Fungicide suppression of flight performance in the honeybee ( Apis mellifera ) and its amelioration by quercetin

Abstract

As a managed agricultural pollinator, the western honeybee Apis mellifera frequently encounters agrochemicals as contaminants of nectar and pollen. One such contaminant, the fungicide boscalid, is applied at bloom in orchards for fungal floral pathogen control. As an inhibitor of complex II in the mitochondrial electron transport chain of fungi, boscalid can potentially interfere with high energy-demanding activities of bees, including flight. We designed an indoor flight treadmill to evaluate impacts of ingesting boscalid and/or quercetin, a ubiquitous phytochemical in bee food that also affects mitochondrial respiration. Boscalid reduced the wingbeat frequencies of foragers during flight but did not alter the duration of flight. At the colony level, boscalid ingestion may thereby affect overall health by reducing forager efficiency. The consumption of quercetin, by contrast, led to higher adenosine triphosphate levels in flight muscles and a higher wingbeat frequency. Consuming the two compounds together increased wingbeat frequency, demonstrating a hitherto unrecognized mechanism by which dietary phytochemicals may act to ameliorate toxic effects of pesticides to promote honeybee health. In carrying out this work, we also introduce two methodological improvements for use in testing for pesticide effects on flight capacity—a ‘force-feeding’ to standardize flight fuel supply and a novel indoor flight treadmill.

Pesticide risk assessment in honeybees: Toward the use of behavioral and reproductive performances as assessment endpoints

“…However, there is now growing evidence for lethal and sublethal effects induced by such pesticides (Cullen et al, 2019). Notably, fungicides may affect honeybee energetic metabolism (Degrandi-Hoffman et al, 2015), which can translate into impaired behavioral performance (Liao et al, 2019;Prado et al, 2019). In addition, in terms of tonnage, insecticide use is outweighed by fungicides and herbicides (Cullen et al, 2019).…”

“…It requires more sophisticated apparatus like flight mills, whereby the tested bees are tethered to a balanced arm and allowed to fly circularly around an axis (Tong et al, 2019;. Alternatively, bees may be harnessed to a fixed support and exposed to air flow and optic flow stimuli in order to elicit flight (Liao et al, 2019). Flight experiments typically document flight duration until exhaustion, total covered distance, as well as average flight velocity.…”

“…However, common patterns are difficult to identify across studies due to the broad variety of experimental designs and peculiarities related with bee age (Charreton et al, 2015), topical vs. oral exposure (El Hassani et al, 2008, exposure duration (Williams et al, 2020) or timescale after exposure (Kadala et al, 2019). Similarly, if a reduction in flying capacities was generally reported by experiments with flight mills (Liao et al, 2019;Tong et al, 2019;, depending on the type of exposure, opposite effects could also be induced on specific flight traits (Tong et al, 2019).…”

“…However, as for PER conditioning, the ecological relevance of bee activity recorded in indoor conditions remains to be determined. Impairment of locomotion ability, due to alteration of either energetic metabolism (Liao et al, 2019) or brain and muscle excitability (Kadala et al, 2019), may affect the performance of foragers or in-hive bees (like nurse bees). For instance, flight mills have been largely used for better understanding migration in insects, and flight studies have been shown to support field observations (Minter et al, 2018).…”

“…Even if it has been validated for only thiamethoxam, there is growing evidence for low-dose effects of others insecticides, fungicides and herbicides, on honeybee navigation, foraging activities and flight performances (e.g. Balbuena et al, 2015;Bortolotti et al, 2003;Liao et al, 2019;Matsumoto, 2013;Prado et al, 2019;Vandame et al, 1995). Such endpoints have a high ecological relevance because of the obvious link between the loss of foragers and/or decreased foraging activity and colony development.…”