RESULTS
The number of pollinator visits by the three pollinator groups
(honeybee, bumblebee, and other pollinators) varied considerably among
observed flowers (ranges: honeybees = 0–7, bumblebees = 0–38, other =
0–54; χ2 = 16.12, df = 2, p = 0.0003). Honeybees had
fewer visits compared to bumblebees (p = 0.0003) but did not differ from
combined other pollinator visits (p = 0.15; Figure 1a; Appendix S1:
Table S3, S5, and S6). On the other hand, the time bees spent on flowers
per visit (seconds) did not differ among honeybees, bumblebees, and
other pollinators (Figure 1b; χ2 = 4.95, df = 2, p =
0.08), despite substantial variation in total duration per visit among
flowers observed (ranges: honeybees = 0–219.25, bumblebees = 0–222.75,
other = 0–484 seconds). We further explored how bee species may differ
in how much time per visit they spend interacting with different aspects
of the flower, including the petals, pollen, and simultaneously
contacting the pollen and nectar (pollen+nectar). Bumblebees spent less
time per visit on petals compared to honeybees (p < 0.0001) or
other pollinators (p < 0.0001; Figure 1c). Other pollinators
spent more time per visit on pollen-only visits relative to honeybees (p
= 0.0025) and bumblebees (p < 0.0001; Appendix S1: Fig. S1).
On average, all three pollinator groups spent similar amounts of time
per visit in contact with pollen+nectar (Figure 1d; χ2= 3.60, df = 2, p = 0.17), though there was a wide range of visit times
for pollen+nectar (ranges: honeybees = 0–197.75, bumblebees =
0–218.75, other = 0–295 seconds). Overall, each pollinator group
differed in the number of visits and duration of time spent per visit
interacting with different aspects of the flowers, which could
contribute to variation in the likelihood of bees depositing or picking
up parasite spores during floral visits.
V. ceranae was highly prevalent in both honeybees and bumblebees
at all six field sites. In total, 68.0% (95% CI: 56.7–77.9%) of
honeybees and 64.0% (95% CI: 52.9–73.6%) of bumblebees had V.
ceranae detected in their midguts. V. ceranae prevalence did not
significantly differ between host species (χ 2 =
0.14, df = 1, p = 0.71). Among different sites, V. ceranaeprevalence ranged from 57.1% to 81.3% in honeybees and from 40.0% to
93.8% in bumblebees (Appendix S1: Fig. S2, Table S9).
To determine whether floral visitation behaviors were linked withV. ceranae prevalence, we explored how the number of pollinator
visits and the duration of time per visit spent interacting with certain
parts of the flower correlated with V. ceranae prevalence in
honeybees and bumblebees. Despite a lower number of honeybee visits
compared to bumblebee visits (Figure 1a), the number of honeybee visits
was the only factor that had a significant impact on V. ceranaeprevalence. V. ceranae prevalence in bumblebees was positively
linked with honeybee flower visits (p = 0.005; Table 1, Figure 2a) but
not bumblebee flower visits (p = 0.98, Figure 3a). In contrast, V.
ceranae prevalence in honeybees was not linked with honeybee flower
visitation (p = 0.57, Table 1, Figure 2a) or bumblebee flower visitation
(p = 0.47, Figure 3a). V. ceranae prevalence in honeybees and
bumblebees was also not linked with flower visitation by other bee
genera (both p > 0.54, Figure 3b; Table 1, Appendix S1:
Table S7 and S8).
We also expected that greater amounts of time bees spent per visit on
flowers and interacting with different aspects of the flower (e.g.,
petals, pollen, and pollen+nectar) would increase the V. ceranaeprevalence by increasing the chances of parasite transmission. For the
duration per visit models, we used a Bonferroni-corrected significance
threshold of 0.0125 because the durations per pollinator visit to each
part of the flower were analyzed separately. V. ceranae in
honeybees and bumblebees was not associated with the total duration per
visit of honeybees, bumblebees, or other pollinators (Table 1). However,V. ceranae prevalence in bumblebees was marginally, but not
significantly, higher the longer that honeybees spent interacting with
flowers per visit (p = 0.014, Figure 2b). We further explored this
result by breaking down the total floral visit duration by the duration
of time that bees spent interacting with different flower parts,
including petals, pollen, and pollen+nectar to determine which specific
behaviors contributed most to V. ceranae prevalence in each host
species (Table 1; Appendix S1: Table S7 and S8). V. ceranaeprevalence in bumblebees was higher the longer honeybees interacted with
pollen+nectar (p = 0.009; Figure 2c), despite no overall differences in
time spent on pollen+nectar per visit among honeybees, bumblebees, and
other pollinators (Figure 1d). V. ceranae in both host species
was not impacted by bumblebee or other pollinator duration spent per
visit on pollen+nectar (Figure 3c,d; Table 1). V. ceranae in
honeybees and bumblebees was not correlated with the time per visit that
bees spent on petals or pollen, regardless of bee species (Table 1).