using any other technique. The tendons of some steering muscles buckle on every wingbeat to accommodate high amplitude movements of the wing hinge. Other steering muscles absorb kinetic energy from an oscillating control linkage, which rotates at low wingbeat amplitude but translates at high wingbeat amplitude. Kinetic energy is distributed differently in these two modes of oscillation, which may play a role in asymmetric power management during flight control. Structural flexibility is known to be important to the aerodynamic efficiency of insect wings, and to the function of their indirect power muscles. We show that it is integral also to the operation of the steering muscles, and so to the functional flexibility of the insect flight motor.     

Dynamics of in vivo power output and efficiency of Nasonia asynchronous flight muscle

By simultaneously measuring aerodynamic performance, wing kinematics, and metabolic activity, we have estimated the in vivo limits of mechanical power production and efficiency of the asynchronous flight muscle (IFM) in three species of ectoparasitoid wasps genus Nasonia (N. giraulti, N. longicornis, and N. vitripennis). The 0.6 mg animals were flown under tethered flight conditions in a flight simulator that allowed modulation of power production by employing an open-loop visual stimulation technique. At maximum locomotor capacity, flight muscles of Nasonia are capable to sustain 72.2 +/- 18.3 W kg(-1) muscle mechanical power at a chemo-mechanical conversion efficiency of approximately 9.8 +/- 0.9%. Within the working range of the locomotor system, profile power requirement for flight dominates induced power requirement suggesting that the cost to overcome wing drag places the primary limit on overall flight performance. Since inertial power is only approximately 25% of the sum of induced and profile power requirements, Nasonia spp. may not benefit from elastic energy storage during wing deceleration phases. A comparison between wing size-polymorphic males revealed that wing size reduction is accompanied by a decrease in total flight muscle volume, muscle mass-specific mechanical power production, and total flight efficiency. In animals with small wings maximum total flight efficiency is below 0.5%. The aerodynamic and power estimates reported here for Nasonia are comparable to values reported previously for the fruit fly Drosophila flying under similar experimental conditions, while muscle efficiency of the tiny wasp is more at the lower end of values published for various other insects.     

Hovering and intermittent flight in birds

Two styles of bird locomotion, hovering and intermittent flight, have great potential to inform future development of autonomous flying vehicles. Hummingbirds are the smallest flying vertebrates, and they are the only birds that can sustain hovering. Their ability to hover is due to their small size, high wingbeat frequency, relatively large margin of mass-specific power available for flight and a suite of anatomical features that include proportionally massive major flight muscles (pectoralis and supracoracoideus) and wing anatomy that enables them to leave their wings extended yet turned over (supinated) during upstroke so that they can generate lift to support their weight. Hummingbirds generate three times more lift during downstroke compared with upstroke, with the disparity due to wing twist during upstroke. Much like insects, hummingbirds exploit unsteady mechanisms during hovering including delayed stall during wing translation that is manifest as a leading-edge vortex (LEV) on the wing and rotational circulation at the end of each half stroke. Intermittent flight is common in small- and medium-sized birds and consists of pauses during which the wings are flexed (bound) or extended (glide). Flap-bounding appears to be an energy-saving style when flying relatively fast, with the production of lift by the body and tail critical to this saving. Flap-gliding is thought to be less costly than continuous flapping during flight at most speeds. Some species are known to shift from flap-gliding at slow speeds to flap-bounding at fast speeds, but there is an upper size limit for the ability to bound (~0.3 kg) and small birds with rounded wings do not use intermittent glides.     

The constraints of body size on aerodynamics and energetics in flying fruit flies: an integrative view

Reynolds number and thus body size may potentially limit aerodynamic force production in flying insects due to relative changes of viscous forces on the beating wings. By comparing four different species of fruit flies similar in shape but with different body mass, we have investigated how small insects cope with changes in fluid mechanical constraints on power requirements for flight and the efficiency with which chemical energy is turned into aerodynamic flight forces. The animals were flown in a flight arena in which stroke kinematics, aerodynamic force production, and carbon dioxide release were measured within the entire working range of the flight motor. The data suggest that during hovering performance mean lift coefficient for flight is higher in smaller animals than in their larger relatives. This result runs counter to predictions based on conventional aerodynamic theory and suggests subtle differences in stroke kinematics between the animals. Estimates in profile power requirements based on high drag coefficient suggest that among all tested species of fruit flies elastic energy storage might not be required to minimize energetic expenditures during flight. Moreover, muscle efficiency significantly increases with increasing body size whereas aerodynamic efficiency tends to decrease with increasing size or Reynolds number. As a consequence of these two opposite trends, total flight efficiency tends to increase only slightly within the 6-fold range of body sizes. Surprisingly, total flight efficiency in fruit flies is broadly independent of different profile power estimates and typically yields mean values between 2–4%.     

Male load-lifting capacity and mating success in the swarming caddis fly Athripsodes cinereus

Abstract. Males of the caddis fly Athripsodes cinereus (Curtis) (Trichoptera: Leptoceridae) swarm above the water surface of lakes and streams. Females enter swarms and are pursued until grasped by a male. The pair couple their genitalia in the air, and then the male alone flies the pair to the shore where they settle and complete the copulation. About 8% of the pairs (total n = 384 pairs) dipped in the water soon after the coupling manoeuvre and about 25% of those then separated. Males in dipping pairs ( n = 13) were on average smaller and relatively older than the males that successfully carried their mate to the shore ( n = 54). No differences were found for flight muscle ratio (weight of flight muscles/total body weight) or relative load (total load/flight muscle weight). Males were larger than females (wing length), though typically female Trichoptera are the larger sex. Large male body size in A. cinereus may be an adaptation for flight during pairing; i.e. larger males are more likely to be able to carry larger loads.     

Development of fast singing muscles in a katydid

In males of the katydid Neoconocephalus robustus, mesothoracic wings are used in flight (wing stroke frequence = 20 Hz) and stridulation (200 Hz), while the metathoracic wings are used in flight alone. Most mesothoracic wing muscles produce much briefer isometric twitches than metathoracic counterparts. The mesothoracic first tergocoxal muscle (TCX1) has a twitch duration (onset to 50% relaxation, 35 degrees C) of 6-8 ms and the metathoracic TXC1 a twitch duration of 12-15 ms. The TCX1 muscles from animals one and two instars from adulthood produce twitches similar in duration to those of the adult metathoracic TCX1. The twitch duration of the mesothoracic TCX1 acquires its adult brevity gradually over the first 5 days of adult life. Both TCX1 muscles increase greatly in size and mitochondrial content around the time of the terminal molt. During this period the mesothoracic TCX1 develops narrower myofibrils and a smaller ratio of fibril volume to sarcoplasmic reticulum volume than is characteristic of the metathoracic TCX1. Changes in the ultrastructure of the mesothoracic TCX1 precede changes in contraction kinetics around the time of the terminal molt so that there is not a strict correlation between muscle structure and performance during the period of rapid growth.     

Hindlimb Motion during Steady Flight of the Lesser Dog-Faced Fruit Bat,Cynopterus brachyotis

In bats, the wing membrane is anchored not only to the body and forelimb, but also to the hindlimb. This attachment configuration gives bats the potential to modulate wing shape by moving the hindlimb, such as by joint movement at the hip or knee. Such movements could modulate lift, drag, or the pitching moment. In this study we address: 1) how the ankle translates through space during the wingbeat cycle; 2) whether amplitude of ankle motion is dependent upon flight speed; 3) how tension in the wing membrane pulls the ankle; and 4) whether wing membrane tension is responsible for driving ankle motion. We flew five individuals of the lesser dog-faced fruit bat, Cynopterus brachyotis (Family: Pteropodidae), in a wind tunnel and documented kinematics of the forelimb, hip, ankle, and trailing edge of the wing membrane. Based on kinematic analysis of hindlimb and forelimb movements, we found that: 1) during downstroke, the ankle moved ventrally and during upstroke the ankle moved dorsally; 2) there was considerable variation in amplitude of ankle motion, but amplitude did not correlate significantly with flight speed; 3) during downstroke, tension generated by the wing membrane acted to pull the ankle dorsally, and during upstroke, the wing membrane pulled laterally when taut and dorsally when relatively slack; and 4) wing membrane tension generally opposed dorsoventral ankle motion. We conclude that during forward flight in C. brachyotis, wing membrane tension does not power hindlimb motion; instead, we propose that hindlimb movements arise from muscle activity and/or inertial effects.     

Physiological trade‐offs between flight muscle and reproductive development in the wing‐dimorphic cricket Velarifictorus ornatus

Morphology, flight muscles, and reproductive development were compared between long‐winged (LW) and short‐winged (SW) morphs of the cricket Velarifictorus ornatus (Shiraki) (Orthoptera: Gryllidae). There was no difference in body weight and pre‐oviposition between the two morphs, but LW individuals had better‐developed flight muscles than SW individuals during and after emergence of the adult. The flight muscles at adult emergence represented 11.9% of the total body weight in the LW female and 4.9% in the SW female. In addition, the weight of the flight muscle of LW females increased by 50% during the first 5 days, whereas the flight muscle of the SW variant increased only slightly after adult emergence. The process of oviposition in LW, SW, and de‐alated females varied: SW females produced more eggs at the early stage than LW females, but de‐alation could shorten the time until the peak of egg laying and caused histolysis of flight muscles of LW females. There was no significant difference in total egg production between the above three groups. In the male, unlike the female, the accessory glands of the two wing morphs enlarged continuously at the same rate. There was no difference between the two wing morphs in the mass of the testes during the first 7 days after adult emergence.     

Genetic Variability of Flight Metabolism in DROSOPHILA MELANOGASTER. I. Characterization of Power Output during Tethered Flight

The mechanical power imparted to the wings during tethered flight of Drosophila melanogaster is estimated from wing-beat frequency, wing-stroke amplitude and various aspects of wing morphology by applying the steady-state aerodynamics model of insect flight developed by Weis-Fogh (1972, 1973). Wing-beat frequency, the major determinant of power output, is highly correlated with the rate of oxygen consumption. Estimates of power generated during flight should closely reflect rates of ATP production in the flight muscles, since flies do not acquire an oxygen debt or accumulate ATP during flight. In an experiment using 21 chromosome 2 substitution lines, lines were a significant source of variation for all flight parameters measured. Broadsense heritabilities ranged from 0.16 for wing-stroke amplitude to 0.44 for inertial power. The variation among lines is not explained by variation in total body size (i.e., live weight). Line differences in flight parameters are robust with respect to age, ambient temperature and duration of flight. These results indicate that characterization of the power output during tethered flight will provide a sensitive experimental system for detecting the physiological effects of variation in the structure or quantity of the enzymes involved in flight metabolism.     

Morphological variation associated with dispersal capacity in a tree‐killing bark beetle Dendroctonus ponderosae Hopkins

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Changing motor patterns of the 3rd axillary muscle activities associated with longitudinal control in freely flying hawkmoths

The 3rd axillary muscles (3AXMs) in the mesothorax in hawkmoths are direct flight muscles and pull forewings back along to the body axis. The 3AXMs are regarded as steering muscles because of their changeable activities during turning flight under tethered conditions. We investigated activities of the upper unit of the 3AXMs during free flight with a micro-telemetry device and captured body and wing movements by high-speed cameras. The 3AXM was activated with 1 to 3 spikes per each wingbeat cycle but sometimes ceased to fire. The phase of the onset of the activities was, even though it was variable, close to the phase of the elevator muscle activities. Therefore the upper unit of the 3AXM activities would affect upstroke properties phasically including wing retractions. We focused on longitudinal flight control and identified a correlation between the phase of the 3AXM and body pitch angle, which is important kinematical parameter for longitudinal control in insect flight. The phasic changes of the 3AXM activities would support quick changes in longitudinal control.     

Relationship between body size and flying-related structures in Neotropical social wasps (Polistinae,Vespidae, Hymenoptera)

Body size influences wing shape and associated muscles in flying animals which is a conspicuous phenomenon in insects, given their wide range in body size. Despite the significance of this, to date, no detailed study has been conducted across a group of species with similar biology allowing a look at specific relationship between body size and flying structures. Neotropical social vespids are a model group to study this problem as they are strong predators that rely heavily on flight while exhibiting a wide range in body size. In this paper we describe the variation in both wing shape, as wing planform, and mesosoma muscle size along the body size gradient of the Neotropical social wasps and discuss the potential factors affecting these changes. Analyses of 56 species were conducted using geometric morphometrics for the wings and lineal morphometrics for the body; independent contrast method regressions were used to correct for the phylogenetic effect. Smaller vespid species exhibit rounded wings, veins that are more concentrated in the proximal region, larger stigmata and the mesosoma is proportionally larger than in larger species. Meanwhile, larger species have more elongated wings, more distally extended venation, smaller stigmata and a proportionally smaller mesosoma. The differences in wing shape and other traits could be related to differences in flight demands caused by smaller and larger body sizes. Species around the extremes of body size distribution may invest more in flight muscle mass than species of intermediate sizes.     

Temporary flightlessness in pre‐laying Common Eiders Somateria mollissima: are females constrained by excessive wing‐loading or by minimal flight muscle ratio?

Large body size, small wings and relatively low flight muscle mass are general attributes of flightlessness in birds, but a general analysis is lacking when considering these factors simultaneously. Common Eiders Somateria mollissima are large sea ducks characterized by short, pointed wings of low surface area. Because females fast throughout incubation, they need to accumulate large body reserves prior to laying. During this pre‐laying period, many females cannot take off, and dive when approached under still‐air conditions, whereas males take off readily when disturbed. In this paper, we examine how pre‐laying female Common Eiders fit the maximum wing‐loading ratio of Meunier, the marginal flight muscle ratio (FMR) of Marden and predictions of a general model of take‐off performance (also by Marden). Wing morphology was recorded and flight muscles were dissected from specimens collected during the pre‐laying period near one breeding colony. In addition, take‐off ability, as observed during collection, was compared with the proposed thresholds for flightlessness and outputs from the general model of take‐off performance. The results indicated that half of the pre‐laying females exceeded the wing‐loading ratio of Meunier, although all females had values above 0.160, the flight muscle ratio below which take‐off would be impossible. We suggest that wing‐loading and flight muscle ratio interact in Eiders, with higher FMR compensating for excessive wing‐loading. Nevertheless, the model of take‐off performance predicted, with reasonable accuracy, the behavioural observations under still‐air conditions. Indeed, females that were predicted to be temporarily flightless could produce a specific lift of 8.8 N/kg on average (less than the 9.8 N/kg required to overcome gravity). In contrast, the average specific lift predicted for males capable of flight was estimated to be 11.4 N/kg. These results agree with our observations that female Common Eiders are at the limit of flight capability in vertebrates.     

Morphology, Velocity, and Intermittent Flight in Birds

Body size, pectoralis composition, aspect ratio of the wing,and forward speed affect the use of intermittent flight in birds.During intermittent non-flapping phases, birds extend theirwings and glide or flex their wings and bound. The pectoralismuscle is active during glides but not during bounds; activityin other primary flight muscles is variable. Mechanical power,altitude, and velocity vary among wingbeats in flapping phases;associated with this variation are changes in neuromuscularrecruitment, wingbeat frequency, amplitude, and gait. Speciesof intermediate body mass (35–158 g) tend to flap-glideat slower speeds and flap-bound at faster speeds, regardlessof the aspect ratio of their wings. Such behavior may reducemechanical power output relative to continuous flapping. Smallerspecies (<20 g) with wings of low aspect ratio may flap-boundat all speeds, yet existing models do not predict an aerodynamicadvantage for the flight style at slow speeds. The behaviorof these species appears to be due to wing shape rather thanpectoralis physiology. As body size increases among species,percent time spent flapping increases, and birds much largerthan 300 g do not flap-bound. This pattern may be explainedby adverse scaling of mass-specific power or lift per unit poweroutput available from flight muscles. The size limit for theability to bound intermittently may be offset somewhat by thescaling of pectoralis composition. The percentage of time spentflapping during intermittent flight also varies according toflight speed.     

The physiology and biomechanics of avian flight at high altitude

Many birds fly at high altitude, either during long-distanceflights or by virtue of residence in high-elevation habitats.Among the many environmental features that vary systematicallywith altitude, five have significant consequences for avianflight performance: ambient wind speeds, air temperature, humidity,oxygen availability, and air density. During migratory flights,birds select flight altitudes that minimize energy expenditurevia selection of advantageous tail- and cross-winds. Oxygenpartial pressure decreases substantially to as little as 26%of sea-level values for the highest altitudes at which birdsmigrate, whereas many taxa reside above 3000 meters in hypoxicair. Birds exhibit numerous adaptations in pulmonary, cardiovascular,and muscular systems to alleviate such hypoxia. The systematicdecrease in air density with altitude can lead to a benefitfor forward flight through reduced drag but imposes an increasedaerodynamic demand for hovering by degrading lift productionand simultaneously elevating the induced power requirementsof flight. This effect has been well-studied in the hoveringflight of hummingbirds, which occur throughout high-elevationhabitats in the western hemisphere. Phylogenetically controlledstudies have shown that hummingbirds compensate morphologicallyfor such hypodense air through relative increases in wing size,and kinematically via increased stroke amplitude during thewingbeat. Such compensatory mechanisms result in fairly constantpower requirements for hovering at different elevations, butdecrease the margin of excess power available for other flightbehaviors.     

Aerodynamic corrections for the flight of birds and bats in wind tunnels

Few wind tunnel studies of animal flight have controlled or corrected for distortions to behaviour, physiology or flight aerodynamics representing the difference between flight in the tunnel and flight in free air. Aerodynamic correction factors are derived based on lifting-line theory and the method of images for an animal flying freely within closed- and open-section wind tunnels; the method is very similar to that used to model flight in ground effect, and as in ground effect the corrections to induced drag may be substantial. These correction factors are used to estimate bound wing circulation, drag and mechanical power for comparison with free flight, and to derive testable predictions of optimum flight strategies for an animal in a tunnel. In an open-section tunnel, mechanical power is increased compared to free flight, and the animal should fly at the tunnel centre. In a closed tunnel mechanical power is usually reduced, and substantial savings are available, particularly at low speeds, if the animal flies close to the tunnel roof. Anecdotal observations confirm that birds and bats adopt this strategy. The mechanical power-speed curve in a closed tunnel is flatter than the curve for free flight, and this may explain the flat metabolic power-speed curves for birds and bats obtained in some measurements.     

How Insect Flight Steering Muscles Work

Insights into how exactly a fly powers and controls flight have been hindered by the need to unpick the dynamic complexity of the muscles involved. The wingbeats of insects are driven by two antagonistic groups of power muscles and the force is funneled to the wing via a very complex hinge mechanism. The hinge consists of several hardened and articulated cuticle elements called sclerites. This articulation is controlled by a great number of small steering muscles, whose function has been studied by means of kinematics and muscle activity. The details and partly novel function of some of these steering muscles and their tendons have now been revealed in research published in this issue of PLOS Biology. The new study from Graham Taylor and colleagues applies time-resolved X-ray microtomography to obtain a three-dimensional view of the blowfly wingbeat. Asymmetric power output is achieved by differential wingbeat amplitude on the left and right wing, which is mediated by muscular control of the hinge elements to mechanically block the wing stroke and by absorption of work by steering muscles on one of the sides. This new approach permits visualization of the motion of the thorax, wing muscles, and the hinge mechanism. This very promising line of work will help to reveal the complete picture of the flight motor of a fly. It also holds great potential for novel bio-inspired designs of fly-like micro air vehicles.The ability for powered flight has evolved four times in the animal kingdom and, thanks to their ability to fly, insects have diversified and moved into new regions and habitats with enormous success [1]. Powered flight requires an integrated system consisting of wings to generate aerodynamic force, muscles to move the wings, and a control system to modulate power output from the muscles. Insects are bewilderingly diverse with respect to flight morphology and behaviors, which in turn provides a real challenge to researchers wishing to understand how insects fly. In particular, the impressive flight maneuvers in flies, such as blowflies and fruit flies, have inspired scientists for many years [2]. The ability of a fly to accelerate, make tight turns, rolls, and loops that allow the creature to land upside down on a ceiling is unparalleled in any other organisms, as well as any manmade aircraft. Everybody knows how difficult it is to swat a fly with bare hands—the fly''s capacity for rapid take-off and accurate movement away from a perceived approaching threat is exquisite [3].The flight muscles of many insects, including flies, bees, and mosquitoes, are divided into a few large power muscles that simply contract cyclically to generate sheer power output and a greater number of smaller steering muscles that control the force transmission from the power muscles to the wing [4]–[6]. The power muscles of a fly consist of two sets of antagonistic muscles attached to the inside of the thorax (exoskeleton) (Figure 1). In many insects, including flies, these muscles are asynchronous, which means their contractions are uncoupled to the firing rate of the associated motor neuron [6],[7], i.e., the muscles continue to contract as long as the nerve tickles them. Another characteristic feature of the power muscles is that they are stretch-activated and contract as a response to being lengthened. Both sets of power muscles deform the thorax when contracted such that when the dorso-ventral muscles contract, the thorax is squeezed together dorso-ventrally while expanding longitudinally, and vice versa when the dorsal-longitudinal muscles contract as a response to prior lengthening. The result is an alternate contraction and lengthening of these perpendicular muscle groups and a resonance of the entire thorax that drives the wingbeat. Typical wingbeat frequencies are in the range from 100 Hz and even up to 1,000 Hz in the smallest species [5],[8].Open in a separate windowFigure 1The thorax with and dorsal longitudinal (upper left) and dorso-ventral (upper right) power flight muscles of a fly.The cartoon (bottom) shows a transverse section through the thorax with dorso-ventral muscles (DVM) and dorsal longitudinal muscles (DLM) indicated. The two upper illustrations are redrawn from [6].The forces from the flight muscles are transmitted to the wing through an intricate hinge mechanism (Figure 2). The hardened plates of cuticle between the thorax and wing (sclerites) are mobile and their positions relative to the thoracic outgrowths and wing determine the extent of the wing motion, i.e., the angular amplitude of the wingbeat [6].Open in a separate windowFigure 2Cartoon illustration of a transverse section of the thorax of a fly in rear view, showing some elements of the complex wing hinge of a fly, consisting of ridges and protrusions on the thorax and a number of hardened plates of cuticle (sclerites) between the body (thorax) and the wing root.The basalare sclerite (not shown) is positioned anterior of the first axillary sclerite (Ax1). The indicated structures are dorso-ventral power muscle (DVM), pleural wing process (PWP), post-medial notal process (PMNP), parascutal shelf (PSS), axial wing sclerites (Ax1, Ax2, Ax3), and radial stop (RS). Redrawn and modified from [18].Flight maneuvers arise owing to asymmetric force generation between the left and right wing. Aerodynamic force is proportional to the angle of attack (the angle between the wing surface and the airflow) and the speed squared relative to the air [9],[10]. Except from the turning points of each half-stroke, when the wings rotate about their span wise axes, the angle of attack is usually quite constant during the translational phases of the wingbeat [10], while asymmetric forces are mainly created by changing the wingbeat amplitude in flies [11]–[14]. With wingbeat frequency kept constant, changed amplitude changes the speed and hence force generated.The control of the elements forming the hinge mechanism of the wing is achieved by the steering muscles, which are tiny in terms of mass (<3% of the power muscle mass), but mean everything when it comes to making flight maneuvers. In contrast to the power muscles the steering muscles are synchronous, i.e., there is a 1∶1 correspondence between neural spikes and muscle contraction. No less than some 22 pairs of steering muscles are involved in the force transmission; a few of these indirectly modulate the output by affecting the resonating properties of the thorax, while others are directly attached to the sclerite elements of the hinge mechanism [6],[15]. Three small muscles (b1–b3) are attached to the basalare plate that is directly involved in wing articulation (Figure 3). The actual wing sclerites (Figure 2) are also controlled by specific steering muscles, also with the function of moving the sclerites in relation to required wing motion. The main control function of the hinge mechanism appears to be of the downward movement of the wing, i.e., the angle at the turning point at end of downstroke. For a detailed review about the steering muscles and their function see Dickinson and Tu [6].Open in a separate windowFigure 3The position of the three steering flight muscles b1–b3 inserted to the nail-shaped basalare sclerite.Contraction by the b1 and b2 muscles move the basalare forward and their antagonist b3 moves it backwards when contracted. Redrawn from [6].To date, the function of the steering muscles has been revealed mainly by electrophysiological studies on tethered subjects. Tethering means that the animal is glued to the end of a thin rod, often with force sensors attached to it, and then stimulated to “fly.” In many insects this can be achieved by simply blowing at them or placing them in a wind tunnel. On the tether the insect can either be presented with a visual stimulus or be rotated, which flies can sense via their halteres (hind wings modified to sensory gyroscopic sensory organs) [16]. By inserting electrode wires into the steering muscles, the neural impulses are measured at the same time as the wingbeat kinematics is recorded [13],[17]. What we know about the function of the steering muscles comes from the meticulous studies of correlations between muscle activity and the associated wing movement, including how the hinge mechanism works [6],[18]. Needless to say, such experiments are extremely difficult to achieve in small insects like blowflies and fruit flies that flap their wings at high frequencies. Recent studies of the wing and hinge kinematics provide some support for the hypothesis that the hinge may have a gear function that affects stroke amplitude, as well [18]. However, there are still many open questions regarding the exact function of the steering muscles and how they help in generating laterally asymmetric forces during a fly''s flight maneuver [6].In an article published in this issue of PLOS Biology, Walker and colleagues take a new approach for studying how steering muscles regulate the power output from power muscles [19], using time-resolved x-ray microtomography [20]. By rotating tethered blowflies (Calliphora vicina) in the X-ray beam, a 3D-movie was captured that shows how the steering muscles move. This by itself is a grand achievement at a wingbeat frequency of 145 Hz. As the flies could sense being rotated the steering muscles acted accordingly to achieve an asymmetric power output as a response to a perceived turn. The movies that accompany the article show how several of the key steering muscles and their sclerites operate in concert during the course of a wingbeat, and the visual results are supported by advanced statistical analyses of muscle strain rates and their phase offset. For example, the b1 and b3 muscles (Figure 3) work antagonistically, as was known before, but on the low-amplitude wing the oscillations are delayed by about a quarter of a wingbeat. The strain amplitudes of b1 and b3 were different between the two wings, which were found to be due to dorso-ventral movement of the basalare sclerite on the high-amplitude side and rotation on the low-amplitude side. This shows even higher complexity of the wing hinge than was previously envisaged.The measurements of strain rate in the muscle confirmed the results of a previous study, which showed that asymmetric power output is partially achieved by negative work [21], i.e., absorption of work, by the b1 muscle on the low-amplitude wing. As with other muscles, the steering muscles insert on the skeletal parts and sclerites by tendons. The tendon of the muscle (I1) associated with the first axillary sclerite was observed to buckle when the wing was elevated above the wing hinge, indicative of compressive force acting on it near the top of the wing stroke. This buckling of the tendon forces a reinterpretation of the function of this muscle: it is involved in reducing stroke amplitude at the bottom of the downstroke rather than exerting stress near the opposite end of the stroke. Tendon buckling was seen in some other muscles as well, and although this is its first observation, it may be a more general mechanism involved in control of insect wingbeat kinematics.What are the wider implications of this new study? First, it demonstrates the utility of a new approach to examine the in vivo operation of several insect flight muscles. This alone signals a methodological breakthrough that promises more. So far the flies were tethered and studied during one behavioral treatment (rotation about the yaw axis). Real flight maneuvers, however, also involve angular rotation about pitch and roll axes, acceleration, and braking. Thus, it remains to be seen how the steering muscles operate to control more subtle changes in wing kinematics during the turning saccades and advanced flight maneuvers that take place during free flight. The method involved exposure to lethal X-ray doses, which of course limits how long the experiments can be. Second, tethering is the prevailing paradigm for studying insect flight, but because it interrupts the sensory feedback loop [22], it would be useful for future studies to compare tethered and free flight in some commonly studied species. Furthermore, a more complete understanding of the flight muscle-hinge mechanism may help bio-inspired design of wing articulation systems for fly-like micro air vehicles. Until then, we can enjoy the stunning videos of the oscillating thorax and flight muscle system of the blowfly [19]. See the video from the related research article here (http://youtu.be/P6lBkK3J9wg) or [19].