The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta

Within an appetitive context, Manduca sexta, a nectivorous nocturnal hawkmoth, can be attracted by a range of stimuli including floral volatiles and visual display, carbon dioxide and water vapor. Several studies on this and other flower-visiting insects have shown how olfactory and visual stimulation play (or do not play) a role in attraction and feeding. Nevertheless, these studies have consistently manipulated stimuli in a 'presence-absence' manner. Here, we experimentally decoupled the presentation of both stimuli spatially and temporally in a wind tunnel, rather than entirely eliminating either one, and found that the decision-making process based on these stimuli is more flexible and complex than previously asserted. Manduca sexta was most responsive when both cues were present and emanated from the same source. When stimuli were spatially separated, responsiveness levels were comparable to those elicited by a single stimulus. However, transient olfactory stimulation either before or after visually guided approach (temporal decoupling) enhanced responsiveness to an odorless visual target. Additionally, searching times were increased by either a transient olfactory stimulation before take-off or by having the flower model spatially separated from the odor source tracked by the moths. Finally, in a dual-choice experiment, moths showed a strong bias for the visual display over the odor plume, suggesting the former to be the ultimate indicator of a nectar source. Our manipulation of floral cues shows that the feeding behavior of M. sexta, and probably of other nectivorous insects, is based not only on the sensory stimulation per se but also on the temporal and spatial pattern in which these stimuli are perceived.