Landing maneuvers of houseflies on vertical and inverted surfaces

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.