Genetic and Usurpation Data Support High Incidence of Bumble Bee Nest Invasion by Socially Parasitic Bumble Bee, Bombus insularis - Oxford ...
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Journal of Insect Science, (2021) 21(5): 3; 1–7
https://doi.org/10.1093/jisesa/ieab063
Research
Genetic and Usurpation Data Support High Incidence of
Bumble Bee Nest Invasion by Socially Parasitic Bumble
Bee, Bombus insularis
Jonathan Berenguer Uhuad Koch,1, Lindsie M. McCabe, Byron G. Love, and
Downloaded from https://academic.oup.com/jinsectscience/article/21/5/3/6363718 by guest on 03 November 2021
Diana Cox-Foster
Department of Agriculture, Agricultural Research Service, Pollinating Insect–Biology, Management, Systematics Research Unit,
Logan, UT 84341, USA and 1Corresponding author, e-mail: jonathan.koch@usda.gov
Subject Editor: Guy Bloch
Received 4 March 2021; Editorial decision 6 August 2021
Abstract
Cuckoo bumble bees (Psithyrus) (Lepeletier, 1832) (Hymenoptera: Apidae) are a unique lineage of bees that
depend exclusively on a host bumble bee species to provide nesting material, nutritional resources, and labor to
rear offspring. In this study, we document usurpation incidence and population genetic data of Bombus insularis
(Smith, 1861) (Hymenoptera: Apidae), a bumble bee species in the Psithyrus subgenus, on field-deployed B. huntii
colonies in northern Utah, United States. Within 12 d of deploying B. huntii Greene, 1860 (Hymenoptera: Apidae)
colonies at two field sites, 13 of the 16 colonies contained at least one established B. insularis female. Although
our results demonstrate that field-deployed bumble bee colonies are highly susceptible to B. insularis usurpation,
applying a fabricated excluder to prevent the inquiline from invading a colony was 100% effective. Sibship analysis
using microsatellite genotype data of 59 B. insularis females estimates that they originated from at least 49 unique
colonies. Furthermore, sibship analysis found siblings distributed between the field sites that were 7.04 km apart.
Our result suggests that B. insularis females have the capacity to disperse across the landscape in search of host
colonies at distances of at least 3.52 km and up to 7.04 km. Our study underscores the detrimental impact B. insularis
usurpation has on the host bumble bee colony. As B. insularis significantly impacts the success of bumble bee
colonies, we briefly discuss how the utilization of excluders may be useful for commercial bumble bee colonies that
are used to pollinate open field crops.
Key words: cuckoo bumble bee, inquiline, dispersal, bombiculture, Psithyrus excluder
There are more than 260 described species of bumble bees (Apidae: colonies, kill the foundress queen, and coerce the host workers to
Bombus L.), with species richness peaking in predominantly tem- care for her young.
perate and alpine environments (Cameron et al. 2007, Hines 2008, There are 28 described species of bumble bees in the subgenus
Williams et al. 2014). Bumble bees are primitively eusocial insects Psithyrus, all of which are obligate social parasites (Lhomme and
with an annual life cycle (Lhomme and Hines 2019). The life cycle Hines 2019). Unlike other bumble bees, Psithyrus species lack cor-
begins with a gyne emerging from the ground in the spring months biculae, do not produce a worker caste, and do not have the cap-
to search for a nest location. Once a site is identified, the found- acity to produce wax necessary for nest construction. Because of
ress gyne (now queen) raises a colony of female workers followed these biological differences, Psithyrus species depend exclusively
by sexuals, i.e., gynes and drones. Gynes, which subsequently leave on non-Psithyrus bumble bee workers to rear their own offspring.
the colony after they emerge from their cocoon, are pursued by Upon entering a bumble bee nest, a Psithyrus female will attempt
drones when they are receptive to mating. At the end of the bumble to kill or suppress the queen and coerce the workers into rearing
bee colony cycle, the foundress queen, female workers, and drones her offspring (Strange et al. 2014). In some cases, the Psithyrus fe-
die. The newly mated gynes find a space in the ground suitable for male will also kill some of the adult workers during the usurpation
hibernacula and undergoes diapause. However, one group of bumble event. If the takeover is successful, the Psithyrus female will lay her
bees in the subgenus Psithyrus (Lepeletier, 1832) have evolved a eggs in the nest, both males and females, which the host workers
unique reproductive strategy that bypasses the work of nest building will care for until they emerge as adults. Ultimately, the takeover
and brood raising. Psithyrus females invade other bumble bee by a Psithyrus female results in the loss of reproduction of the host
Published by Oxford University Press on behalf of Entomological Society of America 2021.
This work is written by (a) US Government employee(s) and is in the public domain in the US.
1
2 Journal of Insect Science, 2021, Vol. 21, No. 5
colony, resulting in no successful output of gynes for the host colony (PIRU). In the laboratory, individual queens were placed in a small
(Lhomme and Hines 2019). plastic rearing chamber (178 × 152 × 101 mm) and initially fed
There are six described species in the bumble bee subgenus a 2-g provision of commercial pollen mixed with artificial nectar
Psithyrus in the United States and Canada, making up 13% of (i.e., pollen loaf). In turn, each chamber was placed on a bladder
the described bumble bee species in this region (Williams et al. filled with artificial nectar. Once the queen produced five workers,
2014). The six species are B. variabilis (Cresson, 1872), B. citrinus the chamber was transferred to a larger plastic colony box (292 ×
(Smith, 1854), B. insularis (Smith, 1861), B. suckleyi Greene, 1860, 229 × 127 mm) and monitored. Colonies were fed pollen loaves
B. bohemicus Seidl, 1837 [including B. ashtoni (Cresson, 1864)], and additional artificial nectar ad libitum. “Rocky Mountain”
and B. flavidus Eversmann, 1852 [including B. fernaldae (Franklin, pollen was purchased from Moon Shine Trading Company (https://
1911)]. Because Psithyrus depends exclusively on other bumble bee zspecialtyfood.com/product/delicious-fresh-bee-pollen/) and steril-
species to reproduce, they are sensitive to the population dynamics ized with ethylene oxide to reduce the abundance of known patho-
of their host species (Antonovics and Edwards 2011) and subject gens to be associated with honey bee-collected pollen. Materials and
to conservation concerns. For instance, B. bohemicus is endan- protocol for preparing pollen loaves and artificial nectar solution are
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gered in Canada, with its decline linked to the decline of its hosts found in Appendix 3 of Smith et al. (2020).
(COSEWIC 2014). Bombus suckleyi and B. variabilis have been
identified as critically endangered by the International Union for Field Study
the Conservation of Nature Red List (Hatfield et al. 2014). Bombus Colonies were deployed when they reached a minimum of five
suckleyi is currently being petitioned for protection under the workers (x̄ = 7. 43 ± 0.99 SE, range = 3–20). In total, 16 initial
United States Endangered Species Act (Hatfield et al. 2014, Center colonies were randomly deployed at one of two field sites (8 col-
for Biological Diversity 2020). onies per site) on 10 June 2020 in the Cache National Forest. One
Although some North American Psithyrus bumble bee species field site was adjacent to a commercial apiary of 48 honey bee hives,
are exhibiting concerning trends of population decline and range re- hereafter presented as the apiary site (41.69, −111.46). The other
duction, other species are of least concern and, in some instances, site was 7.04 km away from the apiary, hereafter presented as the
may be considered pests to agriculture (Strange et al. 2014). For ex- nonapiary site (41.75, −111.47). Managed honey bee hives have
ample, the Indiscriminate Cuckoo Bumble Bee, B. insularis, is asso- been used on the apiary field site for more than 20 yr (D. Cox, per-
ciated with the most documented bumble bee hosts of all Psithyrus sonal communication), whereas we could find no evidence of man-
species (Lhomme and Hines 2019). Twelve species in six bumble aged honey bee hives ever being placed at the nonapiary field site.
bee genera are documented to be hosts of B. insularis (Lhomme and Bumble bee colonies were placed inside a plastic container with an
Hines 2019). Furthermore, attempted usurpation by B. insularis aerated plenum (to prevent overheating) on top of a table in the field
of commercial honey bee hives (Apis mellifera L.) has been docu- (Fig. 1), approximately 1 m off the ground. Colonies were protected
mented, as evidenced by deceased B. insularis females outside of from wild and domesticated animals using an electrified fence, and
hives in apiaries (Strange et al. 2014). Bumble bee colonies reared in Tree Tanglefoot Insect Barrier was applied on the legs of each table
artificial domiciles placed above the ground (as is common in agri- to deter the invasion of insect pests. Artificial nectar bladders were
culture and research) are readily invaded by a number of species in removed from each colony 1 week after deployment to wean col-
the bumble bee subgenus Psithyrus, including B. insularis, with up to onies from supplemental feeding and encourage foraging on natur-
100% parasitism rates reported (Pelletier and McNeil 2003, Carvell ally occurring floral resources.
et al. 2008, Strange et al. 2014). Despite our efforts to protect the deployed B. huntii colonies
In this study, we report on the effect of B. insularis usurpation on from the elements and pests, we found live B. insularis females estab-
colonies of B. huntii Greene, 1860, reared in plastic domiciles and lished inside the B. huntii colonies during a routine inspection 12 d
deployed in the Bear River Mountains of northern Utah, USA. Upon after field deployment. Parasitism by B. insularis typically resulted in
discovering B. insularis usurpation of B. huntii colonies, we aimed the death of the B. huntii queen and some or all of her adult workers.
to determine the effectiveness of a fabricated plastic excluder placed In response to this incident, an additional eight colonies were de-
at the nest entrance of the domicile in reducing B. insularis usurp- ployed across the two field sites on 1 July 2020 (four colonies per
ation. Furthermore, we sought to determine the underlying popula- site), following the protocols described above. A plastic excluder was
tion genetic structure and diversity of wild B. insularis detected in subsequently fabricated with a single hole measuring 7 mm in diam-
B. huntii colonies across our field sites. Genetic analysis enabled us eter (Bees Love Trees S.P., North Logan, UT; https://beeslovetrees.
to estimate how far B. insularis females may disperse from a central com/) and affixed to the pollen trap (Judd et al. 2020) of all colonies.
location to seek out potential hosts. Based on the results of our study The size of the hole served three purposes: 1) prevented access to the
and a brief synthesis of the literature, we discuss how the widespread colony by B. insularis of noninvaded colonies; 2) allowed B. huntii
and abundant B. insularis may become a pest of commercial bumble workers the free access to forage for floral resources; and 3) pre-
bee colonies placed in an agricultural context. vented the escape of B. insularis gynes produced in invaded colonies
(for downstream genetic analysis). Pollen traps were used to collect
pollen loads from returning foragers as part of another ongoing pro-
Materials and Methods
ject. Traps were engaged for about 5 h every 2 wk to minimize nega-
Bumble Bee Rearing tive impacts due to their engagement. However, the plastic excluder
Eighty wild B. huntii queens emerging from winter dormancy were was engaged during the entire deployment of the colonies and there
net collected in the spring 2020 in northern Utah, United States, was no evidence that it negatively affected foraging by the workers.
at three primary field sites: North Logan (41.76, −111.81), Red At the conclusion of the study, the colonies were removed from
Butte Garden (40.77, −111.83), and Richmond (41.9, −111.79). the field sites and brought back to PIRU for inspection and decon-
Upon removal from the net, queens were transferred to a 10-dram tamination. The eight replacement colonies that were fixed with the
plastic collection vial and transported in a cooler to the United plastic excluder were not used in downstream analysis as they were
States Department of Agriculture, Agricultural Research Service, not invaded by B. insularis. All dead and alive B. insularis detected
Pollinating Insect–Biology, Management, Systematics Research Unit within a B. huntii colony and additional B. insularis netted in theJournal of Insect Science, 2021, Vol. 21, No. 5 3
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Fig. 1. Three artificial domiciles used to rear B. huntii colonies in situ. Nest entrance includes a pollen trap developed by Judd et al. (2020).
field were stored in 95% EtOH at PIRU for downstream population multiple comparisons for both populations and loci, respectively
genetic analysis. (Rice 1989). We considered the Bonferroni correction test significant
at P < 0.05.
DNA Extraction and Microsatellite PCR We estimated genetic diversity with three different metrics:
Amplification 1) allelic richness, 2) expected heterozygosity (He) using Nei’s gen-
etic metric, and 3) the private allelic richness. We tested for differ-
We extracted DNA from B. insularis females by macerating leg tissue
ences in genetic diversity using a Wilcoxon signed-rank test. Next,
from each specimen in 150 µl of 5% Chelex solution and 5 µl of
we performed an analysis of molecular variance (AMOVA) to test
Proteinase K (Strange et al. 2009). Samples were incubated for 1 h at
for differences in genetic structure across the two populations. We
55°C, 15 min at 99°C, 1 min at 37°C, and 15 min at 99°C. Extracted
identified full siblings across the two field sites by assigning individ-
DNA was then screened at 16 microsatellite loci: B96, B124, BT30,
uals to families (e.g., colonies) with Colony v2.0 (Jones and Wang
BT28, BTERN01, BTMS0081, BT10, BL13, BTMS0059, BTERN02,
2010). In this exercise, we set the mistyping error rate to 0.05 based
BTMS0062, BTMS0066, BTMS0086, B126, BTMS0083, BTMS0044
on error rates documented in previous studies (Lozier et al. 2011)
(Estoup et al. 1995, 1996; Reber Funk et al. 2006; Stolle et al. 2009).
and set the sex-determination systems to ‘haplodiploid’. Only one
Polymerase chain reactions (PCR) for each locus were multiplexed
representative from each full-sibling family (≥95% genotype simi-
in a final reaction volume of 10 µl, containing approximately 1 µl of
larity) was retained for downstream population genetic analysis.
extracted DNA, 1× Promega (Madison, WI) reaction buffer, 0.6 mM
Except for the Colony analysis, all population genetic analyses were
dNTP mixture, 0.2–0.4 µM primer, 1.4 mM MgCl2, 0.001 mg BSA,
conducted with the base, strataG, poppr, and adegent libraries in R
0.4 units Taq polymerase (Promega, Madison, WI), and ddH20 to
version 4.0.3 (R Core Team 2020). Data and R scripts to support
fill to volume. The thermal cycler for PCR began with denaturation
the described analysis are available at https://github.com/jbkoch/
at 95°C for 7 min, 30 cycles of 95°C for 30 s, annealing temperature
psythirus_blacksmithfork.
53°C for 1 min 30 s, 72°C for 30 s, and a final extension for 10 min
at 72°C. DNA amplifications were performed with fluorescent 5’
dye-labeled primers and separated on an Applied Biosystems 3730xl
automated sequencer. Alleles were scored manually using Geneious Results
Prime 2021.0.1 (https://www.geneious.com). Samples with more Field Study Analysis
than nine loci scored per individual were included in the popula- Of the initial 16 B. huntii colonies (each colony with ≤20 workers)
tion genetic analysis. Microsatellite data will be available on GitHub deployed on the 10 June 2020, 13 colonies had either a dead or alive
upon acceptance of this manuscript. B. insularis upon inspection on 22 June 2020 or 12 d after installation
(Fig. 2A and B; Table 1). The average and median number of dead
Population Genetic Analysis or alive B. insularis detected across colonies is 1.25 and 1, respect-
To determine population genetic diversity and sibship across the ively (n = 20, maximum = 5, minimum = 0; Table 1). Furthermore,
two B. insularis populations, we first are required to determine of the colonies found to be invaded by B. insularis at 12 d after de-
whether the microsatellite loci that were amplified in our study ployment, 5 of the 13 colonies contained dead B. huntii foundress
were in Hardy–Weinberg equilibrium (HWE) and that there was a queens (Table 1). Later in the season (19 d postinstallation), we also
nonrandom association of alleles at two or more loci (i.e., linkage detected up to eight dead B. insularis in a single B. huntii colony
disequilibrium [LD]). Deviations from HWE and LD of a locus re- that did not receive a B. insularis excluder because it lost their queen
sulted in their removal from the final analyses. We tested for HWE early in the experiment (Fig. 2C). In this case, the small B. huntii
and LD with the Genepop algorithm (Raymond and Rousset 1995). colony completely failed as nearly all workers died or went missing.
Furthermore, sequential Bonferroni corrections were applied to the The installation of excluders in queen-right colonies and an add-
HWE and LD P-values to minimize type I errors associated with itional eight B. huntii colonies deployed on 1 July 2020 resulted in4 Journal of Insect Science, 2021, Vol. 21, No. 5
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Fig. 2. A selection of photos demonstrating (A) B. huntii colony development without B. insularis female inquiline, (B) B. huntii colony development with
B. insularis inquiline (dead B. huntii queen removed from colony), (C) attempted usurpation and death of eight B. insularis females in a poorly-developed
B. huntii colony (all B. insularis are in photograph), and (D) the utility of a Psithyrus excluder (yellow-colored gate with 7-mm-diameter hole that is attached to
pollen trap developed by Judd et al. 2020) in preventing usurpation by B. insularis female (see Supp Material 1 [online only] for video documentation). Orange
arrow identifies B. huntii queen; black arrow identifies B. insularis female.
100% exclusion of subsequent usurpation by B. insularis (Fig. 2D). We found no significant differences in expected heterozygosity
Video documentation of an attempted usurpation by a B. insularis (Wilcox test: W = 28, P = 0.71), allelic richness (Wilcox test:
female on a B. huntii colony outfitted with an excluder is provided in W = 27.5, P = 0.75), or number of private alleles (Wilcox test:
Supp Material 1 (online only). Finally, in addition to dead B. insularis W = 30.5, P = 0.47) between the two sampling sites of B. insularis
being documented in deployed B. huntii colonies, we also detected (Table 2). Furthermore, AMOVA results found only 0.20% of the
dead B. fervidus Fabricius, 1798 (n = 2) and B. vancouverensis genetic variation among the two populations, 11.56% among indi-
Cresson, 1878 (n = 1) queens in the colonies that did not receive a viduals within the two populations, and 88.21% within individuals.
B. insularis excluder, serving as evidence for attempted usurpation The lack of genetic variation partitioned among the two popula-
by these non-Psithyrus bumble bees. tions or sampling sites is supported by low genetic structure (overall
FST = 0.05, P = 0.41; FIS = −0.002, P = 0.59; Table 3).
Of the 59 B. insularis analyzed (field-netted and B. huntii colony-
Population Genetic Analysis
collected individuals), we identified six colonies consisting of at least
Four loci (BT30, B96, BTMS0083, BL13) did not consistently amp-
two or more full sibships (Family IDs: 10, 13, 19, 22, 25, 36; Supp
lify across B. insularis specimens and were excluded from continued
Information 4 [online only]). Individuals were considered full sib-
analysis. Of the remaining 11 loci, only seven loci were found to be
lings in the colony analysis if the inclusion probability (i.e., genotype
in HWE after Bonferroni corrections: BT10, BTERN01, BTERN02,
similarity) was ≥95%. Two full sibship families were composed of
BTMS0066, BTMS0081, BTMS0062, and BRMS0086 (all
B. insularis females that were found at both the apiary and nonapiary
P > 0.05). B124, BT28, BTMS0044, and BTMS0059 were not in
sites over the course of the 12 d in the beginning of B. huntii colony de-
HWE (all P < 0.05). Of the 55 pairwise loci comparisons, only five
ployment (Family IDs: 22 and 36; Supp Information 4 [online only]).
loci comparisons exhibited significant LD. All five loci comparisons
We did not detect full siblings for 35 (85%) of the B. insularis females.
that exhibited significant LD involved BT28 (BTMS0044, BTMS0059,
BTMS0081, BT10, and B124). Given the results of the HWE and LD
analysis, we elected to retain BT10, BTERN01, BTERN02, BTMS0066,
BTMS0081, BTMS0062, and BRMS0086 for final analyses. BTMS0081 Discussion
was retained for the analysis as it was in HWE. See Supp Information 2 In our study, we found that B. insularis readily invaded early-stage
and 3 (online only) for HWE and LD results, respectively. B. huntii colonies in artificial domiciles that were not equipped withJournal of Insect Science, 2021, Vol. 21, No. 5 5
Table 2. Genetic diversity metrics of B. insularis at two field sites in
B. insularis females
Number of dead
northern Utah (June 2020)
Site Locus He Allelic Number of
0
0
0
0
0
0
0
0
0
0
0
0
1
3
0
0
richness private alleles
Apiary BT10 0.73 0.45 4
Apiary BTERN01 0.66 0.32 3
Apiary BTERN02 0.84 0.42 3
B. insularis females
Apiary BTMS0066 0.72 0.35 3
Number of live
Apiary BTMS0081 0.67 0.25 2
Apiary BTMS062 0.95 0.83 6
0
1
1
1
1
0
2
1
1
1
2
1
0
1
2
1
Apiary BTMS086 0.71 0.33 3
Table 1. Summary of B. insularis usurpation of deployed B. huntii colonies in northern Utah on 22 June 2020. Queen-Right = B. huntii foundress queen present
Nonapiary BT10 0.75 0.46 4
Nonapiary BTERN01 0.62 0.25 1
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Nonapiary BTERN02 0.88 0.50 5
Queen-Right
Nonapiary BTMS0066 0.70 0.32 2
Nonapiary BTMS0081 0.69 0.26 2
0
0
1
0
1
1
0
1
1
0
1
0
0
1
0
1
Nonapiary BTMS062 0.93 0.75 4
Nonapiary BTMS086 0.65 0.27 2
Mean 0.75 0.41 3.14
SEM 0.03 0.05 0.36
time of B. insularis invasion
Number of workers dead at
Table 3. Results of analysis of molecular variance (AMOVA) for
B. insularis (n = 49) at two field sites (apiary vs nonapiary) based
0
3
0
0
0
9
1
0
0
0
9
7
0
7
0
23
on the allele frequencies of seven loci
Source of variation df Sum of Variance % Variation
squares components
Between populations 1 5.00 0.01 0.20
Between individuals 47 215.65 0.48 11.58
time of B. insularis invasion
Number of workers alive at
within populations
Within individuals 49 178.05 3.63 88.21
Total 97 398.70 4.12 100
4
5
4
6
6
10
6
3
13
15
15
8
3
4
5
6
Source of variation is described as follows: Between populations = genetic
variation partitioned across apiary and nonapiary populations; Between indi-
viduals within populations = genetic variation partitioned among individuals
within a population (apiary or nonapiary populations); and Within individ-
uals = genetic variation partitioned within each individual.
FIS = 0.05, P = 0.41; FST = −0.002, P = 0.59.
Number of workers
at deployment
excluders. In total, 13 of the 16 colonies were invaded by B. insularis,
5
7
9
7
5
5
11
5
4
8
7
3
10
7
6
20
implicating the species to be highly successful at usurping bumble bee
colonies deployed in artificial domiciles (Pelletier and McNeil 2003,
Carvell et al. 2008, Sramkova and Ayasse 2009, Strange et al. 2014).
The invaded colonies did not survive until the end of the season
and did not produce sexuals as the host queen was terminated by
(g) at deployment
B. insularis. Furthermore, additional B. insularis females were found
Colony weight
near honey bee colonies at the apiary site either in flight or dead on
499
532
528
510
545
498
531
519
479
488
517
514
540
524
527
513
the ground next to the colonies (Strange et al. 2014).
Our study failed to find significant differences in genetic diver-
sity and structure across the study sites. However, this result is not
surprising given that non-Psithyrus species are suspected to dis-
perse and potentially migrate across great distances to nesting sites
Site location
Nonapiary
Nonapiary
Nonapiary
Nonapiary
Nonapiary
Nonapiary
Nonapiary
Nonapiary
and hibernacula (Lepais et al. 2010, Jha 2015, Koch et al. 2018,
Fijen 2020). We found genetic evidence for full-sibling females
Apiary
Apiary
Apiary
Apiary
Apiary
Apiary
Apiary
Apiary
present at both of the field sites, which were 7.04 km apart. These
B. insularis female siblings were found on the same date in the early
part of the season. Although it is possible that hibernacula of the
siblings may be centrally located between two field sites (3.52 km),
HUN064
HUN056
HUN060
HUN043
HUN044
HUN052
HUN027
HUN037
HUN019
HUN023
HUN026
HUN012
HUN013
HUN007
HUN009
HUN010
Colony
we are the first to document the dispersal potential of B. insularis fe-
males in search of a host colony. Our estimates of B. insularis female
ID6 Journal of Insect Science, 2021, Vol. 21, No. 5
dispersal are comparable to research on queens of other bumble bee you!) to T. Lindsay, J. Knoblett, A. Teague, J. Tabor, J. Pugsley, B. Redman,
species, which demonstrate that queens can disperse up to 8 km M. Hagadorn, C. Huntzinger, and A. Rohde for their assistance in this study,
away from their origin (Lepais et al. 2010). specifically in light of the ongoing coronavirus (COVID-19) pandemic and
the added safety practices to help prevent exposure to the virus. We thank
Bombus insularis and other Psithyrus species are critically de-
Tim McCabe for supporting efforts to produce the excluders. This project
pendent on their host population. If the host population is small
was funded in part by a grant from Project Apis m. to D. Cox-Foster, J. Koch,
and dispersed, it is likely that the fitness of Psithyrus species will
L. McCabe, and B. Love. The United States Department of Agriculture, Agri-
decrease due to the inability to secure a host colony (Lhomme and cultural Research Service (USDA-ARS) is an equal opportunity/affirmative ac-
Hines 2019). In our study, 13 B. huntii research colonies were tion employer and all agency services are available without discrimination.
readily invaded by at least 20 B. insularis. In some colonies, mul- The mention of commercial products and organizations in this manuscript is
tiple females were detected. Given the abundance of B. insularis solely to provide specific information. It does not constitute an endorsement
detected in B. huntii colonies in our study, we hypothesize that by USDA-ARS over other products and organizations not mentioned.
the high detection of this species in our study area is evidence of
robust and healthy bumble bee communities, specifically since we
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detected four host bumble bee species of B. insularis in the area Author Contributions
including B. fervidus, B. vancouverensis, B. huntii, and the imperiled
J.B.U.K.: Conceptualization; Data Curation; Formal analysis; Funding acqui-
B. occidentalis (Lhomme and Hines 2019). Sheffield et al. (2013)
sition; Investigation; Methodology; Project administration; Resources; Soft-
suggest that kleptoparasites such as Psithyrus represent the apex of ware; Supervision; Validation; Visualization; Writing – original draft; Writing
the bee communities and are the first guild to respond to environ- – reviewing & editing. L.M.M.: Funding acquisition; Investigation; Resources;
mental and biological disturbances. Furthermore, the lack of signifi- Writing – original draft; Writing – reviewing & editing. B.G.L.: Funding acqui-
cant differences in genetic diversity is an important discovery since it sition; Investigation; Resources; Writing – original draft; Writing – reviewing
suggests that the honey bee apiary may not be impacting the native & editing. D.C.F.: Conceptualization; Funding acquisition; Investigation; Re-
bee populations in the previous season or that this long-term apiary sources; Supervision; Validation; Writing – original draft; Writing – reviewing
has not had a lasting impact. However, further research is needed & editing.
to determine other aspects of wild bee health in response to sym-
patric apiary placement (e.g., floral resource interactions, pathogen
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