The flavonoid rutin protects the bumble bee Bombus impatiens against cognitive impairment by imidacloprid and fipronil

Abstract

The ongoing decline of bee populations and its impact on food security demands integrating multiple strategies. Sublethal impairments associated with exposure to insecticides, affecting the individual and the colony levels, have led to insecticide moratoria and bans. However, legislation alone is not sufficient and remains a temporary solution to an evolving market of insecticides. Here, we asked whether bees can be prophylactically protected against sublethal cognitive effects of two major neurotoxic insecticides, imidacloprid and fipronil, with different mechanisms of action. We evaluated the protective effect of the prophylactic administration of the flavonoid rutin, a secondary plant metabolite, present in nectar and pollen, and known for its neuroprotective properties. Following controlled or ad libitum administration of rutin, foragers of the North American bumble bee Bombus impatiens received oral administration of the insecticides at sublethal realistic dosages. Learning acquisition, memory retention and decision speed were evaluated using olfactory absolute conditioning of the proboscis extension response. We show that the insecticides primarily impair acquisition but not retention or speed of the conditioned proboscis extension response. We further show that the administration of the flavonoid rutin successfully protects the bees against impairments produced by acute and chronic administration of insecticides. Our results suggest a new avenue for the protection of bees against sublethal cognitive effects of insecticides.

Keywords: Bee decline; Flavonol; Neonicotinoid; Pollinator.

Fig. 1.

Controlled prophylactic administration of rutin protects learning and memory against acute exposure to imidacloprid. (A) Innocuous and protective effect against imidacloprid (Imid) of rutin (Rut) administration on learning. (B) Average latency of the conditioned proboscis extension response (PER) for bees that responded at least twice during training. (C) Acquisition curves for bees in all treatments. (D) Memory retention 28 h after exposure to imidacloprid and 40 h after the last administration of rutin. A, C and D include the same bees. Only statistically significant planned comparisons (see Materials and Methods) are indicated to facilitate visualization in A and D. Data are means±s.e.m. *P<0.05, **P<0.01, ***P<0.001.

Fig. 2.

Ad libitum prophylactic administration of rutin protects learning and memory against impairment by acute exposure to imidacloprid and fipronil. (A) Innocuous and fully protective effect against imidacloprid (Imid) and fipronil (Fip) of rutin (Rut) administration on learning. (B) Administration of insecticides did not significantly affect the latency of the conditioned PER. (C) Acquisition curves for bees in all treatments. (D) Innocuous and protective effect of rutin administration on memory retention 28 h after exposure to imidacloprid/fipronil and 40 h after the last administration of rutin. A, C and D include the same bees. Only statistically significant planned comparisons (see Materials and Methods) are indicated to facilitate visualization in A and D. Data are means±s.e.m. *P<0.05, ***P<0.001.

Fig. 3.

Ad libitum prophylactic administration of rutin protects learning and memory against impairment by chronic exposure to fipronil but not imidacloprid. (A) Innocuous and protective effect against imidacloprid (Imid) and fipronil (Fip) of rutin (Rut). (B) Effect of feeding treatments on the latency of the conditioned PER of bees that responded at least twice. (C) Acquisition curves for bees in all treatments. (D) Effect of rutin administration on memory retention 40 h after the last administration of rutin. A, C and D include the same bees. Only statistically significant planned comparisons (see Materials and Methods) are indicated to facilitate visualization. Data are means±s.e.m. *P<0.05, **P<0.01, ***P<0.001.