Behavior of Bees Associated with the Wild Blueberry Agro-ecosystem in the USA

Behavior of Bees Associated with the Wild Blueberry Agro-ecosystem in the USA
IJEN
Behavior of Bees Associated with the Wild Blueberry
Agro-ecosystem in the USA
*Francis A. Drummond
*School of Biology and Ecology, 305 Deering Hall, University of Maine, Orono, Maine USA 04469
Email: frank.drummond@umit.maine.edu, Tel.: 207 581-2989, Fax: 207 581-2969
Greenhouse and field studies were conducted between 1996 and 2014 in Maine to assess the
behavior of selected bee taxa that visit wild blueberry, Vaccinium angustifolium (Ericaceae)
Aiton. Some of my findings are as follows. When individual foraging efficiency was assessed on
wild blueberry for four common bee pollinators, bumble bees were most efficient and honey
bees were the least efficient in terms of the number of pollen grains deposited on a stigma in a
single visit (P< 0.0001). However, I also found that the prior bumble bee visitation to flowers
enhanced the pollination efficacy of honey bees. Field observations suggested that bumble
bees recruit to plants with higher floral density and that bumble bees and andrenids forage for
longer periods of time in the day than sweat bees and Osmia leaf cutting bees; honey bees
showed intermediate foraging durations. Honey bees and solitary native bees were found to
forage at an increasing rate with increasing air temperature, while bumble bee queens tended to
forage independently of air temperature. Foraging patterns among the following bee taxa such
as bumble bees, andrenids, megachilids, and honey bees also varied and the implications of
these differing foraging patterns relative to pollination are discussed.
Keywords: Bees, wild blueberry, Vaccinium angustifolium, pollination efficiency, flower handling time, pollen deposition,
foraging pattern
INTRODUCTION
Wild lowbush blueberry, Vaccinium angustifolium
(Ericaceae) Aiton, is the largest (in terms of land area)
managed native wild fruit crop grown in North America
(Jones et al.; 2014). Wild blueberry naturally occurs from
the mountains of Virginia and West Virginia to the
Canadian Maritimes and Quebec west to Ontario and
Michigan (Vander Kloet, 1988, Jones et al., 2014). This
plant species generally grows in acidic, sandy soils and is
an early colonizer of disturbed areas (Hall et al., 1979;
Jones et al., 2014). It is a natural occurring understory
plant species in Northern Mixed Hardwood, Acadian, and
Boreal Forests (Jones et al., 2014) and a valuable food
resource for wildlife (Martin et al., 1951; Eaton, 1957).
Management or cultivation of wild blueberry was first
practiced by Native Americans (Munson, 1901;
Hedrick,1919) and later introduced to European colonists
(Davis, 1993). This tradition of clearing forest followed by
frequent burning of the landscape to reduce plant
competition with wild blueberry is still practiced by several
farmers today (Rose et al., 2014).
Currently, Maine is the largest producer of wild
blueberry in the world with more than 24,300 hectares
under cultivation (Yarborough, 2009). Insect pollination is
critical for the set of wild blueberry flowers and fruit
development (Lee, 1958; Vander Kloet, 1988; Bell et al.,
2009; Asare, 2013). The morphology of the flower with
poricidal anthers limits the species of insects that can
effectively pollinate wild blueberry (Ritzinger and Lyrene,
1999; Bell et al., 2009). There are more than 120 native
International Journal of Entomology and Nematology
Vol. 2(1), pp. 027-041, September, 2016. © www.premierpublishers.org.ISSN: 2326-7262
Research Article

Drummond FA. 028
bee species that are associated with wild blueberry
landscapes and pollination (Boulanger et al., 1967;
Finnamore and Neary, 1978; Bushmann and Drummond,
2015). Many wild blueberry growers in Maine heavily rely
on honey bees for pollination (Hanes et al., 2013);
however, there are still several growers that rely solely
upon native bees for their pollination needs (Rose et al.;
2014). There has been a concerted effort to conserve
native bees in wild blueberry habitats by identifying their
floral resources, providing nests, and identifying threats
from pesticide applications and pathogens (Stubbs et al.,
1992; Stubbs et al., 1997; Stubbs and Drummond, 1998;
1999; Bushmann et al., 2012; Drummond 2012b; Groff et
al., 2016). The importance of wild native bee pollinators
in wild blueberry production reflects the development of
field techniques for assessing bee populations by
researchers and blueberry growers (Drummond and
Stubbs, 1997b; Drummond et al., 2015). Research on
the efficacy of honeybee pollination began at the
University of Maine in the 1950's (Boulanger unpublished
data; Boulanger et al., 1967). The importation of
commercial honeybee colonies has grown from
approximately 500 hives per year in the mid-1960's to
approximately 60,000 hives imported for the blueberry
blooming season in the year 2000 (Drummond, 2002)
and more than 85,000 in 2016 (Jadczak, Maine state
apiculture inspector, personal communication), an
increase that reflects increasing numbers of honeybee
hives per acre (Yarborough, 2013). In addition, the use
of commercial bumblebees (Bombus impatiens Cresson)
has become popular over the past 15 years with
approximately 2,300 colonies being purchased per year
for wild blueberry pollination in Maine (Stubbs and
Drummond, 2001; Desjardins and Olivereira, 2006;
Drummond, 2012b). In addition, several other potential
commercial bees have been evaluated for wild blueberry
pollination (Stubbs et al., 1994; Drummond and Stubbs,
1997a; Stubbs and Drummond, 1997a; 1997b; 1997c;
2000). Given this reliance on pollination by commercial
bees, the wild blueberry production is vulnerable to
disruption by lack of pollination services. However,
despite the increasing reliance on commercial bee
pollinators in wild blueberry, native bees are still
significant in determining the fruit set and yield (Asare,
2013; Yarborough et al., 2016). Indeed, U.S. consumers
are willing to pay more for blueberries pollinated by native
bees (Stevens et al., 2015).
However, there have been few studies on their
efficacy as pollinators of wild blueberry. Whidden (1996)
and Drummond (2012b) both showed how bumble bees
are floral constant with respect to wild blueberries and
only Javorek et al. (2002) addressed the performance of
native bees as pollinators and showed that the efficacy of
native bees on a per bee basis is much greater than that
of honey bees.
Because of this lack of knowledge about native
bee foraging in wild blueberry, the pollination efficacy of a
range of both native and exotic bee species with regards
to wild blueberry was studied in Maine. We measured
and quantified: 1) selection choice of bumble bees when
foraging among wild blueberry flowers with regards to
flower age, size or previous visitation history, 2) the effect
of flower number on stems and if this affects the bumble
bee visitation choice of those stems, 3) attractiveness of
five co-flowering species during wild blueberry bloom, 4)
bee species-specific pollen deposition on wild blueberry
flower stigmas during single visits to naive flowers, 5) bee
species-specific handling time of flowers, 6) effects of
sequential multiple flower visits on pollen deposition by
more than one species of bee, and 7) bee-specific spatial
foraging patterns in wild blueberry fields during bloom.
MATERIALS AND METHODS
This study was conducted over a period of twenty
years (1996-2015) in the greenhouse, laboratory, and
wild blueberry fields in Maine, USA. All cage studies were
conducted at the University of Maine in Orono, Maine
(Penobscot county). Field studies were conducted in
fifteen managed wild blueberry fields in Hancock, Lincoln,
Waldo, and Washington counties, Maine. Seven
experiments grouped under three studies were
conducted during this period. Methods for each
experiment are described below and a schematic (Fig. 1)
has been included to provide an outline of the studies
and experiments.
Bee Preference Studies
Blueberry Flower Selection Choice By Bumble
Bees, Flower Size And Age – During March – April 2007
and then in March – April 2008, the effects of wild
blueberry flower age, corolla length (mm) and corolla
diameter (mm) on bumble bee, Bombus impatiens (Say),
choice measured by visitation frequency was studied in
the greenhouse. This study was conducted in three
replicate 2 m x 2 m x 3.5 m mesh cage in the University
of Maine Clapp greenhouse in Orono, Maine, USA. Three
bumble bee colonies (100 worker strength) were
purchased from Koppert Inc. (Romulus, Michigan, USA)
and placed in the flight cage for several days without
flowers. The colonies derived their nutritional
requirements on sugar syrup provided with the colonies
upon purchase. During the previous autumn, 12 clones
(genets) of Vaccinium angustifolium Aiton blueberry sods
were cut and excavated from blueberry fields in
Jonesboro, Maine, USA and placed in 50.8 x 40.6 cm
plastic tote boxes. The boxes were kept in a walk-in
refrigerator (2-4ºC) over the winter. In late February, the
blueberry boxes were brought into the greenhouse
(maintained at 15-22º C) and allowed to mature flowers.
Upon the bloom initiation, the flowers were measured
with a micrometer, dated, marked, and coded. In the

Int. J. Entomol. Nematol. 028
Figure 1. Outline of experiments conducted between the years 1996 and 2015, bee preference studies (A) and pollination efficacy and
foraging studies (B). Cage studies are surrounded by dashed line boxes and open field studies are surrounded by solid line boxes.
early morning prior to an assay, boxes of blueberry in
bloom, not used for experimentation, were placed into the
cages, bumble bee hives were opened and access to
floral resources were allowed. Immediately prior to the
start of a choice assay, all blueberry boxes were removed
and two stems with a single open flower on each
(standardized by either flower age (1-8 days old), corolla
length, or diameter) were presented to foraging bumble
bees. The stems were placed in a test tube holder such
that stems were 23 cm apart. Flowers were observed
until a bumble bee landed on the flower and began to
extract either nectar or pollen. At this point the visited
flower was recorded.
Bees, Previously Visited Flowers - In 2008, one choice
bioassay was conducted to determine if flowers that had

Drummond FA. 029
not previously been visited by a bee compared to similar
age and size flowers that had been visited by a bee were
differentiated by foragers. Sixteen replicates of paired
flowers categorized by presence or absence of previous
visitation were run in the exact same manner as
described above for the flower size and age assays. A
non-choice bioassay using visited flowers from the
previously described bioassays was used to determine if
previously visited flowers (ranging from 1-6 visits)
affected the flower choice by bumble bee foragers. Fifty-
three replicate trials were used in this bioassay. In all
bioassays conducted over both years, if no visitation
occurred in 15 minutes then the trial was terminated and
new pairs of stems were introduced. A total of 106 choice
assays were conducted over the two-year study. Nominal
logistic regression was used to test if differences among
years, flower age, corolla length, and previous visitation
influenced flower selection for first visit (JMP
®
, 2015).
Choice For Blueberry Flowers Compared To Five
Co-Flowering Native Shrubs - This study was performed
on 21 and 22 May, 2008. Flowering shrubs that bloom
during wild blueberry bloom in Maine that are often found
growing around the field edges of wild blueberry fields.
We selected five of the most common co-flowering
shrubs in Downeast Maine to test the preference of B.
impatiens foragers for blueberry over the five co-flowering
shrubs. The species selected for study were shadbush,
Amelanchia spp.; apple, Malus pumila; rhodora,
Rhododendron canadense; choke cherry, Prunus
virginiana; and bunch berry, Cornus canadensis. Several
flowering stems of these species were collected and each
was tested against the wild blueberry stems in flower
collected at the same time. A paired choice bioassay in
the same manner as discussed in the former experiment
in a 2 x 2 x 3 m mesh flight cage was setup in a
greenhouse at the University of Maine, Orono, Maine.
Commercial bumble bees, B. impatiens were purchased
prior to the experiment (Koppert, Inc.) and used in all
assays. All paired choice bioassays consisted of a vase
of cut flowering wild blueberry stems and a vase of cut
flowering stems from one of the five co-flowering
shrubs.Pairs of cut stems were exposed to foraging
commercial worker bumble bees (B. impatiens) for five
consecutive trials. For this experiment, since the age of
the gathered blossoms could not be determined, the age
of the blueberry blossoms was not taken into account. It
was important to keep the floral displays between the
blueberries and the gathered blossoms in the same
volume to ensure bees would not be attracted to a larger
blossom display, ensuring each flower species an equal
opportunity to be chosen. For example, the apple
blossoms, being rather large were paired with several
blueberry stem cuttings so the overall total blossom area
was similar for each flower species. Data recorded for
each assay was the first floral species visited in the
paired presentation and the amount of time spent on
each floral species in a five-minute period of observation.
The pair of stems was removed from the cage after each
assay and a new pair of stems was selected. At least ten
replicates for each pair of co-flowering and blueberry
stems were conducted. After the trials, the flowers that
had been presented in each vial were photographed and
scanned into a computer to measure the amount of area
associated with each presented flower blossom.
Analyses of covariance (ANCOVA, covariate was area of
floral display; JMP
®
, 2015) was used to determine if the
total time bumble bees spent foraging on wild blueberry
was significantly greater than the time spent on the other
flowering shrubs during the 5-minute assay. Nominal
logistic regression (JMP
®
, 2015) was used to assess
differences in initial choice in visitation of blueberry
compared to other co-flowering plant species.
Recruitment of Foraging Honey Bees,
Commercial Bumble Bees And Native Wild Bees To
Clone Flower Density In The Field - Two studies were
conducted at three locations in Maine in 2008. The first
study was conducted in Union and Winterport, Maine.
The fields were visited during bloom on 14 and 15 May.
Ten clones (genets) in a blueberry field in Union were
randomly located and flagged and 24 clones in a
blueberry field in Winterport were located and flagged. In
each clone 30 stems were arbitrarily selected and the
total number of flowers (pre-bloom and blooming) on
each stem was counted. This provided a mean floral
density for each clone. A square meter quadrat was
marked out with string in each clone in both fields. Bee
observations were made in each clone for three minutes
and the number of bumble bee queens, native wild bees
other than bumble bees, and honey bees visiting each
quadrat during the three minute period were recorded
over the two day period. Linear general models (JMP
®
,
2015) were used to determine if the bees recruit more
heavily to clones with higher floral density.
The second study was designed to assess the
flowering stem selection by commercial bumble bees as
a function of total and open flowers. During bloom (May)
in 2008, at the University of Maine blueberry research
farm, Blueberry Hill in Jonesboro, Maine a field study was
conducted to determine the frequency of visitation by B.
impatiens workers to wild blueberry stems with opened
and non-opened flowers. Prior to bloom 20 commercial
bumble bee quads (Koppert, Inc.) were placed in one of
the blueberry fields (ca. 8 ha). The density of bumble
bees from this stocking density of commercial bumble
bees is approximately 3,500-4,000 workers. Thirty-six
stems were each marked by a thread tied about the stem
base. The stems were apportioned to six clones (6
marked stems in each clone). During ten observation
times throughout 12-15 May, each stem was observed for
2 minutes and the number of B. impatiens workers
visiting flowers on each stem was recorded. A general
linear model was used to determine if B. impatiens

worker visitation to stems was related to clone, total floral
density, or solely open floral density (JMP
®
, 2015).
Bee Pollination Efficacy Studies
During May and June of 1996 a preliminary study
was conducted to assess individual bee pollination
efficacy in flight cages. This study enabled us to refine
methods to repeat a study with higher replication, using
the modified methods in May and June of 2006, and May
2014.These studies were conducted using field cage
studies in both the greenhouse and field to determine the
efficacy of common bee pollinators of wild blueberry.
Single Floral Visits - The bee species used in the
studies were the bumble bee, Bombus impatiens
(Apidae) Cresson; the leaf cutting bee, Osmia atriventris
(Megachilidae) Cresson; the digging bee, Andrena carlini
(Andrenidae) Cockerell, and the honey bee Apis mellifera
(Apidae) (L.). Studies conducted during bloom (mid-May
to mid-June) in 1997 and 2006 were aimed at
determining flower handling time and the number of
pollen grains placed on a new previously non-visited
stigma in a wild blueberry (V. angustifolium) flower. The
study was conducted in mesh flight cages either placed in
a non-flower bearing field over Andrena carlini nest
aggregations or in the greenhouse (see study 1 above).
Bumble bee colonies, honey bee colonies, or Osmia
atriventris nest blocks with active females provisioning
cells, were placed in cages with 1-4 totes of flowering
wild blueberries to allow foraging to take place and pollen
acquisition by each of the bee species. Several of the
stems in each tote (5-20) were covered with fine mesh
bags to prevent bee access to the flowers. Flowers on
each bagged stem were marked and the day that each
flower opened was recorded. Once bees were observed
actively foraging and pollinating non-bagged flowers on
stems in the totes placed in the cages, the bags were
removed from stems with 1-5 day old flowers. Bee visits
of each bee species (only a single bee species per cage)
to newly un-bagged flowers were recorded. During
visitation to each un-bagged flower the handling time
(from initial contact of the flower until the time when the
bee left the flower) was measured with a stopwatch. As
soon as the visiting bee left the flower, the stem was put
in an ice filled cooler for temporary storage until the end
of the day’s assay. All stems with marked visited flowers
were taken immediately to the laboratory where the
stigma was stained (Alexander stain, Alexander 1980)
and inspected under the microscope for V. angustifolium
tetrad pollen grains. Twenty-five replicate recordings of
flower handling time and pollen deposition were made for
each species in 2006.
One-way analyses of variance (Welch’s adjusted
F-test for unequal variances, complete randomized
design; JMP
®
, 2015) were used to determine if
differences due to bee species existed when considering
handling time and pollen deposition per visit. Tukey post-
hoc multiple comparison tests were used to compare all
means with one another (JMP
®
, 2015).
Sequential Floral Visits - In May 2014, a similar
flight cage study to that described above was used to
assess potential interactions in pollen deposition between
honey bees and bumble bees when flowers were visited
twice by bees. The goal of this study was to determine if
pollination synergy occurs when bumble bees and honey
bees both forage on blueberry flowers sequentially
compared to only one of the two bee species visiting
flowers sequentially.
This study was conducted using two mesh flight
cages in the greenhouse (see above). The bee species
used in the study were the bumble bee, Bombus
impatiens Cresson and the honey bee Apis mellifera (L.).
Bumble bee colonies or honey bee colonies were placed
in cages with 1-4 totes of flowering wild blueberries to
allow foraging to take place and pollen acquisition by
each of the bee species. Only a single bee was allowed
to forage at a time. Stems were protected from foraging
bees with mesh bags as described above and marked
when flowers opened. Once bees were observed actively
foraging and pollinating non-bagged flowers on stems in
the totes placed in the cages, bags were removed from
stems with 1-5 day old flowers and the cages were
removed of all bees. Individual new bee visits of each
bee species (only a single bee species per cage) to
newly un-bagged flowers were recorded. As soon as a
visiting bee left the first un-bagged stem (flower A), the
bee was allowed to visit a second un-bagged stem
(flower B). The second visited un-bagged stem (flower B)
was excised and placed in a cooler until it was brought to
the lab. The bee in the cage was discarded and the stem
with the first visited flower (flower A) was excised and put
into a test tube filled with water and transported to the
flight cage with the other bee species. A new bee in this
flight cage was allowed to visit the flower on the stem
(flower A) that was previously visited in the other cage by
the other species. After the visit to flower A in the other
cage the stem (flower A) was tagged and placed in a
cooler. Immediately after a bout of visitations, stems
placed in the cooler were brought immediately to the
laboratory where the stigma was stained and inspected
under the microscope for V. angustifolium terad pollen
grains as described above. Twenty replicates of each of
the four treatments were performed: 1. single visit by
honey bee that had previously visited a flower; 2. single
visit by bumble bee that had previously visited a flower; 3.
A single visit by a bumble bee that had just previously
visited a flower visited by a honey bee; and 4. A single
visit by a honey bee that had just previously visited a
flower visited by a bumble bee. One-way analysis of
variance (Welch’s adjusted F-test for unequal variances,
complete randomized design; JMP
®
, 2015) was used to
determine if differences in pollen deposition occurred
between treatments. A Tukey post-hoc multiple

Drummond FA. 031
comparison test was used to compare all means with one
another (JMP
®
, 2015).
Foraging Studies
Diurnal Foraging Patterns Of Bees In Wild
Blueberry And Response To Air Temperature - On May
21-31, 2001, observations of bee activity were made in a
wild blueberry field in Winterport, Maine during peak
bloom. Bees were sampled with a 30.5 cm diam.
sweepnet. A total of 10-50 locations in the field were
sampled. At each sampling location ten 180º sweeps in
the blooming crop were conducted. Sampling was
conducted every 2-3 hrs starting at 6 AM, shortly after
sunrise, and ending at dusk, 8 PM. Sampling was
conducted each day between 21 may and 31 May. On
most sampling periods, the air temperature was recorded
on-site with a handheld weather data logger (Kestrel®).
Bees were classified in the field into taxonomic groups
and their numbers recorded. The groups were the
following: honey bees, bumble bees (Bombus spp.),
digger bees (Andrena spp.), sweat bees (Halictidae), and
leaf cutting and mason bees (Megachilidae, almost
entirely Osmia spp.). Sweepnet capture of each taxon
grouping was tallied for each sampling time and the
percent of relative capture by sampling time was
calculated and plotted. Visual inspection of the data in a
graph was used to draw conclusions about the diurnal
activity of the different groups of bee foragers. Linear
regression analysis was used to assess the relationship
between air temperature and the percent of the honey
bee, bumble bee queen, and native solitary bee (Andrena
spp. + Megachilidae + Halictidae) population for each day
that was foraging.
Bee Spatial Foraging Patterns Within And Among
Clones - During wild blueberry bloom (mid-May to mid-
June) in 2003, 2004, 2005, 2006, 2007, 2008, 2009, and
2010; the spatial movement patterns of foraging honey
bees and native wild bees were delineated and recorded.
The blueberry fields were located in Union (Knox Co.),
Winterport (Waldo Co.), and Columbia, Jonesboro, T-18,
and T-19 (Washington Co.), Maine. Using a digital audio
recorder, we assessed the distances between stems that
were visited by foraging bees, distances between visited
flowers within a stem, the number of flowers visited per
stem by bees, and the cardinal direction bees flew when
moving from one stem to the next. The bees observed
and mapped in this study were honey bees, (Apis
mellifera), Bombus spp. (mostly B. ternarius), Andrena
spp., and Osmia spp. Data was recorded on individual
bees until the bee was lost among the blueberry foliage
or it left on a long distance flight where it was not possible
to follow it any longer. At this point the foraging bout was
marked as terminated and another bee was selected for
observation. Care was taken not to disturb the bee by
observers maintaining a one-meter distance from the
foraging bee, minimizing casting shadows on the foragers,
and moving slowly while observing foragers. Frequency
distributions of distances among visited stems, cardinal
direction between stems, flowers, number of flowers
visited per stem, and stems visited per bout were
constructed and fit to theoretical probability distributions
for each bee taxon group observed (JMP
®
, 2015).
RESULTS
Study
Bee Preference Studies
Bees, Flower Size And Age - Over both years (2007 and
2008) wild blueberry flower corolla length and diameter
were highly correlated (r = +0.527, n=90, P< 0.0001).
Flower age was not correlated with either corolla length
or diameter (P> 0.05). Because of this only year, corolla
length and flower age were modeled to determine if
bumble bees select flowers to visit in choice bioassays.
Bumble bees appear to demonstrate preference for
longer wild blueberry flowers (x
2
(1) = 7.221, P = 0.007,
Figure 2), but they did not discriminate for flower age (P>
0.05) when the choice was made between flowers that
differed in age up to 6 days. However, a non-significant
trend was found, which suggests a tendency to select
younger flowers (P = 0.106). Year and the interaction
between corolla length and flower age was also not
significant. The odds ratio for the significant corolla length
effect suggests that for every difference in 1.0 mm length
between flowers that it is 2.3 times more likely that the
larger flower will be first selected by a bumble bee
forager.
Bees, Previously Visited Flowers - The trials that focused
on previously visited flowers compared to flowers that
had never been by a bumble bee showed no evidence of
choice (P = 0.715) and the trials assessing visitation to
flowers that had been previously visited from 1 to 6 times
showed no evidence of an effect on bumble bee foragers
(P = 0.363).
Recruitment Of Foraging Honey Bees,
Commercial Bumble Bees And Native Wild bees To
Clone Flower Density In The Field - I found that floral
density per stem (both open and non-opened flowers) in
clones did determine the recruitment of honey bees,
bumble bee queens, and native bees other than bumble
bees, but this effect was dependent upon site (Table
1).With regards to the entire foraging bee community (all
bee taxa), bees recruited to clones with higher total
flower density. There was an effect of bee density due to
site which is not unexpected as bee densities, especially
native bees, vary by an order of magnitude from field to
field and geographic region to region.
In the field,the frequency at which stems were
selected by foraging bumble bees in Jonesboro, Maine
was not influenced by clone (genet; P = 0.178), nor the

Figure 2. Modeled probability of a bumble bee forager selecting a flower when given a choice of two flowers. As number become
more negative on x-axis the flower chosen was smaller compared to larger flower (mm), as number become more positive, the flower
chosen was larger compared to smaller flower (mm).
Table 1. Recruitment of foraging bees to flower density / stem in a clone.
Bee taxa group Significant Factors F-test Proportion
variance
explained, r
2
Total bee community site
flower density
F(1,30) = 5.407, P=0.027
F(1,30) = 12.628, P=0.001
0.584* (0.418)**
Bumble bee queens site
flower density
F(1,30) = 5.707, P=0.023
F(1,30) = 6.221, P=0.020
0.331 (0.224)
Native bees (other
than bumble bees)
flower density F(1,30) = 6.101, P=0.019 0.364
Honey bees site
flower density
site x flower density
F(1,30) = 14.716, P=0.0006
F(1,30) = 19.864, P=0.0001
F(1,30) = 17.484, P=0.0002
0.512 (0.350)
* proportion variance explained by entire model
** proportion variance explained by flower density, based upon sequential sums of squares
number of open flowers (P = 0.417) on the stem. The
initial choice to land on the stem was significantly
determined by the number of total flowers (open and non-
open flowers: F(1,28) = 4.292, P = 0.0476), but only 12% of
the variance in the frequency of visitation to stems was
explained by the total number of flowers per stem.
Choice For Blueberry Flowers Compared To Five
Co-Flowering Native Shrubs - Bumble bee foragers do
appear to prefer wild blueberry flowers to most of the co-
flowering species both in % first visits (x
2
(4) = 21.996, P =
0.0002) and time spent foraging on flowers (F(4,111) =
2.568, P = 0.042; Figure 3). Comparing the ratio of initial
visitation to blueberry vs. the other species (t-test
comparing percent choice of blueberry to 50%, no
difference in species choice) and relative time on flowers
of blueberry compared to the other species (t-test
comparing relative time to 1.0, no difference in relative
time on two species), it can be seen that blueberry is
highly attractive to bumble bee foragers compared to the
other five species (Figure 3). The only co-flowering

Drummond FA. 033
Figure 3. Preference of Bombus impatiens workers (stipled bar) for species other than blueberry (measured in paired bioassays as
the percentage of first landings on blueberry vs the other species). In addition the relative time spent on blueberry flowers relative to
the co-flower (hatched bar). The red dashed line indicates a region where foragers spent the same time on blueberry and the co-
flowering plant and the blue dotted line indicates the region of no-preference in initial floral choice between blueberry and a co-
flowering plant species. Asterisks indicate significant differences in 1) time spent on the co-flower relative to blueberry and 2)
preference for choice of initial flower selection.
species that appeared to be as attractive to bumble bees
as blueberry in initial visitation were apple and choke
cherry, but even these two species had 3-4 times the
foraging effort on blueberry once the initial flower was
selected. There were no visits to bunch berry for any of
the assays. Rhodora was almost ignored when first initial
visits were considered, but the amount of time that
bumble bees spent foraging on this species was
equivalent to blueberry.
Bee Pollination Efficacy Studies
Single Floral Visits - Efficacy in pollinating wild
blueberry, on a per bee basis, varied by species. This
was the case for pollen deposition on floral stigmas after
single visits (F(3,43.8) = 26.977, P< 0.0001) and for
handling time of flowers for each visit (F(3,50.2) = 9.377, P<
0.0001). Figure 4 shows that pollen deposition on the
blueberry flower stigma was significantly greater after a
single visit by B. impatiens and O. atriventris, and least
by the honey bee, A. mellifera. The amount of time spent
handling the flower was greatest for the honey bee and
least for the bumble bee and leaf cutting bee. When one
considers both pollen deposition / visit and handling time,
the bumble bee and Osmia leaf cutting bee were the
most efficient pollinators tested on wild blueberry.
Javorek et al. (2002) showed similar results of bee
pollination efficiency with several of the same taxa
associated with wild blueberry.
Sequential Floral Visits - When sequential visits
were assessed by honey bees, bumble bees, or a
mixture of both bee species, we found that honey bees
visiting a flower previously visited by a bumble bee
significantly (F(3,33.8) = 19.654, P< 0.0001), increased the
amount of pollen deposited on the stigma of the
subsequent flower visited. This pattern was not seen for
bumble bees visiting previously visited flowers by bumble
bees or honey bees (Figure 5).
Foraging Studies
Diurnal Foraging Patterns Of Bees In Wild
Blueberry - Figure 6 shows that during the peak bloom,
honey bees do not start foraging until mid-morning and
they terminate foraging by early evening. The
megachilids (mostly Osmia spp. during this study) were
similar to honey bees in their foraging periodicity. The
halictids had a shorter foraging period, starting in the mid-
morning and ending by mid-afternoon. The bumble bees
started the earliest of the foraging bee community and
continued until dark. The digger bees (Andrena spp.) also
started foraging around dawn, but they finished foraging
by early evening.
Response To Air Temperature - Air temperature
was often found to be a major determinant of bee
foraging, however, light intensity, precipitation and wind
can also contribute. We found that honey bees and native
solitary bees as groups responded in their foraging
activity to increasing air temperatures (F(1,26) = 22.628,
P<0.0001, and F(1,26) = 11.841, P< 0.0001; solitary native
bees and honey bees, respectively). The proportion of
the variance in foraging activity for solitary native bees

Figure 4. Average pollen deposition on floral stigmas after a single visit and flower handling time by common wild blueberry pollinators: bumble bees,
B. impatiens, digger bees, Andrena carlini, leaf cutting bees, O. atriventris, and honey bees, A. mellifera. Bars with the same letters (uppercase –
handling time, lowercase – pollen deposition) are not significantly different, Tukey’s test, experiment-wise error rate at P< 0.05.
Figure 5. Pollen deposition on a floral stigma by a bumble bee visiting a flower previously visited by a bumble
bee and then visiting a new flower (BB/BB), or by a bumble bee visiting a flower previously visited by a honey
bee and then visiting a new flower (HB/BB), or by a honey bee visiting a flower previously visited by a honey
bee and then visiting a new flower, or by a honey bee visiting a flower previously visited by a bumble bee and
then visiting a new flower (BB/HB). Bars with the same letters are not significantly different, Tukey’s test,
experiment-wise error rate at P< 0.05.
and honey bees was 44.1 and 79.1%, respectively. It can
be seen in Figure 7 that the threshold for foraging of
native solitary bees was approximately 8ºC and that for
honey bees was approximately 11ºC. Bumble bee queen
foraging did not appear to respond to increases in air
temperature (P> 0.05). This can be expected due to the
thermoregulation exhibited by bumble bees, especially
queens (Heinrich, 1972a; 1972b; 1972c).
Bee Spatial Foraging Patterns Within And Among
Clones - The foraging bee taxa that we observed had

Drummond FA. 035
Figure 6. Diurnal foraging periodicity of honey bees and native bees, 20-31 May, 2001 in
Winterport, Maine.
Figure 7.Relationship between air temperature at time of sampling and the percent of a specific taxon group’s population (native solitary
bees, bumble bee queens, and honey bees) for a given day.
very different spatial patterns (Table 2). For instance, the
cardinal direction that a forager took upon leaving a stem
to move to the subsequent stem was fairly random and
non-directional for bumble bees and honey bees, but
almost unidirectional as if bees were following a trap line
for Andrena spp. The number of flowers per stem visited
were low for honey bees (mean = 1.6 flowers / stem,
range 1-16 flowers visited per stem) compared to bumble
bees (mean = 2.5 flowers / stem, ra nge = 1-27 flowers
visited per stem), Osmia spp. (mean = 2.2 flowers / stem,
range = 1-7 flowers visited / stem), and Andrena spp.
(mean = 2.7 flowers / stem, range = 1-10 flowers visited /
stem). The average distance that honey bees moved
between stems for foraging was 0.1 m, while Bombus
spp. was 0.3 m, Osmia spp. was 0.4 m, and Andrena spp.
was 1.7 m. An example of the distribution of flowers
visited per stem between honey bees and Andrena spp.
is shown in Figure 8.

Table 2. Probability density function fit to the frequency distributions of the number of stems per bout, distance between
stems (m), cardinal direction to the next stem, and flowers visited per stem for four taxa of common bee pollinators of wild
blueberry in Maine.
bee taxon
group
sample size
of measure
measure distribution parameters goodness of
fit*
Osmia
spp.
47 stems / bout Gamma
Poisson


0.118 (P)
45 distance between stems
(m)
Gamma 

0.073 (CM)
38 cardinal direction Gamma
Poisson


0.708 (P)
87 flowers visited / stem Poisson 

0.351 (P)
Andrena
spp.
15 stems / bout Exponential  0.150 (K)
(m)
Weibull 

0.779 (LR)
24 cardinal direction Gamma
Poisson


0.364 (K)
81 flowers visited / stem Exponential  0.999 (LR)
Bombus
spp.
173 stems / bout Log Normal u = 2.767
 = 1.061
0.10 (D)
(m)
Weibull 

0.994 (LR)
2508 cardinal direction uniform na** na
2536 flowers visited / stem Beta 



0.204 (K)
Honey
bee, A.
mellifera
610 stems / bout Beta 



0.251 (K)
(m)
Exponential  0.298 (LR)
4903 cardinal direction uniform na na
5333 flowers visited / stem Poisson  0.999 (P)
* probability value for goodness of fit to theoretical distribution, (test statistic) = P: Pearson chisquare, CM: Cramer von Mises, K:
Kolmogorov’s D, LR: adequacy LR test.
** na: not applicable.
DISCUSSION
Over 120 species of bees have been found to be
associated with wild blueberry in Maine (Bushmann and
Drummond, 2015). Little is known, however, about their
behavior and activity during the blooming season. The
collection of studies, reported here, begin to shed light on
how individual bee species or groups of species play a
role in wild blueberry pollination.
There are several major areas that I would like to address
in this discussion.
First of all, it is apparent that bees, as shown by
our work with bumble bees, make choices both at the
blueberry flower level, but also at the stem floral density
level and they make choices between competing
flowering shrub species and wild blueberry
flowers.Bumble bees (B. impatiens) apparently choose
flowers according to size, the longer (or wider, as the two
traits are highly correlated)were preferred. Blueberry
flowers reflect UV light (Schaefer et al., 2004) and is
attractive to several species of bees (Kevin and Baker,
1983); thus, it is not surprising that such a preference
takes place during foraging. It was surprising to see that
flower age did not affect the choice in foraging bumble
bees. Despite intact floral resources and most likely not
lower than younger flowers, it has been demonstrated
that wild blueberry flowers lose their receptivity to pollen
over a 8-10 day period with maximal receptivity only

Drummond FA. 037
Figure 8. Frequency distribution for distance between stems moved by honey bees (a) and Andrena spp.
(b).
lasting for 4-5 days (Drummond, unpublished data). It has
been shown that as many flowers age and start to
senesce they change in color and become less attractive
to bees (Gori, 1989). This could be interpreted as a plant
signaling phenomenon, beneficial to the plant and the
bees (Casper and La Pine, 1984). I found a non-
significant trend (P = 0.106), which suggests that
rejection of older resource depleted flowers by bees
might be occurring among a background of relatively rich
nectar and pollen resources. In most bee pollinated crops
the choice of visitation may not operate in the field since
most crops are monocultures of a single genotype, unlike
wild blueberries (Bell et al., 2009).
Wild blueberry is a mass flowering crop that
produces up to 8,000 flowers / m
2
(Jones et al., 2014).
Flower production per stem can vary greatly from clone
(genet) to clone (Bell, 2009). Therefore, despite a
managed field being a continuous “carpet” of plants or
clones, flower density varies spatially across fields. We
found that bumble bees, and we hypothesize that this is
the case with other bee taxa, recruit preferentially to
clones with a higher density of flowers. The proportion of
variance in bumble bee foragers recruiting to clones was
high (r
2
= 0.418), which suggests that there may be a
selective advantage to individual plants or genotypes to
produce as many flowers per stem as possible as has
been suggested in other mass flowering plant species
(Augspurger, 1980). One would also presume that this is
an advantage to foraging bees as high floral density
should minimize the energy output per unit energy
acquired from flowers per unit of time (Waddington et al.,
1979).
The last of my findings relative to flower choice
by bumble bees was contrary to the findings of previous
studies (Goulson et al., 1998; Stout et al., 1998). It has
been observed in other studies that bumble bees tend not
to visit flowers that have previously been visited as
frequently. It is often suggested that several species of
bumble bees mark flowers when visiting them and this
chemical signal is thought to communicate a lower level
of floral resources to subsequent bees potentially
decreasing the chance that they will visit a flower
previously visited and marked (Cameron, 1981). In two
different experiments we did not find any evidence that
suggests this is happening with bumble bees visiting wild
blueberry flowers multiple times. Wild blueberry flowers
each have on average 60-70 ovules (Bell et al., 2012a).
Flowers may need to be visited several times by bees in
order to result in enough ovules fertilized by deposited
pollen grains for fruit to be retained by the plant. Thus
mechanisms that would lower the chance of multiple
visits might reduce fruit production. However, this is
probably not the case with bumble bee queens, probably
the most efficient pollinator of wild blueberry (see below).
Bushmann and Drummond (2015) demonstrated
that there is great floral constancy in native bees in wild

blueberry fields. We had hypothesized that this might be
due to the ratio of wild blueberry flowers in a location
compared to other flowering plants that might compete
for bees adjacent to where blueberries grow. However,
our cage study suggests that at least with five species of
woody shrubs that overlap with blueberry bloom there is
a moderate degree of preference for visiting and foraging
on wild blueberry (3 of 5 species preferred and 4 of 5
species foraged on more intensely). The flowering shrubs
that are less preferred relative to blueberry might be good
candidate species for pollinator plantings used to
enhance densities of native bees for wild blueberry
pollination (Venturini, 2015). However, these species
would be important during the every other non-flowering
year of blueberry production. Under typical wild blueberry
management, flowers only occur every other year in the
two year production cycle, the other year being the prune
year where plants are in a vegetative growth phase
(Yarborough, 2009).
Not all bees appear to be equal as pollinators of
wild blueberry. Our field cage studies suggest that when
measuring both pollen deposition per visit and flower
handling time, queen B. impatiens and O. atriventris are
more efficient that A. carlini and A. mellifera. The non-
native honey bee (A. mellifera) is the least efficient, but
this bee is often placed in fields during bloom providing a
foraging force of hundreds of thousands per hectare (up
to 10 colonies per hectare, Drummond, 2012a).
Therefore, in this case, the inefficiency of the species as
a pollinator of wild blueberry can be countered by its high
density, a factor often overlooked by pollination
ecologists. It is most likely the poricidal anthers (Bell et al.,
2009) that make wild blueberry a difficult flower for honey
bees to extract and then deposit pollen. Our observations
suggest that honey bees exclusively nectar feed on wild
blueberry flowers and lack a behavioral repertoire for
manipulating the anthers; thus, they only extract pollen
inadvertently while probing nectaries. The native bees we
studied had behavioral mechanisms for extracting
copious amounts of pollen. Bumble bees and andrenids
vibrated (buzz pollinated the flowers; Buchmann et al.,
1983) wild blueberry flowers and Osmia leaf cutting bees
crawled into the flowers and drummed the anthers with
their forelegs displacing pollen.
I found that the efficiency of the honey bee as a
pollen vector can be enhanced if the honey bee visits a
flower previously visited by a bumble bee and then
subsequently visits a new flower. We think that this might
be due to the following phenomenon. When a bumble
visits a flower it either vibrates the flower releasing a
large amount of pollen that coats the interior of the flower
or a bumble bee that has previously vibrated a flower
itself gets coated with pollen on its head and abdomen,
then when nectar-feeding, the bumble bee will coat the
interior of the flower. Now when a honey bee visits a
flower to nectar feed it might transfer much of the pollen
residue from the inside of a flower to the stigma. This is a
conjecture that will need to be tested.
Another aspect of pollination efficiency might be
the spatial pattern of bee movement between stems and
within a stem between flowers. Wild blueberry flowers, for
the most part are obligate out-crossers, except for 10-
20 % of clones in a field that have the capacity to self
fertilize (Bell et al., 2010; Bell et al., 2012b). The
implications of this is that bees that forage with larger
intra-stem movements and fewer visits of flowers per
stem, and with directional movement in a blueberry field
(i.e., not randomly moving independent of cardinal
direction) should be a better pollinator from the “plant’s
perspective”. My data suggests that honey bees might
not be the best pollinator relative to its random movement
and short distance moved between stems. The bumble
bee might not be the best pollinator relative to its random
directional movement. The andrenids might not be the
best pollinator relative to the number of flowers that they
visit on a stem, but this might be the best in terms of their
long flights made between stems. These attributes along
with the efficiency of pollen deposition and flower
handling time will have to be tested with simulation in
order to determine which bee species might be the best
pollinators in the wild blueberry ecosystem.
The last aspect of bee behavior that I looked at
was diurnal foraging and how temperature affects bee
activity. Certainly, different taxa of bees forage at
different times of day, but all taxa that we observed
foraged during the middle of the day during what would
be suspected of being the warmest time of the day. Early
morning after dawn and early and late evening had a
lower percentage of each taxon actively foraging and
some bees such as honey bees and megachilids were
not seen at these times. This is most likely due to air
temperatures (Corbet et al., 1993), but also possibly due
to light levels, although this is best documented for
crepuscular bees (Kelber et al., 2006). We observed that
the solitary bees and honey bees that we sampled
increased in activity in relation to increasing temperature.
Bumble bee queens appear to be active, for the most part,
independently of air temperature. This is most likely due
to their ability to thermoregulate and increase their
internal body temperature metabolically (Heinrich, 1972a).
A question might be asked how climate change might
affect bee foraging in wild blueberry. The first response
might be that warmer temperatures during bloom would
increase the length of time during the days that bees
forage on flowers, increasing pollination. However, during
our study we did not have exceptionally high
temperatures during the day. From personal experience
during the summer when temperatures can occasionally
reach > 30ºC, bumble bees will stop foraging at mid-day
and then commence foraging in the evening. If air
temperatures during bloom (mid-May to mid-June) in

Drummond FA. 039
Maine increase dramatically, then, at least for some bee
taxa, foraging activity might decrease. This could be
detrimental for the range of some species of bumble bees
as has been documented by (Kerr et al., 2015).
CONCLUSION
An understanding of crop pollination requires an
understanding of the interactions between: bees and crop
plant reproductive biology, as well as among morphology,
bee species, the abiotic environment and bee behavior
and plant behavior and physiology. This work reports on
several isolated studies that begin to increase our
understanding of several of these interactions. The
contribution of these studies is in providing quantitative
relationships that can be used to construct a computer
simulation model of bee pollination of wild blueberry.
Specifically, I have shown that bumble bees
discriminate and select larger flowers, but that flower age
or whether flowers were previously visited did not affect
flower selection. Flower density does affect long-distance
recruitment to clones, with clones characterized by higher
flower density receiving higher bee visitation. I also found
that blueberry flowers are much more attractive than five
other native co-flowering shrubs. This is important
because highly attractive shrubs that flower at the same
time as blueberry might pull bees away from the
blueberry crop during pollination. Another important
finding is that native bees are much more efficient, on a
per bee basis, than the introduced honey bee at
pollinating blueberry, in terms of flower handling time and
pollen deposition on the stigma of the flower. However,
the presence of bumble bees visiting flowers prior to
honey bees appears to increase the pollination efficacy of
honey bees. The last important finding in this study that
has direct implications to modeling pollination is that I
found differential lengths of time during the day that
different taxa foraged on blueberry and that this was
partly explained by air temperature. Bee movement in
blueberry fields was found to be dependent upon the
taxon. This aspect of bee foraging has not been
investigated in simulation models constructed to
investigate the dynamics of crop pollination. I believe that
all of my findings will allow the construction of a
preliminary model.
ACKNOWLEDGEMENTS
I would like to thank the assistance of Constance Stubbs,
Stephanie L. Allard, Lisa Campbell, Judith Collins, and
several undergraduate research assistants that helped on
data collection for these studies over the past 20 years.
This is Maine Agricultural and Forest Experiment Station
Publication3500.Financial support for some of the
objectives in this project (2011-2015) was provided by the
U.S. Department of Agriculture National Institute of Food
and Agriculture - Specialty Crops Research Initiative
Contract/Grant/Agreement No. 2011-51181-30673.
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Accepted 29 August, 2016
Citation: Drummond FA (2016). Behavior of Bees
Associated with the Wild Blueberry Agro-ecosystem in
the USA. International Journal of Entomology and
Nematology, 2(1): 027-041.
Copyright: © 2016 Drummond FA. This is an open-
access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium,
provided the original author and source are cited.

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