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Assessing declines of North American bumble bees (Bombus spp.) using museum specimens


Abstract and Figures

Bumble bees are an important group of wild pollinators in North America and considerable concern has been expressed over declines in their populations. However, before causes for declines can be assessed, it is essential that the geographical and chronological patterns of decline be discovered. Hitherto a lack of assessment of historical data has hindered our efforts to determine which species are most at risk. Here, the status of 21 North American bumble bee species (Hymenoptera: Apidae) occurring in the eastern nearctic biogeographic region is assessed using a specimen-level database from compiled museum and survey records dating back to the late nineteenth century from various institutional collections. Using a combination of measures, bumble bee declines were assessed over their entire native ranges. We report here that half of the selected fauna is in varying levels of decline (especially Bombus ashtoni, B. fervidus, and B. variabilis), with the remaining species exhibiting stable or increasing trends (e.g., B. bimaculatus, B. impatiens, and B. rufocinctus). Suggestions for prioritizing conservation efforts for this important group of pollinators are given.
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Assessing declines of North American bumble bees
(Bombus spp.) using museum specimens
Sheila R. Colla Fawziah Gadallah Leif Richardson
David Wagner Lawrence Gall
Received: 28 January 2012 / Accepted: 4 October 2012 / Published online: 11 October 2012
ÓSpringer Science+Business Media Dordrecht 2012
Abstract Bumble bees are an important group of wild pollinators in North America and
considerable concern has been expressed over declines in their populations. However,
before causes for declines can be assessed, it is essential that the geographical and chro-
nological patterns of decline be discovered. Hitherto a lack of assessment of historical data
has hindered our efforts to determine which species are most at risk. Here, the status of 21
North American bumble bee species (Hymenoptera: Apidae) occurring in the eastern
nearctic biogeographic region is assessed using a specimen-level database from compiled
museum and survey records dating back to the late nineteenth century from various
institutional collections. Using a combination of measures, bumble bee declines were
assessed over their entire native ranges. We report here that half of the selected fauna is in
varying levels of decline (especially Bombus ashtoni,B. fervidus, and B. variabilis), with
the remaining species exhibiting stable or increasing trends (e.g., B. bimaculatus,B.
impatiens, and B. rufocinctus). Suggestions for prioritizing conservation efforts for this
important group of pollinators are given.
Keywords Pollinator decline Bumble bees Bombus Grid cell Museum data
Insect collections
S. R. Colla (&)
Department of Biology, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada
F. Gadallah
University of Ottawa, 550 Cumberland St, Ottawa, ON K1N 6N5, Canada
L. Richardson
Dartmouth College Life Sciences Center, 78 College Street, Hanover, NH 03755, USA
D. Wagner
Department of Ecology and Evolutionary Biology,
University of Connecticut, Storrs, CT 06269-3043, USA
L. Gall
Entomology Division, Peabody Museum of Natural History,
Yale University, New Haven, CT 06511, USA
Biodivers Conserv (2012) 21:3585–3595
DOI 10.1007/s10531-012-0383-2
In recent years, the loss of pollinators and the services they provide has become a sig-
nificant conservation issue because of potentially enormous ecological and economic
impacts (Aizen et al. 2009; Beismeijer et al. 2006; Berenbaum et al. 2007). Bumble bees
(Bombus spp.) are the primary pollinators of many wild and cultivated plants, especially in
temperate latitudes (Berenbaum et al. 2007; Kearns and Inouye 1997). These eusocial
insects accumulate pollen and nectar resources throughout the spring and summer and
produce reproductive individuals (queens and males) primarily towards the end of the
growing season (Heinrich 2004; Laverty and Harder 1988). Colony fitness is thus directly
related to resource accumulation over a relatively long period of activity (e.g. Morandin
et al. 2005; Otti and Schmid-Hempel 2008). Because of their haplodiploid sex determi-
nation genetics, at low effective population sizes bumble bees may produce high pro-
portions of sterile males, leading to local extirpation (Whitehorn 2009; Zayed and Packer
Bumble bee declines have been noted worldwide, including in North America, Britain,
continental Europe and China (Cameron et al. 2011; Williams and Osborne 2009; Williams
et al. 2009). However, while some Bombus species have declined, others have remained
common throughout their native ranges, have expanded into new regions (e.g. Sheffield
et al. 2003) or have been successfully introduced (e.g. Ruz 2002) indicating differential
vulnerability among species. In North America, changes in bumble bee distribution and
abundances have been studied only in a few historically common species (Cameron et al.
2011; Colla and Packer 2008; Thorp 2005), or at small spatial scales (Colla and Packer
2008; Giles and Ascher 2006; Grixti et al. 2009). Regional studies have found evidence of
decline for some species over recent decades (Cameron et al. 2011; Colla and Packer 2008;
Grixti et al. 2009; Thorp 2005). In particular, historically common members of the sub-
genus Bombus sensu stricto (B. affinis,B. terricola,B. franklini and B. occidentalis) and
their social parasite (B. ashtoni) have been found to have declined wherever good baseline
data exist (Cameron et al. 2011; Colla and Packer 2008; Grixti et al. 2009; Thorp 2005;
Wagner and Van Driesche 2010). Less is known about other species, as declines may have
been more subtle; having occurred in more difficult to identify or already rare species.
Additionally, given the scarcity of good historical comparative data, most declines have
been inferred primarily using relative abundance data from a subset of species, which even
with other corroborating sources may be a difficult source for assessment given the biases
in many historic collections (Pyke and Ehrlich 2009). Also, yearly fluctuations in bee
numbers make comparisons of modern short-term studies to long-term historical data
collections problematic (Roubik and Wolda 2001).
In Europe, where bumble bees have been the subject of study for over two centuries,
historical data have allowed detailed analyses of the whole bumble bee fauna. In Britain
and Ireland, the conservation statuses for up to 17 bumble bee species has been assessed for
a portion of their native ranges based upon 50 950 km grid cells using multiple long-term
datasets from taxonomists, museums and naturalist groups (e.g. Williams 2005; Fitzpatrick
et al. 2007). The extent of decline for the UK fauna and ecological characteristics shared
among declining species has been determined by comparing grid cell occupancy between
historical and recent time periods with appropriate ecological data (Williams 1982,1989).
Historically uncommon species show the greatest declines (Fitzpatrick et al. 2007). In
North America, we have yet to assess the status of the majority of bumble bee species,
including several historically less common ones. Here we use a dataset compiled from
museum collections to assess the conservation status of the entire eastern North America
3586 Biodivers Conserv (2012) 21:3585–3595
bumble bee fauna throughout their native ranges. We measure decline using changes in
grid cell occupancy and look at changes in relative abundance over four time periods.
Using these decline measures, we assess the conservation status of each species and make
practical recommendations.
Electronic records for North American occurrences of all species of Bombus were
assembled from the holdings and survey data of the American Natural History Museum;
the Canadian National Collection of Insects, Arachnids and Nematodes; the Peabody
Museum of Natural History, University of Connecticut; Steve Javorek (Agriculture Can-
ada); the Packer Collection at York University, University of Guelph Insect Collection; the
Royal Ontario Museum; Sam Droege (USGS); Kevin Matteson (Fordham University);
Rachel Winfree (Rutgers University); Zadock Thompson Natural History Collection of the
University of Vermont; Middlebury College; Vermont Forests, Parks, and Recreation
Entomology Laboratory; Vermont State Colleges Entomology Collections; Canadian
Museum of Nature; University of Massachusetts; University of New Hampshire; New
York State Museum; Connecticut Agricultural Experiment Station and various private
collections. Incomplete records (e.g. those lacking determinations or essential label data)
were removed. Records without georeference were either removed or assigned coordinates
based on the site description on the label. ArcGIS (ESRI 2010) was used to check
georeference accuracy against associated label data. Records with erroneous coordinates
were either corrected or removed from the dataset. Publicly available records of Bombus
occurrence from the Illinois Natural History Survey were also included (http:// These data underwent the same quality checks as data from
other sources; in addition, specimens that were not recorded as having been identified by a
mellitologist were removed from this dataset.
Measuring decline
After data cleaning, a total of 69,600 North American Bombus records were accumulated,
encompassing the period from 1864 to 2009. For these analyses we used 44,797 records,
considering only species which occur primarily in the eastern Nearctic bumble bee bio-
geographic region (Williams 1996). To test whether there have been changes in distri-
bution or abundance of these species, data were divided into four time periods: pre-1931,
1931–1960, 1961–1990, and 1991–2009. These divisions were chosen based on the tem-
poral spread of samples (Fig. 1), to consider time periods before agricultural intensification
(pre-1931), before large-scale urbanization (pre-1961) and to look for possible long term
declines in Bombus s.s. before the documented rapid declines in the mid-1990s (COSEWIC
2010; Evans 2008; Thorp 2005). We consider here 21 species occurring primarily in the
eastern region of North America, but our analyses cover the entire North American ranges
for these species permitting us to assess whether declines occur throughout their ranges
(Fig. 2). Due to insufficient data, we do not treat species found in subarctic eastern Canada.
For comparison with previous European bumble bee studies (Fitzpatrick et al. 2007;
Williams 2005), the continent was divided into 50 950 km grid cells, and the presence of
our target species in each cell for each time period was determined. Historic range size was
Biodivers Conserv (2012) 21:3585–3595 3587
estimated to be the total number of grid cells occupied over all time periods also following
Fitzpatrick et al. (2007) and Williams (2005).
In order to determine the current status of species in their former ranges, we considered
only grid cells from prior time periods which contained a record (for any of the 21 species)
in the 1991–2009 time period and therefore were known to have been sampled for bumble
bees. This ‘persistence’ value was calculated as the proportion of re-sampled historical
cells (1864–1990; determined by the presence of at least one Bombus specimen in the
database) occupied by the species in the most recent time period (1991–2009). Only re-
sampled squares were considered because fewer grid cells were sampled in the most recent
time period than historically.
The relative abundance of each species for each time period was calculated by dividing
the number of specimens for that species by the total number of eastern specimens in the
given time period. A logistic regression treating, for each species, the proportion of
individuals in a given period as the dependent variable and time period as a continuous
explanatory variable was performed using SAS, Proc Genmod.
Using these measures, the conservation status of each species was assessed using cri-
teria modified from the IUCN red list (IUCN 2001). IUCN red list criteria assess declines
in the previous 10 years, or three generations, whichever is the longer. However, as rel-
atively few cells were sampled within the last 10 years in comparison to the historical data
available, we determine conservation status based on changes between our historical (all
pre-1991) and recent time (1991–2009) periods instead of ten years.
North American bumble bee species vary substantially in their patterns of abundance over
the past century. The most declining species was the cuckoo bumble bee B. variabilis
which showed severe decline in both measures, being completely absent from all samples
from our dataset in the most recent time period (1991–2009). Other species which persisted
in less than 50 % of their re-sampled range include B. affinis,B. ashtoni,B. auricomus,B.
borealis,B. fernaldae,B. fraternus,B. insularis,B. pensylvanicus, and B. sandersoni
Fig. 1 Eastern Nearctic Bombus specimens collected by decade from our combined and cleaned dataset
3588 Biodivers Conserv (2012) 21:3585–3595
(Table 1). Species which remained persistent through the majority of their resampled range
include B. citrinus,B. griseocollis,B. impatiens,B. ternarius, and B. bimaculatus
(Table 1). There was a significant positive relationship between pre-1990 range size (i.e.
grid cell occupancy) and persistence (Fig. 3,R
=0.34, p\0.05).
Our analyses considering relative abundance of our species over time found significant
declines in B. ashtoni,B. fervidus,B. fraternus and B. variabilis (p\0.05; Table 2).
Conversely, B. bimaculatus,B. impatiens, and B. rufocinctus were found to have signifi-
cantly increased (p\0.05; Table 2). Using our occupancy and relative abundance decline
measures, we assessed one species as Critically Endangered, six species as Endangered and
four as Vulnerable (Table 3).
Biological collections and their associated taxonomic databases and utility in systematic
research have recently proved to be an invaluable resource to address conservation issues
(Pyke and Ehrlich 2009). Using these resources, this study is the first to assess the status of
eastern nearctic bumble bee species throughout their native ranges. However, long-term
studies of bumble bee declines face problems of biased sampling and inconsistent sampling
effort among time periods (Kosior et al. 2008; Williams and Osborne 2009). Additionally,
historical collections tend to be geographically and temporally biased (Pyke and Ehrlich
2009). To reduce the effects of these biases, our dataset combined specimen data from
numerous collections and surveys in Canada and the United States. Our spatial analyses
used only grid cells which were sampled both historically and in the most recent time
period, taking into account the smaller geographical spread of recent surveys, and we used
coarse time periods to decrease temporal biases from collection-effort fluctuations. By
using coarse grid cells instead of smaller cells (e.g. Maes et al. 2012), we were able to
reduce the effect of imprecise locality information for most historical records.
Fig. 2 Distribution of Bombus records for species which occur in the eastern Nearctic biogeographic region
Biodivers Conserv (2012) 21:3585–3595 3589
Table 1 Estimated historical range size as the number of grid cells occupied over all time periods and
persistence measured as the proportion re-sampled historical cells (1864–1990) occupied of recent time
period sampled cells (1991–2009) for each species
Species Estimated range size: 50 950 km cells occupied (area km
) Persistence
B. affinis 163 (407,500 km
) 0.265
B. ashtoni* 209 (522,500 km
) 0.347
B. auricomus 147 (367,500 km
) 0.492
B. bimaculatus 235 (587,500 km
) 0.837
B. borealis 242 (605,000 km
) 0.271
B. citrinus* 177 (442,500 km
) 0.759
B. fernaldae* 141 (352,500 km
) 0.233
B. fervidus 561 (1,402,500 km
) 0.552
B. fraternus 59 (147,500 km
) 0.273
B. frigidus 154 (385,000 km
) 0.571
B. griseocollis 357 (892,500 km
) 0.722
B. impatiens 426 (1,065,000 km
) 0.841
B. insularis* 251 (627,500 km
) 0.444
B. pensylvanicus 322 (805,000 km
) 0.344
B. perplexus 254 (635,000 km
) 0.631
B. rufocinctus 283 (707,500 km
) 0.667
B. sandersoni 122 (305,000 km
) 0.268
B. ternarius 309 (772,500 km
) 0.722
B. terricola 323 (807,500 km
) 0.518
B. vagans 386 (965,000 km
) 0.631
B. variabilis* 35 (87,500 km
Total (all N.A. species) 2,171
* Denotes cuckoo species
Fig. 3 Scatterplot showing the relationship between the ranges of 21 North American bumble bees (x-axis)
as the total number of 50 950 km grid cells occupied and persistence (y-axis) as the proportion of
historical (pre-1991) range recently occupied (1991–2009)
3590 Biodivers Conserv (2012) 21:3585–3595
Table 2 Number of records and relative abundance of eastern Bombus species by time period and results of logistic regression on relative abundance. Statistically significant
values in bold
Species Total records \1931 1931–1960 1961–1990 1991–2009 Slope (sign indicates
direction of change)
B. affinis 1,563 355 303 812 93 -0.2779 0.5281 0.4674
B. ashtoni*941 311 280 267 83 20.5166 13.7488 0.0002
B. auricomus 493 140 79 192 82 -0.2538 1.7924 0.1806
B. bimaculatus 2952 202 149 863 1,738 0.7152 16.0216 0.0001
B. borealis 1,067 303 501 125 138 -0.5508 2.9737 0.0846
B. citrinus* 1,202 222 217 178 585 0.1750 0.4106 0.5217
B. fernaldae* 474 77 277 97 23 -0.5064 1.0955 0.2952
B. fervidus 3,937 1,346 1,213 736 642 20.4905 24.0150 <0.0001
B. fraternus 145 41 64 30 10 20.5740 4.2850 0.0385
B. frigidus 1,830 134 1,282 217 197 -0.4056 0.4080 0.5230
B. griseocollis 2,870 398 337 606 1,529 0.3807 3.2199 0.0727
B. impatiens 9,111 1,141 851 2,709 4,410 0.3984 6.7176 0.0095
B. insularis* 1,025 159 361 470 35 -0.3099 0.5251 0.4687
B. pensylvanicus 2,024 435 525 912 152 -0.3001 0.9360 0.3333
B. perplexus 1,735 354 288 597 496 -0.0258 0.0842 0.7717
B. rufocinctus 2,671 215 503 745 1,208 0.3426 15.7771 0.0001
B. sandersoni 472 91 131 219 31 -0.2832 0.6915 0.4056
B. ternarius 2,502 461 300 621 1,120 0.1978 1.1654 0.2803
B. terricola 3,724 963 456 1,632 673 -0.1723 0.4516 0.5016
B. vagans 3,965 659 376 1,518 1,412 0.1705 0.8186 0.3656
B. variabilis*94 76 11 7 0 21.7406 39.2118 <0.0001
Total (eastern species) 44,797 8,083 8,504 13,553 14,657 0.0417 1.1907 0.2752
Total (all species) 69,600 12,375 16,093 21,386 19,746 -0.0682 1.2002 0.2733
* Indicates the species is a social parasite (cuckoo) and bold face indicates significant change in relative abundance over time
Biodivers Conserv (2012) 21:3585–3595 3591
These methods do have limitations, however. Re-sampled grid cells were selected
because at least one bumble bee was collected in the most recent time period. We cannot
assume all species were searched for equally, meaning a species may be absent due to
actual absence or from lack of collection. Additionally, areas not sampled due to difficulty
of access or distance from roads and urban centers are not well represented in sampled grid
cells. Thus, the true historic range or presence in recent time periods for each species may
be underrepresented. Finally, because we consider only resampled grid cells, our method
does not allow us to assess whether there is spatial autocorrelation among the grid cells lost
in species declines. Anecdotal information suggests, however, that for many of these
species, there is geographic patterning to their decline (e.g. persistence in some areas of
their historic range and extirpation in others).
By combining data from numerous museums and collections from both Canada and the
USA, we determined that 11 of the 21 native eastern Bombus species have likely suffered
substantial population declines (i.e. [50 %). These declines were striking given the
increase in the number of Bombus specimens collected (i.e. sampling effort) in the most
recent time period (Fig. 1). Eight of the 21 species show signs of stability or increases in
relative abundance. Consistent with European studies (Fitzpatrick et al. 2007; Williams
1982,1989,2005), we found that species with smaller historically occupied ranges had
lower persistence (Fig. 3). In particular, B. variabilis, the eastern species with the lowest
number of historically occupied grid cells, is assessed as most at risk, and the extensive
extent of decline had not been noted previously.
Using this dataset, alternative methods of analyses, and considering each species’ entire
North American range, our results contribute additional information about the status of
wild bumble bees gained from recent Bombus decline studies (Cameron et al. 2011; Colla
and Packer 2008; Grixti et al. 2009). Our study recommends 11 species (B. affinis,
B. ashtoni,B. auricomus,B. borealis,B. fernaldae,B. fervidus,B. fraternus,B. insularis,
B. pensylvanicus,B. sandersoni and B. variabilis) for immediate conservation attention.
Table 3 Assessment of declining eastern North American bumble bee species using modified IUCN red list
Species Rank Rationale
B. affinis EN RD [70 %
B. ashtoni* VU RD [50 %
B. auricomus VU RD [50 %
B. borealis EN RD [70 %
B. fernaldae* EN RD [70 %
B. fervidus EN ID [70 %
B. fraternus EN RD [70 %
B. insularis* VU RD [50 %
B. pensylvanicus VU RD [50 %
B. sandersoni EN RD [70 %
B. variabilis* CR RD [90 %
The rationale ‘‘RD’’ (range decline) provides the decline in occupancy in re-sampled historical range
between 1960–90 and 1991–2009 time periods, ‘‘ID’’ (index decline) provides the decline in index of
relative abundance over all time periods
CR critically endangered, EN endangered, VU vulnerable
* Denotes cuckoo species
3592 Biodivers Conserv (2012) 21:3585–3595
It should be noted that using a more conservative approach to deal with Type I error due to
performing multiple statistical tests affects the interpretation of extent of decline for B.
fraternus only (Table 3).
While B. affinis has previously been described as suffering large-scale declines
throughout its North American range (Cameron et al. 2011; Colla and Packer 2008;
COSEWIC 2010) and B. ashtoni,B. borealis,B. pensylvanicus and B. variabilis have been
found to be in decline at the regional level (Cameron et al. 2011; Colla and Packer 2008;
Grixti et al. 2009), the declines of the remaining species have been thus far unnoticed. This
is likely due to the fact that they have been uncommon historically, are more difficult to
identify, and may be more specialized to certain habitat types.
The declines estimated here are less marked than previously reported in B. affinis (e.g.
87 % decline, Cameron et al. 2011), likely due to the coarse time scale we used. This
suggests that the decline of B. affinis occurred most precipitously within our most recent
time period (1991–2009) as has been previously hypothesized (Thorp and Shepherd 2005).
Additionally, previous studies considering only a portion of the range for B. terricola found
this species to be among the most sharply declining species (Cameron et al. 2011; Colla
and Packer 2008). However, our analyses take into consideration the full native range of
this widespread species and rank it as of lower conservation concern. In fact, B. terricola
remains common in portions of its Canadian and Northeastern US range with suitable
habitat (Colla and Dumesh 2010; L. Richardson, Pers. Obs.).
Future work determining the cause of differential vulnerability among species is
required to further understand Bombus conservation issues. Williams et al. (2009) found
species with narrow climatic niche, species locally at the edge of their climatic niche and
species with late queen emergences to be more vulnerable to extrinsic threats. Here, we
show select species with shared ecological traits to be most at risk. Similar to previous
findings (e.g. Dupont et al. 2011; Goulson et al. 2005; Williams et al. 2009), we find the
late-emerging, long-tongued species to be in decline (B. auricomus,B. fervidus,B. pen-
sylvanicus). Additionally, as is commonly found amongst other taxa (e.g. Stefanescu et al.
2011), species restricted to certain habitat types were also found to be more at risk
(B. borealis,B. fraternus,B. sandersoni). Lastly, the majority of the eastern cuckoo
bumble bees (B. ashtoni,B. insularis,B. fernaldae,B. variabilis) were also found to be
among the most at-risk. The cuckoo species must be sensitive to changes in the abundance
of host species and, depending upon their degree of host specificity, have likely always
been rarer than their hosts. Further work to better assess the intrinsic patterns of vulner-
ability of these species in addition to assessments of threats is urgently needed to conserve
our bumble bee fauna as a whole. Until then, habitat protection of current populations of
species found to be at higher risk should be implemented.
Acknowledgments This work would not have been possible without the use of valuable insect specimens
from many well-curated collections and recent surveys. We thank additional data providers J. Ascher,
Caroline Scully, Mike Arduser, Steve Javorek and Kevin Matteson. We would like to thank Michael
Otterstatter for help with statistical analyses and Paul Williams, Ignasi Bartomeus, Sarina Jepsen and
reviewers for valuable comments. We thank NSERC-CANPOLIN and NSERC CGS to Fawziah Gadallah
and Sheila Colla respectively for providing funding for this work. Data capture at the American Museum of
Natural History (AMNH), the University of Connecticut, Rutgers University, and Cornell University was
supported by NSF DBI Grant (0956388, P. I. John S. Ascher), with additional support at AMNH from
Robert G. Goelet and at University of Connecticut and the Peabody Museum of Natural History by a state
wildlife Grant (09DEP10012AA, P.I. DLW). This is contribution No. 58 from the Canadian Pollination
Initiative (NSERC-CANPOLIN).
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... Widespread phenomena of urbanization are driving deep changes on landscape features, their temperature and pollutants, creating conditions that impact biodiversity (Foley et al. 2005;Weng et al. 2007;Wenzel et al. 2020). Plants and animals can respond to these environmental variations by shifting their distribution (Colla et al. 2012), phenology (Huchler et al. 2020), and/or shaping some morphological traits considered "functional", i.e. relevant for their ecology, fitness and behavior (Alberti et al. 2017;Eggenberger et al. 2019;Nooten and Rehan 2020). In bees, trait variation due to environmental alteration could affect the efficiency of the pollination ecosystem service they provide though impacting the way they interact with plants (Buchholz and Egerer 2020;Biella et al. 2019a, b). ...
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The way urbanization shapes the intraspecific variation of pollinator functional traits is little understood. However, this topic is relevant for investigating ecosystem services and pollinator health. Here, we studied how urbanization affects the functional traits of workers in two bumblebee species (Bombus terrestris and B. pascuorum) sampled in 37 sites along a gradient of urbanization in North Italy (an area of 1800 km 2 including the metropolitan context of Milan and other surrounding capital districts). Namely, we investigated the effect of land use composition, configuration, air temperature, flower resource abundance, and air pollutants on the variation of traits related to flight performance and of stress during insect development (i.e., wing size, wing shape and size fluctuating asymmetry). The functional traits of the two bumblebees responded idiosyncratically to urbanization. Urban temperatures were associated with smaller wing sizes in B. pascuorum and with more accentuated fluctuating asymmetry of wing size in B. terrestris. Moreover, flower abundance correlated with bigger wings in B. terrestris and with less asymmetric wing size in B. pascuorum. Other traits did not vary significantly, and other urban variables played minor effects. These species-specific variation patterns highlight that environmental stressor linked to urbanization negatively impact the traits related to flight performance and development stability of these syntopic bumblebees, with possible consequences on the pollination service they provide.
... Growing evidence, mostly from western Europe and North America, shows widespread but heterogeneous declines in the abundance and diversity of many wild pollinators (Potts et al. 2010;Ollerton et al. 2011;Colla et al. 2012;Zattara and Aizen 2021). Abundance changes (declines and increases) can vary geographically within species (Aizen and Harder 2009b;Thomson 2016) and among congeneric species and taxonomic families (Biesmeijer et al. 2006;Cameron et al. 2011;Richardson et al. 2019;Zattara and Aizen 2021). ...
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ABSTRACT. Mounting evidence shows that pollinators are declining as a result of widespread environmental degradation. This loss raises concerns that a global pollination crisis could threaten the human food supply by decreasing crop yield and even promote famine under a hypothetical scenario of total pollinator extinction. This catastrophic possibility has prompted intense interest from scientists, politicians and the general public. However, three lines of evidence do not support such an apocalyptic scenario. First, even though the abundance and diversity of wild pollinators are declining worldwide, the global population of managed honey-bee hives has increased by ~80% since the early 1960s. Second, agricultural production would decrease by <10% in the total absence of bees because relatively few crops are completely pollinator dependent. Lastly, despite widespread pollination deficits, current evidence is inconsistent with deceleration in yield growth with increasing pollinator dependence at a global scale, probably due to improvements in crop breeding and external agricultural subsidies. Overall, this evidence refutes simplistic claims of human starvation caused by a hypothetical total pollinator extinction. Nevertheless, pollination problems may loom. Although pollinators are responsible for a minor fraction of global agriculture production, this fraction has increased ~600% since 1961, greatly outpacing human population growth and the growth of the global population of managed honey bees. This large production increase is explained to a considerable extent by the rapid expansion of pollinator-dependent monocultures at the expense of natural and diverse agricultural habitats. By driving pollinator decline, this land-use transformation could worsen pollination deficits and promote further crop expansion given sustained market demands. Therefore, although the human food supply is not currently subject to a global pollination crisis, a spiraling positive-feedback between the impacts of agriculture expansion and pollinator decline on crop yield could accelerate precipitous biodiversity loss by promoting further habitat destruction and homogenization.
... Indeed, studies evaluating the potential effects of these two stressors have revealed both synergistic and additive negative effects on lethal (Linguadoca et al., 2021;Tosi et al., 2017) and sublethal endpoint measurements (Schmehl et al., 2014;Stuligross and Williams, 2020), respectively. Given that similar negative effects are observed on key reproductive physiological parameters in bumble bees, such as on the glands required for digestion and brood care (i.e., hypopharyngeal glands (HPGs)) or sperm traits (i.e., spermatozoa counts and viability), this may provide an additional plausible mechanistic explanation for recent population declines (Bommarco et al., 2012;Colla et al., 2012). However, the impact of any given stressor can vary depending upon the level, e.g. in ants additive effects of virus and pesticide were observed at the level of individuals and castes, while co-exposure with both stressors elicited antagonistic effects on colony size (Schläppi et al., 2021). ...
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Global insect biodiversity declines due to reduced fitness are linked to interactions between environmental stressors. In social insects, inclusive fitness depends on successful mating of reproductives, i.e. males and queens, and efficient collaborative brood care by workers. Therefore, interactive effects between malnutrition and environmental pollution on sperm and feeding glands (hypopharyngeal glands (HPGs)) would provide mechanisms for population declines, unless buffered against due to their fitness relevance. However, while negative effects for bumble bee colony fitness are known, the effects of malnutrition and insecticide exposure singly and in combination on individuals are poorly understood. Here we show, in a fully-crossed laboratory experiment, that malnutrition and insecticide exposure result in neutral or antagonistic interactions for spermatozoa and HPGs of bumble bees, Bombus terrestris, suggesting strong selection to buffer key colony fitness components. No significant effects were observed for mortality and consumption, but significant negative effects were revealed for spermatozoa traits and HPGs. The combined effects on these parameters were not higher than the individual stressor effects, which indicates an antagonistic interaction between both. Despite the clear potential for additive effects, due to the individual stressors impairing muscle quality and neurological control, simultaneous malnutrition and insecticide exposure surprisingly did not reveal an increased impact compared to individual stressors, probably due to key fitness traits being resilient. Our data support that stressor interactions require empirical tests on a case-by-case basis and need to be regarded in context to understand underlying mechanisms and so adequately mitigate the ongoing decline of the entomofauna.
... This implies that increasing aridity vis-à-vis temperature are probably going to have detrimental effects on wild bees, albeit their thermophilic character. The individualistic response to climate change has also been observed in other insect groups [64,139], in high-altitude occurring species [63] and in other regions as well [39,138,[140][141][142], pointing that even phylogenetically close and ecologically similar species might differ in their vulnerability against climate stressors [143]. It might as well be that abrupt future temperature rise will exceed the species' thermal tolerance and/or the species' ability to track their niche, especially in areas with low environmental heterogeneity, such as low altitude Aegean islands. ...
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Pollinators’ climate change impact assessments focus mainly on mainland regions. Thus, we are unaware how island species might fare in a rapidly changing world. This is even more pressing in the Mediterranean Basin, a global biodiversity hotspot. In Greece, a regional pollinator hotspot, climate change research is in its infancy and the insect Wallacean shortfall still remains unaddressed. In a species distribution modelling framework, we used the most comprehensive occurrence database for bees in Greece to locate the bee species richness hotspots in the Aegean, and investigated whether these might shift in the future due to climate change and assessed the Natura 2000 protected areas network effectiveness. Range contractions are anticipated for most taxa, becoming more prominent over time. Species richness hotspots are currently located in the NE Aegean and in highly disturbed sites. They will shift both altitudinally and latitudinally in the future. A small proportion of these hotspots are currently included in the Natura 2000 protected areas network and this proportion is projected to decrease in the coming decades. There is likely an extinction debt present in the Aegean bee communities that could result to pollination network collapse. There is a substantial conservation gap in Greece regarding bees and a critical re-assessment of the established Greek protected areas network is needed, focusing on areas identified as bee diversity hotspots over time.
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Bees provide an important ecosystem service by contributing to the pollination of crop and wild plant species. Multiple bee species, however, are in decline due to factors such as habitat loss and fragmentation, inadequate food availability, improper management practices, climate change, and pressures from pathogens and pests, including exotic species. Concerns about pollinator declines and implications for ecosystem services have led to efforts to create and restore pollinator habitat, refine pest management practices, improve detection of pests and exotic species that threaten native bees, and monitor populations to identify and protect vulnerable bee species and communities. A variety of methods are used to monitor bee populations, some of which use visual stimuli that mimic natural cues used to locate floral resources. Bees also find their way into traps that use both visual and olfactory cues to attract pest insects. On one hand, researchers work to improve pest monitoring tools to increase target captures and reduce bee bycatch. On the other, analysis of bee bycatch can help assess biodiversity, determine population fluctuations and range expansions or contractions, support monitoring efforts, and identify patterns and processes of broader ecological interest. These different fields of research should not be seen as conflicting goals, but rather an opportunity for greater complementarity and collaboration. This article reviews the biological and ecological bases for bee attraction to traps, summarizes recent trends in bycatch research, highlights future research priorities, and identifies opportunities for collaborative data sharing to maximize existing resources.
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This book celebrates the natural history of the Klamath Mountains of northwest California and southwest Oregon through stories of diversity and resilience over deep time. Shaped by geology, these mountains form an ancient jigsaw puzzle and topographic mosaic dissected by big-shouldered river canyons and sharp ridgelines that create localized climatic gradients. Within the geomorphic province, the rocks are much older than in surrounding regions. This dichotomy has allowed many distinct evolutionary lineages of plants and animals to adapt, survive, and sometimes speciate where elsewhere they became extirpated long ago. The Klamath Mountains: A Natural History • Describes and documents one of the most biodiverse temperate mountain ranges on Earth. • The first comprehensive Natural History written for this region. • 34 contributing authors–all experts in their fields. • Chapters including Mammals, Birds, Amphibians, Plant Communities, First Peoples, Geology, Climate, Fire Ecology, and much more. • Full color, rich illustrations, and well-curated photographs bring 496 pages to life!
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Research on plant-pollinator interactions requires a diversity of perspectives and approaches, and documenting changing pollinator-plant interactions due to declining insect diversity and climate change is especially challenging. Natural history collections are increasingly important for such research and can provide ecological information across broad spatial and temporal scales. Here, we describe novel approaches that integrate museum specimens from insect and plant collections with field observations to quantify pollen networks over large spatial and temporal gradients. We present methodological strategies for evaluating insect-pollen network parameters based on pollen collected from museum insect specimens. These methods provide insight into spatial and temporal variation in pollen-insect interactions and complement other approaches to studying pollination, such as pollinator observation networks and flower enclosure experiments. We present example data from butterfly pollen networks over the past century in the Great Basin Desert and Sierra Nevada Mountains, United States. Complementary to these approaches, we describe rapid pollen identification methods that can increase speed and accuracy of taxonomic determinations, using pollen grains collected from herbarium specimens. As an example, we describe a convolutional neural network (CNN) to automate identification of pollen. We extracted images of pollen grains from 21 common species from herbarium specimens at the University of Nevada Reno (RENO). The CNN model achieved exceptional accuracy of identification, with a correct classification rate of 98.8%. These and similar approaches can transform the way we estimate pollination network parameters and greatly change inferences from existing networks, which have exploded over the past few decades. These techniques also allow us to address critical ecological questions related to mutualistic networks, community ecology, and conservation biology. Museum collections remain a bountiful source of data for biodiversity science and understanding global change.
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Climate change (CC) is expected to negatively impact global biodiversity and ecosystems, resulting in profound ecological impacts and placing complex networks of biological interactions at risk. Despite this worrying scenario, the existing knowledge deficiencies may be overcome with species distribution models (SDMs), providing estimates of the effects of CC upon biodiversity. We evaluate the impact of CC on the distribution of the bumble bee species Bombus (Funebribombus) funebris Smith, 1854 (Apidae: Bombini) in South America. The Andean region will remain suitable for B. funebris under models of future CC. Nonetheless, the distribution range size will decrease, especially in protected areas. We believe this is due to the elevation zones preferentially occupied by the bees. The existence and prevalence of the species may be affected by anthropic actions and CC. The growing use of SDMs is critical to minimizing information deficits related to insect species and providing estimates of their distribution ranges. Implications for insect conservation: Implications for insect conservation Our results show a retraction in the future distribution range of this bumble bee, dispersing to higher elevations. Therefore, it has the potential for the loss of plant–insect interactions by affecting its crucial role in Andean pollination.
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The suggested recent decrease in the distributional ranges of certain species of bumble bees was investigated in the data collected by the Bumblebee Distribution Maps Scheme, using a numerical classificatory approach. Three major biogeographic elements and four biogeographic regions are defined, and changes in their composition and distribution described. Large reductions in the distributional ranges recorded after 1960 were found for two of the biogeographic elements (especially for the Southern Local Species: Bombus subterraneus (L.), B. sylvarum (L.), B. ruderatus (F.) and B. humilis Ill.), which have resulted in the emergence of a new Central Impoverished Region covering 23 vice-counties in Central England.
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We present the results of a survey of the bee fauna of Black Rock Forest, Orange County, New York, USA. The survey focused on bees, with more limited data gathered for other incidentally collected groups such as apoid and vespid wasps. Surveys in 2003 with nets and bowls recorded 144 bee species (26 genera), 22 vespid species (9 genera) and 23 crabronid species (12 genera). Noteworthy records are detailed. A preliminary checklist of the bee fauna of the BRF is presented and discussed in relation to that of New York State, selected sites within the state, and of the northeastern USA as a whole. The cleptoparasitic species Sphecodes fattigi Mitchell, Sphecodes johnsonii Lovell, and Lasioglossum (Dialictus) michiganense (Mitchell), and the oligolectic species Osmia (Melanosmia) inermis (Zetterstedt) are newly recorded from New York State. Ecological patterns pertaining to sociality, nest type, pollen specialization, parasitism, and phenology, are summarized and discussed, as are the efficacies of different collecting methods. The net collected sample was richer than the bowl trapped sample in total bee species (117 vs. 113) and in the number of unique species (29, 20.4% vs. 25, 17.6%).
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Current distribution of bumblebee species in Cracow was studied in 2000-2003 in 23 atlas squares. The results were compared with historical data available for last 150 years, including published materials and museum collections. A total 28 bumblebee species were recorded throughout that period. Among them, 11 species are currently threatened in the study area. There were stated three tendencies among the studied bumblebee species. After 1850, 10 species were strongly regressing (withdrew from the Cracow area altogether or range contraction); further 11 species were more or less stable in their area; the next 6 species were strongly expanding in Cracow. 6 species were stated as a new for Cracow, including 2 species recorded between 1901-1972 and 4 between 1973-2003. Negative population tendencies by the Bombini in the Cracow area were the result of both natural and anthropogenic factors. Species protection and conservation of the most valuable areas as nature reserves are expected to prevent further decrease of bumblebees in the Cracow area.
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We review evidence from around the world for bumblebee declines and review management to mitigate threats. We find that there is evidence that some bumblebee species are declining in Europe, North America, and Asia. People believe that land-use changes may be having a negative effect through reductions in food plants in many parts of the world, but that other factors such as pathogens may be having a stronger effect for a few species in some regions (especially for Bombus s. str. in North America). Evidence so far is that greater susceptibility to land-use change is associated world-wide with small climatic ranges, range edges, and late-starting colony-development cycles. More evidence is needed on the roles of pollen specialization, nest sites, hibernation sites, and pesticides. It is still too early to assess the success of schemes aimed at improving forage in agricultural and conservation areas. However, schemes aimed at raising public awareness have been very successful. Until proven safe, we recommend that live bumblebees should not be moved across continents or oceans for commercial pollination.
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Biogeographic regions are widely regarded as real entities, or at least as useful summaries of the complex patterns of spatial concordance among species. The problem is that, whereas some parts of the transition zones between regions may be strong and abrupt, other parts of the same zones may be weak or broad, so that the corresponding parts of border lines drawn on maps, although convenient, are arbitrary constructs. One approach to investigating transition zones ascribes values to the area units themselves, by quantifying the spatial turnover among species within the surrounding neighbourhoods of areas on maps. Using data for bumble bee distributions world-wide, I show that quantitative measures of neighbourhood turnover can discover many of the transition zones that are found by classification techniques when applied to the same data. But unlike classification techniques, turnover measures, particularly when used in combination, can show how a transition zone varies along its length, not only in its strength (the proportion of species contributing to the zone) but also in its breadth (the degree of spatial overlap or the degree of coincidence among species replacements across it). For bumble bees at least, these transition zones are also negatively associated with areas that have a combination of both high species richness and high species nestedness.
Conference Paper
... compelling but untested hypothesis for the cause of decline in the United States (10) entails the spread of a putatively introduced pathogen , Nosema bombi, which is an obligate intracellular microsporidian parasite found commonly in bumble bees throughout Europe (13–16 ...
We provide keys for identifying the 26 bumble bee species (Bombus and Psithyrus) found in Canada east of Manitoba, and information on their ecology and distribution. The keys are designed for field use and rely primarily on colour patterns rather than on microscopic features.
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