Synergistic and Antagonistic Interactions Between Varroa destructor Mites and Neonicotinoid Insecticides in Male Apis mellifera Honey Bees

Abstract

Pressures from multiple, sometimes interacting, stressors can have negative consequences to important ecosystem-service providing species like the western honey bee (Apis mellifera). The introduced parasite Varroa destructor and the neonicotinoid class of insecticides each represent important, nearly ubiquitous biotic and abiotic stressors to honey bees, respectively. Previous research demonstrated that they can synergistically interact to negatively affect non-reproductive honey bee female workers, but no data exist on how concurrent exposure may affect reproductive honey bee males (drones). This is important, given that the health of reproductive females (queens), possibly because of poor mating, is frequently cited as a major driver of honey bee colony loss. To address this, known age cohorts of drones were obtained from 12 honey bee colonies—seven were exposed to field-relevant concentrations of two neonicotinoids (4.5 ppb thiamethoxam and 1.5 ppb clothianidin) during development via supplementary pollen patties; five colonies received patties not spiked with neonicotinoids. Artificially emerged drones were assessed for natural V. destructor infestation, weighed, and then allocated to the following treatment groups: 1. Control, 2. V. destructor only, 3. Neonicotinoid only, and 4. Combined (both mites and neonicotinoid). Adult drones were maintained in laboratory cages alongside attendant workers (1 drone: 2 worker ratio) until they have reached sexual maturity after 14 days so sperm concentration and viability could be assessed. The data suggest that V. destructor and neonicotinoids interacted synergistically to negatively affect adult drone survival, but that they interacted antagonistically on emergence mass. Although sample sizes were too low to assess the effects of V. destructor and combined exposure on sperm quality, we observed no influence of neonicotinoids on sperm concentration or viability. Our findings highlight the diverse effects of concurrent exposure to stressors on honey bees, and suggest that V. destructor and neonicotinoids can severely affect the number of sexually mature adult drones available for mating.

Drone honey bees are disproportionately sensitive to abiotic stressors despite expressing high levels of stress response proteins

“…Furthermore, HSPs have been demonstrated to have antiviral effects in workers 42 , yet heat-shock appears to repress other humoral immune genes 43 , suggesting further interactions between heat-stress and immunity. Determining the additive and synergistic effects of multistressor drone exposure as well as indirect effects of drone exposure on queens (such as work done by Kairo et al 8,44 and Bruckner et al 45 ) is an important study area to broaden.…”

Neonicotinoid exposure increases Varroa destructor (Mesostigmata: Varroidae) mite parasitism severity in honey bee colonies and is not mitigated by increased colony genetic diversity

“…Force-feeding of pollen lasted 30 days, and visual inspection confirmed pollen patty consumption. Overall, this approach to achieving field-realistic forced-feeding of neonicotinoid-dosed pollen precisely mirrors numerous other studies to better allow comparison of results between studies using this model exposure scenario (e.g., Straub et al 2016 , 2019 , 2021 , Forfert et al 2017 , Friedli et al 2020 , Bruckner et al 2021 ). Colony monitoring proceeded throughout the experiment as described below.…”

“…3 ) and is the first (to our knowledge) demonstration of this link between neonicotinoid and Varroa parasitism using a manipulated field experiment. We emphasize that neonicotinoid exposure increasing vulnerability to Varroa parasitism and subsequent increased mite abundance is a subtly different, possibly supplementary, mechanism to simply demonstrating whether the combination of pesticide exposure and parasitism has antagonistic, additive, or synergistic impacts on honeybee health compared to either effect in isolation—possibly explaining the mixed range of outcomes reported for these interactions ( Straub et al 2019 , Harwood and Dolezal 2020 , Bird et al 2021 , Bruckner et al 2021 , Siviter et al 2021 ).…”

Differential Production of Nitric Oxide and Hydrogen Peroxide among Drosophila melanogaster, Apis mellifera, and Mamestra brassicae Immune-Activated Hemocytes after Exposure to Imidacloprid and Amitraz

“…Thus, cell-based-system methodologies must be continued by in vivo application and field applications. The social construct must also be taken to account when deriving the effects of pesticides on the colony level with the inclusion of honeybee drones whose haploid genome may be more sensitive to these risk factors, leading to a weak colony [ 59 ].…”