10.5061/DRYAD.ZS7H44J7M
Guezen, Jessica M.
0000-0001-5841-6699
University of Guelph
Forrest, Jessica R. K.
0000-0002-5273-9339
University of Ottawa
Seasonality of floral resources in relation to bee activity in agroecosystems
Dryad
dataset
2021
FOS: Biological sciences
Bees (Anthophila)
agricultural landscape
spatiotemporal scale
floral volume
crop pollinators
University of Ottawa
https://ror.org/03c4mmv16
Ontario Graduate Scholarship*
Ontario Graduate Scholarship
2022-01-25T00:00:00Z
2021-10-08T00:00:00Z
en
https://doi.org/10.1002/ece3.7260
965813 bytes
10
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
The contribution of wild insects to crop pollination is becoming
increasingly important as global demand for crops dependent on animal
pollination increases. If wild insect populations are to persist in
agricultural landscapes, there must be sufficient resources over time and
space. The temporal, within‐season component of floral resource
availability has rarely been investigated, despite growing recognition of
its likely importance for pollinator populations. Here, we examined the
visitation rates of common bee genera and the spatiotemporal availability
of floral resources in agroecosystems over one season to determine whether
local wild bee activity was limited by landscape floral resource
abundance, and if so, whether it was limited by the present or past
abundance of landscape floral resources. Visitation rates and landscape
floral resources were measured in 27 agricultural sites in Ontario and
Québec, Canada, across four time periods and three spatial scales. Floral
resources were determined based on species‐specific floral volume
measurements, which we found to be highly correlated with published
measurements of nectar sugar mass and pollen volume. Total floral volume
at varying spatial scales predicted visits for commonly observed bee
genera. We found Lasioglossum and Halictus visits were highest in
landscapes that provided either a stable or increasing amount of floral
resources over the season. Andrena visits were highest in landscapes with
high floral resources at the start of the season, and Bombus visits
appeared to be positively related to greater cumulative seasonal abundance
of floral resources. These findings together suggest the importance of
early‐season floral resources to bees. Megachile visits were negatively
associated with the present abundance of floral resources, perhaps
reflecting pollinator movement or dilution. Our research provides insight
into how seasonal fluctuations in floral resources affect bee activity and
how life history traits of bee genera influence their responses to food
availability within agroecosystems.
Study sites and landscape structure The study was conducted in 27 farms
growing fruit or vegetable crops in Eastern Ontario and the Outaouais
region of Québec, Canada (map of sites in Figure S1). Farms planning to
grow cucurbit crops were chosen initially for inclusion because we wished
to focus on pollinator‐dependent, late‐season crops; however, many farms
were not able to grow cucurbits due to drought conditions experienced
throughout the region. To maximize independence among farm sites (i.e., to
minimize the chance that an individual bee could move between farms),
chosen farms were 4–211 km apart. Across all farm sites, 102 locations
were sampled for bees and floral resource abundance (as described below),
with one to six locations per farm, depending on the number of distinct
land patches in which resource‐providing flowers were present, and when
permission was given from landowners. Sampling locations within patches of
land were selected based on the estimated location of the patch's
centre or, if the patch was over 25 m wide, was located at least 10 m from
an edge. In three patches wider than 25 m, sampling locations less than 10
m from the edge were used due to a complete absence of flowers in bloom in
the centre. The distance between sampling locations within a farm ranged
from 3.8 m to 1,040 m. Sites were visited in rotation over four time
periods during one season in 2016: the first took place in late spring,
between May 20 and June 10 (n = 38 sampling locations), the second in
early summer, from June 10 to July 4 (n = 33), the third in mid‐summer,
from July 5 to August 1 (n = 37), and the fourth in late summer, from
August 1 to September 1 (n = 39). If sampling locations contained open
flowers during more than one sampling period, the same location was
sampled in multiple time periods. The composition of the landscape within
250, 500, and 750 m radii of each sampling location was quantified to
estimate landscape‐scale floral resource abundance. The 250–750 m scale
has been found in previous studies to be the range at which non‐Apis bees
respond to landscape structure (Steffan‐Dewenter et al., 2002), and 500 m
was chosen as an intermediate spatial scale. Sampling locations within the
same farm site (and with overlapping radii at the 750 m scale) were not
treated as independent (see Statistical analysis). Within a 750 m radius
around each sampling location, the boundaries between land patches were
manually digitized in QGIS version 2.18.7, using both waypoints taken
on‐site with a Trimble® Juno SD handheld GPS unit (Trimble Navigation
Limited), and from Google Earth and Bing Aerial satellite imagery. Each
land patch was then categorized by the type of land‐use (hereafter, “land
type”), through ground‐truthing and raster imagery from Agriculture and
Agri‐Food Canada's (AAFC) 2016 Annual Crop Inventory. Land types fell
into three categories: non‐resource land, resource‐providing land, and
unknown land (see Table S1 for detailed descriptions of each land type).
Non‐resource land was defined as any area that did not provide floral
resources, which included crops with exclusively wind‐pollinated flowers
and crops with anecdotal or no evidence of bees collecting resources from
flowers. Urban and developed land, which comprised approximately 8.5% of
all area surrounding sampling locations, was also included in non‐resource
land; although residential gardens may provide floral resources for bees,
the amount is inconsistent over time and space (Cane, 2005; Matteson et
al., 2008) and appeared in our study to be highly variable across
locations. Furthermore, other components of urban and developed land
(e.g., pavement, mown lawns) are often devoid of floral resources.
Resource‐providing land was defined as land areas that provided floral
resources for bees at some point during the season and was categorized
into 14 different land types (Table S1). Sampling locations were located
only within resource‐providing land, and at least one of each
resource‐providing land type was sampled during each time period. Unknown
land was comprised of areas where we could not determine the crop grown
(2.3% of all area surrounding sampling locations); hedgerow (1.8%); crop
land where potentially resource‐providing crops were grown, but floral
resources were not measured (0.7%); and soybean (10%), which is of
uncertain value as a floral resource for bees. There is some anecdotal
evidence for cross‐pollination by honey bees resulting in increased
soybean yields (Ahrent & Caviness, 1994; Erickson et al., 1978),
and 29 species of wild bees (including eight of the species observed in
this study) have been found visiting soybean in Delaware, Wisconsin, and
Missouri, USA (Rust et al., 1980). However, many varieties of soybean are
cleistogamous, or self‐fertilize before flowers open, and insect
pollination of Ontario‐grown varieties is not expected to increase yields
(OMAFRA, 2015). Bee observations Bee observation methods were adapted from
frequently used pollinator surveying designs (Alarcón et al., 2008; Gibson
et al., 2011; Memmott, 1999). At each sampling location, a transect was
set up to survey bee activity within a 30 m × 4 m area (89 transects); a
30 m × 2 m area was surveyed when only one crop row (< 4 m wide)
was present (eight transects); and 25 m × 4 m (one transect) or 24 m × 4m
areas (four transects) were surveyed when crop rows were shorter than 30
m. Bee observations occurred over 1 min per 4 m2 of transect intervals by
slowly walking the length of the transect. The shaded and unshaded
temperature, maximum wind speed, and average wind speed were recorded for
at least 1 min using a Kestrel® 2000 Pocket Weather® Meter
(Nielsen‐Kellerman) held at approximately 1.5 m above ground preceding
each observation period. If there was a noticeable change in conditions
during the observation period, temperature and wind speed were recorded
again at the end of the period and averages were recorded. All bee
observations were conducted when shaded temperatures were above 11.9°C
(mean ± SD = 25.3°C ± 4°C), average wind speeds were below 1.9 m/s, and
maximum wind speeds were below 4 m/s. During observation periods, all
occurrences of bees visiting open flowers were recorded by two observers,
standing on either side of the transect width, and recording all visits
within 2 m each. A visit was counted when a bee was seen contacting sexual
organs of an entomophilous flower or was probing a flower for nectar. All
visited flowers were identified to genus (9 out of 77 taxa) or species (68
out of 77 taxa), and bees were identified on the wing to genus or species.
When identification was not possible on the wing, observations were paused
and both observers attempted to catch the bee to take a photograph from
inside a glass vial or to collect it as a voucher (79 specimens total).
Vouchers were then identified to species or genus and are stored in the
Forrest laboratory's collection at the University of Ottawa (Ottawa,
ON, Canada). Overall, 82% of bees were identified to species, 17% to
genus, 0.1% to family, and 1% as Anthophila. The full list of bee taxa can
be found in Table S2. Floral resources Floral density was recorded at each
sampling location, using three quadrats of 1.5 m × 1.5 m. Quadrats were
placed in random locations within the same transect used for bee
observations, immediately following the observation period. If no open
flowers were present in all three quadrat locations, an additional
location was randomly selected and the mean count across the four quadrats
was recorded. Within a quadrat, the number of open flowers was counted for
each nongraminoid species encountered; for species with many‐flowered
inflorescences, five individuals were haphazardly selected, and the number
of flowers was counted on a randomly selected inflorescence. The mean
number of flowers per inflorescence for many‐flowered species was then
multiplied by the number of inflorescences in a quadrat to obtain the
number of flowers per quadrat. In members of the Asteraceae family,
capitula were treated as single flowers (see Table S3 for descriptions of
floral units used for counts of each species). For 29 out of 96 species
encountered, the number of flowers per inflorescence was obtained from
either literature sources or digital images of herbarium specimens because
of the large number of flowers encountered in the field or because (in a
few cases) the species was inadvertently overlooked in the field (see
Table S3 for literature values for each species). To estimate the amount
of floral resources (nectar and pollen) provided by a species, floral
dimensions were measured on five haphazardly selected individuals of each
species. The length and width of the receptacle (or capitulum in
Asteraceae species) were measured at right angles to each other, as well
as the height from the receptacle to the end of the longest sexual organ
(stamen or pistil); in species with sexual organs completely hidden within
a corolla, height was measured from the receptacle to the end of the
corolla. Measurements were made using calipers and were rounded to the
nearest 1 mm. Thirty‐one of 96 species were not measured in the field, and
floral measurements were instead obtained from literature sources or
digital images of herbarium specimens (see Table S3 for measurements and
literature sources for each species). Floral measurements were used to
calculate both the surface area of flowers (A = πab) and the volume of
flowers (V = πabh), where a is the semi‐major axis, or half the length or
width (whichever was longest) of a flower's receptacle or capitulum,
b is the semi‐minor axis, or half the length or width (whichever was
shortest) of a flower's receptacle or capitulum, and h is the height
of a flower or inflorescence (Figure 2c and Table S3). To determine which
measurement of floral dimensions was the best proxy for floral resource
amount, literature searches for daily nectar sugar mass (µg/day) and
pollen volume (in µl/flower) were conducted for all flowering species
encountered; these measurements have been previously used to assess floral
resources available to pollinators (Baude et al., 2016; Hicks et al.,
2016). Literature sources that provided counts of pollen grains per flower
and volumes of individual pollen grains were used to calculate an estimate
of pollen volume per flower for species for which we could not find
measurements of total pollen volume. Nectar sugar mass was obtained for 46
species and pollen volume for 33 species of the 96 encountered (see Tables
S4–S5 for full species lists). Pearson correlations between nectar sugar
mass or pollen volume and the length, width, height, surface area, and
volume measurements of each species (all variables log‐transformed to
approximate normal distributions) were used to determine which floral
dimension could best estimate the amount of floral resources. In addition,
to determine whether the source of floral volume measurements (literature,
in‐field measurements, or combination of both; see Table S3) influenced
the relationship between floral volume and either nectar or pollen, we ran
ANCOVAs on daily nectar sugar mass and pollen volume as functions of
floral volume, measurement source, and their interaction. The interaction
was nonsignificant for both nectar (F2,40 = 0.82, p = .45) and pollen
(F2,28 = 0.18, p = .83), indicating that it was reasonable to combine data
sources. For all bee genera other than Peponapis, the abundance of floral
resources in the landscape surrounding each sampling location was
calculated by determining the mean floral resource value per flower of
each species and multiplying this value by the count of each flower in a
quadrat. Peponapis collect pollen exclusively from squash (Cucurbita spp.;
Hurd et al., 1974), and we only observed Peponapis visiting squash and
cucumber (Cucumis sativus) flowers (both Cucurbitaceae). Therefore, in
models of Peponapis visits, the abundance of floral resources in the
landscape surrounding each sampling location was calculated from the mean
floral resource value per squash or cucumber flower. While other bee
genera such as Andrena likely included some oligolectic
(pollen‐specialist) species, we included all rewarding plant taxa in
calculations of floral resources for genera other than Peponapis, as
oligolectic species would make up a much smaller proportion of the total
than in Peponapis. Furthermore, collectively, all oligolectic species
within other genera would likely be specialized on pollen from multiple
taxonomic groups, rather than a single family as in Peponapis. The mean
abundance of floral resources per 1 m2 was then calculated across quadrats
for each transect, and the median of the transect‐level values was
calculated for each land type during each time period. This number was
then multiplied by the total area of each land type within 250, 500, and
750 m around a sampling location to obtain an estimate of the total floral
resources at a given spatial scale during a given time period.
Guezen_Forrest_shapefiles_2021 folder: See ReadMe file included.
Bee_visits.csv, Floral_counts.csv, Full_dataset.csv: See
ReadMe_for_CSV_files.csv for description of all columns.