Review Received: 13 May 2014

Revised: 4 October 2014

Accepted article published: 27 October 2014

Published online in Wiley Online Library:

(wileyonlinelibrary.com) DOI 10.1002/ps.3928

Integrated pest management and weed management in the United States and Canada Micheal DK Owen,a* Hugh J Beckie,b Julia Y Leeson,b Jason K Norsworthyc and Larry E Steckeld Abstract There is interest in more diverse weed management tactics because of evolved herbicide resistance in important weeds in many US and Canadian crop systems. While herbicide resistance in weeds is not new, the issue has become critical because of the adoption of simple, convenient and inexpensive crop systems based on genetically engineered glyphosate-tolerant crop cultivars. Importantly, genetic engineering has not been a factor in rice and wheat, two globally important food crops. There are many tactics that help to mitigate herbicide resistance in weeds and should be widely adopted. Evolved herbicide resistance in key weeds has influenced a limited number of growers to include a more diverse suite of tactics to supplement existing herbicidal tactics. Most growers still emphasize herbicides, often to the exclusion of alternative tactics. Application of integrated pest management for weeds is better characterized as integrated weed management, and more typically integrated herbicide management. However, adoption of diverse weed management tactics is limited. Modifying herbicide use will not solve herbicide resistance in weeds, and the relief provided by different herbicide use practices is generally short-lived at best. More diversity of tactics for weed management must be incorporated in crop systems. © 2014 Society of Chemical Industry Keywords: integrated pest management; integrated herbicide management; integrated weed management; glyphosate; herbicide resistance

1

INTRODUCTION

Organisms adapt to all control tactics used in agriculture. Unfortunately, agriculture does not proactively address pest problems until they cause considerable economic loss. Agriculture fails to address pest issues proactively not because of pest biology or ecology but because of the socioeconomic features of modern agriculture.1 Historically, when a new herbicide resistance is discovered, agriculture will deny or ignore the problem and presume that effective herbicides still exist that will help to control the new issue. Unfortunately, denial of the problem allows the herbicide-resistant (HR) weed biotypes to increase until the problem is so widespread that management options are costly and difficult. Evolved resistance to glyphosate best represents the failure of agriculture to address an inevitable problem that has now become a global issue.2,3 The rapid evolution of resistance to acetolactate synthase (ALS)-inhibiting herbicides in a number of agriculturally important weeds is another example of the failure of agriculture weed management to address issues proactively.4 Agriculture in these examples was negligent in formulating and adopting strategies to steward the important herbicides proactively and to keep widespread herbicide resistance from evolving. Given the high adoption rate of genetically engineered (GE) glyphosate-tolerant maize (Zea mays L.), cotton (Gossypium hirsutum L.), soybean (Glycine max L.) and sugar beet (Beta vulgaris L.) in the United States (US) and Canada, and how the technology was used, it should have been intuitively evident that weeds would rapidly evolve resistance to glyphosate.5 In 2012, estimates suggested that more than 24.7 million ha had been affected by Pest Manag Sci (2014)

glyphosate-resistant weeds, which was a 34% increase from 2011; approximately 50% of the growers surveyed reported problems of glyphosate resistance.6 However, the simplicity and convenience of using glyphosate in a glyphosate-tolerant crop and the relatively low cost of weed management undoubtedly clouded the judgment of growers and agribusiness such that the basic principles of integrated pest management (IPM) and integrated weed management (IWM) were not practiced. Other major characteristics of glyphosate-based weed management contributing to the hesitancy of agriculture to adopt IWM tactics were improved time management, the ability to minimize tillage and reductions in the use of petroleum fuels and presumed more toxic herbicides.7 Furthermore, the improved time efficiency in agriculture attributable to glyphosate-based crop systems facilitated a major socioeconomic change in agriculture. Fewer farmers could manage larger farms over greater distances.8

∗

Correspondence to: Micheal DK Owen, Department of Agronomy, Iowa State University, 3218 Agronomy Hall, Ames, IA 50011, USA. E-mail: [email protected]

a Department of Agronomy, Iowa State University, Ames, IA, USA b Agriculture and Agri-Food Canada, Saskatoon Research Center, Saskatchewan, Canada c Department of Crop, Soil and Environmental Sciences, University of Arkansas, Fayetteville, AR, USA d Department of Plant Sciences, University of Tennessee, Knoxville, TN, USA

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www.soci.org The adoption of practices with greater complexity and presumed risk (e.g. IWM), as perceived by growers, has been limited. Growers focused more on the economics than the evolution of herbicide resistance.9 One new ‘approach’ that is being considered for the mitigation of HR weeds is the integration of the social and economic sciences with the biophysical and technological sciences.10 The objectives of this paper will be to assess the adoption of integrated approaches for weed management in several major crop systems in the US and Canada, and to describe whether these approaches are effective at mitigating the evolution of HR weeds.

2 DEFINITIONS OF INTEGRATED PEST MANAGEMENT AND INTEGRATED WEED MANAGEMENT AND IMPLICATIONS FOR HERBICIDE-RESISTANT WEEDS There are numerous definitions of IPM, although most of these focus on other pest complexes and typically are more appropriate for insect pests than for weeds. This statement is based on the biological and ecological differences in the important pest complexes and the crops in which they are problems. For example, it is likely more effective to address the management of insect pests with crop rotation (i.e. Diabrotica spp.) or with pest thresholds than the management of weeds. Given the greater similarities between weeds and crops than between insects and crops, the crop rotations needed to have a major impact on the weed community are necessarily more complex and longer term than the rotation needed to affect insect pests. Thresholds may function for insect pest management, but are not often advisable in weed management, particularly HR weed management. Allowing weeds to survive in a crop system results in ever-increasing future problems due to seed dormancy. Furthermore, the relative competitive ability of weeds with crop yield changes with the environmental conditions. The United States Council on Environmental Quality published a report in 197211 that defined IPM as: An approach that employs a combination of techniques to control the wide variety of potential pests that may threaten crops. It involves maximum reliance on natural pest population controls, along with a combination of techniques that may contribute to suppression – cultural methods, pest-specific diseases, resistant crop varieties, sterile insects, attractants, augmentation of parasites or predators, or chemical pesticides as needed. More recently, Bottrell refined the definition of IPM to include the ‘selection, integration and implementation of control based on predicted economic, ecological and sociological consequences’.12 Nevertheless, it is clear that these definitions address insects, diseases and nematodes and do not readily adapt to weeds and weed management. In fact, there were only five paragraphs specifically dedicated to IPM and weeds in the 120-page publication Integrated Pest Management.12 Weed scientists quickly became aware that the push towards IPM needed to be modified to accommodate the most economically important and ubiquitous pest complex in global agriculture.13 Shaw in 1964 described the need for a diverse approach to controlling weeds beyond chemical weed control methods.14 The weed science literature is replete with scholarly publications that describe individual components that could contribute to a diverse strategy for weed management (i.e. weed thresholds, soil pH, crop

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population density and row configuration). However, the concept of manipulating the entire crop system to manage weeds was not ‘formally’ recognized until the 1970s.15 The term ‘integrated weed management’ (IWM) was described in a 1982 review by Walker and Buchanan who suggested that IWM had been a term used and accepted by the weed science community since the early 1970s, but there was discord among individuals with regard to the core concepts. Conceptually, the need to include a range of technologies rather than only herbicides for weed control was commonly lost, given the successes of chemical weed control.15 Numerous reviews describing IWM can be referenced for specific details.16 Regardless of the definition, HR weed management programs that include a diverse suite of tactics have not been widely practiced and possibly not seriously considered in many commercial agriculture systems until HR weed populations have become so serious that they have forced the issue. The authors recognize that tactics adopted by a small portion of growers are useful, but wonder how impactful some of these tactics actually are on HR weeds and question how widely tactics (i.e. controlling weed escapes) have been implemented and whether growers have successfully organized tactics into more robust weed management programs.17 A national symposium to address issues surrounding HR weeds, including the adoption of IWM, was sponsored by the National Academies of Sciences (NAS) and hosted by the National Research Council (NRC) in Washington, DC, in 2012 (http://www.nap.edu/catalog.php?record_id = 13518). At this meeting, the problem of HR weeds was described and potential solutions to the issue were discussed. However, no clear courses of action were proposed. Subsequently, there has been a concerted effort by the Weed Science Society of America (WSSA) to work closely with government agencies and commodity organizations to refocus weed management policies and tactics on a more diverse and integrated strategy to address widespread herbicide resistance.18 The tactics suggested in resulting papers describe best management practices (BMPs) and in total encompass conceptually an IWM approach.18 However, regardless of how weed management tactics are characterized, whether IPM, IWM or BMP, the reality is that alternative tactics with respect to herbicides have not been successful, given the increasing evolution of HR weeds in many crop systems in the US and Canada. Currently, diversification of weed management practices can best be described as integrated herbicide management (IHM). Importantly, diverse approaches to weed management described in the historic and current weed management literature are recognized, but most tactics other than herbicides are not widely adopted by growers. Important historic weed management tactics need to be reviewed, with an emphasis on using multiple diverse strategies to best address the burgeoning issues of HR weeds. Current technologies have improved some historically important tactics (i.e. sensor-guided tillage equipment), making them more acceptable in modern agriculture. Efforts to engage a wider audience and utilize approaches that include the social sciences are under way to better effect changes in the management of HR weeds.10

3 EVOLUTION OF HERBICIDE RESISTANCE IN WEEDS Harper predicted herbicide resistance in weeds as early as 1956.19 Baker described weed adaptation to specific conditions and crops

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Integrated pest and weed management in the US and Canada and provided insight into the genetic flexibility in weeds that has made them successful in all forms of agriculture.20 Gressel and Segel (1978) developed a model for herbicide resistance and detailed how various factors affected the evolution of HR weeds.21 A clear understanding of why weeds are ubiquitous problems in agriculture has been historically available. Adaptability of weeds owing to genetic diversity must be considered in the development of consistent HR weed management. Historic research on weed biology, ecology and genetics and the implications for management tactics must be revisited, in light of the increasing issues with evolved herbicide resistance in weeds. Given the trajectory that agriculture appears to have taken during the last 50 years and the apparent hesitancy to make widespread tactical adjustments, problems with HR weeds will escalate. Currently, 435 unique cases of HR weed biotypes are reported globally.4 This number changes frequently with new reports. Herbicide resistance is found in 238 weed species, including 138 dicots and 100 monocots. Resistance has evolved to most of the commercially available herbicide sites of action, and instances of HR weeds continue to increase globally.4 Several possible ways in which weeds could evolve resistance to glyphosate were reported in 1996.22 Mutation conferring resistance to glyphosate in specific weeds is now suggested as being the most important pest problem for global agriculture. While this problem has been linked to the adoption of GE crops, glyphosate-resistant weeds evolved owing to a lack of diversity in weed management tactics and is only indirectly a factor of GE crops.23 Glyphosate-resistant weeds were first reported in conventional crops and orchards in 1996 but became a major problem in GE crops where glyphosate was used recurrently without other tactics to manage weeds.4,23 The economic damage was the result of the way in which glyphosate was used in the glyphosate-resistant crops and attributable to the management decisions made by growers and others.2 There are currently 30 weed species reported to have glyphosate resistance.4 However, resistance to other important mechanisms of action (MOAs) evolved in weeds prior to glyphosate resistance. Photosystem II inhibitors (i.e. atrazine and simazine) were used on millions of hectares and predictably resulted in widespread resistance in a reported 100 weed species.4 The introduction of ALS-inhibiting herbicides was viewed as a solution to the photosystem II herbicide resistance until evolved resistance to these herbicides became an issue.24 Resistance to ALS-inhibiting herbicides is widespread and has evolved in 145 weed species.4 It helped to speed up the adoption of glyphosate-resistant crops, and growers became less concerned about ALS herbicide resistance when glyphosate could be applied post-emergence in crops.24 Historically, herbicides with newly discovered MOAs became commercially available in a timely fashion and were presumed to resolve the problems of existing herbicide resistance in key weeds. Unfortunately, there are no new herbicide MOAs identified, and it is unlikely that significant discoveries will occur soon to solve the current HR weed problems, particularly glyphosate resistance. While there are new GE crop cultivars with herbicide tolerance (i.e. to auxin herbicides) under commercial development, the herbicides for these new GE crop cultivars are older, previously available products and have existing resistance in important weeds (i.e. Amaranthus tuberculatus).25 3.1 Specific weeds with evolved herbicide resistance Several economically important weeds have evolved resistance to glyphosate and other herbicides.26 These weeds include, but are Pest Manag Sci (2014)

www.soci.org not limited to, Amaranthus palmeri, A. tuberculatus, Ambrosia trifida, Conyza canadensis, Lolium rigidum and Sorghum halepense. Importantly, several of these weeds have evolved multiple herbicide resistance and cross-resistance; L. rigidum biotypes have been identified with resistance to at least seven herbicide MOAs in Australia, and A. tuberculatus populations in Iowa demonstrate resistance to five MOAs, including glyphosate (Table 1).4 A. palmeri resistance has been well publicized and has brought renewed attention to the importance of weeds and weed management for economic crop production.27 While the issues of herbicide resistance are severe in cotton and soybean production in the southern US, issues with herbicide resistance in A. tuberculatus are suggested to be of greater economic importance than the losses attributable to A. palmeri simply because of the greater area infested with A. tuberculatus in the Midwest US. A recent survey of Iowa fields supported by the Iowa Soybean Association estimated (P ≥ 0.05) that 65–74% of fields have A. tuberculatus visible above the soybean canopy at harvest. The occurrence of weeds above the soybean canopy in the fall is coincidental with herbicide resistance detected in these populations. Greenhouse evaluations of five herbicide MOAs on more than 200 A. tuberculatus populations from Iowa estimated (P > 0.05) that resistance to ALS-inhibiting herbicides occurred in 62–77% of the fields, resistance to photosystem II-inhibiting herbicides in 44–51%, glyphosate resistance in 42–48%, resistance to protoporphyrinogen oxidase (PPO)-inhibiting herbicides in 10–12% and resistance to 4-hydroxyphenyl-pyruvate-dioxygenase (HPPD)-inhibiting herbicides in 24–27% of Iowa fields.25 Of particular concern is the estimate that 57–65% of Iowa fields have A. tuberculatus populations with multiple herbicide resistance, and that three-way herbicide resistance occurs in approximately 24% of the Iowa fields. The most common three-way herbicide resistance was to ALS-inhibiting herbicides, photosystem II herbicides and glyphosate. Five-way herbicide resistance was estimated to occur in 7% of Iowa fields.25 Clearly, management of A. tuberculatus populations with evolved resistance to five herbicide MOAs will be a great challenge. Nevertheless, the Amaranthaceae have become prominent economic problems in many US crop systems and demonstrate a high potential to evolve resistance to many important herbicides, including the auxins. Currently, the herbicide MOAs commonly available in US and Canadian crop systems to which Amaranthaceae has not evolved resistance include the glutamine synthase inhibitor, microtubule inhibitors, very-long-chain fatty acid inhibitors and photosystem I inhibitors.

4

ADOPTION OF GE CROPS

The US is the global leader in production of biotech crops, with 69.5 million ha, representing 41% of global use.28 US agriculture has an average adoption rate of ∼90% across its principal biotech crops. Genetically engineered maize, cotton and soybean continue to be the most widely planted crop cultivar types in the US (Fig. 1). GE maize is planted on 90% of the US maize area, while GE soybean and GE cotton are planted on 93 and 90% of the area planted to those crops respectively.29 The dominant GE trait in these crop cultivars is tolerance to glyphosate, although in maize and cotton, cultivars may have stacked traits with herbicide tolerance and Bacillus thuringiensis (Bt) for insect pest management. Alfalfa (Medicago sativa) has the fourth largest crop area in the US and is planted on approximately 8 million ha. The deregulation of GE alfalfa allows grower adoption, and the area planted to GE alfalfa is

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Table 1. Evolved herbicide resistance for selected weed speciesa Weed species Herbicide mechanism of actionb

Amaranthus palmeri

Amaranthus tuberculatus

Ambrosia trifida

Conyza canadensis

Lolium rigidumc

Sorghum halepense

ACCase inhibitors (group 1) No No No No Yes ALS inhibitors (group 2) Yes Yes Yes Yes Yes Microtubule inhibitors (group 3) Yes No No No Yes Auxins (group 4) No Yes No No No Photosystem II inhibitors (group 5) Yes Yes No Yes Yes Lipid inhibitors (group 8) No No No No Yes EPSPS inhibitors (group 9) Yes Yes Yes Yes Yes Carotenoid inhibitors (group 13) No No No No Yes PPO inhibitors (group 14) No Yes No No No Very-long-chain fatty acid inhibitors No No No No Yes (group 15) Photosystem I electron diverters No No No Yes Yes (group 22) Mitosis inhibitors (group 23) No No No No Yes HPPD inhibitors (group 27) Yes Yes No No No Yes, three-way Yes, five-way Yes, two-way Yes, two-way Yes, seven-way No Multiple resistanced (groups 2, 3, 5, (groups 2, 5, 9, (groups 2 and (groups 2, 5, 9 (groups 1, 2, 3, 9 and 27) 14 and 27) 9) and 22) 8, 9, 13, 15, 22 and 23)

Yes Yes Yes No No No Yes No No No No No No

a Adapted from www.weedscience.com (accessed 7 July 2014).4 b Herbicides described using the Weed Science Society of America classification system. c Multiple resistance in Australia, Chile, Israel, South Africa and Spain. d

Multiple resistance will be a combination of the herbicide groups listed but may not include all of the herbicide groups listed in all biotypes.

100 Percentage of hectares planted

90 80 70 60 50 Cotton

40 30

Soybeans

20 Maize

10

0 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Figure 1. The percentage of the US crop area planted to genetically modified crop cultivars from 2000 to 2013. Adapted from http://www.ers. usda.gov/data-products/adoption-of-genetically-engineered-crops-in-the-us/recent-trends-in-ge-adoption.aspx#.Uuk1HPbqL2A.29

likely to increase rapidly.30 It is estimated that GE alfalfa currently is planted on approximately 200 000 ha, and the area is projected to increase by 35–50% in 2015.30 Genetically engineered sugar beet adoption by growers has been faster than any other biotech crop, and GE cultivars are now planted on approximately 95% of the 480 000 ha planted to sugar beets in the US.30 The adoption rate of GE canola (Brassica napus L.) in the US is 97.5% of the area planted to canola.28 Canada has approximately 11.6 million ha of GE crops and is the fourth leading country with regard to GE crop adoption.28 Genetically engineered canola, maize, soybean and sugar beet are grown in Canada, and herbicide tolerance is the primary GE trait

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in these cultivars. As in the US, Canada has experienced a rapid adoption of GE canola since its introduction in 1995 (Fig. 2). Most growers in Canada switched to GE cultivars within 15 years of their introduction.

4.1 Implications of GE crop adoption for farm demographics in the US A key consideration with regard to the adoption of GE crop technologies was the resultant change in farm demographics. Factors such as agricultural policy issues and the economics of crop production also affected pesticide use, GE crop adoption and subsequently farm practices.31 Specifically, the average farm

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Figure 2. Adoption of herbicide-resistant canola cultivars in Canada from 1995 to 2010 (Beckie H, unpublished).

size in the US increased by 7% from 1969 to 2007.32 Farm size increased again from 2007 to 2012 by almost 4%.33 Furthermore, the number of farms declined in the US by 19% from 1969 to 2007, and by another 4% from 2007 to 2012.32,33 While the number of 0.4–202 ha farms declined in the US from 1969 to 2007, the greatest decline being for 40–202 ha farms, the number of farms with a size ranging from 202 to >809 ha almost doubled and the number of farms with 405 ha or more increased fourfold.32 Similar changes were reported in the 2012 Census of Agriculture Preliminary Report.33 Given that the area under crop production was steady or increasing over the period from 1969 to 2007, significant time management issues evolved in agriculture; fewer farmers are now managing more hectares over greater distances in the same 24 h day. Considering the importance and variability of days available for field operations, increased farm size, shortages of qualified labor and perceptions of risk, the simplified and effective weed control available with GE crops was highly desirable.34 Another important consideration of farm demographics is the increasing percentage of farm land that is not farmed by the landowner (Fig. 3). More than 50% of farmland is not farmed by the owner across the Midwest US and the Mississippi Delta, and often the landowner is located more than 40 km from the farm.35 In Iowa, 56% of the landowners are not related to the farmer, and 64% of farmers have more than one landlord. Landlords tend to require farmers to use the least expensive weed management tactics because production costs and short-term profitability are often a greater concern than long-term sustainability, return on investments and the use of best agronomic practices. Concerns for weed management cost typically result in the use of glyphosate rather than the adoption of more diverse and durable weed management programs. The adoption of GE crops also supports the flexibility of the farmer to have off-farm employment.10,33 Pest Manag Sci (2014)

4.2 Presumed benefits from the adoption of GE crops GE crop technologies and the use of glyphosate for weed control were extremely attractive given the ‘new’ agricultural demographics because growers perceived that the glyphosate-based systems were effective, easy, economical, safe and simple.36 Reducing the time dedicated to weed management is a key driver of the use of glyphosate-based crop systems and supported the changes in agricultural demographics.37 Other positive characteristics attributed to the GE technologies were crop safety, consistency of weed control and a positive health perspective for farm families.38 Interestingly, these characteristics were valued by adopters more than the lower costs attributed to weed control, and this was consistent across the major glyphosate-based crop systems.38 Society also benefited from the adoption of GE crops as a result of the improved environmental quality attributable to less soil erosion and better water quality.39 Clearly, the GE technologies and glyphosate have provided important pecuniary and non-pecuniary benefits since their 1996 commercial introduction.1,10 4.3 Presumed risks from the adoption of GE crops Interestingly, many of the same factors and considerations described as benefits of GE crops can also be interpreted as risks. The unprecedented adoption of GE crops and the convenience and simplicity of the glyphosate-based crop systems for weed control have caused weed shifts and evolved glyphosate resistance in weeds.3,40 Time constraints due to increasing farm size and costs of herbicides and other inputs (i.e. petroleum fuels) supported decisions to use glyphosate and impeded the ability or desire of many growers to adopt more complex and time-consuming IWM tactics. Given that glyphosate-based crop systems dominate cotton, maize and soybean in the US, it can be argued that IWM and IHM have not been widely practiced by growers, and thus there has been a loss of ‘institutional’ knowledge about

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0 200 Miles

Percent of Land in Farms Rented or Leased: 2007

2007 Census of Agriculture

Percent Less than 20 20 - 24 25 - 29 30 - 39 40 - 49 50 or more 0 0

100

Miles

100

Miles 07-M117 U.S. Department of Agriculture, National Agricultural Statistics Service

United States 38.0 Percent

Figure 3. The percentage of US farmland rented or leased in 2007. Adapted from http://www.agcensus.usda.gov/Publications/2007/Online_Highlights/ Fact_Sheets/Demographics/demographics.pdf.

weeds, weed management, herbicides and other diverse cultural and mechanical weed management tactics. Also, the decline in support for industrial research limited herbicide discovery, and there has been no new herbicide MOAs in commercial herbicide products for several decades. A similar decline or lack of research support occurred in federal grant programs and support from state and national commodity associations. There are other concerns, such as the displacement of smaller farms, food safety issues and the introgression of GE traits to wild and weedy species, but there is little objective scientific evidence that supports these perceived risks.41 The exception for the introgression of GE traits is in canola, and the GE traits have moved into sexually compatible weedy relatives.42 One risk that is often attributed to the adoption of GE crops is the evolved herbicide resistance in weeds. Herbicide resistance in weeds is the result of the overuse of a specific herbicide (i.e. glyphosate) and represents a management decision. For example, the evolution of resistance to photosystem II- and ALS-inhibiting herbicides occurred widely in the US and Canada without any involvement of GE crop technologies.

5 ADOPTION OF SELECTED IWM STRATEGIES TO MANAGE HR WEEDS There has been recent discussion and interest in developing greater diversity in weed management (e.g. IWM and BMPs)

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because of the increasing difficulties in managing HR weeds (Table 2). However, many growers are only willing to consider changing, adjusting or adding herbicides (IHM).35 Using herbicide rotations and including multiple herbicide MOAs in a weed management program to improve HR weed management have gained traction in the US and Canada. However, given the lack of experience with herbicides other than glyphosate for many growers, there may not be a good appreciation of how to implement herbicide diversity effectively (Table 3).18,35 In part, socioeconomic issues (e.g. time management and perceived higher costs of weed control) have slowed the adoption of more effective herbicide programs, but also the limited communication by the industry about how their proprietary products might fit into a more diverse and effective weed management program is also a problem. These issues are compounded by the loss of grower experience and knowledge about herbicides and weed management (e.g. understanding the MOAs of herbicides, knowing herbicide resistance in specific fields).10,43 The loss of ‘institutional’ knowledge about weed management, herbicides and alternative tactics also contributed to unwillingness of growers to diversify weed management strategies. Historically, part of the problem hampering the adoption of IWM has been the remarkable success of herbicides to manage weeds in most crop production systems.13,44 The ability to use a herbicide that provided control of weeds rapidly became the standard practice in the US, Canada and developed countries globally in the 1950s to 1970s.44 Herbicides effectively replaced a more

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Table 2. Assessment of tactics to help manage herbicide-resistant weedsa Tactic Herbicide MOA rotation Herbicide mixtures

Variable application rate and timing

Adjusted herbicide rates

Benefits

Risks

Reduced selection pressure, control of herbicide resistant weeds, greater diversity Reduced selection pressure, improved control, broader weed spectrum, greater diversity Better control of target weeds, more efficient use of herbicides, fall applications for winter annuals Better control of target species, longer residual activity

Precision application

Decreased herbicide use, reduced selection pressure

Primary tillage

Decreased selection pressure, greater diversity, consistent efficacy, depletion of weed seedbank Decreased selection pressure, consistent efficacy, relatively inexpensive, greater diversity

Mechanical tactics

Crop selection/rotation

Improved diversity, allows different herbicide options, reduced selection pressure

Adjusted planting time

Improved efficacy on target weeds, reduced selection pressure

Adjusted seeding rate

Improved crop competitive ability, reduced selection pressure

Planting configuration

Improved crop competitive ability, reduced selection pressure Greater diversity, improved competitive ability, reduced selection pressure, possible allelopathy

Cover crops, mulches, intercrop systems

Weed seedbank management

Reduced HR weed pressure, reduced selection pressure

Manipulation of nutrients

Improved crop competitive ability, efficient use of nutrients, lower nutrient costs, greater diversity Greater diversity, decreased selection pressure, relatively inexpensive equipment Ability to use specific herbicides, no crop injury, control of existing specific herbicide resistance

Flaming

Herbicide-resistant crops

a

Relative effectiveness

Adoption rate

Lack of new and available MOAs, phytotoxicity, limited weed spectrum of alternatives Poor activity on HR weed species, increased cost, potential phytotoxicity, use of reduced herbicide rates Reduced residual activity, poor application timing, more applications, selection for non-target-site resistance Increased target-site selection pressure with higher rates, increased non-target-site selection with reduced rates Increased application cost, weed maps unavailable, poor understanding of weed seedbank dynamics, variable control Increased time required, increased soil erosion, increased costs, more fuel used, supplemental tactics required

Fair to excellent

High

Fair to excellent

High

Fair

Medium

Excellent (high rates), poor (reduced rates)

High

Fair

Low

Good to excellent

Medium

Increased time required, possible increased soil erosion, increased costs, more fuel used, possible crop injury Economic risks of alternative rotation crops, rotation crops too similar to increase diversity, inconsistent impact on HR weeds, lack of research base Requires alternative strategies, potential for yield loss, need for increased rotation diversity, useful for specific crops Increased seed costs, potentially increased risk from other pests, increased intraspecific competition, reduced yields Limits mechanical tactics, equipment limitations, places emphasis on herbicides Inconsistent impact on HR weeds, poor understanding of the system and lack of research information, lack of good cover crops, need to manage the cover crop/mulch Poor understanding about seed bank dynamics, need for aggressive tillage, emphasis on herbicides, high level of management skill required, need for novel equipment Poor research base, inconsistent results, potential for crop yield loss

Fair to good

Low

Fair to good

Low to high

Fair to excellent

Low

Fair

Low to medium

Fair

Low to medium

Fair to good

Low

Fair

Low to medium

Poor to fair

Low

Increased time required, increased costs, more fuel used, possible crop injury Lack of diversity, increase selection pressure, concerns for non-target crops, possible limited weed spectrum

Fair to good

Low

Fair to excellent

Medium to high

Adapted from Green and Owen.36 Used with permission.

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Table 3. Use and effectiveness of tactics by Iowa growers to manage herbicide-resistant weedsa

Tactic

Not Effectivenessb effective (%) (%)

Do not know (%)

Yes (%)

No (%)

93 80

7 20

97 92

2 1

2 7

74 71

26 29

93 86

3 1

4 13

60

40

79

1

18

49 29 27

51 71 73

74 77 60

11 9 5

15 14 35

25

75

81

6

13

23

77

74

3

23

16

84

62

6

32

Crop rotation Multiple herbicide application timings Tillage Multiple MOAs3 each season Multiple MOAs in each application Higher planting rates Hand weeding Herbicide-resistant cultivars, not glyphosate Mechanical tactics (i.e. cultivation) Inclusion of a forage in rotation plan Cover crop

a Adapted from Arbuckle, Jr, and Lasley.35 b Combined percentages of responses ‘somewhat effective’, ‘effective’

and ‘very effective’. c Mechanisms of action.

diverse suite of tactics used to manage weeds (i.e. mechanical cultivation and crop rotation), resulting in less labor requirements, greater time utilization efficiency, reduced energy costs in crop production and potentially improved crop yields.13,44 However, this remarkable success with herbicides facilitated the evolution of new weed problems, which in turn required more intensive use of herbicides.45 The adoption of glyphosate-resistant crops and the use of glyphosate have been major impediments to IWM adoption since

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1996 (Figs 1 and 4). Consider that 37.5 million ha of GE maize with herbicide tolerance, 29.2 million ha of soybean and 3.4 million ha of cotton cultivars with GE herbicide tolerance were planted in 2013.46 Estimates made in 2010 suggested that approximately 9% of the glyphosate-tolerant maize, 53% of the glyphosate-tolerant soybean and 22% of the glyphosate-tolerant cotton received only glyphosate for weed control.47 While these figures have likely changed somewhat in the following years, there is a clear indication that a majority of the area planted to row crops in the US has only limited IWM strategies in place and may not have IHM practiced on a large percentage of the glyphosate-tolerant crops planted. The size of the farming enterprise also influences the willingness of the grower to adopt IWM. A survey of Indiana growers suggested that larger farm operations (800 ha or more) were more likely to use IWM than smaller farms.48 A survey of Iowa growers indicated that awareness of HR weeds on individual farms ranged from 60 to 78% (Fig. 5). Growers farming 100 ha or less were less aware of HR weeds and did not adopt IWM readily when compared with growers farming more than 100 ha.49 Adoption of IWM programs by growers farming 101–1011 ha was similar to but less than adoption by growers farming 1012–2024 ha, who were most likely to adopt IWM strategies. Growers with farms larger than 2024 ha were the least likely to adopt IWM (Fig. 5). It is important to recognize that the IWM strategies that the Iowa growers were willing to adopt focused primarily on herbicide diversity and considerably less on other more diverse tactics for weed management.35 In the Canadian Prairie provinces, IWM also focused on herbicide diversity more often than alternative tactics, depending on the specific crop. Weed management surveys indicated that the total herbicide active ingredients applied to each of the main cereal crops (not glyphosate tolerant) did not change from the 1990s to the early 2000s (Fig. 6).50 Additionally, the active ingredient (kg ha−1 ) applied to canola, whether GE or non-GE, was similar in the 1990s. The herbicide active ingredient (kg ha−1 ) applied to canola was similar to the amount applied to barley (Hordeum vulgare L.) but greater than the amount applied to spring wheat (Triticum aestivum L.) and oat (Avena fatua L.). The herbicide active ingredient (kg ha−1 ) applied to imidazolinone-HR canola was much

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Figure 6. Influence of crop on herbicide use in terms of (a) active ingredient and (b) environmental impact, based on data from the Canadian Prairie province weed management surveys (bars denote standard error). Adapted from Kovach et al.50

less than for the other canola types and the cereal crops, with the exception of oat in the 1990s. The environmental impact of herbicides applied to oat has increased from the 1990s to the 2000s, whereas the environmental impact of herbicides applied to other cereals has remained similar (Fig. 6). Glyphosate- and imidazolinone-HR canola had a lower environmental impact than non-HR canola in the 1990s, whereas glufosinate-HR canola had a similar environmental impact to non-HR canola.50 Alternative tactics for weed management that required more knowledge, time and expense were largely abandoned over time for the simple herbicide-based approaches to kill weeds. One of the results of this simple approach for weed management has been the evolution of herbicide resistance in weeds.51 However, historically, at each occurrence of a major herbicide resistance evolutionary ‘event’ (i.e. ALS-inhibiting herbicide resistance), new technologies were introduced that circumvented the HR weed problems and were then widely adopted by growers. Unfortunately, this historic information has not been considered in the decisions made for current weed management. It was not widely understood that, with the new herbicide-based technologies, the focus was once again solely on herbicides and not on developing a durable weed management system.52 Pest Manag Sci (2014)

Clearly, weed management discussions must not focus only on herbicides. The principles of IWM have changed little, but have been revised and revisited to meet current crop systems.36,53 While many of the IWM tactics are not new, if implemented in a crop system increasing the diversity of approaches for weed management, problems with HR weeds can be lessened. The greater the diversity and number of tactics adopted, the more successful and durable the overall weed management program becomes.36 Generally, the combination of many tactics provides better weed management than the simple addition of individual tactics.54

5.1 Crop rotation Historically, agronomic systems with complex crop rotations support weed management. Weed population densities and biomass are markedly reduced by crop rotation systems that provide temporal diversity (Table 2).55 A complex crop rotation system creates different ecological environments by changing features of the field, such as competition for resources, soil disturbance or other aspects of the system resulting in an unstable environment for weeds that have been successful.55 Rotations with crops

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Figure 7. Number of different crops included in a 6 year crop rotation, based on data from Canadian Prairie province weed management surveys (shortest unbiased 95% confidence limits for the proportions are shown). Adapted from Neeser et al.59

with different growth habits (i.e. spring monocot grains and summer annual dicot crops) provide considerable ecological diversity, which improves weed management opportunities. The herbicide options available for all rotational crops in a diverse crop rotation system should also be considered in order to best supplement the impact of crop rotation on weeds. Where herbicides are not used on specific crops in a diverse crop rotation system, the weed seedbank may increase.56 However, for more complex crop rotation schemes, one crop without a herbicide treatment may not negatively affect the overall reduction in the weed seedbank. Tillage as part of a crop rotation system can improve weed management, crop yield and profitability (Table 2).54 Crop rotation used for HR weed management was reported to be effective for 97% of the respondents to the 2013 Iowa Farm and Rural Life Poll (Table 3).35 However, the dominant crop rotations in Iowa are maize rotated to maize or maize rotated to soybean, and the cultivars planted of both are largely glyphosate tolerant, which results in limited herbicide diversity as well as limited growth habit diversity. Similarly, in many southern US agricultural systems, glyphosate-tolerant cotton is grown continuously or rotated with glyphosate-tolerant soybean and, in a limited area, glyphosate-tolerant maize (Culpepper AS, private communication). In these situations there is little positive impact on weed management owing to the selection for glyphosate-resistant weeds with the recurrent use of glyphosate.57 In recent years, glyphosate-tolerant maize has been included in southern crop rotation plans, but on a very limited area. Generally, a monoculture system is more prevalent in the southern US than in the Midwest.58 In the Canadian Prairie provinces, a majority of growers use crop rotation to help manage weeds on their farms. In Alberta and Saskatchewan, 90–92% of growers reported using crop rotation to improve weed management.59 The frequency of this practice was higher in Manitoba, with 99% of respondents rotating crops for weed control in 2002, and not significantly different from that reported in 1997. In 2010, Alberta growers ranked crop rotation as their most important weed management tool, even surpassing herbicides.59 The complexity of crop rotations was evaluated on the basis of a 6 year crop history. Overall, the participants in the 2000s Canadian Prairie province weed management surveys reported growing 66 different crops or crop mixes, including fallow. Few growers only grew one crop during this time ( oat > barley > wheat.85 Another aspect of using the competitiveness of crops as a tactic to help manage HR weeds is the large range in competitiveness that may exist among cultivars of the same crop. Again, in US row crop agriculture there is limited opportunity for growers to adopt this as an IWM tactic. Improving crop cultivar competitive ability is an achievable goal for seed companies. However, seed company emphasis is to improve crop yield potential, and the breeding programs are conducted without interference from weeds, such that improved competitive ability of specific cultivars may be lost. Research in Canada has identified cultivars of wheat, barley, field pea (Pisum sativum L.) and canola that are able to suppress weeds significantly better than other cultivars of the same species.86 – 88 5.3.5 Crop population density, planting configuration and planting date Typically, factors such as crop population density, planting configuration and planting date have been addressed from the perspective of improved crop yield potential. However, these factors are also important with regard to IWM and are best utilized in collaboration with other alternative tactics for weed management.70 Increasing maize population density reduced the competitiveness of weeds and increased maize yield.89 Narrow row and other planting configurations also provided benefits for weed and pest management, as well as for increased yield potential in maize, cotton and soybean.90,91 Research from Canada demonstrated that increased crop seeding rates contributed to weed suppression in several crops and was used by growers as a weed control tactic.92,93 Planting configuration, specifically row width, also affects the crop canopy microclimate, which may change the crop morphology and resource utilization and improve weed management.94 Narrow row soybean systems are more competitive with weeds than wider row planting configurations.95 Decreasing row spacing in spring barley potentially increases crop yield and suppresses weeds.96 While narrow row planting configurations may reduce weed competition, they generally are more dependent on herbicides for most of the weed management and may eliminate some mechanical options such as row cultivation.78 Crop planting dates have also changed over time in an effort to improve crop yield potential. For example, maize planting dates have moved progressively earlier in the growing season over several decades. This can have the unintended consequence of a less competitive crop and places greater emphasis on herbicidal weed control.97 Delayed planting dates may improve weed management, particularly when mechanical tactics and tillage are components of the program.77,78 However, delayed planting dates may

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Figure 9. Number of different herbicide groups defined by mechanism of action applied to a field in a 6 year period, based on data from Canadian Prairie province weed management surveys. Adapted from Leeson and Beckie.73

also reduce yield potential, particularly in maize, and may represent a greater risk to crop yield than the benefits of improved weed management. 5.3.6 Nitrogen and fertilizer management Manipulation of fertilizer, and nitrogen specifically, can be an important factor in IWM.55 Placement of fertilizer for preferential access by the crop rather than weeds is a beneficial IWM practice.98 Given the greater responsiveness of some weeds than crops to nitrogen fertilizer, it is important to optimize the amount and timing of fertilization to enhance the competitive ability of the crop species.99 Timing of fertilizer applications also influences the availability of the nutrients to weeds. Various studies have concluded that spring-applied fertilizer can reduce weed abundance.100,101 However, given the importance of environmental conditions to crop responses to fertilizer, there are significant risks to crop yield potential when adapting nitrogen applications from an IWM perspective. There are also risks to water quality from fertilizers applied to crops, and this risk must be considered when developing IWM strategies that include manipulation of fertilizers. 5.3.7 Sanitation An IWM goal is to limit the introduction and spread of new weeds.102 This objective can be achieved by using weed sanitation techniques, such as using certified weed-free seed, cleaning harvesting and tillage equipment, covering grain trucks and mowing or spraying ditches and weed patches. While these practices are promoted in the extension literature, the benefits of many of them are difficult to quantify directly, and thus they have not been a research focus and may not be widely adopted by growers. An exception is a study conducted in conjunction with the 1990s surveys, which indicated that consistent use of weed sanitation decreased the likelihood of occurrence of HR weeds.103 Recent introductions of A. palmeri into new areas in the Midwest US not contiguous with historic infestations of this important weed have reinforced the importance of sanitation as a tactic to manage all HR weeds.104 While alternative practices for weed management described in this section provide a level of effective weed control and represent an important opportunity to establish more diverse IWM programs, anecdotal information suggests that they are not widely adopted owing to time use requirements, perceived Pest Manag Sci (2014)

costs and other factors relating to the socioeconomic changes in agricultural demographics. Individually, each tactic may provide only a modicum of weed management, but when combined with a number of other tactics, weed management increases significantly, specific selection pressures on weed populations decline and profitability improves.36,71 5.4 Herbicide rotations, combinations and application rates to manage HR weeds A common and accepted tactic for adding diversity to weed management is to include more herbicide MOAs. This approach is more appropriately described as IHM (Table 2).18 A tactic to help manage HR weeds that was reported by 71% of the respondents to an Iowa survey was the use of multiple herbicide MOAs, and 60% of the respondents used multiple MOAs in each application (Table 3).35 However, it is critical to include effective herbicide MOAs because simply using several different herbicides does not necessarily provide IHM. Many growers and other agricultural advisers do not recognize the importance of identifying effective herbicide MOAs when developing an HR weed management program. It is also important to recognize existing multiple herbicide resistance in weed populations and select herbicide MOAs that are still effective on weed populations with previously evolved herbicide resistance. Rotating or combining herbicide MOAs are the ‘grower-acceptable’ ways in which IHM can be established in HR weed management programs. Combining herbicide MOAs is preferred for managing HR weeds and slowing the evolution of herbicide resistance when compared with herbicide MOA rotation.105 The key to herbicide-based HR weed management is understanding the selection pressure imparted on the weed population by each herbicide. The complexity of herbicide rotations varied among Canadian Prairie provinces, but has generally increased over time (Fig. 9). There was no difference among provinces in the length of time that herbicide rotations had been used on their farms among growers who rotated herbicides. Each application of a herbicide MOA combination imparts several selection pressures instead of a single annual selection that typifies the rotation of herbicide MOAs. Ideally, every herbicide application would contain multiple effective herbicide MOAs that would each impart the same selection pressure as the herbicides in the mixture.106 The reality is that different herbicides implement

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www.soci.org different selection pressures, and this differential selection pressure can eventually result in evolved resistance to the most effective herbicide. Thus, it is imperative to consider tactics in addition to herbicide diversity for long-term IWM. Herbicide application rate is also an important factor when developing effective HR weed management programs. Cost of herbicides is often the primary concern for growers, and as a result growers will opt to use lower rates than described on the herbicide label. This decision may result in variable control of target weeds, which then requires additional expense for additional herbicide treatments and a potential loss of crop yield. The savings growers believe they are gaining by choosing to use reduced herbicide rates may result in greater expenditure and loss than the cost of applying the labeled herbicide rate.18 If synergism exists for specific herbicide combinations, reduced rates may provide the same control as that achieved with full herbicide rates.107 Importantly, reduced herbicide rates can result in faster evolution of herbicide resistance than full herbicide rates.108

6 CURRENT WEED MANAGEMENT PRACTICES IN ROW CROPS Two decades ago, maize, cotton, soybean and sugar beet producers in the US would implement multiple tactics for weed management: preplant tillage to control weeds and incorporate herbicides, pre-emergence and post-emergence applications of herbicides, row cultivation, post-directed herbicide applications, as well as limited manual weed removal.55,109 – 111 The unprecedented adoption of glyphosate-tolerant crop cultivars resulted in weed management reliance almost exclusively on glyphosate.112 Importantly, the number of herbicide MOAs used in glyphosate-tolerant crops also declined.113 Glyphosate became the most widely used herbicide in the US in 2001, and its usage increased from 0.7 Mt in 1997 to 3.9 Mt in 2006.113 Glyphosate-resistant C. canadensis and A. palmeri forced growers in the southern US to consider more diverse weed management systems. These ‘new’ weed management tactics, if adopted, may be in some ways more diverse than those utilized two decades ago. Along with herbicides and tillage, tactics may include intense manual weeding, cover crops, crop rotations and field border weed management.18,114 Similar issues with glyphosate resistance in A. tuberculatus, A. trifida and C. canadensis are found in the Midwest US. However, observations suggest that enough disturbance occurs with conservation tillage, which is widely practiced in Midwest US crop systems, seemingly to slow the rate of increase in glyphosate-resistant weeds compared with the southern US, where no-tillage systems are more prevalent. The discussions about increasing the diversification of weed management have not dramatically changed US practices, as evidenced by the continued use of glyphosate as the sole herbicide in a high percentage of the row crop area and the relatively low adoption rates of alternative tactics (Fig. 5 and Tables 2 and 3).35,47 The adoption of more diverse weed management tactics (i.e. cover crops) beyond herbicides is on a small percentage of the area planted, and even when a different GE crop cultivar (i.e. glufosinate-tolerant cotton and soybean) is planted, a number of growers may only use the herbicide (glufosinate) to which the GE crop cultivars have tolerance and may not diversify weed management practices (Norsworthy JK, unpublished). The recurrent and exclusive use of any herbicide will inevitably result in weeds with evolved resistance to the herbicide.

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6.1 Weed management in maize More than 39 million ha of maize were planted in the US in 2012, which represents a 5.7% increase from 2011.115 The market for maize-derived biofuel has resulted in more continuous maize rotations in the Midwest US. Growers in the southern US have also increased the area planted to maize in recent years. From 2000 to 2002, in Arkansas, North Carolina, Mississippi and Tennessee the area planted to maize increased by 40%.8 Weed management in US maize should start with a clean seed bed, either through tillage or herbicide applications, to best protect the maximum potential yield.116 In the US, 98% of the maize grown was treated with a herbicide and typically with more than two herbicides or two herbicide applications. The average amount of herbicide used on each hectare of maize in 2009 was 1.12 kg of active ingredient (AI) (http://www.ers.usda.gov/briefing/ARMS/ resourceregions/resourceregions.htm). Glyphosate was applied to 75% of the US maize hectares, and much of the area was treated more than once (Fig. 4).47 Atrazine was applied to 67% of the US maize area planted, and the average application rate was 1.1 kg AI ha−1 . Acetochlor and metolachlor were used on 25 and 24% of the maize area planted respectively, while mesotrione was used on 18% of the maize area planted (http://www.ers.usda.gov/briefing/ARMS/resourceregions/ resourceregions.htm). Other herbicides, including 2,4-D (9.3%), bromoxynil (0.1%), clopyralid (4.6%), dicamba (4%) and isoxaflutole (6%), were used. Herbicides inhibiting ALS were applied on less than 10% of the maize area. Glyphosate was the only herbicide used on approximately 35% of the US maize area planted in 2009.39,47 This lack of diversity of weed management has important implications for weed shifts, evolved herbicide resistance and the ability of growers to manage these problems.52 Many growers in the southern and Midwest US find that rotation to maize can be an effective tactic for glyphosate-resistant weed management because of the herbicides available for maize, particularly the pre-emergence applications. Approximately 30% of the maize grown in the US is in a no-tillage system, and herbicides are the primary if not the sole tactic to manage weeds.117 Traditionally, in states such as Tennessee, approximately 80% of the maize is planted no-tillage, while in Arkansas, maize is planted on beds that are built in the fall. Therefore, the use of spring tillage as a weed management tactic has been minimal.118 In the Midwest US, typically some tillage (e.g. chisel plow) is done after harvest in the fall and generally one tillage trip (i.e. disc harrow) is performed in the spring immediately prior to planting. Importantly, the tillage that is done in the Midwest US improves overall weed management by burying weed seeds. A recent survey of consultants indicated that tillage helps to control glyphosate-resistant A. palmeri.57 If tillage is not used prior to planting, existing vegetation in maize fields may be treated with a non-selective herbicide application, which is typically tank mixed with atrazine. In most cases, a second post-emergence application is applied that consists of a premix of a HPPD-inhibiting herbicide plus glyphosate plus atrazine.119 Another IWM option that has recently been adopted by growers in the southern US to manage glyphosate-resistant A. palmeri is post-maize-harvest weed control.120 Amaranthus palmeri often emerges as the maize dries in early July and can produce huge amounts of seed before a killing frost, thereby rendering rotation to maize to manage this weed ineffective.121 Therefore, growers have applied paraquat plus residual herbicides to reduce the seed

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Integrated pest and weed management in the US and Canada production from the late germinating A. palmeri or are mowing and tilling small A. palmeri after maize harvest.121 In summary, maize weed control in the US is heavily reliant on herbicides. There is minimal row cultivation, and adoption of other alternative tactics (e.g. cover crops) is limited at best. In recent years, more tillage has been integrated into maize production systems to supplement weed management, largely on account of HR weeds.

6.2 Weed management in soybean More than 31 million ha of soybeans were planted in the US during 2012.115 No-tillage soybean production approaches 50% or more of the area planted and is a higher percentage than all other row crops planted in the US.117 The trend to adopt no-tillage soybean production has increased during the last decade and likely is attributable, in part, to the adoption of GE soybean cultivars.122 As a result, the greatest change in weed management has occurred in soybean production, where glyphosate is used to the exclusion of other herbicides.113 Herbicides other than glyphosate were used on an extremely limited area as early as 2002, and this trend continues today. Soybean cultivars with tolerance to glyphosate are planted on more than 95% of the US soybean area, and glyphosate is used on 98% of that area (Figs 1 and 4). Given the lack of herbicide diversity, it is not surprising that the first US glyphosate-resistant weeds were identified in soybean production systems.123,124 In the late 1990s, weed control in soybeans started with a clean seed bed primarily utilizing tillage or glyphosate as a burndown application.114 This changed in 2001 with the evolution of glyphosate-resistant C. canadensis. In the southern US, growers resumed tilling or included dicamba or 2,4-D with the glyphosate to control glyphosate-resistant C. canadensis.125 Tactics changed again in 2008 when, in addition to the early burndown herbicide application, paraquat plus a residual herbicide was applied pre-emergence to control any emerged glyphosate-resistant A. palmeri in the southern US.126 In the Midwest US, growers producing soybeans without tillage continued to rely upon glyphosate applied either before planting or early after crop emergence. Cultural practices for weed management in soybeans are adopted at relatively low percentages, with the exception of crop rotation and planting narrow row spacing.35 However, the impact of a maize/soybean (Midwest US) or cotton/soybean (southern US) crop rotation on the management of glyphosate-resistant weeds is questionable given the high percentage of glyphosate-tolerant crop cultivars planted and the frequency of glyphosate applications in both crops. Cover crops have been adopted on a relatively small area, and row cultivation is practically non-existent in Midwest US soybean production. The adoption of glufosinate-tolerant soybean cultivars has been very limited, and thus the use of glufosinate in Midwest US soybean weed management is currently low. Given the prevalence of glyphosate-resistant weeds, it is anticipated that a greater area of glufosinate-tolerant soybean cultivars will be planted in the future, and more glufosinate applied in order to help manage the glyphosate-resistant weeds. The use of soil-applied residual herbicides in soybean production has increased but is impeded by time requirements, planning and economic concerns that occur with this herbicide use practice.127 Importantly, A. tuberculatus with evolved resistance to six herbicide MOAs limits herbicide choices in many soybean fields. Pest Manag Sci (2014)

www.soci.org A high percentage of fields in Iowa have A. tuberculatus populations with multiple herbicide resistance limiting the choices for effective soil-applied herbicides.25 In-season weed control tactics for soybeans in the southern US have changed as well, most notably owing to the attempt to manage glyphosate-resistant A. palmeri. The reason for this change is that the PPO herbicides used in place of glyphosate to control emerged A. palmeri in soybean, such as fomesafen and lactofen, must be applied before A. palmeri is 8 cm tall to be effective.126 Post-emergence application of herbicides in a timely manner is a problem, as A. palmeri grows as much as 5 cm in a day. Residual herbicides should be the focal point for managing glyphosate-resistant A. palmeri in soybean.121 The most consistently effective herbicide program in southern US soybean production systems is the pre-emergence application of herbicides with good activity on A. palmeri, followed by fomesafen or lactofen when A. palmeri plants are less than 7 cm tall.128 However, there is a concern that there will be strong selection pressure on A. palmeri for evolved resistance to the PPO herbicides.126 One way to reduce the selection pressure from the PPO herbicides and glyphosate is to use glufosinate in glufosinate-tolerant soybean cultivars. It was reported that 12, 4, 2 and