Diverse pollen nutrition can improve the development of solitary bees but does not mitigate negative pesticide impacts.

Floral resource loss and pesticide exposure are major threats to bees in intensively managed agroecosystems, but interactions among these drivers remain poorly understood. Altered composition and lowered diversity of pollen nutrition may reinforce negative pesticide impacts on bees. Here we investigated the development and survival of the solitary bee Osmia bicornis provisioned with three different pollen types, as well as a mixture of these types representing a higher pollen diversity. We exposed bees of each nutritional treatment to five pesticides at different concentrations in the laboratory. Two field-realistic concentrations of three nicotinic acetylcholine receptor (nAChR) modulating insecticides (thiacloprid, sulfoxaflor and flupyradifurone), as well as of two fungicides (azoxystrobin and tebuconazole) were examined. We further measured the expression of two detoxification genes (CYP9BU1, CYP9BU2) under exposure to thiacloprid across different nutrition treatments as a potential mechanistic pathway driving pesticide-nutrition interactions. We found that more diverse pollen nutrition reduced development time, enhanced pollen efficacy (cocoon weight divided by consumed pollen weight) and pollen consumption, and increased weight of O. bicornis after larval development (cocoon weight). Contrary to fungicides, high field-realistic concentrations of all three insecticides negatively affected O. bicornis by extending development times. Moreover, sulfoxaflor and flupyradifurone also reduced pollen efficacy and cocoon weight, and sulfoxaflor reduced pollen consumption and increased mortality. The expression of detoxification genes differed across pollen nutrition types, but was not enhanced after exposure to thiacloprid. Our findings highlight that lowered diversity of pollen nutrition and high field-realistic exposure to nAChR modulating insecticides negatively affected the development of O. bicornis, but we found no mitigation of negative pesticide impacts through increased pollen diversity. These results have important implications for risk assessment for bee pollinators, indicating that negative effects of nAChR modulating insecticides to developing solitary bees are currently underestimated.

Pollen-feeding behavior of diverse insects on Geranium delavayi, a flower with large, accessible pollen grains.

PREMISE: Why have pollen grains evolved to be exceptionally large in some species? Pollen-feeding hypothesis suggests that if the proportion of pollen amounts for feeding is reduced in a flower, the low allocation to pollen number would allow pollen grains to be larger. METHODS: To examine whether species with large pollen grains experience low pollen consumption, the behavior of insects feeding on nectar and pollen was observed and pollen transfer efficiency was estimated for four visitor types in Geranium delavayi. To see whether bees actively collected pollen, the numbers of grains in pollen baskets and on the body were compared. Both nutritional value (total protein and lipid) and chemical defense (phenolic metabolites) in pollen against pollen feeders were measured. RESULTS: Bumblebees and honeybees foraged for nectar, rarely groomed pollen into corbiculae, and had >5× higher pollen transfer efficiency than smaller solitary bees and flies, which were pollen eaters that removed more pollen but deposited less. Pollen grains were characterized by low protein and high lipid content with a low protein-lipid ratio, an unfavorable combination for bumblebees. Three secondary metabolites were significantly higher in pollen grains (7.77 mg/g) than in petals (1.08 mg/g) or in nectar (0.44 mg/g), suggesting stronger chemical defense in pollen. CONCLUSIONS: Our results indicated that large bees took nectar but little of the nutritionally poor and highly toxic pollen. These data support one prediction of the pollen-feeding hypothesis, that species with few and large pollen grains would also have low pollen-consumption rates.

Bee community preference for an invasive thistle associated with higher pollen protein content.

Non-native plant species reliant on insect pollination must attract novel pollinators in their introduced habitat to reproduce. Indeed, pollination services provided by resident floral visitors may contribute to the spread of non-native species, which may then affect the pollination services received by native plants. To determine the mechanisms by which an invasive thistle attracts pollinators in its introduced range, and whether its presence changes the pollinator visitation to native plant species, we compared bee visitation to native plants in the presence or absence of the invader. We experimentally tested the effect of a thistle invasion into a native plant community. We found that the non-native thistle was the most attractive of the plant species to visiting bee species. However, there was no effect of experimental treatment (presence of thistle) on bee abundance or visitation rate (bees per unit floral area per sample) to native plant species. Across 68 bee and 6 plant species, we found a significant correlation between pollen protein content and bee abundance and visitation rate. Thistle pollen also had a similar protein:lipid ratio to legumes, which correlated with bumble bee visitation. The high protein content of the thistle pollen, as compared to four native asters, may allow it to attract pollinators in novel ecosystems, and potentially contribute to its success as an invader. At the same time, this high protein pollen may act as a novel resource to pollinators in the thistle's invaded range.