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Navigating a Critical Juncture for Sustainable Weed Management
Author(s): David A. Mortensen, J. Franklin Egan, Bruce D. Maxwell, Matthew R. Ryan,
Richard G. Smith
Reviewed work(s):
Source:
BioScience,
Vol. 62, No. 1 (January 2012), pp. 75-84
Published by: University of California Press on behalf of the American Institute of Biological Sciences
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www.biosciencemag.org January 2012 / Vol. 62 No. 1 • BioScience 75
Navigating a Critical Juncture for
Sustainable Weed Management
DaviD a. Mortensen, J. Franklin egan, Bruce D. Maxwell, Matthew r. ryan, anD richarD g. sMith
Agricultural weed management has become entrenched in a single tactic—herbicide-resistant crops—and needs greater emphasis on integrated
practices that are sustainable over the long term. In response to the outbreak of glyphosate-resistant weeds, the seed and agrichemical industries
are developing crops that are genetically modified to have combined resistance to glyphosate and synthetic auxin herbicides. This technology will
allow these herbicides to be used over vastly expanded areas and will likely create three interrelated challenges for sustainable weed management.
First, crops with stacked herbicide resistance are likely to increase the severity of resistant weeds. Second, these crops will facilitate a significant
increase in herbicide use, with potential negative consequences for environmental quality. Finally, the short-term fix provided by the new traits
will encourage continued neglect of public research and extension in integrated weed management. Here, we discuss the risks to sustainable
agriculture from the new resistant crops and present alternatives for research and policy.
Keywords: agriculture production, agroecosystems, transgenic organisms, sustainability, biotechnology
the production and dispersal of dormant seeds or vegeta-
tive propagules, weeds are virtually impossible to eliminate
from any given field. The importance of weed management
to successful farming systems is demonstrated by the fact
that herbicides account for the large majority of pesticides
used in agriculture, eclipsing inputs for all other major pest
groups. To no small extent, the success and sustainability of
our weed management systems shapes the success and sus-
tainability of agriculture as a whole.
In the mid-1990s, the commercialization of GM crops
resistant to the herbicide glyphosate (Monsanto’s Roundup
Ready crops) revolutionized agricultural weed management.
Prior to this technology, weed control required a higher
level of skill and knowledge. In order to control weeds
without also harming their crop, farmers had to carefully
select among a range of herbicide active ingredients and
carefully manage the timing of herbicide application while
also integrating other nonchemical control practices. Gly-
phosate is a highly effective broad-spectrum herbicide that
is phytotoxically active on a large number of weed and crop
species across a wide range of taxa (Duke and Powles 2009).
Engineered to express enzymes that are insensitive to or can
metabolize glyphosate, GM glyphosate-resistant crops have
enabled farmers to easily apply this herbicide in soybean,
corn, cotton, canola, sugar beet, and alfalfa and to control
problem weeds without harming the crop (Duke and Powles
2009).
Growers were attracted to the flexibility and simplicity
of the glyphosate and glyposhate-resistant crop technol-
ogy package and adopted the technology at an unprec-
edented rate. After emerging on the market in 1996,
Overreliance on glyphosate herbicide in genetically
modified (GM) glyphosate-resistant cropping systems
has created an outbreak of glyphosate-resistant weeds (Duke
and Powles 2009, NRC 2010). Over recent growing seasons,
the situation became severe enough to motivate hearings in
the US Congress to assess whether additional government
oversight is needed to address the problem of herbicide-
resistant weeds (US House Committee on Oversight and
Government Reform 2010). One of our coauthors (DAM)
delivered expert testimony at these hearings, in which he
expressed the views described in this article. Biotech nology
companies are currently promoting second-generation GM
crops resistant to additional herbicides as a solution to
glyphosate-resistant weed problems. We believe that this
approach will create new resistant-weed challenges, will
increase risks to environmental quality, and will lead to
a decline in the science and practice of integrated weed
management (IWM). The rapid rise in glyphosate-resistant
weeds demonstrates that herbicide-resistant crop biotech-
nology is sustainable only as a component of broader inte-
grated and ecologically based weed management systems.
We argue that new policies are needed to promote integrated
approaches and to check our commitment to an accelerat-
ing transgene-facilitated herbicide treadmill, which has sig-
nificant agronomic and environmental-quality implications
(figure 1).
Effective weed management is critical to maintaining
agricultural productivity. By competing for light, water,
and nutrients, weeds can reduce crop yield and quality and
can lead to billions of dollars in global crop losses annu-
ally. Because of their ability to persist and spread through
BioScience 62: 75–84. ISSN 0006-3568, electronic ISSN 1525-3244. © 2012 by American Institute of Biological Sciences. All rights reserved. Request
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glyphosate-resistant soybeans accounted for 54% of US
hectares by 2000 (Duke and Powles 2009). In 2008, crops
resistant to glyphosate were grown on approximately 96
million hectares (ha) of cropland internationally and
account for 63%, 68%, and 92% of the US corn, cotton, and
soybean hectares, respectively (Duke and Powles 2009). The
technology is effective and easy to use, and farmers have
often responded to these benefits by exclusively planting
glyphosate-resistant cultivars and applying glyphosate her-
bicide in the same fields, year after year (Duke and Powles
2009, NRC 2010).
Unfortunately, this single-tactic approach to weed
management has resulted in unintended—but not
unexpected—problems: a dramatic rise in the number
and extent of weed species resistant to glyphosate (Heap
2011) and a concomitant decline in the effectiveness of
glyphosate as a weed management tool (Duke and Powles
2009, NRC 2010). As the area planted with glyphosate-
resistant crops increased, the total amount of glyphosate
applied kept pace, creating intense selection pressure
for the evolution of resistance. This dramatic increase
in glyphosate use would not have been possible without
glyphosate-resistant crop biotechnology. The number and
extent of weed species resistant to glyphosate has increased
rapidly since 1996, with 21 species now confirmed glob-
ally (Heap 2011). Although several of these species first
appeared in cropping systems where glyphosate was being
used without a resistant cultivar, the most severe outbreaks
have occurred in regions where glyphosate-resistant crops
have facilitated the continued overuse of this herbicide.
The list includes many of the most problematic agronomic
weeds, such as Palmer amaranth (Amaranthus palmeri),
horseweed (Conyza canadensis), and Johnsongrass (Sor-
ghum halepense), several of which infest millions of hect-
ares (Heap 2011).
The next generation of
herbicide-resistant crops
To address the problem of gly-
phosate-resistant weeds, the seed
and agrichemical industries are
developing new GM cultivars of
soybean, cotton, corn, and canola
with resistance to additional her -
bicide chemistries, including
dicamba (Monsanto) and 2,4-D
(2,4-dichlorophenoxyacetic acid;
Dow AgroSciences) (Behrens
MR et al. 2007, Wright et al.
2010). Dicamba and 2,4-D are
both in the synthetic auxin class
of herbicides, which have been
widely used for weed control in
corn, cereals, and pastures for
more than 40 years. These her-
bicides mimic the physiological
effects of auxin-type plant-
growth regulators and can cause abnormal growth and
eventual mortality in a wide variety of broadleaf plant spe-
cies. In addition to species with recently evolved resistance,
several important broadleaf weed species are naturally
tolerant to glyphosate but susceptible to synthetic auxins.
In cropping systems where glyphosate-resistant or -tolerant
weeds are major problems, dicamba and 2,4-D applications
would provide an effective weedmanagement tool. Although
several other transgene–herbicide combinations are cur-
rently in the research and development pipeline (Duke and
Powles 2009), these modes of action already have significant
resistant-weed issues or do not control weeds as effectively
as dicamba or 2,4-D herbicides. Consequently, we expect
that synthetic auxin–resistant cultivars will be embraced
by growers and planted on rapidly increasing areas in the
United States and worldwide over the next 5–10 years.
In addition to their weed management utility, there are
a number of agronomic drivers that may further acceler-
ate the adoption of the new resistant cultivars. First, soy-
bean, c otton, and many other broadleaf crops are naturally
extremely sensitive to synthetic auxin herbicides and show
distinctive injury symptoms when they encounter trace
doses (figure 2; Breeze and West 1987, Al-Khatib and Peter-
son 1999, Everitt and Keeling 2009, Sciumbato et al. 2004).
Most US growers rely on commercial applicators to spray
herbicides, and when susceptible and synthetic auxin–
resistant fields are interspersed, there may be a high proba-
bility for application mistakes in which susceptible fields are
accidentally treated with dicamba or 2,4-D. Second, synthetic
auxins are extremely difficult to clean from spray equip-
ment (Boerboom 2004), and low residual concentrations of
these compounds in equipment could damage susceptible
cultivars. Growers and applicators may need to have equip-
ment dedicated to dicamba or 2,4-D to avoid damage from
residual concentrations. Third, some formulated products of
Figure 1. A conceptual model of the alternative solutions—and their potential
consequences—presently available for addressing glyphosate-resistant weed
problems.
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First, similar arguments were made during the release of
glyphosate-resistant crops. Various industry and university
scientists contended that details of glyphosate’s biochemical
interactions with the plant enzyme EPSPS (5-enolpyru-
vylshikimate-3-phosphate synthase) combined with the
apparent lack of resistant weeds after two decades of previ-
ous glyphosate use indicated that the evolution of resistant
weeds was a negligible possibility (Bradshaw et al. 1997).
Second, it is not the case that “very few” weed species
have evolved resistance to the synthetic auxin herbicides.
Globally, there are 28 species, with 6 resistant to dicamba
specifically, 16 to 2,4-D, and at least 2 resistant to both active
ingredients (table 1). And although many of these species
are not thought to infest large areas or cause significant
economic harm, data on the extent of resistant weeds are
compiled through a passive reporting system, in which area
estimates are voluntarily supplied by local weed scientists
after a resistant-weed problem becomes apparent. Synthetic
auxin–resistant weeds may appear unproblematic because
these species currently occur in cropping systems in which
other herbicide modes of action are used that can effec-
tively mask the extent of the resistant genotypes (Walsh
et al. 2007). Furthermore, the claim that 2,4-D resistance is
unlikely to evolve because of the complex and essential func-
tions that auxins play in plants is unsubstantiated. In many
cases in which resistance has evolved to synthetic auxins,
the biochemical mechanism is unknown. However, in at
least two cases, dicamba-resistant Kochia scoparia (Preston
et al. 2009) and dicamba-resistant Sinapis arvensis (Zheng
and Hall 2001), resistance is conferred by a single dominant
allele, indicating that resistance could develop and spread
quite rapidly (Jasieniuk and Maxwell 1994).
The final dimension of the industry argument is that by
planting cultivars with stacked resistant traits, farmers will
be able to easily use two distinct herbicide modes of action
and prevent the evolution of weeds simultaneously resistant
to both glyphosate and dicamba or 2,4-D. The logic behind
this argument is simple. Because the probability of a muta-
tion conferring target-site resistance to a single-herbicide
mode of action is a very small number (generally estimated
as one resistant mutant per 10–5 to 10–10 individuals [Jasie-
niuk and Maxwell 1994]), and because distinct mutations
are assumed to be independent events, the probability of
multiple target-site resistance to two modes of action is the
product of two very small numbers (i.e., 10–10 to 10–20). For
instance, if the mutation frequency for a glyphosate-resistant
allele in a weed population is 10–9, and the frequency for
a dicamba mutant is also 10–9, the frequency of individu-
als simultaneously carrying both resistant alleles would be
10–18. If the population density of this species is assumed to
be around 100 seedlings per square meter (m2) of cropland
(106 per ha), it would require 1012 ha of cropland to find just
one mutant individual with resistance to both herbicides.
For point of reference, there are only about 15 × 108 ha
of cropland globally. Therefore, even if the weed species
were globally distributed, and all of the world’s crop fields
dicamba and 2,4-D have high volatility (Grover et al. 1972,
Behrens R and Lueschen 1979), and the combination of par-
ticle and vapor drift may generate frequent incidents of sig-
nificant injury or yield loss to susceptible crops. Moreover,
the seed and chemical industries are becoming increasingly
consolidated, making it more difficult for growers to find
high-yielding varieties that do not also contain transgenic
herbicide-resistance traits. Combined, these four agronomic
drivers suggest that once an initial number of growers in a
region adopts the resistant traits, the remaining growers may
be compelled to follow suit in order to reduce the risk of
crop injury and yield loss.
If herbicide-resistant-weed problems are addressed
only with herbicides, evolution will most likely win
Glyphosate-resistant weeds rapidly evolved in response to
the intense selection pressure created by the extensive and
continuous use of glyphosate in resistant crops. Anticipating
the obvious criticism that the new synthetic auxin–resistant
cultivars will enable a similar overuse of these herbicides
and a new outbreak of resistant weeds, scientists affiliated
with Monsanto and Dow have argued that synthetic auxin–
resistant weeds will not be a problem because (a) currently
very few weed species globally have evolved synthetic auxin
resistance, despite decades of use; (b) auxins play complex
and essential roles in the regulation of plant development,
which suggests that multiple independent mutations would
be necessary to confer resistance; and (c) synthetic auxin
herbicides will be used in combination or rotation with
glyphosate, which will require weeds to evolve multiple
resistance traits in order to survive (Behrens MR et al. 2007,
Wright et al. 2010). Although these arguments have been
repeated in several high-profile journals, the authors of
those arguments have conspicuously left out several impor-
tant facts about current patterns in the distribution and
evolution of herbicide-resistant weeds.
Figure 2. Photo of soybean responding to a drift-level
exposure to dicamba herbicide, exhibiting typical
symptoms of cupped-leaf morphology and chlorotic-leaf
margins. Photograph: J. Franklin Egan.
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Table 1. Global diversity and extent of the 28 weed species with resistance to synthetic auxin herbicides.
Year Common name Scientific name Herbicides Location Acres
1952 Wild carrot Daucus carota 2,4-D Ontario <1
1957 Spreading dayflower Commelina diffusa 2,4-D Hawaii No data
1964 Field bindweed Convolvulus arvensis 2,4-D Kansas No data
1975 Scentless chamomile Matricaria perforata 2,4-D France 101–500
1975 Scentless chamomile Matricaria perforata 2,4-D United Kingdom 101–500
1979 Canada thistle Cirsium arvense MCPA Sweden No data
1981 Musk thistle Carduus nutans 2,4-D, MCPA New Zealand 1001–10,000
1983 Gooseweed Sphenoclea zeylanica 2,4-D Philippines 1–5
1985 Canada thistle Cirsium arvense 2,4-D, MCPA Hungary No data
1985 Common chickweed Stellaria media Mecoprop United Kingdom No data
1988 Yellow starthistle Centaurea solstitialis Picloram Washington 1–5
1988 Tall buttercup Ranunculus acris MCPA New Zealand 1001–10,000
1989 Globe Fingerrush Fimbristylis miliacea 2,4-D Malaysia 51–100
1990 Wild mustard Sinapis arvensis 2,4-D, dicamba, dichloprop,
MCPA, mecoprop, picloram
Manitoba 51–100
1993 Wild carrot Daucus carota 2,4-D Michigan 11–50
1993 Corn poppy Papaver rhoeas 2,4-D Spain 10,001–100,000
1994 Wild carrot Daucus carota 2,4-D Ohio 1001–10,000
1995 Kochia Kochia scoparia Dicamba North Dakota 101–500
1995 Kochia Kochia scoparia Dicamba, fluroxypr Montana 1001–10,000
1995 Yellow Burhead Limnocharis flava 2,4-D Indonesia 1001–10,000
1995 Gooseweed Sphenoclea zeylanica 2,4-D Malaysia No data
1996 False cleavers Galium spurium Quinclorac Albera 51–100
1997 Italian thistle Carduus pycnocephalus 2,4-D New Zealand No data
1997 Kochia Kochia scoparia Dicamba Idaho 1–5
1998 Barnyardgrass Echinochloa crus-galli Quinclorac Louisiana 501–1,000
1998 Common hempnettle Galeopsis tetrahit Dicamba, fluroxypr, MCPA Alberta 101–500
1998 Yellow Burhead Limnocharis flava 2,4-D Malaysia 11–50
1999 Barnyardgrass Echinochloa crus-galli Quinclorac Brazil 1–5
1999 Barnyardgrass Echinochloa crus-galli Quinclorac Arkansas 1–5
1999 Gulf cockspur Echinochloa crus-pavonis Quinclorac Brazil 1–5
1999 Wild radish Raphanus raphanistrum 2,4-D Australia 10,001–100,000
1999 Carpet burweed Soliva sessilis Clopyralid, picloram, triclopyr New Zealand 6–10
2000 Junglerice Echinochloa colona Quinclorac Colombia 11–50
2000 Gooseweed Sphenoclea zeylanica 2,4-D Thailand 11–50
2002 Smooth crabgrass Digitaria ischaemum Quinclorac California 11–50
2002 Marshweed Limnophila erecta 2,4-D Malaysia 501–1,000
2005 Common lambsquarters Chenopodium album Dicamba New Zealand 11–50
2005 Indian hedge-mustard Sisymbrium orientale 2,4-D, MCPA Australia 51–100
2006 Wild radish Raphanus raphanistrum 2,4-D, MCPA Australia 1–5
2007 Prickly lettuce Lactuca serriola 2,4-D, dicamba, MCPA Washington 101–500
2008 Wild mustard Sinapis arvensis Dicamba Turkey 101–500
2009 Barnyardgrass Echinochloa crus-galli Quinclorac Brazil No data
Note: Some species have evolved resistance to various synthetic auxin herbicides on multiple independent occasions in different locations. Compiled
from Heap (2011).
2,4-D, 2,4-Dichlorophenoxyacetic acid; MCPA, 2-methyl-4-chlorophenoxyacetic acid.
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were treated with both herbicides, it would appear virtually
impossible to select a single weed seedling exhibiting mul-
tiple resistance.
The problem with this reassuring analysis is that it con-
tradicts recent evidence. Weed species resistant to multiple
herbicide modes of action are becoming more widespread
and diverse (figure 3). There are currently 108 biotypes in
38 weed species across 12 families possessing simultaneous
resistance to two or more modes of action, with 44% of these
having appeared since 2005 (Heap 2011). Common water-
hemp (Amaranthus tuberculatus) simultaneously resistant to
glyphosate, ALS, and PPO herbicides infests 0.5 million ha
of corn and soybean in Missouri (Heap 2011). Rigid ryegrass
(Lolium rigidum) populations resistant to seven distinct
modes of action infest large areas of southern Australia
(Heap 2011). Weeds can defy the probabilities and evolve
multiple resistance through a number of mechanisms.
First, when a herbicide with a new mode of action is
introduced into a region or cropping system in which
weeds resistant to an older mode of action are already
widespread and problematic, the probability of selecting
for multiple target-site resistance is not the product of two
independent, low-probability mutations. In fact, the value
is closer to the simple probability of finding a resistance
mutation to the new mode of action within a population
already extensively resistant to the old mode of action. For
instance, in Tennessee, an estimated 0.8–2 million ha of soy-
bean crops are infested with glyphosate-resistant horseweed
(C. canadensis) (Heap 2011). Assuming seedling densities of
100 per m2 or 106 per ha (Dauer et al. 2007) and a mutation
frequency for synthetic auxin resistance of 10–9, this implies
that next spring, there will be 800–2000 horseweed seedlings
in the infested area that possess combined resistance to gly-
phosate and a synthetic auxin herbicide ((2 × 106 ha infested
with glyphosate resistance) × (106 seedlings per ha) × (1
synthetic auxin–resistant seedling per 109 seedlings) = 2000
multiple-resistant seedlings). In this example, these seedlings
would be located in the very fields where farmers would
most likely want to plant the new stacked glyphosate- and
synthetic auxin–resistant soybean varieties (the fields where
glyphosate-resistant horseweed problems are already acute).
Once glyphosate and synthetic auxin herbicides have been
applied to these fields and have killed the large number of
susceptible genotypes, these few resistant individuals would
have a strong competitive advantage and would be able to
spread and multiply rapidly in the presence of the herbicide
combination.
Second, several weed species have evolved cross-resistance,
in which a metabolic adaptation allows them to degrade
several different herbicide modes of action. Mutations to
cytochrome P450 monooxygenase genes are a common
mechanism for cross-resistance (Powles and Yu 2010). Plant
species typically have a large number of P450 genes (e.g.,
the rice genome contains 458 distinct P450 genes), which
are involved in a variety of metabolic functions, including
the synthesis of plant hormones and the hydrolyzation or
dealkylation of herbicides and other xenobiotics. Weeds
with P450 mediated resistance are widespread and increas-
ingly problematic. For instance, across Europe and Australia,
numerous populations of L. rigidum and Alopecurus myo-
suroides occur with various combinations of P450 resistance
to the ALS-, ACCase-, and photosystem II–inhibitor herbi-
cides (Powles and Yu 2010). Given the diversity and ubiquity
of P450 monoxygenases in plant genomes, it is possible
that in the near future, a weed species could evolve a muta-
tion that enables it to degrade glyphosate and the synthetic
auxins.
Historically, the use of the synthetic auxin herbicides has
been limited to cereals or as preplant applications in broad-
leaf crops. The new transgenes will allow 2,4-D and dicamba
to be applied at higher rates, in new crops, in the same fields
in successive years, and across dramatically expanded areas,
creating intense and consistent selection pressure for the
evolution of resistance. Taken together, the current number
of synthetic auxin–resistant species, the broad distribution
of glyphosate-resistant weeds, and the variety of pathways
by which weeds can evolve multiple resistance suggest that
the potential for synthetic auxin–resistant or combined syn-
thetic auxin– and glyphosate-resistant weeds in transgenic
cropping systems is actually quite high. One hundred nine-
ty-seven weed species have evolved resistance to at least 1 of
14 known herbicide modes of action (Heap 2011), and the
discovery and development of new herbicide active ingredi-
ents has slowed dramatically over recent decades. Given that
herbicides are a cornerstone of modern weed management,
it seems unwise to allow the new GM herbicide-resistant
Figure 3. Global increases in the number of weed
populations since 1980 across 38 species that exhibit
simultaneous resistance to two or more distinct herbicide
modes of action (MOA). Data compiled from Heap 2011.
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crops to needlessly accelerate and exacerbate resistant-weed
evolution.
Increasing herbicide applications and the
consequences for environmental quality
In the early promotions of their new resistant cultivars,
scientists from Dow and Monsanto have been advocating
herbicide programs that combine current rates of glyphosate
with 225–2240 grams (g) per ha of dicamba (Arnevik 2010)
or 560–2240 g per ha of 2,4-D (Olson and Peterson 2011).
Therefore, the technology will not involve a substitution of
herbicide active ingredients but will instead lead to additional
herbicide use. If the rate of adoption of this technology fol-
lows the general trajectory of glyphosate-resistant crops, the
result could be a profound increase in the total amount of
herbicide applied to farmland (figure 4). This trend would
move us in the opposite direction of the reduced chemical
inputs that scientists in sustainable agriculture have long
advocated. As the seed and agrichemical industries move
closer to the commercialization of new resistant traits, it is
worth pausing to ask what the environmental-quality conse-
quences of this increase may be.
Dicamba and 2,4-D have been widely used in agriculture
for over 40 years, and recent US Environmental Protection
Agency (USEPA) reviews have classified both herbicides
as being relatively environmentally benign (USEPA 2005,
2006). Both herbicides have low acute and chronic toxicities
to mammalian, bird, and fish model organisms; degrade
fairly rapidly in the soil; and are not known to bioaccumu-
late. Not surprisingly, however, both dicamba and 2,4-D are
extremely toxic to broadleaf plants. For many terrestrial and
aquatic plant species, the USEPA assessments rank the eco-
toxicological risks for both dicamba and 2,4-D well above
their set levels of concern (USEPA 2005, 2006). In a relative-
risk assessment comparing a suite of 12 herbicides com-
monly used in wheat, Peterson and Hulting (2004) reported
the risk to terrestrial plants for dicamba and 2,4-D as being
75 and 400 times greater than glyphosate, respectively.
All herbicides can have negative impacts on nontarget
vegetation if they drift from the intended areas either as
wind-dispersed particles or as vapors evaporating off of the
application surface. Because of their volatility and effects at
low doses, past experience with injury to susceptible crops
has indicated that the synthetic auxin herbicides may be
especially prone to drift problems (Behrens R and Lueschen
1979, Sciumbato et al. 2004, US House Committee on Over-
sight and Government Reform 2010). Research has shown
that using recommended application equipment (e.g., spray
nozzle types) and applying herbicides under appropriate
weather conditions can reduce particle drift. Modern for-
mulations and chemistries of synthetic auxin products also
can minimize vapor drift. However, growers and commercial
applicators do not always use appropriate or recommended
herbicide application practices, especially if these technolo-
gies are more costly. The new resistant cultivars will enable
growers to apply synthetic auxin herbicides several weeks
later into the growing season, when higher temperatures
may increase volatility and when more varieties of suscep-
tible crops and nontarget vegetation are leafed out, further
increasing the potential for nontarget drift damage.
Plant diversity plays fundamental roles in agroecosystem
sustainability, and major increases in dicamba and 2,4-D
use may negatively affect multiple aspects of this important
resource. First, as was discussed above, herbicide drift or
misapplications could create a strong incentive for growers
to plant resistant seeds as insurance against crop damage
from herbicide drift or applicator mistakes, even if they are
not interested in applying synthetic auxin herbicides them-
selves. This effect could further augment the portion of the
Figure 4. Total herbicide active ingredient applied to
soybean in the United States. The data from 1996 to
2007 are adapted from Figure 2-1 in NRC (2010), and
the projected data are based on herbicide programs
described by Arnevik (2010) and Olson and Peterson
(2011). To forecast herbicide rates from 2008 to 2013 we
assumed that the applications of glyphosate and other
herbicides will remain constant at 2007 levels until 2013,
when new resistant soybean varieties are likely to become
available. We estimated yearly increases in synthetic
auxin herbicides (assumed to drive increases in other
herbicides) by assuming that the adoption of stacked
synthetic auxin–resistant cultivars mirrors the adoption
of glyphosate-resistant cultivars, such that 91% of soybean
hectares are resistant to synthetic auxin herbicides within
12 years. We further assumed that all soybean hectares
with stacked resistance to glyphosate and synthetic auxin
herbicides will receive an annual application of glyphosate
and dicamba or 2,4-D. We assumed that the use rates of
glyphosate will remain at current levels, and our estimates
for dicamba and 2,4-D encompass lower (0.28 kilograms
[kg] per hectare [ha]) and higher (2.24 kg per ha) use
rates, which are in line with the rates currently used on
tolerant crops (i.e., corn and wheat) and with rates being
researched and promoted by Dow and Monsanto.
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profit margins were comparable to those of a conventional
system (Liebman et al. 2008).
The introduction of glyphosate-resistant crops was a key
factor enabling no-till crop production, which increased
from 45 million to 111 million ha worldwide between 1999
and 2009 (Derpsch et al. 2010). Although no-till produc-
tion can provide soil-quality and conservation benefits, it
is dependent on herbicides, and the overreliance on gly-
phosate now threatens its sustainability. Effective IWM
typically involves some tillage, such as interrow cultivation
over a multiyear crop rotation. Despite a common miscon-
ception that tillage is always destructive to soil, a growing
body of cropping systems research has demonstrated that
where limited tillage is balanced in an IWM context with
soil-building practices such as cover-cropping or manure
applications, high levels of soil quality can be maintained.
For example, rotational-tillage systems have recently been
reported to accumulate and store more soil organic mat-
ter than no-till systems (Venterea et al. 2006). Greater soil
carbon and nitrogen were observed in integrated systems
that used tillage, cover crops, and manure than in a conven-
tionally managed no-till system, regardless of whether cover
crops were used in the no-till system (Teasdale et al. 2007).
These results illustrate that soil-quality benefits associated
with no-till systems can also be achieved using IWM that
includes limited tillage.
Recent research has also demonstrated that IWM strate-
gies are effective in managing herbicide-resistant weeds. For
example, glyphosate-resistant horseweed in no-till soybean
can be controlled by integrating cover crops and soil-applied
residual herbicides (Davis VM et al. 2009). In a recent exper-
iment in which the integration of tillage and cover crops
was evaluated for controlling glyphosate-resistant Palmer
amaranth in Georgia, the combination of tillage and rye
cover crops reduced Palmer amaranth emergence by 75%
(Culpepper et al. 2011). In addition to cultivation and cover
crops, other practices can be used to manage resistant-weed
populations. Researchers in Australia suggested two cul-
tural weed management practices for reducing glyphosate-
resistant weed populations: increasing a crop’s competitive
ability through higher seeding rates and preventing seed rain
of resistant weeds by collecting or destroying weed seed at
harvest (Walsh and Powles 2007). Area-wide management
plans in which farmers cooperate to limit the hectares over
which a single herbicide is applied can prevent the spread of
a resistant species across a landscape (Dauer et al. 2009).
Unfortunately, the knowledge infrastructure needed to
practice IWM in the future may be atrophying. Although
seed and chemical companies can generate enormous rev-
enues through the packaged sales of herbicides and trans-
genic seeds, the IWM approaches outlined above are based
on knowledge-intensive practices, not on salable products,
and lack a powerful market mechanism to push them along.
For instance, delaying the planting date one or two weeks
until after a flush of summer annual weeds have germinated
can facilitate the control of these weeds with burndown
seed market and of the landscape garnered by the resistant
seed varieties, which would reduce genotypic diversity and
restrict farmers’ access to different crop varieties. Second, a
large number of agronomic, fruit, and vegetable crops are
susceptible to injury and yield loss from drift-level expo-
sures to these herbicides (figure 2; Breeze and West 1987,
Al-Khatib and Peterson 1999, Everitt and Keeling 2009). In
the past, growers have reported issues with injury from drift
and have recently voiced concerns about the expanded use
of the synthetic auxin herbicides (Behrens R and Lueschen
1979, Boerboom 2004, Sciumbato et al. 2004, US House
Committee on Oversight and Government Reform 2010).
Landscapes dominated by synthetic auxin–resistant crops
may make it challenging to cultivate tomatoes, grapes,
potatoes, and other horticultural crops without the threat
of yield loss from drift. Finally, a growing body of research
has demonstrated that wild plant diversity in uncultivated,
seminatural habitat fragments interspersed among crop
fields helps support ecosystem services valuable to agri-
culture, including pollination and biocontrol (Isaacs et al.
2009). More research is needed in order to understand the
impact that increased synthetic auxin applications may
have on the quality and function of these plant diversity
resources.
IWM: An alternative path forward
Glyphosate-resistant weeds—and herbicide-resistant weeds
in general—represent a significant challenge to our food
system. However, simply inserting additional resistant traits
into crops and promoting the continuous application of gly-
phosate and dicamba or 2,4-D is by no means the only avail-
able or practical solution to this problem (figure 1). Growers
and scientists have been working together for decades to
develop a robust set of management practices that could be
implemented to address resistant-weed issues.
Integrated weed management is characterized by reliance
on multiple weed management approaches that are firmly
underpinned by ecological principles (Liebman et al. 2001).
As its name implies, IWM integrates tactics, such as crop
rotation, cover crops, competitive crop cultivars, the judi-
cious use of tillage, and targeted herbicide application, to
reduce weed populations and selection pressures that drive
the evolution of resistant weeds. Under an IWM approach,
a grain farmer, instead of relying exclusively on glyphosate
year after year, might use mechanical practices such as rotary
hoeing and interrow cultivation, along with banded pre- and
postemergence herbicide applications in a soybean crop
one year, which would then be rotated to a different crop,
integrating different weed management approaches. In fact,
long-term cropping-system experiments in the United States
have demonstrated that cropping systems that employ an
IWM approach can produce competitive yields and realize
profit margins that are comparable to, if not greater than,
those of systems that rely chiefly on herbicides (Pimentel
et al. 2005, Liebman et al. 2008, Anderson 2009). In one
study, herbicide inputs were reduced by up to 94%, and
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attesting to the economic and environmental benefits that can
be realized if these technologies are used judiciously (Duke and
Powles 2009). Rather, we are advocating that concrete policy
steps be taken to ensure that we learn from our problematic
experiences with glyphosate resistance, such that the new
herbicide-resistant crops are adopted as only one component of
fully integrated weed management systems. Such policies could
include USEPA-mandated resistant-weed management plans,
fees discouraging single-tactic weed management, improved
grower educa tion programs implemented through industry–
university–government collaborations, and environmental
payments that connect IWM to broader environmental
goals.
First, the USEPA, and similar agencies in other countries,
should require that registration of new transgene–herbicide
crop combinations explicitly address herbicide-resistant-
weed management. Weed scientists and industry spokes-
people have frequently expressed skepticism that resistance
management regulations would be enforceable and have
instead placed the burden on education and promotional
efforts by agribusinesses or the responsible behavior of indi-
vidual growers (NRC 2010). However, in Bacillus thuringi-
ensis (Bt) cropping systems, regulations requiring non-Bt
refugia have largely prevented the evolution of insect resis-
tance to Bt and protected the effective and sustainable use
of this biotechnology (NRC 2010), although improvements
may be needed in monitoring and compliance (NRC 2010).
For herbicides, regulations need not be focused on local
refugia but could implement spatially explicit, area-wide
management plans that work to reduce selection pressure
at landscape or regional scales. These plans could mandate
carefully defined patterns of herbicide rotation or could set
upper limits on the total sales of a specific herbicide active
ingredient or of a resistant seed variety within an agricul-
tural county. Efficient allocation of crop hectares treated
with a specific herbicide or planted with a resistant variety
could be achieved through a tradable-permit system.
Second, fees directly connected to the sale of herbicide-
resistant seeds or the associated herbicides could provide
a disincentive for overreliance on the technology package
(Liebman et al. 2001). These fees could be scaled to spe-
cifically discourage overuse, such that a grower or applicator
would be charged only if a specified threshold in planted
hectares or successive applications were exceeded. The pro-
ceeds from the fees could be funneled directly into funds for
public university research and education programs that pro-
mote the understanding and adoption of IWM techniques
among farmers. In Iowa, similar levies on pesticides are used
to fund Iowa State University’s Leopold Center, which has
played a significant role in the development of IWM science
(Liebman et al. 2001).
Third, stronger partnerships among industry, universities,
and government could foster IWM through more effective
education and extension efforts. When new herbicide active
ingredients or herbicide-resistant crop varieties are brought
to market, seed and agrichemical companies often develop
herbicides and eliminate the need for postemergence her-
bicide applications. To apply this IWM practice, a farmer
would need detailed, region-specific information on crop
and weed ecology in order to choose the planting date that
optimizes a tradeoff between better weed control and a
shorter growing season (Nord et al. 2011). Because the use
of this practice might reduce the need for herbicide inputs,
modern seed-chemical firms would have little incentive to
pursue the required research or to extend the knowledge
to growers. IWM knowledge serves as a public good, and
it requires locally adapted and ongoing public research,
combined with effective extension education programs,
in order to address current and future weed management
challenges.
In his congressional testimony, Troy Roush (Indiana
farmer and vice president of the American Corn Grower’s
Association) remarked that farmers are “working on the
advice largely of industry anymore.… Public research is
dead; it’s decimated” (US House Committee on Oversight
and Government Reform 2010). Indeed, several trends
indicate that the public support needed for IWM research
and extension is declining. First, the formula funds in the
US Farm Bill that have historically provided support for
land-grant universities to pursue farming systems research
tailored to their growing regions have been steadily phased
out in favor of competitive grant programs, in which the
research topics and agendas are set by federal funding agen-
cies (Huffman et al. 2006, Schimmelpfennig and Heisey
2009). The total amount of federal public funding for
agriculture has basically remained flat since 1980, whereas
private research investments have steadily increased (Schim-
melpfennig and Heisey 2009). During this period, partner-
ships between land-grant universities and chemical and
biotechnology companies have increased in number and
extent (Schimmelpfennig and Heisey 2009), and in several
respects, research activities in public colleges of agriculture
have transitioned to parallel the activities and priorities of
the biotechnology industry (Welsh and Glenna 2006). A
recent survey of the membership of the Weed Science Soci-
ety of America suggests that these patterns are influencing
the research priorities of scientists who specialize in weed
management (Davis AS et al. 2009). As of 2007, 41% of the
membership reported topics related to herbicide efficacy as
their primary research focus, whereas only 22% reported
focusing on topics with a broader integrated perspective.
When the next major weed management challenge arrives,
will we be prepared with the knowledge and skilled work-
force capable of implementing an integrated solution?
Policies to cultivate IWM
Several changes in policy could reduce the likelihood that the
next generation of herbicide-resistant crops will result in neg-
ative consequences for food production and the environment
and could ensure that IWM thrives as a sustainable alterna-
tive in the future. To be clear, we are not advocating the pro-
hibition of herbicide-resistant crops; there is ample evidence
Forum
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to be scaled up if sufficient willingness to pay for alternatives
can be achieved.
No single policy will adequately address our growing
overreliance on a transgenic approach to weed management.
Rather, a combination of policies will be necessary to secure
a more sustainable agriculture, including (a) regulatory
mandates for resistant-weed management, (b) enhanced
funding for IWM research and education, (c) collaboratively
designed herbicide stewardship plans, and (d) environmen-
tal payment incentives for the adoption of IWM practices.
Next-generation GM herbicide-resistant crops are rapidly
moving toward commercialization. Given this critical junc-
ture, it is time to consider the implications of accelerating
the transgene-facilitated herbicide treadmill and to rejuve-
nate our commitment to alternative policies that safeguard
agriculture and the environment for the long term.
Acknowledgments
We thank Bill Curran, Leland Glenna, Bob Hartzler, and
the Penn State weed ecology lab for helpful comments and
insights on earlier versions of the manuscript. Ian Graham
provided assistance compiling and analyzing data from the
International Survey of Herbicide Resistant Weeds database
(www.weedscience.org).
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