Honey bees and bumble bees may be exposed to pesticides differently when foraging on agricultural areas.

In an agricultural environment, where crops are treated with pesticides, bees are likely to be exposed to a range of chemical compounds in a variety of ways. The extent to which different bee species are affected by these chemicals, largely depends on the concentrations and type of exposure. We quantified the presence of selected pesticide compounds in the pollen of two different entomophilous crops; oilseed rape (Brassica napus) and broad bean (Vicia faba). Sampling was performed in 12 sites in Ireland and our results were compared with the pollen loads of honey bees and bumble bees actively foraging on those crops in those same sites. Detections were compound specific, and the timing of pesticide application in relation to sampling likely influenced the final residue contamination levels. Most detections originated from compounds that were not recently applied on the fields, and samples from B. napus fields were more contaminated compared to those from V. faba fields. Crop pollen was contaminated only with fungicides, honey bee pollen loads contained mainly fungicides, while more insecticides were detected in bumble bee pollen loads. The highest number of compounds and most detections were observed in bumble bee pollen loads, where notably, all five neonicotinoids assessed (acetamiprid, clothianidin, imidacloprid, thiacloprid, and thiamethoxam) were detected despite the no recent application of these compounds on the fields where samples were collected. The concentrations of neonicotinoid insecticides were positively correlated with the number of wild plant species present in the bumble bee-collected pollen samples, but this relationship could not be verified for honey bees. The compounds azoxystrobin, boscalid and thiamethoxam formed the most common pesticide combination in pollen. Our results raise concerns about potential long-term bee exposure to multiple residues and question whether honey bees are suitable surrogates for pesticide risk assessments for all bee species.

Pesticide mixtures detected in crop and non-target wild plant pollen and nectar.

Cultivation of mass flowering entomophilous crops benefits from the presence of managed and wild pollinators, who visit flowers to forage on pollen and nectar. However, management of these crops typically includes application of pesticides, the presence of which may pose a hazard for pollinators foraging in an agricultural environment. To determine the levels of potential exposure to pesticides, their presence and concentration in pollen and nectar need assessing, both within and beyond the target crop plants. We selected ten pesticide compounds and one metabolite and analysed their occurrence in a crop (Brassica napus) and a wild plant (Rubus fruticosus agg.), which was flowering in field edges. Nectar and pollen from both plants were collected from five spring and five winter sown B. napus fields in Ireland, and were tested for pesticide residues, using QuEChERS and Liquid Chromatography tandem mass spectrometry (LC-MS/MS). Pesticide residues were detected in plant pollen and nectar of both plants. Most detections were from fields with no recorded application of the respective compounds in that year, but higher concentrations were observed in recently treated fields. Overall, more residues were detected in B. napus pollen and nectar than in the wild plant, and B. napus pollen had the highest mean concentration of residues. All matrices were contaminated with at least three compounds, and the most frequently detected compounds were fungicides. The most common compound mixture was comprised of the fungicides azoxystrobin, boscalid, and the neonicotinoid insecticide clothianidin, which was not recently applied on the fields. Our results indicate that persistent compounds like the neonicotinoids, should be continuously monitored for their presence and fate in the field environment. The toxicological evaluation of the compound mixtures identified in the present study should be performed, to determine their impacts on foraging insects that may be exposed to them.

Glyphosate used as desiccant contaminates plant pollen and nectar of non-target plant species.

Pesticide products containing glyphosate as a systemic active ingredient are some of the most extensively used herbicides worldwide. After spraying, residues have been found in nectar and pollen collected by bees foraging on treated plants. This dietary exposure to glyphosate could pose a hazard for flower-visiting animals including bees, and for the delivery of pollination services. Here, we evaluated whether glyphosate contaminates nectar and pollen of targeted crops and non-target wild plants. Oilseed rape was selected as focal crop species, and Rubus fruticosus growing in the hedgerows surrounding the crop was chosen as non-target plant species. Seven fields of oilseed rape, where a glyphosate-based product was applied, were chosen in east and southeast Ireland, and pollen and nectar were extracted from flowers sampled from the field at various intervals following glyphosate application. Pollen loads were taken from honeybees and bumblebees foraging on the crop at the same time. Glyphosate and aminomethylphosphonic acid (AMPA) residues were extracted using acidified methanol and their concentrations in the samples were determined by a validated liquid chromatography tandem mass spectrometry (LC-MS/MS) method. Glyphosate was detected in R. fruticosus nectar and pollen samples that were taken within a timeframe of two to seven days after the application on the crop as a desiccant. No glyphosate was detected when the application took place before or more than two months prior to our sampling in any of the evaluated matrices. The metabolite AMPA was not detected in any samples. To gain further insight into the potential extent of translocation within both plants and soil when a crop is desiccated using glyphosate before harvesting, and the potential impacts on bees, we recommend a longitudinal study of the presence and fate of glyphosate in non-target flowering plants growing nearby crop fields, over a period of several days after glyphosate application.

Bumblebees can be Exposed to the Herbicide Glyphosate when Foraging.

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. Environ Toxicol Chem 2022;41:2603-2612. © 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Plant protection product residues in plant pollen and nectar: A review of current knowledge.

Exposure to Plant Protection Products, PPPs, (fungicides, herbicides and insecticides) is a significant stressor for bees and other pollinators, and has recently been the focus of intensive debate and research. Specifically, exposure through contaminated pollen and nectar is considered pivotal, as it presents the highest risk of PPP exposure across all bee species. However, the actual risk that multiple PPP residues might pose to non-target species is difficult to assess due to the lack of clear evidence of their actual concentrations. To consolidate the existing knowledge of field-realistic residues detected in pollen and nectar directly collected from plants, we performed a systematic literature review of studies over the past 50 years (1968-2018). We found that pollen was the matrix most frequently evaluated and, of the compounds investigated, the majority were detected in pollen samples. Although the overall most studied category of PPPs were the neonicotinoid insecticides, the compounds with the highest median concentrations of residues in pollen were: the broad spectrum carbamate carbofuran (1400 ng/g), the fungicide and nematicide iprodione (524 ng/g), and the organophosphate insecticide dimethoate (500 ng/g). In nectar, the highest median concentration of PPP residues detected were dimethoate (1595 ng/g), chlorothalonil (76 ng/g), and the insecticide phorate (53.5 ng/g). Strong positive correlation was observed between neonicotinoid residues in pollen and nectar of cultivated plant species. The maximum concentrations of several compounds detected in nectar and pollen were estimated to exceed the LD50s for honey bees, bumble bees and four solitary bee species, by several orders of magnitude. However, there is a paucity of information for the biggest part of the world and there is an urgent need to expand the range of compounds evaluated in PPP studies.