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Article

Bee Community of Commercial Potato Fields in Michigan and Bombus impatiens Visitation to Neonicotinoid-Treated Potato Plants

Department of Entomology, Michigan State University, East Lansing, MI 48824, USA
*
Author to whom correspondence should be addressed.
Insects 2017, 8(1), 30; https://doi.org/10.3390/insects8010030
Received: 14 November 2016 / Revised: 2 March 2017 / Accepted: 3 March 2017 / Published: 9 March 2017

Abstract

:
We conducted a bee survey in neonicotinoid-treated commercial potato fields using bowl and vane traps in the 2016 growing season. Traps were placed outside the fields, at the field edges, and 10 and 30 m into the fields. We collected 756 bees representing 58 species, with Lasioglossum spp. comprising 73% of all captured bees. We found seven Bombus spp., of which B. impatiens was the only known visitor of potato flowers in our region. The majority of the bees (68%) were collected at the field edges and in the field margins. Blue vane traps caught almost four-times as many bees and collected 30% more species compared to bowl traps. Bee communities did not differ across trap locations but they were different among trap types. We tested B. impatiens visitation to neonicotinoid treated and untreated potato flowers in field enclosures. The amount of time bees spent at flowers and the duration of visits were not significantly different between the two treatments. Our results demonstrate that a diverse assemblage of bees is associated with an agroecosystem dominated by potatoes despite the apparent lack of pollinator resources provided by the crop. We found no difference in B. impatiens foraging behavior on neonicotinoid-treated compared to untreated plants.

1. Introduction

Potato (Solanum tuberosum L., Solanaceae) is the fourth main food-crop in the world after corn, wheat and rice [1], but is the only one of these that is not wind pollinated. It is the leading vegetable crop in the United States in terms of production area and farm-gate value [2]. Pollinators are not required for its commercial production because harvested tubers are vegetative plant parts and the plants are effectively propagated vegetatively. Similarly to many other members in the Solanaceae, it has prominent flowers during about two weeks of its growing season. Flower petals can be various shades of white, purple, pink or blue, and bright yellow cone-shaped anthers in the middle of the flower release pollen when vibrated [3]. Multiple flowers are arranged in inflorescences and flowering plants emit large amounts of methyl phenylacetate, which has a sweet floral fragrance [4]. Since potato flowers do not produce nectar, they attract pollen-collecting insects [5]. A few species of bees (Apoidea: Anthophila) have been recorded visiting potato flowers [3,5,6,7,8,9] but information on bees that can be found in or near potato fields is generally lacking.
Potatoes are grown in large-scale monocultures that lack diverse resources for pollinators [10]. Despite agricultural landscape simplification, about 50–60 species of pollinators have been collected from soybean and corn monocultures, indicating that pollinators use and persist in these agroecosystems [11,12,13]. Potato fields produce temporary flushes of flowers that may attract species of polylectic native bees nesting in nearby undisturbed areas. Native bee conservation efforts require surveys and identification of the pollinator composition found in and near under-sampled regions such as potato fields. The identification of rare bee species, for example, could warrant further detailed research into their use of potatoes that could eventually lead to changes in crop management efforts.
Potatoes, like corn and soybean, are produced commercially with neonicotinoid insecticides to control several arthropod pests [14]. This group of systemic insecticides can persist for weeks in plant tissue and is translocated to flowers [15]. The main neonicotinoid used in Michigan commercial potatoes is imidacloprid, applied as an at-planting drench application to >80% of the acreage in the state [16]. Imidacloprid is often cited as the most toxic of the neonicotinoids to bees and it can readily translocate from seed treatment into nectar and pollen [17,18]. Neonicotinoids can often be detected in pollen samples taken from field collected bees; therefore, contact exposure and oral ingestion can both play key roles in causing lethal and sublethal effects in bees [17,18].
Bumblebees (Apidae: Bombus) are one of the most common and abundant buzz-pollinators in potato growing regions [5], thus they are likely at a risk of pesticide exposure. Although not studied in potato specifically, pesticides can affect bumblebee physiology and behavior. For example, bumblebee foraging behavior was altered by chronic exposure to a neonicotinoid insecticide [19,20] and their fecundity and colony growth was also negatively impacted by neonicotinoid consumption [21,22,23]. While these studies suggest bees may be negatively affected by neonicotinoids, other work suggests that realistic exposures to neonicotinoids in the field do not negatively affect bees and that sublethal effects do not necessarily result in lasting colony effects, especially if pesticide-free alternative forage is available [24,25,26,27,28,29].
Our goals in this study were to (1) survey and identify the bee community in commercial, neonicotinoid-treated potato fields in Michigan and; (2) evaluate the effect of neonicotinoid (imidacloprid) treatment on bumblebee visitation to potato flowers in field enclosures.

2. Materials and Methods

2.1. Bee Community Survey in Neonicotinoid-Treated Commercial Potato Fields

2.1.1. Data Collection

Bees in commercial potato fields were surveyed using bowl and blue vane traps [30,31] in 12 potato fields (‘sites’) from 21 June to 22 July 2016. Site elevation was 255 m, daily average maximum temperature was 27 °C, daily average minimum was 13.5 °C, and total precipitation was 2 mm during the sampling period [32]. Seasonal climate information for this area is available in Figure S1. All potato seeds were treated with imidacloprid (0.02 L/ha active ingredient) 5–7 days pre-planting, and foliar insecticides were applied during the growing season (Table S1). Plants were 7–9 weeks post-planting at the time of sampling and all were ware potatoes used for chips (Table 1). Fields were sampled when 40–100% blooms were open. Traps were collected after 48 h in the field. Sites 1–4 were established on 21 June 2016, and traps were deployed on 23 June 2016 and again on 25 June 2016. Sites 5–8 were established 5 July 2016 and traps were deployed on 7 July 2016. Sites 9–12 were established on 18 July 2016 and traps were deployed on 20 July 2016 and again on 22 July 2016. Sites were 0.8–18.2 km apart (average minimum distance between sites = 3.6 km) and 6–42 ha in size (mean size 21 ± 4 ha, Figure 1 and Table 1).
Sites were located in a region where 45% of the land has been converted to agricultural fields, and deciduous hardwoods comprise about 25% of the landscape (primarily maple (Acer spp.), oak (Quercus spp.), ash (Fraxinus spp.), beech (Fagus spp.), and hemlock (Tsuga spp.); [33]). About 30% of the landscape is either open land or turned into housing developments (urban spaces, open water or wetlands, and treeless meadow areas; [33]). In this region, potato field margins typically contain species of Poaceae (Poa spp., Festuca spp., Lolium spp., Agrostis spp.); Fabaceae (Trifolium spp.); Plantaginaceae (Plantago spp.); Caryophyllaceae (common chickweed, Stellaria media L. Vill.; mouse-ear chickweed, Cerastium fontanum Baumg.; and white campion, Silene latifolia Poir.); Lamiaceae (purple dead-nettle, Lamium purpureum L.); Oxalidaceae (wood sorrel, Oxalis stricta L.); and Asteraceae (e.g., dandelion Taraxacum officinale F.H. Wigg; and other Cichoriae, corn chamomile, Anthemis arvensis L.). In addition, several species of Solanaceae (eastern black nightshade, Solanum ptychanthum Dunal; climbing nightshade, S. dulcamara L.; and Carolina horsenettle, S. carolinense L.) are common weed species in the sampled region that are congeners of the cultivated potato.
Each bowl trap consisted of a 40-cm-diameter circular plastic platform elevated to canopy height, on which three plastic bowls (blue #181677, yellow #14260, and white #14258, Party City Corporation, Rockaway, NJ, USA; 19 cm diameter, 0.35 L) were glued. The platforms were attached to the tops of 1-m metal conduits (2 cm diameter) that were pounded into the soil. At the beginning of each 48-h sampling period, bowls were filled to capacity with soapy water (Dawn® dish soap, unscented, colorless, Procter & Gamble, Cincinnati, OH, USA). Each blue vane trap (SpringStar LLC, Woodinville, WA, USA) consisted of a blue vane and 2 L collection container suspended on a metal pole at canopy height. Containers were filled with approximately 1 L of 1:1 propylene glycol:water solution. Traps were set out in transects of four traps with the first located in vegetation outside the potato field (roughly 10 m from the field edge), the second at the potato field edge, the third 10 m into the field, and the fourth 30 m into the potato field (Figure 2). We chose potato field edges that were near mixed hardwoods (about 30 m away from the potatoes). Between the potato field and the woods was a 5–10 m wide strip of mowed grasses and forbs. The average size of wooded areas in this region was 2 km2, and the average width of treeless meadow areas adjacent to potato fields was 5–10 m, running the length of the cropped area. Each field had one transect of bowl and one transect of blue vane traps 10 m apart. Bees were collected by pouring the trap solution through a strainer and placing all insects into zip top bags that were labeled with collection location, type of trap, and date of collection. Trapped insects were frozen initially, then placed into vials with 70% ethanol for storage. Bees were dried to restore pubescence before being pinned, databased, and labeled with collection information. Bees were identified to species using published keys [34,35,36,37,38,39] and reference material in the A. J. Cook Arthropod Research Collection (Michigan State University). Voucher specimens are deposited at Michigan State University.

2.1.2. Statistical Analysis

Bee abundance was analyzed with a generalized nonlinear mixed effects model using the ‘glmer’ function in the ‘lme4’ package [40] in R version 3.2.2 [41]. The model was fit with a Poisson distribution after visual assessment of the count data. The total number of bees collected was analyzed in response to trap type and trap location, with site and date as random factors. Inclusion of both site and date accounted for some sites receiving fewer collection periods than others, and for non-independence between sites receiving two collection deployments. Significant main effects at α = 0.05 were followed by pairwise comparisons using Tukey’s HSD.
Non-metric multidimensional scaling was used to visualize similarities among bee communities for each trap type and field location, summed across all sites and dates. Bray-Curtis distances among communities were analyzed using the ‘adonis’ function in the ‘vegan’ package [42] in R. Goodness-of-fit was estimated with stress (S) and fit (adonis R) values. Species vectors were fitted to the NMDS using the ‘envfit’ function in the ‘vegan’ package [42]. Shannon-Weiner diversity indices were calculated for bee communities across trap types. An indicator species analysis was conducted to determine if any particular species were strongly associated with any trap type or trap location. Analysis was conducted using the ‘indval’ function in the ‘labdsv’ package [43], generating indicator values for each species.
To confirm that bee communities were sufficiently sampled, species accumulation curves were generated using the ‘specaccum’ function in the ‘vegan’ package [11]. Random resampling with 100 permutations estimated the number of species expected as sampling increased [44]. Species accumulation curves were generated for the entire experiment and for each trap type.

2.2. Bumblebee Potato Flower Visitation

2.2.1. Data Collection

Potato (Solanum tuberosum L. var. Atlantic) plants were grown in the greenhouse at Michigan State University, East Lansing, MI from seed potatoes in 12 cm diameter plastic pots in a perlite soil mix (Suremix Perlite, Michigan Grower Products Inc., Galesburg, MI, USA). Plants were fertilized weekly with a 5 g/L 20-20-20 N-P-K (Scott’s Miracle-Grow Products, Inc., Marysville, OH, USA) solution. When plants first started emerging from the soil, each pot received 18.7 µL Admire Pro® (imidacloprid, Bayer Crop Science, Monheim am Rhein, Germany; equivalent to the high label rate of 0.36 L/ha active ingredient) diluted in 20 mL distilled water. The experiment was replicated over two time periods (4 replications/period, N = 8) in the summer of 2016. Half of the plants received imidacloprid on 9 June 2016, and bee visitation observations were conducted between 11 July and 14 July 2016. Half of the plants in the second time period received imidacloprid on 24 June 2016, and visitation observations were conducted between 22 July and 27 July 2016. Plants that were starting to flower (10–20% open bloom) were moved from the greenhouse to outdoor enclosures at the Entomology Research Farm at Michigan State University, East Lansing, MI, USA. Four 1.8 × 1.8 × 1.8 m mesh enclosures each contained 10 plants (five imidacloprid-treated and five untreated plants placed randomly within the enclosure) and one bumblebee (Bombus impatiens Cresson, Hymenoptera: Apidae) colony. MINIPOL® colony boxes were obtained from Koppert Biological Systems™ Inc., (Berkel en Rodenrijs, The Netherlands), shipped overnight from Howell, MI, USA. Each box contained one small colony of 10–15 individuals. Colony boxes were placed immediately into the enclosures upon arrival to Michigan State University and visitation observations began 2–5 days later when bees were acclimated to their new surroundings.
Observations were conducted each morning from 8 to 9 a.m. with one observer rotating among the four cages for one hour, counting bee visits to flowers and noting plant treatment. Duration of observations was limited to one minute per cage before moving to the next cage to limit counting the same bee multiple times. Observations were conducted during peak bloom (50–100% open bloom) and ceased when flowers began to drop. After the 1 h observation period, floral visit duration was recorded for 10–20 additional pollinator visits. On 14 July 2016, flowers and aboveground vegetative material were collected from two treated and two untreated plants per cage, dried, and weighed. Samples of flower and plant tissue were analyzed at Michigan State University for imidacloprid using the QuEChERS method [45].

2.2.2. Statistical Analysis

Dry biomass of flowers per plant and plant tissue per plant, visitation frequency (total visits/hour for each trial, square-root transformed) and visitation duration (seconds/visit, log-transformed) were each analyzed with a linear mixed effects model, using the ‘lme’ function in the ‘nlme’ package [46] in R. Data transformation were performed so that distributions of residuals met the assumptions of linear models, confirmed by quantile-quantile plots. Models included imidacloprid treatment as a fixed factor, and date and enclosure (frequency analysis only) as random factors. For effects 0.5 > p > 0.1, a power analysis using the ‘pwr’ package [47] was performed to estimate the effect size needed to observe significant differences at α = 0.5 with our sample size.

3. Results

3.1. Bee Community Survey in Commercial Potato Fields

Fifty-eight species of bees from 16 genera and five families were captured in potato field traps (Table 2). Lasioglossum spp. (Halictidae) comprised 73% of all bees captured. Most bees in our samples were host plant generalists except for four species of the family Apidae: Melissodes agilis Cresson (specialist on Helianthus spp., Asteraceae), M. desponsus Smith (specialist on Cirsium spp., Asteraceae), M. subillatus LaBerge (specialist on Asteraceae), and Peponapis pruinosa (Say) (specialist on Cucurbitaceae, [48]). In addition to the European honeybee Apis mellifera L., we found two exotic, but naturalized species, Lasioglossum zonulum (Smith) and L. leucozonium (Schrank) [48], but all other sampled species are native in our area. Ground nesting bees comprised 74% of all species; we found just a few species that nest in cavities, plant stems, or rotting wood (Table 2). The proportion of eusocial (28 species) to solitary species (26 species) was about equal in our samples.
Out of the 756 bees we collected, 68% were found in traps placed either at the field edge or in the border outside the field (Table S2). There was an interactive effect of trap type and trap location (interaction: χ2 = 36.7, df = 9, p < 0.001; trap type: χ2 = 315.6, df = 3, p < 0.001; trap location: χ2 = 88.9, df = 4, p < 0.001). Blue vane traps caught almost four-times as many bees as the bowls, and this effect was greatest in the bordering vegetation and at the potato field edge (Figure 3 and Table S3). Blue vane traps captured 438 individuals representing 41 species. Blue bowl traps captured 103 individuals representing 27 species. White bowl traps captured 116 individuals representing 28 species. Yellow bowl traps captured 105 individuals representing 29 species (Table S3).
Bee communities did not differ across trap location within field (S = 0.2, R2 = 0.2, F = 1.1, df = 3, p = 0.4), but differed across trap types (S = 0.2, R2 = 0.3, F = 2.0, df = 3, p < 0.001). Species with significant NMDS scores were Apis mellifera (r2 = 0.5, p = 0.02), Bombus fervidus (Fabricius) (r2 = 0.6, p = 0.001), Lasioglossum bruneri (Crawford) (r2 = 0.4, p = 0.04), L. imitatum (Smith) (r2 = 0.4, p = 0.02), L. lineatulum (Crawford) (r2 = 0.8, p = 0.01), L. zonulum (r2 = 0.3, p = 0.05), Melissodes agilis (r2 = 0.5, p = 0.01), M. bimaculatus (Lepeletier) (r2 = 0.4, p = 0.004), and Peponapis pruinosa (r2 = 0.6, p = 0.003) (all species scores listed in Table S4). All of these species were associated with blue vane traps, except L. bruneri, L. imitatum, and L. lineatulum, which were associated with white and yellow bowl traps (Figure 4). Indicator species values showed that individual species were not significantly associated with any trap type or trap location (Holm-corrected, all species p > 0.07). Shannon-Weiner diversity indices were 2.7-2.9 for all trap types.
Species accumulation curves estimated approximately 60 bee species in these potato fields (Figure 5A); therefore, it seems unlikely that further sampling would add many new species. Bowls appear slower than blue vane traps in accumulating species (Figure 5B).

3.2. Bumblebee Potato Flower Visitation

Visitation frequency and duration were not statistically different between imidacloprid-treated and untreated flowers (p = 0.09, p = 0.8, respectively; Figure 6a,b). Power analysis estimated differences in visitation rates would need to be approximately five times greater to be significant at α = 0.05 with our sample size. Imidacloprid levels were 2.53 ± 0.62 µg/g in leaf tissue and 2.02 ± 0.71 μg/g in flower tissue of treated plants (mean ± SEM). Imidacloprid was not present in leaves or flowers of untreated control plants. The weight of vegetative tissue and floral tissue biomass were not different between imidacloprid-treated and untreated plants (all p > 0.08).

4. Discussion

In our community survey, 58 species of bees were found in or near Michigan potato fields, despite the relative lack of diverse resources in these monocultures. Since most of the trapped species are host generalists, it is likely that at least some of them visit potato flowers, although field visitation observations were not part of this study. Areas around potato fields likely provide nesting and foraging resources for many of these bees. Alternatively, the large flush of flowers offered by hectares of potatoes blooming at the same time may attract bees from distant areas to the field. For example, some bumblebees have a nearly 10 km foraging range [93].
Bumblebees are main pollinators of Solanum spp. in North America, but out of the seven Bombus species we found, Bombus impatiens is the only one that has been confirmed pollinating potato flowers [94]. Five bumblebee species we recorded were also found in surveys of New York potato fields, but these were associated with plants located near the fields [5]. Bombus fervidus, one of the more abundant bumblebees in our samples, was not attracted to potato flowers in a cage experiment [94]. As in our samples, honeybees have been observed in potato fields previously and may be initially interested in potato flowers, but due to the lack of nectar and the honeybees’ inability to buzz-pollinate, these bees are not considered pollinators of potatoes [94].
Lasioglossum was the most diverse genus with 25 species in our samples. These bees are typically polylectic and are known to visit Solanum spp. Although Lasioglossum and some other halictid bee genera we collected are known to buzz-pollinate [95,96], Lasioglossum may be primarily pollen scavengers of Solanum [97], collecting accessible pollen from the flower surface, but providing little pollination benefit. Their visitation to potato flowers is supported by the fact that 27% of Lasioglossum spp. were found in traps 10 and 30 m inside the potato field. In addition, their small body size should result in a short foraging range [98] that implies their ability to nest in and around potato fields. Two species of small Sphecodes, potentially cleptoparasites of Lasioglossum, were also found 10 m into the field. While Lasioglossum was the most diverse genus in our samples, their abundance and species richness responded negatively to pesticides in apples, indicating that these bees are sensitive to pesticide toxicity [99]. Therefore, further studies should explore the interactions of these bees with potatoes and the potential impact of pesticides on them.
Simplified landscapes of non-pollinator dependent crops constitute a substantial proportion of the Midwest US land cover and are blamed, in part, for declining bee populations [100]. Research investigating bee communities within non-pollinator dependent crops is rare; however recent studies in corn, soybean, biofuel crops (corn, switchgrass, mixed prairie species) [11,12,13,101,102], and now potato fields (this study) are improving understanding of bee diversity in non-pollinator dependent crops. Bee abundance and richness is typically lower in intensive crops relative to more diversified habitats [101], however a substantial number of bee species remain in these landscapes. An exhaustive comparison of non-pollinator dependent crops is difficult due to different sampling efforts and the extent of taxonomic resolution among studies, however some similarities are evident. Ground-nesting bees, such as Melissodes and Lasioglossum spp., dominate in these areas as expected given the limited opportunities for cavity-nesters in crop fields. Some stem-nesting species such as Ceratina and Hylaeus remain in low abundance relative to semi-natural areas, although they can be abundant in switchgrass biofuel crops [101]. The bulk of individuals are hyper-generalist foragers that visit flowers across many plant families, including Melissodes bimaculatus, Agapostemon virescens, and Lasioglossum spp., which dominate the few studies identifying bee species in non-pollinator-dependent crop systems [11,12,101,102]. Melissodes bimaculatus, honey bees, and halictid bees, in particular Lasioglossum, are known to use floral resources such as corn and grass pollen [103,104] that are typically avoided by other bees in the region.
Trap type, color, and height can influence wild bee captures [105,106,107,108]. Indeed, we captured mostly Lasioglossum spp. in bowl traps, but the only representatives of Anthophora, Peponapis, and some species of Bombus and Melissodes were collected in blue vane traps. In our study, large-bodied apid bees, such as Bombus, were collected in greater numbers in blue vane traps relative to bowl traps. Blue vane traps are effective at collecting bees, especially large-bodied Apidae, which is consistent with other studies that have employed them [31,105,107,108,109]. In fact, blue vane traps in a simple agricultural landscape (soybean) collected a surprising number of large-bodied apid bees, including oligoleges of non-crop flowers [11]. Oligolectic bees may appear to be positively associated with increasing area of field crops when blue vane traps are used [109]. One possible explanation is that UV-reflecting vane traps have greater relative attractiveness to bees flying in simple landscapes with few resources.
The third-most abundant species in our study, Peponapis pruinosa, is a cucurbit specialist [48], which does not visit potato for pollen but was collected in relatively high abundance in blue vane traps. The presence of oligolectic bees in non-host crop fields should not be interpreted as evidence that they use or persist in those crop fields. They may instead be far-flying species moving between sparse foraging resources that become attracted to the conspicuous traps deployed to capture them. Although oligolectic bees may be found in potato fields, the lack of nectar and suitable pollen rewards mean these bees are unlikely to forage on the neonicotinoid-treated potato plants.
The field survey allowed us to identify bee species associated with Michigan potato fields over the course of a field season, and our manipulative enclosure study provided preliminary insights to potential impacts of neonicotinoid-treated potatoes on the most common potato pollinator, the bumblebee [5]. Sublethal effects of neonicotinoids on bumblebee foraging have been observed [110], but in our study bumblebee visitation to potato flowers with or without neonicotinoid treatment was statistically similar. This may have been due to insufficient sample size, as our power analysis indicated that effect sizes would have had to be five times greater to see significant differences at our current sample size, or due to the fact that insecticide residues in pollen were low and had no measureable impact on foraging behavior. Since the hives were supplied with sugar water and potato flowers do not contain nectar, the only exposure bees had in our study to the neonicotinoid was through contact with potato flowers and ingestion of pollen. Although we did not specifically measure imidacloprid content in pollen, previous results indicate that low levels may have been the underlying cause of the lack of neonicotinoid effect on bees [17,24]. Field studies with neonicotinoid seed-treated crops, such as oil seed rape, sunflower, and corn, have also concluded that exposure to these crops poses low risks to bumblebees, even over several years [26,27,28,111].
Laboratory exposure to imidacloprid-laced food reduced subsequent bumblebee foraging efficiency on pollen, but not on nectar [110]. One hypothesis proposed to explain this was that the insecticide may have impaired the ability of bees to collect pollen [110]. Pollen is important for rearing young workers [112] and if bumblebees are feeding neonicotinoid-laced pollen to their brood, it may result in lower colony growth [21], but several field studies with bumblebees foraging on neonicotinoid-treated plants did not find negative impacts on their offspring [20,23]. Our results from the enclosures should be interpreted with caution, since we had a limited number of colonies (N = 8) and we did not mark bees individually.

5. Conclusions

Our study fills a knowledge gap by providing information on bees found in commercial potato fields. Since much previous attention has been focused on honeybees interacting with neonicotinoids, our contribution on bumblebees adds new details in this area. While further experiments with sufficiently larger sample sizes are needed to confirm our findings, our results are aligned with previous results indicating that many bee species found in potato cropping systems are also represented in other field crops in North America and that bumblebee exposure to imidacloprid-treated flowers did not have significant negative impacts on foraging behavior. Although here we did not measure other potential effects of imidacloprid on bumblebees, in the future, we need to investigate bumblebee colony responses to neonicotinoids under field conditions over several field seasons. This study will provide useful information for future research on the bee fauna in potato fields in other parts of the world.

Supplementary Materials

The following are available online at https://www.mdpi.com/2075-4450/8/1/30/s1, Table S1: Planting and insecticide application dates and rates for field sites; Table S2: The total number of bees by genus and trap location; Table S3: The total number of bees by genus and trap type; Table S4: Ordination scores of bee species; Figure S1: seasonal temperature and precipitation data of field study region.

Acknowledgments

Thanks to the potato growers who allowed access to and trap placement in their fields, and to Mark Otto (Agri-Business Consultants, Inc., Lansing, MI, USA) who helped us locate flowering potato fields. Post-doctoral support for J.G. was made available by funding from the USDA Specialty Crop Research Initiative (2012-51181-20105).

Author Contributions

Zsofia Szendrei conceived and designed the experiments; Amanda L. Buchanan, Zsofia Szendrei, and Lidia Komondy performed the experiments; Amanda L. Buchanan analyzed the data; Jason Gibbs identified specimens; Zsofia Szendrei contributed reagents and materials; Amanda L. Buchanan, Zsofia Szendrei, and Jason Gibbs wrote the paper.

Conflicts of Interest

The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

References

  1. FAO International Year of the Potato. Available online: www.fao.org/potato-2008 (accessed on 11 November 2016).
  2. USDA NASS National Agricultural Statistics Service. Available online: https://www.nass.usda.gov/ (accessed on 12 January 2017).
  3. Buchmann, S.L.; Cane, J.H. Bees assess pollen returns while sonicating Solanum flowers. Oecologia 1989, 81, 289–294. [Google Scholar] [CrossRef]
  4. Karlsson, M.F.; Birgersson, G.; Cotes Prado, A.M.; Bosa, F.; Bengtsson, M.; Witzgall, P. Plant odor analysis of potato: Response of Guatemalan Moth to above- and belowground potato volatiles. J. Agric. Food Chem. 2009, 57, 5903–5909. [Google Scholar] [CrossRef] [PubMed]
  5. Batra, S.W.T. Male-fertile potato flowers are selectively buzz-pollinated only by Bombus terricola Kirby in Upstate New York. J. Kans. Entomol. Soc. 1993, 66, 252–254. [Google Scholar]
  6. Free, J.B. Insect Pollination of Crops; Academic Press: London, UK, 1993. [Google Scholar]
  7. White, J.W. Pollination of potatoes under natural conditions. CIP Circ.—Int. Potato Cent. 1983, 11, 1–2. [Google Scholar]
  8. Marfil, C.F.; Masuelli, R.W. Reproductive ecology and genetic variability in natural populations of the wild potato, Solanum kurtzianum. Plant Biol. 2014, 16, 485–494. [Google Scholar] [CrossRef] [PubMed]
  9. Celis, C.; Scurrah, M.; Cowgill, S.; Chumbiauca, S.; Green, J.; Franco, J.; Main, G.; Kiezebrink, D.; Visser, R.G.F.; Atkinson, H.J. Environmental biosafety and transgenic potato in a centre of diversity for this crop. Nature 2004, 432, 222–225. [Google Scholar] [CrossRef] [PubMed]
  10. Koh, I.; Lonsdorf, E.V.; Williams, N.M.; Brittain, C.; Isaacs, R.; Gibbs, J.; Ricketts, T.H. Modeling the status, trends, and impacts of wild bee abundance in the United States. Proc. Natl. Acad. Sci. USA 2016, 113, 140–145. [Google Scholar] [CrossRef] [PubMed]
  11. Wheelock, M.J.; Rey, K.P.; O’Neal, M.E. Defining the insect pollinator community found in Iowa corn and soybean fields: Implications for pollinator conservation. Environ. Entomol. 2016, 45, 1099–1106. [Google Scholar] [CrossRef] [PubMed]
  12. Gill, K.A.; O’Neal, M.E. Survey of soybean insect pollinators: Community identification and sampling method analysis. Environ. Entomol. 2015, 44, 488–498. [Google Scholar] [CrossRef] [PubMed]
  13. Wheelock, M.J.; O’Neal, M.E. Insect pollinators in Iowa cornfields: Community identification and trapping method analysis. PLoS ONE 2016, 11, e0143479. [Google Scholar] [CrossRef] [PubMed]
  14. Elbert, A.; Haas, M.; Springer, B.; Thielert, W.; Nauen, R. Applied aspects of neonicotinoid uses in crop protection. Pest Manag. Sci. 2008, 64, 1099–1105. [Google Scholar] [CrossRef] [PubMed]
  15. Dively, G.P.; Kamel, A. Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J. Agric. Food Chem. 2012, 60, 4449–4456. [Google Scholar] [CrossRef] [PubMed]
  16. Szendrei, Z. Results of the 2010 Michigan potato pest survey. Mich. Potato Newsline 2011, 22, 4–5. [Google Scholar]
  17. Walters, K.F.A. Neonicotinoids, bees and opportunity costs for conservation. Insect Conserv. Divers. 2016, 9, 375–383. [Google Scholar] [CrossRef]
  18. Blacquière, T.; Smagghe, G.; van Gestel, C.A.M.; Mommaerts, V. Neonicotinoids in bees: A review on concentrations, side-effects and risk assessment. Ecotoxicology 2012, 21, 973–992. [Google Scholar] [CrossRef] [PubMed]
  19. Stanley, D.A.; Raine, N.E. Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants. Funct. Ecol. 2016, 30, 1132–1139. [Google Scholar] [CrossRef] [PubMed]
  20. Stanley, D.A.; Russell, A.L.; Morrison, S.J.; Rogers, C.; Raine, N.E. Investigating the impacts of field-realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth. J. Appl. Ecol. 2016, 53, 1440–1449. [Google Scholar] [CrossRef] [PubMed]
  21. Whitehorn, P.R.; O’Connor, S.; Wackers, F.L.; Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 2012, 336, 351–352. [Google Scholar] [CrossRef] [PubMed]
  22. Laycock, I.; Lenthall, K.M.; Barratt, A.T.; Cresswell, J.E. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 2012, 21, 1937–1945. [Google Scholar] [CrossRef] [PubMed]
  23. Rundlöf, M.; Andersson, G.K.S.; Bommarco, R.; Fries, I.; Hederström, V.; Herbertsson, L.; Jonsson, O.; Klatt, B.K.; Pedersen, T.R.; Yourstone, J.; et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 2015, 521, 77–80. [Google Scholar] [CrossRef] [PubMed]
  24. Pilling, E.; Campbell, P.; Coulson, M.; Ruddle, N.; Tornier, I. A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS ONE 2013, 8, e77193. [Google Scholar] [CrossRef] [PubMed]
  25. EFSA Panel on Plant Protection Products and their Residues (PPR). Scientific opinion on the science behind the development of a risk assessment of Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees): Risk assessment for bees. EFSA J. 2012. [Google Scholar] [CrossRef]
  26. Cutler, G.C.; Scott-Dupree, C.D. A field study examining the effects of exposure to neonicotinoid seed-treated corn on commercial bumble bee colonies. Ecotoxicology 2014, 23, 1755–1763. [Google Scholar] [CrossRef] [PubMed]
  27. Cutler, G.C.; Scott-Dupree, C.D.; Sultan, M.; McFarlane, A.D.; Brewer, L. A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ 2014. [Google Scholar] [CrossRef] [PubMed]
  28. Thompson, H.M.; Wilkins, S.; Harkin, S.; Milner, S.; Walters, K.F. Neonicotinoids and bumblebees (Bombus terrestris): Effects on nectar consumption in individual workers. Pest Manag. Sci. 2015, 71, 946–950. [Google Scholar] [CrossRef] [PubMed]
  29. Elston, C.; Thompson, H.M.; Walters, K.F.A. Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie 2013, 44, 563–574. [Google Scholar] [CrossRef]
  30. Leong, J.M.; Thorp, R.W. Colour-coded sampling: The pan trap colour preferences of oligolectic and nonoligolectic bees associated with a vernal pool plant. Ecol. Entomol. 1999, 24, 329–335. [Google Scholar] [CrossRef]
  31. Stephen, W.P.; Rao, S. Unscented color traps for non-Apis bees (Hymenoptera: Apiformes). J. Kans. Entomol. Soc. 2005, 78, 373–380. [Google Scholar] [CrossRef]
  32. MSU Enviroweather. Available online: https://mawn.geo.msu.edu/ (accessed on 7 January 2017).
  33. USDA-NASS CropScape and Cropland Data Layer. Available online: https://www.nass.usda.gov/Research_and_Science/Cropland/SARS1a.php (accessed on 7 February 2017).
  34. Gibbs, J. Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 2011, 3073, 1–216. [Google Scholar]
  35. Gibbs, J.; Packer, L.; Dumesh, S.; Danforth, B.N. Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in eastern North America (Hymenoptera: Apoidea: Halictidae). Zootaxa 2013, 3672, 1–117. [Google Scholar] [CrossRef]
  36. LaBerge, W.E. A revision of the bees of the genus Melissodes in North and Central America. Part III (Hymenoptera, Apidae). Univ. Kans. Sci. Bull. 1961, 42, 283–663. [Google Scholar]
  37. Mitchell, T.B. Bees of the Eastern United States I. Tech. Bull. N. C. Agric. Exp. Stn. 1960, 141, 1–538. [Google Scholar]
  38. Rehan, S.M.; Sheffield, C.S. Morphological and molecular delineation of a new species in the Ceratina dupla species-group (Hymenoptera: Apidae: Xylocopinae) of eastern North America. Zootaxa 2011, 2873, 35–50. [Google Scholar]
  39. Mitchell, T.B. Bees of the Eastern United States II. Tech. Bull. N. C. Agric. Exp. Stn. 1962, 152, 1–557. [Google Scholar]
  40. Bates, D.; Maechler, M.; Bolker, B.; Walker, S.E. lme4: Linear Mixed-Effects Models Using Eigen and S4. Available online: http://CRAN.R-project.org/package=lme4 (accessed on 14 November 2016).
  41. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2015. [Google Scholar]
  42. Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Wagner, H. Vegan: Community Ecology Package. Available online: http://CRAN.R-project.org/package=vegan (accessed on 14 November 2016).
  43. Roberts, D.A. labdsv: Ordination and Multivariate Analysis for Ecology. Available online: http://CRAN.R-project.org/package=labdsv (accessed on 14 November 2016).
  44. Gotelli, N.J.; Colwell, R.K. Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 2001, 4, 379–391. [Google Scholar] [CrossRef]
  45. Anastassiades, M.; Lehotay, S.J.; Stajnbaher, D.; Schenck, F.J. Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J. AOAC Int. 2003, 86, 412–431. [Google Scholar] [PubMed]
  46. Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D. Nlme: Linear and Nonlinear Mixed Effects Models. Available online: http://CRAN.R-project.org/package=nlme (accessed on 14 November 2016).
  47. Champley, S. pwr: Basic Functions for Power Analysis. Available online: http://CRAN.R-project.org/package=pwr (accessed on 14 November 2016).
  48. Hurd, P.D.J.; Linsley, E.G.; Michelbacher, A.E. Ecology of the Squash and Gourd Bee, Peponapis Pruinosa, on Cultivated Cucurbits in California (Hymenoptera: Apoidea). Smithson. Contrib. Zool. 1974, 168, 1–17. [Google Scholar]
  49. Giles, V.; Ascher, J.S. A survey of the bees of the Black Rock Forest Preserve, New York (Hymenoptera: Apoidea). J. Hymenopt. Res. 2006, 15, 208–231. [Google Scholar]
  50. Hurd, P.D. Superfamily Apoidea. In Catalog of Hymenoptera in America North of Mexico; Smithsonian Institution Press: Washington, DC, USA, 1979. [Google Scholar]
  51. Ashmead, W.H. The habits of the aculeate Hymenoptera IV. Psyche J. Entomol. 1894, 7, 75–79. [Google Scholar] [CrossRef]
  52. Batra, S.W.T. Behavior of the social bee, Lasioglossum zephyrum, within the nest (Hymenoptera: Halictidæ). Insectes Sociaux 1964, 11, 159–185. [Google Scholar] [CrossRef]
  53. Breed, M.D. Life cycle and behavior of a primitively social bee, Lasioglossum rohweri (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 1975, 48, 64–80. [Google Scholar]
  54. Coelho, B.W.T. A review of the bee genus Augochlorella (Hymenoptera: Halictidae: Augochlorini). Syst. Entomol. 2004, 29, 282–323. [Google Scholar] [CrossRef]
  55. Eickwort, G.C. Aspects of the nesting biology of five Nearctic species of Agapostemon (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 1981, 54, 337–351. [Google Scholar]
  56. Eickwort, G.C. First steps into eusociality: The sweat bee Dialictus lineatulus. Fla. Entomol. 1986, 69, 742–754. [Google Scholar] [CrossRef]
  57. Ivanochko, M. Taxonomy, Biology and Alfalfa Pollinating Potential of Canadian Leaf-Cutter Bees--Genus Megachile Latreille (Hymenoptera: Megachilidae); McGill-Queen’s University Press: Montreal, QC, Canada, 1979. [Google Scholar]
  58. Krombein, K.V. Trap-Nesting Wasps and Bees: Life Histories, Nests, and Associates; Smithsonian Press: Washington, DC, USA, 1967. [Google Scholar]
  59. McGinley, R.J. Studies of Halictinae (Apoidea: Halictidae). Smithson. Contrib. Zool. 2003, 429, 1–294. [Google Scholar] [CrossRef]
  60. Medler, J.T. Anthophora (Clisodon) terminalis Cresson in trap-nests in Wisconsin (Hymenoptera: Anthophoridae). Can. Entomol. 1964, 96, 1332–1336. [Google Scholar] [CrossRef]
  61. Michener, C.D. The Social Behavior of the Bees: A Comparative Study; Harvard University Press: Cambridge, MA, 1974. [Google Scholar]
  62. Michener, C.D. The parasitic groups of Halictidae (Hymenoptera, Apoidea). Univ. Kans. Sci. Bull. 1978, 51, 291–339. [Google Scholar] [CrossRef]
  63. Michener, C.D. The Bees of the World; Johns Hopkins University Press: Baltimore, MD, USA, 2000. [Google Scholar]
  64. Michener, C.D.; Wille, A. The bionomics of a primitively social bee, Lasioglossum inconspicuum. Univ. Kans. Sci. Bull. 1961, 42, 1123–1202. [Google Scholar]
  65. Miliczky, E.R. Observations on the nesting biology of Tetralonia hamata Bradley with a description of its mature larva (Hymenoptera: Anthophoridae). J. Kans. Entomol. Soc. 1985, 58, 686–700. [Google Scholar]
  66. Mueller, U.G. Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 1996, 69, 116–138. [Google Scholar]
  67. Nininger, H.H. Notes on the life-history of Anthophora stanjordiana. Psyche 1920, 27, 135–137. [Google Scholar] [CrossRef]
  68. Norden, B.B. Nesting biology of Anthophora abrupta (Hymenoptera: Anthophoridae). J. Kans. Entomol. Soc. 1984, 57, 243–262. [Google Scholar]
  69. Ordway, E. The bionomics of Augochlorella striata and A. persimilis in Eastern Kansas (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 1966, 39, 270–313. [Google Scholar]
  70. Packer, L. Multiple-foundress associations in a temperate population of Halictus ligatus (Hymenoptera; Halictidae). Can. J. Zool. 1986, 64, 2325–2332. [Google Scholar] [CrossRef]
  71. Packer, L. The social organisation of Lasioglossum (Dialictus) laevissimum (Smith) in southern Alberta. Can. J. Zool. 1992, 70, 1767–1774. [Google Scholar] [CrossRef]
  72. Packer, L.; Jessome, V.; Lockerbie, C.; Sampson, B. The phenology and social biology of four sweat bees in a marginal environment: Cape Breton Island. Can. J. Zool. 1989, 67, 2871–2877. [Google Scholar] [CrossRef]
  73. Packer, L.; Sampson, B.; Lockerbie, C.; Jessome, V. Nest architecture and brood mortality in four species of sweat bee (Hymenoptera; Halictidae) from Cape Breton Island. Can. J. Zool. 1989, 67, 2864–2870. [Google Scholar] [CrossRef]
  74. Ribble, D.W. The monotypic North American subgenus Larandrena of Andrena (Hymenoptera: Apoidea). Bull. Univ. Neb. State Mus. 1967, 6, 27–42. [Google Scholar]
  75. Richards, M.H.; Packer, L. Annual variation in survival and reproduction of the primitively eusocial sweat bee Halictus ligatus (Hymenoptera: Halictidae). Can. J. Zool. 1995, 73, 933–941. [Google Scholar] [CrossRef]
  76. Richards, M.H.; Richards, M.H.; Vickruck, J.L.; Rehan, S.M. Colony social organisation of Halictus confusus in southern Ontario, with comments on sociality in the subgenus H. (Seladonia). J. Hymenopt. Res. 2010, 19, 144–158. [Google Scholar]
  77. Roberts, R.B. Biology of the bee genus Agapostemon (Hymenoptera: Halictidae). Kans. Univ. Sci. Bull. 1969, 48, 101–124. [Google Scholar]
  78. Roberts, R.B. Revision of the bee genus Agapostemon (Hymenoptera: Halictidae). Kans. Univ. Sci. Bull. 1972, 49, 437–590. [Google Scholar]
  79. Soucy, S.L. Nesting biology and socially polymorphic behavior of the sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Ann. Entomol. Soc. Am. 2002, 95, 57–65. [Google Scholar] [CrossRef]
  80. Stockhammer, K.A. Nesting habits and life cycle of a sweat bee, Augochlora pura (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 1966, 39, 157–192. [Google Scholar]
  81. Stockhammer, K.A. Some notes on the biology of the blue sweat bee, Lasioglossum coeruleum (Apoidea: Halictidae). J. Kans. Entomol. Soc. 1967, 40, 177–189. [Google Scholar]
  82. Vickruck, J.l.; Rehan, S.M.; Sheffield, C.S.; Richards, M.H. Nesting biology and DNA barcode analysis of Ceratina dupla and C. mikmaqi, and comparisons with C. calcarata (Hymenoptera: Apidae: Xylocopinae). Can. Entomol. 2011, 143, 254–262. [Google Scholar] [CrossRef]
  83. Williams, P.H.; Thorp, R.W.; Richardson, L.L.; Colla, S.R. Bumble Bees of North America: An Identification Guide; Princeton University Press: Princeton, NJ, USA, 2014. [Google Scholar]
  84. Zayed, A.; Constantin, Ş.A.; Packer, L. Successful biological invasion despite a severe genetic load. PLoS ONE 2007, 2, e868. [Google Scholar] [CrossRef] [PubMed]
  85. Abrams, J.; Eickwort, G.C. Nest switching and guarding by the communal sweat bee Agapostemon virescens (Hymenoptera, Halictidae). Insectes Sociaux 1981, 28, 105–116. [Google Scholar] [CrossRef]
  86. Abrams, J.; Eickwort, G.C. Biology of the communal sweat bee Agapostemon virescens (Hymenoptera: Halictidae) in New York State. Agriculture 1980, 1, 1–20. [Google Scholar]
  87. Graenicher, S. Some observations on the life history and habits of parasitic bees. Bull. Wis. Nat. Hist. Soc. 1905, 3, 153–167. [Google Scholar]
  88. Pesenko, Y.A.; Banaszak, J.; Radchenko, V.G.; Cierzniak, T. Bees of the Family Halictidae (excluding Sphecodes) of Poland: Taxonomy, Ecology, Bionomics; Wyzszej Szkoly Pedagogicznej: Bydgszsz, Poland, 2000. [Google Scholar]
  89. Rau, P. Ecological and behavior notes on Missouri insects. Trans. Acad. Sci. St. Louis 1922, 24, 1–71. [Google Scholar]
  90. Batra, S.W.T. Ethology of the vernal eusocial bee, Dialictus laevissimus (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 1987, 60, 100–108. [Google Scholar]
  91. Atwood, C.E. Studies on the Apoidea of western Nova Scotia with special reference to visitors to apple bloom. Can. J. Res. 1933, 9, 443–457. [Google Scholar] [CrossRef]
  92. Gibbs, J.; Brady, S.G.; Kanda, K.; Danforth, B.N. Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Mol. Phylogenet. Evol. 2012, 65, 926–939. [Google Scholar] [CrossRef] [PubMed]
  93. Goulson, D.; Stout, J.C. Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae). Apidologie 2001, 32, 105–111. [Google Scholar] [CrossRef]
  94. Sanford, J.C.; Hanneman, R.E. The use of bees for the purpose of inter-mating in potato. Am. Potato J. 1981, 58, 481–485. [Google Scholar] [CrossRef]
  95. Buchmann, S.L. Buzz pollination in angiosperms. In Handbook of Experimental Pollination Biology; Van Nostrand Reinhold: New York, NY, USA, 1983; pp. 73–113. [Google Scholar]
  96. Teppner, H. Pollinators of tomato, Solanum lycopersicum (Solanaceae), in Central Europe. Phyton 2005, 45, 217–235. [Google Scholar]
  97. Bowers, K.A.W. The pollination ecology of Solanum rostratum (Solanaceae). Am. J. Bot. 1975, 62, 633–638. [Google Scholar] [CrossRef]
  98. Greenleaf, S.S.; Williams, N.M.; Winfree, R.; Kremen, C. Bee foraging ranges and their relationship to body size. Oecologia 2007, 153, 589–596. [Google Scholar] [CrossRef] [PubMed]
  99. Mallinger, R.E.; Werts, P.; Gratton, C. Pesticide use within a pollinator-dependent crop has negative effects on the abundance and species richness of sweat bees, Lasioglossum spp., and on bumble bee colony growth. J. Insect Conserv. 2015, 19, 999–1010. [Google Scholar] [CrossRef]
  100. Winfree, R.; Aguilar, R.; Vázquez, D.P.; LeBuhn, G.; Aizen, M.A. A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 2009, 90, 2068–2076. [Google Scholar] [CrossRef] [PubMed]
  101. Gardiner, M.A.; Tuell, J.K.; Isaacs, R.; Gibbs, J.; Ascher, J.S.; Landis, D.A. Implications of three biofuel crops for beneficial arthropods in agricultural landscapes. BioEnergy Res. 2010, 3, 6–19. [Google Scholar] [CrossRef]
  102. Bennett, A.B.; Isaacs, R. Landscape composition influences pollinators and pollination services in perennial biofuel plantings. Agric. Ecosyst. Environ. 2014, 193, 1–8. [Google Scholar] [CrossRef]
  103. Adams, D.E.; Perkins, W.E.; Estes, J.R. Pollination systems in Paspalum dilatatum Poir. (Poaceae): An example of insect pollination in a temperate grass. Am. J. Bot. 1981, 68, 389–394. [Google Scholar] [CrossRef]
  104. Terrell, E.E.; Batra, S.W.T. Insects collect pollen of eastern wildrice, Zizania aquatica (Poaceae). Castanea 1984, 49, 31–34. [Google Scholar]
  105. Geroff, R.K.; Gibbs, J.; McCravy, K.W. Assessing bee (Hymenoptera: Apoidea) diversity of an Illinois restored tallgrass prairie: Methodology and conservation considerations. J. Insect Conserv. 2014, 18, 951–964. [Google Scholar] [CrossRef]
  106. Droege, S.; Tepedino, V.J.; LeBuhn, G.; Link, W.; Minckley, R.L.; Chen, Q.; Conrad, C. Spatial patterns of bee captures in North American bowl trapping surveys. Insect Conserv. Divers. 2010, 3, 15–23. [Google Scholar] [CrossRef]
  107. Kimoto, C.; DeBano, S.J.; Thorp, R.W.; Rao, S.; Stephen, W.P. Investigating temporal patterns of a native bee community in a remnant North American bunchgrass prairie using blue vane traps. J. Insect Sci. Online 2012. [Google Scholar] [CrossRef] [PubMed]
  108. Joshi, N.K.; Leslie, T.; Rajotte, E.G.; Kammerer, M.A.; Otieno, M.; Biddinger, D.J. Comparative trapping efficiency to characterize bee abundance, diversity, and community composition in apple orchards. Ann. Entomol. Soc. Am. 2015, 108, 785–799. [Google Scholar] [CrossRef]
  109. Mogren, C.L.; Rand, T.A.; Fausti, S.W.; Lundgren, J.G. The effects of crop intensification on the diversity of native pollinator communities. Environ. Entomol. 2016, 45, 865–872. [Google Scholar] [CrossRef] [PubMed]
  110. Feltham, H.; Park, K.; Goulson, D. Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 2014, 23, 317–323. [Google Scholar] [CrossRef] [PubMed]
  111. Tasei, J.N.; Ripault, G.; Rivault, E. Hazards of imidacloprid seed coating to Bombus terrestris (Hymenoptera: Apidae) when applied to sunflower. J. Econ. Entomol. 2001, 94, 623–627. [Google Scholar] [CrossRef] [PubMed]
  112. Harder, L.D. Behavioral responses by bumble bees to variation in pollen availability. Oecologia 1990, 85, 41–47. [Google Scholar] [CrossRef]
Figure 1. Commercial potato fields were surveyed for bees in Montcalm County (shown in red on the state map), Michigan, USA. Red triangles represent the locations of 12 commercial potato fields, which were used to survey bees. Fields were 0.8–18.2 km apart, with an average of 3.6 km distance between sites.
Figure 1. Commercial potato fields were surveyed for bees in Montcalm County (shown in red on the state map), Michigan, USA. Red triangles represent the locations of 12 commercial potato fields, which were used to survey bees. Fields were 0.8–18.2 km apart, with an average of 3.6 km distance between sites.
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Figure 2. Transects of bowl traps and blue vane traps were placed in each potato field to survey the bee community. Bowl and vane transects were 10 m apart and extended from the field border to 30 m into the field; figure not to scale (A); Bowl trap platforms were elevated to canopy height on metal poles; blue vane traps were suspended at canopy height from a metal pole (B). Traps were emptied after 48 h.
Figure 2. Transects of bowl traps and blue vane traps were placed in each potato field to survey the bee community. Bowl and vane transects were 10 m apart and extended from the field border to 30 m into the field; figure not to scale (A); Bowl trap platforms were elevated to canopy height on metal poles; blue vane traps were suspended at canopy height from a metal pole (B). Traps were emptied after 48 h.
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Figure 3. Mean ± SEM number of bees captured in commercial potato fields in Michigan in 2016 by trap type and trap location. Bowl traps were elevated on a platform at canopy height, with one bowl of each color on each platform. A transect of four bowl trap platforms ran from bordering vegetation roughly 10 m from the potato field (“border”), at the edge of the field (“edge”), 10 m into the potato field (“10 m”), and 30 m into the potato field (“30 m”). Blue vane traps were suspended from a metal pole at canopy height, and placed in a parallel transect 10 m from the bowl trap transect. Different letters above bars indicate significantly different (α = 0.05) abundances in Tukey’s HSD test within locations.
Figure 3. Mean ± SEM number of bees captured in commercial potato fields in Michigan in 2016 by trap type and trap location. Bowl traps were elevated on a platform at canopy height, with one bowl of each color on each platform. A transect of four bowl trap platforms ran from bordering vegetation roughly 10 m from the potato field (“border”), at the edge of the field (“edge”), 10 m into the potato field (“10 m”), and 30 m into the potato field (“30 m”). Blue vane traps were suspended from a metal pole at canopy height, and placed in a parallel transect 10 m from the bowl trap transect. Different letters above bars indicate significantly different (α = 0.05) abundances in Tukey’s HSD test within locations.
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Figure 4. Visualization of bee communities by trap type in non-metric multidimensional ordination space. Bowl traps were elevated on a platform at canopy height, with one bowl of each color on each platform. A transect of four bowl trap platforms ran from bordering vegetation roughly 10 m from the potato field (“border”), at the edge of the field (“edge”), 10 m into the potato field (“10 m”) and 30 m into the potato field (“30 m”). Blue vane traps were suspended from a metal rod at canopy height, and placed in a parallel transect 10 m from the bowl trap transect. Bee communities (+) are the sum of individuals found in each trap type and location, summed across sites and dates. Ellipses represent 95% confidence intervals around communities defined by trap type: blue vane trap (black ellipse), blue bowl trap (blue ellipse), white bowl trap (grey ellipse), and yellow bowl trap (yellow ellipse). Bee communities did not differ across trap locations; 95% CIs for trap location are not presented. Red vectors are species with significant (p < 0.05) effects in the ‘adonis’ model (see text for values).
Figure 4. Visualization of bee communities by trap type in non-metric multidimensional ordination space. Bowl traps were elevated on a platform at canopy height, with one bowl of each color on each platform. A transect of four bowl trap platforms ran from bordering vegetation roughly 10 m from the potato field (“border”), at the edge of the field (“edge”), 10 m into the potato field (“10 m”) and 30 m into the potato field (“30 m”). Blue vane traps were suspended from a metal rod at canopy height, and placed in a parallel transect 10 m from the bowl trap transect. Bee communities (+) are the sum of individuals found in each trap type and location, summed across sites and dates. Ellipses represent 95% confidence intervals around communities defined by trap type: blue vane trap (black ellipse), blue bowl trap (blue ellipse), white bowl trap (grey ellipse), and yellow bowl trap (yellow ellipse). Bee communities did not differ across trap locations; 95% CIs for trap location are not presented. Red vectors are species with significant (p < 0.05) effects in the ‘adonis’ model (see text for values).
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Figure 5. Species accumulation curves for bees surveyed in commercial potato fields in Michigan. Bees were collected in four different trap types at 12 field sites during the 2016 growing season. Species accumulation curve for all trap types pooled together (A) and by trap type (B). Dashed lines indicate 95% confidence intervals.
Figure 5. Species accumulation curves for bees surveyed in commercial potato fields in Michigan. Bees were collected in four different trap types at 12 field sites during the 2016 growing season. Species accumulation curve for all trap types pooled together (A) and by trap type (B). Dashed lines indicate 95% confidence intervals.
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Figure 6. Mean ± SEM flower visits per hour (A) and seconds per visit (B) by Bombus impatiens bees in mesh field enclosures. Enclosures contained five imidacloprid-treated and five untreated flowering potato plants and a single bee colony of 10–15 foragers. Bees were allowed to forage and were observed for 15 min/enclosure/day.
Figure 6. Mean ± SEM flower visits per hour (A) and seconds per visit (B) by Bombus impatiens bees in mesh field enclosures. Enclosures contained five imidacloprid-treated and five untreated flowering potato plants and a single bee colony of 10–15 foragers. Bees were allowed to forage and were observed for 15 min/enclosure/day.
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Table 1. Site descriptions of commercial potato fields used for bee surveys in 2016. Bees were surveyed with four white, yellow, and blue bowls and four blue vane traps at each site.
Table 1. Site descriptions of commercial potato fields used for bee surveys in 2016. Bees were surveyed with four white, yellow, and blue bowls and four blue vane traps at each site.
Site IDFlower ColorPotato VarietyLatitudeLongitude
1white‘Pike’43.4480−84.8882
2white‘Pike’43.4444−84.8974
3purple‘Lamoka’43.4444−84.8974
4purple‘FL1922’43.3209−85.0123
5white‘Pike’43.4480−84.8882
6purple‘FL2137’43.4106−84.9183
7pink‘Lamoka’43.3867−84.9707
8pink‘Lamoka’43.3369−85.0547
9purple‘FL2137’43.3956−84.9047
10white‘Snowden’43.3828−84.9027
11pink‘Lamoka’43.3722−85.0747
12purple‘FL2137’43.3564−85.0493
Table 2. Species names and characteristics of bees captured in bowl and blue vane traps in 12 commercial potato fields in Michigan in 2016. Biological data are based on published studies and reviews [36,37,38,39,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90].
Table 2. Species names and characteristics of bees captured in bowl and blue vane traps in 12 commercial potato fields in Michigan in 2016. Biological data are based on published studies and reviews [36,37,38,39,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90].
TaxaNestingBehaviorNative/ExoticReferencesNo. of Individuals% of Total
ANDRENIDAE
Andrena miserabilis Cresson 1872groundsolitarynative[74]10.1
APIDAE
Anthophora abrupta Say 1837groundsolitarynative[68]10.1
An. bomboides Kirby 1837groundsolitarynative[67]20.3
An. terminalis Cresson 1869wood/cavitysolitarynative[60]60.8
Apis mellifera Linnaeus 1758hiveadv. eusocialexotic[61]243.2
Bombus auricomus (Robertson 1903)hiveeusocialnative[61]10.1
B. bimaculatus Cresson 1863hiveeusocialnative[61]70.9
B. fervidus (Fabricius 1798)hiveeusocialnative[61]50.7
B. griseocollis (DeGeer 1773)hiveeusocialnative[61]20.3
B. impatiens Cresson 1863hiveeusocialnative[61]50.7
B. perplexus Cresson 1863hiveeusocialnative[61]10.1
B. ternarius Say 1837hiveeusocialnative[61]10.1
Ceratina mikmaqi Rehan and Sheffield 2011stemsolitarynative[82]10.1
Eucera hamata (Bradley 1942)groundsolitarynative[65]50.7
Melissodes agilis Cresson 1878 1groundsolitarynative[36,89]131.7
M. bimaculatus (Lepeletier 1825)groundsolitarynative[36,51]131.7
M. communis Cresson 1878 2groundsolitarynative[36]30.4
M. desponsus Smith 1854 2,3groundsolitarynative[36]111.5
M. subillatus LaBerge 1961 2,4groundsolitarynative[36]20.3
Peponapis pruinosa (Say 1837) 5groundsolitarynative[48]648.5
COLLETIDAE
Hylaeus affinis (Smith 1853) 2stemsolitarynative 30.4
H. mesillae (Cockerell 1896)stemsolitarynative[89]10.1
HALICTIDAE
Augochlora pura (Say 1837)rotten woodsolitarynative[80]40.5
Augochlorella aurata (Smith 1853)groundsolitary/eusocialnative[66,69,72,73]20.3
Agapostemon texanus Cresson 1872groundsolitarynative[55,77]20.3
Ag. virescens (Fabricius 1775)groundcommunalnative[85,86]91.2
Halictus confusus Smith 1853groundsolitary/eusocialnative[76]30.4
H. ligatus Say 1837groundeusocialnative[70,75]70.9
H. rubicundus (Christ 1791)groundsolitary/eusocialnative[79]10.1
Lasioglossum albipenne (Robertson 1890) 2groundeusocialnative 20.3
L. anomalum (Robertson 1892) 2groundeusocialnative 10.1
L. bruneri (Crawford 1902) 2groundeusocialnative 131.7
L. cinctipes (Provancher 1888)groundeusocialnative[72,73]10.1
L. coeruleum (Robertson 1893)rotten woodeusocialnative[81]101.3
L. coriaceum (Smith 1853) 2groundsolitarynative 121.6
L. cressonii (Robertson 1890) 2rotten woodeusocialnative[39]20.3
L. ellisiae (Sandhouse 1924) 2groundeusocialnative 30.4
L. heterognathum (Mitchell 1960) 2groundeusocialnative 40.5
L. illinoense (Robertson 1892) 2groundeusocialnative 131.7
L. imitatum (Smith 1853)groundeusocialnative[64]263.4
L. laevissimum (Smith 1853)groundeusocialnative[71,72,73]20.3
L. leucocomum (Lovell 1908) 2groundeusocialnative 486.4
L. leucozonium (Schrank 1781)groundsolitaryexotic[88,91]678.9
L. lineatulum (Crawford 1906)groundeusocialnative[56]364.8
L. macoupinense (Robertson 1895) 2groundsolitarynative 10.1
L. oceanicum (Cockerell 1916) 2groundeusocialnative 202.6
L. paraforbesii McGinley 1986 2groundsolitarynative 141.9
L. pectorale (Smith 1853) 2groundsolitarynative 314.1
L. perpunctatum (Ellis 1913) 2groundeusocialnative 486.4
L. pilosum (Smith 1853) 2groundeusocialnative 15720.8
L. smilacinae (Robertson 1897) 2groundeusocialnative 40.5
L. versatum (Robertson 1902)groundeusocialnative[53]111.5
L. zephyrum (Smith 1853)groundeusocialnative[52]10.1
L. zonulum (Smith 1848)groundsolitaryexotic[88,91]243.2
Sphecodes coronus Mitchell 1956groundcleptoparasitenative[62]10.1
S. cressonii (Robertson 1903)groundcleptoparasitenative[62]10.1
S. mandibularis Cresson 1872groundcleptoparasitenative[62]10.1
MEGACHILIDAE
Megachile latimanus Say 1823groundsolitarynative[87]20.3
1 specialist on Helianthus; 2 nesting data based on consubgeners (e.g., [92]); 3 specialist on Cirsium; 4 specialist on Asteraceae; 5 specialist on Cucurbitaceae.

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MDPI and ACS Style

Buchanan, A.L.; Gibbs, J.; Komondy, L.; Szendrei, Z. Bee Community of Commercial Potato Fields in Michigan and Bombus impatiens Visitation to Neonicotinoid-Treated Potato Plants. Insects 2017, 8, 30. https://doi.org/10.3390/insects8010030

AMA Style

Buchanan AL, Gibbs J, Komondy L, Szendrei Z. Bee Community of Commercial Potato Fields in Michigan and Bombus impatiens Visitation to Neonicotinoid-Treated Potato Plants. Insects. 2017; 8(1):30. https://doi.org/10.3390/insects8010030

Chicago/Turabian Style

Buchanan, Amanda L., Jason Gibbs, Lidia Komondy, and Zsofia Szendrei. 2017. "Bee Community of Commercial Potato Fields in Michigan and Bombus impatiens Visitation to Neonicotinoid-Treated Potato Plants" Insects 8, no. 1: 30. https://doi.org/10.3390/insects8010030

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