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1 June 2015 The Potential Management of a Ground-Nesting, Solitary Bee: Anthophora abrupta (Hymenoptera: Apidae)
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Abstract

In Apr 2010, Anthophora abrupta (Say) (Hymenoptera: Apidae) was discovered nesting in open bags of colloidal clay in Gainesville, Florida, USA, in an open-air shed. Label data from A. abrupta specimens in the Hymenoptera holdings of the Florida State Collection of Arthropods indicated that no specimen had been collected previously from Alachua County and that the most recent Floridian specimen was collected in 1987. This suggests that A. abrupta may be locally rare and possibly in decline or threatened regionally. Many of the plants that A. abrupta is reported to visit are listed as threatened or endangered in 1 or more states. In an effort to study the potential management and conservation of this species, the original nest aggregation was split in 2012 and 2013, and the splits were moved to new nest sites to see if they would establish at the new sites. Both mother and daughter nest aggregations were monitored in Spring of 2012–2014. Herein, a brief review of A. abrupta natural history, an account of the attempts to split the aggregations for new nest establishment, and suggestions for the potential management of this beneficial insect are discussed.

Anthophora abrupta Say (Hymenoptera: Apidae), also called the chimney or miner bee, nests gregariously in clay or adobe substrate in the eastern half of the U.S. (Graham et al. 2013). A female A. abrupta digs a tunnel for her nest and uses the excavated earth to sculpt a chimney-like turret around the nest entrance. Each turret corresponds to a single nest (Frison 1922; Norden 1984). The neighboring nests are clustered together in such a way that at first glance the bee activity resembles that of a social bee colony. However, the chimney bees exhibit no generational overlap and each female builds and provisions only her own nest for the benefit of her own offspring (Rau 1929; Norden 1984).

Male and female A. abrupta visit a variety of flowers to collect pollen, nectar, or other plant compounds. Mating occurs on flowers. After mating, the female begins nesting, usually in the same location from which she emerged (Frison 1922). The later-emerging females nest in a clumped distribution around the early-emerging females' nests (Norden 1984).

Mated female A. abrupta collect water to soften the hard-packed clay and begin excavating a tunnel (Rau 1929). The clay removed from the tunnel is built up around the entrance, creating a chimney-like turret. The turrets are smooth on the interior, rough exteriorly, oriented in various directions with no obvious pattern, have a characteristic dorsal slit on the ceiling, and average approximately 8 cm in length (Frison 1922; Norden 1984). There have been many suggestions for the purpose of the turrets including: (1) protection from rain, nearby excavations, windblown debris, or parasites; (2) functioning as a landmark for nest recognition; (3) providing a social significance for the nest aggregation; or (4) serving a thermoregulatory function for the nest (North & Lillywhite 1980; Brooks 1983; Norden 1984).

After turret construction concludes, the female finishes excavating the tunnel and begins constructing the cells. The completed tunnels average about 11 cm in length and contain around seven urn-shaped cells that are excavated into the sidewalls of the tunnel (Frison 1922; Norden 1984). The females waterproof the tunnel and cells using a glandular secretion excreted from their Dufour's gland (Norden 1984). The cells are provisioned by the female with pollen and nectar that they collect from several plants and mix with more secretions from the Dufour's gland (Norden et al. 1980). The female oviposits a single egg onto the pollen mixture, seals the cell with a clay capping, and proceeds to provision a new cell (Frison 1922). The female plugs the tunnel entrance with clay once all cells are provisioned with food and an egg (Rau 1929; Norden 1984).

The eggs hatch after about 5 d (Frison 1922; Norden 1984). The larvae develop over the next 3 wk, all while consuming the food pellet and much of the cell lining (Norden 1984). Fourth instar larvae transform into prepupae without molting. They remain prepupae for about 9.5 mo, with their head capsule oriented below the cell capping (Norden 1984). The bees shed their pupal skin at the end of the pupation period, darken for about 2.5 wk, and emerge from their burrows to begin life as adult bees (Frison 1922; Norden 1984).

The current project is an attempt to determine if A. abrupta from an identified nesting site will: 1) nest in containers of clay provided close to their original nests; 2) survive being transported as nest splits to a new location and emerge the following year; and 3) nest in clay provided at their new nest location. Furthermore, A. abrupta distribution in Florida and elsewhere is discussed based on a review of the A. abrupa collection at the Florida State Collection of Arthropods (FSCA), Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Florida, USA, and a review of the literature. Next, plant visitation habits of A. abrupta are considered. This is followed by a discussion of conservation efforts for A. abrupta, of its potential use as a provider of crop pollination services, and of ways to promote educational awareness for native bees. We conclude with suggestions for the future management of A. abrupta.

Materials and Methods

In 2010, A. abrupta was discovered nesting in Gainesville, Florida, USA (29°40′45″N, 82°22′2″W), in an open air shed, in horizontally oriented open, weathered bags of loose, colloidal clay and soft rock phosphate (Fig. 1). The nesting site was investigated in Apr 2010 and an adult bee specimen was collected for identification. The A. abrupta collection in the Hymenoptera holdings of the Museum of Entomology of the FSCA was examined to understand better the local and national distribution of this bee. According to these collection data, the most recent specimen of A. abrupta in Florida was collected in 1987. Furthermore, there are no records of A. abrupta specimens being collected from Alachua County (Table 1).

Observations of the A. abrupta nest continued in Apr, May, and Jun in 2010. Adults were seen only rarely in mid Jun 2010. After Jun 28, adults were not observed until the following Spring. The observations of the 1st season led to the hypothesis that A. abrupta adults emerging from the existing nest in Spring 2011 would excavate and provision nests in nearby clay if it was provided in portable containers. By using the containers, the nests could be dispersed to seed new areas. With only 1 nesting aggregation of locally rare A. abrupta identified for use, attempts at augmenting the population carried the risk of causing unintended harm to the very population being studied. However, a small split was taken carefully from the original (mother) aggregation and used to seed a new area (daughter nest aggregation).

Fig. 1.

The original (mother) nest aggregation of Anthophora abrupta discovered in Apr 2010. The bees were nesting in colloidal clay, in an open air shed, in Gainesville, Florida. Photo: Jason R. Graham.

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Artificial nest material was created in order to encourage the bees to nest in portable containers. Naturally occurring, unacidulated, soft rock phosphate colloidal clay (Manko, Co., Dunnellon, Florida, USA) was mixed with water in plastic storage bins (17.9 L). The mix was allowed to set and dry for 6 mo with excess moisture poured off as needed. After the clay had hardened, about 20 “starter holes” (9.5 mm ID, 2.5 cm deep) were drilled into the face of each of the clay blocks. The dry clay blocks, contained in the plastic storage bins, were placed around the periphery of the existing, dormant mother nest aggregation in Apr 2011. These artificial nesting sites were positioned horizontally (n = 3) and vertically (n = 6). Loose clay also was provided horizontally (n = 3) in containers.

In Mar 2012, a split was made from the mother nest aggregation at a time when the larvae were known to have grown large enough and to have consumed enough food to avoid their drowning in the liquid diet when moved (Frison 1922; Norden 1984). This same day, 3 male bees were observed emerging from the original aggregation. Splitting the original mother aggregation consisted of carefully removing about one-eighth of the original mother nest aggregation and removing 2 of the clay blocks that had been prepared in containers and in which some bees nested the previous year. This material was transported to the University of Florida Bee Biology Unit, Gainesville, FL, USA (29°37′63″N, 82°21′41″) and placed under an open-air shed, on a large metal tray filled with clay premixed as before (Fig. 2). This daughter aggregation (daughter 1) was positioned on a workspace approximately 1 m above the ground.

In Mar 2014, another split was made from the mother aggregation. This split (daughter 2) was moved to High Springs, Florida, USA (29°47′43″N, 82°36′20″W), placed under an open-air shed, and supplemented with unprocessed blocks of clay that had been obtained from the mine site (Fig. 3).

Nesting activity was observed and recorded at each site when the bees began emerging from nests the weeks of Apr 5, 2012; Apr 25, 2013, and Apr 26, 2014. The activity levels were monitored as frequently as possible at each site using hand-held push button counters to record each time a bee returned to a nest entrance. These observations were taken at various times of the day, and for various lengths of time. The flight data were standardized as the average number of bees returning to the nesting site per minute in order to compare activity between sites (Fig. 4).

Table 1.

The distribution and seasonality of Anthophora abrupta according to data from the Florida State Collections of Arthropods (FSCA, Florida Department of Agriculture and Consumer Services, Division of Plant Industry) and found in the literature.

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Results

The bees at the original mother site did not use any of the 3 containers housing loose colloidal clay and positioned horizontally. On the other hand, 4 of the 6 hardened clay blocks positioned vertically in containers were observed to have nesting activity in Apr 2011. In 2012, 2 blocks in which bees successfully nested at the original mother site were transported to the Bee Biology Unit along with all of the unused loose and hardened clay from the 2 horizontally oriented containers. In 2013, nesting at the 1st daughter site was observed in all of the hardened blocks that had been provided to the mother nest aggregation but not used in 2011. Nesting continued and spread at the mother nest aggregation into an additional 5 horizontally oriented containers filled with hardened clay as before. Nesting continued in hardened clay that was provided to both the mother and daughter nest aggregations after the split was made. The 1st split was a success as both mother and 1st daughter nest aggregations survived the split and were active in 2013, the season following the split (Fig. 4).

On Apr 5, 2012 the first adult bees, 15 male A. abrupta, were observed emerging from the 1st daughter aggregation of nests. Female A. abrupta were seen inspecting holes at the daughter nest aggregation on Apr 10, 2012 and actively building nests on Apr 11, 2012. The first pollen observed being brought back by foraging females at the daughter nest aggregation was on Apr 14, 2012. Three male bees were observed emerging from the nesting material at the mother nest aggregation on Mar 30, 2012, and nesting females were observed on Apr 10, 2012. Nesting continued at the daughter site until May 7, 2012 and at the mother site until May 11, 2012, after which no adult bees were seen until the following spring.

In Apr 2013, the nest sites were checked daily for the anticipated emergence of the adult A. abrupta. On Apr 20, 2013 a crackling sound was heard coming from the clay nesting material at the mother nest aggregation. Upon inspection, the sound was heard at the 1st daughter nest aggregation the following day. On Apr 25, 2013, the first male adults were seen emerging from the daughter site, and the first adults were observed on Apr 27, 2013 at the mother site. Nesting continued until May 20, 2013 at the 1st daughter site and May 26, 2013 at the mother site, after which adult bees were not seen at either nest site for the rest of the season.

Fig. 2.

The 1st daughter nesting aggregation of Anthophora abrupta established 10.3 km from the original nest site in Gainesville, Florida. It was created as a split from the mother nesting aggregation in Mar 2012. Photo: Jason R. Graham.

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In Apr 2014, the nest aggregations were observed in anticipation of emerging adult A. abrupta. At the mother nest aggregation, on Apr 21, a faint crackling sound in the clay was noted, and adult A. abrupta bees were observed emerging at the mother site on Apr 26, 2014. At the 1st daughter site, the adults were seen emerging on Apr 28, 2014. Adults were not observed emerging at the 2nd daughter site until Apr 30, 2014. Nesting by A. abrupta continued at the mother site and 1st daughter nest sites until Jun 10 and Jun 9 2014, respectively. The last recorded A. abrupta activity at the 2nd daughter nest site was May 20, 2014.

Fig. 3.

A 2nd daughter nesting aggregation of Anthophora abrupta established 35.7 km from the original nest site in Gainesville, Florida. It was created as a split from the mother nesting aggregation in Mar 2014. Photo: Amanda M. Ellis.

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The activity levels at the mother and both daughter nest aggregations followed similar patterns each year (Fig. 4), although the mother nest aggregation was more active each year than was either daughter nest aggregation. Both the mother and the 1st daughter nest aggregations peaked in activity in late Apr in 2012 and 2013 (Fig. 4). In 2014, the activity at the daughter nest aggregations peaked in early May whereas the activity at the mother nest aggregation peaked in late May (Fig. 4).

Discussion

In this study, A. abrupta from an identified nesting site were shown to: 1) nest in containers of clay provided close to their original nests; 2) survive being transported as dormant nest splits to a new location and to emerge the following year; and 3) nest in clay provided at their new nest location.

SUCCESSFUL ESTABLISHMENT OF NEW NESTING SITES

Our observations at the daughter nest aggregations suggest that we were able to establish 2 new nest aggregations of chimney bees successfully. Flight activity at the daughter nest sites was lower than that at the mother nest site. However, this gradually increased in the 1st daughter nest aggregation to reach that of the mother nest aggregation by the 3rd year after the establishment of the 1st daughter nest aggregation. The 2nd daughter nest aggregation had comparable activity levels in 2014, its first season post establishment, to that of the 1st daughter nest aggregation in 2012, its first season post establishment. The activity of each nest aggregation increased yearly.

Fig. 4.

Bee activity as indicated by the average number of Anthophora abrupta returning to the nesting site per minute at the mother and daughter nesting aggregations in 2012, 2013, and 2014. The error bars indicate standard error.

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Nest sites of A. abrupta have been observed persisting in the same location for over 50 yr (Norden 1984), and nest sites have been estimated as having as many as 5,000 brood cells (Frison 1922). If the 3 nesting aggregations observed in this study continue to grow, each could provide additional splits, thus producing more colonies for future, involved studies of this bee species.

CHARACTERISTICS FAVORING MANAGEMENT

Other Anthophora species are managed commercially around the world. In Germany, A. pilipes acervorum, which has a nearly identical life history to the closely related A. abrupta, is managed commercially as a pollinator of orchard crops (Thalmann & Dorn 1990; Thalmann 1991) as reported by Batra (1997). The closely related subspecies A. p. villosula was imported from Japan, where it is considered a superior pollinator of blueberries (Maeta et al. 1990), and was tested as a potential pollinator of blueberries in Beltsville, Maryland (Batra 1994, 1997), and Maine (Stubbs & Drummond 1999), USA. In both cases, A. p. villosula was considered an excellent candidate for commercial management as a provider of crop pollination services. However, the concern that mass importation and rearing could impact closely related native species negatively apparently hindered the commercialization of A.p. villosula in North America (Batra 1997; Stubbs & Drummond 1999).

Anthophora abrupta is native to North America and exhibits several characteristics that support its potential for management. First, they tend to nest where they emerge as adults (termed “philopatry,” see Cane 1997), even after they have been moved prior to emerging, provided that they have the requisite materials in which to nest, as demonstrated in this study. Nest sites of A. abrupta have been observed persisting in the same location for over 50 yr (Norden 1984). Second, female A. abrupta, although endowed with a sting, do not defend their nests by stinging (Frison 1922) and apparently are unable to sting humans (Norden 1984). This makes them a good candidate to use because the threat of stings is minimal. Third, A. abrupta will feed readily on a honey-water solution in captivity as an artificial diet (Frison 1922). Fourth, adults of A. abrupta have emerged successfully under laboratory conditions from collected pupae (Frison 1922; Norden 1984), suggesting the possibility for population augmentation using rearing programs. Fifth, A. abrupta has a flight range of up to 3.2 km (Batra 1997), thus making these bees able to pollinate large areas. Sixth, male and female A. abrupta visit a variety of flowers, foraging in light rain and in temperatures of 11–39 °C (Rau 1929; Norden 1984). Finally, mature nest sites found in the wild have been estimated conservatively to contain as many as 5,000 cells based on nest dissections from a portion of the sites (Frison 1922). These characteristics make A. abrupta a good candidate for use as a managed pollinator.

MANAGEMENT CONSIDERATIONS

Nest Characteristics

Anthophora abrupta nests have been found on cliff banks (Rau 1929), on clay adobe walls (Norden 1984), on clay banks at the edge of creeks and rivers (Frison 1922), and often under a protective overhang such as a bridge or tree (Frison 1922; Rau 1929). The 3 requisites, a patch of hardened clay, shelter from the rain, and close proximity to a water source, were found at the mother nesting aggregation in Gainesville, Florida, USA. Frison (1922) noted that A. abrupta prefers perpendicular or steeply inclined surfaces in which to nest, a finding supported by the data presented herein.The adobe walls in which Norden (1984) observed A. abrupta nesting had a pH of 6.0 and were composed predominantly of clay and mica. Cane (1991) surveyed and compared nest characteristics and other variables associated with 32 species of ground-nesting bees and reported the soil of an A. abrupta nest from Alabama to be a sandy clay loam (29.5% clay, 11.9% silt, 58.6% sand). Analysis of the nest material used in the present study indicated that the soil at both the mother and daughter site was clay (58.6% clay, 27.1% silt, 14.2% sand) with a pH of 6.7.

Protecting Nests

Birds, lizards (at the mother site), and squirrels (at the 1st daughter site) damaged portions of nests. Consequently, the nest aggregations were protected from additional bird or mammal predation by using galvanized steel chicken wire having 5 cm hexagonal gaps and 19-gauge (1 mm) wire. The first few foraging bees that encountered the newly installed chicken wire seemed to hesitate before flying through it. However, all flying bees navigated through the chicken wire with apparent ease shortly thereafter. There was no further observed predation or destruction of the nesting material, until 2014, when at the mother site, broad-headed skinks (Plestiodon laticeps (Schneider); Squamata: Scincidae) were observed preying on adult A. abrupta on multiple occasions from inside the chicken wire. It is unclear what level of predation these A. abrupta populations can tolerate, or if the exclusion of predators is necessary for the success of the nest aggregation.

Mating System

Norden & Batra (1985) studied groups of male chimney bees chewing parsnip (Pastinaca sativa L.; Apiales: Apiaceae) tissue. The fragrant plant liquids are absorbed into the male bees' labral hairs and reportedly are mixed with mandibular gland secretions. Males then use these compounds to attract females by marking mating areas with these volatile components (Norden & Batra 1985; Lee 1998). In Missouri, USA, Rau (1929) observed males biting rambler roses (perhaps to collect oils) and eating rust from several metal objects, a behavior that may or may not be important to the mating system.

VALUE OF MANAGEMENT

Most of the literature about this organism comes from researchers who found A. abrupta nest aggregations in the wild (Frison 1922; Rau 1929, 1930) or on the property of a concerned homeowner (Norden et al. 1980; Norden & Scarborough 1982; Norden 1984; Norden & Batra 1985; Giblin-Davis et al. 1993; Lee 1998; current study). Management of A. abrupta colonies could provide future native bee researchers with a consistent population with which to investigate life history parameters, catalogue nest commensals, conduct pollination studies, and more.

There is also an educational value to managing A. abrupta that can be extended to the general public. Like most solitary bees, A. abrupta is not defensive of its nests and does not sting readily, if at all. When roughly handled, these bees are reported to defend themselves by biting but are otherwise docile and typically should not be considered a threat (Frison 1922; Rau 1929; Norden 1984). The bees are not timid around humans, so the interested observer can watch as the turrets multiply and the bees stock their burrows with pollen and nectar. Managed colonies located in public parks, zoos, and botanical gardens can be used to teach the general public a variety of concepts such as the development of sociality in hymenopterans, animal architecture, native bee diversity, and the ecological service of pollination. Due to their docile nature and ecological importance, solitary bees make excellent model organisms for citizen science projects (Graham et al. 2014). Interaction with A. abrupta could reduce the innate fear of bees as stinging insects and replace this emotion with a healthy respect for and appreciation of bees as beneficial organisms.

The value of A. abrupta as pollinators can be demonstrated by the diversity of flowers that they visit. A summary of the plants which A. abrupta has been recorded to visit is provided in Table 2. Plant species that are listed as threatened or endangered in 1 or more states (USDA, NRCS 2013) are indicated as such under the column heading “Conservation Need.” Of the 59 plants that A. abrupta has been reported visiting, 26 plants (44%) are listed in 1 or more states as endangered or threatened (USDA, NRCS 2013). Parallel declines between plants and their pollinators emphasize the importance of pollinator conservation for ecological health (Buchmann & Nabhan 1996; Biesmeijer et al. 2006). Also shown on Table 2, among plants visited by A. abrupta are several fruit, vegetable, and forage plants such as asparagus, blackberry, clover, cranberry, parsnip, persimmon, raspberry, and tomato. This suggests that A. abrupta may be helpful for the pollination of agricultural crops. The wide variety of plants on this list, representing 28 different families, indicates that A. abrupta is a generalist forager.

The natural population of A. abrupta appears limited in Florida, and further study should focus on the health and population dynamics of this species throughout the native range of eastern North America. In Florida, these bees are represented in the FSCA from Columbia, Franklin, Gulf, Lee, Liberty, Nassau, and Osceola Counties, although the collected specimens date to the 1930s, 1960s, 1970s, and 1980s (Table 1). Although this lack of specimens may be due in part to collector biases, A. abrupta also has not been reported in any of the major bee surveys that have been conducted in Florida (Graenicher 1927, 1928, 1930; Krombein 1967; Pascarella et al. 1999; Deyrup et al. 2002; Serrano 2006; Deyrup 2011; Hall & Ascher 2011, 2012) except for the web resource “Bees of Florida” that lists A. abrupta from Lee and Liberty Counties (Pascarella & Hall 2013). There were no A. abrupta specimens collected in Florida present in the FSCA collection more recently than 1987 and none present in the FSCA collection from the rest of the country after 1994 (Table 1). Correspondence with the curators at The Stuart M. Fullerton Collection of Arthropods at the University of Central Florida (UCF) and the Archbold Biological Station Reference Collection (ABS), confirmed an absence of A. abrupta from both collections (Stuart M. Fullerton (UCF) and Mark Deyrup (ABS), personal communication). Between 2006 and 2014, there were 74 specimens of A. abrupta reported to the United States Geological Survey (USGS) Patuxent Wildlife Research Center in Beltsville, Maryland, USA, from: Delaware (1), Georgia (3), Maryland (47), Michigan (10), Virginia (2), and West Virginia (11) (Sam Droege (USGS), personal communication). Other entomology reference collections around the state and country should be evaluated to see if a decline in curated specimens is a regional or nationwide trend. If A. abrupta populations are in decline, then conservation management techniques such as those presented here should be applied to avoid losing this bee as a natural resource.

The agricultural sector and food security are primarily dependent on the pollination services provided by the European honey bee (Apis mellifera L.). Alternative pollinators are needed to support the U.S. agricultural industry and reduce overdependence on a single species. Most bee species in the U.S. are solitary, ground-nesting bees (Michener 2007), and ground-nesting bees continue to be underutilized as managed pollinators for agriculture (Cane 1997). Through development of management techniques for A. abrupta, challenges may be overcome that will accelerate our ability to manage additional species of ground-nesting bees.

Table 2.

A summary of plants that Anthophora abrupta has been reported to visit. This list should not be considered all-inclusive, as this bee seems to be a polylectic flower generalist. The “conservation need” column indicates plants that have been listed as of special concern, threatened, and/or endangered in 1 or more states (USDA, NRCS, 2013).

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Acknowledgments

We thank Katie Buckley and Glenn Hall for their assistance in the field and valuable insight. We thank Amanda Ellis, Analy Ellis, Evelyn Grace Ellis, Jude Ellis, Mathias Ellis, Felix Graham, Emily Helton, Jeanette Klopchin, Cory Stanley-Stahr, Qin Tan, and Anthony Vaudo for their help with artificial nest construction and monitoring efforts. We are thankful for the support by Mark Deyrup, Sam Droege, Stuart M. Fullerton, and Jim Wiley and for their respective assistance with the Archbold Biological Station Reference Collection, the USGS Patuxent Wildlife Research Center, The Stuart M. Fullerton Collection of Arthropods at the University of Central Florida, and the Florida State Collection of Arthropods.

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Jason R. Graham, Everett Willcox, and James D. Ellis "The Potential Management of a Ground-Nesting, Solitary Bee: Anthophora abrupta (Hymenoptera: Apidae)," Florida Entomologist 98(2), 528-535, (1 June 2015). https://doi.org/10.1653/024.098.0220
Published: 1 June 2015
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