Pesticide risk to managed bees during blueberry pollination is primarily driven by off-farm exposures

Abstract

When managed bee colonies are brought to farms for crop pollination, they can be exposed to pesticide residues. Quantifying the risk posed by these exposures can indicate which pesticides are of the greatest concern and helps focus efforts to reduce the most harmful exposures. To estimate the risk from pesticides to bees while they are pollinating blueberry fields, we sampled blueberry flowers, foraging bees, pollen collected by returning honey bee and bumble bee foragers at colonies, and wax from honey bee hives in blooming blueberry farms in southwest Michigan. We screened the samples for 261 active ingredients using a modified QuEChERS method. The most abundant pesticides were those applied by blueberry growers during blueberry bloom (e.g., fenbuconazole and methoxyfenozide). However, we also detected highly toxic pesticides not used in this crop during bloom (or other times of the season) including the insecticides chlorpyrifos, clothianidin, avermectin, thiamethoxam, and imidacloprid. Using LD₅₀ values for contact and oral exposure to honey bees and bumble bees, we calculated the Risk Quotient (RQ) for each individual pesticide and the average sample RQ for each farm. RQ values were considered in relation to the U.S. Environmental Protection Agency acute contact level of concern (LOC, 0.4), the European Food Safety Authority (EFSA) acute contact LOC (0.2) and the EFSA chronic oral LOC (0.03). Pollen samples were most likely to exceed LOC values, with the percent of samples above EFSA's chronic oral LOC being 0% for flowers, 3.4% for whole honey bees, 0% for whole bumble bees, 72.4% for honey bee pollen in 2018, 45.4% of honey bee pollen in 2019, 46.7% of bumble bee pollen in 2019, and 3.5% of honey bee wax samples. Average pollen sample RQ values were above the EFSA chronic LOC in 92.9% of farms in 2018 and 42.9% of farms in 2019 for honey bee collected pollen, and 46.7% of farms for bumble bee collected pollen in 2019. Landscape analyses indicated that sample RQ was positively correlated with the abundance of apple and cherry orchards located within the flight range of the bees, though this varied between bee species and landscape scale. There was no correlation with abundance of blueberry production. Our results highlight the need to mitigate pesticide risk to bees across agricultural landscapes, in addition to focusing on the impact of applications on the farms where they are applied.

Figure 1

Average sample risk quotient by sample type. Risk quotient (RQ) was calculated with contact (purple) and oral (pink) LD₅₀ values. Toxicity data for Apis mellifera and Bombus terrestris were used depending on the sample type. Individual sample RQs are represented by the dots. Horizontal black lines are the mean, and the error bars represent standard error of the mean. RQ is displayed in relation to the EPA and EFSA levels of concern (proportion of the LD50). The green dashed line is the EFSA level of concern for chronic exposure (relevant for oral toxicity). The blue dashed line is the EFSA level of concern for acute exposure, and the red dashed line is the EPA level of concern for acute exposure. Graph created in GraphPad Prism 9.

Figure 2

Contribution of individual active ingredients to the pollen risk quotient calculations for each bee species and year (2018/2019). This was determined both for RQs calculated with contact LD₅₀ values (A) and oral LD₅₀ values (B). Toxicity data for Apis mellifera and Bombus terrestris were used depending on the pollen source. Graph created in GraphPad Prism 9.

Figure 3

Contribution of pesticide active ingredients to pollen risk quotient values based on whether they are registered for use on blueberries, or not. A product was considered registered for use on blueberries if the label indicated it is permitted to be applied to blueberry bushes at any time of the year. RQs were calculated with contact LD₅₀ values and oral LD₅₀ values. Toxicity data for Apis mellifera and Bombus terrestris were used depending on which species collected the pollen (HB-honey bees, Apis mellifera, BB-bumble bees, Bombus impatiens). Graph created in GraphPad Prism 9.

Figure 4

Average pollen sample risk quotient at each farm where pollen was collected from honey bees in 2018 (triangles) and 2019 (squares) and bumble bees in 2019 (circles). Contact (x-axis) and oral (y-axis) LD₅₀ values were used to calculate risk quotient using Apis mellifera toxicity values for honey bee pollen, and Bombus terrestris values were used whenever possible for bumble bee pollen. RQ is displayed in relation to the EPA and EFSA levels of concern (proportion of the LD50). The green dashed line is the EFSA level of concern (LOC) for chronic oral exposure (0.03). The blue dashed line is the EFSA level of concern for acute exposure (0.2), and the red dashed line is the EPA level of concern for acute exposure (0.4). However, EPA and EFSA do not use acute LOCs for oral exposure. These are included on the y-axis for illustrative purposes only. Graph created in R version 4.1.1 with the package ggplot2.