Increase in longevity and amelioration of pesticide toxicity by natural levels of dietary phytochemicals in the honey bee, Apis mellifera

Abstract

For the past decade, migratory beekeepers who provide honey bees for pollination services have experienced substantial colony losses on a recurring basis that have been attributed in part to exposure to insecticides, fungicides, or their combinations applied to crops. The phytochemicals p-coumaric acid and quercetin, which occur naturally in a wide variety of bee foods, including beebread and many types of honey, can enhance adult bee longevity and reduce the toxicity of certain pesticides. How variation in concentrations of natural dietary constituents affects interactions with xenobiotics, including synthetic pesticides, encountered in agroecosystems remains an open question. We tested the effects of these two phytochemicals at a range of natural concentrations on impacts of consuming propiconazole and chlorantraniliprole, a triazole fungicide and an insecticide frequently applied as a tank mix to almond trees during bloom in California’s Central Valley. Propiconazole, even at low field concentrations, significantly reduced survival and longevity when consumed by adult bees in a sugar-based diet. The effects of propiconazole in combination with chlorantraniliprole enhanced mortality risk. The detrimental effects of the two pesticides were for the most part reduced when either or both of the phytochemicals were present in the diet. These findings suggest that honey bees may depend on non-nutritive but physiologically active phytochemical components of their natural foods for ameliorating xenobiotic stress, although only over a certain range of concentrations; particularly at the high end of the natural range, certain combinations can incur additive toxicity. Thus, efforts to develop nectar or pollen substitutes with phytochemicals to boost insecticide tolerance or immunity or to evaluate toxicity of pesticides to pollinators should take concentration-dependent effects of phytochemicals into consideration.

Pollen nutrition fosters honeybee tolerance to pesticides

“…Similarly, the reduced mortality risk upon exposure to pesticide was observed over a range of relatively low natural concentrations (5, 50 and 500 µM) for p-coumaric acid. Higher concentrations (1000 µM) increased or did not change the toxicity of pesticides [45]. Our results are, therefore, consistent with these royalsocietypublishing.org/journal/rsos R. Soc.…”

“…The pollen-induced differences in pesticide sensitivity reported in our study could not be explained by this nutritional factor since both pollen diets had similar P : Ls. However, several studies have shown that the pollen phytochemicals quercetin and p-coumaric acid, upon ingestion, can significantly enhance bee longevity [46,104] and also tolerance to several pesticides [45][46][47]. However, the effects of these phytochemicals are concentration-dependent; lower concentrations tend to have a positive effect on honeybee longevity ( p-coumaric acid at 5, 50 and 500 µM and quercetin at 12.5, 25 and 250 µM), while higher natural concentrations (1000 µM) have no effects [45,46].…”

“…However, several studies have shown that the pollen phytochemicals quercetin and p-coumaric acid, upon ingestion, can significantly enhance bee longevity [46,104] and also tolerance to several pesticides [45][46][47]. However, the effects of these phytochemicals are concentration-dependent; lower concentrations tend to have a positive effect on honeybee longevity ( p-coumaric acid at 5, 50 and 500 µM and quercetin at 12.5, 25 and 250 µM), while higher natural concentrations (1000 µM) have no effects [45,46]. Similarly, the reduced mortality risk upon exposure to pesticide was observed over a range of relatively low natural concentrations (5, 50 and 500 µM) for p-coumaric acid.…”

“…Regarding the potential mechanisms underlying this nutritional modulation of pesticide sensitivity, pollen intake upregulates the expression of several xenobiotic-metabolizing cytochrome P450 genes [31], as well as the activity of glutathione S-transferases [39], which are involved in Phases I and II of the detoxification pathways, respectively [40][41][42]. More specifically, upon ingestion, several constituents of pollen, like the phytochemicals p-coumaric acid and quercetin, can upregulate the expression of cytochrome P450 genes [43,44] and increase the survival rate of bees exposed to pesticides [3,[45][46][47]. Such an effect on the detoxification capacity of bees was further confirmed by measuring pesticide metabolism.…”

Metabolomics-Guided Comparison of Pollen and Microalgae-Based Artificial Diets in Honey Bees

“…19,20 In addition to protein content, pollen contains a variety of necessary lipids, essential fatty acids, 21−23 and a broad diversity of bee health-modulating bioactive compounds, such as vitamins and phenolic acids. 24,25 Thus, there are opportunities to enhance feed to more closely mimic the chemical composition of pollen, especially to serve the growing demands of a majority of US beekeepers who feed supplemental nutrition to their colonies. 20 Importantly, given the challenges of feeding the world's human population, sustainable ingredients that do not compete with human food production are good candidates to address this crucial need of modern beekeeping.…”