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Pesticide Resistance: Strategies and Tactics for Management. 1986. National Academy Press, Washington, D.C. Resistance in Weeds FRED W. SLIFE The evolution of herbicide development and use is presented. Weed control began around 1900, with little success. The current weed- control era began in the early 1940s and has been very successful. Problems, however, are increasing. A few weed species are becom- ing resistant to herbicides and are filling the ecological niches opened when herbicides are used. Soil microorganisms are increasing the rate of degradation of herbicides. Programs need to be developed to identify the problem early. Possible elective control methods (mixtures, rotations, and cultivations are described. INTRODUCTION Ever since man first disturbed the natural flora to cultivate desirable plants, weeds have been a problem. The weed problem has persisted because of the great reproductive capacity of weeds, primarily seed production. By 1900 the native weed flora in the United States had been supplemented with nearly all of the major agricultural weeds from around the world. The universal occurrence of weeds as constant components of the agricultural environment, as compared with the epidemic nature of other pests, delayed recognition of weed control in crop production. The first attempts to use selective herbicides to control broadleaf weeds in small grains, around the year 1900, were unsuccessful. Weed-control methods consisted of crop rotation, row cultivation, fallowing, hand pulling, and hoeing. The introduction of the tractor in the early l900s resulted in a rapid expansion of crop production and improved weed control to some degree. 327

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328 TACTICS FOR PREVENTION AND MANAGEMENT During the 1 930s, crop rotation was emphasized because it was considered to be the best weed-control method available. Growing crops with different life cycles, along with the variation in management associated with each crop, prevented any one type of weed from becoming dominant. Unfortu- nately rotations allowed a great diversity of weed species (annuals, water annuals, perennials) to persist in harmony. Most weed seeds have a high degree of dormancy that extends longer than any practical rotation (Chepil, 19461. Also, rotations and tillage practices seem to have little effect on weed populations (Dunham et al., 19581. The current weed-control era began with the introduction of 2,4-D and MCPA in the early 1940s. The success of 2,4-D and MCPA to control broadleaf weeds in grass crops undoubtedly was the stimulus for the chemical industry to search for new herbicides. By 1960, however, problems with herbicides began surfacing, especially with 2,4-D in the U.S. Corn Belt. Although herbicides decreased, the dominant broadleaf weed complex, an- nual grasses, became the dominant problem. The use of 2,4-D created var- iations within a species and injured some corn cultivars, depending on the genetic base. Some populations of Canada thistle (cirsium arvense) were severely affected by a single treatment of 2,4-D while others were not af- fected. From the mid-19SOs to the early 1960s a series of soil-applied herbicides became available. These compounds were so successful that soil herbicide treatments used as preplan" incorporated or preemergence became the pre- dominant mode of use. Use of combinations of herbicides increased and postemergence herbicides were used as needed. Since the mid-1960s, weed-control programs using herbicides as the pri- mary control measure have given the highest degree of weed control yet achieved on agricultural lands. The magnitude of the weed problem in both cultivated and noncultivated areas has been greatly reduced. POTENTIAL PROBLEMS Many weed scientists see the changing weed spectrum as being the greatest challenge facing chemical weed control. Herbicides have successfully opened a niche in the weed ecosystem that a few weed species tolerant to herbicides are filling. For example, broadleaf perennials are increasing in the cultivated areas, and other tolerant species have come in as seeds dispersed by air and other means. Enhanced degradation of compounds by soil microorganisms, as is oc- curring with the thiocarbamate herbicide EPTC, is another potential problem. Enhanced degradation has been found only where EPTC has been used annually for 10 years. It may be that other carbamate pesticides, particularly soil-applied insecticides, are also subject to enhanced degradation. Pesticide

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RESISTANCE IN WEEDS 329 rotation seems to modify the problem since EPTC performs well when rotated with other herbicide treatments. There is no indication that enhanced deg- radation is occurring with other classes of herbicides. The development of resistance is both a blessing and a curse. It has appeared early enough that it can be corrected, and it may be possible to transfer the herbicide resistance in weeds to closely related crop species (LeBaron and Gressel, 19821. Currently it is limited to herbicides that have a specific site of action. Resistance first developed with the intensive use of the s-triazine herbicides, particularly atrazine and simazine in ornamental plantings where relatively high rates of herbicides were used annually for 10 years. Because these herbicides have been so effective, they are used extensively in minimum-till or no-till corn production, and they have often been used at high rates to control all vegetation for-prolonged periods (for example, along railroads, roadsides, and industrial sites). The triazine herbicides made it practical to grow large acreages of monoculture crops (e.g., corn and sorghum) and to depend more exclusively on these herbicides for weed control. In recent years, especially since the expiration of the triazine patents, the cost of these herbicides has decreased, providing incentive for even greater use. It is not surprising that weed resistance appeared in these heavy triazine- use areas by 1970. Currently some 38 weed species with biotypes resistant to the s-triazine herbicides (atrazine) have been identified. Resistance has been identified in 25 states in the United States, 4 Canadian provinces, and 10 other countries. Perhaps the most critical areas are in Hungary and Austria, where resistance has developed extensively in monocultural corn systems. Failure to react to the problem by crop rotation or alternative controls has made atrazine an ineffective herbicide in some areas of these countries. In North America large areas of atrazine-resistant weeds have appeared in the intensive corn area of Ontario, Canada, and in the mid-Atlantic states, par- ticularly Maryland. Weed resistance has been confirmed in at least six classes of herbicides, the most recent being the emergence of a resistant biotype of goosegrass (Eleusine indica) to the dinitroaniline herbicides (Mudge et al., 19841. Weed resistance seems to be occurring rapidly in many areas where a single her- bicide is used repeatedly with liKle or no cultivation. Resistance will develop most rapidly in orchards, nurseries, railroads, and other noncultivated areas if the potential for resistance is not recognized quickly. IDENTIFICATION OF PROBLEM Herbicide-resistant weeds are probably present in most weed populations. Since they may not be morphologically different than sensitive biotypes, identification can be difficult. Herbicide users know that results vary greatly

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330 TACTICS FOR PREVENTION AND MANAGEMENT with environmental weed-control conditions. Weed "escapees" are common with most treatments; in the past this has been attributed to lack of control rather than resistance. Education programs aimed at identifying weed escapees can do a great deal in identifying the problem early. For example, in the case of atrazine use on corn, extension programs could be aimed at scouting treated fields for weed escapees, particularly when environmental conditions are ideal for herbicide performance. Additional emphasis could be placed on the appear- ance of Amaranthus spp. (pigweeds) or Chenopodium spp. (lambsquarters). These species, normally sensitive to atrazine, have developed resistance very rapidly with continuous atrazine use. With any herbicide treatment the appearance of weed species normally sensitive to that treatment is cause for concern. Prompt identification and verification of resistance should be made. CONTROL Control techniques that can be used to prevent weeds from becoming dominant and to reduce the seriousness of resistant populations include her- bicide mixtures, herbicide rotation, crop rotation, and increased cultivation. Some of these measures will be more costly than current programs. In coun- tries where agricultural production is highly developed, weed-control pro- grams will change to meet the challenge of weed resistance. In other countries where crop production is less productive, the use of new, more expensive control programs will be much slower. Herbicide Mixtures Mixtures generally give superior weed control, compared with a single herbicide treatment. Mixtures are selected for the weed spectrum each com- ponent will control; thus, high rates are avoided. This strategy delays the emergence of weed resistance, compared with using a single herbicide at higher rates. In addition herbicides known to produce weed resistance when used at high rates alone can still be used effectively in mixtures to control . . ~ sensitive species. Herbicide Rotation Change in the herbicide program has been recommended for many years to prevent rapid changes in the weed spectrum. Shaw (1957) emphasized the need for rotational herbicide programs to present rapid changes in weed spectrum. In the countries where herbicide use is high, a wide variety of herbicide treatments are available for major crops. Preplant, preemergence, and postemergence can be utilized effectively to prevent and control resistant

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RESISTANCE lN WEEDS TABLE 1 Soil Weed Seed Level in 10 Years of Continuous Corn as Affected by the Same Herbicide Treatment, Herbicide Rotation, and No Herbicide with Cultural Practices Only 331 Seeds/kg of Soil 1965 1970 1975 Grass Seeds Corn, Corn, Corn Same herbicide 23129130 Herbicide rotation 2052 No herbicide 217895 BE Seeds Corn, Corn, Corn Same herbicide 102424 Herbicide rotation 98305 No herbicide 95120126 Total Seeds Corn, Corn, Corn Same herbicide 126171134 Herbicide rotation 119356 No herbicide 116198221 SOURCE: Agronomy Department, University of Illinois. weeds. Recently several new herbicides have become available and more are in late development stages. The effectiveness of herbicide rotation, compared with using the same herbicide treatment, is demonstrated in Table 1. Herbicide rotation greatly reduced the soil seed bank by preventing seed production, while the contin- uous use of the same herbicide allowed tolerant species to increase soil seed numbers. In this study the continuous use of atrazine over a 10-year period allowed annual grasses to increase rapidly, but greatly reduced the broadleaf population. This study also indicates that monoculture corn production is possible if herbicide treatments are changed frequently to prevent rapid shifts in the weed spectrum and to prevent or delay the emergence of resistance. Corn yields (Table 2), however, are significantly higher in a rotation than in a monoculture system. TABLE 2 Crop Yields (1966-1977) as Affected by Weed Management Systems and Crop Rotation (bu/A) No Herbicide Some Herbicide Herbicide Rotation Rotation 3 Cultivations 1 Cultivation 1 Cultivation Corn, Corn, Corn 104.1 127.1 131.4 Corn, Corn, Soybeansa 114.8 135.7 140.0 Corn, Corn, Soybeansb 111.6 133.3 138.3 Corn, Soybeans, Wheat 116.7 138.8 142.0 aFirst year corn yields. bSecond year corn yields. SOURCE: Agronomy Department, University of Illinois.

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332 TACTICS FOR PREVENTION AND MANAGEMENT The rapid decline in soil-weed seed in some areas is an opportunity to refine weed-control systems by effectively utilizing postemergence herbi- cides. For example, in cotton growing regions soil-applied grass herbicides have been used for many years. Many farmers also grow soybeans. The dinitroaniline herbicides are widely used on both crops. The grass-weed pressure in these crops is low, giving the farmer the alternative of using new postemergence grass herbicides. Row cultivation, which is a part of the weed management system, may be effective enough to eliminate the need for grass herbicides in a particular year. The strategy of using postemergence herbi- cides to treat the existing weed problem has high potential for delaying the emergence of resistant weeds. Weed resistance has appeared as early as five to six years after the con- tinuous use of the same herbicide. Most common areas are no-till corn production, nurseries, railroads, and other noncultivated areas. By stopping seed production of the herbicide-sensitive species, the resistant weeds, which are generally less fit, can dominate quickly and rapidly build up the soil seed bank. Roberts (1968), in a series of eloquent studies over a period of years' clearly showed that the longevity of weed seeds in cultivated areas of the soil was relatively short. He demonstrated that seed loss out of the soil seed bank would occur at the rate of 50 percent per year if no new seeds were allowed to replenish the soil. Schweizer and Zimdahl (1984a,b) reported a 96 percent decline in the soil seed bank after six years in a crop-herbicide rotation study and a 98 percent decline in a continuous corn system. Crop Rotation Crop rotation is an important strategy that can delay the development of resistance and reduce resistant weed populations. This is true only if a variety of well-chosen herbicides are used for weed control. Unfortunately farmers are often reluctant to change their current cropping system, especially if their present program has been successful. Changing the crop is the last option most farmers will choose, since they have acquired knowledge and experience in growing, harvesting, and marketing the crop at a profit. Crop rotation will probably receive additional emphasis because of the developing resistance problem in all pest-control disciplines. For example, in the U.S. Corn Belt alternating corn and soybeans has greatly reduced the need for corn rootworm treatments. Because crop rotation also controls the soybean cyst nematode, soybeans can be a viable crop in areas heavily infested with the nematode. Increased Cultivation Herbicides have been so effective that the amount of tillage previously used in crop production has been reduced. (Reduced tillage has the added

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RESISTANCE IN WEEDS 333 benefit of decreasing soil erosion.) In no-till agriculture row cultivation is seldom used, and even in clean tillage fields row cultivation has declined. In the U.S. Corn Belt most corn is grown in rotation, usually with soy- beans. But several Corn Belt states have as much as 25 percent of the crop in continuous corn. Atrazine is generally used annually, either alone or in combination with a grass-specific herbicide in the continuous corn areas, and one- or two-row cultivations are common. Weed resistance has not been a factor in these areas thus far, possibly because of the tillage component. Weed resistance, however, is slowly evolving in areas where cultivation is a part of the management program. In reduced tillage systems, and particularly no-till, herbicide rotation will delay the appearance of resistance. Increased rates of herbicides are required for no-till fields; thus, cross-resistance may develop. Developing tillage equipment that will control weed escapees but not destroy the surface residue would be highly desirable. Weed control in the noncultivated areas will become more difficult and expensive as resistance becomes more widespread. Chemical rotation is crit- ical for these areas, since there are a limited number of herbicides available for use along railroads, industrial sites, and highways. Excellent progress has been made in reducing and even eliminating grass mowing on many highways. Perennial grass competition has eliminated most annual and per- ennial weeds, resulting in less herbicide use. It may be possible to extend this type of weed control to other areas. Several plant growth regulators are available that inhibit foliage growth and reduce grass mowing costs. This approach to weed control is more economical than the continuous use of herbicides. CONCLUSION Chemical weed control used with good cultural practices has become the standard weed-control program in many parts of the world. As yet no good alternatives to these programs exist in high-production agricultural areas. Excellent progress has been made in biological control, and as more infor- mation becomes available on weed threshold levels, it may be possible to reduce herbicide use. Integrated Pest Management (IPM) programs are needed that are designed to identify more precisely and to control tolerant and re- sistant weed species and to enhance chemical degradation in the soil. The high degree of weed control achieved in recent years can continue if the seriousness of these problem areas is lessened. REFERENCES Chepil, W. S. 1946. Germination of weed seeds. Longevity, periodicity of germination and viability of seeds in cultivated sods. Sci. Agric. 26:307.

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334 TACTICS FOR PREVENTION AND MANAGEMENT Dunham, R. S., R. G. Robinson, and R. N. Anderson. 1958. Crop rotation and associated tillage practices for controlling annual weeds in flax and reducing the weed seed population of the soil. Minn. Agric. Exp. Stn. Tech. Bull. 230. LeBaron, H. M., and J. Gressel, eds. 1982. Herbicide Resistance in Plants. New York: John Wiley and Sons. Mudge, L. C., B. J. Gossett, and T. R. Murphy. 1984. Resistance of goosegrass (Eleusine indica) to dinitroaniline herbicides. Weed Sci. 32:591. Roberts, H. A. 1968. The changing population of viable weed seeds in arable soil. Weed Res. 8:253. Schweizer, E. E., and R. L. Zimdahl. 1984a. Weed seed decline in irrigated soil after six years of continuous corn (Zea mays) and herbicides. Weed Sci. 32:76. Schweizer, E. E., and R. L. Zimdahl. 1984b. Weed seed decline in irrigated soil after rotation of crops and herbicides. Weed Sci. 32:84. Shaw, W. C. 1957. Basic research the key to efficient weed control in cotton in the future. Rep. Proc. Beltwide Cotton Production-Mech. Conf. 11:5-9. Memphis, Tenn.: National Cotton Council of America.