New records and range extensions of several species of native bees (Hymenoptera: Apoidea) from Mississippi

Abstract Background The native bee fauna of Mississippi, USA has been historically poorly sampled, but is of particular relevance to determine range limits for species that occur in the southern United States. Currently published literature includes 184 species of bees that occur within the state of Mississippi. Additions to the list of native bees known for Mississippi are reported with notes on range, ecology and resources for identification. New information The geographic ranges of seven additional species are extended into the state of Mississippi: Andrena (Melandrena) obscuripennis Smith, 1853, Anthemurgus passiflorae Robertson, 1902, Dieunomia bolliana (Cockerell 1910), Diadasia (Diadasia) enavata (Cresson 1872), Peponapis crassidentata (Cockerell 1949), Triepeolus subnitens Cockerell and Timberlake, 1929 and Brachynomada nimia (Snelling and Rozen 1987). These records raise the total number of published species known from the state to 191. Anthemurgus and Brachynomada are also genera new to Mississippi.


Introduction
The native bee fauna of Mississippi is poorly known and sampled, but is of particular relevance to determining range limits of many species (Smith et al. 2012). Mississippi is composed of four distinct ecoregions: the Southeastern Plains, the Mississippi Alluvial Plain, the Mississippi Valley Loess Plains and the Southern Coastal Plain (Chapman et al. 2004).
The majority of the recorded bee species currently known from Mississippi are from Mitchell, who summarised state level distributions across the eastern United States and recorded 122 species from Mississippi (Mitchell 1960, Mitchell 1962. The majority of the records included therein are those from collections made by Michener in the 1940s near Hattiesburg, MS, in the South-eastern Plains (Michener 1947). Smith et al. (2012) listed 53 more records from the Black Belt Prairies, also part of the South-eastern Plains, while Rightmyer (2008) listed an additional five species in a revisionary study of the cleptoparasite Triepeolus Robertson. An additional series of papers (MacGown and Scheifer 1992, Cane et al. 1996, Colla et al. 2011, Parys et al. 2015 each added singular records, bringing the published total number of species reported from the state of Mississippi to 184. Of the four ecoregions that occur within the state, the Mississippi Alluvial Plain is of particular interest as it is almost completely un-sampled for native bee fauna with the exception of Parys et al. (2015) and is part of the Mississippi Alluvial Valley (MAV) which also includes portions of Arkansas, Louisiana and Missouri. This region of Mississippi is colloquially referred to as the "Delta" of the state. The MAV is the largest floodplain in the United States, comprising over 10 million hectares of historically bottomland hardwood forest that was seasonally flooded (Frederickson 2005). Today, the majority of the floodplain has been controlled with a system of levees constructed during the twentieth century, allowing the majority of the landscape to be converted to commercial agriculture (Faulkner et al. 2011). Landscapes fragmented by agriculture generally have less biodiversity than those left as natural habitats, though mass flowering crops can influence the densities of generalist pollinators (Westphal et al. 2003, Potts et al. 2010. Baseline data on the presence and distribution of native bee species of these previously unsampled areas across the MAV can inform decision-making by land managers and potentially be Notes: This species is monotypic and oligolectic on a native passionflower, Passiflora lutea L. (Fig. 2). Neff and Rozen (1995) described foraging behaviour and larval characteristics. This species' known range is from central Texas, Kansas, Illinois and east to North Carolina in the United States (Michener et al. 1994, Neff and Rozen 1995, GBIF 2017b; this is the first report of this species in Mississippi. All 23 specimens of A. passiflorae reported here were net collected from P. lutea growing at a single location in Cleveland, MS, located in Bolivar County (Fig. 3).   (Cockerell, 1910) Notes: Originally described from Texas (Cockerell 1910), this species is smaller than Dieunomia heteropoda (Say), the more commonly encountered species in northern Mississippi. Two subspecies are currently recognised, the second of which is D. (D.) bolliana helenii (Cockerell 1936). We choose not to use a subspecific classification here, given their questionable status. Notably, Cockerell himself admits that a specimen collected alongside the type of his subspecies "approaches the typical form in having the mesothorax and sides of thorax black" (Cockerell 1936). Similar variation in other collections of this species and other Dieunomia has been observed by MCO. Ultimately, it seems unlikely that this subspecific epithet will survive subsequent taxonomic treatment. The currently known distribution is reported only for the south-western United States of Texas and New Mexico and ranges south into México (Hurd et al. 1980). Cockerell (1910) reported collections made from Dracopis amplexicaulis (Vahl) Cass (listed as Rudbeckia amplexicaulis) and Helianthus sp. Additional observations of D. bolliana individuals collecting pollen and nectar were reported from Helenium microcephalum DC. and Polypteris texana (DC) A. Gray (Cockerell 1936). Hurd et al. (1980) regard this species as a oligolege of composites, secondarily associated with Helianthus.
Of the ten specimens of D. bolliana reported here from Mississippi ( Fig. 4), nine were collected in the month of June and three of those were collected by sweeping roadside patches of Coreopsis sp. for other insects. Two specimens were collected in soybeans on the USDA ARS' research farm outside Leland, MS. The remaining four June specimens were also collected from roadsides by sweeping, but no host plant was recorded. The last specimen was collected in a blue vane trap during July at the Alcorn State University Research Farm located in Mound Bayou, MS.

Notes:
Little is known about the distribution or specific biology of this species. The original type material was collected and described from Chase and Woodson Counties in Kansas, with additional records recently from Illinois (Snelling and Rozen 1987, Ascher and Pickering 2017). Images of the collection labels from Woodson County specimens indicate that they were collected from Amphiachyris dracunculoides D.C. Nutt (GBIF 2017a). All known members of this group are cleptoparasitic nest associates of Exomalopsis spp. (Rozen 1984).
Eight specimens were collected by malaise trap during the fall (autumn) of 2016 in Tallahatchie National Wildlife Refuge, located near Phillip, Mississippi in Tallahatchie County (Fig. 5). The malaise traps were located not far from each other on the shore of an oxbow lake filled with emergent vegetation.  (Rightmyer 2008). Specimens have been taken from 4 May through 12 October and observed on a variety of host plants (Rightmyer 2008). This group is also cleptoparasitic, with T. subnitens observed entering a burrow of Svastra (Epimelissodes) obliqua (Say) (Hurd et al. 1980).

Triepeolus subnitens
The three specimens reported from Mississippi were all females (Fig. 6) and collected during 2015 and 2016 in two counties (Sharkey and Sunflower). They were taken from both Helianthus sp. and from a blue vane trap located within a soybean field. a b c Figure 6.

Notes:
The genus Diadasia only occurs in the New World and has been traditionally collected in western and south-western parts of the United States, though it also occurs in western Canada (Hurd et al. 1980, Sheffield et al. 2017. This species has the largest distribution of any species of Diadasia, ranging from Washington and California on the west coast, east through Texas and Missouri (Hurd et al. 1980). Descriptions and illustrations of the ground nests have been published (Bohart 1952, Linsley andMacSwain 1957). The documented range of D. enavata was recently extended into Arkansas (Stephenson et al. 2018) and now into Mississippi.
Over 100 specimens of D. enavata have been collected from Bolivar, Sunflower, Sharkey and Washington Counties in the Delta region of Mississippi (Fig. 7). The majority of the specimens were picked up in bee bowls in or around sunflower fields, though specimens were also picked up in corn, soybeans and sorghum fields. planted sunflower fields. The single specimen of P. crassidentata was also collected from an agricultural field, but as a singleton, it may be a tourist or suggest a low population density. While this specimen was collected from a trap in a soybean field, members of Peponapis are known to be Cucurbita specialists and, ergo, unlikely to be foraging in the soybean field.
These seven species were unexpected in collections made in the Mississippi Delta, especially given their prior known ranges. Their presence, especially those that are abundant, indicates that established populations occur in the region. Further collections within the Mississippi Alluvial Valley and, in particular, the Mississippi Delta, are expected to yield additional records for the state and clarify distributional records of other species collected within the state of Mississippi. This study may also have implications for undersampled areas in other places, with distributions of species unexpectedly extending into these areas.