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.     

EVOLUTION AND CLASSIFICATION OF INSECT FLIGHT KINEMATICS

Classification of the main types of insect in-flight kinematics is proposed here, based on comparative data of wing movement during flapping flight. By comparing the described kinematic patterns with the results of studies of the vortex-wake structures of flying insects, these patterns can be explained as adaptations for overcoming the negative effects of mutual deceleration of fore- and hind wing starting vortex bubbles, which take place in insects with the most primitive type of wing kinematics. The aerodynamic efficiency of the flying system can be decreased if natural selection favors behavioral patterns that involve suboptimal wing kinematics.     

Kinematic compensation for wing loss in flying damselflies

Flying insects can tolerate substantial wing wear before their ability to fly is entirely compromised. In order to keep flying with damaged wings, the entire flight apparatus needs to adjust its action to compensate for the reduced aerodynamic force and to balance the asymmetries in area and shape of the damaged wings. While several studies have shown that damaged wings change their flapping kinematics in response to partial loss of wing area, it is unclear how, in insects with four separate wings, the remaining three wings compensate for the loss of a fourth wing. We used high-speed video of flying blue-tailed damselflies (Ischnura elegans) to identify the wingbeat kinematics of the two wing pairs and compared it to the flapping kinematics after one of the hindwings was artificially removed. The insects remained capable of flying and precise maneuvering using only three wings. To compensate for the reduction in lift, they increased flapping frequency by 18 ± 15.4% on average. To achieve steady straight flight, the remaining intact hindwing reduced its flapping amplitude while the forewings changed their stroke plane angle so that the forewing of the manipulated side flapped at a shallower stroke plane angle. In addition, the angular position of the stroke reversal points became asymmetrical. When the wingbeat amplitude and frequency of the three wings were used as input in a simple aerodynamic model, the estimation of total aerodynamic force was not significantly different (paired t-test, p = 0.73) from the force produced by the four wings during normal flight. Thus, the removal of one wing resulted in adjustments of the motions of the remaining three wings, exemplifying the precision and plasticity of coordination between the operational wings. Such coordination is vital for precise maneuvering during normal flight but it also provides the means to maintain flight when some of the wings are severely damaged.     

昆虫平衡棒的发育及功能

平衡棒(haltere)是双翅目昆虫后翅特化而成的结构,可在飞行中起重要作用。平衡棒基部的感受器可以检测到飞行中的惯性力,向运动神经元提供反馈,迅速地平衡身体并纠正航向。昆虫的平衡棒由成虫盘发育形成,其特化受HOX基因(Ultrabithorax,Ubx)调控。发育成熟的平衡棒由两层上皮细胞组成,末端球状结构内部充满高度空泡化的细胞,基部具有大量感器。平衡棒的运动由独立的肌肉控制,相对于同侧的翅反向移动,翅与平衡棒的协同运动对于昆虫起飞和维持平衡十分重要。近年来,平衡棒的导航原理越来越多地应用于仿生学研究中,基于果蝇平衡棒的结构和功能,研制出多种飞行器的导航设备。本文结合近年来相关领域的研究成果,就平衡棒的发育、形态结构、功能和仿生应用等方面的研究进展进行综述,为深入理解昆虫平衡棒的发育机制和生物学功能提供参考。     

Falling with Style: Bats Perform Complex Aerial Rotations by Adjusting Wing Inertia

The remarkable maneuverability of flying animals results from precise movements of their highly specialized wings. Bats have evolved an impressive capacity to control their flight, in large part due to their ability to modulate wing shape, area, and angle of attack through many independently controlled joints. Bat wings, however, also contain many bones and relatively large muscles, and thus the ratio of bats’ wing mass to their body mass is larger than it is for all other extant flyers. Although the inertia in bat wings would typically be associated with decreased aerial maneuverability, we show that bat maneuvers challenge this notion. We use a model-based tracking algorithm to measure the wing and body kinematics of bats performing complex aerial rotations. Using a minimal model of a bat with only six degrees of kinematic freedom, we show that bats can perform body rolls by selectively retracting one wing during the flapping cycle. We also show that this maneuver does not rely on aerodynamic forces, and furthermore that a fruit fly, with nearly massless wings, would not exhibit this effect. Similar results are shown for a pitching maneuver. Finally, we combine high-resolution kinematics of wing and body movements during landing and falling maneuvers with a 52-degree-of-freedom dynamical model of a bat to show that modulation of wing inertia plays the dominant role in reorienting the bat during landing and falling maneuvers, with minimal contribution from aerodynamic forces. Bats can, therefore, use their wings as multifunctional organs, capable of sophisticated aerodynamic and inertial dynamics not previously observed in other flying animals. This may also have implications for the control of aerial robotic vehicles.     

A new genus of long-legged flies displaying remarkable wing directional asymmetry

A previously unknown group of flies is described whose males exhibit directional asymmetry, in that the left wing is larger than, and of a different shape from, the right wing. To our knowledge, wing asymmetry of this degree has not previously been reported in an animal capable of flight. Such consistent asymmetry must result from a left-right axis during development, a level of differentiation whose existence has been questioned for insects. Wing asymmetry of this magnitude has implications for questions in areas of development, natural selection, flight, mate selection and communication in insects. The 'handicap principle' provides a possible explanation: females will choose a mate with the greatest handicap because his survival, in spite of his handicap, is a measure of his genetic superiority.     

Centripetal Acceleration Reaction: An Effective and Robust Mechanism for Flapping Flight in Insects

Despite intense study by physicists and biologists, we do not fully understand the unsteady aerodynamics that relate insect wing morphology and kinematics to lift generation. Here, we formulate a force partitioning method (FPM) and implement it within a computational fluid dynamic model to provide an unambiguous and physically insightful division of aerodynamic force into components associated with wing kinematics, vorticity, and viscosity. Application of the FPM to hawkmoth and fruit fly flight shows that the leading-edge vortex is the dominant mechanism for lift generation for both these insects and contributes between 72–85% of the net lift. However, there is another, previously unidentified mechanism, the centripetal acceleration reaction, which generates up to 17% of the net lift. The centripetal acceleration reaction is similar to the classical inviscid added-mass in that it depends only on the kinematics (i.e. accelerations) of the body, but is different in that it requires the satisfaction of the no-slip condition, and a combination of tangential motion and rotation of the wing surface. Furthermore, the classical added-mass force is identically zero for cyclic motion but this is not true of the centripetal acceleration reaction. Furthermore, unlike the lift due to vorticity, centripetal acceleration reaction lift is insensitive to Reynolds number and to environmental flow perturbations, making it an important contributor to insect flight stability and miniaturization. This force mechanism also has broad implications for flow-induced deformation and vibration, underwater locomotion and flows involving bubbles and droplets.     

Time-Varying Wing-Twist Improves Aerodynamic Efficiency of Forward Flight in Butterflies

Insect wings can undergo significant chordwise (camber) as well as spanwise (twist) deformation during flapping flight but the effect of these deformations is not well understood. The shape and size of butterfly wings leads to particularly large wing deformations, making them an ideal test case for investigation of these effects. Here we use computational models derived from experiments on free-flying butterflies to understand the effect of time-varying twist and camber on the aerodynamic performance of these insects. High-speed videogrammetry is used to capture the wing kinematics, including deformation, of a Painted Lady butterfly (Vanessa cardui) in untethered, forward flight. These experimental results are then analyzed computationally using a high-fidelity, three-dimensional, unsteady Navier-Stokes flow solver. For comparison to this case, a set of non-deforming, flat-plate wing (FPW) models of wing motion are synthesized and subjected to the same analysis along with a wing model that matches the time-varying wing-twist observed for the butterfly, but has no deformation in camber. The simulations show that the observed butterfly wing (OBW) outperforms all the flat-plate wings in terms of usable force production as well as the ratio of lift to power by at least 29% and 46%, respectively. This increase in efficiency of lift production is at least three-fold greater than reported for other insects. Interestingly, we also find that the twist-only-wing (TOW) model recovers much of the performance of the OBW, demonstrating that wing-twist, and not camber is key to forward flight in these insects. The implications of this on the design of flapping wing micro-aerial vehicles are discussed.     

Aerodynamics of a bio-inspired flexible flapping-wing micro air vehicle

MAVs (micro air vehicles) with a maximal dimension of 15 cm and nominal flight speeds of around 10 m s?1, operate in a Reynolds number regime of 10? or lower, in which most natural flyers including insects, bats and birds fly. Furthermore, due to their light weight and low flight speed, the MAVs' flight characteristics are substantially affected by environmental factors such as wind gust. Like natural flyers, the wing structures of MAVs are often flexible and tend to deform during flight. Consequently, the aero/fluid and structural dynamics of these flyers are closely linked to each other, making the entire flight vehicle difficult to analyze. We have recently developed a hummingbird-inspired, flapping flexible wing MAV with a weight of 2.4-3.0 g and a wingspan of 10-12 cm. In this study, we carry out an integrated study of the flexible wing aerodynamics of this flapping MAV by combining an in-house computational fluid dynamic (CFD) method and wind tunnel experiments. A CFD model that has a realistic wing planform and can mimic realistic flexible wing kinematics is established, which provides a quantitative prediction of unsteady aerodynamics of the four-winged MAV in terms of vortex and wake structures and their relationship with aerodynamic force generation. Wind tunnel experiments further confirm the effectiveness of the clap and fling mechanism employed in this bio-inspired MAV as well as the importance of the wing flexibility in designing small flapping-wing MAVs.     

Positive Relationship between Signalling Time and Flight Capability in the Texas Field Cricket, Gryllus texensis

A trade‐off between dispersal ability and reproduction is generally thought to explain the persistence of wing dimorphism in insects, although this trade‐off has received minimal attention in male insects. Research on male sand cricket, Gryllus firmus, supports the trade‐off hypothesis insofar as flight capable cricket’s spend significantly less time signalling for potential mates than their flightless counterparts. By contrast, here I show that this expected trade‐off between signalling time and wing dimorphism does not exist in a male congener, the Texas field cricket (Gryllus texensis). In G. texensis, flight capable males signal twice as often as flightless males. Thus, unless male G. texensis express trade‐offs between dispersal ability and other, presently unmeasured components of reproduction, the trade‐off hypothesis may not explain the persistence of wing dimorphism in all male insects.     

Structural dynamics and aerodynamics measurements of biologically inspired flexible flapping wings

Flapping wing flight as seen in hummingbirds and insects poses an interesting unsteady aerodynamic problem: coupling of wing kinematics, structural dynamics and aerodynamics. There have been numerous studies on the kinematics and aerodynamics in both experimental and computational cases with both natural and artificial wings. These studies tend to ignore wing flexibility; however, observation in nature affirms that passive wing deformation is predominant and may be crucial to the aerodynamic performance. This paper presents a multidisciplinary experimental endeavor in correlating a flapping micro air vehicle wing's aeroelasticity and thrust production, by quantifying and comparing overall thrust, structural deformation and airflow of six pairs of hummingbird-shaped membrane wings of different properties. The results show that for a specific spatial distribution of flexibility, there is an effective frequency range in thrust production. The wing deformation at the thrust-productive frequencies indicates the importance of flexibility: both bending and twisting motion can interact with aerodynamic loads to enhance wing performance under certain conditions, such as the deformation phase and amplitude. By measuring structural deformations under the same aerodynamic conditions, beneficial effects of passive wing deformation can be observed from the visualized airflow and averaged thrust. The measurements and their presentation enable observation and understanding of the required structural properties for a thrust effective flapping wing. The intended passive responses of the different wings follow a particular pattern in correlation to their aerodynamic performance. Consequently, both the experimental technique and data analysis method can lead to further studies to determine the design principles for micro air vehicle flapping wings.     

Biomechanics and physiology of gait selection in flying birds

Two wing-beat gaits, distinguished by the presence or absence of lift production during the upstroke, are currently used to describe avian flight. Vortex-visualization studies indicate that lift is produced only during the downstroke in the vortex-ring gait and that lift is produced continuously in the continuous-vortex gait. Tip-reversal and feathered upstrokes represent different forms of vortex-ring gait distinguished by wing kinematics. Useful aerodynamic forces may be produced during tip-reversal upstroke in slow flight and during a feathered upstroke in fast flight, but it is probable that downstroke forces are much greater in magnitude. Uncertainty about the function of these types of upstroke may be resolved when more data are available on wake structure in different flight speeds and modes. Inferring from wing kinematics and available data on wake structure, birds with long wings or wings of high aspect ratio use a vortex-ring gait with tip-reversal upstroke at slow speeds, a vortex-ring gait with a feathered upstroke at intermediate speeds, and a continuous-vortex gait at fast speeds. Birds with short wings or wings of low aspect ratio use a vortex-ring gait with a feathered upstroke at all speeds. Regardless of wing shape, species tend to use a vortex-ring gait for acceleration and a continuous-vortex gait for deceleration. Some correlations may exist between gait selection and the function of the muscular and respiratory system. However, overall variation in wing kinematics, muscle activity, and respiratory activity is continuous rather than categorical. To further our understanding of gait selection in flying birds, it is important to test whether upstroke function varies in a similar manner. Transitions between lifting and nonlifting upstrokes may be more subtle and gradual than implied by a binomial scheme of classification.     

Biomechanics and biomimetics in insect-inspired flight systems

Insect- and bird-size drones—micro air vehicles (MAV) that can perform autonomous flight in natural and man-made environments are now an active and well-integrated research area. MAVs normally operate at a low speed in a Reynolds number regime of 10⁴–10⁵ or lower, in which most flying animals of insects, birds and bats fly, and encounter unconventional challenges in generating sufficient aerodynamic forces to stay airborne and in controlling flight autonomy to achieve complex manoeuvres. Flying insects that power and control flight by flapping wings are capable of sophisticated aerodynamic force production and precise, agile manoeuvring, through 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. In this article, we give a selective review on the state of the art of biomechanics in bioinspired flight systems in terms of flapping and flexible wing aerodynamics, flight dynamics and stability, passive and active mechanisms in stabilization and control, as well as flapping flight in unsteady environments. We further highlight recent advances in biomimetics of flapping-wing MAVs with a specific focus on insect-inspired wing design and fabrication, as well as sensing systems.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

Avian brachial index and wing kinematics: putting movement back into bones

The relationship between wing kinematics, wing morphology and the brachial index of birds (BI=humerus length/ulna length) was examined. BI was found to differ between three groups of birds, which were classified on the basis of similar wing kinematics. In addition, a comparative analysis of a large dataset, using phylogenetically independent contrasts, suggested a significant, albeit weak, correlation between BI and four measures of wing morphology (wing loading, wing area, wing length and aspect ratio). Although wing kinematics and wing morphology are both correlated with BI in birds, the dominant selective pressure upon this ratio is probably wing kinematics. The previously identified clade specificity of BI within Neornithes is most likely because birds with similar BIs fly with kinematic similarity and closely related birds have similar flight styles. A correlation between BI and wing kinematics means that it may be possible to characterize the wing beat of fossil birds. A more robust relationship between wing morphology and BI may emerge, but only after the relationship between wing kinematics and BI is quantified. A comparative and quantitative study of wing-bone anatomy and wing kinematics is a priority for future studies of avian wing-skeleton evolution and functional morphology.     

Habitat-specific sensory-exploitative signals in birds: propensity of dipteran prey to cause evolution of plumage variation in flush-pursuit insectivores

Sensory exploitation occurs when signals trigger behavioral reactions that diminish the receiver's fitness. Research in this area focuses on the match between the signal's form and the receiver's sensitivity, but the effect of habitat on interspecific sensory exploitation is rarely addressed. Myioborus redstarts use conspicuous wing and tail displays of contrasting black-and-white plumage patches to flush dipteran insects, which are then pursued and captured in flight. Previous studies have shown that by increasing the distance at which insects perform an escape response, conspicuous visual displays improve the birds' foraging performance. We tested the hypothesis that selection for a visual signal that maximizes prey escape distance under local habitat conditions can lead to the evolution of geographic variation in plumage pattern among Myioborus redstarts. Using models of foraging birds, we recorded the escape responses of Dipterous insects to a range of plumage patterns and background tones (from light to dark) to determine whether the plumage pattern that maximizes prey flushing is dependent upon that habitat (background) against which birds are viewed by their prey. Our results indicate that the effectiveness of a particular plumage pattern in flushing dipteran prey depends strongly on the background against which that plumage pattern is displayed, and darker habitat (background) conditions generally favor plumages with more extensive patches of white in the tail. However, the addition of white wing patches that imitate the plumage of the painted redstart (Myioborus pictus) generally increases insect escape responses but reduces the effect that tail pattern variation and background tone have on escape behavior. These experiments support the hypothesis that habitat-specific natural selection to enhance sensory exploitation of prey escape responses could produce geographic variation in plumage patterns of flush-pursuers.     

Pitching Moment Generation in an Insect-Mimicking Flapping-Wing System

Unlike birds, insects lack control surfaces at the tail and hence most insects modify their wing kinematics to produce control forces or moments while flapping their wings. Change of the flapping angle range is one of the ways to modify wing kinematics, resulting in relocation of the mean Aerodynamic force Center （mean AC） and finally creating control moments. In an attempt to mimic this feature, we developed a flapping-wing system that generates a desired pitching moment during flap- ping-wing motion. The system comprises a flapping mechanism that creates a large and symmetric flapping motion in a pair of wings, a flapping angle change mechanism that modifies the flapping angle range, artificial wings, and a power source. From the measured wing kinematics, we have found that the flapping-wing system can properly modify the flapping angle ranges. The measured pitching moments show that the flapping-wing system generates a pitching moment in a desired direction by shifting the flapping angle range. We also demonstrated that the system can in practice change the longitudinal attitude by generating a nonzero pitching moment.     

Dipteran insect flight dynamics. Part 1 Longitudinal motion about hover

This paper presents a reduced-order model of longitudinal hovering flight dynamics for dipteran insects. The quasi-steady wing aerodynamics model is extended by including perturbation states from equilibrium and paired with rigid body equations of motion to create a nonlinear simulation of a Drosophila-like insect. Frequency-based system identification tools are used to identify the transfer functions from biologically inspired control inputs to rigid body states. Stability derivatives and a state space linear system describing the dynamics are also identified. The vehicle control requirements are quantified with respect to traditional human pilot handling qualities specification. The heave dynamics are found to be decoupled from the pitch/fore/aft dynamics. The haltere-on system revealed a stabilized system with a slow (heave) and fast subsidence mode, and a stable oscillatory mode. The haltere-off (bare airframe) system revealed a slow (heave) and fast subsidence mode and an unstable oscillatory mode, a modal structure in agreement with CFD studies. The analysis indicates that passive aerodynamic mechanisms contribute to stability, which may help explain how insects are able to achieve stable locomotion on a very small computational budget.     

Structure, form, and function of flight in engineering and the living world

By combining appearance and behavior in animals with physical laws, we can get an understanding of the adaptation and evolution of various structures and forms. Comparisons can be made between animal bodies and various technical constructions. Technical science and theory during the latest decades have resulted in considerable insight into biological adaptations, but studies on structures, forms, organs, systems, and processes in the living world, used in the right way, have also aided the engineer in finding wider and better solutions to various problems, among them in the design of micro-air vehicles (MAVs). In this review, I discuss the basis for flight and give some examples of where flight engineering and nature have evolved similar solutions. In most cases technology has produced more advanced structures, but sometimes animals are superior. I include how different animals have solved the problem of producing lift, how animal wings meet the requirements of strength and rigidity, how wing forms are adapted to various flight modes, and how flight kinematics are related to flight behavior and speed. The dynamics of vorticity is summarized. There are a variety of methods for the determination of flight power; it has been estimated adequately by lifting-line theory, by physiological measurements, and from mass loss and food intake. In recent years alternative methods have been used, in which the mechanical power for flight is estimated from flight muscle force used during the downstroke. Refinements of these methods may create new ways of estimating flight power more accurately. MAVs operate at the same Reynolds numbers as large insects and small birds and bats. Therefore, studies on animal flight are valuable for MAV design, which is discussed here.     

Kinematic plasticity during flight in fruit bats: individual variability in response to loading

All bats experience daily and seasonal fluctuation in body mass. An increase in mass requires changes in flight kinematics to produce the extra lift necessary to compensate for increased weight. How bats modify their kinematics to increase lift, however, is not well understood. In this study, we investigated the effect of a 20% increase in mass on flight kinematics for Cynopterus brachyotis, the lesser dog-faced fruit bat. We reconstructed the 3D wing kinematics and how they changed with the additional mass. Bats showed a marked change in wing kinematics in response to loading, but changes varied among individuals. Each bat adjusted a different combination of kinematic parameters to increase lift, indicating that aerodynamic force generation can be modulated in multiple ways. Two main kinematic strategies were distinguished: bats either changed the motion of the wings by primarily increasing wingbeat frequency, or changed the configuration of the wings by increasing wing area and camber. The complex, individual-dependent response to increased loading in our bats points to an underappreciated aspect of locomotor control, in which the inherent complexity of the biomechanical system allows for kinematic plasticity. The kinematic plasticity and functional redundancy observed in bat flight can have evolutionary consequences, such as an increase potential for morphological and kinematic diversification due to weakened locomotor trade-offs.     

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.