Odor source localization in complex visual environments by fruit flies

Abstract

Flying insects routinely forage in complex and cluttered sensory environments. Their search for a food or a pheromone source typically begins with a whiff of odor, which triggers a flight response, eventually bringing the insect in the vicinity of the odor source. The precise localization of an odor source, however, requires the use of both visual and olfactory modalities, aided by air currents that trap odor molecules into turbulent plumes, which the insects track. Here, we investigated odor tracking behavior in fruit flies (Drosophila melanogaster) presented with low- or high contrast visual landmarks, which were either paired with or separate from an attractive odor cue. These experiments were conducted either in a gentle air stream which generated odor plumes, or in still air in which odor dissipates uniformly in all directions. The trajectories of the flies revealed several novel features of their odor-tracking behavior in addition to those that have been previously documented (e.g. cast and-surge maneuvers). First, in both moving and still air, odor-seeking flies rely on the co-occurrence of visual landmarks with olfactory cues to guide them to putative odorant objects in the decisive phase before landing. Second, flies abruptly decelerate when they encounter an odor plume, and thereafter steer towards nearby visual objects that had no inherent salience in the absence of odor. This indicates that the interception of an attractive odor increases their salience to nearby high-contrast visual landmarks. Third, flies adopt distinct odor tracking strategies during flight in moving vs. still air. Whereas they weave in and out of plumes towards an odor source when airflow is present, their approach is more gradual and incremental in still air. Both strategies are robust and flexible, and can ensure that the flies reliably find the odor source under diverse visual and airflow environments. Our experiments also indicate the possibility of an olfactory 'working memory' that enables flies to continue their search even when the olfactory feedback is reduced or absent. Together, these results provide insights into how flies determine the precise location of an odor source.