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Abstract

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.
royalsocietypublishing.org/journal/rspb
Research
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:
20200922.
http://dx.doi.org/10.1098/rspb.2020.0922
Received: 23 April 2020
Accepted: 7 July 2020
Subject Category:
Ecology
Subject Areas:
ecology
Keywords:
pollination limitation, economic value, wild
bees, crop yield, ecosystem services, honeybee
Author for correspondence:
J. R. Reilly
e-mail: jreilly45@gmail.com
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5063437.
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
1
Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ 08901, USA
2
USDA-Agricultural Research Service, Pollinating Insects Research Unit, Logan, UT 84322, USA
3
Department of Entomology, Pennsylvania State University Fruit Research and Extension Center, Biglerville,
PA 17307, USA
4
Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A1S6 Canada
5
Department of Entomology, University of Manitoba, Winnipeg, MB R3T 2N2 Canada
6
Department of Entomology and Nematology, University of California Davis, Davis, CA 95616, USA
7
Department of Entomology, University of Minnesota, St. Paul, MN 55113, USA
8
Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611, USA
9
USDA Agricultural Research Service, Northern Plains Agricultural Research Laboratory, Sidney, MT 59270, USA
10
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA
11
Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA
12
Agriculture and Natural Resource Program, Wenatchee Valley College, Wenatchee, WA 98801, USA
13
Department of Entomology, Michigan State University, East Lansing, MI 48824, USA
14
Department of Crop and Soil Science, Oregon State University, Corvallis, OR 97331, USA
15
Department of Entomology and Plant Pathology, University of Arkansas, Fayetteville, AR 72701, USA
16
Department of Ecology, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden
17
Department of Applied Ecology, North Carolina State University, Raleigh, NC 27695, USA
18
AgPollen, 14540 Claribel Road, Waterford, CA 95386, USA
19
Northwest Michigan Horticultural Research Center, Michigan State University, Traverse City, MI 49684, USA
20
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
honeybees.
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
p
ollinator visits
pollination
is limiting
pollination
is not limiting
pollination limiting
in some places
(a)(b)(c)
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.)
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
2
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
pollinator
is the annual economic value attributable to a
particular pollinator group (either wild bees or honeybee),
V
crop
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
pollinator
is
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
pollinator
), but rather
assumed a P
honeybee
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
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
3
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
almond
(CA)
apple
(MI)
blueberry
(BC)
apple
(PA)
blueberry
(MI)
blueberry
(OR)
sweet
cherry
(WA)
tart
cherry
(MI)
pumpkin
(PA)
watermelon
(CA)
watermelon
(FL)
blueberry
(FL)
pollination limitation (%)
100
75
50
25
0
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.)
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
4
($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]),
FL CA
blueberry almond
watermelon
pumpkin
PA
MI
tart cherry
MI PA
apple sweet cherry
FL BC OR
MI
PA CAWA
fraction of total pollen grains
deposited by wild bees
1.0
0.8
0.6
0.4
0.2
0
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
0
1000
2000
3000
4000
US value (millions of USD)
blueberry pumpkin
literature
this study
honey bee wild bees
sweet
cherry
tart
watermelon
0
100
300
500
600
200
400
valuation source
cherry
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.)
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
5
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
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
6
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: https://doi.org/10.5061/dryad.
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,
NWO, ECCyT and NSF.
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). ...
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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). ...
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... 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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... 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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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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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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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.
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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.