How do hoverflies use their righting reflex?

When taking off from a sloping surface, flies have to reorient themselves dorsoventrally and stabilize their body by actively controlling their flapping wings. We have observed that righting is achieved solely by performing a rolling manoeuvre. How flies manage to do this has not yet been elucidated. It was observed here for the first time that hoverfly reorientation is entirely achieved within 6 wingbeats (48.8 ms) at angular roll velocities of up to 10×103 deg s-1 and that the onset of their head rotation consistently follows that of their body rotation after a time lag of 16 ms. The insects' body roll was found to be triggered by the asymmetric wing stroke amplitude, as expected. The righting process starts immediately with the first wingbeat and seems unlikely to depend on visual feedback. A dynamic model for the fly's righting reflex is presented, which accounts for the head/body movements and the time lag recorded in these experiments. This model consists of a closed-loop control of the body roll, combined with a feedforward control of the head/body angle. During the righting manoeuvre, a strong coupling seems to exist between the activation of the halteres (which measure the body's angular speed) and the gaze stabilization reflex. These findings again confirm the fundamental role played by the halteres in both body and head stabilization processes.

Role of the light source position in freely falling hoverflies' stabilization performances.

The stabilization of plummeting hoverflies was filmed and analysed in terms of their wingbeat initiation times as well as the crash and stabilization rates. The flies experienced near-weightlessness for a period of time that depended on their ability to counteract the free fall by triggering their wingbeats. In this paradigm, hoverflies' flight stabilization strategies were investigated here for the first time under two different positions of the light source (overhead and bottom lighting). The crash rates were higher in bottom lighting conditions than with top lighting. In addition, adding a texture to the walls reduced the crash rates only in the overhead lighting condition. The position of the lighting also significantly affected both the stabilization rates and the time taken by the flies to stabilize, which decreased and increased under bottom lighting conditions, respectively, whereas textured walls increased the stabilization rates under both lighting conditions. These results support the idea that flies may mainly base their flight control strategy on visual cues and particularly that the light distribution in the visual field may provide reliable, efficient cues for estimating their orientation with respect to an allocentric reference frame. In addition, the finding that the hoverflies' optic flow-based motion detection ability is affected by the position of the light source in their visual field suggests the occurrence of interactions between movement perception and this visual vertical perception process.

Flies tune the activity of their multifunctional gyroscope.

Members of the order Diptera, the true flies, are among the most maneuverable flying animals. These aerial capabilities are partially attributed to flies' possession of halteres, tiny club-shaped structures that evolved from the hindwings and play a crucial role in flight control. Halteres are renowned for acting as biological gyroscopes that rapidly detect rotational perturbations and help flies maintain a stable flight posture. Additionally, halteres provide rhythmic input to the wing steering system that can be indirectly modulated by the visual system. The multifunctional capacity of the haltere is thought to depend on arrays of embedded mechanosensors called campaniform sensilla that are arranged in distinct groups on the haltere's dorsal and ventral surfaces. Although longstanding hypotheses suggest that each array provides different information relevant to the flight control circuitry, we know little about how the haltere campaniforms are functionally organized. Here, we use in vivo calcium imaging during tethered flight to obtain population-level recordings of the haltere sensory afferents in specific fields of sensilla. We find that haltere feedback from both dorsal fields is continuously active, modulated under closed-loop flight conditions, and recruited during saccades to help flies actively maneuver. We also find that the haltere's multifaceted role may arise from the steering muscles of the haltere itself, regulating haltere stroke amplitude to modulate campaniform activity. Taken together, our results underscore the crucial role of efferent control in regulating sensor activity and provide insight into how the sensory and motor systems of flies coevolved.

Substrate-mediated leg interactions play a key role in insect stability on granular slopes.

Locomotion on granular inclines is a subject of high relevance in ecological physics as well as in biomimmetics and robotics. Enhancing stability on granular materials represents a huge challenge due to the fluidization transition when inclination approaches the avalanche angle. Our motivating example is the predator-prey system made of the antlion, its pit, and its prey. Recent studies have demonstrated that stability on granular inclines strongly depends on the pressure exerted on the substrate. In this work we show that for multilegged locomotion, along with pressure, the distance between the leg contacts on the substrate also plays a major role in the determination of the stability threshold. Through a set of model experiments using artificial sliders, we determine a critical distance below which stability is importantly affected by the interactions between the perturbed regions generated by each contact point. A simple model based on the Coulomb method of wedges allows us to estimate a stability criterion based on pressure, interleg distance, and substrate characteristics. Our work suggests that mass to leg-length allometric relationships, as the ones observed in ants, may be an important key in determining the locomotion success of multilegged locomotion on granular inclines.

Sensory fusion in the hoverfly righting reflex.

We study how falling hoverflies use sensory cues to trigger appropriate roll righting behavior. Before being released in a free fall, flies were placed upside-down with their legs contacting the substrate. The prior leg proprioceptive information about their initial orientation sufficed for the flies to right themselves properly. However, flies also use visual and antennal cues to recover faster and disambiguate sensory conflicts. Surprisingly, in one of the experimental conditions tested, hoverflies flew upside-down while still actively flapping their wings. In all the other conditions, flies were able to right themselves using two roll dynamics: fast ([Formula: see text]50ms) and slow ([Formula: see text]110ms) in the presence of consistent and conflicting cues, respectively. These findings suggest that a nonlinear sensory integration of the three types of sensory cues occurred. A ring attractor model was developed and discussed to account for this cue integration process.