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Review

Received: 21 August 2017 Revised: 2 December 2017 Accepted article published: 9 December 2017 Published online in Wiley Online Library:

(wileyonlinelibrary.com) DOI 10.1002/ps.4821

The challenge of herbicide resistance around


the world: a current summary
Mark A Peterson,a* Alberto Collavo,b Ramiro Ovejero,c Vinod Shivraind
and Michael J Walshe

Abstract
Herbicide-resistant weeds have been observed since the early years of synthetic herbicide development in the 1950s and
1960s. Since that time there has been a consistent increase in the number of cases of herbicide resistance and the impact of
herbicide-resistant weeds. Although the nature of crop production varies widely around the world, herbicides have become a
primary tool for weed control in most areas. Dependence on herbicides continues to increase as global populations migrate
away from rural areas to cities and the agricultural labor force declines. This increased use of herbicides and the concurrent
selection pressure have resulted in a rise in cases of multiple resistance, leaving some farmers with few or no herbicide options
for certain weed infestations. Global population and economic forces drive many farmer choices regarding crop production and
weed control. The challenge is how to insert best management practices into the decision-making process while addressing
various economic and regulatory needs. This review endeavors to provide a current overview of herbicide resistance challenges
in the major crop production areas of the world and discusses some research initiatives designed to address portions of the
problem.
© 2017 Society of Chemical Industry

Keywords: Asia; Australia; Europe; Latin America; North America; South America

1 INTRODUCTION Another measure of HR is the area infested with various HR


It is difficult to deny the importance of herbicides to modern crop biotypes. This is a much more difficult figure to ascertain.6 Results
production. In most developed nations, agriculture involves the from farmer surveys regarding resistance on their farms can be
widespread use of herbicides for weed control, and in develop- biased depending on the prominence of resistance to certain
ing countries, mass migration from rural to urban areas is reduc- herbicides in the news, product failures unrelated to resistance,
ing the labor pool for hand-weeding and other labor-intensive or discussions with neighbors that can lead to farmer perceptions
operations.1 Until the 1970s, reported instances of herbicide resis- about resistance on their farm that may not be accurate. Detailed
tance (HR) appeared to be limited and lagged behind the number studies of resistance conducted by researchers that randomly
of resistance reports for insecticides and fungicides.2 However, by collect seed and run greenhouse screenings are usually done for
the 1980s, HR had begun to appear at a much greater rate. In some only one species within a limited geography due to cost. Similar to
areas, herbicides have become the only means by which weeds the situation with reported cases, estimates of infestations tend to
are controlled, leading to widespread HR by means of increasingly be more common in more developed agricultural areas.
powerful and complex resistance mechanisms.3,4 Within these limitations, this review endeavors to provide an
Current reports of confirmed resistance in various species can be overview of the current state of HR around the world, and to
found on the International Survey of Herbicide Resistant Weeds explore differences and commonalities among geographies as to
website.5 A few caveats must be stated regarding the data. The how resistance is developing and how farmers are dealing with the
survey depends largely on voluntary reporting and researchers problem.
are most apt to submit cases that involve the first instances
of resistance in a weed species, whether that be for a given
site of action (SOA) or new combinations of multiple resistance. ∗ Correspondence to: MA Peterson, Dow AgroSciences, 9330 Zionsville Road,
Once a given SOA/species resistance becomes more common, Indianapolis, IN 46268, USA. E-mail: mapeterson@dow.com
researchers tend to stop investigating and reporting cases of
a Dow AgroSciences, Indianapolis, IN, USA
that nature. Also, reporting of cases occurs most in areas where
there are more active university or institute scientists interested b Bayer AG Crop Science Division, Frankfurt, Germany
in studying resistance. For instance, countries such as Australia
and the USA have fairly high numbers of reports, whereas there c Monsanto, São Paulo, SP, Brazil
are fewer reports from Asia and some Latin American coun-
d Syngenta, Singapore
tries. Significantly fewer cases are reported in Africa even though
there are some areas of intensive agriculture where herbicides are e School of Life and Environmental Sciences, University of Sydney, Narrabri,
routinely used.5 Australia

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www.soci.org MA Peterson et al.

resistance (Liu D, Hunan Plant Protection Institute, personal com-


Table 1. Overview of herbicide resistant weeds’ presence in Asian
countries infesting rice, wheat and corn production5
munication). Rice production in Japan and South Korea is also
significantly impacted by HR due to a heavy dependence on
Country Rice Wheat Corn Palm/Rubber herbicides. The first documented case of an HR weed in Japanese
rice was ALS-resistant M. korsakowii in Hokkaido prefecture in
Bangladesh –* NA NA NA
1994.5 Since then, the number of resistant weeds in Japanese rice
China xx xx x NA
fields has increased year-on-year (Fig. 1). Currently, 35 prefectures,
India – xxx – NA
representing >95% of the Japanese rice production area, face
Indonesia x NA – xx
heavy ALS resistance in all major rice weeds. Major resistant weeds
Japan xxx NA NA NA
in Japan include M. korsakowii, Lindernia spp., Rotala spp., Scirpus
Malaysia xx NA NA xx
juncoides, Ammania coccinea, Schoenoplectus juncoides11 and
Pakistan x xx – NA
Sagittaria trifolia.12 Another important rice weed, E. crus-galli, was
Philippines x NA – NA
first documented as resistant to acetyl-CoA carboxylase (ACCase)
South Korea xxx NA NA NA
inhibitors in the dry-seeded rice production area of Okayama.13
Sri Lanka xx NA NA NA
Two biotypes of E. crus-galli from this area were also reported
Taiwan xx NA NA NA
to have multiple resistance to ACCase and ALS inhibitors.14 ALS
Thailand xx NA – –
and ACCase inhibitors have been used continuously in rice for
Vietnam xx NA – NA
broad-spectrum weed control in Korea, which has led to the
NA, not a major crop on an area basis in that particular country. selection of HR E. crus-galli and other broadleaf weeds, similar
*No major resistance reported; x, resistance has been reported but to the situation in Japan. In Korea, resistance to ALS inhibitors
is not a very significant threat to crop production; xx, resistance has was first reported in Monochoria korsakowii in 1998.5 Multiple
been reported and is a severe threat to crop production, but options
remain in terms of other modes of action available to manage resistant
resistance to ACCase inhibitors and ALS inhibitors first reported in
weeds; xxx, resistance is a severe threat to crop production and limited Echinochloa phyllopogon in 2006, soon followed by resistance to
options are available to manage resistance. the same herbicides in E. crus-galli in 2008.5 Recent reports indi-
cate multiple-resistant (ALS and ACCase) E. crus-galli populations
are becoming more widespread.15 Currently, in Korea all major
2 HERBICIDE RESISTANCE IN ASIA rice-growing provinces, representing >90% of the country’s rice
Agriculture in Asia is very diverse in terms of crops grown and the production area, have ALS-resistant weeds.
climatic zones across the region. There are nearly 500 million farm- By contrast, reports of resistant weeds in rice production across
ers across Asia with an average farm size of <1.5 ha. Adoption of India, Southeast Asia, and the Philippines are less common, pos-
new agricultural technologies among small farmers occurs slowly sibly because of the greater use of hand-weeding in these areas
and technologically related problems, such as HR, tend to evolve compared with China, Japan and South Korea.16 Current estimates
more slowly as well. By contrast, in some areas such as commercial are that 70% of the rice production area in India is treated with her-
palm oil plantations in Indonesia and state-run facilities in China, bicides for weed control and the remainder depends on manual
farms can be large and technologically advanced. In Asia, HR has weeding. The majority of the herbicides being used in rice belong
been less of a concern than insecticide and fungicide resistance. to the very long chain fatty acid (VLCFA) inhibitor and ALS inhibitor
However, during the past decade, HR in some cases has become groups. VLCFA inhibitors, which appear to have a lower tendency
a major impediment to growing crops across various Asian coun- to develop resistance,17 are generally applied at pre or early post
tries. Most readily available information on HR in Asia is related to emergence to control grasses. This is often followed by appli-
the major grain crops rice (Oryza sativa), wheat (Triticum aestivum) cations of ALS inhibitors post emergence to manage broadleaf
and maize (Zea mays), as well as palm oil (Elaeis guineensis) and weeds and supplemental manual weeding at a later stage.
natural rubber (Hevea brasiliensis). A brief overview of resistance Wheat is commonly grown in rotation with rice across Asia and in
in these crops is presented in Table 1. some cases, exhibits more difficult resistance issues. Resistance in
Rice is the dominant grain crop across much of Asia, with over grass weeds to ACCase and ALS herbicides is one of the major chal-
139 × 106 ha accounting for ∼ 87% of the world’s production area.7 lenges for wheat farmers across much of the region. This includes
As hand-weeding has declined in favor of more intensive herbicide widespread resistance of Phalaris minor to photosystem II (PSII),
use, resistant weeds in rice have become common. In northeast ACCase, and ALS chemistries across the wheat-producing areas of
Asia, the Yangtze River area, and southern China, nearly 25, 18 and India, Pakistan, Bangladesh, and Sri Lanka. Current estimates put
12% of rice production is impacted with acetolactate synthase nearly 4 × 106 ha infested with HR P. minor in northern India (Fig. 2).
(ALS) resistance, respectively, and 8, 12, and 10% of the area is Multiple herbicide resistance development in P. minor is a classic
impacted with quinclorac resistance.8 In China, ALS resistance was example of the loss of effectiveness of different herbicide SOAs
first documented in Echinochloa crus-galli in 2000. Since then other over a period (Fig. 3). In some areas wheat production declined sig-
major rice weeds such as Monochoria korsakowii, Sagittaria mon- nificantly due to widespread HR in P. minor.18–20
tevidensis and Monochoria vaginalis have evolved resistance to ALS In the Yangtze River area of China. ACCase and ALS inhibitors
inhibitors.5 In 2013 E. crus-galli was found resistant to penoxsulam, are the two major classes of herbicides that have been used post
the most widely used herbicide in China.9 Penoxsulam is one of emergence to selectively control grasses in wheat for the past
the most important herbicides to be used in China since 2008, and two decades.21 ACCase resistance was first reported in Beckmannia
has been an excellent tool for rice weed management. However, syzigachne in 201422 and many farmers shifted to ALS inhibitors
recent reports of cross- and multiple-resistant E. crus-galli have such as mesosulfuron-methyl for the control of ACCase-resistant
raised concerns about sustainable weed control options in rice.10 weeds.23 This, in turn, led to multiple-resistance in B. syzigachne
Current estimates are that nearly 2 × 106 ha in the Yangtze River and A. japonicus.21,24,25 Current estimates are that nearly 10% of
area and Ningxia Province are severely impacted by ALS inhibitor the area in the Chinese provinces of Anhui and Jiangsu are under

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Figure 1. Top 10 wheat-producing states in India. The multiple herbicide-resistant Phalaris minor impacts nearly 4 × 106 ha in the encircled region.

serious threat of resistance to both ACCase and ALS inhibitors especially in rice and wheat production. In developed countries
across all key grasses, and farmers are once again shifting herbicide such as Japan and South Korea, labor for farm work has been
use to PSII inhibitors.21 limited for some time and hand-weeding is largely impractical.1
Maize production is spread across Asia, with even smaller Countries with developing economies have seen significant
countries such as Vietnam and Thailand planting over 1 × 106 ha migrations of people from rural to urban areas and are already
annually.7 However, maize production in many Asian countries experiencing labor shortages in agriculture.1,27 Herbicide selection
is predominated by smallholdings where a significant amount pressure will increase significantly and more weeds with multiple
of weed control is achieved by mechanical or hand-weeding. resistance are likely to arise. Because the evolution of HR weeds is
This may in part limit the number of resistant weeds reported in outpacing the development of new SOA, it is critical for farmers to
maize for these countries. China, however, has a large planted utilize a diversity of weed management tools to maintain sustain-
area of maize (38 × 106 ha).7 Because China does not grow able crop production. Non-chemical weed management practices
herbicide-tolerant maize at this point, herbicides such as ace- that do not involve high amounts of labor should be more
tochlor, s-metolachlor, atrazine, nicosulfuron and mesotrione are thoroughly researched and communicated. Many agronomic
the foundations of weed control. At present, there are no data practices like stale seedbed, early planting, higher wheat seeding
available on the extent of resistant weeds in Chinese maize, but rates, herbicide rotations and sequential herbicide applications are
recent estimates are that ∼ 15–20% of the maize area is infested currently being recommended for the management of problem
with PSII- or ALS-resistant weeds (Liu D, personal communication). species such as P. minor.31 In some areas, producers are undertak-
Palm oil production is concentrated mainly in Indonesia and ing efforts to diversify weed control programs. For example, in one
Malaysia, often on large commercial plantations where herbicide survey of palm oil producers in Indonesia, 72% of respondents
use is intense.7,26,27 Natural rubber plantations also are heavily indicated that they rotated herbicides to prevent resistance.26
concentrated in these countries and make extensive use of The low number of HR weeds reported in some Asian countries
herbicides.27 Consequently, resistance to several SOAs, including may be indicative of under-reporting due to limited resources for
glyphosate, paraquat, ALS, auxin, ACCase and glufosinate, have public institutions associated with weed science, which may in
been documented in species such as Eleusine indica, Hedyotis turn hamper research and education efforts. Private organizations,
verticillata, Clidemia hirta and Chromolaena odorata.28 In the case government scientists and extension services should capitalize
of glufosinate-resistant E. indica reported on a palm plantation, on recent advancements in communication technology to reach
the grower had indicated using up to 24 applications annually.29 growers with greater ease, and share relevant scientific informa-
Multiple-resistant E. indica has also been identified in these areas.30 tion and advice that will help farmers to manage HR. Given the
importance of maintaining high levels of food production in the
2.1 Herbicide resistance management most populous region of the world, international agencies may
Across Asia, changing demographics will continue to drive a want to consider increased emphasis on assisting these countries
greater dependence on herbicides and potentially greater HR, in resistance management efforts.

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www.soci.org MA Peterson et al.

Australia, a key difference is that L. rigidum was established and


adapted throughout the production region.36,37 For most of the
20th century, livestock production dominated the current crop-
ping region and L. rigidum pastures were established as a valuable
source of forage. Thus, by the 1970s, when crop production and
herbicide use intensified, L. rigidum was established in large,
naturalized populations throughout the grain production regions.
L. rigidum is the world’s most resistance prone weed, hav-
ing evolved resistance to 11 herbicide SOAs.5 However, in total
there are 48 HR weed species in Australia with a number of
these resistant to multiple SOAs, such as Raphanus raphanistrum
(five SOAs),38–40 Avena fatua (three SOAs),41,42 Hordeum leporinum
(three SOAs)43–45 and Poa annua (five SOAs).5 However, with-
Figure 2. Phalaris minor cyclical herbicide resistance challenge in India.
In the early 1990s, isoproturon was solely used. With isoproturon resis- out doubt, it is the frequency and distribution of multi-resistant
tance in the mid-2000s, selection pressure was shifted to FOPS and sulfo- annual ryegrass populations that dominates weed management
sulfuron. Pinoxaden became the dominant herbicide to manage ALS and decision-making in Australian cropping.
ACCase-inhibitor resistance around 2010. Since then, pinoxaden resistance The consequence of HR evolution in Australian weed popula-
has been documented in the major wheat-growing areas of India.
tions has been that many previously effective herbicides are no
longer useful. The predominant HR scenario in Australian crop-
3 HERBICIDE RESISTANCE IN AUSTRALIA ping fields is demonstrated by the evolution of ACCase inhibit-
In the first decade of the 21st century Australia led the world in the ing and/or ALS inhibiting HR in L. rigidum populations.33–35,46
number of HR cases, with high frequencies of multi-resistant popu-
lations evolving on a grand scale throughout all cropping regions.
In the decade prior to this, there was wholesale adoption of highly
productive conservation cropping systems based on no-till and
stubble retention by Australian producers.32 Adoption of this
production system was facilitated by highly effective herbicides
that subsequently became the entire focus of weed management
programs. Conservation agriculture has dramatically increased the
productivity and sustainability of Australian cropping. However,
a consequence is the widespread evolution of HR across the Aus-
tralian grain-producing region (Fig. 4).33–35 Now, a little over two
decades since herbicide reliance became widespread, herbicide
susceptibility in Australian Lolium rigidum populations is rare.
The presence of large populations of genetically diverse,
well-adapted, L. rigidum resulted in the evolution of multi-resistant
populations on a large scale. Although HR weed populations have
evolved in many parts of the world,5 nowhere has multiple resis-
tance evolution been more extensive than across the Australian Figure 4. Frequency of herbicide resistance in randomly collected
grain-producing region (Table 2). Although herbicide reliance for annual ryegrass populations across the Australian grain-production region
the control of resistance-prone weed species is not unique to (shaded green).

Figure 3. Progression of ALS-resistance in different weed species across various prefectures of Japan. Source: http://jhrwg.ac.affrc.go.jp/JHRWG.html

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Table 2. Herbicide resistance in annual ryegrass populations Table 3. Annual ryegrass plant densities in randomly surveyed
randomly collected across Australia’s cropping regions wheat fields across the Australian cropping region

Southern Region Annual ryegrass density (plants/m2 )


Mode of Western New South South
South Australis and Victoria* < 5.0
Herbicide action Australia* Wales* Australia† Victoria† Tasmania
Western Australia† <1.0
Diclofop ACCase 96 64 58 73 46 New South Wales‡ <1.0
Sethoxdim ACCase 79 – – – – Tasmania‡ <1.0
Clethodim ACCase 65 12 9 8 8 Data from
Tralkoxydim ACCase – 32 – – – *Boutsalis P (personal communication),
Chlorsulfuron ALS – 53 70 71 – †Broster J (personal communication) and.
Sulfometuron ALS 98 64 – – 16 ‡Owen et al.33 and Lewelleyn et al.52
Imazamox/ ALS – 49 58 31 20
imazapyr
Trifluralin VLCFA 27 12 57 8 8 available herbicide options. The maintenance of control is likely
Simazine PSII – 0 – – – a response to awareness of resistance issues combined with the
Atrazine PSII 2 – – – – use of new and existing alternate weed control technologies (e.g.
Glyphosate EPSPS 7 2 3 2 0 harvest weed seed control, strategic tillage, crop competition).
Paraquat PSI 0 – – – – Additionally, recent random surveys indicate that the rates of
resistance evolution have slowed and potentially even halted,
*Data from Han et al.,48Rey-Caballero et al.63
and Boutsalis P (personal commu-
nication).
albeit at very high levels.33 Although resistance frequencies will
†Southern NSW and WA values are populations with ≥1% survival, Vic and SA remain high, lower weed densities mean that these populations
values are for ≥20% survival at recommended rate. have a greatly reduced impact on crop production. It now seems
–, herbicide not used in screening; ACCase, acetyl-CoA carboxylase
inhibitor; ALS, acetolactate synthase inhibitor; VLCFA, very long chain clear that Australia no longer leads the world in HR, but instead is
fatty acid inhibitor; PSII, photosynthesis at photosystem II inhibitor; EPSPS, now the global leader in HR management.
5-enolpyruvulshikimate-3-phosphate synthase inhibitor; PSI, photosynthesis at
photosystem I inhibitor.
4 HERBICIDE RESISTANCE IN EUROPE
Europe is characterized by a highly diversified agricultural sector.
The resistance mechanisms involved are typically dominant to Besides the geographical differences, a diversified agricultural sec-
semi-dominant3,47–50 with little or no fitness penalty,51 ensuring tor is likely to be the consequence of differences in political and
that HR L. rigidum populations will remain in perpetuity. The economic systems across European countries. The European Union
ubiquitous occurrence of HR L. rigidum populations in Australian (EU) has around 10.8 million farms covering 174 × 106 ha of agricul-
cropping systems has resulted in the loss of many highly effective tural land, as a result, the average farm size is 16 ha.53 Farm size and
herbicides from weed management programs. land properties vary greatly among EU countries and most likely
are among the more important factors that influence the adoption
3.1 Herbicide resistance management of agricultural practices. Compared with other regions around the
The extent and severity of HR in Australia ensures that the cost world, minimum tillage is still expanding and is being adopted to
to grain growers of managing resistance reactively is considerable help protect land from erosion and reduce carbon dioxide emis-
and escalating. Recent results from a national grower survey esti- sions, fossil fuel use, nitrogen and pesticide leaching, and improve
mated that HR costs growers an additional A$187 million annu- soil structure.54,55 The relatively complex and diverse weed flora
ally just in additional herbicide costs.52 These costs are associated and cropping systems, as well as highly variable farm sizes found in
with the use of alternate herbicides and herbicide mixtures, as well Europe may have delayed the emergence of resistance compared
as higher application rates and equate to approximately an extra with other regions of the world.56
A$8 ha−1 . Not surprisingly, most of these additional costs (A$103 Although EU cropping systems are diverse, crop rotations are
million) are used in attempts to control HR L. rigidum populations. dominated by winter crops (wheat/barley, 36.5 × 106 ha and
It is more difficult to determine the impact of HR on the use of oilseed rape, 6.4 × 106 ha) and maize (9.3 × 106 ha) or other sum-
additional weed control practices such as tillage, hay cutting and mer crops according to the climate zone because temperature
harvest weed seed control. However, data from this survey allow and water requirements limit maize-growing areas. Europe is the
comparison of overall weed control costs (yield and revenue loss, largest producer of wheat, the second most widely grown cereal
contamination, herbicides, tillage, etc.) between growers with and crop in the world after rice.57 France, Germany, Poland and the
without HR. This comparison estimated that the annual cost due to UK produce more than half the EU’s cereals. In those countries,
HR was an additional weed control cost of A$55 ha−1 . This is con- crop rotations with winter cereals are dominated by annual winter
siderably more than the cost of the herbicide alone and likely more weeds.
accurately reflects the financial burden of HR on Australian grain Although it is difficult to collect precise information on the
growers. spread and intensity of HR, countries where it has been widely
However, despite the dramatic levels of HR in Australian weed reported are the UK, France, Germany and Belgium in central
populations and the consequential loss of herbicide efficacy, L. Europe; Spain and Italy in southern Europe; and Poland, Czech
rigidum densities remain low and may even be declining in some Republic and Hungary in eastern Europe.5 The most intense infes-
areas (Table 3). In particular, across the Western Australia cropping tations are reported in Western Europe. Cases of resistance in
region where the frequency of HR is arguably the highest in the southern Europe seem to be less uniformly spread than in central
world, in-crop densities of L. rigidum remain low despite very few and northern Europe.

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www.soci.org MA Peterson et al.

9 × 106 ha, mainly olive and citrus groves in the Mediterranean


area.5,65 Other cases of resistance to EPSPS involve Lolium spp.
in vineyards, and to a lesser extent in wheat, where the use of
glyphosate after harvesting and before sowing is high.66–68
A rough estimate based on the author’s interviews with weed
resistance experts from public institutions and the agrichemical
industry led to an area of almost 9 × 106 ha affected by resistant
weeds in wheat and oilseed rape cropping systems, 0.2 × 106 ha in
maize, 0.14 × 106 ha in rice and >0.22 × 106 ha in perennial crops.

4.1 Herbicide resistance management


Some countries in Europe have virtually lost the use of ACCase
inhibitors to control A. myosuroides, and resistance to ALS is
steadily increasing. Some simulations have indicated that, if left
unchecked, resistant A. myosuroides may eliminate profitability
for some European farmers.69 The same study indicates that a
proactive approach that utilizes a greater diversity of crops, tillage
and herbicides may reduce net profitability by 4–24% compared
Figure 5. Area of wheat production and general areas of major herbicide with an intensive cropping system without resistance, but in
resistant weeds (adapted from Trnka et al.57 ). the long term will be more profitable compared with resistance
development.70 The consequence of evolution of resistance to
Considering all the available information, the most important ACCase and ALS inhibitors in grass species in small grain crops
resistant weeds infesting cereals involve grass species (Fig. 5). has been an increase in the adoption of pre-emergence herbi-
Alopecurus myosuroides is spread mainly in central–northern cides, along with greater use of cultural practices such as occa-
regions, whereas Lolium spp. are common in most countries sional inversion tillage and use of false seedbeds, in order to reduce
regardless of latitude. A. myosuroides and Lolium spp. are the resistance selection pressure and eventually exhaust the seed-
most reported species evolving multiple resistance cases, mainly bank. Studies in the UK, where almost every farm is affected by A.
to ACCase and ALS inhibitors.5,58,59 Particularly troubling is the myosuroides resistant to ACCase inhibitors and resistance to ALS
widespread presence of metabolic resistance in A. myosuroides inhibitors is increasing, have demonstrated that a weed manage-
because this may result in broader cross-resistance, potentially ment system based on only herbicides is not sustainable, and resis-
even to new herbicides.59,60 Multiple resistance in these species tance can increase costs up to €240 ha−1 (cost based on author’s
continues to grow, with reports of L. rigidum populations resis- estimation of on-farm prices plus ancillary costs of cultivation).
tant to both glyphosate and protoporphyrinogen oxidase (PPO) Major changes in cultural practices are being implemented when
inhibitors recently found in southern Spain.61 Apera spica-venti there are no other economically feasible options. In those areas of
is found in central–eastern regions and is generally resistant to the UK where HR is not manageable with alternative herbicides,
ALS inhibitors, but cases of resistance or multiple resistance to implementation of the following has been observed: (1) innovative
ACCase or PSII inhibitors have also been found in this species.5,62 planting and cultivation tools, such as redesigned drilling equip-
Avena spp. (A. fatua and A. sterilis in northern and southern Europe, ment that causes minimal soil disturbance; (2) delayed drilling
respectively), are resistant to ACCase and/or ALS inhibitors. HR combined with stale seedbeds to reduce early-germinating weeds
Papaver rhoeas is reported mainly in the Iberian peninsula but cohorts; (3) diversity in crop rotation/cultivation, such as the inclu-
is also present in northern Europe. It is generally resistant to sion of summer crops to disrupt winter grasses; (4) adoption of
ALS inhibitors and, especially in the Iberian peninsula, cases of cover crops to improve soil structure and drainage to allow flexi-
multiple resistance to ALS and synthetic auxins are increasing.63 ble drilling dates on heavy land, as well as give spring crops a head
Most of the cases reported in maize are old cases related to start over weeds; (5) increasing crop competitiveness by choosing
the triazines, but more recently some cases of resistance in E. more competitive varieties, helping to reduce grass weed tiller-
crus-galli, Sorghum halepense and Amaranthus spp. to ACCase ing, heading and seed production; and (6) enhancing herbicide
and/or ALS inhibitors have been reported.5 The past selection performance in various ways (i.e. improved application methods,
pressure exerted by triazines on certain weeds is even now proper growing stage and avoiding applications under adverse
affecting active ingredients like metribuzin, terbuthylazine and conditions). The key lesson from the UK is that it is all about man-
metamitron. aging the weed population density and soil seed bank, irrespective
Rice production (0.6 × 106 ha EU + Turkey) occurs mainly in Italy of resistance status.
and Turkey and a few other Mediterranean counties. The usual Because of a scarcity of new products in the pipeline and the
weed flora is dominated by Echinochloa spp., mainly resistant to withdrawal or enforced dose rate reduction of many active ingre-
ALS or ACCase inhibitors and a few multiple resistant cases to both dients resulting from the re-registration process, resistance cases
SOA. However other resistant species can be found in rice such are likely to increase in the near future.70 The biggest problems are
as Cyperus difformis resistant to ALS inhibitors and red rice (Oryza encountered where simplified and standardized agronomic prac-
sativa var. sylvatica) resistant to ALS where the adoption of ALS tices are adopted, such as monoculture and the use of herbicides
herbicide tolerant rice is prominent.5,64 with the same SOA.69 It is not surprising that the most affected
Among broadleaves, Conyza spp. has been reported to be resis- cropping systems with major HR issues are those where a limited
tant to the 5-enolpyruvulshikimate-3-phosphate synthase (EPSPS) number of SOAs are used, for example, winter cereals. The adop-
inhibitor glyphosate in perennial crops, which cover around tion of conservation agriculture, which has major benefits for the

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soil, also has a side effect of promoting the occurrence of species


Table 4. Number of reported herbicides resistant weeds in South
germinating from the surface (i.e. A. myosuroides, A. spica-venti and America in soybean crop by site of action5,81–83
Lolium spp.).71
Herbicide tolerant (HT) crop varieties are convenient technolo- Country Total EPSPS ALS ACCase PPO PSI Multiple*
gies for weed management, nevertheless the adoption of HT crops
Brazil 26 8 6 4 1 1 6
also poses the risk of selecting resistance. ALS-tolerant oilseed rape
Argentina 17 11 2 2 – – 2
and sugar beet introduce the opportunity of using ALS herbicides
Bolivia 9 2 1 4 1 – 1
across rotations with cereals where ALS herbicides are a major
Uruguay 3 3 – – – – –
component of weed management programs. Thus, an aggressive
Paraguay 3 2 1 – – – –
and proactive anti-resistance management strategy needs to be
Total 58 26 10 10 2 1 9
implemented in such rotations.
Efforts to convey a common and effective message promoting EPSPS, 5-enolpyruvulshikimate-3-phosphate synthase inhibitor; ALS,
the introduction of diversity into cropping systems through the acetolactate synthase inhibitors; ACCase, acetyl-CoA carboxylase
adoption of integrated weed management (IWM) are being made inhibitors; PPO, protoporphyrinogen oxidase inhibitors; PSI, photosyn-
thesis at photosystem I inhibitor.
by the EU, universities and agricultural research centers, as well as
*Resistance to two or more sites of action.
the industry. Education is critical, and its importance cannot be
underestimated.
and grasses (28 cases), and in some areas together in the same
field, creating issues with tank mix compatibility and antagonisms
5 HERBICIDE RESISTANCE IN SOUTH among different herbicides.
AMERICA In the 1990s, weed resistance to ALS and ACCase herbicides were
South America represents ∼ 20–25% of the cultivated area in the predominant across the region because of the intensive use of
world, with a key role in production and global trade. Row crops are those herbicide groups in conventional soybean fields. Between
dominant in terms of planted area with 58.7 × 106 ha of soybean 1993 and 2004, resistance to ALS was reported for Bidens pilosa,
(Glycine max), 20.6 × 106 ha of maize and 0.97 × 106 ha of cotton.7 B. subalternans, Euphorbia heterophylla and Amaranthus hybridus
From the farmers’ perspective, soybean is the main crop that in countries such as Brazil, Paraguay and Argentina, and these
drives decision-making across each region and this can limit crop biotypes are now widespread.5 Early reports (before 2005) of
rotation. Farm size varies widely, but in general farms >1000 ha resistance to ACCase for Urochloa plantaginea, Digitaria ciliaris and
account for almost 40–50% of the area in crop production.72 By E. indica were in Brazil and Bolivia.5 The first multiple resistance
contrast, some countries have large numbers of small farmers with case in soybean occurred in Euphorbia heterophylla resistant to ALS
holdings of <50 ha. and PPO herbicides.5,77
Climate across South America varies greatly depending on lat- Within a few years of the widespread adoption of
itude. In much of Brazil, Bolivia, Paraguay and northern areas of glyphosate-tolerant soybeans across the region, GR weeds began
Argentina, the climate is tropical with high temperatures for most to appear in many South American countries (Table 4). Several of
of the year, but also with a pronounced dry season during the the more problematic GR species are grasses. In 2003/2004, GR
winter months.73 The southern-most portion of Brazil, most of Lolium multiflorum populations were found in annual crops such
Uruguay, and a large portion of Argentina is an area known as the as soybean, wheat and maize in Rio Grande do Sul.84 L. multiflorum
Pampa, which is a steppe landscape with a more temperate climate is well adapted to the southern region of Brazil, where it is used
and generally deep, fertile soils. as a winter cover crop in the no-till agriculture system, as well as a
No-till farming is used by ∼ 90% of South American growers74 cover crop in orchards, or as forage.85 The presence of this weed
and glyphosate is a key part of this system. Crops tolerant to can reduce wheat yield up to 62%.86 After the first GR case in Rio
glyphosate account for almost 96% of the total soybean area in Grande do Sul, farmers began to use ACCase inhibitors to manage
South America.75,76 Glyphosate is often applied at least three to GR L. multiflorum prior to sowing soybean or ALS inhibitors in
five times a year to fields where glyphosate-tolerant soybean is corn as alternative management tool.78,84,87 Consequently, in
grown.77,78 This technology has been used successfully over the 2010/2011 L. multiflorum populations with multiple resistance to
past 20 years in Argentina, Brazil, Paraguay, Bolivia and Uruguay. glyphosate and ACCase inhibitors were reported. Then, in 2017
However, the use of glyphosate with no herbicide rotation or a population resistant to glyphosate and ALS inhibitors was also
mixtures has led to the selection of tolerant weed species through found.5 The main infestation is in southern Brazil and studies
weed shifts and the evolution of glyphosate-resistant (GR) weed indicate that in 2015 the area infested with GR L. multiflorum was
populations across the main agricultural regions.79,80 >4 × 106 ha.88 In Uruguay HR L. multiflorum is estimated to affect
Across South America, there are 126 documented cases of weed more than 290 000 ha.83
resistance: 49 in Brazil, 25 in Argentina, 19 in Chile, 8 in Bolivia, 10 The first control failures of the perennial weed Sorghum
in Venezuela, 6 in Colombia, 5 in Uruguay, 3 in Paraguay, and 1 halepense in Argentina were observed in 2003 in soybean pro-
in Ecuador.5,81–83 Approximately 70% of the reported cases are in duction areas of the northwest provinces of Salta and Tucumán.
the main soybean-producing countries (Brazil, Argentina, Bolivia, This area has 90% of its agricultural production under no-tillage
Uruguay and Paraguay) and over half are in soybean (Table 4). Even and is highly dependent on glyphosate with the first GR case
though most of the reported cases are species resistant to one confirmed in 2005.89–92 Currently, GR biotypes are found in all
single herbicide SOA, in recent years more cases of multiple resis- Argentinian production regions, where they have spread by har-
tance to glyphosate and other modes of action (MOA) have been vester movement.85,91,93–95 S. halepense can cause up to 40% yield
reported. The frequency of new weed resistance cases is increas- loss and is a key weed in the region.89 In Argentina, the estimated
ing and spreading in South America, changing the herbicide mar- area infested with GR Sorghum halepense is currently estimated to
ket. Cases of resistance include both broadleaf species (30 cases) be ∼ 5.0 × 106 ha.96

Pest Manag Sci (2018) © 2017 Society of Chemical Industry wileyonlinelibrary.com/journal/ps


www.soci.org MA Peterson et al.

Another key grass weed with widespread GR is Digitaria insularis, areas should be consider resistant to glyphosate and ALS herbi-
which is common across many areas of Brazil, Bolivia and Paraguay. cides when planning weed management strategies.80 A. palmeri
The first report of D. insularis resistant to glyphosate occurred resistant to glyphosate and ALS inhibitors was first detected in
in soybean fields of Paraná in 2008.97 GR D. insularis has spread Brazil in Mato Grosso state 2015, but has been contained so far
rapidly from western Paraná State to the central region of Brazil, through cooperative efforts between the Brazilian government
mainly in the grain-producing areas and possibly through har- and local farmer associations.107–110 A 2016 survey of HR weeds in
vester movement as well as independent selections. GR D. insularis Uruguay found 3500 ha affected by GR A. palmeri.83
populations are now found in all geographical regions of Brazil,
with an estimated infestation area of 8.2 × 106 ha.98,99 It is the most
5.1 Herbicide resistance management
important GR species in Paraguay, having spread to approximately
In South America, weed resistance is one of the most important
75% of the soybean-producing regions (Adegas F, personal com-
concerns for farmers, mostly due to new cases, increasing areas
munication). For most GR grasses, farmers have turned to ACCase
of infestation, populations with multiple resistance, and mixed
inhibitors and the overuse of this SOA is leading to the selection of
GR populations (grasses + broadleaves) in the same field. This
multiple resistant populations of these weeds in Brazil, Bolivia and
situation leads to increased complexity and higher costs for farm
Argentina.78,81,82
management. In Brazil, the area with weed resistance has been
Conyza spp. can cause >50% yield loss in soybean and are now
estimated at >20 × 106 ha, and the costs for weed resistance
the most troublesome GR broadleaf weeds in the region.82,95,100,101
management were close to US $3 billion (additional control and
The first reports of GR Conyza bonariensis and C. canadensis in
yield losses).78 In the 2016/2017 season, the costs of weed control
Brazilian soybean occurred in 2005 in Rio Grande do Sul and
in Brazil were US $40–120 ha−1 . For example, mixed infestations of
Paraná.102,103 Subsequently, in 2010, Conyza sumatrensis resis-
GR weeds can increase management costs by US $25–84 ha−1 .88
tant to glyphosate was also reported in Paraná.5 C. canaden-
The cost of weed control in Argentina during the 2016/2017
sis, C. bonariensis and C. sumatrensis infestations are now spread
season varied between US $100 and 131 ha−1 , 40% higher than
across all soybean-producing regions, with an infested area of
during the 2013/2014 season. For example, the cost to man-
10.6 × 106 ha.98 Argentina encountered the first reports of C. bonar-
age mix infestation of resistant grasses and A. hybridus was US
iensis populations suspected to be resistant to glyphosate dur-
$131 ha−1 .111 Additionally, South America’s growers are not highly
ing the 2008/09 season in the Pampa region and Entre Rios.
experienced in the use of alternative herbicides or non-chemical
Currently, C. sumatrensis, infests around 10 × 106 ha in Argentina
weed control practices. Therefore, resistance management to
and has become one of the key weeds due to increasingly
prevent or slow weed resistance evolution remains challenging.
high levels of GR and few effective alternative herbicide sites of
The implementation of comprehensive stewardship programs in
action.101 C. sumatrensis resistant to glyphosate was first observed
South America is critical to the long-term sustainability and viabil-
in Paraguay in 2008, and is now thought to cover ∼ 30% of the
ity of glyphosate-based weed control systems by reducing selec-
soybean-producing area (Adegas F, personal communication). A
tion pressure with the use of alterative herbicides. This includes
2016 survey of HR weeds in Uruguay found C. bonariensis to be
developing diversified weed control recommendations for each
the most serious weed problem in that country, with >1000 pro-
growing region, education programs targeting farm consultants
ducers and almost 600 000 ha affected.83 Once farmers across the
and farmers to communicate best management practices, and
region started to encounter GR Conyza spp. their first reaction was
commercial programs consistent with science-based weed man-
to increase applications of ALS herbicides to control it. Unfortu-
agement recommendations. In some cases, changes in national
nately, this has led to a growing problem with multiple resistance
export policies and land lease arrangements, as well as the expan-
to both glyphosate and ALS herbicides.5 Another Conyza con-
sion of public research will be necessary to support greater diver-
trol strategy has been application of a contact herbicide, such as
sification of cropping and improved resistance management.112
paraquat, shortly after the burndown application of combinations
For the future, a general analysis of forthcoming technologies
of glyphosate with 2,4-D (2,4-dichlorophenoxyacetic acid). This
in soybeans shows that they are efficient and offer alternatives
‘double knockdown’ strategy has been largely successful for con-
for controlling broadleaves (2,4-D, dicamba, glufosinate), but not
trol of GR Conyza, but unfortunately reports of paraquat-resistant
grasses. Because no new herbicide SOA is likely to be introduced
Conyza are now starting to appear.5
soon, one can speculate that grasses resistant to glyphosate will
A new problem has been the recent appearance and spread
continue to be a primary problem for South American farmers.
of GR Amaranthus species, especially in Argentina. Amaranthus
hybridus is a native species found across the central and northern
regions of Argentina and it is a major weed of summer crops, such
as soybean, peanut, corn and sunflower. The presence of this weed 6 HERBICIDE RESISTANCE IN NORTH
can reduce soybean yield by between 9 and 40%.104 Populations of AMERICA
GR A. hybridus were reported in 2013 and 2015 with multiple resis- North America (including Canada, Mexico and the USA) produces a
tance to glyphosate and ALS inhibitors in south Cordoba and Santa significant portion of the world’s grains and oilseeds. This includes
Fe.82 Amaranthus palmeri populations resistant to glyphosate were 8% of all wheat, 34% of all soybean, and 36% of all maize.7
first detected in Argentina in 2013.105 The introduction of A. Production areas for these crops are largely in the USA and Canada,
palmeri into the south of Córdoba is probably associated with and the vast majority of North American HR cases are reported in
the importation of cereals, oilseeds or forages contaminated with these two countries.5
weed seeds, or from agricultural machinery brought from the The first case of HR reported in North America was Daucus carota
USA.105 Between 2013 and 2015, the presence of this weed was to the auxin SOA in 1957.5 However, very few additional reports
detected in much of the grain-growing area of Argentina.80,106 occurred until the first case of triazine resistance was recorded
Also, A. palmeri resistant to ALS was reported in 2014 in southwest 1970. Triazine resistance dominated reports over the next 17 years
of Cordoba and east of San Luis.82 A. palmeri populations in these until 1987 when the first instances of ALS-resistant species started

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Herbicide resistance around the world www.soci.org

Avena resistant to ACCase herbicides are commonly found in the


north central USA and the Canadian prairies.129 Resistant L. multi-
florum is problematic in many wheat-growing areas across North
America, and GR and ALS-resistant grasses are found in both row
crops and cereals across the continent.130–136
GR is probably the most widespread and economically impactful
resistance across a large swath of North America. GT varieties of
maize, soybean and cotton account for >90% of the area planted
to those crops.137 The use of GT crops also enabled many farmers
to adopt no-till systems, saving time and soil but also increasing
dependence on glyphosate.138,139 This dependence has made GR
weeds tremendously disruptive.
The recent emergence of widespread resistance to PPO inhibitor
herbicides has been particularly troubling for US row crop pro-
ducers. Results from 593 field samples of A. tuberculatus and A.
palmeri collected in 10 Midwestern states indicated as many as
Figure 6. General distribution of key resistant weed species across Canada
82% testing positive for both GR and PPO resistance, depend-
and the USA. ing on the state.140 PPO-resistant biotypes of A. palmeri have also
been discovered across much of the mid-South in states such as
to appear. Reports of resistance to ACCase herbicides began about Arkansas and Tennessee.141,142 Resistance in these biotypes tends
the same time. By the mid to late 1990s, cases of ALS resistance to be more strongly exhibited to foliar applications of PPO herbi-
were beginning to dominate the survey and instances of multi- cides compared with soil-applied products within the same SOA,
ple resistant populations were appearing. The first case of resis- with lower resistance ratios for the soil-applied materials.143 This
tance to glyphosate was noted on L. rigidum in California in 1998 may be mainly due to the relatively high dose of soil-applied prod-
and within 2 years C. canadensis in Delaware was the first reported ucts made to ensure sufficient length of residual control.
GR broadleaf species. Since 2005, the number of GR broadleaf
weeds has increased significantly. Figure 6 provides an overview 6.1 Herbicide resistance management
of the primary problem weeds in different areas of North America. The first reaction to GR is often to increase the rate or num-
Amaranthus species are probably the most impactful HR species ber of applications of glyphosate. Given the relatively low cost
in most of the USA. Much of the southeastern USA is infested of glyphosate and the high tolerance of GT crops the ‘more is
with A. palmeri that is resistant to both glyphosate and ALS herbi- better’ strategy has been a natural response. However, when this
cides, and increasingly multiple resistant to glyphosate, ALS and approach worked it was usually not for long because the weed
PPO SOAs.113,114 HR Amaranthus tuberculatus is common across populations were simply driven to higher levels of resistance. In
most of the US Midwest and many populations have multiple some instances, farmers used other herbicide SOA as ‘rescue’ treat-
resistance.5,115,116 In some cases, resistance to five different SOA ments following glyphosate failure. This placed higher selection
has been documented in the same population.117 Amaranthus pressure on the alternative herbicide because it was often applied
species can germinate throughout the growing season and often under less than ideal circumstances regarding weed size and sus-
produce seed in very short periods.118 Years of glyphosate use, ceptibility. Another, more proactive next step usually consists of
given its lack of residual control, has helped encourage dom- additional applications of herbicides or mixtures of other herbi-
inance by species with extended germination periods such as cides with glyphosate. In many cases, this can be a highly effec-
Amaranthus. HR C. canadensis is widely distributed in the cen- tive means of managing the problem if the herbicides overlap in
tral and eastern portions of North America from Mississippi to spectrum and are equally effective.144 According to proprietary
Ontario.5 It is often resistant to glyphosate along with ALS, but market research, from 2000 to 2015, the use of pre-plant and
has also demonstrated resistance to PSII inhibitors and, in iso- pre-emergence herbicides in soybeans increased from 25% to
lated instances, PSI inhibitors. Early infestations of GR Conyza were almost 70%, largely in response to GR weeds. The use of herbicides
identified in California (orchard floors) and Delaware (soybean) with longer soil residual properties has been helpful to control
where glyphosate use was high.119,120 Although it has typically weeds with extended periods of germination such as Amaranthus
been considered a winter annual, with the majority of germina- and Conyza.
tion in the fall, researchers have noted significant germination in However, there has been somewhat of a ‘domino effect’ from
the spring.121,122 Shifting emergence patterns combined with resis- these strategies. As glyphosate failed, farmers who simply moved
tance to herbicides have made C. canadensis a primary weed prob- to the next best alternative herbicide without implementing other
lem for many soybean growers in North America. Ambrosia trifida is diversification tactics often saw development of resistance to the
another species that has developed resistance to both glyphosate alternative herbicide and more multiple-resistant populations in
and ALS herbicides, and these biotypes are found in much of the their fields. Recent increases in Amaranthus populations with resis-
eastern USA and Canada.5 Kochia scoparia is a problematic weed tance to both glyphosate and PPO herbicides are prime examples
in the plains of North America that has widespread resistance to of this sequence of events.140,141 In some crops such as soybeans,
ALS and glyphosate, with some populations resistant to auxinic the herbicide options for foliar control of some species have
herbicides.123–126 This species spreads readily because the plants narrowed sharply. New herbicide-tolerant soybeans and cotton
often break off at the base following senescence and roll across enable use of auxin herbicides (i.e. 2,4-D and dicamba), a SOA pre-
the landscape with the wind.127,128 Resistant grasses are less com- viously unavailable in these crops.145 However, these technologies
mon than broadleaves in most US row crops, but are common in will have to be carefully stewarded to avoid rapid development of
the cereal-producing areas of the USA and Canada.5,129 Setaria and resistance.

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www.soci.org MA Peterson et al.

All these strategies resulted in increased costs for weed con- that could work on a large scale. Flaming of weeds has also been
trol. As additional herbicides have become necessary to control investigated163 although mainly for organic crop production and
GR weeds, overall herbicide costs have nearly doubled.146 In some other specialty crop situations. RNA interference has shown some
cases hand-weeding, costing $57 ha−1 on average, has become promise in early stage testing as a means to disrupt herbicide resis-
necessary.147 In cotton-growing areas where GR has become tance mechanisms in weeds, but still faces some significant tech-
widespread, estimates of overall weed control costs have doubled nical and regulatory challenges.164,165
or tripled, depending on specific geography.147,148 Often alterna-
tive herbicides or weed control measures can also add complexity.
Residual herbicides bring a risk of carryover injury to succeeding 7 CONCLUSIONS
crops. The timing and precision of application of some herbicides is On a global basis, HR weeds continue to grow and ultimately
significantly more difficult than for glyphosate on GT crops. Farm- threaten crop production. How farmers in different countries
ers also have to spend more time understanding the weed species respond varies. Unfortunately, the responses still are largely
present in their fields in order to match the right herbicide. reactive rather than proactive. Farmers in Australia have become
Alternatives to herbicides are important in an overall weed adept at managing resistance through non-chemical means
management plan. These may include tillage, both pre-plant and mainly because they have lost so many SOAs. To date, reaction to
in-season. Narrow row spacings, increased crop density, cover GR in the Americas has focused on looking for alternative herbi-
crops, and other cultural practices can enhance crop competitive- cide options. A similar situation exists in Asia with ALS and ACCase
ness with weeds and put less selection pressure on herbicides.149 herbicides, but returning to hand-weeding is increasingly imprac-
Given that a large seed bank increases the odds of having resis- tical. Although cropping systems in Europe tend to be more
tant individuals in a field, programs that have a ‘zero tolerance’ diverse, farmers there are highly dependent on ALS inhibitors
for weed escapes are being examined.150 Tools supporting this which are used across many crops. Factors such as climate change
approach include post-harvest control of late-emerging weeds, may impact the basic ecology of weed populations,166 but more
controlling weeds along field edges, burial of weed seed through importantly will change cropping patterns in some areas and
deep plowing, and harvest weed seed control.149,150 Once again, interject greater uncertainty into planned weed control practices
however, these practices introduce more complexity and invest- via greater fluctuations in weather. Abnormally low rainfall may
ment of labor. reduce the effectiveness of soil-applied herbicides, while heavy
Changes in the structure of farms in the USA have compli- rainfall during some years will adversely impact the ability to
cated the implementation of herbicide resistance management. conduct tillage. Water shortages will complicate maintenance
US farms can be categorized into two main groups.151 One set of of water layers in rice to manage weeds. Increasingly affluent
farms is characterized by large size and income from the farm- populations in developing countries will eat more animal protein
ing operation is the primary focus of the operator. These farms and increase demand for feed grains,167 potentially decreasing
account for the majority of crop production. The other group of incentives to diversify crop rotations.
farms is characterized by smaller size and the farm operator often At a very basic level, HR is an evolutionary process driven by
has other sources of income. In the first case, farmers are driven intensive use of single SOAs in the absence of other weed control
to use practices that are quick and efficient to allow them to practices. In this sense, it seems that the solution to the problem is
manage large areas. This usually means a focus on a limited num- straightforward; farmers should diversify their weed control prac-
ber of crops, often only two or three, and therefore crop rotation tices. However, beyond this basic level the issues become more
is also limited. These farmers also tend to eschew herbicide resis- complicated. Although differences in cropping systems, farm size
tance management practices that take more time such as cleaning and degree of technology adoption vary by country, some basic
equipment between fields, inter-row tillage, selective removal of concepts tend to drive and influence the issue. The availability of
escaped weeds, and post-harvest weed control.152 Cover crops suf- labor for agricultural operations continues to decrease around the
fer a similar fate given the time and money required both to plant world as younger generations move to urban areas where living
them and to control them prior to planting the main crop of inter- standards tend to be higher than in rural areas. This has placed a
est. Farmers who run smaller, part-time operations are similarly heavier emphasis on mechanization and herbicides for weed con-
time-constrained because their off-farm employment consumes trol. The heavy dependence on herbicides increases selection pres-
a majority of their time. In all cases, farmers tend to believe that sure and subsequent resistance. In many areas, multiple resistance
the advent of new herbicides will ultimately solve their resistance is eliminating most herbicide options and may force farmers to
problems and are therefore less incentivized to adopt more diffi- adopt non-chemical options or switch to different crops. In some
cult resistance management practices.153 cases, regulatory pressures are reducing the availability of herbi-
Research into herbicide programs continues to examine ways cides and the number of SOAs available for a given crop, while
to combine various SOA in effective and economical ways. Addi- food chain pressure to meet secondary residue standards is forcing
tionally, some ongoing work is examining non-herbicidal means farmers to use less than optimum rates.168 This is putting increased
of supplementing weed control. This work is currently focused selection pressure on the SOAs that remain. Grains are global
on two areas, harvest weed seed control and cover crop suppres- commodities and global demand drives prices and consequently
sion of weeds.154–158 Mechanical weed control has been revived in farmer choice as to what crops to grow. Weed-control decisions
some areas. Deep plowing has been shown to reduce emergence are heavily influenced by economics and utilize systems that pro-
of small-seeded weed species such as Palmer amaranth.156,159 vide the greatest measurable, near-term economic return. In many
Inter-row cultivation in crops such as corn, cotton and soybeans is cases, proactive resistance management comes at a short-term
an effective means of removing many weed species, but is sparsely cost, even though it may enhance long-term profits.69
adopted due to labor concerns.160,161 Robotic removal of weeds The above issues heavily influence farmer adoption of resistance
has been posited as a possible tool for weed management,162 management practices and make some of these practices diffi-
but currently there are no such devices commercially available cult to implement. Continued education and incentives will be

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Herbicide resistance around the world www.soci.org

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