Sublethal glyphosate exposure reduces honey bee foraging and alters the balance of biogenic amines in the brain.

Abstract

Glyphosate is a broad-spectrum herbicide that inhibits the shikimate pathway, which honey bees (Apis mellifera), a non-target beneficial pollinator, do not endogenously express. Nonetheless, sublethal glyphosate exposure in honey bees has been correlated to impairments in gustation, learning, memory and navigation. While these impacted physiologies underpin honey bee foraging and recruitment, the effects of sublethal glyphosate exposure on these important behaviors remain unclear, and any proximate mechanism of action in the honey bee is poorly understood. We trained cohorts of honey bees from the same hives to forage at one of two artificial feeders offering 1 mol l-1 sucrose solution, either unaltered (N=40) or containing glyphosate at 5 mg acid equivalent (a.e.) l-1 (N=46). We then compared key foraging behaviors and, on a smaller subset of bees, recruitment behaviors. Next, we quantified protein levels of octopamine, tyramine and dopamine, and levels of the amino acid precursor tyrosine in the brains of experimental bees collected 3 days after the exposure. We found that glyphosate treatment bees reduced their foraging by 13.4% (P=0.022), and the brain content of tyramine was modulated by a crossover interaction between glyphosate treatment and the number of feeder visits (P=0.004). Levels of octopamine were significantly correlated with its precursors tyramine (P=0.011) and tyrosine (P=0.018) in glyphosate treatment bees, but not in control bees. Our findings emphasize the critical need to investigate impacts of the world's most-applied herbicide and to elucidate its non-target mechanism of action in insects to create better-informed pollinator protection strategies.