Neonicotinoid pesticides severely affect honey bee queens

Abstract

Queen health is crucial to colony survival of social bees. Recently, queen failure has been proposed to be a major driver of managed honey bee colony losses, yet few data exist concerning effects of environmental stressors on queens. Here we demonstrate for the first time that exposure to field-realistic concentrations of neonicotinoid pesticides during development can severely affect queens of western honey bees (Apis mellifera). In pesticide-exposed queens, reproductive anatomy (ovaries) and physiology (spermathecal-stored sperm quality and quantity), rather than flight behaviour, were compromised and likely corresponded to reduced queen success (alive and producing worker offspring). This study highlights the detriments of neonicotinoids to queens of environmentally and economically important social bees, and further strengthens the need for stringent risk assessments to safeguard biodiversity and ecosystem services that are vulnerable to these substances.

Figure 1. Queen survival after 4 weeks.

Percent honey bee queens that were alive after 4 weeks. No significant difference was observed between treatments. *P ≤ 0.1, **P ≤ 0.05, ***P ≤ 0.01 (comparison with Controls).

Figure 2. Queen oviposition and survival after 4 weeks.

(a) Percent of honey bee queens that oviposited (i.e. laid worker eggs). (b) Percent of honey bee queens that were alive and had produced diploid offspring by the end of the experiment (= Successful). Significant differences between treatments denoted by *P ≤ 0.1, **P ≤ 0.05, ***P ≤ 0.01.

Figure 3. Queen flight over a 4-week interval.

(a) Number of flights by honey bee queens. (b) Total duration of flights by honey bee queens (c) Number of signs of mating. Boxplots show inter- quartile range (box), median (black line within interquartile range), means (grey asterisk), data range (dashed vertical lines), and outliers (open dots). No significant difference was observed between treatments for any measure. *P ≤ 0.1, **P ≤ 0.05, ***P ≤ 0.01 (comparison with Controls).

Figure 4. A marked queen returning to the entrance of a baby mating nucleus hive during experimental observations; arrow denotes mating sign (remnants of a male’s everted endophallus protruding from the queen’s vagina20).

Figure 5. Queen anatomy and physiology after 4 weeks.

(a) Ovary size, represented by number of ovarioles, of honey bee queens. (b) Number of spermatozoa stored in spermathecae of honey bee queens. (c) Percent viable spermatozoa stored in spermathecae of honey bee queens. Boxplots show inter- quartile range (box), median (black line within interquartile range), means (grey asterisk), data range (dashed vertical lines), and outliers (open dots). *P ≤ 0.1, **P ≤ 0.05, ***P ≤ 0.01 (comparison with Controls).

Figure 6. Experimental baby mating nuclei; each nucleus was equipped with a modified entrance consisting of a flat plastic flask and apiculture queen-excluding screen to observe exiting and returning queens without disrupting workers.