Original article
Microflora associated with the alfalfa leafcutting bee, Megachile rotundata (Fab) (Hymenoptera:
Megachilidae) in Saskatchewan, Canada
DW Goerzen
Saskatchewan Alfalfa Seed Producers Association 107 Science Crescent, Saskatoon, SK, Canada S7M 0X2
(Received
10 December 1990;accepted
1August
1991)Summary —
The microflora associated withMegachile
rotundata was isolated from adult bees, lar- val cadavers, cellprovisions,
bee cell surfaces, and nest material. Dominantfungi
included Alternar-ia alternata,
Aspergillus niger,
Eurotium chevalieri, Mucor sp, Penicillium spp,Saccharomyces
sp, Trichoderma citrinoviride, andTrichosporonoides
sp. Bacteria commonly isolated included Bacilluscirculans, Bacillus mycoides, Enterobacter
agglomerans,
and Pseudomonas spp. Thesemicroorgan-
isms may be involved in activities such as
spoilage
of provisions, production of enzymes, antibiotics, mycotoxins, andgrowth
factors (vitamins, amino acids), metabolic conversion ofprovisions,
and inhi-bition of
competing microorganisms.
Microbial succession was observedinvolving
yeast and bacteri-al fermentation of
provisions
followedby
mould overgrowth of cell contents; this process was often associated with larvalmortality.
The microflora isolatedlikely
has a range of beneficial and deleteri-ous effects on M rotundata. Some
fungal species reported
here may also bepotentially
harmful tothe health of
leafcutting
bee managers.Megachlle rotundata / associated microflora / fungus / bacteria / Canada
INTRODUCTION
The alfalfa
leafcutting bee, Megachile
ro-tundata
(Fab),
is animportant
domesticat- edpollinator
of alfalfa and iswidely
uti-lized for alfalfa seed
production
in westernCanada
(Richards, 1987).
Concerns relat- ed to the presence of chalkbrood(Ascos- phaera aggregata Skou)
in M rotundatapopulations
in the northwestern United States and southern Alberta have led to extensivesurveying
of Saskatchewanpopulations.
While Aaggregata
has been detectedonly sporadically
and at very low levels in thisprovince
over thepast
5years
(Goerzen, 1990),
numerous othermicroorganisms
have been isolated from variouscomponents
of thesepopulations.
In this paper, the dominant microflora as- sociated with M rotundata is
reported
andthe
impact
of thesefungi
and bacteria onM rotundata
populations
is discussed.MATERIALS AND METHODS
Isolates of
microorganisms
associated with M rotundatapopulations
were obtained by sam-pling
adult bees, larval cadavers,spoiled
cellprovisions
(ie storedpollen
and nectar), beecell surfaces, and tunnel surfaces in wood and
polystyrene
bee nest material.In order to detect microflora on adult bees, female M rotundata adults were captured in the
field as
they
entered or exited nest tunnels andwere
placed
in 1 dram glass vialscontaining
1 ml sterile distilled water. Individuals were re-
leased
following
30 shand-agitation
and sam- ples were transferred to the laboratory for cul-ture. As well, male and female M rotundata adults newly
emerged
from cells incubated in the laboratory were individually placed in testtubes
containing
1 ml sterile distilled water,agi-
tated in a vortex mixer for 30 s, and the insects removed prior to sample culture. To evaluate microflora on the foliar exterior of leafcutting
bee cells, groups of 150 cells from various pop- ulations were
placed
in 30-dram crystallite vialsand washed with 25 ml sterile distilled water.
Tunnels in leafcutting bee nest material were
sampled
with sterilecotton-tipped
woodapplica-
tors wetted with sterile distilled water. Applica-
tors were stored in sterile
glass
culture tubes for transfer to thelaboratory
andrehydrated
with 2ml sterile distilled water
prior
to culture of sam-ples.
All
samples
collected from adult bees, cell surfaces, and nest tunnels wereplated
in the la- boratory as 0.1 ml aliquots on potato dextrose agar (PDA), nutrient agar(Difco®),
or Sabou-raud’s dextrose agar, incubated at 28 °C, and assessed at 24-h intervals.
Cells
containing
larval cadavers andspoiled
cell provisions were identified from samples of leafcutting bee cells examined in annual sur-
veys of M rotundata populations and from mate-
rial collected in trapnests. Microflora associated with these
specimens
wasplated directly
onmedia via sterile loop transfer and incubated un- der the conditions described above.
Purified isolates from all sources were sub- cultured on PDA slants and stored at 4 °C. Iso- lates were examined using lactophenol cotton
blue mounts for
preliminary
identification; bacte- rial isolates were Gram-stained.Fungal
isolateswere submitted to the Biosystematics Research Centre, Ottawa, for identification; selected larval cadaver and cell
provision
specimens were alsosubmitted. Bacterial isolates were submitted to the
Agriculture
Canada Research Station, Leth- bridge, for identification. Voucher cultures of most isolates reported here have beendeposit-
ed at DAOM, Ottawa.
RESULTS
The presence and relative abundance of microflora isolated from M rotundata
adults,
larvalcadavers, spoiled
cellprovi- sions,
cellsurfaces,
and nest material aregiven
in table I. Prevalentmicroorganisms
associated with field-collected M rotundata females included Alternaria
alternata,
As-pergillus niger,
Enterobacteragglomerans,
Penicillium spp, Pseudomonas solanacear- um,
Rhizopus arrhizus,
andTrichosporo-
noides sp.
Likely
sources of these microor-ganisms
were alfalfaplant
surfaces and the leaves of otherplants, including
Chen-opodium, Fagopyrum, Melilotus,
and Rosaspp, which are
commonly
utilized for cell construction(Richards, 1984).
The relative abundance offungal
and bacterialspecies
fluctuated with
temperature
and moisturechanges during
the field season. Male andfemale M rotundata
emerging
from labora-tory-incubated
cells were found to be car-rying primarily
Aalternata, Aspergillus
ni-ger, Enterobacter
agglomerans,
Eurotiumchevalieri,
andTrichosporonoides
sp. All of thesespecies
were isolatedfrequently
from the leaf surfaces of cells and
likely picked
upby
individualsthrough
contactduring
emergence.Fungi commonly
associated with larval cadavers included Aniger,
Echevalieri,
Penicillium purpurogenum, Psimplicissi-
mum, other Penicillium spp, and Trichos-
poronoides
sp, while dominantmicroorgan-
isms found in
conjunction
withspoiled
cellprovisions
includedAscosphaera polleni-
cola, Avariegata, Aspergillus glaucus,
Aniger,
Bacilluscirculans,
Enterobacter ag-glomerans,
Eurotiumchevalieri,
Penicillium spp, Pseudomonas spp, andTrichosporo-
noides sp. Surfaces of M rotundata cells
were inhabited
by
a microfloralcomplex
similar to that found in
leafcutting
bee nestmaterial,
withpredominance
of Alternariaalternata, Aspergillus niger,
Enterobacteragglomerans,
Eurotiumchevalieri,
Mucor sp, Penicillium spp,Rhizopus
spp, and Tri-chosporonoides
sp. Otherspecies
com-monly
isolated from nest material were Ba- cilluscirculans,
Bmycoides, Coryne-
bacterium sp, Pseudomonas spp, and Tri- choderma citrinoviride. The
yeast
Saccha-romyces sp was
frequently
found in cul- tures from wood nest material butrarely
isolated from
polystyrene
nest material.DISCUSSION
The dominant
species
of filamentousfungi
listed
(ie A alternata, Aspergillus niger,
Echevalieri,
Mucor sp, Penicillium spp, R ar-rhizus,
and Tcitrinoviride)
aregenerally saprophytic
in nature,growing
on availablematerial
including
cellprovisions,
larval ca-davers,
and the foliar surface of cells.However,
otherfungal species reported here, including Aspergillus
spp and Tricho- thecium roseum, can bepathogenic
onwild bees
(Batra
etal, 1973).
While A ag-gregata,
the causativeagent
of chalkbrood in Mrotundata,
israrely
detected in Sas-katchewan
leafcutting
beepopulations,
several other
Ascosphaera
spp have been isolated and 2 ofthem,
Apollenicola
and Avariegata,
arefrequently
found inspoiled
cell
provisions, usually
inconjunction
withE chevalieri and
Trichosporonoides
sp.The
species
A atra and Apollenicola
ap- pear to beprimarily saprophytic
on cellprovisions,
while A larvis and Avariegata
are
usually
isolated from M rotundata lar- val cadavers and may bepathogenic
tothe
leafcutting
bee(Bissett, 1988).
Extensive research in the identification of
fungal species
associated with the hon-eybee (Apis mellifera)
indicated that the mostcommonly occurring
moulds wereAspergilli, Mucorales,
and Penicillia(Gilli-
am and
Prest, 1987;
Gilliamet al, 1989a, 1989b).
Richards(1985),
in surveys to de- tectAscosphaera aggregata
in M rotunda-ta
populations,
noted the occurrence of Fu-sarium, Mucor, Penicillium,
andRhizopus
spp.
Except
for the absence of Fusarium sp, the dominant mouldspecies reported
for M rotundata in this
study
aresimilar,
with Alternaria and Eurotium spp also com-
monly
isolated. As notedby
Gilliam et al(1989a),
moulds merit intensivestudy
dueto their
activity
in theproduction
of en-zymes and numerous
secondary
metabo-lites
including antibiotics, terpenes,
andpolysaccharides.
Researchcurrently
un-derway
toinvestigate possible antagonistic
interactions between A
aggregata
and oth-er microflora associated with M rotundata
(Goettel, Agriculture Canada, Lethbridge, personal communication)
isimportant
forthe
insight
it willprovide
into thecomplex relationships existing
among these micro-organisms.
Seven of the 22fungal species reported
here are known toproduce
myco- toxins. These includeAspergillus niger (malformin C),
E chevalieri(gliotoxin),
Ppurpurogenum
(rubratoxin),
Psimplicissi-
mum
(penicillic acid),
Pspinulosum (spinu- losin),
T citrinoviride(T-2 toxin),
and Troseum
(trichothecin) (Wyllie
and More-house,
1977;Moreau, 1979).
Members of the genus
Trichosporo- noides,
which were isolated in abundance from everycomponent
of theleafcutting
bee
system
examinedhere,
areyeast-like fungi
which are not well known and are in need of taxonomic revision. The strains ofTrichosporonoides
isolated were some-what variable in cultural characteristics and
morphology,
and mayrepresent
asingle species complex
which hasyet
to be de- scribed(Bissett, personal communication).
The
unique morphology
anddevelopment
of this genus was first described
by
Ha-skins and
Spencer (1967),
who isolatedTrichosporonoides oedocephalis
Haskinsand
Spencer
from brood cell material inApis
melliferahoneycomb.
Saccharomyces
sp wasfrequently
iso-lated from wood nest material and
spoiled
cell
provisions,
but was neverpresent
in abundance. An additional 2 asyet
uniden- tifiedyeast-like species
arecurrently
underevaluation at the
Biosystematics
ResearchCentre,
Ottawa(DAOM 212-057,
DAOM212-058).
Thesespecies, along
with uni-dentified
yeast-like species designated
Y01 and
Y02,
were isolatedoccasionally
from
field-captured
adultbees,
cell surfac- es, or nest material. In workdescribing yeasts
inpollen
and beebread,
Gilliam(1979a)
isolated 113yeasts
in 7 genera which were associated with almond(Pru-
nus
dulcis) pollen
either from the flower orstored in comb cells of A mellifera hives.
This demonstrates the
diversity
ofyeast
flora which may be associated with beepopulations.
As notedby
Gilliam(1979a),
the role of
yeasts
in processesrelating
tobee nutrition is as
yet poorly defined,
butmay involve
production
of necessarygrowth
factorsincluding
vitamins and ami-no acids.
Bacteria dominant in this
study
includedBacillus
circulans,
Bmycoides,
Entero-bacter
agglomerans,
and Pseudomonas spp. These were isolated most often from adultbees,
cellprovisions,
and nest mate-rial. Enterobacter
agglomerans
was alsoabundant on cell surfaces. Two unidenti- fied bacterial
species, designated
B01 andB02,
were isolatedinfrequently
from adultbees and cell surfaces. In
reports
of bacte- ria associated with A mellifera(Gilliam, 1979b),
thestingless bee, Melipona
fascia-ta
(Gilliam
etal, 1990a),
and 5species
ofsolitary
bees(Gilliam et al, 1984, 1990b),
Bacillus spp weredominant,
and in all cas- es, B circulans was isolated. Gilliam et al(1990b)
concluded that Bacillus spp arecommon associates of
Apoidea
and couldparticipate
in metabolic conversion of pro- visions and in inhibition ofcompeting
andspoilage microorganisms.
The presence of this diverse group of
fungi
and bacteria associated with M ro-tundata
populations
in Saskatchewanprobably
has a broad range of effects on thesepopulations.
Asnoted,
the microor-ganisms
may contribute to theproduction
of many beneficial
compounds
such as an-tibiotics, vitamins,
aminoacids,
and anti-spoilage agents. However,
many of thespecies
listed may also harmleafcutting
bee
populations by interfering
with larvaldevelopment
andspoiling
cellprovisions.
In
laboratory studies,
B circulans and Pseudomonas spp, inconjunction
withSaccharomyces
andTrichosporonoides
spp, were observed to cause larval mortal-
ity through
fermentation of cellprovisions.
The
spoilage
of cellprovisions
often led tosubsequent overgrowth
of cell contentsby Aspergillus niger,
Penicillium spp, and R arrhizus(Goerzen, unpublished data).
Thisprocess of microbial succession in cells
was
reported previously
in the alkalibee,
Nomiamelanderi (Batra et al, 1973).
In ad-dition to
exhibiting
antibacterial andfungis-
tatic
activity,
toxins associated with somefungal species
isolated here have been shown to elicit responsesincluding feeding
aversion and inhibition of
protein synthesis (Moreau, 1979). Any
of these processes could contribute toleafcutting
bee larvalmortality
found inpopulations
evaluated inthis
study. Surveys
of Saskatchewan leaf-cutting
beepopulations
undertaken over the5-year period
1985 to 1989 haveshown the
percentage
of cellscontaining
dead
larvae, mouldy larvae, and spoiled provisions
to range from6.9-11.9%
of to- tal cells evaluated(Goerzen, 1990).
Many
of the mouldspecies
found in as-sociation with the alfalfa
leafcutting
beemay be
potentially
harmful to the health ofleafcutting
bee managers as well. Alternar-ia, Aspergillus,
Penicillium andRhizopus
spp are among those
fungi
which are con-sidered most
important medically (Aukrust
et
al, 1985).
Thesespecies
have been im-plicated
inallergic
reactions and broncho-pulmonary
disease and may cause condi- tionsranging
frompulmonary hypersensi- tivity
disease(eg allergy, asthma)
to life-threatening
infection(Pennington, 1986).
During leafcutting
bee incubation and cell-harvesting operations, large
numbers ofemerging
bees or loose cells concentrated in confined areas may lead tohigh
levelsof airborne spores of these
species.
Sev-eral less
frequently
isolated mouldspecies reported here, including Cylindrocarpon, Trichoderma,
and Ulocladium spp, are notordinarily
associated with human diseases but under certain conditions may act asopportunistic pathogens (Rippon, 1987).
Identification of the microflora associat- ed with M rotundata is
important
in eluci-dation of the
complex
interactions between thiseconomically important solitary
beespecies
and themicroorganisms present
in its environment. A reduction in
high
lev-els of mould
species
which may interfere with larvaldevelopment
andspoil
cell pro- visions will assist inincreasing
thequality
of alfalfa
leafcutting
beepopulations.
Anawareness of the presence of mould spe- cies which have been
implicated
in humanallergic
reactions will allowleafcutting
beemanagers to take measures to reduce contact with
potentially
harmful spores and toincorporate
controltechniques
whichwill reduce levels of non-beneficial micro-
organisms
in M rotundatapopulations.
However,
the beneficial effects associated with the presence of a balancedcomple-
ment of
microorganisms
in theleafcutting
bee
ecosystem
are doubtless ofgreat
im-portance
andrequire
furtherstudy.
ACKNOWLEDGMENTS
I thank M Erlandson and D Murrell for continu-
ing assistance and encouragement, M Goettel and K Moore for critical review of the manu-
script,
J Bissett for determination offungal
spe- cies, and RPhillipe
for determination of bacteri-al
species.
This research wassupported by
theCanada-Saskatchewan Economic
Regional
De-velopment Agreement
and the SaskatchewanAgriculture Development
Fund.Résumé —
Étude
de la microflore asso-ciée à la
mégachile Megachile
rotundata(Fab) (Hymenoptera: Megachilidae)
auSaskatchevan,
Canada. Des isolats dechampignons
et debactéries,
associés à despopulations
deMegachile rotundata,
ont été obtenus par
échantillonnage
d’abeilles
adultes,
de cadavres delarves,
deprovisions endommagées
contenuesdans des
cellules,
de la surface de cellules decouvain,
et de la surface des tunnelsprésents
dans le nid. Les abeilles adultes et les surfaces des cellules ont été traitées parlavage
dans de l’eau distilléestérile,
alors que les
prélèvements
des tunnels ont été réalisés avec destiges
de bois munies de coton à leur extrémité. Aulaboratoire,
les échantillons ont été recouverts avec del’agar
dextrose de pomme de terre, del’agar nutritif,
et del’agar
dextrose de Sa-bouraud,
et incubés à 28 °C. La microflore associée aux cadavres de larves et auxprovisions endommagées
a été transférée dans les milieux au moyen d’un instrument stérile. Les isolatspurifiés
dechampignons
ont été examinés en utilisant du
lactophé- nol,
et les isolats de bactéries ont été colo- rés par la coloration de Gram.La
présence
et l’abondance de la micro- flore isolée depopulations
de M rotundatasont données dans le tableau I. Les micro-
organismes
dominants sont : leschampi-
gnons Alternaria
alternata, Aspergillus niger,
Eurotiumchevalieri,
Mucor sp, Peni- cillium spp,Rhizopus arrhizus,
Saccharo- myces sp, Trichodermacitrinoviride,
andTrichosporonoides
sp; les bactéries Ba- cilluscirculans,
Bmycoides,
Enterobacteragglomerans,
and Pseudomonas spp. Ungrand
nombre desespèces
dechampi-
gnons
présents
sontsaprophytes,
et crois-sent sur les
provisions
et les cadavres de larves.Cependant, Aspergillus
spp et Tri- chothecium roseum sont connus pour êtrepathogènes
pour les abeilles sauvages.Les
champignons peuvent également jouer
un rôleimportant
pour leur activité dans laproduction d’enzymes,
d’antibioti- ques et demycotoxines.
Lechampignon,
voisin des
levures, Trichosporonoides
aété isolé dans tous les
types
d’échantillonsanalysés.
Le rôle des levures dans la nutri- tion de l’abeillepeut
consister en la pro- duction de vitamines et d’acides aminés.Les bactéries dominantes dans cette étude
peuvent participer
à la transforma- tionmétabolique
desprovisions
et à l’inhi-bition des
microorganismes
encompétition
avec elles.
La microflore isolée des
populations
demégachiles
a vraisemblablement à la fois des effetsbénéfiques
et nuisibles. Tandis quebeaucoup d’espèces
dechampignons
et de
bactéries peuvent
contribuer à laproduction
decomposés utiles,
d’autrespeuvent
interférer avec ledéveloppement
larvaire et abîmer les
provisions.
Cette mi-croflore est souvent associée à des morta- lités larvaires. Les moisissures, incluant Al-
ternaria, Aspergillus,
Penicillium etRhizopus
spppourraient également
êtrepotentiellement
nocives pour les éleveurs de ces abeilles. Pendant lesopérations
derécolte en
particulier,
un trèsgrand
nom-bre d’abeilles et de
cellules, qui
sont main-tenues dans des zones
confinées, peuvent
émettre dans l’airambiant,
degrandes quantités
de sporesprovenant
de ces moi-sissures, qui
ont étéimpliqués
dans desréactions
allergiques
et des maladiesbronchopulmonaires.
L’identification de la microflore associée à M rotundata est im-portante
pour lacompréhension
des inté-ractions
complexes
existant entre cette im-portante espèce
d’abeilles solitaires et lesmicroorganismes présents
dans l’environ- nement. Tandisqu’une
réduction du ni-veau élevé
d’espèces
de moisissures nui- sibles pour M rotundatapermettrait
d’ac-croître la
qualité
despopulations
de cetteabeille,
les effetsbénéfiques
dequelques microorganismes pourraient
être d’unegrande importance,
et nécessitent des étu- des ultérieures.Megachile
rotundata / microflore asso-ciée /
champignons
/ bactéries / CanadaZusammenfassung —
Die mit der Lu- zerne-Blattschneiderbiene(Megachile rotundata)
inSaskatchewan, Kanada,
assoziierte Mikroflora. Durch Probenent- nahme von erwachsenenBienen,
toten Larven, verdorbenenZellvorräten,
der Oberfläche der Bienenzellen sowie des Materials der Neströhre wurden Isolatevon Pilzen und Bakterien gewonnen, die
zusammen mit den
Populationen
von Me-gachile
rotundata vorkommen. Die Probenvon den Bienen und der Zelloberfläche wurden durch Waschen in destilliertem Wasser gewonnen, während die Proben
von dem Material der Neströhren mittels eines sterilen Wattebausches entnommen wurden. Die Proben wurden im Labora- torium auf
Kartoffel-Dextrose-Agar,
Nähra-gar oder Sabouraud’s
Dextrose-Agar
aus-gestrichen
und bei 28 °C inkubiert. Die Mi- kroflora in toten Larven oder verdorbenen Zellvorräten wurden mittels einer sterilenÖse
auf das Nährmediumübertragen.
Ge-reinigte
Pilzisolate wurden in mitLactophe-
nolblau
gefärbten Präparaten untersucht,
Bakterien-Isolate wurdengramgefärbt.
DieArt und relative
Häufigkeit
der von M ro-tundata-Populationen
isolierten Mikroflora ist aus Tabelle I ersichtlich. Unter den vor-herrschenden
Mikroorganismen
befandensich die Pilze Alternaria
alternata, Asper-
gillus niger,
Eurotiumchevalieri,
Mucor sp, Penicillium spp,Rhizopus arrhizus,
Sac-charomyces
sp, Trichoderma citrinoviride undTrichosporonoides
sp; an Bakterienwurden Bacillus
circulans,
Bmycoides,
Enterobacter
agglomerans
und Pseudo-monas spp
gefunden.
Viele von den Pilz-arten sind
Saprophyten,
die aufderartigen
Materialen wie Zellvorräten und toten Larven wachsen. Von
Aspergillus
spp und Trichothecium roseum istjedoch bekannt,
daß sie für Wildbienenpathogen
sind.Pilze können auch für die Produktion von
Enzymen,
Antibiotika undMykotoxinen wichtig
sein. Der Hefe-ähnliche Pilz Tricho-sporonoides
wurde von allenkomponen-
ten des
Blattschneiderbienen-Systems
iso-liert. Die Rolle von Hefen in
Bezug
auf dieErnährung
der Bienen kann dieErzeugung
von Vitaminen und Aminosäuren einschlie-
ßen. Die in dieser
Untersuchung
vorherr-schenden Bakterien können bei der Um-
wandlung
der Zellvorräte im Stoffwechsel und bei derHemmung
von anderen Mikro-organismen
vonBedeutung
sein.Die von den
Populationen
der Luzerne-Blattschneiderbiene isolierte Mikroflora be- sitzt wahrscheinlich
Effekte,
die von nütz-lich bis schädlich reichen. Während viele Pilz- und Bakterienarten zu der
Erzeugung
nützlicher
Verbindungen beitragen mögen,
können andere dieLarvenentwicklung
stören und die Zellvorräte verderben. Die mikrobielle
Entwicklung,
wie sie im Labora-torium beobachtet wurde und welche die Hefe- und bakterielle
Gärung
der Vorräte und eineSchimmelüberwucherung
desZellinhalts
betraf,
war oft mit dem Abster- ben der Larven verbunden.Schimmelpil-
ze, einschließlich
Alternaria-, Aspergillus-,
Penicillium- und
Rhizopus-Arten
könnenpotentiell
auch für die Betreuer der Blatt- schneiderbienen schädlich sein. Während des Ausbrütens der Bienen und derTätig-
keiten der Ernte reifer
Zellen,
könnengroße Mengen
von Bienen oder Bienen- zellen ingeschlossenen
Räumen zu einerhohen
Sporenkonzentration
dieser medizi- nischwichtigen Schimmelpilze
in der Luft führen und in derFolge
zuallergischen
Reaktionen und
bronchopulmonalen
Er-krankungen.
Die
Bestimmung
der mit M rotundata assoziierten Mikroflora ist für die Aufklä- rung derkomplexen Wechselwirkungen
zwischen dieser
wirtschaftlich wichtigen
solitären Bienenart und den in ihrer Umwelt vorhandenen
Mikroorganismen wichtig.
Während die Reduktion einerÜberzahl
für M rotundata schädlicherSchimmelpilze
die Qualität derPopulatio-
nen von Blattschneiderbienen verbessern
wird,
kann dergünstige
Einflußeiniger
Mi-kroorganismen
von sogroßer Bedeutung sein,
daß weitereUntersuchungen
ge-rechtfertigt
werden.Megachile
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