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
pollination limitation, economic value, wild
bees, crop yield, ecosystem services, honeybee
Author for correspondence:
J. R. Reilly
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
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 world’s 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.
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 . 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 [4–6] 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 [7–8], with little information available about the fre-
quency or circumstances in which pollination limits crop
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) . 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 plant’s 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 plant’s 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 ).
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 [18–20], and that the diversity of
wild bee visitors is higher when crops are grown in their bio-
geographic region of origin . 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 [24,27–30]. 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 . 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
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
is not 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.)
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
production or yields? (iii) How do these contributions
translate into economic value?
(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 . 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. ). 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
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’,‘Xylocopa’or ‘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,
(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
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
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 ) 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 . 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
extrapolations to the national level, are discussed in the electronic
supplementary material, Methods.
(a) Frequency of pollinator limitation
For each crop–state 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 (64–94% 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 crop–state 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 .
(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.)
royalsocietypublishing.org/journal/rspb 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.
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]),
apple sweet cherry
FL BC OR
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 crop–region 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.)
US value (millions of USD)
honey bee wild bees
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 , (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
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 [11–13,18,44,46]. An
earlier meta-analysis found little or no evidence of limitation
in most global crop systems , 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  where much of the previous research on wild
bees and almond pollination has been conducted. This pattern
has also been seen in watermelon  and blueberry .
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. ). 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 . 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
[54–56], 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 .
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
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 ), even though these
changes can have significant implications for yield . 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
), fertilizer (about $23 billion ), 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.
Authors’contributions. 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 project’s advisory board for the input and feedback.
1. IPBES. 2016 The assessment report of the
Intergovernmental Science-Policy Platform on
Biodiversity and Ecosystem Services on pollinators,
pollination and food production (eds S Potts,
V Imperatriz-Fonseca, H Ngo). Bonn, Germany:
2. Calderone N. 2012 Insect pollinated crops, insect
pollinators and US agriculture: trend analysis
of aggregate data for the period 1992–2009.
PLoS ONE 7,1–27. (doi:10.1371/journal.pone.
3. Bauer D, Wing I. 2016 The macroeconomic cost of
catastrophic pollinator declines. Ecol. Econ. 126,
4. van Engelsdorp D, Hayes Jr J, Underwood R. 2008 A
survey of honey bee colony losses in the US, Fall
2007 to Spring 2008. PLoS ONE 3, e4071. (doi:10.
5. Potts S, Biesmeijer J, Kremen C, Neumann P,
Schweiger O, Kunin W. 2010 Global pollinator
declines: trends, impacts and drivers. TREE 25,
6. Cameron S, Lozier J, Strange J, Koch J, Cordes N,
Solter L, Griswold T. 2011 Patterns of widespread
decline in North American bumble bees. PNAS 108,
7. Ashman T et al. 2004 Pollen limitation of plant
reproduction: ecological and evolutionary causes
and consequences. Ecology 85, 2408–2421. (doi:10.
8. Knight T et al. 2005 Pollen limitation of plant
reproduction: pattern and process. Annu. Rev. Ecol.
Evol. Syst. 36, 467–497. (doi:10.1146/annurev.
9. Benjamin F, Winfree R. 2014 Lack of pollinators
limits fruit production in commercial blueberry
(Vaccinium corymbosum). Environ.Entomol. 43,
10. Isaacs R, Kirk A. 2010 Pollination services provided
to small and large highbush blueberry fields by
wild and managed bees. J. Appl. Ecol. 47, 841–849.
11. Garibaldi L et al. 2016 Mutually beneficial pollinator
diversity and crop yield outcomes in small and large
farms. Science 351, 388–391. (doi:10.1126/science.
12. Garratt M, Bishop J, Degani E, Potts S, Shaw R, Shi
A, Roy S. 2018 Insect pollination as an agronomic
input: strategies for oilseed rape production. J. app.
ecol. 55, 2834–2842. (doi:10.1111/1365-2664.
13. Fijen T, Scheper J, Boom T, Janssen N, Raemakers I,
Kleijn D. 2018 Insect pollination is at least as
important for marketable crop yield as plant quality
in a seed crop. Ecol. Lett. 21, 1704–1713. (doi:10.
14. Haig D, Westoby M. 1988 On limits to seed
production. Am. Nat. 131, 757–759. (doi:10.1086/
15. Burd M. 2008 The Haig-Westoby model revisited.
Am. Nat. 171, 400–404. (doi:10.1086/527499)
16. Rosenheim J, Williams N, Schreiber S, Rapp J. 2016
Modest pollen limitation of lifetime seed production
is in good agreement with modest uncertainty in
whole-plant pollen receipt. Am. Nat. 187, 397–404.
17. Klein A, Hendrix S, Clough Y, Scofield A, Kremen C.
2015 Interacting effects of pollination, water and
nutrients on fruit tree performance. Plant Biol. 17,
18. Garibaldi L et al. 2013 Wild pollinators enhance
fruit set of crops regardless of honey-bee
abundance. Science 339, 1608–1611. (doi:10.1126/
19. Kleijn D et al. 2015 Delivery of crop pollination
services is an insufficient argument for wild
pollinator conservation. Nat. Commun. 6,1–24.
20. Rader R et al. 2016 Non-bee insects are
important contributors to global crop pollination.
PNAS 113, 146–151. (doi:10.1073/pnas.
21. Brown J, Cunningham SA. 2019 Global scale drivers
of crop visitor diversity and the historical
development of agriculture. Proc. R. Soc. B 286,
22. Winfree R, Williams N, Dushoff J, Kremen C. 2007
Native bees provide insurance against ongoing
honey bee losses. Ecol. Lett. 10, 1105–1113.
23. Blitzer E, Gibbs J, Park M, Danforth B. 2016
Pollination services for apple are dependent on
diverse wild bee communities. Agric. Ecosyst.
Environ. 221,1–7. (doi:10.1016/j.agee.2016.01.004)
24. Kremen C, Williams N, Thorp R. 2002 Crop
pollination from native bees at risk from agricultural
intensification. PNAS 99, 16 812–16 816. (doi:10.
25. Greenleaf S, Kremen C. 2006 Wild bees enhance
honey bees pollination of hybrid sunﬂower. PNAS
USA 103, 13 890–13 895. (doi:10.1073/pnas.
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922
26. Brittain C, Williams N, Kremen C, Klein A. 2013
Synergistic effects of non-Apis bees and honey bees
for pollination services. Proc. R. Soc. B 280, 1754.
27. Ricketts T et al. 2008 Landscape effects on crop
pollination services: are there general patterns? Ecol.
Lett. 11, 499–515. (doi:10.1111/j.1461-0248.2008.
28. Garibaldi L et al. 2011 Stability of pollination
services decreases with isolation from natural areas
despite honey bee visits. Ecol. Lett. 14, 1062–1072.
29. Kennedy C et al. 2013 A global quantitative
synthesis of local and landscape effects on wild bee
pollinators in agroecosystems. Ecol. Lett. 16,
30. Koh I, Lonsdorf E, Williams N, Brittain C, Isaacs R,
Gibbs J, Ricketts T. 2016 Modeling the status,
trends, and impacts of wild bee abundance in the
United States. PNAS 113, 140–145. (doi:10.1073/
31. Gallai N, Salles J, Settele J, Vaissière B. 2009 Economic
valuation of the vulnerability of world agriculture
confronted with pollinator decline. Ecol. Econ. 68,
32. Klein A, Vaissiere B, Cane J, Steffan-Dewenter I,
Cunningham S, Kremen C, Tscharntke T. 2007
Importance of pollinators in changing landscapes
for world crops. Proc. Biol. Sci. 274, 303–313.
33. Winfree R, Gross B, Kremen C. 2011 Valuing
pollination services to agriculture. Ecol. Econ. 71,
34. Kammerer M, Biddinger D, Rajotte E, Mortensen D.
2015 Local plant diversity across multiple habitats
supports a diverse wild bee community in
Pennsylvania apple orchards. Environ. Entomol. 45,
35. Willmer P, Finlayson K. 2014 Big bees do a better
job: intraspecific size variation influences pollination
effectiveness. J. Pollination Ecol. 14, 244–254.
36. Stavert J, Liñán-Cembrano G, Beggs J, Howlett B,
Pattemore D, Bartomeus I. 2016 Hairiness: the
missing link between pollinators and pollination.
PeerJ 4, e2779. (doi:10.7717/peerj.2779)
37. Bartomeus I et al. 2014 Contribution of insect
pollinators to crop yield and quality varies with
agricultural intensification. PeerJ 2, e328. (doi:10.
38. Losey J, Vaughan M. 2006 The economic value of
ecological services provided by insects. Bioscience
56, 311–323. (doi:10.1641/0006-3568(2006)56[311:
39. Morse R, Calderone N. 2000 The value of honey bees as
pollinators of US crops in 2000. Bee Culture 128,15.
40. Eeraerts M, Vanderhaegen R, Smagghe G, Meeus I.
2019 Pollination efficiency and foraging behaviour
of honey bees and non-Apis bees to sweet cherry.
Agric. For. Entomol. 22,75–82. (doi:10.1111/afe.
41. Aizen M, Garibaldi L, Cunningham S, Klein A. 2009
How much does agriculture depend on pollinators?
Lessons from long-term trends in crop production.
Ann. Botany 103, 1579–1588. (doi:10.1093/aob/
42. Biesmeijer J et al. 2006 Parallel declines in
pollinators and insect-pollinated plants in Britain
and the Netherlands. Science 313, 351–354.
43. Oldroyd B. 2007 What’s killing American honey
bees? PLoS Biol. 5, 1195–1199. (doi:10.1371/
44. Garibaldi L, Aizen M, Klein A, Cunningham S,
Harder L. 2011 Global growth and stability of
agricultural yield decrease with pollinator
dependence. PNAS 108, 5909–5914. (doi:10.1073/
45. Aizen M et al. 2019 Global agricultural productivity
is threatened by increasing pollinator dependence
without an increase in crop diversification. Glob.
Change Biol. 25, 3516–3527. (doi:10.1111/gcb.
46. Garibaldi L, Aizen M, Cunningham S, Klein A. 2009
Pollinator shortage and global crop yield: looking at
the whole spectrum of pollinator dependency.
Commun. Integr. Biol. 2,37–39. (doi:10.4161/cib.2.
47. Aizen M, Garibaldi L, Cunningham S, Klein A. 2008
Long-term global trends in crop yield and
production reveal no current pollination shortage
but increasing pollinator dependency. Curr. Biol. 18,
48. Klein A, Brittain C, Hendrix S, Thorp R, Williams N,
Kremen C. 2012 Wild pollination services to
California almond rely on semi-natural habitat.
J. Appl. Ecol. 49, 723–732.
49. Gibbs J, Elle E, Bobiwash K, Haapalainen T, Isaacs R.
2016 Contrasting pollinators and pollination in
native and non-native regions of highbush
blueberry production. PLoS ONE 11, e0158937.
50. McGrady C, Troyer R, Fleischer S. 2019 Wild bee
visitation rates exceed pollination thresholds in
commercial Cucurbita agroecosystems. J. Econ.
Entomol. 113, 562–574. (doi: 10.1093/jee/toz295)
51. Schuler R, Roulston T, Farris G. 2005 Farming
practices influence wild pollinator populations on
squash and pumpkin. J. Econ. Entomol. 98,
52. Tepedino V. 1981 The pollination efficiency of the
squash bee (Peponapis pruinosa) and the honey bee
(Apis mellifera) on summer squash (Cucurbita pepo).
J. Kansas Entomol. Soc. 54, 359–377.
53. Winfree R, Reilly J, Bartomeus I, Cariveau D,
Williams N, Gibbs J. 2018 Species turnover promotes
the importance of bee diversity for crop pollination
at regional scales. Science 359, 791–793. (doi:10.
54. Blüthgen N, Klein A. 2011 Functional
complementarity and specialisation: the role of
biodiversity in plant–pollinator interactions. Basic
Appl. Ecol. 12, 282–291. (doi:10.1016/j.baae.2010.
55. Rader R, Reilly J, Bartomeus I, Winfree R. 2013
Native bees buffer the negative impact of climate
warming on honey bee pollination of watermelon
crops. Glob. Change Biol. 19, 3103–3110. (doi:10.
56. Fründ J, Dormann C, Holzschuh A, Tscharntke T.
2013 Bee diversity effects on pollination depend on
functional complementarity and niche shifts.
Ecology 94, 2042–2054. (doi:10.1890/12-1620.1)
57. Delaplane K, Mayer D. 2000 Crop pollination by
bees. New York, NY: CABI Publishing.
58. Woodcock T. 2012 Pollination in the Agricultural
Landscape: Best Management Practices for Crop
Pollination. Canadian Pollination Initiative (NSERC-
CANPOLIN): University of Guelph.
59. American Beekeeping Federation. 2018 Pollination
facts. See http://www.abfnet.org/page/
60. Blaauw B, Isaacs R. 2014 Flower plantings increase
wild bee abundance and the pollination services
provided to a pollination-dependent crop. J. Appl.
Ecol. 51, 890–898. (doi:10.1111/1365-2664.12257)
61. Grab H, Poveda K, Danforth D, Loeb G. 2018
Landscape context shifts the balance of costs and
benefits from wildflower borders on multiple
ecosystem services. Proc. Roy. Soc. B 285, 20181102.
62. Isaacs R, Williams N, Ellis J, Pitts-Singer T,
Bommarco R, Vaughan M. 2017 Integrated crop
pollination: combining strategies to ensure stable
and sustainable yields of pollination-dependent
crops. Basic Appl. Ecol. 22,44–60. (doi:10.1016/j.
63. Pitts-Singer T, Artz D, Peterson S, Boyle N, Wardell
G. 2018 Examination of a managed pollinator
strategy for almond production using Apis mellifera
(Hymenoptera: Apidae) and Osmia lignaria
(Hymenoptera: Megachilidae). Environ. Entomol. 47,
64. McGregor S. 1976 Insect pollination of cultivated
crop-plants. USDA Agriculture Handbook 496,
65. Eaton L, Nams V. 2012 Honey bee stocking numbers
and wild blueberry production in Nova Scotia.
Can. J. Plant. Sci. 92, 1305–1310. (doi:10.4141/
66. Geslin B, Aizen M, Garcia N, Pereira A, Vaissiere B,
Garibaldi L. 2017 The impact of honey bee colony
quality on crop yield and farmers’profit in apples
and pears. Agric. Ecosyst. Environ. 248, 153–161.
67. EPA. 2017 Pesticides industry sales and usage:
2008–2012 market estimates. Washington, DC: EPA.
68. USDA-NASS. 2017 QuickStats online database. See
69. Reilly JR et al. 2020 Data from: Crop production in
the USA is frequently limited by a lack of
pollinators. Dryad Digital Repository. (doi:10.5061/
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20200922