Abstract

BackgroundCombinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear.Methodology/Principal FindingsUsing M. sexta and the floral traits of two important nectar resources in southwestern USA, Datura wrightii and Agave palmeri, we examined the relative importance of olfactory and visual signals. Natural visual and olfactory cues from D. wrightii and A. palmeri flowers permits testing the cues at their native intensities and composition – a contrast to many studies that have used artificial stimuli (essential oils, single odorants) that are less ecologically relevant. Results from a series of two-choice assays where the olfactory and visual floral displays were manipulated showed that naïve hawkmoths preferred flowers displaying both olfactory and visual cues. Furthermore, experiments using A. palmeri flowers – a species that is not very attractive to hawkmoths – showed that the visual and olfactory displays did not have synergistic effects. The combination of olfactory and visual display of D. wrightii, however – a flower that is highly attractive to naïve hawkmoths – did influence the time moths spent feeding from the flowers. The importance of the olfactory and visual signals were further demonstrated in learning experiments in which experienced moths, when exposed to uncoupled floral displays, ultimately chose flowers based on the previously experienced olfactory, and not visual, signals. These moths, however, had significantly longer decision times than moths exposed to coupled floral displays.Conclusions/SignificanceThese results highlight the importance of specific sensory modalities for foraging hawkmoths while also suggesting that they learn the floral displays as combinatorial signals and use the integrated floral traits from their memory traces to mediate future foraging decisions.

Highlights

  • Multimodal signals – where the signaler uses two or more signals that operate on different modalities of the ‘receiver’ – have been shown to mediate a variety of critical ecological and evolutionary processes, including sexual selection and mate choice, predator-prey interactions [3], and plantpollinator interactions [4,5,6]

  • Individual moths were tested in a suite of assays examining the relative importance of visual and olfactory cues using combinations of the odors from the two flower species, D. wrightii and A. palmeri, and visual stimuli including conical paper flowers – that serve as an attractive visual stimulus while controlling for morphological and tactile differences between flower species, and bagged flowers

  • M. sexta moths have been shown to elicit feeding responses when presented with a visual stimulus [34], but moths are strongly attracted to stimuli that display both visual and olfactory cues [18]

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Summary

Introduction

Multimodal signals – where the signaler uses two or more signals that operate on different modalities of the ‘receiver’ – have been shown to mediate a variety of critical ecological and evolutionary processes, including sexual selection and mate choice (reviewed by [1,2]), predator-prey interactions [3], and plantpollinator interactions [4,5,6]. Pollinator attraction to a certain floral trait, or combination of traits, will operate as a strong selective pressure on the plant species. Night-blooming plants adapted to hawkmoth pollination show a convergence of common floral features (e.g., fragrant nocturnal scent emissions, highly reflective corollas) [20]. The commonality of these floral features makes night blooming plants excellent models in which to examine plantpollinator interactions and the behavioral effects of floral traits. Combinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear

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