Herbicide resistance, the evolved capacity of a previously herbicide-susceptible weed population to withstand a herbicide and complete its life cycle when the herbicide is used at its normal dose in an agricultural situation, has increased steadily over the past several years (Heap and LeBaron, 2001). Although the great majority of cases of herbicide resistance have occurred in the developed world, several important weeds have evolved resistance in developing countries having an important economic impact on specific crops. This short review focuses on the management of herbicide-resistant weeds in developing countries, therefore preference is given to cases evolved and practices suitable for coping with herbicide resistance in these countries.
Worldwide herbicides represented 47 percent of the ca US$28 billion agrochemical sales in 2001 (Agrow, 2002a). The developed economies (North America, Europe and Japan) account for approximately 70 percent of the global agrochemical market (Bryant, 1999). Sales in Latin America, which exhibited the largest increases in 1996 (Agrow, 1996, 1997a) were down by almost 8 percent (to US$3.5 billion) mostly because of the collapse of the economy in Argentina and exchange rate fluctuations in Brazil (Agrow, 2002a). Despite a 3 percent sales increase in 2000, the Japanese pesticide market resumed its downward trend in 2001 as a result of reduced rice plantings, price pressure and low insect outbreaks (Agrow, 2002a). In 2001, the leading seven agrochemical companies (Syngenta, Monsanto, Aventis, BASF, Dow AgroSciences, DuPont and Bayer) reported sales of about US$22 billion ((Agrow, 2002a). The most widely- used herbicide in the world is glyphosate (Woodburn, 2000), which accounts for about 11 percent of the total value of the agrochemical market (Agrow, 2002b). Glyphosate represents 67 percent of the US$3.9 billion agrochemical market share of Monsanto (Agrow 2001). There are also several companies worldwide producing generic glyphosate, many of them based in developing countries (Woodburn, 2000). Other widely used compounds are paraquat, considered the second largest-selling agrochemical, triazines and metolachlor. In developing countries, paraquat continues to be one of the herbicides of preference.
RESISTANCE CASES IN DEVELOPING COUNTRIES
The first case of herbicide resistance (to 2,4-D) was reported by Hilton (1957) but weed resistance to herbicides began to receive recognition only after the first case of triazine resistance in Senecio vulgaris was reported by Ryan (1970). For several years, resistance to triazines was most prominent. There are 64 species that have evolved resistance to triazines and other Photosystem II inhibitors (Heap, 2002). In contrast, only four species have been confirmed resistant to glyphosate even though this herbicide has been widely used for more than 25 years. Currently and worldwide, there are 261 confirmed resistant biotypes that belong to 157 species (95 dicotyledonous and 62 monocotyledonous) (Heap, 2002). Two modes of action (MOA) groups of more recent commercialization, those of herbicides that inhibit the enzyme acetolactate synthase (ALS), which include the sulfonylureas (SFU), imidazolinones, triazolopyrimidines, pyridinilbenzoates and sulfonylaminocarbonyltriazolinones, and the inhibitors of acetyl CoA carboxylase (ACCase) comprised by the aryloxyphenoxy propanoates and cyclohexanediones, have contributed to the aggravation of the herbicide resistance problem. There are 73 species (104 biotypes) resistant to ALS herbicides and 28 species (59 biotypes) resistant to ACCase herbicides (Heap, 2002).
Based on the database maintained by Heap (2002), developing countries contribute 22 percent of the herbicide resistance incidences (a total of 465 reported up to September, 2002). There are differences in the relative distribution of resistance cases based on MOA between developed and developing countries (Figure 1). The three most important groups (Triazine, ALS and ACCase herbicides) account for 74 percent and 65 percent of resistance cases in developed and developing countries, respectively. In both groups of countries, resistance to triazines remains most frequent (on a per-biotype basis), but in the developed world ALS resistance is proportionally twice as frequent as ACCase resistance. In developing countries, frequency of resistance cases to these two MOAs is practically identical. Bipyridilium, auxinic and urea/amide herbicides in proportion also contribute more resistance cases in developing countries than in industrial ones. A possible explanation for this is the relatively higher use of the herbicides paraquat, 2,4-D and propanil in developing countries.
EVOLUTION OF RESISTANT WEEDS
Weed populations become resistant because of the interaction of a few key factors. Plants, in general, and particularly weeds, are variable. The genes conferring resistance are present naturally in wild populations; resistance mutations are thought not to be induced by the herbicide (Jasieniuk et al. 1996). But these genes occur in wild populations at a very low frequency because, in absence of the herbicide, they practically do not confer any adaptive advantage to those plants. The frequency of these resistance genes, however, is important in determining how long it would take for resistance to become noticeable once we start relying on a particular herbicide. For example, the rapid increase in resistance to ALS herbicides is attributed in part to the high mutation frequency in the target site enzyme and the existence of several mutations that can confer resistance (Chaleff and Day, 1984, Devine and Preston, 2000). Preston and Powles (2002) determined the frequency of individuals resistant to ALS-inhibiting herbicides in populations of Lolium rigidum never previously exposed to these herbicides. The frequency of individuals resistant to sulfometuron-methyl and imazapyr varied from 2.2 ×10-5 to 1.2 ×10-4 and from 1 ×10-5 to 5.8 × 10-5, respectively, depending on the population. These high frequency values help explain the rapid evolution of resistance once the populations are subjected to the selection imposed by the ALS-herbicides. Unfortunately, the frequency of resistant individuals in a weed population is not known before the introduction of a new herbicide with a novel MOA as baseline data are not required for product registration and seldom are generated for future monitoring purposes (Moss, 2001).
Figure 1. Distribution of cases of herbicide resistance in developing and developed countries according to mode of action. (Based on data compiled by Heap, 2002)
Two other important characteristics of a weed in terms of herbicide-resistance evolution are the size and viability of the soil seed bank and the weed fitness. The soil seed bank may act as a buffer, thus delaying the evolution of resistance. This is because over the years the soil seed bank has been enriched by the seed shed by the predominant susceptible individuals. In some cases, individuals carrying a mutation (such as those conferring resistance to herbicides) are penalized by being less adapted or less fit in absence of the herbicide. Reduced fitness is difficult to measure but it can be related to impaired efficiency of key physiological processes such as photosynthesis or whole plant characteristics such as decreased seed production or reduced competitive ability. Often resistant biotypes, however, are no less fit than the normal, susceptible ones.
The most significant factor that governs the evolution of herbicide resistance is the selection pressure imposed by the herbicide (Jasieniuk et al. 1996). Higher selection pressure is imposed when we use herbicides at high doses, highly effective and/or persistent compounds and when we spray them too frequently. As the mortality rate increases so does the selection pressure we impose with the herbicide. Thus resistant weed populations can be considered a case of rapid adaptive evolution (Reznick and Cameron, 2001). The independent evolution of resistance to a particular herbicide within a species across sites and times has been proposed as an example of recurrent evolution in response to the same selective force (the herbicide) across populations (Levin, 2001). Weed populations also respond to agricultural practices, including herbicides, by changes in their composition and abundance. Weed shifts are often associated with the continued use of a particular herbicide. Species that are naturally not affected by the herbicide become more prevalent (Hyvönen and Salonen, 2002), including those few that escape to non-selective herbicides such as glyphosate used in glyphosate-resistant crops, as documented in Argentina and in no-till production systems in Brazil (Merotto et al. 1999, Moreno 2001, Valverde 2002, Vita et al. 2001). These changes in the flora at a specific site should not be confused with herbicide-resistance evolution.
Several mechanisms confer resistance to herbicides. The most common and important are those related to target-site insensitivity and enhanced herbicide metabolism or breakdown to inactive products. Additionally, resistance can be attributed to herbicide sequestration (or avoidance owing to physical or temporal separation of the herbicide from sensitive tissues or target sites), and reduced uptake (Devine and Preston, 2000). The sequestration mechanism has mostly been proposed for cases of paraquat resistance. For example, a paraquat-resistant biotype of the annual Asteraceae weed Crassocephalum crepidioides, was found in 1990 in tomato fields near Tanah Rata, Malaysia, where paraquat had been applied twice a year for ten years (Ismail et al. 2001a). Physiological studies determined that paraquat was not metabolized in the leaf tissues of either the susceptible or resistant biotype. Plants of both biotypes absorbed paraquat similarly and resistance appeared to be endowed by a sequestration mechanism that renders the paraquat inactive (Ismail et al. 2001a). Recently, an additional mechanism previously identified in tissue culture selections, the overproduction of the target site, was proposed as the resistance mechanism to graminicides (ACCase inhibitors) in a johnsongrass (Sorghum halepense) biotype (Bradley et al. 2001).
There are cases in which more than one mechanism is involved in conferring resistance to herbicides in a single individual or a plant population (multiple resistance). It is also common that a weed that has evolved resistance to a specific herbicide also exhibits resistance to other herbicides in the same chemical or MOA family because they share the same binding site. Thus, a modification of this binding site results in target-site cross resistance. For example, populations of Ixophorus unisetus selected resistant by imazapyr (an ALS inhibitor) in Costa Rica were also cross-resistant to a group of imidazolinone and SFU herbicides (Chaves et al. 1997). When resistance is endowed by another mechanism such as enhanced degradation of the herbicide, cross-resistance to herbicides of unrelated MOA or chemistries can occur. For example, a population of Digitaria sanguinalis from Australia that was selected by, and resistant to, the ACCase herbicide fluazifop-p-butyl was found to be cross-resistant to the ALS- inhibitor imazethapyr, despite never being treated with any ALS-herbicide. Resistance to the ALS herbicide was not target-site based but was probably because of increased herbicide metabolism. But the enzyme responsible for fluazifop acid detoxification in D. sanguinalis is different from the enzyme that detoxifies imazethapyr (Hidayat and Preston, 2001). Most commonly, however, multiple resistance is conferred by the accumulation of two or more resistance mechanisms such as in populations of L. rigidum, Alopecurus myosuroides and Phalaris minor (Preston and Mallory-Smith 2001). Extreme cases do occur. A biotype of L. rigidum from Australia selected by the sustained use of a number of herbicides (diuron, chlorsulfuron and atrazine) and just two exposures to diclofop, exhibits (cross-) resistance to nine herbicide classes, representing five MOA categories (Burnet et al. 1994). Knowledge of both the MOA and the mechanism of resistance is important in designing and implementing herbicide prevention and management practices. Groupings of herbicides according to their MOA have been developed as a guidance in resistance management. The most well known are those of the Herbicide-Resistance Action Committee (HRAC) and the Weed Science Society of America (WSSA), (Retzinger and Mallory-Smith, 1997; Schmidt, 1997).
In Australia, where resistance problems are of the greatest magnitude, it is now mandatory for herbicide labels to carry a large letter identifying the herbicide MOA (Powles, 1997). Selection of herbicide products for mixtures, sequential applications or rotations is facilitated by easily identifying the mode-of-action class to which they belong.
HERBICIDE RESISTANCE PREVENTION AND MANAGEMENT
Herbicide resistance is an indication of overdependency of herbicides in a particular production system. Developing countries are not excluded from the current trend of herbicide dependence; these chemicals are widely used in highly sophisticated crop production systems as well as by poor resource farmers. Indeed some of the most troublesome cases of herbicide resistance in developing countries have occurred in areas and in crops where both large-scale commercial farms as well as small farmers have embraced a single herbicide or MOA as the main tool for eliminating a key weed. This is the case of propanil resistance in junglerice (Echinochloa colona) in Central America, Mexico and parts of South America (Valverde et al. 2000) and that of isoproturon resistance to graminicides in Phalaris minor in India (Malik and Singh, 1995). It is also the case of one of the few reported cases of resistance to glyphosate. Goosegrass (Eleusine indica) evolved resistance to glyphosate in several regions in the Malaysian Peninsular in orchards, vegetable areas, nurseries and oil palm plantations (Ismail et al. 2001b). At a guava farm in Teluk Intan, after failure of glyphosate to control goosegrass at the recommended dose of 540 g a.e. ha-1 (Lee and Ngim, 2000), experimental application of the herbicide at 4.32 kg a.e. ha-1only provided 25 percent control of the resistant biotype. Resistance evolved in a short period (about three years) of intensive glyphosate use (6-7 sprays per year at increasing doses). Other areas where resistance has been confirmed were exposed to more intense regimes (up to ten times per year for five years). Characterization of some biotypes indicates that at optimum temperature seeds of both resistant and susceptible biotypes germinate in the same manner, but the resistant biotypes appeared to be more vigorous and productive than the susceptible ones (Ismail et al. 2001b). The mechanism of resistance to glyphosate in goosegrass has recently been elucidated by the work of Baerson and co-workers (2002). Basal or glyphosate-induced activity levels of the enzyme targeted by glyphosate, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), between a resistant and a susceptible biotype were similar, indicating that resistance was not related to target enzyme overexpression in the resistant biotype. The two biotypes also contain identical EPSPS gene copy numbers. Resistance was confirmed to be the result of an altered EPSPS enzyme that exhibits reduced sensitivity to glyphosate. In the altered EPSPS, the amino acid proline is substituted by serine at position 106. This mechanism differs from that observed in a recently detected population of L. rigidum that also evolved resistance to glyphosate in Australia, in which an over-production of the EPSPS enzyme was associated with the observed resistance (Gruys et al. 1999).
Most herbicide-resistance management practices discussed here refer to arable cropping systems and preference has been given to examples from developing countries to illustrate their development and implementation. There are, however, cases of resistance in plantation crops and pastures which may deserve adapting specific practices to cope with herbicide resistance. An in-depth compilation of herbicide resistance management practices in world grain crops has recently become available (Powles and Shaner, 2001).
Prevention of herbicide resistance
In geographical areas or specific farms where herbicide resistance has not yet appeared, efforts should be made to integrate weed control tactics that would avoid or delay the selection of resistant populations. Since selection pressure is the driving force for resistance evolution, tactics that decrease the selection pressure imposed on the population should be implemented. Herbicide dose, efficacy and frequency of application largely determine selection pressure. Monoculture, intensive herbicide use having the same MOA and reduced cultivation often characterize systems where resistance has evolved (Mortensen et al. 2000). Highly effective herbicides, used persistently, impose a high selection pressure that can result in herbicide-resistant populations evolving in just a few generations. This has been well documented in developing countries with the ALS and ACCase herbicides that are considered especially prone for resistance evolution. Repeated herbicide application in the same cropping season increases selection pressure, especially if a weed germinates and emerges in different flushes and completes more than one generation per season. Such herbicide regimes are responsible for propanil resistance in E. colona in Central America (Valverde et al. 2000) and for cases of paraquat resistance in Malaysia (Itoh et al. 1992), two contact herbicides with no soil persistence.
If farmers have to rely on herbicides to control weeds, a useful approach to delay or prevent herbicide resistance is to use mixtures or to rotate herbicides. Conventionally, herbicides are combined with the aim of broadening the weed control spectrum, often lowering the doses of the products in mixture. For resistance management, however, there are other requirements: both herbicides in the mixture must be at full dose and effective on the target weed species, and possess similar persistence but different mechanisms of action and/or degradation pathways in the plant (Wrubel and Gressel, 1994). Many rice farmers in Central America combine propanil with pendimethalin for E. colona control. Pendimethalin is an excellent partner for propanil in resistance prevention since it meets most of these requirements. Thus resistance to propanil has been delayed or has not occurred in rice fields where propanil is regularly mixed with pendimethalin, a herbicide also useful as an alternative product when propanil resistance has already evolved (Garita et al. 1995; Garro et al. 1991; Riches et al. 1996, 1997).
By the same rationale, herbicide rotation helps in delaying the selection of herbicide-resistant populations. According to model predictions with regard to two herbicides which have different MOA but are equally effective against a target weed, mixtures are better than yearly rotations in delaying the appearance of herbicide resistance (Powles et al. 1997). In developing countries and especially with generic herbicides, it is common to find a variety of commercial products that contain the same active ingredient. Farmers not properly advised sometimes rotate with or even tank-mix formulated products containing the same active ingredient, but sold under a different brand name. Farmers are also frequently misled by the introduction of new products that are no more than members of the same chemical or MOA group.
Use of certified seed, weed-free seeds and avoidance of contaminated farm equipment should help in preventing the introduction of resistant material to new areas or fields. Unfortunately, seed-saving from previous harvests is common in many developing countries. In Vietnam, for example, less than 5 percent of the total rice seed used by farmers is certified and the self-supplied seed is of poor quality and heavily contaminated with weed seeds (Chin, 2001). Dispersal of herbicide resistant weeds through contaminated crop seed is poorly documented although there are cases suggesting such a movement (Thill and Mallory-Smith, 1997). The importance of thorough machinery-cleaning in preventing the spread of resistant weeds was illustrated by Itoh et al. (1997a, 1997b). A farmer in Japan selected a resistant population of Lindernia dubia var. major after five years of using bensulfuron plus mefenacet in a rice field. Movement of farm machinery (transplanting tools and a combine harvester) infested a completely separated uproad field with resistant individuals in a pattern, following the movement of equipment from the field entrance onwards.
Weed seeds are characterized for having adaptations to facilitate their dispersal and generally there are no differences in seed size or weight between those produced by resistant and susceptible plants. Thus weed seeds of resistant biotypes can naturally travel short and long distances aided by these adaptations and the corresponding disseminating agents. For example, it has been suggested that migratory birds may have played an important role in spreading seeds of Solanum nigrum resistant to triazines in Europe (Stankiewicz et al. 2001). Russian thistle (Salsola iberica) is a very prolific plant adapted for wind dispersal. Mature plants break from the soil and tumble with the wind, shedding their seed along their path of travel. SFU-resistant Russian thistle plants infest new areas over entire regions in this manner (Stallins et al. 1994).
While problem weeds in general, and herbicide resistant ones in particular, can be dispersed, it is important to emphasize that selection pressure is the main driving force in the appearance of resistant populations at a farm or specific field. Indeed, studies using molecular markers in Lindernia micrantha established that resistance to ALS-herbicides evolved as multiple events and that it was not the result of a founder population being spread over several locations, either pollen or plant introductions in contaminated equipment (Shibaike et al. 1999).
Managing weed populations already resistant to herbicides
The most common situation faced by the farmer is to control weeds that already have become resistant to herbicides. Although the immediate response is to switch to a different herbicide still active on the weed population, long-lasting management of resistance can only be achieved by integration of appropriate tactics based on an adequate knowledge of the biology and ecology of the weed and of the herbicide MOA and resistance mechanism. Very seldom is information complete in all these respects, especially for developing-country agricultural systems. But understanding the fundamentals of herbicide resistance evolution, benefiting from the experience gained elsewhere with similar cases and returning to good agricultural husbandry allows for the design and implementation of suitable management programs.
Several agronomic tactics can help in limiting the local spread, density increase and impact of resistant populations. It should be emphasized that management practices should be directed to decreasing the proportion of seed of resistant individuals in the soil seed bank, especially for those species whose seed has limited longevity and soil persistence. Thus practices that prevent seed setting and shedding by plants that have survived all control practices during the cropping cycle would help in the decline of infestations with resistant individuals. In Australia, for example, some farmers use special attachments or have modified their harvesters to retain seeds of L. rigidum at harvest, a practice valued as an important component for managing populations that exhibit multiple resistance (Powles 1997, Gill and Holmes, 1997). Stubble-burning or incorporation can also destroy weed seeds or prevent seed production of plants that are still maturing at crop harvest. In Taiwan and China, farmers burn rice straw after harvest to control remnant weeds and to prevent the buildup of soil seed banks (De Datta and Baltazar, 1996). Stubble incorporation, however, had no effect on E. colona density in the following cropping season or within the span of a series of field trials conducted for up to three years in Costa Rica (Valverde et al. 2001a). To decrease the seed set of L. rigidum in Australia, some farmers also spray paraquat at low doses very late in the growing season, a practice called crop topping (Powles, 1997).
Soil preparation affects weed seed dynamics and seedling densities at planting and thus can contribute to manage herbicide resistant populations (Buhler et al 1997). Success of an annual weed is largely dependent on time of emergence, which determines whether a plant competes successfully with its neighbours, is consumed by herbivores, infected with diseases, and whether it flowers, reproduces, and matures properly by the end of the growing season (Forcella et al. 2000). Tillage systems affect weed emergence by modifying the composition, vertical distribution and density of weed seed banks. Weed species whose seeds can germinate at or near the soil surface and become established have the greatest potential to proliferate under conservation tillage systems (Buhler et al 1997).
In conventional tillage, disking or ploughing at intervals before crop sowing achieves control of initial weed populations that otherwise would emerge with the seeded crop. A three-week delay in wheat sowing enables control of multiple-resistant L. rigidum by non-selective herbicides still effective on the weed or by cultivation before seeding. This practice, however, may be limited by the shortening of the season available for crop growth, which reduces the yield potential of the crop (Gill and Holmes, 1997). Delayed planting to allow weeds to emerge and be eliminated with herbicides is widely used in some Latin American countries for weedy rice (Oryza spp.) and E. colona management, especially in rainfed rice (Fischer, 1996) and has proven useful for controlling propanil-resistant E. colona (Valverde et al. 2001a). In Italy, resistance to ALS herbicides was not observed in rice fields where contamination with red rice forced farmers to use stale seed bed preparation and to apply oxadiazon before planting (Sattin et al. 1999).
If resistant and susceptible weeds have differential emergence patterns in the field because of differences in seed dormancy, control tactics can be adapted to eliminate most of the resistant individuals before the crop is planted (Dyer et al. 1993, Alcocer-Ruthking et al. 1992). Seeds of SFU-resistant kochia (Kochia scoparia) germinate earlier than those of susceptible plants making it possible to control them mechanically or with a herbicide having a different MOA before planting a crop such as wheat (Thompson et al. 1994). Similarly, Solanum nigrum seedlings resistant to triazine herbicides emerged faster and in greater proportion than triazine-susceptible seedlings, because of the interaction between soil temperature and differential minimum germination requirements of seeds between the biotypes (Kremer and Lotz, 1998).
Crops usually have a typical weed flora associated with them. Thus, crop rotation modifies the species composition of weed communities (Hyvönen and Salonen, 2002). Intensive production in monoculture selects for weed floras highly compatible with the particular agricultural system; these weeds usually are also very competitive and hard to kill. Crop rotations brings about changes in planting patters, tillage practices, life cycles, competitive characteristics, and weed management that disrupt regeneration niches of weed species and prevents the buildup of those highly adapted (Buhler, 2002). In India, where the rice-wheat sequence was interrupted by the rotation with other crops, the incidence of isoproturon-resistant P. minor was substantially lower (Malik and Singh, 1995). A. myosuroides is an annual grass weed that has evolved resistance to several herbicides in Europe (Heap, 2002). A recent study in France (Chauvel et al. 2001) evaluated the effect of selected management practices, including crop rotation, on an A. myosuroides population resistant to both fenoxaprop and clodinafop. This population exhibited cross-resistance to the SFU-herbicide flupyrsulfuron, which had never been used in that field. The percentage of the ACCase-resistant plants did not change during the three-year rotation even though herbicides with this MOA were not used, probably because the resistant plants do not carry a fitness penalty compared to the susceptible ones. Crop rotation, however, decreased blackgrass density, especially when spring crops were introduced into the rotation scheme.
Crop competitive advantage
There are additional agronomic practices that can provide competitive advantage to the crop, reducing the impact of the weeds associated with them and decreasing the need for chemical control. Increased attention is being paid to breeding and identifying crop varieties with ability to suppress weeds, especially in grain crops such as wheat and rice (Coleman et al 2001, Fasoula and Fasoula, 1997). Crop varieties should be evaluated according to the local cropping systems and their problem weeds. Lemerle et al. (2001) found minimal competitive grain-yield advantage of wheat varieties growing with L. rigidum in Australia making it necessary to develop other tactics to increase the competitiveness of the crop. Garriti et al. (1992) evaluated 25 rice cultivars for their competitive ability against weeds under low- and high-weed densities. Tall cultivars suppressed weeds better, compared with intermediate and semi-dwarf cultivars. The most competitive cultivar suppressed weed dry weight by up to 75 percent. Tall cultivars, however, are more susceptible to lodging, have a lower tillering capacity and a relatively large leaf area index that results in mutual shading of the leaves. In Colombia, Fischer et al. (1997) found a rice cultivar, which, under severe weed pressure, produced sufficient grain and was able to suppress E. colona. Competitiveness of the rice cultivars tested was correlated with increased leaf area index, tiller number and canopy light interception. An important body of literature and practical experience has also been gained in identifying traits and testing rice cultivars that are allelopathic to weeds (see Olofsdotter et al. 2002).
The competitive advantage of the crop can also be increased by increasing its density. In Australia, as a result of heavy infestations with herbicide resistant L. rigidum, farmers have widely adopted the practice of increasing wheat seeding rates by 20-40 percent to suppress the weed (Powles, 1997). Rates should be adjusted according to the prevalent competitive weed to be suppressed. Higher wheat densities supplemented by selective herbicides were required to control Avena ludoviciana than to control Phalaris paradoxa (Walker et al. 2002).
Rice, with its unique cropping systems, offers additional alternatives to make the crop more competitive. These include transplanting, puddling the soil and management of the water table in flooded or irridated rice (Valverde and Itoh, 2001). Other practices that influence weed flora composition and herbicide load are intercropping and the use of cover crops.
Alternative chemical control
Once resistance to a herbicide has become evident to the farmer, usually after a re-application of the same product at a maximum dose fails again to control the weed, the typical solution is to switch to another herbicide. Selection of alternative herbicides must be judicious since it has been already proven that herbicide use patterns have been such that resistance has evolved. To the surprise of farmers and advisors, sometimes the selected resistant population also result resistant to a herbicide that has not been applied before or that has been used to a very limited extent. In addition to previous examples, other cases are illustrative. Some populations of A. myosuroides are resistant to the PS II herbicide chlortoluron because of enhanced mixed function oxydase activity that results in rapid metabolism of both chlortoluron and pendimethalin (James et al. 1995). Thus, for this population, pendimethalin is not a viable alternative herbicide. In a few cases, to the surprise of scientists, farmers continue using the same herbicide to which the key weed in the production system has become resistant. This occurs when the herbicide still controls other important weeds and is very inexpensive. Such is the case of the continued use of bensulfuron in rice in California and Australia, where important weeds evolved resistance to this ALS-herbicide (Valverde and Itoh 2001). Similarly, in Costa Rica, some farmers continue using propanil, despite having selected propanil-resistant junglerice, as propanil still selectively controls several dicotyledonous weeds (Valverde et al. 2000).
An example of the use of herbicides with alternative MOAs to cope with a resistance problem in developing countries is illustrated by the management of resistant broadleaf weeds in soybean in Brazil and Argentina, which are the second and third largest soybean producers in the world, respectively. According to FAO statistics, in 2001 Brazil planted 13.9 million ha and Argentina, 10.3 million ha. For the year 2002, the area planted in Brazil increased by an estimated 16 percent to a total of 16.3 million ha (CONAB 2002). In Brazil, the most important producer- states are located in the south and midwest of the country. Paraná and Rio Grande do Sul in the south and Mato Grosso in the midwest plant more that 3 million ha each. The other two major producers, both in the midwest, are Goiás and Mato Grosso do Sul. No transgenic, herbicide-resistant soybean is planted legally in Brazil. On the other hand, Argentina plants glyphosate-resistant varieties almost entirely (James, 2001). The main soybean-producing provinces in Argentina are Cordoba, Santa Fe and Buenos Aires. In Argentina, of the US$600 million agrochemicals market in 2001, two-thirds corresponded to herbicides. As expected, glyphosate was the most widely used herbicide but no cases of resistance to this herbicide have been reported in Argentina yet.
Three broadleaf weeds (Bidens pilosa, Bidens subalternans and Euphorbia heterophylla) have evolved resistance to ALS herbicides in Brazil. Amaranthus quitensis also became resistant to this group of herbicides in the provinces of Cordoba and Tucuman in Argentina. In addition, in Brazil, Brachiaria plantaginea was confirmed as resistant to ACCase herbicides (Christoffoleti et al. 2001, Gazziero et al. 2000, Vidal and Fleck 1997), resistance apparently being endowed by a target-site mutation (Cortez et al. 2000). Several studies have been conducted to understand the nature of resistance, determine cross-resistance patterns and elucidate the resistance mechanism. These studies compare biotypes suspected or known to be resistant to ALS herbicides from different locations, all selected by imazethapyr and chlorimuron ethyl or both, to a respective susceptible one. Patterns of cross-resistance appear to be quite consistent among biotypes.
Initial reports stated that B. pilosa had become resistant to ALS inhibitors (Ponchio et al. 1997) but later it was confirmed that this species grows in very close relation to B. subalternans. Thus both species are now confirmed resistant to ALS herbicides (Gelmini et al. 2001, Christoffoleti 2002). A B. pilosa biotype from Mato Grosso do Sul, field-treated with ALS herbicides for at least eight years, exhibits resistance indices, RI (based on whole plant bioassays) of 40 for chlorimuron-ethyl, 60 for metsulfuron-methyl and imazethapyr, and 175 for nicosulfuron (Christoffoleti, 2002). The RI is calculated as the ratio between the herbicide doses that inhibits growth by 50 percent (GR50) in the population of interest over the GR50 value of the susceptible, reference population. This cross-resistance pattern is widely documented for both Bidens spp. (Gelmini et al. 2002, Monqueiro et al. 2000, Monqueiro and Christoffoleti 2001b). Under Brazilian conditions, the seed of B. pilosa survives in the soil for 3-4 years (Voll et al. 2001). In a seed burial experiment, it was also demonstrated that germination and decay of B. pilosa seeds was more intense on the soil surface. About 80 percent of the seed on the soil surface was lost as a result of germination and decay within the first two months (rainy season); the remaining 20 percent maintained its viability until experiment completion (one year). When buried at 10 cm, seed losses were about 50 percent (Carmona and Villas-Bôas, 2001). Thus, the use of pre-emergence and early-post emergence herbicides in no-till soybean production systems could rapidly decrease the soil seed bank and help to control the build up of ALS- resistant populations. Resistant biotypes of these species can be controlled with lactofen, fomesafen, bentazon, glufosinate and glyphosate (Christoffoleti, 2002, Gelmini et al. 2002). A susceptible and ALS-resistant biotype of B. pilosa showed similar growth as individuals in a pot study (Christoffoleti, 2001).
Tuesca and Nisensohn, (2001) evaluated the response to herbicides of three populations of A. quitensis from no-till agricultural systems in Argentina that were allegedly resistant to ALS-herbicides. Two of these populations came from fields where imazethapyr had been used in soybeans for the past 4-5 years; the third population came from a field where imazethapyr had been rotated with nicosulfuron (in maize) and chlorimuron-ethyl during the same period. The reference, susceptible population was collected in a field where conventional tillage was practised and soybean was rotated with maize, being exposed to an ALS-herbicide (imazethapyr) only once, five years before the seed was collected. The two populations selected by imazethapyr were resistant to this herbicide but not to chlorimuron-ethyl. The population exposed to both the imidazolinone and SFU herbicides was resistant to both imazethapyr and chlorimuron-ethyl. Mortality of the susceptible biotype was 95 percent at half the recommended dose of either herbicide and total at the full commercial dose. Lactofen, fomesafen and bentazon controlled ALS-resistant A. quitensis (Monqueiro and Christoffoleti 2001b). Resistance to ALS herbicides in Bidens spp. and in A. quitensis is conferred by an insensitive target enzyme (Monqueiro and Christoffoleti, 2001a).
E. heterophylla resistant to ALS-herbicides has also been confirmed in soybean fields in the states of Paraná, Rio Grande do Sul, Sao Paulo and, indirectly in an efficacy field study, in Mato Grosso do Sul (Gazziero et al. 1998, Vidal and Merotto, Jr. 1999, Oliveira et al. 2002, Gelmini et al. 2001, Melhorança and Pereira, 2000). Resistant populations tested so far are susceptible to other soybean herbicides having different MOA (Gazziero et al. 1998, Vidal and Merotto Jr. 1999). Thus a population of this species collected in the irrigated soybean area of Sao Paulo state that was resistant to both chlorimuron-ethyl and imazethapyr (RI > 20 for both herbicides) was effectively controlled by the pre-emergence Protox-herbicides, fomesafen, lactofen and flumiclorac-pentyl, and by glufosinate and glyphosate (Gelmini et al. 2001). Other herbicides that control ALS-resistant E. heterophylla are sulfentrazone, auxinic herbicides, and paraquat (Gazziero et al. 1998, Vidal and Merotto, Jr. 1999). No differential growth of individual plants has been observed between resistant and susceptible plants, including their seed production (Vidal and Trezzi, 2000, Brighenti et al. 2001, Santos et al. 2002). Resistance is conferred by an altered ALS enzyme (Oliveira et al. 2002) and inherited as a single, dominant gene (Vargas et al. 2001).
Thus, there are several chemical options to deal with ALS-resistant weeds. According to local recommendations (EMBRAPA, 2000) cultivation is carried out up to three times during the cropping cycle, but before flowering. Application of herbicides is the most widely-used control method. In no-till soybean production, recommended herbicides before planting are paraquat, 2,4-D, a formulated mixture of paraquat plus diuron, and glyphosate or sulfosate. Chlorimuron-ethyl is also recommended to control Raphanus sativum, Senecio brasilienses, and Bidens pilosa where resistance has not occurred. Several herbicides are available for pre-plant (PRE) or post-emergence (POST), in-crop control, many of them effective on ALS-herbicide resistant species. These include Protox POST herbicides, acifluorfen-sodium, fomesafen, lactofen, and the PRE sulfentrazone; the PRE inhibitors of the synthesis of very long chain fatty acids, alachlor and metolachlor; the PS-II herbicides, bentazon (POST), cyanazine (PRE), linuron (PRE), metribuzin (pre-plant incorporated (PPI) or PRE); the tubulin-polymerization inhibitors, pendimethalin (PRE), trifluralin (PPI); and the pigment synthesis inhibitor, clomazone (PRE, at least 150 days before planting). Despite the increasing problem with resistance, the two most widely used MOA groups are still those of the ALS inhibitors, including the POST chlorimuron-ethyl, cloransulam-methyl, oxasulfuron and imazethapyr, the PPI diclosulam and flumetsulam, and imazaquin (applied PPI or PRE) and the ACCse inhibitors, clethodym, fenoxaprop-p-ethyl, fluazifop-p-butyl, propaquizafop, quizalofop-p-ethyl, sethoxydim, and tepraloxydim.
Another chemical option to manage herbicide-resistant weeds is the use of specific synergists. These compounds, when mixed with herbicides, result in a level of biological activity substantially higher than that of the added efficacy of each chemical separately. Synergists are useful when resistance results from enhanced metabolism but are ineffective against target-site resistance. They may be used as components of a tank mixture or as part of a formulation to overcome resistance. To the authors knowledge, the only practical situation in which a synergist has been used commercially to control a herbicide-resistant weed is that of the mixing of piperophos or anilofos with propanil to control propanil-resistant E. colona.
For some years now it has been known that some organophosphate and carbamate insecticides block the action of aryl-acylamidase (AAA), which is responsible for propanil hydrolysis in rice (Frear and Still, 1968, Matsunaka 1968, Leah et al. 1994). When these insecticides are applied just before or after propanil, rice can be damaged by the herbicide because the insecticide prevents propanil metabolism. The resistance mechanisms of junglerice to propanil involves increased activity of AAA (Leah et al. 1994, 1995). Based on knowledge about the resistance- mechanism, the organophosphate herbicides piperophos and anilofos, which are selective in rice, were developed as synergists (Caseley et al. 1996, Valverde et al. 1997, 1999). Mixtures of these herbicides at very low doses with propanil also at a reduced dose (usually 1.76 kg ha-1 as opposed to the common dose of 3.84 kg ha-1) are not more phytotoxic to the crop than propanil alone but successfully overcome resistance in E. colona (Valverde et al. 2000). A formulation containing piperophos and propanil was first used commercially in Costa Rica and then in other areas of Latin America; anilofos has been used in tank mixtures (Valverde, 1996). Both mixtures were widely accepted by rice farmers (Valverde and Itoh, 2001).
Other attempts have been made to develop synergists to combat herbicide resistant weeds. More frequently, however, synergists are used as a tool to elucidate resistance mechanisms. Copper-chelating agents have been tested as possible synergists of paraquat and other oxidant-generating herbicides (Rogachev et al. 1998). Chelators capable of removing copper and/or zinc from superoxide dismutase and copper from ascorbate peroxidase could be of practical use in controlling paraquat-resistant Conyza bonariensis biotypes whose resistance is related to constitutive and/or herbicide induced elevated levels of antioxidant enzymes (Ye and Gressel, 2000, Ye et al. 2000). The aminotriazole herbicide amitrole was found to inhibit metabolism of diclofop acid in a resistant (SLR 31) biotype of L. rigidum, whose resistance to dichlofop was conferred by both target-site insensitivity and enhanced metabolism. Amitrole synergized the effect of diclofop-methyl on both the resistant and a susceptible biotype (Preston and Powles, 1998).
Herbicide-resistant crop cultivars
Herbicide-resistant crop cultivars (HRC) produced by genetic engineering or by mutation breeding are commercially available. Introduction of these cultivars has allowed farmers to use new chemical alternatives to control hard-to-kill species and herbicide-resistant weeds. An estimated 52.6 million hectares of transgenic crops was planted worldwide in 2001, which represents an increase of 19 percent (or 8.4 million ha) from the previous year. 25 percent of this area (equivalent to 13.5 million ha) was grown in developing countries, mostly in Argentina where 11.8 million ha of transgenic soybean and maize were planted in 2001. Genetically modified (GM) crops are also planted in China (mostly Bt cotton) and in South Africa, Mexico, Bulgaria, Uruguay, Romania, and Indonesia. Globally, the main GM crops are soybean, maize, cotton and canola or oil seed rape. Almost 80 percent of the planted GM crops are those carrying genes that confer herbicide tolerance (James, 2001).
In relation to herbicide resistance in weeds, there are also concerns about the wide use of HRCs (see Duke 1996 for a thorough review), including those in developing-country agriculture and biodiversity (Madsen et al. 2002, Olofsdotter et al. 2000, Riches and Valverde, 2002). Several developing countries lack proper legislation for HRCs and FAO has made an effort to develop simple guidelines to help these countries make decisions about the introduction and release of such crops (Valverde et al. 2001b, FAO, 2001). In addition to the new selection pressures imposed by the new chemicals used in HRCs, one of the most discussed risks of these crops in terms of herbicide resistance in weeds is the possibility of the resistance genes moving from the crop to weedy compatible species or biotypes and the HRC itself becoming a hard-to-kill weed when grown as a volunteer in a rotational crop.
Integration of control practices
As pointed by Mortensen et al. (2000) we should go beyond the notion of regarding weeds as a problem that can be solved solely with herbicides to one that can be managed through a better design of cropping systems. Even the most troublesome herbicide-resistance problems could have been prevented by an appropriate integrated weed management strategy, and now we are forced to look back to good agronomy and integrated weed management to deal with them. It is important that farmers realize the negative impact of herbicide resistance and understand the rationale for integrating control tactics as the basis for their acceptance. We must also demonstrate that the proposed alternatives are profitable and realistic. Opportunities for integrated management are illustrated with perhaps the two most important herbicide-resistance cases in the developing world: P. minor in wheat in India and E. colona in rice in several countries of Latin America.
P. minor is considered the most troublesome winter-season grass weed of wheat in India, where the crop is grown in the winter following summer production of rice (Malik and Singh, 1995). The weed is very competitive with wheat and at high infestation levels may result in complete crop failure (Singh et al. 1999). Since 1982, Indian wheat farmers have relied on oproturon, a broad-spectrum, substituted-urea herbicide for the control of P. minor, because it provided cost effectiveness, a wide-application window, flexibility in the application method, and a broad-spectrum weed-kill (Walia et al. 1997, Chhokar and Malik, 2002). But the selection pressure imposed by the overdependency of isoproturon resulted in the selection of resistant populations that were confirmed in the early 1990s (Malik and Singh, 1995, Walia et al. 1997). Resistance levels vary among biotypes, some having RIs of up to 13-18. After the first resistant populations were confirmed in Haryana State the problem increased in this area and in adjoining states, especially Punjab (Singh et al. 1998b). It is estimated that about 1 million ha are infested with resistant biotypes in these two states (Singh et al. 1998c). Studies by Singh et al. (1997a) indicated that a target-site mutation is not implicated in the resistance mechanism to isoproturon in this weed. Isoproturon uptake and translocation did not differ between a resistant and a susceptible biotype (Singh et al. 1996) but resistance appears to be conferred by an enhanced ability of the resistant plants to metabolize the herbicide as a result of increased activity of monooxygenase enzymes (Singh et al. 1998b). Indeed, both the mixed function oxidase inhibitors, 1-aminobenzotriazole (ABT) and piperonyl butoxide (PBO), inhibited the degradation of the herbicide in the R biotype (Singh et al. 1998b, 1998c).
Herbicides with alternative MOA control isoproturon-resistant P. minor, including the ACCase-inhibiting herbicides tralkoxydim and diclofop-methyl (Walia et al. 1997). However, more recently it has been reported that some isoproturon-resistant biotypes exhibit cross-resistance to diclofop-methyl (Kirkwood et al. 1997) and probably clodinafop-propargyl (Singh et al. 1997b, Singh et al. 1998a) without any prior field use, but remain susceptible to the structurally and physiologically related herbicide chlorotoluron, which can be used selectively in wheat. Other herbicides are also effective in controlling isoproturon-resistant P. minor: fenoxaprop-p-ethyl, sethoxydim, tralkoxydim, sulfosulfuron and the dinitroanilines, trifluralin and pendimethalin (Kirkwood et al. 1997, Malik and Yadav, 1997, Chhokar and Malik, 2002).
The integration of several agronomic practices combined with properly selected herbicides has been proposed to manage resistant populations; these include: planting of competitive wheat cultivars with aggressive canopy growth, modifying sowing date to ensure rapid crop establishment, appropriate and timely soil fertilization and moisture to favour crop growth, increased seeding rates, and narrow row spacing of bi-directional sowing to give a competitive advantage to the crop (Singh et al. 1999). Crop rotation, as previously mentioned, has been an important factor in delaying the appearance of isoproturon-resistant populations and can also be used as part of an integrated management strategy. Sugarcane can break the dominance of P. minor; winter maize, and the green fodder crops, clover (Trifolium alexandrium) and lucerne (Medicago sativa), have also proven useful as a rotation crops (Singh et al. 1999). Finally, there has been a trend towards no-till systems in areas affected by isoproturon resistance. Under this system, wheat can be planted earlier in the season, when temperatures are less conducive for P. minor germination, giving the crop a head start over the weed. Additionally, savings in fuel, machinery and labour have allowed no-till farmers to afford switching to herbicides with alternative MOAs that are much more expensive than isoproturon (Gill, 2001).
E. colona has evolved resistance to propanil in rice in Central America, Mexico, Colombia and Venezuela (Valverde et al. 2000) and several options have been developed to control resistant populations. In addition to herbicides with alternative MOAs and the already discussed use of synergists, several agronomic practices have been tested and used for resistance management, including modified herbicide regimes (Valverde et al. 2001a).
Elimination of the first junglerice populations that emerge before or with the crop, substantially reduces the in-crop infestation and the need for additional chemical control. A broad spectrum herbicide such as glyphosate or a light tillage operation can kill these initial populations before planting. Further benefits were obtained by substituting pendimethalin for propanil or other herbicides that effectively control junglerice (Valverde et al. 2001a). These include ACCase inhibitors such as fenoxaprop, cyhalofop, sethoxydim and clefoxydim, ALS herbicides (bispyribac-sodium and pyribenzoxim), pendimethalin, clomazone, pretilachlor, and the auxinic herbicide quinclorac (Valverde et al. 2000, 2001a). Unfortunately, resistance to the ACCase herbicide fenoxaprop evolved on a limited scale, following use of this herbicide for controlling propanil-resistant junglerice (Riches et al. 1996).
No single herbicide or management tactic can solve a particular herbicide-resistance problem. Both to prevent and manage resistance, once it occurs, requires a basic knowledge of the biology of the weeds and their population dynamics. A fundamental understanding of the forces that select resistant individuals and the processes by which resistance is accelerated or delayed, plus the experience gained over a broad range of growing conditions and countries, should better prepare us to combat herbicide resistance. The author hopes that the information presented here will stimulate researcher and practitioners from developing countries to document, study and innovate better solutions to local weed problems.
Agrow. 1996. World Crop Protection News. December 13.
Agrow. 1997a. World Crop Protection News. February 14 and 28.
Agrow. 1997b. World Crop Protection News, July 11.
Alcocer-Ruthling, M., Thill, D.C. & Shafii, B. 1992. Seed biology of sulfonylurea-resistant and -susceptible biotypes of prickly lettuce (Lactuca serriola). Weed Tech. 6: 858-864.
Baerson, S. R., Rodriguez, D. J., Tran, M., Feng, Y., Biest, N.A. & Dill, G.M. 2002. Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiology 129: 265-1275.
Bradley, K. W., Wu, J., Hatzios, K.K. & Hagood, E.S., Jr. 2001. The mechanism of resistance to aryloxyphenoxypropionate and cyclohexanedione herbicides in a johnsongrass biotype. Weed Sci. 49: 477-484.
Brighenti, A. M., Gazziero, D. L. P., Voll, E., Adegas, F.S. & Val, W.M.C. 2001. Análise de crescimento de biótipos de amendoim-bravo (Euphorbia heterophylla) resistente e suscetível aos herbicidas inibidores da ALS. Planta Daninha 19: 51-59.
Bryant, R. 1999. Agrochemicals in perspective: Analysis of the worldwide demand of agrochemical active ingredients. The Fine Chemicals Conference, Kensington, London, 29-30 November, 1999.
Buhler, D. D. 2002. Challenges and opportunities for integrated weed management. Weed Sci. 50: 273-280.
Buhler, D. D., Hartzler, R.G. & Forcella, F. 1997. Implications of weed seedbank dynamics to weed management. Weed Sci. 45: 329-336.
Burnet, M. W. M., Hart, Q., Holtum, J.A.M. & Powles, S.B. 1994. Resistance to nine herbicide classes in a population of rigid ryegrass (Lolium rigidum). Weed Sci. 42: 369-377.
Carmona, R. & da C. Villas-Bôas, H.D. 2001. Dinâmica de sementes de Bidens pilosa no solo. Pesquisa Agropecuaria Brasileira 36: 457-463.
Caseley, J. C., Leah, J.M., Riches, C.R. & Valverde, B.E. 1996. Combating propanil resistance in Echinochloa colona with synergists that inhibit acylamidase and oxygenases. Proc. of the Second Int. Weed Control Congress, Copenhagen, Denmark. 2: 455-460.
Chaves, L., Valverde, B.E. & Garita, I. 1994. Resistencia del pasto Honduras (Ixophorus unisetus) a herbicidas inhibidores de la sintetasa del acetolactato. Resúmenes V Congreso Internacional de Manejo Integrado de Plagas. San José, Costa Rica, p. 197.
Chin, D. V. 2001. Biology and management of barnyardgrass, red sprangletop and weedy rice. Weed Biology and Management 1: 37-41.
Chhokar, R. S. & Malik, R.K. 2002. Isoproturon-resistant littleseed canarygrass (Phalaris minor) and its response to alternate herbicides. Weed Tech. 16: 116-123.
Christoffoleti, P. J. 2002. Curvas de dose-resposta de biótipos resistente e suscetível de Bidens pilosa L. aos herbicidas inibidores da ALS. Scientia Agricola 59: 513-519.
Christoffoleti, P. J. 2001. Análise comparativa do crescimento de biótipos de picão-preto (Bidens pilosa) resistente e suscetível aos herbicidas inibidores da ALS. Planta Daninha 19: 75-83.
Christoffoleti, P. J., Kehdi, C. A. & Cortez, M.G. 2001. Manejo da planta daninha Brachiaria plantaginea resistente aos herbicidas inibidores da ACCase. Planta Daninha 19: 61-66.
Coleman, R. K., Gill, G. S. & Rebetzke, G.J. 2001. Identification of quantitative trait loci for traits conferring weed competitiveness in wheat (Triticum aestivum L.). Australian J. of Agricultural Res. 52: 1235-1246.
CONAB. Companhia Nacional de Abastecimento, 2002.
Acompanhamento da safra 2001/02. Sexto levantamento. Julho/2002.
(also available at http://www.conab.gov.br/politica_agricola/Safra/avalia.html)
Cortez, M. G., Christoffoleti, P.J., Victoria Filho, R. & de Prado, R. 2000. Resistência cruzada e mecanismo de resisência em biotipos de Brachiaria plantaginea resistentes a herbicidas inibidores da ACCase. Resumos. XXII Congreso Brasileiro da Ciência das Plantas. Daninhas. Foz do Iguaçu, Brasil, p. 498.
De Datta, S. K. & Baltazar, A.M. 1996. Integrated weed management in rice in Asia. pp.145- 165, In Naylor, R., ed. Herbicides in Asian rice: Transitions in weed management. Institute for Int. Studies, Stanford University, Palo Alto, California, & the Int. Rice Research Institute, Manila, Philippines.
Devine, M. D. & Preston, C. 2000. The molecular basis of herbicide resistance. pp. 72-104. In Cobb, A.H. & Kirkwood, R.C., eds. Herbicides and their mechanisms of action. Sheffield Academic Press Ltd, England.
Duke, S. O., ed. 1996. Herbicide resistant crops. Agricultural, environmental, regulatory, and technical aspects. CRC Press, Boca Raton, Florida, USA. 420 pp.
Dyer, W. E., Chee, P.W. & Fay, P.K. 1993. Rapid germination of sulfonylurea-resistant Kochia scoparia L. accessions is associated with elevated seed levels of branched chain amino acids. Weed Sci. 41: 18-22.
EMBRAPA. Empresa Brasileira de Pesquisa Agropecuaria. 2000. Recomendações técnicas para a cultura da soja no Paraná - safra 2000/2001. EMBRAPA, Brazil, 225 pp.
Fasoula, D. A. & Fasoula, V.A. 1997. Competitive ability and plant breeding. Plant Breeding Reviews 14: 89-138.
Fischer A. J. 1996. Integrated red rice management in Latin American rice fields. Proc.of the Second Int. Weed Control Congress. Copenhagen, Denmark, 2: 53-664.
Fischer, A., Ramírez, J., H. V. & Lozano, J. 1997. Suppression of junglerice (Echinochloa colona) (L.) Link by irrigated rice cultivars in Latin America. Agronomy J. 89: 516-521.
Forcella, F., Benech Arnold, R. L., Sanchez, |R. & Ghersa, C.M. 2000. Modeling seedling emergence. Field Crops Res. 67: 23-139.
Garita, I., Valverde, B. E., Chacón, L.A., de la Cruz, R., Riches, C.R. & Caseley, J.C. 1995. Occurrence of propanil resistance in Echinochloa colona in Central America. Proc. Brighton Crop Protection Conference - Weeds 1: 193-196.
Garriti, D. P., Movillon, M. & Moody, K. 1992. Differential weed suppression ability in upland rice cultivars. Agronomy J. 84: 586-591.
Garro, J. E., de la Cruz, R. & Shannon, P.J. 1991. Propanil resistance in Echinochloa colona populations with different herbicide use histories. Proc. Brighton Crop Protection Conference - Weeds 3: 1079-1083.
Gazziero, D. L. P., Brighenti, A. M., Maciel, C.D.G., Christofolleti, P.J., Adegas, F.S. & Voll, E. 1998. Resistência de amendoim - bravo aos herbicidas inibidores da enzima ALS. Planta Daninha 16: 117-125.
Gazziero, D. L. P., Christoffoleti, P. J., Brighenti, A. M., Prete, C.E.C. & Voll, E. 2000. Resistência da planta daninha capim-marmelada (Brachiaria plantaginea) aos herbicidas inibidores da enzima accase na cultura da soja. Planta Daninha 18: 169-184.
Gelmini, G. A., Victória-Filho, R., Soares-Novo, M. C. S. & Adoryan, M.L. 2001. Resistência de biótipos de Euphorbia heterophylla L. aos herbicidas inibidores da enzima ALS utilizados na cultura de soja. Bragantia 60: 93-99.
Gelmini, G.A., Victória Filho, R., Novo, M.C.S.S. & Adoryan, M.L. 2002. Resistência de Bidens subalternans aos herbicidas inibidores da enzima acetolactato sintase utilizados na cultura da soja. Planta Daninha 20: 319-325.
Gill, G. S. 2001. Resistance management in Australian wheat and Indian rice/wheat cropping systems. Japan-Australia Seminar, Utsunomiya University, 5-7 November 2001, pp. 33- 37.
Gruys, K. J., Biest-Taylor, N. A., Feng, P. C. C., Baerson, S. R., Rodriguez, D. J., You, J., Tran, M., Feng, Y., Kreuger, R.W., Pratley, J.E., Urwin, N.A. & Stanton, R.A. 1999. Resistance of glyphosate in annual ryegrass (Lolium rigidum). II Biochemical and molecular analyses. Weed Sci. Society of America Abstracts 39: 163.
Heap, I. & LeBaron, H. 2001. Introduction and overview of resistance. pp. 1-22, In S. B. Powles &. Shaner, D.L., eds. Herbicide resistance in world grains. CRC Press, Boca Raton, Florida, USA.
Hidayat, I. & Preston, C. 2001. Cross-resistance to imazethapyr in a fluazifop-P-butyl- resistant population of Digitaria sanguinalis. Pesticide Biochemistry and Physiology 71: 190-195.
Hyvönen, T. & Salonen, J. 2002. Weed species diversity and community composition in cropping practices at two intensity levels - a six-year experiment. Plant Ecology 154:73-81.
Itoh, K., Uchino, A., Wang, G.X. & Yamakawa, S. 1997a. Distribution of Lindernia spp. resistant biotypes to sulfonylurea herbicides in Yuza Town, Yamagata Prefecture. J. of Weed Sci. and Tech. 42 (supplement): 22-23.
Itoh, K., Wang, G. X. & Uchino, A. 1997b. Non-effective problems of Lindernia weeds to one-shot application herbicides including sulfonylureas in Tohoku area. J.of Weed Science and Technology 42 (supplement): 12-13.
Itoh, K., Azmi, M. & Ahmad, A. 1992. Paraquat resistance in Solanum nigrum, Crassocephalum crepidioides, Amaranthus lividus and Conyza sumatrensis in Malaysia. Proc. 1st Int. Weed Control Congress, Melbourne, Australia, 17-21 February, 1992. 2: 224-228.
Ismail, B. S., Chuah, T. S. & Khatijah, H.H. 2001. Metabolism, uptake and translocation of 14 C-paraquat in resistant and susceptible biotypes of Crassocephalum crepidioides (Benth.) S. Moore. Weed Biology and Management 1: 176-181.
Ismail, B. S., Chuah, T.S. & Salmijah, S. 2001. Germination, emergence and growth of glyphosate resistant and susceptible biotypes of goosegrass (Eleusine indica). Proc.II, 18th Asian-Pacific Weed Sci. Society Conference, The Asian-Pacific Weed Science Society, Beijing, pp. 471-481.
James, C. 2001. Global review of commercialized transgenic crops: 2001. ISAAA Briefs, 24. Ithaca, NY: Int. Service for the Acquisition of Agri-Biotech Applications. 20 p.
James, E. H., Kemp, M.S. & Moss, S.R. 1995. Phytotoxicity of trifluoromethyl- and methyl-substituted dinitroaniline herbicides on resistant and susceptible populations of black-grass (Alopecurus myosuroides). Pesticide Science 43: 273-277.
Jasieniuk, M., Brûlé-Babel, A.L. & Morrison, I.N. 1996. The evolution and genetics of herbicide resistance in weeds. Weed Sci. 44: 176-193.
Kirkwood, R., Singh, S. & Marshall, G. 1997. Resistance of Phalaris minor to isoproturon: Mechanism and management implications. Proc. 16th Asian-Pacific Weed Sci. Society Conf., Kuala Lumpur, Malaysia, 8-12 September 1997. pp. 204-207.
Kremer, E. & Lotz, L.A.P. 1998. Germination and emergence characteristics of triazine- susceptible and triazine-resistant biotypes of Solanum nigrum. J. of Applied Ecology 35: 302-310.
Lee L. J. & Ngim, J. 2000. A first report of glyphosate-resistant goosegrass (Eleusine indica (L) Gaertn) in Malaysia. Pest Management Science 56: 336-339.
Lemerle, D., B. Verbeek & Orchard, B. 2001. Ranking the ability of wheat varieties to compete with Lolium rigidum. Weed Res. 41: 197-209.
Levin, D. D. 2001. The recurrent origin of plant races and species. Systematic Botany 26: 197-204.
Madsen, K. H., Valverde, B. E., & Jensen, J.E. 2002. Risks assessment of herbicide resistant crops: A Latin American perspective using Oryza sativa as a model. Weed Tech.16:215-223.
Malik, R. K. & Singh, S. 1995. Littleseed canarygrass (Phalaris minor) resistance to isoproturon in India. Weed Tech. 9: 419-425.
Malik, R. K. & Yadav, A. 1997. Potency of alternative herbicides against isoprotyron- resistance littleseed canary grass. Proc. 16th Asian-Pacific Weed Sci. Society Conf., Kuala Lumpur, Malaysia, 8-12 September 1997, pp. 208-210.
Melhorança, A. L. & Pereira, F. A. R. 2000. Eficiência do herbicida lactofen no controle de Euphorbia heterophylla resistente aos herbicidas inibidores da enzima acetolactato sintasa (ALS). Revista Brasileira de Herbicidas 1: 53-56.
Merotto, A., Jr., Vidal, R.A. & Fleck, N.G. 1999. Soybean tolerance to synthetic auxin and potential of mixtures with protox-inhibiting herbicides. Proc. British Crop Protection Conference - Weeds 1: 319-324.
Monqueiro, P. A. & Christoffoleti, P.J. 2001a. Bioensaio rápido de determinação da sensibilidade da acetolactato sintase (ALS) a herbicidas inibidores. Scientia Agricola 58: 193-196.
Monqueiro, P. A. & Christoffoleti, P.J. 2001b. Manejo de populações de plantas daninhas resistentes aos herbicidas inibidores da acetolactato sintase. Planta Daninha 19: 67-74.
Monqueiro, P.A., Christoffoleti, P. J. & Dias, C.T.S. 2000. Resistência de plantas daninhas aos herbicidas inibidores da ALS na cultura da soja (Glycine max). Planta Daninha 18: 419-425.
Moreno, R. E. 2001. Soybean weed management in Argentina [abstract]. In Abstracts of the Third Int. Weed Sci. Congress, 2000 June 6-11; Foz do Iguassu, Brazil, pp. 520. CD-ROM. Available from the Int. Weed Science Society, Oxford, MS, USA.
Mortensen, D. A., Bastiaans, L. & Sattin, M. 2000. The role of ecology in the development of weed management systems: an outlook. Weed Res. 40: 49-62.
Oliveira, M. F., Prates, H.T., Brighenti, A.M., Gazziero, D.L.P., Vidal, R.A., Vargas, L., Oliveira, R.S., Jr. & Purcino, A. A. C. 2002. Atividade da acetolactato sintase de plantas de milho e de amendoim-bravo (Euphorbia heterophylla) resistentes e suscetíveis ao imazaquin. Planta Daninha 20: 77-82.
Olofsdotter, M., Jensen, L.B. & Courtois, B. 2002. Improving crop competitive ability using allelopathy-an example from rice. Plant Breeding 121: 1-9.
Olofsdotter, M., Valverde, B. E. & Madsen, K.H. 2000. Herbicide resistant rice (Oryza sativa L.): Global implications for weedy rice and weed management. Annals of Applied Biology 137: 279-295.
Ponchio, J. A., Victoria-Filho, R. & Christoffoleti, P.J. 1997. Resistencia de biotipos de Bidens pilosa aos herbicidas inibidores da ALS/AHAS. Resumos. XXI Congresso brasileiro da sciencia das plantas daninhas. Caxambu, MG, pp.126.
Powles, S. B. 1997. Success from adversity: herbicide resistance can drive changes to sustainable weed management systems. Proc. Brighton Crop Protection Conference - Weeds.3: 119-1126.
Powles, S. B. & Shaner, D.L. eds. 2001. Herbicide resistance in world grains. CRC Press, Boca Raton, Florida, USA. 308 pp.
Preston, C. & Mallory-Smith, C.A. 2001. Biochemical mechanisms, inheritance, and molecular genetics of herbicide resistance in weeds. pp. 23-60 In S. B. Powles & Shaner, D.L. eds. Herbicide resistance in world grains. CRC Press, Boca Raton, Florida, USA.
Preston, C. & Powles, S.B. 1998. Amitrole inhibits diclofop metabolism and synergises diclofop-methyl in a diclofop-methyl-resistant biotype of Lolium rigidum. Pesticide Biochemistry and Physiology 62: 179-189.
Preston, C. & Powles, S.B. 2002. Evolution of herbicide resistance in weeds: initial frequency of target site-based resistance to acetolactate synthase-inhibiting herbicides in Lolium rigidum. Heredity 88: 8-13.
Retzinger, E. J. & Mallory-Smith, C. 1997. Classification of herbicides by site of action for weed resistance management strategies. Weed Tech.11: 384-393.
Reznick, D. N. & Cameron, K.G. 2001. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112-113: 183-198.
Riches, C. R. & Valverde, B.E. 2002. Agricultural and biological diversity in Latin America: Implications for development, testing and commercialization of herbicide resistant crops. Weed Tech.16: 200-214.
Riches, C. R., Caseley, J.C., Valverde, B.E. & Down, V.M. 1996. Resistance of Echinochloa colona to ACCase inhibiting herbicides. pp. 14-16, In de Prado, R., Jorrín, J., García-Torres, L. & Marshall, G. eds. Proc. of the Int. Symposium on Weed and Crop Resistance to Herbicides, 3-6 April 1995. University of Cordoba, Spain.
Riches, C. R., Knights, J.S., Chaves, L., Caseley, J.C. & Valverde, B.E. 1997. The role of pendimethalin in the integrated management of propanil-resistant Echinochloa colona in Central America. Pesticide Science 51: 341-346.
Rogachev, I., Kampel, V., Gusis, V., Cohen, N., Gressel, J. & Warshawsky, A. 1998. Synthesis, properties, and use of copper-chelating amphiphilic dithiocarbamates as synergists of oxidant-generating herbicides. Pesticide Biochemistry and Physiology 60:133-145.
Santos, J. B., Procópio, S.O., Silva, A.A. & Costa, L.C. 2002. Produção e características qualitativas de sementes de plantas daninhas. Planta Daninha 20: 237-241.
Sattin, M., Berto, D., Zanin, G. & Tabacchi, M. 1999. Resistance to ALS inhibitors in weeds of rice in north-western Italy. Proc. Brighton Crop Protection Conference Weeds, Brighton, UK, 3: 783-790.
Shibaike, H., Uchino, A. & Itoh, K. 1999. Genetic variation and relationships of herbicide- resistant and -susceptible biotypes of Lindernia micrantha. Proc. Brighton Crop Protection Conference - Weeds 1: 197-202.
Singh, S., Kirkwood, R.C. & Marshall, G. 1999. Biology and control of Phalaris minor Retz. (littleseed canarygrass) in wheat. Crop Protection 18: 1-16.
Singh, S., Kirkwood, R. C. & Marshall, G. 1997a. Effects of isoproturon on photosynthesis in susceptible and resistant biotypes of Phalaris minor and wheat. W ed Res. 37: 315-324.
Singh, S., Kirkwood, R. C. & Marshall, G. 1997b. New management approaches for isoproturon-resistant Phalaris minor in India. Proc. Brighton Crop Protection. Conference - Weeds. 1: 357-362.
Singh, S., Kirkwood, R.C. & Marshall, G. 1998b. Effect of ABT on the activity and rate of degradation of isoproturon in susceptible and resistant biotypes of Phalaris minor and wheat. Pesticide Sci. 53: 123-132.
Singh, S., Kirkwood, R. C. & Marshall, G. 1998c. Effect of the monooxygenase inhibitor piperonyl butoxide on the herbicidal activity and metabolism of isoproturon in herbicide resistant and susceptible biotypes of Phalaris minor and wheat. Pesticide Biochemistry and Physiology 59: 143-153.
Singh, S., Kirkwood, R. C. & Marshall, G. 1998a. Control of isoproturon resistant biotypes of Phalaris minor by chorotoluron and clodinafop-propargyl. Resistance Pest Management 10: 5-18.
Singh, S., Kirkwood, R. C. & Marshall, G. 1996. Uptake, translocation and metabolism of isoproturon in wheat, susceptible and resistant biotypes of Phalaris minor. Proc. Second Int. Weed Control Congress, Copenhagen, Denmark, 25-28 June 1996, 2: 529-534.
Stankiewicz, M., Gadamski, G. & Gawronski, S.W. 2001. Genetic variation and phylogenetic relationships of triazine-resistant and triazine-susceptible biotypes of Solanum nigrum-analysis using RAPD markers. Weed Res. 41: 287-300.
Stallings, G. P., Thill, D, & Mallory-Smith, C.A. 1994. Sulfonylurea-resistant Russian thistle (Salsola iberica) survey in Washington state. Weed Tech. 8: 258-264.
Thill, D. C. & Mallory-Smith, C.A. 1997. The nature and consequence of weed spread in cropping systems. Weed Sci. 45: 337-342.
Thompson, C. R., Thill, D. C. & Shafii, B. 1994. Germination characteristics of sulfonylurea-resistant and -susceptible Kochia (Kochia scoparia). Weed Sci. 42: 50-56.
Tuesca, D. & Nisensohn, L. 2001. Resistencia de Amaranthus quitensis a imazetapir y clorimurón-etil. Pesquisa Agropecuaria Brasileira 36: 601-606.
Valverde, B. E. 2002. Weed Management in Latin America. Pesticide Outlook 13: 79-81.
Valverde, B. E. 1996. Management of herbicide resistant weeds in Latin America: The case of propanil-resistant Echinochloa colona in rice. Proc. Second Int. Weed Control Congress, Copenhagen, pp. 415-420.
Valverde, B. E. & Itoh, K. 2001. World rice and herbicide resistance. pp. 195-249. In Powles, S. R. & Shaner, D. eds. Herbicide Resistance in World Grains. CRC Press, Boca Raton, Florida, USA.
Valverde, B., Garita, I., Vargas, E., Chaves, L., Ramírez, F., Fischer, A.J. & Pabón, H. 1999. Anilofos as a synergist to propanil for controlling propanil-resistant junglerice, Echinochloa colona. WSSA Abstracts 39: 318.
Valverde, B. E., Chaves, L., Garita, I., Ramírez, F., Vargas, E., Carmiol, J., Riches, C.R. & Caseley, J.C. 2001a. Modified herbicide regimes for propanil-resistant junglerice control in rain-fed rice. Weed Sci. 49: 395-405.
Valverde, B. E., Madsen, K. H., Streibig, J. E. & Labrada, R. 2001b. Assessment of environmental hazards of herbicide and insect-resistant crops. Preparation of Guidelines. VALDOR - Values in Decisions On Risk. Proc. Stockholm. Sweden. pp.132-141.
Valverde, B. E., Chaves, P., Garita, I., Vargas, E., Riches, C.R. & Caseley, J.C. 1997. From theory to practice: Development of piperophos as a synergist to propanil to combat herbicide propanil resistance in Junglerice, Echinochloa colona. WSSA Abstracts 37: 33.
Valverde, B. E., Riches, C.R. & Caseley, J.C. 2000. Prevention and management of herbicide-resistant weeds in rice: Experiences from Central America with Echinochloa colona. Cámara de Insumos Agropecuarios, Costa Rica, pp. 123.
Vargas, L., Borém, A. & Silva, A.A. 2001. Herança da resistência aos herbicidas inibidores da ALS em biótipos da planta daninha Euphorbia heterophylla. Planta Daninha 19: 331-336.
Vidal, R. A. & Fleck, N.G. 1997. Three weed species with confirmed resistance to herbicides in Brazil. WSSA Abstracts 37: 251.
Vidal, R. A. & Merotto, A., Jr. 1999. Resistência de amendoim-bravo aos herbicidas inibidores da enzima acetolactato sintase. Planta Daninha 17: 367-373.
Vidal, R. A. & Trezzi, M.M. 2000. Análise de crescimento de biótipos de leiteira (Euphorbia heterophylla) resistentes e suscetível aos herbicidas inibidores da ALS. Planta Daninha 18: 427-433.
Vitta, J., Tuesca, D., Puricelli, E., Nisensohn, L., Faccini, D. & Leguizamon, E. 2001. Glyphosate-tolerant soybean and weed management in Argentina: present and prospects [abstract]. In Abstracts of the Third Int. Weed Sci. Congress, 2000, June 6-11; Foz do Iguassu, Brazil, pp. 343. CD-ROM. Available from the Int. Weed Science Society, Oxford, MS, USA.
Voll, E., Torres, E., Brighenti, A.M. & Gazziero, D.L.P. 2001. Dinâmica do banco de sementes de plantas daninhas sob diferentes sistemas de manejo de solo. Planta Daninha19: 171-178.
Walia, U. S., Bar, L. S. & Dhaliwal, B.K. 1997. Resistance to isoproturon in Phalaris minor Retz. In Punjab. Plant Protection Quarterly 12: 138-140.
Walker, S. R., Medd, R. W., Robinson, G.R. & Cullis, B.R. 2002. Improved management of Avena ludoviciana and Phalaris paradoxa with more densely-sown wheat and less herbicide. Weed Res. 42: 257-270.
Wrubel, R. P. & Gressel, J. 1994. Are herbicide mixtures useful for delaying the rapid evolution of resistance? A case study. Weed Tech. 8: 635-648.
Ye, B. & Gressel, J. 2000. Transient, oxidant-induced antioxidant transcript and enzyme levels correlate with greater oxidant-resistance in paraquat-resistant Conyza bonariensis. Planta 211: 50-61.
Ye, B., Faltin, Z., Ben-Hayyim, F., Eshdat, Y. & Gressel, J. 2000. Correlation of glutathione peroxidase to paraquat/oxidative stress resistance in Conyza determined by direct fluorometric assay. Pesticide Biochemistry and Physiology 66: 182-194.