Chronic exposure to imidacloprid or thiamethoxam neonicotinoid causes oxidative damages and alters carotenoid-retinoid levels in caged honey bees (Apis mellifera)

Abstract

Over the last decade, the persistent dwindling of the populations of honey bees has become a growing concern. While this phenomenon is partly attributed to neonicotinoids (NEOCs), chronic exposures to these insecticides at environmentally-relevant concentrations are needed to fully estimate their implications. In this study, honey bees were orally exposed for 10 days to low field-realistic concentrations of NEOCs known for their effects on the cholinergic system (imidacloprid - IMI or thiamethoxam - THM). Selected biomarkers were measured such as acetylcholinesterase (AChE) activity, lipid peroxidation (LPO), α-tocopherol as well as several forms of vitamin A (retinoids) and carotenoids. Bees exposed to IMI showed lower levels of two carotenoids (α-carotene and α-cryptoxanthin) and α-tocopherol. The THM exposure increased the oxidized vitamin A metabolites in bees conjointly with the LPO. These results could be the consequence of a pro-oxidant effect of NEOCs and were observed at levels where no effects were recorded for AChE activity. This study reveals that exposure to low levels of NEOCs alters the carotenoid-retinoid system in honey bees. This would merit further investigation as these compounds are important in various aspects of bees' health. Overall, this study contributes to the development of biomonitoring tools for the health of bees and other pollinators.

Figure 1

Overview of carotenoid-retinoid metabolism. The name of the proteins mediating the different steps in vertebrates are in grey roman letter while their equivalents in insects, when known, are in grey italics. (A) NPC1L1 (Niemann–Pick C1-like 1)/NinaD (Neither inactivation nor afterpotential D); (B) CMO1 (Carotenoid mono-oxygenase 1)/NinaB (Neither inactivation nor afterpotential B); (C) RALDH (Retinal dehydrogenase) or ALDH (Aldehyde dehydrogenase); (D) Rrd (Retinal reductase/SDRs (Short chain dehydrogenases/reductases); (E) Rdh (Retinol dehydrogenase); (F) LRAT (Lecithin retinol acyltransferase) or ARAT (Acyl CoA:retinol acyltransferase; (G) REH (Retinyl ester hydrolase); (H) CYP26 (Cytochrome P450 26).

Figure 2

TBARS measured in honeybees exposed to increasing concentrations of IMI (A) and THM (B). Boxes (8 pools of 10 bees) extend from 25th to 75th percentile; line is the median and whiskers show the largest to smallest observed values. Δp < 0.05 Jonkheere-Terpstra trend test.

Figure 3

Retinoid contents (13/9-cis-RA, ROL and RALD) in honeybees exposed to increasing concentrations of IMI (A) and THM (B). Boxes (6–8 pools of 10 bees) extend from 25th to 75th percentile; line is the median and whiskers show the largest to smallest observed values. *p < 0.05 GLM one-way analysis of variance followed by Dunnett t test. ^#p < 0.1 Kruskal–Wallis one-way analysis of variance followed by Dunn’s test.

Figure 4

Retinoid contents (sum of 13-cis-4-oxo and all-trans-4-oxo-RA) in honeybees exposed to increasing concentrations of IMI (A) and THM (B). Boxes (5–8 pools of 10 bees, except 4 pools for 12 ng/100 ml) extend from 25th to 75th percentile; line is the median and whiskers show the largest to smallest observed values. ^Δp < 0.05 Jonkheere-Terpstra trend test.