Interaction between Varroa destructor and imidacloprid reduces flight capacity of honeybees

Abstract

Current high losses of honeybees seriously threaten crop pollination. Whereas parasite exposure is acknowledged as an important cause of these losses, the role of insecticides is controversial. Parasites and neonicotinoid insecticides reduce homing success of foragers (e.g. by reduced orientation), but it is unknown whether they negatively affect flight capacity. We investigated how exposing colonies to the parasitic mite Varroa destructor and the neonicotinoid insecticide imidacloprid affect flight capacity of foragers. Flight distance, time and speed of foragers were measured in flight mills to assess the relative and interactive effects of high V. destructor load and a field-realistic, chronic sub-lethal dose of imidacloprid. Foragers from colonies exposed to high levels of V. destructor flew shorter distances, with a larger effect when also exposed to imidacloprid. Bee body mass partly explained our results as bees were heavier when exposed to these stressors, possibly due to an earlier onset of foraging. Our findings contribute to understanding of interacting stressors that can explain colony losses. Reduced flight capacity decreases the food-collecting ability of honeybees and may hamper the use of precocious foraging as a coping mechanism during colony (nutritional) stress. Ineffective coping mechanisms may lead to destructive cascading effects and subsequent colony collapse.

Keywords: Apis mellifera; body mass; flight performance; pollination; wing dimensions.

Figure 1.

The direct and indirect relationships that were tested explaining flight distance of forager honeybees tethered on a flight mill. The arrow numbers refer to the models in table 1. For example, model 4 includes the effects of the treatments (Varroa destructor, imidacloprid and the interaction) and wing length on flight distance.

Figure 2.

(a) Mean flight distance, (b) mean flight time, (c) average flight speed and (d) maximum flight speed of honeybees tethered on a flight mill that were exposed to different levels of Varroa destructor infestation (V− refers to colonies that were treated against V. destructor, whereas the colonies V+ were not treated) and to different concentrations of a field-realistic, chronic sub-lethal dose of the neonicotinoid insecticide imidacloprid (I− refers to colonies with no exposure, whereas colonies I+ were exposed). Error bars indicate the standard error of the mean. The letters give the significant differences between groups based on linear mixed models (see statistics in table 1 and electronic supplementary material, table S1 in appendix S3). The asterisks in panels (a,b) indicate significant differences for the main effect V. destructor. (e–g) Mean (e) body mass and (f) wing length for the treatments (respectively, model 6 and model 7 in table 1), and (g) mean flight distance for the colonies that survived April of the next year and the colonies that did not survive. The asterisk indicates a significant difference (see text for statistics of this test).

Figure 3.

Mean flight speed per minute of honeybees in a flight mill that are exposed to one of the four treatments (V− refers to colonies that were treated against V. destructor, whereas the colonies V+ were not treated, I− refers to colonies with no exposure to a field-realistic, chronic sub-lethal dose of imidacloprid, whereas colonies I+ were exposed) after being fed (a) a 10 µl 1 M glucose solution or (b) a 10 µl 2 M glucose solution. Mean speed was calculated for every flying minute from all individual bees per treatments (indicated in the legend), including those bees that have stopped flying due to depletion of their reserves. Honeybees that stopped flying at a certain time were included for illustration purposes and were considered to have a speed of zero.