Characterization of Selected Common Lambsquarters (Chenopodium album) Biotypes with Tolerance to Glyphosate
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1 Weed Science : Characterization of Selected Common Lambsquarters (Chenopodium album) Biotypes with Tolerance to Glyphosate Andrew M. Westhoven, Greg R. Kruger, Corey K. Gerber, Jeff M. Stachler, Mark M. Loux, and William G. Johnson* Biotypes of common lambsquarters with tolerance to glyphosate have been identified in a number of states, but little is known about their fitness characteristics. Field and greenhouse studies were conducted to characterize the response of selected glyphosate-tolerant common lambsquarters biotypes to glyphosate, and also their biological and reproductive characteristics. In a greenhouse dose-response study, GR 50 and GR 90 values for four tolerant biotypes ranged from 1.48 to 3.22 and 8.73 to 18.7 kg ae ha 21, respectively, compared to 0.57 and 2.39 kg ae ha 21, respectively, for a glyphosatesensitive biotype. In a field dose-response study, the GR 50 and GR 90 values were 0.06 and 0.48 kg ae ha 21, respectively, for a tolerant biotype, compared to and 0.19 kg ae ha 21, respectively, for the sensitive biotype. The growth rate, time until flowering, and seed production of eight tolerant and two sensitive biotypes was evaluated in a field study. The tolerant biotypes grew taller, amassed more leaf area and dry weight, and advanced through growth stages more rapidly than sensitive biotypes during the early portion of the growing season. The tolerant biotypes were taller than sensitive biotypes at 6 and 10 wk after transplanting, but had lower dry weight at maturity. Tolerant biotypes initiated flower primordia approximately 6 to 8 wk after transplanting, whereas sensitive biotypes required 12 wk. However, no apparent fitness penalties were observed in glyphosate-tolerant biotypes based on seed-production estimates. Nomenclature: Glyphosate; common lambsquarters, Chenopodium album L. Key words: Fitness, glyphosate dose response, glyphosate tolerance. Common lambsquarters is one of the most problematic weeds to control in agronomic crops in Indiana (Gibson et al. 2005). Common lambsquarters is a summer annual that is typically one of the first weeds to emerge in the spring (Buhler et al. 1997; Hilgenfeld et al. 2004). It can be difficult to control in soybean [Glycine max (L.) Merr.] because of the relatively rapid early-season growth in cool weather, the ability to germinate at shallow depths (Uva et al. 1997), and the lack of effective postemergence herbicides. Common lambsquarters has been shown to compete with soybean, ultimately reducing soybean yields (Conley et al. 2003; Crook and Renner 1990; Harrison 1990). Common lambsquarters can be found in the most common tillage and crop rotation practices in the north central region (Cardina et al. 2002; Thomas et al. 2004), and is one of the most widespread weed species observed in Indiana. In a late-season field survey conducted in 2003 through 2005, common lambsquarters was observed in 14% of randomly surveyed soybean fields (Davis et al. 2007). Currently, common lambsquarters is listed as the fourth most important herbicide-resistant weed species in the world, with biotypes resistant to triazines, ureas and amides, and acetolactate synthesis (ALS) inhibitors (Heap 2007). In glyphosate-based systems, weed scientists have concluded that weed shifts have occurred, with common lambsquarters becoming more problematic (Culpepper 2006). Hite et al. (2007) documented the first differential response of glyphosate sensitivity between two common lambsquarters biotypes that were collected in Application of 0.84 kg ae ha 21 of glyphosate resulted in a 49% difference in visual control between two biotypes 30 d after treatment (DAT). Biotypes with tolerance to glyphosate have been identified in eight states (Curran 2005; Harder et al. 2007; Kniss et al. 2007; DOI: /WS * First, second, and sixth authors: Department of Botany and Plant Pathology, Purdue University, 915 West State Street, West Lafayette, IN 47907; third author: Department of Agronomy, Purdue University, 915 West State Street, West Lafayette, IN 47907; fourth and fifth authors: The Ohio State University, 2021 Coffey Road, Columbus, OH Corresponding author s wgj@purdue.edu Loux et al. 2005; Schuster et al. 2007). Research has been conducted to investigate factors aside from glyphosate tolerance that may reduce common lambsquarters control with glyphosate, including stem-boring insects (Harder et al. 2007), large plant size (Boerboom et al. 2006; Schuster et al. 2007), short photoperiods (Kniss et al. 2005), low glyphosate rate, rainfall following application, and dust (Boerboom et al. 2006). Boerboom et al. (2006) observed up to 8.9-fold greater tolerance to glyphosate when applied to 20-cm-tall common lambsquarters plants, compared to 10-cm-tall plants. Schuster et al. (2007) reported up to 5.5-fold greater tolerance to glyphosate when applied to 15-cm-tall common lambsquarters plants compared to 2.5-cm-tall plants. However, growth stage and differences in flowering dates among the biotypes investigated were not mentioned in these reports. A number of researchers have examined the growth characteristics of triazine-sensitive and -resistant biotypes. Marriage and Warwick (1980) observed more rapid seedling growth of triazine-sensitive versus resistant common lambsquarters biotypes under a noncompetitive environment. However, the resistant biotype accumulated greater vegetative, floral, and total biomass than the sensitive biotypes during the growing season, but biomass was similar at plant maturity. Similar results were reported by Warwick and Black (1981). Bulke et al. (1985) and Parks et al. (1996) found greater aboveground total and reproductive biomass production of triazine-sensitive biotypes. In contrast, Jansen et al. (1986) found that a resistant biotype was more vigorous than a sensitive biotype under noncompetitive environments. However, seed-production estimates among the resistant and sensitive biotypes were not reported. The biological characteristics of weeds with tolerance or resistance to glyphosate has been investigated by a number of researchers. Degennaro and Weller (1984) documented leafmorphology differences among biotypes of field bindweed (Convolvulus arvensis L.) and that biotypes that required more days to flower also had fewer number of flowers plant 21. However, differences between sensitive and resistant biotypes were not reported. A glyphosate-resistant biotype of common Westhoven et al.: Glyphosate-tolerant common lambsquarters N 685
2 ragweed was 1.6- to 2-fold shorter and had fewer leaf nodes compared to a sensitive biotype (Sellers et al. 2004). However, differences in leaf area, dry weight, and relative growth rate were not observed at any stage of growth. Glyphosate-resistant Palmer amaranth was shorter (Haider et al. 2007), but did not appear to incur a biomass accumulation penalty compared to the sensitive biotypes (Vencill et al. 2006). It is well documented that common lambsquarters has adapted to numerous agronomic practices, is competitive with crops, and control with glyphosate can be erratic. However, there are little comparative data on the biological characteristics of glyphosate-tolerant vs. -sensitive common lambsquarters biotypes. The objective of these studies was to quantify the level of glyphosate tolerance among selected biotypes, and compare the biological characteristics of glyphosate-sensitive and -tolerant common lambsquarters biotypes. Materials and Methods Materials and Greenhouse Conditions. There were three separate studies conducted: a greenhouse dose-response study, a field dose-response study, and a field biology study. Preliminary studies were conducted to identify the glyphosate-tolerant or -sensitive biotypes used in these studies and are described in Westhoven (2008). The glyphosate-tolerant biotypes used in the greenhouse dose-response study were from the counties of Benton, Huntington, Jay, and Ripley in Indiana. The glyphosate-sensitive biotype was from Jefferson County, Indiana. Ripley and Jefferson County biotypes were used in the field dose-response study. The biotypes used in the field biology study included the Benton, Huntington, Jay, Ripley, and Jefferson county biotypes, plus tolerant biotypes from the counties of Darke (two different biotypes), Mercer, and Preble, Ohio. The other sensitive biotype used in this study was from Coshocton County, Ohio. For all studies, seeds were treated 1 in 95.9% H 2 SO 4 for 15 min, washed with running water for 45 min, and dried for approximately 24 h at 24 C (Hocombe 1961). For the greenhouse dose-response study, treated seeds were planted 0.5 cm deep in Sun-Gro Redi-Earth 2 germinating potting soil mixture in 12 by 12 by 12 cm plastic pots. One week after emergence, plant densities were thinned to four plants per pot per biotype. Plants were watered daily and fertilized every 5 d with a fertilizer solution 3 to maintain active growth. Greenhouse growing conditions were maintained at a 29/18 C day/night temperature rotation. Plants were grown under natural lighting supplemented with high-pressure sodium lamps that provided 350 mmol m 21 s 21 photosynthetic photon flux density and a 16-h photoperiod. For the field dose-response study and the field biology study, treated seeds were planted at the same seed depth in potting soil, as used earlier, in 288-cell plastic trays. These trays were maintained in the greenhouse under the same conditions as previously described. When the plants reached a three to four node growth stage, they were transplanted into the field study site. Greenhouse Dose-Response Study. A total of four glyphosate-tolerant (T) biotypes and one sensitive (S) biotype were used in this study. When common lambsquarters plants reached a seven to eight node growth stage T biotypes were treated with 0, 0.084, 0.42, 0.84, 2.1, 4.2, 8.4, 12.6, and 21 kg ae ha 21 and the S biotype with 0, 0.008, 0.084, 0.21, 0.42, 0.84, 2.1, 4.2, and 8.4 kg ae ha 21 of glyphosate. 4 All treatments were applied with 2.8 kg ha 21 ammonium sulfate 5 and 0.5% (v/v) nonionic surfactant. 6 The treatments were applied with the use of a compressed-air laboratory sprayer. To address spray coverage issues, treatments were applied with 8001E nozzle 7 at 95 L ha 21 carrier volume, the plants were rotated 90 degrees on the spray table, and treated again with 95 L ha 21 carrier volume at a pressure of 275 kpa. All aboveground plant biomass was harvested 21 DAT. Plant biomass was dried for 5 d in a forced-air drying room at 50 C, and then weighed to obtain dry weights. Treatments were arranged as a two-way factorial in a randomized complete block with four replications, where the factors were biotype and glyphosate rate, and the experiment was repeated. Prior to initial analysis in SAS, 8 the dry weights of all plants in each pot were averaged and converted to a percentage of the untreated control. Because there was no significant treatment-by-experiment interaction, data from both studies were pooled and fit to a dose-response curve to estimate glyphosate GR 50 and GR 90 values with the use of R software 9 (Knezevic et al. 2007). The GR 50 is defined as the herbicide dose required to reduce plant biomass 50% compared to the untreated control. A hormesis model (Equation 1) was used to evaluate the response, and a lackof-fit test indicated that the regression model accurately described the data (P ). Hormesis is an effect where a toxic substance acts as a stimulant in small doses, but an inhibitor in large doses. Nonlinear regression parameters were predicted with the use of a modified four-parameter logistic model that relates actual dry weight means as the percentage of the untreated control (Y ) to the herbicide rate (x): Y ~ 0 z d { 0 z f exp ½{1= ðx0:25þš 1 z expfb½logðþ{ x logðþ e Šg In this equation, d is the upper response limit, f is the hormesis estimate, e is the inflection point, and b is the slope of the curve around the GR 50. Independent t tests were used to determine significance of GR 50 and GR 90 values between all biotypes at P The level of tolerance was determined by calculating a T/S ratio (GR 50 for the T biotype divided by GR 50 for the S biotype). The same procedure was performed to calculate T/S ratios based on GR 90 values. Field Dose-Response Study. A field dose-response study was conducted in 2007 at the Agronomy Center for Research and Education, located near West Lafayette, IN. The soil type was a Raub silt loam (fine silty, mixed, superactive, mesic Aquic Argiudolls; 35% sand, 65% silt, and 10% clay) with a ph of 6.3 and 3% organic matter with one S and one T biotype. Seeds germinated in the greenhouse 6 d apart and three to four node plants were transplanted on June 12 and 18, respectively, for a total of two experimental runs. Plots were 2.3 by 2.3 m in size and plants were transplanted at a 10-cm spacing. To ensure plant establishment, plots were irrigated with the use of irrigation tape 10 for at least 2 wk after planting with a total of 1 to 2 cm of water per irrigation. When the plants were 10 to 20 cm tall (six to eight node growth stage), the glyphosate treatments were applied perpendicular to the plant rows with a 1.5-m boom. Treatments were applied in a volume of 142 L ha 21, at 4.8 km hr 21 with the use of ½1Š 686 N Weed Science 56, September October 2008
3 Table 1. Regression parameters for greenhouse dose response based on dry weight of common lambsquarters. The glyphosate-tolerant biotypes include Ripley, Jay, Huntington, and Benton. A lack-of-fit test indicated that the regression model accurately described the data (P ). Regression parameters d a f b e GR 50 (SE) GR 90 (SE) b T/S ratio 50 c T/S ratio kg ae ha Ripley (0.29) (4.00) Jay (0.39) (4.52) Huntington (0.20) (4.31) Benton (0.28) 8.73 (1.99) Sensitive (0.05) 2.39 (0.60) 1 1 a Abbreviations: d, upper response limit; f, hormesis estimate; b, slope of the curve; e, the inflection point; GR 50, rate to reduce dry weight by 50%; (SE), standard error; GR 90, rate to reduce dry weight by 90%; T, tolerant; S, sensitive; Ripley, Ripley County, IN; Jay, Jay County, IN; Huntington, Huntington County, IN; Benton, Benton County, IN. b Determined by dividing the GR 50 values for the tolerant and sensitive biotype. c Determined by dividing the GR 90 values for the tolerant and sensitive biotype. XR11002 nozzles. The S biotype was treated with glyphosate rates of 0, 0.05, 0.10, 0.15, 0.20, 0.42, 0.84, 1.68, and 3.36 kg ae ha 21. The T biotype was treated with rates of 0, 0.20, 0.42, 0.60, 0.84, 1.68, 3.36, and 6.72 kg ae ha 21 of glyphosate. All treatments were applied with ammonium sulfate 5 at 2.8 kg ha 21 and 0.5% (v/v) nonionic surfactant. 6 The aboveground biomass of 10 plants was harvested 21 DAT, dried for 5 d in a forced-air drying room at 50 C, and weighed. The dry weights of all plants within each plot were averaged and converted to a percentage of the nontreated control prior to data analysis. Treatments were arranged as a two-way factorial in a randomized complete block design with four replications, where the factors were biotype and glyphosate rate. Because there was no significant treatmentby-experiment interaction, data were pooled for subsequent analysis. Combined data were fit to a dose-response curve (Equation 2) to estimate glyphosate GR 50 and GR 90 values with the use of R software (Knezevic et al. 2007). A lack-of-fit test indicated that the regression model accurately described the data (P ). Nonlinear regression parameters were predicted with the use of a three-parameter logistic model that relates actual dry-weight means as the percentage of the untreated control (Y ) to the herbicide rate (x). d { c Y ~ c z ½2Š 1 z expfb½logðþ{ x logðgr 50 ÞŠg In this equation, d is the upper response limit, c is the lower response limit, GR 50 the herbicide rate that results in a 50% reduction in dry weight, and b is the slope of the curve around the GR 50. Independent t tests were used to determine significance of GR 50 and GR 90 values between all biotypes at P The level of tolerance was determined by calculating a T/S ratio, as described previously. Independent t tests were used to determine significance of GR 50 and GR 90 values between biotypes at P Field Biology Study. A biology study focusing on glyphosatetolerant biotypes was conducted in 2006 and 2007 to investigate growth and fitness characteristics of common lambsquarters. This study was conducted at the Agronomy Center for Research and Education, located near West Lafayette, IN, on a Raub silt loam (fine silty, mixed, superactive, mesic Aquic Argiudolls; 35% sand, 65% silt, and 10% clay) with a ph of 6.3 and 3% organic matter. Four T biotypes and one S biotype were selected for the study from both Ohio and Indiana (n 5 8, 2, respectively), based on the greenhouse dose-response study and other greenhouse screens for glyphosate response (Mark M. Loux, unpublished data). Seed were germinated in the greenhouse and three-to fournode plants were transplanted into the field on June 16, 2006, and June 12, Biotypes were grown in 2.5-m-long rows with 10-cm plant spacing and 76 cm between rows. Plots were irrigated with the use of irrigation tape for at least 2 wk after planting, with approximately 1 to 2 cm of water per irrigation, and irrigation was repeated as necessary until plants were established. From each common lambsquarters biotype, one to five randomly selected plants were harvested from each replication at 2, 6, and 10 wk after transplanting (WAT), and at 16 WAT (plant maturity). Plant height, leaf area, and aboveground dry weight were measured at the time of each harvest. Leaf area was measured by separating all leaves from the stem and branches, and using a leaf area meter 11 to calculate the total leaf area plant 21. Plant biomass was dried for 5 d in a forced-air drying room at 50 C, and weighed to obtain dry weight. At 16 WAT, plant height, dry weight, and the Figure 1. Dry-weight response of four biotypes tolerant to (Ripley, Ripley County, IN; Jay, Jay County, IN; Huntington, Huntington County, IN; Benton, Benton County, IN) and one biotype sensitive to glyphosate in the greenhouse at 21 DAT. Westhoven et al.: Glyphosate-tolerant common lambsquarters N 687
4 Table 2. Independent t tests of GR 50 and GR 90 values based on dry weight for the greenhouse dose-response study. The glyphosate-tolerant biotypes include Ripley, Jay, Huntington, and Benton. a GR 50 P. F b GR 90 P. F Dry weight Ripley vs. Jay 3.22 vs vs Ripley vs. Huntington 3.22 vs vs Ripley vs. Benton 3.22 vs vs Ripley vs. Sensitive 3.22 vs. 0.57, vs Jay vs. Huntington 3.10 vs vs Jay vs. Benton 3.10 vs vs Jay vs. Sensitive 3.10 vs. 0.57, vs Huntington vs. Benton 2.10 vs vs Huntington vs. Sensitive 2.10 vs. 0.57, vs Benton vs. Sensitive 1.48 vs vs a Abbreviations: GR 50, rate to reduce visual control or dry weight by 50%; GR 90, rate to reduce visual control or dry weight by 90%; Ripley, Ripley County, IN; Jay, Jay County, IN; Huntington, Huntington County, IN; Benton, Benton County, IN; vs., versus. b Independent t tests were used to determine significance between values. Values of significance at P are in boldface. number of seeds per plant were measured. Seed production was estimated by weighing two subsamples of 100 seeds for each plant. Total seed plant 21 was calculated with the use of Equation 3 (Mager et al. 2006): S ~ ðw =AÞ 100, ½3Š where S is the total seed amount from each plant, W is the total seed weight from each plant, and A is the average weight of the two subsamples. Treatments were arranged in a split-plot design with three replications in 2006 and four replications in Biotypes were the main plots and plant collection timings were the subplots. The values for height and number of nodes were square-root transformed prior to ANOVA as determined by the Box Cox procedure (Box et al. 1978). Data were pooled over years due to the lack of an interaction between year and biotype. There were no significant differences between the T biotypes or between the S biotypes. All T and S biotypes were then grouped for subsequent analysis via orthogonal contrasts within plant collection timings. Results and Discussion Greenhouse Dose-Response Study. Differences in response to glyphosate among biotypes were observed in dry weight (Table 1; Figure 1) data. The T/S ratios showed that the T biotypes were 2.6- to 7.8-fold more tolerant than the S biotype. The GR 50 values for dry weight for the T biotypes ranged from 1.48 to 3.22 kg ae ha 21, respectively. The GR 50 value for the same parameters for the S biotype was 0.57 kg ae ha 21. The GR 90 values for dry weight for the T biotypes ranged from 8.73 to kg ae ha 21, respectively. The GR 90 value was 2.39 kg ae ha 21 for the S biotype. GR 50 and GR 90 values for all four T biotypes were significantly different than the S biotype (Table 2). In general, the hierarchy of glyphosate tolerance of the T biotypes was Ripley. Jay. Huntington. Benton. Field Dose-Response Study. Differences in dry weight between biotypes were observed in response to glyphosate (Table 3; Figure 2). The T/S ratios indicated that the Ripley county T biotype were (based on GR 50 ) and (based on GR 90 ) fold more tolerant than the S biotype, respectively. The GR 50 and GR 90 values were and kg ae ha 21 for the S biotype and and kg ae ha 21 for the T biotype, respectively. The S and T biotypes showed no significant difference between GR 50 values (P ) (Table 4). However, the GR 90 values were significantly different at the 0.05 level, indicating a significant difference between biotypes in the field (Table 4). Several researchers have been able to identify differential response to glyphosate among common lambsquarters biotypes (Hite et al. 2007; Kniss et al. 2006, 2007; Loux et al. 2005; Schuster et al. 2007; Taylor et al. 2005). Hite et al. (2007) documented the first report of unsatisfactory control of common lambsquarters with glyphosate from seed collections during the 2002 growing season, where a T/S ratio of 2.8-fold in the greenhouse was observed. Other research has shown 4.4-fold (Loux et al. 2005) and 3.0-fold (Kniss et al. 2006) differences in glyphosate sensitivity between T and S biotypes in greenhouse experiments. The results from our study are similar to the T/S ratios reported by Hite et al. (2007), Loux et al. (2005), and Kniss et al. (2006). However, published experiments focusing on common lambsquarters field response to glyphosate are somewhat limited (Hite et al. 2007; Kniss et al. 2006, 2007; Taylor et al. Table 3. Regression parameters for field dose response based on dry weight of common lambsquarters. A lack-of-fit test indicated that the regression model accurately described the data (P ). Regression parameters d a c b GR 50 (SE) GR 90 (SE) b T/S ratio 50 c T/S ratio kg ae ha Ripley (0.034) (0.286) Sensitive (0.005) (0.058) 1 1 a Abbreviations: d, upper response limit; c, lower response limit; b, slope around the curve; GR 50, rate to reduce dry weight by 50%; GR 90, rate to reduce dry weight by 90%; (SE), standard error; T, tolerant; S, sensitive; Ripley, Ripley County, IN. b Determined by dividing the GR 50 values for the tolerant and sensitive biotype. c Determined by dividing the GR 90 values for the tolerant and sensitive biotype. 688 N Weed Science 56, September October 2008
5 Figure 2. Dry-weight response of one tolerant (Ripley, Ripley County, IN) and one sensitive biotype to glyphosate in the field dose-response study at 21 DAT. 2005). To characterize biotypes effectively, dose-response curves and GR 50 and GR 90 values from field dose-response studies are necessary, because researchers have reported that the magnitude of tolerance to glyphosate between T and S biotypes is typically less in the field and false confirmation of T or glyphosate resistance is possible if only the results of greenhouse experiments are used for common lambsquarters (Kniss et al. 2006; Loux et al. 2005). Numerous dose-response studies have been conducted on other glyphosate-resistant weed species. Resistance has been documented up to 110-fold in horseweed (Conyza canadensis L. Cronq.) (Davis et al. 2007), 8-fold in Palmer amaranth (Culpepper et al. 2006), 9-fold in common waterhemp (Amaranthus rudis Sauer) (Smith and Hallett 2006), 10-fold in common ragweed (Sellers et al. 2004), 6.1-fold in giant ragweed (Ambrosia trifida L.) (Stachler et al. 2007), 10-fold in hairy fleabane [Conyza bonariensis (L.) Cronq.] (Urbano et al. 2007), 6.3-fold in goosegrass [Eleusine indica (L.) Gaertn.] (Ng et al. 2004), 5-fold in Italian ryegrass (Lolium perenne L. ssp. Multiflorum Lam. Husnot) (Perez and Kogan 2003), and 3.4-fold in rigid ryegrass (Lolium rigidum Gaudin) (Neve et al. 2004). Our results are similar to giant ragweed, goosegrass, and rigid and Italian ryegrass, which exhibit a lower level of resistance in glyphosate response. Field Biology Study. Early-season leaf area (P ) and dry weight (P ) data suggest that there was slightly greater leaf area and dry weight of S biotypes at the 2 WAT collection timing (Table 5). T biotypes were taller at 6 and 10 WAT and advanced more rapidly through growth stages based on the number of nodes plant 21. At 6 and 10 WAT, there were no differences in leaf area and dry weight between T and S biotypes. By 16 WAT, S biotypes had accumulated more dry weight than T biotypes, even though S and T biotypes were similar in height. S biotypes required 12 WAT to initiate flower primordial, whereas T biotypes required only 6 to 8 WAT (Table 6). There were no differences between biotypes in the total number of seeds produced, of the number of seed per g of plant dry weight or per cm 2 of leaf area. Based on these results, there did not appear to be a fitness penalty associated with the presence of glyphosate tolerance in common lambsquarters plants with regard to seed production. Marriage and Warwick (1980) also observed differences in growth, time to flower, and total dry weight among triazineresistant and -sensitive common lambsquarters biotypes. The early-flowering biotypes grew more rapidly throughout the season and accumulated less biomass at plant maturity. Similar results were observed with the glyphosate-tolerant biotypes in this study. The T biotypes grew more rapidly and flowered earlier in the growing season, and produced less biomass at plant maturity. DeGennaro and Weller (1984) found five distinctly different types of leaf morphology out of nine glyphosate-tolerant field bindweed biotypes and found that biotypes that required more days to flower also had fewer number of flowers plant 21. However, differences compared to sensitive biotypes were not reported. Glyphosate-resistant Palmer amaranth was shorter than the S biotype early in the growing season (Haider et al. 2007). Glyphosate-resistant Palmer amaranth biotypes do not incur a biomass accumulation penalty compared to sensitive biotypes (Vencill et al. 2006). Sellers et al. (2004) investigated glyphosate-resistant common ragweed and found that the resistant biotype was 1.6- to 2-fold shorter at times of measurement. Fewer growth stages early in the growing season, associated with the resistant biotype, were also observed. However, there were no differences in leaf area, dry weight, or relative growth rate at any harvest time. The results in our study are dissimilar to the aforementioned studies, because the glyphosate-tolerant common lambsquarters biotypes were taller and advanced through growth stages more rapidly in the early part of the season, and accumulated more biomass by the end of the growing season than the S biotypes. In summary, when comparing glyphosate response, higher overall levels of tolerance to glyphosate were observed among biotypes in the greenhouse, compared to the field. Greenhouse studies also showed very clear differences in response to glyphosate between T and S biotypes. However, under the parameters of this field study, a commonly used rate of glyphosate (0.84 kg ae ha 21 ) was effective in controlling the tolerant biotype. Even though glyphosate tolerance levels appeared lower in the field studies, the field studies confirmed Table 4. GR 50 and GR 90 values based on dry weight for the field dose-response study. a GR 50 P. F GR 90 P. F (kg ae ha 21 ) (kg ae ha 21 ) Ripley vs. Sensitive vs b vs a Abbreviations: GR 50, rate to reduce dry weight by 50%; GR 90, rate to reduce dry weight by 90%; Ripley, Ripley County, IN; vs., versus. b Independent t tests were used to determine significance between values. Values of significance at P are in boldface. Westhoven et al.: Glyphosate-tolerant common lambsquarters N 689
6 Table 5. Various growth characteristics of glyphosate-sensitive vs. glyphosate-tolerant biotypes of common lambsquarters. Results represent the average of two field experiments conducted in 2006 and Timing Nodes Height Leaf area Leaf area cm 21 of height Dry weight (WAT) a Biotype No. plant 21 P. F cm plant 21 P. F cm 2 plant 21 P. F P. F g plant 21 P. F 2 S b 4, T S T S 100, , , T 130 1,400 1, S , T , a Abbreviations: WAT, weeks after transplant; S, sensitive; T, tolerant. b Orthogonal contrasts are between means within collection timings. Means significantly different at P are in boldface. Table 6. Various flowering and seed production characteristics for glyphosatesensitive vs. glyphosate-tolerant biotypes of common lambsquarters. Results represent the average of two field experiments conducted in 2006 and Parameter Biotype Mean P. F Weeks until flower primordia S a 12 WAT, b T 8 WAT Total seed plant 21 S 35, T 22,100 Seed g 21 of dry weight S T 400 Seed cm 22 of leaf area c S 1, T 1,200 a Abbreviations: S, sensitive; T, tolerant; WAT, weeks after transplant. b Orthogonal contrasts were used to determine comparisons between means within a parameter. Means significantly different are in boldface at P c Leaf area from 10 wk after transplant collection timing. differences in response to glyphosate between T and S biotypes. In the field biology study, common lambsquarters biotypes with tolerance to glyphosate exhibited a higher growth rate early in the growing season in terms of height, growth stage, leaf area, and dry weight. No fitness penalty was observed when comparing seed production. Other research has shown that as plant height increases, glyphosate tolerance increases (Boerboom et al. 2006; Schuster et al. 2007). The early-season growth characteristics of glyphosate-tolerant biotypes may contribute to glyphosate tolerance and erratic control in production fields. Sources of Materials 1 Sulfuric acid, Mallinckrodt Baker, Inc., Red School Lane, Phillipsburg, NJ Sun Gro Redi-Earth plug and seedling mix, Sun Gro Horticulture Canada Ltd., Northeast 8th Street, Suite 100, Bellevue, WA Miracle-GroH Water-Soluble All Purpose Plant Food ( ), Scotts Miracle-Gro Products, Inc., P.O. Box 606, Marysville, OH Touchdown HiTech, EPA Reg. No , 0.60 kg ae L 21, Syngenta Crop Protection, Inc., P.O. Box 18300, Greensboro, NC N Pa K ammonium sulfate, Agriliance, P.O. Box 64089, MS 385, St. Paul, MN Preference nonionic surfactant, Agriliance, LLC, P.O. Box 64089, St. Paul, MN Sprayer tip, TeeJet XP Spraying Systems Co., P.O. Box 7900, Wheaton, IL SAS software, Version 9.1, , SAS Institute Inc., Cary, NC R software, Version 2.6.0, The R Foundation for Statistical Computing, Vienna University of Technology, Wiedner Hauptstrasse 8 10/1071, 1040 Vienna, Austria. 10 RO-DRIP, 8 MIL, 30.5-cm spacing, 91 L hr 21, Roberts Irrigation Products, Inc., 700 Rancheros Drive, San Marcos, CA LI-3100 Area Meter, LI-COR, Inc., 4647 Superior Street, Lincoln, NE Acknowledgments The authors would like to thank the many graduate and undergraduate research assistants for the data collection and field preparation. This article is Purdue University Agricultural Research Programs Manuscript Literature Cited Boerboom, C. M., D. E. Stoltenberg, M. R. Jeschke, T. L. Trower, and J. M. Gaska Factors affecting glyphosate control of common lambsquarters. Proc. N. Cent. Weed Sci. Soc. 61:54. Box, G.E.P., W. G. Hunter, and J. S. Hunter Statistics for Experimenters: An Introduction to Design, Data Analysis, and Model Building. New York: Wiley. Pp. 10,158 10,180. Buhler, D. D., R. G. Hartzler, F. Forcella, and J. Gunsolas Relative Emergence Sequences of Weeds of Corn and Soybeans. Publication SA-11. Ames, IA: Iowa State University Cooperative Extension. Bulke, R., J. De Vleeschauwer, J. Vercruysse, and J. Stryckers Comparison between triazine-resistant and susceptible biotypes of Chenopodium album L. and Solanum nigrum L. Meded. Fac. Landbouwkd. 50: Cardina, J., C. P. Herms, and D. J. Doohan Crop rotation and tillage system effects on weed seedbanks. Weed Sci. 50: Conley, S. P., D. E. Stoltenberg, C. M. Boerboom, and L. K. Binning Predicting soybean yield loss in giant foxtail (Setaria faberi) and common lambsquarters (Chenopodium album) communities. Weed Sci. 51: Crook, T. M. and K. A. Renner Common lambsquarters (Chenopodium album) competition and time of removal in soybeans (Glycine max). Weed Sci. 38: Culpepper, S. A Glyphosate-induced weed shifts. Weed Technol. 20: Culpepper, S. A., T. L. Grey, W. K. Vencill, J. M. Kichler, T. M. Webster, S. M. Brown, A. C. York, J. W. Davis, and W. W. Hanna Glyphosateresistant Palmer amaranth (Amaranthus palmeri) confirmed in Georgia. Weed Sci. 54: Curran, B Herbicide Resistance Weed Update. New_2005/resistance05.html. Accessed September Davis, V. M., K. D. Gibson, and W. G. Johnson A field survey to determine distribution and frequency of glyphosate-resistant horseweed (Conyza canadensis) in Indiana. Weed Technol. 22: N Weed Science 56, September October 2008
7 DeGennaro, F. P. and S. C. Weller Differential susceptibility of field bindweed (Convolvulus arvensis) biotypes to glyphosate. Weed Sci. 32: Gibson, K. D., W. G. Johnson, and D. E. Hillger Farmer perceptions of problematic corn and soybean weeds in Indiana. Weed Technol. 19: Haider, J. B., W. K. Vencill, S. Culpepper, and T. L. Grey Physiological response of glyphosate-resistant Palmer amaranth (Amaranthus palmeri). Proc. Weed Sci. Soc. 47:269. Harder, D. B., C. L. Sprague, C. D. Difonzo, K. A. Renner, E. J. Ott, and W. G. Johnson Influence of stem-boring insects on common lambsquarters (Chenopodium album) control in soybean with glyphosate. Weed Technol. 21: Harrison, S. K Interference and seed production by common lambsquarters (Chenopodium album) in soybeans (Glycine max). Weed Sci. 38: Heap, I. M International Survey of Herbicide Resistant Weeds. www. weedscience.com. Accessed September Hilgenfeld, K. L., A. R. Martin, D. A. Mortensen, and S. C. Mason Weed management in a glyphosate resistant soybean system: weed species shifts. Weed Technol. 18: Hite, G. A., S. R. King, E. S. Hagood, and G. I. Holtzman Differential response of a Virginia common lambsquarters (Chenopodium album) collection to glyphosate. Weed Sci. 56: Hocombe, S. D Simple Experiments on the Greenhouse Germination of Some East African Weed Species. Miscellaneous Report No Arusha, Tanzania: Colonial Pesticides Research Unit. P. 8. Jansen, M.A.K., J. H. Hobé, J. C. Wesselius, and J.J.S. van Rensen Comparison of photosynthetic activity and growth performance in triazineresistant and susceptible biotypes of Chenopodium album. Physiol. Vég. 24: Knezevic, S. Z., J. C. Streibig, and C. Ritz Utilizing R software package for dose-response studies: the concept and data analysis. Weed Technol. 21: Kniss, A. R., S. D. Miller, and R. G. Wilson Common lambsquarters control with glyphosate: What s the problem? Proc. N. Cent. Weed Sci. Soc. 60:200. Kniss, A. R., S. D. Miller, P. H. Westra, and R. G. Wilson Glyphosate susceptibility in common lambsquarters (Chenopodium album) is influenced by parental exposure. Weed Sci. 55: Kniss, A. R., S. D. Miller, R. G. Wilson, and P. H. Westra Response of two common lambsquarters biotypes to glyphosate. Proc. N. Cent. Weed Sci. Soc. 61:168. Loux, M. M., J. M. Stachler, B. A. Miller, and J. B. Taylor Response of common lambsquarters to glyphosate in the greenhouse and growth chamber. Proc. N. Cent. Weed Sci. Soc. 60:202. Mager, H. J., B. G. Young, and J. E. Preece Characterization of compensatory weed growth. Weed Sci. 54: Marriage, P. B. and S. I. Warwick Differential growth and response to atrazine between and within susceptible and resistant biotypes of Chenopodium album L. Weed Res. 21:9 15. Neve, P., J. Sadler, and S. B. Powles Multiple herbicide resistance in a glyphosate-resistant rigid ryegrass (Lolium rigidum) population. Weed Sci. 52: Ng, C. H., W. Ratnam, S. Surif, and B. S. Ismail Inheritance of glyphosate resistance in goosegrass (Elusine indica). Weed Sci. 52: Parks, R. J., W. S. Curran, G. W. Roth, N. L. Hartwig, and D. D. Calvin Herbicide susceptibility and biological fitness of triazine-resistant and susceptible common lambsquarters (Chenopodium album). Weed Sci. 44: Perez, A. and M. Kogan Glyphosate resistant Lolium multiflorum in Chilean orchards. Weed Res. 43: Schuster, C. L., D. E. Shoup, and K. Al-Khatib Response of common lambsquarters (Chenopodium album) to glyphosate as affected by growth stage. Weed Sci. 55: Sellers, B. A., J. M. Pollard, and R. J. Smeida Comparative biology of glyphosate-resistant and glyphosate-susceptible common ragweed. Proc. N. Cent. Weed Sci. Soc. 59:54. Smith, D. A. and S. G. Hallett Variable response of common waterhemp (Amaranthus rudis) populations and individuals to glyphosate. Weed Technol. 20: Stachler, J. M., M. M. Loux, W. G. Johnson, and A. M. Westhoven Characterizing the response to glyphosate of giant ragweed (Ambrosia trifida) biotypes from Ohio and Indiana. Proc. Weed Sci. Soc. 47:23. Taylor, J. B., B. A. Miller, M. M. Loux, and J. M. Stachler Field response of six Ohio common lambsquarters populations to glyphosate. Proc. N. Cent. Weed Sci. Soc. 60:201. Thomas, A. G., D. A. Derksen, R. E. Blackshaw, R. C. Van Acker, A. Légère, P. R. Watson, and G. C. Turnbull A multistudy approach to understanding weed population shifts in medium- to long-term tillage systems. Weed Sci. 52: Urbano, J. M., A. Borrego, V. Torres, J. M. Leon, C. Jimenez, G. Dinelli, and J. Barnes Glyphosate-resistant hairy fleabane (Conyza bonariensis) in Spain. Weed Technol. 21: Uva, R. H., J. C. Neal, and J. M. Tomaso Weeds of the Northeast. Ithaca, NY: Cornell University Press. Pp. 110, 204. Vencill, W. K., J. B. Haider, T. L. Grey, and A. S. Culpepper Physiological aspects of glyphosate-resistant Palmer amaranth (Amaranthus palmeri). Proc. N. Cent. Weed Sci. Soc. 61:96. Warwick, S. I. and L. Black The relative competitiveness of atrazine susceptible and resistant populations of Chenopodium album and C. strictum. Can. J. Bot. 59: Westhoven, A. M Distribution, biology, and management of glyphosatetolerant common lambsquarters. M.S. thesis. Purdue University: West Lafayette, IN Received January 25, 2008, and approved April 29, Westhoven et al.: Glyphosate-tolerant common lambsquarters N 691
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