Abstract
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.
Highlights
Chemical analysis of honey bees (Apis mellifera) and hive products show that most managed bee colonies in North America and Europe are repositories of a suite of chemical contaminants, including an assortment of insecticides, acaricides, herbicides and fungicides [1,2,3]
Amitraz did not interact with any fungicides or antimicrobials, but did demonstrate an antagonistic interaction with a single acaricide, oxalic acid
Any sterol biosynthesis inhibiting (SBI) fungicide that inhibits P450mediated detoxification has the potential to interact with taufluvalinate, and likely coumaphos and fenpyroximate as well
Summary
Chemical analysis of honey bees (Apis mellifera) and hive products show that most managed bee colonies in North America and Europe are repositories of a suite of chemical contaminants, including an assortment of insecticides, acaricides, herbicides and fungicides [1,2,3]. Some of the most ubiquitous contaminants of bees and bee products, coumaphos and tau-fluvalinate [3], are abundant in the hive environment because both are deliberately introduced as therapeutic acaricides to control the ectoparasitic mite, Varroa destructor. Varroa is the most serious pest of managed honey bee colonies in Europe and North America and clearly plays a role in the recent colony losses associated with colony collapse disorder [4,5,6]. 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
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