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Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine.

ABSTRACT: Insecticides are thought to be among the major factors contributing to current declines in bee populations. However, detoxification mechanisms in healthy, unstressed honey bees are poorly characterised. Alkaloids are naturally encountered in pollen and nectar, and we used nicotine as a model compound to identify the mechanisms involved in detoxification processes in honey bees. Nicotine and neonicotinoids have similar modes of action in insects. Our metabolomic and proteomic analyses show active detoxification of nicotine in bees, associated with increased energetic investment and also antioxidant and heat shock responses. The increased energetic investment is significant in view of the interactions of pesticides with diseases such as Nosema spp which cause energetic stress and possible malnutrition. Understanding how healthy honey bees process dietary toxins under unstressed conditions will help clarify how pesticides, alone or in synergy with other stress factors, lead to declines in bee vitality.

SUBMITTER: Rand EED

PROVIDER: S-EPMC4488760 | biostudies-literature | 2015 Jul

REPOSITORIES: biostudies-literature

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Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine.

Rand Esther E du EED Smit Salome S Beukes Mervyn M Apostolides Zeno Z Pirk Christian W W CWW Nicolson Susan W SW

Scientific reports 20150702

Insecticides are thought to be among the major factors contributing to current declines in bee populations. However, detoxification mechanisms in healthy, unstressed honey bees are poorly characterised. Alkaloids are naturally encountered in pollen and nectar, and we used nicotine as a model compound to identify the mechanisms involved in detoxification processes in honey bees. Nicotine and neonicotinoids have similar modes of action in insects. Our metabolomic and proteomic analyses show active ...[more]

PMID: 26134631

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Project description:BackgroundThe presence of the neonicotinoid imidacloprid in nectar, honey, pollen, beebread and beeswax has been implicated in declines worldwide in the health of the western honey bee Apis mellifera. Certain phytochemicals, including quercetin and p-coumaric acid, are ubiquitous in the honey bee diet and are known to upregulate cytochrome P450 genes encoding enzymes that detoxify insecticides. Thus, the possibility exists that these dietary phytochemicals interact with ingested imidacloprid to ameliorate toxicity by enhancing its detoxification.ApproachQuercetin and p-coumaric acid were incorporated in a phytochemical-free artificial diet individually and together along with imidacloprid at a range of field-realistic concentrations. In acute toxicity bioassays, honey bee 24- and 48- hour imidacloprid LC50 values were determined in the presence of the phytochemicals. Additionally, chronic toxicity bioassays were conducted using varying concentrations of imidacloprid in diets with the phytochemicals to test impacts of phytochemicals on longevity.ResultsIn acute toxicity bioassays, the phytochemicals had no effect on imidacloprid LC50 values. In chronic toxicity longevity bioassays, phytochemicals enhanced honey bee survival at low imidacloprid concentrations (15 and 45 ppb) but had a negative effect at higher concentrations (105 ppb and 135 ppb). p-Coumaric acid alone increased honey bee longevity at concentrations of 15 and 45 ppb imidacloprid (hazard ratio (HR): 0.83 and 0.70, respectively). Quercetin alone and in combination with p-coumaric acid similarly enhanced longevity at 45 ppb imidacloprid (HR:0.81 and HR:0.77, respectively). However, p-coumaric acid in combination with 105 ppb imidacloprid and quercetin in combination with 135 ppb imidacloprid increased honey bee HR by approximately 30% (HR:1.33 and HR:1.30, respectively).ConclusionsThe biphasic concentration-dependent response of honey bees to imidacloprid in the presence of two ubiquitous dietary phytochemicals indicates that there are limits to the protective effects of the natural diet of honey bees against neonicotinoids based on their own inherent toxicity.

Project description: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.

Dataset Information

Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine.

Publications

Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine.

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