Impact of Currently Used or Potentially Useful Insecticides for Canola
Agroecosystems on Bombus impatiens (Hymenoptera: Apidae),
Megachile rotundata (Hymentoptera: Megachilidae), and
Osmia lignaria (Hymenoptera: Megachilidae)
C. D. SCOTT-DUPREE,1L. CONROY, AND C. R. HARRIS
Department of Environmental Biology, University of Guelph, Guelph, ON, Canada N1G 2W1
J. Econ. Entomol. 102(1): 177Ð182 (2009)
Pest management practices may be contributing to a decline in wild bee populations
in or near canola (Brassica napus L.) agroecosystems. The objective of this study was to investigate
the direct contact toxicity of Þve technical grade insecticidesÑimidacloprid, clothianidin, delta-
methrin, spinosad, and novaluronÑcurrently used, or with potential for use in canola integrated pest
management on bees that may forage in canola: common eastern bumble bees [Bombus impatiens
(Cresson); hereafter bumble bees], alfalfa leafcutting bees [Megachile rotundata (F.)], and Osmia
deltamethrin and spinosad were intermediate in toxicity, and novaluron was nontoxic. Bumble bees
were generally more tolerant to the direct contact applications ? O. lignaria ? leafcutting bees.
clothianidin was only 4.9 and 1.3? more toxic, deltamethrin was 53 and 68? more toxic to leafcutting
bees than to bumble bees and O. lignaria, respectively. Laboratory assessment of direct contact
may differ greatly depending on management practices. Research conducted using only honey bees
of their unique biology and differential susceptibility. Research programs focused on determining
nontarget impact on pollinators should be expanded to include not only the honey bee but also wild
bee species representative of the agricultural system under investigation.
bumble bee, alfalfa leafcutting bee, O. lignaria, insecticides, direct contact toxicity
(Free 1993, Allen-Wardell et al. 1998, Kearns et al.
bee (Apis mellifera L.) is generally regarded as the
most important bee pollinator (Allen-Wardell et al.
1998, Kearns et al. 1998, Delaplane and Mayer 2000,
important (Free 1993, Williams 1996, Kevan 1999,
Westerkamp and Gottsberger 2000, Kremen et al.
2002). There has been growing concern about sus-
pected declines in wild bee populations and the im-
plications for agricultural and natural ecosystems
and Phillips 2001, Klein et al. 2007, NRC 2007).
Wild bee declines have, in part, been attributed to
insecticide use (Kearns et al. 1998, Westerkamp and
Gottsberger 2000, Tasei 2002). Bees maybe uninten-
tionally exposed to insecticides during or after spray
application while foraging in crops and nesting in
insecticide residues in nectar and pollen from treated
crops. Wild bees are particularly vulnerable to foliar
insecticides because, unlike honey bees, nesting sites
cannot be moved or protected during spray applica-
tion (Tasei 2002), and different foraging behaviors
may bring wild bees into contact with insecticides
applied at times designed to reduce foraging honey
bee exposure (Corbet et al. 1993). Although there is
limited information on the toxicity of pesticides to
nontarget beneÞcial insects such as common eastern
bumble bees [Bombus impatiens (Cresson)] (hereaf-
ter bumble bees), alfalfa leafcutting bees [Megachile
rotundata (F.)], and Osmia lignaria Cresson com-
pared with honey bees (Tasei 2002), in recent years,
several studies have been conducted that focus on
et al. 2004, Morandin et al. 2005, Malone et al. 2007,
Abbott et al. 2008). Morandin and Winston (2003)
concluded that ?7 ppb of imidacloprid in pollen
1Corresponding author, e-mail: firstname.lastname@example.org.
0022-0493/09/0177Ð0182$04.00/0 ? 2009 Entomological Society of America
health or foraging ability; however, 30 ppb in pollen
(i.e., ?4? the highest imidacloprid residues found in
Þeld situations) resulted in sublethal effects on for-
aging. Franklin et al. (2004) determined that colony
health and foraging ability of B. impatiens was not
adversely affected by six ppb of clothianidin in pollen
(representing the highest residues in pollen found in
Þeld studies) or 36 ppb. Studies on the impact of the
biopesticide spinosad on B. impatiens at concentra-
ppb) had minimal impact on colony health, whereas
8 ppb caused signiÞcant mortality of brood and adults
(Morandin et al. 2005). Sublethal effects to workers
exposed to 0.2 and 0.8 ppb spinosad during larval
2005). Novaluron, an insect growth regulator (IGR)
(i.e., chitin synthesis inhibitor) was fed to microcolo-
(a realistic Þeld exposure concentration), 0.09, and
0.135 ppb for 35 d followed by monitoring to day 70
drones produced by workers in microcolonies were
determined only at 0.135 ppb. In laboratory and Þeld
lethal effects of either imidacloprid on O. lignaria or
clothiandin on M. rotundata at three (low), 30 (inter-
mediate), or 300 (high) ppb. Minor sublethal effects
on O. lignaria were detected at 30 and 300 ppb imi-
dacloprid resulting in increased larval development,
whereas no sublethal effects were detected with
clothianidin at any concentration on M. rotundata.
Canola (Brassica napus L.) is the second most im-
million ha planted in 2007 (Statistics Canada 2007). It
attractive to bees (Delaplane and Mayer 2000). Man-
agement of economically important insect pests in-
cluding ßea beetles (Phyllotreta spp.), bertha army-
worm (Mamestra configurata Walker), diamondback
moth [Plutella xylostella (L.)], lygus bugs (Lygus
spp.), root maggots (Delia spp.), and the weevil Ceu-
torhynchus obstrictus Marsham requires use of seed
and/or foliar insecticide treatments (Canola Council
of Canada 2007), which can be highly toxic to bees
(Mayer et al. 1998, OMAFRA 2006). The large area of
land devoted to canola production coupled with the
frequency and toxicity of insecticides applied for pest
suspected declines of wild bee populations in canola
agro-ecosystems (NRC 2007).
Our objectives were to 1) investigate the direct
nicotinoids imidacloprid and clothianidin; the micro-
bial bioinsecticide spinosad; the pyrethroid delta-
methrin; and the IGR novaluronÑcurrently used, or
with potential for use in canola pest management on
three bee pollinators that may forage on this crop:
bumble bees, alfalfa leafcutting bees, and O. lignaria;
and 2) determine whether toxicity of these insecti-
cides was similar between the pollinators.
Materials and Methods
are important indigenous North American pollinators
workers were purchased from Biobest Canada Ltd.
a well-ventilated plastic container (?20 by 28 by 18
cm) housed in a cardboard box, with the nectar sub-
stitute Biogluc (Biobest Canada Ltd.) available ad
at the Townsend House Bee Research Facility at the
Each colony was given ?5 ml of pollen twice weekly.
Female worker bees were aspirated under red light
from each colony and were placed into 1 liter mason
jars until testing. Each jar of bees was randomly as-
signed to a treatment.
Alfalfa leafcutting bee pupae were purchased from
Northstar Seeds Inc. (Neepawa, MB, Canada) and
until fully developed according to a standard emer-
gence protocol (Agriculture Canada 1989) in plastic
containers (20 by 10 by 8 cm) with metal mesh lids.
Emerging adults were transferred to new containers
wicks (2 by 0.9 cm), one soaked in 50% sucrose, and
of 2 females:1 male) were removed from the contain-
ers and were placed into a 1-liter mason jar that was
randomly assigned to a treatment.
O. lignaria were purchased from Beediverse Prod-
ucts of CPC Ltd. (Coquitlam, BC, Canada) in Sep-
tember and were stored at 2Ð4?C and 40Ð60% RH.
They were incubated until fully developed according
to a standard emergence protocol (Dogterom 2005)
and were maintained in the same manner as alfalfa
leafcutting bees until required for testing. The sex
ratio of O. lignaria is 1 female:1.7 males in nests with
a typical tunnel diameter of 7.5 mm and length of 14
cm (Dogterom 1999).
were all commercially available, but for our purposes
we considered them to be wild bees because com-
mercial stocks are invigorated with wild caught spec-
imens annually. In recent years, B. impatiens has in-
creasingly been used for pollination in commercial
greenhouses. M. rotundata is used in western Canada
and the United States for pollination of alfalfa and
canola. O. lignaria is used for pollinating fruit crops,
e.g., apple, cherry, almonds and berry bushes (blue-
berries) and other ßowering crops wherever they are
Insecticides. Insecticides tested were: clothianidin,
imidacloprid, deltamethrin (Bayer CropScience Inc.,
Calgary, AB, Canada), spinosad (Dow AgroSciences
Canada Inc., Calgary, AB, Canada), and novaluron
(Makhteshim-Agan North America via Crompton
Co./Cie, Middlebury, CT). Clothianidin and imida-
cloprid are systemic neonicotinoid insecticides cur-
178JOURNAL OF ECONOMIC ENTOMOLOGY
Vol. 102, no. 1
are treated with formulated insecticide before plant-
ing and it is translocated through the growing plant.
Deltamethrin is a pyrethroid insecticide, registered
for use in canola. Spinosad, a microbial bioinsecticide
and novaluron, a benzoylphenyl urea IGR, also may
have potential for use on canola in Canada. All insec-
ticides tested were technical grade (?95% purity),
with exception of spinosad (90% purity). Stock solu-
tions (1.0%, wt:vol) were prepared by dissolving each
insecticide in a 19:1 acetone:olive oil solvent mixture
(Harris and Svec 1969).
Insecticide Application. Direct contact toxicity of
the insecticides was determined using a Potter spray
tower (PST) (Potter 1952) located at the Southern
Crop Protection and Food Research Centre-Agricul-
ture and Agri-Food Canada-London, ON, Canada.
Four to six concentrations of each insecticide were
prepared by serial dilutions of the appropriate stock
solutions. For each concentration, four to six repli-
cates, each containing nine to 11 bees, were tested.
Control insects, treated with acetone:olive oil only,
were included with each insecticide. Control mortal-
ity did not exceed 10%. Before treatment, bees were
anesthetized with CO2for 3 s, placed ventral side up
in a 10-cm glass petri dish containing a single sheet of
ml aliquots of the desired concentration of each in-
secticide were then applied.
After treatment bees were transferred to waxed
petri dishes. Cotton dental wicks (2 by 0.9 cm) were
soaked in Biogluc for bumble bees, and 50% sucrose-
water solution for alfalfa leafcutting bees and O. lig-
naria and stapled to the inside of the cups. Posttreat-
ment containers were placed at 25 ? 1?C in the dark
immediately after treatment. Mortality was assessed
48 h posttreatment. Bees that could not move when
touched with a blunt probe were considered dead.
Data Analysis. Statistical analyses were performed
using SAS version 8.02 (SAS Institute 2001). The pro-
concentration (LC50), 95% Þducial limits, and chi-
square goodness-of-Þt for each insecticide tested.
Each LC50determination was based on between four
and six concentrations causing ?15Ð90% mortality.
AbbottÕs formula was used to correct for control mor-
tality (Abbott 1925). Direct contact toxicity data for
the three wild bees were compared with data from
Bailey et al. (2005) on honey bees to determine the
relative susceptibility of both wild and domesticated
bees frequenting the agroecosystems.
bees was clothianidin ? imidacloprid ? delta-
bees was clothianidin ? deltamethrin ? imidaclo-
prid ? spinosad ? novaluron; and to O. lignaria bees
was imidacloprid ? clothianidin ? spinosad ? delta-
methrin (Table 1). Novaluron, not tested on O. lig-
est rate tested (0.1% solution) to either alfalfa
leafcutting or bumble bees.
The neonicotinoid insecticides clothianidin and to
a lesser extent imidacloprid were highly toxic to the
three bee species. For example, clothianidin was ?23,
16, and 47? more toxic to bumble bees, alfalfa leaf-
cutting bees, and O. lignaria bees, respectively, than
was the microbial bioinsecticide spinosad. The pyre-
toxicity, being highly toxic to alfalfa leafcutting bees
Table 1.Direct contact toxicity of technical grade insecticides after 48 h to bumble bees, alfalfa leafcutting bees, and O. lignaria
No. adult bees
Slope ? SE
Bumble bees (? only)
Alfalfa leafcutting bees (? and ?)
O. lignaria (? and ?)
1.9 ? 0.34
1.9 ? 0.19
4.4 ? 0.53
4.2 ? 0.70
2.4 ? 0.26
1.2 ? 0.23
2.0 ? 0.23
4.5 ? 0.49
2.7 ? 0.35
2.3 ? 0.43
2.2 ? 0.34
3.09 ? 0.37
aConcentrations are expressed as percentage of solution (wt:vol) (? 10?3).
bFiducial limits (? 10?3).
cFor each bee species tested, values followed by the same letters are not signiÞcantly different as determined by overlap of 95% Þducial
dNo mortality at the highest concentration tested (0.1% solution).
February 2009SCOTT-DUPREE ET AL.: IMPACT OF INSECTICIDES ON BEES
but much less toxic to bumble bees and O. lignaria
bees (Table 1; Fig. 1).
Bee species have been reported to vary in suscep-
tibility to insecticides (Mayer et al. 1998, Devillers et
al. 2003), and our data followed a similar pattern with
lignaria bees or bumble bees (Table 1; Fig. 1). Bees
with larger surface area to volume ratios are thought
to generally be more susceptible to direct contact
insecticide applications than those with smaller ratios
because they are exposed to relatively larger doses
(Tasei 2002, Johansen et al. 1983). However, differ-
ences in relative toxicity of the insecticides between
the three species were not consistent, e.g., whereas
clothianidin was only 4.9 and 1.3? more toxic, delta-
methrin was 53 and 68? more toxic to alfalfa leafcut-
ting bees than to bumble bees and O. lignaria bees,
Bailey et al. (2005), using the same bioassay tech-
nique, determined the direct contact toxicities of
clothianidin, imidacloprid, and spinosad to honey
bees. Comparison of their data with those obtained in
this study showed some signiÞcant differences in in-
secticide toxicity. Although clothianidin was highly
toxic to honey bees, imidacloprid and spinosad were
only moderately toxic. O. lignaria and alfalfa leafcut-
ting bees were more susceptible to the neonicotinoid
insecticides than honey bees (Fig. 1).
Discussion and Conclusions
ambient wild bee populations to ensure seed set in
bee is an important pollinator of canola, recent dra-
matic losses in honey bee populations worldwide due
to colony collapse disorder (Oldroyd 2007), reduced
efÞcacy to the miticide ßuvalinate used to control
Varroa destructor Anderson & Trueman (Macedo et
al. 2002), and the impact of Nosema ceranae (Williams
et al. 2008) likely will result in an increasingly impor-
been shown to increase as a result of increased wild
bee abundance (Morandin and Winston 2005). Thus,
it is essential to assess the impact on wild bee polli-
nators of insecticides considered suitable for canola
pest management. The study showed that the direct
times very substantially, with insecticide and species.
Clothianidin and imidacloprid were generally highly
toxic, deltamethrin and spinosad being less so, with
bumble and honey bees being more tolerant than
mason and leafcutter bees (Table 1; Fig. 1). It was not
unexpected that novaluron was nontoxic to adult
as a chitin synthesis inhibitor its activity is restricted
to immature life stages (Cutler and Scott-Dupree
Laboratory assessment of direct contact toxicity is
only one measure of potential impact, and mortality
on management practices such as methods, rates, and
timing of pesticide applications. For example, al-
though highly toxic by direct contact, the neonicoti-
noid insecticides are applied as seed treatments on
canola, thus minimizing impact other than through
possible minimal exposure to very low residues in
nectar and pollen (Tasei et al. 2001, Maus et al. 2003,
Cutler and Scott-Dupree 2007b). Conversely, al-
though generally less toxic by contact, foliar applica-
tions of deltamethrin or spinosad could have imme-
diate impact on foraging bees. Situations where
potential hazard has been identiÞed in laboratory
studies must be validated under Þeld conditions using
before reaching conclusions about insecticide impact
on either domesticated or wild bees.
Research conducted using only honey bees as the
indicator species may not adequately reßect the risk
posed by insecticides to wild bees because of their
LC (% solution x10 )
Alfalfa leafcutting bees
bees, bumble bees, O. lignaria bees, and honey bees. LC50values for honey bees are from Bailey et al. (2005). Bars within
each category followed by the same letter are not signiÞcantly different as determined by overlapping 95% Þducial limits.
180JOURNAL OF ECONOMIC ENTOMOLOGY
Vol. 102, no. 1
(Thompson and Hunt 1999). Pesticide impacts on
may vary substantially depending on foraging pat-
terns, nesting behavior, seasonal activity, and diurnal
ßight activity; all need to be considered in future
The signiÞcance of these data goes much beyond
just canola agroecosystems because these, and other
insecticides, are used on numerous horticultural and
Þeld crops that beneÞt from wild bee pollination.
Protecting wild bees from exposure to insecticides is
essential, particularly given their increasing impor-
promised. To this end, it is important to establish
for comparative assessment, before registration, of le-
thal and sublethal pollinator responses to novel insec-
ticides and other control products.
and Agri-Food CanadaÐLondon, Ontario for advice and use
of facilities and equipment throughout this study. We also
thank Amanda King for contributions while completing her
M.S. in the Scott-Dupree Agro-Eco Research Laboratory.
between the Natural Sciences and Engineering Research
Council of Canada (NSERC), Agriculture and Agri-Food
Canada, associated industrial collaborators: Bayer Crop-
Science, Dow AgroSciences, Crompton Co./CIE and Mon-
A.K. sponsored by Bayer CropScience.
Abbott, W. S. 1925. A method of computing the effective-
ness of an insecticide. J. Econ. Entomol. 18: 265Ð267.
Abbott, V. A., J. L. Nadeau, H. A. Higo, and M. L. Winston.
2008. Lethal and sub-lethal effects of imidacloprid on
Osmia lignaria and clothianidin on Megachile rotundata
(Hymenoptera: Megachildae). J. Econ. Entomol. 101:
Agriculture Canada. 1989. Alfalfa leafcutter bee manage-
ment in Western Canada. Publication 1495/E., Ottawa,
Allen-Wardell, G., P. Bernhardt, R. Bitner, A. Burquez, S.
Buchmann, J. Cane, P. A. Cox, V. Dalton, P. Feinsinger,
M. Ingram, et al. 1998. The potential consequences of
pollinator declines on the conservation of biodiversity
and stability of food crop yields. Conserv. Biol. 12: 8Ð17.
B. J. Harris. 2005. Contact and oral toxicity to honey
bees (Apis mellifera L.) of agents registered for use for
Canola Council of Canada. 2007. Growing canola. Canola
Councilof Canada. (http://canola-council.org/icp.
Corbet, S. A., M. Fussell, M. Ake, R. Fraser, C. Gunson, A.
Savage, and K. Smith. 1993. Temperature and the polli-
nation activity of social bees. Ecol. Entomol. 18: 17Ð30.
Cutler, G. C., and C. D. Scott-Dupree. 2007a. Novaluron:
Technol. 1: 38Ð46.
Cutler, G. C., and C. D. Scott-Dupree. 2007b. Exposure to
on honey bees. J. Econ. Entomol. 100: 765Ð772.
Delaplane,K.S.,andD.F.Mayer. 2000. Croppollinationby
bees. CABI Publishing, New York.
Devillers, J., A. Decourtye, H. Budzinski, M. H. Pham-Dele-
gue, S. Cluzeau, and G. Maurin. 2003. Comparative tox-
icity and hazards of pesticides to Apis and non-Apis bees.
A chemometrical study. SAR QSAR Environ. Res. 14:
Dogterom, M. H. 1999. Pollination by four species of bees
Biological Sciences, Simon Fraser University, Burnaby,
Dogterom, M. H. 2005. Pollination with mason bees. Bee-
diverse Publishing of CPC Ltd., Coquitlam, BC, Canada.
Franklin, M. T., M. L. Winston, and L. A. Morandin. 2004.
Effects of clothianidin on Bombus impatiens (Hymento-
ptera: Apidae) colony health and foraging behaviour. J.
Econ. Entomol. 97: 369Ð373.
Free, J. B. 1993. Insect pollination of crops, 2nd ed. Aca-
demic, San Diego, CA.
Harris,C.R.,andH.J.Svec. 1969. Laboratorystudiesonthe
contact toxicity of some insecticides to honeybees. Proc.
Entomol. Soc. Ont. 100: 165Ð167.
Johansen, C. A., D. F. Mayer, J. Eves, and C. W. Kious. 1983.
Pesticides and bees. Environ. Entomol. 12: 1513Ð1518.
Kearns, C. A., D. W. Inouye, and N. M. Waser. 1998. En-
interactions. Annu. Rev. Ecol. Syst. 29: 83Ð112.
Kevan, P. 1999. Pollinators as bioindicators of the state of
the environment: species, activity, and diversity. Agric.
Ecosyst. Environ. 74: 373Ð393.
Kevan,P.,andT.P.Phillips. 2001. Theeconomicimpactsof
pollinator declines: an approach to assessing the conse-
quences. Conserv. Ecol. 5: 8.
Klein, A. M., B. E. Vaissiere, J. H. Cane, I. Steffan-Dewenter,
S. A. Cunningham, C. Kremen, and T. Tscharntke. 2007.
Importance of pollinators in changing landscapes for
world crops. Proc. R. Soc. Biol. Sci. 274: 303Ð313.
Kremen, C., N. M. Williams, and R. W. Thorp. 2002. Crop
pollination from native bees at risk from agricultural
intensiÞcation. Proc. Natl. Acad. Sci. 99: 16812Ð16816.
Macedo, P. A., M. D. Ellis, and B. D. Siegfried. 2002. De-
tection and quantiÞcation of ßuvalinate resistance in
varroa mites in Nebraska. Am. Bee J. 142: 523Ð526.
Malone, L. A., C. D. Scott-Dupree, J. H. Todd, and P. Ra-
mankutty. 2007. No sub-lethal toxicity to bumblebees,
Bombus terrestris, exposed to Bt-corn pollen, captan and
novaluron. N Z J. Crop. Hortic. Sci. 35: 435Ð439.
Matheson, A., S. I. Buchman, C. O’Toole, P. Westrich, and
I. H. Williams. 1996. The conservation of bees. Aca-
demic, Harcourt Brace, London, United Kingdom.
Maus, C., G. Cure, and R. Schmuck. 2003. Safety of imida-
cloprid seed dressings to honey bees: a comprehensive
overview and compilation of the current state of knowl-
edge. Bull. Insectol. 56: 51Ð57.
Mayer, D. F., G. Kovacs, and J. D. Lunden. 1998. Field and
Megachile rotundata, Nomia melanderi. J. Apic. Res. 37:
Morandin, L. A., and M. L. Winston. 2003. Effects of novel
pesticides on bumble bee (Hymentoptera: Apidae) col-
ony health and foraging ability. Environ. Entomol. 32:
Morandin, L. A., and M. L. Winston. 2005. Wild bee abun-
dance differences in conventional, organic and geneti-
February 2009SCOTT-DUPREE ET AL.: IMPACT OF INSECTICIDES ON BEES
cally modiÞed canola and its effect on seed production.
Ecol. Appl. 15: 871Ð881.
Morandin, L. A., M. L. Winston, M. T. Franklin, and V. A.
Abbott. 2005. Lethal and sub-lethal effects of spinosad
on bumble bees (Bombus impatiens Cresson). Pest
Manag. Sci. 61: 619Ð626.
[NRC] National Research Council. 2007. Status of pollina-
tors in North America. National Academies Press, Wash-
Oldroyd, B. P. 2007. WhatÕs killing American honey bees?
PloS Biol. 5: 1195Ð1199.
[OMAFRA] Ontario Ministry of Agriculture, Food and Ru-
ralAffairs. 2006. Fieldcropprotectionguide2006Ð2007.
812. QueenÕs Printer for Ontario, Toronto, ON, Canada.
Potter, C. 1952. An improved laboratory apparatus for ap-
plying direct sprays and surface Þlms, with data on the
electrostatic charge on atomized spray ßuids. Ann. Appl.
Biol. 39: 1Ð28.
SAS Institute. 2001. PROC usersÕ manual, version 8.02 ed.
SAS Institute, Cary, NC.
Stark,J.D.,P.C.Jepson,andD.F.Mayer. 1995. Limitations
to use of topical toxicity data for predictions of pesticide
side effects in the Þeld. J. Econ. Entomol. 88: 1081Ð1088.
Statistics Canada. 2007. Field and specialty crops-seeded
area (2003Ð2007). (http://www40.statcan.ca/101/cst01/
Tasei,J.N. 2002. Impactofagrochemicalsonnon-Apisbees,
pp. 101Ð131. In J. Devillers and M.-H. Pham-Delegue
of chemicals. Taylor & Francis, New York.
Tasei, J. N., G. Ripault, and E. Rivault. 2001. Hazards of
imidacloprid seed coating to Bombus terrestris (Hyme-
noptera: Apidae) when applied to sunßower. J. Econ.
Entomol. 94: 623Ð627.
Thompson,H.M.,andL.V.Hunt. 1999. Extrapolatingfrom
honeybees to bumblebees in pesticide risk assessment.
Ecotoxicology 8: 147Ð166.
Westerkamp, C., and G. Gottsberger. 2000. Diversity pays
in crop pollination. Crop Sci. 40: 1209Ð1222.
Williams, I. H. 1996. Aspects of bee diversity and crop pol-
lination in the European Union, pp. 64Ð80. In A. Mathe-
son, S. Buchmann, C. OÕToole, P. Westrich, and I. H.
Williams [eds.], The conservation of bees. Academic,
Toronto, ON, Canada.
D.T.Stewart. 2008. FirstdetectionofNosemaceranae,a
microsporidian parasite of European honey bees (Apis
meliifera), in Canada and central USA. J. Invertebr.
Pathol. 97: 189Ð192.
Received 2 July 2008; accepted 16 September 2008.
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