The Alfalfa Leafcutting Bee, Megachile rotundata: The World's Most Intensively Managed Solitary Bee*

Abstract

The alfalfa leafcutting bee (ALCB), Megachile rotundata F. (Megachildae), was accidentally introduced into the United States by the 1940s. Nest management of this Eurasian nonsocial pollinator transformed the alfalfa seed industry in North America, tripling seed production. The most common ALCB management practice is the loose cell system, in which cocooned bees are removed from nesting cavities for cleaning and storage. Traits of ALCBs that favored their commercialization include gregarious nesting; use of leaves for lining nests; ready acceptance of affordable, mass-produced nesting materials; alfalfa pollination efficacy; and emergence synchrony with alfalfa bloom. The ALCB became a commercial success because much of its natural history was understood, targeted research was pursued, and producer ingenuity was encouraged. The ALCB presents a model system for commercializing other solitary bees and for advancing new testable hypotheses in diverse biological disciplines.

Full text

EN56CH12-PittsSinger ARI 14 October 2010 11:43
The Alfalfa Leafcutting Bee,
Megachile rotundata:The
World’s Most Intensively
Managed Solitary Bee∗
Theresa L. Pitts-Singer and James H. Cane
USDA ARS Bee Biology & Systematics Laboratory, Utah State University, Logan,
Utah 84322; email: Theresa.Pitts-Singer@ars.usda.gov, Jim.Cane@ars.usda.gov
Annu. Rev. Entomol. 2011. 56:221–37
First published online as a Review in Advance on
August 30, 2010
The Annual Review of Entomology is online at
ento.annualreviews.org
This article’s doi:
10.1146/annurev-ento-120709-144836
Copyright c
2011 by Annual Reviews.
All rights reserved
0066-4170/11/0107-0221$20.00
∗This is a work of the U.S. Government and is not
subject to copyright protection in the United
States.
Key Words
Apoidea, bivoltinism, chalkbrood, Fabaceae, pollination, Megachilidae
Abstract
The alfalfa leafcutting bee (ALCB), Megachile rotundata F.
(Megachildae), was accidentally introduced into the United States by
the 1940s. Nest management of this Eurasian nonsocial pollinator
transformed the alfalfa seed industry in North America, tripling seed
production. The most common ALCB management practice is the
loose cell system, in which cocooned bees are removed from nesting
cavities for cleaning and storage. Traits of ALCBs that favored their
commercialization include gregarious nesting; use of leaves for lining
nests; ready acceptance of affordable, mass-produced nesting materials;
alfalfa pollination efficacy; and emergence synchrony with alfalfa
bloom. The ALCB became a commercial success because much of its
natural history was understood, targeted research was pursued, and
producer ingenuity was encouraged. The ALCB presents a model
system for commercializing other solitary bees and for advancing new
testable hypotheses in diverse biological disciplines.
221
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
Alfalfa a.k.a. lucerne:
Medicago sativa L.
(Fabaceae).
Originating in
southwest Asia, the
tetraploid is now
widely naturalized in
Europe and North
America
Alfalfa leafcutting
bee (ALCB):
Megachile
(Eutricharaea)
rotundata Fab.
(Apoidea:
Megachilidae)
INTRODUCTION
Fifty-three years ago in the second volume of
the Annual Review of Entomology,George“Ned”
Bohart summarized the wild bees that polli-
nate the world’s leading forage legume, alfalfa
(Medicago sativa). He concluded that only honey
bees, although mediocre pollinators, could sat-
isfy this crop’s need for an abundant bee (7). At
that time, U.S. alfalfa seed production was shift-
ing west to California, where fields packed with
hived honey bees increased seed yields fivefold
to 450 kg ha−1. Fifteen years later, Bohart again
wrote for these pages about an unheralded new
agricultural pollinator from Eurasia, the alfalfa
leafcutting bee (ALCB) (8). Although detected
in the United States without fanfare by the
1940s (122), the ALCB revolutionized the al-
falfa seed industry, boosting yields to a remark-
able 1300 kg ha−1(95). No other solitary bee is
produced and managed so intensively, although
several species are propagated to fill regional
niche markets. What are this bee’s attributes
that have made its management uniquely suc-
cessful, but only where it and alfalfa are not na-
tive? Is ALCB management a model for other
solitary bee pollinators or, like honey beekeep-
ing, is it peculiar and unlikely to be replicated?
In reviewing the ALCB’s life history, manage-
ment, and ecological impacts, we highlight the
factors that enable successful solitary bee man-
agement for crop pollination.
TAXONOMY AND
BIOGEOGRAPHY
The bee genus Megachile is massive (ca.
1,478 described species, or one-third of all
megachilids) and cosmopolitan (76); most cut
leaf pieces to line their nests, a behavior to
which they owe their common name (76,
144). This genus is subdivided into 52 sub-
genera (76), in part reflecting their collec-
tive diverse behaviors and morphologies. The
largest subgenus, Eutricharaea, has more than
230 described species, all from the Eastern
Hemisphere (37, 76). It includes the ALCB,
which has been introduced widely (e.g., the
Americas, Australia) to pollinate alfalfa.
Fossil Megachile are unknown. However,
trace fossils have been reported periodically
for more than a century. These are leaf im-
prints that bear the characteristic semicircular
marginal notches that remain after females clip
leaf discs for nest building (see Life Cycle, be-
low). Most examples come from the Eocene
(34–55 Ma) (66); the oldest one dates to the
Paleocene (55–65 Ma) (144).
POLLINATION
Owing to its use in alfalfa, the value of the
ALCB is surpassed only by the honey bee for
pollination of field crops. For example, ALCB
use yielded 46,000 metric tons of alfalfa seed
in North America in 2004, two-thirds of world
production (80, 95). Planted worldwide for hay,
alfalfa is fed to livestock, especially dairy cows.
Alfalfa seed and resultant hay constitute one-
third of the $14 billion value ascribed to honey
bees pollinating U.S. crops (139); managed
ALCBs account for an additional 50% of alfalfa
seed production in the northwestern United
States (139) and central Canada. Paradoxically,
the ALCB remains uncommon and irrelevant
for pollinating alfalfa in its native range. It con-
stituted just 0.03% of the 8,168 wild bees taken
in 27 Hungarian alfalfa fields (78). In wild re-
gions of Spain where alfalfa is also grown, the
ALCB was absent from the 59 species sampled
(82), and even in southern France, large popu-
lations are difficult to sustain for alfalfa (126).
Bees pollinate alfalfa flowers when they trip
the staminal column, for which ALCBs are ef-
fective (29) (Figure 1). Rates of pod and seed
set reflect primarily the frequencies of tripping
(15), with lesser benefits from cross-pollination
(124). Females of the ALCB and the alkali bee
(Nomia melanderi; Halictidae) excel at pollinat-
ing alfalfa, tripping 80% of visited flowers (15),
comparable to alfalfa’s effective but unmanaged
European pollinators (23). In North America,
diverse bee species—including native Megachile
species—also pollinate alfalfa well (8, 45, 68),
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Scopa: abrushof
setae (hairs) beneath
the female bee’s
abdomen for
transporting dry pollen
but their abundances are never adequate to sat-
isfy modern seed yield expectations.
Rates and distances of alfalfa gene flow can-
not be reliably extrapolated from the flight
range of ALCBs. ALCBs readily fly more than
100 m from the nest but then forage locally in
a field, moving pollen only short distances of
about 4 m (117). Among isolated alfalfa plots or
plants, however, minor pollen-mediated gene
flow occurs over much greater distances, 8%
between plots 200 m apart (10) and 0.5% be-
tween plots 330 m apart (139).
The name alfalfa leafcutting bee belies its
moderate foraging and pollination versatility.
ALCBs have varying success in pollinating sev-
eral other North American field crops. They
are reportedly in extensive use for producing
hybrid seed of canola (Brassica napus) in western
Canada. In cage studies, they pollinated several
annual clovers well (Trifolium spp.) (72, 104),
but not vetches (Vicia spp.) (107). They polli-
nate some native legumes farmed for wildland
restoration seed (16). ALCBs pollinate the small
flowers of lowbush blueberries (Vaccinium an-
gustifolium) grown commercially in the Cana-
dian Maritimes (54) but are exposed to lethally
cold nights there during bloom (113). ALCBs
foraged at and pollinated cranberry in field
cages (19), but in open bogs they foraged lit-
tle and dispersed (69).
The ALCB can also be amenable to pol-
linating in confinement. Along with mason
bees (Osmia lignaria) and honey bees, ALCBs
are useful in cages to increase or regenerate
germplasm accessions stored at crop seed repos-
itories (21). Caged ALCBs effectively pollinated
carrot (130) and canola (116) for hybrid seed,
but they eschewed bloom of field-grown carrot
(129). Greenhouse pollination of vegetables or
fruits by ALCBs receives scant attention; they
forage readily in glasshouses (15, 70, 136) but
orient poorly under some plastic films (133).
LIFE CYCLE
Adult ALCBs naturally emerge and nest dur-
ing the hot days of summer. Females mate
once, soon after emergence, and then consume
nectar and pollen as their first eggs mature
(106); within a week females begin constructing
and provisioning cells sequentially. Like most
other Megachile species, they nest in existing
holes above ground, fashioning nest walls, par-
titions, and plugs from strips and disks of leaves
that are transported singly. Each nest cell re-
quires 14–15 leaf pieces, both for wall strips and
partition disks (58, 70) (Figure 1). They cut
these pieces using the opposing beveled edges
of their mandibles like scissors (Figure 1). At
the nest, the female thoroughly chews the edges
of each new leaf piece. The resultant sticky pulp
binds the new leaf piece to the others (136). An
ALCB can line and later cap one cell with leaf
pieces on average in 81 min (70) to 2.5 h (58).
Leaf piece dimensions and cell architecture rep-
resent precisely measurable physical manifesta-
tions of the bee’s complex behaviors (44).
A female spends from 5 to 6 h per day forag-
ing (58, 70), returning from flowers with both
dry pollen in her scopa and nectar in her crop.
The female enters the cavity headfirst to regur-
gitate her crop full of nectar. She then backs
out, turns, and backs into the nest, using her
metatarsal hair combs to sweep her abdomi-
nal scopa clean of its pollen load (32). Early
in the provisioning sequence, the female car-
ries mostly pollen (ca. 80%), but with each sub-
sequent trip, she returns with proportionally
more nectar (59, 136). On her final foraging
trip, a female invariably returns with just nec-
tar (58, 59, 70). Regurgitated atop the provision
mass, this nectar constitutes the young larva’s
largely liquid diet (136). The final provision
mass has a wet pasty consistency, weighs about
90–94 mg, and consists of 33%–36% pollen and
64%–67% nectar by weight (18, 59). It con-
tains 1.3 million pollen grains and is 47% sugar
by weight (18). Male progeny receive 17% less
provision than do females (59). Larval provision
masses of ALCBs contain diverse aerobic bac-
teria, filamentous fungi, and yeasts, but neither
their removal by irradiation (50) nor individ-
ual restoration to sterile provisions (49) affected
larval performance.
Under ideal greenhouse conditions with
abundant sweetclover (Melilotus officinalis),
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
bloom for forage, ALCB females sometimes
laid two eggs per day, and each female com-
pleted on average 57 cells with eggs over their
7–8 week life spans (71). Far fewer cells result
when floral resources become limited (92, 96).
Interference between females, or excessive male
harassment of females, slows the pace of many
nesting activities and curtails reproductive out-
put, at least in cages (70, 112).
The immature ALCB develops rapidly
(Figure 1). Embryogenesis takes 2–3 days, fol-
lowed by five larval instars (136). The first in-
star is spent inside the egg chorion from which
the second instar larva hatches to begin feeding
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Banner
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Staminal
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
Facultative
bivoltinism: refers to
some progeny
emerging as a second
generation in the same
reproductive season
(136). As with A. mellifera, young ALCB lar-
vae consume a liquid diet, but they imbibe it
from a shallow trough that the larva carves atop
its provision mass (136). After 3–4 more days of
development, the larva molts to its final fifth in-
star. In just the next three days, it eats the entire
pollen provision. Few insects rival ALCB nitro-
gen and energy assimilation efficiencies (146);
moreover, only 2% of the provision is left un-
eaten. Only when the larva is done feeding
does it defecate (76). As with other megachilids
and Apis species (among other long-tongued
bees) (76), the larva then weaves a tough mul-
tilayered cocoon of secreted silk of unknown
composition.
Typical of other Megachile and many
summer-flying bees (76), the ALCB brood
overwinters as a postfeeding, diapausing larva,
the prepupa. Diapause terminates with warm-
ing conditions of late spring or early summer, or
when they are artificially incubated (see Com-
mercial Management, below). Alternatively, in-
stead of diapause, up to half of the early ALCB
summer brood completes development to yield
a second generation before late summer (48, 62,
126). This facultative bivoltinism is irreversible
(131). The cues and mechanism(s) that induce
diapause or bivoltinism are unknown, but sus-
pected factors that elicit summer emergence
include maternal and/or larval responses to long
photoperiods, excessive heat, and poor larval
nutrition, as well as maternal inheritance (57,
84, 86, 101, 127, 132).
MATING
The courtship behaviors and mating biology
of the ALCB resemble those of many soli-
tary bees (24). Male ALCBs are usually smaller
than females (83), having received smaller pro-
visions as larvae (32). Females vary more in size
than males (83), perhaps because daughters are
more likely to receive less food when forage is
sparse (92). Like most bees (111), the ALCB
is protandrous. The first adult males emerge
1–3 days before females regardless of thermal
regime (56, 109). Protandry facilitates an or-
derly exodus from a linear cavity nest whose
male cells are nearer the entrance (Figure 1),
as well as early access to receptive females.
Sib-mating within intact ALCB nests is not
reported. Confined to desktop cages, some fe-
male ALCBs mated and their spermathecae re-
ceived sperm within hours of emergence (61).
However, when newly emerged marked females
were released in the field, only one-third of re-
captured females were inseminated within 48 h;
←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure 1
Tripping alfalfa flower, alfalfa leafcutting bee (ALCB) life cycle, and ALCB field domicile. (a) Banner petal
and keel of untripped alfalfa flower. (b) Staminal column snaps upward to banner petal when tripped by a
bee. (c) The ALCB female lands on a flower and applies pressure to keel; the flower is tripped; pollen is
exposed and released. (d) Extended proboscis of ALCB female while taking nectar. (e) ALCB female always
probes flower for nectar. ( f) ALCB egg laid atop provision mass of pollen and nectar that is enveloped in leaf
pieces. ( g) First instar usually remains inside the chorion; second instar then hatches to imbibe nectar pooled
atop the provision. (h) Third and fourth instars continue feeding but do not defecate. (i) Fifth instar
consumes final portions of the provision and defecates before spinning a cocoon. ( j) In the cocoon stage, the
postfeeding late fifth instar is called a prepupa. (k) ALCB cells are arranged linearly within a nest, with
female cells made before male cells (left to right =back to front). (l) An X-radiograph of the same nest.
(k) reveals healthy diapausing prepupae, with larger females in the first (left) cells. (m) Scanning electron
micrograph of female ALCB mandibles. Beveled, chisel-like opposing mandibular edges are used to cut leaf
ovals and discs for lining nest cavities and capping individual nest cells, respectively. (Micrograph courtesy of
N. Dakota State Univ., Fargo, North Dakota.) (n) ALCB domicile aside a blooming alfalfa field. (o) Crowded
polystyrene nesting boards with thousands of ALCBs (black dots) seeking nest cavities. ( p) Close-up view of
ALCB nesting board surface showing a female completing a nest plug made of leaf discs; the face of another
female peers out from a cavity from which second-generation bees chewed through the leaf plug and have
already emerged. (Except where noted, all images are property of USDA ARS Bee Biology & Systematic
Laboratory.)
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Loose cell bee
management system:
nest cells are removed
from cavities of bees’
nesting boards and
then are separated,
cleaned, and sorted
using specialized
equipment, rather than
leaving cells within
nests in boards
all were inseminated within a week (106). Mat-
ing is commonly seen at commercial nesting
shelters (32), but its frequency at flowers is not
known, particularly for bees emerging from in-
tact natal nests at natural nesting densities. Ter-
ritoriality is not evident, but males do pounce
on perched females and other males.
ALCB males have simple genitalia (85),
and copulation for ALCBs is apparently brief
(8–10 s) (112). Copulation is preceded by
male wing flipping and accompanied by pulsed
buzzing and lateral sweeps of his antennae
(32). Males firmly grip females in a stereotypi-
cal embrace that employs distinctive forecoxal
spines and basal mandibular protrusions (147)
but without the paddle-like foretarsi of some
other Megachile species (147). Putative female
sex pheromones of ALCBs are reported among
their cuticular alkenes (88). Glandular regions
of the male’s foretarsi are pressed against the
female’s antennae during mating (147), but the
possible exudates have not been isolated or
studied for their functionality.
Males undoubtedly inseminate multiple fe-
males when they can (polygyny), as seems ubiq-
uitous with non-Apis bees (24). As for many
solitary bees (89), female ALCBs seem to be
monogamous (31) and, in confinement at least,
physically reject later suitors (61). Allozyme
markers (74) and early genetic studies us-
ing RAPD markers indicated singular pater-
nity among nestmates (6). Oogenesis can begin
without mating in ALCBs, but as is the case for
many other insects (145), eggs will not mature
unless the female eats pollen (106). Overall, the
mating biology of ALCBs seems unexceptional
for Megachile (147) and solitary bees in general.
COMMERCIAL MANAGEMENT
Several works over the decades have described
ALCB management for alfalfa seed production
(8, 28, 46, 47, 105, 119, 120). Unless otherwise
cited, most of the following information is
from comprehensive guides by Richards (105)
and Frank (28) written for alfalfa pollination
in Canada. U.S. bee managers tailor Canadian
guidelines for their climate to maximize alfalfa
seed yield. Depending on the age, quality, and
production potential of the alfalfa, growers seek
to optimize the ALCB stocking rate for pollina-
tion. Because of their higher seed yield poten-
tial, U.S. producers use more bees (100,000–
150,000 bees per hectare) than do Canadian
producers (50,000–75,000 bees per hectare)
(96). A loose cell bee management system is
most commonly practiced in North America,
consisting of four sequential phases: spring/
summer incubation, summer brood produc-
tion, fall/winter cleanup, and winter storage.
ALCB prepupae spend the winter in cold
storage (at 4◦C–5◦C for 7–10 months), usually
as cells removed from their nests (i.e., loose
cells). In the spring, nest cells bearing prepu-
pae are poured into large, shallow trays to in-
cubate at constant 30◦C and 50%–60% rela-
tive humidity for safe, synchronous, and timely
adult emergence. Emergence is timed for when
alfalfa bloom is expected to be at 25%–50%
(3, 28). Prior to bee emergence, wasp para-
sitoids emerge and must be controlled (see Par-
asitoids and Predators, below). Male ALCBs
emerge by day 17–20, and females emerge a
few days later (97). Once ∼75% of females
have emerged, bees are taken to domiciles in
blooming alfalfa fields for release from incu-
bation trays. However, if weather is unfavor-
able, alfalfa bloom is delayed, or an insecticide
application is needed for alfalfa pests, deliber-
ate cooling (15◦C–20◦C) during incubation will
slow adult emergence.
Prior to bee release, field domiciles contain-
ing nesting boards are readied. Occurring in
many shapes, sizes, and materials, domiciles can
be uniformly dispersed throughout the fields
or placed around field borders. The domicile
opening is oriented southeastward (121) so that
bees and brood are warmed by the morning sun
but shaded during the heat of the day. Nest
materials are wood or polystyrene boards con-
taining evenly spaced holes (hole length is 95–
150 mm; diameter is 5–7 mm) (32) (Figure 1).
Bees will only fly once the sun has risen and am-
bient temperature has warmed to 21◦C; flight
ceases at twilight, regardless of temperature
(65, 125).
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
Most bees immediately fly out of the opened
trays into the blooming field. However, bees
that have not eclosed that continue to develop
under field conditions emerge slowly and may
even die. Nesting begins a few days after re-
lease and continues for about 11 weeks, al-
though later activity may represent only the
second-generation bees. After bee activity sub-
sides, brood-filled nesting boards are moved
from the field to a shop or incubator for
storage.
Conscientious bee management using con-
trolled conditions during the fall is practiced
more in Canada than in the United States. Nests
are allowed to dry in boards, with some of the
larvae maturing to the prepupal stage if kept
warm enough (>15◦C); parasitoids may need
to be controlled. Bees are gradually cooled for
winter storage (about 5◦C), arresting develop-
ment. During fall and winter, bee nests are re-
moved from boards by stripping them from
grooved wooden boards or “punching” them
from polystyrene molded boards. This process
is followed by cell tumbling, breaking, and sep-
aration, which are mechanized techniques for
minimizing extraneous matter and helping to
rid the bee stock of chalkbrood (see Chalkbrood
Disease, below). During winter storage, stocks
are sampled for the percent of live progeny and
their sex ratio. Healthy, diseased, parasitized,
and other dead bees can be diagnosed from X-
radiographs of cells or manual cell dissections
(123).
ALCB management is strikingly different
from honey bee management. Migratory honey
beekeepers move hives to follow bloom, but
moving ALCB domiciles or boards disorients
most nesting females and increases dispersal.
Because ALCB adults are active for only about
two months, most ALCB care focuses on prepu-
pae in nest cells. Farmers can manage ALCBs
amid regular duties or can contract with spe-
cialists to handle all ALCB management, in the
same way farmers can rent honey bee hives.
To control A. mellifera hive pests, pesticides
are placed in direct contact with adult bees. For
ALCBs, most pests are controlled while larvae
are protected in their cells and no adults are
present (see Parasitoids and Predators, below).
Nevertheless, ALCB adults and brood may be
exposed to pesticides and fungicides applied to
the crop plant during the nesting season. Bees
may be killed or sublethally affected if toxins are
sprayed during daylight or if active residues per-
sist (1, 110). Poisoned adult bees are evidenced
by their corpses or irregular behavior, but it is
difficult to ascertain if brood succumb to toxins
that have reached them directly in their nests,
as provision contaminants, or through transo-
varial transport to eggs from mother bees after
their topical or oral exposure to active chem-
icals (79). Generally, pesticides toxic to honey
bees are toxic to ALCBs, bumble bees, and wild
bees, although LD50 levels can differ (64, 110,
134). Toxicological screening of new pesticide
formulations and classes are vital for safekeep-
ing all bees whose different life histories and
foraging behaviors may render some more sus-
ceptible than others (e.g., ALCBs handling con-
taminated leaves) (1, 79, 90, 118, 134).
CHALKBROOD DISEASE
ALCBs are attacked by disease pathogens just
like other bees (5, 52). The most common
pathogen that infects ALCB brood is the fun-
gus Ascosphaera aggregata (Ascomycete), which
causes chalkbrood (34, 35). The related A. apis
causes chalkbrood in honey bees (20), but the
two Ascosphaera species do not cross-infect. In
the 1970s, chalkbrood disease was devastating
to ALCB production; controls used today have
lessened disease impact (≤20% of U.S. brood)
(36, 98). In Canada, chalkbrood is stringently
controlled (≤2%) (28), and Canadian bees are
sold to the United States, but not vice versa.
Larval cadavers filled with A. aggregata
spores are the source of future disease. When
emerging bees are trapped in nests behind
chalkbrood cadavers, they must chew through
the cadavers and thus are dusted with fungal
spores. Spore-laden adults may then contam-
inate provisions of their own brood and also
may contaminate other bees through physi-
cal contact or by depositing spores in tun-
nels when investigating future nest cavities
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(102, 141). Although loose cell management
keeps adults from chewing through cadavers
(105), spores erupting from cadavers during cell
removal and processing may contaminate loose
cells (53). In addition, where ALCB bivoltinism
is prevalent in the United States, the spread of
chalkbrood disease is exacerbated by summer-
emerging bees that must chew through any
spore-filled siblings (140).
Canadian managers use paraformaldehyde
fumigation to kill fungal spores on loose cells,
trays, nesting boards, and any bee equipment
(35). Paraformaldehyde is not registered for this
use in the United States, so U.S. managers have
tried to cleanse nesting boards with methyl bro-
mide fumigation, heat (wood boards only), and
chlorine dips (51). New chalkbrood controls
are desired because paraformaldehyde is car-
cinogenic, methyl bromide is now banned, and
heat and chlorine treatments are difficult and
labor-intensive.
PARASITOIDS AND PREDATORS
ALCBs host many natural enemies native to
both North America and Eurasia (8, 25). For-
tunately, no pest that accompanied ALCBs
from Europe has affected North American na-
tive bees. Most knowledge of ALCB parasitism
and predation comes from managed popula-
tions. Where the ALCB has been used around
the world, the same groups of parasitoids and
predators have followed or adapted (63, 108,
126, 148).
Up to 20% of ALCB cells produced in
U.S. western states can be parasitized by wasps
(98), which are known natural enemies of other
Megachile and Osmia spp. (25, 60) in their na-
tive ranges. The prevalent parasitoids are the
European Pteromalus venustus (Pteromalidae)
(25) and the native minute Tetrastichus megachi-
lidis (Eulophidae). Also, the European Mon-
odontomerus aeneus (Torymidae) (40, 60) once,
but no longer, devastated ALCB populations.
Adult parasitoids are typically killed with
dichlorvos pest strips (73) that are placed in
storage or incubator chambers, but that do not
harm ALCBs enclosed in nest cells. Ultraviolet
lamps above liquid traps also can be effective.
During nesting, parasitoids are physically de-
terred from nests by the thick walls of artificial
cavities and by felt cloth tightly affixed to the
back of nesting boards.
Sapyga pumila (Sapygidae) is a North
American wasp that attacks native bees in sev-
eral genera and quickly adopted the ALCB as
a host (25, 60). A trap designed for this wasp
(2, 25, 135) is seldom used because S. pumila
parasitism is no longer a major concern. A trap
also exists, but is rarely used, for the checkered
flower beetle, Trichodes ornatus (Cleridae) (22,
67). Larvae of these beetles are pests during the
nesting season and while bees are stored (25).
They attack other megachilids, bees in other
families, and some wasps (67).
Less persistent or problematic parasitoids,
predators, and pests include the wasp par-
asitoids Melittobia chalybii and M. acasta
(Eulophidae) (73), six native Coelioxys species
(60), one Stelis species (cuckoo bees) (Megachil-
idae), the parasitic beetle Nemognatha lutea
(Meloidae), and the beetles Trogoderma spp.
(Dermestidae) and Tribolium spp. (Tene-
brionidae), which eat immature bees and
their provisions (25). Predators also include
yellowjacket wasps (Vespidae: Vespula spp.),
earwigs (Forficulidae: Forficula auricularia),
ants (Formicidae), birds, and rodents (25).
As with honey bees, nest and brood de-
stroyers can be problematic year-round. Un-
like honey bees, ALCB adults are present only
in summer with their brood sealed inside leafy
capsules. Thus, pests can be treated with insec-
ticides while ALCBs are protected within their
cells.
UNEXPLAINED MORTALITY
ALCB populations are difficult to sustain in
the United States, so U.S. producers import
ALCBs from Canada to supplement or com-
pletely supply their bees (95). Although all
bee stocks suffer pestilence (chalkbrood, par-
asites, and predators), unexplained mortality
occurs more often in U.S. than Canadian
populations.
Poor management may account for some
U.S. bee mortality. Compared to Canadian
228 Pitts-Singer ·Cane
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
Pollen ball: intact
pollen and nectar
provision mass
remaining at end of
the field season
samples, more U.S. ALCBs died over the win-
ter and during incubation, with most bees dying
as prepupae (97). Although optimal durations
and temperatures for winter storage and incu-
bation are reliable (56, 100, 109, 137, 138), less
is known about potential bee losses due to con-
ditions during the handling of completed nests
prior to winter storage (57, 99). The duration of
prewinter storage at the recommended temper-
ature of 16◦C can subtly affect bee survival to
adulthood (99), but effects of excessive heat for
various storage durations need study. Storage
differences may underlie the superior survival
of Canada-raised bees.
Unexplained brood mortality in the United
States includes pollen ball (at times 40%–60%
of brood), which are cells containing the pollen
and nectar provision at a time when the pro-
vision should have been consumed by a larva.
Many pollen ball cells lack eggs or larvae; oth-
ers contain collapsed eggs, dead larvae, or fungi
(93). Causes of pollen balls probably include
unsuitable microclimates and overly dense bee
populations (96, 98). Overstocked bees used in
U.S. alfalfa fields quickly drain floral resources,
suffer crowded nesting sites, and may increase
the spread of disease (41, 52). Depleted re-
sources constrain ALCB reproduction (91, 92,
96), and adults likely perish or depart crowded
sites. Often under such conditions during the
hot U.S. summers, less than half of ALCBs
released into fields are replaced through re-
production. Other suspected causes of larval
mortality include molds, viruses, other as yet
identified pathogens, and pesticides (34, 35).
Second-generation emergence in the
United States can reach 90% for the first
nests made in the season, tapering to none
for the season’s last nests (55); over an entire
season, summer emergence can total about
40% progeny loss. In contrast, summer adult
emergence in Alberta, Canada, is quite low
(e.g., <5%) (62). Reproduction by second-
generation bees is constrained by sparse floral
resources on farms and their progeny’s race to
become prepupae before cool weather arrests
their development.
VISUAL AND CHEMICAL
CUES FOR ALFALFA
LEAFCUTTING BEES
Just as honey bees orient to a hive, ALCBs must
orient to their nests after foraging bouts. Large
field domiciles can serve as long-distance visual
cues for ALCBs flying over seed fields (32,
105, 121). Once at the domicile, a female bee
finds her nest among thousands of holes using
three-dimensionality, color contrast, and color
patterns (27, 41, 42). If visual cues are manipu-
lated, females become temporarily disoriented.
Poor local orientation can result in wasted
time, an increase in bee collisions, dropped
nest-building materials, or further spread of
disease that diminishes efficient, productive
nesting.
Olfactory cues detected in close proximity or
upon antennation seem to be important when
initiating or recognizing nests. Females prefer
once-used nesting boards over new ones, im-
plicating olfactory attractants at nest initiation
(14, 26, 87, 142). Isolating effective cues from
the old nests has proven difficult. In laboratory
Y-tube assays, ALCB females were attracted to
a complete nest cell (after the adult emerged),
larval feces, and solvent-extracted components
from leaf pieces that once lined a cell (94). How-
ever, field bioassays were less conclusive, find-
ing that only cavities cued with feces and a co-
coon were somewhat more attractive than other
components (142). Fractionation of chemicals
from old nest components and testing them
in field assays are needed for understand-
ing chemical mediation of nest initiation and
aggregation.
A nesting ALCB female distinguishes her
own nest from others. ALCB females mark
their nests by dragging the abdomen through-
out the cavity (32, 43). Replacing an outer bee-
marked section of a nest cavity with a clean sec-
tion causes a returning female to be confused
and hesitant to enter, indicating an individual
nest recognition pheromone. Cuticular waxes
and/or the Dufour’s gland may be the origin of
the nest recognition cue (13). For honey bees, in
which many individuals need to recognize the
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
colony odor to discern kin from nonkin, recog-
nition requires them to learn odors both from
cuticles of nestmates and from the colony’s wax
comb (11). Solitary bees need to recognize only
their own nests.
ALFALFA LEAFCUTTING BEES AS
ECOLOGICAL DISRUPTORS
Exotic species can become ecologically disrup-
tive invaders. Feral honey bees have penetrated
far into wildlands (77), as have introduced Eu-
ropean Bombus terrestris that are now escaping
around the world (39). Among the few surveys
of U.S. wildland bee communities where the
ALCB might be expected, it has been rare or
absent. In Wyoming short-grass prairie, none
of the 13 species of Megachile (52 species of
Megachilidae) were ALCBs (128). ALCB was
similarly absent from the 125 bee species netted
in tallgrass prairie remnants and restorations
(103). In the shrub-steppe of eastern Oregon,
12 species of Megachilidae were trap-nested,
but no ALCB was found (30). At a reserve amid
intensive agriculture in central California, the
ALCB was more common, but occupied only
3%–4% of available nesting cavities; it was
outnumbered both by native cavity-nesters
and by another escaped Eurasian species of
Eutricharaea,M. apicalis, known to aggressively
compete for nesting sites (4, 122). The ALCB
is also rare or absent in southern Europe, even
in alfalfa seed fields. The ALCB seems not
to venture far from agricultural or otherwise
disturbed sites in North America and so ap-
pears to be an inconsequential competitor with
native bees for nesting sites or floral resources.
Some nonnative bees prefer and pollinate
nonnative forbs, contributing to the invasions
of weedy species that can outcompete native
wildflowers for pollination services (38). Feral
honey bees and feral bumble bees have been
widely implicated in pollinating invasive
Eurasian weeds in the Americas, New Zealand,
Tasmania, and Australia (39). ALCBs also
avidly visit several Eurasian weeds in North
America, notably sweetclovers (Melilotus alba
and M. officinalis) (58, 81) and purple loosestrife
(Lythrum salicaria), preferring both to alfalfa in
choice tests (114). However, these and other
exotic and invasive weeds are eagerly sought
and pollinated by honey bees and bumble bees
too (12).
A MODEL SOLITARY BEE
Management of ALCBs is an exemplary system
for solitary bee commercial pollination. For-
tuitously, ALCBs are efficient crop pollinators
that also thrive as aggregating cavity-nesters in
anthropogenic habitats. In contrast, the solitary
ground-nesting alkali bee is restricted in its use
as a managed alfalfa pollinator because it re-
quires specific soil moisture, temperature, and
alkalinity. Few growing areas naturally or arti-
ficially can satisfy such requirements (95).
Where farming is intense and an abundance
of pollinating bees is needed, managed cavity-
nesting bees are advantageous. Cavity-nesters
are transportable as packaged nests or loose
cells; some species tolerate nesting in large ag-
gregations. With progeny in nests or as loose
cells, dead or parasitized cells can be culled, cells
and management equipment can be treated for
diseases, and the bee number and sex ratio can
be determined. Other megachilids (e.g., Osmia
spp. for orchard and berry crops) can be used as
pollinators (9), but today they are not available
at the scale of ALBCs (9, 17).
Just as honey bees and bumble bees rep-
resent the social bees for studies in evolution,
genetics, behavior, learning, neurophysiology,
and ecology (e.g., 33, 75), the readily avail-
able ALCB can serve as a model for solitary
bees. ALCB laboratory maintenance is rela-
tively simple, and adults can be kept to emerge
through most of the year. Beyond management
research, ALCB studies already include the ef-
fects of male harassment on reproductive suc-
cess and the lack of response to proboscis ex-
tension reflex elicitation used in learning and
conditioning experiments (112, 143). Recent
reports have identified ALCB genes related to
diapause regulation and bee immunity (149,
150). Future ALCB studies might reveal solitary
bee commonalities in recognition, aggregation
230 Pitts-Singer ·Cane
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EN56CH12-PittsSinger ARI 14 October 2010 11:43
behavior, mating strategies and courtship be-
haviors, and pheromone use. On the horizon
are genome sequences of ALCB and other bees
from which ancestral and shared traits in soli-
tary, subsocial, and primitively eusocial bees
may be found and thus contribute to the un-
derstanding of the mechanisms and evolution-
ary origins of bee sociality (115).
SUMMARY POINTS
1. Accidentally introduced into the United States, the ALCB has become the world’s most
effectively used and intensely managed solitary bee. Its use transformed the alfalfa seed
industry in North America. The most common management practice is the loose cell
system.
2. Traits of ALCBs that contribute to their commercialization include their gregarious na-
ture; philopatry; use of leaves for lining nests; ready acceptance of cheap, mass-produced
nesting materials; and pollination efficacy at and emergence synchrony with alfalfa bloom.
3. The ALCB became a commercial success because its natural history was studied, targeted
research was performed, and producer ingenuity was encouraged. ALCB management is
a model system for commercializing other solitary bees and for advancing new testable
hypotheses in diverse biological disciplines.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We thank Gordon Frank for insights into ALCB pollination of canola. Vincent Tepedino and
James Pitts kindly provided helpful reviews.
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EN56-Frontmatter ARI 28 October 2010 7:29
Annual Review of
Entomology
Volume 56, 2011
Contents
Bemisia tabaci: A Statement of Species Status
Paul J. De Barro, Shu-Sheng Liu, Laura M. Boykin, and Adam B. Dinsdale ppppppppppppp1
Insect Seminal Fluid Proteins: Identification and Function
Frank W. Avila, Laura K. Sirot, Brooke A. LaFlamme, C. Dustin Rubinstein,
and Mariana F. Wolfner ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp21
Using Geographic Information Systems and Decision Support Systems
for the Prediction, Prevention, and Control of Vector-Borne Diseases
Lars Eisen and Rebecca J. Eisen pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp41
Salivary Gland Hypertrophy Viruses: A Novel Group of Insect
Pathogenic Viruses
Verena-Ulrike Lietze, Adly M.M. Abd-Alla, Marc J.B. Vreysen,
Christopher J. Geden, and Drion G. Boucias pppppppppppppppppppppppppppppppppppppppppppppp63
Insect-Resistant Genetically Modified Rice in China: From Research
to Commercialization
Mao Chen, Anthony Shelton, and Gong-yin Ye ppppppppppppppppppppppppppppppppppppppppppppp81
Energetics of Insect Diapause
Daniel A. Hahn and David L. Denlinger ppppppppppppppppppppppppppppppppppppppppppppppppp103
Arthropods of Medicoveterinary Importance in Zoos
Peter H. Adler, Holly C. Tuten, and Mark P. Nelder pppppppppppppppppppppppppppppppppppp123
Climate Change and Evolutionary Adaptations at Species’
Range Margins
Jane K. Hill, Hannah M. Griffiths, and Chris D. Thomas ppppppppppppppppppppppppppppppp143
Ecological Role of Volatiles Produced by Plants in Response
to Damage by Herbivorous Insects
J. Daniel Hare ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp161
Native and Exotic Pests of Eucalyptus: A Worldwide Perspective
Timothy D. Paine, Martin J. Steinbauer, and Simon A. Lawson pppppppppppppppppppppppp181
vii
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Urticating Hairs in Arthropods: Their Nature and Medical Significance
Andrea Battisti, G¨oran Holm, Bengt Fagrell, and Stig Larsson pppppppppppppppppppppppppp203
The Alfalfa Leafcutting Bee, Megachile rotundata: The World’s Most
Intensively Managed Solitary Bee
Theresa L. Pitts-Singer and James H. Cane ppppppppppppppppppppppppppppppppppppppppppppppp221
Vision and Visual Navigation in Nocturnal Insects
Eric Warrant and Marie Dacke pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp239
The Role of Phytopathogenicity in Bark Beetle–Fungal Symbioses:
A Challenge to the Classic Paradigm
Diana L. Six and Michael J. Wingfield pppppppppppppppppppppppppppppppppppppppppppppppppppp255
Robert F. Denno (1945–2008): Insect Ecologist Extraordinaire
Micky D. Eubanks, Michael J. Raupp, and Deborah L. Finke ppppppppppppppppppppppppppp273
The Role of Resources and Risks in Regulating Wild Bee Populations
T’ai H. Roulston and Karen Goodell ppppppppppppppppppppppppppppppppppppppppppppppppppppppp293
Venom Proteins from Endoparasitoid Wasps and Their Role
in Host-Parasite Interactions
Sassan Asgari and David B. Rivers pppppppppppppppppppppppppppppppppppppppppppppppppppppppp313
Recent Insights from Radar Studies of Insect Flight
Jason W. Chapman, V. Alistair Drake, and Don R. Reynolds ppppppppppppppppppppppppppp337
Arthropod-Borne Diseases Associated with Political and Social Disorder
Philippe Brouqui ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp357
Ecology and Management of the Soybean Aphid in North America
David W. Ragsdale, Douglas A. Landis, Jacques Brodeur, George E. Heimpel,
and Nicolas Desneux pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp375
A Roadmap for Bridging Basic and Applied Research
in Forensic Entomology
J.K. Tomberlin, R. Mohr, M.E. Benbow, A.M. Tarone, and S. VanLaerhoven pppppppp401
Visual Cognition in Social Insects
Aurore Avargu`es-Weber, Nina Deisig, and Martin Giurfa pppppppppppppppppppppppppppppp423
Evolution of Sexual Dimorphism in the Lepidoptera
Cerisse E. Allen, Bas J. Zwaan, and Paul M. Brakefield ppppppppppppppppppppppppppppppppp445
Forest Habitat Conservation in Africa Using Commercially Important
Insects
Suresh Kumar Raina, Esther Kioko, Ole Zethner, and Susie Wren pppppppppppppppppppppp465
Systematics and Evolution of Heteroptera: 25 Years of Progress
Christiane Weirauch and Randall T. Schuh ppppppppppppppppppppppppppppppppppppppppppppppp487
viii Contents
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