Pollen nutrition structures bee and plant community interactions.

As bees' main source of protein and lipids, pollen is critical for their development, reproduction, and health. Plant species vary considerably in the macronutrient content of their pollen, and research in bee model systems has established that this variation both modulates performance and guides floral choice. Yet, how variation in pollen chemistry shapes interactions between plants and bees in natural communities is an open question, essential for both understanding the nutritional dynamics of plant-pollinator mutualisms and informing their conservation. To fill this gap, we asked how pollen nutrition (relative protein and lipid content) sampled from 109 co-flowering plant species structured visitation patterns observed among 75 subgenera of pollen-collecting bees in the Great Basin/Eastern Sierra region (USA). We found that the degree of similarity in co-flowering plant species' pollen nutrition predicted similarity among their visitor communities, even after accounting for floral morphology and phylogeny. Consideration of pollen nutrition also shed light on the structure of this interaction network: Bee subgenera and plant genera were arranged into distinct, interconnected groups, delineated by differences in pollen macronutrient values, revealing potential nutritional niches. Importantly, variation in pollen nutrition alone (high in protein, high in lipid, or balanced) did not predict the diversity of bee visitors, indicating that plant species offering complementary pollen nutrition may be equally valuable in supporting bee diversity. Nutritional diversity should thus be a key consideration when selecting plants for habitat restoration, and a nutritionally explicit perspective is needed when considering reward systems involved in the community ecology of pollination.

Impacts of soil nutrition on floral traits, pollinator attraction, and fitness in cucumbers (Cucumis sativus L.).

Annual plants allocate soil nutrients to floral display and pollinator rewards to ensure pollination success in a single season. Nitrogen and phosphorus are critical soil nutrients whose levels are altered by intensive land use that may affect plants' fitness via pollinator attractiveness through floral display and rewards. In a controlled greenhouse study, we studied in cucumbers (Cucumis sativus) how changes in soil nitrogen and phosphorus influence floral traits, including nectar and pollen reward composition. We evaluated how these traits affect bumble bee (Bombus impatiens, an important cucumber pollinator) visitation and ultimately fruit yield. While increasing nitrogen and phosphorus increased growth and floral display, excess nitrogen created an asymptotic or negative effect, which was mitigated by increasing phosphorus. Male floral traits exhibited higher plasticity in responses to changes in soil nutrients than female flowers. At 4:1 nitrogen:phosphorus ratios, male flowers presented increased nectar volume and pollen number resulting in increased bumble bee visitation. Interestingly, other pollinator rewards remained consistent across all soil treatments: male and female nectar sugar composition, female nectar volume, and pollen protein and lipid concentrations. Therefore, although cucumber pollination success was buffered in conditions of nutrient stress, highly skewed nitrogen:phosphorus soil ratios reduced plant fitness via reduced numbers of flowers and reward quantity, pollinator attraction, and ultimately yield.

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.

Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences.

To fuel their activities and rear their offspring, foraging bees must obtain a sufficient quality and quantity of nutritional resources from a diverse plant community. Pollen is the primary source of proteins and lipids for bees, and the concentrations of these nutrients in pollen can vary widely among host-plant species. Therefore we hypothesized that foraging decisions of bumble bees are driven by both the protein and lipid content of pollen. By successively reducing environmental and floral cues, we analyzed pollen-foraging preferences of Bombus impatiens in (i) host-plant species, (ii) pollen isolated from these host-plant species, and (iii) nutritionally modified single-source pollen diets encompassing a range of protein and lipid concentrations. In our semifield experiments, B impatiens foragers exponentially increased their foraging rates of pollen from plant species with high protein:lipid (P:L) ratios; the most preferred plant species had the highest ratio (∼4.6:1). These preferences were confirmed in cage studies where, in pairwise comparisons in the absence of other floral cues, B impatiens workers still preferred pollen with higher P:L ratios. Finally, when presented with nutritionally modified pollen, workers were most attracted to pollen with P:L ratios of 5:1 and 10:1, but increasing the protein or lipid concentration (while leaving ratios intact) reduced attraction. Thus, macronutritional ratios appear to be a primary factor driving bee pollen-foraging behavior and may explain observed patterns of host-plant visitation across the landscape. The nutritional quality of pollen resources should be taken into consideration when designing conservation habitats supporting bee populations.

Effects of the herbicide dicamba on nontarget plants and pollinator visitation.

Nearly 80% of all pesticides applied to row crops are herbicides, and these applications pose potentially significant ecotoxicological risks to nontarget plants and associated pollinators. In response to the widespread occurrence of weed species resistant to glyphosate, biotechnology companies have developed crops resistant to the synthetic-auxin herbicides dicamba and 2,4-dichlorophenoxyacetic acid (2,4-D); and once commercialized, adoption of these crops is likely to change herbicide-use patterns. Despite current limited use, dicamba and 2,4-D are often responsible for injury to nontarget plants; but effects of these herbicides on insect communities are poorly understood. To understand the influence of dicamba on pollinators, the authors applied several sublethal, drift-level rates of dicamba to alfalfa (Medicago sativa L.) and Eupatorium perfoliatum L. and evaluated plant flowering and floral visitation by pollinators. The authors found that dicamba doses simulating particle drift (≈1% of the field application rate) delayed onset of flowering and reduced the number of flowers of each plant species; however, plants that did flower produced similar-quality pollen in terms of protein concentrations. Further, plants affected by particle drift rates were visited less often by pollinators. Because plants exposed to sublethal levels of dicamba may produce fewer floral resources and be less frequently visited by pollinators, use of dicamba or other synthetic-auxin herbicides with widespread planting of herbicide-resistant crops will need to be carefully stewarded to prevent potential disturbances of plant and beneficial insect communities in agricultural landscapes.