# Herbicide-tolerant transgenic crops and resistant weeds, overview and agro-economic impacts

Sylvie Bonny

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Sylvie Bonny. Herbicide-tolerant transgenic crops and resistant weeds, overview and agro-economic impacts. 29 th International Conference of Agricultural Economists, International Association of Agricultural Economists (IAAE). INT., Aug 2015, Milan, Italy. 25 p. hal-01568874

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# Herbicide-Tolerant Transgenic Crops and Resistant Weeds: Overview and Agro-economic Impacts

By Sylvie Bonny,

INRA, UMR 210 Economie publique, F-78850 GRIGNON, FRANCE
AgroParisTech, UMR Economie publique, F-78850 GRIGNON, FRANCE

Genetically modified (GM) crops have been rapidly adopted where approved. However, GM herbicide-tolerant (HT) crops have been the most cultivated GMOs since 1996. Their cultivation involves the use of an associated herbicide, generally glyphosate. The repetition of glyphosate-tolerant crops and of glyphosate only applications in the same fields without sufficient alternation and herbicide diversity has contributed to the appearance of glyphosate-resistant weeds, which are now a significant issue. This paper examines the spread of GMHT crops worldwide, and their outcomes as regards herbicide use in the case of the USA. It then addresses the global development of glyphosate-resistant weeds and its impact, particularly focusing on the USA, where glyphosate-resistant weeds are an important issue. Finally the way the involved actors are coping with the spread of resistant weeds is studied. This illustrates that scientific progress needs adequate direction, implementation and use to sustainably and lastingly contribute to productivity growth.
## Acronyms

<table><tr><td>BMPs</td><td>Best Management Practices</td><td>HR</td><td>Herbicide-Resistant (for weeds)</td></tr><tr><td>GM:</td><td>Genetically Modified</td><td>HT:</td><td>Herbicide-Tolerant (for crops)</td></tr><tr><td>GMHT:</td><td>Genetically Modified Herbicide-Tolerant</td><td>USDA:</td><td>United States Department of Agriculture</td></tr><tr><td>GMGT</td><td>Genetically Modified Glyphosate-Tolerant</td><td>APHIS:</td><td>USDA Animal and Plant Health Inspection Service</td></tr><tr><td>GR:</td><td>Glyphosate-Resistant (for weeds)</td><td>USDA-ERS:</td><td>USDA Economic Research Service</td></tr><tr><td>GT:</td><td>Glyphosate-Tolerant (for crops)</td><td>USDA-NASS:</td><td>USDA National Agricultural Statistics Service</td></tr></table>

# 1. Introduction

Since their beginnings, transgenic crops have been the subject of debate and controversy in spite of their quick adoption by farmers where they were available. For the last 15 years, a new factor has fueled the controversy: the development of weeds that are resistant to glyphosate, since GM glyphosate-tolerant (GT) crops are the most widespread GMOs. Admittedly, since the 1950s when weedkillers began to be widely used, 246 herbicide-resistant weeds have appeared over the years and many weed species have developed resistance to 22 of the 25 known herbicide sites of action and to 157 different types of herbicide (Heap, 1997, 2014, 2015). This paper focuses mainly on glyphosate, because it is by far the most widely used herbicide and because, since 1996, the majority of GM crops have been glyphosate-tolerant. Hence, they are greatly affected by glyphosate-resistant (GR) weeds. Although there are fewer weed species resistant to glyphosate today than there are species resistant to some other herbicides, the impact of GR weeds is substantial. Indeed, if a GMGT crop can no longer be weeded by glyphosate, it seems to be called into question. GT crops are often described by their promoters and supporters as having revolutionized farming and as having provided significant agro-economic and environmental benefits, which may now be challenged by the rise of GR weeds (Behrens et al., 2007). GT crops have induced a repeated use of glyphosate, without sufficient alternation of weedkillers or weeding practices. This has contributed to the evolution of resistant weeds. In a similar manner, many pests and pathogens have developed resistance to pesticides and drugs (Bourguet et al., 2013; Tabashnik et al., 2014).

It seems useful to study the importance of glyphosate-resistant weeds in relation to GMHT crops in more depth, as well as their effects and the remedial measures that the involved stakeholders are implementing or looking for. Indeed, if GR weeds are rather often mentioned in the media, their real development and consequences are poorly known, except by some specialists. After the
introductory section, the second part of this paper describes the worldwide expansion of GMHT
crops and some of its outcomes in terms of herbicide application, particularly in the case of the
USA. The development of herbicide-resistant weeds, notably of glyphosate-resistant weeds, is
addressed in the third section of this paper, as well as some of its side-effects. The last section
examines how the GM seed industry, weed scientists, farmers, and advisors cope with the
development of weed resistance.

Links between HR weeds and HT crops

To many biotechnology promoters, herbicide-resistant weeds are only a herbicide problem, not a
GMO problem. However, glyphosate-resistant weeds are linked to GM crops with respect to
several aspects:

- for two decades, GM glyphosate-tolerant (GMGT) crops have been by far the most numerous GM crops.

- GMGT crops inherently imply the application of glyphosate on the crop, and glyphosate has replaced many other herbicides used before. Hence, on GMGT crops, there has been little or no alternation of herbicide applications or of weeding techniques. In addition, some crop rotations have involved a frequent repetition of glyphosate-tolerant crops. Thus there has been an overreliance on glyphosate.

- in multiple locations, because of glyphosate-resistant weeds, glyphosate is losing its efficacy in weeding transgenic GT crops. In those places, GMGT crops seem to be called into question.

- the number of weed species resistant to glyphosate is higher for GMGT crops -soybean, corn, cotton- than for non-glyphosate tolerant crops.

- a low number of new herbicides has been put onto the market in the last decade because of the costs to launch a new herbicide and of the high rate of adoption of GMHT crops. This increases the impact of resistant weeds, since few new weedkillers can replace the old weedkillers that are now becoming ineffective.

Therefore, there exists a link between GMGT crops and increasing glyphosate-resistant weeds, because GT crops have furthered an increased use of glyphosate, which has resulted in the selection of GR weeds.

This article is based on an extensive search for, and analysis of, updated precise data and recent statistics on GM herbicide-tolerant crops, particularly GT crops, and on herbicide-resistant weeds,
especially glyphosate-resistant weeds, as well as on their side-effects. Data on HT crops is drawn
from ISAAA reports (James, 2014) and from the US Department of Agriculture (USDA) Economic
Research Service's statistics (USDA-ERS, 2014a). For the herbicide use on GMHT crops in the
USA, we particularly analysed survey results from the USDA National Agricultural Statistics
Service, notably the last ones (USDA-NASS, 1991-2013). However, these surveys of chemical
usage on field crops, which were generally annual for the main crops from 1990 to 2006, have
become much less frequent since 2006. After the 2006 survey on soybean, the next one was in
2012, and the following is scheduled for 2017 (USDA ERS, 2014b). Thus, the monitoring of
pesticide use on GM crops is less detailed. Admittedly, private surveys of chemical use on field
crops are made by some specialized companies, but their results are generally not accessible. With
regard to herbicide-resistant weeds, especially GR weeds, we examined data from "The
International Survey of Herbicide Resistant Weeds", which is a collaborative effort of world weed
scientists to report herbicide resistant weeds globally (Heap, 2015). In addition, besides doing a
literature survey, we looked for papers and presentations by weed scientists, seed companies, and
professional and environmental organisations.

## 2. The Widespread Planting of GMHT Crops and the Outcomes in Terms of Herbicide Use

From 1996 to 2014, the expansion of GM crops was rapid but uneven: in 2014, three countries (USA, Brazil, and Argentina) represented 77% of GM crop area, three crops (soybean, corn, and cotton) represented 95%, and two traits (herbicide tolerance and insect resistance) 99% (Table 1). Concerning GM traits, herbicide tolerance traits – increasingly often stacked with insect resistance traits – have been continually predominant over the last 18 years: they have always represented more than 81% of all traits (Fig. 1). In addition, the overwhelming majority of HT crops have been tolerant to glyphosate, while only a tiny percentage were glufosinate-tolerant, as was the case for HT corn in the first few years. However, the rate of adoption of GT crops was different between countries as well as among crops, depending on regulatory aspects and agro-economic profitability (Fig. 2).

When the context was favourable, GT crops were rapidly adopted, since they allow for easier weed
management in their first years. This is particularly the case for HT soybeans, which are the most
widely cultivated HT crops: in 2014, GT soybeans represented 50% of all HT crops, and about 80% of all globally cultivated soybeans. Their rate of adoption was rapid in the USA, Argentina, and Brazil. As there are variations between crops and contexts, it is necessary to choose a detailed case to present a more thorough assessment of the trends in herbicide use. The case of GT soybean in the USA will be discussed here as it is the most cultivated GM crop, and as USDA statistics provide unbiased data (based on random surveys) on herbicide use and on the percentage of GM crops within each crop.

For the GM crops in the USA, glyphosate applications replaced a large part of previously used herbicides (Bonny, 2008; Osteen and Fernandez-Cornejo, 2013). Between 1996 and 2005 the number of the different types of herbicide applied on soybean acreage diminished with the growing adoption of GT varieties (Figs. 3,4) (USDA-NASS, 2014). From 1996 to 2005, this decline led at first to a small decrease, then to stagnation in the total amount of herbicide applied per unit of soybean surface and in the number of applications. Thus, the environmental impacts of GT crops were frequently assessed as beneficial due to the replacement of some rather noxious herbicides used before by one herbicide, at that time generally considered to be more benign (glyphosate), and with the concomitant expansion of soil conservation practices. Indeed, glyphosate-tolerant crops may have facilitated the adoption of soil conservation practices (Bonny, 2011; Fernandez-Cornejo et al., 2014; Givens et al., 2009), which have significant advantages, such as preventing soil erosion and degradation, and diminishing soil leaching. The large-scale adoption of GMGT crops was favoured by diminishment of glyphosate prices that occurred when its patent expired in 2000 in the USA. Large quantities of glyphosate generics were produced in some countries, such as China. Thus, there has been a huge increase in global glyphosate use linked to the development of GT crops. Glyphosate became the main herbicide used globally. Its annual worldwide sales were approximately 5.5 billion USD in 2012, i.e. about 30% of the global herbicide market, far ahead of other herbicides. In the USA, glyphosate use multiplied tenfold from 1993 to 2007 (Grube et al., 2011). For soybean, the glyphosate proportion of total herbicides used grew from 4% in 1990-1993 to 89% in 2006.

In the first few years after the adoption of HT crops, a small decrease in herbicide use per soybean unit area was observed in comparison with the 1990 to 1996 period (Figs. 3, 4). Later, particularly after 2005, herbicide use per soybean unit surface started to rise again, and additional herbicides
were increasingly added to glyphosate. So, although GT crops induced a decrease in pesticide use at the beginning, a trend-reversal occurred rapidly, linked to the development of herbicide-resistant weeds (Bonny, 2008; Benbrooks, 2012).

### 3. The Expansion of Glyphosate-Resistant Weeds

Many herbicide-resistant weeds have appeared since the 1950s, when the use of weedkillers became widely spread. In late May 2015, there were "457 unique cases (species x site of action) of herbicide resistant weeds globally, with 246 species. Weeds have evolved resistance to 22 of the 25 known herbicide sites of action and to 157 different herbicides. Herbicide resistant weeds have been reported in 86 crops in 65 countries." (Heap, 2015). Herbicides do not cause weeds to evolve resistance per se. The manner in which herbicides are used is a major factor in explaining why weeds evolve resistance. Herbicides exert a high selection pressure on weed populations. Resistant weed populations develop from rare random genetic mutations that may exist in individuals within a weed population. Repeated use of the same herbicide (or herbicide mode of action) increases the frequency of these mutations by selection pressure, particularly in the absence of other weedkillers or weeding methods. Hence, some weed populations become predominant and are resistant to one or several herbicides.

Although many herbicide families now have HR weed populations, there are variations in susceptibility of the different weedkillers (Fig. 5). Today, there are fewer GR weeds than there are weeds that have developed resistance to some other herbicides. Nevertheless, the impact of GR weeds is strong since glyphosate is widely used and since GT crops are designed to tolerate this specific herbicide, which at first led to easier weed management. If several noxious weeds become resistant to glyphosate, the concept of GT crops becomes highly questionable.

The expansion of GR weeds was slow in the first few years. However, after 2003 it grew more rapidly. At the end of May 2015, there were 32 GR weeds in the world, of which 14 were in the USA (Fig. 6). The number of GR weeds per crop is high for GT crops, particularly soybean, corn, and cotton, as well as for orchards and grapes, on which glyphosate has been repeatedly applied (Fig. 7). The frequency of glyphosate treatments has been reinforced by the most current type of crop rotation. According to the data on crop production practices from the USDA Agricultural
Resource Management Survey (ARMS), in the USA in 2006, soybeans were preceded by corn on approximately 72% of acreage, and by another soybean on 13%. These preceding corn and soybean were themselves predominantly glyphosate-tolerant.

The impact of GR weeds on a given crop varies according to several factors: location, type of weeds, total number of HR weeds, etc. GR weeds are not all the same; some have high interference with crop yields, such as Palmer amaranth (Ward et al., 2013). Moreover, some weeds have developed multiple herbicide resistances, i.e. resistance to several herbicides with different modes of action (Beckie and Tardif, 2012). Hence, their control is more difficult as it is limited to fewer management choices since a reduced number of herbicides can be used. In the USA, some weeds such as Palmer Amaranth (*Amaranthus palmeri*), Tall Waterhemp (*Amaranthus tuberculatus*), Common Ragweed (*Ambrosia artemisiifolia*), Giant Ragweed (*Ambrosia trifida*) have developed resistance to glyphosate and to one or more other herbicides (Heap, 2015). Their impact is increased by this multi-resistance, which seems to be increasing (Rabobank, 2012; Service, 2013).

Globally, 24 countries have experienced GR weeds, although their number and expansion is limited in many countries (Heap, 2015). The USA has experienced the highest number (14) of GR weeds, but their growth rate has slowed since 2008 due to the increased use of other weedkillers and the implementation of better weed control practices. However, the US states growing HT crops are increasingly affected by GR weeds: in late May 2015, 39 US states have experienced the rise of one or several GR weeds – and up to ten GR weeds in one state (Fig. 8). It is difficult to assess the global crop area affected. Heap (2013) estimated that in 2012, the area affected by GR weeds was about 6.3 million ha globally, of which approximately 6 million ha (95%) were in the USA in GT cropping systems; however, some assessments were much higher.

## 4. How Do Weed Scientists, Farmers, and Companies Cope With Glyphosate-Resistant Weeds?

The development of GR weeds has a broad impact. In HT crops and elsewhere, glyphosate is now often increasingly supplemented, and sometimes replaced, by other herbicides; however, the latter are frequently more harmful and difficult to use due to their profile (Boerboom, Owen, 2007). The result appears to be a loss as regards environmental aspects (Service, 2007). More generally, in
some areas glyphosate's loss of efficacy is seen as having great repercussions because of the
economic importance of GT crops and the widespread use of glyphosate. The control of weeds is
more difficult. Since 1997, the number of new active herbicide ingredients put onto the market has
declined, and, in the USA, the number of patents dealing with new weedkillers has also dropped
(Adler, 2011; Duke, 2012; Gerwick, 2010). This decrease in the commercialisation of new active
ingredients is partly an outcome of the expansion of GT crops. Indeed, the market for new
herbicides has grown smaller, and at the same time, the number of agrochemical companies has
been reduced due to consolidation in the crop protection industry; in addition, the
commercialisation costs have increased. Journalists and organisations opposed to GM crops often
greet glyphosate-resistant weeds with sarcastic comments such as "revenge of the weeds",
according to a paper title (Coombs, 2012), seeing it as almost a fulfilment of their predictions.
However, the appearance of these weeds does not mean that glyphosate will no longer be used.

4.1. *Weed scientists.*

In the 1990s, Monsanto believed that there was almost no risk of the occurrence of glyphosate-
resistant weeds, because of glyphosate's specificities (Bradshaw et al., 1997). Thus, advice for good
herbicide management was, most likely, not provided at the beginning of the diffusion of HT
varieties, and the weed scientists who did provide some were hardly listened to. Yet, in 1996, a first
weed species resistant to glyphosate was discovered in Australia. At that time several weed
scientists warned about the risk of the development of glyphosate resistance with its increased usage
and call for integrated weed management strategies (Powles et al., 1998).

Since 2005, in contrast, many measures have been recommended and are being sought by the
concerned stakeholders in order to cope with GR weeds (Frisvold and Reeves, 2010; Green and
Owen, 2011; Gustafson, 2008; Nandula, 2010). Many scientists from weed science extension
services and universities have become involved in this issue and many meetings and conferences
have been dedicated to this topic. Weed scientists advocate increased research activities, the
exploration of new approaches, as well as better weed control management (Gressel, 2010; Vencill
et al., 2012). The need for "glyphosate stewardship" is stressed, which "refers to the management
decisions and practices subsequently employed to preserve the utility of a crop trait" (Beckie,
2011). Weed scientists emphasise the importance of diversity in weed management and recommend
the use of Best Management Practices (BMPs), in order, notably, to understand the biology of
weeds, diversify weed management practices, use multiple herbicide mechanisms of action, and prevent weed seed production and spreading (Norsworthy et al., 2012; Stokstad, 2013 Owen et al. 2014).

## 4.2. Farmers’ attitudes.

Before the 2005-2006 period, Webster and Sosnokie (2010) wrote, “agricultural practices aimed at delaying or preventing the development of herbicide resistance are not viewed as being economical in the short term, and are not readily used by all growers.” To these authors, at least two factors kept farmers from adopting better weed management practices around 2005: (i) the belief that a new technology would be developed to solve the resistance problems; and (ii) the belief that resistance management strategies would be futile. Actually, a survey of growers developed by weed scientists from six states in 2005–2006 showed that “at this time, farmers did not have a high level of awareness of the potential risks to the sustainability of the GR crop systems with regard to evolved glyphosate resistance” (Owen et al., 2011). Frisvold and Reeves (2010, 2014), who analysed a telephone survey of farmers conducted at the end of 2007 concerning their use of ten BMPs to delay weed resistance, assessed that "the current rate of BMP adoption has proved insufficient to delay resistance in many areas,” notably the adoption of some of the most critical BMPs.

However, more recent studies showed that “growers are moving towards a better understanding of the implications of their herbicide use practices and thus improved sustainability for GR crops and glyphosate” (Johnson et al., 2009; Owen et al., 2011). Indeed, since 2005-2006, cultural practices have begun to change, given the increasing extent of GR weeds and also the advice provided by weed scientists, grower associations, advisors, and seed companies. Farmers have more frequently applied other herbicides in addition to glyphosate (Figs. 2, 3). A 2010 survey of 1,300 growers from 22 US states showed that in 2010, a higher percentage of growers integrated herbicides other than glyphosate, even if many farmers continued to use only glyphosate (Prince et al., 2012). Another survey conducted at the end of 2011 in the Mid-South of the USA testified that some BMPs, particularly cultural practices, are less implemented because of extra costs, time constraints, weather, and a certain difficulty on the part of a number of farmers in adopting a proactive strategy when they have not experienced resistant weeds on their own farms (Riar et al., 2013). More recently, a US scientific team surveyed Certified Crop Advisors (Asmus et al., 2013). When asked
to describe the growers' actions or thoughts when considering the adoption of weed resistance BMPs, 40% of survey takers said that farmers would only adopt BMPs if resistant weeds became a problem in their fields. However, 15% responded that farmers were trying BMPs on a few acres first, and 13% that growers were plunging into BMPs.

At the farm level, one main impact of GR weeds is that farmers need to use weed control methods other than glyphosate applications alone, varying from the application of other herbicides to mechanical weeding, and sometimes hand weeding to dig out certain weeds (Waltz, 2010). The most common way is to apply some additional herbicides to GT crops, notably persistent herbicides. These additional weeding methods have induced a rise in related costs, particularly after 2005 and above all after 2011, and especially for certain weeds (Rabobank, 2012; Service 2013; Sosnoskie and Culpepper, 2014).

The application of additional herbicides also leads to a certain increase in the total amount of herbicide applied (Fig. 3), as well as to the loss of some of the advantages farmers had derived from glyphosate-tolerant crops, such as easier weed control. Another notable consequence is the side-effect of GR weeds on soil conservation practices. As GT crops may have contributed to the adoption of the latter, nowadays the expansion of GR weeds, particularly of GR Palmer amaranth, threatens conservation tillage (Duke and Powles, 2009). In some instances, tillage is one of the few effective options to manage HR weeds (CAST, 2012; Price et al., 2011). The necessity of increasing tillage again in order to cope with some weeds is considered a substantial loss, because of the environmental and agro-economic benefits of soil conservation practices. Figure 9 shows the evolution in the rate of adoption of several resistance management practices by soybean growers from 1996 to 2012. Throughout these 16 years, there were noticeable changes in the use of herbicides other than glyphosate, rotation of herbicides, and tillage or cultivation for weed control. There was a turning point in these practices in 2005-2006 resulting from the necessity to cope with GR weeds.

In addition, farmers and other operators have to implement measures to avoid the spreading of GR weeds in the neighbourhood, which complicates some farm operations (Livingston et al. 2015). GR weeds can easily spread from one field or an area to another, which has a great impact on the newly affected area. Herbicide resistance can be transferred through the weed pollen, vegetative structures
(rhizomes, tubers) and above all weed seeds (Bagavathiannan et al., 2013). Weed seeds can be disseminated very far by transportation, in the same way as many plant pathogens have spread from one country or continent to another. Besides, some herbicides which could be increasingly used with the HT crops under approval need to be applied cautiously, because of their risk of drifting (Egan et al., 2014). The involved companies have conducted investigations to develop new formulations reducing off-target movement, but will they be sufficient?

### 4.3. *The companies' answers to the spread of resistant weeds.*

The involved agbiotech/ agchemical firms often qualify weed resistance as a common issue of pesticide resistance that should be resolved with the use of other weedkillers, stating that this is not linked to genetic engineering. These companies, such as Monsanto, Pioneer, Dow, Bayer, and Syngenta, propose weeding programs with complementary herbicides and other weed management practices. They are also working to market new HT plants that are tolerant to other herbicides. They work sometimes on new single HT traits, but mainly on combined traits of resistance to glyphosate and to other herbicide(s), i.e. to launch new HT crops with stacked herbicide tolerance traits (Table 2). In addition to being glyphosate-tolerant, the new varieties will be tolerant to other herbicides such as dicamba, 2,4-D, ALS inhibitor, mesotrione, or isoxaflutole (Duke and Powles, 2009; Feng et al., 2010; Green and Owen, 2011, Green 2014; Croplife 2014; USDA-APHIS 2015). The first new HT crops were approved in 2014 and early 2015, following registration of the corresponding herbicide combinations. In early April 2015 for example, "Enlist Duo" (2,4-D + glyphosate) was approved by the US Environmental Protection Agency for use in 15 states. These new HT crops could be cultivated in 2016 and later.

Yet, these new HT traits raise significant questions, because some involved herbicides (which sometimes date back from several decades, such as 2,4-D, commercially released in 1946) do not have a very favourable toxicological or environmental profile. The planned GMHT crops will lead to an increase in the use of herbicides, and, above all, will lead to using some more risky herbicides, even if their registration conditions require a safe use. In its first few years, GMHT crop introduction was often seen as leading to applying more benign herbicides than those previously used. Today, there is risk of the opposite occurring: because of GR weeds, some more toxic herbicides are likely to be used in the next few years to complement glyphosate. These new HT crops represent a substantial part of the upcoming new GM soybeans (Croplife, 2014) (Table 2). In
addition, the high use of glyphosate appears more and more questionable, particularly since in
March 2015 the International Agency for Research on Cancer (IARC) classified this herbicide as
"probably carcinogenic to humans" (Guyton et al. 2015; IARC 2015). Moreover, some new HT
plants such as wheat, rice, and sugarcane are the subject of field trials (James, 2014), a prelude to a
possible future commercialization if they are authorized.

Some scientists think that these new HT crops are a short-term solution, which is likely to increase
the severity of resistant weeds (Mortensen et al., 2012; Nature's Editorial, 2014). Even the
Committee on the Impact of Biotechnology on Farm-Level Economics and Sustainability of the US
National Research Council, who published a report on the impact of GM crops on farms, warned
that if new GM cultivars "*are managed in the same fashion as the current genetically engineered HR cultivars, the same problems of evolved herbicide resistance and weed shifts may occur*" (Ervin
et al., 2010). Environmental organisations have warned about the risks of the associated herbicides
and have asked the USDA to conduct more thorough investigations before issuing approvals.

Meanwhile, agbiotech companies and the main growers associations are promoting the quick
authorisation of these new HT crops, without conducting an Environmental Impact Statement (EIS).
For example, the American Soybean Association wrote in a letter to The Animal and Plant Health
Inspection Service (APHIS), the regulatory agency, that soybean growers quickly needed these new
technologies to increase yields, manage weed resistance and maintain profitability, as well as to
maintain the United States as the largest producer of soybeans globally while meeting growing
global demand (ASA, 2013). An identical statement was expressed by the Weed Science Society of
America in its letter to APHIS where it "*urges USDA to expedite the necessary reviews leading to final approval of 2,4-D resistant corn and soybeans and dicamba resistant cotton and soybeans*" (WSSA, 2013).

**Conclusion**

Today, herbicide-resistant weeds have become an important issue, notably in herbicide-tolerant
crops and in the USA. As many transgenic crops are herbicide-tolerant and as the huge majority of
the latter are tolerant to glyphosate, GR weeds call into question the first generation of HT crops, at
least in certain areas. In some countries such as the USA, Argentina, and Brazil, GT crops are
cultivated in very large areas and play a major economic role. Therefore, the impact of glyphosate-
resistant weeds is significant. Moreover, glyphosate is an important weedkiller, since it is by far the
most sold herbicide in the world. Because of its characteristics, some weed scientists have called it
"*a once-in-a-century herbicide*" (Duke and Powles, 2008) and, in an interview by journalist David
Bennett from Delta Farm Press on 10/02/2005, Powles compared it to penicillin: "*glyphosate is a
very precious resource. I'd argue that glyphosate is up there with penicillin as a once-in-a-
hundred-years discovery.*" However, many scientists and environmental or consumer organisations
do not share these views, and consider glyphosate formulations as dangerous, notably because of
the 2015 classification of glyphosate as "probably carcinogenic to humans" (Guyton et al. 2015;
IARC 2015) and because of adjuvants and of degradation products such as AMPA
(aminomethylphosphonic acid). Some people express also concerns about food derived from GT
crops.

Because of the high impact of herbicide-resistant weeds, weed scientists, crop advisors, and GM
seed companies prompt farmers to adopt better weed management practices. Since 2005, several of
them have been gradually implemented, and the number of GR weeds from 2010 to 2014 has
stabilized to 14. In addition, the solution the involved companies propose is to offer either new GM
crops tolerant to other herbicides (2,4-D, Dicamba, glufosinate, etc.), or, more often, GM crops with
a glyphosate-tolerance trait stacked with one or two other HT traits. The aim is to endeavour to
pursue the path of HT crops with the use of additional herbicide(s) complementing glyphosate
(Behrens et al., 2007). Besides this, the backlash of GR weeds is frequently minimised or denied.
However, with these planned HT crops, there may be a risk of inducing additional weed resistances
to the associated herbicides, which sometimes date back several decades, and to which some weeds
are already resistant (Powles and Yu, 2010; Mortensen et al., 2012). This may worsen the problem
of HR weeds, because it may to lead to an increase in multi-resistance, which is much more difficult
to control (Harker et al., 2012). Furthermore, this strategy increases herbicide applications and
includes the use of some relatively harmful weedkillers.

Faced with the problem of GR weeds, it seems that many US farmers are looking for rapid
solutions, such as crops with additional tolerance to other herbicides. The growers association has
asked for the expedited authorisation of new HT crops and hence, for the pursuit of a solution in
this direction, since GT crops allowed for easier weed management and were well-suited to no-
tillage. After nearly two decades of HT crops, farmers frequently seem somewhat reluctant to search for new ways to manage weeds. Several factors can explain farmers' attitudes: the necessity of rapid economic results, particularly when they are in debt, the pressure from landowners, the uncertainty of alternative methods, and risk aversion (Cowan and Gunby, 1996). Yet, this continuation of HT crops with other herbicide tolerance traits, either stacked with the glyphosate-tolerance trait or replacing it, may be considered as a kind of treadmill (Binimelis et al., 2009; Harker et al., 2012).

A number of farmers and weed scientists think that a new paradigm, a new way of tackling weed management and weed-resistance to herbicides, is necessary. This would be, notably, *integrated weed management* (IWM), which integrates and combines the coordinated use of multiple techniques for optimising weed control in an ecologically and economically sound manner (Ehler, 2006; Harker, 2013). IWM requires, amongst other aspects, more knowledge, preventive measures, regular monitoring of weeds, and integrated use of several methods, such as crop rotations, cover crops and mulches, reduced tillage, crop interactions, etc. However, IWM implies some uncertainty in the results, all the more so as there has been less research in this domain over the last few years. These facts explain why there are some difficulties and a certain reluctance to adopting this method, not only on the part of farmers, but also scientists (Shaner and Beckie, 2014).

At the outset, the way that biotechnology was presented led to the expectation that it would lead to a better use of the biological capacities of plants and to a valorisation of life processes. Thus, it was hoped that it would contribute to freeing agriculture from pesticides through a better use of life processes. On the contrary, until today, the main widespread implementation of genetic engineering in agriculture has been HT crops, which lead to a crop's linkage to a herbicide (generally glyphosate) instead of contributing to freeing it from pesticides. This first kind of application is often considered as resulting from economic reasons, because Monsanto could sell glyphosate while it was heavily investing in biotechnology, plant breeding, and germplasm, i.e. glyphosate sales could partly finance its costly research and development investments and its buyouts of seed companies. In addition, American farmers were interested and HT crops were widely adopted where approved. When GR weeds began to develop and spread, this direction in biotech-derived applications continued to be pursued, even if other kinds of traits are under development. Moreover, new GM glyphosate-tolerant or other herbicide-tolerant GM crops are under investigation.
Agbiotech companies appear to be unwilling to gradually diminish reliance on these kinds of herbicide tolerance traits, probably because their profitability appears better and more assured than that of some future developments, especially since many American farmers seem to be willing to continue HT crops. Agbiotech companies are looking to add new herbicide tolerance traits, rather than to progressively withdraw from this direction and choose other developments, notably other agbiotech applications. The other kinds of agbiotech traits dealing with drought tolerance, health, nutrition, food quality, bioenergy, chemical and polymers, etc., which have often been presented as the next wave of agbiotech developments, are under investigation, but the first generation is still being pursued, despite the high economic and environmental costs of GR weeds.

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Tables and Figures

<table><caption>**Table 1.** Predominance of three countries, three crops, and one trait in total GM crop area in the world in 2014 (area in Million ha). The last line gives the percentage of the three main countries, crops, or traits in total GM crop area (from James, 2014).</caption><thead><tr><th>Country</th><th>Area (Mha)</th><th>Crop</th><th>Area (Mha)</th><th>GM trait</th><th>Area (Mha)</th><th>% total including stacked traits</th></tr></thead><tbody><tr><td>USA</td><td>73</td><td>Soybean</td><td>91</td><td>Herbicide tolerance (HT) alone</td><td>103</td><td rowspan="2">} HT: 85% <br> } IR: 43%</td></tr><tr><td>Brazil</td><td>42</td><td>Corn</td><td>55</td><td>Herbicide tolerance & Insect resistance</td><td>51</td></tr><tr><td>Argentina</td><td>24</td><td>Cotton</td><td>25</td><td>Insect resistance (IR) alone</td><td>27</td></tr><tr><td>% total GM crop area</td><td>77%</td><td>% total GM crop area</td><td>94%</td><td>% total GM crop area</td><td>99.8%</td><td></td></tr></tbody></table>

<table><caption>**Table 2.** New traits for soybeans in the pipeline of the major agbiotech companies (adapted from Croplife, 2014)</caption><thead><tr><th colspan="3">Near to market/Advanced development</th><th colspan="3">Early development (research, discovery, early phase)</th></tr><tr><th>Type of trait</th><th>Specific trait</th><th>Company</th><th>Type of trait</th><th>Specific trait</th><th>Company</th></tr></thead><tbody><tr><td rowspan="5">Herbicide Tolerance (HT)</td><td>Enlist™: 2,4-D + Glyphosate.</td><td>Dow AgroSciences</td><td rowspan="2">Herbicide Tolerance</td><td rowspan="2">4<sup>th</sup> Generation Herbicide Tolerance</td><td rowspan="2">Monsanto</td></tr><tr><td>Enlist E3™: 2,4-D + Glyphosate + Glufosinate</td><td>Dow AgroSciences, M.S. Technologies</td></tr><tr><td>Roundup Ready® 2 Xtend. 3<sup>rd</sup> Generation Herbicide Tolerance: RR® Xtend (Glyphosate + Dicamba tolerances) + 3<sup>rd</sup> Mode of Action</td><td>Monsanto</td><td rowspan="2">Insect Resistance</td><td rowspan="2">3<sup>rd</sup> Generation Insect Protection<br>Hemiptera/Stink Bug<br>Lepidopteran</td><td rowspan="2">Monsanto<br>DuPont Pioneer<br>DuPont Pioneer</td></tr><tr><td>Multiple Mode</td><td>Monsanto</td></tr><tr><td>HPPDi + Glufosinate</td><td>Syngenta, Bayer CropScience</td><td>Nematode Resistance</td><td>Soybean Cyst Nematode</td><td>Syngenta<br>Bayer CropSc.<br>BASF, Monsanto</td></tr><tr><td>Balance™ GT/LL: Glyphosate + HPPDi + Glufosinate</td><td>Bayer CropScience, M.S.Technologies</td><td>Disease Resistance</td><td>Asian Soybean Rust II</td><td>DuPont Pioneer<br>Syngenta</td></tr><tr><td>Balance™ GT: Glyphosate + HPPDi<br>Cultivance: Imidazolinone</td><td>Bayer CropSc., M.S.Tech<br>BASF, Embrapa/ Brazil</td><td>Fungal resistance</td><td></td><td>BASF</td></tr><tr><td>HT & IR</td><td>Enlist E3™ + 2 Bt Traits: 2,4-D + Glyphosate + Glufosinate + 2 Bt Traits</td><td>Dow AgroSciences</td><td>Higher Yielding</td><td>Next Generation Higher Yielding</td><td>Monsanto, BASF</td></tr><tr><td>IR</td><td>2<sup>nd</sup> Generation Insect Protection</td><td>Monsanto</td><td>Increased Oil & Improved Feed Efficiency</td><td></td><td>DuPont Pioneer</td></tr><tr><td>Product composition</td><td>Steridonic acid Omega-3 Vistive® Gold Low Saturated, Zero Trans-Fat Oil</td><td>Monsanto</td><td></td><td></td><td></td></tr></tbody></table>

Note: 2,4-D, Glyphosate, Dicamba, HPPDi, Glufosinate, Imidazolinone are herbicides

Acronyms:

Bt = Bacillus thuringiensis

Enlist™ = Dow AgroSciences herbicide trait providing tolerance to glyphosate, 2,4-D, glufosinate

HPPD inhibitors = HydroxyPhenylPyruvate Deoxygenase inhibitor (herbicide family)

LL = LibertyLink®, tolerance to glufosinate herbicides

RR = Roundup Ready® (glyphosate tolerance)
<figure><img src="image_12.png" /><figcaption>**Fig. 2.** Variations in the rate of adoption of glyphosate-tolerant crops in the USA: Percentage of HT varieties cultivated in soybean, corn, and cotton areas, 1997-2014 (USDA-ERS 2014)</figcaption></figure>

<figure><img src="image_13.png" /></figure>
<figure><img src="image_14.png" /><figcaption>**Fig. 4.** Trends in herbicide applied on soybean in the USA, 1990-2012 (herbicide quantity in kg/ha, all soybean acreage) (same source as Fig. 3).</figcaption></figure>

<figure><img src="image_15.png" /></figure>
<figure><img src="image_16.png" /><figcaption>**Fig. 6.** Number of glyphosate-resistant weed species globally and in the USA, and global GM herbicide-tolerant crops area, 1996 - end May 2015 (adapted from Heap, 2015; James, 2014).</figcaption></figure>

<figure><img src="image_17.png" /></figure>
<figure><img src="image_18.png" /><figcaption>**Fig 8.** Number of GR weed species in the USA and number of USA states with GR weeds, 1998- end May 2015. (Author's calculation from Heap, 2015)</figcaption></figure>

<figure><img src="image_19.png" /></figure>
<figure><img src="image_20.png" /><figcaption>**Fig. 9.** Rate of adoption of several resistance management practices by US soybean growers, 1996-2012 (adapted from Livingstone et al., 2015).</figcaption></figure>