First lift-off and flight performance of a tailless flapping-wing aerial robot in high-altitude environments.

Flapping flight of animals has captured the interest of researchers due to their impressive flight capabilities across diverse environments including mountains, oceans, forests, and urban areas. Despite the significant progress made in understanding flapping flight, high-altitude flight as showcased by many migrating animals remains underexplored. At high-altitudes, air density is low, and it is challenging to produce lift. Here we demonstrate a first lift-off of a flapping wing robot in a low-density environment through wing size and motion scaling. Force measurements showed that the lift remained high at 0.14 N despite a 66% reduction of air density from the sea-level condition. The flapping amplitude increased from 148 to 233 degrees, while the pitch amplitude remained nearly constant at 38.2 degrees. The combined effect is that the flapping-wing robot benefited from the angle of attack that is characteristic of flying animals. Our results suggest that it is not a simple increase in the flapping frequency, but a coordinated increase in the wing size and reduction in flapping frequency enables the flight in lower density condition. The key mechanism is to preserve the passive rotations due to wing deformation, confirmed by a bioinspired scaling relationship. Our results highlight the feasibility of flight under a low-density, high-altitude environment due to leveraging unsteady aerodynamic mechanisms unique to flapping wings. We anticipate our experimental demonstration to be a starting point for more sophisticated flapping wing models and robots for autonomous multi-altitude sensing. Furthermore, it is a preliminary step towards flapping wing flight in the ultra-low density Martian atmosphere.

Analysis of Odor-Tracking Performance of Silk Moth Using a Sensory-Motor Intervention System.

Animals can adaptively behave in different environmental conditions by converting environmental information obtained from their sensory organs into actions. This sensory-motor integration enables the accomplishment of various tasks and is essential for animal survival. This sensory-motor integration also plays an important role in localization to females, relying on sex pheromones floating in space. In this study, we focused on the localization behavior of the adult male silk moth, Bombyx mori. We investigated sensory-motor integration against time delay using odor plume tracking performance as an index when we set a certain time delay for the sensory and motor responses. Given that it is difficult to directly intervene in the sensory and motor functions of the silk moth, we constructed an intervention system based on a mobile behavior measurement system controlled by them. Using this intervention system, not only can timing the detection of the odor in the environment and timing the presentation of the odor to the silk moth be manipulated, but timing the reflection of the movement of the silk moth can also be manipulated. We analyzed the extent to which the localization strategy of the silk moth could tolerate sensory delays by setting a delay to the odor presentation. We also evaluated behavioral compensation by odor sensory feedback by setting a delay to the motor. The results of the localization experiment have shown that the localization success rate did not decrease when there was a motor delay. However, when there was a sensory delay, the success rate decreased depending on the time delay. Analysis of the change in behavior after detection of the odor stimulus has shown that the movement was more linear when we set a motor delay. However, the movement was accompanied by a large rotational movement when there was a delay in the sensory input. This result has suggested that behavior is compensated for the delay in motor function by feedback control of odor sensation, but not when accompanied by sensory delay. To compensate for this, the silk moth may acquire appropriate information from the environment by making large body movements.

Modeling the musculoskeletal system of an insect thorax for flapping flight.

Indirect actuation of the wings via thoracic deformation is a unique mechanism widely observed in flying insect species. The physical properties of the thorax have been intensively studied in terms of their ability to efficiently generate wingbeats. The basic mechanism of indirect wing actuation is generally explained as a lever model on a cross-sectional plane, where the dorsoventral movement of the mesonotum (dorsal exoskeleton of the mesothorax) generated by contractions of indirect muscles actuates the wing. However, the model considers the mesonotum as an ideal flat plane, whereas the mesonotum is hemispherical and becomes locally deformed during flight. Furthermore, the conventional model is two-dimensional; therefore, three-dimensional wing kinematics by indirect muscles have not been studied to date. In this study, we develop structural models of the mesonotum and mesothorax of the hawkmothAgrius convolvuli, reconstructed from serial cross-sectional images. External forces are applied to the models to mimic muscle contraction, and mesonotum deformation and wing trajectories are analyzed using finite element analysis. We find that applying longitudinal strain to the mesonotum to mimic strain by depressor muscle contraction reproduces local deformation comparable to that of the thorax during flight. Furthermore, the phase difference of the forces applied to the depressor and elevator muscles changes the wing trajectory from a figure eight to a circle, which is qualitatively consistent with the tethered flight experiment. These results indicate that the local deformation of the mesonotum due to its morphology and the thoracic deformation via indirect power muscles can modulate three-dimensional wing trajectories.

Pheromone binding protein is involved in temporal olfactory resolution in the silkmoth.

Male moths utilize spatio-temporal female sex pheromone information to orient toward conspecific females. Pheromones are distributed as discontinuous plumes owing to air turbulence; thus, efficient tracking of intermittent stimuli is expected to require a high temporal resolution. Here, using pheromone binding protein (BmPBP1)-knockout silkmoths, we showed that a loss of functional PBP lowered the temporal sensory resolution of male antennae. This altered temporal resolution resulted in significantly reduced straight walking and longer turning behavior, which respectively occurred when males detected and lost contact with pheromones, indicating that temporal resolution was also lowered at the behavioral level. BmPBP1-knockout males required significantly longer time than wild-type males in locating pheromone sources and female moths. Our results suggest that BmPBP1 plays a critical role in determining olfactory response kinetics. Accordingly, high temporal olfactory and behavioral resolutions, as shaped by PBP, are essential for tracking pheromone plumes and locating females efficiently.

Effects of uniform vertical inflow perturbations on the performance of flapping wings.

Flapping wings have attracted significant interest for use in miniature unmanned flying vehicles. Although numerous studies have investigated the performance of flapping wings under quiescent conditions, effects of freestream disturbances on their performance remain under-explored. In this study, we experimentally investigated the effects of uniform vertical inflows on flapping wings using a Reynolds-scaled apparatus operating in water at Reynolds number ≈ 3600. The overall lift and drag produced by a flapping wing were measured by varying the magnitude of inflow perturbation from J Vert = -1 (downward inflow) to J Vert = 1 (upward inflow), where J Vert is the ratio of the inflow velocity to the wing's velocity. The interaction between flapping wing and downward-oriented inflows resulted in a steady linear reduction in mean lift and drag coefficients, C ¯ L and C ¯ D , with increasing inflow magnitude. While a steady linear increase in C ¯ L and C ¯ D was noted for upward-oriented inflows between 0 < J Vert < 0.3 and J Vert > 0.7, a significant unsteady wing-wake interaction occurred when 0.3 ≤ J Vert < 0.7, which caused large variations in instantaneous forces over the wing and led to a reduction in mean performance. These findings highlight asymmetrical effects of vertically oriented perturbations on the performance of flapping wings and pave the way for development of suitable control strategies.

Performance of passively pitching flapping wings in the presence of vertical inflows.

The successful implementation of passively pitching flapping wings strongly depends on their ability to operate efficiently in wind disturbances. In this study, we experimentally investigated the interaction between a uniform vertical inflow perturbation and a passive-pitching flapping wing using a Reynolds-scaled apparatus operating in water at Reynolds number ≈3600. A parametric study was performed by systematically varying the Cauchy number (Ch) of the wings from 0.09 to 11.52. The overall lift and drag, and pitch angle of the wing were measured by varying the magnitude of perturbation fromJVert= -0.6 (downward inflow) toJVert= 0.6 (upward inflow) at eachCh, whereJVertis the ratio of the inflow velocity to the wing's velocity. We found that the lift and drag had remarkably different characteristics in response to bothChandJVert. Across allCh, while mean lift tended to increase as the inflow perturbation varied from -0.6 to 0.6, drag was significantly less sensitive to the perturbation. However effect of the vertical inflow on drag was dependent onCh, where it tended to vary from an increasing to a decreasing trend asChwas changed from 0.09 to 11.52. The differences in the lift and drag with perturbation magnitude could be attributed to the reorientation of the net force over the wing as a result of the interaction with the perturbation. These results highlight the complex interactions between passively pitching flapping wings and freestream perturbations and will guide the design of miniature flying crafts with such architectures.

Internal state transition to switch behavioral strategies in cricket phonotaxis.

Animals employ multiple behavioral strategies for exploring food and mating partners based on both their internal state and external environment. Here, we examined how cricket phonotaxis, which was considered an innate reactive behavior of females to approach the calling song of conspecific males, depended on these internal and external conditions. Our observation revealed that the phonotaxis process consisted of two distinctive phases: wandering and approaching. In the latter phase, crickets moved directly towards the sound source. The transition into this phase, referred to as the 'approach phase', was based on changes in the animal's internal state. Moreover, retention of the approach phase required recognition of the calling song, while song loss downregulated cricket mobility and induced frequent stopping. This is a typical movement in local search behaviors. Our results indicate that phonotaxis is not only a reactive response but a complicated process including multiple behavioral strategies.

Insect-machine hybrid robot.

Recently, insect-machine hybrid robots have been developed that incorporate insects into robots or incorporate machines into insects. Most previous studies were motivated to use the function of insects for robots, but this technology can also prove to be useful as an experimental tool for neuroethology. We reviewed hybrid robots in terms of the closed-loop between an insect, a robot, and the real environment. The incorporated biological components provided the robot sensory signals that were received by the insects and the adaptive functions of the brain. The incorporated artificial components permitted us to understand the biological system by controlling insect behavior. Hybrid robots thus extend the roles of mobile robot experiments in neuroethology for both model evaluation and brain function analysis.

Dropping Counter: A Detection Algorithm for Identifying Odour-Evoked Responses from Noisy Electroantennograms Measured by a Flying Robot.

The electroantennogram (EAG) is a technique used for measuring electrical signals from the antenna of an insect. Its rapid response time, quick recovery speed, and high sensitivity make it suitable for odour-tracking tasks employing mobile robots. However, its application to flying robots has not been extensively studied owing to the electrical and mechanical noises generated. In this study, we investigated the characteristics of the EAG mounted on a tethered flying quadcopter and developed a special counter-based algorithm for detecting the odour-generated responses. As the EAG response is negative, the algorithm creates a window and compares the values inside it. Once a value is smaller than the first one, the counter will increase by one and finally turns the whole signal into a clearer odour stimulated result. By experimental evaluation, the new algorithm gives a higher cross-correlation coefficient when compared with the fixed-threshold method. The result shows that the accuracy of this novel algorithm for recognising odour-evoked EAG signals from noise exceeds that of the traditional method; furthermore, the use of insect antennae as odour sensors for flying robots is demonstrated to be feasible.

Using insects to drive mobile robots - hybrid robots bridge the gap between biological and artificial systems.

The use of mobile robots is an effective method of validating sensory-motor models of animals in a real environment. The well-identified insect sensory-motor systems have been the major targets for modeling. Furthermore, mobile robots implemented with such insect models attract engineers who aim to avail advantages from organisms. However, directly comparing the robots with real insects is still difficult, even if we successfully model the biological systems, because of the physical differences between them. We developed a hybrid robot to bridge the gap. This hybrid robot is an insect-controlled robot, in which a tethered male silkmoth (Bombyx mori) drives the robot in order to localize an odor source. This robot has the following three advantages: 1) from a biomimetic perspective, the robot enables us to evaluate the potential performance of future insect-mimetic robots; 2) from a biological perspective, the robot enables us to manipulate the closed-loop of an onboard insect for further understanding of its sensory-motor system; and 3) the robot enables comparison with insect models as a reference biological system. In this paper, we review the recent works regarding insect-controlled robots and discuss the significance for both engineering and biology.

Flexibility and control of thorax deformation during hawkmoth flight.

The interaction between neuromuscular systems and body mechanics plays an important role in the production of coordinated movements in animals. Lepidopteran insects move their wings by distortion of the thorax structure via the indirect flight muscles (IFMs), which are activated by neural signals at every stroke. However, how the action of these muscles affects thorax deformation and wing kinematics is poorly understood. We measured the deformation of the dorsal thorax (mesonotum) of tethered flying hawkmoths, Agrius convolvuli, using a high-speed laser profilometer combined with simultaneous recordings of electromyograms and wing kinematics. We observed that locally amplified mesonotum deformation near the wing hinges ensures sufficient wing movement. Furthermore, phase asymmetry in IFM activity leads to phase asymmetry in mesonotum oscillations and wingbeats. Our results revealed the flexibility and controllability of the single structure of the mesonotum by neurogenic action of the IFMs.

Insect-controlled Robot: A Mobile Robot Platform to Evaluate the Odor-tracking Capability of an Insect.

Robotic odor source localization has been a challenging area and one to which biological knowledge has been expected to contribute, as finding odor sources is an essential task for organism survival. Insects are well-studied organisms with regard to odor tracking, and their behavioral strategies have been applied to mobile robots for evaluation. This "bottom-up" approach is a fundamental way to develop biomimetic robots; however, the biological analyses and the modeling of behavioral mechanisms are still ongoing. Therefore, it is still unknown how such a biological system actually works as the controller of a robotic platform. To answer this question, we have developed an insect-controlled robot in which a male adult silkmoth (Bombyx mori) drives a robot car in response to odor stimuli; this can be regarded as a prototype of a future insect-mimetic robot. In the cockpit of the robot, a tethered silkmoth walked on an air-supported ball and an optical sensor measured the ball rotations. These rotations were translated into the movement of the two-wheeled robot. The advantage of this "hybrid" approach is that experimenters can manipulate any parameter of the robot, which enables the evaluation of the odor-tracking capability of insects and provides useful suggestions for robotic odor-tracking. Furthermore, these manipulations are non-invasive ways to alter the sensory-motor relationship of a pilot insect and will be a useful technique for understanding adaptive behaviors.

A simple behaviour provides accuracy and flexibility in odour plume tracking--the robotic control of sensory-motor coupling in silkmoths.

Odour plume tracking is an essential behaviour for animal survival. A fundamental strategy for this is to move upstream and then across-stream. Male silkmoths, Bombyx mori, display this strategy as a pre-programmed sequential behaviour. They walk forward (surge) in response to the female sex pheromone and perform a zigzagging 'mating dance'. Though pre-programmed, the surge direction is modulated by bilateral olfactory input and optic flow. However, the nature of the interaction between these two sensory modalities and contribution of the resultant motor command to localizing an odour source are still unknown. We evaluated the ability of the silkmoth to localize an odour source under conditions of disturbed sensory-motor coupling, using a silkmoth-driven mobile robot. The significance of the bilateral olfaction of the moth was confirmed by inverting the olfactory input to the antennae, or its motor output. Inversion of the motor output induced consecutive circling, which was inhibited by covering the visual field of the moth. This suggests that the corollary discharge from the motor command and the reafference of self-generated optic flow generate compensatory signals to guide the surge accurately. Additionally, after inverting the olfactory input, the robot successfully tracked the odour plume by using a combination of behaviours. These results indicate that accurate guidance of the reflexive surge by integrating bilateral olfactory and visual information with innate pre-programmed behaviours increases the flexibility to track an odour plume even under disturbed circumstances.

Dynamic use of optic flow during pheromone tracking by the male silkmoth, Bombyx mori.

Several insects require both olfactory and visual cues during odour-source localisation to successfully locate an odour source. In the male silkmoth, Bombyx mori, detection of the female sex pheromone triggers a programmed walking pattern, starting from a surge (straight-line walking) followed by zigzag walking. Although pheromone-triggered behaviour in silkmoths is well understood, the role of visual cues remains obscure. To address this question, we performed behavioural experiments on tethered-walking moths by recording their locomotion during stimulation with a pheromone and a visual motion pattern (optic flow). The experiments were conducted under open- and closed-loop visual stimuli. We found that the use of optic flow input was determined by the behavioural state of surge and zigzagging. Silkmoths exhibited an optomotor response, which is a behavioural visual response, by turning towards the same direction as optic flow stimuli only during surge, but not during zigzagging. In addition, modulation of the zigzag walking pattern was observed when the moths were presented with biased closed-loop visual stimuli (visual feedback with biased constant optic flow); however, the directional preference mechanism was different from that of the optomotor response. Based on these findings, we suggest that the optomotor response is utilised for course control during straight-line walking, whereas the absence of optomotor response during zigzagging is used to effectively perform the programmed walking pattern. Considering the neural basis of programmed behaviour, we speculate that at least two visual pathways are involved in the state-dependent use of optic flow during odour tracking behaviour in silkmoths.

Insect-machine hybrid system for understanding and evaluating sensory-motor control by sex pheromone in Bombyx mori.

To elucidate the dynamic information processing in a brain underlying adaptive behavior, it is necessary to understand the behavior and corresponding neural activities. This requires animals which have clear relationships between behavior and corresponding neural activities. Insects are precisely such animals and one of the adaptive behaviors of insects is high-accuracy odor source orientation. The most direct way to know the relationships between neural activity and behavior is by recording neural activities in a brain from freely behaving insects. There is also a method to give stimuli mimicking the natural environment to tethered insects allowing insects to walk or fly at the same position. In addition to these methods an 'insect-machine hybrid system' is proposed, which is another experimental system meeting the conditions necessary for approaching the dynamic processing in the brain of insects for generating adaptive behavior. This insect-machine hybrid system is an experimental system which has a mobile robot as its body. The robot is controlled by the insect through its behavior or the neural activities recorded from the brain. As we can arbitrarily control the motor output of the robot, we can intervene at the relationship between the insect and the environmental conditions.

Central projections of the wing afferents in the hawkmoth, Agrius convolvuli.

Flight behaviors in various insect species are closely correlated with their mechanical and neuronal properties. Compared to locusts and flies which have been intensively studied, moths have "intermediate" properties in terms of the neurogenic muscle activations, power generation by indirect muscles, and two-winged-insect-like flapping behavior. Despite these unique characteristics, little is known about the neuronal mechanisms of flight control in moths. We investigated projections of the wing mechanosensory afferents in the central nervous system (CNS) of the hawkmoth, Agrius convolvuli, because the mechanosensory proprioceptive feedback has an essential role for flight control and would be presumably optimized for insect species. We conducted anterograde staining of nine afferent nerves from the fore- and hindwings. All of these afferents projected into the prothoracic, mesothoracic and metathoracic ganglia (TG1, 2 and 3) and had ascending fibers to the head ganglia. Prominent projection areas in the TG1-3 and suboesophageal ganglion (SOG) were common between the forewing, hindwing and contralateral forewing afferents, suggesting that information from different wings are converged at multiple levels presumably for coordinating wing flapping. On the other hand, differences of projections between the fore- and hindwing afferents were observed especially in projection areas of the tegulae in the TG1 and contralateral projections of the anterior forewing nerve in the TGs and SOG, which would reflect functional differences between corresponding mechanoreceptors on each wing. Afferents comprising groups of the campaniform sensilla at the wing bases had prominent ascending pathways to the SOG, resembling the head-neck motor system for gaze control in flies. Double staining of the wing afferents and flight or neck motoneurons also indicated potential connectivity between them. Our results suggest multiple roles of the wing proprioceptive feedback for flight and provide the anatomical basis for further understanding of neuronal mechanisms of the flight system in moths.

Active control of free flight manoeuvres in a hawkmoth, Agrius convolvuli.

By combining optical triangulation with the comb-fringe technique and dual-channel telemetry, wing kinematics and body attitudes accompanying muscle activities of free-flying male hawkmoths were recorded synchronously when they performed flight manoeuvres elicited by a female sex pheromone. The results indicate that the wing leading edge angular position at the ventral stroke reversal, which can be decomposed by two orthogonal angular parameters (a flapping angle and a deviation angle), is well controllable. Two specific flight muscles, the dorsal-ventral muscle (DVM, indirect muscle, a wing elevator) and the third axillary muscle (3AXM, direct muscle, a wing retractor), can modulate the flapping angle and the deviation angle, respectively, by means of regulating the firing timing of muscle activities. The firing timing can be expressed by the firing latency absolutely, which is just before the timing of ventral stroke reversal. The results illustrate that lengthening the firing latency of the DVM and of the 3AXM can increase the flapping angle and the deviation angle, respectively, which both strengthen the downstroke at the ventral stroke reversal. The relationship of bilateral asymmetry shows that the bilateral differences in the firing latency of the DVM and of the 3AXM will cause bilateral differences in the wing position, which accompany the variations of yaw and roll angles in time course. This implies the contribution of the two muscles to active steering controls during turning or banking, though the DVM being an indirect muscle was generally treated as a power generator. Finally, the relationship between the pitch angle and the 3AXM latency, deduced from the relationships between the pitch angle and the deviation angle and between the deviation angle and the 3AXM latency, shows that lengthening the 3AXM latency can increase the pitch angle at the ventral stroke reversal by moving the wing tip far away from the centre of gravity of the body, which indicates a functional role of the 3AXM in active pitching control.

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.