Low doses of neonicotinoid pesticides in food rewards impair short-term olfactory memory in foraging-age honeybees

Abstract

Neonicotinoids are often applied as systemic seed treatments to crops and have reported negative impact on pollinators when they appear in floral nectar and pollen. Recently, we found that bees in a two-choice assay prefer to consume solutions containing field-relevant doses of the neonicotinoid pesticides, imidacloprid (IMD) and thiamethoxam (TMX), to sucrose alone. This suggests that neonicotinoids enhance the rewarding properties of sucrose and that low, acute doses could improve learning and memory in bees. To test this, we trained foraging-age honeybees to learn to associate floral scent with a reward containing nectar-relevant concentrations of IMD and TMX and tested their short (STM) and long-term (LTM) olfactory memories. Contrary to our predictions, we found that none of the solutions enhanced the rate of olfactory learning and some of them impaired it. In particular, the effect of 10 nM IMD was observed by the second conditioning trial and persisted 24 h later. In most other groups, exposure to IMD and TMX affected STM but not LTM. Our data show that negative impacts of low doses of IMD and TMX do not require long-term exposure and suggest that impacts of neonicotinoids on olfaction are greater than their effects on rewarding memories.

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

“…Both neonicotinoid insecticides and parasites alter associative learning and cognitive functions of bees [5][6][7][8][9]. Acting as nicotinic acetylcholine receptor (nAChR) agonists [10], exposure to very low levels of neonicotinoids can disrupt normal function of neurons in the bee brain [11,12] and lead to disruptions in learning and memory [8,13].…”

“…[8,9,24,25] whereas potential impacts on other pollinators such as bumblebees are as yet poorly known [13,26]. In addition to honeybees, bumblebees play a major role in providing pollinating services to wild and crop plants [27].…”

Neonicotinoid-induced impairment of odour coding in the honeybee

“…Various modifications in honeybee behaviour, which seem to be associated with cognitive impairment, have been described. General motion56, waggle dancing7, homing flights8910, and olfactory learning and memory11121314 were shown to be disrupted by chronic and acute treatment with various neonicotinoids at doses comparable to those experienced by animals in the field.…”

“…Imidacloprid has been shown to impair olfactory learning and memory in a number of studies111314232425. As revealed by in vivo electrophysiological recordings, imidacloprid application produces a tonic inward current in Kenyon cells of the MBs, making them unresponsive to acetylcholine.…”

Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death

“…In another study, evidence for clear impacts on learning and memory were observed upon exposure of honey bees to dietary imidacloprid resulting in a dose of 1.2 ng/bee (estimates based on consumption rates) using the PER assay (Williamson and Wright, 2013). Similarly, honey bees that were fed sucrose solution containing 10 nM imidacloprid or 1 nM thiamethoxam exhibited impaired olfactory learning and short-term memory, as evaluated using the PER (Wright et al, 2015).…”