Spatial partitioning of floral volatiles provides a “chemosensory roadmap” for bumblebee pollinators

How do plants with structurally complex flowers promote effective pollination? From the pollinator's perspective, complex flowers can be reimagined as mechanical puzzles that require the manipulation of a 3D object in search of a concealed reward.1 The spatial partitioning of volatile organic compounds (VOCs) within flowers may help flower-naive pollinators to successfully complete such puzzles, thereby increasing their foraging proficiency and, from the plant's perspective, promoting flower constancy and pollination efficiency.2,3 Here, we construct "chemosensory roadmaps" for Impatiens capensis and I. pallida, two North American plants pollinated by Bombus impatiens bumblebees. Although many VOCs are known to elicit olfactory responses,4 the presence of unique compounds in floral nectar,5 coupled with reports of inexperienced bees probing different flower parts as they learn how to manipulate flowers,6 suggest that VOCs might also elicit gustatory responses. Accordingly, we found that bumblebees showed no differential responses to VOCs when encountered as odorants but showed highly differential responses to the same VOCs when ingested with sugar rewards. VOCs present in nectar had agreeable flavors, whereas VOCs of other floral tissues such as nectar spurs were avoided. These findings suggest that VOC partitioning in Impatiens functions as a gustatory preference gradient that encourages legitimate pollination and potentially discourages nectar robbing by bumblebee visitors. Our findings highlight the non-olfactory functions of floral VOCs as flavors or contact chemical stimuli and their potential to structure plant-pollinator networks and filter their interactions with other organisms, including larcenists and other non-pollinating visitors.