Identities, concentrations, and sources of pesticide exposure in pollen collected by managed bees during blueberry pollination

Abstract

Bees are critical for crop pollination, but there is limited information on levels and sources of pesticide exposure in commercial agriculture. We collected pollen from foraging honey bees and bumble bees returning to colonies placed in blooming blueberry fields with different management approaches (conventional, organic, unmanaged) and located across different landscape settings to determine how these factors affect pesticide exposure. We also identified the pollen and analyzed whether pesticide exposure was correlated with corbicular load composition. Across 188 samples collected in 2 years, we detected 80 of the 259 pesticide active ingredients (AIs) screened for using a modified QuEChERS method. Detections included 28 fungicides, 26 insecticides, and 21 herbicides. All samples contained pesticides (mean = 22 AIs per pollen sample), with pollen collected from bees on conventional fields having significantly higher average concentrations (2019 mean = 882.0 ppb) than those on unmanaged fields (2019 mean = 279.6 ppb). Pollen collected by honey bees had more AIs than pollen collected by bumble bees (mean = 35 vs. 19 AIs detected at each farm, respectively), whereas samples from bumble bees had higher average concentrations, likely reflecting differences in foraging behavior. Blueberry pollen was more common in pollen samples collected by bumble bees (25.9% per sample) than honey bees (1.8%), though pesticide concentrations were only correlated with blueberry pollen for honey bees. Pollen collected at farms with more blueberry in the surrounding landscape had higher pesticide concentrations, mostly AIs applied for control of blueberry pathogens and pests during bloom. However, for honey bees, the majority of AIs detected at each farm are not registered for use on blueberry at any time (55.2% of AIs detected), including several highly toxic insecticides. These AIs therefore came from outside the fields and farms they are expected to pollinate. For bumble bees, the majority of AIs detected in their pollen are registered for use on blueberry during bloom (56.9% of AIs detected), though far fewer AIs were sprayed at the focal farm (16.7%). Our results highlight the need for integrated farm and landscape-scale stewardship of pesticides to reduce exposure to pollinators during crop pollination.

Figure 1

Average number of active ingredients (AIs) detected at each farm. Dark lines indicate the median, diamonds indicate the mean, boxes represent the upper and lower quartile, whiskers indicate the maximum and minimum number of AIs detected. Data are separated by which bee collected the pollen (HB honey bee, BB bumble bee) and in which year the data were collected. Upper case letters indicate significant differences within the 2018 data, and lower case letters indicate significant differences within the 2019 data. Graph created in R v3.6.2 with the package ggplot2.

Figure 2

Concentrations of pesticides detected in bee-collected pollen from colonies. Each data point represents the concentration of an active ingredient found in an individual sample. Pesticides were detected in pollen collected from honey bees in 2018 (grey), pollen collected from honey bees in 2019 (yellow), and pollen collected from bumble bees in 2019 (blue). Dark lines indicate the median, diamonds indicate the mean, boxes represent the upper and lower quartile, whiskers indicate the maximum and minimum concentration detected (besides outliers), and the dots represent outliers. Letters indicate significant differences between the pesticide types and this pattern was consistent when all samples were combined for analyses, or when samples were separated out by bee and year for analyses. Graph created in R v3.6.2 with the package ggplot2.

Figure 3

Average percent contribution of pesticides to the (A) number of active ingredients (AIs) detected at a site, and (B) overall sample concentration. Contributions were determined by spray records and registration status. Active ingredients are separated into those that were either applied on the focal field during bloom (black), registered for use on blueberries during bloom but not sprayed in the focal fields (dark grey), registered for use on blueberries outside bloom (light grey) or not registered for use on blueberries at any time (white). Graph created in GraphPad Prism 9.

Figure 4

Relationships between percent of the landscape in blueberry production within 1000 m of bee colonies and the concentration of pesticides detected in pollen collected by bumble bees (red) and honey bees (blue). Lines indicate smoothed linear regression lines with 95% confidence intervals. Graph created in R v3.6.2 with the package ggplot2.