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.

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

“…(min = 1.8 km). Pollen collection is described in detail in Graham et al 38 and summarized briefly here. We sampled pollen from colonies delivered by commercial beekeepers in the field margins at each farm.…”

“…An internal standard solution (d 4 -imidacloprid 0.07 ng/µL; d 10 -chlorpyrifos 0.2 ng/µL: d 7 -bentazon 0.1 ng/µL; d 5 -atrazine 0.02 ng/µL; d 7 -propamocarb 0.1 ng/µL) was used. Detailed methods can be found in Graham et al 38 . Retention times and optimized SRM acquisition parameters are provided in Table S1 .…”

“…Additionally, multiple active ingredients in combination may have synergistic effects, further complicating estimates of risk 35 – 37 . We previously estimated the concentrations of active ingredients in pollen collected by honey bees and bumble bees returning to colonies in blueberry fields during bloom 38 . Eighty active ingredients were found in pollen samples, in different combinations that varied over time (the same farm in 2 years) and space (multiple farms in the same year), highlighting the wide range of pesticides that bees can be exposed to.…”

“…The study linked pesticide risks to sources outside apple orchards where the bee colonies were located, showing that combining exposure data, toxicity information, and landscape analysis can provide insights into sources of pesticide risk. Our recent analysis of pesticide residues in pollen trapped at the entrances to colonies of honey bees and bumble bees in blueberry fields for pollination 38 revealed that pesticides applied for disease and insect control were at the highest concentrations, but many of the other pesticides detected were not used in this crop during bloom or at other times of the year. This indicated that bees were collecting some of the contaminated pollen from crops across the landscape, supported by correlations to landscape composition.…”

“…In this study, we expanded on the results presented in Graham et al 38 by sampling a greater number of relevant bee and plant matrices to develop a more complete view of pesticide risk to managed honey bees and bumble bees during blueberry pollination. This included the collection of whole blueberry flowers, which would include exposure from nectar, pollen, or contact with flower parts such as the corolla.…”