Bee positive: the importance of electroreception in pollinator cognitive ecology

Abstract

The global atmospheric circuit generates a permanent electric field between the Earth surface and outer atmosphere (Rycroft et al., 2000). The ground and plants conductively linked to it are negatively charged (Bowker and Crenshaw, 2007), whereas animals build up positive charge as they move in contact with air molecules (Jackson and McGonigle, 2005). Electric fields emanating from plants and pollinators, such as bees, are believed to promote pollination by enabling pollen grains to jump from flowers to pol-linators and vice versa (Corbet et al., 1982). Two recent studies reveal that bees not only detect these electric fields but also learn to discriminate them, indicating that electroreception should be seriously considered alongside vision and olfaction when studying bee behavior and ecology. Writing in Science, Clarke et al. (2013) demonstrated that bumblebees (Bombus terrestris) detect electric fields around plants and learn to use them to decide whether or not to visit flowers. Using a Faraday pail to measure electric fields generated by bees and plants, the team described how a bee visit temporarily modifies the electric charge of (Petunia) flowers, suggesting that floral electric properties could be used by future visitors to assess the reward value without necessarily needing to probe the flower. To explore this possibility, the authors used differential conditioning in which bees were trained to associate an electrically charged feeder (30 V) with a sucrose reward (CS+) and an uncharged feeder with an aversive quinine solution (CS−). After extensive training (50 trials), bees chose the rewarding feeder in around 80% of trials. Similar levels of performance were observed when bees were trained with two feeders carrying the same charge but different electric field patterns (homogeneous vs. bull's eye shape), indicating that these insects can learn both the magnitude and geometry of an electric field. Bees learned to perform even better in discrimination tasks if the two feeders differed both in color (shade of green) and their electric field pattern compared to if they differed only in color. Natural electric fields around flowers may therefore contribute to the multimodal sources of information that bees use to learn and memorize floral rewards, in conjunction with color, pattern, shape, texture,