BackgroundChemical analysis shows that honey bees (Apis mellifera) and hive products contain many pesticides derived from various sources. The most abundant pesticides are acaricides applied by beekeepers to control Varroa destructor. Beekeepers also apply antimicrobial drugs to control bacterial and microsporidial diseases. Fungicides may enter the hive when applied to nearby flowering crops. Acaricides, antimicrobial drugs and fungicides are not highly toxic to bees alone, but in combination there is potential for heightened toxicity due to interactive effects.Methodology/Principal FindingsLaboratory bioassays based on mortality rates in adult worker bees demonstrated interactive effects among acaricides, as well as between acaricides and antimicrobial drugs and between acaricides and fungicides. Toxicity of the acaricide tau-fluvalinate increased in combination with other acaricides and most other compounds tested (15 of 17) while amitraz toxicity was mostly unchanged (1 of 15). The sterol biosynthesis inhibiting (SBI) fungicide prochloraz elevated the toxicity of the acaricides tau-fluvalinate, coumaphos and fenpyroximate, likely through inhibition of detoxicative cytochrome P450 monooxygenase activity. Four other SBI fungicides increased the toxicity of tau-fluvalinate in a dose-dependent manner, although possible evidence of P450 induction was observed at the lowest fungicide doses. Non-transitive interactions between some acaricides were observed. Sublethal amitraz pre-treatment increased the toxicity of the three P450-detoxified acaricides, but amitraz toxicity was not changed by sublethal treatment with the same three acaricides. A two-fold change in the toxicity of tau-fluvalinate was observed between years, suggesting a possible change in the genetic composition of the bees tested.Conclusions/SignificanceInteractions with acaricides in honey bees are similar to drug interactions in other animals in that P450-mediated detoxication appears to play an important role. Evidence of non-transivity, year-to-year variation and induction of detoxication enzymes indicates that pesticide interactions in bees may be as complex as drug interactions in mammals.
Acaricides are used to treat honey bee (Apis mellifera L.) colonies to control the varroa mite (Varroa destructor Anderson & Trueman), a worldwide threat to honey bee health. Although acaricides control a serious honey bee parasite and mitigate bee loss, they may cause harm to bees as well. We topically applied five acaricides, each with a different mode of action, to young adult queen and worker bees to generate dose-response curves and LD50. Twenty-four hours after treatment, queens were found to be three times more tolerant of tau-fluvalinate and six times more tolerant of thymol than workers when adjusted for body weight differences between workers (108 mg) and queens (180 mg). Queens survived the highest administered doses of fenpyroximate (1620 μg/g) and coumaphos (2700 μg/g) indicating that queens are at least 11-fold more tolerant of coumaphos and at least 54-fold more tolerant of fenpyroximate than workers. However, queens treated with as little as 54 μg/g of fenpyroximate exhibited reduced survival over 6 wk after treatment. Amitraz was the only acaricide tested for which queens were not more tolerant than workers. The striking difference in acaricide tolerance of queen and worker honey bees suggests physiological differences in how the two castes are affected by xenobiotics. D A H L G R E N E T A L . , J O U R N A L O F E C O N O M I C E N T O M O L O G Y1 0 5 (2 01 2 ) 2 Keywords: Varroa destructor, pesticide, Apis mellifera, miticide, queenThe eusocial honey bee lives in a colony in which a single mated queen is mother to thousands of semisterile female workers. Genetically identical female eggs may develop into either a queen or a worker depending only on their diet. Queen and worker larvae receive different diets (Beetsma 1979), with queen larvae receiving a blend of larval food that includes the protein royalactin that results in a faster growth rate, larger body size, and increased ovary development (Reginato and Cruz-Lamdim 2003, Kamakura 2011). Adult workers and queens differ physiologically in their energetic and metabolic requirements, their susceptibility to pathogens, and the circulating proteins found in the hemolymph (Chan et al. 2006). Despite pronounced differences between the castes, there is little information on how queens and workers differ in their tolerance of pesticides in general, or to the in-hive acaricides used by beekeepers to control the ectoparasitic mite Varroa destructor Anderson & Trueman.The widespread distribution of Varroa mites poses a global threat to honey bee colony health (Sammataro et al. 2000). Varroa mites weaken the hive by consuming hemolymph from pupal and adult bees and by transmitting viruses that may increase colony susceptibility to both abiotic and biotic environmental stressors (Shen et al. 2005). Many honey bee colonies infested with Varroa mites perish without beekeeper intervention (Kraus and Page 1995, National Acad. of Sciences [NAS] 2007). While labor-intensive alternatives to chemical control exist (Sammataro et al. 2000) many beekeep...
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