Bumblebees learn to use peripheral taste to predict the presence of nectar in flowers

Learning cues such as tastes associated with palatable food is an important mechanism animals have for foraging optimally. Insects can use gustatory receptor neurons (GRNs) in their mouthparts to detect nutrients and toxins, but they also taste compounds using sensilla on peripheral organs such as their antennae. Bees are adept at learning to associate floral traits with the presence of nectar rewards, but few studies have examined how they incorporate gustatory information from their antennae with rewards. Here, we characterize the ability of adult worker bumblebees (Bombus terrestris) to taste sugar, salt, and bitter compounds using their antennae and then tested whether they could use this sensory information to associate it with food. We show that bumblebees have antennal GRNs sensitive to sugars, salts, and bitter compounds and that they can use surface chemistry differences detected by their periphery to learn about the presence or absence of flower rewards in a free-flight assay. Naive bumblebees showed no instinctual preferences toward or against any surface chemistry tested. Bumblebees performed best when sucrose surface cues were associated with sucrose reward, but they could learn to associate any cue with the presence or absence of sucrose solution. Interestingly, the bees found it more difficult to associate quinine surface chemistry with the presence of reward than its absence. These results indicate that bees have the potential to learn to associate another floral trait - chemicals on the surfaces of petals - with the quality of floral rewards. Summary statementBehavioural experiments and electrophysiological recordings show bumblebees can detect peripheral taste cues on surfaces of artificial flowers, including bitter toxins, and learn to use these to predict rewards.