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.

Distributions of neonicotinoid insecticides in the Commonwealth of Massachusetts: a temporal and spatial variation analysis for pollen and honey samples

“…Adult worker bees exposed to imidacloprid, clothianidin or thiamethoxam at levels as low as 0.02 ppb would have difficulty performing normal foraging activities. [18][19][20][21][22][23][24] Sub-lethal exposure to acetamiprid, imidacloprid, clothianidin, dinotefuran, fipronil, thiacloprid or thiamethoxam could lead to developmental impairments, including poor colony growth at levels of 2-5 ppb, [25,26] olfactory learning at levels as low as 0.1 mg bee À1 of acetamiprid, [18,[27][28][29] behavioural and cognition-neurological learning at a level of 0.45 ng bee -1 [30][31][32][33] and increasing susceptibility to pathogens at levels of 0.7 ppb of imidacloprid and 0.1 mg kg À1 of thiacloprid. [34][35][36][37] There are several limitations associated with this study.…”

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

“…They found that long-term memory, but not short-term or larval survival, was affected by the treatment. Also using Apis cerana in an earlier study, these authors found that trained exposed bees foraged less and had a lower avoidance of predators (i.e., Asian hornet Vespa velutina) (Tan et al 2014). Wright et al (2015) used a choice assay with imidacloprid and thiamethoxam influencing olfactory memory.…”

A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults

“…Some studies suggest that xenobiotics can be harmful to A. cerana cognitive processes. Apis cerana foragers feeding on sugar solution with imidacloprid at 40 μg/L (<0.52 ng/bee) had impaired decision-making and did not avoid nectar with a dangerous hornet predator, unlike controls31. Flumethrin, a pyrethroid commonly used to kill Varroa mites in honey bee colonies, interferes with A. cerana olfactory learning40.…”