A century of wild bee sampling: historical data and neural network analysis reveal ecological traits associated with species loss.

We analysed the wild bee community sampled from 1921 to 2018 at a nature preserve in southern Michigan, USA, to study long-term community shifts in a protected area. During an intensive survey in 1972 and 1973, Francis C. Evans detected 135 bee species. In the most recent intensive surveys conducted in 2017 and 2018, we recorded 90 species. Only 58 species were recorded in both sampling periods, indicating a significant shift in the bee community. We found that the bee community diversity, species richness and evenness were all lower in recent samples. Additionally, 64% of the more common species exhibited a more than 30% decline in relative abundance. Neural network analysis of species traits revealed that extirpation from the reserve was most likely for oligolectic ground-nesting bees and kleptoparasitic bees, whereas polylectic cavity-nesting bees were more likely to persist. Having longer phenological ranges also increased the chance of persistence in polylectic species. Further analysis suggests a climate response as bees in the contemporary sampling period had a more southerly overall distribution compared to the historic community. Results exhibit the utility of both long-term data and machine learning in disentangling complex indicators of bee population trajectories.

High pesticide exposure and risk to bees in pollinator plantings adjacent to conventionally managed blueberry fields.

Wildflower plantings adjacent to agricultural fields provide diverse floral resources and nesting sites for wild bees. However, their proximity to pest control activities in the crop may result in pesticide exposure if pesticides drift into pollinator plantings. To quantify pesticide residues in pollinator plantings, we sampled flowers and soil from pollinator plantings and compared them to samples from unenhanced field margins and crop row middles. At conventionally managed farms, flowers from pollinator plantings had similar exposure profiles to those from unenhanced field margins or crop row middles, with multiple pesticides and high and similar risk quotient (RQ) values (with pollinator planting RQ: 3.9; without pollinator planting RQ: 4.0). Whereas samples from unsprayed sites had significantly lower risk (RQ: 0.005). Soil samples had overall low risk to bees. Additionally, we placed bumble bee colonies (Bombus impatiens) in field margins of crop fields with and without pollinator plantings and measured residues in bee-collected pollen. Pesticide exposure was similar in pollen from sites with or without pollinator plantings, and risk was generally high (with pollinator planting RQ: 0.5; without pollinator planting RQ: 1.1) and not significant between the two field types. Risk was lower at sites where there was no pesticide activity (RQ: 0.3), but again there was no significant difference between management types. The insecticide phosmet, which is used on blueberry farms for control of Drosophila suzukii, accounted for the majority of elevated risk. Additionally, analysis of pollen collected by bumble bees found no significant difference in floral species richness between sites with or without pollinator plantings. Our results suggest that pollinator plantings do not reduce pesticide risk and do not increase pollen diversity collected by B. impatiens, further highlighting the need to reduce exposure through enhanced IPM adoption, drift mitigation, and removal of attractive flowering weeds prior to insecticide applications.

Identity and diversity of pollens collected by two managed bee species while in blueberry fields for pollination.

The nutritional needs and foraging behavior of managed bees often lead to pollen collection from flowers other than the focal crop during crop pollination. To understand the pollen needs and preferences of managed bees during blueberry pollination, we identified pollen collected by Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae) and Bombus impatiens Cresson, 1863 (Hymenoptera: Apidae) colonies across two years. Bumble bees collected a wider diversity of pollens compared to honey bees, whereas honey bees were more focused on abundant resources. Despite blueberries being the most abundant resource in the landscape, it was not the most collected pollen by either bee species in 2018. However, it was the most collected pollen by bumble bees in 2019 and they collected substantially more blueberry pollen than honey bees in both years. In 2018, buckthorn, Rhamnus L. (Rosales: Rhamnaceae) or Frangula Mill. (Rosales: Rhamnaceae), and willow, Salix L. (Malpighiales: Salicaceae), pollens were abundantly collected by both bee species. In 2019, cherry, Prunus L. (Rosales: Rosaceae), and willow (Salix) pollens were collected at high proportions by both species. Brambles, Rubus L. (Rosales: Rosaceae), and white clover, Trifolium repens L. (Fabales: Fabaceae), were also common pollen sources for honey bees, whereas oak, Quercus L. (Fagales: Fagaceae), was collected by bumble bees. Landscape analyses also revealed that certain land cover types were positively correlated with the collection of preferred pollen types. Herbaceous wetlands were associated with collection of buckthorn (Rhamnus/Frangula), willow (Salix), and cherry (Prunus) pollen, which were primary pollen resources for both bee species. There was no correlation between landscape diversity and pollen diversity, suggesting that colonies forage based on nutritional requirements rather than resource availability.

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

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.

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

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.

The European wool-carder bee (Anthidium manicatum) eavesdrops on plant volatile organic compounds (VOCs) during trichome collection.

The plant-pollinator relationship is generally considered mutualistic. This relationship is less clear, however, when pollinators also cause tissue damage. Some Megachilidae bees collect plant material for nests from the plants they pollinate. In this study, we examined the relationship between Anthidium manicatum, the European wool-carder bee, and the source of its preferred nesting material - Stachys byzantina, lamb's ear. Female A. manicatum use their mandibles to trim trichomes from plants for nesting material (a behaviour dubbed "carding"). Using volatile organic compound (VOC) headspace analysis and behavioural observations, we explored (a) how carding effects S. byzantina and (b) how A. manicatum may choose specific S. byzantina plants. We found that removal of trichomes leads to a dissimilar VOC bouquet compared to intact leaves, with a significant increase in VOC detection following damage. A. manicatum also visit S. byzantina plants with trichomes removed at a greater frequency compared to plants with trichomes intact. Our data suggest that A. manicatum eavesdrop on VOCs produced by damaged plants, leading to more carding damage for individual plants due to increased detectability by A. manicatum. Accordingly, visitation by A. manicatum to S. byzantina may incur both a benefit (pollination) and cost (tissue damage) to the plant.