Bumble Bees (Hymenoptera: Apidae) of Oklahoma: Past and

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Bumble Bees (Hymenoptera: Apidae) of Oklahoma: Past andPresent BiodiversityAuthor(s): Laura L. Figueroa and Elizabeth A. BergeySource: Journal of the Kansas Entomological Society, 88(4):418-429.Published By: Kansas Entomological SocietyDOI: http://dx.doi.org/10.2317/0022-8567-88.4.418URL: http://www.bioone.org/doi/full/10.2317/0022-8567-88.4.418

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Bumble Bees (Hymenoptera: Apidae) of Oklahoma: Past and PresentBiodiversity

LAURA L. FIGUEROA1,2,3,4 AND ELIZABETH A. BERGEY1,2

ABSTRACT: Bumble bees (Bombus Latreille) provide indispensable ecosystem services for naturaland agricultural systems by increasing crop yield and quality. With documented bumble beedeclines throughout the world, the need for baseline data on these important insects becomesapparent. The bumble bees of Oklahoma have previously not been surveyed, hamperingassessment of temporal change. The objectives of this study were to determine the past and presentbumble bee species richness of Oklahoma and indicate possible temporal trends. Records weregathered from museum and university collections, as well as from a field survey of 46 sites in 21counties. Historical records indicated ten bumble bee species in Oklahoma, four of which hadfewer than ten total records. Only five species have been recorded since 2000, four being found inthe targeted survey: B. pensylvanicus (DeGeer), B. griseocollis (DeGeer), B. fraternus (Smith) andB. impatiens (Cresson). The American bumble bee (B. pensylvanicus) has been, and continues tobe, the most common bumble bee species in Oklahoma, despite showing clear patterns of declinein other regions of North America. Our results parallel several recent studies that failed to locateextant populations of the variable cuckoo bee, Bombus variabilis (Cresson), supporting possibleextirpation in portions of its North American range. A targeted survey for this species is warranted,as its host, B. pensylvanicus, remains common in Oklahoma.

KEY WORDS: Bombus, Pollinator decline, Entomological collections, Bee conservation, regional fauna

Pollinators provide essential ecosystem services that benefit nature and human society(Kearns et al., 1998, Goulson et al., 2008). Their services have an estimated global valueof $215 billion USD per year, largely because of fruit and vegetable production (Gallaiet al., 2009). The global dependence on pollinator-reliant crops has steadily increased since1961, and this increase is projected to continue (Aizen et al., 2008). Commercial and wildbumble bees are some of the most important pollinators of crops, enhancing yield, quality(Lye et al., 2011, Chauta-Mellizo et al., 2012, Button and Elle, 2014) and nutritional value(Brittain et al., 2014), while decreasing production costs (Velthuis and van Doorn, 2006).Wild pollinating insects, such as bumble bees, are significantly more effective than honeybees in maximizing yields within pollinator-dependent agricultural systems (Garibaldi etal., 2013, Button and Elle, 2014). Thus, widespread and long-term decline of bumblebees could have devastating consequences for human and natural systems alike, includingloss of plant diversity (Potts et al., 2010) and increased demand for agricultural land (Aizenet al., 2009).

Wide-scale bumble bee declines are occurring around the world (Williams and Osborne,2009), with documented declines in Britain (Ollerton et al., 2014), Canada (Colla andPacker, 2008), Ireland (Fitzpatrick et al., 2007), and the United States (Cameron et al.,2011, Colla et al., 2012, Tripodi and Szalanski, 2015). Factors associated with bumblebee decline include large-scale land-use change, particularly related to agriculture (Goul-son, 2003, Osborne et al., 2008, Grixti et al., 2009, Ollerton et al., 2014), loss of pollenhost-plants (Scheper et al., 2014), high pathogen load and pathogen spillover (Colla

1 Oklahoma Biological Survey, University of Oklahoma, Norman, Oklahoma 73019, USA.2 Department of Biology, University of Oklahoma, Norman, Oklahoma 73019, USA.3 Current address: Entomology Department, Cornell University, Ithaca, New York 14853, USA.4 Corresponding author, e-mail: [email protected]

Received 14 July 2015; Accepted 7 December 2015E 2015 Kansas Entomological Society

JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY88(4), 2015, pp. 418–429

et al., 2006, Otterstatter and Thomson, 2008, Cameron et al., 2011, Meeus et al., 2011,Cordes et al., 2012, Graystock et al., 2013, Murray et al., 2013), plant and pollinator phe-nological changes (Burkle et al., 2013), genetic diversity loss (Lozier and Cameron, 2009,Charman et al., 2010), pesticide exposure (Whitehorn et al., 2012, Gill and Raine, 2014,Laycock et al., 2014), and the numerous interactions among stressors (Goulson et al.,2015). However, not all bumble bee species are declining. Some species appear to havestable populations (Cameron et al., 2011) and others have become problematic non-nativesafter introduction as greenhouse pollinators (Schmid-Hempel et al., 2014).

Assessment of native pollinator populations and the geographic extent of decline is ofgreat conservation and societal importance (Biesmeijer et al., 2006). Bumble bees inmany regions of North America lack assessment (Colla and Packer, 2008, Warriner, 2012).Oklahoma is one such area, cited by Williams et al., (2014) as one of the states with the low-est number of specimens collected per area in the continental United States, likely due to thelack of historical sampling. Oklahoma is tied with Texas as the state with the second mostEPA level III ecoregions (Woods et al., 2005), yet has historically lacked consistent inverte-brate inventorying and monitoring efforts (Murray and McCallister, 1996).

In this study, we compared historic and current records of bumble bees in Oklahoma toindicate changes in species richness through time. We compiled a historic baseline ofspecies records from entomological collections and conducted a bumble bee survey inOklahoma during the summer of 2013.

Materials and Methods

Collection of Historic Data

Historic to recent (1900–2013) data were obtained from entomological collectionsdeposited at museums and universities, using a combination of site visits and access toonline databases. Collections with information databased in the Global Biodiversity Infor-mation Facility (GBIF) were accessed online (127 records from six collections: IllinoisNatural History Survey (INHS), Ohio State University Insect Collection (OSUC), SamNoble Oklahoma Museum of Natural History (SNOMNH), the University of Kansas Bio-diversity Institute (KU), USDA-ARS Bee Biology and Systematics Laboratory (USDA),and the Yale University Peabody Museum (PMNH)). Records were also obtained frommuseum and university collections that did not have their information databased throughcorrespondence with curators and visits (636 records from six collections: K.C. EmersonEntomology Museum (KCE), Oklahoma State University Insect Collection (OSU), South-western Oklahoma State University Insect Collection (SWOSU), University of CentralOklahoma Insect Collection (UCO), University of Oklahoma EntomologyCollection (OU), and the Hymenoptera Collection at the Smithsonian Museum of NaturalHistory (SI)) (see Appendix II for additional information on collections). The total numberof records was 763, many of which had been verified by Jennifer Grixti for the Cameronet al. (2011) study, while the remaining records were verified by the authors.

Bumble Bee Biodiversity Survey

In 2013, sampling of the Oklahoma bumble bee fauna was conducted in 46 sites(Appendix 1; Fig. 1), corresponding to 21 counties and 6 ecoregions (Central Great Plains,Cross Timbers, South Central Plains, Ouachita Mountains, High Plains, and Central Irregu-lar Plains; Woods et al., 2005). The number of sites sampled per county ranged from one tofour. The sites were determined based on the distribution of historical records: the counties

VOLUME 88, ISSUE 4 419

that had greater number of records received a greater number of visits in order to have amore accurate comparison with historical data. Selected sites were located in urban andstate parks, state Wildlife Management Areas (WMAs), and unmown roadsides. The cri-teria for site selection were: availability of floral resources known to be pollinated by bum-ble bees, such as Cirsium spp. (thistles), Solidago spp. (goldenrods), Helianthus spp.(sunflowers), and other members of the Asteraceae family; high density of targeted flowerspecies; and an area between 0.2–0.4 ha.

The methods for the survey follow Grixti et al. (2009) with some modifications. Siteswere sampled once from July to September between the hours of 8:00 A.M. and 4:00P.M. A two-person team spent an average of 1.34 ¡ 0.25 person-hours per site, with sam-pling time based on bumble bee activity (one-person hour if no bumble bees were presentand one-and-a-half person hours if bumble bees were observed). To maintain consistencyin sampling, the senior author was one of the collectors at all sites. Bees were caughtwith aerial nets while on flowers or in flight, and kept in plastic vials inside a coolerwith ice for the duration of the survey to eliminate double counting. After the samplingtime concluded, bees were identified to species and caste, and the number of individualsper species recorded. All males and at least one worker female voucher specimen per spe-cies were collected at each site. Females, except those kept as vouchers, were released on-site to minimize possible effects of the survey. Vouchers of species identifications made inthe field were corroborated with the reference collection at Sam Noble Museum of NaturalHistory, where identifications were previously verified by J. Grixti, and with the Collaet al. (2011) and Koch et al. (2012) identification guides. Vouchers were deposited at theSam Noble Museum of Natural History at the University of Oklahoma.

In addition to our survey, we received data from researchers at Oklahoma State Univer-sity, who surveyed pollinators associated with canola crops on the Marvin Klemme RangeResearch Station (2009–2010) and the Stillwater Agronomy Research Station (2006–2011). These records were part of a targeted multi-year effort that was not specific to bum-ble bee species and was analyzed within the 2000–2013 time period.

Data Analysis

Temporal patterns of species richness were analyzed graphically. A rarefaction analysisusing SigmaPlot was conducted to assess whether our 2013 survey adequately measuredbumble bee species richness within the sampled region.

Fig. 1. Location of the 46 sites surveyed in Oklahoma in 2013. Regions are delineated by average annualrainfall (lower in the west and increasing eastward) and temperature (cooler in the north than in the south).

420 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

In order to compare historic and present bumble bee species richness and relative abun-dance, the 2013 sampling was contingent upon available records, most of which fellwithin two ecoregions (Woods et al., 2005). The state was delineated into six generalregions based on mean annual rainfall and mean annual temperature (Fig. 1). The northwas delineated by a mean annual temperature ranging from 12.7 to 15.5uC, while thesouth was delineated by a mean annual temperature ranging from 15.5 to 17.2uC. Thelongitudinal divisions were based on average annual precipitation: 50 cm or less in thewest, 70–100 cm in the center, and 100 cm and greater in the east. Thus, the six state divi-sions were northwest, northcentral, northeast, southwest, southcentral, and southeast(Fig. 1). For the 2013 survey, longitudinal and latitudinal patterns of species abundancewere analyzed, using a MANOVA to test across species, followed by ANOVA tests tocompare distributions of individual species. To normalize data, specimen counts werelog-transformed. Survey sites were selected based on presence of appropriate floralresources and not by land use, thus sites included a spectrum from urban sites to wildlifemanagement areas. Urbanization was included as a factor, analyzed using a MANOVA,and was determined based on city limit information. Patterns of species’ latitudinal distri-bution over the three time intervals (1900–1949, 1950–1999, 2000–2013) were evaluatedusing Chi-square when sufficient historic records were available. The temporal divisionswere determined based on spread of historical records and temporal ranges made in simi-lar studies (Grixti et al., 2009).

Results

Historical records – all available before the 2013 survey – show 10 bumble beespecies in Oklahoma. In decreasing order of records, these species were: Bombuspensylvanicusx (DeGeer), Bombus fraternus (Smith), Bombus griseocollis (DeGeer),Bombus auricomus (Roberston), Bombus impatiens (Cresson), Bombus variabilis (Cres-son), Bombus bimaculatus (Cresson), Bombus morrisoni (Cresson), Bombus appositus(Cresson), and Bombus insularis (Smith) (Table 1). The earliest set of records, from1900 to 1949, had both the highest number of records and the highest richness(Fig. 2). The three other datasets had a comparable number of records but showed atemporal decrease in richness (Fig. 2).

The 2013 survey yielded four bumble bee species, in decreasing number of records:B. pensylvanicus, B. griseocollis, B. fraternus, and B. impatiens. The only species thatwe failed to locate in the 2013 survey that had been recorded since 2000 was B. auricomus,which was found in the Marvin Klemme Range Research Station (northwest region: 7 of34 bumble bee records in 2009–2010) and the Stillwater Agronomy Research Station(northcentral region: 2 out of 79 specimens collected in six years of sampling from 2006to 2011). The rarefaction trend suggests that there was adequate sampling in our survey(Fig. 3).

We found differences in bee abundance across longitudinal and latitudinal gradients inthe 2013 survey. The southern half of the state had a significantly greater bee abundancethan the northern half (MANOVA F1,44 5 14.854; P 5 0.0004). This pattern held forB. pensylvanicus (ANOVA F1,44 5 8.855; P 5 0.0047) and B. fraternus (F1,44 5 4.786;P5 0.0340), but no pattern was found for B. impatiens and B. griseocollis. The eastern thirdof the state had a significantly greater bee abundance than the western third (F2,29 5 3.421;P 5 0.0463), a pattern that was significant for B. griseocollis (F2,29 5 4.388; P 5 0.0216).There were no statistical differences between bee abundance at urban and rural sites(see Table 2).


The American Bumble Bee, B. pensylvanicus, was the most common species in all timeintervals, and the 2013 survey. From historical data, records available for this speciesincreased in the north relative to the south over the three time intervals (1900–1949,1950–1999, 2000–2013; X2 5 11.52, P , 0.01). This may be product of collection effortand not necessarily indicative of population dynamics.

Based on all available records from 1900 to 2013, some Oklahoma bumble bee specieswere not well represented, and thus, were not necessarily expected in the 2013 survey, withfour species having under ten records (B. bimaculatus 5 9, B. morrisoni5 3, B. appositus5 2, and B. insularis 5 2; see Fig. 2). Although never abundant, B. variabilis was histori-cally the sixth most commonly collected species (n 5 21 records). The most recent

Fig. 2. Temporal pattern of the number of bumble bees collected (bars) and the number of bumble bee speciescollected (line) in Oklahoma. Dashed line was expected number of species based on historical records. Asterisk(*) represents authors’ 2013 survey.

Table 1. Presence, relative abundance and distribution of historic and recent bumble bee records in Oklahoma.Distributions refer to six general regions of the state (see Fig. 1).

Species

Presence (or -) and relative abundance (%) Distribution in Oklahoma

1900–1949 1950–1999 2000–2013 2013* Available records 2013 Survey{

B. auricomus (Roberston) 7.85 3.67 5.53 – 5 (all but SW) –B. bimaculatus (Cresson) 1.71 1.83 – – 3 (NC,SC,SE) –B. fraternus (Smith) 15.02 13.30 6.45 3.33 5 (all but SW) 3 (NC, SC,SE)B. griseocollis (DeGeer) 2.05 1.38 31.34 18.15 5 (all but SW) 2 (NC,SE)B. impatiens (Cresson) 1.02 0.92 14.29 2.59 3 (NC,SC,SE) 3 (NC,SC,SE)B. pensylvanicus (DeGeer) 65.53 75.69 42.40 75.93 6 4 (NC,NW,

SC,SE)B. variabilis (Cresson) 5.12 2.29 – – 4 (NE,NC,

NW,SC)–

B. morrisoni (Cresson) 1.02 – – – 1 (NW) –B. appositus (Cresson) 0.68 – – – 1 (SC) –B. insularis (Smith) – 0.92 – – 1 (NW) –Individuals per interval 293 218 217 270

* Results from the authors’ 2013 survey.{ The SW and NE areas were under-surveyed in the 2013 survey, with 0 and 1 site, respectively.


specimen (and therefore the most recent Oklahoma record to our knowledge) was from1975 in Oklahoma County, in the center of the state.

Discussion

Bumble bee species richness appears to have declined over time in Oklahoma, from tenspecies recorded from 1900–1949 to five species documented from 2000–2013. Naturalhistory collections provide invaluable baseline information for describing biodiversity(Lister et al., 2011) and are the most important, and often the exclusive, source of historicaldata on the range of species, despite possible temporal and spatial biases (Boakes et al.,2010). A targeted survey was used as a means for measuring current bee species diversity,a method known to yield a high number of species (Nielsen et al., 2011). The five speciesinclude four species from the 2013 survey and an additional fifth from records availablesince 2000: B. pensylvanicus, B. griseocollis, B. impatiens, B. fraternus, and B. auricomus.All species were found in urban and rural areas. Bombus variabilis was expected given itsabundance in the historic record had no declines occurred. Bombus pensylvanicus was his-torically, and continues to be, the most common bumble bee in Oklahoma and was presentin both urban and non-urban sites.

The historic range of B. pensylvanicus included a majority of the United States(Cameron et al., 2011). The historic pattern of B. pensylvanicus as the most abundant

Table 2. Counts and percentages of Bombus spp. found in 2013 survey from urban and rural sites.

Bee Species

Count Percentage

Rural Urban Rural Urban

B. fraternus 2 7 0.22 0.78B. griseocollis 44 5 0.90 0.10B. impatiens 2 5 0.29 0.71B. pensylvanicus 115 90 0.56 0.44

Fig. 3. Rarefaction analysis showing the pattern of bumble bee species richness accumulation with increasedsampling effort. The line plateaus at four species: Sobs is number of bumble bee species observed and Scal is thenumber of bumble bee species expected.


species coincides with neighboring Texas (Warriner, 2012) and Arkansas (Chandler andMcCoy Jr, 1965). Recent sampling efforts in the south-central region of the United Stateshave found B. pensylvanicus as a common bumble bee species –the most common speciesin Black Belt Prairie of Mississippi from 1991–2001 (Smith et al., 2012), the second mostcommon species in Kansas canola fields from 2011–2013 (Tripodi et al., 2014), and thethird most common species in Arkansas remnant grasslands from 2002–2008 (Warriner,2011, but see Tripodi and Szalanski, 2015).

The pattern of persistence of B. pensylvanicus in the southern part of its range differsfrom reports in the north, including in Illinois where the species declined from being nearly1/3 of all bumble bees collected from 1900–1949 to only 4.4% of bumble bees sampledfrom 2000–2007 (Grixti et al., 2009) and, even more severely, in southern Ontario wherethe species was not found at all in a 2004–2006 sampling effort, despite being present inhistorical records (Colla and Packer, 2008).

Following IUCN guidelines, Colla et al., (2012) determined B. pensylvanicus as “Vul-nerable” because of considerable reduction in range. The Cameron et al., (2011) nation-wide survey sampled eight target bumble bee species (B. affinis, B., bifarius, B.bimaculatus, B. impatiens, B. occidentalis, B. pensylvanicus, B. terricola, and B. vosne-senskii) at four sites in three counties of Oklahoma from 2008–2009, and found onlyB. pensylvanicus. There appears to be a distinction between northern North America,where B. pensylvanicus has had an estimated 23% reduction in range, and southern regionswhere the species appears to maintain high relative abundance (Cameron et al., 2011).Possible explanations include the large-scale agricultural growth that occurred mid-20th

century in the North (Grixti et al., 2009). Even though B. pensylvanicus remains themost abundant species in Oklahoma, temporal changes in population (including declines)cannot be assessed because density data is unavailable, a situation common for otherbumble bee species (Goulson et al., 2015). Further analysis of latitudinal differences ofB. pensylvanicus is warranted, particularly since it has experienced significant range reduc-tions (Cameron et al., 2011, Colla et al., 2012).

Evidence for decline is particularly strong for Bombus variabilis, a cuckoo bee whosefemales replace B. pensylvanicus queens in their nest (Williams et al., 2014). B. variabiliswas once a moderately common species in Oklahoma (,4% percent relative abundancefrom 1900–1999), but has not been recorded in the state since 1975. This species wasnot located in the 2013 survey or in records available since 2000, consistent with currentliterature regarding B. variabilis in North America (Colla et al., 2012), including Illinois(Grixti et al., 2009) and Arkansas (Warriner, 2011, Tripodi and Szalanski, 2015). Indeed,the status of B. variabilis is uncertain in North America, where the species is, at best, ex‐tremely rare (Colla et al., 2011). Golick and Ellis (2006) recently found B. variabilis in onecounty in Nebraska, but did not find the species in nine additional counties with historicrecords, and the species has recently been reported from two counties in Mississippi (Smithet al., 2012). There is taxonomic ambiguity across its possible range, particularly in Mex-ico and Central America (Williams, 1998). Given that the host of B. variabilis in NorthAmerica is B. pensylvanicus, the most common species observed in each surveyed regionof the state, a targeted search for B. variabilis in Oklahoma is warranted.

Acknowledgements

We would like to thank the property owners, land managers and resident biologists ofthe sites that we sampled, including Wildlife Management Areas, State Parks, National


Forests, and city parks. We would also like to thank Kristen Baum and Shaun McCoshumfrom Oklahoma State University for access to bee records from their canola field study. Wethank Oklahoma City and the State Parks systems for the permits to collect. We would liketo thank the University and Museum collection managers listed in Appendix 2 for access totheir collections. Special thanks to Marisol Amaya, Eric Bright, Mike Mather, and AdamWilkey for field work. We would also like to acknowledge Marisol Amaya, HeatherKetchum, Ola Fincke, and two anonymous reviewers for comments on an earlier versionof the manuscript and Eric Bright for assistance in formatting figures.

Literature Cited

Aizen, M. A., L. A. Garibaldi, S. A. Cunningham, and A. M. Klein. 2008. Long-term global trends in crop yieldand production reveal no current pollination shortage but increasing pollinator dependency. CurrentBiology 18:1572–1575.

Aizen, M. A., L. A. Garibaldi, S. A. Cunningham, and A. M. Klein. 2009. How much does agriculture depend onpollinators? Lessons from long-term trends in crop production. Annals of Botany 103:1579–1588.

Biesmeijer, J. C., S. P. M. Roberts, M. Reemer, R. Ohlemuller, M. Edwards, T. Peeters, A. P. Schaffers, S. G. Potts,R. Kleukers, C. D. Thomas, J. Settele, and W. E. Kunin. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354.

Boakes, E. H., P. J. K. McGowan, R. A. Fuller, D. Chang-qing, N. E. Clark, K. O’Connor, and G. M. Mace. 2010.Distorted views of biodiversity: spatial and temporal bias in species occurrence data. PLoS Biology 8:e1000385.

Brittain, C., C. Kremen, A. Garber, and A. M. Klein. 2014. Pollination and plant resources change the nutritionalquality of almonds for human health. PLoS ONE 9:7.

Burkle, L. A., J. C. Marlin, and T. M. Knight. 2013. Plant-pollinator interactions over 120 years: loss of species,co-occurrence, and function. Science 339:1611–1615.

Button, L., and E. Elle. 2014. Wild bumble bees reduce pollination deficits in a crop mostly visited by managedhoney bees. Agriculture Ecosystems & Environment 197:255–263.

Cameron, S. A., J. D. Lozier, J. P. Strange, J. B. Koch, N. Cordes, L. F. Solter, and T. L. Griswold. 2011. Patternsof widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences,U.S.A. 108:662–667.

Chandler, L., and C. McCoy Jr. 1965. The bumble bees of Arkansas (Hymenoptera, Apidae, Bombinae).Proceedings of the Arkansas Academy of Science 19:46–53.

Charman, T. G., J. Sears, R. E. Green, and A. F. G. Bourke. 2010. Conservation genetics, foraging distance andnest density of the scarce Great Yellow Bumblebee (Bombus distinguendus). Molecular Ecology19:2661–2674.

Chauta-Mellizo, A., S. A. Campbell, M. A. Bonilla, J. S. Thaler, and K. Poveda. 2012. Effects of natural andartificial pollination on fruit and offspring quality. Basic and Applied Ecology 13:524–532.

Colla, S., L. Richardson, and P. H. Williams. 2011. Bumble Bees of the Eastern United States. FS-972; USDAForest Service and the Pollinator Partnership; Washington, D.C. 103 pp.

Colla, S. R., F. Gadallah, L. Richardson, D. Wagner, and L. Gall. 2012. Assessing declines of North Americanbumble bees (Bombus spp.) using museum specimens. Biodiversity and Conservation 21:3585–3595.

Colla, S. R., M. C. Otterstatter, R. J. Gegear, and J. D. Thomson. 2006. Plight of the bumble bee: pathogenspillover from commercial to wild populations. Biological Conservation 129:461–467.

Colla, S. R., and L. Packer. 2008. Evidence for decline in eastern North American bumblebees (Hymenoptera:Apidae), with special focus on Bombus affinis Cresson. Biodiversity and Conservation 17:1379–1391.

Cordes, N., W. F. Huang, J. P. Strange, S. A. Cameron, T. L. Griswold, J. D. Lozier, and L. F. Solter. 2012.Interspecific geographic distribution and variation of the pathogens Nosema bombi and Crithidiaspecies in United States bumble bee populations. Journal of Invertebrate Pathology 109:209–216.

Fitzpatrick, U., T. E. Murray, R. J. Paxton, J. Breen, D. Cotton, V. Santorum, and M. J. F. Brown. 2007. Rarity anddecline in bumblebees - a test of causes and correlates in the Irish fauna. Biological Conservation136:185–194.

Gallai, N., J. M. Salles, J. Settele, and B. E. Vaissiere. 2009. Economic valuation of the vulnerability of worldagriculture confronted with pollinator decline. Ecological Economics 68:810–821.

Garibaldi, L. A., I. Steffan-Dewenter, R. Winfree, M. A. Aizen, R. Bommarco, S. A. Cunningham, C. Kremen, L.G. Carvalheiro, L. D. Harder, O. Afik, I. Bartomeus, F. Benjamin, V. Boreux, D. Cariveau, N. P. Chacoff,


J. H. Dudenhoffer, B. M. Freitas, J. Ghazoul, S. Greenleaf, J. Hipolito, A. Holzschuh, B. Howlett, R.Isaacs, S. K. Javorek, C. M. Kennedy, K. M. Krewenka, S. Krishnan, Y. Mandelik, M. M. Mayfield, I.Motzke, T. Munyuli, B. A. Nault, M. Otieno, J. Petersen, G. Pisanty, S. G. Potts, R. Rader, T. H.Ricketts, M. Rundlof, C. L. Seymour, C. Schuepp, H. Szentgyorgyi, H. Taki, T. Tscharntke, C. H.Vergara, B. F. Viana, T. C. Wanger, C. Westphal, N. Williams, and A. M. Klein. 2013. Wild pollinatorsenhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611.

Gill, R. J., and N. E. Raine. 2014. Chronic impairment of bumblebee natural foraging behaviour induced bysublethal pesticide exposure. Functional Ecology 28:1459–1471.

Golick, D. A., and M. D. Ellis. 2006. An update on the distribution and diversity of Bombus in Nebraska(Hymenoptera: Apidae). Journal of the Kansas Entomological Society 79:341–347.

Goulson, D. 2003. The conservation of bumble bees. Bee World 84:105–106.Goulson, D., G. C. Lye, and B. Darvill. 2008. Decline and conservation of bumble bees. Annual Review of

Entomology 53:191–208.Goulson, D., E. Nicholls, C. Botías, and E. L. Rotheray. 2015. Bee declines driven by combined stress from

parasites, pesticides, and lack of flowers. Science 347:1255957.Graystock, P., K. Yates, S. E. F. Evison, B. Darvill, D. Goulson, and W. O. H. Hughes. 2013. The Trojan hives:

pollinator pathogens, imported and distributed in bumblebee colonies. Journal of Applied Ecology50:1207–1215.

Grixti, J. C., L. T. Wong, S. A. Cameron, and C. Favret. 2009. Decline of bumble bees (Bombus) in the NorthAmerican Midwest. Biological Conservation 142:75–84.

Kearns, C. A., D. W. Inouye, and N. M. Waser. 1998. Endangered mutualisms: the conservation of plant-pollinatorinteractions. Annual Review of Ecology and Systematics 29:83–112.

Koch, J., J. Strange, and P. H. Williams. 2012. Bumble Bees of the Western United States. USDA Forest Serviceand the Pollinator Partnership, Washington, D.C. 143 pp.

Laycock, I., K. C. Cotterell, T. A. O’Shea-Wheller, and J. E. Cresswell. 2014. Effects of the neonicotinoidpesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumblebees. Ecotoxicology and Environmental Safety 100:153–158.

Lister, A. M. 2011. Natural history collections as sources of long-term datasets. Trends in Ecology & Evolution26:153–154.

Lozier, J. D., and S. A. Cameron. 2009. Comparative genetic analyses of historical and contemporary collectionshighlight contrasting demographic histories for the bumble bees Bombus pensylvanicus and B. impatiensin Illinois. Molecular Ecology 18:1875–1886.

Lye, G. C., S. N. Jennings, J. L. Osborne, and D. Goulson. 2011. Impacts of the use of nonnative commercialbumble bees for pollinator supplementation in raspberry. Journal of Economic Entomology 104:107–114.

Meeus, I., M. J. F. Brown, D. C. De Graaf, and G. Smagghe. 2011. Effects of invasive parasites on bumble beedeclines. Conservation Biology 25:662–671.

Murray, N. L., and C. McCallister. 1996. Oklahoma’s Biodiversity Plan: A Shared Vision for Conserving OurNatural Heritage. Oklahoma Department of Wildlife Conservation; Oklahoma City, OK. 129 pp.

Murray, T. E., M. F. Coffey, E. Kehoe, and F. G. Horgan. 2013. Pathogen prevalence in commercially rearedbumble bees and evidence of spillover in conspecific populations. Biological Conservation 159:269–276.

Nielsen, A., I. Steffan-Dewenter, C. Westphal, O. Messinger, S. G. Potts, S. P. M. Roberts, J. Settele, H.Szentgyorgyi, B. E. Vaissiere, M. Vaitis, M. Woyciechowski, I. Bazos, J. C. Biesmeijer, R. Bommarco,W. E. Kunin, T. Tscheulin, E. Lamborn, and T. Petanidou. 2011. Assessing bee species richness in twoMediterranean communities: importance of habitat type and sampling techniques. Ecological Research26:969–983.

Ollerton, J., H. Erenler, M. Edwards, and R. Crockett. 2014. Extinctions of aculeate pollinators in Britain and therole of large-scale agricultural changes. Science 346:1360–1362.

Osborne, J. L., A. P. Martin, C. R. Shortall, A. D. Todd, D. Goulson, M. E. Knight, R. J. Hale, and R. A.Sanderson. 2008. Quantifying and comparing bumblebee nest densities in gardens and countrysidehabitats. Journal of Applied Ecology 45:784–792.

Otterstatter, M. C., and J. D. Thomson. 2008. Does pathogen spillover from commercially reared bumble beesthreaten wild pollinators? PLoS ONE 3:e2771.

Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, and W. E. Kunin. 2010. Global pollinatordeclines: trends, impacts and drivers. Trends in Ecology & Evolution 25:345–353.

Scheper, J., M. Reemer, R. van Kats, W. A. Ozinga, G. T. J. van der Linden, J. H. J. Schaminee, H. Siepel, and D.Kleijn. 2014. Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline inThe Netherlands. Proceedings of the National Academy of Sciences, U.S.A. 111:17552–17557.


Schmid-Hempel, R., M. Eckhardt, D. Goulson, D. Heinzmann, C. Lange, S. Plischuk, L. R. Escudero, R. Salathe,J. J. Scriven, and P. Schmid-Hempel. 2014. The invasion of southern South America by importedbumblebees and associated parasites. Journal of Animal Ecology 83:823–837.

Smith, B. A., R. L. Brown, W. Laberge, and T. Griswold. 2012. A faunistic survey of bees (Hymenoptera:Apoidea) in the Black Belt Prairie of Mississippi. Journal of the Kansas Entomological Society 85:32–47.

Tripodi, A. D., X. Cibils-Stewart, B. P. McCornack, and A. L. Szalanski. 2014. Nosema bombi (Microsporidia:Nosematidae) and Trypanosomatid prevalence in spring bumble bee queens (Hymenoptera: Apidae:Bombus) in Kansas. Journal of the Kansas Entomological Society 87:225–233.

Tripodi, A. D., and A. L. Szalanski. 2015. The bumble bees (Hymenoptera: Apidae: Bombus) of Arkansas, fiftyyears later. Journal of Melittology 50:1–17.

Velthuis, H. H. W., and A. van Doorn. 2006. A century of advances in bumblebee domestication and the economicand environmental aspects of its commercialization for pollination. Apidologie 37:421–451.

Warriner, M. D. 2011. Bumblebees (Hymenoptera: Apidae) of remnant grasslands in Arkansas. Journal of theKansas Entomological Society 84:43–50.

Warriner, M. D. 2012. Bumble bees (Hymenoptera: Apidae) of Texas: historical distributions. SouthwesternNaturalist 57:442–445.

Whitehorn, P. R., S. O’Connor, F. L. Wackers, and D. Goulson. 2012. Neonicotinoid pesticide reduces bumble beecolony growth and queen production. Science 336:351–352.

Williams, P. H., 1998. An annotated checklist of bumble bees with an analysis of patterns of description(Hymenoptera: Apidae, Bombini). Bulletin of the Natural History Museum (Entomology) 67:79–152.

Williams, P. H., and J. L. Osborne. 2009. Bumblebee vulnerability and conservation world-wide. Apidologie40:367–387.

Williams, P. H., R. W. Thorp, L. L. Richardson, and S. R. Colla. 2014. Bumble Bees of North America: AnIdentification Guide. Princeton University Press, Princeton, NJ. 208 pp.

Woods, A., J. Omernik, D. Butler, J. Ford, J. Henley, B. Hoagland, D. Arndt, and B. Moran. 2005. Ecoregions ofOklahoma (color poster with map, descriptive text, summary tables, and photographs). US GeologicalSurvey (map scale 1: 1,250,000), Reston, VA.


Appendix 1. List of the 46 sites sampled in Oklahoma in 2013. Regions refer to one ofthe six general areas of the state (see Fig. 1).


Appendix 2. List of entomological collections used in the present study. Asterix (*)indicates that collection information was obtained the Global Biodiversity Information

Facility (GBIF) database in 2013.


Documents

Bumble Bees (Hymenoptera: Apidae) of Oklahoma: Past and