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Habitat Preference and Phenology of Nest Seeking and Foraging Spring Bumble Bee Queens in Northeastern North America (Hymenoptera: Apidae: Bombus).


Bumble bees (Bombus spp. Latreille) are abundant and widely recognized as economically and ecologically important pollinators. Because they are larger bodied than most wild bees, they are better able to forage and transport pollen over long distances and to fly in cooler weather (Willmer, 1983; Cresswell et al., 2000; Osborne et al, 2008; Pope and jha, 2018). The queens of nonparasitic Bombus species initiate their eusocial nests in the early spring. They are adapted to forage in conditions that are not ideal for most bees, making them key pollinators of native spring wild flowers (Fye and Medler, 1954; Macior, 1968, 1978; Thomson, 1986; Prusnek, 1999) and orchard crops (Javorek et al, 2002; Drummond, 2012).

Although bumble bees are among the most common wild bees in the Holarctic, their nests are notoriously difficult to find, because they are typically underground in abandoned rodent burrows and have their entrances concealed by dense vegetation, herbaceous debris, fallen logs, tree stumps, buttressing tree bases, brush piles, or manmade objects and structures (Franklin, 1912; Frison, 1923; Plath, 1934; Hobbs, 1965, 1966a, 1966b, 1967, 1968). Some species are also known to dig false entrances or to camouflage the nest entrance with moss or grass (e.g. B. fervidus Fabricius, B. occidentals Greene) (Hobbs, 1966a, 1968; Richards, 1975). Historic studies often relied on placing large numbers of artificial domiciles to attract queens to obtain colonies for experiments (Sladen, 1912; Frison, 1923; Hobbs, 1964-1968). Contemporary studies have located nests using large groups of volunteers (Frison, 1923; Fussell and Corbet, 1992; Osborne et al, 2008; Lye et al, 2012; O'Connor et al, 2012), trained detection dogs (Waters et al, 2011; O'Connor et al, 2012), and transect searches (Svensson et al, 2000; Kells and Goulson, 2003; Lye et al, 2009; O'Connor et al, 2017). Advances in modern genetic tools have made it possible to estimate summer nest density from worker genetic diversity (Darvill et al, 2004; Knight et al, 2009; Lepais et al, 2010; Dreier et al, 2014; Carvell et al, 2017). Direct surveys of spring foundress queens, however, provide essential ecological and phenological information on bumble bee natural history that can advance conservation efforts. In Europe studies have largely focused on how land management, particularly urbanization (Osborne et al., 2008) and agriculture (Svensson et al., 2000; Kells and Goulson, 2003; Lye et al, 2009; Samuelson et al, 2018), affect bumble bee nesting. The majority of work on the nesting ecology of North American species is limited to high latitudes and high-altitude montane habitat or was conducted before the period of documented bumble bee declines in the latter half of the 1900's (Plath, 1934; Hobbs, 1964, 1965, 1966a, 1966b, 1967, 1968; Macior, 1968; Macfarlane, 1974; Richards, 1975, 1978; Bowers, 1985; Macfarlane et al, 1994). It is a barrier to bee conservation efforts that our understanding of their nesting biology and habitat use is incomplete for many species.

Recent and historic surveys and museum specimens have recorded 20 Bombus species in the state of Ohio, which is located at the convergence of the Midwestern and Northeastern regions of the United States. However, almost half of them have not been seen in Ohio for more than 20 y (Table Al) and several Bombus species have recently declined. Notably, the once common rusty-patched bumble bee (B. affinis Cresson) has declined dramatically in the last two decades and was listed as federally endangered in 2017 (Colla and Packer, 2008; Grixti et al, 2009; Colla et al, 2012; USFWS, 2017; Jacobson et al, 2018). The cause of its sudden decline remains a mystery. Previous studies have investigated diet breadth, tongue length, body size, genetic diversity, pesticide exposure, and parasites and pathogens as possible agents of bumble bee decline worldwide (Williams et al., 2007; Kleijn and Raemakers, 2008; Williams and Osborne, 2009; Williams et al., 2009; Cameron et al, 2011; Szabo et al, 2012; Maebe et al, 2015; Cameron et al., 2016), although nesting ecology has received little attention.

The early stages in the bumble bee colony life cycle are a sensitive time (Macfarlane, 1974), yet the process of queen nest site selection and nest initiation are less understood than later colony growth and reproduction. Previous work on nesting biology suggest many species share similar nest site preferences, leading to strong intra- and inter-specific competition for nest sites (Plath, 1934; Hobbs, 1964-1968; Richards, 1975). For example the U.S. Federally Endangered B. affinis shares its nesting niche with other species (Plath, 1934) and so may experience high rates of usurpation and competition. Higginson (2017) concluded species with late-emerging queens, especially those with a relatively large body size, are at a disadvantage when competing for limited high-quality nest sites. On the other hand, queens that found nests early in the season may be more vulnerable to usurpation by other foundresses and invasion by social parasites in the Bombus subgenus Psithyrus (Hobbs, 1968; Richards, 1975). In addition to pressure from competitors and parasites, if climate change alters the onset and duration of spring weather, it could also change the dynamics of bumble bee nest founding. The timing of queen emergence and nesting, preferred nesting habitat, and other natural history traits will influence the evolution and long-term persistence of species. Therefore, contemporaiy baseline data are needed on the timing of queen emergence and nesting activities of both common and declining bumble bee species.

In this study the nesting and foraging ecology of bumble bees in Ohio, U.S.A. was investigated using standardized field surveys of spring foundress queens, augmented with observations of nest seeking queens submitted by trained volunteers. The objectives of this study were to: (1) identify the habitats where bumble bee queens search for nest sites and to evaluate the possible influence of the local landscape; (2) to delineate the phenology (timing and duration) of queen emergence and nest seeking; and (3) to compile a list of important food plants for foraging bumble bee queens.


From 1 May-8 June 2018, researchers conducted nonlethal surveys of foraging and nest seeking bumble bee queens at 115 field sites in 28 counties in Ohio, U.S.A. (see Table A2 for GPS coordinates and other survey details). Survey sites included public parks, preserves, and private properties, with >0.5 ha of potential bee foraging and nesting habitat, and separated from one another by at least 3 km. Surveys were conducted on fair weather days when the air temperature was at least 15.5 C (mean temperature at time of survey 25.5 C [+ or -] 4.0) with little wind, between the hours of 0800 and 1900. Teams of one to five observers walked slowly and continuously through a site for a total of 60 min searching all available habitat types but paying particular attention to areas with dense vegetative or woody debris (e.g., grass clumps, leaf litter, or fallen logs) or complex microtopography (e.g., stream banks, buttressing tree bases, and road embankments). This approach allowed observers to cover a large area while maximizing survey yield. If bees were netted for identification, handling time was not included in the 60 min of searching time. Observers sought to minimize double-counting individual queens by moving to a new patch of flowers or potential nesting habitat after a queen was observed. At each site the start and end time of survey, the temperature, cloud conditions (sunny, partly sunny, or cloudy), average ground wind speed, and the amount of time spent searching each habitat type were recorded. Within a site habitats searched were classified into five categories based on their floral and nesting resources for bees: (1) wooded (evergreen and deciduous forest, riparian forest, and woodland); (2) edge (interface between wooded and open habitat); (3) field (grasslands and meadows); (4) wetland (seasonally inundated area); and (5) maintained area (flower beds, gardens, and lawns). The growing degree day (GDD) for each survey was obtained from the location and sample date using an online calculator available from the Ohio State University Extension ( Queen surveys ceased after the first week of June when workers of most species had emerged (see also Macior, 1968).

Bumble bee queens, and later workers, were either identified to species in the field or netted and photographed in plastic vials for later identification using Williams et al. (2014) then rereleased on site. In rare cases, where species identity could not be verified in the field (such as the B. sandersotii), the specimen was vouchered.

During timed surveys researchers recorded a list of the flowering plant species in bloom at the site that were potential food sources for bumble bees, noting which species were flowering abundantly and likely to attract bumble bees. This method was chosen over the transect or quadrat methods typically used to survey plant communities because it captured bee-preferred flowers better given the wide foraging radii of queens and the patchy and three-dimensional distribution of tree, shrub, and herbaceous flower resources.

At the time of observation, each queen's behavior was categorized as either flying, foraging, or nest seeking. Flying queens made fast and mostly linear flights, usually >2 m above the ground. Foraging queens were those observed visiting flowers, and the species of plant was recorded. Nest seeking queens were recognized by their behavior; they mostly flew slowly and low to the ground, frequently changing direction and stopping to investigate crevices and cavities. For foraging and nest seeking queens, it was noted whether or not each queen was carrying pollen in her corbiculae, an indicator that she had already founded a nest.

For nest seeking queens, additional information was collected. The habitat type in which each nest seeking queen was observed was categorized as wooded, edge, field, wetland, or maintained area as in timed surveys. The presence or absence of each of the following microhabitat features was noted in an approximately 2 m radius area around the location where a queen was searching for a nest site: leaf litter, herbaceous litter, grass clumps or tussocks, fallen logs or large woody debris, rock piles, mounds of bare soil, moss, stream or river, lake or pond, trees in full bloom, shrubs in full bloom, and herbaceous plants in full bloom.

Citizen science data were used to augment observations of Bombus queen nest seeking behavior collected by researchers in timed surveys. Fifty adult volunteers were recruited from the Ohio Certified Volunteer Naturalist program of the Ohio State University Extension program. Volunteers were trained in bumble bee species identification and nest seeking queen data collection through a combination of in-person (6 h workshop) and on-line tutorials (1.5 h interactive video lectures, They were instructed to report queens encountered in any habitat, submit a photograph for species verification, and enter all locality, habitat, and microhabitat data on nest seeking using a dedicated Google Forms survey or by email on standardized data collection sheets. Assistance with data reporting and verification of species identifications was provided by email. Ultimately, 21 volunteers submitted data on 80 nest seeking queens between 1 April and 1 June, 2018, following the same format as the researchers for collecting data on individual nest seekers, but not participating in the timed researcher surveys.

This sampling approach yielded two data sets. The Timed Survey data set was used to investigate the influence of growing degree day, flower richness, and landscape factors on queen abundance and species richness, and to compose a list of key spring food plants for queens. The Augmented Nest Seekers data set, which included verified citizen science observations, was used to infer the habitat and microhabitat preferences of individual nest seeking queens.

For all sites where researchers conducted timed queen surveys, the surrounding land use was extracted in ArcGIS 10.6.1 software (ESR1, 2018) within a 1 km buffer area of the site center, a radius which encompassed all habitats types researchers searched and was relevant to bumble bee foraging distances. Land cover was taken from the National Land Cover Dataset (NLCD, Homer et al., 2015), which classifies land use with 30 m resolution into 15 categories for the conterminous U.S. For this study land cover categories in the original dataset were simplified into broader categories based on the quality of bumble bee nesting and food resources they offer, as follows: open water, developed lands, forest, shrubland, herbaceous land (including pasture), row crop agriculture, and wetland.

Data on the first sighting of each species during this study were compared to regional spring queen emergence data gleaned from the literature. The earliest emergence dates for each species in our study and in 11 other field surveys of bumble bee queens in Northeastern North America were compiled. Growing degree day for emergence dates in earlier studies could not be calculated because the survey locations were not reported in sufficient detail.


All data analyses were conducted in R version 3.5.2 (R Development Core Team, 2018). To test the influence of time of day, weather, and habitat on total queen abundance, species richness, and nest seeking queens per minute of search time by habitat, nonparametric Kruskal-Wallis rank sum tests with Dunn's post hoc group-wise comparisons (function dunn.test, Dinno, 2017) were used. Spearman correlation analysis was used to determine the influence of growing degree day (GDD), flowering plant richness, temperature, and surrounding land use components on queen abundance and richness. The model residuals in parametric analyses (Pearson correlation and ANOVA) were tested for normality using Shapiro-Wilks tests (function shapiro. test) and found not to conform to a Gaussian distribution. Queens that were observed flying overhead (neither foraging nor nest seeking) that were not identifiable to species were included in tallies of queen abundance, but not in species-specific analyses or in analyses of nest-seeking or foraging queens.

To understand how land use, GDD, and flower richness influenced queen abundance and species richness in timed surveys, multivariate models were constructed. First, all predictor variables were standardized by subtracting the variable average from each observation and dividing by SD. Principal components analysis (PCA) with varimax rotation was then used to account for correlations among predictor variables (prcomp function, varimax function). The three factors that had eigenvalues greater than one were retained. Those principal components were used as predictors in generalized linear models (GLMs) of nest seeking and foraging queen abundance and queen species richness. The full models were constructed using Gaussian, Poisson, and Negative Binomial family error distributions, and the model with the lowest AIC value was selected for each response variable.

In order to compare earliest queen observation dates between this and 11 other surveys across northeastern North America (1920-2018), latitude and year were regressed against earliest calendar observation day for each bumble bee species using Spearman correlation. If observation location was given only as a state or province, the latitude of the geographic center of that area was used. If observation dates were given as a range of years instead of a precise day, the most recent year was used.


In 108 timed field surveys, researchers observed a total of 1089 bumble bee queens of nine different species (Table 1). These species differed widely in abundance (ordered from most to least): Bombus impatiens Cresson (55.1 % of total queens), B. griseocollis De Geer (17.7 %), B. bimaculatus Cresson (5.1 %), B. vagans Smith (3.1 %), B. fervidus Fabricais (1.7 %), B. auricomus Robertson (0.6 %), B. citrinus Smith (0.4 %), B. perplexus Cresson (0.2 %), and B. sandersoni (<0.1 %). Of those 451 queens were searching for nest sites and 555 were foraging on 47 species of flowering plants. The remainder were observed flying overhead and exhibiting neither nest seeking nor foraging behavior. On average 10.08 [+ or -] 9.62 SD queens were observed per hour (range: 1-46, n = 108). Out of the 1006 nest seeking and foraging queens, 241 were observed carrying pollen, indicating they had already founded a nest. The raw data from timed bumble bee queen surveys, as well as additional information on individual nest seeking queens, is available through Dryad Digital Repository.


In timed surveys significantly more nest seeking queens per minute were found along field-forest edges and in maintained areas (including flower beds, gardens, and mowed lawn) than in strictly wooded, field, or wetland habitats (H= 14.91, df= 4, P < 0.01; Fig. 1). This pattern was largely driven by the dominant species, B. impatiens (H = 13.26, df= 4, P = 0.01). No significant differences in habitat use by nest seeking queens of other species were detected, likely due to low sample sizes. However, queens of B. auricomus and B. feruidus were only found searching for nest sites in open areas (meadows, roadsides, and maintained flower beds/ lawns). The parasitic species, Bombus citrinus, on the other hand was only observed seeking host nests in wooded areas. Several of the less common queen species in this dataset (B. vagans, B. perplexus, B. dtrinus, and B. auricomus) were observed nest seeking in natural habitats but not in heavily maintained areas (lawns, gardens, and flower beds) (Table 2).

Queen abundance and species richness in timed surveys increased with the amount of forest in the surrounding 1 km landscape (abundance: Spearman [r.sub.s] = 0.31, n = 108, P < 0.01, Fig. 2; diversity: [r.sub.s] = 0.33, n= 108, P < 0.01). Queen species richness declined with the proportion of annual row crop agriculture ([r.sub.s] = -0.22, n = 108, P = 0.02). The number of nest seekers was significantly lower in landscapes with greater proportions of urban developed areas ([r.sub.s] = -0.26, n= 108, P = 0.02). Queen abundance, species richness, and activity (foraging versus nest seeking) were not influenced by the amount of herbaceous and pasture lands, shrubland, open water, or wetlands in a 1 km landscape.

A principal components analysis of predictor variables (standardized landscape components, GDD, and flowering species richness) generated three main components. After varimax rotation Principal Component One loaded heavily on herbaceous/hay habitat (loading = 0.52) and negatively on developed land (-0.74). Principal Component Two loaded heavily on forest cover (0.71) and negatively on crops (-0.67). Principal Component Three reflected GDD (0.74) and flowering species richness (0.58). Total queen abundance per timed survey increased significantly with Principal Components One (- developed, + herb/hay) and Two (+ forest, - crop), and decreased with Principal Component Three (+GDD, +flowering species richness) in a generalized linear model with negative binomial family error (Table 3). Nest seeking and foraging queen abundance increased significantly with Principal Component One (- developed, + herb/hay). Meanwhile, queen species richness was positively related to Principal Components One (- developed, + herb/hay) and Two (+ forest, - crop). This analysis supports the importance of forest for overall queen abundance and diversity, and the negative effect of crop and developed land.

Individual nest seeking queens typically investigated several different microhabitats during our observations. They were most often found searching for nest sites near holes or crevices in leaf litter (70.8 % of queens were observed near this feature), beneath woody debris or at the base of a tree (46.7 %), in herbaceous plant debris (31.9 %), or near grass clumps (7.9 %). Some were also found investigating holes in mounds of bare soil, mulch piles, or in flower beds mulched with wood chips. The majority (64.4 %) of nest seeking queens were investigating potential nest sites with no flowers nearby. The associations between microhabitat features and nest seeking queens was similar among the three most abundant species in this survey - B. impatiens, B. griseocollis, and B. bimaculatus (Fig. 3).


In 2018 the earliest nest seeking queen was observed on 11 April (GDD = 69), and the latest was observed on 29 June (GDD = 1179). Queen activity peaked between GDD 221-466 (Fig. 4), a period corresponding to mid-May in Ohio. By growing degree day, the earliest bumble bee species to be active in Ohio in spring 2018 was B. impatiens, followed closely by B. bimaculatus, B. griseocollis, B. fervidus, and B. vagans (Table 1). However, because many more queens of B. impatiens were observed compared to other species, its status as the earliest emerging species may be overstated. In mid-May B. perplexus, B. auricomus, and B. sandersoni queens were observed. The last to emerge was the social nest parasite B. citrinus (24 May, about 1 mo after its primary host taxa--B. impatiens, B. bimaculatus, and B. vagans). Bombus pensylvanicus queens were not observed, although workers were found on the 8th of June.

Queen abundance in timed surveys showed a strong relationship with growing degree day (Fig. 4). The proportion of queens per timed survey that were observed nest seeking decreased with GDD (Spearman correlation [r.sub.s] = -0.24, n = 108, P = 0.01), whereas the proportion of queens carrying pollen loads increased ([r.sub.s] = 0.35, n= 108, P < 0.01). There was no significant difference in the number of nest searching or foraging queens based on time of day when the survey was conducted (nest seekers: Kruskal-Wallis H= 5.95, df = 4, P = 0.20; foragers: H= 5.57, df= 4, P = 0.23).

The first workers were observed on 24 May 2018. By the first week ofjune, 255 workers of seven species had been observed during timed surveys (Table 1), from earliest to latest: B. impatiens (24 May), B. griseocollis (24 May), B. bimaculatus (24 May), B. vagans (29 May), B. feividus (7 June), B. perplexus (7 June), and B. pensylvanicus (8 June).

By comparing earliest emergence dates in this and 11 other surveys (Table 4), a continuum of bumble bee species queen phenologies has emerged (Table 5). In northeastern North America, the earliest species to emerge, in late March or early April, are B. bimaculatus, B. affinis, B. terricola, B. impatiens, and B. temarius. They are followed in mid or late April by B. griseocollis, B. fenndus, B. auricomus, B. vagans, and B. perplexus (Table 5). The latest to emerge, beginning in May, are B. pensylvanicus and B. sandersoni and the more northerly-distributed B. rufocinctus and B. borealis. The social parasites, Bombus ashtoni (mid-April-mid-May) and B. citrinus (mid-May-June), appear about 1 mo after their hosts.

In a comparison of these 12 datasets (Table 4), there was a 1 to 3 wk range in the earliest observation date by species, depending more on the latitude of the study location than on the year. Several widespread and well-studied bumble bee species emerged significantly earlier at lower latitudes than higher ones (B. bimaculatus [r.sub.s] = 0.75, n = 9, P = 0.01; B. impatiens [r.sub.s] = 0.63, n = 11, P = 0.04; B. perplexus [r.sub.s] = 0.65, n = 9, P = 0.06; Fig. 5). However, several of the less common species, that occur regularly in Ohio and elsewhere in northeastern North America, showed no relationship between spring queen emergence date and latitude (B. auricomus, B. fervidus, and B. vagans:, Fig. 5). Although sample size was low (n = 12 datasets), there was no detectable general trend of earlier emergence by species over time between 1920 and 2018 (Fig. A1).


There was no significant effect of flowering plant species richness per site on foraging queen abundance ([r.sub.s] = 0.08, n = 108, P = 0.38) or species richness ([r.sub.s] = 0.18, n = 108, P = 0.06).

In timed surveys queen pollen and nectar sources included 47 different flowering plant species. The plant species that received at least five queen visits (out of 476 foraging queens identified to species in timed surveys) are listed in Table 6. The flowering species that were highly visited by queens were primarily woody plants that occurred along field-forest margins (* denotes species considered invasive in the study region): Malus spp., Lonicera spp.*, Ligustrum vulgare*, Elaeagnus umbeUata*, Aesculus glabra, Robinia spp, and Rubus spp. Temporarily-profitable habitats like patches of lupine (Lupinus perennis) in sand barrens, Rhododendron spp. in maintained areas, or purple deadnettle (Lamium purpureum) in untreated agricultural fields were also high yielding. Key native spring wildflowers used by queens included Mertensia virginica and Hydrophyllum spp. Nonnative weedy flowers that attracted large numbers of queens were: Taraxacum officinale, Trifolium pratense, Glechoma hederacea, Trifolium pratense, Securigera varia*, and Vinca minor. Queens seemed to prefer abundantly flowering plants in the families Rosaceae, Fabaceae, and Lamiaceae, regardless of whether native or introduced.


Researchers have advanced the study of bumble bee nesting biology using some innovative survey techniques to locate their cryptic nests, including trained dogs, intensive field surveys, and citizen science volunteers (Fussell and Corbet, 1992; Osborne et al, 2008; Lye et al, 2012; Waters et al, 2011; O'Connor et al, 2012). In our study observers took advantage of easily recognizable behavior in bumble bee queens--nest seeking--to survey queen abundance and distribution among habitats. Timed surveys also included foraging queens, which precede the workers and males by several weeks in the spring and are readily distinguished by their large size. These surveys provided an opportunity to study queen nesting and foraging behavior and habitat use during a vulnerable and poorly understood stage in the colony life cycle. Through more than 100 h of searching, 1006 nest seeking and foraging queens of nine species were documented, one of which (B. sandersoni) is very rarely observed in Ohio and other nearby states. With the phenological data from this and other field surveys in the North American bumble bee literature, a timeline for spring emergence by species has been established. In the most common species, individual queens preferentially searched for nest sites along the forest-field interface (a partially wooded transitional habitat), and landscapes with more wooded cover were more likely to harbor high numbers of nest seekers. Spring queens relied on a mixture of flowering woody and herbaceous plants, both native and nonnative, that occurred primarily along the edges of forests but also in other seasonally flower-rich habitats like lupine sand barrens and untreated agricultural fields.


Several criteria by which bumble bee queens select nest sites have been proposed--that the site should require little preparation by the queen, be situated in well-drained soil, and be sheltered from the elements (Frison, 1923; Alford, 1969). The greater abundance of nest seeking queens found in transitional zones between wooded and open habitats in our study, along with the large numbers of queens investigating areas with dense leaf litter, fallen logs and other features of woody habitats, supports these criteria. Queens' preference for these partially wooded habitats scaled up from the microhabitat- to the landscape level, as evidenced by increased queen abundance and species diversity in landscapes with higher proportions of forest.

In this study nest seeking B. impatiens queens demonstrated a strong association with wooded habitats, or boundaries between wooded and field habitats. Less abundant species, B. bimaculatus, B. griseocollis, and B. citrinus, appeared to share this habitat preference, although small sample sizes made it difficult to test rigorously. Frison (1923) noted similar habitat associations for B. impatiens and B. bimaculatus, saying that when attempting to lure them to use artificial nest boxes it was "folly to 'plant' the domiciles in the open fields or pastures." Nevertheless, individuals of the most abundant species in this survey opportunistically searched for nest sites in other habitats as well, such as mulched flower beds, fields, and rodent holes in mowed lawns, suggesting an adaptability to features of human-dominated habitats. Observations of the few B. auricomus and B. fervidus nest seeking in open grasslands and fields in this study corroborate other published accounts (Frison, 1923; Macfarlane, 1974).

This pattern, in which the majority of bumble bee species seek nest sites in at least partially wooded habitats, with fewer species nesting primarily in grasslands, seems to be consistent across the temperate Holarctic region (North America and Europe). Several European studies have also documented bumble bee queens' preference for the forest-field interface or wooded habitats (Svensson and Lundberg, 1977; Svensson et al, 2000; Lye et al., 2009). Rather than comparing habitats based on vegetation alone, Osborne et al. (2008) suggested more nests occur in linear (fence lines, hedgerows) versus nonlinear habitats (large patches of either woodland or grassland). Boundary zones and wooded habitats typically have more complex microtopography and vegetation structure than do large tracts of grasslands, as well as higher abundance and wider variety of potential nest sites (tree and shrub bases, stumps, brush piles, holes beneath fallen logs, partially eroded stream banks with exposed roots, and dense leaf litter). Woods also harbor small rodents, whose abandoned burrows are prime nesting places for bumble bees (Frison, 1917; Plath, 1934). Grasslands, on the other hand, have the advantage of higher light exposure to warm the nest and potentially a closer proximity to summer forage, which can be limited in forests.

Bumble bee queens likely rely on multiple sensory inputs to locate potential nest sites. In this study potential visual cues were assessed within 2 m of each nest seeking queen. The most common species, B. impatiens, B. bimaculatus, and B. griseocollis, were most often found investigating apparent holes in leaf litter or bare soil in herbaceous plant debris, beneath fallen logs, and at the bases of trees. However, there were not sufficient numbers of queens observed for most species to determine species-specific preferences. In addition to visual cues, queens may also detect olfactory or chemical cues that help them to locate one of their preferred nest sites--abandoned rodent burrows. Frison (1917, 1923), guided by Sladen (1912), reported high colonization of artificial domiciles that he had baited with grasses from field mouse nests. Future research on bumble bee queen nest site selection is needed to quantify the relative importance of visual and olfactory cues on nest seeking behavior.

In northeastern North America, bumble bee queens appear to select nest sites without regard to cues indicating where food will be most available later in the season, as approximately 60% of nest seeking queens in our study were observed searching in places with few or no flowers. Research elsewhere also suggests a queen's choice of nesting habitat is independent of her choice of foraging habitat (Suzuki et al, 2009; O'Connor et al, 2017). Nevertheless, there is likely value for queens that choose nest sites that are in sheltered locations but also within flight range of multiple habitat types to ensure the availability of summer forage. Landscapes in the eastern U.S. are often mosaics of forest patches interspersed with open field habitats. Based on our findings, to maximize conservation potential for bumble bees land managers should seek to maintain patches of high-quality wildflower foraging habitat in close proximity to at least partially wooded sheltered nesting habitat.


Based on this study and 11 other datasets of earliest queen observation dale, the order of bumble bee species' seasonal appearance in northeastern North America has been fairly consistent (Howard, 1920, in Fye, 1953; Frison, 1923; Plath, 1934; Fye, 1953; Medler, 1962; Medler and Carney, 1963; Macior, 1968; Macfarlane, 1974; Prusnek, 1999; iNaturalist 2018; Table 4). Notably, several of the rare or endangered species in Ohio have emergence times on the tail ends of the emergence season for queens, either tending to appear earlier (B. affinis, B. terricola) or later (B. pensylvanicus) than the majority of species. To the best of our knowledge, no other North American surveys have reported spring queen emergence dates for the rare B. sandersoni, which we collected on 14 May in Lake County, OH.

First observation dates for queens in this study were somewhat earlier for many species (B. bimaculatus, B. citrinus, B. fervidus, B. griseocollis, and B. impatiens) than those of older published studies from eastern North America (Plath, 1934; Medler, 1962; Medler and Carney, 1963; Macior, 1968; Macfarlane, 1974). Early emergence is a predicted consequence of climate change, which has caused warmer spring temperatures in Ohio and the U.S.A. (Calinger et al., 2013). However, there was no relationship between study year and emergence date for most species. Earlier emergence dates were more likely an artefact of the lower latitudes where we surveyed, although long-term change in bumble bee phenology due to climate change cannot be ruled out. The fact our earliest observation dates did not differ dramatically from those in more northern locations, such as Wisconsin and Ontario, may suggest local adaptation to climate. Alternatively, shifts to more northerly distributions of some species over time may be masking local earlier emergence dates. Notably, the citizen science platform iNaturalist (which relies on crowd-sourced identification of uploaded photos by local and national bee experts) had the earliest verified spring observations of several common species in recent years (e.g. B. bimaculatus and B. griseocollis queens posted in late March). In the future studies that include verified citizen science observations may be better able to detect broad temporal and geographic changes in spring bee phenology than those that rely on the traditional museum specimens and published observations alone.

Queen nest seeking activity peaked in May for our study. However, queens of the most common species, B. impatiens, were observed searching for nest sites into late June in Ohio. Likewise, Frison (1923) observed queens of B. fervidus, B. griseocottis, B. pensylvanicus, B. perplexas, and B. vagans nest seeking in mid-late June in nearby Illinois. Plath (1934) observed B. impatiens and B. fervidus queens nest seeking as late as July in the more northern state of Massachusetts. There are several possible explanations for the long-tailed temporal distribution in nesting activity. First, the extended nesting phenology of B. impatiens may simply reflect its greater abundance, so even slender tails of the distribution are more readily observed. Second, widespread and abundant species like B. impatiens may have high natural variation in spring queen emergence time. While late-emerging bumble bees are at a disadvantage in competing for limited high-quality nest sites, they also lessen their risk of starving or freezing to death in bouts of inclement spring weather. Third, delayed nest founding may be a means of avoiding nest invasion by social parasites in the subgenus Psithyrus (like B. citrinus), if they establish their nests after their parasite's typical period of host seeking. Fourth, queens exhibiting later season nest seeking behavior may have been infected with the widespread nematode parasite Sphaetvlaria bombi Dufour, which prevents ovar)' development (Medler, 1962; Rutrecht and Brown, 2008) and causes queens to continuously seek, but never establish, a nest (Lundberg and Svensson, 1975). Other studies in northeastern North America have reported high queen infection rates by S. bombi (up to 38%) that differ among Bambus species (Fye, 1953; Medler, 1962; McCorquodale et al, 1998). Lastly, highly successful species like B. impatiens or early-emerging species like B. bimaculatus may, under ideal conditions, have two generations per summer (Frison, 1923). Facultative bivoltinism is known in solitary bees (e.g. Megachile rotundata; Krunic, 1972), but nest initiation by nondiapausing mated queens has only been conclusively documented in captive bumble bee colonies in temperate regions (Roseler, 1985; Beekman et al, 1999; but see. also Potapov et al, 2018, for anecdotal evidence of bivoltinism in bumble bees). In our study it is unlikely nest seeking queens of B. impatiens in late June were nondiapausing mated queens because males of that species were not observed until 5 July (although males of B. bimaculatus, B. griseocollis, and B. citrinus were sighted on 13 June).


The boundary between wooded and open habitats offered the most plentiful forage for spring bumble bee queens, because of the prevalence of early-flowering invasive shrubs (Lonicera, Ligustrum vulgare, and Elaeagnus umbellata) and other woody plants (especially those in the Rosaceae: Crataegus, Malus, Prunus, Rosa, and Rubus). Rich woods offered large patches of spring ephemeral wildflowers including Meitensia virginica and Hydrophylhim. Gardens and other planted areas had concentrated pockets of highly-rewarding resources like Rhododendron and Vaccinium. In agricultural fields and roadsides, Taraxacum officinale, Lamium purpureum, Trifolium pratense, and View spp. attracted large numbers of queens. Lastly, pockets of lupine (Lupinus) in oak savanna and sand barrens, which are a rare habitat type in Ohio, were especially high-yielding for queen bumble bees and attracted large numbers of B. griseocollis in particular. In surveys of flower use by spring bumble bee queens in the northern state of Wisconsin, Fye (1953) and Macior (1968) found many of the same plants to be staples of queen diets, including Malus, Prunus, Rubus, Rosa, Lonicera, Taraxacum, TrifoUum, and Vicia.

Bumble bees, including queens, are generalist foragers that use a wide variety of plants, native and nonnative, of many families and floral morphologies. Therefore, the abundance and proximity of flowers to potential nesting habitat is likely more important than the particular species. From a management perspective, ensuring few gaps exist in seasonal flower availability is crucial. A continuous supply of floral resources is required to support the nest-founding stage of the bumble bee life cycle because each queen must forage for food as well as tend the nest, potentially limiting her mobility.


This study provides much-needed contemporary baseline data on the natural history and nesting behavior of North American bumble bee queens during this critical spring nest founding stage. However, much more work is needed to evaluate other aspects of their nesting biology, such as the prevalence of parasite infection in late season nest seeking queens, the relative importance of visual and olfactory cues in nest site selection, or the possibility of bivoltinism in temperate species. Long-term monitoring of spring Bombus queens that includes both traditional and citizen science approaches may reveal broad-scale responses to changes in climate or land use, or provide additional data on less common species to help refine interspecific differences in nest site preference.

Acknowledgments.--This study was funded by lhe Ohio Department of Transportation, as part of a larger effort to inventory bumble bee diversity and distribution in Ohio. Field assistants Megan Varvaro, Andrew Lybbert, Audrey Bezilla, Jules Christensen, Kevin Conroy, Elizabeth DiCesare, Marko Jesenko, Kelly Peterson, and Jesse Smith contributed essential data. We also thank the volunteers who submitted data on nest seeking bumble bee queens and Denise Ellsworth of the Ohio State University Extension program who helped us to recruit volunteers. The cooperation of many state, county, and municipal park districts in Ohio (especially the Cleveland Metro Parks, the Columbus and Franklin County Metro Parks, MetroPark Toledo, and Erie, Geauga, Lake, Medina, and Summit County Park Districts) was key to the success of the project. Data on the most recent sightings of rare bumble bee species in Ohio were contributed bv Leif Richardson, Paul Williams, and curators at the Ohio State University C.A. Triplehorn Insect Collection and the Cleveland Museum of Natural History. Mau Perlik (ODOT), Keng-Lou james Hung, Andrew Lybbert, and John Bailas of the Goodell lab provided helpful feedback on earlier drafts of this manuscript.


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TABLE A1.--Bumble bee species known to occur in Ohio.
Species are listed alphabetically. The most recent observation
of each species (not including the present survey) and the
source of that record is given. Note that some species lists
for Ohio include Bombus ternarius, but there are no verifiable
specimens or sightings of that species from the state

                                 Recorded in the     Most recent
Species                          present survey?   record from Ohio

B. affinis Cresson 1863                no                2013
B. ashtoni Cresson 1864                no                1998
B. auricomus Robertson 1903            yes               2018
B. bimaculatus Cresson 1863            yes               2018
B. borealis Kirby 1837                 no                2018
B. citrinus Smith 1854                 yes               2018
B. fervidas Fabricais 1798             yes               2018
B. flavidus (incl. fernaldae)          no                1936
  Eversmann 1852
B. fratemus Smith 1854                 no                1967
B. griseocollis De Geer 1773           yes               2018
B. impatiens Cresson 1863              ves               2018
B. insularis Smith 1861                no                1933
B. nevadensis auricomus                no                1988
  Cresson 1874 ([dagger])
B. pensylvanicus De Geer 1773          yes               2018
B. perplexus Cresson 1863              yes               2018
B. rufocinctus Cresson 1863            no                1919
H. sandersoni Franklin 1913            yes               2018
B. temcola Kirby 1837                  no                1981
B. vagans Smith 1854                   yes               2018
B. variabilis Cresson 1872             no                1962

                                 Source of most recent record if not
Species                            observed in the present survey

B. affinis Cresson 1863          Toledo Zoo specimen, coll. Mitch
B. ashtoni Cresson 1864          Prusnek 1999
B. auricomus Robertson 1903      --
B. bimaculatus Cresson 1863      --
B. borealis Kirby 1837           Cleveland Museum of Natural
                                   History specimen, coll. Jessie
B. citrinus Smith 1854           --
B. fervidas Fabricais 1798       --
B. flavidus (incl. fernaldae)    in Williams et al. 2014
  Eversmann 1852
B. fratemus Smith 1854           Ohio State University Triplehorn
                                   Insect Collection, OSUC
B. griseocollis De Geer 1773     --
B. impatiens Cresson 1863        --
B. insularis Smith 1861          Cleveland Museum of Natural
                                   History specimen
B. nevadensis auricomus          Ohio State University Triplehorn
  Cresson 1874 ([dagger])          Insect Collection, OSUC
B. pensylvanicus De Geer 1773    --
B. perplexus Cresson 1863        --
B. rufocinctus Cresson 1863      in Williams et at. 2014
H. sandersoni Franklin 1913      Cleveland Museum of Natural
                                   History specimen, coll. Jessie
B. temcola Kirby 1837            Ohio State University Triplehorn
                                   Insect Collection, OSUC
                                   100532; USDA-ARS Bee
                                   Biology & Systematics Lab,
B. vagans Smith 1854             --
B. variabilis Cresson 1872       Ohio State University Triplehorn
                                   Insect Collection, OSUC

([dagger]) not included in species count due
to likely synonymy with B. auricomus

TABLE A2.--Bumble bee queen field survey sites, spring 2018.
This list includes timed 60 min research surveys only, without
additional citizen science observations of nest seeking queens.
Sites are listed in chronological order of sampling date

Site                   Latitude (N)   Longitude (W)   Date

Walter Best Wildlife   41.55459400    81.20030800     1-May
Frohring Meadows       41.41235556    81.36186944     1-May
Old Field South        41.44574167    81.40938056     l-May
Foxfield               40.68200700    81.63214100     1-May
Big Creek Park         41.60851389    81.20902778     2-May
Skok Meadows           41.65725833    81.19035000     2-May
Highban ks             40.15072300    83.03264000     2-May
Burton Wetlands        41.44282778    81.18068889     5-May
Hiram College Field    41.29954200    81.11062600     5-May
Eagle Creek State      41.28956900    81.05710800     5-May
  Nature Preserve
Hellbender Bluff       40.69371944    80.64580833     6-May
Sheepskin Hollow       40.74944400    80.52551700     6-May
  State Nature
Hinckley Buzzard       41.21546400    81.70842500     8-May
Brecksville Nature     41.31861200    81.61697300     8-May
Hinckley Redwing       41.21982000    81.72292000     8-May
University of Akron    41.18438300    81.65144200     9-May
  Field Station
Mogadore Reservoir     41.06020900    81.32205900     9-May
  Congress Lake Rd
Swine Creek            41.44208889    81.02785278     9-May
Wilson Cemetery        40.12079100    82.42827200     9-May
Wolfrun Regional       40.39845210    82.43246010     9-May
Brown Family           40.37439000    82.40645000     9-May
Thomas Swift           41.23933600    80.91774400     9-May
Grand River            41.38919444    80.91515556     9-May
  Wildlife Area
Furnace Run at         41.25014100    81.62355800     9-May
  Brush Creek Rd
Hogback Ridge          41.74396944    81.03079444     14-May
Observatory Park       41.58586389    81.08312500     14-May
Springfield Bog        41.01042500    81.39771700     15-May
Kokosing State         40.51347300    82.58913500     16-May
  Wildlife Area
Orchard Hills Park     41.56203056    81.36681667     16-May
Killbuck               40.80235000    81.76260500     17-May
Oak Hill Entrance      40.83617800    81.96042400     17-May
Friends of             41.89799100    80.55799100     18-May
  Conneaut Creek
Dorset Wildlife Area   41.69124500    80.64290600     18-May
Penn Line Fen          41.70033300    80.52156800     18-May
Lake Erie Bluffs       41.78842222    81.17471389     21-May
Pleasant Valley        41.58903056    81.40321944     21-May
Rogers Rd Field        41.56947222    81.41544167     21-May
University of Akron    41.18438300    81.65144200     22-May
  Field Station
Shawnee Superior       39.61007000    82.21098000     23-May
Driscoll Farm          41.11538056    82.29348611     23-May
Maumee Bay State       41.67550833    83.37435000     24-May
Toledo Solar Panel     41.62741000    83.57286800     24-May
Pearson Park           41.64305278    83.44251667     24-May
Highban ks             40.15072300    83.03264000     24-May
Scioto Audubon         39.94535278    83.00676389     24-May
Rock Run               39.58486389    82.22050000     24-May
  reclaimed mine
Spencer Hollow         39.52135000    82.17408000     24-May
  reclaimed mine
Sharon Woods           40.11708889    82.96375833     24-May
Innis Woods            40.10154700    82.89956600     24-May
Lou Campbell           41.59167984    83.77754200     24-May
Norma Johnson          40.51199167    81.53874722     24-May
Kitty Todd- South      41.61830382    83.78563300     24-May
Irwin Prairie          41.65643600    83.78191400     24-May
Oak Openings           39.80399300    84.06096400     24-May
Dawes Arboretum        39.98004000    82.40808000     24-May
Meilke Road-           41.63804700    83.76545300     24-May
Kitty Todd--Sweet      41.61163936    83.80451100     24-May
  Fern Savanna
SR-64                  41.52668889    83.87331667     25-May
Brandywine Falls       41.27627500    81.53948889     25-May
Prairie Oaks           39.98928889    83.25982778     25-May
Eber Road Prairie      41.56719167    83.78464167     25-May
Scioto Grove           39.85537200    83.02304600     25-May
Baltelle Darby         39.89121111    83.20126667     25-May
Walnut Woods           39.83528000    82.86269000     25-May
Blossom/Porthouse      41.18399300    81.55225200     25-May
Oak Openings           41.55723600    83.85397600     25-May
North Road             41.22584400    80.75860000     26-May
Cascade MetroPark      41.34590000    84.00239000     27-May
Denison Bio            40.08371000    82.51744000     27-May
Smuckers Cafe          41.00595500    81.97617000     29-May
  Pollinator Plot
Rupp Prairie           40.89422500    82.31842300     29-May
Infirmary Mound        40.02506200    82.51275100     29-May
Tallmadge Meadows      41.13057200    81.43557600     29-May
Johnson Woods          40.88925300    81.74658700     29-May
Huston-Brumbaugh       40.82230000    81.09396900     29-May
  Nature Center
Three Creeks           39.89391700    82.90946400     29-May
Clear Creek            39.59676389    82.55215833     29-May
Quail Hollow           40.97898400    81.31004700     29-May
Scenic Vista Park      40.73636667    80.81840556     29-May
Highlandtown           40.65263000    80.77216000     29-May
  Wildlife Area
Slate Run              39.76173600    82.85087700     29-May
Spangler Wooster       40.81212500    82.02295100     29-May
  Memorial Park
Malek Park             41.94321667    80.59560278     29-May
Hellhollow             41.68829722    81.11610556     29-May
  Wilderness Area
North Kingsville       41.93105300    80.64820300     29-May
  Sand BatTens
Mugrage Park           41.13828100    81.78343600     30-May
Granville GIS Land     40.52173000    82.32428900     30-May
Spring Valley          40.05850000    82.53020000     30-May
Buck Creek             39.97000000    83.72920000     4Jun
Waterman Farm          40.01083611    83.04063611     (i-)un
Blendon Woods          40.06901944    82.87453611     6Jun
Olentangy Park         40.11082000    83.03209500     6-Jun
Mill Creek Preserve    40.98850278    80.70032778     7-ftui
Woodbury WMA           40.25680000    81.96020000     7-Jun
  site 3
Woodbury WMA           40.23370000    81.91560000     7-Jun
  site 4
Mosquito Creek         41.44710833    80.78189167     7-Jun
  Parking Lot #15
Austintown             41.07384400    80.77872700     7-Jun
  Township Park
Fellows Riverside      41.09987900    80.67490700     7-Jun
OARDC Pomerene         40.30880000    81.84020000     7-Jun
Mustill Store          41.09061300    81.51760700     7Jun
Woodbury WMA           40.27090000    82.00860000     7-Jun
  site 2
1-77 Roadside          40.79222200    81.38944400     8-Jun
  Camden Ave
Egypt Valley           40.07053100    81.16986500     8-Jun
Holden Arboretum       41.59955000    81.30634722     8-Jun
Barkcamp Stale         40.03361400    81.01810500     8-Jun
Buffalo Hill           40.38750000    80.88584400     8-Jun
Libert) Park           41.33350600    81.41073200     8-Jun
Spring Hill Park       41.30411700    81.30422200     8-Jun

                             Flowering   Total     Queen
                              species    bombus   species
Site                   GDD   richness    queens   richness

Walter Best Wildlife   139      10         1         1
Frohring Meadows       142      10         4         2
Old Field South        143       7         5         2
Foxfield               162       0         10        1
Big Creek Park         157       2         5         1
Skok Meadows           153      14         6         1
Highban ks             271      12         6         2
Burton Wetlands        214      11         16        2
Hiram College Field    208      19         25        3
Eagle Creek State      208      19         33        4
  Nature Preserve
Hellbender Bluff       238      18         12        2
Sheepskin Hollow       238       7         20        4
  State Nature
Hinckley Buzzard       241      15         11        1
Brecksville Nature     242      20         12        2
Hinckley Redwing       241      16         13        2
University of Akron    258      13         5         1
  Field Station
Mogadore Reservoir     256      16         7         1
  Congress Lake Rd
Swine Creek            260      14         14        2
Wilson Cemetery        302      12         14        4
Wolfrun Regional       279      17         18        2
Brown Family           281      18         18        3
Thomas Swift           258      19         21        2
Grand River            259       8         24        1
  Wildlife Area
Furnace Run at         258      15         28        4
  Brush Creek Rd
Hogback Ridge          276      12         19        2
Observatory Park       293      14         43        4
Springfield Bog        320      15         5         1
Kokosing State         365      24         9         3
  Wildlife Area
Orchard Hills Park     323      12         37        3
Killbuck               384       4         6         1
Oak Hill Entrance      379       4         7         2
Friends of             302       9         14        2
  Conneaut Creek
Dorset Wildlife Area   330       7         19        2
Penn Line Fen          329      16         39        4
Lake Erie Bluffs       358      20         10        2
Pleasant Valley        385      23         17        4
Rogers Rd Field        388      22         19        3
University of Akron    436      20         7         1
  Field Station
Shawnee Superior       632      17         1         1
Driscoll Farm          440       0         8         1
Maumee Bay State       415       2         1         1
Toledo Solar Panel     423       2         2         1
Pearson Park           420       4         3         2
Highban ks             607      19         4         2
Scioto Audubon         618      21         4         1
Rock Run               658      18         6         3
  reclaimed mine
Spencer Hollow         679      19         6         3
  reclaimed mine
Sharon Woods           611      13         8         3
Innis Woods            612      26         8         2
Lou Campbell           429      10         12        4
Norma Johnson          506      16         12        2
Kitty Todd- South      424      11         15        3
Irwin Prairie          449      13         16        2
Oak Openings           621       5         22        2
Dawes Arboretum        617      18         26        4
Meilke Road-           421      12         32        2
Kitty Todd--Sweet      426       9         46        4
  Fern Savanna
SR-64                  460       0         1         1
Brandywine Falls       471      17         1         1
Prairie Oaks           639      16         1         1
Eber Road Prairie      454       0         3         1
Scioto Grove           641      11         3         1
Baltelle Darby         640      16         4         2
Walnut Woods           641      21         5         2
Blossom/Porthouse      473      25         6         1
Oak Openings           456       1         20        3
North Road             497       0         12        2
Cascade MetroPark      522      22         1         1
Denison Bio            688      13         10        2
Smuckers Cafe          588      26         1         1
  Pollinator Plot
Rupp Prairie           604      23         1         1
Infirmary Mound        745      12         1         1
Tallmadge Meadows      587       7         2         1
Johnson Woods          605      14         2         1
Huston-Brumbaugh       617       2         2         1
  Nature Center
Three Creeks           748      18         2         1
Clear Creek            781      18         3         1
Quail Hollow           590       3         5         1
Scenic Vista Park      622       2         5         2
Highlandtown           621       5         6         3
  Wildlife Area
Slate Run              752      12         7         4
Spangler Wooster       618      12         8         1
  Memorial Park
Malek Park             498      35         9         3
Hellhollow             537       8         14        1
  Wilderness Area
North Kingsville       497      21         20        3
  Sand BatTens
Mugrage Park           617      21         9         1
Granville GIS Land     651      21         2         1
Spring Valley          771      17         4         2
Buck Creek             889      17         4         3
Waterman Farm          911      13         1         1
Blendon Woods          909      17         2         '2
Olentangy Park         905      21         6         2
Mill Creek Preserve    757      20         1         0
Woodbury WMA           883      21         1         0
  site 3
Woodbury WMA           894      21         1         i
  site 4
Mosquito Creek         750      17         3         2
  Parking Lot #15
Austintown             759      24         4         3
  Township Park
Fellows Riverside      760      27         4         2
OARDC Pomerene         855      19         6         I
Mustill Store          763       4         12        2
Woodbury WMA           876      24         12        3
  site 2
1-77 Roadside          801       1         2         1
  Camden Ave
Egypt Valley           954       5         9         1
Holden Arboretum       742      43         5         2
Barkcamp Stale         863       7         9         1
Buffalo Hill           836      11         10        2
Libert) Park           785      20         15        3
Spring Hill Park       789      12         15        3

JESSIE LANTERMAN (1) The Ohio State University, Department of Evolution, Ecology, and Organismal Biology, 31S W 12th Ave, Columbus 43210

PAIGE REEHER and RANDALL J. MITCHELL The University of Akron, Department of Biology, 244 Sumner St, Akron, Ohio 44325


KAREN GOODELL The Ohio State University, Department of Evolution, Ecology, and Organismal Biology, 1179 University Drive, Newark 43055

(1) Corresponding author: Telephone: (440)-983-0234; E-mail:

Caption: FIG. 1.--Habitat associations of nest seeking queens. Queen abundance is given as the number of nest seeking queens observed per minute by habitat type in timed surveys (n = 78 sites at which queens were observed nest seeking). The dark line represents the median queens per minute, with boxes as the upper and lower 25% quartiles

Caption: Fig. 2.--Influence of the proportion of forest in the landscape on queen abundance in timed field surveys. The proportion of forest was calculated in a lkm buffer area surrounding each site, for n = 108 queen survey sites. Queen abundance includes all queens observed during timed field surveys. The correlation between proportion of forest and queen abundance is shown as a black line (r= 0.27, t = 2.84, df= 106, P = 0.01)

Caption: Fig. 3.--Microhabitat associations of nest seeking queens. The proportions of queens nest seeking near each microhabitat feature are shown for the three most abundant species: B. impatiens (n = 435 queens), B. griseocollis (n = 26), and B. bimaculatus (11 = 25). Microhabitat features include leaf litter, herb litter (herbaceous plant litter), wood (fallen logs and branches, tree bases), grass clump / tussocks, bare soil mounds, moss (carpeting moss clumps), rock pile, pond (pond/lake), stream (stream/river), flower (flowering herbs, shrubs, or trees). Totals sum to >1 within each panel because each queen typically investigated more than one feature type

Caption: Fig. 4.--Phenology of nest searching and foraging queens during timed field surveys. Phenology is categorized by growing degree day (GDD) into 10 equal-interval bins. The black portion of each bar indicates the proportion of nest seekers and gray bars the proportion of foragers out of the total nest seeking and foraging queens found in all surveys. Growing degree day was calculated for each survey based on location and date

Caption: Fig. 5.--Earliest queen emergence date by latitude for each of 15 Hominis species in northeastern North America (1920-2018). Earliest collection date is given as day of the year. Species are in alphabetical order: (a) Ii. affinis, (b) H. ashtoni, (c) B. auricomus, (d) B. bimaculatus, (e) B. borealis, (f) B. ntrinus, (g) B. fervidus, (h) B. griseocollis, (i) B. impatiens, (j) B. pensylvanicus, (k) B. perplexus, (1) B. rufocinctus, (m) B. ternarius, (n) B. terricola, (o) B. vagans. For species with a significant relationship between earliest observation day and latitude, the Spearman correlation values are given.

Caption: Fig. A1--Temporal variation in earliest queen emergence date by year for each of 15 Bombus species in northeastern North America (1920-2018). Earliest collection date is given as day of the year. Species are in alphabetical order: (a) R. affinis (n = 9), (b) B. ashtoni (n = 7), (c) B. auricomus (n=7), (d) B. bimaculatus (n =11), (e) B. borealis (n =(i), (1) B. citrinus (n = 7), (g) B.fervidus (n = 11), (h) B. griseocollis (il = 11), (i) B. impatiens (n = 11), (j) B. pensylvanicus (n = 10), (k) B. pnplexus (n =9), (I) li. mfocinctus (n = (j), (m) B. ternarius (n = 7), (n) B. terricola (n = 7), (o) B. vagans (n = 11). For species with a significant relationship between earliest observation day and latitude, the Spearman correlation values are given.
TABLE 1.--Summary of bumble bee observations in timed field surveys.
Bombus species are listed in order of most to least abundant.
Queen abundance (Total Queens) includes the total number of nest
seeking, foraging, and fixing queens of each species
(sum of 108 one-hour surveys). The number of nest seeking queens
and foraging queens of each species is also given, as well as the
number of plant species used by foraging queens. GDD stands for
cumulative growing degree day. The earliest queen observation,
the earliest observation of queens with pollen loads, and the
earliest worker observations are given for each species

                   Total     Nest                 spp.
Species            queens   seekers   Foragers   visited

B. impatiens        602       331       260        37
B. griseocollis     193       24        168        23
B. bimaculalus       55       19         36        11
B. vagans            34        3         29        14
B. fervidus          18        3         15         6
B. auricomus         7         2         5          4
B. citrinus          4         4         0          0
B. perplexus         2         9         0          0
B. sandersoni        1         0         1          1
B. pensylvanicus     0         0         0          0

                     Date       GDD      Date earliest
                   earliest   earliest       queen
Species             queen      queen      with pollen

B. impatiens       11-Apr.       69          5 May
B. griseocollis     1-May       148          9 May
B. bimaculalus     13-Apr.       97         18 May
B. vagans           9-May       143          5 May
B. fervidus        13-Apr.       98         18 May
B. auricomus        9-May       301          9 May
B. citrinus         24-May      607           --
B. perplexus        9-May       275           --
B. sandersoni       14-May      276         14 May
B. pensylvanicus      --         --           --

                   GDD earliest     Date       GDD
                      queen       earliest   earliest
Species            with pollen     worker     worker

B. impatiens           208         24 May      426
B. gtiseocollis        279         24 May      429
B. bimaculalus         329         24 May      426
B. vagans              208         29 May      752
B. fervidus            330         7 June      763
B. auricomus           302           --         --
B. citrinus             --           --         --
B. perplexus            --         7 June      760
B. sandersoni          276           --         --
B. pensylvanicus        --         8 June      1046

TABLE 2.--Habitat associations of nest seeking bumble bee
queens during timed field surveys. Included in this table
are the 438 nest seeking queens observed during timed
researcher surveys. Total nest seeking queens are given
separately by species: B. imp (Bombus impatiens), B. gri
(B. griseocollis), B. bill) (B. bimaculatus), B. aur
(B. auricomus), B. cit (B. alrinus), B. fer (B. fervidus),
B. per (B. perplexas). B. vag (B. vagans), and B. sp
(Bombus sp. undetermined)

               Total time       Total nest
Habitat      searched (min)   seeking queens   B.imp   B.gri

Wooded            1810             245          186     13
Field              955              90           56      7
Edge               460              77           60      3
Maintained         125              24           22     --
Wetland             40               2            2     --
Total             3390             438          326     23

Habitat      B.bim   B.cit   B.fer   B.vag   B.per   B.aur   B.sp

Wooded        15       4      --       1       1      --      25
Field         --      --       2      --       1       1      23
Edge           4      --      --       2      --      --       8
Maintained     1      --       1      --      --      --      --
Wetland       --      --      --      --      --      --      --
Total         20       4       3       3       2       1      56

TABLE 3.--Influence of Principal Components on bumble
bee queen abundance and species richness in generalized
linear models. Model estimates are shown for principal
components (PC) 1-3, along with the predictor variables
that loaded heavily on each principle component.
Significant model coefficients are in bold text.
* P < 0.01, ** P < 0.001

Model                                  Total queen
parameter     PC heavily loaded on      abundance

Intercept   -                            2.22 **#
PC 1        - developed, + herbhay       0.23 **#
PC 2        + forest, - crop             0.19 **#
PC 3        + CDD, + flower richness    -0.23 **#

Model       Nest seeking   Foraging   Queen species
parameter      queens       queens      richness

Intercept      1.53 **#     1.93 **#     0.66 **#
PC 1           0.29 **#     0.23 *#      0.09 *#
PC 2           0.00         0.22         0.13 **#
PC 3          -0.12        -0.21         0.02

Note: Significant model coefficients are indicated with #.

TABLE 4.--Bumble bee spring queen emergence dales for present
and historic field surveys. Datasets 1-12 and approximate
GPS location were (1) present study, (2) iNaturalist 2018:
40.30437/-82.69029, (3) Prusnek 1999: 41.2501/-81.6236,
(4) Macfarlane 1974a: 43.5329/-80.2262, (5) Macfarlane 1974b:
43.5329/-80.2262, (6) Mador 1968: 42.6781/-88.2762, (7) Medler
and Carney 1963: 44.437257/-90.13216, (8) Medler 1962:
44.437257/-90.13216, (9) Fve 1953: 44.437257/-90.13216, (10)
Plath 1934: 42.307223,-71.120776, (11) Frison 1923: 40.102,-88.2272,
(12) Howard 1920 (in Fye 1953): 38.9072/-77.0369. Note that in
historic literature B. griseocollis-was also known as B. separatus,
B. pensylvanicus as B. americanorum, and B. citrinus as a variety
of II. laboriosus. From the !Naturalist Ohio liee Atlas citizen
science dalaset only verified observations from March-June
were considered

Dataset               1          2          3
location           OH, USA    OH, USA    OH, USA
year(s)             2018     2012-2018    1998

B. affinis           --         --        8-Apr
B. ashtoni           --         --        1-Apr
B. auricomus        9-May      9-May       --
B. bimaculatus     13-Apr     25-Mar       --
B. borealis          --         --         --
B. centralis         --         --         --
B. citrinus        24-May     29-May       --
B. fervidus        13-Apr      4-May       --
B. griseocollis     1-May     28-Mar       --
B. impatiens       11-Apr      3-Apr       --
B. pensylvanicus     --        3-May       --
B. pnplexus         9-May     15-Apr       --
B. rufocinctus       --         --         --
B. sandersoni      14-May     14-May       --
B. temarius          --         --         --
B. terricola         --         --         --
B. vagans           1-May     26-Apr       --
B. variabilis        --         --         --

Dataset               4          5          6
location           ONT, CAN   ONT, CAN   WI, USA
year(s)              1973       1972      1965

B. affinis          20-Apr     6-May     27-Apr
B. ashtoni          10-May     13-May    14-May
B. auricomus          --         --      1 1-May
B. bimaculatus      18-Apr     4-May      6-May
B. borealis         2-Jun      2-Jun       --
B. centralis          --         --        --
B. citrinus         29-May     5-Jun       --
B. fervidus         21-May     6-May     12-May
B. griseocollis     22-May     20-May    12-May
B. impatiens        21-Apr     10-May     6-May
B. pensylvanicus    31-May     11-May    14-May
B. pnplexus         21-Apr     11-May      --
B. rufocinctus      2-Jun      2-Jun     14-May
B. sandersoni         --         --        --
B. temarius         23-Apr     23-Apr      --
B. terricola        15-Apr     30-Apr      --
B. vagans           21-Apr     6-May     14-May
B. variabilis         --         --        --

Dataset               7          8           9
location           WI, USA    WI, USA     WI, USA
year(s)              n/a     1955-1961   1910-1953

B. affinis         21-Apr     30-Apr      26-Apr
B. ashtoni         30-Apr       --         5-May
B. auricomus       30-Apr      4-May      30-Apr
B. bimaculatus     21-Apr     21-Apr      25-Apr
B. borealis        25-May     27-May      25-May
B. centralis         --         --          --
B. citrinus         6-Jun       --          --
B. fervidus        22-Apr      4-May      26-Apr
B. griseocollis    12-Apr      4-May      12-Apr
B. impatiens       18-Apr     22-Apr      18-Apr
B. pensylvanicus   14-May     19-May       2-May
B. pnplexus        20-Apr     27-May      28-May
B. rufocinctus     28-May     28-May      10-Jun
B. sandersoni        --         --          --
B. temarius        24-Apr     11-May      24-Apr
B. terricola       22-Apr     22-Apr      22-Apr
B. vagans           4-May      4-May       9-May
B. variabilis        --         --          --

Dataset              10         11          12
location           MA, USA    IL, USA    D.C., USA
year(s)              n/a     1915-1920      n/a

B. affinis          7-Apr       --        30-Apr
B. ashtoni          6-May       --          --
B. auricomus         --       13-Apr       6-Apr
B. bimaculatus      7-Apr     21-Mar      31-Mar
B. borealis        29-May       --          --
B. centralis         --        6-Jun        --
B. citrinus        28-May      6-Jul      17-May
B. fervidus         6-May     29-May      28-Apr
B. griseocollis    13-May     20-Apr       7-May
B. impatiens       15-Apr     13-Apr      16-Apr
B. pensylvanicus   27-May     23-Apr      22-Apr
B. pnplexus        12-Apr     19-Apr        --
B. rufocinctus       --         --          --
B. sandersoni        --         --          --
B. temarius         5-Apr      8-May        --
B. terricola        6-Apr     13-May        --
B. vagans          19-Apr      1-May      28-Apr
B. variabilis        --       22-Apr        --

TABLE 5.--Spring queen emergence period of bumble bee species
for historical and current field surveys in northeastern
North America. Cell values indicate the number of studies
that recorded that species' earliest observation during a
given time period. Cells are also color-coded on a gray scale
(from 1-light to 6-dark) by the number of studies that list
earliest emergence in that time period. Studies are listed in
reverse chronological order: (1) our study, (2) Ohio Bee Atlas
2012-2018, (3) Prusnek 1999; (4) Macfarlane 1974 (1973 dataset),
(5) Macfarlane 1974 (1972 dataset), (6) Macior 1968,
(7) Medler & Carney 1963, (8) Medler 1962, (9) Fye 1953, (10)
Plath 1934, (11) Frison 1923, and (12) Howard 1920 (in Fye 1953).
See Literature Cited for full citations

Species             21-31   1-10    11-20   21-30
                    March   April   April   April

B. bimaculatus        2       1       2       3
B. terricola                  1       1       4
B. affinis                    2               6
B. impatiens                  1       6       2
B. ternarius                  1
B. fervidus                           1       3
B. ashtoni                            1       1
B. auricomus                  1       1       2
B. griseocollis       1               3
B. vagans                             1       3
B. perplexus                          4       1
B. variabilis                                 1
B. pensvlvanicus                              2
B. sandersoni
B. rufocinctus
B. borealis
B. citrinas
B. centralis

Species             1-10   11-20   21-31   1-10   1-10
                    May     May     May    June   July

B. bimaculatus       2
B. terricola                 1
B. affinis           1
B. impatiens         2
B. ternarius         1       1
B. fervidus          4       1       2
B. ashtoni           3       2
B. auricomus         3       1
B. griseocollis      3       3       1
B. vagans            6       1
B. perplexus         1       1       2
B. variabilis
B. pensvlvanicus     2               2
B. sandersoni                1
B. rufocinctus               1       2      3
B. borealis                          4      2
B. citrinas                  1       4      2      1
B. centralis                                1

Species             Studies

B. bimaculatus      1, 2, 4, 5, 6, 7, 8, 9, 10, 11, 12
B. terricola        4, 5, 7, 8, 9, 10, 11
B. affinis          3, 4, 5, 6, 7, 8, 9, 10, 12
B. impatiens        1, 2, 4, 5, 6, 7, 8, 9, 10, 11, 12
B. ternarius        4, 5, 7, 8, 9, 10, 11
B. fervidus         1, 2, 4, 5, 6, 7, 8, 9, 10, 11, 12
B. ashtoni          3, 4, 5, 6, 7, 9, 10
B. auricomus        1, 2, 6, 7, 8, 9, 11, 12
B. griseocollis     1, 2, 4, 5, 6, 7, 8, 9, 10, 11, 12
B. vagans           1, 2, 4, 5, 6, 7, 8, 9, 10, 11, 12
B. perplexus        1, 2, 4, 5, 7, 8, 9, 10, 11
B. variabilis       11
B. pensvlvanicus    2, 4, 5, 6, 7, 8, 9, 10, 11, 12
B. sandersoni       1
B. rufocinctus      4, 5, 6, 7, 8, 9
B. borealis         4, 5, 7, 8, 9, 10
B. citrinas         1, 2, 4, 5, 7, 10, 11, 12
B. centralis        11

TABLE 6.--Host-plant associations of foraging bumble bee queens
in timed field surveys. Plant species were excluded thai received
<5 visits. Bombus species are abbreviated: B.aur (B. auricomus),
B.bim (B.bimaculatus), B.cit (B. citrinus), B.fer (B. fervidus),
B.gri (B. griseocollis), B.imp (B. impatiens), B.per (B. perplexus),
B.san (B. sandersoni), B.vag (B. vagans). Queens not identified to
species were not included. Species origin is given as N (native) or
I (introduced). Growth habit is denoted by 11 (herbaceous) or
W (woody)

Species                                        Family         Origin

Lupinus perennis L.                        Fabaceae             N
Malus sp. Mill.                            Rosaceae            n/a
Taraxacum officinale F.H. Wigg             Asteraceae           I
Lonicera spp. L.                           Caprifoliaceae       I
Lamium purpureumL.                         Lamiaceae            I
Glechoma hederaceaL.                       Lamiaceae            I
Trifolium pratense L.                      Fabaceae             I
Ligustrum vulgare L.                       Oleaceae             I
Mertensia virginica (L.) Pers. Ex Link     Boraginaceae         N
Elaeagnus umbellata Thunb.                 Elaeagnaceae         I
Vicia spp. L.                              Fabaceae            n/a
Pedicularis canadensis L.                  Scrophulariaceae     N
Hydrophyllum spp. L.                       Hydrophyllaceae      N
Aesculus glabra Willd.                     Hippocastanaceae     N
Robinia spp. L.                            Fabaceae             N
Rhododendron spp. L.                       Ericaceae           n/a

                                           Growth   Total queen
Species                                    habit      visits      B.aur

Lupinus perennis L.                          H          135         1
Malus sp. Mill.                              W          56          0
Taraxacum officinale F.H. Wigg               H          44          0
Lonicera spp. L.                             W          34          0
Lamium purpureumL.                           H          39          0
Glechoma hederaceaL.                         H          27          0
Trifolium pratense L.                        H          26          1
Ligustrum vulgare L.                         W          24          0
Mertensia virginica (L.) Pers. Ex Link       H          18          0
Elaeagnus umbellata Thunb.                   W          14          0
Vicia spp. L.                                H          13          0
Pedicularis canadensis L.                    H          10          0
Hydrophyllum spp. L.                         H           9          0
Aesculus glabra Willd.                       W           8          2
Robinia spp. L.                              W           6          0
Rhododendron spp. L.                         W           5          1

Species                                    B.bim   B.cit   B.fer

Lupinus perennis L.                          4       0       5
Malus sp. Mill.                              0       0       0
Taraxacum officinale F.H. Wigg               1       0       0
Lonicera spp. L.                             0       0       0
Lamium purpureumL.                           8       0       2
Glechoma hederaceaL.                         5       0       0
Trifolium pratense L.                        2       0       4
Ligustrum vulgare L.                         0       0       0
Mertensia virginica (L.) Pers. Ex Link       5       0       0
Elaeagnus umbellata Thunb.                   0       0       0
Vicia spp. L.                                0       0       2
Pedicularis canadensis L.                    5       0       0
Hydrophyllum spp. L.                         3       0       0
Aesculus glabra Willd.                       1       0       0
Robinia spp. L.                              1       0       0
Rhododendron spp. L.                         1       0       0

Species                                    B.gri   B.imp   B.per

Lupinus perennis L.                         109     16       0
Malus sp. Mill.                              3      50       0
Taraxacum officinale F.H. Wigg               0      41       0
Lonicera spp. L.                             4      27       0
Lamium purpureumL.                           3      20       0
Glechoma hederaceaL.                         3      17       0
Trifolium pratense L.                       13       4       0
Ligustrum vulgare L.                         1      20       0
Mertensia virginica (L.) Pers. Ex Link       2       9       0
Elaeagnus umbellata Thunb.                   1      11       0
Vicia spp. L.                                7       3       0
Pedicularis canadensis L.                    0       5       0
Hydrophyllum spp. L.                         1       5       0
Aesculus glabra Willd.                       3       1       0
Robinia spp. L.                              2       3       0
Rhododendron spp. L.                         1       1       0

Species                                    B.san   B.vag

Lupinus perennis L.                          0       0
Malus sp. Mill.                              0       3
Taraxacum officinale F.H. Wigg               1       1
Lonicera spp. L.                             0       3
Lamium purpureumL.                           0       6
Glechoma hederaceaL.                         0       2
Trifolium pratense L.                        0       2
Ligustrum vulgare L.                         0       3
Mertensia virginica (L.) Pers. Ex Link       0       2
Elaeagnus umbellata Thunb.                   0       2
Vicia spp. L.                                0       1
Pedicularis canadensis L.                    0       0
Hydrophyllum spp. L.                         0       0
Aesculus glabra Willd.                       0       1
Robinia spp. L.                              0       0
Rhododendron spp. L.                         0       1
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Author:Lanterman, Jessie; Reeher, Paige; Mitchell, Randall J.; Goodell, Karen
Publication:The American Midland Naturalist
Geographic Code:1U3OH
Date:Oct 1, 2019
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