Landing maneuvers of houseflies on vertical and inverted surfaces

Abstract

Landing maneuvers of flies are complex behaviors which can be conceptually decomposed into sequences of modular actions, including body-deceleration, leg-extension, and body rotations. These behavioral ‘modules’ must be coordinated to ensure well-controlled landing. The composite nature of these behaviors induces kinematic variability, making it difficult to identify the central rules that govern landing. Many previous studies have relied on tethered preparations to study landing behaviors, but tethering induces experimental artefacts by forcing some behaviors to operate in open-feedback control loop while others remain closed-loop. On the other hand, it is harder for the experimenter to control the stimuli experienced by freely-flying insects. One approach towards understanding general mechanisms of landing is to determine the common elements of their kinematics on surfaces of different orientations. We conducted a series of experiments in which the houseflies, Musca domestica , were lured to land on vertical ( wall landings ) or inverted ( ceiling landings ) substrates, while their flight was recorded with multiple high-speed cameras. We observed that, in both cases, well-controlled landings occurred when the distance at which flies initiated deceleration was proportional to flight velocity component in the direction of substrate. The ratio of substrate distance and velocity at onset of deceleration ( tau ) was conserved, despite substantial differences in mechanics of vertical vs. ceiling landings. When these conditions were not satisfied, their landing performance was compromised, causing their heads to collide into the substrate. Unlike body-deceleration, leg-extension in flies was independent of substrate distance or approach velocity. Thus, the robust reflexive visual initiation of deceleration is independent of substrate orientation, and combines with a more variable initiation of leg-extension which depends on surface orientation. Together, these combinations of behaviors enable flies to land in a versatile manner on substrates of various orientations.

A single touch can provide sufficient mechanical stimulation to trigger Venus flytrap closure

“…Reasoning that hair deflection induced by spiders, ants, and flies-i.e., the "classical" prey of D. muscipula [21]-would be rather quick, we operated the microrobotic system at full speed to simulate these stimuli, resulting in high initial angular velocities ranging from 10 to 20 rad s −1 . This is in the same range as Scherzer and colleagues found for moving ants, which deflect the sensory hair with an angular velocity of 0.25-7.8 rad s −1 [20] but much slower than the leg movements of houseflies [22]. At such high velocities, the duration of a deflection is much shorter than other involved time-dependent factors, such as the decay of the RP [19] and the relaxation of the sensory hair ( Fig 1F).…”

Bumblebees land rapidly and robustly using a sophisticated modular flight control strategy

“…The animal's motion relative to the landing surface generates a radially expanding optic flow field, in which various features in the image appear to move radially outward from the center of expansion ( Gibson, 1955 ; Edwards and Ibbotson, 2007 ). Flying animals can use this rate of optical expansion along with the retinal size of an object ( Wagner, 1982 ) or angular position of features in the visual field ( Baird et al., 2013 ) to compute the “relative rate of expansion ( r )” or its inverse, the instantaneous “time to contact” (τ = 1/ r , referred to as parameter tau in literature) ( Lee, 1976 ; Sun and Frost, 1998 ; Lee et al., 2009 ; Balebail et al., 2019 ). The relative rate of expansion provides information about the ego-motion of the animal and equals the ratio between approach speed V and distance from the landing surface y ( r = V / y ); instantaneous time-to-contact equals the time until contact with the landing surface, should the animal continue to fly at its current flight speed (τ = y / V ).…”

Landing mosquitoes bounce when engaging a substrate

“…aegypti mosquitoes employ bouncing sequences, leg compression, and proboscis deformation to engage landing surfaces. Unlike bees 38 , houseflies 7 , and fruit flies 8 , we do not witness mosquitoes prepare for landing by adjusting leg posture or body rotation. Their substrate interactions often have head and torso contact with the substrate (Fig.…”

“…Insect flight is an enduring topic, with numerous studies on takeoff 1 – 3 , in-flight mechanics 4 – 6 , and landing 7 – 9 . Landings are unique from other flight maneuvers because they require matching the relative motion of a target, demanding highly-coordinated movements in response to visual, thermal, acoustic, and olfactory signals 10 – 15 .…”

“…A female housefly (Musca domestica) approaches a landing surface at a constant velocity until the object reaches a critical size on its retina to induce deceleration 11 . Upon approach to a vertical landing surface, legs extend and bodies pitch upward 7 , most likely as a means to decelerate-flight velocity and pitch are inversely related in houseflies 41 . In contrast, fruit flies (Drosophila melanogaster) accelerate towards their landing surface and, upon touchdown, use leg forces to undergo nearly instant deceleration 8 .…”