PROC. ENTOMOL. SOC. WASH. 96(1). 1994, pp. 98-119 ANTHOPHORA PILIPES VILLOSULA SM. (HYMENOPTEIL\: ANTHOPHORIDAE), A MANAGEABLE JAPANESE BEE THAT VISITS BLUEBERRIES AND APPLES DURING COOL, RAINY, SPRING WEATHER Suzanne W. T. Batra Bee Research Laboraton. ARS. U.S. Department ofAgriculture, Bldg. 476, Beltsville, Mar>land 20705. Abstract.—Jht vernal, univoltine solitar\ Japanese bee, Anthophora pilipes villosula, promises to be a worthy addition to our pollinator fauna. It was easily maintained in inexpensive, portable adobe blocks. It is gentle, forages during inclement weather, also from before dawn until after dusk in fine weather. It is polylectic, does not steal nectar, flies rapidly, forages to 500 m, visits numerous flowers including blueberry and apple, and sonicates. Its active period coincides well with spring fruit blossom in the temperate zone. Females may make several nests, learning new nest locations. Dormant nests in adobe blocks were kept outdoors through five years in Maryland with minimal insulation, and the population approximately tripled each year. Details are provided regarding its behavior in Japan and Maryland, including phenology in relation to crops, wild plants and other bees, hosts, foraging beha\ior, effects ofweather, management, substrate and nesting behavior, territorial behavior ofmales and mating. Key Words: Pollination, bee, apple, blueberry, bionomics, management, Japan, U.S.A. This report concerns the biology ofa dy- cranberries, tomatoes, potatoes, eggplants, namic pollinator that efficiently utilizes the peppers, cotton, okra, and many crops that abundant floral resources of spring, dis- are grown in greenhouses {Boyle and Philo- cusses its limiting environmental factors, gene 1983. Parker et al. 1987). and its potential management for the pol- Blueberries are particularly poorly polli- lination ofcrops that bloom in the spring. nated by honey bees. The short spring flow- Honey bees are versatile, manageable pol- ering season is often rainyorcool, and hon- linators for most crops, and they also pro- ey bees do not sonicate, which pollinates \ideuswith valued honeyandwax.butthey blueberry flowers efficiently. Because pop- are not the best pollinating species for all ulations of the well-adapted and effective crops, under all conditions. For example, native blueberry pollinators are often low. they do not perform as well as bumble bees due to habitat destruction and pesticides, and some solitary bees in cool or rainy growers may saturate their blueberry fields weather. Theyflyrelatively slowly,andthey with honey bees in order to achieve ade- have morphological limitations or behav- quate pollination. Nevertheless, rainy iors that makethem lessefficient than some weathermaypreventthesehoneybeesfrom other bee species as pollinators of certain foraging. crops, including alfalfa, red clover. 'Deli- Doubts about the effectiveness of honey cious" apples, blueberries, huckleberries. bees arose early during the development of VOLUME 96, NUMBER 1 99 blueberries as a cultivated crop. Shaw et al. thoracic flight muscles without fanning her (1939) madedetailed field observationsand wings, producing a distinct buzz. Certain performed controlled pollination trials in speciesthatarecapableofsonication belong cagesduringthreeyears. Theserevealed that to several genera, including Colletes, An- bumble bees were the most abundant pol- drena. Melilta, Augochloropsis, Xylocopa, hnators, and that individual bumble bees Bomhiis. Amegilla, Tetrapedia, Habropoda. were three times more efficient as pollina- Anthophora. and some other anthophorids. tors than individual honey bees. Subse- Bumble bees have been artificially reared quent studies have confirmed the superior for many years, but no method provides a efficacy of bumble bees. Now their popu- largenumberofforagersearlyinspringwhen lationshavedeclinedin manyareas(Bigras- bees are most needed for blueberr\ polli- Huot et al. 1973, Finnamore and Neary nation. New bumblebee mass-rearingtech- 1978, Plowright and Laverty 1987 and ref- niques may ameliorate this shortage even- erences therein). tually(PlowrightandLaverty 1987). Colletes The flowers of blueberries (highbush, validiis Cresson is a native solitary bee that lowbush, rabbiteye, and others in the sec- specializeson blueberriesand sonicatestheir tion Cyanoccocus) have pendant, inverted, flowers. Pheromones may be used to assist globosetourceolatecorollas. Aflower'snec- relocation of their nest sites, but more re- tariesandanthersareaccessibleonlythrough search is needed (Batra 1980). Torchio a small ventral hole. This structure requires (1990) found that the native megachilid, pollinators to hang upside-down while Osmia hbifloris biedermannii Michener is probing into the hole. The poricidally-de- a good blueberry pollinator, and it is poten- hiscent anthers do not readily release their tially manageable. Cane and Payne (1988, pollen. Bees use three methods to obtain 1990) found that the "southeastern blue- nectar, pollen, or both, from these flowers: berrybee," a nativeanthophorid, Habropo- 1. Nectar-robbers cut slits at the top ofthe da labonosa (F.), is an excellent sonicating corolla, through which they sip from the pollinator of rabbiteye blueberries in the nectaries, but these do not accomplish any southern states. Techniques to manage its pollination,becauseanthersandstigmasare populations are needed. Because the timing not contacted. Carpenter bees (Xylocopa oftheadult activityofthisspeciescoincides spp.) usually make these slits, but honey with blueberry bloom and they have little bees, bumble bees and Andrena bees soon need for other floral resources, these bees learn to use them. The widespread use of are superior to bumble bees for blueberry robber slits by honey bees may have been pollination. Their relatively short foraging responsible for recent poorblueberry yields range is beneficial because they stay in the in Florida (Morse 1991). 2. Pollen-grabbers blueberry fields. Further research concern- reach into the ventral pores with their man- ing the conservation, enhancement, and dibles and front legs, to bite the anthers, movementoflargepopulationsofthesethree loosen the pollen, and rake it out, while im- solitary blueberry pollinatingspecies would bibing the nectar. This method is used by be beneficial. many species ofandrenids, halictids, mega- Anthophorapilipes villosula forbrevity is chilids, and honey bees. Some pollination referred to as A. pilipes in this report. This isaccomplished, but thesebees usually work follows the revision by Day (1979), al- slowly. 3. The most efficient technique to though in Europe it is often named A. ac- loosen, collect, and transfer the pollen is ervorum (L.), a synonym. In Sasayama, Hy- buzz-pollination or sonication. A foraging ogo Prefecture, Japan, it is polylectic and bee,afteralighting, positionstheventral side visits a wide variety ofhosts from April to ofher thorax over the pore and shivers her June, including species oiAstragalus. Wis- 100 PROCEEDINGS OFTHE ENTOMOLOGICALSOCIETY OF WASHINGTON tarla. Corydalis, Eleagmis, Viola, Rhodo- adobe walls, and he made detailed obser- dendron. Glechoma, Ajuga, Lamium, Bras- vationsofnestsconstructed in adobeblocks. sica. Rosa. Potentilia. Chaenomeles. Rubiis. Van Lith (1947) found them nesting as a Taraxicum. Weigela. Abelia. Ranunculus, perennial aggregation in dry, sandyclaysoil Xanthoxyluniand A/ar(K(Miyamoto 1958, beneath a verandah. The nearly vertical 1960, 1962). In the temperate forest at Ki- broodcellswereinseriesandtheywerelined bune, near Kyoto, Inoue et al. (1990) found with a thick, whitish-gray waxy substance. it on Corydalis. and Kakutani et al. (1990) Cellswerehalf-fullofprovisionsbearingeggs found it visiting Rhododendron. Lonicera or young larvae in early May. Pupation be- and Viburnum in Kyoto. Murakimi and Iti- gan by July, and young diapausing adults no 990)foundthatA.pilipespreferentially appeared in September. The inquiline, Me- (1 visited Astragalus early in the morning and lecta punctata (F.) was present. The pun- lateintheafternoon,whentheflowersyield- gent, rancid odor noted by Fabre (1920) ed the most abundant nectar. In Europe. probably is that of butyric acid, which is Anthophorapilipes forages on 93 species of liberated from triglycerides in the provision plants, fromtheendofApriluntilearlyJune; and the cell lining, probably secreted by the Lamiumspp. are preferredhosts(Malyshev abdominal Dufour's gland, as in other An- 1928, Thalmann and Dom 1990, Westrich thophora bees (Norden et al. 1980). 1990). Recently, Thalmann (1991) and Thal- The nesting behavior of.-1. pilipes in Ja- mann and Dom (1990) investigated the bi- panwasfirstinvestigatedbyTorikata(1931), ology of,-1. pilipes and its management as a who found that the oval, 10-15 cm long crop pollinator in Germany. In 1988 and brood cells formed an oblique series ofup 1989. they tested various soil textures and to four cells. Each cell was about half full moisture levels, todetermine howthey may of semiliquid provision. Parasites were aff"ect nesting success, and they developed Meloe carinus Marseul, Monodontomerus portable blocks of soil for use by growers. japonicus Ashmead. and Saproglyphus ne- They found that provisioned cells became glectus Berlese. In Hyogo Prefecture, Mi- moldy when soil moisture was high. They yamoto (1958) found .-1. pilipes nesting gre- were also favorably impressed by the po- gariously in the adobe wall ofa cottage and tential usefulnessofthisbee, whichhassuch in a dry cliff". They were active from April assets as a long glossa, long daily foraging 17 to May 17. Some females made more period (upto 18 hours), ability to workdur- than one nest, and they preferred to reoc- ing cool (8-9°C) and sunny (20.000 lux), or cupy and refurbish an abandoned old nest duringwarm(20°C)andcloudydays, aswell rather than to construct a new nest. Thus as early and late in the day, from 4:00 at some burrows contained cells that were 600 lux to 21:00 at 300 lux. Theynoted that made by more than one individual. Males it was active in spring before bumble bees slept in burrows and patrolled the nest ag- producedworkers, itspolylecty. thelongac- gregations. Astragalus sinicus L. was the tivelivesofindividual females, andthe large preferred host at this location. Togashi numbers of flowers visited for provisions (1990) noted .4. pilipes nests in the adobe (for example, 2500 Brassica flowers were wall ofan old thatched college in Ishikawa visited to make a 522-mg pollen mass). In Prefecture. Germany, adults flew from the end ofApril Anthophorapilipesalsoliveinadobewalls until earlyJune, eggs hatched 1-2 daysafter in Europe. Fabre (1920) observed theirgre- laying, larvae matured (at 400 mg) after 4 garious nests in adobe, and noted the nau- weeks, pupation occurred 70-80 days after seating odor of the bees" provisions. Ma- oviposition, and diapausing adults ap- lyshev (1928) also found A. pilipes nests in peared in September. Parasites were Mon- VOLUME NUMBER 96. 1 101 odontomerus obscurus Westwood and Me- subtropical southwestern Honshu, Japan lecta punctata. (36°N). Earlyduringmyfirst morningin this Materials and Methods house (May 15, 1988), I heard loud hums originating below the tatami floor. On in- The equipment that was used was simple vestigation, I found an aggregation ofeight and inexpensive. It included a 35 mm SLR nests ofthis bee in the adobe wall that sup- camera with macro lens, high speed film, ported the lower part ofthe western wall of stopwatch, watch, photovoltaic light meter, the house. This adobe was made of dried thermometers, insect net, quick-drying ochre clay mixed with chopped rice straw. enamel, cages, microscope, etc. The adobe Thebees' nestswerebehindsomelooseroof substrate for nesting was made ofthe local tilesthat were leaningagainst thewall. Very red marineclay. This fine-grained, acid nat- impressivewere the continuous swift flights ural clay was put into wooden, metal, or ofthis species, its willingness to fly during styrofoam boxes ofvarious sizes but small light rain, aswellas in cloudyorcool weath- enough to be portable by one person when er, and its long daily period offlight, from full ofclay. The clods were chopped, mixed before sunrise to until after sunset. I im- with water and pressed; the surface was mediately thought that this species might smoothedandallowedtodrythoroughly for be a valuable addition to our North Amer- several weeks, forming a very hard, brick- ican pollinator fauna. Its habit ofnesting in like adobe 15-20 cm deep. Before dry, 10- adobe indicated that it could be managed 15 smooth holes, ca. 1 cm diam. x 5 cm for crop pollination relatively easily. .4/;- deep, were punched into the moist adobe; thophora panetina F. has been managed in theseattractednest-seekingbees. Theadobe Europe for legume pollination; it also nests blocks were placed under rain shelters, with in adobe (Wojtowski 1964). a southerly exposure. They could be used Because it was already late in the bees' singly, or stacked to form a wall, with the flight season, which ended on May 29, it adobe face exposed. The white polystyrene was possible to make only a few observa- boxes{= insulated shippingcontainers)were tionsofforagingbehaviorinJapan. Females most satisfactory, being waterproof light- foraged for nectar and pollen on red azaleas weight, and providing them some insula- (Rhododendronsp.) in thegarden. Theyalso tion. The adobe blocks were durable and collected pollen from the pendulous white maintenance-free, remaining uncracked af- flowers ofStyraxjaponica Sieb. & Zucc, a ter 4 years, even when riddled with bees" small tree in this area. The bees hung up- nest tunnels. Gray squirrels destroyed some side-down and sonicated the Styra.x flowers adobeand bees' nestsin 1992, so protection toreleasetheirpollen.Thus, Iwasreminded during dormancy is recommended. Nests of similar pollinator behavior on blueber- were color-coded and numbered sequen- ries. There were no blueberries in the area, tially each year as they were constructed by so it was not possible to study the bee pol- the bees. linating this crop. Sugden (1986) observed bumble bee queens pollinating a North Behavior in Japan American species of Styra.x. Although he Researchonthebiologyandmanagement did not mention it, sonication probably oc- ofAnthophora pilipes villosula Smith (det. curred. Y. Maeta) began incidentally, while I was A total ofnine hours from May 15 to 29, in Japan working with other projects. I had 1988, were spent observing A. pilipes be- rented a century-old farm house in Higashi haviorinJapan. Matsue isclimatically sim- Mochida Cho, just outside Matsue, Shi- ilartocoastal Georgia (Nuttonson 1949), or mane Prefecture. This location is in humid, approximately comparable to USDA Plant 102 PROCEEDINGS OFTHE ENTOMOLOGICAL SOCIETY OF WASHINGTON Hardiness Zone 8. Vegetation in the area Establishment includes bamboos, camellias, palms, Cryp- Because their potential as manageable tomeria, kumquats, loquats, kaki, Styrax. crop pollinators is good, a permit for im- and azaleas. The nest site, which was near portation into the United States was ob- sea level in the village, was surrounded by tainedfromAPHIS,andinDecember 1988, rice fields set amid steep, densely forested Dr. Maeta shipped 109 diapausingadults in mountains. USDA cells to the Beneficial Insects Re- Foraging females began flights as early as search Laboratory at Newark, Delaware. 5:03, 15 minutes before sunrise, and they These had been collected at Sugata-Cho, remained continuously active until 19:30, Matsue. Someadultshademergedfromtheir aftersunset. Morningactivity began at 10°C, when the nest site received only 150 lux, cellsduringshipment.Thosethatlivedwere placed in gelatin capsules to resume their although the brightest part ofthe visible sky to the east registered 2000 lux. The nest diapause. Unopened cells were cracked entrances, which were covered by the roof open, to check for dead bees or parasites, tiles, received only 10 lux at dawn. In the which were destroyed in quarantine. After evenings ofcleardays, the bees ceased their microscopic inspection, all 56 diapausing activity when the brightest part of the sky adultsincapsulesorcellswerestoredat 3°C, tothewest, visibleatthenestsite, registered until April 1989. 100lux. Thegeneralappearanceoftheland- Two Saran screen cages (4 x 4 x 2 m) scape when the bees began and ended their were set up over a dense growth of wild, flights was grayish, although some bright understory lowbush and highbush blueber- colorswerestillsomewhat visibletothe hu- ries, deerberries, and huckleberries in the man eye. oak-pine forest at Beltsville. Each cage con- The femalescollected pollen from at least tained a small rain shelter over an adobe three hosts,judging from the colors oftheir block. They were set up underthe rain shel- pollen loads. They continued to forage dur- ters at ground level and facing south. The ing light rain. When the rooftiles that cov- cages contained various cut plants, includ- ered their nest entrances were removed, six ing apple, crabapple, azalea, mustard, and returningforagersbecameconfused,and re- otherflowers. Cultivatedblueberryvarieties fused to enter their newly-visible nests. growing in pots were also placed in the cag- When these tiles were replaced, they es. Water in shallow trays was provided for promptly entered nests. Evidently the tiles nesting females, but they were never seen wereimportantlandmarks,eventhoughthey to collect water. concealed and darkened the nest entrances. Duringthe eveningofApril 18, 1989, the The nests and their surroundings had a dis- cells and capsules containing bees were tinctcheesyorbutyricodor,andafewMon- placed in the cages. They were put next to odontomerus sp. were present. Captured fe- the adobe blocks, so that emerging bees males emitted a penetrating citronella-like would perform their first orientation flights odor from their mandibular glands. Ac- at these blocks, thus memorizing their lo- cording to Y. Maeta, (pers. comm.), this cations. Bees began to emerge within 15 species is active from April 8 to June 1 1 in minutes,andmostofthemimmediatelyflew ShimaneandFukuoka Prefectures. Beesthat up to the roofs of the cages. By the next nest in the adobe walls ofvillage houses are morning (April 19), many ofthe bees had tolerated by the occupants, because these adjusted to the confinement of the cages, bees are not aggressive. However, large and both sexes were foraging on cut azalea, numbers ofbee tunnels may cause the col- crabapple and narcissus. Males had begun lapse ofsuch walls. toclosely pursue females in flight, pouncing VOLUME 96, NUMBER 1 103 on them when they ahghted on flowers. appearance (males) on March 14, February Males were already attracted to the holes in 9, February 12 and February 28: Colletes the clay blocks, which they patrolled and inaequalisSaymalesfirstappearedon March inspected while hovering, although no fe- 14, March 13, March 1,andMarch 2; males maleshadyetoccupiedtheholesortheado- of the introduced Japanese pollinator Os- be blocks. By the end ofthis first day, both niia cornifrons Radoszkowski began emerg- sexes expertly and rapidly darted through ing on April 18, March 10, March 27, and smallgapsin the vegetationandtheyavoid- March 31, respectively (Fig. 1). Apples be- ed hitting the cage mesh or other objects. gan to bloom on April 20, March 28, April This facile adaptation suggested that this 9, and April 22; highbush blueberries sim- species may be suitable for use in green- ilarly began blooming April 19, March 22, houses or other confinement, where honey April8,andApril 14(Fig. 1).Theartificially bees do not thrive. delayed emergence of A. pilipes began on By April 21, after a rainy day, males and April 18 in 1989, but it began on March 15, females had begun overnight occupancy of 1990, March 26. 1991,and March 27,1992, the holes in the adobe blocks. On emerging after overwintering in a sheltered area at in the morning, they performed normal ori- ambientwintertemperatures. The first bum- entation flights. Some bees also slept in the ble bee queens were also seen on the latter open, whilegraspingtwigs orthe cage mesh two dates. The more numerous, pollinating bytheirmandibles. Thefirst femalewasseen bumble bee workers appeared a month lat- to excavate a nest burrow on April 25. It er, but by then the blueberries and apples was started in a hole in the adobe. By April had almost finished blooming. The well 27, several females were nesting in the ado- publicized blooming ofthe Japanese cherry be blocks in the cages. trees during five years at the Tidal Basin in Details regarding phenology, pollination, Washington, D.C., proved to be a reliable mating and nesting behavior during five indicator for the time of emergence of .^. years are discussed below. In 1989, emer- pilipesin nearby Maryland, which isslightly gence was somewhat delayed due to pro- coolerthanWashington.Thus, in 1990when longed refrigeration, but the data for 1990, the cherry trees bloomed earlierthan usual, 1991, 1992 and 1993 reflect the bees' nor- .4. pilipes also emerged early (Fig. 1). The mal behavior under prevailing environ- flight period and maximum abundance of mental conditions at Beltsville duringthose A. pilipes coincided well with the flowering years. A total of 339 hours were spent ob- of apples, blueberries, pears, plums, and serving.4. pilipesin Marylandbetween April cherries. Itendedsoonaftertheendofblue- 18, 1989, andJune9, 1992;a fewadditional berry bloom. By then, most females had observations were made in 1993. died, and the forest canopy had fully leafed out (Figs. 1, 2). Phenology of the Bees, Their Hosts, Males of the local native species, An- AND Their Associates in Maryland thophora abntpta Say, were just beginning In the Beltsville area, red maple (Acer ru- their annual activity after the canopy had brum L.) is a dominant species that indi- leafed out (mean emergence date for males cates the onset ofspring. It is the first major June 10; females June 15 (Norden, 1984)]. food source for bees to appear each year The active period of A. pilipes does not (Batra 1985). In 1989, 1990, 1991,and 1992, overlapsignificantlywiththisnativespecies male flowers began to bloom on February ofAnthophora and local .-1. bomboides Kir- 5, February 9, February 12, and March 5, by. There should be almost no competition respectively. Theearliestofthe solitary bees, for food, which is abundant in spring. Andrenafenningeri Viereck, made its first Parasites of native bees may transfer to 104 PRcxTrniNGs orTiir fntomoi ocicm socirn' or Washington 92 VOLIJMF. yd, NIJMDLK 1 105 Adults began emerging in spring while gan foraging about 30 minutes before sun- nocturnal frosts still regularly occurred, and rise, and continued foraging until well after there were some snowy days during their dusk. Theeveningthreshold forbeestoleave flight season. For example, in 1991, the nests on foraging trips was 70 lux, even males began to emerge on March 20, but it though the returning foragers had difficulty snowed during the following night. From locating their nests. At low light levels (600 March 26-28, both sexes were active, the lux), the bees flew hesitantly and slowly, females began nesting, and apples began to emitting a soft low-pitched buz/, and with bloom, but then it snowed several cm dur- prolonged hovering orientation. Some re- ing April 6-7. Usually bees avoided the turningbeesalightedon theclaysurfaceand frostsby retreatingtotheirburrowsand oth- then crawled into their nests; normally in er holes. When chilled, resting bees ofboth bright light, bees enter nests directly and sexes vigorously pumped their abdomens rapidly. (2/s) and visibly shivered their flight mus- Rainfall: This species foraged for nectar cles, apparently thus endothermicaliy and some pollen in the rain at 15°C' at 1600 warming themselves in preparation for lux, when other bees did not, including flight. A related species, A. pliiniipcs(Pallas) bumble bees, Osmia coniifrons. and honey has by far the highest metabolic warm-up bees. In light, steady rain ordri/zle, at 10°C, rate among 52 bee species in six families A. pilipes regularly foraged for nectar on tested; this permits them to begin flights in soaking-wet a/alea flowers. During a thun- cool weather (Stone and Willmer 1989). derstorm, which interrupted their busy af- The threshold for initial morning flight ternoon, foragers continued to leave nests activity at insulated nests in Maryland after at 190 lux beneath the lowering, dark clouds. a frosty night was 9.0°C', with clear sky at They flew straight into thedownpourbefore 3000-3500 lux visible from the nests. Pre- they apparently realized their mistake and dation by birds may occurat such low tem- promptly returned to their sheltered dry peratures, when these normally alert, active nests. Anthophora ahnipta also forages dur- bees are sluggish. In Japan, females began ing light rain (Norden 1984). Anthophora foraging before dawn on clear days at IO°C crinipcs Smith was able to locate its nests and 2000 lux. Once started, flight activity insideadark barn (Cirozdanicand Mucalica continued at air temperatures of7.0-7.5°C 1969), and I noted that A. pilipes females when bumble bees, honey bees and other that had accidentally entered my house flew bees were inactive. On April 2. 1992. both about normally in dim light. The foraging sexes swarmed back to their nests through performance of A. pilipes in rain was su- windand snow flurriesat 3.5°Cwhenclouds periorto that oflocal bumble beesand their suddenly appeared. They had been flymg activity level was similar to that of Arctic through ambient airat 7°Cto forage on sun- bumble bees, which regularly forage in light lit forbs in a 15°-17°C microclimate within rain at 100-300 lux (Lundberg 1980). The 6-15 cm ofthe soil surface. As the females Australian anthophorid bee, Anwgilla daw- aged, they became relatively less active in soni (Rayment) also forages from before cool weather, and subject to predation by sunrise until aftersunset, at temperaturesas birds. Forexample,on May 7, 1992at 1 1°C, lowas7°C,and in light rain (Houston 1991). only three foragers were seen returningwith Pollinating Behavior and Hcsts pollen duringfive minutesat mid-day. Dur- ing recent warm days, or during cool days In Maryland, A. pilipesvisitedthe follow- when they were young, there was far more inghosts(N: femalesormalestakingnectar; foraging activity. P: femalescollectingpollen): Rhododendron Light: On warm, cleardays, the bees be- spp. cv, N & P; pinxter. Rhododendron nu- 106 PROCEEDINGS OFTHE ENTOMOLOGICAL SOCIETY OFWASHINGTON dillorum (L.) Torr., N & P; apple and crab- Brassica, grew in nearby fields. .A.t the sub- applecv,N& P. 18 flowerspermin; redbud. urban location, five of nine sampled bees Cercis canadensis L., N; Biassica rapa L.. hadcollectedappleorcrabapplepollen: their N & P; Kerria japonica (L.) DC. N & P; loads contained 20%, 50%, 80%, 90% and Robiniapseudo-acacia L., N «& P (with son- 100% of this pollen. Many of these apple icalion); Lonicera tatarica L.. N & P; Lo- pollen grains and other pollens from scopae nicerafragrantissima. N; Lonicera japoni- begantogerminatewhenheldforafewhours ca. Thunb. N; Paeo)\ia cv. P; Chaenonwlcs in glass vials. Suburban bees collected pol- japonica. Lindl. N; Pulnionaria cv. N: Sar- len from at least seven hosts: individual cissus c\. N; Viola papilionacea Pursh. N: loads contained pollen from 1-4 hosts. At Taraxicuni officinale Weber. N; Dicentra the forest location, two of 17 bees included spectabilis, L. N; Ajiiga rcpians. L. N; Pieris blueberry pollen in theirmixed pollen loads. japonica, N & P (sonication); Lawiumpw- Bees visited the fields to collect crabapple piireiini L., N & P; Viburniini carlesic\. N: pollen and the distinctive orange pollen of ]'inca minor L.. N; wild Vacciniuni cor- Laniiuni purpurcuni. as well as pollen from ymbosiini L.. N. 13 flowers min and N & P four additional hosts. Foragers collecting (with sonication) 18-25 flowers min: wild nectarand pollen from apple flowersalways Vacciniuni vacillans Torr.. N & P 18-25 stood on the anthers, which is the most ef- flowers/min; and cultivated h>brid blue- fective position for pollination. berries. All hosts were legitimately visited, During a day's foraging, and during the and there was no nectar robbing. course of several days" foraging needed to Wild and cultivated Rhododendron were provision several cellsand complete a nest, preferred pollen and nectarsources forthese some individually marked bees returned polylectic bees, and males patrolled bushes with series ofpollen loads ofthe same color where females were foraging that were 300 and texture, others alternated loads ofdif- m from the nests. One individually marked ferentcolors, orbrought back pollensoftwo female regularly tlew one km roundtrip to or more colors in the same load. Foragers forageon apatch ofearly-bloomingazaleas, changed pollen sources (colors) over time, bypassing later-blooming bushes nearer to as new hosts came into bloom. Several se- the nests, which were being ^ isited b> other quential bee trips may return with pollen, females. Possibly thisbeewasexhibitingsite or foragers may alternately return with pol- fidelity, having been initially attracted by len or without it (presumably with nectar). the early bloom. Because ofthis preference. Aseach cell nearedcompletion, the foragers A. pilipes villosula may popularly be called returned without pollen, bearing liquid to "a/alea bees." In North America. Rhodo- be regurgitated and used to complete and dendron spp. are pollinated mainh by bum- sealcells. They often approached theirnests ble bee queens (Lovell and Lovell 1932). with their probosces extended. The flight range oC Anthophora abrupta is Several new cultivated blueberry varie- at least two miles (Rau 1931). ties that were being developed at Beltsville Pollen loads taken from 26 bees entering were tested during three weeks in 1989 in nests at two locations were microscopically cagestudies. Both malesand femalesreadih analyzed. At one suburban location, apples, visited the flowers for nectar, and the fe- crabapples. azaleas. Lonicera tatarica and males sonicated all \arieties to collect the various ornamentals were in full bloom. At pollen. No nectar-robbing was seen, and no the second location, highbush and lowbush holes were cut in any of the hundreds of wild blueberries in full bloom formed the caged blueberry flowers. Flowers varied understory ofa forest; crabapples and se^- greatly among varieties in shape and acces- eral floweringweeds, mcludingLantiuniand sibility to bees. Surprisingly. T-339, the va- VOLUME NUMBER 96, 1 107 riety with the narrowest ventral hole, was fromtheglossa. Anemergingmalemaytake the most attractive to A. pilipes foragers. Its up to an hourto chew through the nest seal. mm holes, 1.5-2.5 in diameter, were largely Once exposed, the young, dust-covered blocked by its stigmas. Nevertheless, for- males at first rested at their nest entrances agers pushed the stigmas aside and inserted for 2-3 minutes, then they suddenly began their long glossas into the nectaries, while to jerk their heads from side-to-side and theybuzzed loudly to releasethe pollen (the wiped their faces, antennae, and protruded buzzwasaudible from two m). They visited glossae repeatedly, using their front legs. 12-15 T-339 flowers/min. Variety G-139 These males then abruptly ceased their Converse, which had more accessible nec- grooming and left their natal nests, to per- tar, with a hole of4-5 mm, was less attrac- form spiralingorientation flights that lasted tive. The bees worked 12 of the globular 20-30 seconds. Such flights formed ever flowers of this variety per minute. Other wider, higher arcs, while the males faced varieties that foragers visited for nectarand toward their nest entrances, before disap- pollen were G-600; T-117; G-494: T-460 pearing. One male crawled out and faced (10/min);andT-256(alatebloomer). These toward his natal nest before beginning his visitation rates include the time spent flying orientation flight. Malesreturnedtothenests between widely spaced flowersand crawling after 30^0 min, where they began to patrol between clustered flowers. Foragers packed briefly (10-50 s visits), and began to chase the pollen into their scopae while probing, each other (Fig. 3), even though no females flying, or hanging from flowers. It is inter- had yet emerged. esting that this bee, which probably did not Territories: From before dawn to after coevolvewith Vacciniiim. provedtobesuch dusk, male A. pilipes jointly patrolled ter- aneffective pollinator, and that its behavior ritories that included floral hosts, such as on Styra.x was a good predictor ofsuccess. bushes up to 300 m away from nests, and Maeta et al. (1990) subsequently confirmed the area around the nests. Individual that A. pilipes is a superior pollinator for (marked) males alternated between these cultivated blueberries. sitesat different timesofday, oron different days, throughout their lives. Males occa- Behaviors of Males sionallyalighted in the sun tobask orto rest Emergence: The first male A. pilipes fora few seconds, and they stopped at flow- emerged one to ten days before the first fe- ers briefly to forage. At these times, objects males appeared; such proterandry is char- delimitingtheterritorymay bemarked with acteristic of solitary bees. The spread be- the male'sscent. No scent could bedetected tween the dates ofemergence ofmales and on the hairs of the mid and hind legs of females each year appeared to depend on maleA. pilipes, but their mandibularglands transient weather conditions. The first sign producedadistinct unidentifiedgeranial-to that the bees were about to emerge each citronellal-likeodorthatresemblesthatfrom springwas the appearance ofsmall (ca. 0.5- femaleA.pilipesmandibularglands. Vinson 2.0 mm) holes in the hard, shiny earth that andFrankie(1990)foundthatXylocopabees sealed the nest entrances throughout dor- rub volatile mesosomal gland secretion onto mancy. These pinholes remained un- their legs during territorial hovering dis- changed for several days to three weeks be- plays and apply it to vegetation; this secre- fore the nest occupants began to emerge. tion is believed to attract females and repel The males were responsible for breaking other males. Like several other species of open the nest seals. Their small mandibles Anthophora, aswellas some speciesoiCen- appear to be weaker than those of female tris, Euglossa. Xylocopa, and Megachile, bees but they softened the soil with liquid males of.4. pilipes have conspicuous tufts