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Most of the world’s crops depend on pollinators, so declines in both managedand wild bees raise concerns about food security. However, the degree towhich insect pollination is actually limiting current crop production ispoorly understood, as is the role of wild species (as opposed to managed hon-eybees) in pollinating crops, particularly in intensive production areas. Weestablished a nationwide study to assess the extent of pollinator limitation inseven crops at 131 locations situated across major crop-producing areas ofthe USA. We found that five out of seven crops showed evidence of pollinatorlimitation. Wild bees and honeybees provided comparable amounts of pollina-tion for most crops, even in agriculturally intensive regions. We estimated thenationwide annual production value of wild pollinators to the seven crops westudied at over $1.5 billion; the value of wild bee pollination of all pollinator-dependent crops would be much greater. Our findings show that pollinatordeclines could translate directly into decreased yields or production formost of the crops studied, and that wild species contribute substantially topollination of most study crops in major crop-producing regions.
Cite this article: Reilly JR et al. 2020 Crop
production in the USA is frequently limited by
a lack of pollinators. Proc. R. Soc. B 287:
Received: 23 April 2020
Accepted: 7 July 2020
Subject Category:
Subject Areas:
pollination limitation, economic value, wild
bees, crop yield, ecosystem services, honeybee
Author for correspondence:
J. R. Reilly
Electronic supplementary material is available
online at
Crop production in the USA is frequently
limited by a lack of pollinators
J. R. Reilly1, D. R. Artz2, D. Biddinger3, K. Bobiwash4,5,
N. K. Boyle2,11, C. Brittain6, J. Brokaw7, J. W. Campbell8,9, J. Daniels8,10,
E. Elle4, J. D. Ellis8, S. J. Fleischer11, J. Gibbs5, R. L. Gillespie12,
K. B. Gundersen13, L. Gut13, G. Hoffman14, N. Joshi15, O. Lundin16, K. Mason13,
C. M. McGrady17, S. S. Peterson18, T. L. Pitts-Singer2, S. Rao7, N. Rothwell19,
L. Rowe13, K. L. Ward6,20, N. M. Williams6, J. K. Wilson13, R. Isaacs13
and R. Winfree1
Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ 08901, USA
USDA-Agricultural Research Service, Pollinating Insects Research Unit, Logan, UT 84322, USA
Department of Entomology, Pennsylvania State University Fruit Research and Extension Center, Biglerville,
PA 17307, USA
Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A1S6 Canada
Department of Entomology, University of Manitoba, Winnipeg, MB R3T 2N2 Canada
Department of Entomology and Nematology, University of California Davis, Davis, CA 95616, USA
Department of Entomology, University of Minnesota, St. Paul, MN 55113, USA
Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611, USA
USDA Agricultural Research Service, Northern Plains Agricultural Research Laboratory, Sidney, MT 59270, USA
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA
Agriculture and Natural Resource Program, Wenatchee Valley College, Wenatchee, WA 98801, USA
Department of Entomology, Michigan State University, East Lansing, MI 48824, USA
Department of Crop and Soil Science, Oregon State University, Corvallis, OR 97331, USA
Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, AR 72701, USA
Department of Ecology, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden
Department of Applied Ecology, North Carolina State University, Raleigh, NC 27695, USA
AgPollen, 14540 Claribel Road, Waterford, CA 95386, USA
Northwest Michigan Horticultural Research Center, Michigan State University, Traverse City, MI 49684, USA
National Park Service, Yosemite National Park, CA 95389, USA
JRR, 0000-0002-2355-3535; DRA, 0000-0003-2082-4974; SJF, 0000-0001-5314-6538;
JG, 0000-0002-4945-5423; JKW, 0000-0003-0807-5421; RW, 0000-0002-1271-2676
Most of the worlds crops depend on pollinators, so declines in both managed
and wild bees raise concerns about food security. However, the degree to
which insect pollination is actually limiting current crop production is
poorly understood, as is the role of wild species (as opposed to managed hon-
eybees) in pollinating crops, particularly in intensive production areas. We
established a nationwide study to assess the extent of pollinator limitation in
seven crops at 131 locations situated across major crop-producing areas of
the USA. We found that five out of seven crops showed evidence of pollinator
limitation. Wild bees and honeybees provided comparable amounts of pollina-
tion for most crops, even in agriculturally intensive regions. We estimated the
nationwide annual production value of wild pollinators to the seven crops we
studied at over $1.5 billion; the value of wild bee pollination of all pollinator-
dependent crops would be much greater. Our findings show that pollinator
declines could translate directly into decreased yields or production for
most of the crops studied, and that wild species contribute substantially to
pollination of most study crops in major crop-producing regions.
1. Introduction
Pollination by insects is a critical ecosystem service that is necessary for pro-
duction of most crops, including those providing essential micronutrients,
© 2020 The Author(s) Published by the Royal Society. All rights reserved.
and is thus essential for food security [1]. In the USA, the pro-
duction of pollinator-dependent crops is valued at over $50
billion per year [2,3]. Recent evidence that both European
honeybees (Apis mellifera) and some native wild bee species
are declining [46] raises concern about negative impacts on
crop yield (amount produced per area). However, a decline
in pollinators will only affect crop yield if yield is limited
by a lack of pollination. Research on pollinator limitation,
or the degree to which a lack of pollinators is restricting full
seed or fruit production, has focused mainly on wild plant
species [78], with little information available about the fre-
quency or circumstances in which pollination limits crop
production [913].
Theoretically, for any pollinator-dependent crop, we
expect a relationship between pollination and crop yield,
such that yield increases with pollination until the crop is
fully pollinated, at which point additional pollinators
contribute no further service (figure 1) [7]. When a crop is
pollination limited, we expect a positive relationship between
pollination and yield, such that crop fields receiving more
pollination also produce higher yields. Conversely, if pollina-
tion is not limiting, we expect no relationship between
pollination and yield. Across farms that differ in pollination,
we would expect farms with lower visitation to show lower
yield, but there might not be a relationship between visitation
and yield among farms with high visitation rates. Pollination
may not be limiting for two fundamentally different reasons.
First, yield is not pollination limited if the crop plants pollina-
tion threshold is met (i.e. the number of pollen grains
deposited is sufficient for maximum fruit production under
ideal growth conditions). Second, even if the plants pollina-
tion threshold is not met, pollination will not be a limiting
factor if some other factor is more limiting to yield (e.g. [14
16]). Common limiting factors for crop production include a
lack of water or nutrients (fertilizer) and injury from plant
pests and diseases [7,17]. When other factors are limiting,
crop yield will not increase with increasing pollination, even
if pollination is insufficient. Thus, we expect that commercial
farms, which typically have high inputs for irrigation, fertilizer
and pest management, would be particularly sensitive to
deficits in pollination. However, whether intensively managed
crops in major production areas are in fact limited by pollination
has rarely been tested (but see [12]).
In many agricultural situations, pollination is provided by
a combination of managed honeybees (or sometimes other
managed bees) and wild insects (primarily wild bees).
While honeybees have long been considered the most
economically valuable pollinators, recent global syntheses
have revealed that wild pollinators are often as abundant as
honeybees on crop flowers [1820], and that the diversity of
wild bee visitors is higher when crops are grown in their bio-
geographic region of origin [21]. Furthermore, flower visits
by wild bees are more strongly correlated with crop yields
than are visits by honeybees [18,22,23]. The reason for this
association is not known, but could include some wild bee
species depositing more pollen per visit than honeybees
[22,24], wild bees moving more often between compatible
plants, or wild bees increasing the pollination provided by
honeybees through interspecific interactions [25,26]. Wild
pollinators might be contributing significantly to crop polli-
nation at the national scale in the USA, but this has not
been evaluated in a comprehensive way.
An ideal nationwide assessment of crop pollination
should study multiple economically important bee-pollinated
crops, each in its main region(s) of production. An assess-
ment should also capture the effects of typical management
practices, including honeybee stocking rates. We expect
high stocking density in major production regions because
in intensively managed landscapes many wild bee species
have reduced abundance or fail to persist [24,2730]. Thus,
in the settings where most crop production occurs, the contri-
bution of wild bees might be considerably less than that of
The economic value of honeybees and wild bees can be
estimated based on their relative contributions to crop polli-
nation. The production value method, which has most often
been used to economically value pollination [2,31], begins
with the market value (price × quantity) of the crop and attri-
butes to pollinators the fraction of this value that would be
lost in the absence of pollination. This fraction can be less
than the entire market value for crops that still produce
some yield when pollinators are absent [32]. This total econ-
omic value can then be partitioned into components
attributable to honeybees and to wild bees. Estimates from
the production value method are best interpreted as short
term, on a time scale in which alternative strategies such
as switching to less pollinator-dependent varieties are not
available [33].
In this paper, we report the results of a national-scale
empirical study of seven pollinator-dependent crops and
131 commercially managed fields across the USA and part
of Canada. We answer the following questions. (i) How
prevalent is pollinator limitation? (ii) What are the relative
contributions of wild bees and the honeybees to crop
crop yield
ollinator visits
is limiting
is not limiting
pollination limiting
in some places
Figure 1. Conceptual figure showing the general relationship between pollinator visitation (or pollen deposition) and crop yield. As the number of visits from
pollinators increases, crop yield is expected to increase until the crop is fully pollinated, at which point the relationship reaches an asymptote. Data from a particular
farm or set of farms may indicate the full asymptotic relationship, as shown in (c), or they may fit a strictly positive relationship (a), or no relationship at all (b),
corresponding to lower or higher sections of the full visits versus yield relationship in (c). (Online version in colour.) Proc. R. Soc. B 287: 20200922
production or yields? (iii) How do these contributions
translate into economic value?
2. Methods
(a) Study design
We collected data on insect pollination and crop production for
highbush blueberry (Vaccinium corymbosum), apple (Malus
pumila), sweet cherry (Prunus avium), tart cherry (Prunus cerasus),
almond (Prunus dulcis), watermelon (Citrullus lanatus) and
pumpkin (Cucurbita pepo) at farms across the USA and part
of Canada (electronic supplementary material, figure S1). All of
these crops depend very strongly or absolutely on insect pollina-
tion [32]. For each crop, we selected study farms within
economically important areas for the national production of
that crop, so these farms were representative of the majority
of production in terms of growing conditions, pollinator
communities and farm management practices. In addition, the
individual farm fields selected were reasonably large and well-
maintained as per standard agricultural practice, and were
growing a regionally common cultivar. All fields were stocked
with honeybee hives at rates typical for the region. For pumpkin
and apple in Pennsylvania, not all farmers routinely stock honey-
bees because native bees are thought to provide sufficient
pollination (e.g. [34]). However, even when honeybees were not
stocked at our study sites, they were still found on crop flowers.
(b) Data collection: pollinator visitation rates and crop
production metrics
Within each crop field, insect pollinators were observed during
bloom along four 100 m transects, positioned approximately 0,
25, 50 and 100 m into the field from one edge. Along each trans-
ect, observers stopped every few metres and observed a small
patch of flowers to which all visiting bees could reliably be
counted. Each visiting bee was identified to an on-the-wing
species group, such as Bombus,Xylocopaor green bee(elec-
tronic supplementary material, table S2). Bee species were
grouped based on body size and hairiness, which are the two
main predictors of pollen deposition per visit [35,36]. Honeybees
were always identified uniquely to species. In each year (two or
three years depending on crop), bees were counted on up to
three different days during peak crop bloom, and up to three
times per day, during weather conditions when bees were
active. Methods for observing bee visits were standardized to
the extent possible, but also tailored to each crop based on, for
example, the density and distribution of flowers. Crop-specific vis-
itation assessment protocols are listed in electronic supplementary
material, table S3.
Crop production data were collected for each crop field
within the same four transects where bee observations were per-
formed. In each transect, production was assessed for a standard
number of trees (orchard crops), bushes (berry crops) or quadrats
(field crops). For each crop, we measured a crop production
variable that was potentially related to pollination and also
relevant to economic value. We used fruit weight when
available or otherwise fruit set or number of fruit. Thus for
some crops (watermelon and pumpkin), our crop production
measurements are explicitly per area and thus correspond
directly to yield. For the other crops, our measurements are not
explicitly per area and are thus better referred to more generally
as production. Regardless, our measures of production match
commonly used proxies for yield in the insect pollination litera-
ture [18,37]. Flower counts were performed during peak bloom,
then paired later with post-bloom fruit counts from the same
sample locations to determine fruit set. Fruit weights and fruit
counts were measured just prior to harvest. Crop-specific
protocol details are listed in electronic supplementary material,
table S4.
(c) Analysis 1: frequency of pollinator limitation
To measure the frequency of pollinator limitation across all
locations for a given crop, we created three potential statistical
models relating the number of bee visits observed to crop pro-
duction and used AIC to choose between them (figure 1;
electronic supplementary material, Methods). The three models
were: (i) a linear positive relationship, implying that all locations
were pollinator limited; (ii) no relationship (an intercept only
model), implying that no locations were limited; or (iii) an
asymptotic (piecewise) regression model in which production
increases with visitation to a certain visit rate breakpoint, then
remains flat, implying that the crop is pollinator limited in
some locations and not others. If the third model was selected,
we estimated the frequency of pollinator limitation as the
proportion of locations falling below the breakpoint.
(d) Analysis 2: contribution of honeybees versus
wild bees
For each crop, the fraction of total pollen grains deposited by
honeybees and each species group of wild bee was estimated
by multiplying flower visits by that bee group (data collection
described above) with an estimate of pollen grains deposited
per visit ( pollinator efficiency) for that group, and then calculat-
ing the proportion of the total pollination provided by each bee
group (details in electronic supplementary material, Methods).
Values of pollinator efficiency were taken from the literature
and are listed in electronic supplementary material, table S2,
along with associated sample sizes.
(e) Analysis 3: economic valuation
The economic value delivered to each crop in each state by
honeybees and wild bees was calculated using the equation
Vpollinator ¼Vcrop DPpollinator,ð2:1Þ
where V
is the annual economic value attributable to a
particular pollinator group (either wild bees or honeybee),
is the annual production value of the crop, Dis the pollina-
tor dependency value for the crop (the proportion by which yield
is reduced in the absence of pollination [32]) and P
the proportion of total pollination of the crop provided by the
pollinator group, as estimated above.
Our approach updates previous national-scale estimates of
the value of wild and honeybee pollination in several ways.
First, previous national valuations (e.g. [2,38]) did not have
access to empirical data for the percentage of pollinator visits
provided by each pollinator group (P
), but rather
assumed a P
value of 0.9 for crops in which honeybees
were routinely supplied, unless expert opinion suggested the
use of a different value [39]. In our study, we actually measured
honeybee and wild bee visitation to each crop. Second, most
previous studies come from one area in the USA, which often
is not within the main production area for the crop. Our field
sites were in states that are among the top national producers
of each crop (electronic supplementary material, table S5),
which is essential when such estimates are used to extrapolate
to national value. Third, we based our economic valuations on
estimated pollen deposition by each type of pollinator (by
weighting flower visitation rates by the number of pollen
grains deposited per flower visit), not merely on flower visitation
rates, as has been done by most previous national-scale
valuations. Details of our valuation methods, including Proc. R. Soc. B 287: 20200922
extrapolations to the national level, are discussed in the electronic
supplementary material, Methods.
3. Results
(a) Frequency of pollinator limitation
For each cropstate combination in our study, we used AIC
model selection to estimate the frequency of pollinator limit-
ation (figure 2; electronic supplementary material, tables S6
and S7). For tart cherry in Michigan, sweet cherry in
Washington, and for blueberry in Michigan, Oregon and
British Columbia, we found evidence of pollinator limitation
for most sampled areas (6494% of transects). For waterme-
lon, pumpkin and almond, we found little to no evidence
of pollinator limitation. For apple in both Michigan and
Pennsylvania, the best model was a linear relationship
between visitation and crop production across all transects
with no evidence of an asymptote, suggesting pollinator
limitation across all sampled areas. Apples are typically
thinned to achieve fruit that meet fresh-market standards;
thus, our apple fruit counts were taken post-thinning to be
more directly related to harvestable yield. This is a conserva-
tive approach, because post-thinning measurements are less
likely than those taken pre-thinning to detect the effect of
pollinator limitation. Plots of best-fit lines for each of the
three models and estimated breakpoints between limiting
and asymptotic pollination are shown in electronic supple-
mentary material, figure S2. For blueberry, we performed a
second analysis of pollen limitation using additional field
data from hand-pollination experiments (electronic sup-
plementary material, supplementary analysis 3). Results
from this analysis were qualitatively similar to the results
from the main analysis, in that they showed pollen limitation
in farms with lower visitation, but not in farms with higher
visitation (i.e. the segmented relationship was selected) for
northern blueberry and showed no evidence of pollen limit-
ation in Florida blueberry.
(b) Contribution of honeybees versus wild bees
On average across the 13 cropstate combinations measured
in our study, 74% of observed visits were performed by
honeybees and the other 26% by wild bees. However, this
proportion differed greatly by crop (electronic supplementary
material, figure S3). Wild bee visits accounted for the largest
proportion in pumpkin (74.6%) and the lowest in almond
(0%). The proportion of wild bee visits was higher for
cherry and apple (average of 43.5% in sweet cherry, 34.7%
in tart cherry, and 32.9% in apple) than for blueberry (average
of 8.9%). The proportion of visits from each type of bee was
remarkably consistent across states within each crop, with
the exception of watermelon, for which wild bees were four
times as abundant in Florida as compared with California.
Incorporating the data on pollen deposition per visit into
the calculations increased the relative contribution of wild
bees for most crops (figure 3). Although visitation rates of
honeybees were higher than those of wild bees in apple
and tart cherry, the amount of pollen deposited by wild
bees was equal or even somewhat greater because wild bee
groups deposited an estimated 1.5 to 2 times more pollen
per visit in these crops (electronic supplementary material,
table S2). Wild bees contributed slightly more in Florida
watermelon, and continued to be dominant in pumpkin.
Incorporating pollen deposition per visit into calculations
for blueberry, almond and California watermelon made
little difference due to the low abundance of wild bees. The
exception was sweet cherry, in which wild bees provided
43% of visits, but only 28% of pollen deposition. This was
because the most abundant wild pollinators in this system
were bumblebees, which have been shown to be ineffective
pollinators of cherry flowers [40].
(c) Economic valuation
For the crops in our study, a high value of wild bees was esti-
mated when the relative importance of wild bees was greater
than that of honeybees (e.g. in pumpkin in Pennsylvania), or
when the value of the crop was high overall (e.g. in Washing-
ton cherry and Michigan apple). However, for almond, which
had the largest total national value, the subset of value
attributable to wild bees was negligible because they were
very rare or absent in the observations of pollinators in
those farms. At the national level, we estimated the value
of wild pollinators to be highest in apple, with a value of
$1.06 billion, with significant value also in sweet cherry
pollination limitation (%)
Figure 2. Frequency of study transects predicted to be pollination limited using the AIC selection method. The best of three models were selected by AIC: (i)
limitation across all sampling locations; (ii) limitation at no sampling locations; and (iii) limitation at lower levels of visitation, but not at higher levels of visitation.
If model 3 was selected, limitation frequency is the percentage of transects occurring below the model-estimated breakpoint between the positive relationship
between visits and crop production or yield, and no relationship. (Online version in colour.) Proc. R. Soc. B 287: 20200922
($145 million), watermelon ($146 million), pumpkin ($101
million), blueberry ($50 million) and tart cherry ($32 million)
(figure 4), totalling approximately $1.5 billion across these
crops alone. By contrast, wild bees provided very limited
value to almond (actually $0 based on our study farms).
The economic value of honeybees to crop yield across these
crops, when estimated in the same manner, totalled about
$6.4 billion, with this value dominated by their $4.2 billion
value to almond. An alternative analysis that accounts for
the potential for farmers to reduce financial losses by limiting
other input costs when pollination fails and the crop will not
be harvested is presented as electronic supplementary
material, analysis 1. Using this method, estimated values
are considerably lower for both wild bees and honeybees
because variable production costs are subtracted from the
yield value attributable to bees.
4. Discussion
Global reliance on pollinator-dependent crops has increased
over the past several decades [1,41], while wild and managed
pollinators have declined in many places (e.g. [5,42,43]),
blueberry almond
tart cherry
apple sweet cherry
fraction of total pollen grains
deposited by wild bees
Figure 3. Boxplots of relative pollen deposition rate of wild bees (as a proportion of total pollen deposition) across the cropregion combinations in our study.
Estimates of pollen deposition were based on visits × pollen deposition per visit for each type of pollinator observed (electronic supplementary material, table S2),
with the remainder of pollen deposition provided by honeybees. Black line is the median, boxes show the first and third quartiles, and whiskers extend to 1.5 times
the interquartile range or to the most extreme data point. The number of farms and years differed by crop (electronic supplementary material, table S7). (Online
version in colour.)
almond apple
US value (millions of USD)
blueberry pumpkin
this study
honey bee wild bees
valuation source
Figure 4. Value estimates for honeybee (orange) and wild bees (green), extrapolated to the level of the United States. Bars encompass the range of estimates in the
published literature [2,39]. Square points show our final value estimates. Our estimates differ from literature estimates for several reasons: (i) we used new data on
flower visitation rates collected in important production areas for each crop, (ii) we used updated pollinator dependency values from [32], (iii) we transformed our
visitation rates into pollen deposition rates by incorporating pollen deposition per visit estimates from the literature and (iv) we sampled in large-scale commercial
farms. All values have been adjusted to 2015 dollars. (Online version in colour.) Proc. R. Soc. B 287: 20200922
prompting concern that pollinator limitation could pose a
risk to yield stability and food security [44,45]. In a multi-
region study focusing on major production regions for fruits,
vegetables and nuts in North America, we found evidence
of pollinator limitation in five of the seven pollinator-
dependent crops we examined. This is consistent with a grow-
ing body of literature that suggests pollination may be limiting
across a wide range of crops worldwide [1113,18,44,46]. An
earlier meta-analysis found little or no evidence of limitation
in most global crop systems [47], but these conclusions were
based on an indirect analysis of temporal trends in yield,
rather than measuring the relationship between bee abun-
dance and yield directly. Our new evidence of pollinator
limitation is particularly valuable in comparison to previous
analyses, because we specifically targeted larger commercial
farms that represent the context for the majority of production.
We found the overall contribution of wild bees to be simi-
lar to (or higher than) that of honeybees in most of the crops
we studied (figure 3). This result is in contrast to our expec-
tation that sampling in agriculturally intensive areas would
reveal greatly reduced wild bee contributions to crop pollina-
tion. Our data suggest that instead, wild bees are able to
persist in many of these managed landscapes and make a sig-
nificant, although variable, contribution to crop pollination.
Furthermore, in all six crops we studied, the wild bee species,
on average, deposited more pollen per visit than did the
honeybee, by a factor of 1.4 to 3.2. (electronic supplementary
material, table S2 and figure S4). We found a predominance
of pollination by honeybees in certain crops (blueberry,
California watermelon and almond), and this may be due
to landscape factors, farm management intensity and/or
pesticide use patterns that limit the ability of wild bees to
persist and contribute to crop yield in these crops, in addition
to differences in honeybee stocking rates. For instance, in
California almond, visitation rates by wild bees are much
lower (or more often non-existent) in the large-scale orchards
we surveyed than in smaller farms surrounded by natural
habitat [48] where much of the previous research on wild
bees and almond pollination has been conducted. This pattern
has also been seen in watermelon [24] and blueberry [10].
Our study reconciles previous conflicting evidence for the
relative importance of honeybees, a managed agricultural
input that growers must pay for each year, and wild bees,
which provide a free ecosystem service, in pollination of
crops grown across the United States. Previous national-
level studies of the USA have estimated honeybees to be
much more important than wild bees [2,38,39], but did not
actually measure wild bee abundance in crop fields. By con-
trast, more recent syntheses of global literature have
concluded wild bees may be at least as important as honey-
bees, if not more so [18,19,28]. We found that wild bee
abundance on crop flowers in major US and Canadian pro-
duction regions is higher than previously thought, and that
this, combined with the greater pollination efficiency of
many native bees, makes their importance in agricultural pol-
lination more in line with previous estimates from other parts
of the world than with previous estimates from the USA.
It is important to note that even when the proportion of
visits by wild bees was fairly similar between two crops,
including crops that are in the same genus and flower at
the same time of year, the actual species of wild bee pollinat-
ing each crop differed (e.g. [49]). For instance, the vast
majority of wild bee visits in sweet cherry in Washington
were performed by bumblebees, while most wild insect visits
in tart cherry in the eastern USA were performed by distantly
related bee species (in this case various species in the genus
Andrena).Similar differences are also known for squash/pump-
kin in the Northeast and mid-Atlantic, where bumblebees and
squash bees comprise most of thewild bee visits [50,51], versus
California, where bumblebee visits are relatively rare [52]. This
variability in bee fauna highlights the need to sample broadly
across production regions [49,53] to better understand the
role of specific types of wild bees for crop yields.
The natural history of specific crops and pollinators may
explain some of the variation in pollinator limitation that we
found among crops. The most obvious difference appeared
to be between the early spring-blooming tree and perennial
bush crops (apple, cherry and blueberry) that generally had
much higher levels of pollinator limitation than the later
summer-blooming annual crops (watermelon and pumpkin).
Early bloom phenology is expected to negatively affect the
abundance of both honeybees and wild bees. In the early
spring, cool or rainy weather often suppresses bee visitation
[5456], and if too few bees are active when flowers are bloom-
ing, pollinator limitation can result. Honeybees, even if
maintained at high densities, do not typically fly in inclement
weather, making spring-blooming crops more dependent on
wild pollinators than those flowering in summer. These
include species that are adapted to spring weather, but often
do not achieve high abundance both due to lack of suitable
habitat or, in the case of Bombus spp., because bees present
at that time are foraging queens who have yet to produce a
worker-filled colony. Later in the season, temperatures are
more suitable for bee flight in general, resulting in a greater
chance of good foraging weather during bloom of summer
crops such as watermelon and pumpkin.
Another possible explanation for the pattern we observed
is that apples, cherries and blueberries have intrinsically
much higher flower densities than watermelon and pumpkin.
This is at least somewhat mitigated by higher recommended
honeybee stocking densities [57,58], but nevertheless the bee
to flower ratio is likely lower in these crops. An exception to
this pattern is almond, which is the earliest blooming crop in
its region (February) and yet showed little evidence of limit-
ation at the sites we sampled. One might expect pollination
limitation in almond, because wild bees of most local species
have not yet emerged from winter diapause. However, an
entire beekeeping industry has focused on providing large
numbers of honeybees for this crop, and extensive research
and management effort is allocated to insure reliable pollina-
tion. In fact, during almond bloom, two thirds of all
honeybee colonies in the United States are employed for
California almond pollination [59].
Given the evidence of widespread pollinator limitation,
especially in tree fruits and blueberry, our results suggest
that the adoption of practices that conserve or augment
wild bees, such as wildflower enhancements [60,61] and the
use of alternative managed pollinators [62,63], is likely to
be successful for increasing yields. Furthermore, the high
value (over $1.5 billion for the crops in this study alone) we
estimate for the contribution of wild bees to crops under-
scores the importance of their conservation, as well as the
economic benefits that investment in conservation and aug-
mentation strategies could bring. Increasing investment in
honeybee colonies is an alternative approach to reducing pol-
linator limitation. Traditionally recommended stocking rates Proc. R. Soc. B 287: 20200922
could be too low for several reasons, including the use of
modern cultivars and horticultural practices that result in
greater flower density per unit area, and more intensive agricul-
tural practices, whereby fertilizer, pests and water are often less
limiting than in the past. Most recommendations for honeybee
stocking densities in fruit and vegetable crops were developed
decades ago [57,64] when production levels were lower, honey-
bee colonies were stronger, and feral honeybees and wild bees
were more numerous. Research on optimal honeybee colony
stocking density has generally not been updated to keep pace
with horticultural advances (but see [65]), even though these
changes can have significant implications for yield [66]. In
cases where pollination is limiting, there may be little benefit
to spending large amounts of money on pest control (US
farms currently spend about $9 billion annually on pesticides
[67]), fertilizer (about $23 billion [68]), water, or other farming
practices without also finding ways to reduce pollinator limit-
ation. Additionally, addressing pollinator limitation should
increase yields and food security.
Data accessibility. Datasets used in this study are available online from
the Dryad Digital Repository:
hdr7sqvfj [69].
Authorscontributions. R.I., R.W. and J.G. conceived and designed the
study. D.R.A., D.B., K.B., N.K.B., C.B., J.B., J.W.C., J.D., E.E., J.D.E.,
S.J.F., J.G., R.L.G., K.B.G., L.G., G.H., N.J., O.L., K.M., C.M.M., S.S.P.,
T.L.P.-S., S.R., N.R., L.R., K.L.W., N.M.W. and J.K.W. carried out the
observations and experiments. J.R.R. designed and performed the ana-
lyses. J.R.R., R.W. and R.I. wrote the manuscript. All authors assisted
with interpretation of the data and revision of the manuscript.
Competing interests. We declare we have no competing interests.
Funding. The authors acknowledge funding provided by the United
States Department of Agriculture, National Institute for Food and
Agriculture through the Specialty Crop Research Initiative Projects
2012-01534 (Developing Sustainable Pollination Strategies for US
Specialty Crops) and PEN04398 (Determining the Role of and Limit-
ing Factors Facing Native Pollinators in Assuring Quality Apple
Production in Pennsylvania; a Model for the Mid-Atlantic Tree
Fruit Industry), the State Horticultural Association of Pennsylvania,
the Michigan Apple Committee, and the Michigan Cherry Commit-
tee, Operation Pollinator, the Almond Board of California (grant
no.13.Poll13A), and the 2017-2018 Belmont Forum and BiodivERsA
joint call for research proposals, under the BiodivScen ERA-Net
COFUND programme, and with the funding organisations AEI,
Acknowledgements. We thank the numerous research technicians and
students for their work to collect the bee and crop data for this pro-
ject, including Christine Bell, Andrew Buderi, Mike Epperly, Jillian
Gall, Alisa Kim, Betty Kwan, Justin Scioli, Kevin Tahara, Rachael
Troyer, Kristal Watrous and Stephanie Wilson. Special thanks to the
many grower collaborators and their families and staff who hosted
our research at their farms and facilitated the logistics of this project,
and to the projects advisory board for the input and feedback.
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... This study is one of the first to assess trends in wild bee abundance in an agricultural system, where bees are providing an economically important ecosystem service (see also Graham et al., 2021). Bee declines in agricultural systems could impact crop yields: Wild bees enhance the production of many crops globally (Bommarco et al., 2012;Garibaldi et al., 2013;Reilly et al., 2020), and yield for several important North American crops, although not for watermelon, are pollen limited (Bommarco et al., 2012;Garibaldi et al., 2013;Reilly et al., 2020). Pollinator visitation frequency and total pollen deposition are highly correlated in many plant-pollinator networks Kleijn et al., 2015;Vázquez et al., 2005). ...
... This study is one of the first to assess trends in wild bee abundance in an agricultural system, where bees are providing an economically important ecosystem service (see also Graham et al., 2021). Bee declines in agricultural systems could impact crop yields: Wild bees enhance the production of many crops globally (Bommarco et al., 2012;Garibaldi et al., 2013;Reilly et al., 2020), and yield for several important North American crops, although not for watermelon, are pollen limited (Bommarco et al., 2012;Garibaldi et al., 2013;Reilly et al., 2020). Pollinator visitation frequency and total pollen deposition are highly correlated in many plant-pollinator networks Kleijn et al., 2015;Vázquez et al., 2005). ...
Full-text available
1. Despite widespread recognition of the need for long-term monitoring of pollinator abundances and pollination service provision, such studies are exceedingly rare. 2. In this study, we assess changes in bee visitation and net capture rates for 73 species visiting watermelon crop flowers at 19 farms in the mid-Atlantic region of the United States from 2005 to 2012. 3. Over the 8 years, we found a 58% decline in wild bee visitation to crop flowers, but no significant change in honey bee visitation rate. Most types of wild bees showed similar declines in both the visitation and the net capture data; bumble bees, however , declined by 56% in the visitation data but showed no change in net capture rates. Trends in pollination services, that is, estimated pollen deposition, largely followed the trends in visitation and net capture rates. 4. While we detected large and significant declines in wild bees when using generalised linear mixed models (GLMMs), permutation analyses that account for non-directional variation in abundance were non-significant, demonstrating the challenge of identifying and describing trends in highly variable populations. 5. As far as we are aware, this article represents one of fewer than 10 published time-series (defined as >5 years of data) studies of changes in bee abundance, and one of only two such studies conducted in an agricultural setting. More such studies are needed in order to understand the magnitude of bee decline and its ramifications for crop pollination.
... Insufficient insect pollinators in the community may lead to pollination limitation, whereby seed production is less than would be reached with supplemental pollen treatments. Diverse communities of wild pollinators are necessary to ensure sufficient pollination (Garibaldi et al. 2013;Reilly et al. 2020), including in apples (Osterman et al. 2021;Radzevičiūtė et al. 2021). Insect pollinators are in decline in some parts of the world (Biesmeijer et al. 2006;Nieto et al. 2014;Potts et al. 2016;Hallmann et al. 2017) but for many areas, insufficient baseline information of diversity and abundance is available (Didham et al. 2020). ...
Full-text available
Apples are one of the most important global crops that relies heavily on insect pollination, which has been shown to increase apple production and value. However, recent reports indicate that apple production has been declining in certain regions, including in Bhutan. One of the potential causes of declining production are pollination deficits driven by a low abundance and diversity of pollinators, a phenomenon that has received little attention in Bhutan to date. Here, we present the first study examining the diversity of flying insects in Bhutanese apple orchards in relation to apple quality. During the apple flowering season, 1,006 insects comprising 44 unique (morpho-)species from the orders Hymenoptera, Diptera, and Lepidoptera were recorded using a standardized method of passive and active trapping within nine different orchards in Thimphu, Paro, and Haa districts, in the western part of Bhutan. During the harvest season, 495 apples were collected from these nine orchards, and we measured five different parameters; weight, size, sugar concentration, seed number, and malformation score. The most dominant flower visitors across all orchards were honey bees (mostly Apis mellifera, followed by A. cerana and A. dorsata). Orchards with a higher abundance of flying insects (both managed and wild) had better apple quality (weight, size and sugar concentration). Contrary to reports from other regions of the world, flower visitor diversity did not correlate with the quality of the apples. This represents the first study reporting on apple pollination in Bhutan and highlights the importance of pollinators in apple production and reinforces the need to develop pollinator friendly practices to ensure sustainable apple production in Bhutan.
... Therefore, more cultivars need to be tested in regard to their pollinator friendliness and they should be combined with further activities to protect pollinators and increase their biodiversity. (Kremen et al. 2002;Klein et al. 2003;Kremen & Chaplin-Kramer 2007;Garibaldi et al. 2011 (Kearns & Inouye 1997;Klein et al. 2007;Ollerton et al. 2011;Reilly et al. 2020). Eine deutliche Mehrheit der weltweit natürlich vorkommenden Blühpflanzen wird dabei von Insekten bestäubt und der prozentuale Anteil an insektenbestäubten Pflanzen reicht schätzungsweise von 78% in den temperaten Zonen bis zu 94% in den Tropen. ...
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Aktuell ist weltweit eine zunehmende Ausdehnung der städtischen Gebiete zu beobachten, was ein Verlust von natürlichen Lebensräumen bedeutet. Soll die derzeitige Biodiversität jedoch erhalten bleiben, müssen vermehrt Anstrengungen unternommen werden, um heimischer Flora und Fauna auch im urbanen Gebiet Ersatzlebensräume bieten zu können. Hinsichtlich der Artenvielfalt und der Bewertung des Lebensraums „Stadt“ kommen wissenschaftliche Studien zu stark unterschiedlichen Ergebnissen, wenngleich sie jedoch alle betonen, dass urbane Grünflächen einen wertvollen Beitrag zur Förderung eines städtischen Artenreichtums leisten können. Während vielfach darauf hingewiesen wird, dass ausreichende und geeignete Nahrungsressourcen für die Bestäuberinsekten bereitgestellt werden müssen, wurde in den seltensten Fällen untersucht, ob Zierpflanzen von den urbanen Bestäubern überhaupt als Nahrungsquelle genutzt werden. Dies war für lange Zeit umstritten, wird aber inzwischen zunehmend durch Publikationen belegt, wobei die ökologische Bedeutung der Zierpflanzen nach wie vor kontrovers diskutiert wird. So gibt es offenbar große Attraktivitätsunterschiede innerhalb der Zierpflanzen und darüber hinaus können wohl nicht alle Bestäubergruppen gleichermaßen von den zumeist exotischen Zierpflanzen als Nahrungsressource profitieren. Da zum jetzigen Zeitpunkt nicht zu jeder Zierpflanze wissenschaftlich erhobene Daten vorliegen, war es zunächst ein Ziel dieser Arbeit, belastbare Daten hinsichtlich der Bestäuberfreundlichkeit bestimmter Zierpflanzen, insbesondere solche mit einem hohen Markanteil, zu gewinnen. Für solche Versuche sollten darüber hinaus entsprechende Erfassungsmethoden beurteilt und weiterentwickelt werden. Ein weiterer und bisher kaum untersuchter Schwerpunkt der Arbeit war die Frage, welche Faktoren sich in welcher Form auf die Zusammensetzung und Abundanz der urbanen Bestäuber auswirken. Um diese Fragestellungen bearbeiten zu können, wurden in den Jahren 2017 – 2019 in Freiland- und Semifreilandversuchen Zählungen, Beobachtungen sowie Kescherfänge zur Bestäuberattraktivität bestimmter Zierpflanzen durchgeführt. Im ersten Versuchsansatz wurde an 13 verschiedenen Standorten im Stadtgebiet Stuttgart jeweils ein Hochbeet aufgestellt, welches mit einer identischen Auswahl an Zierpflanzen bepflanzt wurde. In den Jahren 2017 und 2018 wurden alle Standorte während der Sommermonate wöchentlich besucht und die Hochbeete 20 Minuten lang beobachtet. In dieser Zeit wurde die Anzahl der Bestäuberinsekten sowie deren Zugehörigkeit zu bestimmten Insektengruppen erfasst. Es konnten im Rahmen dieser Erfassungen insgesamt 10.565 pollen- und/oder nektarsammelnde Blütenbesucher gezählt werden. Dies bestätigt zunächst einmal, dass unsere Auswahl an Zierpflanzen von Bestäuberinsekten als Nahrungsquelle genutzt wurde. Die Attraktivität der getesteten Zierpflanzen unterschied sich jedoch in erheblichem Maße innerhalb der Pflanzenarten und reichte von durchschnittlich 1,2 Blütenbesuche pro 20 Minuten bei Bracteantha bracteata (Garten-Strohblume) bis zu 5,3 Besuche bei Bidens (Goldmarie). Die Attraktivität variierte jedoch auch – und dies teilweise in stärkerem Maße – zwischen den Sorten einer Art. Statistische Modelle zeigten darüber hinaus signifikante Einflüsse von Untersuchungsjahr und Standort. Dies unterstreicht die Notwendigkeit einer kontinuierlichen Testung aller Zierpflanzen hinsichtlich der Bestäuberfreundlichkeit, wofür die hier beschriebenen Methoden sich als gut geeignet erwiesen haben. Bemerkenswert ist, dass sich nicht nur die Abundanz, sondern auch die Zusammensetzung der Bestäuber signifikant zwischen getesteten Zierpflanzen unterschied (Publikation I). Bei ihrer Nahrungssuche und zur Entscheidungsfindung, ob sich eine Ressource als Nahrungsquelle eignet, ziehen Bestäuberinsekten die charakteristischen und oftmals gattungs-, art- oder gar sortenspezifischen Merkmale der Blüten heran. Während diese bei vielen heimischen Blühpflanzen gut untersucht sind, ist sehr wenig über die Rolle der Blütenmerkmale wie Farbe, morphologische Ausprägungen oder Blütenduft bei den Zierpflanzen bekannt. Da die einzigen diesbezüglichen Untersuchungen bei Astern keine klaren Ergebnisse erbrachten, wurden in dieser Arbeit erstmals anhand der Beispielkultur Calibrachoa und dem Modellbestäuber Bombus terrestris untersucht, welche Blütenmerkmale mit der Attraktivität für Bestäuber korreliert sind. Wie im oben angeführten Stadtversuch zeigte sich, dass die Attraktivität zwischen den getesteten Calibrachoa Sorten stark variierte. Während der Blütenduft die beobachteten Attraktivitätsunterschiede nur in geringem Maße erklären konnte, hatte die Blütenfarbe einen signifikanten Einfluss auf die Attraktivität bei B. terrestris. Für die Frage, ob und welche spezifische Blütenmerkmale bei Calibrachoa und anderen Zierpflanzen die Attraktivität für Bestäuberinsekten beeinflussen, sind aber weitere Untersuchungen notwendig (Publikation II).
... Due to their fast generation times, large reproductive potential, ease of sampling, and known responses to management, insects are one group of organisms that can provide valuable insight into the sustainability of a farming practice to support biodiversity and their important ecosystem services (Boinot et al., 2019;Martin-Chave et al., 2019;Lami et al., 2020). Insects are also a diverse and globally relevant taxon for agriculture and conservation (Landis et al., 2000;Winfree et al., 2011;Reilly et al., 2020;Welti et al., 2020;Wilson and Fox, 2021) with important pollinators (e.g., honey bees, Syrphid flies), beneficial predators (e.g., ladybird beetles, green lacewings), and voracious pests (e.g., fall armyworm, corn earworm) that can serve as bioindicators of ecosystem health. Furthermore, ecological hypotheses about resource heterogeneity suggest linkages exist between plant diversity and insect diversity (Root, 1973;Russell, 1989;Stamps and Linit, 1997;Haddad et al., 2001). ...
The role plant diversity has played in regulating insect communities has been of interest for decades. Recent syntheses from agroecosystems suggest increasing plant diversity can positively affect beneficial insects like predators, reducing pest pressure and increasing yield. However, the agricultural landscape of the Midwestern United States is dominated by just two crops—corn and soybean—which cover approximately 180 million acres of arable land yearly. New ideas to conserve wildlife that additionally provide economic opportunities for farmers must be developed in order to promote sustainable and resilient ecosystems. Here we tested the capacity of an alternative cropping system to support more diverse insect populations than conventional cropping systems. We quantified differences in the diversity of an insect taxon, ants (Hymenoptera: Formicidae), over an annual cycle using pitfall traps in thirty-two 2-m2 plots of either woody perennial polycultures that contained apples, chestnuts, currants, hazelnuts, and raspberries or conventional corn-soybean rotations. In doing so, we found that woody perennial polycultures supported 2.4-fold more ant species and maintained a unique fauna of specialist and predatory ants. The observed differences in diversity were linked to higher levels of predation as 18.2-fold more sentinel prey were consumed during each month of the growing season. Combined, our results suggest that agricultural landscapes in the Midwestern United States can be modified to support important beneficial insects like ants while still producing commodities that can be economically beneficial to farmers.
... This decline is estimated to have a major economic impact on the agricultural sector, with catastrophic losses globally (Bauer and Wing, 2016). In countries such as the US, the decline in pollinators can directly translate into reduced yields or production for most agricultural crops (Reilly et al., 2020). For Brazil, it was demonstrated that climate change can affect crop pollinator bees, with detrimental economic impacts for most municipalities (Giannini et al., 2017). ...
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With the growing demand for food production worldwide, natural landscapes are increasingly being replaced by agricultural areas, which directly affects biodiversity and local ecosystem services. Agroforestry systems, which are the intentional integration of trees and shrubs into crop and animal farming systems, are a more sustainable production approach that has been increasing in several forested areas around the globe. Here, we examine the trends of agroforestry in the Brazilian Legal Amazon and estimate the associated value of ecosystem services mediated by pollinators. Using data from 2006 and 2017, we detected an increase in agroforestry activity in the Amazon, both in the number (3.27%) and in the area (23.18%) of establishments. Crop production in forested areas increased by 45.61% in the same period, and the main products cultivated in both years were native products from the Amazon, such as açaí , Brazil nut and babassu. Although the crop data are from forested areas, all the five crops with the highest production value are associated with agroforestry in the Amazon. Pollination services also increased during the same period from US$73.3 to US$156.7 million (113.76%). In 2006, the value of pollination services corresponded to 44% of the total crop production, and it jumped to 64.43% in 2017. Bees and beetles were the two main groups of pollinators quoted for the analysed crops. Our estimates show the important contribution of pollinators to crop production in the Amazon forest. However, a growing loss of Amazon forest has been observed, and this can jeopardize pollinators and have detrimental consequences on food production in the near future. Public policies are urgently needed to encourage crop production in harmony with natural areas, combining the protection of forests and pollinators with food production.
... A large proportion of global crop production relies on insect pollinators (Gallai et al. 2009;Reilly et al. 2020). Human welfare depends on the crucial ecosystem services provided by the pollinator community as they directly influence agricultural yield (Klein et al. 2007;Aizen et al. 2009;Cohen et al. 2020). ...
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Pesticide usage associated with intensive agriculture is implicated as a major factor for pollinator decline. Apart from developmental and physiological impairments, pesticide exposure has been shown to cause major cognitive anomalies in honey bees. However, there are gaps in our understanding about the physiological and molecular mechanism that causes the impairments. The present study evaluates the tissue damages at the molecular level with focus on apoptosis in the wild population of honey bees exposed to pesticide cocktails corroborated by observations in laboratory experiments. The study, for the first time, reports increase in both mitochondria and endoplasmic reticulum-mediated apoptosis in the honeybee body tissues underpinned by significant oxidative stress leading to programmed cell death. There was heightened reactive oxygen species level and caspase3 activity in the tissue homogenates from bees exposed to pesticides. Western blot experiments showed a significant increase in the expressions of the apoptotic markers like p53, cytochrome C, and GADD153/CHOP (DNA damage 153 or C/EBP homologous protein) in the pesticide-exposed bee populations in both field and laboratory conditions. Expressions of these apoptotic markers and oxidative stress were more pronounced in the heads as compared to the abdomens of the pesticide-exposed bees. These findings clearly indicate greater tissue damage in the honeybee head tissue. The cognitive implication of this finding has been discussed.
Urban green areas can play a crucial role in establishing spaces that are valuable for pollinators. However, to help ‘pollinator-friendly’ management of urban areas, complete information on the quantity and quality of available floral reward is needed. In this paper, the nectar and pollen of six Cotoneaster species (Rosaceae) were investigated in a two-year experiment established in Lublin city, SE Poland. In temperate climate, Cotoneaster species can ensure nectar and pollen in the full spring period (May/early June) or in early summer (June). A single species can support pollinators on average for 22.9 days. Flowers of Cotoneaster species produce high quantities of nectar (2.27-9.48 mg per flower) and low amounts of pollen (0.11-0.33 mg per flower). On average, the total sugar yield in Cotoneaster species was 11.5 g/m² (2.3-22.2 g/m²), whereas the total pollen yield was 1.3 g/m² (0.8-2.8 g/m²). Due to the high potential for total sugar yield, C. macrophyllus, C. lucidus, and C. horizontalis should be recommended to optimize the management of food resources in urban areas. Honeybee was the main insect visitor (70.1% of the total number of visitors); therefore, Cotoneaster species can be considered valuable for urban beekeepers. However, conservation schemes for bumblebees (21.3% of the total number of visitors) might also benefit from arrangements with these shrubs. Nevertheless, considering Cotoneaster species in conservation protocols, good-yielding pollen plants should be introduced to compensate for insufficient nutrient intake from pollen in spring.
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Bumblebee pollination is crucial to the production of tomato in protected cultivation. Both tomato yield and flavor play important roles in attracting attentions from growers and consumers. Compared with yield, much less work has been conducted to investigate whether and how pollination methods affect tomato flavor. In this study, the effects of bumblebee pollination, vibrator treatment, and plant growth regulator (PGR) treatment on tomato yield and flavor were tested in Gobi Desert greenhouses. Compared with vibrator or PGR treatments, bumblebee pollinated tomato had higher and more stable fruit set, heavier fruit weight, and more seed. We also found that the seed quantity positively correlated with fruit weight in both bumblebee pollinated, and vibrator treated tomato, but not in PGR treated tomato. Besides enhancing yield, bumblebee pollination improved tomato flavor. Bumblebee pollinated tomato fruits contained more fructose and glucose, but less sucrose, citric acid, and malic acid. Furthermore, the volatile organic compounds of bumblebee pollinated tomato were distinctive with vibrator or PGR treated tomato, and more consumer liking related compounds were identified in bumblebee pollinated tomato. Our findings provide new insights into the contributions of bee pollinator towards improving crop yield and quality, emphasizing the importance of bumblebee for tomato pollination.
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Demand for food is growing along with the human population, leading to an increase in plant production. Many crops are pollinated by insects, so the global demand for managed pollinators is also increasing. The honey bee has traditionally been considered the main provider of crop pollination services. For providing it beekeepers seasonally transport hives to different locations after the flowering of different crops. These movements could be detrimental to pollinators by: i) stressing honey bees, making them more susceptible to pathogens and parasites; ii) spreading bee parasites and pathogens across locations; iii) increasing the transmission of parasites and pathogens between managed and wild pollinators and vice versa (spillover and spillback, respectively). To understand the impact of migratory beekeeping on bee health, we conducted a systematic review to identify the main trends and provide a complete picture of existing knowledge on the subject. We found 52 studies analysing pathogen-related impacts of migratory beekeeping on honey bees. However, only 16 investigations tested the effect of migratory practices on the prevalence and spread of pathogens and parasites. We found no studies that assessed the impact of migratory beekeeping on the occurrence and spread of pests and diseases in wild bees. In general, migratory beekeeping tends to increase the prevalence of pathogens and parasites in honey bee colonies. However, the results were very heterogeneous, probably due to several uncontrolled underlying factors such as management, biological and geographical factors, and the interactions between them. In conclusion, there is an urgent need for studies to assess the impact of migratory beekeeping on bee health, given the current global bee decline and the expected increase in migratory beekeeping due to climate change and crop pollination demand.
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Understanding diversity in flower-visitor assemblages helps us improve pollination of crops and support better biodiversity conservation outcomes. Much recent research has focused on drivers of crop-visitor diversity operating over spatial scales from fields to landscapes, such as pesticide and habitat management, while drivers operating over larger scales of continents and biogeographic realms are virtually unknown. Flower and visitor traits influence attraction of pollinators to flowers, and evolve in the context of associations that can be ancient or recent. Plants that have been adopted into agriculture have been moved widely around the world and thereby exposed to new flower visitors. Remarkably little is known of the consequence of these historical patterns for present-day crop-visiting bee diversity. We analyse data from 317 studies of 27 crops worldwide and find that crops are visited by fewer bee genera outside their region of origin and outside their family's region of origin. Thus, recent human history and the deeper evolutionary history of crops and bees appear to be important determinants of flower-visitor diversity at large scales that constrain the levels of visitor diversity that can be influenced by field- and landscape-scale interventions.
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Crop pollination generally increases with pollinator diversity and wild pollinator visitation. To optimize crop pollination, it is necessary to investigate the pollination contribution of different pollinator species. In the present study, we examined this contribution of honey bees and non-Apis bees (bumble bees, mason bees and other solitary bees) in sweet cherry. We assessed the pollination efficiency (fruit set of flowers receiving only one visit) and foraging behaviour (flower visitation rate, probability of tree change, probability of row change and contact with the stigma) of honey bees and different types of non-Apis bees. Single visit pollination efficiency on sweet cherry was higher for both mason bees and solitary bees compared with bumble bees and honey bees. The different measures of foraging behaviour were variable among non-Apis bees and honey bees. Adding to their high single visit efficiency, mason bees also visited significantly more flower per minute, and they had a high probability of tree change and a high probability to contact the stigma. The results of the present study highlight the higher pollination performance of solitary bees and especially mason bees compared with bumble bees and honey bees. Management to support species with high pollination efficiency and effective foraging behaviour will promote crop pollination.
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The global increase in the proportion of land cultivated with pollinator‐dependent crops implies increased reliance on pollination services. Yet agricultural practices themselves can profoundly affect pollinator supply and pollination. Extensive monocultures are associated with a limited pollinator supply and reduced pollination, whereas agricultural diversification can enhance both. Therefore, areas where agricultural diversity has increased, or at least been maintained, may better sustain high and more stable productivity of pollinator‐dependent crops. Given that >80% of all crops depend, to varying extents, on insect pollination, a global increase in agricultural pollinator dependence over recent decades might have led to a concomitant increase in agricultural diversification. We evaluated whether an increase in the area of pollinator‐dependent crops has indeed been associated with an increase in agricultural diversity, measured here as crop diversity, at the global, regional, and country scales for the period 1961–2016. Globally, results show a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. At regional and country levels, there was no consistent relationship between temporal changes in pollinator dependence and crop diversification. Instead, our results show heterogeneous responses in which increasing pollinator dependence for some countries and regions has been associated with either an increase or a decrease in agricultural diversity. Particularly worrisome is a rapid expansion of pollinator‐dependent oilseed crops in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding. Our analysis has thereby identified world regions of particular concern where environmentally damaging practices associated with large‐scale, industrial agriculture threaten key ecosystem services that underlie productivity, in addition to other benefits provided by biodiversity. Increasing cultivation of pollinator‐dependent crops has placed a stress on global pollination capacity, which could have been ameliorated by a concomitant increase in agricultural diversification. However, this study reports a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. Particularly worrisome is a rapid expansion of pollinator‐dependent monocultures in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding.
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• Bumblebees (Bombus spp.) are efficient pollinators of many flowering plants, yet the pollen deposition performance of individual bees has not been investigated. Worker bumblebees exhibit large intraspecific and intra-nest size variation, in contrast with other eusocial bees; and their size influences collection and deposition of pollen grains. • Laboratory studies with B. terrestris workers and Vinca minor flowers showed that pollen grains deposited on stigmas in single visits (SVD) were significantly positively related to bee size; larger bees deposited more grains, while the smallest individuals, with proportionally shorter tongues, were unable to collect or deposit pollen in these flowers. Individuals did not increase their pollen deposition over time, so handling experience does not influence SVD in Vinca minor. • Field studies using Geranium sanguineum and Echium vulgare, and multiple visiting species, confirmed that individual size affects SVD. All bumblebee species showed size effects, though even the smallest individuals did deposit pollen, whereas there was no detectable effect with Apis with its limited size variation. Two abundant hoverfly species also showed size effects, particularly when feeding for nectar. • Mean size of foragers also varied diurnally, with larger individuals active earlier and later, so that pollination effectiveness varies through a day; flowers routinely pollinated by bees may best be served by early morning dehiscence and visits from larger individuals. • Thus, while there are well-documented species-level variations in pollination effectiveness, the fine-scale individual differences between foragers should also be taken into account when assessing the reproductive outputs of biotically-pollinated plants.
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The sustainability of agriculture can be improved by integrating management of ecosystem services, such as insect pollination, into farming practices. However, large‐scale adoption of ecosystem services‐based practices in agriculture is lacking, possibly because growers undervalue the benefits of ecosystem services compared to those of conventional management practices. Here we show that, under representative real‐world conditions, pollination and plant quality made similar contributions to marketable seed yield of hybrid leek (Allium porrum). Relative to the median, a 25% improvement of plant quality and pollination increased crop value by an estimated $18 007 and $17 174 ha−1 respectively. Across five crop lines, bumblebees delivered most pollination services, while other wild pollinator groups made less frequent but nevertheless substantial contributions. Honeybees actively managed for pollination services did not make significant contributions. Our results show that wild pollinators are an undervalued agricultural input and managing for enhancing pollinators makes sense economically in high‐revenue insect‐pollinated cropping systems.
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In the face of global biodiversity declines driven by agricultural intensification, local diversification practices are broadly promoted to support farmland biodiversity and multiple ecosystem services. The creation of flower-rich habi- tats on farmland has been subsidized in both the USA and EU to support biodiversity and promote delivery of ecosystem services. Yet, theory suggests that the landscape context in which local diversification strategies are implemented will influence their success. However, few studies have empirically evaluated this theory or assessed the ability to support multiple ecosystem services simultaneously. Here, we evaluate the impact of creating flower-rich habitats in field margins on pollination, pest control, and crop yield over 3 years using a paired design across a landscape gradient. We find general positive effects of natural habitat cover on fruit weight and that flowering borders increase yields by promoting bee visitation to adjacent crops only in landscapes with intermediate natural habitat cover. Flowering borders had little impact on biological control regardless of landscape context. Thus, knowledge of landscape context can be used to target wildflower border placement in areas where they will have the greatest likelihood for success and least potential for increasing pest populations or yield loss in nearby crops.
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Pollination services provided by managed bees are essential for California almond (Prunus dulcis Mill.; Rosales: Rosaceae) production. Currently, pollination needs are met by rented or owned Apis mellifera L. (Hymenoptera: Apidae; honey bee) colonies. Excessive demand on a challenged A. mellifera industry to provide strong colonies in early spring has caused sharp increases in rental prices over the past decade, inviting the consideration of alternative pollinators in addition to, or in place of, A. mellifera. Osmia lignaria Say (Hymenoptera: Megachilidae; the blue orchard bee) is an excellent pollinator of fruit and nut trees, but its pollination impacts when used in tandem with A. mellifera have yet to be evaluated in commercial almond orchards. A 2-yr study was conducted in California orchards to compare almond pollination and production using A. mellifera as sole pollinator to an alternative practice of adding O. lignaria as a co-pollinator with A. mellifera. Almond orchard managerial decisions, such as for pesticide use and irrigation intensity, vary between almond growing regions because of local climates. Therefore, both north-central and southern sites of California's San Joaquin Valley are represented. We compared bee visitation, nut set, and nut yield between orchards and between tree rows within orchards. Also, O. lignaria reproductive success was recorded to assure that these bees remained in the orchards as pollinators and to assess the ability to sustain these bees under regional orchard conditions. We demonstrated that augmenting large commercial almond orchards with O. lignaria can significantly increase nut set and sometimes nut yield in both regions evaluated.
Wild bees supply sufficient pollination in Cucurbita agroecosystems in certain settings; however, some growers continue to stock fields with managed pollinators due to uncertainties of temporal and spatial variation on pollination services supplied by wild bees. Here, we evaluate wild bee pollination activity in wholesale, commercial pumpkin fields over 3 yr. We identified 37 species of bees foraging in commercial pumpkin fields. Honey bees (Apis mellifera L. [Hymenoptera: Apidae]), squash bees (Eucera (Peponapis) Say, Dorchin [Hymenoptera: Apidae]), and bumble bees (Bombus spp., primarily B. impatiens Cresson [Hymenoptera: Apidae]) were the most active pollinator taxa, responsible for over 95% of all pollination visits. Preference for female flowers decreased as distance from field edge increased for several bee taxa. Visitation rates from one key pollinator was negatively affected by field size. Visitation rates for multiple taxa exhibited a curvilinear response as the growing season progressed and responded positively to increasing floral density. We synthesized existing literature to estimate minimum 'pollination thresholds' per taxa and determined that each of the most active pollinator taxa exceeded these thresholds independently. Under current conditions, renting honey bee hives may be superfluous in this system. These results can aid growers when executing pollination management strategies and further highlights the importance of monitoring and conserving wild pollinator populations.
Ecological intensification involves the incorporation of biodiversity-based ecosystem service management into farming systems in order to make crop production more sustainable and reduce reliance on anthropogenic inputs, including fertilizer and insecticides. The benefits of effectively managing ecosystem services such as pollination and pest regulation for improved yields have been demonstrated in a number of studies, however, recent evidence indicates that these benefits interact with conventional agronomic inputs such as fertilizer and irrigation. Despite the important contribution of biodiversity-based ecosystem services to crop production their management is rarely considered in combination with more conventional agronomic inputs. This study combines a number of complementary approaches to evaluate the impact of insect pollination on yield parameters of Brassica napus and how this interacts with a key agronomic input, fertilizer. We incorporate data from a flight cage trial and multiple field studies to quantify the relationships between yield parameters to determine whether insufficient insect pollination may limit crop yield. We demonstrate that, by producing larger seeds and more pods, B. napus has the capacity to modulate investment across yield parameters and buffer sub-optimal inputs of fertilizer or pollination. However, only when fertilizer is not limiting can the crop benefit from insect pollination, with yield increases due to insect pollination only seen under high fertilizer application. A nonlinear relationship between seed set per pod and yield per plant was found, with increases in seed set between 15 and 25 seeds per pod resulting in a consistent increase in crop yield. The capacity for the crop to compensate for lower seed set due to sub-optimal pollination is therefore limited. Synthesis and applications. Oilseed rape has the capacity to compensate for sub-optimal agronomic or ecosystem service inputs although this has limitations. Insect pollination can increase seed set and so there are production benefits to be gained through effective management of wild pollinators or by utilizing managed species. Our study demonstrates, however, that increased insect pollination cannot simply replace other inputs, and if resources such as fertilizer are limiting, then yield potential cannot be reached. We highlight the need to consider insect pollination as an agronomic input to be effectively managed in agricultural systems.
Ecologists have shown through hundreds of experiments that ecological communities with more species produce higher levels of essential ecosystem functions such as biomass production, nutrient cycling, and pollination, but whether this finding holds in nature (that is, in large-scale and unmanipulated systems) is controversial. This knowledge gap is troubling because ecosystem services have been widely adopted as a justification for global biodiversity conservation. Here we show that, to provide crop pollination in natural systems, the number of bee species must increase by at least one order of magnitude compared with that in field experiments. This increase is driven by species turnover and its interaction with functional dominance, mechanisms that emerge only at large scales. Our results show that maintaining ecosystem services in nature requires many species, including relatively rare ones.