Herbivory-induced changes in the olfactory and visual display of flowers and extrafloral nectaries affect pollinator behavior

Abstract

Plants communicate with animals by means of multimodal displays and reward mutualistic partners with resources such as nectar. Floral nectar is a key resource for pollinators, whereas extrafloral nectaries (EFNs) support indirect plant defense. Animal-pollinated flowers advertise their rewards using modalities such as scent, color and morphology. In EFNs the role of olfactory and visual traits is less well understood. Herbivory has been shown to induce changes in the multimodal display and in resource related characteristics of flowers and EFNs. This may consequently affect the behavior of nectar consumers such as pollinators that occasionally feed on extrafloral nectar in addition to floral nectar. We tested the effect of herbivory (simulated by jasmonic acid treatment) on olfactory, visual and resource related floral and EFN traits in Vicia faba, tracked alterations in bumblebee (Bombus terrestris) preference and evaluated potential outcomes for plant reproduction. In control plants, flowers and EFNs differed in olfactory and visual cues and also in nectar quantity and quality and pollinators clearly preferred to forage on flowers. After jasmonic acid treatment (JA), linalool emissions of EFNs increased in a large proportion of plants, the visual display of EFNs became more salient and nectar volumes increased. In flowers of JA-treated plants we found lower emissions of cinnamic aldehyde and lower sugar concentration in nectar, however visual cues were unaffected. Potentially because of these phenotypic changes bumblebees no longer preferred flowers over EFNs in JA-treated plants. Consequently, this may negatively affect reproductive success in V. faba, which is highly dependent on floral visitation for fruit set. Our study adds another aspect to the complexity of plant–pollinator interactions and reveals how herbivory may interfere with plant–pollinator communication. Our findings emphasize that the foraging behavior of pollinators not only depends on floral traits, but is affected by the whole plants’ multimodal phenotype.