Anthrophora pilipes villosula sm. (Hymenoptera: Anthrophoridae), a manageable Japanese bee that visits blueberries, and apples during coll, rainy, spring weather

22 Pages·1994·7.7 MB·

by  S W T Batra

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