Bumblebees can be Exposed to the Herbicide Glyphosate when Foraging

Abstract

Herbicides are the most widely used pesticides globally. Although used to control weeds, they may also pose a risk to bee health. A key knowledge gap is how bees could be exposed to herbicides in the environment, including whether they may forage on treated plants before they die. We used a choice test to determine if bumblebees would forage on plants treated with glyphosate at two time periods after treatment. We also determined whether glyphosate and its degradation product aminomethylphosphonic acid were present as residues in the pollen collected by the bees while foraging. Finally, we explored if floral resources (nectar and pollen) remained present in plants after herbicide treatment. In general bees indiscriminately foraged on both plants treated with glyphosate and controls, showing no avoidance of treated plants. Although the time spent on individual flowers was slightly lower on glyphosate treated plants, this did not affect the bees' choice overall. We found that floral resources remained present in plants for at least 5 days after lethal treatment with glyphosate and that glyphosate residues were present in pollen for at least 70 h posttreatment. Our results suggest that bees could be exposed to herbicide in the environment, both topically and orally, by foraging on plants in the period between herbicide treatment and death. Identifying this route of exposure is a first step in understanding the risks of herbicides to bees. The effects of herbicides on bees themselves are uncertain and warrant further investigation to allow full risk assessment of these compounds to pollinating insects.

Effects of glyphosate and glyphosate‐based herbicide on learning and memory of the buff‐tailed bumblebee (Bombus terrestris)

“…Importantly, bumblebees do not seem to discriminate between flowers that have been recently treated with either GBHs (K Kaakinen et al., unpubl.) or pure glyphosate (Thompson et al., 2022), confirming that they can be exposed to glyphosate residues while foraging. We determined that a field‐realistic amount of glyphosate that a foraging bumblebee can potentially obtain orally while visiting recently treated flowers is 35 μg.…”

Contrasting effects of fungicide and herbicide active ingredients and their formulations on bumblebee learning and behaviour

“…In general, our study could be considered conservative with regards to the dose and route of exposure of the active ingredients and formulations used. Bees may be exposed to glyphosate through nectar and pollen simultaneously when foraging ( Thompson et al, 2014 ), and glyphosate concentrations can be detected for at least 3–7 days after plant treatment ( Thompson et al, 2014 ; 2022 ), which is a longer time period than tested here. Therefore, our exposure to a low concentration through nectar alone for 3–4 days could result in a lower exposure than might be expected in the field, and it would be interesting to test a range of glyphosate concentrations and chronic exposure periods within the field-relevant range.…”

“…Glyphosate is also the most applied herbicide in the world (in terms of kg used; Benbrook, 2016 ), and is a broad-spectrum and non-selective herbicide employed for a variety of uses in agriculture, but also heavily used in domestic and amenity settings ( Duke and Powles, 2008 ). Bees can also come into contact with glyphosate in the environment; for example, bees forage on plants treated with glyphosate and return nectar and pollen containing residues to their colony ( Thompson et al, 2014 ; 2022 ). Prothioconazole is a broad-spectrum fungicide, commonly applied to a variety of crops such as oilseed rape and cereals ( FAO, 2021 ), and is widely used across the EU ( López-Ballesteros et al, 2022 ).…”

“…Glyphosate has been recorded at 1–1.30 mg kg −1 in nectar stores of honeybee colonies, 2.78–31.3 mg kg −1 in the honeybee stomach, and 87.2–629 mg kg −1 in pollen after honeybees foraged on treated plants over a 7 day period ( Thompson et al, 2014 ). Additionally, glyphosate has been detected in corbicular pollen at 5 mg kg −1 up to 3 days post-spray ( Thompson et al, 2022 ). Therefore, we chose a 1 mg kg −1 concentration for both active ingredient and formulation treatments to mimic conservative but environmentally relevant concentrations in nectar that bees could feed on (see Table S3 ).…”

“…However, globally, fungicides and herbicides are more heavily used than insecticides (in terms of kg applied). Just as with insecticides, bees may come into contact with plants recently treated with these pesticides and as such consume contaminated floral resources ( Gradish et al, 2019 ; Zioga et al, 2020 , 2022 ; Thompson et al, 2022 ). Despite this, our knowledge of whether the use of fungicides and herbicides has impacts for bees is lacking ( Cullen et al, 2019 ; FAOSTAT, 2020 ), most likely as these classes are not designed to target insect pests.…”