Distribution and floral hosts of Anthophorula micheneri ( Timberlake , 1947 ) and Hylaeus sparsus ( Cresson , 1869 ) , ( Insecta : Hymenoptera : Apoidea : Anthophila ) , with new state records in Giles and Loudoun counties , Virginia , eastern USA

New collection records for Anthophorula micheneri (Timberlake, 1947) from Loudoun County and other locations in Virginia, USA document an approximately 1,350 km extension of its previously recorded geographic range. New state records for the rarely seen Hylaeus sparsus (Cresson, 1869) collected in Giles County and from a blue vane trap in Loudoun County, Virginia add to our knowledge of this species’ range and phenology in the USA. Floral records for both species are documented with a discussion of possible host preferences.

An inventory of bee species (Hymenoptera: Apoidea) was conducted from March to October 2010 and from February to October 2011 at Banshee Reeks Nature Preserve (BRNP), Loudoun County, Virginia, USA.The inventory resulted in a new distribution record for Anthophorula micheneri (Timberlake, 1947) indicating either a possible range extension or more likely a confirmation of a previously broader range than is currently known; and a new distribution record for the uncommonly collected Hylaeus sparsus (Cresson, 1869).Both A. micheneri and H. sparsus are represented in United States and Canadian collections by a limited number of specimens, consequently little information is available regarding their geographic distribution, ecological behavior, preferred habitats, and potential plant associations in North America.
The Banshee Reeks Nature Preserve is a 293 ha preserve located in the northern piedmont region or foothills of the Blue Ridge Mountains in Loudoun County, Virginia, USA (39.029586°, -77.598799°, 80-105 m elevation).The Preserve includes old agricultural fields and wetland habitats colonized by native and introduced herbs and shrubs; a rare mountain/piedmont basic seepage swamp community; and mixed hardwood forests of oak (Quercus spp.), walnut (Juglans spp.), and hickory (Carya spp.) and is bordered in the south and southwest by Goose Creek.In 2010, six sites were selected at BRNP to sample bee species occurring in a variety of habitats including upland forest (site 1), open grassland (site 2), savannah (site 3), pond edge/pine forest (site 4), successional field (site 5), and mountain piedmont basic seepage swamp (site 6).Site 5, from which the A. micheneri specimen was collected, was located west of the intersection of the Western Watercress and Greenway trails at the BRNP (39.0256°, -77.5898°, 87.8 m elevation).Dominant flowering plants at site 5 included multiflora rose (Rosa multiflora Thunb.) and autumn olive (Elaeagnus umbellata Thunb.)(Figure 1).
Sampling materials and methods used to conduct this inventory are detailed in Droege (2012).While examination of the efficacy of different sampling methods was not a specific goal for this study, a combination of 96 ml or 3.25 U.S. fluid oz plastic Solo® cup pan traps (plain white, and painted fluorescent yellow, and fluorescent blue) placed on the ground or elevated with wire stakes (where thick vegetation prevented ground placement); 2 L plastic blue vane traps (blue vanes, white bottle) suspended in tree canopies, and hand netting methods were used in order to collect as great a variety of species as possible.Different colored pan traps were used because they have been shown to attract different bee species.In one example from a prairie restoration study, blue colored pan and vane traps in particular, have been shown to attract a greater number of individuals and hung from branches of selected trees using green wire hooks prior to buds opening or as early as possible in the flowering period and samples were collected from them every two weeks until the trees stopped flowering.Care was taken to position the vane traps among or as close to canopy flowers and if possible, on the east side of trees to reduce wind exposure.On 23 April 2011, a blue vane trap was hung in a flowering pawpaw tree (Asimina triloba (L.) Dunal) in a stand of 3-4 individuals of the same species, located at the southern end of the Cathedral trail on the banks of Goose Creek, BRNP, Loudoun County, VA, USA (39.0216°, -77.5981°, 82 m elevation) (Figure 2).Specimens were collected from the vane trap on 20 April 2011 (when the propylene glycol and Dawn® solution was also refreshed), and again on May 6.
Weather conditions and flowering plants were observed and recorded during sampling.Daytime high temperatures recorded by the nearby (5 km away) Leesburg Executive Airport weather station (KJYO) were referenced for this study site.
Specimens collected at BRNP were prepared, pinned, labeled, identified and deposited in the Smithsonian National Museum of Natural History's National Collection (NMNH), Washington, District of Columbia, USA.The specimen labels included a unique data matrix symbol generated using Discover Life's Web Labeling System (http://www.discoverlife.org/label/).Electronic data associated with each BRNP specimen are accessible from the United States Geological Survey (USGS) Patuxent Wildlife Research Center (PWRC) Native Bee Inventory and Monitoring Lab (BIML) database that is hosted online by Discover Life (http://www.discoverlife.org), a project administered by the 501-C3 non-profit Polistes Foundation; and also available for download from the USGS Biodiversity Information Serving Our Nation (BISON) mapping application (http://bison.usgs.ornl.gov/).The USGS will also soon make these variety of species than yellow colored traps (Geroff et al. 2014).The pan traps were filled to ¾ of their volume (a depth of approximately 3 cm) with a solution of water and blue Dawn® dishwashing liquid and placed on the ground or in elevated wire trap holders (Figure 1).The vane traps were filled to 2.5 cm depth with a solution of red dyed propylene glycol and blue Dawn® dishwashing liquid.Propylene glycol was used in the vane traps, which would be operated for longer periods (up to two weeks at a time), because of its slower evaporation rate and preservative properties.Pan trap sampling began when daytime high temperatures were above 18°C (65°F).Every two weeks, 30 alternating color pan traps were placed 5 m apart along a 150 m linear transect or circular array (Site 5 only) at each site before 9 am Eastern Time (ET) and removed after 5 pm ET.Pan traps were placed at site 5 at 7:40 am ET and retrieved at 6:15 pm ET on 6 September 2010 by David McCarthy.
Blue vane traps were added to the sampling methodology in 2011 to more effectively sample bee species that may forage in the canopy of flowering trees, especially early in spring (Ulyshen et al. 2010).Trees selected for blue vane trap sampling were separate from and did not fall within pan-trapping sites 1-6.They were selected opportunistically from a variety of locations across the Preserve based on their accessibility (e.g., height, approachability on foot); their position in relation to other flowering trees of the same species (e.g., center of a monospecific stand); and their flowering status (e.g., buds forming or about to open).Blue vane traps were  and other records in the USGS PWRC BIML database available through the Global Biodiversity Information Facility (GBIF) (http://www.gbif.org).All scientific names used in this article were validated against the Integrated Taxonomic Information System (ITIS) (http://www.itis.gov) and the Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila) (Ascher and Pickering 2014;ITIS 2014).Additional collection and distribution records for both bee species and the plant species off which they were collected (where available) were solicited and obtained directly from published literature and museum, university, and researchers' private collections (Tables 1 and 2).The taxonomic literature describing A. micheneri and H. sparsus was also examined to inform search and detection of historical collection records (Cresson 1869;Robertson 1898Robertson , 1929;;Lovell, 1901;Metz 1911;Timberlake 1947Timberlake , 1980;;Michener and Moure 1957;Krombein 1958;Hurd 1979;Mitchell 1951Mitchell , 1960Mitchell , 1962;;Snelling 1968Snelling , 1970;;Silveira 1995;Michener 1942Michener , 2007;;Edens-meier et al. 2011;Moure et al. 2012;Poole and Gentili 2014).
Taxonomic determinations for the A. micheneri and H. sparsus specimens collected at BRNP were completed by S. Droege (USGS, Patuxent Wildlife Research Center, Native Bee Inventory and Monitoring Laboratory, Beltsville, MD, USA).The male A. micheneri specimen was identified using the Discover Life Anthophorula Guide (http://www.discoverlife.org/mp/20q?guide=Anthophorula) and the keys in Mitchell (1962) and associated species accounts.It was also compared with specimens at the NMNH of both A. micheneri and A. asteris (Mitchell, 1962) and was distinguished from the latter by the extensive dark or black areas around the basal and lateral areas of the clypeus with the central and apical regions yellow.
The male H. sparsus specimen was identified using the Discover Life Hylaeus Male Guide (http://www.discoverlife.org/mp/20q?guide=Hylaeus_male) and the keys in Mitchell (1960).It is distinguished in particular by the pointed shape of the front coxae.
A male specimen of A. micheneri was among the 58 specimens collected by David McCarthy from pan traps at site 5 on 6 September 2010.Carolina horsenettle (Solanum carolinense L.) was the only plant recorded in flower at site 5 on this date.The weather recorded that day included a clear sky with a temperature of 18°C (65°F) at 7:40 am ET when the pan traps were placed, and a maximum of 29°C (85°F) for the day.A male specimen of H. sparsus was collected in a sample of five specimens removed from the pawpaw tree blue vane trap by Elizabeth Sellers at 10:30 am ET on 6 May 2011.No other plants were observed in flower within sight of the pawpaw tree at the time of sampling on 6 May 2011.
The scientific name of a species is often the central datum to which all other existing information about the species is linked.Therefore, an understanding of the species' taxonomy is key to the successful search and detection of historical collection records for the species.Charles D. Michener collected the female holotype of A. micheneri from Hattiesburg, Mississippi in October 1943, which was first described as Exomalopsis (Anthophorula) micheneri in Timberlake's (1947) revision of the species of Exomalopsis Spinola, 1853 occurring in the United States.The holotype specimen is currently stored in the collections of the American Museum of Natural History, New York (AMNH 2014).Michener also collected 2 male and 15 female paratype specimens of A. micheneri from the same type locality (at least 10 of which are reported to also reside in the collections at AMNH); and 2 more female paratypes from Camp Shelby, near Hattiesburg, Lamar County, Mississippi in 1943and 1944. Timberlake (1947) states that all of these specimens were collected off Agalinis purpurea (L.) Pennell (as Gerardia purpurea) (family Orobanchaceae) (ITIS 2014).Michener and Moure (1957) proposed a new subgenus Anthophorisca of Exomalopsis, which included A. micheneri as Exomalopsis (Anthophorisca) micheneri.Timberlake (1980) retained the E. (Anthophorisca) micheneri taxonomy in his review of North American Exomalopsis.But the subgenus and species was moved to Anthophorula, which was elevated to genus by Silveira (1995), with the taxonomy currently settled at Anthophorula (Anthophorisca) micheneri.The distribution of all species in the Anthophorisca subgenus has been consistently described as restricted to the southern and central United States, as far north as central California, Utah, Colorado, Nebraska, and Indiana; east to Mississippi and south to Oaxaca, Mexico (Michener and Moure 1957;Silveira 1995;Michener 2007).However, with the exception of the A. micheneri occurrence records described here for Virginia, historical collection records examined to date indicate restriction of this particular species' distribution only to the south-central U.S. (Texas and Mississippi) with a notable absence in the southeastern U.S.
Timberlake referenced a series of 118 specimens of A. micheneri collected off the same plant species (Agalinis purpurea) at two sites in Flatonia, Fayette County, Texas by Baker, Kamm, and Michener on 12 September 1970 (Timberlake 1980).Although this plant species has been recorded in neighboring Washington County and other counties east of Fayette County, Texas, J. L. Neff (pers.comm.2012) suggests that Baker, Kamm, and Michener's A. purpurea identification was likely a misidentification of the plant as that species is not known to occur in Fayette County, while other species of Agalinis it is easily confused with, such as A. strictifolia (Benth.)Pennell and A. heterophylla (Nutt.)Small, do occur in that location (USDA PLANTS 2014a, 2014b).Neff also reported collecting A. micheneri from Agalinis strictifolia in Texas in September and October 1994, and in September 2010.Agalinis purpurea, along with Agalinis tenuifolia (Vahl) Raf.var.tenuifolia, is native to and has been recorded historically and more recently in Loudoun County, VA, while A. setacea occurs in Virginia but has not yet been recorded specifically in Loudoun County (Virginia Botanical Associates 2014).Agalinis strictifolia occurs only in Texas (National Museum of Natural History 2014b;USDA PLANTS 2014a, 2014b).No species in the genus Agalinis were recorded in flower at site 5 at BRNP during the 2010-2011 study.However a 2004 floristic survey of the broader Eastern Goose Creek Watershed that encompasses the BRNP did detect Agalinis species (Williams pers. comm. 2012).Accurate plant identification is important especially when potential species associations are being reported.Thus in addition to reporting the name(s) of the taxonomist(s) who confirmed the insect specimen identification and the disposition of the insect specimens, researchers and authors should also report the same information for the plants, and where appropriate, associated plant specimens from which the insects were collected (Vink et al. 2012).
Hylaeus sparsus (Cresson) (Colletidae: Hylaeinae) While Hylaeus sparsus is known to have a relatively broad geographic distribution ranging from southeastern Canada south to Georgia, USA, west to central Texas, and northwest to Indiana (Mitchell 1960;Snelling 1968;Michener 2007), its collection in 1997 and 2011 are the only occurrences of the species in Virginia known to date (Figure 4).And the more recent collection of two female specimens from southern Saskatchewan, Canada in 2013 is a further western extension of the species' known range in Canada and North America.
Specimen records gathered to date indicate that at least 115 specimens of H. sparsus have been collected and documented in the U.S. and Canada, usually singly during individual collection events, between 1867 and 2013 (Table 2).Hylaeus sparsus (Cresson, 1869) was originally described by Ezra T. Cresson as Prosopis sparsa Cresson, 1869 from a female specimen collected in Pennsylvania in 1867 (Cresson 1869;AMNH 2014a).Robertson (1898) described Prosopis thaspii Robertson, 1898 from two female specimens he collected in 1897.Metz (1911) in a revision of the genus Prosopis, synonymized P. sparsa under P. modestus Say, 1837, and described a new species P. potens.Michener (1942), while treating Hylaeus as the valid genus for species formerly included as Prosopis, described a monotypic subgenus Hylaeus (Metziella) to include H. potens.Krombein (1958) listed H. sparsus as a valid species, along with Hylaeus thaspii (Robertson) as a new synonym based on T. B. Mitchell's examination of the type specimens of both names.Two years later, Mitchell (1960) recognized both H. potens and H. sparsus as members of the subgenus H. (Metziella).Snelling (1968) subsequently synonymized H. potens under H. (Metziella) sparsus (Hurd 1979;Michener 2007).
Hylaeus sparsus has been collected off or observed visiting (the latter in the case of Robertson (1929) 2).
Females of several species in the Colletidae family are either oligolectic or "exhibit narrow polylectic tendencies" (Hurd 1979(Hurd : 1748)).Although records show collection of females of H. sparsus off Salix nigra in Texas, Erigeron philadelphicus in Pennsylvania, and Cornus canadensis in Ontario, Arduser notes that to his knowledge females of the species have never been collected from any family of plants other than the Apiaceae in the Midwestern U.S., while males have been found on flowers of plant species in other families as evidenced by the historical collection records examined here (Arduser, pers. comm. 2012).If this affiliation with plants in the Apiaceae also holds true for females in the Eastern U.S. then future detection efforts could focus on the plant species in the Apiaceae family mentioned by other collectors.
Apiaceae species currently known to occur within the Eastern Goose Creek Watershed include Thaspium barbinode, Osmorhiza longistylis, Daucus carota L., and the early flowering spring ephemeral Erigenia bulbosa (Michx.)Nutt.within the Preserve itself (Williams 2004;Cour 2008).Thaspium trifoliatum, Chaerophyllum procumbens, Sanicula odorata, Taenidia integerrima, Zizia aurea, and Z. aptera are (or were historically) present in both Giles and Loudoun County (USDA PLANTS 2014a, 2014b; Virginia Botanical Associates 2014).Historical collection locations for these plants in northern Virginia may no longer exist due to rapid development.And neither Williams (2004) nor Cour (2008) PLANTS 2014aPLANTS , 2014b)).However, this plant species' distribution in the U.S. is similar to that of H. sparsus in states in the western portion of the Mississippi River watershed (USDA PLANTS 2014a, 2014b).Phacelia patuliflora is found only in Texas, and while P. purshii is present in some counties in Virginia, these do not include Giles or Loudoun (USDA PLANTS 2014a, 2014b).Field-based behavioral observations or an analysis of pollen extracted from the specimen (pollen is carried internally by this species (Mitchell 1960)), at the time of collection may determine whether or not this species was actively foraging on the flowers of Asimina triloba at the time of capture.
Arduser describes H. sparsus (in the Midwestern U.S.) as a vernal univoltine natural community-dependent species and primary oligolege of Apiaceae, restricted to woodlands and forests.That is to say, H. sparsus is a species that occurs in relatively intact, high quality diverse natural habitats rather than back yards, old fields, roadsides, etc., (Arduser pers. comm. 2014).He considers its conservation status in the Ozark Mountains of Missouri to be secure, but this may not be the case throughout its entire range.Michener (1979: 287) listed the Hylaeinae as being "most abundant and diversified in mesic or humid areas".Collection records and published references to this species being collected in or near riparian or seasonally flooded forests, piedmont watersheds and bottomland habitats such as those associated with the Oconee River in Georgia (Ulyshen et al. 2010;Hanula and Horn 2011;Hudson 2013;Hanula, pers. comm. 2014); Tanglewood Spring in South Carolina; Cascade Falls and Goose Creek in Virginia; and in and around the shores of Lake Erie, Ontario (Marshall 2009; University of Guelph 2014) may be purely coincidental, a reflection of collectors' habits, or may suggest a possible habitat affinity worth further exploration.Mitchell (1960) describes the nesting habit of Hylaeus species as including the pithy stems of plants such as sumac (Rhus L.), at least two species of which Rhus copallinum L. and Rhus glabra L. occur at BRNP among numerous other pithy stemmed plant species such as those in the genus Rubus L. (Williams 2004;Cour 2008).Hylaeus species are also known to nest in pre-existing tunnels and burrows in rocks or soil (Mitchell 1960;Barrows 1975;Michener 1979).The BRNP sites were not inspected for these signs as part of this study.
These new data for Anthophorula micheneri in Virginia, USA extend the known geographic distribution for this species and indicate that although rarely detected this species may exhibit a broader distribution across the United States than initially suspected.This new detection and historical records indicate that collecting later in the year (September -October) and especially from flowers of plants in the genus Agalinis may reveal more information about A. micheneri's distribution and foraging habits in the U.S. The Virginia records for Hylaeus sparsus in combination with the historical collection records and plant associations published here, advance our knowledge of this rare species and indicate possibilities for further study of its habitat preferences and foraging habits, especially on plant species in the family Apiaceae.

Figure 1 .
Figure 1.Pan trap filled with a solution of water and blue Dawn® dishwashing liquid in an elevated wire pan trap holder at Site 5 (Successional Field; from which the Anthophorula micheneri specimen was collected), Banshee Reeks Nature Preserve, Loudoun County, Virginia, USA (39.0256S, -77.5898W, 87.8m elev.).Multiflora rose (Rosa multiflora) is flowering in the background.Credit: Elizabeth Sellers, 20 May 2011.
Sellers and McCarthy | Anthophorula micheneri and Hylaeus sparsus in Virginia, USA michen eri at BRNP in September 2010, a male specimen was collected in September, 2013 by R. Morawe in Colonial Beach, Virginia (38.1979°, -76.9285°) 109 km southeast of BRNP.Two female specimens of A. micheneri (located in the NMNH National Collection in 2010) were collected in October 1983 by R. Duffield (Howard University, District of Columbia, USA) at Quantico Marine Base (62 km southeast of BRNP), whose boundaries intersect Prince William, Stafford, and Fauquier counties in northeastern Virginia.Duffield's A. micheneri specimens were identified by George Eickwort and labeled as Exomalopsis micheneri Timberlake, 1947 and were collected from Agalinis setacea (J.F. Gmel.)Raf.(as Gerardia setacea) (ITIS 2014).A third female specimen also identified by George Eickwort as A. micheneri in the National Collection at NMNH was collected in or near the town of Falfurrias, Texas by A. C. Morgan in 1907 but appears not to be the same species.All other collection records examined by the authors indicate that A. micheneri has not been collected in the United States (U.S.) any further north and east than Hattiesburg, Lamar and Forrest counties in southern Mississippi (1,353 km southwest of Quantico Marine Base and 1,364 km southwest of BRNP, VA respectively) (Figure 3).Thus the NMNH specimens along with recent collections from the BRNP and Virginia Beach represent an extension of the known range of A. micheneri of over 1,350 km (Table

Figure 3 .
Figure 3. Map summarizing Anthophorula (Anthophorisca) micheneri (Timberlake, 1947) historical and modern collection events in the United States.Map Insert: Northern Virginia, showing recent and BRNP collection events.