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

Abstract

Accepted 6 September 2011 SUMMARY 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.

Dynamic use of optic flow during pheromone tracking by the male silkmoth, Bombyx mori

“…Several studies have demonstrated the necessity for visual cues while localising an odour source (Frye et al, 2003;Willis et al, 2011) and have suggested an interaction between visual and olfactory pathways (Stewart et al, 2010). Our results show that silkmoths used visual feedback for course compensation during surge behaviour, which supports the idea that visual information is required during pheromone-source localisation.…”

“…Studies in the fruit fly and the flying moth have demonstrated that olfactory information as well as visual information play a crucial role during odour searching by providing information about self-motion in space via visual feedback (Frye et al, 2003;Willis et al, 2011). In addition, attractive odour can modulate visual control of flight in the RESEARCH ARTICLE 1 Graduate School of Information Science and Technology, University of Tokyo, Tokyo 113-8654, Japan.…”

Olfactory searches with limited space perception

“…Insects can direct themselves over large distances (19)(20)(21)(22) and find sources of pheromone (23)(24)(25)(26)(27)(28) or food from the rare cues transported by wind-induced turbulent flow (29,30). There is great variability in the search capacities of different insects depending on the typical distances they have to travel, the physical and ecological characteristics of their environments, the amount of information they can extract from visual cues, the need to go back to a nest, and so on.…”

“…It seems unlikely, although not impossible (31,32), that (some) insects have access to space perception similar to that of rodents (33). Hence, when butterflies or other insects navigate among pheromone plumes (23)(24)(25)(26)(27)(28), they can perform the search without full access to their positions with respect to their environments. However, they can find their mates or specific vegetal compounds without advanced space perception.…”

One antenna, two antennae, big antennae, small: total antennae length, not bilateral symmetry, predicts odor tracking performance in the American cockroach, Periplaneta americana L

“…step counting) (Buehlmann et al, 2012;Collett and Collett, 2000;Wittlinger et al, 2006). Previous work by our lab has demonstrated that P. americana successfully track an odor plume with their eyes (both compound eyes and ocelli) covered with black paint (Willis et al, 2011), suggesting that a visually guided temporal search strategy is not being used by these cockroaches. Antennal movement information could be gained through processes like proprioceptive feedback or efference copies.…”