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

Abstract

SUMMARY 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.

Flexible responses to visual and olfactory stimuli by foragingManduca sexta: larval nutrition affects adult behaviour

“…On the other hand, M. sexta has consistently shown more significant responses to visual targets when olfactory stimuli were also provided (Raguso & Willis 2002;Goyret et al 2007;Riffell et al 2008). Here, the combined results from our behavioural experiments and spectroradiometric measurements support the hypothesis that naive M. sexta has difficulty recognizing an odourless visual target as a nectar source when their vision is impaired by suboptimal b-carotene intake during their larval stages.…”

“…Our previous studies using naive M. sexta (reared on standard diet) showed that floral odours can elicit both upwind odour plume tracking and visually guided flower searching (Goyret et al 2007). When olfactory stimulation was spatially or temporally decoupled from the visual target (i.e.…”

Context- and scale-dependent effects of floral CO 2 on nectar foraging by Manduca sexta

“…3). For these hawkmoths, responses to floral CO 2 clearly depend on the sex of the moth and the conditions under which it perceives this stimulus; non-host-plant floral odors attract both sexes of M. sexta in the absence of CO 2 (44). The contextdependent responses of female moths to the combined stimulus of host-plant odor and CO 2 are conflated with nonappetitive behaviors likely to be associated with oviposition, as discussed above.…”

“…(42,43) and floral approach is elicited by olfactory and/or visual stimuli (43) that are most effective when combined (44), after which probing is guided by visual and tactile inputs (7). Upon closer inspection, these behavioral ''rules'' are somewhat flexible, depending on the spatial and temporal scale (44) and the context in which specific stimuli are perceived [e.g., after appetitive conditioning (45,46)]. With this framework in mind, we explored how CO 2 might interact with other floral stimuli in behavioral assays with M. sexta.…”

“…Here, synergism is broadly defined as a nonadditive (ϩ or Ϫ) interaction with odor, as indicated by the two-headed arrow within the bar. The potential for strict synergism, in which only the combination of odor and CO 2 elicits the appropriate behavior, has already been falsified for tracking, floral approach, and probing in previous experiments (7,43,44 Experiment 3. In this experiment, 95% of the males and 85% of the females that were tested flew and probed at the experimental flowers.…”