Directional Sensitivity and Mechanical Coupling Dynamics of Campaniform Sensilla During Chordwise Deformations of the Fly Wing

The complex morphology of an insect campaniform sensillum is responsible for transforming strains of the integument into a displacement of the campaniform dome and subsequently a deformation of the dendritic membrane. In this paper, the first step in this coupling process was investigated in identified campaniform sensilla on the wing of the blowfly by stimulating the sensilla with chord-wise deflections of the wing blade. Campaniform sensilla neurones were sensitive to both dorsal and ventral deflections of the wing, and thus exhibited no strong directional sensitivity to the chord-wise components of wing deformation. These results are consistent with a simplified mechanical model in which the wing veins act as cylinders that undergo bending and torsion during chord-wise wing deformation. By comparing the responses of campaniform neurones to chord-wise deflections of the wing with those evoked by direct punctate stimulation of the dome, it is possible to estimate the dynamic properties of the coupling process that links wing deformation to dome deformation. In the identified campaniform neurone examined, wing-dome coupling attenuates high frequencies and transforms the chord-wise deflections of the wing into dome deformation similar in degree of excitation to that caused by direct punctate indentions that are two or more orders of magnitude smaller in size

The Effects of Wing Rotation on Unsteady Aerodynamic Performance at Low Reynolds Numbers

The downstroke-to-upstroke transition of many insects is characterized by rapid wing rotation. The aerodynamic consequences of these rapid changes in angle of attack have been investigated using a mechanical model dynamically scaled to the Reynolds number appropriate for the flight of small insects such as Drosophila. Several kinematic parameters of the wing flip were examined, including the speed and axis of rotation, as well as the duration and angle of attack during the wing stroke preceding rotation. Alteration of these kinematic parameters altered force generation during the subsequent stroke in a variety of ways. 1. When the rotational axis was close to the trailing edge, the model wing could capture vorticity generated during rotation and greatly increase aerodynamic performance. This vortex capture was most clearly manifested by the generation of lift at an angle of attack of 0°;. Lift at a 0°; angle of attack was also generated following rotation about the leading edge, but only if the downstroke angle was large enough to generate a von Karman street. The lift may be due to an alteration in the effective angle of attack caused by the inter-vortex stream in the downstroke wake. 2. The maximum lift attained (over all angles of attack) was substantially elevated if the wing translated backwards through a wake generated by the previous stroke. Transient lift coefficient values of nearly 4 were obtained when the wing translated back through a von Karman street generated at a 76.5°; angle of attack. This effect might also be explained by the influence of the inter-vortex stream, which contributes a small component to fluid velocity in the direction of translation. 3. The growth of lift with angle of attack was significantly elevated following a 7.5 chord stroke with a 76.5°; angle of attack, although it was relatively constant under all other kinematic conditions. 4. The results also indicate the discrepancies between transient and time-averaged measures of performance that arise when unsteady mechanisms are responsible for force generation. Although the influence of wing rotation was strong during the first few chords of translation, averaging the performance over as little as 6.5 chords of motion greatly attenuated the effects of rotation. 5. Together, these modeling results suggest that the unsteady mechanisms generated by simple wing flips could provide an important source for the production of aerodynamic forces in insect flight. Furthermore, the extreme sensitivity to small variations in almost all kinematic parameters could provide a foundation for understanding the aerodynamic mechanisms underlying active flight control

Linear and Nonlinear Encoding Properties of an Identified Mechanoreceptor on the Fly wing Measured with Mechanical Noise Stimuli

The wing blades of most flies contain a small set of distal campaniform sensilla, mechanoreceptors that respond to deformations of the cuticle. This paper describes a method of analysis based upon mechanical noise stimuli which is used to quantify the encoding properties of one of these sensilla (the d-HCV cell) on the wing of the blowfly Calliphora vomitoria (L.). The neurone is modelled as two components, a linear filter that accounts for the frequency response and phase characteristics of the cell, followed by a static nonlinearity that limits the spike discharge to a narrow portion of the stimulus cycle. The model is successful in predicting the response of campaniform neurones to arbitrary stimuli, and provides a convenient method for quantifying the encoding properties of the sensilla. The d-HCV neurone is only broadly frequency tuned, but its maximal response near 150 Hz corresponds to the wingbeat frequency of Calliphora. In the range of frequencies likely to be encountered during flight, the d-HCV neurone fires a single phase-locked action potential for each stimulus cycle. The phase lag of the cell decreases linearly with increasing frequency such that the absolute delay between stimulus and response remains nearly constant. Thus, during flight the neurone is capable of firing one precisely timed action potential during each wingbeat, and might be used to modulate motor activity that requires afferent input on a cycle-by-cycle basis

Comparison of Encoding Properties of Campaniform Sensilla on the Fly Wing

The wing blade of the blowfly Calliphora vomitoria (L.) carries an array of campaniform sensilla which have previously been divided into slowly and rapidly adapting classes based on their responses to step indentations. In the present study, the physiological characteristics of six sensilla of these two classes are examined within a 20–400 Hz frequency range, using a noise analysis that quantifies linear and nonlinear encoding properties. Both classes exhibit a broad response maximum near 150 Hz, corresponding to the typical wingbeat frequency of the blowfly, and display rectification, limiting the spike response to a narrow portion of a stimulus cycle. The similarity in the encoding properties between the two groups is largely a consequence of the high wingbeat frequency of flies, which precludes any individual neurone from acting as a magnitude detector. Instead, during flight the campaniform neurones might act as ‘one-shot’ detectors, firing a single action potential at a precise phase of each wing stroke cycle. An array of such detectors would be capable of monitoring the passage of a deformational wave as it travels along the wing during each wingbeat

Modulation of Negative Work Output from a Steering Muscle of the Blowfly Calliphora Vicina

Of the 17 muscles responsible for flight control in flies, only the first basalar muscle (b1) is known to fire an action potential each and every wing beat at a precise phase of the wing-beat period. The phase of action potentials in the b1 is shifted during turns, implicating the b1 in the control of aerodynamic yaw torque. We used the work loop technique to quantify the effects of phase modulation on the mechanical output of the b1 of the blowfly Calliphora vicina. During cyclic length oscillations at 10 and 50 Hz, the magnitude of positive work output by the b1 was similar to that measured previously from other insect muscles. However, when tested at wing-beat frequency (150 Hz), the net work performed in each cycle was negative. The twitch kinetics of the b1 suggest that negative work output reflects intrinsic specializations of the b1 muscle. Our results suggest that, in addition to a possible role as a passive elastic element, the phase-sensitivity of its mechanical properties may endow the b1 with the capacity to modulate wing-beat kinematics during turning maneuvers

A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster

Flies exhibit extraordinary maneuverability, relying on feedback from multiple sensory organs to control flight. Both the compound eyes and the mechanosensory halteres encode angular motion as the fly rotates about the three body axes during flight. Since these two sensory modalities differ in their mechanisms of transduction, they are likely to differ in their temporal responses. We recorded changes in stroke kinematics in response to mechanical and visual rotations delivered within a flight simulator. Our results show that the visual system is tuned to relatively slow rotation whereas the haltere-mediated response to mechanical rotation increases with rising angular velocity. The integration of feedback from these two modalities may enhance aerodynamic performance by enabling the fly to sense a wide range of angular velocities during flight

Rotational accelerations stabilize leading edge vortices on revolving fly wings

The aerodynamic performance of hovering insects is largely explained by the presence of a stably attached leading edge vortex (LEV) on top of their wings. Although LEVs have been visualized on real, physically modeled, and simulated insects, the physical mechanisms responsible for their stability are poorly understood. To gain fundamental insight into LEV stability on flapping fly wings we expressed the Navier–Stokes equations in a rotating frame of reference attached to the wing's surface. Using these equations we show that LEV dynamics on flapping wings are governed by three terms: angular, centripetal and Coriolis acceleration. Our analysis for hovering conditions shows that angular acceleration is proportional to the inverse of dimensionless stroke amplitude, whereas Coriolis and centripetal acceleration are proportional to the inverse of the Rossby number. Using a dynamically scaled robot model of a flapping fruit fly wing to systematically vary these dimensionless numbers, we determined which of the three accelerations mediate LEV stability. Our force measurements and flow visualizations indicate that the LEV is stabilized by the `quasi-steady' centripetal and Coriolis accelerations that are present at low Rossby number and result from the propeller-like sweep of the wing. In contrast, the unsteady angular acceleration that results from the back and forth motion of a flapping wing does not appear to play a role in the stable attachment of the LEV. Angular acceleration is, however, critical for LEV integrity as we found it can mediate LEV spiral bursting, a high Reynolds number effect. Our analysis and experiments further suggest that the mechanism responsible for LEV stability is not dependent on Reynolds number, at least over the range most relevant for insect flight (100<Re<14,000). LEVs are stable and continue to augment force even when they burst. These and similar findings for propellers and wind turbines at much higher Reynolds numbers suggest that even large flying animals could potentially exploit LEV-based force augmentation during slow hovering flight, take-offs or landing. We calculated the Rossby number from single-wing aspect ratios of over 300 insects, birds, bats, autorotating seeds, and pectoral fins of fish. We found that, on average, wings and fins have a Rossby number close to that of flies (Ro=3). Theoretically, many of these animals should therefore be able to generate a stable LEV, a prediction that is supported by recent findings for several insects, one bat, one bird and one fish. This suggests that force augmentation through stably attached (leading edge) vortices could represent a convergent solution for the generation of high fluid forces over a quite large range in size

Summation of visual and mechanosensory feedback in Drosophila flight control

The fruit fly Drosophila melanogaster relies on feedback from multiple sensory modalities to control flight maneuvers. Two sensory organs, the compound eyes and mechanosensory hindwings called halteres, are capable of encoding angular velocity of the body during flight. Although motor reflexes driven by the two modalities have been studied individually, little is known about how the two sensory feedback channels are integrated during flight. Using a specialized flight simulator we presented tethered flies with simultaneous visual and mechanosensory oscillations while measuring compensatory changes in stroke kinematics. By varying the relative amplitude, phase and axis of rotation of the visual and mechanical stimuli, we were able to determine the contribution of each sensory modality to the compensatory motor reflex. Our results show that over a wide range of experimental conditions sensory inputs from halteres and the visual system are combined in a weighted sum. Furthermore, the weighting structure places greater influence on feedback from the halteres than from the visual system

Biofluiddynamic scaling of flapping, spinning and translating fins and wings

Organisms that swim or fly with fins or wings physically interact with the surrounding water and air. The interactions are governed by the morphology and kinematics of the locomotory system that form boundary conditions to the Navier–Stokes (NS) equations. These equations represent Newton's law of motion for the fluid surrounding the organism. Several dimensionless numbers, such as the Reynolds number and Strouhal number, measure the influence of morphology and kinematics on the fluid dynamics of swimming and flight. There exists, however, no coherent theoretical framework that shows how such dimensionless numbers of organisms are linked to the NS equation. Here we present an integrated approach to scale the biological fluid dynamics of a wing that flaps, spins or translates. Both the morphology and kinematics of the locomotory system are coupled to the NS equation through which we find dimensionless numbers that represent rotational accelerations in the flow due to wing kinematics and morphology. The three corresponding dimensionless numbers are (1) the angular acceleration number, (2) the centripetal acceleration number, and (3) the Rossby number, which measures Coriolis acceleration. These dimensionless numbers consist of length scale ratios, which facilitate their geometric interpretation. This approach gives fundamental insight into the physical mechanisms that explain the differences in performance among flapping, spinning and translating wings. Although we derived this new framework for the special case of a model fly wing, the method is general enough to make it applicable to other organisms that fly or swim using wings or fins