system appendpdf cover-forpdf - university of toronto t-space...49 imi herbicides, and diverse...

Draft

Introduction of Imidazolinone Herbicide and Clearfield®

Rice between Weedy Rice Control Efficiency and

Environmental Concerns (Residues/Resistance)

Journal: Environmental Reviews

Manuscript ID er-2017-0096

Manuscript Type: Review

Date Submitted by the Author: 22-Dec-2017

Complete List of Authors: BZOUR, MAHYOUB; University of Malaya - City Campus, Institute of

Biological Science, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia. Mohamed Zuki, Fathiah; University Malaya, Department of Chemical Engineering, Faculty of Engineering Mispan, Muhammad Shakirin; University Malaya, Institute of Biological Sciences, Faculty of Science

Keyword: Imidazolinone, Clearfield ® rice, carry over, resistance, Integrated Weed Management Systems, weedy rice.

https://mc06.manuscriptcentral.com/er-pubs

Environmental Reviews

Draft

1

Introduction of Imidazolinone Herbicide and Clearfield® Rice between Weedy Rice 1

Control Efficiency and Environmental Concerns (Residues/Resistance): A Review 2

Mahyoub Izzat Bzour1, Fathiah Mohamed Zuki2*, Muhamad Shakirin Mispan 3 3

4

5

6

1 Institute of Biological Science, Faculty of Science, University of Malaya, 50603, Kuala 7

Lumpur, Malaysia. 8

2 Department of Chemical Engineering, Faculty of Engineering, University of Malaya, 50603, 9

Kuala Lumpur, Malaysia. 10

3 Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603, 11

Kuala Lumpur, Malaysia. 12

13

14

15

16

17

18

19

*Corresponding author: 20

Dr. Fathiah Mohamed Zuki 21

Department of Chemical Engineering 22

Faculty of Engineering 23

University of Malaya 24

50603, Kuala-Lumpur, Malaysia. 25

([email protected]), 26

Tel. 603-79676879, Mobile: 0060196090504. 27

28

29

Page 1 of 70



Draft

2

Abstract: 30

Water scarcity and increasing labor costs of rice cultivation have prompted many agro-31

ecosystems in the world to adopt the Direct Seeded Rice (DSR) system instead of the hand-32

transplanting system. However, there is a downside to this approach, which is the prevalence and 33

spread of weedy rice (WR), a troublesome weed in paddy fields, because it has the potential to 34

cause a loss of 90% of the total yield in high-infested areas. The progression, infestation, and 35

dynamics of WR are linked to environmental circumstances, types of rice cultivar, established 36

techniques, and field management. WR is viewed as a critical problem, as it may prove 37

counterproductive in rice cultivation, as WR causes the overall increase in the production cost of 38

paddy harvesting. For the purpose of our discussion, there is a method that can be used to 39

eliminate, or at least mitigate the spread of WR, which is the Clearfield Production System 40

(CPS). This system consists of Imidazolinone herbicide (IMI), Clearfield® certified seeds, and 41

the Stewardship Guide. However, the use of CPS has been known to negatively affect the 42

environment, as it transfers resistance traits to WR, increasing IMI persistence in the cultivated 43

soils and contaminating soils and water with herbicide residues. These negative environmental 44

effects could be dealt by using the Integrated Weed Management Systems (IWMS) that include 45

the use of all viable tools and should be incorporated with the proper Stewardship Guide to 46

reduce the growth of herbicide-resistant WR. This review aims to elucidate information 47

pertaining to WR infestation, the characteristics thereof, sustainable techniques for WR control, 48

IMI herbicides, and diverse methods for the extraction and determination of IMI residues in the 49

environment. Understanding the conspecific nature of WR serves as a baseline for constructing 50

novel WR control strategies in the future. 51

Key words: Imidazolinone, Clearfield® rice, carry over, resistance, Integrated Weed 52

Management Systems, weedy rice. 53

Page 2 of 70



Draft

3

1. Introduction 54

Rice (Oryza sativa L.) is regarded as one of the oldest cultivated crops in the history of 55

mankind (Chauhan 2013). It has been cultivated for more than 10,000 years, and is currently the 56

second most planted crop in the world after wheat (Kraehmer et al. 2016). It is considered a 57

staple food, providing the daily caloric requirements for many people in Latin America, North 58

Africa, Asia, the Caribbean, and sub-Saharan countries (Siwar et al. 2014), by which 59

approximately half of the world’s population regards rice as their staple food (Jabran and 60

Chauhan 2015). Paddy (the crop for rice) is grown in central Africa, Japan, Indonesia, central 61

and south America, Malaysia, the Philippines, India, China, Australia, and Italy (Kaloumenos et 62

al. 2013). 63

Human environmental interference such as genetic introgression between wild plants and 64

rice cultivars has resulted in the occurrence of weedy relatives of rice crops (Burgos et al. 2008). 65

The presence of these weeds compromises rice production (Ziska et al. 2015). The adoption of 66

new practices in the rice agro-ecosystem could influence the relationship between weeds and rice 67

crops, as both are related to each other via the wild Oryza species and a gene called AA genome, 68

making cross-breeding or -contamination a distinct possibility (Sweeney and McCouch 2007). 69

Generally, the total yield from rice cultivation is relatively low due to unstable global 70

temperatures, diverse land size, irregular pest management, and shortages of water. 71

Most farmers adopted the DSR method (Singh et al. 2013), a technique that establishes 72

rice crops from seeds sown in the field rather than transplanting seedlings from a nursery (Jabran 73

and Chauhan 2015). The transplanted seedling rice system method requires additional labor, 74

time, and energy compared to the DSR method. As an illustration, labor costs in the transplanted 75

seedling approach represent approximately 79% of the total cost of rice production per hectare 76

Page 3 of 70



Draft

4

(Najim et al. 2007). It is also interesting to note the range of age of the farmers from a study 77

conducted in Malaysia in 2015, which revealed that most farmers are above the age of 40, 78

following the movement of youth towards a more urban lifestyle; this has increased the cost of 79

rice cultivation (Terano et al. 2016). As younger generations from the farming community 80

acquire higher education grades and as the economic sector is offering more attractive alternative 81

jobs at the same time, the agricultural sector is facing a chronic labor shortage (Najim et al. 82

2007). 83

It shall be noted that the application of the DSR method is increasing in Asia, where 84

farmers in Malaysia, China, the Philippines, and India report DSR usages of 71%, 9%, 40%, and 85

70%, respectively, from each of the countries rice areas (Gressel and Valverde 2009). The DSR 86

method significantly reduces the cost of rice production in diverse ways, as it is quicker and 87

simpler to implement, labor saving, and consumes less water. Furthermore, the crop seeds 88

mature ~10 days earlier and is reported to have higher yields compared to the transplanting 89

method (Farooq et al. 2011). However, the occurrence of WR has been reported in many rice-90

growing regions of the world where paddy is grown by DSR (Ferrero and Finassi 1995), and is 91

constraining rice cultivation due to the perception that it causes the increased production costs. 92

There is a debate as to the origin of WR, with some researchers positing that it is the 93

result of hybridization between types of cultivars, cultivars and wild rice, and natural selection 94

between WR and escaped domesticated rice seeds (He et al. 2017; Rathore et al. 2016). WR was 95

first detected in Selangor-Malaysia in 1988, but its infestation at that time was a minor 96

occurrence; unfortunately, this infestation spread to many fields, finally encompassing 19,900 ha 97

of rice farms (Wahab and Suhaimi 1991). The adoption of DSR cultivation methods prompted 98

WR infestation in most rice granaries and farms in Malaysia, such as in the cases in Tanjung 99

Page 4 of 70



Draft

5

Karang, Selangor and Besut, where more than 50% of the granaries were infested with WR 100

plants (Baki and Mispan 2010). An approximately 35% field infestation of WR contributed a 101

yield loss of 50–60%, or 3.20–3.84 tons/ha/season, which is equivalent to RM 2,816–102

3,379/ha/season; in the most extreme cases, yield losses of about 74 –100% have been recorded 103

(Bakar 2004). Undoubtedly, WR infestation is not limited to Asia alone (Baki et al. 2000). Sales 104

et al. (2011) reported Arkansas as the largest rice growing state, including over 45% of the total 105

USA rice acreage; about 60% of these rice fields are infested by WR plants, causing an estimated 106

loss of $275 ha in 2006. According to the reports, these losses were caused by rice plant lodging 107

and the decrease in rice grain prices, as well as the continuous consumption of fertilizers from 108

the soil. The highest WR infestations have been reported to be 80% in Cuba, 75% in Europe, 109

70% in Italy, and 60% in Costa Rica, accounting for 40% of the total area of rice cultivation in 110

these countries (Olajumoke et al. 2016). In the USA, WR has been reported in paddy fields for 111

the past 150 years (Fish et al. 2015); (Table 1) tabulates WR infestations in other countries. 112

Abraham and Jose (2015) exposed the correlation of the heavy infestation of WR in some fields 113

and the accelerated reduction in rice crop yield during recent years which has forced farmers and 114

growers to abandon rice cultivation. 115

Early control of the WR population is important, as it may cause the partial or even 116

complete failure of rice crops if it is not managed. However, it is difficult to differentiate 117

between WR plants and commercial paddy plants during the initial stages. There are some 118

general characteristics that can distinguish between these conspecific WR plants in the field, 119

such as the greater seed longevity and dormancy, as they are relatively taller than paddy plants 120

and are comprised of either white/red pericarp. They were also characterized to have weaker 121

culms and be more susceptible to lodging in the final stage of life, to have high susceptibility to 122

Page 5 of 70



Draft

6

shattering of seeds in the field, with more tiller and panicles, but giving fewer seeds compared to 123

rice plants, and they also increase the cost of rice cultivation (Abraham and Jose 2015; Marambe 124

2009). Azmi and Karim (2008) showed that the direct and indirect cost of WR control ranges 125

from 3–5% and 17–28%, respectively, of the total costs, which is equivalent to approximately, 126

USD 636–850. These characteristics of the WR plant negatively affect paddy fields, either 127

directly or indirectly. Some examples of the direct effects include its greater height, which results 128

in it overshadowing paddy plants and taking in more sunlight (Shivrain et al. 2010), where the 129

shade results in increased rates of fungi and insect infestations, which are difficult to detect due 130

to the concealed nature of the plants in the field. WR plants not only compete with rice crop 131

plants affecting yield, they also reduce harvest efficiency and contribute to the spread of pests 132

and diseases. The shading of these WR also cause paddy plants to be more susceptible to other 133

plant-related diseases, such as rice-blast disease (He et al. 2017). Abraham and Jose (2015) 134

reported that short rice crop cultivars in the field are more susceptible to WR plants compared to 135

their taller counterparts, which leads to interference in rice growth and decreased future yield. On 136

the other hand, an indirect effect of tall WR plants is the tillering capacity, where certain types of 137

WR report lower tillering, but the majority report high tillering, resulting in increased panicle 138

length, rapid vegetative growth, where leaves take longer to shed, and increased fertilizer 139

absorption, which affects the quality of future rice seeds (Van Chin et al. 2007). Additionally, 140

WR plants produce fewer grains per plant compared to cultivated rice (He et al. 2017). 141

Moreover, the shattering characteristic, because of the genes conferring WR, is regarded as one 142

of the most important traits in the field. Changbao et al. (2006) revealed that there is a gene 143

called sh4-, which is one of the major genes controlling the shattering trait; this gene is present in 144

WR plants, and actually plays an important role in grain shattering in the early stages, while the 145

Page 6 of 70



Draft

7

easy shattering trait helps with the dispersion of seeds. WR seeds could, in theory, find their way 146

into rice fields in diverse ways, whether directly or indirectly. This can take place directly via 147

contaminated harvester machines, seeds, and the use of contaminated tools, or indirectly via 148

animals, wind, and water channels. It could also spread the infestation to new areas or be hidden 149

in the seedbank store, meaning that it will repeatedly complete the cycle or remain dormant 150

(enter seed dormancy stage) (Baki and Mispan 2010), as shown in (Figure 1). 151

Seed dormancy is defined as the seed being prevented from completing germination (Li 152

and Foley 1997). Seed dormancy favors the preservation of WR seeds in soil banks for long 153

periods; therefore, the availability of seed dormancy renders the control of WR in the field 154

difficult, due to the ability of WR to remain dormant for different periods in the field (Gianinetti 155

and Vernieri 2007). The seedbank is important in the infestation process and also affects the 156

quantity of yield loss. There are diverse factors in the field that control the seedbank size in the 157

cultivated land that would also lead to the increase or decrease in its size (Chauhan et al. 2015), 158

as shown in (Figure 2). The re-emergence of WR seeds in the seedbank is greatly affected by the 159

water concentration in the soil, depth of grains, and the composition of the soil, or its texture 160

(Ferrero and Finassi 1995). WR seed dormancy in the seedbank is the most important 161

characteristic to ensure the success of the WR species in the next season or years to come, as this 162

trait stimulates the survival of seeds in the seedbank to grow and transfer WR seeds to different 163

environments via disseminating germination; eventually, the transfer and proliferation of this 164

WR seeds leads to increased infestation in other fields and yield loss. It is interesting to also note 165

that the level of WR infestation is dependent on the size of seedbank (Azmi et al. 1999). Hakim 166

et al. (2013) revealed that WR is a global menace, resulting in an annual global cultivation loss 167

of 9–10%. Notably, the percentage of yield loss differed from one country to another (Table 2). 168

Page 7 of 70



Draft

8

Recorded losses in the rice crop domain were estimated to exceed 10%, and can reach as high as 169

68–100% with DSR method (Farooq et al. 2011). Percentage losses in yield depend on the 170

infestation density of WR in rice crops and the growth rate. For example, it has been reported 171

that 1 WR plant/m2 can cause yield losses of 100–755 kg/ha in specific types of rice cultivars 172

(Ottis et al. 2005). Watanabe et al. (1996) showed that when the WR was present at an 173

infestation level of 35%, it caused a 60% yield loss, while under heavy infestation, a yield loss of 174

74% was reported by the DSR method. When the percentage of WR reached between 15 and 20 175

panicles/m2, the yield loss reached 50–60%, 21–30 panicles/m2 if the percentage was 70–80%, 176

and 100% if it was >31 panicles/m2 (Area 2010). Busconi et al. (2012) revealed that in the fields 177

studied in the USA, the decrease in yield was 5–40% due to the infestation of ~4 red rice 178

plants/m2. In Arkansas fields, the main effect of WR on rice cultivation was the reported annual 179

cost of USD 274.00/ha (Goulart et al. 2014). Ratnasekera et al. (2014) reported that WR caused 180

yield losses of ≤88% in the USA, 90% in Sri Lanka, and 100% in Thailand. Rathore et al. (2013) 181

revealed in high infestation fields (about 10 mature weedy rice/m2) in India, the crop yield 182

decreased by 30–60%. Also, weedy rice infests approximately 3 million (m) ha of fields in China 183

and has decreased the total rice yield by about 3.4 m metric tons. Recently, Azmi et al. (2012), 184

showed that more than 10% of Malaysian granaries (~20,500 ha) reported severe WR infestation, 185

which contributed to a total loss of about 50,000 tons/season (RM55 million). Busconi et al. 186

(2012) revealed yield loss due to WR infestation in up to 30% of Italian fields (in the presence of 187

10–20% WR rice plants). 188

Infestation and the rapid proliferation of the WR population across paddy fields was 189

found to be compounded by farmers’ negligence and poor agricultural practices, such as shared 190

use of machineries and tools (Sudianto et al. 2016). The individual choice in determining rice 191

Page 8 of 70



Draft

9

seed selection among farmers could lead to the failure of the approach towards WR control. Most 192

farmers are free to choose which rice seeds will be planted. At the same time, Malaysia has no 193

clear regulation of WR contamination in conventional certified rice seeds (Sudianto et al. 2013). 194

Chauhan et al. (2014) showed that the rice cultivation method using clean seeds decreased WR 195

seed production by 29–41%. Some farmers detached WR panicles but failed to remove these 196

panicles completely from the field, which increased infestation during other seasons. The careful 197

elimination of WR in the fields is not a simple task, but the successful control of WR plants is 198

crucial to ensure continuity of production of rice crops in most fields. This problem can be 199

mitigated by using common herbicides such as Paraquat; however, the excessive use of 200

herbicides could result in environmental and public health issues, as there have been numerous 201

studies and reports confirming that the prolonged use of Paraquat has led to many negative 202

consequences and this is a known public health risk (Figure 3). 203

204

2. Introduction of the IMI-herbicide family and non-transgenic resistant IMI 205

herbicide-tolerant rice (Clearfield® rice) 206

To meet the accelerated demands for agricultural production, methods have been 207

developed to increase the output of crops in the fields. Herbicides are part of the pesticides that 208

play an important role in fulfilling the high productivity percentage as they can reduce weed 209

populations to acceptable levels while not affecting the yield. The introduction of IMI-herbicides 210

has provided an efficient tool to selectively control WR in the post-emergence in fields (Scarabel 211

et al. 2012). IMI-herbicides are a class of herbicides used for the protection of a wide variety of 212

agricultural crops, but they can harm other types of crops. Members of the IMI-herbicide family 213

have similar structural properties centered round the IMI-ring and an attached aromatic system 214

Page 9 of 70



Draft

10

bearing a carboxylic acid moiety. They belong to group 2 herbicides, which are relatively new 215

broad spectrum herbicides, and can be used to control weeds and grasses in a variety of 216

agricultural areas (Krynitsky et al. 1999). IMI-herbicides were developed in the 1970s and were 217

field-tested, mostly in the USA by the American Cyanamid Company; they were also tested in 218

South America and Japan. The IMI family includes a group of herbicides consisting of imazapyr, 219

imazapic, imazethapyr, imazamethabenz, imazamox, and imazaquin (Grey et al. 2012). They 220

work as selective herbicides that inhibit the acetolactate synthase (ALS) gene, also known as 221

acetohydroxyacid synthase, or (AHAS) and branched chains of three amino acids: isoleucine, 222

leucine, and valine (Shivrain et al. 2009). Also, IMI-herbicides are used as non-selective 223

herbicides in non-crop areas, or in forestry and plantation crops, such as oil palm and rubber 224

(Ramezani et al. 2008). They are absorbed via weeds’ organs and are then diffused by the 225

phloem and xylem organs of weeds, moving to the meristematic tissue. IMI herbicides block the 226

biochemical pathway of the substrate to the catalytic site, which is essential in the branched-227

chain amino acid synthesis process. Moreover, IMI stops protein and nucleic acid (DNA) 228

synthesis, thereby slowing down the plant’s cell division rate and impeding the transport of 229

important materials to growth points. Eventually, it causes a decrease in regular plant growth and 230

kills any susceptible plants (weeds), including WR (Croughan 2003; Sudianto et al. 2013). 231

However, WR plants may exhibit a variety of responses according to the doses used and the time 232

of application. 233

IMI class herbicides are characterized by their chemical effects at minimum 234

concentrations, their significant influence on weed control, generally low mammalian toxicity, 235

and their increased persistence in soil and water (Alister and Kogan 2005). In view of this, IMI-236

herbicides were selected to control a broad spectrum of weed species in Malaysia (Sondhia et al. 237

Page 10 of 70



Draft

11

2015). This includes the IMI-herbicide family including imazapyr, which is a generic name for 238

[2-(4-isopropyl-4-methyl-5-oxo-2-imidazoline-2-yl) nicotinic acid], with the trade names 239

Arsenal and Chopper (Helling and Doherty 1995), and imazapic, the generic name of [2-240

(4,5dihydro-4-methy-4-(1-methylethyl)-5-oxo-1Himidazol-2-yl)5-methyl-3-pyridinecarboxylic 241

acid], with the trade names Cadre and Plateau (Azmi et al. 2012). These herbicides are regarded 242

as the main groups of the IMI herbicide family due to their low application rates, decreased 243

environmental hazards, high soil persistence, and selectivity for a wide range of crops such as 244

rice and wheat (Marcia 2014). Also, IMI-tolerant rice allows the use of imazethapyr (5-ethyl-2-245

(4-isopropyl-4-methyl-5-oxo-4,5-dihydro-1H-imidazol-2-yl) nicotinic acid) with the trade label 246

Newpath® in fields in the USA and Brazil for the control of WR and other severe weeds (Fish et 247

al. 2015). In the 1990s, global evolution and the presentation of non-transgenic resistant 248

herbicide-tolerant rice such as IMI-resistant rice (Clearfield® rice) (Meins et al. 2003) was 249

discovered due to the heavy infestation of WR in paddy fields, which accelerated yield losses. 250

Clearfield® rice varieties were first introduced by Louisiana State University in the USA in 2002 251

by introducing Clearfield® rice 121 and Clearfield® 141 (Sudianto et al. 2013). Likewise, 252

Clearfield® rice cultivars, developed by mutation breeding without the addition of any foreign 253

gene, were commercialized in 2002 (Croughan et al. 1996). The main reason for developing 254

Clearfield® rice was to control weedy Oryza species. Diverse IMI herbicide-resistant rice 255

cultivars containing the mutations Ala122Thr, Gly654Glu, and Ser653Asn in the ALS gene have 256

recently been commercialized (Roso et al. 2010). 257

The adoption of Clearfield® rice is increasing annually; for example, in 2004, ~19% of 258

long grain rice acres of the total cultivation land in Arkansas, 27% in Louisiana, 15% in Texas, 259

13% in Missouri, and 23% in Mississippi were cultivated using Clearfield® rice (Shivrain et al. 260

Page 11 of 70



Draft

12

2006). This method was also adopted by other countries, such as Malaysia, due to the need to 261

control the heavy infestation of WR. Azmi et al. (2012) reported that the Clearfield Production 262

System (CPS) technology was launched on the 8th July in 2010 at the Malaysian Agricultural 263

Research and Development Institute (MARDI), whereby the Malaysian government released two 264

corps cultivars: MR220CL1 and MR220CL2. Both varieties were obtained from crosses between 265

CL1770 from Louisiana State University (LSU) and a Malaysian local rice variety MR220 266

(Azmi et al. 2012). Sudianto et al. (2013) revealed using DNA analysis techniques that the 267

genetic similarity between the two cultivars (MR 220CL1 and MR 220CL2) used in Malaysia 268

reached 98.5%. The CPS technique package was used to overcome the problems caused by WR 269

(Bakar et al. 2016). This is composed of three major components: Clearfield® rice, IMI, and 270

Stewardship quid (Azmi et al. 2012). IMI class herbicides are characterized by their chemical 271

effects at minimum concentrations, a wide range of effects on weed control, and increased 272

persistence in soil and water (Alister and Kogan 2005). The global status of the CPS system has 273

been used in specific countries which used IMI-herbicides and different types of Clearfield® 274

cultivars, based on specific conditions; for example, the CPS system supported by the Malaysian 275

government was commercialized using imazapic and imazapyr herbicides, as well as MR220-276

CL1/MR220-CL2 cultivars. Due to the lack of crop rotation and the practice of a monoculture 277

system (Azmi et al. 2012), Italy officially marketed the herbicide imazamox and the cultivar 278

CL161 in 2006, which was cultivated on about 52,000 ha from an area of about 235,000 ha 279

(equivalent to more than one-fifth of the total rice area) (Scarabel et al. 2012). The USA used 280

cultivars CL152 and CL162, along with imazethapyr herbicide, which was developed for use in 281

USA paddy fields and other crops due to its efficacy against WR (red rice) (Solomon et al. 282

2012). In addition, this technology has been used in approximately one million ha in the USA 283

Page 12 of 70



Draft

13

and Brazil (Gealy et al. 2003). The introduction of Clearfield® rice provided the selective control 284

of WR in fields, which, together with integrated management practices, increased the rice yield 285

in Brazil by approximately 2500 kg ha, which was an increase of 50% (Merotto et al. 2006). 286

Clearfield® rice technology is also used in Arkansas, USA, to mitigate significant red rice 287

infestation (Burgos et al. 2008). Cassol et al. (2015) reported that Clearfield® technology was 288

used in Rio Grande do Sul in 2012, resulting in more than 50% of rice acreage being planted. 289

Also, in Brazil, this IMI herbicide resistant-cultivar was used on an area equivalent to 290

approximately 1.1 million ha due its effectiveness in controlling the population of red rice (Singh 291

et al. 2017b), a known plant pest in many countries, which causes increased yield loss and 292

decreased crop quality (Dauer et al. 2017). The CPS system is also used in paddy fields in 293

Colombia, Brazil, Nicaragua, and Costa Rica. For example, about 22% of the rice cultivated area 294

in Costa Rica was planted using Clearfield® rice, while types CL121, CL141 and CL161 were 295

applied in Louisiana (USA) (Sudianto et al. 2013). 296

Therefore, there are four main reasons for developing Clearfield® rice and IMI 297

herbicides: 1) to eliminate WR plants in paddy fields; 2) to increase the yield of rice cultivation 298

systems via optimum WR controls; 3) to reduce the amount of land required to satisfy the global 299

rice demands; and 4) to decrease the usage of fossil fuel in agricultural production (Mannion 300

1995). The following are the review questions: 1) what is the efficacy of IMI herbicides on WR 301

control, 2) does the IMI herbicide leave residues and persist in the soil with crop rotation, 3) does 302

the application of IMI herbicides result in a resistant form of WR in the field, and 4) is there any 303

comprehensive management strategy that can control the spread of WR? These questions will be 304

discussed in the review paper presenting the success and risk aspects related to the introduction 305

of the CPS system in the diverse rice-producing areas of the world. 306

Page 13 of 70



Draft

14

3. The successful story of IMI herbicides and Clearfield rice application 307

Clearly, using herbicide-resistant rice varieties has been proven to be one of the most 308

effective methods by which to eliminate WR from fields (Song et al. 2017). The CPS system 309

provides an efficient tool to selectively control WR in the post-emergence stage (Novakova 310

1994). Before Clearfield® rice was developed there were no marketed herbicides that would 311

selectively control this weed without injuring the rice crop. CPS technology is more readily 312

attainable than transgenic herbicide-tolerant crops; for instance, there was a quick expansion of 313

CPS to develop IMI-tolerant diverse crops. It was also noted that farmers have been using CPS 314

systems since 2001; however, in contrast, glyphosate-tolerant rice and wheat have still not been 315

commercialized, even though they have also been developed (Gealy et al. 2003). Azmi et al. 316

(2012) reported a wide scale evaluation of the CPS system for cultivation areas (47.62 ha) in the 317

off-season year 2010; it was found that yield production increased from 4.93ton ha to 5.69ton ha, 318

where the returns ranging from 5–8 times, translating to a difference of USD1000 toUSD1600. 319

The introduction of Clearfield® rice in 2002 in the US made the selective control of red rice 320

possible via the use of IMI herbicides. Reports showed that imazethapyr herbicide could reduce 321

the population of WR (red rice) plants in US fields by more than 90% (Singh et al. 2017a). Also, 322

Pellerin et al. (2003) reported that imazethapyr reduced the population of WR by 98% in US rice 323

fields. CPS technology is used in Arkansas to eliminate red rice. It was reported that the level of 324

control reached 90% when CPS was used (Burgos et al. 2008). The effectiveness of IMI 325

herbicides in eliminating weeds was studied in the USA, by a study reporting that imazapic is 326

effective in eliminating certain weeds, such as peanut (Arachis hypogaea L.) (Ducar et al. 2004). 327

Also, a study of imazapic showed that it is capable of eliminating many types of weeds, such as 328

jointed goat grass and downy brome. Rainbolt et al. (2004) reported that the herbicide imazamox 329

Page 14 of 70



Draft

15

can eliminate the presence of red rice by up to 99%. In the USA, where the efficacy of the CPS 330

system on diverse types of weeds that infest crops has been proven; for example, many weeds 331

that infest rice, including barnyard grass (Echinochloa crus-galli), and severe types of weeds in 332

wheat, such as cheat (Bromus secalinus L.) can be controlled. In addition to the aforementioned 333

weeds, the list also involves Italian ryegrass (Lolium multiflorum Lam), shatter cane (Sorghum 334

bicolor), and Johnson grass (Sorghum alepense) (Tan et al. 2005). 335

IMI herbicides are prevalent in CPS technology on their own, as imazethapyr in Arkansas 336

(USA) and imazamox in Italy, or as mixtures, for example, imazapyr and imazapic were used in 337

Clearfield® rice cultivars in Malaysia. Furthermore, imazapyr and imazapic were used on IMI-338

resistant wheat in Australia (Tan et al. 2005). Studies also showed that the cooperation and 339

mixing of two or more compounds results in a combined effect that exceeds their respective 340

constituents (Bakar 2006b). The synergistic nature of the IMI herbicide family, as per (Table 3), 341

was developed via various experiments to increase the efficiency of IMI herbicides in controlling 342

WR and reducing the risk of injuries (carryover) (Blouin et al. 2010). However, we should pay 343

attention to the fact that mixing can lead to complications in certain cases; an example of this is 344

that the mixtures of imazapyr and imazapic can result in increased carryover compared to 345

imazapyr with imazethapyr (Grymes et al. 1995). Many countries still use and develop cultivars 346

from CPS technology due to the subsequent high yields, such as in Italy, USA, and Vietnam 347

(Sudianto et al. 2013). In specific fields where WR is the most problematic weed, Clearfield® 348

rice is considered an effective WR management option. However, the failure to prevent the 349

development of IMI-herbicide resistance to WR could leave the growers in more dangerous 350

circumstances than prior to the introduction of the CPS system. Any responsible local 351

government should consider continuous evaluation and follow-up of this system to take into 352

Page 15 of 70



Draft

16

consideration the related usage. Therefore, extensive research should be conducted on this 353

technology in the future. This is related to first review question, which questions the efficacy of 354

IMI herbicide on WR control. 355

4. Environmental Concerns 356

In general, pesticides play an important role in the size of crop yields; herbicides work 357

by eliminating different types of weeds in the field. However, the usage is prolonged in field 358

soils because the chemical properties of the herbicide as an absorption mechanism may affect the 359

environment. CPS technology could be harmful to humans, domestic animals, and other crops if 360

not used properly, as per the recommendations of the manufacturer (Ibrahim et al. 2017). There 361

are several environmental concerns regarding the misuse of this technology from countless 362

farmers in the field; for instance, by not committing to Steward quid lines prescribed for this 363

technology, which is regarded as one of the three significant sectors of CPS technology. There 364

are no specific herbicides that will selectively control WR in paddy fields but not injure 365

cultivated rice (Gealy and Black 1999). Despite the immense success of CPS, it was unable to 366

achieve the complete elimination of WR in paddy fields (100%), due to several factors; these 367

include the different emergence of WR due to genetic variation, receiving a sub-lethal dose of 368

IMI herbicides, and the environmental circumstances during IMI application, such as wind 369

direction during application, water availability in the soil, timing, and temperature. These factors 370

will be discussed in the following subsections. 371

a) IMI-herbicide-resistant WR 372

The development of new herbicide-resistant weeds and mitigating gene flow from crops 373

to weeds are important; however, the introduction of a new herbicide-resistant crop to the field 374

must be comprehensively studied. Genetically, WR plants are closely related to commercial rice 375

Page 16 of 70



Draft

17

and are very similar to paddy plants (physiological and morphological similarities) (Baki and 376

Mispan 2010). The repeated use of the same herbicide and modes of action in the same field, 377

especially in monocrop systems, could impose what is known as selection pressure on WR; this 378

could occur due to the possibility of gene flow from Clearfield® rice to WR. Subsequently, this 379

newly formed WR gains the IMI-herbicide-tolerance characteristics from the cultivated rice. In 380

addition, a spontaneous mutation could also occur due to the significant usage of IMI-herbicides 381

(Sudianto et al. 2013). The gene flow from cultivated rice crops is fast becoming a major 382

problem. Escaped WR plants could be exchanged and hybridized with the alleles of cultivated 383

rice during the flowering process (Dauer et al. 2017). This forms herbicide-resistant WR, which 384

increases the cost of rice production and decreased cultivation field and yield. Herbicide-resistant 385

weeds are not something new, and have been around for quite some time. Previously, when 386

traditional herbicides were resorted to, the usage of glyphosate leads to the glyphosate-resistance 387

of weed (Norsworthy et al. 2013), (Table 4). Highly resistant weeds cause high yield losses and 388

create a complicated weed dynamic in the fields. The use of new CPS technology creates a 389

strong bias towards the introgression of resistance alleles of one plant population into the gene 390

pool of another (Li et al. 2017; Singh et al. 2017a). The most significant effect of IMI herbicides 391

is prompting modifications to certain crop structures and developments. Notably, these 392

modifications are not immediate, and could have carryover effects, which are usually overlooked 393

by farmers (Qi et al. 2017). WR resistant mechanism could be induced by increasing the 394

selection of previously existing alleles in specific genes, known as spontaneous mutation, and the 395

complicated outcrossing of WR plants with Clearfield® rice (Busconi et al. 2012). Wang et al. 396

(2006) revealed that introgression is possible due to both WR plants and Clearfield® rice being 397

related to diploids (2n = 24) in the ‘AA’ genome. Similarly, the herbicide resistance character in 398

Page 17 of 70



Draft

18

Clearfield® rice is governed by a single dominant gene (Kaloumenos et al. 2013). It should also 399

be pointed out that the result of the outcrossing gene is rather diverse, variable, and mostly less 400

than 1%. However, within sequential generations between WR plants, these introgression alleles 401

could lead to the increased development of a more aggressive WR population (Burgos et al. 402

2014). These developments result in changing the genetic structure and population dynamic for 403

WR; the example of this is the emergence of new biotypes of WR, which botanically appear 404

similar to cultivated rice plants in the field (i.e. MR220 and MR219), especially in height, 405

making WR plants almost undetectable and harder to differentiate from paddy stalks (Mispan 406

and Baki 2008). 407

The presence of genetic variation in the WR population leads to genes moving from 408

cultivated rice to the WR population, leading to the development of increased resistance. The 409

interaction exchange increases as the distance decreases, and the increasing CO2 could enhance 410

the competition from wild WR in rice production; therefore, consumable rice production reduces, 411

and the gene flow in the fields becomes easier (Ziska et al. 2012). The distance for fertilization 412

and movement of pollen in the air is crucial with regard to hybridization (Ziska et al. 2012). Jia 413

(2002) showed other factors that influence fertilization, including wind speed and direction 414

affecting pollen movement, the quantities of pollens being produced, environmental conditions 415

such as temperature and humidity, and the rice cultivar variety. For example, Indica rice 416

produces more pollen than Japonica rice. Muker and Sharma (1991) reported the ability of rice 417

pollen to cross approximately 31meters (m). However, (Khush 1993) pointed out that an 418

isolation with a suitable distance of ~10 m is safe, and could prevent the transfer of pollens from 419

the cultivation rice and WR. The sexual compatibility between cultivated rice and WR plants 420

was found to be perfect for gene ingression, as shown in (Table 5) (Engku et al. 2016). 421

Page 18 of 70



Draft

19

Therefore, the presence of herbicide-resistant weeds in agro-ecosystems increases the interest in 422

the environmental risk of herbicides in the future (Qi et al. 2017). In most countries, scientists 423

and farmers are concerned about the resistance trait being passed on from Clearfield® rice to WR 424

(Shivrain et al. 2009). Zhang et al. (2006) reported that 0.17% of outcrossing was detected 425

between Clearfield® rice cultivars (cultivar121, cultivar 141, cultivar161, and cultivar 8) and 426

WR, which was proven by phenotypic and DNA marker analyses. Costa Rica is still reluctant to 427

adopt Clearfield® rice, reporting an adoption rate of ~20–30%. However, there are many 428

solutions to overcoming gene flow between rice and WR plants. Some of these solutions were 429

accepted, such as the suggestion to choose special conventional rice cultivars, called 430

cleistomgamous, due to the pollination process taking place prior to flowering, rendering the rice 431

plants able to self-pollinate. Other mitigation techniques used genes conferring traits such as 432

non-shattering, dwarfism, and the lack of secondary dormancy as mitigation (Gressel and 433

Valverde 2009). 434

On top of the previously mentioned concerns, certain studies reported that IMI herbicides 435

were sometimes unsuccessful or could only minimally control WR, such as broadleaf (Bailey 436

and Wilcut 2003). Cassol et al. (2015) reported that more than 56% of red rice plants in Brazil 437

were resistant to imazethapyr and imazapic. Also, Merotto et al. (2006) reported that this 438

emerged because of the IMI-herbicide resistance in WR and the escalation of production costs. 439

Many rice growers and farmers in Brazil had to leave the business, selling off or renting their 440

lands out, which led to the escalation of the average farm size. In these WR populations, the 441

mechanism of resistance was modified target site; approximately 80% of these WR plants had 442

the same mutation as the IMI-tolerant cultivar, which was the most widely used in the fields 443

(Roso et al. 2010). The resistance mechanism could be the activated metabolic reaction of 444

Page 19 of 70



Draft

20

mixed-function oxidases which remove toxins from this type of herbicide. For example, 445

sulfonylurea resistance in lettuce is due to the modified site of action of acetolactate synthase 446

(Carol et al. 1990). In certain regions, Clearfield® rice seeds were removed from the fields in 447

2004, and replaced with other cultivars such as CFX-18/CL 16 in Costa Rica (Sudianto et al. 448

2013). Therefore, Clearfield® rice cultivars could be a short-term solution, due to the selection of 449

herbicide-resistant WR. It could be deduced from interviews conducted in Malaysia and from the 450

observations in paddy fields in Malaysia that some local farmers do not have confidence in CPS 451

(Terano et al. 2016); CPS technology is limited to the appearance of IMI-resistant WR post-452

second application, which could be explained by the fact that WR eschewed the application of 453

IMI due to erroneous farming practices, or from a spontaneous mutation in the WR population or 454

gene flow from cultivated rice cultivars to WR. Nonetheless, the IMI herbicide family is 455

currently being used globally. The questions which need be discussed are as follows: 1) has IMI 456

solved the WR problem, 2) has it detrimentally affected another plant species, and 3) does it 457

leave residues or persist in the soil for a long period of time? 458

b) IMI-herbicide residues in soil, water, and animals 459

The World Health Organization (WHO) has defined residues as “any substance or 460

mixture of substances in food for man or animals resulting from the use of a pesticide and 461

includes any specified derivatives, such as degradation and conversion products, metabolites, 462

reaction products, and impurities that are considered to be of toxicological significance”. 463

Herbicides play an important and much needed role in food production worldwide, which 464

improves the production of high crop yields at a low cost. It is evaluated that without the use of 465

pesticides, approximately half of the world’s agricultural production could be lost (Ramezani et 466

al. 2009). Therefore, herbicides in particular are considered an important tool to produce high 467

Page 20 of 70



Draft

21

crops in agro-ecosystems; these are recognized as the most successful weed control tool ever 468

developed. The environmental fate of herbicides after their application is a major concern for 469

producers responsible for maintaining good-quality water. Concern should also be given to the 470

interaction and destination of these dangerous chemical particles, which may be adsorbed in 471

different forms, such as minerals and organic compounds, and to their reaction with other 472

compounds, forming complexes. Refatti et al. (2017) reported that the extensive use of 473

herbicides close to water sources is considered a risk of contamination to the environment. There 474

is no doubt that the fate of herbicides in the crop fields causes pollution both on the surface and 475

in groundwater, as it is also harmful to human health by affecting the food chain; studies 476

revealed that less than 1% of herbicide components can reach the target in plants, and the rest of 477

the herbicide penetrates and moves through soil pores in surface and groundwater (Gavrilescu 478

2005). 479

The continuous use of herbicides for a long period of time in agriculture systems has 480

generated diverse consequences to the environment. Currently, the intensive use of herbicides in 481

crop cultivation is due to the issue of weed infestation, thus accelerating the problem of 482

pollution. Changing the method or technique in cultivation may solve the problem, but may lead 483

to another setback. As an illustration, the formulation of a new method for rice crop planting, 484

such as the DSR method, can save labor efforts and costs, but may lead to higher levels of 485

herbicide applications for weed control management (Ismail et al. 2011). The IMI-herbicide 486

family represents a new type of herbicide that can be widely used in agriculture due to its low 487

rate of application, reduced environmental concern, and low toxicity (Ramezani et al. 2009). 488

However, IMI-herbicide use may limit the success of non-tolerant crops due to the long residual 489

Page 21 of 70



Draft

22

activity in the soil; this can cause an agronomic problem and complicated environmental 490

problems (Ulbrich et al. 2005). 491

The movement and persistence of IMI-herbicides in cultivation regions is very important 492

to modify the agronomic quality of IMI-herbicides in the future and to lessen concerns about 493

environmental pollution. Leaching (the vertical movement of herbicide components along the 494

soil matrix) and degradation are both key factors determining the mobility of herbicides 495

downstream. The persistence and leaching of the of IMI herbicides in the soil are due to many 496

factors such as photodegradation, chemical degradation, microbial activity, and the hydrolysis 497

process (Refatti et al. 2017). The two mechanisms (microbial and chemical) are correlated with 498

water availability and high temperature (Süzer and Büyük 2010).The photodegradation process 499

has been considered one of the main processes, especially in tropical and subtropical areas, due 500

to the hot temperatures and high solar radiation all day long (Ramezani et al. 2009). The nature 501

of the chemical compounds for IMI-herbicides and the environmental conditions play a critical 502

role in the fate of the herbicide in the environment. As an example, the availability of both acid 503

and basic IMI-herbicides led these types of herbicides to present in triple states: cationic, anionic, 504

and neutral (Marcia 2014). Quivet et al. (2006) reported that complex interactions in the soil 505

matrix between IMI-herbicides such as imazapyr and metal ions such as Na+, Ca2+ and Cu2+ 506

decreased the photolysis and degradation of imazapyr, and therefore increased the persistence 507

time in the soil. These previous states are controlled by the pH of the matrix, as soil and water, as 508

IMI-herbicides are anionic at higher pH values. Higher pH values lead to the increased 509

dissipation and degradation of some IMI-herbicides in the matrix, such as imazethapyr and 510

imazaquin (Aichele and Penner 2005). In the field, IMI-herbicide (imazapyr) half-lives were 511

estimated to be more than 325 days for dissipation in the upper layer of the soil compared to the 512

Page 22 of 70



Draft

23

lower layer (El. Azzouzi et al. 1998). Therefore, these previous triple states allow researchers to 513

extract IMI-herbicides from the soil and water and separate them from other interfering 514

compounds in the matrix with high efficiency. The spread and movement of small particles of 515

herbicides due to heavy rainfall in tropical and semitropical areas increases the chance of water 516

pollution. The general effect of contamination with most herbicides on the aquatic eco-system 517

has been studied and reported (Ismail et al. 2011). 518

Studies have revealed that the lifetime (the time needed to degrade about 50% of the 519

substance) in the soil for IMI varies; for example, imazapic remained in the soil for 90 days 520

(Grymes et al. 1995; Ulbrich et al. 2005), while for imazethapyr this was ~60-360 days, and for 521

imazapyr this was ~141 days (Alister and Kogan 2005). The persistence of imazethapyr residues 522

in the soil remains for between four and 20 weeks in clay and sandy soil, respectively (Hollaway 523

et al. 2006). Herbicides sometimes persist for a period of time in the soil to kill weeds in the 524

crop; this is called the critical period of weed competition, but should not persist for a long time 525

because it causes injury to crops and subsequent rotational crops (Santos et al. 2014). The 526

depletion of IMI-herbicides in the field is quicker than any external study, because the water 527

content (soil moisture), photodegradation, biodegradation, and temperature fluctuation in the 528

field affected the draining process and the persistence of chemical substances. Experiments and 529

reports on the availability of IMI-herbicides in sandy soils revealed that approximately 50% of 530

herbicides were broken and drained following two days of extensive ultraviolet light (UV) 531

(Aichele and Penner 2005). Consequently, it was observed that continuous monitoring is a 532

suitable technique for determining residues in both water and soil (Table 6), as the appreciation 533

for the main factors related to IMI-herbicides in the soil are of high importance to comprehend 534

Page 23 of 70



Draft

24

the behavior of herbicides and ascertain suitable dosages to avoid unwanted consequences on the 535

ecosystem. 536

Generally, IMI-herbicides are weakly adsorbed by the soil’s components, which eases 537

their movement through plants, causing serious contamination (Sondhia et al. 2015). This 538

movement is affected by the soils’ impurities, organic matter, clay percentages, and pH. For 539

example, when the pH decreases, IMI-herbicide binding to soil particles increases (Goetz et al. 540

1986). The persistence of IMI-herbicides in clay soils is greater than in other types of soil; 541

however, this also depends on the concentration of organic carbon in the soil samples (Hollaway 542

et al. 2006). Recently, a study clarified that IMI-herbicides can persist and leach to different 543

depths in the soil (Bzour et al. 2017). As pointed out previously, this translocation and movement 544

via deep soil layers are connected via several factors. As an example, one of these factors is the 545

soil composition (the soil texture), which is a physical item determined by the percentage of 546

sand, silt, and clay in the soil body. Sondhia et al. (2015) reported that IMI-herbicides persisted 547

for a longer period in Romanian soil and demonstrated residual effects on the next crop rotation 548

after two to three years. (Table 7) summarizes the studies exploring the different depths which 549

IMI-herbicides could leach into; here, it is revealed that the translocation and leaching of IMI-550

herbicide components between soil particles and the continuation of IMI-herbicides at diverse 551

depths in the soil may increase their persistence, possibly due to the lower temperature at greater 552

depths, less solar radiation, and the decreased activity of microorganisms in the soil (Refatti et al. 553

2017). Battaglin et al. (2000) showed that approximately 2.5% of the applied pesticide was 554

wasted in runoff during rainfall from one to two days after the application of herbicides. 555

Therefore, low soil pH, clay soil, highly organic matter, and low rainfall are the climatic 556

conditions and soil types that raise the persistence of IMI-herbicides. Extensive future research 557

Page 24 of 70



Draft

25

should be conducted in this domain to determine these factors and to understand the maximum 558

depth that IMI herbicides can penetrate and the correlated environmental risks. 559

There are a number of methods that were proposed to determine the extraction of IMI 560

from the soil. To understand this, the water solubility of IMI is generally relatively high (Sondhia 561

et al., 2015), but the PKa for each is relatively low. This solubility of IMI-herbicides in water 562

helps to determine the leaching potential at different depths, where the pKa values of the IMI-563

herbicides are 1.3–3.9 (Martins et al. 2014). However, its persistence in the soil is linked to the 564

pH value of the soil (Marcia 2014; Neto et al. 2017). Furthermore, the presence of these 565

herbicides in the form of ions influences the extraction approach in both soil and water 566

(Ramezani et al. 2009). Santos et al. (2014) pointed out that IMI-herbicides (imazethapyr, 567

imazapic, and imazapyr) are used in USA fields and when applied post-emergence they were 568

reported to cause high residual activities in the soil with different effects, depending on internal 569

characters such as pKa values and lifetime of the soil. IMI-herbicides present a high risk of 570

contamination for soil and water sources because of their high solubility. Moreover, due to the 571

special physicochemical traits of IMI-herbicides, they exhibit long residual activity (retained in 572

the soil matrix), which is highlighted as the most important feature; also, IMI-herbicides could 573

lead to phytotoxic damage of rotational crops in succession to rice plants in the future. Curran 574

(2001) reported that volatilization is compatible with temperature and the presence of water in 575

the soil, as it increases with these two factors; however, IMI-herbicides are relatively nonvolatile 576

under field conditions, which increases the adsorption and persistence for a longer time in the 577

soil. IMI-herbicides have relative half-lives of 1–5 months; this persistence could affect the next 578

round of crops, which could reduce their quality of production. Due to numerous complaints 579

about the carryover effects, many researchers have recommended the use of IMI for two 580

Page 25 of 70



Draft

26

consecutive years only, leaving the soil undisturbed for at least a year (Santos et al. 2014). It 581

should also be pointed out that IMI-herbicides do not leach easily because their translocation and 582

movement is influenced by diverse factors, as previously mentioned. Similarly, Neto et al. 583

(2017) also reported the transformation and leaching of IMI-herbicides to be influenced by 584

multiple factors, such as chemical compounds and the amount of rainfall in the area. Organic 585

matter and pH concentration are both negatively correlated with the adsorption of IMI. Studies 586

revealed that clay soil samples, which have high concentrations of organic matter, have a 587

tendency to hold high moisture quantities; therefore, the microorganisms present, such as 588

microbial flora and fauna, flourish, becoming more active in the degradation of IMI-herbicides, 589

especially when temperatures are high, as found in tropical and sub-tropical regions (Süzer and 590

Büyük 2010). Sondhia (2013) reported that IMI-herbicides could leach to greater depths in 591

tropical countries with higher rainfall. 592

The management practices and methods used by farmers in the fields are considered 593

contributory factors to the presence of these herbicides. For instance, when farmers neglect the 594

proper way to cultivate fields accordingly, such as ploughing not being done as often, resulting 595

in the decreased uptake of sunlight, this may lead to the accumulation of IMI-herbicide residues 596

throughout the seasons (Bzour et al. 2017). Plausibly, only a certain number of countries have 597

started to adopt procedures related to IMI-herbicides, while countries such as Norway and France 598

are prohibiting the use of IMI-herbicides due to their high persistence in soil (Shaifuddin et al. 599

2014). In Sweden, it was reported that IMI-herbicides were found 8 years after their application, 600

and that IMI-herbicides display high activity against diverse annual weeds when applied either 601

pre- or post-emergence. Sweden resorted to using IMI-herbicides for the long-term removal of a 602

wide spectrum of broad-leaved weeds along railway lines in the country, with different 603

Page 26 of 70



Draft

27

concentrations used because the plants demonstrate a relatively wide range of sensitivity; as the 604

accumulation takes a long time, this allows the herbicide to leach through soil pores and 605

subsequently transport into both of natural surface and ground water alongside railway tracks 606

(Börjesson et al. 2004b). Battaglin et al. (2000) revealed that there are 16 herbicide components 607

related to IMI-herbicides that were found in water samples collected from both surface and 608

ground water in USA areas. On the other hand, rice fields in Brazil are considered a focus of 609

water pollution, with the extensive use of IMI-herbicides detected in surface waters, rivers, lakes 610

and groundwater. Herbicides such as Clomazone, for example, are the most frequently found 611

herbicides in rice fields in studies in Arkansas and Australia (Silva et al. 2009). 612

Recently, Refatti et al. (2017) reported that the IMI-herbicides used in the Clearfeld® rice system 613

could leach up to 25 cm or more. Similarly, IMI-herbicides were found to exceed the method 614

reporting limit (MRL) of 0.01 µg/l in 83% of total water samples in US (Battaglin et al. 2000). 615

Also, IMI-herbicides have been found to leach into groundwater in Canada streams and the 616

pollution of groundwater with noticeable concentrations of herbicides would be unlikely (Cessna 617

et al. 2012). However, IMI-herbicides persist for longer in the surface soil due to the adsorption 618

mechanism potentially affecting the quality and yield of the next round of crops, and negatively 619

affecting the environment. Studies and experiments revealed that low levels of imazapic 620

herbicide are efficient to decrease the fresh weight of rice crops, sorghum, and maize (Shaw and 621

Wixson 1991). Also, a study has been done on IMI-herbicides to evaluate the effect and 622

carryover in the soil and factors causing injuries to the next planting in the fields; the results 623

show that IMI-herbicide residues in the soil have some negative effects, because IMI can persist 624

in the soil for a long time, reaching several months (Alister and Kogan 2005). IMI herbicides 625

remain in the soil for quite some time, depending on the application rate (D'Ascenzo et al. 1998). 626

Page 27 of 70



Draft

28

Therefore, a safe re-planting period is suggested between IMI-herbicide application and the 627

planting of non-tolerant crops. Marchesan et al. (2010) showed that plants demonstrate a wide 628

range of sensitivity to IMI-herbicides and plant injury was still present about 705 days after 629

application (imazethapyr), but without a decrease in grain yield. IMI-herbicide residues in the 630

cultivation soil have affected and damaged the following crops in Canada about one year after 631

the application of IMI-herbicides (Sullivan, 1998). Süzer and Büyük (2010) showed that IMI-632

herbicide residues also affect the second rotation crop, and seed yield decreased significantly, by 633

35.7%. The pH-value for IMI-herbicides and the type of soil play significant roles in the 634

carryover process for the next generation of plants. Loux and Reese (1993) reported that the 635

carryover of IMI-herbicides (imazaquin) in Hoytville clay soil led to corn plant injury in the 636

second year; yield reduction was increased as pH decreased in the soil because the persistence of 637

imazaquin increases as soil pH decreases to 4.5. Also, James et al. (1996) showed that IMI-638

herbicide residues in the soil can damage the next rotational crop, such as sugar beet, canola, 639

cauliflower [Brassica oleracea (Botrytis group)], broccoli [Brassica oleracea (Botrytis group)], 640

lettuce (Lactuca sativa L.), and potato. These inequalities in the size and shape of potato revealed 641

that IMI-herbicides significantly decreased potato yields and reduced marketable yields (Figure 642

4). A study was conducted in Texas (in the cities of Denver and Munday) to evaluate the effect 643

of the activity of IMI-herbicides in the soil of cotton plant fields. The results showed that cotton 644

plants were stunted, and the yield was decreased comparing to that of the untreated control plants 645

(Grichar et al. 2011). Due to the small application rates, the properties of these herbicides and the 646

presence of other interfering chemicals from soil samples render the analysis of IMI at low 647

detection limits complex. Therefore, current methods for analyzing these herbicides in soils are 648

regarded as slow, expensive, and complex, requiring numerous steps (Martins et al. 2014). Most 649

Page 28 of 70



Draft

29

extraction methods rely on the pH concentration and the nature of the extracted chemical 650

compounds; some of the common techniques used in this context are HPLC-UV and 651

LC/MS/MS. Recently, the solid phase extraction (SPE) was widely used to clean up the final 652

process; this is a very simple and inexpensive tool, but its silica compound is susceptible to 653

acids. Therefore, on this note, this paragraph encompasses the answers to the second and third 654

review questions, of whether the IMI-herbicides leave residues and persist in the soil, influencing 655

rotational crops, and whether the application of IMI-herbicides results in a resistant form of WR 656

in the field. 657

A recent survey revealed that the adoption of CPS is quite abysmal, due to its strict 658

system and related quid lines (Terano et al. 2016). In addition, IMI herbicide has toxic effects to 659

human, animals and its residual activity in soil remains for up to 18 weeks after application in the 660

field (Ibrahim et al. 2017). As pointed out previously, the IMI family of herbicides affects the 661

ALS enzyme in plants, which is absent in animals such as fishes (Gagne et al. 1991). Also, IMI-662

herbicides are not manufactured for aquatic ecosystem use; however, they can be moved into 663

aquatic systems by leaching and surface water runoff. IMI-herbicides move from their applied 664

sites by many means, including volatilization, hydrolysis, photolysis, and biodegradation, 665

because of the high-water solubility and low vapor pressure. However, a study reported that 666

certain species of Cyprinus carpio, which is a fish found in lakes and rivers in Europe and Asia, 667

showed changes to metabolic rate and oxidative states (Moraes et al. 2011), encompassing 668

changes in the liver, muscle, and brain activities. The study also showed that the decrease of 669

hepatic glycogen, showing a stress response, is attributed to herbicide motivated hypoxic 670

circumstances (Begum 2004). Similarly, the increased ammonia rate and decreased protein 671

Page 29 of 70



Draft

30

concentration in the muscle of Cyprinus carpio could be due to increased protein metabolism 672

(Moraes et al. 2011). 673

The effect of these herbicides has been extensively studied in many countries but, until 674

now, there are no reference scales to identify an optimal value, especially for soil residues, as 675

these residues are affected by many other factors. According to the WHO, no databases or 676

adequate information are available on the health effects or risk of poisoning during 677

manufacturing and for workers exposed to IMI-herbicides in the field. Kanungo and Buffinton 678

(2013) reported a two-year study of toxicity in mice; the results revealed that the toxicity started 679

at about 10,000ppm per day. Therefore, there is no need to establish an acute reference dose for 680

IMI-herbicides in view of the low acute toxicity and the absence of developmental toxicity. The 681

meeting committee concluded that IMI-herbicides are unlikely to pose a carcinogenic risk to 682

humans. Also, Low et al. (2013) reported that the estimated acceptable daily intake and levels 683

relevant for risk assessments of IMI-herbicides for rats, rabbits and dogs is 0–0.7 mg/kg; to cause 684

toxicity in rats, about 20,000 ppm daily is required, while the oral LD 50 of IMI-herbicides 685

(imazapic) is >5,000 mg/kg. The starting effects were observed in the acute neurotoxicity 686

experiment, and occurred above 500 mg/kg. Therefore, until now, the IMI-herbicide residues 687

have not been shown to contribute any health hazard to human beings. Furthermore, although 688

IMI-herbicides are not considered carcinogenic to humans, they can cause eye and skin irritation 689

from misuse. According to The Environmental Protection Agency (EPA) classification, it is a 690

“Group E” compound, with no evidence of mutagenic potential related to humans; this is based 691

on the experiments that have been carried out on animals (American Cyanamid 2000). 692

Nevertheless, Koutros et al. (2015) recently reported that there is an increased risk and an 693

association of bladder cancer with the use of two IMI-herbicides (imazethapyr and imazaquin) in 694

Page 30 of 70



Draft

31

the field. However, the EPA currently characterizes IMI-herbicides (including imazethapyr) as 695

unlikely carcinogens based on two carcinogenicity studies conducted in rats over a 2-year period. 696

To decrease the risk of the expansion of IMI-herbicide WR resistance and gene flow 697

movement, stewardship guides have been developed and should be implemented strictly; for 698

example, the planting of Clearfield rice cultivars in the same field and the use of diverse 699

herbicides (herbicides rotation) is prohibited. Clearfield® certified seeds must be used during 700

cultivation, and IMI-herbicides should be used according to the manufacturer’s instructions to 701

obtain high WR control. Farmers should also use Integrated Weed Management Systems 702

(IWMS) in the field and incorporate this system within CPS quid lines. Therefore, the 703

development of the biotechnological-based strategies prepared to decrease gene flow 704

introgression between Clearfield® rice and WR should be considered for the diverse traits 705

involved in gene flow reduction (Merotto et al. 2006). 706

The CPS system is a good tool for WR control compared to other control methods, and 707

the successful control of WR in cultivation fields requires a holistic and integrated approach 708

constituting diverse agricultural management methods, such as a correct ploughing approach, 709

using only certified rice cultivars, resorting to a high crop seeding rate, removing escaped WR, 710

and a good planting time in addition to the application of herbicides and other WR management 711

control approaches. 712

5. WR management approaches 713

714

Managing the WR population in the field and the gene flow process are important and 715

need to be discussed alongside the development of any herbicide-resistant crop. WR 716

management practice has been proven to be effective in the past few decades; the progression of 717

the IWMS process is crucial to the agricultural sector (Li et al. 2016). IWMS has an important 718

Page 31 of 70



Draft

32

part in WR control and management, as if the control of WR plants is not managed, could lead to 719

almost complete yield loss; therefore, the role that IWMS plays includes actions and procedures 720

(mechanical, physical, biological, behavior, and chemical) that can be used to control/eliminate 721

weeds, reduce competition with cultivation crops, and increase crop yields (Chauhan 2012). 722

Essentially, IWMS focuses on the procedures and information that deliberates the real reason 723

behind the appearance of weeds, causing problems by analyzing materials, drafting preventive 724

plans, and implementing management skills. The IWMS approach was adopted as a novel future 725

tool by diverse researchers for weed management (Azmi 2002) (see Figure 5). 726

• Cultural procedures 727

Cultural procedures are crucial to the cultivation system, which includes these steps: 728

1) Selecting certified seeds to minimize the presence of contaminated seeds in those that are 729

to be cultivated, because rice cultivars contaminated with WR seed are the main reason for the 730

escalation of WR infestation in the field (Azmi and Karim 2008). However, in certain cases, the 731

certified cultivars are not viable, which leads the farmers to procure seed loans or even use 732

contaminated seeds. A study conducted in Sri Lanka revealed that the percentage of certified 733

seeds viable for farmers did not exceed 15% (Marambe 2009). Another study in Vietnam 734

reported that the number of weed seeds, including barnyard grass/kg of rice seeds, is 46.6 times 735

higher than the permitted level (Mai et al. 1998). It is imperative to iterate that, according to 736

Chauhan et al. (2014), using clean seeds reduces WR seed production to 29-41%, as WR 737

competes with cultivated rice, leading to a decrease in crop yield, and ultimately causing the 738

price of harvested crops to drop due to seed contamination. 739

2) Uprooting (hand pulling) and chopping are also common cultural approaches. Farmers cut 740

panicles prior to seed shattering; uprooting weeds from the field using bare hands is an old 741

Page 32 of 70



Draft

33

systematic technique that has been used for several years in Asian paddy fields, but is time- 742

consuming and requires strenuous effort (Bakar 2006a). However, Rekha et al. (2002) noted that 743

there is significantly higher WR control efficiency with hand weeding, and a higher yield 744

reported with hand weeding twice at 30 and 40 days post-transplanting. In spite of that, weeding 745

needs to be done before the flowering of WR, otherwise the seeds will descend from the panicles 746

to the ground, thus exacerbating the problem. As noted beforehand, this practice was found to be 747

impractical, especially in broadcast-seeded rice (Azmi and Karim 2008), resulting in accidental 748

damage to the cultivated rice during the process. Furthermore, manual weeding of WR is costly 749

to the growers, both physically (labor effort) and economically. 750

3) Combining and burning the remaining crops and WR plants from the previous season 751

reduces infestation in the following seasons, and helps to reduce WR pre-sowing (Azmi and 752

Karim 2008). However, this traditional procedure causes severe air pollution and leads to acid 753

rain. 754

4) Surface tillage or not-in-depth tillage. The tillage process is important for the soil, as it 755

improves its physicochemical and biological characteristics, also leading to increased soil 756

ventilation and pores, while eliminating invasive WR. A study revealed that 75% of the WR was 757

eliminated due to tillage at a depth of ~8 cm (Chauhan 2012). However, farmers should be 758

mindful and note that the second tillage for the following season should be ~2-5 cm from the soil 759

surface to prevent the buried seeds from reappearing above ground (Thanh et al. 1999). 760

Therefore, when the WR seeds are present on the soil’s surface, the soil’s ability to germinate 761

decreased. The percentage of mortality increases between seed populations, which decreases due 762

to the presence of ants and birds (Mohler and Asdale 1993). 763

Page 33 of 70



Draft

34

5) Increasing crop sowing quantities in the soil to ~160 kg/ha reduces the amount of WR in 764

the field, which acts as an insurance against crop failure from decreased growth (Baki 2006). 765

Rathore et al. (2013) revealed that increasing seeding rates could help to suppress WR in infested 766

fields and that WR quantity decreases when rice seeding quantities are increased from 50 to 150 767

kg/ha-1. Furthermore, by increasing the seeding rates of 80–100 kg/ha, above the optimum rate of 768

60 kg/ha in infested areas, the infestation with WR could be reduced (Bakar et al. 2000). 769

6) Proper transplanting, as an alternative to transplanting rice seeds into the puddled soil, is 770

the most predominant plantation method in the world. It has many merits, such as high crop 771

establishment and the suppression of weed growth due to standing water (Chauhan 2012; Sharma 772

et al. 2003), but it also needs more workers, increased effort, and substantial quantities of water. 773

7) A stale seedbed practice can decrease WR infestation. Here, WR was allowed to grow to a 774

certain point after ploughing, and was slightly irrigated to encourage seed germination, before 775

being sprayed with pre-herbicides such as glyphosate ~15 days before cultivation to eliminate 776

WR (Juraimi et al. 2013). 777

• Crop rotation procedures 778

The rotation system cycle has many advantages, and is more efficient at decreasing the 779

presence of WR. Most studies have reported that wheat and bean have the greatest influence on 780

nitrogen concentrations in soils (Garrido and López-Bellido 2001). Crop rotation grows diverse 781

crops systemically on the same land. In contrast, monoculture crop involves planting only one 782

type of crop all year, which could result in increased weed infestations (Power and Follett 1987). 783

Rotation is important in the cultivation process. For example, an experiment in Utah (USA) 784

showed that the yield production increased significantly compared to the monoculture system, by 785

up to 79%, when wheat was cultivated and rotated with sugar beets (Stewart and Pittman 1931). 786

Page 34 of 70



Draft

35

Thus, the rotation system is an effective system for suppressing weed proliferation. Azmi et al. 787

(2008) reported that the best WR control can be achieved by rotating certified crops, for example 788

soybean and maize, with the combination of traditional herbicide treatments and cultural 789

practices. 790

• Herbicide rotation procedures 791

Herbicide rotation in rice cultivation is an effective way of reducing the exchange of 792

genes between commercial rice and WR plants, as it helps to curtail the WR flowering process 793

that reduces pollen movement via multiple mechanisms. The suitable timing of herbicide 794

applications, as well as the type of herbicide and its application rate, should be taken into 795

consideration by the farmers prior to usage. This is crucial as the controlled application of IMI 796

herbicide can reduce chemical residues, leading to water and soil pollution. Similarly, the 797

synergistic mechanism between the IMI-herbicide family and other traditional herbicides 798

contribute to high WR control, as stated in Table 3. Thiobencarb herbicide, for instance, is a type 799

of traditional herbicide, which is used to control red rice in the US. Similarly, pretilachlor and 800

dimethenamid herbicides were used in European fields to control WR at rates higher than 75% 801

(Abraham and Jose 2015). Moreover, Parameswari and Srinivas (2017) reported that the 802

maximum weed control in the field reached ~95% from the application of bensulfuron methyl 803

herbicide. Due to the diversity of chemical herbicides, certain types of herbicides are used as a 804

pre-application to prevent WR germination. Noldin (1998) showed that using metolachlor pre-805

emergence resulted in a WR control of ~90%. Therefore, farmers should not depend on a single 806

mode of specific herbicide; instead, they should use mixtures or sequential applications of 807

herbicides with different modes of action. 808

809

Page 35 of 70



Draft

36

• Using competitive cultivars 810

Competitive cultivars are more resilient against WR in the field. Recently, short-statured 811

cultivars have been introduced to the market that result in higher yields compared to local taller 812

cultivars, which are found to be more competitive, but have lower reported yields (Chauhan 813

2013). For example, rice cultivars PR-120, IR88633, and IR83927 were found to be strong weed 814

competitors in DSR (Mahajan and Chauhan 2015). Studies also revealed that the 'IR64' rice 815

matured earlier compared to WR plants, which is a trait that is essential for rice seeds battling the 816

contamination of WR seeds during harvest. It also reduced the WR seedbank, which helps to 817

reduce the proliferation of WR (Azmi and Karim 2008). It helps to improve rice cultivars due to 818

its increased seedling vitality and vigor, which decreases crop losses due to WR. 819

• Increasing nitrogen concentration 820

Increased nitrogen rates in the soil could very well strengthen WR to levels that could 821

actually compete with cultivated rice (Khan et al. 2012). Elements and minerals are essential to 822

plant growth due to its roles in the metabolism processes; the addition of nitrogen to the soil 823

resulted in plants that are more resilient vis-à-vis WR. Nitrogen also encourages photosynthesis, 824

which balances the carbon content of the soil (Khan et al. 2012). However, Sweeney and 825

McCouch (2007) showed that the competition depends on the type of weeds, temperature, and 826

humidity. Nevertheless, farmers should also be aware of the fact that increasing nitrogen 827

concentration in the soil could negatively affect the crop. Farooq et al. (2011) pointed out that to 828

overcome the lodging problem in rice cultivation, the DSR method should include decreased 829

nitrogen fertilization, which curtails culm growth. 830

831

832

Page 36 of 70



Draft

37

• Water management process 833

The water seeding process is regarded as one of the most effective methods for 834

controlling WR. It can suppress and control more than 50% of WR, which increases up to 90% if 835

a suitable herbicide is used (Gealy et al. 2003). Fogliatto et al. (2011) concluded that water could 836

better suppress WR. Azmi and Karim (2008) reported that using water to corral WR in the field 837

is essential, and the study showed that a flooding depth of up to 10 cm can decrease the 838

emergence of WR. Additionally, Azmi et al. (1999) showed that the management of water 839

quantity during rice cultivation affects WR emergence and infestation, because the shortage of 840

water in the field encourages WR infestation and thus competes with the rice crop plants. 841

Chauhan (2013) showed that when seeds were sown at a depth of 1 cm in the soil, the flooding 842

decreased the emergence and seedling biomass of all WR accessions by more than 85%. In 843

addition, seeding pre-germinated rice seeds in water decreased the presence of WR by 20% and 844

its recurrence by 70–76% (Azmi and Baki 2003). 845

• Training and Education of Farmers 846

Clearly, farming practices play an important role in WR restriction. It is regarded as being key to 847

the successful management of WR in the field; therefore, there is a need to share effective 848

strategies to control WR with rice farmers. It is equally important to understand how farmers are 849

affected by WR and what they know about it; therefore, researchers need to identify information 850

gaps and behavioral patterns of farmers towards WR (Chauhan and Abugho 2013). Farmers need 851

to be trained on the best approaches to manage WR, from preventive techniques to utilizing the 852

best herbicides. Well-trained farmers will result in a significant reduction of WR in the fields. On 853

the other hand, continuous support funding and increased levels of skill development for farmers 854

(Siwar et al. 2014) are excellent approaches in the prevention of WR infestation. Unfortunately 855

Page 37 of 70



Draft

38

there are extreme cases where the intensive infestation of WR in rice fields forced the farmers to 856

abandon their fields due to the inevitable total loss, as was the case in Costa Rica, where some 857

farmers had to leave their fields due to the severe infestation of WR and its increased resistance 858

to herbicides (Lu and Snow 2005). This has been the focus of agricultural research since the 859

1990s, wherein the subjects of interest include weed management, aggressive limiting factors for 860

rice crops as weeds, and increasing rice yields (Mispan 2008). The high efficiency of the 861

herbicide eliminated most rice weeds; however, there was no selective herbicide control for WR 862

during the post-emergence stages of Clearfield® rice cultivars and IMI-herbicide family (Azmi et 863

al. 2012). CPS technology can go in three directions vis-à-vis WR control, as it reduces WR 864

infestation, increases yield, and is able to target selective WR control; notably, of course, these 865

approaches are not without side effects. To ensure the viability of this approach, the Steward 866

Guide must be implemented. The farmers should practice crop rotation and use different 867

herbicides or a combination of one IMI-herbicide with another. It is also important to eliminate 868

escaped WR before they mature and then shatter the seeds; failing to do this could result in gene 869

crossing with the Clearfield® rice crop, resulting in a more resistant WR plant. This work 870

involves details pertaining to resistant WR plants and CPS technology used to control/eliminate 871

weeds. The tables and figures help to outline a more effective WR control approach in paddy 872

fields, while also helps to develop a novel evaluation method to determine the persistence of 873

IMI-herbicides and leaching in soil/water. 874

6. Conclusion 875

Herbicides are the most economical way of controlling weeds, and the continuous use of 876

certain herbicides could result in the development of herbicide-resistant weeds. The introduction 877

of IMI-herbicides and Clearfield® rice worldwide has resulted in the superb control of WR. 878

Page 38 of 70



Draft

39

Remarkably, there was an increase in rice grain yield in the first years using IMI-rice technology 879

and the rice profitability for the growers improved, resulting in a high economic impact at the 880

regional and state levels. However, the persistence of WR in soil and water invariably affects the 881

subsequent cultivation of crops in the same soil. Furthermore, the resistance of weeds to 882

herbicides due to gene interference is taking root. The effective control of WR cannot be based 883

on a single practice; instead, it should rely on a complex and all-encompassing management 884

program. It is important to study and understand the environmental nature, behavior of IMI-885

herbicides and evaluate their potential concerns to human, animal and environmental health. 886

Avoiding IMI- herbicide resistance and persistence problems necessitates the use of appropriate 887

rates, application timings, selective tillage, and IMI-herbicide combinations to reduce the risk of 888

carryover problems. Wise IMI-herbicide use ensures the continuous availability of these 889

important weed management tools for the future. Therefore, IWMS is regarded as a sustainable 890

technique to control WR, as it reduces the risk of herbicide-resistant weeds, decrease residues 891

and maintains the novelty of the CPS technology. Finally, it is important that future studies on 892

animals and aquatic species be conducted to clarify whether the leaching residues impact non-893

targeted species (useful microorganism) in the soils. 894

895

896

897

898

899

900

Page 39 of 70



Draft

40

901

Acknowledgements 902

The authors would like to thank the Fundamental Research Grant Scheme, FRGS: FP001-2015A 903

and the University Malaya Research Grant, UMRG: RG 311-14AFR. Also, the authors would 904

like to thank the two reviewers (from the same domain) of this article for their comments which 905

have resulted in a significantly improved review. 906

Contributions: All authors contributed equally to the design, information, writing and editing of 907

this work. 908

909

910

911

912

913

914

915

916

917

918

919

920

921

922

923

Page 40 of 70



Draft

41

References 924

Abraham, C., and Jose, N. 2015. Weedy rice invasion and its management. Indian J of Wed Sci. 925

47, 216-223. 926

Alister, C., and Kogan, M. 2005. Efficacy of imidazolinone herbicides applied to imidazolinone-927

resistant maize and their carryover effect on rotational crops. Crop Prot. 24, 375-379. 928

Aichele, T and Penner D. 2005. Adsorption, Desorption, and Degradation of Imidazolinone in 929

Soil. Wed Sci. 19,154–159. 930

American Cyanamid Company. 2000. Plateau herbicide, for weed control, native grass 931

establishment and turf growth suppression on roadsides and other non-crop areas., PE- 932

47015. Parsippany, NJ. 933

Area, R. G. 2010. Morphological Study of the Relationships between Weedy Rice Accessions 934

(Oryza sativa Complex) and Commercial Rice Varieties in Pulau Pinang. 935

936

Arnold, R. N., Murray, M. W., Gregory, E. J., and Smeal, D. 1993. Weed control in pinto beans 937

(Phaseolus vulgaris) with imazethapyr combinations. Weed Technol, 361-364. 938

Azmi, M., Abdullah, M., Mislamah, B., & Baki, B. (2000). Management of weedy rice (oryza 939

sativa l.): The malaysian experience. Wild and Weedy Rice in Rice Ecosystems in Asia-A 940

Review, 91-96. 941

Azmi, M. 2002. Impact of continuous direct seeding culture on weed species diversity in the 942

Malaysian rice ecosystem. In "Proceedings of Regional Symposium on Environment and 943

Natural Resources (Kuala Lumpur, Malaysia 10-11 April 2002)". Universiti Kebangsaan 944

Malaysia. 945

Azmi, M., Azlan, S., Yim, K., George, T., and Chew, S. 2012. Control of weedy rice in direct-946

seeded rice using the Clearfield production system in Malaysia. Pak J Weed Sci Res. 18, 947

49-53. 948

949

Azmi, M., and Baki, B. 2003. Weed species diversity and management practices in the 950

Sekinchan Farm Block, Selangor’s South West Project—a highly productive rice area in 951

Malaysia. In "Proceedings", Vol. 1, pp. 174-184. 952

953

Azmi, M., Hadzim, K., Habibuddin, H., Saad, A., Lim, W., and George, V. 2008. Malaysian rice 954

varieties tolerant to the herbicide imidazolinone for control of weedy rice infestation. 955

MARDI Kepala Batas 39. 956

957

Azmi, M., and Karim, S. 2008. Weedy rice-biology, ecology and management. Kuala Lumpur, 958

Malaysia: Malaysian Agricultural Research and Development Institute (MARDI). 959

960

Bahm, M. A., Barnes, T. G., and Jensen, K. C. 2011. Herbicide and fire effects on smooth brome 961

(Bromus inermis) and Kentucky bluegrass (Poa pratensis) in invaded prairie remnants. 962

Invas Plant Sci Mana. 4, 189-197. 963

964

Page 41 of 70



Draft

42

Bailey, W. A., and Wilcut, J. W. 2003. Tolerance of Imidazolinone-Resistant Corn (Zea mays) to 965

Diclosulam 1. Weed Technol. 17, 60-64. 966

Bakar, B. 2004. Invasive weed species in Malaysian agro-ecosystems: species, impacts and 967

management. Malaysian J of Sci 23. 968

969

Bakar, B., Bakar, M., and Man, A. 2000. Weedy rice (Oryza sativa L.) in peninsular Malaysia. 970

Wild and weedy rice in rice ecosystems in Asia—a review. IRRI, Los Banos, 51-54. 971

972

Bakar, B. H. 2006a. "Weed ecology and management in rice ecosystems," University of Malaya 973

Press. 974

975

Bakar, B. H. 2006b. "Weed Science in the Service of Humanity," Jabatan Penerbitan, Universiti 976

Malaya. 977

978

Bakar, F., Ismail, B., and Bajrai, F. 2016. Application of bioassay technique to determine onduty 979

herbicide resistance in soil. In "AIP Conference Proceedings", Vol. 1784, pp. 060011. 980

AIP Publishing. 981

982

Baki, B., Chin, D., and Mortimer, M. 2000. Wild and weedy rice in rice ecosystems in Asia—a 983

review. In "Limited proceedings", Vol. 2. 984

985

Baki, B., and Mispan, M. S. 2010. Spatio-temporal Distribution Pattern of New Biotypes of 986

Weedy Rice (Oryza sativa L.) in Selangor North-West Project, Malaysia. Kor J Weed 987

Sci. 30, 68-83. 988

989

Baki, H. B. 2006. weed science in the service of Humanity. 990

991

Battaglin, W., Furlong, E., Burkhardt, M., and Peter, C. 2000. Occurrence of sulfonylurea, 992

sulfonamide, imidazolinone, and other herbicides in rivers, reservoirs and ground water 993

in the Midwestern United States, 1998. Sci. Total Environ. 248, 123-133. 994

995

Begum, G. (2004). Carbofuran insecticide induced biochemical alterations in liver and muscle 996

tissues of the fish Clarias batrachus (linn) and recovery response. Aquat. Toxicol. 66, 83-997

92. 998

999

Begum, M., Juraimi, A., Azmi, M., Rajan, A., and Omar, S. S. 2005. Weed vegetation of direct 1000

seeded rice fields in muda rice granary areas of Peninsular Malaysia. Pakistan J. Biol. 1001

Sci. 8, 537-541. 1002

1003

Blouin, D. C., Webster, E. P., and Bond, J. A. 2010. On a method of analysis for synergistic and 1004

antagonistic joint-action effects with fenoxaprop mixtures in rice (Oryza sativa). Weed 1005

Technol 24, 583-589. 1006

1007

Börjesson, E., Torstensson, L., and Stenström, J. 2004b. The fate of imazapyr in a Swedish 1008

railway embankment. Pest Manag Sci 60, 544-549. 1009

1010

Page 42 of 70



Draft

43

Burgos, N. R., Norsworthy, J. K., Scott, R. C., and Smith, K. L. 2008. Red rice (Oryza sativa) 1011

status after 5 years of imidazolinone-resistant rice technology in Arkansas. Weed Technol 1012

22, 200-208. 1013

1014

Burgos, N. R., Singh, V., Tseng, T. M., Black, H., Young, N. D., Huang, Z., Hyma, K. E., Gealy, 1015

D. R., and Caicedo, A. L. 2014. The impact of herbicide-resistant rice technology on 1016

phenotypic diversity and population structure of United States weedy rice. Plant Physiol 1017

166, 1208-1220. 1018

Burke, I. C., Price, A. J., Wilcut, J. W., Jordan, D. L., Culpepper, A. S., and Tredaway-Ducar, J. 1019

2004. Annual Grass Control in Peanut (Arachis hypogaea) with Clethodim and Imazapic 1020

1. Weed technol 18, 88-92. 1021

1022

Busconi, M., Rossi, D., Lorenzoni, C., Baldi, G., and Fogher, C. 2012. Spread of herbicide‐1023

resistant weedy rice (red rice, Oryza sativa L.) after 5 years of Clearfield rice cultivation 1024

in Italy. Plant Biol 14, 751-759. 1025

1026

Bzour, M. I., Zuku, F. M., Mispan, S.M., Khairedeen, M.A., Jodeh, S., and Abdel-latif, M.S. 1027

2017. a simple method for determination and characterization of imidazolinone herbicide 1028

(imazapyr/imazapic) residues in clearfield® rice soil. Applied Ecology. 15(4):891-903. 1029

Cassol, G. V., Avila, L. A. d., Zemolin, C. R., Piveta, A., Agostinetto, D., and Merotto Júnior, A. 1030

2015. Sensitivity of imidazolinone-resistant red rice (Oryza sativa L.) to glyphosate and 1031

glufosinate. Ciência Rural. 45, 1557-1563. 1032

1033

Carol, A., Mallory, S., and Donald, C. 1990. Identification of Sulfonylurea Herbicide-Resistant 1034

Prickly Lettuce (Lactuca serrola). Weed technol, 4, 163-168. 1035

1036

Castro-Gutiérrez, N., McConnell, R., Andersson, K., Pacheco-Antón, F., and Hogstedt, C. 1997. 1037

Respiratory symptoms, spirometry and chronic occupational paraquat exposure. 1038

Scandinavian journal of work, environment & health, 421-427. 1039

1040

Cessna, J. A., Elliott., A. J., Bailey, J. 2012. Leaching of three imidazolinone herbicides during 1041

sprinkler irrigation. J. Environ. Qual. 41, 882. 1042

Changbao, Li., Zhou, A., Sang, T. 2006. Rice Domestication by Reducing Shattering. 1043

Science. 311, pp. 1936-1939. 1044

Chauhan, B. S. 2012. Weed ecology and weed management strategies for dry-seeded rice in 1045

Asia. Weed Technol 26, 1-13. 1046

1047

Chauhan, B. S. 2013. Strategies to manage weedy rice in Asia. Crop Prot 48, 51-56. 1048

1049

Chauhan, B. S., Abeysekera, A. S., Wickramarathe, M. S., Kulatunga, S. D., and Wickrama, U. 1050

B. 2014. Effect of rice establishment methods on weedy rice (Oryza sativa L.) infestation 1051

and grain yield of cultivated rice (O. sativa L.) in Sri Lanka. Crop Prot 55, 42-49. 1052

Page 43 of 70



Draft

44

1053

Chauhan, B. S., and Abugho, S. B. 2013. Weed management in mechanized-sown, zero-till dry-1054

seeded rice. Weed Technol 27, 28-33. 1055

1056

Chauhan, B. S., Awan, T. H., Abugho, S. B., and Evengelista, G. 2015. Effect of crop 1057

establishment methods and weed control treatments on weed management, and rice yield. 1058

Field Crops Res 172, 72-84. 1059

1060

Chauhan, B. S., and Johnson, D. E. 2010. Weedy rice (Oryza sativa) I. Grain characteristics and 1061

growth response to competition of weedy rice variants from five Asian countries. Weed 1062

sci 58, 374-380. 1063

1064

Chen, L. J., Lee, D. S., Song, Z. P., Suh, H. S., and LU, B. R. 2004. Gene flow from cultivated 1065

rice (Oryza sativa) to its weedy and wild relatives. Ann. Bot. 93, 67-73. 1066

1067

Croughan, T., Utomo, H., Sanders, D., and Braverman, M. 1996. Herbicide-resistant rice offers 1068

potential solution to red rice problem. Louisiana agriculture (USA). 1069

1070

Croughan, T. P. 2003. Clearfield rice: It's not a GMO. Louisiana Agriculture. 46, 24-26. 1071

1072

Curran, W. S. 2001. Persistence of herbicides in the soil. Agronomy. The Pennsylvania State 1073

University. 1074

D'Ascenzo, G., Gentili, A., Marchese, S., and Perret, D. 1998. Development of a method based 1075

on liquid chromatography–electrospray mass spectrometry for analyzing imidazolinone 1076

herbicides in environmental water at part-per-trillion levels. J of Chrom A 800, 109-119. 1077

1078

Dauer, J., Hulting, A., Carlson, D., Mankin, L., Harden, J., and Mallory‐Smith, C. 2017. Gene 1079

flow from single and stacked herbicide‐resistant rice (Oryza sativa): modeling occurrence 1080

of multiple herbicide‐resistant weedy rice. Pest Manag Sci. 1081

1082

Ducar, J. T., Wilcut, J. W., and RICHBURG III, J. S. 2004. Weed Management in 1083

Imidazolinone-Resistant Corn with Imazapic 1. Weed technol 18, 1018-1022. 1084

1085

El. Azzouzi, A., Dahchour, A., Ferhat, M. 1998. Study on the behavior of imazapyr in two 1086

Moroccan soils. Weed Res. 38, 217-220. 1087

1088

Engku, A., Norida, M., Juraimi, A., Rafii, M., Abdullah, S., and Alam, M. 2016. Gene flow from 1089

Clearfield® rice to weedy rice under field conditions. Plant, Soil and Environ 62, 16-22. 1090

1091

Farooq, M., Siddique, K. H., Rehman, H., Aziz, T., Lee, D.-J., and Wahid, A. 2011. Rice direct 1092

seeding: experiences, challenges and opportunities. Soil and Tillage Research 111, 87-98. 1093

1094

Page 44 of 70



Draft

45

Ferrero, A., and Finassi, A. 1995. Viability and soil distribution of red rice (Oryza sativa var. 1095

Silvatica) seeds [wild rice, a weed in most rice growing areas in the world]. 1096

Mededelingen-Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen 1097

Universiteit Gent (Belgium). 1098

1099

Fish, J. C., Webster, E. P., Blouin, D. C., and Bond, J. A. 2015. Imazethapyr Co-Application 1100

Interactions in Imidazolinone-Resistant Rice. Weed Technol. 29, 689-696. 1101

1102

Fogliatto, S., Vidotto, F., and Ferrero, A. 2011. Germination of weedy rice in response to field 1103

conditions during winter. Weed Technol. 25, 252-261. 1104

1105

Gagne, J. A., Fischer, J. E., Sharma, R. K., Traul, K. A., Diehl, S. J., Hess, F. G., and Harris, J. 1106

E. 1991. Toxicology of the imidazolinone herbicides. The imidazolinone herbicides, 179-1107

182. 1108

1109

Garrido, R. J. L.-B., and López-Bellido, L. 2001. Effects of crop rotation and nitrogen 1110

fertilization on soil nitrate and wheat yield under rainfed Mediterranean conditions. 1111

Agronomie 21, 509-516. 1112

1113

Gavrilescu, M. 2005. Fate of Pesticides in the environment and its bioremedation. Eng. Life Sci. 1114

5, 497-526. 1115

Gealy, D., and Black, H. 1999. Effect of imazethapyr on several red rice (Oryza sativa L.) 1116

accessions and rice lines. In "Proc. South. Weed Sci. Soc", Vol. 52, pp. 211. 1117

1118

Gealy, D. R., Mitten, D. H., and Rutger, J. N. 2003. Gene flow between red rice (Oryza sativa) 1119

and herbicide-resistant rice (O. sativa): implications for weed management 1. Weed 1120

technol 17, 627-645. 1121

1122

Gianinetti, A., and Vernieri, P. 2007. On the role of abscisic acid in seed dormancy of red rice. J. 1123

Exp. Bot. 58, 3449-3462. 1124

1125

Goetz, A. J., Wehtje, G., Walker, R. H., and Hajek, B. 1986. Soil solution and mobility 1126

characterization of imazaquin. Weed Sci. 788-793. 1127

1128

Goulart, I., Matzenbacher, F., and Merotto, A. 2012. Differential germination pattern of rice 1129

cultivars resistant to imidazolinone herbicides carrying different acetolactate synthase 1130

gene mutations. Weed Res. 52, 224-232. 1131

1132

Goulart, I. C., Borba, T. C., Menezes, V. G., and Merotto Jr, A. 2014. Distribution of weedy red 1133

rice (Oryza sativa) resistant to imidazolinone herbicides and its relationship to rice 1134

cultivars and wild Oryza species. Weed sci 62, 280-293. 1135

1136

Graham, R., Pratley, J., Slater, P., Humphreys, E., Murray, E., Clampett, W., and Lewin, L. 1137

1994. Herbicide resistance in Cyperus difformis, a weed of New South Wales rice crops. 1138

In "Proceedings of Temperate Rice Conference—Achievements and Potential. Leeton, 1139

Page 45 of 70



Draft

46

New South Wales, Australia. Griffith, Australia: Temperate Rice Conference Organising 1140

Committee", pp. 433-435. 1141

1142

Gressel, J., and Valverde, B. E. 2009. A strategy to provide long‐term control of weedy rice 1143

while mitigating herbicide resistance transgene flow, and its potential use for other crops 1144

with related weeds. Pest Manag Sci 65, 723-731. 1145

1146

Grey, T. L., Cutts III, G. S., and Johnson, J. 2012. Imidazolinone-resistant soft red winter wheat 1147

weed control and crop response to ALS-inhibiting herbicides. Weed Technol 26, 405-1148

409. 1149

1150

Grichar, W. J., Nester, P. R., and Colburn, A. E. 1992. Nutsedge (Cyperus spp.) control in 1151

peanuts (Arachis hypogaea) with imazethapyr. Weed Technol, 396-400. 1152

1153

Grichar, W. J., Dotray, A. P., and Baughman, A.T. 2011. Influence of Simulated Imazapic and 1154

Imazethapyr Herbicide Carryover on Cotton (Gossypium hirsutum L.). J. Agron. 1155

1156

Grymes, C. F., Chandler, J. M., and Nester, P. R. 1995. Response of soybean (Glycine max) and 1157

rice (Oryza sativa) in rotation to AC 263,222. Weed technol, 504-511. 1158

1159

Hakim, M. A., Juraimi, A. S., Musa, M. H., Ismail, M. R., Rahman, M. M., and Selamat, A. 1160

2013. Impacts of weed competition on plant characters and the critical period of weed 1161

control in rice under saline environment. Aust J Crop Sci. 7, 1141. 1162

1163

He, Q., Kim, K. W., and Park, Y. J. 2017. Population genomics identifies the origin and 1164

signatures of selection of Korean weedy rice. Plant biotechno j. 15, 357-366. 1165

1166

Heap, I. 2014. Herbicide resistant weeds. In "Integrated pest management", pp. 281-301. 1167

Springer. 1168

Helling, C. S., and Doherty, M. A. 1995. Improved method for the analysis of imazapyr in 1169

soil. Pestic Sci. 45, 21-26. 1170

1171

Hollaway, K., Kookana, R. S., Noy, D., Smith, J., and Wilhelm, N. 2006. Persistence and 1172

leaching of sulfonylurea herbicides over a 4-year period in the highly alkaline soils of 1173

south-eastern Australia. Australian J of Experim Agri. 46, 1069-1076. 1174

1175

Hossain, F., Ali, O., D'Souza, U. J., and Naing, D. K. S. 2010. Effects of pesticide use on semen 1176

quality among farmers in rural areas of Sabah, Malaysia. Journal of occupational health 1177

52, 353-360. 1178

1179

Ibrahim, M. B., Juraimi, A. S., Hakim, M., Aslani, F., Karim, S., and Alam, M. A. 2017. 1180

Residual effect of imidazolinone herbicide used in clearfield (r) rice on non-clearfield 1181

rice. BANGL J BOT. 46, 335-341. 1182

1183

Ismail, B., Sameni, M., and Halimah, M. 2011. Evaluation of herbicide pollution in the kerian 1184

ricefields of Perak, Malaysia. World. Appl. Sci. J 15, 5-13. 1185

Page 46 of 70



Draft

47

1186

Itoh, K., Azmi, M., and Ahmad, A. 1992. Paraquat resistance in Solanum nigrum, 1187

Crassocephalum crepidioides, Amaranthus lividus and Conyza sumatrensis in Malaysia. 1188

In "Proceedings of the 1st International Weed Control Congress", Vol. 2, pp. 224-228. 1189

1190

Jabran, K., and Chauhan, B. S. 2015. Weed management in aerobic rice systems. Crop Prot 78, 1191

151-163. 1192

1193

James, R. M., and Esau, R. 1996. Imidazolinone Herbicide Effects on Following Rotational 1194

Crops in Southern Alberta. Wed Sci. 10, 100-106. 1195

1196

Jason K. Norsworthy, R. C. S. 2011. weed management in furrow - irrigated imidazoline - 1197

resistant hybrids rice production system. weed Technol. 25, 25-29. 1198

1199

Jia, S. 2002. Studies on gene flow in China–a review. In "The 7th International Symposium on 1200

the Biosafety of Genetically Modified Organisms", pp. 92. 1201

1202

Juraimi, A. S., Uddin, M. K., Anwar, M. P., Mohamed, M. T. M., Ismail, M. R., and Man, A. 1203

2013. Sustainable weed management in direct seeded rice culture: a review. Australian J 1204

of Crop Sci. 7, 989. 1205

1206

Kaloumenos, N. S., Capote, N., Aguado, A., and Eleftherohorinos, I. G. 2013. Red rice (Oryza 1207

sativa) cross-resistance to imidazolinone herbicides used in resistant rice cultivars grown 1208

in northern Greece. Pestici Biochem and Physio. 105, 177-183. 1209

1210

Kanungo, D., Buffinton, G. (2013). Food Safety and Standards Authority of India, Delhi, India. 1211

355–391. 1212

Karim, R. S., Man, A. B., and Sahid, I. B. 2004. Weed problems and their management in rice 1213

fields of Malaysia: An overview. Weed Biol. Manag 4, 177-186. 1214

1215

Khan, N., Khan, N., Khan, S., Khan, M., and Marwat, K. 2012. Combined effect of nitrogen 1216

fertilizers and herbicides upon maize production in Peshawar. J ANIM PLANT SCI 2, 1217

12-18. 1218

1219

Khush, G. 1993. Floral structure, pollination biology, breeding behaviour, transfer distance and 1220

isolation considerations. World bank technical paper. Biotechnology Series. 1221

1222

Kim, S.-C., and Ha, W.-G. 2005. Direct seeding and weed management in Korea. Rice Is Life: 1223

Scientific Perspectives for the 21st Century. Los Banos, Philippines: International Rice 1224

Research Institute, and Tsukuba, Japan: Japan International Research Center for 1225

Agricultural Sciences, 181-184. 1226

1227

Klingman, T. E., King, C. A., and Oliver, L. R. 1992. Effect of application rate, weed species, 1228

and weed stage of growth on imazethapyr activity. Weed Sci, 227-232. 1229

Page 47 of 70



Draft

48

1230

Kohara, H. 1996. Resistance to sulfonylurea herbicides in Monochoria korsakowii Regel et 1231

Maack. in Hokkaido. J. Weed Sci Technol. 41, 236-237. 1232

1233

Koutros, S., Silverman, D.T., Alavanja, M.C., Andreotti, G., Lerro, C.C., Heltshe, S., Beane 1234

Freeman, L.E. 2015. Occupational exposure to pesticides and bladder cancer risk. Int. j. 1235

epidemiol, 45(3), 792-805. 1236

Kraehmer, H., Jabran, K., Mennan, H., and Chauhan, B. S. 2016. Global distribution of rice 1237

weeds–A review. Crop Prot 80, 73-86. 1238

1239

Krynitsky, A. J., Stout, S. J., Nejad, H., and Cavalier, T. C. 1999. Multiresidue determination and 1240

confirmation of imidazolinone herbicides in soil by high-performance liquid 1241

chromatography/electrospray ionization mass spectrometry. J. AOAC. 82, 956-962. 1242

1243

Kumar, V., Bellinder, R., Gupta, R., Malik, R., and Brainard, D. 2008. Role of herbicide-1244

resistant rice in promoting resource conservation technologies in rice–wheat cropping 1245

systems of India: a review. Crop Prot. 27, 290-301. 1246

1247

Laganà, A., Fago, G., and Marino, A. 1998. Simultaneous determination of imidazolinone 1248

herbicides from soil and natural waters using soil column extraction and off-line solid-1249

phase extraction followed by liquid chromatography with UV detection or liquid 1250

Chromatography/Electrospray mass spectroscopy. Anal. Chem 70, 121-130. 1251

Langevin, S. A., Clay, K., and Grace, J. B. 1990. The incidence and effects of hybridization 1252

between cultivated rice and its related weed red rice (Oryza sativa L.). Evolution, 1000-1253

1008. 1254

1255

Li, B., and Foley, M. E. 1997. Genetic and molecular control of seed dormancy. Trends Plant Sci 1256

2, 384-389. 1257

1258

Li, L.-F., Li, Y.-L., Jia, Y., Caicedo, A. L., and Olsen, K. M. 2017. Signatures of adaptation in 1259

the weedy rice genome. Nature Genetics. 49, 811-814. 1260

1261

Li, M., Jordan, N. R., Koide, R. T., Yannarell, A. C., and Davis, A. S. 2016. Meta-analysis of 1262

crop and weed growth responses to arbuscular mycorrhizal fungi: Implications for 1263

integrated weed management. Weed Sci. 64, 642-652. 1264

1265

Loux, M. M, and Reese, D. K. (1993). Effect of Soil Type and pH on Persistence and Carryover 1266

of Imidazolinone Herbicides. Weed Sci. (7) 2. 452-458. 1267

Low, K., Boobis, A., and. Moretto, A. (2013). Health Evaluation Directorate, Pest Management 1268

Regulatory Agency, Health Canada, Ottawa, 317–353. 1269

Lu, B.-R., and Snow, A. A. 2005. Gene flow from genetically modified rice and its 1270

environmental consequences. BioScience 55, 669-678. 1271

Mahajan, G., and Chauhan, B. 2015. Weed control in dry direct-seeded rice using tank mixtures 1272

of herbicides in South Asia. Crop Prot. 72, 90-96. 1273

Page 48 of 70



Draft

49

1274

Mai, V., Chien, H., Suong, V., and Thiet, L. 1998. Survey and Analysis of Farmers’ Seed 1275

Contamination by Weed and Weedy Rice Seeds in South Vietnam. 1997. In 1276

"International Symposium on Wild and Weedy Rices in Agroecosystems", pp. 10-11. 1277

1278

Manning-Bog, A. B., McCormack, A. L., Li, J., Uversky, V. N., Fink, A. L., and Di Monte, D. 1279

A. 2002. The Herbicide Paraquat Causes Up-regulation and Aggregation of α-Synuclein 1280

in Mice PARAQUAT AND α-SYNUCLEIN. J. Biol. Chem. 277, 1641-1644. 1281

Mannion, A. M. 1995. Agriculture, environment and biotechnology. Agric. Ecosyst. Environ 53, 1282

31-45. 1283

1284

Marambe, B. 2009. Weedy rice—evolution, threats and management. Trop Agriculturist 157, 43-1285

64. 1286

1287

Marcia, e. a. 2014. Amethod for determination of imazapic and imazethapyr residues in soil 1288

using an ultrasonic assisted extraction. Bull Environ Contam Toxical 93, 360-364. 1289

1290

Martins, G. L., Friggi, C. A., Prestes, O. D., Vicari, M. C., Friggi, D. A., Adaime, M. B., and 1291

Zanella, R. 2014. Simultaneous LC–MS/MS Determination of Imidazolinone Herbicides 1292

Together with Other Multiclass Pesticide Residues in Soil. CLEAN–Soil, Air, Water 42, 1293

1441-1449. 1294

1295

Masson, J. A., and Webster, E. P. 2001. Use of Imazethapyr in Water-Seeded Imidazolinone-1296

Tolerant Rice (Oryza sativa) 1. Weed technol. 15, 103-106. 1297

1298

Mastan, J., Srinivas, B., Rao, T. N., and Apparao, K. 2016. Determination of Imazamox and 1299

Imazethapyr Herbicide Residues in Soybean oil. 1300

1301

Meins, K., Scott, R., Dillon, T., and Pearrow, N. 2003. Tolerance of Clearfield rice to imazamox. 1302

BR Wells Rice Research Studies, 132-136. 1303

1304

Merotto, A., Goulart, I.G., Nunes, A., Kalsing, A., Markus, C., Menezes, V. and Wander, A 1305

.2006. Evolutionary and social consequences of introgression of non -transgenic herbicide 1306

resistance from rice to weedy rice in Brazil. Evolutionary appl. 9. 837-846. 1307

Messeguer, J., Marfa, V., Catala, M., Guiderdoni, E., and Melé, E. 2003. A field study of pollen-1308

mediated gene flow from GM rice to conventional rice and the red rice weed [M-30]. 1309

1310

Mispan, M., and Baki, B. 2008. They stand among equals: Descriptive analysis on the new 1311

biotypes of weedy rice (Oryza sativa L.) in Malaysia. In "Abstracts V International Weed 1312

Science Congress,” Vancouver, Canada, Abstract", Vol. 724. 1313

1314

Mispan, M. S. 2008. Descriptive analyses on the new biotype of weedy rices in Selangor North-1315

West project, Malaysia Masters thesis.University of Malaya. 1316

1317

Page 49 of 70



Draft

50

Mohler, C., and Asdale, J. 1993. Response of weed emergence to rate of Vicia villosa Roth and 1318

Secale cereale L. residue. Weed Res. 33, 487-499. 1319

1320

Moraes, B. S., Clasen, B., Loro, V. L., Pretto, A., Toni, C., de Avila, L. A., Marchesan, E., de 1321

Oliveira Machado, S. L., Zanella, R., and Reimche, G. B. 2011. Toxicological responses 1322

of Cyprinus carpio after exposure to a commercial herbicide containing imazethapyr and 1323

imazapic. Ecotoxicol Environ Safety. 74, 328-335. 1324

1325

Mortimer, A., Ulf-Hansen, P., and Putwain, P. 1992. Modelling herbicide resistance-A study of 1326

ecological fitness. In "Resistance’91: Achievements and Developments in Combating 1327

Pesticide Resistance", pp. 148-164. Springer. 1328

1329

Muker, H., and Sharma, H. 1991. Isolation distance for producing hybrid rice seed. Intern. Rice 1330

Res. Notes 16, 6. 1331

1332

Mukherjee, P., Sarkar, A., and Maity, S. K. 2008. Critical period of crop-weed competition in 1333

transplanted and wet-seeded kharif rice (Oryza sativa L.) under Terai conditions. Indian J 1334

of Wed Sci. 40, 147-152. 1335

1336

Mukhopadhyay, S. 1995. Current scenario and future lines of weed management in rice crop 1337

with particular references to India. In "Proc. 15th APWSS, conf. Tsukuba, Japan", Vol. 1, 1338

pp. 28-41. 1339

1340

Najim, M., Lee, T., Haque, M. A., and Esham, M. 2007. Sustainability of rice production: A 1341

Malaysian perspective. J of Agri Scie 3. 1342

1343

Neto, M. D. d. C., Souza, M. d. F., Silva, D. V., Faria, A. T., da Silva, A. A., Pereira, G. A. M., 1344

and de Freitas, M. A. M. 2017. Leaching of imidazolinones in soils under a clearfield 1345

system. Archives of Agronomy and Soil Sci. 63, 897-906. 1346

1347

Noldin, J. 1998. Red rice situation and management in the Americas. In "International 1348

Symposium on Wild and Weedy Rices in Agro-ecosystem. Asian Pacific Weed Science 1349

Society", pp. 36-41. 1350

1351

Noldin, J., Yokoyama, S., Antunes, P., and Luzzardi, R. 2002. Outcrossing potential of 1352

glufosinate-resistant rice to red rice. Planta Daninha. 20, 243-251. 1353

1354

Norsworthy, J. K., Bond, J., and Scott, R. C. 2013. Weed management practices and needs in 1355

Arkansas and Mississippi rice. Weed Technol. 27, 623-630. 1356

1357

Novakova, O. 1994. Determination of imazethapyr and imazapyr residues in soil by coupled-1358

column liquid chromatography. Chromatographia 39, 62-66. 1359

1360

Olajumoke, B., Juraimi, A. S., Uddin, M., Husni, M. H., and Alam, M. 2016. Competitive ability 1361

of cultivated rice against weedy rice biotypes: A review. CHIL J AGR RES. 76, 243-252. 1362

1363

Page 50 of 70



Draft

51

Olsen, K. M., Caicedo, A. L., and Jia, Y. 2007. Evolutionary genomics of weedy rice in the 1364

USA. J of Integrative Plant Biol. 49, 811-816. 1365

1366

O, Sullivan, J., Thomas, R.J., and .Bouw, W.J. 1998. Effect of imazethapyr and imazamox soil 1367

residies on several vegetable crope grown in Ontario. Can. J. Plant Sci. 78, 647-651. 1368

Ottis, B. V., Smith, K. L., Scott, R. C., and Talbert, R. E. 2005. Rice yield and quality as affected 1369

by cultivar and red rice (Oryza sativa) density. Weed sci. 53, 499-504. 1370

1371

Parameswari, Y., and Srinivas, A. 2017. WEED MANAGEMENT IN RICE–A REVIEW. 1372

Internatinonal journal of Applied and Pure science and Agriculture. 1373

1374

Pellerin, K. J., Webster, E. P., Zhang, W., and Blouin, D. C. 2003. Herbicide Mixtures in Water-1375

Seeded Imidazolinone-Resistant Rice (Oryza sativa) 1. Weed technol 17, 836-841. 1376

1377

Pellerin, K. J., Webster, E. P., Zhang, W., and Blouin, D. C. 2004. Potential Use of Imazethapyr 1378

Mixtures in Drill-Seeded Imidazolinone-Resistant Rice 1. Weed technol 18, 1037-1042. 1379

Power, J., and Follett, R. 1987. Monoculture. Scientific American (USA). 1380

1381

Qi, Y., Yan, B., Fu, G., Guan, X., Du, L., and Li, J. 2017. Germination of Seeds and Seedling 1382

Growth of Amaranthus retroflexus L. Following Sublethal Exposure of Parent Plants to 1383

Herbicides. Scientific Reports 7. 1384

1385

Quivet, E., Faure, R., Georges, J., Paıssé, J.O., & Lantéri, P. (2006). Influence of metal salts on 1386

the photodegradation of imazapyr, an imidazolinone pesticide. Pest management science, 1387

62(5), 407-413. 1388

Rainbolt, C. R., Thill, D. C., Yenish, J. P., and Ball, D. A. 2004. Herbicide-Resistant Grass Weed 1389

Development in Imidazolinone-Resistant Wheat: Weed Biology and Herbicide Rotation 1390

1. Weed technol. 18, 860-868. 1391

1392

Ramezani, M., Simpson, N., Oliver, D., Kookana, R., Gill, G., and Preston, C. 2009. Improved 1393

extraction and clean-up of imidazolinone herbicides from soil solutions using different 1394

solid-phase sorbents. J of Chrom A. 1216, 5092-5100. 1395

Ramezani, M., Oliver, D. P., Kookana, R., Gill1, G., and Preston, C. 2008. Abiotic 1396

degradation (photodegradation and hydrolysis) of imidazolinone herbicides. J. Environ. 1397

Sci. Health, Part B. 34, 105-112. 1398

Rathore, M., Singh, R., and Kumar, B. 2013. Weedy rice: an emerging threat to rice cultivation 1399

and options for its management. Current Science 105, 1067. 1400

1401

Rathore, M., Singh, R., Kumar, B., and Chauhan, B. 2016. Characterization of functional trait 1402

diversity among Indian cultivated and weedy rice populations. Scientific reports 6. 1403

1404

Page 51 of 70



Draft

52

Ratnasekera, D., Perera, U. I., He, Z., Senanayake, S. G., Wijesekara, G. A., Yang, X., and Lu, 1405

B. 2014. High level of variation among Sri Lankan weedy rice populations, as estimated 1406

by morphological characterization. Weed Biol. Manag. 14, 68-75. 1407

1408

Refatti, J. P., Avila, L. A. d., Noldin, J. A., Pacheco, I., and Pestana, R. R. 2017. Leaching and 1409

residual activity of imidazolinone herbicides in lowland soils. Ciência Rural 47. 1410

1411

Rekha, K. B., Raju, M., and Reddy, M. 2002. Effect of herbicides in transplanted rice. Indian J of 1412

Wed Sci. 34, 123-125. 1413

1414

Richburg III, J. S., Wilcut, J. W., and Vencill, W. K. 1996. Imazethapyr systems for peanut 1415

(Arachis hypogaea L.). Peanut Science 23, 9-14. 1416

Richburg III, J. S., Wilcut, J. W., and Wiley, G. L. 1995. AC 263,222 and imazethapyr rates and 1417

mixtures for weed management in peanut (Arachis hypogaea). Weed technol, 801-806. 1418

1419

Rong, J., Song, Z., Su, J., Xia, H., Lu, B. R., and Wang, F. 2005. Low frequency of transgene 1420

flow from Bt/CpTI rice to its nontransgenic counterparts planted at close spacing. New 1421

Phytologist. 168, 559-566. 1422

1423

1424

Roso, A., Merotto Jr, A., Delatorre, C., and Menezes, V. 2010. Regional scale distribution of 1425

imidazolinone herbicide-resistant alleles in red rice (Oryza sativa L.) determined through 1426

SNP markers. FIELD CROP RES, 119, 175-182. 1427

1428

Sales, M.A., Burgos, N.R., Shivrain, V.K., Murphy, B., & Gbur, E.E. (2011). Morphological and 1429

physiological responses of weedy red rice (oryza sativa l.) and cultivated rice (o. Sativa) 1430

to n supply. Plant Sci, 2(04), 569. 1431

Santos, L., Pinto, J., Piveta, L., Noldin, J., Galon, L., and Concenço, G. 2014. Carryover effect of 1432

imidazolinone herbicides for crops following rice. American J of Plant Sci 5, 1049. 1433

1434

Sattin, M., Berto, D., Zanin, G., and Tabacchi, M. 1999. Resistance to ALS inhibitors in weeds 1435

of rice in north-western Italy. In "BRIGHTON CROP PROTECTION CONFERENCE 1436

WEEDS", Vol. 3, pp. 783-790. 1437

1438

Scarabel, L., Cenghialta, C., Manuello, D., and Sattin, M. 2012. Monitoring and management of 1439

imidazolinone-resistant red rice (Oryza sativa L., var. sylvatica) in Clearfield® Italian 1440

paddy rice. Agronomy 2, 371-383. 1441

1442

Seng, C. T., Van Lun, L., San, C. T., and SAHID, I. B. 2010. Initial report of glufosinate and 1443

paraquat multiple resistance that evolved in a biotype of goosegrass (Eleusine indica) in 1444

Malaysia. Weed Biol. Manag 10, 229-233. 1445

1446

Shaifuddin, S. N. M., Mazlan, A. Z., Hussain, H., Sameni, M., and Ishak, A. R. 2014. Analytical 1447

Method Development for Imazapyr and Imazapic Herbicides using High Performance 1448

Liquid Chromatography. 1449

1450

Page 52 of 70



Draft

53

Sharma, P. K., Ladha, J. K., and Bhushan, L. 2003. Soil physical effects of puddling in rice–1451

wheat cropping systems. Improving the Productivity and Sustainability of Rice–Wheat 1452

Systems: Issues and Impacts, 97-113. 1453

1454

Shaw, D. R., and Wixson, M. B. 1991. Postemergence combinations of imazaquin or 1455

imazethapyr with AC 263,222 for weed control in soybean (Glycine max). Weed Sci, 1456

644-649. 1457

1458

Shivrain, V., Burgos, N., Agrama, H., LAWTON‐RAUH, A., Lu, B., Sales, M., Boyett, V., 1459

Gealy, D., and Moldenhauer, K. 2010. Genetic diversity of weedy red rice (Oryza sativa) 1460

in Arkansas, USA. Weed Res. 50, 289-302. 1461

1462

Shivrain, V. K., Burgos, N. R., Anders, M. M., Rajguru, S. N., Moore, J., and Sales, M. A. 2007. 1463

Gene flow between Clearfield™ rice and red rice. Crop Prot 26, 349-356. 1464

1465

Shivrain, V. K., Burgos, N. R., Moldenhauer, K. A., Mcnew, R. W., and Baldwin, T. L. 2006. 1466

Characterization of spontaneous crosses between Clearfield Rice (Oryza sativa) and Red 1467

Rice (Oryza sativa) 1. Weed Technol. 20, 576-584. 1468

1469

Shivrain, V. K., Burgos, N. R., Sales, M. A., Mauromoustakos, A., Gealy, D. R., Smith, K. L., 1470

Black, H. L., and Jia, M. 2009. Factors affecting the outcrossing rate between 1471

Clearfield™ rice and red rice (Oryza sativa). Weed Sci. 57, 394-403. 1472

1473

Silva, D. R. O. d., Avila, L. A. d., Agostinetto, D., Dal Magro, T., Oliveira, E. d., Zanella, R., 1474

and Noldin, J. A. 2009. Pesticides monitoring in surface water of rice production areas in 1475

southern Brazil. Ciência Rural. 39, 2383-2389. 1476

1477

Singh, K., Kumar, V., Saharawat, Y., Gathala, M., Ladha, J., and Chauhan, B. 2013. Weedy rice: 1478

An emerging threat for direct-seeded rice production systems in India. 1479

1480

Singh, V., Singh, S., Black, H., Boyett, V., Basu, S., Gealy, D., Gbur, E., Pereira, A., Scott, R. 1481

C., and Caicedo, A. 2017a. Introgression of Clearfield™ rice crop traits into weedy red 1482

rice outcrosses. Field Crops Res. 207, 13-23. 1483

1484

Singh, V., Zhou, S., Ganie, Z., Valverde, B., Avila, L., Marchesan, E., Merotto, A., Zorrilla, G., 1485

Burgos, N., and Norsworthy, J. 2017b. Rice Production in the Americas. In "Rice 1486

Production Worldwide", pp. 137-168. Springer. 1487

1488

Siwar, C., Diana, N., Yasar, M., and Morshed, G. 2014. Issues and challenges facing rice 1489

production and food security in the granary areas in the East Coast Economic Region 1490

(ECER), Malaysia. Research Journal of Applied Sciences, Engineering and Technology 1491

7, 711-722. 1492

1493

Smith Jr, R., Talbert, R., and Baltazar, A. 1992. Control, biology and ecology of propanil-1494

tolerant barnyardgrass. Arkansas Rice Research Studies. University of Arkansas, 46-50. 1495

1496

Page 53 of 70



Draft

54

Solomon, W. L., Kanter, D. G., Walker, T. W., Baird III, G. E., Lanford, L. S., Shaifer, S., and 1497

Fitts, P. W. 2012. Registration of ‘CL162’long-grain rice. J of Plant Registrations. 6, 23-1498

26. 1499

1500

Somaratne, S., Karunarathna, K., Weerakoon, S., and Abeysekera, A. 2014. Salient characters of 1501

Weedy rice (Oryza sativa f. spontanea) populations in highly infested areas in Sri Lanka. 1502

RJS 5. 1503

1504

Sondhia, S. 2013. Evaluation of imazethapyr leaching in soil under natural rainfall conditions. 1505

Indian J of Wed Sci. 45, 58-61. 1506

1507

Sondhia, S., Khankhane, P. J., Singh, P. K., and Sharma, A. R. 2015. Determination of 1508

imazethapyr residues in soil and grains after its application to soybeans. Pestic Sci 40. 1509

1510

Song, D., Wu, G., Vrinten, P., and Qiu, X. 2017. Development of Imidazolinone Herbicide 1511

Tolerant Borage (Borago officinalis L.). Plant Sci. 1512

1513

Stewart, G., and Pittman, D. W. 1931. Twenty years of rotation and manuring experiments at 1514

Logan, Utah. 1515

1516

Sudianto, E., Beng-Kah, S., Ting-Xiang, N., Saldain, N. E., Scott, R. C., and Burgos, N. R. 2013. 1517

Clearfield® rice: Its development, success, and key challenges on a global perspective. 1518

Crop Prot 49, 40-51. 1519

1520

Sudianto, E., Neik, T.-X., Tam, S. M., Chuah, T.-S., Idris, A. A., Olsen, K. M., and Song, B.-K. 1521

2016. Morphology of Malaysian weedy rice (Oryza sativa): diversity, origin and 1522

implications for weed management. Weed Sci. 64, 501-512. 1523

1524

Sweeney, M., and McCouch, S. 2007. The complex history of the domestication of rice. Ann of 1525

Bot. 100, 951-957. 1526

1527

Süzer, S. and Büyük, H. 2010. Residual effects of spraying imidazolinone-family herbicides on 1528

Clearfield®* sunflower production from the point of view of crop rotation. HELIA. 52, 1529

p.p. 25-36. 1530

Tan, S., Evans, R. R., Dahmer, M. L., Singh, B. K., and Shaner, D. L. 2005. Imidazolinone‐1531

tolerant crops: history, current status and future. Pest Manag Sci. 61, 246-257. 1532

1533

Terano, R., Mohamed, Z., and Din, N. S. Z. 2016. Determinants of Farmers’ Adoption of 1534

Clearfield Production System in Malaysia. Agri and Agri Sci Procedia 9, 103-107. 1535

1536

Thanh, N. C., Chin, D., Tai, N. T., and Son, T. 1999. Study on the dormancy characteristic of 1537

five popular weedy rice varieties in the Mekong River Delta. OmonRice 7, 155-157. 1538

1539

Ulbrich, A. V., Souza, J. R. P., and Shaner, D. 2005. Persistence and Carryover Effect of 1540

Imazapic and Imazapyr in Brazilian Cropping Systems 1. Weed Technol. 19, 986-991. 1541

Page 54 of 70



Draft

55

1542

Van Chin, D., Thien, T. C., Bi, H. H., and Nhiem, N. T. 2007. Study on weed and weedy rice 1543

control by imidazolinone herbicides in clearfield TM paddy grown by imi-tolerance 1544

indica rice variety. 1545

1546

Wahab, A., and Suhaimi, O. 1991. Padi angin characteristics, adverse effects and methods of its 1547

eradication. Teknologi Padi. 7, 21-31. 1548

1549

Wang, F., Yuan, Q. H., Shi, L., Qian, Q., Liu, W. G., Kuang, B. G., Zeng, D. L., Liao, Y. L., 1550

Cao, B., and Jia, S. R. 2006. A large‐scale field study of transgene flow from cultivated 1551

rice (Oryza sativa) to common wild rice (O. rufipogon) and barnyard grass (Echinochloa 1552

crusgalli). Plant Biotech J. 4, 667-676. 1553

1554

Watanabe, H., Man, A., and Ismail, M. Z. 1996. Ecology of major weeds and their control in 1555

direct seeding rice culture of Malaysia. Japan International Research Center for 1556

Agricultural Science, Malaysian Agricultural Research and Development Institute, Muda 1557

Agricultural Development Authority. 1558

1559

Webster, E. P., Bryant, K. J., and Earnest, L. D. 1999. Weed control and economics in 1560

nontransgenic and glyphosate-resistant soybean (Glycine max). Weed Technol, 586-593. 1561

1562

Webster, E. P. a. J. A. M. 2001. acetolactate synthysase-inhibiting herbicide on imidazolinone 1563

tolerant rice. Weed sci. 49, 652-657. 1564

1565

Wersal, R. M., and Madsen, J. D. 2007. Comparison of imazapyr and imazamox for control of 1566

parrotfeather (Myriophyllum aquaticum (Vell.) Verdc.). J. Aquat. Plant Manage. 45, 132-1567

136. 1568

1569

Wilcut, J. W., Richburg III, J. S., Eastin, E. F., Wiley, G. R., Walls Jr, F. R., and Newell, S. 1570

1994. Imazethapyr and paraquat systems for weed management in peanut (Arachis 1571

hypogaea). Weed Sci, 601-607. 1572

1573

Ye, H., Feng, J., Zhang, L., Zhang, J., Mispan, M. S., Cao, Z., Beighley, D. H., Yang, J., and Gu, 1574

X.-Y. 2015. Map-based cloning of seed dormancy1-2 identified a gibberellin synthesis 1575

gene regulating the development of endosperm-imposed dormancy in rice. Plant physio 1576

169, 2152-2165. 1577

1578

Yu, Q., Cairns, A., and Powles, S. 2007. Glyphosate, paraquat and ACCase multiple herbicide 1579

resistance evolved in a Lolium rigidum biotype. Planta 225, 499-513. 1580

1581

Zhang, N., Linscombe, S., and Oard, J. 2003. Out-crossing frequency and genetic analysis of 1582

hybrids between transgenic glufosinate herbicide-resistant rice and the weed, red rice. 1583

Euphytica 130, 35-45. 1584

1585

Zhang, W., Webster, E. P., and Selim, H. M. 2001. Effect of Soil Moisture on Efficacy of 1586

Imazethapyr in Greenhouse 1. Weed technol. 15, 355-359. 1587

Page 55 of 70



Draft

56

1588

Zhang, W., Linscombe, S.D., Webster, E., Tan, S., & Oard, J. (2006). Risk assessment of the 1589

transfer of imazethapyr herbicide tolerance from clearfield rice to red rice (oryza sativa). 1590

Euphytica, 152(1), 75-86. 1591

Ziska, L. H., Gealy, D. R., Burgos, N., Caicedo, A. L., Gressel, J., Lawton-Rauh, A. L., Avila, L. 1592

A., Theisen, G., Norsworthy, J., and Ferrero, A. 2015. Chapter three-weedy (red) rice: an 1593

emerging constraint to global rice production. Adv Agron. 129, 181-228. 1594

1595

Ziska, L. H., Gealy, D. R., Tomecek, M. B., Jackson, A. K., and Black, H. L. 2012. Recent and 1596

projected increases in atmospheric CO 2 concentration can enhance gene flow between 1597

wild and genetically altered rice (Oryza sativa). Plo one 7, e37522. 1598

1599

1600

1601

1602

1603

1604

1605

1606

1607

1608

1609

1610

1611

1612

1613

1614

1615

1616

Page 56 of 70



Draft

57

Figures legends

Figure 1.

a) Arrows represent seeds enter the seedbank after shattering due to deep tillage.

b) Arrow represents seeds remain on soil surface after shattering.

c) Arrows represent seeds may be go death, or remaining dormant.

d) Arrows represent seeds break dormancy and germinate again.

m) Arrows represent seeds repeat the cycle continuously.

Figure 2.

• Black triangular represent factors increase seed bank size

• Gray triangular represent factors shift down seed bank size.

• White triangular represent seed bank size.

Figure 5.

A) White squares: represent the others related factors affect IWMS

B) Gray circles represent the main sectors of IMWS.

C) Black square: represent the main Approach IWMS.

Page 57 of 70



Draft

58

Page 58 of 70



Draft

Figure 1. Fate of weedy rice and movement of seeds in seedbank.

a) Arrows represent seeds enter the seedbank after shattering due to deep tillage.

b) Arrow represents seeds remain on soil surface after shattering.

c) Arrows represent seeds may be go death, or remaining dormant.

d) Arrows represent seeds break dormancy and germinate again.

m) Arrows represent seeds repeat the cycle continuously.

Page 59 of 70



Draft

Figure 2. The factors that affect seedbank size in the fields crop.

• Black triangular represent factors increase seed bank size

• Gray triangular represent factors shift down seed bank size.

• White triangular represent seed bank size.

Page 60 of 70



Draft

Figure. 3 series of event of impact of paraquat to humans and environment.

Page 61 of 70



Draft

Figure. 4 Effect of IMI- herbicides residues on potato. (James et al. 1996)

Page 62 of 70



Draft

�

�

�

� Figure 5. Integrated Weeds Management Strategy.

A) Black square: represent the main Approach IWMS.

B) White squares: represent the others related factors affect IWMS

C) Gray circles represent the main sectors of IMWS.

�

Page 63 of 70



Draft

Tables

Table 1. Weed rice first reported in rice production in some countries.

Table 2. The percentage of yield loss due to weedy rice infestation in rice crop globally.

Country Yield loss References

South Korea 5-10% (Kim and Ha 2005)

Worldwide 9-10% (Hakim et al. 2013)

Malaysia 10-42% (Karim et al. 2004)

Philippine 57-61% (Mukherjee et al. 2008)

India 30-90% (Mukhopadhyay 1995)

USA 30-85% (Mukhopadhyay 1995)

Worldwide 5-100% (Mortimer et al. 1992)

Country Year References

US 1846 (Olsen et al. 2007)

Sir Lanka 1990 (Somaratne et al. 2014)

Philippine 1990 (Chauhan and Johnson 2010)

Vietnam 1994 (Chauhan and Johnson 2010)

European

countries

1970 (Tarditi and Verseci 1993)

China 1960 (Gressel and Valverde 2009)

Page 64 of 70



Draft

Table 3. Synergism method efficiency by IMI herbicides application effect on the targeted

weeds.

Imidazolinone

effect

Types of application and

modification Targeted weeds References

a High control

Imazethapyr + propanil +

pendimethalin

Imazethapyr +

nicosulfuron /imazaquin +

imazapyr

Barnyard grass

Barnyard grass

(Kumar et al.

2008)

(Klingman et al.

1992; Masson and

Webster 2001;

Webster 2001)

Imazapic + imazapyr

Imazapic + atrazine

Red rice; weeds in barley

and ryegrass; smooth

brome; Kentucky bluegrass

Texas atrazine

(Webster et al.

1999); (Alister and

Kogan 2005).

(Bahm et al. 2011)

(Ducar et al. 2004)

b Medium control

Imazethapyr + quinclorac

Imazethapyr +

bentazone+aciflurfen

Broad leaf, signal grass

Barnyard grass

(Jason K and

Norsworthy 2011;

Klingman et al.

1992; Pellerin et al.

2004; Webster

2001)

Imazethapyr +

pendimethalin +

metolachlor

Barnyard grass (Arnold et al.

1993)

Imazapic + clethodim Crabgrass (Burke et al. 2004)

Page 65 of 70



Draft

a) High control: IMI has high efficiency control in this mixing procedures

b) Medium control: IMI has medium efficiency control in this mixing procedures

c) Minimal control: IMI has low efficiency control in this mixing procedures

Imazapyr + imazamox

Imazethapyr + metochlor

Myosoton. aquaticum

Yellow and Purple

nutsedge

(Wersal and

Madsen 2007).

(Grichar et al.

1992).

c Minimal control

imazethapyr + paraquat.

Bristly starbur, Prickly

sida, Small flower,

Nutsedge

(Richburg III et al.

1996).

imazethapyr + paraquat.

Sicklepod weeds (Wilcut et al. 1994)

Imazethapyr + propanil

Irwin and Barneby and

Flordia beggar weed

(Richburg III et al.

1995).

Propanil +Imazethapyr

Propanil +Imazethapyr

+Molinate

Imazethapyr

+Halosulfuron,

Imazethapyr

+Carfentrazone.

Indian jointvetch

Sesbania

exaltata and Aeschynomena

indica

(Masson and

Webster 2001)

(Zhang et al. 2001)

Page 66 of 70



Draft

Page 67 of 70



Draft

Table 4. Some weedy species have been evolved resistance to traditionary herbicides Worldwide.

Species Classification Life cycle Herbicide Country References

Fimbristylis miliacea Cyperaceae Annual 2,4-D Malaysia (Watanabe et al. 1996)

Sagittaria montevidensis Alismataceae Perennial Bensulfuron Australia (Graham et al. 1994)

Echinochloa crus-galli Poaceae Annual Propanil USA (Smith Jr et al. 1992)

Monochoria korsakowii Pontederiaceae Annual Sulfonylureas Japan (Kohara 1996)

Limnocharis flava Butomaceae Perennial 2,4-D Indonesia (Heap 2014)

Scirpus mucronatus, Cyperaceae Perennial Bensulfuron cinosulfuron Italy (Sattin et al. 1999)

Page 68 of 70



Draft

Table 5. Gene flow percentage between rice cultivars and weedy rice

Country /study Gene flow References

US From 0.3% - < 1% (Zhang et al. 2003)

USA 1-52% (Langevin et al. 1990)

China 0´011 and 0´046 % (Chen et al. 2004)

Italy 0.05 to 0.53 percent (Lu and Snow 2005)

US 0.003% - 0.25% (Noldin et al. 2002)

Australia 0.006% - 0.036 (Messeguer et al. 2003)

- 0.04 - 0.08% (Rong et al. 2005)

Asia 0.00 to 0.5% (Chen et al. 2004)

Arkansas 0.01–0.2% (Shivrain et al. 2007)

Page 69 of 70



Draft

Table 6. Different studies about Imidazolinone residues in environment

Imidazolinone Samples Residues Country References

Imazapic and

Imazethapyr

Surface water 0.007 – 0.08

mg/L

Brazil (Silva et al. 2009)

Imazapyr Surface water 1µg/L USA (Shaifuddin et al. 2014)

Imazethapyr Soil and grains 0.001-0.0015

µg/g

India (Sondhia et al. 2015)

Imazethapyr Soybean oil 0.003 µg/ml India (Mastan et al. 2016)

Imazethapyr Food 0.01-0.02 µg/g Japan (Akiyama et al. 2009)

Imidazolinone

water and soil 0.1-0.05 ng/g Italy (Laganà et al. 1998)

Table 7. Imidazolinone herbicides movement and leaching depth in various studies.

Imidazolinone type Field samples Leaching depth References

Imazethapyr Soil Below 25cm (Sondhia et al. 2015)

Imazapic, Imazapyr and

Imazethapyr

Soil Up to 25cm (Refatti et al. 2017)

Imazapic and Imazapyr Soil Up to 25cm (Neto et al. 2017)

Imazapyr Soil Up to 10cm (Börjesson et al. 2004a)

Imazethapyr Soil Up to 70cm (Sondhia 2013)

Page 70 of 70



system appendpdf cover-forpdf - university of toronto t-space...49 imi herbicides, and diverse...

Documents