Active sensing in bees through antennal movements is independent of odor molecule

Abstract

When sampling odors, many insects are moving their antennae in a complex but repeatable fashion. Previous works with bees have tracked antennal movements in only two dimensions, with a low sampling rate and with relatively few odorants. A detailed characterization of the multimodal antennal movement patterns as function of olfactory stimuli is thus wanting. The aim of this study is to test for a relationship between the scanning movements and the properties of the odor molecule. We tracked several key locations on the antennae of 21 bumblebees at high frequency (up to 1200 fps) and in three dimensions while submitting them to puffs of 11 common odorants released in a low-speed continuous flow. To cover the range of diffusivity and molecule size of most odors sampled by bees, compounds as different as butanol and farnesene were chosen, with variations of 200% in molar masses. Water and paraffin were used as negative controls. Movement analysis was done on the tip, the scape and the base of the antennae tracked with the neural network Deeplabcut. Bees use a stereotypical motion of their antennae when smelling odors, similar across all bees, independently of the identity of the odors and hence their diffusivity. The variability in the movement amplitude among odors is as large as between individuals. The first oscillation mode at low frequencies and large amplitude (ca. 1-3 Hz, ca. 100{degrees}) is triggered by the presence of an odor and is in line with previous work, as is the speed of movement. The second oscillation mode at higher frequencies and smaller amplitude (40 Hz, ca. 0.1{degrees}) is constantly present. Antennae are quickly deployed when a stimulus is perceived, decorrelate their movement trajectories rapidly and oscillate vertically with a large amplitude and laterally with a smaller one. The cone of air space thus sampled was identified through the 3D understanding of the motion patterns. The amplitude and speed of antennal scanning movements seem to be function of the internal state of the animal, rather than determined by the odorant. Still, bees display an active olfaction strategy. First, they deploy their antennae when perceiving an odor rather than let them passively encounter it. Second, fast vertical scanning movements further increase the flow speed experienced by an antenna and hence the odorant capture rate. Finally, lateral movements might enhance the likelihood to locate the source of odor, similarly to the lateral scanning movement of insects at odor plume boundaries. Definitive proofs of this function will require the simultaneous 3D recordings of antennal movements with both the air flow and odor fields.