title: Caffeinated forage tricks honeybees into increasing foraging and recruitment behaviors.
abstract: In pollination, plants provide food reward to pollinators who in turn enhance plant reproduction by transferring pollen, making the relationship largely cooperative; however, because the interests of plants and pollinators do not always align, there exists the potential for conflict, where it may benefit both to cheat the other [1, 2]. Plants may even resort to chemistry: caffeine, a naturally occurring, bitter-tasting, pharmacologically active secondary compound whose main purpose is to detract herbivores, is also found in lower concentrations in the nectar of some plants, even though nectar, unlike leaves, is made to be consumed by pollinators. [corrected]. A recent laboratory study showed that caffeine may lead to efficient and effective foraging by aiding honeybee memory of a learned olfactory association [4], suggesting that caffeine may enhance bee reward perception. However, without field data, the wider ecological significance of caffeinated nectar remains difficult to interpret. Here we demonstrate in the field that caffeine generates significant individual- and colony-level effects in free-flying worker honeybees. Compared to a control, a sucrose solution with field-realistic doses of caffeine caused honeybees to significantly increase their foraging frequency, waggle dancing probability and frequency, and persistency and specificity to the forage location, resulting in a quadrupling of colony-level recruitment. An agent-based model also demonstrates how caffeine-enhanced foraging may reduce honey storage. Overall, caffeine causes bees to overestimate forage quality, tempting the colony into sub-optimal foraging strategies, which makes the relationship between pollinator and plant less mutualistic and more exploitative. VIDEO ABSTRACT.
authors.affiliation: Laboratory of Apiculture and Social Insects (LASI), School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK. Electronic address: maggiejanec@gmail.com.
authors.forename: Margaret J
authors.initials: MJ
authors.lastname: Couvillon
authors.affiliation: Laboratory of Apiculture and Social Insects (LASI), School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK.
authors.forename: Hasan
authors.initials: H
authors.lastname: Al Toufailia
authors.affiliation: School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK.
authors.forename: Thomas M
authors.initials: TM
authors.lastname: Butterfield
authors.affiliation: Laboratory of Apiculture and Social Insects (LASI), School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK.
authors.forename: Felix
authors.initials: F
authors.lastname: Schrell
authors.affiliation: Laboratory of Apiculture and Social Insects (LASI), School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK.
authors.forename: Francis L W
authors.initials: FLW
authors.lastname: Ratnieks
authors.affiliation: Laboratory of Apiculture and Social Insects (LASI), School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK; Clinical Trials Unit (CTU), University of Bern, 3012 Bern, Switzerland.
authors.forename: Roger
authors.initials: R
authors.lastname: Schürch
mesh_terms: D000818:Animals; D001245:Association Learning / Q000187:drug effects; D001516:Bees / Q000187:drug effects*; D002110:Caffeine / Q000494:pharmacology*; D003214:Conditioning, Classical / Q000187:drug effects; D005247:Feeding Behavior / Q000187:drug effects*; D057048:Plant Nectar; D011058:Pollen; D054817:Pollination; D012201:Reward
chemical_list: D057048:Plant Nectar; D002110:Caffeine