A neonicotinoid pesticide impairs foraging, but not learning, in free-flying bumblebees

Abstract

Neonicotinoids are widely-used pesticides implicated in the decline of bees, known to have sub-lethal effects on bees’ foraging and colony performance. One proposed mechanism for these negative effects is impairment to bees’ ability to learn floral associations. However, the effects of neonicotinoids on learning performance have largely been addressed using a single protocol, where immobilized bees learn an association based on a single sensory modality. We thus have an incomplete understanding of how these pesticides affect bee learning in more naturalistic foraging scenarios. We carried out the first free-foraging study into the effects of acute exposure of a neonicotinoid (imidacloprid) on bumblebees’ (Bombus impatiens) ability to learn associations with visual stimuli. We uncovered dose-dependent detrimental effects on motivation to initiate foraging, amount of nectar collected, and initiation of subsequent foraging bouts. However, we did not find any impairment to bees’ ability to learn visual associations. While not precluding the possibility that other forms of learning are impaired, our findings suggest that some of the major effects of acute neonicotinoid exposure on foraging performance may be due to motivational and/or sensory impairments. In light of these findings, we discuss more broadly how pesticide effects on pollinator cognition might be studied.

The neonicotinoid insecticide imidacloprid disrupts bumblebee foraging rhythms and sleep

“…We found that imidacloprid exposure also reduced the foraging activity of foragers within the colony, with individuals making fewer foraging trips in LD conditions. This is consistent with previous, field-based studies showing that exposure to imidacloprid under field conditions decreased the number of foraging trips carried out by foragers [42,43], and neonicotinoids reduced the quantity of sucrose and pollen collected by Bombus terrestris colonies [44]. This could in part be driven by reduced foraging motivation caused by the apparent appetite suppression that imidacloprid can cause, with 10 µg/L shown to decrease feeding by 30% in Bombus terrestris [13].…”

“…time-givers or entrainment signals) such as light or social cues [48,49]. This may imply that the reduction in foraging rhythmicity observed for bumblebee colonies exposed to imidacloprid in the lab are likely to reflect deleterious consequences in the field, as is the case for reductions in foraging activity [42,43]. A disruption to the clock in foragers may further reduce their foraging efficiency as they will not be able to form the time-memories required to accurately visit different flowers [5,50].…”

“…Neonicotinoids reduce activity and foraging motivation in pollinators [43], in addition continued exposure causes bees to prefer neonicotinoid-laced food sources [58,59], further exacerbating their negative impact. Here we demonstrate that very low field relevant concentrations of neonicotinoids disrupt rhythmicity of foraging activity as well as increasing daytime sleep, further reducing the opportunities for bees to forage and pollinate and having knock-on effects on circadian and sleep regulated physiological and behavioural processes in the bee.…”

Declines in insect abundance and diversity: We know enough to act now

“…For example, negative nontarget effects of pesticides are apparent on pollinator populations (Frampton & Dorne, 2007), even as the behavioral consequences of sublethal insecticide exposure on bee foraging are an area of active research (Muth & Leonard, 2019). For example, negative nontarget effects of pesticides are apparent on pollinator populations (Frampton & Dorne, 2007), even as the behavioral consequences of sublethal insecticide exposure on bee foraging are an area of active research (Muth & Leonard, 2019).…”

“…The associations that have been documented between stressors and insect responses point to causal relationships even though our knowledge of the mechanisms that underlie them are imperfect. For example, negative nontarget effects of pesticides are apparent on pollinator populations (Frampton & Dorne, 2007), even as the behavioral consequences of sublethal insecticide exposure on bee foraging are an area of active research (Muth & Leonard, 2019). As a consequence of imperfect knowledge, we cannot always say which stressors or interactions among stressors are more or less important in a given area or for any one species.…”