Imidacloprid alters foraging and decreases bee avoidance of predators

Abstract

Concern is growing over the effects of neonicotinoid pesticides, which can impair honey bee cognition. We provide the first demonstration that sublethal concentrations of imidacloprid can harm honey bee decision-making about danger by significantly increasing the probability of a bee visiting a dangerous food source. Apis cerana is a native bee that is an important pollinator of agricultural crops and native plants in Asia. When foraging on nectar containing 40 µg/L (34 ppb) imidacloprid, honey bees (Apis cerana) showed no aversion to a feeder with a hornet predator, and 1.8 fold more bees chose the dangerous feeder as compared to control bees. Control bees exhibited significant predator avoidance. We also give the first evidence that foraging by A. cerana workers can be inhibited by sublethal concentrations of the pesticide, imidacloprid, which is widely used in Asia. Compared to bees collecting uncontaminated nectar, 23% fewer foragers returned to collect the nectar with 40 µg/L imidacloprid. Bees that did return respectively collected 46% and 63% less nectar containing 20 µg/L and 40 µg/L imidacloprid. These results suggest that the effects of neonicotinoids on honey bee decision-making and other advanced cognitive functions should be explored. Moreover, research should extend beyond the classic model, the European honey bee (A. mellifera), to other important bee species.

Figure 1. Effect of imidacloprid treatments on bee return rates and nectar collection (imbibing) volume.

a) The mean proportion of trained bees that returned to the test feeders with different imidacloprid treatments. b) The mean volume of 1.25 M sucrose solution collected by bees trained to a safe feeder with no hornet predators. Standard error bars are shown. Different letters indicate treatments that are significantly different from each other (Tukey HSD tests, P<0.05). The imidacloprid concentrations are given in commonly used units, with ppb and µg/Kg shown in the same row because the numeric values are identical. Different shades of gray correspond to different imidacloprid concentrations. Sample sizes are given in the Methods.

Figure 2. Mean proportion of choices for the safe feeder over five trials.

The different treatments are identified above each plot (1 = all choices for safe feeder). Different shades of gray correspond to different imidacloprid concentrations. Standard error bars are shown.

Figure 3. The effect of imidacloprid on the percentage of bees choosing a safe over a dangerous feeder.

Stars above bars indicate treatments in which bees significantly avoided the dangerous feeder (P<0.05). Different shades of gray correspond to different imidacloprid concentrations. A dashed line shows the null hypothesis expectation: 50% of bees choose the safe feeder.