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How much does agriculture depend on pollinators? Lessons from long-term
trends in crop production
Marcelo A. Aizen1,*, Lucas A. Garibaldi1,2, Saul A. Cunningham3and Alexandra M. Klein4,5
1
Laboratorio Ecotono, INIBIOMA-CONICET and Centro Regional Bariloche, Universidad Nacional del Comahue, Quintral
1250, 8400 Bariloche, Rı
´o Negro, Argentina,
2
Ca
´tedra de Me
´todos Cuantitativos Aplicados, Facultad de Agronomı
´a,
Universidad de Buenos Aires, Av. San Martı
´n 4453, 1417 Buenos Aires, Argentina,
3
CSIRO Entomology, GPO Box 1700,
Canberra, ACT 2601, Australia,
4
Environmental Sciences Policy and Management, 137 Mulford Hall, UC Berkeley,
CA 94720-3114, USA and
5
Agroecology, University of Goettingen, Waldweg 26, 37073 Goettingen, Germany
Received: 27 October 2008 Returned for revision: 19 January 2009 Accepted: 13 February 2009 Published electronically: 1 April 2009
†Background and Aims Productivity of many crops benefits from the presence of pollinating insects, so a decline
in pollinator abundance should compromise global agricultural production. Motivated by the lack of accurate esti-
mates of the size of this threat, we quantified the effect of total loss of pollinators on global agricultural pro-
duction and crop production diversity. The change in pollinator dependency over 46 years was also evaluated,
considering the developed and developing world separately.
†Methods Using the extensive FAO dataset, yearly data were compiled for 1961– 2006 on production and culti-
vated area of 87 important crops, which we classified into five categories of pollinator dependency. Based on
measures of the aggregate effect of differential pollinator dependence, the consequences of a complete loss of
pollinators in terms of reductions in total agricultural production and diversity were calculated. An estimate
was also made of the increase in total cultivated area that would be required to compensate for the decrease
in production of every single crop in the absence of pollinators.
†Key Results The expected direct reduction in total agricultural production in the absence of animal pollination
ranged from 3 to 8 %, with smaller impacts on agricultural production diversity. The percentage increase in cul-
tivated area needed to compensate for these deficits was several times higher, particularly in the developing
world, which comprises two-thirds of the land devoted to crop cultivation globally. Crops with lower yield
growth tended to have undergone greater expansion in cultivated area. Agriculture has become more pollina-
tor-dependent over time, and this trend is more pronounced in the developing than developed world.
†Conclusions We propose that pollination shortage will intensify demand for agricultural land, a trend that will
be more pronounced in the developing world. This increasing pressure on supply of agricultural land could sig-
nificantly contribute to global environmental change.
Key words: Agricultural production, biotic pollination, crop diversity, cultivated area, developed world,
developing world, FAO, randomization.
INTRODUCTION
Animal-mediated pollination contributes to the sexual
reproduction of over 90 % of the approximately 250 000
species of modern angiosperms (Kearns et al., 1998). This
interaction diffusely affects human survival through its roles
in sustaining much biodiversity on Earth and contributing to
the integrity of most terrestrial ecosystems. However, we
also depend more directly on this interaction, because many
agricultural crops rely to some degree on pollinators for
setting the seeds or fruits that we consume, or the seeds we
sow or breed. A now well-known estimate proposed that
about one-third of our food, including animal products,
derives from animal-pollinated, mostly bee-pollinated, crops
(McGregor, 1976). This estimate has recently been confirmed
by Klein et al. (2007), although animal production was
excluded. The diversity of crops that depend on animal polli-
nation provides still more impressive estimates. For instance,
biotic pollination improves the fruit or seed quality or quantity
of about 70 % of 1330 tropical crops (Roubik, 1995) and 85 %
of 264 crops cultivated in Europe (Williams, 1994). These
figures are not obviously biased by the inclusion of many
minor crops from a production viewpoint, as pollinating
insects increase fruit or seed quality or quantity of 39 of the
57 major crops worldwide (Klein et al., 2007). Therefore,
the production and diversity of agriculture seem to depend to
a large extent on biotic pollination, particularly on the
service provided by the honey-bee (Apis mellifera), the
single most important pollinator species, and a plethora of
wild bee species.
Currently, stocks of honey-bees are experiencing many
diseases, and populations of wild pollinator species are declin-
ing in several regions (Kluser and Peduzzi, 2007), raising
concern that a potential global ‘pollination crisis’ threatens
our food supply (Withgott, 1999; Kremen and Ricketts,
2000; Richards, 2001; Westerkamp and Gottsberger, 2002;
Steffan-Dewenter et al., 2005). In North America, the number
of managed honey-bee hives has declined almost 60 %
since the mid 1940s, due to the increasing incidence of
parasitic mites and other unidentified factors (National
* For correspondence. E-mail marcelo.aizen@crub.uncoma.edu.ar
#The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: journals.permissions@oxfordjournals.org
Annals of Botany 103: 1579–1588, 2009
doi:10.1093/aob/mcp076, available online at www.aob.oxfordjournals.org
Research Council, 2007; Oldroyd, 2007; Stokstad, 2007).
Correspondingly, the diversity of wild bees has decreased
greatly over much of Western Europe, mostly owing to habitat
destruction (Biesmeijer et al., 2006; Fitzpatrick et al., 2007).
Despite evidence that pollination shortages affect fruit and
seed quality and quantity of many crops in many places
(Klein et al., 2007), data that we compiled previously did not
provide strong evidence of pollinator limitation affecting
global agricultural production (Aizen et al., 2008). However,
we did determine that cultivation of pollinator-dependent
crops has, on average, been expanding faster than that of non-
dependent crops in both developed and developing countries
over the period 1961– 2006, so the demand for pollination
service is rising at the same time that pollinator abundance
and diversity are declining. In the near future, such opposing
trends threaten crop yields, which could be averted either by
further increases in inputs to compensate for a decline in pro-
ductivity or by implementation of technical alternatives to tra-
ditional pollination practices. This bleak scenario calls for
better information on the dependence of agriculture on pollina-
tors: estimates that should be more precise than the enlighten-
ing, but raw values reported so far (see also Klein et al., 2007).
Many studies have attempted to estimate the value of crop
pollination and pollinator dependency in financial terms, gen-
erating net dollar values for this ecosystem service (Southwick
and Southwick, 1992; Costanza et al., 1997; Losey and
Vaughan, 2006; Gallai et al., 2009). In the present study, we
take a more direct approach, focusing only on predicted
changes in crop output and the land requirements necessary
to maintain current levels of production. Rather than exploring
the possibilities of complex economic responses such as crop
substitutions, or shifts in demand, here we have developed a
static model that places more emphasis on the differences
among crops in their range of pollinator dependence and
their consequences for agricultural productivity. We suggest
that this approach will improve our understanding of the
nature of our dependence on crop pollinators, without introdu-
cing assumptions about economic conditions.
The current dependency of global agriculture on pollinator
services can be estimated in terms of either losses related to a
pollination shortage or the cost of mitigation. The first, deficit,
approach requires quantification of the decrease in relevant
measures of productivity, such as total production, yield and
diversity, in the absence of animal pollination. The second,
compensation, approach requires prediction of the increased
agricultural inputs needed to offset the pollination deficiency,
such as increases in cultivated area, number of managed bees,
labour required for hand pollination, breeding for autonomous
pollination and adoption of pheromones to increase the foraging
activity of bees. Both approaches are implicit in calculations of
the value of insect or, more specifically, honey-bee pollination
to particular crops or the agriculture of specific countries (e.g.
Robinson et al., 1989; Morse and Calderone, 2000; Ricketts
et al., 2004; Morandin and Winston, 2006). Regardless of the
approach adopted, estimation of the agricultural dependence
on animal pollination must recognize that most crops provide
some yield in the absence of pollinators and so depend only
partially on pollinators. Therefore, any global estimate of pol-
linator dependency must account for variation among crops in
the contribution of animal pollination to production to guard
against overstating the agricultural importance of pollinators
(Ghazoul, 2005).
Here we combine long-term data on global crop production
and cultivated area provided by the Food and Agriculture
Organization (FAO) of the United Nations (FAOSTAT, 2007)
and comprehensive information on the pollinator dependence
of individual crops (Klein et al., 2007) to estimate both the
current incidence of pollinator dependency in agriculture and
the change in this dependency over the last five decades. This his-
torical perspective provides an indicator of possible future conse-
quences of a global pollinator decline. Although we previously
reported an expansion in the cultivation of pollinator-dependent
crops (Aizen et al., 2008), we did not explore this trend in
terms of the extent to which agricultural production or diversity
might be affected by pollinator decline given the partial depen-
dence on pollinators of most crops. For each year between 1961
and 2006, we calculated two deficit and one compensation
estimate of pollinator dependency in global agriculture.
Specifically, for deficit estimates we calculated the percentage
decrease in agricultural production and decline in the diversity
of agricultural production caused by complete loss of pollinators.
For compensation estimates we predicted the percentage increase
in total cultivated area needed to mitigate the production deficit in
each affected crop. To assess the realism of our compensation
model, we explored the possibility that crops with slow yield
growth (i.e. slow growth in production per area unit) are
already expanding their total cultivated area at higher rates to
keep pace with increasing production demands. This should
result in a negative association between relative growth in culti-
vated area and relative growth in yield across crops. If this
pattern is corroborated, then we can infer that any future global
pollinator shortage will require ongoing expansion in the area
of cultivation for crops that depend highly on pollinators.
We examined data separately for the developed and developing
world, because these two regions differ, additionally to geo-
graphical location, in socioeconomic conditions, agricultural
intensification, habitat destruction rates and subsidy policies
(Conway, 2001; Evenson and Gollin, 2003). Our previous
results showed that pollinator-dependent crops represented a
larger proportion of total agricultural production in the develop-
ing than developed world (Aizen et al., 2008). However, because
we did not consider the differential importance of animal pollina-
tion for the different crops in that study, we do not know to what
extent agriculture in the developing world is more vulnerable to a
pollination shortage than in developed world. This is important
because those tropical crops that are mostly or exclusively culti-
vated in the developing world might differ, on average, in their
degree of pollinator dependency when compared with crops
widely cultivated in both regions. Therefore, in addition to pro-
viding new estimates of pollinator dependency and their change
over time, we compare them between regions with different
levels of development.
MATERIALS AND METHODS
Dataset
Over the last five decades, the FAO has gathered information
on crop cultivation based on the response to questionnaires
sent out annually to member countries. From the extensive
Aizen et al. — Long-term trends of pollinator dependency in agriculture1580
FAO dataset (FAOSTAT, 2007), we compiled annual data for
1961–2006 on production and cultivated area of a total of 87
crops, 52 of which were represented by single species and 35
by two or more often taxonomically related species (Table S1
in Supplementary Data, available online). For instance, the
crop ‘coffee’ represents three congeneric species, Coffea
arabica,C. canephora and C. libarica. The crops in our
dataset collectively accounted for 82.8 % of total global food
production during 2006, and include all the crops listed in
the electronic supplementary material 1 and 2 of Klein et al.
(2007), in which information on their pollinator dependence
status was reported. We considered a crop to be pollinator-
dependent if animal pollination is required to maximize the
production of fruits or seeds consumed by humans, whereas
non-dependent crops are those that are either pollinated abio-
tically (wind) or autogamously, or cultivated for vegetative
parts (leaves, stems, tubers, etc.). Non-dependent crops
include potatoes and other vegetables, for which human con-
sumption does not depend directly on pollinators, but pollina-
tors are important for propagation via seed or in breeding
programmes (Table S1 in Supplementary Data). Although
exclusion of these crops from the dependent group may under-
estimate overall pollinator dependency in agriculture, quantifi-
cation of the indirect contribution of animal pollinators to their
production is complex.
For the present study, we used separate values on production
and area for the developed and developing world in the FAO
dataset. According to the FAO classification, the developed
world includes all of Europe, USA, Canada, Australia and
New Zealand, whereas the developing world includes all of
Africa and Latin America, as well as most of south-east Asia,
China and India. The USSR was considered by the FAO to be
a developing country until its dissolution in 1991. After that
year, Russia, Ukraine and the other European ex-Soviet repub-
lics were reclassified by the FAO as developed countries,
whereas the Asian ex-Soviet republics remained as developing
countries. This reclassification disrupted the regional trends in
total crop production and cultivated area, because USSR agri-
culture, dominated by Russia and Ukraine, represented about
9.8 % of global crop production by 1991. For consistency and
because the USSR showed similar trends to the rest of Europe
until 1991, we considered all former Soviet republics as part
of the developed world for the entire 1961–2006 period.
Therefore, we added the production and cultivated area of
each crop in the USSR for 1961– 1991, and of each crop in
Armenia, Azerbaijan, Georgia, Kazakhstan, Kyrgyzstan,
Tajikistan, Turkmenistan and Uzbekistan for 1992 – 2006 to
the annual data for the developed world (and subtracted from
the data for the developing world).
Crops were categorized according to their dependence on
animal pollinators based on the magnitude of the reduction
in production (i.e. decreased fruit or seed set/weight) when
pollinators are excluded experimentally from flowers, follow-
ing the recommendations of Klein et al. (2007). These
authors defined five classes of pollinator dependence based
on thorough evaluation of the existing literature: (a) none (pro-
duction does not increase with animal pollination; class 0),
(b) little (0 –10 % production reduction; class 1), (c) modest
(10–40 % reduction; class 2), (d) high (40 –90 % reduction;
class 3) and (e) essential (.90 % reduction without
pollinators; class 4). Variation in pollination requirements
among cultivars within single crops and among species in
crop complexes precluded more refined categorization.
However, we do address the impact of uncertainty in the true
degree of dependence for each individual crop on estimates
of pollinator dependency (see below).
Data analysis
We used data on crop production and cultivated area to cal-
culate different estimates of overall agricultural pollinator
dependency in the developed and developing world. For
each year, we calculated the expected percentage decrease in
agricultural production (i.e. production deficit) in the
absence of animal pollination as:
Deficit ¼100 X
i
Pit X
i
P0
it
!
=X
i
Pit
where P
it
is the production (in metric tonnes, Mt) of crop i
during year t, and P0
it
¼P
it
(1 2d
i
). The coefficient d
i
ranges
from 0 for crops that do not depend on pollinators to 1 for
crops that depend fully on pollinators for production.
Similarly, we calculated the percentage decrease in diversity
(i.e. diversity deficit) in the absence of animal pollination
during year tas 100(D
t
2D0
t
)/D
t
,whereD
t
and D0
t
are esti-
mates of a diversity index based on P
it
and P0
it
, respectively.
We assessed the diversity of agricultural production in terms
of how agricultural production was partitioned among the
different crops (i.e. evenness). Estimates of diversity deficit
may depend on the specific index used, so we consider
Pielou’s J(Pielou, 1969) and Hurlbert’s ‘probability of an
interspecific encounter’ or PIE (Hurlbert, 1971):
J¼X
i
pit lnðpitÞ=lnðStÞ
and
PIE ¼St
St1
1X
i
p2
it
!
where S
t
is the number of crops recorded during year tand p
it
is the relative abundance of crop iduring year t, calculated as:
pit ¼Pit=X
i
Pit or P0
it=X
i
P0
it
for D
t
and D0
t
, respectively. Pielou’s Jrepresents the evenness
component of the Shannon diversity index, whereas Hurlbert’s
PIE indicates the probability of finding different crops in two
cultivated parcels (e.g. of 1 ha each) chosen at random. These
two indices range from 0 when there is just one extremely
dominant crop to 1 when production is distributed evenly
among all crops. Both indices would show reduced evenness
of agricultural production if pollinator declines disproportio-
nately affected crops that were already low in production.
For each year, we also calculated the total percentage increase
in cultivated area needed to balance the production deficit of
Aizen et al. — Long-term trends of pollinator dependency in agriculture 1581
each crop (i.e. area compensation) as:
Compensation ¼100 X
i
A0
it X
i
Ait
!
=X
i
Ait
where A
it
is the area (in hectares) cultivated with crop iduring
year tand A0
it
¼A
it
/(1 2d
i
) (i.e. the area needed to produce P
it
in the absence of animal pollination).
To estimate average dependency on animal pollination for
agriculture in either the developed or the developing world,
we assumed that the relevant d
i
was best represented by the
mid-value of the relevant category of pollinator dependency.
Hence, d
i
equalled 0, 0.05, 0.25, 0.65 or 0.95 for dependency
classes 0, 1, 2, 3 or 4, respectively. We addressed how uncer-
tainty in d
i
influenced our estimates of pollinator dependency
by randomization (implemented in R; R Development Core
Team, 2007). For a given randomization, each crop iwas
assigned a pseudo-d
i
drawn randomly from a uniform distri-
bution bounded by the limits of its pollination-dependence cat-
egory. For instance, for a crop categorized as highly dependent
on animal pollination (class 3), d
i
was drawn randomly from
0.4–0.9, whereas for non-dependent crops, d
i
was set con-
stantly at 0. For each year and region, we generated 5000 ran-
domized values of agricultural dependency after 5000
iterations. We then constructed a 95 % confidence interval
around the estimated mean by identifying the index values
that delimited the 2.5 and 97.5 % percentiles of the cumulative
distribution of randomized values.
The distribution of randomized estimates of the extra culti-
vated area needed to compensate for the production deficit of
even a single crop was highly biased, because it approaches
infinity as d
i
!1. Therefore, we were unable to estimate the
upper limit of the confidence interval for this compensation
index using randomization. However, we did calculate a
minimum possible area compensation by setting d
i
for each
crop to the lowest values of its class intervals.
We explored the possibility that some compensation for crop
production deficits has already occurred through an increase in
cultivated area. In this case, growth in relative yield (i.e.
Mt ha
21
) should decrease as growth in cultivated area
increases across all crops. We also explored the relative influ-
ence of growth in area and yield to change in crop production.
For each crop in each region, we first standardized the change
in each variable x(i.e. production, area or yield) during year t
relative to its value during 1961 as Dx
t
¼100(x
t
2x
1961
)/x
1961
.
We then calculated the slope,
b
, of the linear relationship
between Dx
t
and year (i.e. % year
21
) as an estimate of the
average growth of the respective dependent variable. For
instance, a slope of 1.5 for area indicates that the cultivated
area of a given crop increased, on average, by 1.5 % year
21
relative to its cultivated area in 1961. As it is unlikely that
the growth increment of one crop influences another crop
growth, the different slope estimates may be considered inde-
pendent despite the time-related error correlation structure
within each crop (Murtaugh, 2007). For these calculations,
we excluded five and four crops from the developed and devel-
oping world, respectively, for which complete data since 1961
were not available (Table S1 in Supplementary Data, available
online).
RESULTS
Agriculture production and production deficit
Global agricultural production increased by 140 % between
1961 and 2006; however, temporal trends differed between
the developed and developing world. In the developed
world, aggregate production increased slightly until the late
1980s and decreased slightly thereafter, whereas in the devel-
oping world production increased constantly and strongly over
the entire 46-yr period (Fig. 1). Thus, although total agricul-
tural production was similar in the developing and developed
world in 1961, by 2006 production was 2.2 times greater in
the developing world.
The total production deficit that would occur in the absence
of pollinators ranged from 3 –5 % in the developed world up to
approx. 8 % in the developing world (Fig. 1). The predicted
deficit has, however, increased since the 1980s in both
regions. Pollinator dependency, as measured by this estimate,
increased by 50 and 62 % from 1961 to 2006 in the developed
and developing world, respectively. Uncertainty in depen-
dency values of individual crops introduced an error of only
approx. 1 % in our estimation of the true production deficit.
Thus, the patterns depicted in the lower panels of Fig. 1
reveal trends that are robust to uncertainty in the precise
values of pollinator dependence.
Diversity among crops and the diversity deficit
More than half of the 87 crops included in our sample
depended to at least some extent on pollinators (dependency
category .0; Table 1). All 87 of these crops were cultivated
in the developing world and 76 were cultivated in the devel-
oped world. We found no significant differences in pollinator
dependence between crops cultivated in the developed world
and the 11 tropical crops cultivated exclusively in the develop-
ing world in (Fisher’s Exact test, P¼0.18), despite a trend
towards higher pollinator dependence in the latter group
(Table 1). If crops in the highest dependence category pro-
duced nothing in the absence of flower visitors, the number
of productive crops would decline by 8 % globally.
We ordered crops from most to least abundant by production
volume based on data collected during 2006. The resulting
rank-abundance curves show that 81.5 and 78.2 % of all crops
reported for the developed and developing world, respectively,
had production in the range 10
5
–10
8
Mt (Fig. 2). Crop pro-
duction correlated negatively with pollinator dependence
(Spearman’s correlation: developed world, r
S
¼20.225,
n¼76, P¼0.051; developing world, r
S
¼20.317, n¼87,
P,0.005), trends summarized in the lower panels of Fig. 2.
For instance, production of only two of the ten most productive
crops depended to some degree on flower visitors in both world
regions, whereas eight and seven of the ten least productive
crops were pollinator-dependent in the developed and develop-
ing world, respectively (Fig. 2).
Both Hurlbert’s PIE and Pielou’s Jexhibited relatively con-
stant trends, although a weak increase started from the 1990s
(Fig. 3). PIE was larger than Jfor each year of the time
series in both the developed and the developing world. Both
estimators indicate that agriculture was slightly more diverse
in the developing than developed world, over and above
Aizen et al. — Long-term trends of pollinator dependency in agriculture1582
differences in the number of crops grown. Predicted deficits in
diversity of agricultural production in the absence of flower
visitors were relatively small; however, this diversity loss
depended on the particular estimator used, being higher for J
(4–6 %) than for PIE (1 – 2 %). The predicted deficit increased
from the 1980s, especially in the developing world (Fig. 3).
Uncertainty in pollination dependency introduced errors in
our estimation of agriculture diversity deficit of approx. 1 %
for Jand ,0.5 % for PIE. Thus, the patterns depicted in the
lower panels of Fig. 3 reveal trends that are robust to uncer-
tainty in the precise values for pollinator dependence.
Cultivated area and area compensation
Total cultivated area increased almost 25 % from 1961 to
2006, but temporal trends differed greatly between the devel-
oped and developing world. In the developed world, the area
devoted to agriculture increased slightly until the mid 1980s
before starting to decline, whereas in the developing world
agricultural area increased steadily over the entire period
(Fig. 4). In 1961 the cultivated area in the developing world
was only 38 % larger than in the developed world, but as a
consequence of the different trends this difference increased
to about 130 % in 2006.
The percentage increase in total cultivated area needed to
offset the production deficit expected to occur in the absence
of animal pollination was much larger in the developing
than developed world, a difference that has recently accentu-
ated (Fig. 4). In the developed world, an average additional
cultivated area of about 15 % would have been required to
compensate for the production deficit observed in most years
between 1961 and 2006, with a weak intervening decrease
during the 1970s and 1980s. In contrast, in the developing
world the cultivated area needed to compensate for the pro-
duction deficit increased from 28 % in 1961 to 42 % in
2006. Although minimum estimates of area compensation
were half these values, the trends were similar (Fig. 4).
Average annual growth in relative production, area and yield
were all related. Spearman rank correlations showed that
growth in production correlated positively with growth in
TABLE 1. Distribution of crops among categories of pollinator dependency
Pollinator dependence*
Developed world, all crops Developing world, all crops
†
Exclusively in developing world
No. of crops Percentage crops No. of crops Percentage crops No. of crops Percentage crops
0 (none) 33 43.43540
.2218
.2
1 (little) 11 14.51416
.1327
.3
2 (modest) 14 18.41517
.21 9
.1
3 (high) 13 17.11618
.4327
.3
4 (essential) 5 6.678
.1218
.2
* Class 0 (none) ¼production independent of animal pollination; 1 (little) ¼production reduction .0but,10 % without pollinators; 2 (modest) ¼10– 40 %
reduction; 3 (high) ¼40– 90 % reduction; and 4 (essential) ¼reduction .90 %.
†
Includes all the crops sampled in this study.
0
Production (108 Mt)
10
20
30
40
50
Developed world Developing world
1960
0
Production deficit (%)
2
4
6
8
1970 1980
Year
1990 2000 1960 1970 1980
Ye a r
1990 2000
FIG. 1 . Trends in total agricultural production and mean production deficits in the absence of animal pollination for the developed and developing world 1961–
2006. The grey bands in the lower panels include the region delimited by the 2.5 and 97.5 percentiles of randomized distributions and depict uncertainty in the
estimation of the production deficit.
Aizen et al. — Long-term trends of pollinator dependency in agriculture 1583
both area and yield in the developed and developing world,
although the association with area was consistently much
stronger (Fig. 5). Growth in relative area correlated negatively
with growth in yield in both regions; thus, those crops that
showed the lowest relative yield growth expanded their area
faster on average than crops with the highest growth rates
(Fig. 5). The statistical significance of these trends did not
depend on the inclusion of crops with extreme growth
values. For instance, the association between growth in area
and production for the developed world remains highly signifi-
cant if the two crops with either
b
Darea
or
b
Dproduction
.40 %
year
21
are excluded (r
s
¼0.684, n¼69, P,0.0001).
100
0 10203040
Rank
50
(33) (11) (14) (13) (5)
60 70
Production (Mt)
101
102
103
104
105
107
00
00
0
20
0
01
21
0320200
00
0
0
04
0
3
34
31
04
13201
1
3230
301030
4
2
2
0
3
3011
112
2
0
4
00
000
2
2
2
0
0
0
0
00
2
0
0
4
1
1
002
200
1
3
0
3
0230
0
24
1
1
04
3
000
0
0
3
2
002
0
103
201
134
21
2
0
3
0
1
0
3
1
223
2
0
3
330
1
3
24
3
1
4
0
0
04
3
2
1
2
3
30
106
108
109Developed world
010203040
Rank
50 60 70 80
Developing world
100
0123
Dependence category
4
Production (Mt)
101
102
103
104
105
107
106
108
109
0123
Dependence category
4
(35) (14) (15) (16) (7)
FIG. 2. Rank abundance curves of crops cultivated in the developed and developing world (upper panels). Crops were ranked from the most to the least abundant
according to their total production in each region. Each crop was coded based on its pollinator dependence category (0– 4). Crop names are not included for
clarity. In the lower panels, crops were grouped according to their pollinator dependence categories and production data summarized as box plots. Sample
sizes (i.e. number of crops) are given in parentheses. Note the logarithmic scale of the y-axis in both upper and lower panels.
0·4
Diversity
0·6
0·5
0·7
0·8
0·9
1·0
Developed world
1960
0
Diversity deficit (%)
2
4
6
1970 1980
Year
1990 2000 1960 1970 1980
Ye a r
1990 2000
Developing world
Pielou’s J
Hurlbert’s PIE
Pielou’s J
Hurlbert’s PIE
FIG. 3 . Trends in crop diversity and expected mean diversity deficits in the absence of animal pollination for the developed and developing world 1961–2006.
Diversity was estimated by Pielou’s Jand Hurlbert’s PIE evenness indices. The grey bands in the lower panels include the regions delimited by the 2.5 and 97.5
percentiles of randomized distributions and depict uncertainty in the estimate of the diversity deficit.
Aizen et al. — Long-term trends of pollinator dependency in agriculture1584
DISCUSSION
The pollinator dependence of agriculture
The estimate that humans depend on animal pollination for
about one-third of their food is often highlighted in the litera-
ture on the agricultural consequences of a much debated
decline in pollinator abundance (Buchmann and Nabhan,
1996; Kearns et al., 1998; Holden, 2006; Kluser and
Peduzzi, 2007). Indeed, 70 % of crops that account for about
35 % of all agricultural production depend to varying extents
on pollinators for high-quality and high-quantity seed and
fruit production (Klein et al., 2007). However, according to
our results the proportion of the total production that can be
attributed directly to animal pollination, and that may be lost
in the absence of flower visitors, is on the order of 5 % (devel-
oped world) to 8 % (developing world). This is the compound
result of the partial dependence of most pollinator-dependent
crops (i.e. categories 1 – 3, Table 1) and the smaller average
production of the pollinator-dependent than non-dependent
crops (Fig. 2). Deficits in diversity of agricultural production
were of the same magnitude or lower. Our randomization
tests demonstrate that these estimates are little affected by
current fragmentary knowledge about the quantitative pollina-
tion requirements for many crops.
The discrepancy between prior estimates and our estimates
of the agricultural importance of biotic pollination results pri-
marily because, unlike prior estimates, we accounted for the
fact that many animal-pollinated crops depend only partly on
this service. For instance, although about three-quarters of
crops benefit in some way from animal pollination, only
about 10 % depend fully on pollinators to produce the seeds
or fruits we consume, and they collectively account for only
2 % of global agricultural production. The same phenomenon
explains why major pollinator loss will have limited impact on
the diversity of agricultural production, in terms of either crop
richness or crop evenness. Although Ghazoul (2005) has ques-
tioned claims of a global pollination crisis, in part based on the
limited vulnerability of most crops to pollinator losses (see
also Klein et al. 2007), our analysis provides the first long-term
quantitative assessment of the consequences of incomplete
pollinator dependence on agricultural productivity (for
an economic analogue for the year 2005, see Gallai et al.,
2009).
Like previous studies, we have focused on production in
tonnes, but other relevant perspectives on the importance of
both crops and pollinators also warrant consideration. Crops
differ in their nutritional and economic values, which are not
well represented by production alone. The nutritional contri-
bution of many animal-pollinated crops in terms of proteins,
vitamins and minerals may be much more important for the
human diet than the total mass of production would suggest
(Steffan-Dewenter et al., 2005). Similarly, some relatively
small-volume, pollinator-dependent crops may provide dispro-
portionately large economic returns and are often important for
local markets. To support this point, Gallai et al. (2009)
reported that the value of a tonne of a pollinator-dependent
crop was, on average, five times larger than the value of a
tonne of a non-dependent crop. Furthermore, our focus on
total global effects obscures local phenomena. For example,
a decline in coffee production might have limited effect on
global agricultural production, but would significantly
impact countries that specialize in coffee production, such as
Colombia. Finally, considering pollination solely as a service
for human food consumption is unwise, both because indirect
effects on biodiversity of a decline in pollinators may feedback
and affect human welfare (Kremen et al., 2007) and because
0
Area (106 ha)
200
400
600
800
1000
Developed world Developing world
0
Area compensation (%)
10
Average
Minimum
20
30
40
50
1960 1970 1980
Ye a r
1990 2000 1960 1970 1980
Ye a r
1990 2000
FIG. 4 . Trends in total cultivated area and in the extra cultivated land required to compensate for the deficits in crop production in the absence of animal
pollination (i.e. area compensation) for the developed and developing world 1961 –2006. Area compensation was estimated assuming that the pollinator
dependence of individual crops was represented by the mid-value of the range defining its corresponding dependence class (average-area compensation) and
by the lower limit of that range (minimum-area compensation).
Aizen et al. — Long-term trends of pollinator dependency in agriculture 1585
many people value biodiversity for cultural reasons that extend
far beyond the biological processes that depend on it.
Despite the prediction of a ,8 % impact of animal pollina-
tion on agricultural production and diversity, we found that
compensation for pollination shortage would require vigorous
expansion in total cultivated area. Our estimates of area com-
pensation rely on the assumption that decreased yield of a
specific crop can be compensated for, in the absence of
animal pollination, by an expansion of its cultivated area.
The growing diversification of the human diet, particularly
in industrialized nations, and globalization in food trade
(Pelto and Pelto, 1983) have increased demand for many
animal-pollinated crops and have discouraged replacement of
crops that depend strongly on pollinators by less dependent
crops. Indeed, the evidence supported our prediction that
the crops with the least yield growth over the last five
decades generally had the greatest expansion of cultivated
area. This group includes fruit crops such as avocado, blue-
berry, cherry, plums and raspberry, which are highly
pollinator-dependent and already show no or even negative
growth in yield (Table S1 in Supplementary Data, available
online). More generally, yield growth among highly pollinator-
dependent crops seems not to increase as fast as among less
dependent or non-dependent crops (Aizen et al., 2008).
Therefore, the effect of an increasing pollination shortage
might manifest in a disproportionate increase in demand for
agricultural land, which is surely mediated by the much
higher market value of the production derived from pollinator-
dependent than non-dependent crops (Gallai et al., 2009).
Although this effect is more subtle than the collapse in pro-
duction implicit in the language of the ‘pollination crisis’
(Allen-Wardell et al., 1998; Kremen and Ricketts, 2000;
Westerkamp and Gottsberger, 2002), such increased pressure
on supply of agricultural land could nevertheless contribute
significantly to global environmental change.
Change over time and differences between socioeconomic regions
Several indicators reveal an increase in pollinator depen-
dency in agriculture over time in both the developed and the
developing world. We recently estimated that the percentage
of crop land devoted to pollinator-dependent crops in the
developed world increased from 18.2 % in 1961 to 34.9% in
2006, and from 23.4to32
.8 % in the developing world
(Aizen et al., 2008). Despite showing smaller values in polli-
nator dependency, these trends were reflected here in the
0
20
40
60
80
100
120
140
0 20406080
Developed world
area (% year–1)
production (% year–1)
rS= 0·704, n= 71, P< 0·0001
020406080
Developing world
area (% year–1)
rS= 0·838, n= 83, P< 0·0001
0
20
40
60
80
100
120
140
0 5 10 15
yield (% year–1)
production (% year–1)
rS= 0·249, n= 71, P= 0·037
0 5 10 15
yield (% year–1)
rS= 0·248, n= 83, P= 0·024
0
20
40
60
80
0 5 10 15
yield (% year–1)
area (% year–1)
0 5 10 15
yield (% year–1)
rS= –0·386, n= 71, P< 0·0001 rS= –0·238, n= 83, P= 0·030
FIG. 5. Associations of the average annual rates of growth in area (
b
Darea
), production (
b
Dproduction
) and yield (
b
Dyield
) for crops in the developed and developing
world relative to values in 1961. Results of Spearman’s correlations are provided.
Aizen et al. — Long-term trends of pollinator dependency in agriculture1586
increase in the percentage of agricultural production that can
be attributed to animal pollination (Fig. 1). Also relevant is
the differential growth in the degree of pollinator dependency
in agriculture we have found in the developing vs. developed
world, according to any of our measures of pollinator
dependency.
Increasing demand for food, particularly from populous and
fast-growing nations such as China and India (Winters and
Yusuf, 2007), and for a diversity of agricultural products at
the global market (Pelto and Pelto, 1983), including many tro-
pical crops, are at the core of our trends. Today, the developing
world represents more than two-thirds of global agricultural
production and cultivated land, and supports an agriculture
which, in terms of production, is 50 % more pollinator-
dependent than that of the developed world. Correspondingly,
we predict that the area under cultivation needed to compensate
for any pollinator collapse would be six times larger in the
developing than developed world. Although managed honey-
bees are decreasing drastically in North America and some
parts in Europe (Watanabe, 1994; Kluser and Peduzzi, 2007;
Oldroyd, 2007), native crop pollinators seem to be lost faster
in agricultural landscapes in the tropics than in temperate
regions (Ricketts et al., 2008). This situation may further
increase the vulnerability of agriculture in the developing
world, as the large area needed to compensate for a pollination
deficit will accelerate deforestation, intensify pressures on
remnants of natural and semi-natural ecosystems, and increase
conflicts in the use of agriculture lands.
Conclusions
Concerns of an ongoing trend in pollinator decline in several
parts of the world have brought justified attention to the secur-
ity of human food supplies (Kremen and Ricketts, 2000;
Westerkamp and Gottsberger, 2002; Holden, 2006). We have
shown that the erosion of much pollination capacity caused
by different human impacts will have a limited direct effect
on the quantity and diversity of food production. However,
compensation for these direct impacts on production could
have surprisingly large effects. Even the limited direct
reduction in agricultural production expected under increasing
pollinator shortages may impose a disproportionate demand
for agricultural land to meet growing global consumption,
which will accelerate habitat destruction and may cause
further pollinator losses.
SUPPLEMENTARY DATA
Supplementary Data is available online at http://aob.exford
journals.org/ and consists of an Excel file for Table S1 with
details for each of the 87 crops, including category of pollina-
tor dependence, and estimates of average annual growth rates
in production, cultivated area and yield for the developed
and developing world relative to their respective values
in 1961.
ACKNOWLEDGEMENTS
We thank Natacha Chacoff, Lawrence Harder and three anon-
ymous reviewers for useful comments and suggestions. This
work was conducted partly within the framework provided
by the Restoring Pollination Services Working Group sup-
ported by the National Center for Ecological Analysis
and Synthesis, a centre funded by NSF (grant no. DEB-
0072909). Additional funding by the Argentina National
Council for Research (PIP 5066) and the National University
of Comahue (B126/04) is acknowledged. M.A.A. is a career
researcher of the Argentina National Council for Research
and L.A.G. holds a fellowship from the same agency.
A.M.K. is supported by the Alexander von Humboldt
Foundation.
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