Fritz-Olaf Lehmann

Bumblebee flight in heavy turbulence

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

Calcium signalling indicates bilateral power balancing in the Drosophila flight muscle during manoeuvring flight

Manoeuvring flight in animals requires precise adjustments of mechanical power output produced by the flight musculature. In many insects such as fruit flies, power generation is most likely varied by altering stretch-activated tension, that is set by sarcoplasmic calcium levels. The muscles reside in a thoracic shell that simultaneously drives both wings during wing flapping. Using a genetically expressed muscle calcium indicator, we here demonstrate in vivo the ability of this animal to bilaterally adjust its calcium activation to the mechanical power output required to sustain aerodynamic costs during flight. Motoneuron-specific comparisons of calcium activation during lift modulation and yaw turning behaviour suggest slightly higher calcium activation for dorso-longitudinal than for dorsoventral muscle fibres, which corroborates the elevated need for muscle mechanical power during the wings’ downstroke. During turning flight, calcium activation explains only up to 54 per cent of the required changes in mechanical power, suggesting substantial power transmission between both sides of the thoracic shell. The bilateral control of muscle calcium runs counter to the hypothesis that the thorax of flies acts as a single, equally proportional source for mechanical power production for both flapping wings. Collectively, power balancing highlights the precision with which insects adjust their flight motor to changing energetic requirements during aerial steering. This potentially enhances flight efficiency and is thus of interest for the development of technical vehicles that employ bioinspired strategies of power delivery to flapping wings.

Proprioceptive feedback determines visuomotor gain in Drosophila

Multisensory integration is a prerequisite for effective locomotor control in most animals. Especially, the impressive aerial performance of insects relies on rapid and precise integration of multiple sensory modalities that provide feedback on different time scales. In flies, continuous visual signalling from the compound eyes is fused with phasic proprioceptive feedback to ensure precise neural activation of wing steering muscles (WSM) within narrow temporal phase bands of the stroke cycle. This phase-locked activation relies on mechanoreceptors distributed over wings and gyroscopic halteres. Here we investigate visual steering performance of tethered flying fruit flies with reduced haltere and wing feedback signalling. Using a flight simulator, we evaluated visual object fixation behaviour, optomotor altitude control and saccadic escape reflexes. The behavioural assays show an antagonistic effect of wing and haltere signalling on visuomotor gain during flight. Compared with controls, suppression of haltere feedback attenuates while suppression of wing feedback enhances the animal’s wing steering range. Our results suggest that the generation of motor commands owing to visual perception is dynamically controlled by proprioception. We outline a potential physiological mechanism based on the biomechanical properties of WSM and sensory integration processes at the level of motoneurons. Collectively, the findings contribute to our general understanding how moving animals integrate sensory information with dynamically changing temporal structure.

Body appendages fine-tune posture and moments in freely manoeuvring fruit flies

ABSTRACT The precise control of body posture by turning moments is key to elevated locomotor performance in flying animals. Although elevated moments for body stabilization are typically produced by wing aerodynamics, animals also steer using drag on body appendages, shifting their centre of body mass, and changing moments of inertia caused by active alterations in body shape. To estimate the instantaneous contribution of each of these components for posture control in an insect, we three-dimensionally reconstructed body posture and movements of body appendages in freely manoeuvring fruit flies (Drosophila melanogaster) by high-speed video and experimentally scored drag coefficients of legs and body trunk at low Reynolds number. The results show that the sum of leg- and abdomen-induced yaw moments dominates wing-induced moments during 17% of total flight time but is, on average, 7.2-times (roll, 3.4-times) smaller during manoeuvring. Our data reject a previous hypothesis on synergistic moment support, indicating that drag on body appendages and mass-shift inhibit rather than support turning moments produced by the wings. Numerical modelling further shows that hind leg extension alters the moments of inertia around the three main body axes of the animal by not more than 6% during manoeuvring, which is significantly less than previously reported for other insects. In sum, yaw, pitch and roll steering by body appendages probably fine-tune turning behaviour and body posture, without providing a significant advantage for posture stability and moment support. Motion control of appendages might thus be part of the insects trimming reflexes, which reduce imbalances in moment generation caused by unilateral wing damage and abnormal asymmetries of the flight apparatus. Summary: In Drosophila, motion control of appendages allows flies to trim out imbalances in moment generation caused by wing damage and abnormal asymmetries of the flight apparatus.

Neural control and precision of flight muscle activation in Drosophila

Precision of motor commands is highly relevant in a large context of various locomotor behaviors, including stabilization of body posture, heading control and directed escape responses. While posture stability and heading control in walking and swimming animals benefit from high friction via ground reaction forces and elevated viscosity of water, respectively, flying animals have to cope with comparatively little aerodynamic friction on body and wings. Although low frictional damping in flight is the key to the extraordinary aerial performance and agility of flying birds, bats and insects, it challenges these animals with extraordinary demands on sensory integration and motor precision. Our review focuses on the dynamic precision with which Drosophila activates its flight muscular system during maneuvering flight, considering relevant studies on neural and muscular mechanisms of thoracic propulsion. In particular, we tackle the precision with which flies adjust power output of asynchronous power muscles and synchronous flight control muscles by monitoring muscle calcium and spike timing within the stroke cycle. A substantial proportion of the review is engaged in the significance of visual and proprioceptive feedback loops for wing motion control including sensory integration at the cellular level. We highlight that sensory feedback is the basis for precise heading control and body stability in flies.

Sensory processing by motoneurons: a numerical model for low-level flight control in flies

Rhythmic locomotor behaviour in animals requires exact timing of muscle activation within the locomotor cycle. In rapidly oscillating motor systems, conventional control strategies may be affected by neural delays, making these strategies inappropriate for precise timing control. In flies, wing control thus requires sensory processing within the peripheral nervous system, circumventing the central brain. The underlying mechanism, with which flies integrate graded depolarization of visual interneurons and spiking proprioceptive feedback for precise muscle activation, is under debate. Based on physiological parameters, we developed a numerical model of spike initiation in flight muscles of a blowfly. The simulated Hodgkin–Huxley neuron reproduces multiple experimental findings and explains on the cellular level how vision might control wing kinematics. Sensory processing by single motoneurons appears to be sufficient for control of muscle power during flight in flies and potentially other flying insects, reducing computational load on the central brain during body posture reflexes and manoeuvring flight.