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Insecticides are widely used to control pests in agriculture and insect vectors that transmit human diseases. However, these chemicals can have a negative effect on nontarget, beneficial organisms including bees. Discovery and deployment of selective insecticides is a major mission of modern toxicology and pest management. Pyrethroids exert their toxic action by acting on insect voltage-gated sodium channels. Honeybees and bumblebees are highly sensitive to most pyrethroids, but are resistant to a particular pyrethroid, taufluvalinate (τ-FVL). Because of its unique selectivity, τ-FVL is widely used to control not only agricultural pests but also varroa mites, the principal ectoparasite of honeybees. However, the mechanism of bee resistance to τ-FVL largely remains elusive. In this study, we functionally characterized the sodium channel BiNav1–1 from the common eastern bumblebee (Bombus impatiens) in Xenopus oocytes and found that the BiNav1–1 channel is highly sensitive to six commonly used pyrethroids, but resistant to τ-FVL. Phylogenetic and mutational analyses revealed that three residues, which are conserved in sodium channels from 12 bee species, underlie resistance to τ-FVL or sensitivity to the other pyrethroids. Further computer modeling and mutagenesis uncovered four additional residues in the pyrethroid receptor sites that contribute to the unique selectivity of the bumblebee sodium channel to τ-FVL versus other pyrethroids. Our data contribute to understanding a long-standing enigma of selective pyrethroid toxicity in bees and may be used to guide future modification of pyrethroids to achieve highly selective control of pests with minimal effects on nontarget organisms.

The parasitic mite Varroa destructor and the associated viruses it transmits are responsible for most instances of honey bee colony losses in the United States. As such, beekeepers utilize miticides to control Varroa populations. Widespread resistance has developed to the miticides fluvalinate and coumaphos. However, Varroa has largely maintained susceptibility to amitraz despite a long and extensive use history. Anecdotal reports of reduced amitraz effectiveness have been a widely discussed contemporary issue among commercial beekeepers. Amitraz resistance was measured by in vitro bioassays with technical amitraz as well as Apivar® efficacy tests. Amitraz resistance was evaluated in commercial beekeeping operations in Louisiana, New York, and South Dakota with a long history of amitraz use. This research shows that amitraz remains an effective Varroa control product in many operations. However, apiaries across operations displayed a wide range of amitraz resistance from no resistance to high resistance that resulted in Varroa control failure. The resistance ratios from in vitro amitraz bioassays were correlated with reduced Apivar® efficacy, demonstrating bona fide cases of Varroa control failures due to amitraz resistance. Therefore, amitraz resistance monitoring protocols need to be developed. A resistance monitoring network should be established to ensure the sustainability of miticide use for Varroa control.

Recently, the widespread distribution of pesticides detected in the hive has raised serious concerns about pesticide exposure on honey bee (Apis mellifera L.) health. A larval rearing method was adapted to assess the chronic oral toxicity to honey bee larvae of the four most common pesticides detected in pollen and wax--fluvalinate, coumaphos, chlorothalonil, and chloropyrifos--tested alone and in all combinations. All pesticides at hive-residue levels triggered a significant increase in larval mortality compared to untreated larvae by over two fold, with a strong increase after 3 days of exposure. Among these four pesticides, honey bee larvae were most sensitive to chlorothalonil compared to adults. Synergistic toxicity was observed in the binary mixture of chlorothalonil with fluvalinate at the concentrations of 34 mg/L and 3 mg/L, respectively; whereas, when diluted by 10 fold, the interaction switched to antagonism. Chlorothalonil at 34 mg/L was also found to synergize the miticide coumaphos at 8 mg/L. The addition of coumaphos significantly reduced the toxicity of the fluvalinate and chlorothalonil mixture, the only significant non-additive effect in all tested ternary mixtures. We also tested the common 'inert' ingredient N-methyl-2-pyrrolidone at seven concentrations, and documented its high toxicity to larval bees. We have shown that chronic dietary exposure to a fungicide, pesticide mixtures, and a formulation solvent have the potential to impact honey bee populations, and warrants further investigation. We suggest that pesticide mixtures in pollen be evaluated by adding their toxicities together, until complete data on interactions can be accumulated.

Varroa destructor is considered one of the most devastating parasites of the honey bee, Apis mellifera, and a major problem for the beekeeping industry. Currently, the main method to control Varroa mites is the application of drugs that contain different acaricides as active ingredients. The pyrethroid tau-fluvalinate is one of the acaricides most widely used in beekeeping due to its efficacy and low toxicity to bees. However, the intensive and repetitive application of this compound produces a selective pressure that, when maintained over time, contributes to the emergence of resistant mites in the honey bee colonies, compromising the acaricidal treatments efficacy. Here we studied the presence of tau-fluvalinate residues in hives and the evolution of genetic resistance to this acaricide in Varroa mites from honey bee colonies that received no pyrethroid treatment in the previous four years. Our data revealed the widespread and persistent tau-fluvalinate contamination of beeswax and beebread in hives, an overall increase of the pyrethroid resistance allele frequency and a generalized excess of resistant mites relative to Hardy–Weinberg equilibrium expectations. These results suggest that tau-fluvalinate contamination in the hives may seriously compromise the efficacy of pyrethroid-based mite control methods.

The parasitic mite Varroa destructor (Acari: Varroidae) is a major cause of overwintering honey bee (Apis mellifera) colony losses in the United States, suggesting that beekeepers must control Varroa populations to maintain viable colonies. Beekeepers have access to several chemical varroacides and nonchemical practices to control Varroa populations. However, no studies have examined large-scale patterns in Varroa control methods in the United States. Here we used responses from 4 yr of annual surveys of beekeepers representing all regions and operation sizes across the United States to investigate use of Varroa control methods and winter colony losses associated with use of different methods. We focused on seven varroacide products (amitraz, coumaphos, fluvalinate, hop oil, oxalic acid, formic acid, and thymol) and six nonchemical practices (drone brood removal, small-cell comb, screened bottom boards, powdered sugar, mite-resistant bees, and splitting colonies) suggested to aid in Varroa control. We found that nearly all large-scale beekeepers used at least one varroacide, whereas small-scale beekeepers were more likely to use only nonchemical practices or not use any Varroa control. Use of varroacides was consistently associated with the lowest winter losses, with amitraz being associated with lower losses than any other varroacide product. Among nonchemical practices, splitting colonies was associated with the lowest winter losses, although losses associated with sole use of nonchemical practices were high overall. Our results suggest potential control methods that are effective or preferred by beekeepers and should therefore inform experiments that directly test the efficacy of different control methods. This will allow beekeepers to incorporate Varroa control methods into management plans that improve the overwintering success of their colonies.

Chemical 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. Laboratory 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. Interactions 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.

Summary There is growing number of studies demonstrating a close relationship between insect gut microbiota and insecticide resistance. However, the contribution of the honey bee gut microbiota to host detoxification ability has yet to be investigated. In order to address this question, we compared the expression of cytochrome P450s (P450s) genes between gut microbiota deficient (GD) workers and conventional gut community (CV) workers and compared the mortality rates and the pesticide residue levels of GD and CV workers treated with thiacloprid or tau‐fluvalinate. Our results showed that gut microbiota promotes the expression of P450 enzymes in the midgut, and the mortality rate and pesticide residue levels of GD workers are significantly higher than those of CV workers. Further comparisons between tetracycline‐treated workers and untreated workers demonstrated that antibiotic‐induced gut dysbiosis leads to attenuated expression of P450s in the midgut. The co‐treatment of antibiotics and pesticides leads to reduced survival rate and a significantly higher amount of pesticide residues in honey bees. Taken together, our results demonstrated that honey bee gut symbiont could contribute to bee health through the modification of the host xenobiotics detoxification pathways and revealed a potential negative impact of antibiotics to honey bee detoxification ability and health. Our results demonstrated that honey bee gut symbiont could contribute to bee health through the modification of the host xenobiotics detoxification pathways and revealed a potential negative impact of antibiotics to honey bee detoxification ability and health.

Managed honey bees have suffered severe seasonal losses for most of the past 30 years, while at the same time there is a growing need for food crop pollination. Parasitism by Varroa destructor plays a key role in explaining these losses as this parasite directly damages honey bees by feeding on them and by vectoring an array of viruses while doing so. Pyrethroids like tau- fluvalinate and flumethrin are among the few acaricides that may control Varroa mites in honey bee colonies. However, their intensive use has led to the evolution of resistance in many locations. Knockdown resistance ( kdr- type) in Varroa destructor is associated with point mutations that change the amino acid at position 925 in the para -type voltage-gated sodium channel (VGSC) from leucine to valine, methionine or isoleucine. In order to assess the evolution of resistant mutations, we genotyped a region of the VGSC from V. destructor samples collected worldwide. Our phylogenetic analysis supports the hypothesis of independent origin for resistant alleles in Europe and the USA, and a close relation between L925M and L925I alleles. Our data also suggest that uncontrolled trading of parasitised honey bees might be an important route for spreading resistant alleles overseas. The substitution M918L, associated with pyrethroid resistance in other species, is reported here for the first time in V. destructor , in conjunction with L925V in mites from Spain. The implications of these evolutionary and dispersal processes for Varroa mite management are discussed.

Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007–08 growing seasons. We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm). The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.

In Italy a nation-wide monitoring network was established in 2009 in response to significant honey bee colony mortality reported during 2008. The network comprised of approximately 100 apiaries located across Italy. Colonies were sampled four times per year, in order to assess the health status and to collect samples for pathogen, chemical and pollen analyses. The prevalence of Nosema ceranae ranged, on average, from 47-69% in 2009 and from 30-60% in 2010, with strong seasonal variation. Virus prevalence was higher in 2010 than in 2009. The most widespread viruses were BQCV, DWV and SBV. The most frequent pesticides in all hive contents were organophosphates and pyrethroids such as coumaphos and tau-fluvalinate. Beeswax was the most frequently contaminated hive product, with 40% of samples positive and 13% having multiple residues, while 27% of bee-bread and 12% of honey bee samples were contaminated. Colony losses in 2009/10 were on average 19%, with no major differences between regions of Italy. In 2009, the presence of DWV in autumn was positively correlated with colony losses. Similarly, hive mortality was higher in BQCV infected colonies in the first and second visits of the year. In 2010, colony losses were significantly related to the presence of pesticides in honey bees during the second sampling period. Honey bee exposure to poisons in spring could have a negative impact at the colony level, contributing to increase colony mortality during the beekeeping season. In both 2009 and 2010, colony mortality rates were positively related to the percentage of agricultural land surrounding apiaries, supporting the importance of land use for honey bee health.