Lethal and Sublethal Synergistic Effects of a New Systemic Pesticide, Flupyradifurone (Sivanto®), on Honeybees

The authors tested honey bees to determine the lethal and sublethal toxic effects of flupyradifurone (FPF), a newly developed systemic insecticide that shares multiple similarities with the neonicotinoids. FPF is systemic and a nicotinic acetylcholine receptor (nAChR) agonist.

The authors tested FPF over different seasons and worker types, as well as the interaction of FPF with a common Sterol Biosynthesis Inhibiting (SBI ) fungicide propiconazole (PRO) on bee survival and behavior. FPF (Sivanto) labeling restricts using tank mixtures with azole fungicides. However, bees can still be exposed to FPF and PRO simultaneously if one or the other chemicals persist in soil or plant tissue, if bees experience combined exposure from foraging on different crops, if bees are exposed to drift from neighboring fields, or if bees forage on plants exposed to contaminated soil or water.

Bees were fed sucrose spiked with technical-grade FPF or FPF plus PRO. Tested FPF doses ranged from 375 to 12,000 ng/bee. Concentrations of FPF on the lower range of the tested spectrum are considered field-realistic. Propiconazole was tested at a relatively high concentration that on its own has no impact on bee survival (7000 ng/bee).  Bees were observed for abnormal behaviors for 1-4 hours after the test, and for survival from 1-48 hrs after the test. Behavioral attributes measured included motion coordination deficits, hyperactivity, apathy, curved-down abdomen or moribund.

The authors calculated the risk ratio (RR) and the risk difference (RD) to quantitatively express both relative (RR) and absolute (RD) size of the interactive effect of the chemical mixture on bee survival (frequency of dead bees) and behavior (frequency of abnormally behaving bees) compared with effects from FPF alone.

Mortality Effects

FPF alone caused higher mortality at increasing doses, and was significantly more toxic to foragers (compared with in-hive bees) at almost all doses tested. PRO alone did not cause any significant effect on survival. 

The lowest tested FPF dose (375 ng FPF /bee) caused 73% mortality in bees when combined with PRO. The LD50 measured with the FPF + PRO interaction demonstrated synergy for both worker types with in-hive bees exhibiting 4-fold toxicity increase and foragers a 5-fold toxicity increase.

Behavior:

All FPF doses tested significantly impaired bee behavior as compared with the control treatment. 

When tested in combination, FPF plus PRO also demonstrated synergy for behavioral effects. PRO alone did not cause any significant abnormal behavior. Effects on foragers were lower than for in-hive bees.

Under the FPF and combined tests abnormal behaviors usually appeared shortly (1 h) after exposure.

Observed synergistic behavioral alterations occurred at low (750–1500 ng/bee) and high (6000 ng/bee) doses, but not at intermediate ones (3000 ng/bee). 

Influence of worker type and season

The toxic effect of FPF and FPF plus PRO on bee survival and behavior was significantly influenced by worker type and season. Both worker types were more strongly affected by FPF in summer as compared with spring. Foragers were consistently more susceptible to these pesticides (up to 4-fold). This result is troubling because the official guidelines for pesticide risk assessment (RA) only test in-hive bees, thereby underestimating the risk that pesticides pose for foragers The authors surmise that the lower weight of foragers (-11%), as compared with in-hive bees is a possible reason for their increased susceptibility to pesticides.