Acaricide, Fungicide and Drug Interactions in Honey Bees (Apis mellifera)

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.

The effect of dicyclohexylamine and fumagillin on Nosema ceranae-infected honey bee (Apis mellifera) mortality in cage trial assays

“…Previous research has shown that combined exposure to Fumagilin-B ® and to tau -fluvalinate leads to an increase in tau -fluvalinate toxicity to honey bees, resulting in higher bee mortality (Johnson et al 2013). Tau -fluvalinate was reportedly the most abundant pyrethroid found in North American apiaries in wax (98.1 % detection at a median concentration of 3595 ng g −1 ), pollen (88.3 % detection at a median concentration of 5860 ng g ), according to a 2010 study (Mullin et al 2010).…”

“…Tau -fluvalinate was reportedly the most abundant pyrethroid found in North American apiaries in wax (98.1 % detection at a median concentration of 3595 ng g −1 ), pollen (88.3 % detection at a median concentration of 5860 ng g ), according to a 2010 study (Mullin et al 2010). The concentration of Fumagilin-B ® used for the synergism study (designed to evaluate sub therapeutic concentration effects) was however only 0.78 μM (Johnson et al 2013). which is 50 times less than the manufacturer's prescribed therapeutic dosage of 40 μM for Fumagilin-B ® , containing both fumagillin and DCH in equal amounts.…”

“…This study indicated that a significant increase in toxic synergism with tau -fluvalinate can therefore be expected at the therapeutic concentration of Fumidil-B ® (or Fumagilin-B ® ). It would be interesting to establish whether it is fumagillin or whether it is (Johnson et al 2013). Pyrethroids, including tau -fluvalinate, are reportedly also very stable in wax, where they can accumulate, with estimated half-lives of approximately 5 years (Bogdanov 2004).…”

Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees

“…Indeed, the concomitant occurrence of imidacloprid residues makes it difficult to assign the excess mortality to thiamethoxam alone or to a combined effect, as has been revealed in various combined exposure trials [43,44]. An increasing number of studies [45 -47] report substantial contamination of soil and puddles by neonicotinoid residues that may be subsequently taken up by the next crop in the succession.…”

Honey bee‐collected pollen in agro‐ecosystems reveals diet diversity, diet quality, and pesticide exposure

“…An additional concern is that little is known about potential synergisms among pesticides (but see Johnson, Pollock, & Berenbaum, 2009; Johnson, Dahlgren, Siegfried, & Ellis, 2013), whether in‐hive or out‐of‐hive. To illustrate the pesticide problem, one study of honey bee‐collected pollen (hereafter, pollen) in 23 states and one Canadian province found 98 different pesticide residues, with a mean of 7.1 residues per pollen sample (Mullin et al., 2010).…”