Managing pigweeds resistant to EPSPs and ALS in Xtend™ soybeanAbstract:
Background: Amaranthus spp., known as pigweeds, are aggressive weeds, which are highly competitive with soybean crops. Reports of biotypes resistant to the main mechanisms of action (EPSPs and ALS inhibitors) used for management make it essential to integrate new chemical control strategies.
Objective: Assess the efficiency of dicamba and glyphosate and their association with residual herbicides (saflufenacil or flumioxazin), followed by glufosinate alone or combined with metribuzin, in controlling pigweeds resistant to EPSPs and ALS inhibitors, and the effect of phytotoxicity on the final yield of Xtend™ soybean.
Methods: Two experiments were conducted in the 2021/22 (year 1) and 2022/23 (year 2) growing seasons, using a randomized block design with 15 treatments and four replications. The desiccation treatments were applied 15 days before soybean sowing (DBS) and pre-emergens one (1) day after sowing (DAS), as well as after crop emergence (V3/V4). Phytotoxicity, pigweed control, and final soybean yield were assessed.
Results: Initial phytotoxicity, observed mainly via the application of associated pre-emergent herbicides, does not significantly damage the crop. Pigweed control was efficient when dicamba was associated with glyphosate, with sequential application of residual herbicides, especially flumioxazin, as well as glufosinate or glufosinate and metribuzin, in addition to the post-emergent application of fomesafen associated with glyphosate.
Conclusions: Pigweeds resistant to EPSPs and ALS-inhibiting herbicides can be effectively controlled under management programs with sequential application of pre-and post-emergent herbicides in soybean, respecting application intervals.
Keywords:
Competition; Integrated Management; Resistance; Selectivity; Amaranthus spp
1. Introduction
Competition from weeds is one of the most important biotic factors in soybean yield losses. Among the main weeds species that compete with this crop, the most prominent is Amaranthus spp., commonly known as pigweed.
With around 20 Amaranthus species considered weeds in agricultural areas worldwide, the genus is recognized for the broad morphological and genetic variability (Kissmann, Groth, 1999). These annuals are shrubs or herbaceous plants, that reproduce via seeds and are highly prolific, with reports of production reaching 250,000 seeds per plant when in competition with the soybean crop (Schwartz et al., 2016). Seeds are 1–2 mm in diameter, easily dispersed by animals and agricultural machinery, and are physically and/or physiologically dormant, resulting in different weed emergence rates in the field (Braz, Takano, 2022; Kismann and Groth, 1999). The considerable competitive ability of pigweeds in relation to crops is also due to their photosynthetic metabolism, classified as C4, enabling these weeds to use the resources in the environment faster than competing plants (Martínez-Núñez et al., 2019).
Chemical control is the main tool in pigweed management; however, recent years have seen an increase in reports of resistance to different mechanisms of action, particularly to herbicides that inhibit the enzymes 5-enolpyruvylshikimate-3-phosphate synthase (EPSPs) and acetolactate synthase (ALS) (Heap, 2023). Resistance is result of repeated large-scale application of the same herbicide(s) and failure to implement complementary control practices, such as soil cover or crop rotation (Gaines et al., 2020). Plants that escape control can inherit and transmit this trait to the next generation, either within the same species or through hybridization with other species, increasing the spread of resistant biotypes (Sulzbach et al., 2024).
In Brazil, there are currently officially documented cases of resistance in four pigweed species (A. viridis, A. retroflexus, A. palmeri and A. hybridus), the most recent in 2018 in Rio Grande do Sul state, where A. hybridus exhibited multiple resistance to glyphosate and chlorimuron-ethyl (Heap, 2023). Since then, control has been difficult in areas across the state.
Given that competition from pigweed plants can cause yield losses of up to 82% in soybean (Soltani et al., 2017), and that each A. hybridus plant m−2 with multiple resistance to EPSPs and ALS inhibitors can decrease yield by 6.4%, it is important to study and combine different control strategies (Zandoná et al., 2021).
Intacta 2 Xtend™ technology is a tool recently launched on the Brazilian market that enables the herbicides glyphosate and dicamba (auxin mimic) to be applied before soybean planting without affecting the crop (Green, 2018). Dicamba proved to be efficient in controlling pigweeds in the screening of biotypes collected in Rio Grande do Sul, where applications of this mechanism of action provided more than 80% control in all the biotypes tested (Amarante et al., 2021).
Considering the traits of pigweed species, particularly their rapid development and propagation in unfavorable environmental conditions, combining other potential pre- and post-emergent mechanisms of action, such as saflufenacil, flumioxazin (protoporphyrinogen oxidase (PPO) inhibitors) and metribuzin (photosystem II inhibitor) can help reduce infestation levels. Premergent herbicides control weeds before they emerge and can therefore inhibit pigweed emergence, keeping crops free of infestation and competition for longer through residual action (Gonçalves et al., 2018).
In light of the above, and given the importance of correct herbicide management and optimizing new technologies in pigweed control, this study hypothesized that pigweed control, phytotoxicity and Xtend™ soybean yield differ according to the proposed herbicide combination and application timing. As such, the aim was to assess the efficiency of dicamba and glyphosate and their association with pre-emergent herbicides (saflufenacil or flumioxazin), followed by glufosinate alone or combined with metribuzin, in controlling pigweed resistant to EPSPs and ALS inhibitors, and the effect of phytotoxicity on the final yield of soybean.
2. Materials and Methods
Field experiments were conducted in the 2021/22 (year 1) and 2022/23 (year 2) growing seasons in an experimental area belonging to Exacta Agriscience Consultoria Agronômica LTDA, in the municipality of Pelotas, Rio Grande do Sul state, Brazil (31°31’57.1"S and 52°13’56.8"W). Soil in the experimental area is classified as haplic planosol from the Pelotas map unit (EMBRAPA, 2013), with 28% clay, 12% silt and 60% sand. Climate conditions (average daily temperature and daily rainfall) for the two growing seasons are shown in Figure 1.
Average daily air temperature and daily rainfall during the experiment for the 2021/22 (year 1) and 2022/23 growing seasons (year 2)
A standardized block design was used, with plots covering a 13.5 m² area, 15 herbicide treatments and four replications over the two growing seasons (year 1 and 2). Pre-sowing treatments were applied 15 days before sowing (DBS) on November 16, 2021, (year 1) and November 25, 2022 (year 2), using only dicamba and glyphosate or in association with pre-emergent herbicides (saflufenacil or flumioxazin) (Table 1). Soil cover at desiccation consisted mainly of Lolium multiflorum and Conyza spp., Amaranthus spp. and Bidens spp. plants.
Sequential treatments used in the soybean crop 15 days before sowing (DBS)and 1 (one) day after sowing (DAS). Pelotas/RS, 2021/22 and 2022/23
The soybean cultivar AS3595I2X with Intacta 2 Xtend™ technology was used. Basal fertilization was performed using 345 kg ha−1 of the NPK 02-23-23 formulation, and subsequent applications were carried out according to the crop's recommendations. In both growing seasons, the second herbicide treatments were applied one (1) day after sowing (DAS), using glufosinate or dicamba + glyphosate alone, or combined with pre-emergent herbicides (Table 1). To obtain the pigweeds population, the experimental area was previously infested with seeds from a confirmed herbicide-resistant biotype (Amarante, 2024). The pigweed population in the area was 35 and 28 plants m−2 for the first and second growing seasons, respectively, quantified in the infested control at the first assessment (5 days after emergence - DAE).
In both years, the third herbicide application was after crop emergence (V3), corresponding to 26 and 28 DAE for the first and second year, respectively, using glyphosate and standardized fomesafen in all treatments except treatment 1, at rates of 1.5 and 0.8 L ha−1, respectively, added with 0.5% Agral v/v as adjuvant. The following species (stages) were present in the area in both years: Amaranthus spp. (4-6 leaves), Brachiaria spp. (4 leaves to 2 tillers), Digitaria spp. (4 leaves to 1 tiller) and Bidens spp. (4-6 leaves). The treatments were applied using a CO2 pressurized backpack sprayer equipped with 110.015 spray nozzles, calibrated to release a spray volume of 150 L ha−1. Pests and diseases were controlled according to crop needs, by evaluating disease inoculum pressure and pest population density.
The variables analyzed for the two-year study period were crop phytotoxicity and pigweed control at 5 and 14 DAE, and 7 and 15 days after post-emergence treatment (DAT). Pre-harvest pigweed control was also assessed. Phytotoxicity and control were determined on a percentage scale, where zero (0) indicated no crop damage and 100 crop or weed death. Yield was evaluated in a 4.05 m2 study area, whereby samples were harvested, weighed on an analytical balance, and their final weight corrected to a 13% moisture content.
The data from each harvest were individually evaluated for normality (Shapiro-Wilk), homoscedasticity (Bartlett), and homogeneity (Pimentel-Gomes, 2009), and subsequently subjected to analysis of variance (p ≤ 0.05). As the experiments were considered homogeneous, they were analyzed jointly using two factors: year and herbicide treatments. However, due to the detection of a significant interaction (p ≤ 0.05) between the "year" and "herbicide treatment" factors, comparisons among treatment combinations were carried out separately for each year, in accordance with Pimentel-Gomes (2009), using the Scott-Knott test (p ≤ 0.05).
3. Results and Discussion
Analysis of variance demonstrated significance for all the variables analyzed in both years, with year-treatment interaction in pooled data analysis.
In regard to phytotoxicity to the soybean crop after the first and second application times (15 DBS and 1 DAS), differences in visible crop damage were observed for two assessment times (5 and 14 DAE) (Table 2).
Phytotoxicity (%) of herbicides to the soybean crop, assessed at 5 and 14 days after crop emergence (DAE) in experiments conducted in year 1 and 2. Pelotas/RS, 2021/22 and 2022/23
For the first assessment (5 DAE) in both years, higher phytotoxicity scores were recorded in treatments 2, 12 and 15, which involved a single application of dicamba+glyphosate (1 DAS), pre-sowing application of dicamba+glyphosate+flumioxazin (15 DBS) followed by glufosinate (1 DAS), or dicamba+glyphosate+flumioxazin (15 DBS) followed by glufosinate+metribuzin (1 DPS), respectively, all with values greater than 9%. Treatment 15 in year 1 resulted in crop damage reaching 17%. The lowest scores at this assessment time were obtained in treatment 1, with a single glufosinate application (1 DAS), and treatments 3, 4 and 10, with only dicamba+glyphosate (15 DBS) or dicamba+glyphosate (15 DAS) followed by glufosinate alone (1 DAS), respectively. Treatment 3 did not differ statistically from the control (1) (Table 2).
At 14 DAE, treatments 2, 12 and 15 obtained the highest phytotoxicity scores, with reduced crop development generally observed in the two years studied (Table 2). The remaining treatments exhibited scores below 7% at 14 DAE, with the lowest scores observed in treatment 3, in the second year, which did not differ from the control (1), where a single application of glufosinate (1 DAS) resulted in no phytotoxicity.
In general, the phytotoxicity levels observed in both assessments are considered low and the difference between treatments may be due to environmental aspects, herbicide characteristics, and application time. The phytotoxicity observed for dicamba applied after soybean sowing (treatment 2), evidenced by the presence of cupped leaves, may be due to its greater availability in the soil solution, because the experimental soil is considered light, with a high sand content (60%) and dicamba exhibits low adsorption to the soil (Senseman, 2007). By contrast, applications at 15 DBS may result in lower availability of dicamba to plants, due to its easy degradation and solubility (Aguiar et al., 2023; Senseman, 2007), consequently mitigating the effects on the crop.
Certain characteristics of flumioxazin, particularly its high adsorption to soil organic matter (Koc = 889 mL g−1) and low solubility in water (1.79 mg L−1), may also have contributed to its prolonged availability in the soil solution, culminating in the phytotoxic effects observed in treatments 12 and 15, such as reduced plant development. Additionally, the greater damage observed in treatment 15 may be associated with the sequential application of metribuzin (1 DAS), a highly soluble herbicide (1,100 mg L−1) (Senseman, 2007). In these plots, in addition to the symptoms described, necrosis was also observed on the edges of unifoliate leaves, possibly caused by metribuzin. However, it should be noted that soybean plants recovered under the highest phytotoxicity values recorded in both years, that is, despite the symptoms observed, herbicide-related phytotoxicity had no effect on yield.
In control assessments, after the second herbicide application, treatments 6, 9, 12 and 15 obtained scores higher than 95% at 5 DAE for year 1 (Table 3). In the four treatments in question, dicamba was applied at 15 DBS in association with flumioxazin. These treatments were also efficient in year 2, where no statistical difference was observed between treatments, indicating consistent pigweed management. At 5 DAE, control exceeded 90%, except for treatments 1, 3, 4 and 10, in which the first and second application did not involve pre-emergent herbicides. In both years, treatment 3 exhibited the least efficient control (less than 20%), with only dicamba applied at 15 DBS.
Pigweed control (%) by different herbicides, assessed at 5 and 14 days after soybean emergence (DAE) in experiments conducted in year 1 and 2. Pelotas/RS, 2021/22 and 2022/23
In control trials with glyphosate-resistance pigweed, conducted in a greenhouse and the field using 2,4-D, different PPO inhibitors and glufosinate alone, satisfactory control was achieved for all the biotypes tested under both experimental conditions (Lamego et al., 2021). On the other hand, in the present study, crop damage was most significant in year 1, especially in treatments that contained flumioxazin (9, 12 and 15), with more efficient pigweed control observed in year 2.
These differences between growing seasons are largely due to the distinct environmental conditions in the years assessed, which may have influenced the effect of the herbicides on the crop and weeds. More significant rainfall was recorded in year 1, with a cumulative average of 46 mm, compared to 15 mm observed in year 2, measured from the date of the first application, carried out before sowing, until the time of the first evaluation at 5 DAE. This difference may have contributed to the higher levels of phytotoxicity observed in year 1, since the herbicides flumioxazin and dicamba (the latter applied 1 DAS) may have been leached in greater amounts to the crop's root zone, becoming more available for absorption. In contrast, in year 2, the lower rainfall may have reduced the mobility of the herbicides in the soil, keeping them in the upper layers. This may have favored weed control, especially of pigweeds, whose germination tends to occur in the upper soil layers.
Treatments 1, 3, 4 and 10 showed unsatisfactory control (not exceeding 80%) at 14 DAE in year 2 (Table 3), with values below 50% in year 1. In general, treatments 2, 7, 8 and 14 did not differ from those with flumioxazin (6, 9, 12 and 15), achieving over 70% weed control (intermediate), while treatment 3, with only dicamba applied at 15 DBS, was the least efficient.
Comparison between treatments without (6 + 12) and with metribuzin (9 + 15) combined with glufosinate, applied at 1 DAS, or between dicamba and flumioxazin rates (6+9 × 12+15) showed no significant percentage differences (Table 3). This indicates that pigweed was controlled by pre-emergent flumioxazin application at 15 DAS, even without applying metribuzin immediately after sowing (1 DAS). It is important to underscore that increasing the flumioxazin rates from 80 to 100 g, combined with a dicamba reduction from 1 to 0.6L, did not improve control, that is, when associated with dicamba, using lower flumioxazin rates provided almost 100% pigweed control, demonstrating a positive interaction between the two herbicides.
Treatment 4 provided control approximately 47% and 22% higher than treatment 6 at 5 DAE, for years 1 and 2, respectively, considering the lowest associated rates of flumioxazin (Table 3). These responses are due to the diversification of modes of action, combining a contact and a systemic herbicide, as well as variations in their environmental dynamics, providing control advantages under different conditions. In general, flumioxazin performs better under higher moisture conditions, while dicamba maintains control in situations with lower soil moisture availability.
It should be noted that the soil persistence of herbicides depends primarily on the soil type and water content, and weed control may decline in the days after application, making it important to incorporate additional applications immediately after planting. Furthermore, the herbicide metribuzin represents an alternative mechanism of action to commonly used pre-emergents, which may be important in managing resistance.
Corroborating the need to combine sequential application of pre- and post-emergent herbicides, a study that assessed the efficiency of 240 g ai ha−1 of pyroxasulfone and flumioxazin and 300 g ai ha−1 of pyroxasulfone and sulfentrazone in controlling glyphosate-resistant A. tuberculatus found that combining these herbicides with sequential acifluorfen or fomesafen increased control to levels above 98% (Schryver et al., 2017). Positive results were also reported for flumioxazin and s-metolachlor applied before and immediately after sowing, respectively, providing 90% A. palmeri control throughout potato development (Meyers et al., 2010).
In phytotoxicity analysis after post-emergent glyphosate and fomesafen application in soybean, the greatest crop damage at 7 DAT occurred in year 1. In this season, the most damage (between 10 and 12%) was observed in treatments with pre-emergent flumioxazin application (9, 12 and 15), in line with the pattern of previous assessments for the first and second application times (15 DBS and 1 DAS) (Table 2 and 4). In year 2, the incorporation of post-emergent herbicides did not result in statistical differences between treatments, remaining at around 7%, with only the control (1) showing no visible crop damage in both growing seasons studied (Table 4). It is important to note that phytotoxicity of about 10% or less is considered low and does not generally affect crop yield.
Phytotoxicity (%) after soybean emergence, assessed at 7 and 15 days after treatment (DAT) in experiments conducted in year 1 and 2. Pelotas/RS, 2021/22 and 2022/23
In the subsequent assessment (15 DAT), crop recovery was observed in all the treatments, whereby those that produced the most damage in the first assessment in year 1 continued to stand out, albeit with less damage at the second assessment. In year 2 phytotoxicity did not exceed 2.5% in any of the treatments (Table 4).
For weed control evaluated after glyphosate application combined with post-emergent fomesafen, treatments with pre-emergent flumioxazin (6, 9, 12 and 15) obtained the highest control levels in years 1, with values above 96% at all three assessment times (Table 5). In year 2, treatments 2, 7, 8, 9, 13, 14 and 15 did not differ and effectively controlled pigweeds at all the assessment times, with scores greater than 94% (Table 5), whereas treatments 3, 4, 5 and 10 achieved poor control in the same year at all three assessments, not exceeding 86%. Likewise, control was unsatisfactory (less than 72%) in year 1 for treatments 3, 4, 10, and 13.
Pigweed control (%) by different herbicides, assessed at 7 and 15 days after treatment (DAT) and pre-harvest with glyphosate + fomesafen application in soybean in experiments conducted in year 1 and 2. Pelotas/RS, 2021/22 and 2022/23
Additionally, as expected, treatment 1 with no post-emergent application (third herbicide application) obtained the lowest control scores, with 0% at 15 DAT and pre-harvest in year 1 and not exceeding 20% at pre-harvest in year 2.
Fomesafen is a good alternative for controlling pigweeds resistant or not to ALS and EPSP inhibitors in soybean crops; however, its efficiency is limited to plants taller than 10 cm or with more than six leaves (Lamego et al., 2021). In this respect, sustained control, especially in treatments with pre-emergent flumioxazin application (6, 9, 12 and 15), indicated that these treatments reduced weed emergence due to their residual effect, and sequential post-emergent applications kept the plots weed free, with few escapes (Table 5). Thus, when fomesafen was applied, particularly in these treatments, there were few escapes or plants outside the recommended stage, which enabled high control levels to be maintained. However, for treatments in which weed escapes were more developed at the third application, largely due to the absence of a pre-emergent herbicides, there was no significant increase in control.
Corroborating the results presented here, previous research demonstrated high pigweed sensitivity to fomesafen, establishing this herbicide as an alternative for post-emergent application in soybean (Amarante et al., 2021). Similarly, a study that assessed the effect of sequential herbicide use before and after soybean emergence on controlling resistant Amaranthus spp. obtained 95% control with pyroxasulfone + flumioxazin 8 weeks after application and over 80% control 8 weeks after post-emergent glyphosate + fomesafen application (Aicklen et al., 2022).
In both study years, all the treatments, especially those containing residual herbicides such as saflufenacil or flumioxazin, applied at 15 DBS, produced the highest yields, with no statistical difference between the values obtained (Table 6). However, the highest grain yields were recorded in year 1, when treatments generally produced yields greater than 4,000 kg ha−1, with no treatments reaching this level in year 2. The control treatment (1), with only pre-sowing glufosinate application, obtained the lowest yields in both years, and treatment 3 (no pre-emergent or herbicide application at sowing) in year 1. Yield declined by about 43% in the control (treatment 1) when compared to treatments with pre-sowing saflufenacil or flumioxazin application (Table 6), due to competition from the pigweed population.
Soybean yield (kg ha−1) in experiments conducted in year 1 and 2. Pelotas/RS, 2021/22 and 2022/23
Treatments that contained flumioxazin applied before sowing (6, 9, 12 and 15), which exhibited greater soybean phytotoxicity (Table 2), showed efficient pigweed control (Table 3 and 5), with no significant yield difference in relation to the remaining herbicide treatments. In line with these findings, studies that evaluated different flumioxazin rates (71 to 105 g ha−1) in soybean found that the crop recovered even under high phytotoxicity levels, with non-significant yield losses (Taylor-Lovell et al., 2001; McNaughton et al., 2014).
Treatments that obtained more than 70% control at pre-harvest (131 DAT in year 1 and 103 DAT in year 2) were also statistically equal to the remaining treatments, indicating that soybean can maintain its yield potential and tolerate pigweed escapes. However, given the seed production potential of each weed and the contribution of each seed to re-infestation of the resistant soil seed bank in the subsequent year, it may be beneficial to opt for more efficient management practices by investing in herbicide combinations. Additionally, the greater control achieved with pre-emergent herbicides reaffirms the occurrence of different flows throughout the growing season and highlights the importance of combining pre- and post-emergent herbicides to efficiently manage pigweeds.
Application before crop establishment and at planting allow the soybean crop to establish itself in the absence of weeds and use resources in the environment, making them less available to the weeds and extending the pre-interference period (PIP) (Krähmer et al., 2021). The third application was carried out in the critical period for preventing weed interference, when competition from weeds would cause yield losses.
The residual effect of pre-emergent herbicides can reduce pigweed emergence during crop development, which not only decreases infestation and, consequently, competition, but also mitigates selection pressure on pre-emergent herbicides (Gonçalves et al., 2018). Moreover, it is important to use pre-emergent herbicides with different mechanisms of action from those of their post-emergent counterparts, a key management practice in reducing selection pressure for resistance.
In terms of assessing the need to rotate mechanisms of action, it should be noted that in some of the treatments tested, PPO inhibitors were subject to high selection pressure with two applications in the same growing season (saflufenacil or flumioxazin and fomesafen). In this respect, when planning crop management strategies, it is recommended that one or more of these herbicides be substituted at application to reduce selection pressure.
Finally, although the best management approach varies according to the reality of each property, three key points are vital to maintaining yields and preventing the evolution of resistance: Rotating the mechanisms of action used in each crop cycle; combining pre- and post-emergent herbicides; and, when possible, avoiding the use of a same mechanism of action during the crop cycle, even for herbicides that belong to different chemical groups.
4. Conclusions
The phytotoxic damage observed in the Intacta 2 Xtend™ soybean crop after dicamba application did not affect crop yield when the interval between application and sowing was 15 days.
The treatments involving dicamba and glyphosate with sequential application of pre-emergent herbicides, especially flumioxazin, as well as glufosinate or glufosinate and metribuzin at planting and post-emergent fomesafen associated with glyphosate, achieved efficient control of resistant pigweeds.
Intacta 2 Xtend™ technology allows dicamba to be applied up to soybean planting and provides satisfactory pigweed control within an integrated management program with pre- and post-emergent herbicides.
Data Availability Statement
The data supporting the findings of this study are subject to privacy and confidentiality restrictions. They may be accessed upon request and with approval from the corresponding author.
Acknowledgements
The authors thank Vanessa Vital for reviewing this document.
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Edited by
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Editor in Chief:
Carol Ann Mallory-Smith
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Associate Editor:
Aldo Merotto Junior
