The role of vision in odor-plume tracking by walking and flying insects.

The walking paths of male cockroaches, Periplaneta americana, tracking point-source plumes of female pheromone often appear similar in structure to those observed from flying male moths. Flying moths use visual-flow-field feedback of their movements to control steering and speed over the ground and to detect the wind speed and direction while tracking plumes of odors. Walking insects are also known to use flow field cues to steer their trajectories. Can the upwind steering we observe in plume-tracking walking male cockroaches be explained by visual-flow-field feedback, as in flying moths? To answer this question, we experimentally occluded the compound eyes and ocelli of virgin P. americana males, separately and in combination, and challenged them with different wind and odor environments in our laboratory wind tunnel. They were observed responding to: (1) still air and no odor, (2) wind and no odor, (3) a wind-borne point-source pheromone plume and (4) a wide pheromone plume in wind. If walking cockroaches require visual cues to control their steering with respect to their environment, we would expect their tracks to be less directed and more variable if they cannot see. Instead, we found few statistically significant differences among behaviors exhibited by intact control cockroaches or those with their eyes occluded, under any of our environmental conditions. Working towards our goal of a comprehensive understanding of chemo-orientation in insects, we then challenged flying and walking male moths to track pheromone plumes with and without visual feedback. Neither walking nor flying moths performed as well as walking cockroaches when there was no visual information available.

Effects of altering flow and odor information on plume tracking behavior in walking cockroaches, Periplaneta americana (L.).

Animals using odor plumes to locate resources are activated to track these plumes by the presence of an attractive odor, and typically steer toward the source using directional cues from the flowing air or water bearing the odor. We challenged freely walking virgin male cockroaches, Periplaneta americana, to track plumes of airborne female pheromone and then video-recorded and analyzed their responses as the odor plume and wind were independently manipulated. Plume tracking males that experienced the total loss of directional air flow halfway to the odor source showed little change in their performance, and 100% were able to quickly locate the pheromone source. By contrast, males experiencing a sudden loss of odor while tracking a plume rapidly changed their behavior; often turning downwind and retracing their steps to the release point, or walking in loops, but rarely moving upwind to the previous location of the source. In a subsequent experiment, in order to determine whether a memory of the previously experienced wind direction could provide the directional information necessary to locate an odor source, we challenged males to track plumes in zero wind after pre-exposing them to: (1) wind and pheromone, (2) wind only, and (3) neither wind nor pheromone. These were compared to males tracking a wind-borne pheromone plume, in which case, all males were able to locate the pheromone source. Our results show that males require the detection of wind and pheromone simultaneously during plume tracking in order to quickly and efficiently locate the odor source. These results are consistent with those reported from flying moths tracking wind-borne pheromone plumes, and suggest that the control system underlying this behavior requires ongoing simultaneous experience with wind and odor information during the performance of the behavior to operate efficiently.