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Impacts of genetically engineered crops on pesticide use in the U.S.-the first sixteen years

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  • Newcastle University and Benbrook Consulting Services (BCS)

Abstract and Figures

Background Genetically engineered, herbicide-resistant and insect-resistant crops have been remarkable commercial successes in the United States. Few independent studies have calculated their impacts on pesticide use per hectare or overall pesticide use, or taken into account the impact of rapidly spreading glyphosate-resistant weeds. A model was developed to quantify by crop and year the impacts of six major transgenic pest-management traits on pesticide use in the U.S. over the 16-year period, 1996–2011: herbicide-resistant corn, soybeans, and cotton; Bacillus thuringiensis (Bt) corn targeting the European corn borer; Bt corn for corn rootworms; and Bt cotton for Lepidopteron insects. Results Herbicide-resistant crop technology has led to a 239 million kilogram (527 million pound) increase in herbicide use in the United States between 1996 and 2011, while Bt crops have reduced insecticide applications by 56 million kilograms (123 million pounds). Overall, pesticide use increased by an estimated 183 million kgs (404 million pounds), or about 7%. Conclusions Contrary to often-repeated claims that today’s genetically-engineered crops have, and are reducing pesticide use, the spread of glyphosate-resistant weeds in herbicide-resistant weed management systems has brought about substantial increases in the number and volume of herbicides applied. If new genetically engineered forms of corn and soybeans tolerant of 2,4-D are approved, the volume of 2,4-D sprayed could drive herbicide usage upward by another approximate 50%. The magnitude of increases in herbicide use on herbicide-resistant hectares has dwarfed the reduction in insecticide use on Bt crops over the past 16 years, and will continue to do so for the foreseeable future.
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R E S E A R C H Open Access
Impacts of genetically engineered crops on
pesticide use in the U.S. the first sixteen years
Charles M Benbrook
Abstract
Background: Genetically engineered, herbicide-resistant and insect-resistant crops have been remarkable
commercial successes in the United States. Few independent studies have calculated their impacts on pesticide use
per hectare or overall pesticide use, or taken into account the impact of rapidly spreading glyphosate-resistant
weeds. A model was developed to quantify by crop and year the impacts of six major transgenic pest-management
traits on pesticide use in the U.S. over the 16-year period, 19962011: herbicide-resistant corn, soybeans, and
cotton; Bacillus thuringiensis (Bt) corn targeting the European corn borer; Bt corn for corn rootworms; and Bt cotton
for Lepidopteron insects.
Results: Herbicide-resistant crop technology has led to a 239 million kilogram (527 million pound) increase in
herbicide use in the United States between 1996 and 2011, while Bt crops have reduced insecticide applications by
56 million kilograms (123 million pounds). Overall, pesticide use increased by an estimated 183 million kgs (404
million pounds), or about 7%.
Conclusions: Contrary to often-repeated claims that todays genetically-engineered crops have, and are reducing
pesticide use, the spread of glyphosate-resistant weeds in herbicide-resistant weed management systems has
brought about substantial increases in the number and volume of herbicides applied. If new genetically engineered
forms of corn and soybeans tolerant of 2,4-D are approved, the volume of 2,4-D sprayed could drive herbicide
usage upward by another approximate 50%. The magnitude of increases in herbicide use on herbicide-resistant
hectares has dwarfed the reduction in insecticide use on Bt crops over the past 16 years, and will continue to do so
for the foreseeable future.
Keywords: Herbicide-resistant crops, Herbicide-tolerant soybeans, Glyphosate, 2,4-D, Bt crops, Genetically
engineered corn, Roundup Ready crops, Biotechnology and pesticide use, Glyphosate resistant weeds
Background
Public debate over genetically engineered (GE) crops is
intensifying in the United States (U.S.), driven by new
science on the possible adverse health impacts associated
with herbicide-resistant (HR) crop pesticide use, and the
rapid spread of glyphosate-resistant weeds. Still, many
experts and organizations assert that GE crops have
reduced, and continue to reduce herbicide, insecticide,
and overall pesticide use. Fortunately, high quality and
publically accessible U.S. Department of Agriculture
(USDA) pesticide use data are available and can be used to
track changes in pesticide use on crops containing GE
traits. Moreover, the impacts of these traits on U.S.
pesticide use trends are substantial and obvious, especially
in recent years as a result of the growing number and
geographical spread of glyphosate-resistant (GR) weeds.
Stable reductions in insecticide use in Bt-transgenic corn
are also now in jeopardy as a result of the emergence of
corn rootworm (CRW) populations resistant to the Cry
3Bb1 toxins expressed in several corn hybrids [1,2]. To
combat this ominous development, some seed and pesti-
cide companies are recommending a return to use of corn
soil insecticides as a resistance management tool. There is
a degree of irony in such recommendations, given that the
purpose of Cry 3Bb1 corn was to eliminate the need for
corn soil insecticides.
The emergence of herbicide-resistant genetically engi-
neered crops in 1996 made it possible for farmers to use a
broad-spectrum herbicide, glyphosate, in ways that were
Correspondence: cbenbrook@wsu.edu
Centre for Sustaining Agriculture and Natural Resources, Washington State
University, Hulbert 421, PO Box 646242, Pullman, WA 99164-6242, USA
© 2012 Benbrook; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction
in any medium, provided the original work is properly cited.
Benbrook Environmental Sciences Europe 2012, 24:24
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previously impossible. From 1996 through 2011, 0.55 bil-
lion hectares of HR corn (Zea mays), soybeans (Glycine
max), and cotton (Gossypium hirsutum)weregrownin
the U.S. [Additional file 1: Table S7]. In 2011, an estimated
94% of the soybean area planted, 72% of corn, and 96% of
cotton were planted to HR varieties, respectively, while
about 65% of corn and 75% of cotton hectares in the U.S.
were planted to Bt varieties [Additional file 1: Table S6].
Glyphosate-resistant, Roundup Ready (RR) crops now
comprise the overwhelming majority of HR crops. RR
crops were rapidly adopted because they provided farmers
a simple, flexible, and forgiving weed management system,
especially compared to systems reliant on the low-dose,
persistent herbicide chemistries on the market in the late
1990s, such as imazethapyr (43% soybean hectares treated
in 1996) and chlorimuron-ethyl (14% treated). From 1996
through 2008, HR crops resistant to herbicides other than
glyphosate either disappeared from the market (e.g. bro-
moxynil HR cotton), or have been planted on relatively
few hectares (e.g. glufosinate HR, LibertyLink cotton and
corn).
Net reductions in pesticide use, encompassing changes
in both herbicide and insecticide kilograms/pounds ap-
plied, are among the purported claims of GE crops [3-5].
Analysts assessing the impacts of Bt crops on insecticide
use report reductions, or displacement, in the range of
25% to 50% per hectare [6]. A more recent study reports a
24% reduction [5]. On GE and non-GE corn since 1996,
the volume of insecticides applied has declined, because of
the pesticide industry-wide trend toward more biologically
active insecticides applied at incrementally lower applica-
tion rates.
The corn rootworm (CRW) has been the target of the
majority of corn insecticide applications the last several
decades. The average corn insecticide application rate in
1996 was about 0.76 kilograms of active ingredient per
hectare (kgs/ha) (0.7 pounds/acre) and is less than 0.2 kgs/
ha today (0.18 pounds a.i./acre) [Additional file 1: Table
S12]. The two contemporary corn soil insecticide market
leaders tebupirimiphos and tefluthrin are applied at
average rates around 0.13 kgs/ha (0.12 pounds/acre). In
1996, the market leaders were chlorpyrifos and terbufos,
insecticides applied at rates above 1.12 kgs/ha (1.0 pounds/
acre) [Additional file 1: Table S12]. Obviously, planting Bt
corn in 2011 reduced insecticide use less significantly com-
paredtolandplantedtoBt corn in the late 1990s.
Few comprehensive estimates have been made of the
impacts of HR crops on herbicide use. The USDA has
not issued a new estimate in well over a decade; the
USDAs Economic Research Service (ERS) reported an
3.7 million kg (8.2 million pound) decrease in pesticide
use in 1998 as a result of GE corn, soybeans, and cotton
[7], an estimate that is comparable to the present studys
estimate of a 4.4 million kg (9.6 million pound)
reduction [Additional file 1: Table S15]. A series of un-
published simulation studies have been carried out by
the National Center for Food and Agriculture Policy
(NCFAP). In a report covering crop year 2005, NCFAP
projected that HR corn, soybean, and cotton reduced
total herbicide use by 25.6 million kgs, compared to hec-
tares planted to non-HR varieties [6]. Sankulas herbicide
use estimates are based on observations of mostly uni-
versity experts regarding typicalherbicide use rates on
farms planting HR versus non-HR varieties. The rates
incorporated in Sankulas estimates often differ from those
published for the same year by USDAs National Agricul-
tural Statistics Service (NASS) [8]. NASS reported that an
average 1.5 applications of glyphosate were made on HR
soybeans in 2005, while Sankula assumes only 1.18 appli-
cations. Sankulas estimate of total herbicide use on RR
soybeans in 2005, 1.15 kgs/ha (1.03 pounds/acre), is less
than the NASS figure for glyphosate alone, 1.23 kgs/ha
(1.1 pounds/acre). If true, Sankulas data suggests that es-
sentially no other herbicides were applied to RR soybeans
in 2005, when in fact the average soybean hectare in 2002
was treated with 1.66 herbicides according to NASS data.
This paper quantifies the impacts of GE crops on the
kilograms of pesticides applied per hectare and across all
GE hectares, drawing upon publicly accessible USDA data.
The pesticide use impacts of the six major, commercial
GE pest-management traits are modeled and then aggre-
gated over the 16 years since commercial introduction.
While most of the pesticide use data incorporated in the
model were originally reported by U.S. government agen-
cies in pounds of active ingredient, and/or pounds of a.i./
acre, results are reported herein in SI units (kilograms of
active ingredient and kg/ha). Some key results are also
reported in pounds/acre. Convert kilograms to pounds by
multiplying by 2.205, and pounds to kgs by multiplying by
0.454. To convert from kg/ha to pounds/acre, multiply by
0.893; to convert from pounds/acre to kg/ha, multiply by
1.12.
Results and discussion
Farmers planted 0.55 billion hectares (1.37 billion acres) of
HR corn, soybeans, and cotton from 1996 through 2011,
with HR soybeans accounting for 60% of these hectares
[Additional file 1: Table S7]. In terms of overall herbicide
use per hectare based on NASS data, substantial increases
have occurred from 1996 through 2011. In soybeans,
USDA reported herbicide applications totaling 1.3 kgs/ha
(1.17 pounds/acre) in 1996, and 1.6 kgs/ha (1.42 pounds/
acre) in 2006, the last year soybeans were surveyed by
USDA. In cotton, herbicide use has risen from 2.1 kgs/ha
(1.88 pounds/acre) in 1996 to 3.0 kgs/ha (2.69 pounds/
acre) in 2010, the year of the most recent USDA survey.
In the case of corn, herbicide use has fallen marginally
from 3.0 kgs/ha (2.66 pounds/acre) in 1996 to 2.5 kgs/ha
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(2.26 pounds/acre) in 2010, largely as a result of lessened
reliance on older, high-rate herbicides.
Compared to herbicide use rates per hectare on non-HR
hectares, HR crops increased herbicide use in the U.S. by
an estimated 239 million kgs (527 million pounds) in the
19962011 period, with HR soybeans accounting for 70%
of the total increase across the three HR crops. Rising reli-
ance on glyphosate accounted for most of this increase.
In light of its generally favorable environmental and
toxicological properties, especially compared to some of
the herbicides displaced by glyphosate, the dramatic
increase in glyphosate use has likely not markedly
increased human health risks. Because glyphosate cannot
be sprayed on most actively growing, non-GE plants,
residues of glyphosate in food have been rare, at least until
the expansion ~ 2006 in the number of late-season glypho-
sate applications on wheat and barley as a harvest aid and/
or to control escaped weeds. Presumably as a result of
such uses, 5.6% of 107 bread samples tested in 2010 by the
U.K. Food Standards Agency contained glyphosate
residues [9]. Three samples had 0.5 parts per million of
glyphosate [9], a relatively high level compared to the
other pesticides found in these bread samples.
Budget pressures have forced the U.S. Department of
Agriculture to reduce the number of crops included in
its annual NASS pesticide use survey. Soybean pesticide
use has not been surveyed since 2006, about when the
spread of glyphosate-resistant weeds began to signifi-
cantly increase herbicide use in selected areas. Herein,
total herbicide use on HR hectares is projected to rise
13.5% from 20062011 (about 2.7% annually), compared
to a 6.6% (1.3% annually) increase on conventional soy-
bean hectares. By way of contrast, the NASS-reported
glyphosate rate of application per crop year on the aver-
age hectare of soybeans increased 8.9% per annum from
20002006 (see Table 1). So, despite the significant and
widespread challenges inherent in managing glyphosate-
resistant weeds in the 20062011 period, a substantial
decrease is projected in the rate of increase in glyphosate
applications per hectare of HR soybeans. The justifica-
tion for this projected fall in the rate of increase is
recognition by farmers that further increases in glypho-
sate use will likely not prove cost-effective, coupled with
positive responses by farmers to the near-universal
recommendation that corn-soybean farmers incorporate
into their spray programs herbicides that work through
modes of action other than glyphosates [10-15].
Since 1996, about 317 million trait hectares (782 mil-
lion trait acres) have been planted to the three major Bt
traits Bt corn for European corn borer (ECB) and
CRW, and Bt cotton. Bt corn and cotton have delivered
consistent reductions in insecticide applications totaling
56 million kgs (123 million pounds) over 16 years of
commercial use. Bt corn reduced insecticide use by 41
million kgs (90 million pounds), while Bt cotton dis-
placed 15 million kgs (34 million pounds) of insecticide
use.
Taking into account applications of all pesticides tar-
geted by the traits embedded in the three major GE
crops, pesticide use in the U.S. was reduced in each of
the first six years of commercial use (19962001). But in
2002, herbicide use on HR soybeans increased 8.6 mil-
lion kgs (19 million pounds), driven by a 0.2 kgs/ha
(0.18 pounds/acre), increase in the glyphosate rate per
crop year, a 21% increase. Overall in 2002, GE traits
increased pesticide use by 6.9 million kgs (15.2 million
pounds), or by about 5%. Incrementally greater annual
increases in the kilograms/pounds of herbicides applied
to HR hectares have continued nearly every year since,
leading to progressively larger annual increases in overall
pesticide use on GE hectares/acres compared to non-GE
hectares/acres. The increase just in 2011 was 35.3 mil-
lion kgs (77.9 million pounds), a quantity exceeding by a
wide margin the cumulative, total 14 million kg (31 mil-
lion pound) reduction from 1996 through 2002.
Total pesticide use has been driven upward by 183
million kgs (404 million pounds) in the U.S. since 1996
by GE crops, compared to what pesticide use would
likely have been in the absence of HR and Bt cultivars.
This increase represents, on average, an additional ~0.21
kgs/ha (~0.19 pounds/acre) of pesticide active ingredient
for every GE-trait hectare planted. The estimated overall
increase of 183 million kgs (404 million pounds) applied
over the past 16 years represents about a 7% increase in
total pesticide use.
There are two major factors driving the upward trend
in herbicide use on HR hectares compared to hectares
planted to non-HR crops: incremental reductions in the
application rate of herbicides other than glyphosate
applied on non-HR crop hectares, and second, the emer-
gence and rapid spread of glyphosate-resistant weeds.
The first factor is driven by progress made by the
Table 1 Projected rates of change in herbicide use since
the most recent USDA survey, relative to recent annual
percent changes in rates
2010-2011 2005-2010 Per Year 2005-2010
Corn
Total Herbicides 2% 10.2% 2.0%
Glyphosate 2.5% 12.9% 2.6%
Soybeans 2007-2011 2000-2006 Per Year 2000-2006
Total Herbicides 3.2% 35.2% 5.9%
Glyphosate 3.3% 53.4% 8.9%
Cotton 2010-2011 2007-2010 Per Year 2007-2010
Total Herbicides 2.2% 3.1% 1.0%
Glyphosate -1% -10.3% -3.4%
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pesticide industry in discovering more potent herbicidal
active ingredients effective at progressively lower rates of
application.
Twenty-seven percent of U.S. soybean hectares in 1996
were treated with pendimethalin at an average rate of 1.1
kgs/ha and another 22% were sprayed with trifluralin at a
rate of 0.99 kgs/ha, while the market leader (imazethapyr)
was applied to 43% of hectares planted at a rate of 0.07
kgs/ha [16]. By 2002 the combined percentage of soybean
hectares treated with these two high-dose herbicides had
dropped from 49% to 16% [17], and just 5% were treated
in 2006 [18]. Between 1996 and 2006, the number of regis-
tered soybean herbicides applied at rates below 0.11 kgs/
ha increased from nine to 17. As a result, the amount of
herbicides applied to conventional crops has steadily fallen
since 1996. In contrast, glyphosate is a relatively high-dose
herbicide that is usually applied at a rate between 0.67 to
0.9 kgs per hectare.
Resistant weeds
The emergence and spread of glyphosate-resistant weeds
is the second, and by far most important factor driving up
herbicide use on land planted to herbicide-resistant var-
ieties. Glyphosate resistant (GR) weeds were practically
unknown before the introduction of RR crops in 1996.
The first glyphosate-resistant weed (Lolium rigidum)
emerged in Australia in 1996 from canola, cereal crop,
and fence line applications [19]. In the mid-1990s, as the
first glyphosate-resistant crops were moving toward
commercialization and gaining market share, Monsanto
scientists wrote or were co-authors on several papers ar-
guing that the evolution of GR weeds was unlikely, citing
the herbicides long history of use (~20 years) and relative
absence of resistant weeds [20,21].
Other scientists, however, challenged this assertion [22].
Dr. Ian Heap, long-time manager of the international
database on resistant weeds, warned in a 1997 conference
presentation that to limit glyphosate selection pressure in
Roundup Ready cropping systems, the herbicide would
need to be used in conjunction with proven resistance-
management practices and with non-chemical weed con-
trol methods [23]. A 1996 report by Consumers Union
stated that HR crops are custom-madefor accelerating
resistance and called for the Environmental Protection
Agency (EPA) to revoke approval of HR crops when and
where credible evidence of resistance emerges [24].
Today, the Weed Science Society of America (WSSA)
website lists 22 GR weed species in the U.S. [19]. Over
two-thirds of the approximate 70 state-GR weed combina-
tions listed by WSSA have been documented since 2005,
reflecting the rapidly spreading nature of the GR-weed
problem. According to the WSSA, over 5.7 million
hectares (14 million acres) are now infested by GR weeds,
an estimate that substantially underestimates the actual
spread of resistant weeds [16,22], [and personal communi-
cation, Dr. Ian Heap]. Dow AgroSciences carried out a re-
cent survey on the percent of crop acres/hectares in the
U.S. impacted by glyphosate-resistant weeds [25]. Findings
from the survey were provided to USDA in support of
Dow AgroSciencess petition for deregulation of 2,4-D
herbicide-resistant corn, and suggest that around 40 mil-
lion hectares (100 million acres) are already impacted by
glyphosate-resistant weeds, an estimate that Heap consid-
ers inflated [personal communication]. The true extent of
spread in the U.S. likely lies around the midpoint between
the WSSA and Dow AgroSciences estimates (i.e., 2025
million hectares), and by all accounts, will continue to rise
rapidly for several years.
Why have GR weeds become such a serious problem?
Heavy reliance on a single herbicide glyphosate
(Roundup) has placed weed populations under progres-
sively intense, and indeed unprecedented, selection pres-
sure [10]. HR crops make it possible to extend the
glyphosate application window to most of the growing
season, instead of just the pre-plant and post-harvest peri-
ods. HR technology allows multiple applications of gly-
phosate in the same crop year. The common Midwestern
rotation of HR corn-HR soybeans, or HR soybeans-HR
cotton in the South, exposes weed populations to annual
and repetitive glyphosate-selection pressure.
These factors trigger a perfect storm for the emer-
gence of GR weeds. Research has traced the resistance
mechanism in Palmer amaranth (Amaranthus palmeri)
to 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS)
gene amplification. Resistant weed populations from
Georgia contained 5-fold to 160-fold more copies of the
EPSPS gene, compared to susceptible plants [26]. More-
over, EPSPS gene amplification is heritable, leading Gaines
et al. to warn that the emergence of GR weeds endangers
the continued success of transgenic glyphosate-resistant
crops and the sustainability of glyphosate as the worlds
most important herbicide.
Resistant Palmer amaranth (Amaranthus palmeri)has
spread dramatically across southern states since the first
resistant populations were confirmed in 2005, and already
poses a major economic threat to U.S. cotton production.
Some infestations are so severe that cotton farmers have
been forced to leave some crops unharvested.
Responding to resistance
GR weed phenotypes are forcing farmers to respond by
increasing herbicide application rates, making multiple
applications of herbicides, applying additional herbicide
active ingredients, deep tillage to bury weed seeds, and
manual weeding. In recent years the first three of the
above responses have been the most common. Each
response increases the kilograms of herbicides applied on
HR crop hectares. All five interventions increase costs.
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Moreover, if 2,4-D and dicamba herbicide-resistant corn
and soybeans are fully deregulated by the U.S. govern-
ment, there will be growing reliance on older, higher-risk
herbicides for management of glyphosate-resistant weeds.
Based on an upward trajectory in the planting of 2,4-D
HR corn reaching 55% of corn hectares planted by 2019,
coupled with an average of 2.3 applications (the label
allows three) and an average rate of 0.94 kgs/ha (0.84
pounds/acre) (the label allows 1.12 kgs/ha (1.0 pounds/
acre)), 2,4-D use on corn in the U.S. would increase over
30-fold from 2010 levels [Additional file 1: Table S19].
Such a dramatic increase could pose heightened risk of
birth defects [27,28] and other reproductive problems
[29], more severe impacts on aquatic ecosystems [30],
and more frequent instances of off-target movement and
damage to nearby crops and plants. Moreover, the effi-
cacy of 2,4-D corn may well prove short lived, since a
population of 2,4-D resistant waterhemp (Amaranthus
tuberculatus) has now been confirmed in Nebraska [31],
and there are already at least eight other weeds resistant
to 2,4-D [19].
GR weeds typically emerge first on a few isolated fields,
but their pollen, genes, and seeds can travel widely and
spread quickly, especially if glyphosate continues to be
relied on heavily [11]. No substantial change in the inten-
sity of glyphosate use in the U.S. is expected in the fore-
seeable future; nearly all corn, soybean, and cotton
cultivars now carry a RR gene. The seed industry has no
plans to grow and sell more non-HR seed, and indeed is
moving in the opposite direction by developing more
stacked, multiple HR varieties. The share of total national
corn, soybean, and cotton hectares impacted by GR weed
populations is likely to grow and will, as a result, increase
both the number of different herbicides applied, as well as
the total kgs of herbicides applied.
As argued by many weed scientists and extension
specialists, integrated weed management systems, coupled
with markedly lessened reliance on RR technology are
now essential to extend the useful life of RR technology
[10,12,14,32]. Without major change, a crisis in weed
management systems is likely, triggering possibly ominous
economic, public health, and environment consequences.
Higher costs triggered by resistant weeds and HR
technology
Weed management costs per hectare increase by 50% to
100% or more in fields infested with glyphosate-resistant
weeds, as evident in a series of case studies submitted to
the USDA by Dow AgroSciences in support of its petition
to the USDA seeking deregulation of 2,4-D herbicide-
resistant corn [25]. In soybean production in Arkansas, for
example, Dow AgroSciences compared the average cost/
acre of the top-five, most popular herbicide programs in
Roundup Ready soybeans in fields without resistant weeds,
compared to the average of two recommended programs
in fields infested with glyphosate-resistant Palmer amar-
anth. Herbicide costs rise 2.7-fold (from $16.29 to $44.34
per acre) [23], [Table thirty, page 93]. In Illinois soybean
production, the increase in herbicide costs is estimated at
64% ($19.21 to $31.49 per acre) [23], [Table thirty-two,
page 95], while in Iowa corn production, the increase is
67% ($19.23 to $32.10 per acre) [23], [Table thirty-six,
page 99].
The markedly higher cost/hectare of herbicide-
resistant seeds must be added to the higher herbicide
costs noted above to more fully reflect the added costs
associated with HR technology. The cost of a bushel of
conventional, not-GE soybean seed increased during the
GE-crop era from $14.80 in 1996 to $33.70 in 2010,
while a bushel of GE soybean seed cost, on average,
$49.60 in 2010 (all seed price data derived from USDA
data) [33]. Accordingly, the cost of GE soybean seed in
2010 was 47% higher per bushel than non-GE seed. In
the case of corn, conventional seed prices rose from
$26.65 per acre planted in 1996 to $58.13 in 2010. The
average cost of GE corn seed per acre in 2010 was
$108.50, with some GE cultivars selling for over $120
per planted acre. Hence, GE corn seed costs per acre
were about double the cost conventional seed.
Public health concerns
Heightened risk of public health impacts can be
expected in the wake of more intensive herbicide use, es-
pecially applications later in the season on herbicide-
resistant crop varieties. While current risk assessment
science suggests that glyphosate is among the safer her-
bicides per hectare treated in terms of human health
risks, both the frequency of human exposures and levels
of exposure via food, drinking water, and the air have no
doubt risen in the U.S. in recent years. Two-thirds to
100% of air and rainfall samples tested in Mississippi
and Iowa in 20072008 contained glyphosate [34].
The likely approval and use of herbicide-resistant crops
in the U.S. engineered to survive applications of multiple
herbicides adds tricky new dimensions to herbicide-risk
assessments. Applications later in the growing season will
be more likely to lead to residues in silage or forage crops.
As a result, herbicide residues in milk, meat, or other ani-
mal products might become more common. The jump in
herbicide volumes applied during June and July will in-
crease the risk of drift and herbicide movement via
volatilization, possibly exposing people via the air, water,
or crops grown in the proximity of treated fields. Risks
from the drift and volatilization of 2,4-D and dicamba are
of special concern, given that these two herbicides have
triggered thousands of non-target crop damage episodes
over the last 20 years in the U.S. Indeed, for several years,
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2,4-D has been the leading cause of crop damage episodes
investigated by State departments of agriculture [35].
Environmental impacts linked to HR technology
A long list of environmental effects can be triggered, or
made worse, by the more intensive herbicide use required
to keep pace with weeds in farming systems heavily reliant
on herbicide-resistant crops. Glyphosate has been shown
to impair soil microbial communities in ways that can in-
crease plant vulnerability to pathogens [36-38], while also
reducing availability of certain soil minerals and micronu-
trients [39]. Landscapes dominated by herbicide-resistant
crops support fewer insect and bird species; e.g., a study in
the American Midwest reported a 58% decline in milk-
weed and an 81% drop in monarch butterflies from 1999
to 2010 [40]. Heavy use of glyphosate can reduce earth-
worm viability [41] and water use efficiency [42]. Several
studies have documented reductions in nitrogen fixation
in herbicide-resistant soybean fields sprayed with glypho-
sate [43,44]. Transgene flow from herbicide-resistant crops
can occur via multiple mechanisms and can persist in
weedy relatives [45].
Individually, these environmental impacts appear, for the
most part, of the same nature and in the same ballpark as
the risks associated with other herbicide-based farming
systems, but collectively they raise novel concerns over
long-term, possibly serious impacts on biodiversity, soil
and plant health, water quality, aquatic ecosystem integrity,
and human and animal health.
Bt corn and cotton impacts and prospects
While Bt-transgenic corn and cotton have displaced an
estimated 56 million kgs (123 million pounds) of insecti-
cides since 1996, every plant in a Bt corn or cotton field
is manufacturing within its cells one or more forms of
the natural bioinsecticide Bacillus thuringiensis. The rate
of synthesis of Bt Cry protein endotoxins is roughly pro-
portional to the rate of plant growth. As plants mature
and enter senescence, Bt endotoxin expression falls.
Few published estimates are available of Bt endotoxin
expression levels in contemporary corn cultivars. Nguyen
et al. projected that a hectare of Bt-corn for CRW control
expressing the Cry3Bb1 gene in MON88017 corn pro-
duces 905 grams of Cry3Bb1 per hectare (0.8 pounds per
acre) [46]. The amount of Bt Cry proteins produced by a
hectare of Bt corn for ECB and CRW control are calcu-
lated in [Additional file 1: Tables S20S22], with key
results shown in Table 2 for specific corn events, traits,
and endotoxins. [Additional file 1 Tables S2325] cover Bt
cotton events. Expression level data reported by compan-
ies in regulatory documents were used to calculate per
hectare production of specific endotoxins. [Additional file
1: Tables S21 and Table S24 contain the expression level
data for Bt corn and cotton events, and [Additional file 1:
Table S22 and Table S25] report the volumes of Bt Cry
proteins produced per hectare and acre based on contem-
porary seeding rates.
Major contemporary Bt corn events targeting the ECB
synthesize nearly as much or more insecticidal Cry protein
per hectare than the weighted-average rate of conventional
Table 2 Bt cry protein synthesis in major GE corn cultivars
Cry
Protein
Cry/Shoot Cry/Root Cry/Plant Plants
per
hectare
Cry Toxin Plants
per
Acre
Cry Toxin
kg /ha lb/acre
MON 810 Cry1Ab 1193 496 1689 79,040 0.133 32,000 0.119
MON 88017 Cry3Bb1 14915 4030 18945 79,040 1.497 32,000 1.333
MON 89034 Cry1A.105 2826 620 3446 79,040 0.272 32,000 0.242
MON 89034 Cry2Ab2 4553 496 5049 79,040 0.399 32,000 0.355
TC 1507 Cry1F 1207 165 1372 79,040 0.108 32,000 0.097
DAS 59122 Cry34Ab1 26376 2647 29023 79,040 2.294 32,000 2.042
DAS 59122 Cr35Ab1 5825 567 6392 79,040 0.505 32,000 0.45
SmartStax Corn
MON 88017 Cry3Bb1 7536 2015 9551 79,040 0.755 32,000 0.672
MON 89034 Cry1A.105 2983 651 3634 79,040 0.287 32,000 0.256
MON 89034 Cry2Ab2 4553 558 5111 79,040 0.404 32,000 0.36
TC 1507 Cry1F 1413 185 1598 79,040 0.126 32,000 0.112
DAS 59122 Cry34Ab1 24649 2623 27272 79,040 2.156 32,000 1.918
DAS 59122 Cr35Ab1 5275 586 5861 79,040 0.463 32,000 0.412
SmartStax Total 4.191 3.73
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insecticides applied on a hectare planted to Bt corn for
ECB control (about 0.15 kgs insecticide per ha; 0.13
pounds/acre in 2010 [Additional file 1: Table S11]).
MON810, the Cry protein in Monsantos original Yield-
gard corn, expresses 0.2 kgs/ha of endotoxin, whereas Syn-
gentasBt 11 synthesizes 0.28 kgs/ha [Additional file 1:
Table S22]. Newer events for ECB control like Monsantos
Genuity VT Double PRO (MON 89034) produce Cry
1A.105 and Cry 2Ab2 endotoxins totaling 0.62 kgs/ha.
The Dow AgroSciences-Pioneer Hi-Bred Herculex I
(TC1507) event expresses the least endotoxin 0.1 kg Bt
endotoxin per hectare just below the rate of insecticides
applied.
In the case of Bt corn targeting the CRW, every hectare
planted in recent years expresses substantially greater
volumes of Bt endotoxins than the ~0.2 kgs of insecticides
applied on the average hectare for CRW control (0.19
pounds/acre [Additional file 1: Table S12]). MON 88017
expresses 0.62 kgs/ha of Cry 3Bb1, while DAS 591227
expresses two Cry proteins totaling 2.8 kgs/ha, 14-fold
more than the insecticides displaced [Additional file 1:
Table S22]. SmartStax GE corn synthesizes six Cry pro-
teins, three targeting the ECB, and three the CRW. Total
Cry protein production is estimated at 4.2 kgs/ha (3.7
pounds/acre), 19-times the average conventional insecti-
cide rate of application in 2010.
Should Bt endotoxins count as insecticides applied?
Entomologists are divided on the question of whether the
Bt produced by transgenic plants should be counted as
insecticides applied.The case for doing so is strong,
despite the obvious differences in how Cry proteins enter
corn agroecosystems. When a field of corn is sprayed with
a foliar Bt insecticide, the amount of toxin sprayed per
hectare should be counted when computing total insecti-
cide use. The primary difference between the Bt Cry
proteins in a Bt-transgenic plant, and a field of non-GE
plants sprayed with foliar Bt, is that in the later case, the
toxin is present predominantly on plant tissue surfaces,
whereas in the former Bt-crop case, the toxin is inside
plant cells. This distinction does not greatly matter from
the perspective of the overall load of pesticides in the en-
vironment, although the presence of pesticides inside
plants, as opposed to on their surface, alters relative risk
profiles across non-target organisms.
It should also be noted that, in general, the systemic
delivery of Bt Cry proteins poses more significant risks to
animals and humans ingesting Bt crops than applications
of Bt insecticides via liquid sprays. Systemic delivery also
enhances a range of environmental and ecological risks
[47] compared to foliar Bt use patterns that result in rapid
breakdown of Bt Cry proteins as they are exposed to
sunlight and rainfall.
Most corn insecticides are applied in ways that expose
active ingredients to destructive abiotic and biotic forces
that tend to break down the chemicals to generally less
toxic forms. Granular soil insecticides applied via boxes
on corn planters tend to break down within weeks as a
result of soil microbial activity. Because properly applied
granular insecticides are buried in the soil, exposure to
non-target organisms is limited, although poorly operated
or calibrated planting equipment can result in grains of
insecticide remaining on the soil surface, posing a serious
potential risk to some bird species. A significant portion
of the foliar insecticides applied per hectare for ECB
control never hit its plant target, and a portion of the
insecticide that does land and lodge on plant tissues is
washed off within hours, days, or weeks during rainfall
events. This is why insecticide residues are rarely detected
in corn grain and silage at harvest time, and why conven-
tional insecticide applications on corn pose little or no
human dietary risk.
By virtue of their altered environmental fate and risk pro-
file, all systemic pesticides should be counted when meas-
uring pesticide use, and hence so too should the Bt
proteins manufactured in Bt-transgenic crops. If Bt-trans-
genic plants produced proteins that disrupted insect
morphology,feedingbehavior,orreproduction,theab-
senceofatoxicmodeofactionwouldstrengthentheargu-
ment that Bt Cry proteins are not functionally equivalent
to insecticides, and hence should not be counted as insecti-
cides applied. Bt-crop technology that limits Bt-endotoxin
expression to only those tissues that are under active at-
tack, and then only during times when insects are actively
feeding, would also support the view that Bt crops are
compatible with IPM.
Conclusions
Todays pest-management related GE traits have proven
popular and commercially profitable for the biotech-
seed industry, but over-reliance has set the stage for
resistance-driven problems in both herbicide-resistant
and Bt-transgenic crops. Largely because of the spread
of glyphosate-resistant weeds, HR crop technology has
led to a 239 million kg (527 million pound) increase in
herbicide use across the three major GE-HR crops, com-
pared to what herbicide use would likely have been in
the absence of HR crops. Well-documented increases in
glyphosate applications per hectare of HR crop account
for the majority of this 239 million kg increase.
While Bt corn and cotton have reduced insecticide
applications by 56 million kgs (123 million pounds), re-
sistance is emerging in key target insects and substantial
volumes of Bt Cry endotoxins are produced per hectare
planted [corn, Additional file 1: Tables S20S22, cotton,
Additional file 1: Tables S23S25], generally dwarfing
the volumes of insecticides displaced. Documenting the
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full range of impacts on the environment and public
health associated with the Bt Cry proteins biosynthesized
inside Bt-transgenic plants remains a challenging and
largely ignored task, especially given the recent move to-
ward multiple Bt protein, stacked-trait events.
Overall, since the introduction of GE crops, the six major
GE technologies have increased pesticide use by an esti-
mated 183 million kgs (404 million pounds), or about 7%.
ThespreadofGRweedsisboundtotriggerfurther
increases, e.g., the volume of 2,4-D sprayed on corn could
increase 2.2 kgs/ha by 2019 (1.9 pounds/acre) if the
USDA approves unrestricted planting of 2,4-D HR
corn [Additional file 1: Table S19]. The increase in her-
bicides applied on HR hectares has dwarfed the reduction
in insecticide use over the 16 years, and will almost surely
continue to do so for several more years.
Estimating the impacts of GE crops on pesticide use is
growing more complex because of gaps in NASS pesticide
use data collection for the three major crops, increases in
the average number of traits per GE-crop hectare planted,
the registration of HR crops engineered to resist herbi-
cides other than glyphosate, massive disruption in weed
communities, and the presence of one to three, or even
more, glyphosate-resistant weeds in many crop fields. It is
difficult to project what the distribution, population levels,
and phenotypes of weeds would have been over the last
16 years in the absence of HR technology. Inevitably, weed
management systems and technology would have evolved
along other trajectories in the absence of HR crops these
last 16 years, resulting in heightened reliance on both pre-
plant and post-emergence applications of multiple, low-
dose herbicides.
A majority of American soybean, maize, and cotton
farmers are either on, or perilously close to a costly herbi-
cide and insecticide treadmill. Farmers lack options and
may soon be advised, out of necessity, to purchase HR
crop cultivars resistant to multiple active ingredients and
to treat Bt corn with once-displaced corn insecticides. The
seed-pesticide industry is enjoying record sales and profits,
and the spread of resistant weeds and insects opens up
new profit opportunities in the context of the seed indus-
trys current business model. Regulators cannot restrict
the use of a previously approved HR technology because it
increases pesticide use and triggers resistance, nor have
U.S. government agencies turned down an application for
anewHRorBt-transgenic trait because of the likelihood
it would accelerate the spread of resistant weeds or
insects. Whether the USDA has the statutory authority to
deny a petition for HR crop deregulation (i.e., approval)
on the grounds of worsening problems with resistant
weeds is a contested issue in ongoing litigation.
Profound weed management system changes will be
necessary in the three major GE crops to first stabilize,
and then hopefully reduce herbicide use, the costs of weed
management, and herbicide-related impacts on human
health and the environment. Weed management experts
are largely in agreement that the percent of cropland area
planted to glyphosate-based HR seeds must decline
dramatically (e.g., by at least one-third to one-half) for
farmers to have a realistic chance at success in preventing
resistance [10,12,14]. Unfortunately, there appears little
interest across the seed-biotech industry in increasing pro-
duction of non-Roundup Ready or not-Bt transgenic seed.
Since the decisions made by the seed industry in any given
year determine the traits offered by the industry to farmers
in next crop season, the seed industry must act first in
order for farmers to turn the corner toward more sustain-
able weed and insect pest management systems. The many
important ramifications of this practical reality that the
seed industry must act first have yet to be fully appre-
ciated by farmers, weed management experts, and policy
makers in the U.S.
Regulators in the U.S. have thus far done little to pre-
vent the emergence and spread of resistant weeds, while
several resistance-management interventions have been
imposed as part of the approval of Bt crops. In addres-
sing weed resistance, the hands-off regulatory posture in
the U.S. reflects, in part, the basic authorities granted to
the EPA and USDA in federal law. Both agencies regard
weed resistance as an efficacy-economics challenge that
can best be addressed by the private sector consistent
with market forces. The need for novel policy interven-
tions will grow in step with the emergence and spread of
resistance weeds and evidence of adverse economic, en-
vironmental, and public health consequences triggered
by markedly increasing reliance on older, higher-risk
herbicides.
Methods
The model calculates the impact of HR and Bt-trans-
genic crop varieties on pesticide use annually from 1996
through 2011, and aggregates results over this 16-year
period. The model is composed of 16 tables [Additional
file 1: Tables S1S16]. Nine additional tables, [Additional
file 1: Tables S17S25] address changes in pesticide use,
the spread of resistant weeds, and the quantity of Bt
endotoxins produced per hectare by todays major corn
and cotton Bt traits.
The model was developed using the units of measure
typical in USDA-NASS surveys (pounds of active ingre-
dients, acres planted); the Additional files are available
in pounds and acres units only. In this paper, metric
units are used to report results, although selected key
results will be reported in both units of measure.
[Additional file 1: Table S1] records average per acre
herbicide and insecticide use data, drawing on pesticide
use data compiled annually by the USDAs NASS. These
surveys record the percent of crop acres treated with
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specific active ingredients, average one-time rates of ap-
plication, the average number of applications, the rate
per crop year (average rate multiplied by the average
number of applications), and total pounds applied.
In the case of herbicides, [Additional file 1: Table S1]
reports total herbicide, all glyphosate, and Total Herbi-
cides Minus Glyphosate.”“All Glyphosateaggregates the
multiple chemical forms of glyphosate surveyed by NASS,
and calculates average rates of application and number of
applications, weighted by frequency of use. The same pro-
cedure is used to calculate average pounds/acre applied of
other herbicides of interest for which NASS reports use
data for multiple chemical forms (e.g. 2,4-D, dicamba).
[Additional file 1: Table S2] includes national acres planted
to each crop, average pesticide use rates, and total pounds
applied per acre and overall herbicide, insecticide, and
herbicide + insecticide volumes applied.
[Additional file 1: Tables S3S6] record the percent of
national acres planted to a crop variety expressing each
of the six, major commercial GE traits. The USDAsERS
provides data on the percent of total national corn
[Additional file 1: Table S3], soybean [Additional file 1:
Table S4], and cotton hectares [Additional file 1: Table
S5] that were planted to each GE crop trait for 1996
2011. Percent acres planted to all six GE traits by year
are presented in [Additional file 1: Table S6]; there is a
high level of confidence in these data.
[Additional file 1: Table S7] reports acres planted to
each of the six traits, multiplying the percent acres
planted to each trait in ST 6 by total acres planted to
each crop in [Additional file 1: Table S2]. [Additional file
1: Tables S8S10] calculate, for the three HR crops, the
estimated difference in average herbicide use on HR hec-
tares versus land planted to conventional, non-GE
varieties. [Additional file 1: Tables S11S13] report the
basis for calculating the pounds of insecticides displaced
by the planting of Bt corn and cotton traits. [Additional
file 1: Table S14] integrates all of the average per acre
pesticide use rates by crop, trait and year, and reports
the estimated difference between per acre rates on GE
versus non-GE acres. [Additional file 1: Table S15] con-
verts the differences in rates per acre to differences in
pounds applied nationally by crop, trait, and year, and
over the 16-year period. [Additional file 1: Table S16]
provides details on glyphosate use from NASS surveys
over the 19962010 period, and is the source of data on
glyphosate use in other Additional files.
Assumptions, projections, and calculations
A series of assumptions, projections, and calculations are
embedded in the model in order to estimate total herbi-
cide and insecticide use on GE versus not-GE hectares.
Table 3 outlines model assumptions and Table 4 describes
the projections embedded in the models calculations.
NASS surveyed corn, soybean, and cotton pesticide
use in most years from 19962010. None of the crops
were surveyed in 2008; cotton was last surveyed in 2007
and 2010; corn was surveyed in 2005 and 2010; and soy-
beans have not been surveyed since 2006. In estimating
the impacts of GE crops on pesticide use from 1996
2011, average application rates per crop year were inter-
polated in years with no data, when NASS had surveyed
a previous and subsequent year, based on the assump-
tion of linear change in the intervening years.
It is assumed that changes in the volume of herbicides
other than glyphosate applied on the average HR hectare
tracks changes in total herbicide use, and also changes
gradually from year-to-year. With few exceptions, these
Table 3 Data sources and assumptions required to quantify the impact of GE crops on pesticide use in the U.S., 1996-
2011
Parameter Source Supplemental
table impacted
Basis and explanation
National Pesticide Use per Acre/
Hectare
NASS-USDA 1, 2 Best publicly available estimates of annual per acre herbicide
and insecticide use
Annual Gaps in NASS Survey
Data by Crop
Interpolated 1, 2 Changes in total herbicide, glyphosate, and insecticide use
occur linearly/annum when there are gaps in NASS pesticide
use surveys
Annual Application Rates of
"Other Herbicides on HR
Hectares"
(See Table 4) 8, 9, 10 Trends by crop on HR acres track changes in total herbicide use,
as reported by NASS; changes from year to year are gradual
Bt Cry Proteins Produced by Bt
Corn and Cotton Plants
Projected (see text,
Additional files)
20-25 Trait-specific expression levels by tissue taken from documents
submitted by technology developers; used to quantify
volume of each Bt endotoxin produced by plants per acre/hectare
based on typical planting density
Insecticide Use on Bt Corn (Details in Table 4) 11, 12 Insecticide displacement as a result of planting Bt corn corrected
for hectares not likely to have been treated in the absence of
Bt corn cultivars
Insecticide Use on Bt Cotton NASS-USDA 13 Budworm/bollworm control insecticide displacement on
hectares planted to Bt cotton is 100%
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patterns of change in herbicide use are evident in all crops
surveyed by USDA. Significant annual changes in total
herbicide use, as well as non-glyphosate applications, are
almost always linked to an increase or decrease in acres
treated with one or more relatively high-dose herbicides
applied at or around 1 pound/acre, compared to use of
herbicides applied at rates less than 0.5 pound/acre (sev-
eral are sprayed at rates below 0.05 pounds/acre).
The volumes of Bt Cry endotoxins produced per acre/
hectare of Bt corn and cotton are not included in the
estimates of changes in insecticide use on acres/hectares
planted to Bt cultivars, although the volumes are surpris-
ingly significant compared to the volume of insecticides
applied on treated acres/hectares (see Discussion). In the
case of insecticide use on Bt corn, the volume of insecti-
cide use displaced per acre/hectare is adjusted in light of
the likely percent of Bt corn acres/hectares that would
have been treated with an insecticide in the absence of Bt
cultivars. Multiple analysts have reported substantial
planting of Bt corn as insurance against possible insect
feeding damage, on acres/hectares that farmers would not
prophylactically apply insecticides [4,13]. In a January
2010 survey, 73.3% of 518 farmers surveyed at regional
extension meetings in Illinois reported that they planted
Bt corn Knowing That Anticipated Damage Levels Were
Low[48]. USDA has surveyed corn insecticide use 14
times since 1991. The total area treated with an insecticide
has fallen in the range 31% +/5% in all years, with the
average around 33%.
It is assumed that farmers planting Bt cotton do not spray
conventional insecticides against the budworm/bollworm
complex of insecticides, leading to 100% displacement of
such applications. This assumption likely overestimates
displacement marginally, especially in recent years where
isolated populations of less susceptible or resistant popula-
tions have emerged.
Table 3 describes the basis for projecting a number of
missing values over the 1996-2011-time period. In the
years since the last NASS survey, pesticide rates were
projected based on recent trends and changes in weed
pressure.
In the case of corn, total herbicide and glyphosate use
trends from 20052010 are projected to continue un-
changed through 2011, despite the accelerating emer-
gence and spread of resistant weeds in the Midwest. The
rapid rate of increase in total herbicide and glyphosate
use/acre in soybean production systems from 2000
2006 (5.9% and 8.9%/annum) is projected to decline to
an average increase of 3.2% and 3.3% per annum in
20072011. Reductions in annual rates of increase re-
flect the decision by many HR soybean farmers to follow
the advice of weed management specialists [10,11] to di-
versity the modes of action included in herbicide-based
control programs. The rate of increase in total herbicide
use on HR cotton from 2010 to 2011 is projected at
about twice the annual rate, 20072010, whereas the
rate of decline in per hectare glyphosate use is projected
to fall from 3.4% to 1% per annum as farmers increase
rates and/or frequency of applications of glyphosate in
regions where resistant weeds are now posing serious
management challenges.
Estimating herbicide use on conventional and HR
hectares
NASS surveys do not report pesticide use on GE and
conventional crop hectares separately.
The volume of herbicides applied to HR hectares can be
approximated by adding NASS-reported glyphosate use
Table 4 Projections required quantifying the impact of GE crops on insecticide use in the US, 19962011
Parameter Supplemental
table(s)
impacted
Basis for setting value Basis and explanation
Corn
Share of Insecticide Applications
Targeting the European Corn Borer
(ECB) Versus Corn Rootworm (CRW)
11, 12 Guidance from extension IPM
specialists and land grant
university spray guides
Some insecticides applied exclusively for control of ECB,
others for control of CRW; and some target both. The
percent hectares treated with a given insecticide are
apportioned relative to target pests: ECB, CRW, or other
insects.
Other InsecticidesApplied in 2010 for
ECB Control
11 NASS data on Other
Insecticidesapplied in 2010
NASS reported 237,000 pounds of Other Insecticideuse
in 2010; 30% of these Other Insecticidesapplied to corn
in 2010 projected to target the ECB.
Other InsecticidesApplied in 2010 for
CRW Control
12 NASS data on Other
Insecticidesapplied in 2010
NASS reported 237,000 pounds of Other Insecticideuse
in 2010; 60% of Other Insecticidesapplied to corn in
2010 projected to target the CRW.
Cotton
Share of Insecticide Applications
Targeting the Budworm/Bollworm
Complex
13 Guidance from extension IPM
specialists and land grant
university spray guides
Some insecticides applied exclusively or partly for control
of the budworm/bollworm complex, others for other
insects; percent hectares treated with a given insecticide
is apportioned relative to target insects.
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per crop year to an estimate of the volume of herbicides
other than glyphosate (hereafter, other herbicides)ap-
plied on HR hectares. The volume of other herbicides
applied on HR hectares is estimated based on the average
number of non-glyphosate herbicides applied per hectare,
coupled with the average rate per application of non-
glyphosate herbicides. In addition, the rate of other herbi-
cideson HR hectares is adjusted to reflect changes from
year to year in overall herbicide use and glyphosate appli-
cation rates. For example in recent years, other herbi-
cideshave been applied to around one-half of HR
soybean hectares at an average rate of ~0.34 kgs/ha (~0.3
pounds/acre), resulting in an average ~0.17 kgs/ha (~0.15
pounds/acre) of other herbicideapplications on all HR
hectares (0.5 × 0.34).
The shares of total crop hectares in a given year planted
to conventional and HR crop varieties is compiled by the
USDAs ERS [Additional file 1: Tables S3S5] and can be
used in a weighted-average formula to calculate the kgs of
herbicides applied on non-HR hectares
THA Cropx¼%HPHTx
ðÞxHAHT
x
ðÞ½
þ%HPCONx
ðÞxHACON
x
ðÞ½
Where,
THA Crop
x
=Total Herbicides Applied(kgs active
ingredient/hectare in a crop year);
% HPHT
x
= Percent national Hectares Planted to HR
cultivars;
HAHT
x
=Herbicides Applied on HRhectares (kg a.
i./crop year);
% HPCON
x
= Percent national Hectares Planted to
Conventionalnon-HR hectares; and
HACON
x
=Herbicides Applied on Conventional
hectares (kgs a.i./crop year).
The first four of the above-five variables are reported or
can be derived from USDA data; the fifth can be calcu-
lated by solving the above equation for HACON
x
.For
each HR crop and year combination, the impact of HR
cultivars on average herbicide use is calculated by sub-
tracting HAHT
x
from HACON
x
. This difference is then
multiplied by the HR hectares planted, to calculate the im-
pact of HR crops on herbicide use in a given year.
Increases or decreases in the volume of herbicides applied
as a result of the planting of HR crops are then aggregated
across all years (19962011) and the three HR crops.
In the case of Bt transgenic corn, the average rate of ap-
plication of insecticides targeting the ECB and the CRW
must be calculated. This process is complicated by the fact
that several insecticides are applied for control of the ECB
and CRW, as well as other insects. Pesticide labels, treat-
ment recommendations in university spray guides, and
experts in corn Integrated Pest Management (IPM) were
consulted in carrying out this step [Additional file 1:
Tables S11, S12].
Average rates of insecticide application across all corn
hectares treated per crop year are then calculated, weighted
by portions of total hectare treatments. This weighted-
average rate of insecticide application on hectares treated
for ECB control declines from 0.24 kgs/ha (0.21 pounds/
acre) of active ingredient in 1996 to 0.15 kgs/ha (0.13
pounds/acre) in 2010. In the case of CRW insecticides, the
rate falls from 0.76 kgs/ha in 1996 to 0.2 kgs/ha in 2010.
The next step in calculating the pounds of insecticides
displaced by the planting of Bt corn is to estimate the por-
tion of hectares planted to Bt corn for ECB and/or CRW
control that would have been treated with an insecticide if
the corresponding Bt crop had not been planted. Doing so
requires a set of assumptions and projections.
Historically, USDA data shows that before the advent of
Bt corn, 10% +/3% of national corn hectares were trea-
ted for ECB control, while 27% +/4% were treated for
CRW control. Yet by 1998 (third year of commercial
sales), 19% of corn hectares were planted to a Bt cultivar
targeting the ECB about double the historic share of
hectares treated with an insecticide for this pest. Today,
close to two-thirds of corn hectares are planted to Bt for
ECB cultivars, some six-times the historic rate. In the case
of Bt corn for CRW, by the fifth year of commercial sales,
2007, the share of corn hectares planted to CRW hybrids
was 25.6%, roughly equaling the historic share of hectares
treated with CRW insecticides (27% +/4%). In 2011,
60% of corn hectares were planted to a CRW hybrid,
double the historic share of corn hectares treated with a
CRW insecticide.
The impact of Bt corn on the volume of insecticide dis-
placed per hectare should be adjusted downward to ac-
count for hectares that would, in all likelihood, not have
been treated. In the case of Bt corn targeting the ECB, the
likely share of hectares planted to Bt corn that would have
been sprayed for ECB control begins at 90% in 1997, the
first year of commercial planting, and drops incrementally
to 45% in 2007.
This percent is left unchanged from 20082010, despite
the increase in corn hectares planted to Bt corn for ECB
from 49% to 65%, because of reported increases in insect
pest pressure in major corn producing regions [49]. The
result is the projection that in 2011, insecticide applica-
tions were displaced on 10.9 million hectares of corn (27
million acres) planted to Bt hybrids for ECB control (45%
of the 65% of corn hectares planted to Bt for ECB
hybrids). These 10.9-million hectares are 29% of total corn
hectares planted, and is about three-times the historic
level of insecticide applications for ECB control.
In the case of Bt corn for CRW control, the percent of
hectares planted that displaces insecticide use begins at
95% in 2003, the first year of commercial sales, and
Benbrook Environmental Sciences Europe 2012, 24:24 Page 11 of 13
http://www.enveurope.com/content/24/1/24
declines to 55% in 2011. In 2011, 57% of corn hectares
were planted to a Bt CRW hybrid, and hence Bt corn for
CRW displaced insecticide use on 31% of national hec-
tares planted. This estimate assumes that any hectare
planted to a Bt corn for CRW control was not also treated
with a CRW insecticide. In addition, 9.4% of corn hectares
were sprayed for CRW control with an insecticide. Ac-
cordingly, about 40% of corn hectares were either sprayed
for the CRW or planted to a Bt variety for CRW control,
well above the 27% +/4% level treated with insecticide
over the last 20 years.
The historically high, projected level of CRW treatment
is justified, in part, by the emergence in the late 1990s of a
variant of the CRW that learned to overwinter in soybean
fields, thus undermining the efficacy of corn-soybean rota-
tions in reducing CRW populations [50]. Recent, historic-
ally high corn prices have also increased the frequency of
continuous corn, a management factor that surely has
increased CRW pressure.
Bt cotton targets the budworm/bollworm complex, but
does not affect other insect pests, including the boll wee-
vil, plant bugs, white flies, and stinkbugs. Applications of
broad-spectrum insecticides are typically made on essen-
tially 100% of planted cotton hectares to control the bud-
worm/bollworm complex and other insects. Bt cotton will
reduce the use of insecticides on the budworm/bollworm
complex, but will only indirectly impact applications of
insecticides targeting other insects.
[Additional file 1: ST 13] reports the basis for estimat-
ing the pounds of insecticides displaced by each acre
planted to Bt cotton. University insect management guides
and experts were consulted to estimate the portion of hec-
tares treated with each cotton insecticide that targeted the
budworm/bollworm complex, versus other insects. The
number of acres treated with each insecticide is calculated
from NASS data, as well as the share of total acres treated.
Average insecticide use rates are then calculated, weighted
by each active ingredients share of insecticide acre treat-
ments targeting the budworm/bollworm complex. The
weighted average cotton insecticide application rate falls
modestly from 0.46 kgs/ha (0.41 pounds/acre) in 1997 to
0.27 kgs/ha (0.24 pounds/acre) in 20102011.
Table 4 summarizes the basis for projections required to
estimate the volume of insecticide use displaced by the
planting of a hectare to Bt corn or cotton cultivars.
Additional file
Additional file 1: The projection model used is composed of a
series of linked worksheets in a Microsoft Excel workbook. Each
table within the workbook appears below in pdf as sequentially
numbered Additional file 1: Table S1 (e.g., ST 1). The pesticide use data
incorporated in the model were originally reported by U.S. government
agencies in pounds of active ingredient, and/or pounds of a.i./acre, and
so these units are used throughout the Additional files to report data on
herbicide use. Convert pounds to kgs by multiplying by 0.454; to convert
pounds/acre to kg/ha, multiply by 1.12.
Abbreviations
AI: Active ingredient; Bt: Bacillus thuringiensis; CRW: Corn rootworm;
ECB: European corn borer; EPSPS: Enolpyruvylshikimate-3-phosphate
synthase; EPA: Environmental Protection Agency; ERS: Economic Research
Service; GE: Genetically engineered, genetic engineering; GR: Glyphosate
resistant; ha: Hectare; HR: Herbicide Tolerant; IPM: Integrated Pest
Management; kgs: Kilograms; NASS: National Agricultural Statistics Service;
NCFAP: National Center for Food and Agriculture Policy; RR: Roundup Ready;
SI: International System of Units; ST: Supplemental Table; THA: Total hectares;
US: United States; USDA: United States Department of Agriculture;
WSSA: Weed Science Society of America.
Competing interests
The author declares he has no competing interests.
Author contribution
Charles Benbrook (CB) developed the model, carried out the analysis, and
wrote the paper. The author read and approved the final manuscript.
Author information
CB is a Research Professor, Center for Sustaining Agriculture and Natural
Resources, Washington State University, Pullman, Washington, USA. CB has
studied the impacts of agricultural biotechnology since the mid-1980s in a
variety of positions including Executive Director, Board on Agriculture,
National Academy of Sciences/National Research Council, and as Chief
Scientist, The Organic Center.
Acknowledgements
Thanks to the analysts in the U.S. Department of Agricultures (USDA)
National Agricultural Statistics Service and the Economic Research Service
(ERS) for compiling the data essential to carry out this work. Dr. Merritt
Padgitt of the ERS (retired) carried out a special tabulation of USDA survey
data on soybean pesticide use that was used to calibrate the model.
Valuable assistance was provided in developing and refining the model and
underlying dataset by Karen Benbrook and Karie Knoke. Dr. Margaret Mellon,
Dr. Jane Rissler, and Dr. Doug Gurian-Sherman of the Union of Concerned
Scientists (UCS) contributed to the conceptual development of the model.
Mr. Bill Freese, Center for Food Safety, provided helpful suggestions and data
on resistant weeds. Dr. Robert Kremer, Dr. Michael Gray, Dr. Matt Liebman,
and Dr. Michael Owen are among the land grant pest management
scientists that provided guidance as the model was developed. Funding to
support the development of the model was provided by the Institute for
Agriculture and Trade Policy, Consumers Union, UCS, and The Organic
Center.
Received: 28 June 2012 Accepted: 3 September 2012
Published: 28 September 2012
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doi:10.1186/2190-4715-24-24
Cite this article as: Benbrook: Impacts of genetically engineered crops
on pesticide use in the U.S. the first sixteen years. Environmental
Sciences Europe 2012 24:24.
Benbrook Environmental Sciences Europe 2012, 24:24 Page 13 of 13
http://www.enveurope.com/content/24/1/24
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Glyphosate (N-phosphonomethyl-glycine) is the active ingredient in the nonselective herbicide Roundup. The sensitivity of crop plants to glyphosate has limited its in-season use as a postemergence herbicide. The extension of the use of Roundup herbicide to allow in-season application in major crops such as soybeans [Glycine max (L.) Merr.] would provide new weed control options for farmers. A glyphosate-tolerant soybean line, 40-3-2, was obtained through expression of the bacterial 5-enolpyruvylshikimate-3-phosphate synthase (EPSP synthase, EPSPS) enzyme from Agrobacterium sp. strain CP4. Line 40-3-2 is highly tolerant to glyphosate, showing no visual injury after application of up to 1.68 kg acid equivalent (a.e.) ha -1 of glyphosate under field conditions. Molecular characterization studies determined that the single genetic insert in line 40-3-2 contains only a portion of the cauliflower mosaic virus 35S promoter (P-E35S), the Petunia hybrida EPSPS chloroplast transit peptide (CTP), the CP4 EPSPS gene, and a portion of the 3' nontranslated region of the nopaline synthase gene (NOS 3') terminator. Inheritance studies have shown that the transgene behaves as a single dominant gene and is stable over several generations.
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The 1995/6 International Survey of Herbicide-Resistant Weeds recorded 183 herbicide-resistant weed biotypes (124 different species) in 42 countries. The increase in the number of new herbicide-resistant weeds has remained relatively constant since 1978, at an average of nine new cases per year worldwide. Whilst 61 weed species have evolved resistance to triazine herbicides, this figure now only accounts for one-third of all documented herbicide-resistant biotypes. Triazine-resistant weeds have been controlled successfully in many countries by the use of alternative herbicides. Due to the economic importance of ALS and ACCase inhibitor herbicides worldwide, and the ease with which weeds have evolved resistance to them, it is likely that ALS and ACCase inhibitor-resistant weeds will present farmers with greater problems in the next five years than triazine-resistant weeds have caused in the past 25 years. Thirty-three weed species have evolved resistance to ALS-inhibitor herbicides in 11 countries. ALS-inhibitor-resistant weeds are most problematic in cereal, corn/soybean and rice production. Thirteen weed species have evolved resistance to ACCase inhibitors, also in 11 countries. ACCase inhibitor resistance in Lolium and Avena spp. threatens cereal production in Australia, Canada, Chile, France, South Africa, Spain, the United Kingdom and the USA. Fourteen weed species have evolved resistance to urea herbicides. Isoproturon-resistant Phalaris minor infesting wheat fields in North West India and chlorotoluron-resistant Alopecurus myosuroides in Europe are of significant economic importance. Although 27 weed species have evolved resistance to bipyridilium herbicides, and 14 weed species have evolved resistance to synthetic auxins, the area infested and the availability of alternative herbicides have kept their impact minimal. The lack of alternative herbicides to control weeds with multiple herbicide resistance, such as Lolium rigidum and Alopecurus myosuroides, makes these the most challenging resistance problems. The recent discovery of glyphosate-resistant Lolium rigidum in Australia is a timely reminder that sound herbicide-resistant management strategies will remain important after the widespread adoption of glyphosate-resistant crops. ©1997 SCI