Where Does Honey Bee (Apis mellifera L.) Pollen Come from? A Study of Pollen Collected from Colonies at Ornamental Plant Nurseries.

Ornamental nursery plants are both a major agricultural industry in the U.S. and a major feature of the urban and suburban landscape. Interest in their relationship with pollinators is two-fold: the extent to which they provide a nutritional benefit to pollinators, and the extent to which they have the potential to harm pollinators by exposing them to pesticide residues in nectar and pollen. We identified plant genera as sources of trapped pollen collected by honey bee colonies located at commercial ornamental plant nurseries in Connecticut in 2015 and 2018 and quantified the percentage of pollen volume collected from each genus for each weekly sample over two seasons. Plant genera grown at these nurseries, particularly Rosa, Rhus, and Ilex, contributed substantially to pollen volume during weeks 23-27 of the year. Among the genera not grown in nurseries, Toxicodendron was also important during weeks 23 and 24, and Trifolium was important in both frequency and quantity throughout the season. Zea was a major component of pollen volume from weeks 28-36 in both sites, even though cropland was not over 11% of land cover at either site.

Effects of the Neonicotinoid Acetamiprid in Pollen on Bombus impatiens Microcolony Development.

Honey bees and other wild bee species including bumble bees have experienced population declines in recent decades. Although many stressors are implicated in bee population declines, much attention has focused on neonicotinoid pesticides, which are widely used and known to be toxic to pollinators. One neonicotinoid, acetamiprid, has been studied very little in bumble bees, despite its use on bumble bee-pollinated crops. We assessed the impacts of acetamiprid to the North American bumble bee Bombus impatiens using the microcolony model. We examined nest growth, development, and subsequent nest productivity as measured by drone production. We found that high concentrations of acetamiprid in pollen (4520 µg/kg) significantly impacted nest growth, development, and, ultimately, reproduction (drone production). We found the no-observable-adverse effect level to be 45.2 µg/kg. Overall, acetamiprid has the potential to negatively impact reproductive endpoints for B. impatiens. However, effects occurred at concentrations substantially higher than expected environmental concentrations that would be achieved when following label rates. Further work is required to assess the effects of this pesticide on B. impatiens via alternate routes of exposure and on queenright colonies. Environ Toxicol Chem 2020;39:2560-2569. © 2020 SETAC. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

A screening-level assessment of the pollinator-attractiveness of ornamental nursery stock using a honey bee foraging assay.

In urban and suburban landscapes characterized by extensive designed greenspaces, the support of pollinator communities hinges significantly on floral resources provided by ornamental plants. The attractiveness of ornamental plants to pollinators, however, cannot be presumed, and some studies suggest that a majority of ornamental plant varieties receive little or no pollinator visitation. Here, we harness the sampling power of the western honey bee, a generalist pollinator whose diet breadth overlaps substantially with that of other pollinators, to survey the utilization of ornamental plants grown at three commercial nurseries in Connecticut, USA. Using a combination of DNA metabarcoding and microscopy, we identify, to genus-level, pollen samples from honey bee colonies placed within each nursery, and we compare our results with nursery plant inventories to identify the subset of cultivated genera that were visited during pollen foraging. Samples were collected weekly from May to September, encompassing the majority of the growing season. Our findings show that some plant genera known to be cultivated as ornamentals in our system, particularly ornamental trees and shrubs (e.g. Hydrangea, Rosa, Spiraea, Syringa, Viburnum), functioned as major pollen sources, but the majority of plants inventoried at our nurseries provided little or no pollen to honey bees. These results are in agreement with a growing body of literature highlighting the special importance of woody plants as resources for flower-visiting insects. We encourage further exploration of the genera highlighted in our data as potential components of pollinator-friendly ornamental greenspace.

Tracking Pesticide Residues to a Plant Genus Using Palynology in Pollen Trapped from Honey Bees (Hymenoptera: Apidae) at Ornamental Plant Nurseries.

Worldwide studies have used the technique of pollen trapping, collecting pollen loads from returning honey bee (Apis mellifera L.) (Hymenoptera: Apidae) foragers, to evaluate the exposure of honey bees to pesticides through pollen and as a biomonitoring tool. Typically, these surveys have found frequent contamination of pollen with multiple pesticides, with most of the estimated risk of acute oral toxicity to honey bees coming from insecticides. In our survey of pesticides in trapped pollen from three commercial ornamental plant nurseries in Connecticut, we found most samples within the range of acute toxicity in a previous state pollen survey, but a few samples at one nursery with unusually high acute oral toxicity. Using visual sorting by color of the pollen pellets collected in two samples from this nursery, followed by pesticide analysis of the sorted pollen and palynology to identify the plant sources of the pollen with the greatest acute toxicity of pesticide residues, we were able to associate pollen from the plant genus Spiraea L. (Rosales: Rosaceae) with extraordinarily high concentrations of thiamethoxam and clothianidin, and also with high concentrations of acephate and its metabolite methamidophos. This study is the first to trace highly toxic pollen collected by honey bees to a single plant genus. This method of tracking high toxicity pollen samples back to potential source plants could identify additional high-risk combinations of pesticide application methods and timing, movement into pollen, and attractiveness to bees that would be difficult to identify through modeling each of the contributing factors.

Correction: Using a Hazard Quotient to Evaluate Pesticide Residues Detected in Pollen Trapped from Honey Bees (Apis mellifera) in Connecticut.

[This corrects the article DOI: 10.1371/journal.pone.0077550.].

Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut.

Analysis of pollen trapped from honey bees as they return to their hives provides a method of monitoring fluctuations in one route of pesticide exposure over location and time. We collected pollen from apiaries in five locations in Connecticut, including urban, rural, and mixed agricultural sites, for periods from two to five years. Pollen was analyzed for pesticide residues using a standard extraction method widely used for pesticides (QuEChERS) and liquid chromatography/mass spectrometric analysis. Sixty pesticides or metabolites were detected. Because the dose lethal to 50% of adult worker honey bees (LD50) is the only toxicity parameter available for a wide range of pesticides, and among our pesticides there were contact LD50 values ranging from 0.006 to >1000 µg per bee (range 166,000X), and even among insecticides LD50 values ranged from 0.006 to 59.8 µg/bee (10,000X); therefore we propose that in studies of honey bee exposure to pesticides that concentrations be reported as Hazard Quotients as well as in standard concentrations such as parts per billion. We used both contact and oral LD50 values to calculate Pollen Hazard Quotients (PHQ = concentration in ppb ÷ LD50 as µg/bee) when both were available. In this study, pesticide Pollen Hazard Quotients ranged from over 75,000 to 0.01. The pesticides with the greatest Pollen Hazard Quotients at the maximum concentrations found in our study were (in descending order): phosmet, Imidacloprid, indoxacarb, chlorpyrifos, fipronil, thiamethoxam, azinphos-methyl, and fenthion, all with at least one Pollen Hazard Quotient (using contact or oral LD50) over 500. At the maximum rate of pollen consumption by nurse bees, a Pollen Hazard Quotient of 500 would be approximately equivalent to consuming 0.5% of the LD50 per day. We also present an example of a Nectar Hazard Quotient and the percentage of LD50 per day at the maximum nectar consumption rate.

Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo).

There has been recent interest in the threat to bees posed by the use of systemic insecticides. One concern is that systemic insecticides may translocate from the soil into pollen and nectar of plants, where they would be ingested by pollinators. This paper reports on the movement of two such systemic neonicotinoid insecticides, imidacloprid and thiamethoxam, into the pollen and nectar of flowers of squash (Cucurbita pepo cultivars "Multipik," "Sunray" and "Bush Delicata") when applied to soil by two methods: (1) sprayed into soil before seeding, or (2) applied through drip irrigation in a single treatment after transplant. All insecticide treatments were within labeled rates for these compounds. Pollen and nectar samples were analyzed using a standard extraction method widely used for pesticides (QuEChERS) and liquid chromatography mass spectrometric analysis. The concentrations found in nectar, 10 ± 3 ppb (mean ± s.d) for imidacloprid and 11 ± 6 ppb for thiamethoxam, are higher than concentrations of neonicotinoid insecticides in nectar of canola and sunflower grown from treated seed, and similar to those found in a recent study of neonicotinoids applied to pumpkins at transplant and through drip irrigation. The concentrations in pollen, 14 ± 8 ppb for imidacloprid and 12 ± 9 ppb for thiamethoxam, are higher than those found for seed treatments in most studies, but at the low end of the range found in the pumpkin study. Our concentrations fall into the range being investigated for sublethal effects on honey bees and bumble bees.