Bumble Bees (: ) of Oklahoma: Past and Present Biodiversity Author(s): Laura L. Figueroa and Elizabeth A. Bergey Source: Journal of the Kansas Entomological Society, 88(4):418-429. Published By: Kansas Entomological Society DOI: http://dx.doi.org/10.2317/0022-8567-88.4.418 URL: http://www.bioone.org/doi/full/10.2317/0022-8567-88.4.418

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 88(4), 2015, pp. 418–429 Bumble Bees (Hymenoptera: Apidae) of Oklahoma: Past and Present Biodiversity

1,2,3,4 1,2 LAURA L. FIGUEROA AND ELIZABETH A. BERGEY

ABSTRACT: Bumble bees (Bombus Latreille) provide indispensable ecosystem services for natural and agricultural systems by increasing crop yield and quality. With documented bumble bee declines throughout the world, the need for baseline data on these important becomes apparent. The bumble bees of Oklahoma have previously not been surveyed, hampering assessment of temporal change. The objectives of this study were to determine the past and present bumble bee species richness of Oklahoma and indicate possible temporal trends. Records were gathered from museum and university collections, as well as from a field survey of 46 sites in 21 counties. Historical records indicated ten bumble bee species in Oklahoma, four of which had fewer than ten total records. Only five species have been recorded since 2000, four being found in the targeted survey: B. pensylvanicus (DeGeer), B. griseocollis (DeGeer), B. fraternus (Smith) and B. impatiens (Cresson). The American bumble bee (B. pensylvanicus) has been, and continues to be, the most common bumble bee species in Oklahoma, despite showing clear patterns of decline in other regions of North America. Our results parallel several recent studies that failed to locate extant populations of the variable cuckoo bee, Bombus variabilis (Cresson), supporting possible extirpation 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 value of $215 billion USD per year, largely because of fruit and vegetable production (Gallai et al., 2009). The global dependence on pollinator-reliant crops has steadily increased since 1961, and this increase is projected to continue (Aizen et al., 2008). Commercial and wild bumble 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 honey bees in maximizing yields within pollinator-dependent agricultural systems (Garibaldi et al., 2013, Button and Elle, 2014). Thus, widespread and long-term decline of bumble bees could have devastating consequences for human and natural systems alike, including loss of plant diversity (Potts et al., 2010) and increased demand for agricultural land (Aizen et 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 and Packer, 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 bumble bee 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 pollen host-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 2015 E 2015 Kansas Entomological Society VOLUME 88, ISSUE 4 419 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 have stable populations (Cameron et al., 2011) and others have become problematic non-natives after introduction as greenhouse pollinators (Schmid-Hempel et al., 2014). Assessment of native pollinator populations and the geographic extent of decline is of great conservation and societal importance (Biesmeijer et al., 2006). Bumble bees in many 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 the lack of historical sampling. Oklahoma is tied with Texas as the state with the second most EPA 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 to indicate changes in species richness through time. We compiled a historic baseline of species records from entomological collections and conducted a bumble bee survey in Oklahoma during the summer of 2013.

Materials and Methods Collection of Historic Data Historic to recent (1900–2013) data were obtained from entomological collections deposited at museums and universities, using a combination of site visits and access to online databases. Collections with information databased in the Global Biodiversity Infor- mation Facility (GBIF) were accessed online (127 records from six collections: Illinois Natural History Survey (INHS), Ohio State University Collection (OSUC), Sam Noble 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 from museum and university collections that did not have their information databased through correspondence with curators and visits (636 records from six collections: K.C. Emerson Entomology Museum (KCE), Oklahoma State University Insect Collection (OSU), South- western Oklahoma State University Insect Collection (SWOSU), University of Central Oklahoma Insect Collection (UCO), University of Oklahoma Entomology Collection (OU), and the Hymenoptera Collection at the Smithsonian Museum of Natural History (SI)) (see Appendix II for additional information on collections). The total number of records was 763, many of which had been verified by Jennifer Grixti for the Cameron et 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 to four. The sites were determined based on the distribution of historical records: the counties 420 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Fig. 1. Location of the 46 sites surveyed in Oklahoma in 2013. Regions are delineated by average annual rainfall (lower in the west and increasing eastward) and temperature (cooler in the north than in the south). that had greater number of records received a greater number of visits in order to have a more accurate comparison with historical data. Selected sites were located in urban and state 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), spp. (sunflowers), and other members of the Asteraceae family; high density of targeted flower species; and an area between 0.2–0.4 ha. The methods for the survey follow Grixti et al. (2009) with some modifications. Sites were sampled once from July to September between the hours of 8:00 A.M. and 4:00 P.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 present and one-and-a-half person hours if bumble bees were observed). To maintain consistency in sampling, the senior author was one of the collectors at all sites. Bees were caught with aerial nets while on flowers or in flight, and kept in plastic vials inside a cooler with ice for the duration of the survey to eliminate double counting. After the sampling time concluded, bees were identified to species and caste, and the number of individuals per 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 in the field were corroborated with the reference collection at Sam Noble Museum of Natural History, where identifications were previously verified by J. Grixti, and with the Colla et al. (2011) and Koch et al. (2012) identification guides. Vouchers were deposited at the Sam 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 Range Research 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 analysis using SigmaPlot was conducted to assess whether our 2013 survey adequately measured bumble bee species richness within the sampled region. VOLUME 88, ISSUE 4 421

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 fell within two ecoregions (Woods et al., 2005). The state was delineated into six general regions based on mean annual rainfall and mean annual temperature (Fig. 1). The north was delineated by a mean annual temperature ranging from 12.7 to 15.5uC, while the south was delineated by a mean annual temperature ranging from 15.5 to 17.2uC. The longitudinal divisions were based on average annual precipitation: 50 cm or less in the west, 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 abundance were analyzed, using a MANOVA to test across species, followed by ANOVA tests to compare distributions of individual species. To normalize data, specimen counts were log-transformed. Survey sites were selected based on presence of appropriate floral resources and not by land use, thus sites included a spectrum from urban sites to wildlife management 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 evaluated using Chi-square when sufficient historic records were available. The temporal divisions were 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 bee species in Oklahoma. In decreasing order of records, these species were: Bombus pensylvanicusx (DeGeer), Bombus fraternus (Smith), Bombus griseocollis (DeGeer), Bombus auricomus (Roberston), Bombus impatiens (Cresson), Bombus variabilis (Cres- son), Bombus bimaculatus (Cresson), Bombus morrisoni (Cresson), (Cresson), and (Smith) (Table 1). The earliest set of records, from 1900 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 a temporal 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 that we 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 of 34 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 2006 to 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 in the 2013 survey. The southern half of the state had a significantly greater bee abundance than the northern half (MANOVA F1,44 5 14.854; P 5 0.0004). This pattern held for B. pensylvanicus (ANOVA F1,44 5 8.855; P 5 0.0047) and B. fraternus (F1,44 5 4.786; P 5 0.0340), but no pattern was found for B. impatiens and B. griseocollis. The eastern third of 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). 422 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

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).

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

Species 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.

The American Bumble Bee, B. pensylvanicus, was the most common species in all time intervals, and the 2013 survey. From historical data, records available for this species increased 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 effort and not necessarily indicative of population dynamics. Based on all available records from 1900 to 2013, some Oklahoma bumble bee species were not well represented, and thus, were not necessarily expected in the 2013 survey, with four species having under ten records (B. bimaculatus 5 9, B. morrisoni 5 3, B. appositus 5 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 species collected (line) in Oklahoma. Dashed line was expected number of species based on historical records. Asterisk (*) represents authors’ 2013 survey. VOLUME 88, ISSUE 4 423

Fig. 3. Rarefaction analysis showing the pattern of bumble bee species richness accumulation with increased sampling effort. The line plateaus at four species: Sobs is number of bumble bee species observed and Scal is the number of bumble bee species expected. specimen (and therefore the most recent Oklahoma record to our knowledge) was from 1975 in Oklahoma County, in the center of the state.

Discussion Bumble bee species richness appears to have declined over time in Oklahoma, from ten species recorded from 1900–1949 to five species documented from 2000–2013. Natural history collections provide invaluable baseline information for describing biodiversity (Lister et al., 2011) and are the most important, and often the exclusive, source of historical data 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 species include four species from the 2013 survey and an additional fifth from records available since 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 its abundance 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 present in 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.

Count Percentage Bee Species Rural Urban Rural Urban

B. fraternus 2 7 0.22 0.78 B. griseocollis 44 5 0.90 0.10 B. impatiens 2 5 0.29 0.71 B. pensylvanicus 115 90 0.56 0.44 424 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY species coincides with neighboring Texas (Warriner, 2012) and Arkansas (Chandler and McCoy Jr, 1965). Recent sampling efforts in the south-central region of the United States have found B. pensylvanicus as a common bumble bee species –the most common species in Black Belt Prairie of Mississippi from 1991–2001 (Smith et al., 2012), the second most common species in Kansas canola fields from 2011–2013 (Tripodi et al., 2014), and the third 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 differs from reports in the north, including in Illinois where the species declined from being nearly 1/3 of all bumble bees collected from 1900–1949 to only 4.4% of bumble bees sampled from 2000–2007 (Grixti et al., 2009) and, even more severely, in southern Ontario where the species was not found at all in a 2004–2006 sampling effort, despite being present in historical 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 only B. pensylvanicus. There appears to be a distinction between northern North America, where B. pensylvanicus has had an estimated 23% reduction in range, and southern regions where 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 the most abundant species in Oklahoma, temporal changes in population (including declines) cannot be assessed because density data is unavailable, a situation common for other bumble bee species (Goulson et al., 2015). Further analysis of latitudinal differences of B. 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 whose females replace B. pensylvanicus queens in their nest (Williams et al., 2014). B. variabilis was once a moderately common species in Oklahoma (,4% percent relative abundance from 1900–1999), but has not been recorded in the state since 1975. This species was not located in the 2013 survey or in records available since 2000, consistent with current literature 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 one county in Nebraska, but did not find the species in nine additional counties with historic records, and the species has recently been reported from two counties in Mississippi (Smith et 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 North America is B. pensylvanicus, the most common species observed in each surveyed region of 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 of the sites that we sampled, including Wildlife Management Areas, State Parks, National VOLUME 88, ISSUE 4 425

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

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Appendix 1. List of the 46 sites sampled in Oklahoma in 2013. Regions refer to one of the six general areas of the state (see Fig. 1). VOLUME 88, ISSUE 4 429

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.