Sensitivity of Buff-Tailed Bumblebee (Bombus terrestris L.) to Insecticides with Different Mode of Action

Abstract

Systemic insecticides are recognized as one of the drivers of the worldwide bee decline as they are exposed to them through multiple pathways. Specifically, neonicotinoids, some of which are banned for outdoor use in the European Union (EU), have been pointed out as a major cause of bee collapse. Thus, farmers have had to look for alternatives for pest control and use known insecticides or new substances reportedly less harmful to bees. We evaluated the oral acute toxicity of six insecticides (three of them systemic: imidacloprid, thiacloprid and sulfoxaflor) with four different modes of action on buff-tailed bumblebee workers (Bombus terrestris): two banned neonicotinoids (imidacloprid, thiacloprid), two pyrethroids (deltamethrin, esfenvalerate), one sulfoximine (sulfoxaflor) and a microbial insecticide based on Bacillus thuringiensis toxins, present in genetically modified (Bt) maize. The microbial insecticide only caused mortality to bumblebee workers at extremely high concentrations, so it is expected that Bt maize does not pose a risk to them. The toxicity of the other five insecticides on bumblebees was, from highest to lowest: imidacloprid, sulfoxaflor, deltamethrin, esfenvalerate and thiacloprid. This outcome suggests that certain insecticides in use are more toxic to B. terrestris than some banned neonicotinoids. Further chronic toxicity studies, under realistic conditions, are necessary for a proper risk assessment.

Keywords: Bacillus thuringiensis; Cry1Ab; acute toxicity; bioassays; commercial hives; deltamethrin; esfenvalerate; imidacloprid; neonicotinoids; pollinators; pyrethroids; sulfoxaflor; thiacloprid.

Figure 1

Correlation between the weight of B. terrestris workers fed with untreated artificial nectar and the amount of food consumed.

Figure 2

Average daily consumption per bee of artificial nectar treated with different concentrations of the insecticides imidacloprid (a), thiacloprid (b), deltamethrin (c), esfenvalerate (d), sulfoxaflor (e) and B. thuringiensis (f). Values expressed in mg of nectar consumed/bee/day. Average values of untreated nectar consumed daily by control bees in each bioassay are: 153.1 ± 20.3 (imidacloprid), 234.7 ± 44.3 (thiacloprid), 466.8 ± 31.5 (deltamethrin), 204.9 ± 13.9 (esfenvalerate), 177.6 ± 15.5 (sulfoxaflor) and 225.1 ± 17.3 (B. thuringiensis).

Figure 3

Kaplan–Meier survival analyses for B. terrestris workers when they were exposed for 48 h to different concentrations of the insecticides imidacloprid, thiacloprid, deltamethrin, esfenvalerate, sulfoxaflor and B. thuringiensis. Concentrations are represented by different colors and are expressed in ppm (W/V). The probability of survival (%) is defined as the probability that an individual survives longer than time “t”.