Visual control of landing maneuvers in houseflies on vertical and inverted surfaces

Abstract

Landing maneuvers in flies are complex behaviors that may be conceptually decomposed into a sequence of modular behaviors such as body deceleration, extension of legs, and body rotations which are coordinated to ensure controlled touchdown. The composite nature of these behaviors means that there is variability in the kinematics of landing maneuvers, making it difficult to identify the general rules that govern this behavior. Many previous studies have relied on tethered preparations to study landing behaviors, but tethering constrains some behavioral modules to operate in an open feedback control loop while others remain in closed-loop, thereby inducing experimental artefacts. On the other hand, freely flying insects are hard to precisely control, which may also increase behavioral variability. One approach towards understanding the general rules underlying landing behavior is to determine the common elements of landing kinematics on surfaces that are oriented in different ways. We conducted a series of experiments in which the houseflies, Musca Domestica, were lured to specific visual targets on either vertical or inverted horizontal substrates. These conditions elicited landing behaviors in the flies that could be captured accurately using multiple high-speed video cameras. We filmed the houseflies landing on surfaces oriented along two directions: vertical (vertical landings), and upside down (inverted landings). Our experiments reveal that flies that are able to land feet-first in a controlled manner must satisfy specific criteria, failing which their landing performance is compromised causing their heads to bump into the surface during landing. Flies landing smoothly on both surfaces initiate deceleration at approximately fixed distances from the substrate and in direct proportion to the component of flight velocity normal to the landing surface. The ratio of perpendicular distance to the substrate and velocity at the onset of deceleration was conserved, despite the large differences in the mechanics of the vertical vs. inverted landings. Flies extend their legs independently of distance from the landing surface or their approach velocity normal to the surface, regardless of the orientation of the landing substrate. Together, these results show that the visual initiation of deceleration is robust to orientation of the landing surface, whereas the initiation of leg-extension may be context-dependent and variable which allows flies to land on substrates of various orientations in a versatile manner. These findings may also be of interest to roboticists that are interested in developing flapping robots that can land on surfaces of different orientations.