where the cumulative sum of Lijk was calculated
across all time periods since bees first were observed visiting flowers
(including the present time period) and was run both including and
excluding the Tijk term. Models for H3b were only
run for bee genera that might produce multiple broods per season
(Augochlorella , Bombus , Halictus ,Lasioglossum ; Packer et al. 2007).
Model selection with the MuMIn package (Bartoń 2019) was used to
determine which models best predicted bee visits, considering all models
with ΔAICc < 2. Model selection was run in two iterations,
with unknown land area assigned either the median FR value calculated
from all land types within a specific radius during a given time period
(‘median models’), or the minimum FR value calculated from all land
types within a specific radius during a given time period, which was
always zero (‘minimum models’). This was done to test the sensitivity of
our conclusions to the presence of unknown areas; we found no
differences between the identities of models with ΔAICc < 2
when unknown areas were assigned either minimum or median FR values, and
we have presented the results from both iterations.
Results
Floral resources
Floral volume was the best predictor of both daily nectar sugar mass
(µg/day; R2 = 0.39, p = 3.6×10-6, n
= 46, Fig. 2a), and pollen volume (µl/flower; R2 =
0.40, p = 6.0×10-5, n = 33, Fig. 2b), and therefore
was used to represent FR in all subsequent analyses. Flower length,
width, height, and surface area were also significantly correlated with
nectar and pollen volume, but to a lesser degree (R2 ≤
0.34). Floral measurements, pollen volumes, and nectar sugar mass for
individual species can be found in Appendix, Table A2–A4.
Across many of the landscapes sampled in this study, there was a high
degree of correlation between the FR at each spatial scale within a
given time period, particularly between the 500 m and 750 m spatial
scales (Fig. 3). In most landscapes, the fourth (last) time period had
the lowest FR, and the highest FR abundance generally was seen in either
in the second or third time period, with a few landscapes having the
highest FR of the season in the first time period (Fig. 3).
Most
common bee
genera
Over the season, 8422 bee visits were observed across all sites, with
1647 visits observed in the first time period, 1946 in the second, 2211
in the third, and 2618 in the fourth. Bees in the genera Andrena(mining bees), Apis (A. mellifera ; Western honey bee),Bombus (bumble bees), Halictus (furrow bees), andLasioglossum (sweat bees) were observed visiting flowers in at
least four of the 27 sites surveyed during all time periods. Bees in the
genus Augochlorella (A. aurata ; golden green sweat bee)
were observed during just the first and second time periods in at least
four sites, while Megachile (leafcutter bees) were observed in
the second and third, and Peponapis (P. pruinosa ; hoary
squash bee) in the third and fourth. All other bee genera found in at
least four sites were only observed during one time period.
H1: Bee visits are only influenced by local FR
No models for any genera supported the hypothesis that bee visits were
influenced only by local FR (Table 1). Several taxa did, however, show a
positive relationship with the abundance of FR within transects based on
the best models which also included landscape FR abundance as a
predictor (Table 1; Fig, 4 for Halictus and Peponapis ).
H2: Bee visits are influenced by the present abundance of landscape FR
The number of visits observed from Andrena , Augochlorella ,Megachile , and Peponapis supported hypothesis H2b, that
bee visits were negatively associated with the present abundance of
landscape FR (Fig. 4; Table 1). The number of bee visits was best
predicted by models of present landscape FR at a 250 m scale forMegachile (ΔAICc = 0), and at a 750 m scale forAugochlorella (ΔAICc = 0) and Peponapis (ΔAICc = 0).Andrena visits were best predicted by models of the present
landscape FR at a 250 m scale (ΔAICc ≤ 1.00) but showed some support for
hypothesis H3a (Table 1), described in the following section.
H3: Bee visits are influenced by the previous abundance of landscape FR
For Halictus and Lasioglossum , hypothesis H3a—that bee
visits were influenced by the previous abundance of landscape FR within
a season—was best supported (Table 1; Fig. 4). Halictus andLasioglossum visits were best predicted from models including
landscape FR abundance during the first time period, and the
non-positive change in the abundance of landscape FR since the first
time period within 750 m of sampling locations (both ΔAICc = 0). For
both genera, bee visits were negatively associated with landscape FR
during the first time period and were also lower in landscapes that
experienced greater decreases in landscape FR over the season (Table 1;
Fig. 4). Andrena visits also showed some support for hypothesis
H3a, with bee visits predicted by the previous abundance of landscape FR
at the 250 m scale (ΔAICc ≤ 1.81), but in this genus, greater decreases
in FR over the season were associated with a higher number of bee
visits. However, hypothesis H2b had slightly better support inAndrena (Table 1), as described in the previous section.
Bombus visitation rates best supported hypothesis H3b, that bee
visits are influenced by the cumulative abundance of landscape FR since
the first time period (Table 1; Fig 4). Landscape FR was a predictor ofBombus visits at all spatial scales over which it was measured,
but the 250 m scale was the strongest predictor (ΔAICc = 0). Visits fromBombus were positively associated with the cumulative abundance
of landscape FR at all spatial scales.
Discussion
We found that FR in the landscape over preceding months was an important
predictor of bee activity for most bees that were foraging over the
entire season. High FR abundance in previous months was positively
related to the number of visits for bees that were more social and
produced multiple broods per season (Bombus ) , while
stable FR abundance over previous months positively influenced the
number of visits for genera that were less social and produced fewer
broods per season (Halictus and Lasioglossum ). For all
other bees, including solitary bees (Andrena , Megachile ,
and Peponapis ) and bees with shorter observed foraging periods
(Augochlorella , Megachile , and Peponapis ), the
present abundance of FR in the landscape was the best predictor of bee
visits. However, the present abundance of FR was negatively related to
local bee visits, possibly because of a dilution of pollinators across
high-FR landscapes. Individual bee taxa exhibit unique combinations of
foraging distances, foraging periods, and numbers of brood produced per
season, all of which can influence how bees respond to changes in
landscape FR abundance over a season. Our research acknowledged these
taxonomic differences by assuming each bee genus observed would respond
at different spatial and temporal scales to the abundance of FR in a
landscape. By doing this, we were able to document important differences
in the ways in which each genus was influenced by the spatial and
temporal availability of FR.
Much of the previous research on wild bees responding to FR in
agricultural landscapes has found that a higher abundance of FR is
associated with larger populations, higher densities, or greater numbers
of visits (Mandelik et al. 2012, Kovács-Hostyánszki et al. 2013,
Mallinger et al. 2016, Martins et al. 2018). In our study, the number of
visits by Bombus was positively related to cumulative landscape
FR, in line with the hypothesis that bees producing multiple broods in a
season can increase population sizes within one season with access to
more FR through time. This finding agrees with previous research
examining B. vosnesenskii colony responses to FR in
agricultural landscapes, which found that the production of males and
workers was more positively related to high early-season FR abundance in
the surrounding landscape than to late-season FR (Williams et al. 2012).
Bumble bees represent some of the most common and important pollinators
for both wildflowers and crops in the Northern Hemisphere, but many
species are facing declines (Goulson et al. 2008). Our results suggest
that early-season FR in agricultural landscapes could promote high
bumble bee visitation rates later in the season, and potentially
maintain or increase colony sizes over a season.
For Halictus and Lasioglossum , our findings best supported
the hypothesis that these bees were producing a single brood per season,
and therefore were able to maintain (but not increase) their population
sizes when FR was consistent or increased over time. However, in the
region this study was conducted, both Halictus andLasioglossum include eusocial species that produce multiple
broods per season and solitary species that only produce a single brood
(Mitchell 1960, Packer et al. 2007). Given the stronger support for the
hypothesis that these genera responded as expected for
single-brood-producing bees, our results indicate either that more
solitary species were present in our study locations, or that the more
social species in this region were producing too few brood per season to
exhibit a strong response to the cumulative abundance of FR. Geographic
variations can influence both the degree of sociality and the number of
broods produced within single species of Halictus andLasioglossum , with a general pattern of more solitary bees and
fewer broods being produced at higher elevations and latitudes (Richards
and Packer 1995, Wcislo 1997, Davison and Field 2016). In our study
locations, most Halictus and Lasioglossum species are
closer to their northern range limit (Mitchell 1960), which should
increase the prevalence of populations in this region that produce fewer
broods per season and exhibit less social behaviours.
The remaining bee genera (Andrena , Augochlorella ,Megachile , and Peponapis ) were all most influenced by the
present abundance of FR in the landscape. These genera include both
eusocial (Augochlorella ) and solitary bees (Andrena ,Megachile , and Peponapis ). Although Augochlorellavisits were primarily observed during the first and second sampling
periods, the only species of Augochlorella in eastern Canada,A . aurata (Packer et al. 2007), is in flight for the
entire growing season (Mitchell 1960). Similar to Halictus andLasioglossum , some A. aurata populations are solitary,
while others produce just two broods (one worker and one reproductive
brood) per season (Packer et al. 1989). If only two broods were produced
over the entire season by A. aurata populations, we might have
been unable to observe any influence of cumulative FR abundance by the
second time period (only the first and second time periods were analyzed
for this genus). The fact that visits from the solitary bee generaAndrena , Megachile , and Peponapis were apparently
unaffected by past FR makes sense in light of the short flight periods
of individual species within these genera. Although Andrena were
found foraging over the entire season, this genus comprises 75 species
in eastern Canada (Packer et al. 2007), many of which are active as
adults for just one or two months (LaBerge 1986, Larkin et al. 2008).Megachile were observed foraging during the second, third, and
fourth time periods, but a number of the species in this region have
more restricted foraging periods (Mitchell 1962, Sheffield et al. 2011).
The single local species of Peponapis , P. pruinosa , is a
specialist on pollen in the Cucurbitaceae family and has a foraging
period synchronized with its flowering in southern Ontario (Willis and
Kevan 1995). Given the prevalence of species with short flight periods
in our study area, the foraging periods of many individual species were
likely too short to respond to fluctuations in FR at the roughly monthly
scale we considered. Future research should focus on examining how
fluctuations in FR over shorter temporal scales (e.g., weekly) influence
bee activity, which would allow for development of agricultural
landscapes that specifically benefit those species with short flight
periods.
Despite the variety of life-history traits represented byAndrena , Augochlorella , Megachile , andPeponapis , all four genera responded similarly to the present
abundance of FR; visits were generally fewer in landscapes that had a
high abundance of FR. Several studies have previously found that
abundant FR can decrease bee density on crops, either through dilution
of pollinators across a landscape (Kovács-Hostyánszki et al. 2013,
Holzschuh et al. 2016), or through distraction of pollinators from crops
to other resource-rich areas (Lander et al. 2011, Nicholson et al.
2019). This may indicate that the landscapes used in our study generally
provided a high amount of FR outside the local sampling areas, perhaps
because we selected sampling locations based on their proximity to farms
growing fruit or vegetables. Population sizes for solitary bees that
produce a single brood per season (Andrena , Megachile , andPeponapis ) should also be strongly limited by the amount of FR
available in the previous year, which would be used to produce the
generation foraging in the current year. Since we did not know the
relative abundance of FR in the previous year, this may have been the
primary factor limiting bee populations, especially for species that
only forage for a few weeks in a season.
Differences in body size can contribute to differences in the maximum
foraging ranges of bee taxa (Greenleaf et al. 2007) and thus to
availability of FR to bees within the landscape surrounding sampling
locations. For most genera, we found that the number of bee visits
observed within a transect was best predicted by landscape FR at a
consistent spatial scale. Within genera like Andrena ,Halictus , and Lasioglossum , individual species can vary
greatly in body size (Mitchell 1960), but the average body size across a
genus did not seem to correlate with the spatial scale at which
landscape FR was most relevant. Visits for Andrena , a relatively
small-bodied bee (body length ranges from 4–15 mm; Mitchell 1960) were
best predicted by FR at 250 m, the smallest spatial scale we measured,
while visits from other small-bodied bees like Augochlorella(average body length of A. aurata is 5.25 mm; Mitchell 1960),Halictus (body length 7–13 mm; Mitchell 1960) andLasioglossum (body length 3.5–10 mm; Mitchell 1960) were best
predicted by FR at 750 m, the largest spatial scale measured. On the
other hand, visits from the relatively large-bodied Bombus (body
length 5–28 mm; Laverty and Harder 1988) and Megachile (body
length 6–25 mm; Sheffield et al. 2011) were best predicted by the
abundance of FR within just 250 m around a sampling location. The
spatial arrangement of both FR and nesting habitat in a landscape are
likely the more relevant predictors of how far most bees are actually
foraging (Zurbuchen et al. 2010). The spatial scales we have determined
as the best predictor of bee visits may therefore represent the upper
end of foraging areas used by bees in the majority of landscapes that we
examined, with many bees actually foraging in smaller areas of
landscapes with more densely packed resources.
By teasing apart the responses of individual genera, we discovered a
diversity of responses among taxonomic groups, highlighting potential
problems with lumping all non-Bombus bees into a single
functional group, or with examining responses of the entire bee
community to FR. Our research highlights the importance—particularly
for social taxa—of not only the current floral resource landscape but
also the FR present earlier in the season. This information can help
determine how to configure agricultural landscapes in a way that
promotes bee population persistence and growth, and thus, increases the
pollination services crops receive. Our findings suggest that bees with
longer flight periods likely benefit from continuous, consistent
provision of FR throughout a single season, and high FR abundance early
in the season. However, the number of bee visits observed may not be a
good proxy for bee population sizes. An important next step will be to
determine how across-year patterns in visitation rates change with
spatiotemporal fluctuations in FR, particularly for single-brood species
which can only respond positively to FR availability over this
timescale. Though we observed fewer visits by bees with short foraging
periods in landscapes with a high present abundance of FR, this pattern
should not hold across years: if other factors are not limiting, more
abundant floral resources in landscapes should yield higher bee
abundances in subsequent years.
Acknowledgements
Thank you to Lenore Fahrig for providing the GPS unit; to Joseph
Bennett, Lenore Fahrig, Jeremy Kerr, and Risa Sargent for their input on
early drafts; and to Katie Baillie-David, Alexander Hare, and Megan
McAulay for assistance in the field and lab. This work was funded by the
University of Ottawa and an Ontario Graduate Scholarship to JG.