Abstract
Many pollinator insects, especially honey bees [Apis mellifera Linnaeus (Apidae)] and wild bees, are experiencing population decline because of forage and habitat losses. Planting perennial flowering taxa is one method of increasing pollinator habitat. The objectives of this study were to evaluate the potential of 27 native species and ornamental perennial cultivars to determine their ability to attract insect pollinators in a rural and an urban landscape in North Dakota, assess the potential of these perennials to attract other beneficial insects and insect pests, and identify the bee species visiting these perennials. Five to eight native species and/or ornamental cultivars each from four genera, Monarda L. (bee balm), Hylotelephium H. Ohba (stonecrop), Baptisia Vent. (wild indigo), and Symphyotrichum Nees (aster), were tested. Weekly observations of individual plants during flowering and their pollinator visitations from 2018 to 2020 indicated that insect pollinators were present for the earliest flowering perennials in June and until the latest flowering perennials during the second week of October or the first freeze. A total of 16,194 insect pollinators were observed, and 87.8% of these pollinator visitations were Hymenoptera and Diptera. Significant landscapes × perennial flowering taxa interactions were detected for all insect groups, except for syrphid flies, for which both main effects were significantly different. Overall, honey bees and beetles preferred to visit Hylotelephium and Symphyotrichum. The wild bees, lepidopterans, and syrphids preferred Hylotelephium, Symphyotrichum, and Monarda. Tachinids preferred Symphyotrichum. Blow flies preferred Hylotelephium. More beneficial insect visitations (i.e., 96.0%) and fewer insect pest visitations (i.e., 30.4%) were counted on the rural landscape. A total of 3311 bee individuals were identified as species from the following families: Apidae, Andrenidae, Colletidae, Megachilidae, and Halictidae. Thirty-one and 21 bee species were unique to the rural and urban landscapes, respectively. The two most common wild bees were Ceratina calcarata Robertson on the cultivar S. oblongifolium (Nutt.) G.L. Nessom October Skies and Lasioglossum imitatum (Smith) on some Monarda and Hylotelephium. These findings suggest that pollinator visitations are influenced by the landscape and varied among the perennial flowering taxa in some cases. However, all evaluated perennial flower taxa would be suitable for attracting and supporting pollinators in rural or urban landscape settings in the northern Great Plains.
Numerous pollinators, including honey bees [Apis mellifera Linnaeus (Apidae)], bumble bees [Bombus Latreille spp. (Apidae)], and other wild bees, butterflies, moths, flies, and beetles are important pollinators of many cultivated crops and help achieve seed set and fruit production (Kevan et al. 1990; Klein et al. 2007; McGregor 1976; National Research Council 2007; Thapa 2006). However, the overall decline of pollinators is a concern not only for United States citizens but also for the global population (Dicks et al. 2021; Johnson and Corn 2015; Vasiliev and Greenwood 2021; Woteki 2013; Zattara and Aizen 2021). Habitat fragmentation and loss, pesticide usage, diseases, parasites, intraspecific and interspecific competition between native and invasive species, and climate change are factors that lead to pollinator declines (Goulson et al. 2015; National Research Council 2007; Potts et al. 2010; Soroye et al. 2020; Wagner et al. 2021). For example, native bees and butterflies were once abundant in North Dakota and other northern states. Currently, the rusty patched bumble bee (Bombus affinis Cresson) (US Fish and Wildlife Service 2017), dakota skipper [Hesperia dacotae (Skinner)], and poweshiek skipperling [Oarisma Poweshiek (Parker)] (US Fish and Wildlife Service 2014) are species that historically have been present in North Dakota and/or Minnesota and are now listed by the Endangered Species Act of 1973 as endangered or threatened.
Because of pollinator decline, private and public entities such as the Xerces Society (Xerces Society 2022), the United States Fish and Wildlife Service (US Fish and Wildlife Service 2022), and US Department of Agriculture (US Department of Agriculture 2022) have been promoting pollinator conservation. Strategies for promoting pollinator conservation include encouraging landowners and home gardeners to plant pollinator-friendly plants in gardens and pastures to provide habitats for native bees and butterflies.
Pollinator conservation in home gardens and backyards is currently a popular topic, especially in residential areas. Towns, cities, and suburbs can provide habitats for numerous pollinator insects as well as other beneficial insects and floral insect pests because of their diverse and unique managed environments (Harris et al. 2016, 2022; Mader et al. 2011; Melathopoulos et al. 2020). Recently, more than 80.0% of landscape architects surveyed indicated that United States consumers are more likely to request native plants, drought-tolerant native plants, and low-maintenance plants for their residential landscapes (American Society of Landscapes Architects 2018).
Native plant species are recommended for planting (Holm 2014; Mader et al. 2011) because they coevolved with native pollinators with regard to flowering time, floral morphology, pollinator rewards, and geographical covariations (Alexandersson and Johnson 2002; Anderson and Johnson 2008, 2009; Bloch and Erhardt 2008; Ehrlich and Raven 1964; Marquis 2004). Thus, because of specific ecological interactions, innate floral morphologies, and different visitation rates of pollinators, many flower species are constrained to interact with specific pollinators (Thompson 2001). However, home gardeners may have negative perceptions of native plants because they have a reputation for being less attractive and messy (Beck et al. 2002; Nassauer 1995). Homeowners may be more willing to plant a mix of native species and ornamental cultivars rather than just native species. We propose the evaluation and identification of species and ornamental cultivars to determine their pollinator attractiveness in the northern United States.
During the breeding process, improved cultivars may lose some of their natural traits that are attractive to pollinators (Wilde et al. 2015). Ornamental flower cultivars are bred and/or selected to improve traits, such as compact plant height (Flemer 1979), elaborate flower form (e.g., double flowers) (Anonymous 1935), vibrant flower colors, flower abundance (Ault 2008), foliage color (Tenczar and Krischik 2007), bloom time (Ault 2009), and disease resistance (Oudshoorn 2012), to satisfy aesthetic flower demands from consumers (Wilde et al. 2015). Attractive petal color was the most common floral characteristic preferred by consumers (Hopkins et al. 2022). Some ornamental cultivars have been heavily bred for aesthetic purposes and may have lost their ability to produce pollen and nectar because of this breeding and selection process. Therefore, it is important to identify which cultivars are the best for pollinator gardens.
Some cultivars and non-native plant species are used by pollinators (Ricker et al. 2019; Rollings and Goulson 2019), especially when food sources are scarce (Braman and Griffin 2022; Mach and Potter 2018; Marquardt et al. 2021; Riddle and Mizell 2016) and outside of the normal flowering season (Salisbury et al. 2015). Home gardeners, landowners, and landscapers desire to create pollinator gardens and hospitable habitats, but they may be discouraged if nationally recommended cultivars are not well-adapted to grow in their state. Numerous native species and ornamental cultivars are available for sale to the consumer horticulture market, but few contain documented pollinator attraction information.
Studies of insect pollinator visitations to flowering plants have been conducted to assess floral attractiveness (Mach and Potter 2018; Marquardt et al. 2021; Ricker et al. 2019; Rollings and Goulson 2019); however, beneficial insect and insect pest visitations to ornamental flowers have not been sufficiently discussed and little information is available. Beneficial insects such as lady beetles, lacewings, and minute pirate bugs (Walliser 2014) as well as insect pests such as stink bugs, blister beetles, and grasshoppers commonly visit ornamental flowers in gardens (Harris et al. 2016, 2022; Khan et al. 2019). The availability of beneficial insects in an ecosystem can help regulate the pest plant population density and can lead to a healthy ecosystem equilibrium (Getanjaly et al. 2015).
Limited research of ornamental cultivars has been conducted to determine their ability to provide ecosystem services to pollinators and other insects in North Dakota landscapes. Our objectives of this research study were to evaluate the potential of 27 perennial native species and ornamental cultivars to determine their ability to attract insect pollinators in rural and urban landscapes in North Dakota, assess the potential of these 27 perennial flowering taxa to attract other beneficial insects as well as insect pests, and determine which native and non-native bee species are visiting these 27 taxa.
Materials and Methods
Twenty-seven herbaceous perennial flowering taxa from four genera comprising a mix of native species and ornamental cultivars were planted on 21 Jun 2018, at the North Dakota State University (NDSU) Horticulture Research Farm near Absaraka, ND (rural landscape; 46.991581 °N, −97.351462 °W), and on 19 Jun 2018, at the NDSU Horticulture Research and Demonstration Gardens in Fargo, ND (urban landscape; 46.891274 °N, −96.810014 °W). The area surrounding the plots of the rural landscape had 3.6% developed land cover (i.e., land covered with diverse buildings and paved surfaces, such as roads and parking lots), whereas the urban landscape had 88.6% developed land cover; both types of land cover were within a 3-km radius centered from the experimental area according to 2019 cropland data layer using CropScape (US Department of Agriculture, National Agricultural Statistics Service, Cropland Data Layer 2022). The 3-km radius was selected based on the forage distances of wild bees and honey bees. Most wild bees forage approximately 0.5 km from their nests (Gathmann and Tscharntke 2002; Zurbuchen et al. 2010a, 2010b), whereas the average forage distance for honey bees is less than 2.6 km away from their nests (Couvillon et al. 2015; Kirk Visscher and Seeley 1982; Seeley 1995).
Herbaceous perennial native species and ornamental cultivars of the following genera were evaluated: Baptisia, Hylotelephium, Monarda, and Symphyotrichum (Table 1). These genera are considered pollinator-friendly by United States gardening industry. Of the 27 evaluated taxa, eight are species native to the United States, including five native to North Dakota and/or Minnesota (US Department of Agriculture, Natural Resources Conservation Service 2022). Two of the three remaining taxa are native to the Midwest, and the final taxon is native to the southeastern United States. In Table 1, the scientific name, common name, native or cultivar status, flower color, and commercial source for each perennial are summarized. Only the native species Symphyotrichum oblongifolium was started from seed at one of the NDSU greenhouses; the other 26 perennial taxa were purchased from different nurseries.
Native species and ornamental cultivars, common names, origin, flower color, and source of the perennial flowering plant.
At each landscape, perennial flowering taxa were arranged in a randomized complete block design with six replication rows. A single plant was considered an experimental unit. Plants of the same genus were planted together at random within a replication row, and genera were arranged at random within each replication row. Each replication row was 25 m long. The distance between replication rows and genera groups was 1.5 m. The distance between plants was 0.76 m.
Before planting, a black landscape fabric weed barrier (Dewitt Pro 5; Dewitt, Sikeston, MO, USA) was stapled to the ground of each replication row to control weeds. Plants were watered at least once or twice each week during the first year, depending on the temperature and rainfall, until plants were established. Plot edges (beyond weed barrier) and plant bases were weeded by hand when needed. During early spring (before regrowth began), dead vegetation was pruned to ∼15 cm. Plants were not fertilized or sprayed with insecticides or fungicides.
When plants were in bloom, observations of pollinators, other beneficial insects, and floral insect pests were conducted from June to October. Each flowering plant was observed for 3 min on a weekly basis, and all observations were conducted during 1 d per study site. All insects that visited or contacted the flowers were counted and recorded, avoiding duplication when possible. Immature insects such as eggs, caterpillars, or pupae and adult insects such as ants (Formicidae) and aphids (Aphididae) were not counted during this study. Visitation counts were conducted between 10:00 and 16:00 HR, when pollinators are most active, and on days when temperatures were warmer than 10 °C, the wind speed was less than 25 km/h, and there was no rain. Native species and cultivars were evaluated for 2 years at each landscape for Monarda, Hylotelephium, and Symphyotrichum in 2018 and 2019, and for Baptisia in 2019 and 2020 (most Baptisia plants were already blooming when purchased in 2018).
When possible, wild bees were collected during the observation period; however, some bees escaped capture. Specimens of other insect groups were not collected. Bees were captured using a black handheld D-cell-powered insect aspirator (Fulton MX-pp1/U; Gempler’s, Janesville, WI, USA), which comprised a collector container (45 mm × 25 mm, length by internal diameter), or hand-collected using only the aspirator collector container and its lid. When necessary, collector containers with bees were immediately submerged in a 0.95-L clear plastic container (HomeFresh RD 32 oz; Placon Corporation, Madison, WI, USA) filled with 500 mL of tap water to slow their movement and prevent escape. Subsequently, they were transferred to a 4-dram vial (BioQuip Products Inc., Rancho Dominguez, CA, USA) that contained 85% alcohol and labeled with the corresponding field data information.
In the laboratory, collected bees were processed according to the procedures of Droege (2010). Bees were identified to the species level when possible using the taxonomic literature (Gibbs 2010, 2011; Gibbs et al. 2013; McGinley 1986; Michener 2007; Mitchell 1960, 1962; Onuferko 2017; Roberts 1972; Sheffield et al. 2011), the identification guides on the Discover Life website (Ascher and Pickering 2020), and identified reference specimens. Specimens that could not be reliably assigned a species epithet were given a unique “morphospecies” identifier. A Leica M125 stereoscope with a Leica DFC450 camera and image processing software (North Central Instruments, Inc., Brooklyn Park, MN, USA) were used to examine each bee. Location labels containing all collection data were affixed to each specimen. Identification labels and voucher specimen labels with a unique project identifier were also affixed to each specimen. Voucher specimens reside in the NDSU Extension Entomology collection housed at 206 Waldron Hall, NDSU, Fargo, ND, USA.
Statistical analysis.
All insect visitation counts per plant in their respective insect groups (i.e., honey bees, wild bees, wasps, syrphid flies, tachinid flies, blow flies, butterflies, beetles, other beneficial insects, and floral insect pests) were added across each season year for each landscape. Subsequently, these data were analyzed using a two-way mixed-model analysis of variance (ANOVA) (P < 0.05) using the GLIMMIX procedure in SAS (SAS Institute 2013). The landscape, perennial flowering taxa, and their interactions were assigned as fixed effects in the ANOVA table for each insect group; replication was considered a random effect in the experiment. The factor year was combined and, accordingly, removed from the model. Multiple comparisons were performed when appropriate using the LSMEANS/LINES procedure with Tukey’s honestly significant difference test (Tukey 1953) at an alpha level of 0.05 in SAS (SAS Institute 2013).
Additionally, percentage compositions for some specific insects [e.g., blues (Lycaenidae)] were calculated to show more details of the main insect groups (or orders in some cases, e.g., Lepidoptera) visiting the perennial flowering taxa. The percentage composition for each main insect group was calculated based on the total visitation counts of that specific insect member of that group and the total visitation counts of the entire main group; for example, the total visit count of syrphid flies was divided by the total Diptera visitation count and then multiplied by 100. Similarly, the percentage composition of a specific insect among four genera was calculated; for example, the total visitation count of Vanessa cardui (Linnaeus) (Nymphalidae, Lepidoptera) from all Baptisia plants was divided by the total visitation count of V. cardui from the four genera and multiplied by 100. These percentages were calculated across rural and urban landscape years. The percentage compositions of bees and wasps were calculated separately for the Hymenoptera group. The percentage compositions for the beneficial insects or the insect pests were calculated based on all insects that were assigned in that respective group.
Heat maps were generated to show density, range, and diversity of captured bee species per perennial flowering taxa across landscapes using conditional formatting in Microsoft Excel 2016 (Microsoft, Redmond, WA, USA). Colors on heat maps were used to represent density ranges of bee species on each perennial flowering plant. Additionally, for each bee species, we indicated what percentage of perennial flowering taxa (i.e., of the 27 species/cultivars evaluated) they visited, and whether a bee species was captured at rural, urban, or both landscapes. Specimens that were identified only to the genus level were counted as one species to create the heat maps. Count visitation data of honey bees were also used in these maps.
Results
The bloom time varied for the four genera (Fig. 1). Both landscapes had plants flowering from the beginning of June to the second week of October or until the first heavy freeze. More specifically, the Baptisia plants were the first to bloom; this began the first week of June and persisted until the last week of June or first week of July. Most Monarda plants began blooming the second week of July; this ended the first or second week of September. Some Hylotelephium cultivars began blooming in early August; this continued until the end of September or first week of October; however, ‘Autumn Fire’ and ‘Autumn Joy’ continued to bloom until the second week of October. Symphyotrichum species and cultivars began blooming in July through August; this continued to bloom until the second week of October or the first heavy freeze. Some Symphyotrichum species and cultivars did not complete flowering before a heavy freeze (low temperature of <−2 °C) ended the growing season in both study years.
Bloom period of the native species and ornamental cultivars in North Dakota. This represents the bloom of the first plant to the end of the bloom of the last plant within the taxa.
Citation: HortScience 58, 8; 10.21273/HORTSCI17146-23
A total of 17,606 insects were observed and counted across both landscape sites and years. From this total, 16,194 were insect pollinators, 631 were other beneficial insects, and 781 were floral insect pests. Pollinator counts were composed of Hymenoptera (4481 rural and 3816 urban), Diptera (3722 rural and 2206 urban), Lepidoptera (1314 rural and 360 urban), and Coleoptera (270 rural and 25 urban). The beneficial insect counts represented members of Hemiptera and Neuroptera (606 rural and 25 urban) orders. Members of Coleoptera, Hemiptera, and Orthoptera represented the insect pest group (237 rural and 544 urban).
Statistically significant landscape × perennial flowering taxa interactions were detected for honey bees, wild bees, and wasps of the order Hymenoptera (Table 2). Mean visitations of honey bees at the rural landscape (Table 3), regardless of native species or cultivar status, were not significantly different among all perennial taxa. However, at the urban landscape, honey bee visitations to the native species S. novae-angliae and its cultivar, Alma Potschke, were significantly greater than those of the remaining perennial taxa, with the exceptions of ‘Autumn Fire’, ‘Autumn Joy’, ‘Cherry Truffle’, and ‘Night Embers’. Additionally, S. novae-angliae, ‘Alma Potschke’, ‘Night Embers’, ‘Autumn Joy’, and ‘Cherry Truffle’ at the urban landscape had significantly higher numbers of honey bee visits than all the rural landscape taxa.
Analysis of variance of attractiveness of insect pollinators and other insects.
Visitations (mean ± SEM) and comparison of the interaction between the perennial flowering taxa and landscape type for Hymenoptera (average number of insects per plant) across the sampling period in North Dakota.
Hylotelephium ‘Autumn Fire’ and ‘Autumn Joy’ (Table 3) at the rural landscape attracted significantly higher numbers of wild bees than all the remaining perennial taxa at both landscapes, with the exception of ‘Night Embers’. Additionally, ‘Autumn Joy’ from the rural landscape and the native species M. punctata from the urban landscape had more wasp visitations than the rest of the taxa regardless of landscapes, with the exceptions of ‘Autumn Joy’ at the urban landscape and ‘Autumn Fire’ at both landscapes. Overall, the native species B. alba var. alba, B. australis, and B. a. var. minor had no or fewer visits with Hymenoptera.
No statistically significant landscape × perennial flowering taxa interaction was observed for mean syrphid fly (Syrphidae, Diptera) visitations (Table 2). However, significant differences were detected for the main effects of landscape and perennial flower taxa. Syrphid fly visits at the rural landscape were 69.2% significantly greater than those at the urban landscape. The native species S. novae-angliae (Table 4) had the highest numbers of syrphid fly visits compared with those of the other taxa, but this number was not significantly different from those of the native S. laeve or the S. oblongifolium cultivar October Skies. Symphyotrichum laeve and ‘October Skies’ were also not significantly different from Hylotelephium ‘Autumn Joy’ and S. novae-angliae ‘Alma Potschke’ in terms of attracting syrphids. Additionally, in the Diptera order, the landscape × perennial flowering taxa interaction was significant for Tachinidae and Calliphoridae flies (Table 2). The native S. laeve at the rural landscape (Table 4) attracted significantly more tachinid flies than all the other perennial flower species and cultivars at both landscapes. There was no significant difference between the remaining perennial taxa. Similarly, S. laeve at the rural landscape had significantly more Calliphoridae fly visits, but this attraction was not significantly different from that of Hylotelephium ‘Autumn Fire’ at both landscapes and of ‘Autumn Joy’ and ‘Night Embers’ at the urban landscape. All Baptisia and Monarda and the other Symphyotrichum taxa had significantly fewer Calliphoridae visitations at the rural and urban landscapes.
Visitations (mean ± SEM) and comparison of the interaction between the perennial flowering taxa and the landscape type for Diptera (average number of insects per plant) across the sampling period in North Dakota.
A landscape × perennial flowering taxa interaction was also detected for Lepidoptera and Coleoptera insect visitations (Table 2). At the rural landscape (Table 5), the Hylotelephium cultivars Autumn Fire, Autumn Joy, and Neon had significantly more butterfly visits than all Baptisia, Monarda, and Symphyotrichum (except the rural native S. novae-angliae) taxa. However, the rural ‘Autumn Joy’ and ‘Neon’ at both landscapes were not significantly different from the rural S. novae-angliae in terms of Lepidoptera visits. Regarding Coleoptera mean visitations, the native S. novae-angliae species at the rural landscape attracted the most visits compared with all the remaining perennial taxa at both landscapes.
Visitations (mean ± SEM) and comparisons of the interaction between the perennial flowering taxa and the landscape type for Lepidoptera, Coleoptera, beneficial insects, and insect pests (numbers of insects per plant) across the sampling period in North Dakota.
The landscape × perennial flowering taxa interaction was also significant for other beneficial insects and floral insect pests (Table 2). The mean visits of other beneficial insects at the rural landscape (Table 5) were not significantly different among ‘Autumn Fire’, ‘Autumn Joy’, ‘Neon’, S. laeve, S. novae-angliae, and S. oblongifolium ‘Dream of Beauty’. The rural ‘Autumn Fire’, ‘Autumn Joy’, and S. laeve also attracted significantly more beneficial insects than all perennial taxa grown in the urban landscape. Regarding insect pests (Table 5), the urban Baptisia ‘Brownie Points’ and ‘Indigo Spires’ attracted the greatest number of pests compared with the remaining rural and urban flowers, but ‘Indigo Spires’ did not significantly differ from the urban ‘American Goldfinch’. Besides these three Baptisia cultivars, no significant differences occurred between the remaining species and cultivars in terms of insect pests.
The insect pollinator composition in the order Hymenoptera and within the bee group was mainly composed of wild bee (including bumble bees) visitations, at 66.7%, and honey bee visitations, at 33.3% (Table 6). Parasitic wasps were the most predominant insects among the wasp group, with 53.4% of visits. The Diptera order was composed mostly (91.0%) of syrphid flies. The most common butterfly was the painted lady butterfly (V. cardui), with 43.9% of visits, followed by sulphurs and whites (Pieridae), with 30.4% of visits, and the celery looper moth [Anagrapha falcifera (Kirby) (Noctuidae)], with 18.5% of visits. The northern corn rootworm (Diabrotica barberi Smith & Lawrence [Chrysomelidae)] was the most common beetle within the Coleoptera pollinators, with 82.0% of visits. The beneficial insect category was composed mainly of the insidious flower bug [Orius insidiosus Say (Anthocoridae)] visitations. The most common insect pests of flowers were the ash-gray blister beetle [Epicauta fabricii LeConte (Meloidae)], followed by Lygus Hahn spp. (Miridae).
Percentages of specific insect groups visiting perennial flowering taxa in North Dakota across the rural and urban landscapes.
The percentage composition of the insect species or group visitations varied among the four plant genera (Table 6). For example, compared with Hylotelephium, Monarda, or Baptisia, Symphyotrichum received 51.1% of the honey bee visitations. However, bumble bees with 44.8% of visitations were most commonly found on Monarda. Symphyotrichum was visited by 53.8% of the syrphids among the four genera; however, only 3.4% of syrphids visited Baptisia. Visitations by lepidopterans, coleopterans, beneficial insects, and insect pests also varied among the four plant genera studied.
All bees captured during visitations across both landscapes and years totaled 3311 individuals (i.e., 41.4% of 8003 bee visitations) and represented five families: Apidae, with a total of 20 species (Fig. 2); Andrenidae, with four species; Colletidae, with three species; Megachilidae, with 12 species (Fig. 3); and Halictidae, with 33 species (Fig. 4). Totals of 60 and 33 bee species were found at the rural landscape and urban landscape, respectively. Thirty-one species were unique to the rural landscape, whereas only 12 species were unique to the urban landscape; 29 species were common to both landscapes (Figs. 2−4). Clearly, some species were more commonly captured on certain perennial taxa; for example, Ceratina calcarata Robertson was most commonly captured on S. oblongifolium ‘October Skies’, with more than 100 individuals captured (Fig. 2). The most commonly captured bee species ranged from 1 to 10 individuals per perennial taxa (Figs. 2−4). Twenty-five percent of the bee species identified during this study were captured when visiting 1 (4%) of the 27 perennial taxa. Overall, across all bee families (Figs. 2−4), each perennial flowering taxa had a least one captured bee species; the taxa with the greatest bee species diversity were Hylotelephium ‘Night Embers’ (with 29 species visits), followed by ‘Neon’ and ‘Autumn Fire’ (both with 27 species visits). In contrast, B. alba var. alba had the lowest bee diversity, with only one Megachile latimanus Say individual captured.
Heat map of Apidae bee species captured in perennial flowering taxa at rural and urban landscapes in North Dakota during 2018 to 2020. R = rural landscape; U = urban landscape; RU = both landscapes. The percentage of plant visits column indicates the percentage of 27 perennial flowering taxa visited by that bee species. The perennial B. alba var. alba with zero bee species captured was excluded from the heat map.
Citation: HortScience 58, 8; 10.21273/HORTSCI17146-23
Heat map of Andrenidae, Colletidae, and Megachilidae bee species captured in perennial flowering taxa at rural and urban landscapes in North Dakota during 2018 to 2020. R = rural landscape; U = urban landscape; RU = both landscapes. The percentage of plant visits column indicates the percentage of 27 perennial flowering taxa visited by that bee species. Perennial taxa (i.e., ‘Purple Dome’ and ‘Raydon’s Favorite’) with zero bee species captured were excluded from the heat map.
Citation: HortScience 58, 8; 10.21273/HORTSCI17146-23
Heat map of the Halictidae bee species captured in perennial flowering taxa at rural and urban landscapes in North Dakota during 2018 to 2020. R = rural landscape; U = urban landscape; RU = both landscapes. The percentage of plant visits column indicates the percentage of 27 perennial flowering taxa visited by that bee species. Perennial taxa (i.e., B. alba var. alba, B. a. var. minor, B. australis, ‘American Goldfinch’, ‘Grape Taffy’, and ‘Raydon’s Favorite’) with zero bee species captured were excluded from the heat map.
Citation: HortScience 58, 8; 10.21273/HORTSCI17146-23
Discussion
Overall, the rural and urban landscapes had blooming plants during the entire season each year. Baptisia produced the first flowers at each site, followed by Monarda, and the season ended with Hylotelephium and Symphyotrichum. Multiple researchers have demonstrated that the bee community composition is dependent on available floral resources of a landscape and their phenologies (Bennett and Isaacs 2014; Kraemer and Favi 2005; Richards et al. 2011). For example, Andrena asteris Robertson was associated with autumn bloom of Symphyotrichum flowers (Wolf and Ascher 2008). Thus, having flowers blooming throughout the season, especially when food is scarce for pollinators, such as early spring and fall, may encourage and support pollinator visitors that are active at those time periods. Exotic species and cultivars can support bees when native plant food sources are scarce (Braman and Griffin 2022; Mach and Potter 2018; Marquardt et al. 2021; Riddle and Mizell 2016). Riddle and Mizell (2016) suggested that some crape myrtle cultivars in the southern United States can be used when other pollen sources are scarce to reduce pollinator stress caused by food shortages. A clear example from this study was high honey bee visitations on Symphyotrichum, which flowered in late fall. Assessing the pollinator visits during bloom time leads to understanding their active flight period. Mader et al. (2011) mentioned that providing pollinators with a suitable flowering forage area and environments free of pesticides are good practices for supporting pollinators. All the current evaluated native species and cultivars would be suitable for attracting and supporting pollinators in rural or urban landscape settings in the northern Great Plains. However, in this study, the three Baptisia species did not flower in all replications, and flowers were not abundant for those that bloomed. Neither B. australis var. minor, which is native to the Midwest, nor B. alba var. alba, which is native to the southeastern United States, is native to North Dakota or Minnesota; consequently, these two taxa may not be well-adapted to grow in North Dakota. In contrast, B. australis and some of the ornamental cultivars were attractive to Bombus species in the spring and served as a niche in pollinator gardens by providing early season resources.
In this study, we demonstrated that the perennial flowering taxa at the rural landscape had 52.8% greater pollinator visitations when compared with taxa at the urban landscape. Additionally, 65.9% more bee species and 158.3% more unique bee species were found at the rural landscape. Thus, the perennial flowers grown at the rural landscape supported greater numbers and more diversity of pollinators and wild bees. This may be attributable to more diverse habitats near the rural site compared with those near the urban site. Mader et al. (2011) cited that urban landscapes lack suitable habitats to support great pollinator diversity and abundance. Bennett and Isaacs (2014) found that landscape composition had a significant effect on abundance, diversity, and community composition of bees. The surrounding land coverage of the rural landscape site had 126.3% more acreage of diverse vegetation habitats than the urban landscape; this habitat included different forests, shrubland, grass/pasture, and woody/herbaceous wetlands (US Department of Agriculture, National Agricultural Statistics Service, Cropland Data Layer 2022). Highly diverse landscapes offer better nesting and floral resource opportunities for bees (Morrison et al. 2017). Insect and other arthropod biodiversity varies and changes with the surrounding landscape habitat (Gardiner et al. 2009, 2010). The rural site also had larger and more diverse cropland coverage (US Department of Agriculture, National Agricultural Statistics Service, Cropland Data Layer 2022), which may have contributed to the greater number of pollinator visitors. Mader et al. (2011) suggested that heavily developed agricultural lands are not great habitats for supporting the diversity and abundance of pollinators. However, recently, numerous bee species have been documented in North Dakota sunflower and soybean fields (Calles Torrez et al. 2023; Mallinger et al. 2019), with the most common species Melissodes agilis Cresson and Melissodes trinodis Robertson in both crops (Calles Torrez et al. 2023).
Control programs for mosquitos may have affected pollinator visitations at the urban landscape, but not at the rural landscape. Regular applications of pesticides for controlling mosquitos using broad-spectrum active ingredients, such as synthetic pyrethroids, will kill adult mosquitoes as well as other insects exposed during application. Insecticidal spray around yards and gardens for mosquitoes or biting flies can also be harmful to pollinators, even if all precautions are taken (Smitley et al. 2019). Long and Krupke (2016) found low and high concentrations of pyrethroid insecticides used for controlling mosquitoes and other nuisance pests in pollen collected by honey bees, and they suggested that wild bees and nontarget invertebrates are also exposed to these pesticides. Increased toxicity of pyrethroid and some neonicotinoid insecticides to honey bees was reported as a result of the synergistic effect of ergosterol biosynthesis inhibitor fungicides (Pilling and Jepson 1993; Thompson et al. 2014). Some adult butterflies were also at higher risk when exposed to the mosquito control pesticide Trumpet EC (active ingredient: naled) (Bargar 2012). Overall, our results indicated that the rural and urban landscape effects had an important role in pollinator abundance and diversity. However, we cannot make an inference regarding whether spraying for mosquitos influenced our results. Furthermore, future research should focus on whether pollinators such as honey bees, wild bees, syrphids, butterflies, and other nontarget organisms are affected by this issue, especially in urban landscapes, as suggested by Long and Krupke (2016).
Visitations within insect pollinator groups varied significantly in some cases but not significantly different in other cases among the 27 perennial taxa and between landscapes in our study. However, regardless of the landscapes or native species and cultivars, the honey bees and beetles preferred to visit Hylotelephium (rose flower color variations) and Symphyotrichum (pink and lavender to purple flower colors). The wild bees, lepidopterans, and syrphids were attracted to Hylotelephium, Symphyotrichum, and Monarda (lavender, pink, red flower colors). Tachinids visited Symphyotrichum. Blow flies preferred Hylotelephium. These pollinators were most likely attracted by the showy colors of the flowers, as many researchers observed during their studies of other native species and their cultivars (Bischoff et al. 2014; Erickson 1975; Erickson et al. 2020; Ricker et al. 2019), because the color of the petals can signal pollen or nectar rewards (Fambrini et al. 2003; Schlangen et al. 2009; Waser 1983; Waser and Price 1981, 1985; Wojtaszek and Maier 2014). Previous studies found that bees showed preferences for blue and purple flowers, some syrphids preferred yellow and white flowers (Lunau and Maier 1995; Sajjad and Saeed 2010), and moths preferred to visit white flowers (Goyret et al. 2008). Braman et al. (2022) reported that syrphids visited mostly Symphyotrichum cultivars that had white or lavender color variations. Most of these colors, except white (only in Baptisia genus), were represented within each evaluated genus and could potentially attract similar insects. However, Trunschke et al. (2021) indicated that pollinator selection is more complex than just flower color. Factors such as flower structure, display, height, inflorescence (Erickson et al. 2020; Trunschke et al. 2021), aroma (Bischoff et al. 2014; Erickson 1975; Erickson et al. 2020), volume and quality of nectar (Harder 1986; Hodges and Wolf 1981; Klumpers et al. 2019; Severson and Erickson 1984), and pollen (Gaona et al. 2019; Killewald et al. 2019; Kraemer and Favi 2005; Topitzhofer et al. 2019) can influence pollinator foraging or visitations.
The feeding behavior and proboscis extension of these insect pollinators also could have influenced flower visitations, as Hansen et al. (2012) and Thompson (2001) documented. Honey bees have proportionally shorter tongues and body sizes than bumble bees (Triplehorn and Johnson 2005). Visitations of hawkmoths and some butterflies, both with long tongues, occurred more in plants with larger flowers, and their visits increased with the corolla tube length (hawkmoths) and corolla lobe length (butterflies) (Thompson 2001). Therefore, during this study, 45.5% of honey bee visitations were observed on Hylotelephium, and 51.1% were observed on Symphyotrichum; both genera have flower types that possess a smaller corolla tube length than Monarda. The most bumble bee visitations (44.8%) were observed on Monarda, which have flowers with longer tubular corollas. Similarly, bumble bees mainly visited and pollinated Monarda clinopodia L., as well as their hybrids in the southern Appalachian Mountains (Whitten 1981). Additionally, Lasioglossum imitatum (Smith), which are small bees with short tongues found at both landscapes, commonly visited Hylotelephium and Monarda. It is not unusual that smaller bees with short tongues also visit flowers that are preferred by larger bees with long tongues (Rollings and Goulson 2019), which was the case with L. imitatum visiting Monarda during this study. Insect mouthparts and body sizes also vary within a particular insect group (Triplehorn and Johnson 2005), which can explain the preferred taxa variations among the different butterfly species. For example, Papilio glaucus (Linnaeus) (Papilionidae) and Hemaris diffinis (Boisduval) (Sphingidae), which are long-tongued butterflies, only visited Monarda, whereas short-tongued A. falcifera mostly visited Hylotelephium.
Various studies suggested that wild bees and other pollinators prefer to forage on native plants (Harmon-Threatt and Kremen 2015; Morales and Traveset 2009; Morandin and Kremen 2013; Salisbury et al. 2015; Tuell et al. 2008). In contrast, other studies have generally reported no differences between native species and their cultivars regarding pollinator visitations (Mach and Potter 2018; Ricker et al. 2019). In this study, the native perennial taxa did not receive significantly more visits from wild bees when compared with their respective cultivars. Similar patterns were also found for the other pollinator groups in most cases. Interestingly, some evaluated cultivars had significantly more or similar visits compared with their respective native species. A study performed in central Kentucky to test flowering woody landscape trees and shrubs found no overall differences among native and non-native species in terms of bee visitations; in some instances, some cultivars were frequently visited by bees later in the season in urban settings (Mach and Potter 2018). Based on our results, we suggest that the evaluated perennial native species and their respective cultivars were similar attractors of wild bees and for most pollinator groups, regardless of landscapes and flower genera. Special cases involving the native species being significantly greater attractors of visitors, such as honey bees on S. novae-angliae and wasps on M. punctata in urban settings and tachinid and blow flies on S. laeve and beetles on S. novae-angliae in rural settings, may occur. Approximately 60% of the flowering plants were non-native perennial taxa, and we observed several non-native bees, such as honey bees, Anthidium manicatum (Linnaeus), Megachile rotunda (Fabricius), and Lasioglossum leucozonium (Schrank), that were attracted by several of the evaluated cultivars. Pei et al. (2023) also documented that honey bees preferred to visit exotic plants, whereas bumble bees preferred native plants. Therefore, their presence and implications of non-native bees for the native species should be investigated.
Overall, 96.0% of the beneficial insect visitations and 30.4% of the flower insect pest visitations were counted at the rural landscape. In other words, more insect pests and fewer beneficial insect visitations were counted at the urban landscape. Several studies reported that predator abundance depends on its prey abundance (Huffaker 1958; Start and Gilbert 2017) and other factors, such as the behavior of both individuals (DiRienzo et al. 2013; Klecka and Boukal 2013), body sizes (Klecka and Boukal 2013), and their surrounding landscape (Ali et al. 2020). More insect pest visitations at the urban landscape could also be attributable to the surrounding landscape composition. This landscape had fewer plant alternatives to forage when compared with the surrounding area of the rural landscape (US Department of Agriculture, National Agricultural Statistics Service, Cropland Data Layer 2022). In contrast, the increase of beneficial insect visitations at the rural landscape may be attributable to the surrounding diverse vegetation because it offered greater plant alternatives to harbor more beneficial insects as well as pests (e.g., blister beetles, stink bugs, grasshoppers, and others). However, we observed that the pests had not caused injury to the perennial taxa, except to Baptisia ‘Brownie Points’ and ‘Indigo Spires’ cultivars. These two cultivars were heavily attacked by ash-gray blister beetle E. fabricii, which caused noticeable injury, especially at the urban landscape. Therefore, the visitations of beneficial insects and insect pests to garden flowering plants are other important aspects to consider when selecting perennial flowering plants for gardening or landscaping.
This is the first study to evaluate the response of pollinators and specific bee species, other beneficial insects, and insect pests to perennial flowers associated with these native species and ornamental cultivars in North Dakota. However, future studies should increase the replication of landscape sites to strengthen the robustness of the data. Proactive stewardship is necessary to meet the needs of insect pollinators, including bees, wasps, flies, beetles, moths, and butterflies, to maintain abundant, healthy, and diverse pollinators, which benefit us and other organisms (Braman and Griffin 2022). A mixture of co-blooming (early, mid, and late bloom) flowering plants (Tuell et al. 2008) with short and long corolla tube lengths should be planted to ensure the presence of food for pollinators from spring through late fall. This study, concurrent with others (Braman et al. 2022; Marquardt et al. 2021; Ricker et al. 2019; Rollings and Goulson 2019), showed that certain ornamental cultivars are widely used by diverse groups of insect pollinators. However, ornamental cultivars should be evaluated in detail to determine pollinator attractiveness (Ricker et al. 2019) and the rewards they provide. Ornamental cultivars and native species should be integrated into pollinator gardens in rural and urban landscapes to improve aesthetics as well as attract and nourish pollinators. Our findings also help provide a guide for the selection of flowering plants for citizens of the northern Great Plains who wish to attract and support pollinators in their gardens and backyards, especially in urban areas.
References Cited
Alexandersson R, Johnson SD. 2002. Pollinator-mediated selection on flower-tube length in a hawkmoth-pollinated Gladiolus (Iridaceae). Proc Biol Sci. 269:631–636. https://doi.org/10.1098/rspb.2001.1928.
Ali MP, Kabir MMM, Haque SS, Afrin S, Ahmed N, Pittendrigh B, Qin X. 2020. Surrounding landscape influences the abundance of insect predators in rice field. BMC Zool. 5:8. https://doi.org/10.1186/s40850-020-00059-1.
American Society of Landscapes Architects. 2018. ASLA Survey: Demand high for residential landscapes with sustainability and active living elements. https://www.asla.org/NewsReleaseDetails.aspx?id=53135. [accessed 28 Mar 2022].
Anderson B, Johnson SD. 2008. The geographical mosaic of coevolution in a plant–pollinator mutualism. Evol. 62:220–225. https://doi.org/10.1111/j.1558-5646.2007.00275.x.
Anderson B, Johnson SD. 2009. Geographical covariation and local convergence of flower depth in a guild of fly-pollinated plants. New Phytol. 182:533–540. https://doi.org/10.1111/j.1469-8137.2009.02764.x.
Anonymous. 1935. A double-flowered redbud (Cercis candanesis var. plena). Missouri Bot Garden Bull. 23(5):77–78.
Ascher JS, Pickering J. 2020. Discover Life: Bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.org/mp/20q?guide+Apoidea_species. [accessed 2018–2022].
Ault JR. 2008. Baptisia plant named ‘Twilite’. Chicagoland Grows (assignee). US Plant Patent 19,011. (Filed 14 Mar 2007, granted 8 Jul 2008).
Ault JR. 2009. Baptisia plant named ‘Starlite’. Biological Patent Services, LLC. (assignee). US Plant Patent 119812. (Filed 2 Nov 2007, granted 7 May 2009).
Bargar TA. 2012. Risk assessment for adult butterflies exposed to the mosquito control pesticide naled. Environ Toxicol Chem. 31(4):885–891. https://doi.org/10.1002/etc.1757.
Beck TB, Heimlich JE, Quigley MF. 2002. Gardeners’ perceptions of the aesthetics, manageability, and sustainability of residential landscapes. Appl Environ Educ Commun. 1:163–172. https://doi.org/10.1080/15330150214006.
Bennett AB, Isaacs R. 2014. Landscape composition influences pollinators and pollination services in perennial biofuel plantings. Agric Ecosyst Environ. 193:1–8. https://doi.org/10.1016/j.agee.2014.04.016.
Bischoff M, Raguso RA, Jürgens A, Campbell DR. 2014. Context-dependent reproductive isolation mediated by floral scent and color. Evolution. 69(1):1–13. https://doi.org/10.1111/evo.12558.
Bloch D, Erhardt A. 2008. Selection toward shorter flowers by butterflies whose probosces are shorter than floral tubes. Ecology. 89(9):2453–2460. https://doi.org/10.1890/06-2023.1.
Braman SK, Griffin B. 2022. Opportunities for and impediments to pollinator conservation in urban settings: A review. J Integr Pest Manag. 13(1):1–15. https://doi.org/10.1093/jipm/pmac004.
Braman SK, Pennisi SV, Fair CG, Quick JC. 2022. Pollinator cultivar choice: An assessment of season-long pollinator visitation among coreopsis, aster, and salvia cultivars. Front Sustain Cities. 4. https://doi.org/10.3389/frsc.2022.988966.
Calles Torrez V, Beauzay P, St. Clair AL, Knodel JJ. 2023. Survey of bees (Hymenoptera: Apoidea) in flowering soybean and sunflower fields in North Dakota. J Kans Entomol Soc. (in press).
Couvillon MJ, Riddell Pearce FC, Accleton C, Fensome KA, Quah SKL, Taylor EL, Ratnieks FLW. 2015. Honey bee foraging distance depends on month and forage type. Apidologie (Celle). 46:61–70. https://doi.org/10.1007/s13592-014-0302-5.
Dicks LV, Breeze TD, Ngo HT, Senapathi D, An J, Aizen M, Basu P, Buchori D, Galetto L, Garibaldi LA, Gemmill-Herren B, Howlett BG, Imperatriz-Fonseca VL, Johnson SD, Kovács-Hostyánszki A, Kwon YJ, Lattorff HMG, Lungharwo T, Seymour CL, Vanbergen AJ, Potts SG. 2021. A global-scale expert assessment of drivers and risks associated with pollinator decline. Nat Ecol Evol. 5(10):1453–1461. https://doi.org/10.1038/s41559-021-01534-9.
DiRienzo N, Pruitt JN, Hedrick AV. 2013. The combined behavioural tendencies of predator and prey mediate the outcome of their interaction. Anim Behav. 86:317–322. https://doi.org/10.1016/j.anbehav.2013.05.020.
Droege S. 2010. The very handy manual: How to catch and identify bees and manage a collection. https://bee-health.extension.org/wp-content/uploads/2019/08/TheVeryHandyBeeManual.pdf. [accessed 19 Nov 2022].
Ehrlich PR, Raven PH. 1964. Butterflies and plants: A study in coevolution. Evolution. 18:586–608. https://doi.org/10.2307/2406212.
Erickson EH. 1975. Variability of floral characteristics influences honey bee visitation to soybean blossoms. Crop Sci. 15(6):767–771. https://doi.org/10.2135/cropsci1975.0011183X001500060008x.
Erickson E, Adam S, Russo L, Wojcik V, Patch HM, Grozinger CM. 2020. More than meets the eye? The role of annual ornamental flowers in supporting pollinators. Environ Entomol. 49(1):178–188. https://doi.org/10.1093/ee/nvz133.
Fambrini M, Bertini D, Pugliesi C. 2003. The genetic basis of a mutation that alters the floral symmetry in sunflower. Ann Appl Biol. 143:341–347. https://doi.org/10.1111/j.1744-7348.2003.tb00303.x.
Flemer W. 1979. Hydrangea quercifolia. Treesearch (assignee). U.S. Plant Patent 4,458. (Filed 18 Oct 1978, granted 4 Sep 1979).
Gaona FP, Guerrero A, Gusmán E, Iván Espinosa C. 2019. Pollen resources used by two species of stingless bees (Meliponini) in a tropical dry forest of Southern Ecuador. J Insect Sci. 19(6):22; 1–5. https://doi.org/10.1093/jisesa/iez125.
Gardiner MM, Landis DA, Gratton C, Schmidt N, O’Neal M, Mueller E, Chacon J, Heimpel GE. 2010. Landscape composition influences the activity density of Carabidae and Arachnida in soybean fields. Biol Control. 55(1):11–19. https://doi.org/10.1016/j.biocontrol.2010.06.008.
Gardiner MM, Landis DA, Gratton C, Schmidt N, O’Neal ME, Mueller E, Chacon J, Heimpel GE, DiFonzo CD. 2009. Landscape composition influences patterns of native and exotic lady beetle abundance. Divers Distrib. 15:554–564. https://doi.org/10.1111/j.1472-4642.2009.00563.x.
Gathmann A, Tscharntke T. 2002. Foraging ranges of solitary bees. J Anim Ecol. 71:757–764. https://doi.org/10.1046/j.1365-2656.2002.00641.x.
Getanjaly VLR, Sharma P, Kushwaha R. 2015. Beneficial insects and their value to agriculture. Res J Agriculture and Forestry Sci. 3(5):25–30. http://www.isca.in/AGRI_FORESTRY/Archive/v3/i5/5.ISCA-RJAFS-2015-012.pdf.
Gibbs J. 2010. Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera: Halictidae: Halictini). Zootaxa. 2591:1–382. https://doi.org/10.11646/zootaxa.2591.1.1.
Gibbs J. 2011. Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa. 3073(1):1–216. https://doi.org/10.11646/zootaxa.3073.1.1.
Gibbs J, Packer L, Dumesh S, Danforth BN. 2013. Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in eastern North America (Hymenoptera: Apoidea: Halictidae). Zootaxa. 3672(1):1–117. https://doi.org/10.11646/zootaxa.3672.1.1.
Goulson D, Nicholls E, Botías C, Rotheray EL. 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 347(6229):1255957. https://doi.org/10.1126/science.1255957.
Goyret J, Pfaff M, Raguso RA, Kelber A. 2008. Why do Manduca sexta feed from white flowers? Innate and learnt colour preference in a hawkmoth. Naturwissenschaften. 95:569–576. https://doi.org/10.1007/s00114-008-0350-7.
Hansen DM, Van der Niet T, Johnson SD. 2012. Floral signposts: Testing the significance of visual ‘nectar guides’ for pollinator behaviour and plant fitness. Proc Biol Sci. 279:634–639. https://doi.org/10.1098/rspb.2011.1349.
Harder LD. 1986. Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia. 69(2):309–315. https://www.jstor.org/stable/4217946.
Harmon-Threatt AN, Kremen C. 2015. Bumble bees selectively use native and exotic species to maintain nutritional intake across highly variable and invaded local floral resource pools. Ecol Entomol. 40:471–478. https://doi.org/10.1111/een.12211.
Harris B, Braman K, Pennisi B, Putzke M. 2022. The eco-friendly garden: Attracting pollinators, beneficial insects, and other natural predators. Univ. Georgia Cooperative Ext Bull 1456.
Harris BA, Braman SK, Pennisi SV. 2016. Influence of plant taxa on pollinator, butterfly, and beneficial insect visitation. HortScience. 51(18):1016–1019. https://doi.org/10.21273/HORTSCI.51.8.1016.
Hodges CM, Wolf LL. 1981. Optimal foraging in bumblebees: Why is nectar left behind in flowers? Behav Ecol Sociobiol. 9:41–44. https://www.jstor.org/stable/4599408.
Holm H. 2014. Pollinators of native plants: Attract observe and identify pollinators and beneficial insects with native plants (1st ed). Pollination Press LLC, Minnetonka, MN, USA.
Hopkins KA, Hall CR, Arnold MA, Palma MA, Knuth M, Pemberton B. 2022. Consumer preferences of Ratibida columnifera (Nutt.) Wooton & Standl. floral characteristics. HortScience. 57(3):431–440. https://doi.org/10.21273/HORTSCI16233-21.
Huffaker CB. 1958. Experimental studies on predation: Dispersion factors and predator-prey oscillations. Hilgardia. 27(14):343–383. https://doi.org/10.3733/hilg.v27n14p343.
Johnson R, Corn ML. 2015. Bee health: Background and issues for congress. Congressional Research Service R43191, Version 10. https://sgp.fas.org/crs/misc/R43191.pdf. [accessed 20 Nov 2022].
Kevan PG, Clark EA, Thomas VG. 1990. Insect pollinators and sustainable agriculture. Am J Altern Agric. 5(1):13–22. https://doi.org/10.1017/S0889189300003179.
Khan M, Lanjar AG, Chang BH, Bukero A, Rajput A, Magsi FH, Shah R, Solangi AW, Chang AH. 2019. Insect pests associated with ornamental plants. Pak J Sci Ind Res Ser B Biol Sci. 62(3):188–194.
Killewald MF, Rowe LM, Graham KK, Wood TJ, Isaacs R. 2019. Use of nest and pollen resources by leafcutter bees, genus Megachile (Hymenoptera: Megachilidae) in Central Michigan. Gt Lakes Entomol. 52(1):34–44. https://scholar.valpo.edu/tgle/vol52/iss1/8.
Kirk Visscher P, Seeley TD. 1982. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology. 63(6):1790–1801. https://doi.org/10.2307/1940121.
Klecka J, Boukal DS. 2013. Foraging and vulnerability traits modify predator-prey body mass allometry: Freshwater macroinvertebrates as a case study. J Anim Ecol. 82:1031–1041. https://doi.org/10.1111/1365-2656.12078.
Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T. 2007. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci. 274:303–313. https://doi.org/10.1098/rspb.2006.3721.
Klumpers SGT, Stang M, Klinkhamer PGL. 2019. Foraging efficiency and size matching in a plant-pollinator community: The importance of sugar content and tongue length. Ecol Lett. 22:469–479. https://doi.org/10.1111/ele.13204.
Kraemer ME, Favi FD. 2005. Flower phenology and pollen choice of Osmia lignaria (Hymenoptera: Megachilidae) in Central Virginia. Environ Entomol. 34(6):1593–1605. https://doi.org/10.1603/0046-225X-34.6.1593.
Long EY, Krupke CH. 2016. Non-cultivated plants present a season-long route of pesticide exposure for honey bees. Nat Commun. 7:11629. https://doi.org/10.1038/ncomms11629.
Lunau K, Maier EJ. 1995. Innate colour references of flower visitors. J Comp Physiol A. 177:1–19.
Mach BM, Potter DA. 2018. Quantifying bee assemblages and attractiveness of flowering woody landscape plants for urban pollinator conservation. PLoS One. 13(12):e0208428. https://doi.org/10.1371/journal.pone.0208428.
Mader E, Shepherd M, Vaughan M, Black S, LeBuhn G. 2011. Attracting native pollinators: Protecting North America’s bees and butterflies: The Xerces Society guide. Storey Publishing, North Adams, MA, USA.
Mallinger RE, Bradshaw J, Varenhorst AJ, Prasifka JR. 2019. Native solitary bees provide economically significant pollination services to confection sunflowers (Helianthus annuus L.) (Asterales: Asteraceae) grown across the Northern Great Plains. J Econ Entomol. 112(1):40–48. https://doi.org/10.1093/jee/toy322.
Marquardt M, Kienbaum L, Kretschmer LA, Penell A, Schweikert K, Ruttensperger U, Rosenkranz P. 2021. Evaluation of the importance of ornamental plants for pollinators in urban and suburban areas in Stuttgart, Germany. Urban Ecosyst. 24:811–825. https://doi.org/10.1007/s11252-020-01085-0.
Marquis RJ. 2004. Herbivores rule. Sci. 305:619–621. https://doi.org/10.1126/science.1101848.
McGinley RJ. 1986. Studies of Halictinae (Apoidea: Halictidae), I: Revision of new world Lasioglossum Curtis. Smithson Contrib Zool. 429:1–294. https://doi.org/10.5479/si.00810282.429.
McGregor SE. 1976. Insect pollination of cultivated crop plants. US Department of Agriculture, Agricultural Research Service, Tucson, AZ, USA. https://www.ars.usda.gov/arsuserfiles/20220500/onlinepollinationhandbook.pdf. [accessed 13 Jan 2022].
Melathopoulos A, Bell N, Danler S, Detweiler AJ, Kormann I, Langellotto G, Sanchez N, Smitley D, Stoven H. 2020. Enhancing urban and suburban landscapes to protect pollinators. Oregon State Univ Ext Service Bull EM9289.
Michener CD. 2007. The Bees of the World (2nd ed). Johns Hopkins University Press, Baltimore, MD, USA.
Mitchell TB. 1960. Bees of the eastern United States, volume 1. NC Agr Exp Sta Te Bull. 141:1–538.
Mitchell TB. 1962. Bees of the eastern United States, volume 2. NC Agr Exp Sta Te Bull. 152:1–557.
Morales CL, Traveset A. 2009. A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett. 12:716–728. https://doi.org/10.1111/j.1461-0248.2009.01319.x.
Morandin LA, Kremen C. 2013. Bee preference for native versus exotic plants in restored agricultural hedgerows. Restor Ecol. 21(1):26–32. https://doi.org/10.1111/j.1526-100X.2012.00876.x.
Morrison J, Izquierdo J, Plaza EH, González-Andújar JL. 2017. The role of field margins in supporting wild bees in Mediterranean cereal agroecosystems: Which biotic and abiotic factors are important? Agric Ecosyst Environ. 247:216–224. https://doi.org/10.1016/j.agee.2017.06.047.
Nassauer JI. 1995. Messy ecosystems, orderly frames. Landsc J. 14(2):161–170. https://www.jstor.org/stable/43324192.
National Research Council. 2007. Status of pollinators in North America. The National Academies Press, Washington, D.C., USA.
Oudshoorn HG. 2012. Monarda plant named ‘Sugar Lace’. Future Plants Licentie B.V. (assignee). U.S. Plant Patent 22,918. (Filed 7 Feb 2011, granted 31 Jul 2012).
Onuferko TM. 2017. Cleptoparasitic bees of the genus Epeolus Latreille (Hymenoptera: Apidae) in Canada. Can J Arthropod Identif. 30:1–62. https://doi.org/10.3752/cjai.2017.30.
Pei CK, Hovick TJ, Limb RF, Harmon JP, Geaumont BA. 2023. Native and introduced pollinators vary in their seasonal floral resource visitation and selection between native and exotic plant species. J Appl Ecol. 60:1424–1434. https://doi.org/10.1111/1365-2664.14416.
Pilling ED, Jepson PC. 1993. Synergism between EBI fungicides and a pyrethroid insecticide in the honey bee (Apis mellifera). Pestic Sci. 39:293–297. https://doi.org/10.1002/ps.2780390407.
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. 2010. Global pollinator declines: Trends, impacts and drivers. Trends Ecol Evol. 25(6):345–353. https://doi.org/10.1016/j.tree.2010.01.007.
Ricker JG, Lubell JD, Brand MH. 2019. Comparing insect pollinator visitation for six native shrub species and their cultivars. HortScience. 54(11):2086–2090. https://doi.org/10.21273/HORTSCI14375-19.
Richards MH, Rutgers-Kelly A, Gibbs J, Vickruck JL, Rehan SM, Sheffield CS. 2011. Bee diversity in naturalizing patches of Carolinian grasslands in southern Ontario, Canada. Can Entomol. 143:279–299. https://doi.org/10.4039/n11-010.
Riddle TC, Mizell RF. 2016. Use of crape myrtle, Lagerstroemia (Myrtales: Lythraceae), cultivars as a pollen source by native and non-native bees (Hymenoptera: Apidae) in Quincy Florida. Fla Entomol. 99(1):38–46. https://doi.org/10.1653/024.099.0108.
Roberts RB. 1972. Revision of the bee genus Agapostemon (Hymenoptera: Halictidae). Univ Kans Sci Bull. 59(9):437–590.
Rollings R, Goulson D. 2019. Quantifying the attractiveness of garden flowers for pollinators. J Insect Conserv. 23:803–817. https://doi.org/10.1007/s10841-019-00177-3.
Sajjad A, Saeed S. 2010. Floral host plant range of syrphid flies (Syrphidae: Diptera) under natural conditions in southern Punjab, Pakistan. Pak J Bot. 42(2):1187–1200.
Salisbury A, Armitage J, Bostock H, Perry J, Tatchell M, Thompson K. 2015. Enhancing gardens as habitats for flower-visiting aerial insects (pollinators): Should we plant native or exotic species? J Appl Ecol. 52:1156–1164. https://doi.org/10.1111/1365-2664.12499.
SAS Institute. 2013. PROC user’s manual, version 9.4 ed. SAS Institute, Cary, NC.
Schlangen K, Miosic S, Castro A, Freudmann K, Luczkiewicz M, Vitzthum F, Schwab W, Gamsjäger S, Musso M, Halbwirth H. 2009. Formation of UV-honey guides in Rudbeckia hirta. Phytochemistry. 70:889–898. https://doi.org/10.1016/j.phytochem.2009.04.017.
Seeley TD. 1995. The wisdom of the hive: The social physiology of honey bee colonies. Harvard University Press, London, England.
Severson DW, Erickson EH Jr. 1984. Quantitative and qualitative variation in floral nectar of soybean cultivars in southeastern Missouri. Environ Entomol. 13:1091–1096. https://doi.org/10.1093/ee/13.4.1091.
Sheffield CS, Ratti C, Packer L, Griswold T. 2011. Leafcutter and mason bees of the genus Megachile Latreille (Hymenoptera: Megachilidae) in Canada and Alaska. Can J Arthropod Identif. 18:1–107. https://doi.org/10.3752/cjai.2011.18.
Smitley D, Brown D, Finneran R, Elsner E, Landis JN, Shrewsbury PM, Herms DA, Palmer CL. 2019. Protecting and enhancing pollinators in urban landscapes for the US Northern Central Region. Michigan State Univ Ext Bull E3314.
Soroye P, Newbold T, Kerr J. 2020. Climate change contributes to widespread declines among bumble bees across continents. Science. 367:685–688. https://doi.org/10.1126/science.aax8591.
Start D, Gilbert B. 2017. Predator personality structures prey communities and trophic cascades. Ecol Lett. 20(3):366–374. https://doi.org/10.1111/ele.12735.
Thapa RB. 2006. Honeybees and other insect pollinators of cultivated plants: A review. J Inst Agric Anim Sci. 27:1–23. https://doi.org/10.3126/jiaas.v27i0.691.
Tenczar EG, Krischik VA. 2007. Effects of new cultivars of ninebark on feeding and ovipositional behavior of the specialist ninebark beetle, Calligrapha spiraeae (Coleoptera: Chrysomelidae). HortScience. 42(6):1396–1399. https://doi.org/10.21273/HORTSCI.42.6.1396.
Thompson HM, Fryday SL, Harkin S, Milner S. 2014. Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie (Celle). 45(5):545–553. https://doi.org/10.1007/s13592-014-0273-6.
Thompson JD. 2001. How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia. 126:386–394. https://doi.org/10.1007/s004420000531.
Topitzhofer E, Lucas H, Chakrabarti P, Breece C, Bryant V, Sagili RR. 2019. Assessment of pollen diversity available to honey bees (Hymenoptera: Apidae) in major cropping systems during pollination in the Western United States. J Econ Entomol. 112(5):2040–2048. https://doi.org/10.1093/jee/toz168.
Triplehorn CA, Johnson NF. 2005. Borror and DeLong’s introduction to the study of insects (7th ed), Thomson Brooks/Cole, Belmont, CA, USA.
Trunschke J, Lunau K, Pyke GH, Ren Z-X, Wang H. 2021. Flower color evolution and the evidence of pollinator-mediated selection. Front Plant Sci. 12:617851. https://doi.org/10.3389/fpls.2021.617851.
Tuell JK, Fiedler AK, Landis D, Isaacs R. 2008. Visitation by wild and managed bees (Hymenoptera: Apoidea) to eastern U.S. native plants for use in conservation programs. Environ Entomol. 37(3):707–718. https://doi.org/10.1603/0046-225X(2008)37[707:VBWAMB]2.0.CO;2.
Tukey JW. 1953. The problem of multiple comparisons. Department of Statistics, Princeton University, NJ, USA.
US Fish and Wildlife Service. 2014. Endangered and threatened wildlife and plants; threatened species status for dakota skipper and endangered species status for poweshiek skipperling. Fed Regist. 79(206):63672–63748.
US Fish and Wildlife Service. 2017. Endangered and threatened wildlife and plants; endangered species status for rusty patched bumble bee. Fed Regist. 82(7):3186–3188.
US Fish and Wildlife Service. 2022. Pollinators. https://www.fws.gov/initiative/pollinators. [accessed 22 Mar 2022].
US Department of Agriculture. 2022. USDA Annual strategic pollinator priorities report. https://www.usda.gov/sites/default/files/documents/annual-pollinator-report-2022.pdf. [accessed 23 jun 2023].
US Department of Agriculture, Natural Resources Conservation Service. 2022. PLANTS Database. http://plants.usda.gov. [accessed 24 Mar 2022].
US Department of Agriculture, National Agricultural Statistics Service, Cropland Data Layer. 2022. CropScape – cropland data layer. https://nassgeodata.gmu.edu/CropScape/. [accessed 16 Jan 2022].
Vasiliev D, Greenwood S. 2021. The role of climate change in pollinator decline across the northern hemisphere is underestimated. Sci Total Environ. 775:145788. https://doi.org/10.1016/j.scitotenv.2021.145788.
Wagner DL, Grames EM, Forister ML, Berenbaum MR, Stopak D. 2021. Insect decline in the anthropocene: Death by a thousand cuts. Proc Natl Acad Sci USA. 118(2):E2023989118. https://doi.org/10.1073/pnas.2023989118.
Walliser J. 2014. Attracting beneficial bugs to your garden: A natural approach to pest control. Timber Press, Portland, OR, USA.
Waser NM. 1983. The adaptive nature of floral traits: Ideas and evidence, p 241–285. In: Real L. Pollination biology. Academic Press, Orlando, FL, USA.
Waser NM, Price MV. 1981. Pollinator choice and stabilizing selection for flower color in Delphinium nelsonii. Evolution. 35(2):376–390. https://doi.org/10.2307/2407846.
Waser NM, Price M. 1985. The effect of nectar guides on pollinator preference: Experimental studies with a montane herb. Oecologia. 67:121–126. https://www.jstor.org/stable/4217699.
Wilde HD, Gandhi KJK, Colson G. 2015. State of the science and challenges of breeding landscape plants with ecological function. Hortic Res. 2:14069. https://doi.org/10.1038/hortres.2014.69.
Whitten WM. 1981. Pollination ecology of Monarda didyma, M. clinopodia, and hybrids (Lamiaceae) in the southern Appalachian Mountains. Am J Bot. 68(3):435–442. https://doi.org/10.1002/j.1537-2197.1981.tb06382.x.
Wojtaszek JW, Maier C. 2014. A Microscopic review of the sunflower and honeybee mutualistic relationship. Int J Agrisci. 4(5):272–282. https://www.cabdirect.org/cabdirect/abstract/20143217350.
Woteki C. 2013. The road to pollinator health. Science. 341:695. https://doi.org/10.1126/science.1244271.
Wolf AT, Ascher JS. 2008. Bees of Wisconsin (Hymenoptera: Apoidea: Anthophila). Great Lakes Entomol. 41:129–168. https://michentsoc.org/gle-pdfs/vol41no3-4.pdf#page=29.
Zattara EE, Aizen MA. 2021. Worldwide occurrence records suggest a global decline in bee species richness. One Earth. 4:114–123. https://doi.org/10.1016/j.oneear.2020.12.005.
Xerces Society. 2022. Pollinator conservation program. https://www.xerces.org/pollinator-conservation. [accessed 8 Apr 2022].
Zurbuchen A, Cheesman S, Klaiber J, Müller A, Hein S, Dorn S. 2010a. Long foraging distances impose high costs on offspring production in solitary bees. J Anim Ecol. 79(3):674–681. https://doi.org/10.1111/j.1365-2656.2010.01675.x.
Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S. 2010b. Maximum foraging ranges in solitary bees: Only few individuals have the capability to cover long foraging distances. Biol Conserv. 143(3):669–676. https://doi.org/10.1016/j.biocon.2009.12.003.