C O N S E R V A T I O N I S S U E S ABSTRACT: There are several alternative herbicides with different modes of action for control of invasive plants in natural areas. Of the four classes of herbicides commonly used on invasive plants in natural areas of Florida, the acetolactate synthase (ALS) inhibitors, imazapyr, imazapic, and metsulfuron methyl, are the most likely to select for resistance. Invasive plants that have attributes such as numerous seed or spore production and log distance dispersal capabilities are most likely to develop resistance to herbicides following repeated application. In Florida, these species include Old World climbing fern (Lygodium • microphyllum), cogongrass (Imperata cylindrica), torpedo grass (Panicum repens), and tropical soda apple (Solanum viarum). The best scenario for treatment of invasive plants in Florida’s natural areas, to minimize potential for development of resistance, is to rotate herbicides with different modes of action The Potential for or use tank mixtures of two or more herbicides with different modes of action.
Herbicide Resistance Index Terms: herbicide resistance, natural areas, Florida in Non-Native Plants INTRODUCTION (Heap 2007). Currently, there are ca. 313 in Florida’s Natural biotypes of plants that are resistant to Herbicides are chemicals used to control herbicides (Heap 2007). Areas unwanted plants. They target specific plant processes such as amino acid production, In agricultural systems where multiple growth regulator hormones, and photosyn- weeds are targeted, the development of Jeffrey T. Hutchinson1 thesis. In some cases, herbicides can be herbicide resistance by weedy plants has used, through a variety of mechanisms such been associated with the repeated use of Gregory E. MacDonald as deactivation or metabolism and dosage a single herbicide mode of action (Kudsk Kenneth A. Langeland rates, to selectively control specific weed and Streibig 2003). The development of University of Florida species without harming other vegetation. resistance to herbicides by plants is similar Agronomy Department Herbicides have been extensively used for to resistance development of insecticides Center for Aquatic and Invasive Plants over 60 years in a variety of crop and non- by insects (Georghiou 1986). Within the 7922 NW 71st Street crop areas (Anderson 1996). Repeated use population of a particular weedy species, Gainesville, Florida 32653 of certain herbicides has resulted in the lack there exists a small fraction of the popula- of control for certain species, which lead to tion that is less sensitive to the herbicide the discovery of herbicide resistance. (Georghiou 1986). Broad-scale resistance to herbicides occurs only if the resistance • In 2005, the Florida Department of Envi- trait is present in the population and sub- ronmental Protection’s Bureau of Upland sequently selected for by herbicide use Invasive Plant Management funded over (Maxwell and Mortimer 1994). Addition- $9.4 million for invasive plant treatment ally, the development of herbicide-toler- in upland habitat that consisted primarily ant crops amplifies the risk of increased of herbicide treatment (FLDEP 2006). The selection pressure for resistance on weed majority of the county, state, and federal species that are sprayed several times agencies have invasive plant management annually with the same herbicide type in units whose sole purpose is controlling herbicide-resistant crop systems (Kudsk invasive plants. With the large number of in- and Streibig 2003). vasive plant species that occur in Florida’s natural areas (Gordon 1998; Langeland Herbicide resistance can occur through and Burks 1998), it is likely that some target-site or non-target site based mecha- invasive plants may develop resistance to nisms (Heap and LeBaron 2001). Tar- one or more herbicides, creating greater get-site resistance is the most common problems for land managers. mechanism of resistance and occurs when enzymes needed for plant metabolism are Herbicide resistance is the inherited ability modified (generally an altered amino acid 1 Corresponding author: of a plant population to survive herbicide sequence), which eliminates the ability [email protected]fl.edu; 352-392-9981 application that is normally lethal to the ma- of the herbicide to inactivate the enzyme jority of the plants of that species (Powles (Heap and LeBaron 2001). Weeds resistant et al. 1997). Plant resistance to herbicides to target-site inhibiting herbicides are typi- Natural Areas Journal 26:258–263 was first reported by Ryan (1970) and has cally controlled by including an herbicide been increasing in frequency each year tank mix with a different type (i.e., targets
258 Natural Areas Journal Volume 27 (3), 2007 a different enzyme or target site of action) There have been at least 35 herbicide resis- The ALS inhibiting herbicide class was in- or rotating with a different herbicide type. tant weed biotypes reported from roadsides, troduced commercially in 1982. The major Non-target site resistance is less common railroads, and industrial sites (Heap and advantage of ALS herbicides is their high and occurs when the plant metabolizes or LeBaron 2001) that are typically treated specific activity and low dosage rate, which sequesters the herbicide making it inactive with herbicides at a frequency much less is often 100 times lower than conventional or reducing the amount that is translocated than production agriculture sites. Thus, the herbicides such as glyphosate, triclopyr, through the plant. Populations of weeds potential for development of resistance in and 2,4-D (Fairbrother and Kapustka that exhibit non-target site resistance may natural area weeds is high. One advantage 2001). However, since 1982, there are be of greater concern since resistance also to treating natural area weeds versus agri- now more weed species (n = 95) resistant develops to herbicides of different modes cultural weeds is that there are often several to this class of herbicides than any other of action (Preston 2004). alternative herbicides with different modes class (Tranel and Wright 2002; Heap 2007). of action for control of invasive plants in Weed biotypes that have developed resis- Additionally, some plants develop cross re- natural areas. It is therefore believed that tance to ALS herbicides seldom exhibit sistance to several types of herbicides with weeds in non-crop sites that develop resis- cross-resistance to herbicides with other the same mode of action or multiple-resis- tance to one herbicide may easily be treated modes of action (Boutsalis and Powles tance to two or more types of herbicides with an herbicide with a different mode of 1995); thus, alternative herbicides are avail- with different modes of action (Moss 1990; action or tank mixture of two herbicides able to treat resistant biotypes. In Europe, Christopher et al. 1991; Walsh et al. 2004). (Heap and LeBaron 2001). where ALS herbicides have been used in Some weeds in agricultural systems have rotation with herbicides that act through a become resistant to low dose, high potency different mode of action, there have been HERBICIDES USED IN NATURAL herbicides, such as acetolactate synthase few weeds that have developed resistance AREAS OF FLORIDA (ALS) inhibitors, after only several years to ALS herbicides (Heap 1997). of exposure, indicating that this class of The primary herbicides used to control herbicides exerts a strong selective pres- Glyphosate was introduced commercially invasive plants in Florida natural areas are sure on plants (Lovell et al. 1996; Heap in 1974 and is one of the most widely used listed in Table 1 (Langeland and Stocker 1997). It also suggests that the frequency herbicides in the world (Baird et al. 1971). 1997). These include acetolactate synthase for resistance may be higher with this Until recently, this compound was primar- (ALS) inhibitors (imazapyr, metsulfuron chemistry class. The increase of resistance ily used in natural areas and industrial methyl, and imazapic), EPSP synthase in weeds to ALS inhibitor herbicides may sites; with the advent of herbicide resistant inhibitors (glyphosate), synthetic auxin have led to the development of herbicide crops, its use has magnified greatly. Yet, (triclopyr and 2,4-D), and photosystem resistant crops because it was believed that with widespread use over ca. 31 years, II inhibitors (hexazinone). The EPSP better weed control may be obtained in a only eight weed biotypes have developed synthase and synthetic auxin herbicides glyphosate, an EPSP Synthase inhibitor- resistance to glyphosate (Heap 2007). How- have resulted in less resistance in agricul- based cropping system (Owen and Zelaya ever, glyphosate-resistant crops have only tural weeds than the ALS inhibitors and 2005). ALS inhibitor herbicides are ef- been available for a relatively short period, photosystem II inhibitors. The ALS and fective against broadleaf plants and some and this increased pressure is thought to photosystem II inhibitors now account for grasses, while glyphosate is a non-selective greatly increase the likelihood of resistance the majority of the agriculture weeds that herbicide effective against all plants. development in weeds (Owen and Zelaya have developed resistance (Heap 2007). 2005). Horseweed (Conyza canadensis)
Table 1. The most commonly used herbicides in natural areas of Florida (Langeland and Stocker 1997).
Herbicides used in Number of Resistant Natural Areas Product Name Mode of Action Plants (Heap 2007) Chemical Family Glyphosate Roundup, Rodeo, etc. EPSP Synthase 8 Glycines 2,4-D 2,4-D Synthetic Auxin 24 Phenoxy Triclopyr Garlon 3A and 4 Synthetic Auxin Carboxylic acid Imazapyr Arsenal ALS Inhibitor 93 Imidazolinones Metsulfuron methyl Escort XP ALS Inhibitor Sulfonylureas Imazapic Plateau ALS Inhibitor Imidazolinones Hexazinone Velpar Photosystem II Inhibitor 65 Triazinone
Volume 27 (3), 2007 Natural Areas Journal 259 developed resistance to glyphosate within in the early 1950s and have 65 weeds that were treated several times (Michel et three years of use in glyphosate-resistant or biotypes with resistance (Kudsk and al., 2004). Dotted duckweed (Landoltia soybeans (VanGessel 2001). Streibig 2003; Heap 2007). The first re- punctata), a non-native floating aquatic ported case of herbicide resistance for any plant, has developed a 50-fold resistance Several factors may contribute to the lack weed (Senecio vulgaris) was reported for to diquat and cross-resistance to paraquat of resistance from glyphosate use. These photosystem II inhibitors by Ryan (1970). (Tyler Koschnick, University of Florida, include lack of soil residual activity and In 1997, it was estimated that more than pers. comm.). These aquatic examples the absence of metabolic degradation or three million ha were infested with pho- from Florida appear to follow a trend deactivation of glyphosate by plants (Baylis tosystem II inhibitor resistant weeds, but observed in California where herbicide 2000). Rigid ryegrass (Lolium rigidum) these weeds can be controlled with herbi- resistance is most widespread for aquatic developed resistance to glyphosate after 10 cides of different modes of action (Heap weeds in commercial rice fields (Prather treatments over a 15-year period, provid- 1997). Photosystem II inhibitor herbicides, et al. 2000). ing a forewarning that other weeds may such as hexazinone, are only occasionally eventually become glyphosate resistant used in natural areas in Florida. They are Perennial plants, including those with following multiple treatments (Heap 1997). used in forestry, pastures, rangelands, and vegetative reproductive structures, are less Italian ryegrass (Lolium multiflorum) devel- right-of-way areas. likely to develop resistance than weeds with oped resistance to glyphosate after being annual life cycles, which produce abundant treated three times annually for 8-10 years seeds and have greater genetic diversity PROSPECTS OF NATURAL AREA (Perez and Kogan 2003). Recent evidence (Prather et al. 2000). High seed production WEEDS DEVELOPING HERBICIDE also indicates that a weedy morning glory and germination rates increase the likeli- RESISTANCE (Ipomoea purpurea) of agricultural sites hood that a resistant biotype will occur in the southeastern United States has de- within a population of plants as susceptible Based on statistics compiled by Heap veloped resistance to glyphosate (Baucom plants are eliminated by follow-up treat- (2007), there is a greater chance of in- and Mauricio 2004). Some concern has ments. The majority of the invasive plants vasive plants in natural areas developing been voiced that weeds associated with of Florida’s natural areas are perennial or resistance to ALS inhibitor and photosytem glyphosate-resistant crops may spread into woody plants; thus, it would be expected II inhibitor herbicides than synthetic auxin natural areas (Marshall 1998), but most that resistance for most invasive plants in and EPSP synthase inhibitor herbicides. weeds of agroecosystems are poor competi- natural areas of Florida is less probable than Factors that contribute to resistance in tors outside the agricultural environment in agricultural systems where the majority plants may include the repeated use of a (Hancock and Hokanson 2001). of the weeds are annuals. single herbicide over large areas, little or no use of other herbicides with alternative Synthetic auxin inhibiting herbicides, such No shrubs or trees are known to have devel- modes of action, high efficacy of herbicides as triclopyr and 2,4-D, were first discovered oped resistance to herbicides (Heap 2007). on the plant at the rate used, and long soil in the 1940s but only 24 weeds to date Melaleuca (Melaleuca quinquenervia) and residual activity of the herbicide (Tranel have developed resistance to this class of Brazilian pepper (Schinus terebinthifolius) and Wright 2002). High seed production herbicides (Heap 2007). The first reported exhibit some of the characteristics of plants combined with a high germination rate may case of an auxin resistance weed was from that have developed herbicide resistance. accelerate herbicide resistance, because New Zealand in 1981 (Heap 2007). Auxin These characteristics include: (1) inva- susceptible plants are removed and indi- inhibiting herbicides are selective towards sion over large areas in central and south viduals that retain resistant genes remain broadleaf plants and have little effect on Florida, (2) abundant seed production, and in the population (Prather et al. 2000). most grasses. Yellow starthistle (Centaurea (3) repeated herbicide treatments on many solstitialis) is a broadleaf weed of range- populations. It could be theorized that The first occurrence of herbicide resis- lands in the western United States and has multiple treatments on these two invasive tance to fluridone in an aquatic weed was developed cross-resistance to four auxin plants over large areas in Florida would hydrilla (Hydrilla verticillata) in Florida inhibitors, including triclopyr and 2,4-D have been selected for resistant biotypes; in 1999. The mechanism of this resistance (Miller et al. 2001). However, considering but, at present, this has not been observed. was recently reported (Michel et al. 2004), the heavy use of this class of herbicides In addition, several herbicides with dif- and now several populations are currently over the past eight decades, relatively few ferent modes of action (e.g., glyphosate, resistant to fluridone. Fluridone is the only weeds have developed resistance when triclopyr, and imazapyr) are approved for approved systemic herbicide approved to compared to ALS herbicides. For example, treatment of these plants, and biocontrols treat hydrilla (Michel et al. 2004). Fluri- 2-4,D has been used for almost 60 years have been released for both species. More- done was approved for aquatic use in 1986, in Florida to control water hyacinth (Eich- over, most large scale aerial treatments so Florida populations of hydrilla have de- hornia crassipes) without the development of melaleuca stands use tank mixes of veloped resistance to this herbicide in less of resistance (FLDEP 2005). imazapyr and glyphosate. Thus, if a highly than 20 years. Hydrilla biotypes resistant invasive shrub or tree in Florida’s natural to fluridone were found in Florida lakes Photosystem II inhibitors were introduced areas develops resistance to an herbicide,
260 Natural Areas Journal Volume 27 (3), 2007 there are alternative herbicides with dif- of Florida, the ALS inhibitors (imazapyr, CONCLUSION ferent modes of action that can be used imazapic, and metsulfuron methyl) are to control these species. most likely to select for resistance. Within Continuous use of herbicides with the same the past few years, imazapyr and met- mode of action on a specific invasive plant Invasive plants in natural areas of Florida sulfuron methyl have been approved for will inevitably lead to resistance (Kudsk that appear to be the most susceptible to use over wetlands, and are used to treat and Streibig 2003). The rate of herbicide developing herbicide resistance are grasses. infestations of melaleuca and Old World use in natural areas is much less intense Many invasive grasses in Florida reproduce climbing fern (Lygodium microphyllum), than in agriculture systems where some both sexually and vegetatively, produce respectively. Imazapic is also being tested crop-systems may be treated 2-3 times numerous amounts of seeds, are difficult on a number of invasive plants, including annually. To effectively eliminate repro- to eradicate, and require multiple herbi- air potato (Dioscorea bulbifera), Old World duction potential, management of invasive cide treatments for control. In agricultural climbing fern, and Japanese climbing fern plants in natural areas is dependent on systems, the grass family has 27 species (Lygodium japonicum). Due to recent use eliminating or reducing seed and spore that have developed resistance, cross- of ALS inhibitor herbicides on certain production. Extended use of herbicides resistance, or multiple-resistance to the invasive plants, populations of these plants below the recommended label rate may four classes of herbicides typically used in being treated should be closely monitored select for resistance and replenish the seed natural areas (Heap 2007). In natural areas, for development of resistance. bank with resistant seeds (Doyle and Stypa there are several invasive grasses, includ- 2004) that in time will dominant a popu- ing West Indian marsh grass (Hymenachne Herbicide resistance in many weeds is lation and potentially spread the resistant amplexicaulis), cogongrass (Imperata nuclear inherited, controlled by dominant biotype into other areas. cylindrica), silk reed (Neyraudia reynau- alleles, and expressed in gametophytes and diana), torpedo grass (Panicum repens), sporophytes (Richter and Powles 1993; Although there are no known upland inva- Napier grass (Pennisetum purpureum), Darmency 1994). Old World climbing sive plants in natural areas of Florida that natal grass (Rhynchelytrum repens), and fern may be analogous in some ways to have developed herbicide resistance, there paragrass (Urochloa mutica) (Langeland Conyza canadensis, a problematic weed are some herbicides (e.g., ALS inhibitors) in and Burks 1998; FLEPPC 2005). Control of agricultural sites. Horseweed has de- use that have caused rapid development of of these grasses is difficult and requires veloped cross- and multiple-resistance to resistance in agricultural weeds throughout multiple applications of herbicide, possibly herbicides, is primarily self pollinated, the world. Only five years after the intro- creating the selection pressure needed to and produces many seeds that are wind duction of the ALS inhibitors, two species develop herbicide resistant biotypes. dispersed (Owen and Zelaya 2005). Old of agriculture weeds developed resistance World climbing fern has the potential to (Tranel and Wright 2002). Application of Other families that have developed her- cross-fertilize (Lott et al. 2003) and is dose rates below the recommended label bicide resistance in agricultural systems primarily dispersed by wind blown spores. rate using an ACCase inhibiting herbicide and that have related invasive species in In some natural areas, greater than eight ap- have been shown to select for resistance in Florida’s natural areas include morning plications of glyphosate have been applied rigid ryegrass in less than three generations glory (Convolvulaceae), dayflower (Com- to Old World climbing fern to maintain (Neve and Powles 2005). Studies modeling melinaceae), spurge (Euphorbiaceae), and control – a situation that may exert strong herbicide resistance in weeds indicate that nightshade (Solanaceae) (Heap 2007). In selection pressure for resistance. With the smaller populations over a large area are natural areas, members of these families ability for self-fertilization, wind dispersed less likely to develop resistance because include water-spinach (Ipomoea aquatica), spores from a single resistant plant could rare resistance genes are less likely to be green wandering Jew (Tradescantia rapidly spread the resistant biotype of the present (Diggle et al. 2003). These models fluminensis), Chinese tallow (Sapium fern across large areas. Being a relatively would likely predict that invasives that are sebiferum), wetland nightshade (Solanum recent invader to natural areas in south widespread in Florida (such as Old World tampicense), turkey berry (Solanum tor- Florida, Old World climbing fern has climbing fern, cogongrass, torpedo grass, vum), and tropical soda apple (Solanum been exposed to repeated herbicide treat- and tropical soda apple) produce numer- viarum) (Langeland and Burks 1998). Of ments for less than 10 years, a threshold ous spores or seeds and have long distance these, tropical soda apple has been the most well below the time frame at which some dispersal mechanisms; these invasives problematic, invading both agricultural and weedy plants have developed herbicide have the greatest potential to develop natural areas of Florida. A close relative of resistance in agricultural systems (Primiani resistance. tropical soda apple, black nightshade (So- et al. 1990; LeBaron 1991). However, the lanum americanum) is the most prevalent tremendous number of spores increases the In most natural areas of Florida, the use herbicide-resistant weed in Florida (Heap frequency of resistance when compared of herbicide and biocontrol are the only 2007) exhibiting resistance to paraquat. with most angiosperms. practical methods to control invasive plants. Many invasive plants occur in highly iso- Of the four classes of herbicides commonly lated areas that can only be reached by used on invasive plants in natural areas foot, airboat, or helicopter, making treat-
Volume 27 (3), 2007 Natural Areas Journal 261 ment time consuming, difficult, and costly. plant management. Additional research the probability of herbicide resistance in Prescribed fire, mechanical treatments, and activities involve fundamental studies into finite weed populations. Weed Research hand removal are options, but are limited in mechanisms of herbicide action and weed 43:371-382. use due to cost, limited personnel, and other resistance. His teaching responsibilities Doyle, P., and M. Stypa. 2004. Reduced herbi- problems (e.g., smoke management). include courses in Weed Science, Her- cide rates – a Canadian perspective. Weed Technology 18:1157-1165. bicide Technology, and Plant/Herbicide The best scenario for treatment of invasive Interactions. Fairbrother, A., and L.A. Kapustka. 2001. Low- plants in natural areas is to rotate herbicides dose, high-potency herbicides: a historical perspective of environmental concerns to with different modes of action or use tank Kenneth Langeland is Professor and Ex- frame the issues. Pp. 1-17 in S.A. Ferenc, ed., mixtures of two or more herbicides with tension Specialist for aquatic and upland Impacts of Low-Dose, High-Potency Her- different modes of action, since in most invasive plants at the University of Florida, bicides on Nontarget and Unintended Plant cases only one invasive plant is being tar- IFAS Agronomy Department and Center Species. SETAC Press, Pensacola, Fla. geted. Regardless, if a single herbicide is for Aquatic and Invasive Plants. He is well [FLDEP] Florida Department of Environmental being utilized to control an invasive plant, known for his extension activities, such as Protection. 2005. Invasive plant management strict monitoring of the treated population the many short courses and other training history: the non-native aquatic plant invad- is advised in order to detect potential resis- he provides in Florida and elsewhere. His ers. Available online
262 Natural Areas Journal Volume 27 (3), 2007 – a two-edged sword. Weed Research Maxwell, B.D., and A.M. Mortimer. 1994. and management. Advances in Agronomy 43:90-102. Selection for herbicide resistance. Pp. 1-25 58:57-93. Langeland, K.A., and R.K. Stocker. 1997. Con- in S.B. Powles and J.A.M. Holtum, eds., Prather, T.S., J.M. DiTomaso, and J.S. Holt. trol of non-native plants in natural areas of Herbicide Resistance in Plants: Biology 2000. History, mechanisms, and strategies Florida. Institute of Food and Agricultural and Biochemistry. Lewis Publishers, Boca for prevention and management of herbicide Sciences Publication SP242, University of Raton, Fla. resistant weeds. Proceedings of the Califor- Florida, Gainesville. Michel, A., R.S. Arias, B.E. Scheffler, S.O. nia Weed Science Society 52:155-163. Langeland, K.A., and K. Craddock Burks (eds.). Duke, M. Netherland, and F.E. Dayan. 2004. Preston, C. 2004. Herbicide resistance in weeds 1998. Identification and Biology of Somatic mutation-mediated evolution of endowed by enhanced detoxification: com- Non-Native Plants in Florida’s Natural herbicide resistance in the nonindigenous plications for management. Weed Science Areas. University of Florida Press, Gaines- invasive plant hydrilla (Hydrilla verticillata). 52:448-453. Molecular Ecology 13:3229-3237. ville. Primiani, M., M.J C. Cotterman, and L.L. LeBaron, H.M. 1991. Distribution and serious- Miller, T.W., S.L. Shinn, and D.C. Thill. 2001. Saari. 1990. Resistance of kochia (Kochia ness of herbicide resistant weed infestations Cross-resistance in and chemical control of scoparia) to sulfonylurea and imidazolinone world wide. Pp. 27-55 in Z.C. Casely, G.W. auxinic herbicide-resistant yellow starthistle herbicides. Weed Technology 4:169-172. (Centaurea solstitialis). Weed Technology Cussans, and R.K. Atkin, eds., Herbicide Richter, J., and S.B. Powles. 1993. Pollen ex- 15:293-299. Resistance in Weeds and Crops. Butterwarth pression of herbicide target site resistance Heneman, Oxford, U.K. Moss, S.R. 1990. Herbicide cross-resistance in genes in annual ryegrass (Lolium rigidum). Lott, M.S., J.C. Volin, R.W. Pemberton, and D.F. slender foxtail (Alopecurus myosuroides). Plant Physiology 102:1037-1041. Weed Science 38:492-496. Austin. 2003. The reproductive biology of Ryan, G.F. 1970. Resistance to common the invasive ferns Lygodium microphyllum Neve, P., and S. Powles. 2005. Recurrent selec- groundsel to simazine and atrazine. Weed and L. jaonicum (Schizaeaceae): implica- tion with reduced herbicide rates results in Science 18:614-616. tions for invasive potential. American the rapid evolution of herbicide resistance Tranel, P.J., and T.R. Wright. 2002. Resistance Journal of Botany 90:1144-1152. in Lolium rigidum. Theoretical and Applied of weeds to ALS-inhibiting herbicides: Genetics 110:1154-1166. Lovell, S.T., L.M. Wax, M.J. Horak, and D.E. what have we learned? Weed Science Peterson. 1996. Imidazolinone and sulfo- Owen, M.D.K., and I.A. Zelaya. 2005. Her- 50:700-712. nylurea resistance in biotypes of common bicide-resistant crops and weed resistance VanGessel, M.J. 2001. Glyphosate-resistance waterhemp (Amaranthus rudis). Weed Sci- to herbicides. Pest Management Science horseweed from Delaware. Weed Science ence 44:789-794. 61:301-311. 49:703-705. Marshall, G. 1998. Herbicide-tolerant crops Perez, A., and M. Kogan. 2003. Glyphosate- Walsh, M.J., S.B. Powles, B.R. Beard, B.T. – real farmer opportunity or potential en- resistant Lolium multiflorum in Chilean Parkin, and S.A. Porter. 2004. Multiple-her- vironmental problem? Pesticide Science orchards. Weed Research 43:12-19. 52:394-402. bicide resistance across four modes of action Powles, S., C. Preston, I. Bryan, and A. Jut- in wild radish (Raphanus raphanistrum). sum. 1997. Herbicide resistance: impact Weed Science 52:8-13.
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