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.

Are fungicides a driver of European foulbrood disease in honey bee colonies pollinating blueberries?

“…The lack of significant negative effects following fungicide product exposure with and without M. plutonius infection are not surprising, as other researchers also have not found significant negative effects on honey bee larval survival from oral (or contact) exposure to field-relevant concentrations of the active fungicide ingredients in Captan, Luna, and Switch (Everich et al, 2009;Wood et al, 2020). While our highest tested concentrations of the active ingredients in Captan, Luna, and Switch reflected the highest reported residues of these active ingredients in pollen/bee bread and honey (Graham et al, 2021(Graham et al, , 2022Rondeau and Raine, 2022), the transfer rate of residues from pollen into royal jelly and worker jelly is believed to be low (Bohme et al, 2018(Bohme et al, , 2019Milone et al, 2021), and thus, our concentrations are likely an over estimation of exposure. Although most fungicides detected in honey have systemic properties, fludioxonil is a non-systemic fungicide and its residues have never been reported in honey (Rondeau and Raine, 2022), therefore we used residue concentrations for pollen/bee bread in place of honey.…”

“…Although most fungicides detected in honey have systemic properties, fludioxonil is a non-systemic fungicide and its residues have never been reported in honey (Rondeau and Raine, 2022), therefore we used residue concentrations for pollen/bee bread in place of honey. As residue concentrations in pollen/bee bread are many folds higher than concentrations found in nectar/honey (Graham et al, 2021(Graham et al, , 2022Rondeau and Raine, 2022), this again illustrates our tested concentrations as a potential over exposure. On the other hand, water is also an important constituent in worker larval diet (McCune et al, 2021).…”

Ecological traits interact with landscape context to determine bees’ pesticide risk

“…However, we know less about the resulting pesticide risk, especially between bee species and in different landscape contexts (but see refs. 22 , 26 , 46 , 47 ). We found that increasing the proportion of agricultural land increased the risk for B. terrestris and O. bicornis but not for A. mellifera .…”

Phytochemicals, Probiotics, Recombinant Proteins: Enzymatic Remedies to Pesticide Poisonings in Bees

“…For example, crops such as corn or soybean are commonly grown with neonicotinoid-coated seeds and subsequent herbicide use (e.g., glyphosate) in spring . In a landscape with more crop types and a greater diversity of pesticides applied, pesticide exposure is less predictable since honey bees can forage up to 10 km and come into contact with different types of pesticides simultaneously in surrounding landscapes. ,, In these landscapes with more diverse crops and varying pesticide uses, the development of detoxification solutions may be more complicated. ,, Beekeepers, especially commercial operators managing thousands of bee hives located in different apiary locations, face more uncertainties regarding detoxification strategies . While one constituent in a 3P treatment usually works to detoxify one set of pesticides, the challenge presented by complex exposure situations will not be resolved until a product composed of diverse constituents is developed to detoxify different pesticides …”

“…70 In a landscape with more crop types and a greater diversity of pesticides applied, pesticide exposure is less predictable since honey bees can forage up to 10 km and come into contact with different types of pesticides simultaneously in surrounding landscapes. 66,76,77 In these landscapes with more diverse crops and varying pesticide uses, the development of detoxification solutions may be more complicated. 66,76,77 Beekeepers, especially commercial operators managing thousands of bee hives located in different apiary locations, face more uncertainties regarding detoxification strategies.…”