Neonicotinoids and ectoparasitic mites synergistically impact honeybees

Abstract

The Western honeybee, Apis mellifera, is the most important managed pollinator globally and has recently experienced unsustainably high colony losses. Synergistic interactions among stressors are believed to be primarily responsible. However, despite clear evidence of strong effect on honeybee longevity of widely-employed neonicotinoid insecticides and of the ubiquitous ectoparasitic mite Varroa destructor, no data exist to show synergistic effects between these two stressors. Even though neonicotinoids had no significant impact by themselves, we here show for the first time a synergistic time-lag interaction between mites and neonicotinoids that resulted in significantly reduced survival of long-lived winter honeybees. Even though these mites are potent vectors of viruses, the virus-insecticide interaction had no significant impact. The data suggest a previously overlooked mechanism possibly explaining recent unsustainably high losses of managed A. mellifera honeybee colonies in many regions of the world. Future mitigation efforts should concentrate on developing sustainable agro-ecosystem management schemes that incorporate reduced use of neonicotinoids and sustainable solutions for V. destructor mites.

Figure 1

Proportion of honeybee (Apis mellifera) workers exposed to neonicotinoid insecticides and/or Varroa destructor and showing clinical symptoms of Deformed wing virus (DWV). Measurements of DWV clinical symptom levels for each of the four treatment groups were generated by uncapping worker brood cells and investigating wing anatomy for each individual. The level of DWV clinical symptoms was then calculated by dividing the total number of observed workers with symptoms by the total number of uncapped brood cells. The boxplots show the inter-quartile-range (box), the median (black line within box), and outliers (dots). A significant difference (generalized linear mixed model, P < 0.05) between groups is indicated by different letters (a, b).

Figure 2

Effects of neonicotinoid insecticides and Varroa destructor on honeybee (Apis mellifera) worker emergence mass and survival. To obtain a fully crossed experimental design, honeybee colonies were exposed to neonicotinoids (4 ppb thiamethoxam and 2 ppb clothianidin) and to natural V. destructor infestation. Measurements of emergence mass were performed in summer and autumn. For each of the four treatment groups generated, body mass (1A, 1C) of 1430 workers originating from ten colonies was measured 24 h prior expected emergence date. The boxplots show the inter-quartile-range (box), the median (black line within box), and outliers (dots). Survival of the workers (N = 1105) kept in cages in groups of 10 was measured until all individuals died. The Kaplan-Meier curves show the survival over time of the four treatment groups (solid lines) as well as the 95% confidence intervals (CI) (shaded areas). A significant difference (generalized linear mixed model, P < 0.05) between groups is indicated by different letters (a, b, c).

Figure 3

Seasonal effects of neonicotinoid insecticides and Varroa destructor on honeybee (Apis mellifera) worker emergence mass and survival. For each of the four treatment groups, body mass of 1425 workers originating from ten colonies was measured 24 h prior expected emergence date. The boxplots show the inter-quartile-range (box), the median (black line within box), and outliers (dots). Survival of the previously weighed workers (N = 1100) kept in cages in groups of 10 was measured until all individuals died. The Kaplan-Meier curves show the survival over time of the four treatment groups (solid lines) as well as the 95% CI (shaded areas). A significant difference (P < 0.05) between groups within the same cage assay is indicated by different letters (a, b).