To understand ecosystems, the biodiversity responsible for their function must be documented. Pollinators are an essential component of terrestrial ecosystems and of agricultural production. They are needed for the reproduction of three-quarters of the world's flowering plants, which includes a large proportion of the food for wild vertebrates and two-thirds of the crop species (Committee on the Status of Pollinators in North America 2007). Because bees collect pollen as their source of protein, they are overall the most efficient and important pollinators (Michener 2007). Agricultural crops that require pollination are largely dependent on the honey bee Apis mellifera L. Beyond their vital importance in natural communities, native bees contribute significantly to agricultural pollination (Hurd & Linsley 1964; Cane & Payne 1988; Thorp 2003; Torchio 2003; Pascarella 2007; Winfree et al. 2008). Native bees can be diverse in agricultural systems (Tuell et al. 2009) and can potentially have a much greater role in crop pollination, especially in light of recent honey bee losses (Winfree et al. 2007).

Natural bee populations and even species, especially endemic species, are threatened by several factors. The major threat is the loss of natural habitat, including nesting sites and floral resources, due to land development and agricultural intensification (Buchmann & Nabhan 1996; Allen-Wardell et al. 1998; Kearns et al. 1998; Kremen et al. 2002; Klein et al. 2007; Goulson et al. 2008). The expansion of large-scale industrial agriculture eliminates natural areas, along with the associated bee diversity responsible for pollination services that provide stability for the human food supply. Thus, conservation and restoration are “crucial to the preservation of pollinator populations and diversity” (Committee on the Status of Pollinators in North America, 2007).

More than 19,500 described species of bees are known world-wide, about 3,500 of which occur in the United States and Canada (Ascher & Pickering 2010). Much remains to be learned about bee taxonomy, distribution, species richness, abundance, natural history, and floral hosts. The need and importance of thorough systematic surveys to increase our knowledge of bee faunas has been emphasized (Committee on the Status of Pollinators in North America 2007). Existing natural areas, restored natural areas, farms, and other anthropogenic landscapes are all relevant sites for such studies. Ongoing monitoring is required to detect changes over time, including decline or loss of species, which might occur as a consequence of environmental disturbances and land use changes (Deyrup et al. 2002). Given the ability of bees to disperse and occupy newly available habitats, bee communities may serve as quality bio-indicators when comparing restored natural land with established natural areas.

Florida is a unique place for biological studies, being a large peninsular extension of the eastern United States that extends from temperate into subtropical climates. Florida has a large diversity of natural plant communities and a major agricultural industry. The state has had an increasing human population and intense development, which have slowed recently but will likely resume in the future. Thus, there is urgency to document and preserve biodiversity in its remaining natural areas. About 320 described and several undescribed bee species have been recorded from Florida (Mitchell 1960, 1962; Deyrup et al. 2002; updated by Pascarella 2008; additional state records and updated nomenclature in Ascher & Pickering 2010). The state list for Florida is relatively well documented, but county records are fragmentary (Pascarella 2008), and only a few systematic site surveys of the bee fauna have been conducted. Graenicher (1930) studied the bees along the Atlantic coast of southeastern Florida, mainly the Miami area, extending north to Jupiter, south to Homestead, and southwest to the former Royal Palm State Park on the eastern side of what is now Everglades National Park. Pascarella et al. (2000) conducted a broader survey of bees at 4 regions within the Everglades. Their report contains a summary of bee species from the Everglades and from Dade and Monroe counties outside the park including those found by Graenicher, those listed in other published records, and present in regional museum collections. Deyrup et al. (2002) list the bee species and their floral hosts found at Archbold Biological Station on the Lake Wales Ridge, Highlands County, south-central Florida, and discuss the Florida bee fauna. Unpublished surveys at the Tall Timbers Land Conservancy (TTLC) Research Station and the St. Marks National Wildlife Refuge, north and south of Tallahassee, respectively, and the Osceola National Forest, west of Jacksonville, have been done by John Pascarella (Georgia Southern University, personal communication). Despite these multiple surveys, the bees of large areas of Florida, including major regions such as north-central Florida, have not been studied adequately.

This report documents 111 bee species in 34 genera captured in natural areas of Alachua County in the north-central region of peninsular Florida. This survey represents the first in a series that will include additional areas and different plant communities in northern Florida. Bees move between natural and cultivated areas (Kremen et al. 2002, 2004; Kohler et al. 2008; Winfree et al. 2008), so both types of landscapes are being studied.

MATERIALS AND METHODS

RESULTS

In this study, a total of 2,590 bees were captured in the Alachua County natural areas, belonging to 34 genera and 111 species, 1 of which is believed to be undescribed. Six percent of the species were in the family Colletidae, 15% in Andrenidae, 23% in Halictidae, 25% in Megachilidae, and 31% in Apidae. Eighty-eight percent of individuals were female; 12% male. The list of the species, including the earliest and latest dates when captured, the areas and sites where captured (abbreviations from Table 1), and the numbers of females and males captured in cups and on each of the plant species (names and abbreviations in Table 2), is in Table 3. Eight species were captured over a span of 6 months but were far more abundant during a segment of that time. For these species, the 2 or 3 months and the percentage of bees caught during that period that exceed 70% of the total are indicated in the “Remarks” column. The species found in the county previously or reported to be found throughout Florida, according to Pascarella (2008), are indicated by an “AC” in the “Remarks” column. In organic farms of Alachua County, we have captured about 25 bee species not found in this study, which will be reported in a forthcoming article.

TABLE 1.

BEE COLLECTION AREAS AND SITES.

From the spring of 2006 to the spring of 2007, bee collecting was most consistently and systematically done with colored cups, which were particularly useful at locations and at times with little herbaceous flowering. Eighty percent of the bees were caught in cups. As others have found (Cane et al. 2000; Roulston et al. 2007; Wilson et al. 2008), bees caught in the cups were not fully representative of the resident fauna. Some bee species were seen on flowers but not in cups placed nearby. Although the species are not equally attracted to the colored cups, for each species that is caught, the cups provide an objective measure of their abundance at different locations. From 2006 through 2009, bees also were captured in flight over flowers or nests, but this collecting was opportunistic, inconsistent, and done mainly in the fall, when herbaceous flowers were most abundant. The plants on which bees were caught are listed in Table 2 (plant authorities from Wunderlin & Hansen 2003). Most of the sampling sites were open areas near the edges of mixed pine-hardwood forests and wetlands, at boundaries between or near 2 or more natural communities. Thus, the different collections of bees from the sites are not necessarily characteristic of single plant communities.

TABLE 2.

PLANTS FROM WHICH BEES WERE COLLECTED.

Six species are new state records for Florida: Andrena (Callandrena s.l.) asteroides Mitchell, Andrena (Iomelissa) violae Robertson, Xenoglossa (Eoxenoglossa) kansensis Cockerell (discovery reported by Hall (2010) included specimens from this study), Sphecodes antennariae Robertson, Osmia (Melanosmia) collinsiae Robertson, and Nomada annulata Smith. The last 3 had been found previously only as far south as North Carolina (Mitchell 1960, 1962). Three species and 1 subspecies are Florida endemics: Lasioglossum (Dialictus) robertsonellum Michener, Stelis (Stelis) ater Mitchell, Epeolus floridensis Mitchell, and Ceratina (Zadontomerus) dupla floridana Mitchell. The specimens listed as Lasioglossum (Dialictus) aff. raleighense (Crawford) are believed to be a new, undescribed, species (Jason Gibbs, personal communication). The bee species previously recorded from Alachua County together with those listed as “throughout Florida” (Pascarella 2008) include 73 species found in this study and 67 not found. Thirty-seven additional species found in this study are new county records, including the 6 new state records. Thus, a total of 177 bee species are now reported from Alachua County, which does not include those among the additional species found in organic farms, mentioned above.

In descending order, the following species were the most abundant, the first 6 of which were Halictidae: Lasioglossum (Dialictus) reticulatum (Robertson) (527F 1M); Augochlorella aurata (Smith) (268F 1M); Lasioglossum (Dialictus) puteulanum, Gibbs (180F 1M); Lasioglossum (Dialictus) apopkense (Robertson) (146F); Agapostemon (Agapostemon) splendens (Lepeletier) (114F 11M); Halictus poeyi (109F 11M); Melissodes (Melissodes) communis communis Cresson (78F 25M); Melissodes (Melissodes) bimaculata bimaculata (Lepeletier) (78F 17M); Lasioglossum (Dialictus) nymphale (Smith) (80F 1M); Lasioglossum (Dialictus) pectorale (Smith) (53F 5M).

Two Megachile Latreille species were caught emerging from or flying over ground nests. Megachile (Megachiloides) rubi Mitchell had clustered, but well-separated, nests. A single female of M. (Acentron) albitarsis Cresson came from an isolated nest opening (see images by Tim Lethbridge of a similar nest believed to be of this species from Archbold Biological Station, bugguide.net/node/view/375132).

Traps nests were located at Kanapaha and Paynes Prairies primarily for a separate study, but the bee species that occupied the nests are mentioned here. Osmia (Helicosmia) chalybea Smith was the main bee species to construct cells in the nests (the 5/16″ and 3/8″ diameter holes). For the first time, this species was confirmed as a host of Stelis ater which parasitized about a third of the cells. Both species are univoltine and emerge in the spring. The first males of S. ater were discovered earlier in this survey, captured in cups. More detail about these species' nests, immature stages, and other aspects of their association will be discussed in a separate report (Rozen & Hall, in preparation). Megachile (Litomegachile) mendica mendica Cresson constructed cells in 1 to 2 burrows of about 10% of the trap nests. From 1 nest that had been placed in an emergence cage while the cells were still sealed, the first brood emerged within about 2 months after cell construction began (timing was not closely monitored). Bee cleptoparasites emerged from the same nest, viz. 2 females of Coelioxys (Boreocoelioxys) sayi Robertson (established hosts Megachile (Litomegachile) brevis Say and M. mendica) and 2 males of C. (Acrocoelioxys) dolichos Fox. Most of the leaf-cutter bee cells were heavily infested by tiny parasitic eulophid wasps, Melittobia digitata Dahms (the biology of this genus was reviewed by Matthews et al. 2009). Remnants of a female and a male M. m. mendica and 2 male C. dolichos were found in the destroyed cells along 1 burrow. There was no evidence of M. (Melanosarus) xylocopoides Smith, the recognized host of C. dolichos. Although these results suggest that M. m. mendica may be an alternate host of C. dolichos, the possible prior presence of M. xylocopoides, which might have been destroyed by the Melittobia, cannot be ruled out. Xylocopa (Xylocopoides) virginica virginica L. occupied and widened the burrows of a few trap nests of a different design, with U-shaped burrows with a plexiglass side. Offspring began to emerge in late Jun. The bee species that emerged from trap nests are footnoted on our list (Table 3), but the number of individuals is not included in the total bee count.

TABLE 3.

BEES CAUGHT IN NATURAL AREAS OF ALACHUA COUNTY, FLORIDA, 2006-2009.

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The 25 cleptoparasitic bees species found in this study included 4 Sphecodes Latreille, 5 Coelioxys Latreille, 2 Stelis Panzer, 5 Nomada Scopoli, 6 Epeolus Latreille, and 3 Triepeolus Robertson. Coelioxys (Coelioxys) mitchelli Baker were captured flying over Megachile rubi nests, suggesting a potential new host association for this species. Coelioxys (Xerocoelioxys) galactiae Mitchell were also flying over M. rubi nests. The latter new potential host association is not without precedent, as another species of Xerocoelioxys, C. soledadensis Cockerell, is reported as a possible parasite of Megachile (Megachiloides) soledadensis Cockerell (Hurd 1979), which like M. rubi belonged to the former subgenus Xeromegachile (included in an expanded subgenus Megachiloides by Michener 2007). In the Kanapaha Prairie area, we found several Svastra (Epimelissodes) atripes georgica (Cresson) and Triepeolus quadrifasciatus atlanticus Mitchell, suggesting a new host-parasite association. Rightmyer (2008) reported 3 specimens of this Triepeolus cleptoparasite from a nesting site of S. atripes atrimitra (LaBerge), and Cane (1995) observed adults inspecting and entering host nests. Both of these S. atripes subspecies are recorded from Alachua County (Pascarella 2008).

Only 3 non-native species, Megachile (Eutricharaea) concinna Smith, Megachile (Callomegachile) sculpturalis Smith, and Apis mellifera L. were caught. Honey bees were seen consistently in the cups, but only in small numbers, even at a location (KP-W) where managed colonies were located nearby. They were not collected or counted.

Both previously reported and new associations were found between bee species and the sites or floral resources therein. Hylaeus schwarzii Cockerell, a species associated with wetlands (Graenicher 1930) was found in the wet prairie community of Paynes Prairie. Most of the Colletes Latreille and associated cleptoparasitic Epeolus, Andrena F., and Perdita Smith were found either in the spring or fall, as has been well-documented previously (Mitchell 1960, 1962). Colletes were captured almost exclusively on Asteraceae flowers. Lithurgus gibbosus Smith was found at the sites with abundant Opuntia humifusa (Raf.) Raf., reflecting an oligolectic association with that plant genus (Hurd 1979). Only 2 females of Xenoglossa kansensis, an oligolege of Cucurbita L. and an important squash pollinator, were found in the natural areas, in contrast to large numbers found during this survey period in squash-growing organic farms in Alachua County (Hall 2010). In this survey, only 5 females of the southeastern blueberry bee Habropoda laboriosa (Fabricius) were captured from non-native wild radish Raphanus raphanistrum L. However, this bee species is probably more abundant in natural areas than indicated here, as we have captured this bee along roadsides and other locations from several native plants, such as Eastern Redbud, Cercis canadensis L., and Carolina Jessamine, Gelsemium sempervirens (L.) (Pascarella 2007) that are also found in the natural areas. Osmia chalybea was found foraging on Cirsium Mill, in Alachua County, but we also captured this species along with both sexes of Stelis ater on Cirsium in Highlands County (4 miles SW of Old Venus on 1 Apr 2009 by J. S. Ascher and D. Webber; specimens deposited in the American Museum of Natural History), which further reinforces their association.

DISCUSSION

Previously published Florida bee surveys were from southern Florida. Pascarella et al. (2000) recorded species they had captured in the Everglades National Park along with those that Graenicher (1930) and others had found in the Everglades and in Dade and Monroe Counties outside the Park. In total, Pascarella listed 99 species and, for each of 5 of these, 1 additional subspecies. Graenicher had found 61 of these species. Two species, Augochlorella gratiosa (Smith) and Coelioxys mexicana Cresson and 1 additional subspecies of Megachile brevis (Say) were incorrectly attributed to Graenicher. Deyrup et al. (2002) found 107 described and 5 undescribed species at Archbold Biological Station, not counting Augochlorella striata (Provancher) now placed in synonomy with A. aurata (Smith) (Coelho 2004). The morphospecies referred to as Caupolicana sp. has since been described as C. (Caupolicana) floridana (Michener & Deyrup 2004). Pascarella and Deyrup together reported a total of 142 species, 69 of which were shared, and which included 15 of Florida's 20 endemic bee species and 7 of the 9 endemic subspecies. In Alachua County natural areas, we captured 49 of the species shared between these 2 studies, plus 6 species listed only in the Pascarella report and 12 only in the Deyrup report. Thus, of the 142 total species in the 2 reports, we found 67. Two of the 3 endemic species and the 1 endemic subspecies that we found were in either or both of the 2 reports. Of these endemic taxa, absence of Stelis ater from the Archbold list is noteworthy, especially in light of our subsequent collections of this species elsewhere in Highlands County and in Alachua County. The paucity of Andrena and No- mada, a cleptoparasitic genus of Andrena, in southern Florida and Archbold was noted in the earlier reports, compared with greater numbers in the northern part of the state, and especially in states to the north. Only 3 Andrena species were found at Archbold, none at all in the collections from southern Florida, and only 1 species of Nomada (N. fervida Smith, a cleptoparasite of Agapostemon splendens (Lepeletier) rather than of Andrena) from both areas. By contrast, we captured 13 Andrena and 5 Nomada species. Sixteen percent of the species from southern Florida were cleptoparasitic and 27% from Archbold, compared with 23% we found in Alachua County. In comparing our study with the others, we updated species identities as described below.

Compared with southwestern states such as California and Arizona, and to a lesser degree Atlantic coastal states to the north such as North Carolina, Florida has a relatively low bee diversity (Mitchell 1960, 1962; Michener 1979; Ascher & Pickering 2010) which decreases further in the southern part of the state (Graenicher 1930). Deyrup et al. (2002) and Pascarella et al. (2000) discuss possible reasons which include the abundant rainfall flooding ground nests, to which at least 1 Florida bee species has become adapted (Norden et al. 2003), frequent fires characteristic of some plant communities, spoilage of pollen stores because of the high summer heat and humidity, reduced land topography thereby lacking vertical banks available for ground nests, absence of many temperate plant species in the subtropical region, and a peninsular effect (Schwartz 1988).

Although Florida does not have an especially large bee fauna relative to other states, it is a unique area, evident from the endemic bee species and regional specialties present in the fauna. Because Florida extends as a peninsula as the southern-most region of the eastern United States, almost all of the bee species are derived from farther north on the Atlantic coastal plain or from the west along the Gulf Coast. A relatively high diversity and abundance of Colletes and associated Epeolus, Lasioglossum (Dialictus) and associated Sphecodes, Perdita, Megachilinae especially Megachilini, and Eucerini and associated Triepeolus is characteristic of the Florida bee fauna as a whole. Alachua County is an interface between the peninsular-Floridian fauna and northern elements and between Atlantic and Gulf Coast elements. Compared with subtropical southern Florida, temperate Alachua County is notably enriched in Andrena and associated Nomada, Osmia Panzer, and Bombus Latreille. On the other hand, Florida's endemic bee species and subspecies are concentrated toward the southern end of the peninsula. A few species in southern Florida have West Indian affinities and also are found in the Bahamas and Cuba (Deyrup et al. 2002; Pascarella et al. 2000), but none of these is present in north-central Florida. Thus, the entire Alachua County bee fauna can be considered continental. Some species best known from the southwestern United States also are present as disjunct populations in Florida. One of the most distinctive, Centris lanosa Cresson, was not found in this survey but has been reported from Alachua County (Pascarella 2008), and we found it recently in adjacent Putnam County. The new state records resulting from this study indicate that more remains to be learned about state-level distribution of bee species, even in a relatively well-known Eastern state.

Alachua County has a long native bee flight season but with a short hiatus in Dec and Jan, unlike the Keys, Everglades, and other subtropical areas of the state where native bees fly year-round. Conspicuous flowering in natural areas is concentrated in the spring (initially of woody plants followed by herbaceous plants) and especially the fall (largely Asteraceae). At these times, large numbers of bees, including specialists such as various Andrena, Colletes, Eucerini, and their cleptoparasites can be net-collected on flowers. Bees are present in significant numbers in natural areas even at times and places where flowering is inconspicuous. In such situations, bees are most efficiently collected with the colored cups and consist largely of rather cryptic, generalist, halictids. The numerical dominance of certain halictine species may be a function of their eusociality, their small size, and their use of a variety of sparse, scattered, floral food resources. Significant crop pollinators such as Habropoda and Xenoglossa are present in the natural areas of Alachua County, but not in great numbers. Nonetheless, these natural areas can be viewed as potential sources of such bees for colonization of new acreage of relevant crops, possibly even across large dispersal distances.

The bee fauna of Alachua County includes taxa characteristic of the southeastern coastal plain that have recently changed status, or soon will, as a result of modern revisionary studies. Southeastern populations of Halictus ligatus Say, including all present in Florida, are now considered a separate, cryptic species Halictus poeyi (Packer 1999). Many Florida specimens identified as Lasioglossum (Dialictus) coreopsis (Robertson) pertain to L. robertsonellum. From recent integrative studies of DNA and morphology, Lasioglossum (Dialictus) tegulare (Robertson) has been divided into 5 species, 2 of which, L. puteulanum and L. lepidii (Graenicher), are in Florida (Gibbs 2009, 2010). The subspecies Ceratina dupla floridana is now thought to be deserving of specific rank, as DNA analyses readily separate it from typical Ceratina dupla Say (Cory Sheffield, personal communication). Lasioglossum puteulanum and C. dupla floridana are widely distributed in Florida and occur north to North Carolina. Other subspecies present in Alachua County such as Colletes simulans miamiensis Mitchell, Sphecodes heraclei ignitus Cockerell, and Megachile (Litomegachile) brevis pseudobrevis Say are distinctive southeastern elements that may prove to be phylogenetic species and are therefore deserving of further taxonomic study.

Diagnostic features of Florida's cryptic species, putative subspecies, and visually distinctive regional populations lacking formal taxonomic status, include geographic color patterns. Auglochlora pura pura (Say) is green in Alachua County, but the southern Florida subspecies A. p. mosieri Cockerell is blue or even purple in the Keys (Mitchell 1960; Pascarella 2008). Likewise, Augochloropsis anonyma (Cockerell) is green in the northern part of the state and blue or purple farther south (Pascarella 2008). Ceratina dupla dupla and Lasioglossum tegulare north of Florida are dark green, whereas in Florida C. d. floridana is blue (Michell 1962) and L. puteulanum is blue-black (Gibbs 2009, 2010). In Alachua County, species such as Stelis lousiae Cockerell and Anthidiellum notatum (Latreille) have maculae that include more red than in bees north of Florida, in which the maculae are almost entirely yellow. However, they are not as extensively red as bees farther south in Archbold Biological Station where the red mimicry pattern characteristic of southern Florida Hymenoptera is particularly well developed (Mitchell 1962; Deyrup & Eisner 2003).

This study has provided basic knowledge about Florida's bee fauna, thereby contributing to the documentation of the state's biodiversity. Furthermore, discoveries were made regarding bee distribution, taxonomy, and life history, including habitat, floral, and host-parasite associations. Thus, these findings are an example of how such inventories contribute to our understanding of basic bee biology at several levels, and provide information that can inform management for these pollinators, both locally and throughout their range.