Caffeine in Floral Nectar Enhances a Pollinator's Memory of Reward

Abstract

Plant defence compounds occur in floral nectar, but their ecological role is not well-understood. We provide the first evidence that plant compounds pharmacologically alter pollinator behaviour by enhancing their memory of reward. Honeybees rewarded with caffeine, which occurs naturally in nectar of Coffea and Citrus species, were three times more likely to remember a learned floral scent than those rewarded with sucrose alone. Caffeine potentiated responses of mushroom body neurons involved in olfactory learning and memory by acting as an adenosine receptor antagonist. Caffeine concentrations in nectar never exceeded the bees' bitter taste threshold, implying that pollinators impose selection for nectar that is pharmacologically active but not repellent. By using a drug to enhance memories of reward, plants secure pollinator fidelity and improve reproductive success.Many drugs commonly consumed by humans are produced by plants as a form of toxic defence against herbivores (1, 2). While plant-derived drugs like caffeine or nicotine are lethal in high doses (3-5), they have pharmacological effects at low doses that affect mammalian behaviour. For example, low doses of caffeine are mildly rewarding and enhance cognitive performance and memory retention (6). Interestingly, caffeine has been detected in low doses in the floral nectar and pollen of Citrus (7), but whether it has an ecological function is unknown.Two caffeine-producing plant genera, Citrus and Coffea, have large floral displays with strong scents and produce more fruits and seeds when pollinated by bees (8, 9). If caffeine confers a selective advantage when these plants interact with pollinators, we might expect it to be commonly encountered in nectar. We measured caffeine in the nectar of 3 species of Coffea (C. canephora, C. arabica, and C. liberica) and 4 species of Citrus (C. paradisi, C. maxima, C. sinesis, C. reticulata) using liquid chromatography-mass spectrometry (10, Fig. Europe PMC Funders Group Europe PMC Funders Author ManuscriptsEurope PMC Funders Author Manuscripts S1A). When caffeine was present, its concentration ranged from 0.003 -0.253 mM. The median caffeine concentration in both genera was not significantly different (Fig. 1A, MannWhitney, Z = −1.09, P = 0.272). Caffeine was more common in the nectar of C. canephora than in C. arabica or C. liberica (Coffea: logistic regression χ 2 2 = 11.1, P = 0.004); it was always present in Citrus nectar. The mean total nectar sugar concentration ranged from 0.338-0.843 M (Fig. 1B, see Fig S1B for individual sugars). Caffeine concentration in nectar did not correlate with total sugar concentration (Pearson's r = 0.063, P = 0.596).We hypothesized that caffeine could affect the learning and memory of foraging pollinators.To test this, we trained individual honeybees to associate floral scent with 0.7 M sucrose and 7 different concentrations of caffeine and tested their olfactory memory. Using a method for classical conditioning of feeding responses (proboscis extension reflex, 11), bees...

Secondary metabolites in floral nectar reduce parasite infections in bumblebees

“…There are numerous reports of bees poisoned by secondary metabolites in nectar and pollen [6,10], and bees can incur reproductive costs when they consume these compounds [11]. However, limited evidence demonstrates that secondary metabolites can benefit bees, for example by enhancing memory and foraging efficiency [12], reducing parasite infection [13] and controlling pathogenic fungi [14]. The potential therefore exists for plant secondary metabolites to play an important role in mediating tritrophic interactions among plants, pollinators and parasites, but how costs and benefits of chemical consumption affect bee survival and reproduction remains relatively unexplored.…”

Convergent evolution of caffeine in plants by co-option of exapted ancestral enzymes

“…The phylogenetic distribution of caffeine, or xanthine alkaloids more generally, is highly sporadic and usually restricted to only a few species within a given genus (12,13). Caffeine accumulates in various tissues, where it may deter herbivory (14,15) or enhance pollinator memory (16). Numerous studies over the past 30 y have indicated that although several possible routes exist, the same canonical pathway to caffeine biosynthesis has evolved independently in Coffea (coffee) and Camellia (tea) involving three methylation reactions to sequentially convert xanthosine to 7-methylxanthine to theobromine to caffeine ( Fig.…”

Effects of Ibuprofen and Caffeine Concentrations on the Common Bed Bug (Cimex lectulatius L.) Feeding and Fecundity

“…When fed with increasing concentration of caffeine, bed bugs consumed significantly less (36%) blood and produced significantly fewer eggs, 64% between the control and the highest concentration (50 ppm) of caffeine in the blood. Wright et al [42] found that honey bees rewarded with naturally occurring caffeine from Coffea and Citrus species, were three times as likely to remember the floral scent as was honey bees rewarded with sucrose alone. It also improves the honey bees' long-term memory for flowers.…”