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 (https://www.oardc.ohio-state.edu/gdd/). 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, http://u.osu.edu/beelab/bumble-bee-survey/). 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.
HABITAT USE BY NEST SEEKING QUEENS AND INFLUENCE OF LANDSCAPE
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).
PHENOLOGY: TIMING OF SEASONAL AND DIURNAL QUEEN ACTIVITY
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).
FLOWER USE BY FORAGING QUEENS
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.
HABITAT USE AND INFLUENCE OF LANDSCAPE
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.
PHENOLOGY: TIMING OF SEASONAL QUEEN ACTIVITY
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).
FLOWER USE. BY FORAGING QUEENS
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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SUBMITTED 5 FEBRUARY 2019
ACCEPTED 21 JUNE 2019
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 Magditch 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 Lanterman 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 100833 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 100757 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 Lanterman B. temcola Kirby 1837 Ohio State University Triplehorn Insect Collection, OSUC 100532; USDA-ARS Bee Biology & Systematics Lab, BOMBUS27762 B. vagans Smith 1854 -- B. variabilis Cresson 1872 Ohio State University Triplehorn Insect Collection, OSUC 124128 ([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 Preserve Frohring Meadows 41.41235556 81.36186944 1-May Old Field South 41.44574167 81.40938056 l-May Chagrin 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 MetroPark Burton Wetlands 41.44282778 81.18068889 5-May Hiram College Field 41.29954200 81.11062600 5-May Station 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 Preserve Hinckley Buzzard 41.21546400 81.70842500 8-May Roost Brecksville Nature 41.31861200 81.61697300 8-May Center Hinckley Redwing 41.21982000 81.72292000 8-May Cabin 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 Park Brown Family 40.37439000 82.40645000 9-May Environmental Center Thomas Swift 41.23933600 80.91774400 9-May MetroPark 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 MetroPark 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 CMNH Lake Erie Bluffs 41.78842222 81.17471389 21-May Metroparks 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 Fibers Driscoll Farm 41.11538056 82.29348611 23-May Maumee Bay State 41.67550833 83.37435000 24-May Park 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 MetroPark Scioto Audubon 39.94535278 83.00676389 24-May MetroPark 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 MetroPark Innis Woods 40.10154700 82.89956600 24-May MetroPark Lou Campbell 41.59167984 83.77754200 24-May Norma Johnson 40.51199167 81.53874722 24-May Center Kitty Todd- South 41.61830382 83.78563300 24-May Piel Irwin Prairie 41.65643600 83.78191400 24-May Oak Openings 39.80399300 84.06096400 24-May Monclova Dawes Arboretum 39.98004000 82.40808000 24-May Meilke Road- 41.63804700 83.76545300 24-May Blowout 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 MetroPark Eber Road Prairie 41.56719167 83.78464167 25-May Scioto Grove 39.85537200 83.02304600 25-May MetroPark Baltelle Darby 39.89121111 83.20126667 25-May MetroPark Walnut Woods 39.83528000 82.86269000 25-May Blossom/Porthouse 41.18399300 81.55225200 25-May Oak Openings 41.55723600 83.85397600 25-May Evergreen North Road 41.22584400 80.75860000 26-May Preserve Cascade MetroPark 41.34590000 84.00239000 27-May Denison Bio 40.08371000 82.51744000 27-May Reserve 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 SNP Huston-Brumbaugh 40.82230000 81.09396900 29-May Nature Center Three Creeks 39.89391700 82.90946400 29-May MetroPark Clear Creek 39.59676389 82.55215833 29-May MetroPark 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 MetroPark 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 Lab 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 MetroPark 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 Gardens OARDC Pomerene 40.30880000 81.84020000 7-Jun Forest 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 Park Buffalo Hill 40.38750000 80.88584400 8-Jun Cemetery Libert) Park 41.33350600 81.41073200 8-Jun Spring Hill Park 41.30411700 81.30422200 8-Jun Aurora Flowering Total Queen species bombus species Site GDD richness queens richness Walter Best Wildlife 139 10 1 1 Preserve Frohring Meadows 142 10 4 2 Old Field South 143 7 5 2 Chagrin Foxfield 162 0 10 1 Big Creek Park 157 2 5 1 Skok Meadows 153 14 6 1 Highban ks 271 12 6 2 MetroPark Burton Wetlands 214 11 16 2 Hiram College Field 208 19 25 3 Station Eagle Creek State 208 19 33 4 Nature Preserve Hellbender Bluff 238 18 12 2 Sheepskin Hollow 238 7 20 4 State Nature Preserve Hinckley Buzzard 241 15 11 1 Roost Brecksville Nature 242 20 12 2 Center Hinckley Redwing 241 16 13 2 Cabin 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 Park Brown Family 281 18 18 3 Environmental Center Thomas Swift 258 19 21 2 MetroPark 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 MetroPark 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 CMNH Lake Erie Bluffs 358 20 10 2 Metroparks 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 Fibers Driscoll Farm 440 0 8 1 Maumee Bay State 415 2 1 1 Park Toledo Solar Panel 423 2 2 1 Pearson Park 420 4 3 2 Highban ks 607 19 4 2 MetroPark Scioto Audubon 618 21 4 1 MetroPark Rock Run 658 18 6 3 reclaimed mine Spencer Hollow 679 19 6 3 reclaimed mine Sharon Woods 611 13 8 3 MetroPark Innis Woods 612 26 8 2 MetroPark Lou Campbell 429 10 12 4 Norma Johnson 506 16 12 2 Center Kitty Todd- South 424 11 15 3 Piel Irwin Prairie 449 13 16 2 Oak Openings 621 5 22 2 Monclova Dawes Arboretum 617 18 26 4 Meilke Road- 421 12 32 2 Blowout 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 MetroPark Eber Road Prairie 454 0 3 1 Scioto Grove 641 11 3 1 MetroPark Baltelle Darby 640 16 4 2 MetroPark Walnut Woods 641 21 5 2 Blossom/Porthouse 473 25 6 1 Oak Openings 456 1 20 3 Evergreen North Road 497 0 12 2 Preserve Cascade MetroPark 522 22 1 1 Denison Bio 688 13 10 2 Reserve 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 SNP Huston-Brumbaugh 617 2 2 1 Nature Center Three Creeks 748 18 2 1 MetroPark Clear Creek 781 18 3 1 MetroPark 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 MetroPark 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 Lab Spring Valley 771 17 4 2 Buck Creek 889 17 4 3 Waterman Farm 911 13 1 1 Blendon Woods 909 17 2 '2 MetroPark 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 Gardens OARDC Pomerene 855 19 6 I Forest 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 Park Buffalo Hill 836 11 10 2 Cemetery Libert) Park 785 20 15 3 Spring Hill Park 789 12 15 3 Aurora
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: JessieLantermanNovotny@gmail.com
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 Plant 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|
|Date:||Oct 1, 2019|
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