Evidence of Bumble Bee Extirpation and Colonization, Galiano Island, British Columbia, Canada

Abstract

We present evidence for historical change in a bumble bee community on Galiano Island, British Columbia, Canada, including the probable extirpation of three bumble bee species—Bombus insularis Smith, B. occidentalis Greene, and
B. suckleyi Greene—as well as the disappearance of two species represented by singletons in the historical record:
B. fervidus Fabricius and B. flavidus Eversmann. Evidence is based on a comparison of historical and contemporary species occurrence data, including recent data from intensive sampling targeting bumble bees using blue vane traps. The decline of B. occidentalis in southern portions of its range has long been observed, yet to our knowledge this is the first established case of its probable extirpation within an extensively surveyed part of its range. Results indicate that an additional species, B. vosnesenskii Radoszkowski, is a recent arrival on Galiano Island and has been expanding its range concurrently with the decline of B. occidentalis. Elsewhere in the region B. vosnesenskii has become a dominant species, particularly in urban environments. However, our data show it to be the least abundant species on this largely forested island. We also report patterns in the occurrence of B. sitkensis Nylander and B. vosnesenskii, suggesting that niche segregation may confound the effect of competitive exclusion previously reported for these species. Potential factors contributing to this likely case of bumble bee extirpation and subsequent colonization are discussed in the context of Galiano Island’s historical land use and ecology. In conclusion, we assess the potential for community science to aid in the detection of ecological change via comparison of historical baseline and contemporary crowd-sourced biodiversity data.

Full text

206 Northwest Science, Vol. 96, No. 3–4, 2023
Andrew D. F. Simon1, School of Environmental Studies, University of Victoria, PO Box 1700 STN CSC, Victoria, British
Columbia V8W 2Y2 Canada
Lincoln R. Best, Department of Horticulture, Oregon State University, 2750 SW Campus Way, Corvallis, OR 97331
Brian M. Starzomski, School of Environmental Studies, University of Victoria, PO Box 1700 STN CSC, Victoria, British
Columbia V8W 2Y2 Canada
Evidence of Bumble Bee Extirpation and Colonization, Galiano Island,
British Columbia, Canada
Abstract
We present evidence for historical change in a bumble bee community on Galiano Island, British Columbia, Canada,
including the probable extirpation of three bumble bee species—Bombus insularis Smith, B. occidentalis Greene, and
B. suckleyi Greene—as well as the disappearance of two species represented by singletons in the historical record:
B. fervidus Fabricius and B. avidus Eversmann. Evidence is based on a comparison of historical and contemporary species
occurrence data, including recent data from intensive sampling targeting bumble bees using blue vane traps. The decline of
B. occidentalis in southern portions of its range has long been observed, yet to our knowledge this is the rst established
case of its probable extirpation within an extensively surveyed part of its range. Results indicate that an additional species,
B. vosnesenskii Radoszkowski, is a recent arrival on Galiano Island and has been expanding its range concurrently with the
decline of B. occidentalis. Elsewhere in the region B. vosnesenskii has become a dominant species, particularly in urban
environments. However, our data show it to be the least abundant species on this largely forested island. We also report
patterns in the occurrence of B. sitkensis Nylander and B. vosnesenskii, suggesting that niche segregation may confound
the effect of competitive exclusion previously reported for these species. Potential factors contributing to this likely case
of bumble bee extirpation and subsequent colonization are discussed in the context of Galiano Island’s historical land use
and ecology. In conclusion, we assess the potential for community science to aid in the detection of ecological change via
comparison of historical baseline and contemporary crowd-sourced biodiversity data.
Keywords: bumble bee community ecology, extirpation, colonization, rarefaction, ecological change
Introduction
Worldwide, bumble bees face increasing threats
associated with climate and anthropogenic land-
scape change, which have resulted in numerous
population declines and species range restrictions
(Szabo et al. 2012, Sanchez-Bayo and Goka 2014,
Kerr et al. 2015, Biella et al. 2017, Guzman et
al. 2021). In western North America, Bombus
occidentalis Greene is a well-established case of
species’ decline, with declines reported throughout
some southern portions of its range over the last
several decades (Colla and Ratti 2010, Committee
on the Status of Endangered Wildlife in Canada
[COSEWIC] 2014). The decline of B. occidentalis
has largely been attributed to pathogens associ-
ated with commercial rearing of bumble bees
in industrial agricultural settings, including the
parasitic fungus Vairimorpha bombi (Fantham
& Porter) Tokarev et al. (Rao and Stephen 2007,
Otterstatter and Thomson 2008, Colla and Ratti
2010, COSEWIC 2014, Graystock et al. 2016,
Grupe and Quandt 2020). Cuckoo bumble bees
(subgenus Psithyrus) associated with B. occidenta-
lis and other bumble bee species are also in decline,
signaling their vulnerability to uctuations in host
population densities (Antonovics and Edwards
2011, Williams et al. 2014, Hateld et al. 2015a).
Alongside the decline of B. occidentalis,
another bumble bee species—B. vosnesenskii
Radoszkowski—has undergone signicant range
expansion in coastal western British Colum-
bia (Fraser et al. 2012). Research suggests this
1Author to whom correspondence should be addressed.
Email: adfsimon@imerss.org

207Bumble Bee Extirpation and Colonization
species has come to occupy the niche left vacant
by B. occidentalis, showing high potential for
colonization, particularly in urban environments
where its dominance has been associated with
declines among other bumble bee species such as
B. sitkensis Nylander (McFrederick and LeBuhn
2006, Fraser et al. 2012, Cole et al. 2019).
Here we present evidence for historical change
in an insular bumble bee community, establishing
the probable extirpation of B. insularis (Smith), B.
occidentalis, and B. suckleyi Greene from Galiano
Island, British Columbia, Canada, and the island’s
recent colonization by B. vosnesenskii. We also
assess the disappearance of two additional species—
B. fervidus (Fabricius) and B. avidus Evers-
mann—represented by singletons in the historical
record. Evidence for these changes is based on
the rarefaction of: 1) historical species occurrence
data; 2) data collected through intensive sampling
using blue vane traps; and 3) observations on the
community-science platform iNaturalist (2022).
Set against the backdrop of Galiano Island’s land-
use history, these results corroborate previous
ndings concerning the causes of bumble bee
species declines and provide further insight into
the ecology of B. sitkensis and B. vosnesenskii.
Methods
Study Area
Galiano Island lies in the rain shadow of the
Olympic Mountains and the Vancouver Island
Ranges, in southern coastal British Columbia,
Canada, a region dened by its temperate Med-
iterranean-type climate, with mild, wet winters
and warm, dry summers (Klassen et al. 2015).
The combined effects of low precipitation, warm
temperatures, and high sunshine hours result in an
annual moisture decit during summer months,
which varies depending on precipitation (Moore
et al. 2010). Galiano Island remains relatively
intact ecologically, with about 24% of its land
base conserved in protected areas (Island Trust
Conservancy [ITC] 2018). Today, 78% of the
island landscape remains forested, with only 9%
converted for active human use, including rural
development and limited small-scale agriculture
(Emmings and Erickson 2004; Madrone Envi-
ronmental Services Ltd [MES] 2008, 2017; ITC
2018), though forestry and cumulative land-use
effects have altered habitats here, as throughout
the rest of British Columbia (Shackelford et al.
2018). Approximately 60% of the forested land
base comprises regenerating early seral and young
forests with dense canopy structure; the remainder
is in a mature to old-growth state (Emmings and
Erickson 2004). Galiano Island’s forests are mostly
coniferous, composed primarily of Douglas-r
(Pseudotsuga menziesii (Mirb.) Franco), western
redcedar (Thuja plicata Donn ex D. Don), and
grand r (Abies grandis (Douglas ex D. Don)
Lindl.), with pockets of moist deciduous forests
and dry woodlands, including bigleaf maple (Acer
macrophyllum Pursh), red alder (Alnus rubra
Bong.), arbutus (Arbutus menziesii Pursh), and
Garry oak (Quercus garryana Douglas ex Hook.),
species representative of British Columbia’s
Coastal Douglas-r Biogeoclimatic Zone (Klas-
sen et al. 2015).
Bumble Bee Sampling and Analysis
We sampled bumble bees as part of an ecological
study investigating the impact of seasonal drought
on plant-pollinator communities (Simon et al.
2021). Bumble bees were collected using blue
vane traps (Stephen and Rao 2005) systemati-
cally distributed across the landscape in a 2 × 2
factorial study design contrasting dry versus wet,
and disturbed versus undisturbed, site condi-
tions. However, there was an imbalance in the
study design due to difculties in logistics of site
selection and access. We selected eld sites and
stratied site conditions using terrestrial ecosys-
tem mapping data (MES 2008), spanning a broad
range of habitats representative of the Coastal
Douglas-r Biogeoclimatic Zone (Nuszdorfer et
al. 1991), including woodlands and associated
rock outcrop communities, wetlands, clearcuts,
hydro-line corridors, gardens, orchards, and elds.
Sites ranged in size from 0.21 to 6.3 ha and were
spaced between approximately 0.5 km and 23 km
apart (Figure 1). Sampling was conducted over
ve sample periods, from April through August
2018, across 24 eld sites, with three blue vane
traps allocated to each site (representing a single
sample), resulting in 119 samples (120 less one

208 Simon et al.
sample compromised due to human interference)
representing 47,896 individuals. Each sampling
period lasted 11 days—the time required to con-
currently estimate oral resources at each site.
We modelled the abundance of each bumble
bee species as a response to habitat types and
other environmental variables using generalized
linear mixed models (GLMMs) implemented
using ‘lme4’, and ‘glmmTMB’ in cases where
zero-ination proved problematic (Bates et al.
2015, Brooks et al. 2017). Note, however, that
estimates of oral resources and other aspects of
the ecological study conducted in 2018 are not
relevant to our analysis of historical change and
are therefore not reported as results.
Analysis of Historical Change
Two sources of contemporary species occurrence
data were compared with historical occurrence
data to inform our analysis of historical change
in these communities. These include: 1) speci-
mens (n = 47,896) collected from Galiano Island
using blue vane traps during our 2018 ecologi-
cal study, as described above; and 2) iNaturalist
(2022) observations of the local bumble bee fauna
(n = 238), dating from 2016 to 2021. All material,
including historical voucher specimens, were
carefully reviewed, and species determined with
reference to Williams et al. (2014).
Historical species occurrence data are based
on voucher specimens (n = 278) dated from
1970 to 2010, deposited at the Beaty Biodiver-
sity Museum in Vancouver, BC, Canada, and at
the Royal British Columbia Museum (RBCM)
in Victoria, BC. A total of 285 specimens were
databased in collections. However, 6 specimens
at the RBCM were only determined to genus
and could not be located during our visit to the
collection. One specimen was dated to 2017 and
thus was not included among historical records.
No other Galiano Island bumble bee collections
exist as far as the authors are aware. Historical
metadata indicate that specimens analysed in
this study were collected by ight intercept traps
(n = 193), aerial netting (n = 10), light traps
(n = 3), pitfall traps (n = 3), window traps (n = 2),
and otherwise unknown methods (n = 67). The
distribution of historical and contemporary species
occurrence data are presented in Figure 1. Data
from 2018 blue vane samples, including catalog
numbers for synoptic collections deposited at
the RBCM, are summarized in Table 1. Data and
R scripts for implementing analyses are available
on Dryad (2023). Historical and contemporary
species occurrence data were analysed by rarefac-
tion using ‘vegan’, R package v.2.5–5 (Oksanen
et al. 2019, R Core Team 2019) and the Chao2
estimator (Chao 1984) implemented using ‘fossil’
(Vavrek 2011) to estimate species richness, that
is, the number of unique species occurring within
historical and contemporary communities. We then
compared the similarity of rarefaction curves using
the R package ‘rareNMtests’ v.1.1 (Cayuela and
Gotelli 2014), testing the differences in historical
and contemporary species assemblages based on
null models. To do this, we followed the ecological
null hypothesis test procedure outlined in Cayuela
et al. (2015), which reveals whether samples are
more different than would be expected if they were
drawn from a single underlying assemblage. The
same null model test was applied to compare rar-
efaction curves based on iNaturalist observations
with those generated from blue vane trap samples,
to determine whether these two sampling methods
reliably converged on estimates of species richness
for the contemporary bumble bee community. In
these tests, Z scores represent the cumulative area
between the observed sample rarefaction curve
and the composite rarefaction curve; P-values
represent the probability of Z given the distribution
of simulated Z values; low P-values imply that
observed differences among samples in species
composition, richness and/or relative abundance
are improbable if the samples were drawn from
the same assemblage (Cayuela and Gotelli 2014).
For historical data, we used individual-based rar-
efaction to implement null model tests comparing
rarefaction of historical data with rarefaction of
data from iNaturalist observations and blue vane
samples. While historical voucher specimens may
be analysed as sample-based data, we followed
Osazuwa-Peters et al. (2018) in treating these data
as individual-based to control for differences in
random sampling effort and to facilitate compari-
son of rarefaction curves using null model tests.

209Bumble Bee Extirpation and Colonization
Taking this approach, bumble bees collected by blue
vane traps were necessarily treated as individuals
(n = 47,896) for comparison with individual-based
rarefaction curves in null model tests, though a
sample-based curve was also considered for these
data, which converged on the same estimate of
species richness.
Results
Ten bumble bee species were historically reported
for Galiano Island, represented by 278 specimens
in research collections: 1) Bombus fervidus; 2)
B. avidus; 3) B. avifrons Cresson; 4) B. insularis;
5) B. melanopygus Nylander; 6) B. mixtus Cresson;
7) B. occidentalis; 8) B. sitkensis; 9) B. suckleyi;
and 10) B. vancouverensis Cresson. Of these ten
species collected from 1970 to 2010, only ve
have since been detected. The other ve species—
B. fervidus, B. avidus, B. insularis, B. occiden-
talis, and B. suckleyi—have not been detected
through recent sampling (from 2016 to 2021).
Bombus fervidus is represented by a single indi-
vidual in historical collections, collected in 1985;
B. avidus is also represented by a single individual
collected in 1981. These two singletons belong to
a series of collections made on Galiano Island by
G. G. E. Scudder and S. G. Cannings and have been
veried as reliable records (Sydney G. Cannings,
Environment Canada, personal communication;
see supplemental material, available online only).
Figure 1. Choropleth map of bumble bee species richness based on historical records (1970 to 2010) and recent iNaturalist
observations (2016 to 2021) from Galiano Island, BC, Canada. Field sites from 2018 surveys are also indicated, as well
as historical collection sites for three bumble bee species (Bombus insularis. B. occidentalis, and B. suckleyi) reported
as extirpated in this study, and two species represented by singletons in the historical record (B. fervidus, B. avidus).
The six species (B. avifrons, B. melanopygus, B. mixtus, B. sitkensis, B. vancouverensis, B. vosnesenskii) presently
known to Galiano Island were widespread in 2018, occurring in samples from all 24 eld sites. Grid scale = 0.01°; at
this latitude, each cell represents about 82 ha.

210 Simon et al.
Bombus insularis (n = 18), B. occidentalis (n = 9),
and B. suckleyi (n = 26) have not been observed on
Galiano Island since 1990. An additional species,
B. vosnesenskii, was reported locally for the rst
time in 2017 based on an iNaturalist observation
(iNaturalist 2017) and subsequently conrmed
through blue vane sampling. In this observation,
the lateral view of the bumble bee permits the
determination of B. vosnesenskii based on the
absence of extensive yellow hairs on sternite 4,
the short even hair of the dorsum, and the absence
of dark hairs antero-medially on tergite 4, which
rules out B. caliginosus Frison. The presence of
B. vosnesenskii and absence of B. calignosus on
Galiano Island is supported by the determination
of specimens collected through intensive blue
vane sampling in 2018.
Six bumble bee species are currently known
to occur on Galiano Island (Figure 2, Table 2).
In 2018, we found that these six species occurred
throughout all habitats, with little variability in
community composition across the landscape
(Table 3). Only two species varied signicantly in
abundance between certain habitats: B. sitkensis
was signicantly more abundant in wet semi-
natural habitats than in dry modied habitats
(IRRWET.N. = 1.74DRY.M., P = 0.022); conversely,
B. vosnesenskii was signicantly more abundant
in dry modied habitats than in wet semi-natural
habitats (IRRDRY.M = 3.51WET.N., P < 0.001). Wet
modied habitats also hosted signicantly more
B. vosnesenskii individuals than in wet semi-natural
habitats (IRRWET.M. = 2.49WET.N., P = 0.015).
Rarefaction curves based on blue vane samples
and iNaturalist bumble bee community data both
reached an asymptote, predicting 6 species in the
present-day community (Figure 2b, 2c). When
treated as sample-based data, the rarefaction
curve based on blue vane samples also reached an
asymptote, converging on an estimate of 6 species
in the contemporary community, though it was
necessary to treat these data as individual-based
for comparison with historical and iNaturalist
data using null model tests. The rarefaction curve
based on historical specimen data did not reach
an asymptote at 278 iterations, as it was strongly
TABLE 1. Counts of bumble bee individuals sampled in 2018 blue vane surveys, summarized by species, caste (☿ = queen;
♀ = worker; ♂ = male), and monthly sampling periods. Catalog numbers are listed for specimens deposited at the
Royal British Columbia Museum. Note catalog numbers refer to a synoptic sample of each species, including rep-
resentatives of all castes.
Caste APR MAY JUN JUL AUG Total Catalog # (ENT021)
B. avifrons ☿405 1,772 369 161 94 2,801 012788, 012789, 012790,
012791, 012792, 012793,
012794, 012795, 012796
♀0160 273 1,432 115 1,980
♂0 4 36 696 105 841
B. melanopygus ☿147 128 169 70 31 545 012780, 012781, 012782,
012783, 012784, 012785,
012786, 012787
♀11,078 3,126 98 3 4,306
♂038 378 47 2465
B. mixtus ☿757 926 183 305 98 2,269 012798, 012799, 012800,
012801, 012802, 012803,
012804, 012805, 012806
♀0934 1,959 1,347 22 4,262
♂03 69 382 5 459
B. sitkensis ☿1,002 543 193 387 106 2,231 012807, 012808, 012809,
012810, 012811, 012812,
012813, 012814, 012815
♀21,216 1,968 1,036 17 4,239
♂0 101 396 380 9886
B. vancouverensis ☿1,035 1,770 386 158 160 3,509 012771, 012772, 012773,
012774, 012775, 012776,
012777, 012778, 012779
♀01,645 6,023 9,490 271 17,429
♂0 2 183 702 40 927
B. vosnesenskii ☿60 234 39 2 10 345 012763, 012764, 012765,
012766, 012767, 012768,
012769, 012770
♀064 151 142 28 385
♂0 0 13 3 117

211Bumble Bee Extirpation and Colonization
inuenced by the two singleton occurrences of
B. fervidus and B. avidus, with the Chao2 estima-
tor predicting 11 species in the historical bumble
bee community (Figure 2a). When singletons were
removed from the historical dataset, however, the
rarefaction curve reached an asymptote, estimat-
ing a richness of 8 species. Null models testing
rarefaction curves based on blue-vane sampling
(Z = 182966.6) and iNaturalist data (Z = 796.8)
against the curve generated from historical data
showed that the past community assemblage
signicantly differed from the present-day com-
munity (P = 0.005). The null model test comparing
the rarefaction curve of iNaturalist observational
data against the curve based on data from blue
vane sampling (Z = 52.4) indicated that the com-
munity did not signicantly differ (P = 0.115),
conrming that samples were randomly drawn
from the same underlying assemblage. This test,
combined with rarefaction curves shown in Figure
2, indicate that survey efforts based on intensive
Bombus-targeted sampling with blue vane traps,
as well as efforts based on iNaturalist observa-
tions, were sufcient to estimate the richness of
the contemporary bumble bee community.
Discussion
Extirpation: The Case of Galiano Island’s
Missing Bumble Bees
We documented signicant shifts in the com-
position of an insular bumble bee community,
with the apparent loss of half of the historically
occurring fauna and the recent arrival of Bombus
vosnesenskii, making Galiano Island an important
case study in ecological change. These ndings
coincide with regional trends documenting the
historical decline of B. occidentalis (Colla and
Ratti 2010, COSEWIC 2014) and the subsequent
expansion of B. vosnesenskii in British Columbia
(Fraser et al. 2012).
The case for the extirpation of B. fervidus,
B. avidus, B. insularis, B. occidentalis, and
B. suckleyi remains tentative, however, with sev-
eral caveats to be considered. According to the
International Union for Conservation of Nature
(IUCN 2012), “a taxon is presumed Extinct
(in our case, equivalent to Extirpated – locally
extinct) when exhaustive surveys in known and/
or expected habitat, at appropriate times (diurnal,
seasonal, annual), throughout its historic range
have failed to record an individual. Surveys should
Figure 2. Individual-based rarefaction curves of bumble bee
data, with 95% condence intervals: A) Historical
records (1970 to 2010, n = 278); B) iNaturalist
observations (2016 to 2021, n = 238); C) Blue vane
trap samples (2018, n = 47,896).

212 Simon et al.
be over a time frame appropriate to the taxon’s
life cycle and life form.” The evidence we pres-
ent, including one year of intensive blue vane
sampling targeting Bombus, as well as multiple
years of iNaturalist data, establishes the strong
likelihood that at least ve bumble bee species
historically known to Galiano Island no longer
occur. Our sampling focused on a diverse range
of habitats representative of the island landscape
(e.g., woodlands, wetlands, clearcuts, rural areas,
and gardens, all within a forested matrix), includ-
ing areas in the vicinity of historical collection
sites (Figure 1). Studies have consistently dem-
onstrated blue vane traps to be highly effective
at sampling large insects, particularly bumble
bees, though additional sampling methods may
be required to capture a complete picture of bee
communities (Stephen and Rao 2005, 2007; Rao
and Stephen 2007; Wilson et al. 2008; Geroff
et al. 2014; Buchanan et al. 2017; Gibbs et al.
2017; McCravy and Ruholl 2017; Rhoades et al.
2017). Studies have also shown blue vane traps
to be effective at passively sampling the species
concerned in this study, including B. fervidus,
TABLE 2. Specimen counts and proportional abundances of bumble bee species represented by: 1) historical collections;
2) iNaturalist observations; and 3) individuals captured in blue vane traps. Note: the proportional representation of
B. vosnesenskii in iNaturalist observations contrasts strongly with what was found in blue vane samples, indicating
a bias in community science observations toward disturbed environments (see Table 3).
Taxon
Historical specimens
(1970–2010)
iNat observations
(2016–2021)
Blue vane sampling
(2018)
n = 278 Proportion n = 238 Proportion n = 47,896 Proportion
Bombus fervidus 1 < 0.01 — — — —
Bombus avidus 1 < 0.01 — — — —
Bombus avifrons 80 0.29 38 0.16 5,622 0.12
Bombus insularis 18 0.06 — — — —
Bombus melanopygus 38 0.14 30 0.12 5,316 0.11
Bombus mixtus 53 0.19 23 0.10 6,990 0.15
Bombus occidentalis 90.03 — — — —
Bombus sitkensis 18 0.06 24 0.10 7,356 0.15
Bombus suckleyi 26 0.09 — — — —
Bombus vancouverensis 34 0.12 92 0.39 21,865 0.46
Bombus vosnesenskii — — 31 0.13 747 0.01
TABLE 3. Bumble bee community composition, expressed as the relative abundance of species per habitat type, based on
intensive blue vane sampling from April through August 2018. Bumble bee species: B. av. = B. avifrons, B. mel.
= Bombus melanopygus, B. mix. = Bombus mixtus, B. sit. = Bombus sitkensis, B. van. = Bombus vancouverensis,
B. vos. = Bombus vosnesenskii.
Bumble bee species
Habitat type
Number of
sites
Number of
samples B. av. B. mel. B. mix. B. sit. B. van. B. vos.
Dry semi-natural
(woodlands, rock outcrops,
meadows; DRY.N)
8 39 0.13 0.12 0.13 0.15 0.45 0.02
Dry modied
(clearcuts, hydro-line
corridors, etc.; DRY.M)
6 30 0.08 0.12 0.14 0.09 0.54 0.03
Wet semi-natural
(wetlands; WET.N)
4 20 0.12 0.08 0.17 0.26 0.36 < 0.01
Wet modied
(orchards, gardens,
elds, etc.; WET.M)
6 30 0.13 0.11 0.17 0.17 0.42 0.01

213Bumble Bee Extirpation and Colonization
B. avidus, B. insularis, B. occidentalis, and
B. suckleyi (Kimoto et al. 2012, Pampell et al. 2015,
Rhoades et al. 2016, Gibbs et al. 2017, Rivers et al.
2018). Nevertheless, additional targeted sampling
efforts may be necessary to conclusively establish
this case of bumble bee extirpation.
Because historical collection efforts are spatially
limited in extent, individual-based rarefaction
of historical biological specimen data could be
spatially biased. However, recent work has shown
individual-based rarefaction to be preferable to
spatially explicit rarefaction to control for differ-
ences in random sampling effort (Osazuwa-Peters
et al. 2018). Moreover, recent sampling across a
broad range of habitats revealed that bumble bee
species comprising the contemporary fauna are
relatively widespread on Galiano Island. Species
occurred throughout all habitats, and community
composition overall was relatively even across the
landscape, though two species varied signicantly
in abundance between certain habitats. Bumble
bees are known to have broad foraging ranges,
from 1.5 km (Osborne et al. 2008) to as far as
11.6 km (Rao and Strange 2012). Hence, in the
past, bumble bees were likely pervasive across
the extent of this relatively small island (27.5 km
in length and 1.6 km at its narrowest point) as
they are in the present day. Based on the overall
evenness of the communities sampled in 2018,
spatial autocorrelation is not likely to have been
a signicant source of bias in historical collec-
tion efforts, further justifying individual-based
rarefaction as an approach to comparing historical
and contemporary species occurrence data in this
study. With that said, historical collections are
biased toward the north end of the island, and
the occurrence of singletons suggests possible
unevenness in the distribution of the historical
fauna. Differences in habitat diversity between
the north and south ends of Galiano Island (with
more modied rural environs, open woodlands, and
rock outcrops toward the south end) could have
resulted in a biased picture of the historical com-
munity, especially with respect to species having
narrow habitat requirements, such as B. fervidus.
In this study, the historical bumble bee sample
size is small (n = 278). Our estimation of species
decline should thus be considered a minimum
estimate, as other species may well have occurred
on the island in the past. Additionally, while three
of the undetected species occurred in relatively
large numbers historically, two species (B. fervidus
and B. avidus) are represented by singletons in
the historical record. These singletons may rep-
resent small historical populations that have since
disappeared, or vagrants that never successfully
established on the island. The cuckoo bumble
bee B. avidus is a widespread holarctic species
(Lhomme et al. 2021), demonstrating a high
potential for dispersal. Bombus fervidus, on the
other hand, has a range limited to North America,
where it has shown a poorly understood but con-
sistent pattern of decline in relative abundance
since 1990 (Hateld et al. 2015b). In this case,
given its habitat preferences (open grassland, old
elds, and tallgrass habitats), it may have struggled
to get established on this forested island. Yet it
is also possible that certain habitats (e.g., rural
areas) were undersampled in the past, where
B. fervidus may have been well established.
The disappearance of B. occidentalis along
with the cuckoo bumble bees B. insularis and
B. suckleyi is interesting to note in light of known
parasitic relationships between these species
(Thorp et al. 1983, Williams et al. 2014). Yet
while B. insularis is a versatile parasite associated
with multiple species in the local fauna, several of
which persist today, B. suckleyi is not known to
associate with any species reported for the island
other than B. occidentalis. Bombus suckleyi thus
appears to have vanished as an obligate parasite
along with its host, consistent with trends else-
where (Hateld et al. 2015a, COSEWIC 2019).
Bombus suckleyi has not been detected in British
Columbia since 2013, despite extensive surveys,
though it may persist in northern parts of the
province where surveys have been less intensive
(COSEWIC 2019).
Parasitic associations among the Galiano Island
bumble bee fauna could have also resulted in
higher rates of infection by Vairimorpha bombi,
compounding the stressors aficting these species.
Four out of the ve species reported extirpated
from Galiano Island (B. fervidus, B. avidus,

214 Simon et al.
B. occidentalis, B. suckleyi) are frequently infected
by V. bombi (Gillespie 2010, Cameron et al. 2011,
Lozier et al. 2011, Cordes et al. 2012, Pampell et
al. 2015, McArt et al. 2017). Parasitic interactions
among cuckoo bumble bees and their hosts could
result in pathogen spillover involving V. bombi,
which here may have contributed to their mutual
demise. More work is necessary to evaluate the
threat of pathogens such as V. bombi, as some
bumble bee populations have demonstrated high
pathogen prevalence yet no indication of decline
(Koch and Strange 2012).
Other potential sources of environmental stress
on Galiano Island historically include apiculture,
logging, and reforestation, the last of which may
have resulted in the loss of habitat for some bumble
bees. Indeed, logging and subsequent reforestation
represents the most signicant landscape change
that has occurred on Galiano Island over the last
half century (MES 2008, 2017). Disturbance events
such as forest re and clearcuts can potentially
create habitat for pollinators (Hanula et al. 2015,
Korpela et al. 2015, Ponisio et al. 2016, Roberts
et al. 2017, Mola and Williams 2018); subsequent
forest succession may then result in declining bee
biodiversity (Rivers and Betts 2021). That said, the
importance of forests has largely been overlooked
to date in terms of the resources they provide for
bumble bees (Mola et al. 2021). The implications
of forest succession for bumble bee population
dynamics thus remain poorly understood.
Given the limited extent of agriculture on the
island, pesticide use is not likely an important
factor contributing to this case of bumble bee
extirpation. Other potential stressors include the
effects of bumble bee sex determination on genetic
diversity at low population sizes (Zayed and Packer
2005, Lozier et al. 2011). Due to its proximity to
other land masses, however, Galiano Island is
not a strictly insular system, remaining subject
to periodic migration or colonization by outside
populations. Indeed, local Indigenous knowledge
indicates that long-distance dispersal of bumble
bees does occur in this archipelago. According
to Rosemary Georgeson, an Indigenous resident
of Galiano Island, a large bumble bee was once
observed ying across the Salish Sea, landing
on her boar near the mouth of the Fraser River
(Rosemary Georgeson, personal communication;
see supplemental material). The details of this
account, including the size of the bumble bee,
the time of year, and apparent distance traveled,
are consistent with the long-range dispersal of a
new queen.
Colonization: The Arrival of Bombus
vosnesenskii
Bombus vosnesenskii was rst observed on Galiano
Island in 2017 and subsequently collected using
blue vane traps, marking another historical change
in the local fauna. Shifts in bumble bee community
composition may be expected to occur in the wake
of local extinction (extirpation) events, as in the
case of B. vosnesenskii’s recent range expansion
following the decline of B. occidentalis (Fraser
et al. 2012). Bombus vosnesenskii has become
dominant in many urban environments (McFred-
erick and LeBuhn 2006, Cole et al. 2019), though
we found it occurred relatively infrequently on
Galiano Island (Table 3). Researchers have previ-
ously suggested a threshold of urbanization that
must be crossed before B. vosnesenskii assumes
prominence in a community (McFrederick and
LeBuhn 2006). Thus, this species may be struggling
to establish on this largely forested island. On the
other hand, B. vosnesenskii’s low abundance may
simply be the result of its recent colonization of
Galiano Island.
Potential interactions between B. vosnesenskii
and B. sitkensis were also noted in this study.
We found B. sitkensis to be least abundant in dry
modied habitats where B. vosnesenskii was most
prevalent; conversely, B. sitkensis was most abun-
dant in wetland habitats where B. vosnesenskii was
least common. These ndings are consistent with
previous research citing the negative inuence of
B. vosnesenskii on bumble bee community rich-
ness in urban environments, where populations
of B. sitkensis have been found to be particularly
negatively affected (McFrederick and LeBuhn
2006, Cole et al. 2019). Researchers have postu-
lated that this effect may be due to competitive
exclusion; both B. sitkensis and B. vosnesenskii
are subterranean nesters, making them potential

215Bumble Bee Extirpation and Colonization
competitors for nesting habitat (McFrederick and
LeBuhn 2006). However, the signicant habitat
differences that we detected for these species
could simply indicate a preference for wetlands on
the part of B. sitkensis and for disturbed environ-
ments on the part of B. vosnesenskii. From this
perspective, our results indicate that the effect
of competitive exclusion previously reported for
these species could be confounded by, coincide
with, or be mitigated by niche segregation. Further
research is required to understand interactions
between these species given the recent arrival of
B. vosnesenskii on Galiano Island.
Conclusion
Baseline data are rare for many insect groups,
including bumble bees, making population analy-
sis difcult (MacPhail et al. 2019). As a result,
important pollinator species may undergo dra-
matic declines unnoticed (Buchmann and Nabhan
1996). Our study demonstrates the efcacy of
two forms of search effort in detecting ecological
change in a bumble bee community with reference
to a historical baseline dataset comprising 278
museum specimens. Rarefaction curves generated
from intensive blue vane sampling and iNaturalist
observations converged on the same estimate of
bumble bee species richness. Comparison of both
sources of contemporary species occurrence data
against historical data enabled the detection of
changes in community composition, though as
a caveat it should be noted that the local species
pool (maximum of 10 species) and study area
(57 km2) were small.
Blue vane traps are optimal for sampling
large insects such as bumble bees (Stephen
and Rao 2005), yet as the results of this study
demonstrate, they can also result in high mortal-
ity. This mortality is of particular concern with
respect to social insects such as bumble bees,
for which passive sampling of queens during
the early spring period could negatively affect
populations (Gezon et al. 2015, Gibbs et al.
2017). Our ndings demonstrate that bumble
bee surveys need not necessarily be so intensive,
however, depending on research goals, as well
as the size of the species pool and the area under
study. Further research deploying alternative
sampling methods alongside blue vane traps and
iNaturalist is necessary to compare their efcacy
in estimating species diversity, richness, and
evenness in bumble bee communities. Developing
a non-lethal methodology for reliably surveying
bumble bee communities is critical to promote
more sustainable and compassionate wildlife
research practices in the future (Tepedino and
Portman 2020, Zemanova 2020).
In this study, iNaturalist observations crowd-
sourced over the timespan of 5 years produced
a reliable estimate of species richness, compa-
rable to estimates obtained through intensive
sampling using blue vane traps. These results
indicate that iNaturalist might be harnessed to
detect changes in the composition of ecological
communities in limited cases where: a) adequate
historical baseline data are available; b) the
study area and local species pool of the target
taxonomic group is relatively small; and c) there
is low spatial autocorrelation of species occur-
rences. Collection of physical specimens may
still be required to validate difcult taxa such
as Bombus vosnesenskii, which requires careful
examination to discriminate from B. caliginosus
(Williams et al. 2014). Further inventory work
combining methods to sample bumble bees on
different spatial scales is warranted to determine
the reliability of community science data for
monitoring ecological change.
Acknowledgments
We thank the BC Parks Living Lab program,
the Ian McTaggart Cowan Professorship in the
School of Environmental Studies at the University
of Victoria, and the Natural Sciences and Engi-
neering Research Council of Canada for funding
this research. We are likewise grateful to Pascale
Archibald, Sarah Johnson, Daniel Kirkpatrick,
Kevin Toomer, and Marika van Reeuwyk, who
supported eld work and aided with the process-
ing and identication of bumble bees. Thank
you to Claudia Copley, Joel Gibson, and Karen
Needham for facilitating access to specimens
at the Royal British Columbia Museum and
UBC Beaty Biodiversity Museum. Our thanks

216 Simon et al.
to John Ascher who tirelessly identies bees on
iNaturalist, and to Trevor Lantz who provided
valuable feedback on early analyses and drafts.
We also thank the following organizations who
provided access to the sites necessary to con-
duct this research: BC Parks, Crystal Mountain
Society, Islands Trust Conservancy, Galiano
Club, Galiano Conservancy Association, Galiano
Island Parks and Recreation Commission, Garry
Oak Meadow Preservation Society, and Tapovan
Sri Chinmoy Peace Park. Finally, we thank the
many Galiano Island community members who
permitted sampling on private land, and who
otherwise supported this work.
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Supplemental material available online at http://www.bioone.org/loi/nwsc
Submitted 20 December 2021
Accepted 16 September 2022