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Environmental Management (2016) 57:31–48

DOI 10.1007/s00267-015-0589-7

Genetically Modified Herbicide-Tolerant Crops, Weeds,


and Herbicides: Overview and Impact
Sylvie Bonny1,2

Received: 12 April 2015 / Accepted: 4 August 2015 / Published online: 22 August 2015
 Springer Science+Business Media New York 2015

Abstract Genetically modified (GM) crops have been Keywords Agriculture  Transgenic crop  GMO impact 
and continue to be a subject of controversy despite their Herbicide  Weed resistance  Economics
rapid adoption by farmers where approved. For the last two
decades, an important matter of debate has been their Abbreviations
impact on pesticide use, particularly for herbicide-tolerant APHIS USDA Animal and Plant Health
(HT) crops. Some claim that these crops bring about a Inspection Service
decrease in herbicide use, while others claim the opposite. BMPs Best management practices
In fact, since 1996, most cultivated GMOs have been GM Genetically modified
GMHT crops, which involve the use of an associated GMHT Genetically modified herbicide-tolerant
herbicide, generally glyphosate. In their very first years of GMGT Genetically modified glyphosate-tolerant
adoption, HT crops often led to some decrease in herbicide GR Glyphosate-resistant (for weeds)
use. However, the repetition of glyphosate-tolerant crops GT Glyphosate-tolerant (for crops)
and of glyphosate only applications in the same fields HR Herbicide-resistant (for weeds)
without sufficient alternation and herbicide diversity has HT Herbicide-tolerant (for crops)
contributed to the appearance of glyphosate-resistant USDA United States Department of Agriculture
weeds. These weeds have resulted in a rise in the use of USDA-ERS USDA Economic Research Service
glyphosate and other herbicides. This article explores this USDA-NASS USDA National Agricultural Statistics
situation and the impacts of herbicide-resistant weeds, Service
using an interdisciplinary approach and drawing on recent USEPA US Environmental Protection Agency
data. The paper analyzes the spread of GMHT crops USGS US Geological Survey
worldwide and their consequences on herbicide use in the
USA in particular. It then addresses the global development
of glyphosate-resistant weeds and their impact, particularly
focusing on the USA. Finally, the last section explores how
industry, farmers, and weed scientists are coping with the Introduction
spread of resistant weeds. The concluding comments deal
more widely with trends in GM crops. Since their beginnings, transgenic crops have been a sub-
ject of debate in spite of their quick adoption by farmers
where available. In a certain number of countries, part of
the population considers the approved GM crops as rather
& Sylvie Bonny
safe and useful for facing the agricultural and food chal-
bonny@grignon.inra.fr
lenges of the next decades (FAO 2004) and GMOs have
1
INRA, UMR210 Economie publique, 78850 Grignon, France been accepted; they were cultivated in 28 countries in 2014
2
AgroParisTech, UMR Economie publique, 78850 Grignon, (James 2014). At the same time, in other countries, many
France people see them as risky and unsustainable as regards many

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32 Environmental Management (2016) 57:31–48

environmental, health, and socio-economic aspects (Wiki- term availability of the facile and economically
pedia 2015a, b, c). In the last 20 years, almost all GM crops important weed control provided by current herbi-
have been herbicide tolerant (HT) or insect resistant, and cide-resistant crop plants. Also at risk is the greatly
thus an important topic of debate has been their impact on expanded use of no-till or reduced-till planting pro-
pesticide use. However, insect-resistant crops, which pro- cedures that are made possible by ‘‘burndown’’ of
duce their own insecticide (generally Bt proteins), must be weeds before planting of herbicide-resistant crops’’
differentiated from HT crops, which can withstand spray- (Behrens et al. 2007).
ing with certain non-selective herbicides aimed at elimi-
The evolution of resistant weeds has been highly
nating all weeds. Insect-resistant crops have generally led
favored by GT crops, which have induced a repeated use of
to a decrease of previously used insecticides, while the
glyphosate without sufficient alternation of weedkillers or
impact of HT crop varies and is more unclear (Fernandez-
weeding practices. In a similar manner, many pests and
Cornejo et al. 2014; Klümper and Qaim 2014). Further-
pathogens have developed resistance to pesticides and
more, for the last 15 years, a new factor has fueled the
drugs (Tabashnik et al. 2014). In early 2013, Bourguet
controversy: the development of weeds resistant to gly-
et al. noted:
phosate, the weedkiller to which the majority of GM crops
have been made tolerant. ‘‘Almost 8000 cases of resistance to 300 insecticide
Admittedly, since the 1950s when weedkillers began to compounds have been reported in more than 500
be widely used, 245 herbicide-resistant (HR) weeds have species of arthropods (…). Similarly, 300 cases of
appeared over the years and many weed species have field resistance to 30 fungicides have been reported in
developed resistance to different herbicides (Heap 1997, 250 species of phytopathogenic fungi (…). The sit-
2014, 2015). Hence weed resistance is not a new phe- uation is most critical for antibiotic resistance. (…)
nomenon. However, GMHT crops are greatly affected by The Antibiotic Resistance Genes Database (…) lists
glyphosate-resistant (GR) weeds, due to the high predom- more than 23,000 potential resistance genes of
inance of glyphosate-tolerant crops since 1996. In addition, approximately 400 types, conferring resistance to 250
glyphosate is by far the most widely used herbicide, also antibiotics in 1,700 species of bacteria from 270
widely applied on non-HT crops (Agrow 2014). Thus this genera. Strains from highly pathogenic bacteria (…)
paper focuses mainly on glyphosate. Although there are that are resistant to all known classes of antibiotic
fewer weed species resistant to glyphosate today than there have recently been described.’’
are species resistant to some other herbicides, the impact of
Therefore in several domains, it is urgent to sustain the
GR weeds is substantial. Firstly, they can lead to an
efficiency of the control methods and to prevent the
increase in herbicide use and they can be a big problem for
development of resistance in pests or bacteria.
farmers (Benbrook 2012, and data below). Moreover, if a
The aim of this paper is thus to analyze in more depth
glyphosate-tolerant crop can no longer be weeded by gly-
the importance of glyphosate-resistant weeds in relation
phosate, the effectiveness of the method seems to be called
to GMHT crops, as well as their impact and the remedial
into question (Livingston et al. 2015). Hence, as glypho-
measures that the involved stakeholders are implementing
sate-tolerant crops have been the most widely cultivated for
or looking for. Indeed, even though many papers in weed
the last 20 years (James 2014), many GMOs also seem to
science have studied herbicide-resistant weeds and even
be called into question. Glyphosate-tolerant crops have
though the media has sometimes mentioned this issue,
often been described by their promoters and supporters as
their real development and consequences are poorly
having revolutionized farming and as having brought about
known, except by some specialists. After the introductory
considerable agro-economic and environmental benefits.
section, the second part of this paper describes the
Such benefits can now be challenged by the rise of GR
worldwide expansion of GMHT crops and some of its
weeds.
outcome in terms of herbicide application, particularly in
‘‘The advent of biotechnology-derived, herbicide-re- the USA (2). The development of herbicide-resistant
sistant crops has revolutionized farming practices in weeds, notably glyphosate-resistant weeds, as well as
many countries. (…) [It] has led to striking some of its side-effects is addressed in the third section
advancements in agricultural crop management sys- (3). The last section examines how the GM seed industry,
tems throughout the world. (…) The recent emer- weed scientists, and farmers are coping with the increase
gence of weeds resistant to the herbicides used (…) of weed resistance, and some resulting effects of their
has prompted serious concerns regarding the long- actions (4).

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Environmental Management (2016) 57:31–48 33

Links between herbicide-resistant weeds and herbicide-tolerant crops called on (Baker and Stone 2015; Thelin and Stone 2013;
To biotechnology promoters, herbicide-resistant weeds are only a USGS 2015a, b, c). USGS uses two sets of data: (i) pesti-
herbicide problem, not a GMO problem (Kniss 2013; Miller cide-use data compiled by proprietary surveys by GfK
2010). However, glyphosate-resistant weeds are linked to GM Kynetec on the amounts of pesticides applied to individual
crops with respect to several aspects:
crops by Crop Reporting District (CRD) of farm opera-
• For two decades, GM glyphosate-tolerant (GMGT) crops have
been by far the most numerous GM crops
tions, and (ii) annual harvested crop acreage reported by
• GMGT crops inherently imply the application of glyphosate on
USDA-NASS. By compiling these data, USGS calculates
the crop, and glyphosate has replaced many other herbicides an ‘‘estimated pesticide use’’ (EPest) rate for each crop by
used before. Hence, on GMGT crops, there has been little or no year. As pesticide-use data are not available for all CRD
alternation of herbicide applications or of weeding techniques and years, when data are unavailable, EPest extrapolated
(Owen et al. 2014). In addition, some crop rotations have
involved a frequent repetition of glyphosate-tolerant crops.
rates are calculated from adjoining or nearby CRD to
Thus there has been an overreliance on glyphosate ensure that pesticide use is estimated for all counties that
• In multiple locations, because of glyphosate-resistant weeds, report harvested-crop acreage (Thelin and Stone 2013).
glyphosate is losing its efficacy in weeding transgenic GT Thus a list of figures for the period 1992–2012 reflecting
crops. In those places, GMGT crops seem to be called into amounts used per year of 21 herbicides applied to crops is
question
available (USGS 2015b, c).
• The number of weed species resistant to glyphosate is higher
With regard to HR weeds, especially GR weeds, we
for GMGT crops—soybean, corn, and cotton—than for non
glyphosate-tolerant crops (Heap 2015, and figure below) drew data from ‘‘The International Survey of Herbicide
• A low number of new herbicides have been put onto the market Resistant Weeds,’’ which is a collaborative effort of world
in the last 15 years because of the high rate of adoption of weed scientists to report herbicide-resistant weeds globally
GMHT crops and of the costs to launch a new herbicide. This (Heap 2015). Furthermore, besides doing a survey on
increases the impact of resistant weeds, since few new
existing literature, we looked for papers and presentations
weedkillers can replace those that are now becoming
ineffective (Duke 2012; Gerwick 2010; Kraehmer et al. 2014) by weed scientists, seed companies, and professional and
Therefore, there exists a link between GMGT crops and increasing environmental organizations, as many conferences have
glyphosate-resistant weeds, because GT crops have favored an been held on this subject.
increased use of glyphosate, which has resulted in the selection
of GR weeds
The Widespread Cultivation of GMHT Crops
and the Outcome in Terms of Herbicide Use
This article is based on an extensive search for, and
analysis of, updated precise data and detailed statistics on From 1996 to 2014, the expansion of GM crops was rapid
GMHT crops, particularly GT crops, and on herbicide-re- but uneven: in 2014, three countries (USA, Brazil, and
sistant weeds, especially glyphosate-resistant weeds, as Argentina) accounted for 77 % of GM crop area, three
well as on their side-effects. Data on GMHT crops are crops (soybean, corn, and cotton) totaled 95 % of such
mainly drawn from ISAAA reports (James 2014) and from area, and two traits (herbicide tolerance and insect resis-
the US Department of Agriculture (USDA) Economic tance) 99 % (Table 1). Concerning GM traits, herbicide
Research Service’s statistics (USDA-ERS 2015). For the tolerance traits—increasingly stacked with insect resis-
herbicide use on GMHT crops in the USA, we particularly tance traits—have been continually predominant over the
analyzed survey results from the USDA National Agri- last 18 years: the GM crops carrying them have always
cultural Statistics Service, notably the last ones (USDA- represented more than 81 % of all GMOs (Fig. 1). More-
NASS 1991–2013). However, these surveys on the use of over, the overwhelming majority of HT crops have been
chemicals on field crops, which were generally annual for tolerant to glyphosate, while only a tiny percentage were
each major field crop from 1990 to 2006, have become glufosinate tolerant, as was the case for HT corn in the first
much less frequent since 2006; each year only some few years (Livingston et al. 2015). However, the rate of
commodities are surveyed. So, after the 2006 survey on adoption of GT crops was different among different
soybean, the next one was in 2012, and the following is countries as well as among crops, depending on regulatory
scheduled for 2017 (USDA-NASS 2013). Thus, the mon- aspects and agro-economic profitability (Fig. 2).
itoring of pesticide use on GM crops is less detailed. Since they allow for easier weed management in their
Admittedly, private surveys of chemical use on field crops first few years, GT crops were rapidly adopted where
are made by some specialized companies, but their results, regulatory and social conditions were favorable. This is
which are expensive proprietary data, cannot be quoted or particularly the case for HT soybeans, which are the most
disseminated. Nevertheless, some assessments of herbicide widely cultivated HT crops: in 2014, GT soybeans repre-
use from the US Geological Survey (USGS) can also be sented 50 % of all HT crops and about 80 % of all globally

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Table 1 Predominance of three Area Area Area % total including


countries, three crops, and one Country Crop GM trait
(Mha) (Mha) (Mha) stacked traits
trait in total GM crop area in the
world in 2014 (area in Million USA 73 Soybean 91 Herbicide tolerance (HT) alone 103 } HT: 85%
ha) Brazil 42 Corn 55 Herbicide tolerance & Insect resistance 51
Argentina 24 Cotton 25 Insect resistance (IR) alone 27
} IR: 43%
% total GM % total GM
77% 94% % total GM crop area 99.8%
crop area crop area
The last line gives the percentage of the three main countries, crops, or traits in total GM crop area of
181.5 Mha (from James 2014)

Fig. 1 Predominance of
herbicide-tolerant crops
globally: area of HT crops
versus total area of GM crops,
1999–2014 (million hectares)
(adapted from James 2014)

Fig. 2 Variations in the rate of adoption of glyphosate-tolerant crops the USA, Argentina, and Brazil (from James 2014 and various local
according to countries and crops: percentage of herbicide-tolerant sources). b Percentage of HT varieties cultivated in soybean, corn,
varieties in some crops, 1997–2015. a Percentage of HT soybean in and cotton areas in the USA (USDA-ERS 2015)

cultivated soybeans. Their rate of adoption was rapid in the and as USDA statistics provide unbiased data (based on
USA, Argentina, and Brazil. As there are variations random surveys) on herbicide use and on the percentage of
between crops and contexts, it is necessary to choose a GM varieties within each crop.
detailed case to present a more thorough assessment of the For GM crops in the USA, glyphosate applications have
trends in herbicide use. The case of GT soybean in the USA replaced a large part of previously used herbicides (Bonny
will be discussed here as it is the most cultivated GM crop, 2008; Osteen and Fernandez-Cornejo 2013). With the growing

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adoption of GT varieties, the number of the different types of occurrence of glyphosate and its degradates in the Midwest, in
herbicide applied on soybean area diminished between 1996 soils, surface water, groundwater, and precipitation (Coupe
and 2005 (Fig. 3) (USDA-NASS 2014). During the same per- et al. 2012; Battaglin et al. 2014)
iod, this decline led at first to a small decrease, then to stagnation In the first few years after the adoption of HT crops, a small
in the number of applications and in the total amount of her- decrease in herbicide applications was observed in compar-
bicide applied per unit of soybean surface. So the environ- ison with the period 1990–1996. Later, particularly after 2005,
mental impact of GT crops was often assessed as beneficial by a herbicide application started to rise again, and since then,
great number of papers, due to the fact that some rather noxious additional herbicides are increasingly being added to gly-
herbicides previously used were replaced by glyphosate (Cer- phosate (Figs. 3, 4; USGS 2015b). Thus for soybean, gly-
deira and Duke 2006; Kleter et al. 2007). Indeed at that time, phosate share in total herbicides used declined to 83 % in
glyphosate was often considered to be rather benign (USEPA 2012. So, although GT crops induced a decrease in pesticide
1993). Another frequently mentioned benefit was the con- use at the outset, a reversal in this trend occurred rapidly,
comitant expansion of soil conservation practices, to which linked to the development of herbicide-resistant weeds
glyphosate-tolerant crops are well suited (Bonny 2011; Fer- (Fig. 3, 9) (Livingston et al. 2015). As the trend in the amount
nandez-Cornejo et al. 2014; Givens et al. 2009). These soil of herbicide use is frequently not sufficient to evaluate the
conservation practices have several advantages, such as helping environmental impact, it is useful to take into account the
prevent soil erosion and diminish soil leaching (Ervin et al. health and environmental profiles of herbicides. This is,
2010; Price et al. 2011). The development of GM crops has also however, a complicated task because of the high number of
contributed to an increase in the size of farms since it has these indicators and of composite indicators (Bonny 2011), as
resulted in a certain decrease in required labor time per crop. well as of their limitations. If a certain number of articles have
Large-scale adoption of GMGT crops was favored by the used the Environmental Impact Quotient (EIQ) proposed by
decrease of glyphosate prices that occurred when its patent Kovach et al. (1992), the EIQ was recently assessed as ‘‘a poor
expired in 2000 in the USA. Large quantities of glyphosate indicator of potential environmental risk of herbicides’’ (Kniss
generics were produced in some countries, such as China. and Coburn 2015). This negative assessment was linked to
Thus, there has been a huge increase in global glyphosate use several limitations: EIQ does not take into account, or it does
linked to the development of GT crops. Glyphosate became very poorly so, the potential of exposure, the risk factor linked
the main herbicide used globally. Its annual worldwide sales to herbicide systemicity, plant surface half-life, and leaching
totalled about 6 billion USD in 2012, i.e., about 30 % of the and surface runoff potential. Thus Kniss and Coburn (2015)
global herbicide market, far ahead of other herbicides (Agrow call for better approaches.
2014). In the USA, glyphosate use multiplied tenfold from
1993 to 2007, particularly in the Midwest and in some parts of
California (Grube et al. 2011; Coupe et al. 2012). For soy- The Expansion of Glyphosate-Resistant Weeds
bean, the glyphosate proportion of total herbicides used grew
from 4 % in the 1990–1993 to 89 % in 2006 (USDA-NASS Globally, many herbicide-resistant weeds have appeared
1991–2013). Detailed analyses by scientists from USGS since the 1950s, when the use of weedkillers became
Water Science Centers have shown a frequent and widespread widely spread. In early July 2015, there were ‘‘459 unique
Fig. 3 Number of different
types of herbicide applied on
soybean area in relation to the
expansion of glyphosate-
resistant weeds in the USA,
1990–2012 (author’s calculation
from USDA-NASS 1991–2013
and from Heap, 2015). (Right
y-axis number of GR weeds.
Left y-axis number of
herbicides). After 2006, there
was only one survey on
herbicide usage in 2012; thus,
from 2007 to 2011, the number
of herbicides is extrapolated
according to the values in 2006
and 2012 (dotted line)

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Fig. 4 Trends in glyphosate


and other herbicides applied on
soybean in the USA, 1990–2012
(herbicide quantity in kg/ha of
total soybean area) (same source
as Fig. 3) (Right y-axis % of
GM soybean in total US
soybean area. Left y-axis kg/ha
of applied herbicides)

cases (species x site of action) of herbicide resistant weeds The expansion of GR weeds was slow until 2003.
globally, with 246 species (…). Weeds have evolved However, it grew more rapidly after that time. In end June
resistance to 22 of the 25 known herbicide sites of action 2015, there were 32 GR weeds in the world, of which 14
and to 157 different herbicides. Herbicide resistant weeds were in the USA (Fig. 6). The number of GR weeds per
have been reported in 86 crops in 66 countries.’’ (Heap crop is high for GT crops, particularly soybean, corn, and
2015). Herbicides do not cause weeds to evolve resistance cotton, as well as for orchards and grapes, on which gly-
per se. The manner in which herbicides are used is a major phosate has been repeatedly applied (Fig. 7). The fre-
factor in explaining why weeds develop resistance. Her- quency of glyphosate treatments has been reinforced by the
bicides exert a high selection pressure on weed popula- most current type of crop rotation. According to the data on
tions. Resistant weed populations develop from rare crop production practices from the USDA Agricultural
random genetic mutations that may exist in individuals Resource Management Survey (ARMS), in 2012, soybeans
within a weed population. Repeated use of the same her- were preceded by corn on around 65 % of acreage, and by
bicide (or herbicide mode of action) increases the fre- another soybean on 13 % (USDA-ERS 2014). These pre-
quency of these mutations by selection pressure, ceding corn and soybean crops were themselves predomi-
particularly in the absence of other weedkillers or weeding nantly glyphosate tolerant (respectively 73 and 93 % in
methods (Norsworthy et al. 2012). Hence, some weed average) (USDA-ERS 2014).
populations become predominant and are resistant to one or The impact of GR weeds on a given crop varies
several herbicides (Service 2007). according to several factors: total number of HR weeds,
Although many herbicide families now have HR weed type of weeds, etc. GR weeds are not all the same; some
populations, there are variations in susceptibility to the have high interference with crop yields, such as Palmer
different weedkillers (Fig. 5). Today, there are fewer GR amaranth (Ward et al. 2013). Moreover, some weeds have
weeds than there are weeds with resistance to some other developed multiple herbicide resistances, i.e., resistance to
herbicides. Nevertheless, the impact of GR weeds is two or more herbicides with different sites of action
strong because of the wide use of glyphosate and because (Beckie and Tardif 2012). Hence, they are difficult to
GT crops are designed to tolerate this specific herbicide. control as there are fewer herbicides capable of controlling
When several noxious weeds become resistant to gly- them. Furthermore, this multi-resistance is increasing
phosate, the many farmers growing such crops are (Heap 2015; Rabobank International 2012; Service 2013).
severely affected and the concept of GT crops becomes So, in the USA, some weeds such as Palmer Amaranth
questionable. (Amaranthus palmeri), Tall Waterhemp (Amaranthus

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Environmental Management (2016) 57:31–48 37

Fig. 5 Global number of resistant weed species for several herbicide groups, 1970–mid-2015 (in brackets, a representative of each herbicide
family) (adapted from Heap 2015)

tuberculatus), Common Ragweed (Ambrosia artemisiifo-


lia), and Giant Ragweed (Ambrosia trifida) are now resis-
tant to glyphosate and to one or more other herbicides
(Heap 2015).
Globally, 25 countries have experienced GR weeds,
albeit at different levels (Heap 2015). The USA has
experienced the highest number (14) of GR weeds, but
their growth rate has slowed down since 2008 due to the
increased use of other weedkillers and the implementation
of better weed control practices. However, in the US the
states growing HT crops are increasingly affected by GR
weeds: in late March 2015, 38 states had experienced the
rise of one or more GR weeds; up to ten GR weeds were
recorded in Mississippi alone (Fig. 8). It is difficult to
assess the global agricultural area affected. Heap (2013)
Fig. 6 Number of glyphosate-resistant weed species and area of GM estimated that, in 2012, the area affected by GR weeds was
herbicide-tolerant crops, globally and in the USA, 1996–2014 about 6.3 million ha globally, of which approximately 6
(adapted from Heap 2015; James, 2014) (Left y-axis, dotted line
number of GR weed species. Right y-axis, solid line GMHT crop area
million ha (95 %) were in the USA in GT cropping sys-
in Million ha) tems. However, some assessments were much higher:

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Fig. 7 Countries and crops which are the most affected globally by glyphosate-resistant weeds (x-axis number of GR weeds, mid-2015) (adapted
from Heap 2015). a Countries with at least two GR weed species. b Crops with at least five GR weed species

Fig. 8 Number of GR weed


species in the USA and number
of US states with GR weeds,
1998–mid-2015. (Author’s
calculation from Heap 2015)
Left y-axis number of the US
states with GR weeds. Right
y-axis number of GR weed
species in the USA)

another survey reported up to 28 million ha of affected US are frequently more harmful and difficult to use due to their
farmland (Stratus Ag Research 2013). profile (Boerboom and Owen 2007; Service 2007). More-
over, since 1997, the number of new active herbicide
ingredients put onto the market has declined, and, in the
How do Weed Scientists, Farmers, and Companies USA, the number of patents dealing with new weedkillers
Cope with Glyphosate-Resistant Weeds? has also dropped (Adler 2011; Duke 2012; Gerwick 2010;
Kraehmer et al. 2014). Hence weed control may be more
The rise in GR weeds has a broad impact, and glyphosate’s difficult to accomplish. This decrease in the marketing of
loss of efficacy is seen as having great repercussions in the new active ingredients is partly an outcome of the expan-
areas growing many GT crops. In HT crops and elsewhere, sion of GT crops. Indeed, the market for herbicides other
glyphosate is now often increasingly supplemented, and than glyphosate has grown smaller; at the same time, the
sometimes replaced, by other herbicides; however, these number of agrochemical companies has decreased due to

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consolidations in this industry, while commercialization glyphosate was discovered in Australia. Several weed sci-
costs have increased (Duke 2012; Kraehmer et al. 2014; entists warned,
Phillips McDougall 2010). Organizations opposed to GM
‘‘Given the importance of glyphosate in world agri-
crops often greet glyphosate-resistant weeds with sarcastic
culture, its current high use, and impending increased
comments such as ‘‘revenge of the weeds,’’ according to a
usage with transgenic crops, the evolution of gly-
paper title (Coombs 2012), seeing it as almost a fulfillment
phosate resistance is a significant development in
of their predictions. However, the appearance of these
world agriculture. It would be prudent to accept that
weeds does not mean that glyphosate will no longer be
resistance can occur to this highly valuable herbicide
used or that other weed control methods will be adopted.
and to encourage glyphosate use patterns within
integrated strategies that do not impose a strong
Weed Scientists
selection pressure for resistance’’ (Powles et al.
1998).
In the 1990s, Monsanto’s scientists stated that there was
almost no risk of the occurrence of glyphosate-resistant This warning was not isolated; other scientists also
weeds, because of glyphosate’s specificities (Bradshaw alerted on the risk of the development of glyphosate-re-
et al. 1997). Hence, even if the use of selective weedkillers sistant weeds (Erickson and Lemaux 2000; Hartzler 1998;
was not prohibited, during the first 8 years of GT crops, Neve et al. 2003; Reddy 2001; Shaner 2000).
Monsanto generally encouraged farmers to mainly use its In contrast, since 2005, many measures have been rec-
increasingly diverse glyphosate brands and formulations, ommended and are being sought by the concerned stake-
e.g., through its reward programs (Dupraz 2012; Shaner holders in order to cope with GR weeds (Frisvold and
2000; Waltz 2010). In doing so, the need for herbicide Reeves 2010; Green and Owen 2011; Nandula 2010).
rotation or addition was not stated. Furthermore, many Many scientists from weed science extension services and
Monsanto ads and leaflets, as well as many scientific or universities have become involved in this issue. They
media papers, highlighted benefits of GT crops, notably the advocate increased research activities, the exploration of
advantages of using only one herbicide, which allowed new approaches, as well as better weed control manage-
simplicity, convenience, lower costs, labor, and fuel sav- ment (Gressel 2010; Vencill et al. 2012). The need for
ings (Reddy 2001). For example, a Monsanto specialist ‘‘glyphosate stewardship’’ is stressed, which ‘‘refers to the
declared: management decisions and practices subsequently
employed to preserve the utility of a crop trait’’ (Beckie
‘‘Use of other herbicides in a tank mix with Roundup
2011). Weed scientists emphasize the importance of
UltraMAX often adds expense and increases the risk
diversity in weed management and recommend the use of
of crop injury or carryover (…). After years of
best management practices (BMPs), in order notably to
research, Monsanto has concluded that Roundup
understand the biology of weeds, diversify weed manage-
UltraMAX alone is the best choice for most weed
ment practices, use multiple herbicide mechanisms of
control situations’’ (Southwest Farm Press 2001).
action, and prevent weed seed production and spreading
A 2003 leaflet on GT soybeans stated: (Norsworthy et al. 2012; Stokstad 2013; Owen et al. 2014).
‘‘Not All Herbicides Work the Same: (i) The devel-
Farmer Attitudes
opment of weed resistance to glyphosate is less likely
than active ingredients in many other herbicides due
Before the 2005–2006 period, ‘‘agricultural practices
to glyphosate’s unique mode of action. (ii) Resistance
aimed at delaying or preventing the development of her-
to glyphosate has been observed far less often than
bicide resistance [were] not viewed as being economical in
resistance to most other active ingredients. (iii) In
the short term, and [were] not readily used by all growers’’
fact, after almost three decades of worldwide use,
(Webster and Sosnokie 2010). According to these authors,
resistance to glyphosate has been observed in only
two beliefs explained this farmer behavior: (i) a new
four weed species globally (two in the US) (Mon-
technology would be developed to solve the resistance
santo 2003a). Another leaflet assured ‘‘resistance is
issue and (ii) resistance management strategies would turn
easily and economically managed’’ (Monsanto
out to be futile. Actually, a survey of growers developed by
2003b).
weed scientists from six states in 2005–2006 showed that
Thus, at the beginning of the diffusion of HT varieties, ‘‘farmers did not have a high level of awareness of the
rather little advice for good herbicide management was potential risks to the sustainability of the GR crop systems
provided, at least through company documentation and by with regard to evolved glyphosate resistance’’ (Owen et al.
input sellers. Yet, in 1996, a first weed species resistant to 2011). Frisvold and Reeves (2010, 2014), who analyzed a

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40 Environmental Management (2016) 57:31–48

2007 phone survey of farmers about their use of ten BMPs 2005 and above all after 2011, especially for certain weeds
to delay weed resistance, also assessed that their current (Rabobank International 2012; Service 2013; Sosnoskie
rate of adoption has proved insufficient in delaying resis- and Culpepper 2014; WSSA 2014). The application of
tance in many areas. additional herbicides also leads to an increase in the total
However, more recent studies showed that ‘‘growers are use of herbicide (Fig. 4), as well as to the loss of some of
moving towards a better understanding of the implications the advantages farmers had derived from glyphosate-tol-
of their herbicide use practices’’ (Johnson et al. 2009; erant crops, such as easier weed control. Another notable
Owen et al. 2011). Indeed, since 2005–2006, cultural impact is the side-effect of GR weeds on soil conservation
practices have begun to change, given the increasing extent practices, as GT crops may have facilitated their adoption.
of GR weeds and also the advice provided by weed sci- The current expansion of GR weeds, particularly of GR
entists, grower associations, advisors, and seed companies Palmer amaranth, threatens conservation agriculture, as in
(Givens et al. 2011; Livingstone et al. 2015). Farmers have some instances tillage is one of the few effective options to
more often applied other herbicides in addition to gly- manage HR weeds (CAST 2012; Price et al. 2011). In
phosate (Figs. 3 and 4). A 2010 survey in 22 US states addition, farmers and other operators have to implement
showed that a higher percentage of growers integrated measures to avoid the spreading of GR weeds in the
herbicides other than glyphosate, but that many continued neighborhood, which complicates some farm operations.
to use only glyphosate (Prince et al. 2012). A 2011 survey GR weeds can easily spread from one field or area to
in the Mid-South testified that some BMPs, particularly another (Bagavathiannan et al. 2013). Herbicide resistance
cultural practices, are implemented in a limited manner can be transferred through the weed pollen, vegetative
because of time constraints, weather, extra costs, and a structures (rhizomes, tubers), and above all weed seeds.
certain difficulty for some farmers in adopting a proactive The latter can be disseminated very far by transportation, in
strategy when they have not experienced resistant weeds on the same way as many plant pathogens have spread from
their own farms (Riar et al. 2013). Yet, a detailed bench- one country or continent to another. Besides, some herbi-
mark study in more than a hundred farm fields, comparing cides which could be increasingly used with the HT crops
costs, yields, and net returns between growers’ standard need to be applied cautiously, because of their risk of
weed management and BMPs, showed that, despite their drifting (Egan et al. 2014).
higher costs, BMPs could lead to the same net returns However, herbicide resistance management depends not
(Edwards et al. 2014). In a late 2012 survey of Certified only on individual farmer practices, but also on the
Crop Advisors, 40 % said that farmers would only adopt behavior of many actors (Ervin and Jussaume 2014).
BMPs if resistant weeds became a problem in their fields Indeed, the actions of the neighbor farmers and of the
(Asmus et al. 2013). However, 15 % responded that community can have an influence, because of the possible
farmers were trying BMPs on a few acres first and 13 % spread of weed seeds from neighboring fields or due to
that growers were plunging into BMPs. The Spring-2014 certain activities. The spreading of HR weeds can also be
poll of Stratus Research indicated that about 65 % of the influenced by the measures taken by government, compa-
US farmers implemented some BMPs to control HR weeds nies, extension scientists, advisors, and input sellers. All
(Stratus Ag Research 2014). Another 2014 survey showed these stakeholders and the media can also act upon the
that only 13 % of respondents now thought that ‘‘HR decisions about herbicide resistance management, making
weeds are not a major concern because new technologies this a complex issue depending on the interplay of several
will be developed to manage them,’’ while 90 % felt that factors and actors.
‘‘pest (…) management is a never-ending technology
treadmill’’ (Arbuckle 2014). As a result of these growing Industry Response
concerns, BMPs are increasingly adopted at present
(Fig. 9) (Livingstone et al. 2015; Prince et al. 2012). This The involved agbiotech/agchemical firms often sustain that
has borne fruit: from 2010 to 2014, the number of GR weed resistance is a common issue of pesticide resistance
weeds remained stable in the USA. that should be resolved with the use of other weedkillers.
At the farm level, one main impact of GR weeds is that These companies, such as Monsanto, Pioneer, Dow, Bayer,
farmers need to use weed control methods other than gly- and Syngenta, propose weeding programs with additional
phosate applications alone, ranging from the application of herbicides and other weed management tools. They are also
other herbicides to mechanical weeding, and sometimes working on new HT plants that are tolerant to other her-
hand weeding to dig out certain weeds (Waltz 2010). The bicides. They mainly work on combined resistances to
most common way is to apply some additional herbicides glyphosate and to other herbicide(s), i.e., to launch new HT
to GT crops, notably persistent herbicides. These additional crops with stacked herbicide tolerance traits (Table 2). In
methods have led to a rise in related costs, particularly after addition to being glyphosate tolerant, the new varieties

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Environmental Management (2016) 57:31–48 41

Fig. 9 Rate of adoption of


several weed resistance
management practices by the
US soybean growers,
1996–2012 (adapted from
Livingstone et al. 2015). There
were no surveys from 2007 to
2011

could be tolerant to other herbicides such as dicamba, 2,4- benign herbicides than those previously used (Fig. 4).
D, ALS inhibitor, mesotrione, or isoxaflutole (Croplife Today, there is risk of the opposite occurring: because of
2015; Duke and Powles 2009; Feng et al. 2010; Green GR weeds, some more toxic herbicides are likely to be
2014; USDA-APHIS 2015). The first new HT crops were used with the new GMOs in the next few years to com-
approved in 2014 and early 2015, following registration of plement glyphosate (Ervin et al. 2010). These new HT
the corresponding herbicide combinations. These new HT traits represent a substantial portion of the upcoming traits
crops could be cultivated in 2016 and later. In early April (Croplife 2015) (Table 2). At the same time, following the
2015 for example, ‘‘Enlist Duo’’ (2,4-D ? glyphosate) was classification of glyphosate as ‘‘probably carcinogenic to
approved by the US Environmental Protection Agency for humans’’ by the International Agency for Research on
use in 15 states. In its final registration for ‘‘Enlist Duo,’’ to Cancer (IARC) (Guyton et al. 2015; IARC 2015), the high
mitigate risks to non-target plants or animals, the EPA use of this herbicide is becoming increasingly controver-
indicated precise labeling requirements about spray drift sial. So, numerous consumers or environmental organiza-
management with instructions on herbicide application tions are alerting on its intensive utilization with HT crops
dealing with droplet size, adequate nozzles and maximum (Center for Food Safety et al. 2015; Consumer Reports
pressure, wind speed and directions, etc. (USEPA 2014). 2015; EWG 2015; FoE 2015; Just label It 2015; Reuters
Thus their registration requirements demand that they be 2015; Wilson 2015). As a result, food industry operators
used safely. note that the demand for non-GMO and organic products is
Yet, despite these requirements, these new HT traits rapidly rising (Roulac 2015). On the other hand, the latest
raise significant questions, because some involved herbi- EPA reviews on glyphosate have determined that science
cides, notably 2,4-D, might have some harmful health or ‘‘does not provide evidence to show that glyphosate causes
environmental effects (Barker 2014; Freese 2014a, b; cancer’’ (USEPA 2015). In April 2015, the USEPA
HSDB 2015a, b; Loomis et al. 2015; Wikipedia 2015b, c). approved the herbicide ‘‘Enlist Duo’’ which combines
However, this is a controversial topic and these weedkillers glyphosate and 2,4-D for use in 9 additional states after a
have been authorized for HT crops in the USA after the first previous approval for 6 states. Moreover, there are
involved companies conducted research to develop new field trials of new GT plants such as wheat, rice, sugarcane,
formulations reducing for example off-target movement. or for GT/IR corn and cotton adapted to other areas (James
Nevertheless, the planned crops with stacked herbicide 2014). However, in April 2015 USEPA said that ‘‘US
tolerance traits could lead to an increase in the use of regulators may start testing food products for residues of
herbicides (Mortensen et al. 2012, Benbrook 2012; Waltz glyphosate’’ (Reuters 2015).
2015). In its first few years, GMGT crop introduction was Some scientists think that these new HT crops are a
often seen as leading to the application of fewer and more short-term solution, which is likely to increase the severity

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42 Environmental Management (2016) 57:31–48

Table 2 New traits for soybeans in the pipeline of the major agbiotech companies (adapted from Croplife 2015)
Near to market/advanced development Early development (research, discovery, early phase)
Type of trait Specific trait Company Type of trait Specific trait Company

Herbicide EnlistTM: 2,4-D ? Glyphosate. Dow Herbicide 4th Generation Monsanto


Tolerance AgroSciences Tolerance Herbicide
(HT) Tolerance
Enlist E3TM: 2,4- Dow Insect Resistance 3rd Generation Monsanto
D ? Glyphosate ? Glufosinate AgroSciences, Insect Protection DuPont
M.S. Hemipteran Pioneer
Technologies
Lepidopteran DuPont
Pioneer
Roundup Ready 2 Xtend. Monsanto Nematode Soybean Cyst Syngenta
3rd Generation HT: RR XtendTM Crop System Monsanto Resistance Nematode Bayer
(Glyphosate ? Dicamba tolerances) ? 3rd Soybean Cyst CropSc.
Mode of Action Nematode BASF,
2nd generation Monsanto
Soybean Cyst
Nematode
resistance
Multiple Mode DuPont Pioneer Disease Asian Soybean Rust DuPont
Resistance Pioneer
Syngenta
HPPDi ? Glufosinate Syngenta, Bayer Fungal resistance BASF
CropScience
BalanceTM GT/LL: Bayer Higher Yielding Next Generation Monsanto,
Glyphosate ? HPPDi ? Glufosinate CropScience, Higher Yielding BASF
BalanceTM GT: Glyphosate ? HPPDi M.S.
Technologies
Cultivance: Imidazolinone
Bayer CropSc.,
M.S.Tech
BASF, Embrapa/
Brazil
HT & IR Enlist E3TM ? ConkestaTM: 2,4- Dow Increased soy Oil DuPont
D ? Glyphosate ? Glufosinate ? 2 Bt Traits AgroSciences & Improved Pioneer
Meal Value
IR 2nd Generation Insect Protection Monsanto
Product Stearidonic Acid Omega-3 Monsanto
composition Vistive Gold Low Saturated, Zero Trans-Fat Monsanto
Oil
2,4-D, Glyphosate, Dicamba, HPPDi, Glufosinate, and Imidazolinone are herbicides
Bt Bacillus thuringiensis, EnlistTM Dow AgroSciences herbicide trait providing tolerance to glyphosate, 2,4-D and/or glufosinate, HPPD
inhibitors HydroxyPhenylPyruvate Dioxygenase inhibitor (herbicide family), LL LibertyLink, tolerance to glufosinate herbicides, RR Roundup
Ready (glyphosate tolerance)

of resistant weeds (Mortensen et al. 2012; Nature’s Edi- more thorough investigations before issuing approvals
torial 2014). Even the Committee on the Impact of (Bark et al 2014; Beyond Pesticides 2014; Freese 2014a, b;
Biotechnology on Farm-Level Economics and Sustain- Public Comments 2014, 2015).
ability of the US National Research Council warned that if Meanwhile, in the last few years, agbiotech companies
new GM cultivars ‘‘are managed in the same fashion as the and the main corn and soybean growers’ associations
current genetically engineered HR cultivars, the same promoted a quick authorization of these new HT crops,
problems of evolved herbicide resistance and weed shifts without conducting an Environmental Impact Statement
may occur’’ (Ervin et al. 2010). Environmental and con- (EIS).1 For example, the American Soybean Association
sumer organizations, such as Beyond Pesticides or Center
for Food Safety, have also warned about the risks of the 1
To determine that a GM plant is no longer considered a regulated
associated herbicides and have asked the USDA to conduct article, APHIS evaluates data submitted by the Company and

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Environmental Management (2016) 57:31–48 43

wrote in a letter to The Animal and Plant Health Inspection was classified as ‘‘probably carcinogenic for humans’’
Service (APHIS), the regulatory agency: (IARC 2015). Besides, for several years, some scientists, as
well as many environmental and consumer organizations,
‘‘Soybean farmers need new technologies such as
have considered glyphosate formulations as dangerous,
dicamba-tolerant soybeans to increase yields, manage
notably because of their adjuvants (Bøhn et al. 2014;
weed resistance and maintain profitability. (…)
Bradberry et al. 2004; Székács and Darvas 2012). As
Conducting a time-consuming analysis [EIS] (…)
glyphosate is frequently used in HT soybean and corn,
will cause a significant delay in bringing needed
some people are also increasingly expressing concerns
technologies to growers. (…)To meet growing global
about food derived from these crops; this has generated a
demand and maintain the United States as the largest
great movement requiring the labeling of GM food in the
producer of soybeans globally, growers need access
USA (Kling 2014; McFadden and Lusk 2013).
to new and effective technologies (…) ASA advises
Because of the high impact of herbicide-resistant weeds,
USDA (…) to expedite the full deregulation of
weed scientists, crop advisors, and GM seed companies
dicamba-tolerant soybeans’’ (ASA 2013).
prompt farmers to adopt better weed management prac-
An identical statement was expressed by the Weed tices. In addition, the solution the involved companies put
Science Society of America in its letter to APHIS where it forward is to shift toward GM crops with tolerance trait to
‘‘urges USDA to expedite the necessary reviews leading to glyphosate (or another herbicide) stacked with one or two
final approval of 2,4-D resistant corn and soybeans and other HT traits such as tolerance to 2,4-D, Dicamba, glu-
dicamba resistant cotton and soybeans’’ (WSSA 2013). For fosinate, etc. The aim is to cope with the current issue
the time being, it seems difficult to quickly stop using while continuing with the use of HT crops. ‘‘Dicamba-
herbicides in large-scale farming, and the involved com- resistant crops can be a valuable asset in strategies to
panies always put forward that their new herbicides and control currently existing herbicide-resistant weeds and to
GM crops will help farmers fight ‘‘superweeds’’ and meet a suppress the appearance of additional herbicide-resistant
growing food demand. If the organic market is growing, its weeds that ultimately could threaten the long-term use and
share remains small: in the USA, only 0.2 % of soybean value of current herbicides and herbicide-resistant crops.’’
area was certified organic in 2011. (Behrens et al 2007). Besides this, the backlash of GR
weeds is often minimized. However, with these planned
HT crops, there could be a risk of inducing additional weed
Conclusion resistance to the associated herbicides, to which some
weeds are already resistant (Mortensen et al. 2012; Powles
Today, herbicide-resistant weeds have become an impor- and Yu 2010). This may worsen the problem of HR weeds,
tant issue, notably in HT crops and in the USA. As many as it may lead to an increase in multi-resistance, which is
transgenic crops are HT and as the huge majority of these on the rise and much more difficult to control (Harker et al.
are tolerant to glyphosate, GR weeds call into question the 2012; Heap 2015). Furthermore, this strategy increases
first generation of HT crops, at least in certain areas. In herbicide applications and includes the use of some rela-
some countries such as the USA, Argentina, and Brazil, HT tively harmful weedkillers.
crops are cultivated in very large areas and play a major Faced with the problem of GR weeds, many US farmers
economic role. Therefore, the impact of glyphosate-resis- are looking for rapid solutions. After having grown HT
tant weeds is significant. Moreover, glyphosate is an crops for nearly two decades, farmers have frequently
important weedkiller, since it is by far the most sold her- seemed somewhat reluctant to search for new ways to
bicide in the world. Because of its characteristics, some manage weeds. Several factors can explain farmers’ atti-
weed scientists have called it ‘‘a once-in-a-century herbi- tudes: the necessity of rapid economic results, particularly
cide’’ (Duke and Powles 2008) and, in an interview by when they are in debt, the pressure from landowners, the
journalist David Bennett from Delta Farm Press on 10/02/ uncertainty of alternative methods, and risk aversion
2005, Powles compared it to penicillin: ‘‘glyphosate is a (Cowan and Gunby 1996). Moreover, assessment of BMPS
very precious resource. I’d argue that glyphosate is up there or Integrated Pest Management (IPM) adoption is rather
with penicillin as a once-in-a-hundred-years discovery.’’ difficult to do by telephone or even face-to-face surveys or
However, in a 2015 reassessment by experts, glyphosate by questionnaire. Indeed, it is difficult to adequately
describe these practices by just a few options or sentences,
Footnote 1 continued and then to ask the respondents if they are implementing
analyzes publicly available scientific data, as well as comments
them or have implemented them during the last campaign.
received from the public on the petition for non-regulated status and
its associated Environmental Impact Statement (EIS) on one hand and This common kind of surveys is better adapted to stan-
plant pest risk assessments on the other hand (APHIS 2014). dardized practices and less to BMPs or IPM (Puente et al.

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44 Environmental Management (2016) 57:31–48

2011). Nevertheless, the continuation of HT crops with while it was heavily investing in biotechnology, plant
other herbicide tolerance traits, stacked with the glyphosate breeding, and germplasm, i.e., glyphosate sales could
tolerance trait, may be considered as a kind of treadmill partly finance its costly research and development invest-
(Binimelis et al. 2009; Harker et al. 2012; Beckie and Hall ments and its buyouts of seed companies (Bonny 2011).
2014). Therefore, a number of farmers and weed scientists Furthermore, many American and Latin-American farmers
think that a new paradigm, a new way of tackling weed were attracted by HT crops. When GR weeds have begun
management and weed resistance to herbicides, is to develop and spread, this direction in biotech-derived
necessary. applications has continued to be pursued. So agbiotech
This would be, notably, integrated weed management companies are looking to add new herbicide tolerance traits
(IWM) which ‘‘can be defined as a holistic approach to and to stack them, rather than to gradually diminish reli-
weed management that integrates different methods of ance on these kinds of traits. The main reason is probably
weed control to provide the crop an advantage over weeds’’ that HT traits are profitable and provide revenues,2 while
(Harker and O’Donovan 2013). So, IWM combines the the major companies are investing in other future tech-
coordinated use of multiple techniques to reduce weed nologies. The HT traits appears more lucrative at present
pressure, instead of putting the main emphasis on herbi- and more assured for the near future, before the eventual
cides as in conventional weed control (Ehler 2006; Harker launching and marketing of the next kinds of traits or
2013; Knezevic 2014; Owen et al. 2014). IWM ‘‘empha- innovations. Indeed, other kinds of trait dealing with food
sizes the combination of management techniques and sci- quality, drought tolerance, bioenergy, chemical, and poly-
entific knowledge in a manner that considers the causes of mers, which have often been presented as the next waves of
weed problems rather than reacts to existing weed popu- agricultural biotechnology, are under development (Ri-
lations. The goal of weed management is the integration of croch and Hénard-Damave 2015). Companies are also
the best options and tools (…) The best approach may be to investing in other biotech applications and other lines of
integrate cropping system design and weed control strate- products, such as biopesticides, as well as tools for farmers
gies into a comprehensive system that is environmentally to gather and analyze field-level data for precision farming.
and economically viable’’ (Buhler 2002). Thus IWM Thus HT crops may be still used for some time, while the
‘‘provides opportunities to reduce selection pressure for next products or services are under development.
weed resistance’’ (Harker 2013). Among other aspects,
IWM requires better knowledge on weeds, crops, and their Acknowledgments This article is the result of a research work
carried out without special funding, i.e., with the basic support pro-
interactions, preventive measures against weed infestation, vided by INRA (French National Institute for Agricultural Research),
early detection, rapid response, regular monitoring of which is a public research institute and a publicly funded institution.
weeds, and integrated use of several methods, such as crop
rotation, cover crops and mulches, reduced tillage, preci-
sion agriculture, adequate seeding rates, seed quality, etc. References
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