Although no glyphosate-resistant rice or wheat cultivars were commercially available during this time period, glyphosate use also increased in these non-GE crops ( Figure 1 ). By 2013, 0.3 glyphosate area-treatments were applied in rice; 0.5 and 0.4 glyphosate area-treatments were applied to spring wheat and winter wheat, respectively, in 2015. Since no glyphosate-resistant cultivars were available, these glyphosate applications were presumably made either before crop planting or emergence for burndown weed control or, to a lesser extent, as a harvest aid in wheat. The increase in glyphosate use is possibly related to increased conservation tillage adoption requiring herbicides for weed control at planting, but also by a substantial drop in glyphosate prices after patent expiration.

Corn, soybean, and cotton varieties exhibiting resistance to glyphosate were commercialized beginning in the mid-1990s (USDA Economic Research Service 2017 ). Adoption of glyphosate-resistant cotton and soybean varieties in the United States was rapid, reaching over 50% of total crop area within 6 yr of commercial introduction. Glyphosate-resistant corn adoption was slower in comparison, reaching 50% of total corn area 10 yr after introduction. Predictably, glyphosate use in these crops increased steadily following glyphosate-resistant cultivar adoption ( Figure 1 ). Glyphosate area-treatments increased to 0.9, 1.4, and 1.8 for corn, soybean, and cotton, respectively, in the final year of data (2014 for corn, 2015 for soybean and cotton). This compares with non-glyphosate herbicide area-treatments of 2.6, 1.8, and 2.2 for corn, soybean, and cotton, respectively.

In 2015, just three herbicide SOAs (WSSA Groups 2, 4, and 9) accounted for 93% of all herbicide use in winter wheat ( Figure 8 ). The increasing dominance of just three herbicide SOAs resulted in decreasing evenness even as herbicide area-treatments and SOA diversity increased. Reliance on Group 4 (auxin) herbicides in winter wheat has remained relatively steady over time ranging from 28 to 45% of total area-treatments. Group 2 herbicide use has increased, while glyphosate (Group 9) has also increased.

Winter wheat had the fewest herbicide area-treatments and lowest herbicide SOA diversity of the crops analyzed, although increasing trends were observed for both metrics over the 25-yr period ( Figure 8 ). Similar to spring wheat, since there are no glyphosate-resistant wheat cultivars available, glyphosate is presumably being applied mostly as a burndown treatment at or before planting, or possibly during the fallow period the year before wheat planting. The USDA-NASS survey asks respondents to include all herbicide applications made between harvest of the previous crop and the current crop. For the winter wheat–fallow system common in the western United States, this period includes approximately 12 mo of fallow. Glyphosate is among the most common herbicides used for fallow weed control, because it is effective and relatively inexpensive.

Herbicide area-treatments in spring wheat have increased over time, from 1.64 in 1990 to 3.59 in 2015 ( Figure 7 ). Herbicide SOA diversity increased over the last 25 yr, largely as a function of increasing herbicide area-treatments in the crop. Even with this increase, however, herbicide SOA diversity is still less than for corn, soybean, cotton, or rice. Evenness peaked in 2002 at 0.86, then declined to 0.7 by 2015. The use of auxin-type herbicides (WSSA Group 4) remained an important component of spring wheat production throughout the 25-yr period, ranging between 1.15 and 1.44 area-treatments. However, due to the increasing use of other herbicides, Group 4 herbicides have declined from 70% of all area-treatments in 1990 to 35% in 2015. Glyphosate (Group 9) was not recorded in the spring wheat survey data in 1990 through 1992. Even though glyphosate-resistant wheat is not commercially available, glyphosate use in spring wheat increased steadily beginning in 1993. By 2015, glyphosate accounted for 0.51 area-treatments (14% of total area-treatments). Because no glyphosate-resistant spring wheat cultivars are grown commercially, glyphosate was either applied before wheat planting or as a harvest aid, rather than being applied to the growing wheat crop. Glyphosate price reductions probably played a role in the increased use in this crop.

Herbicide use in rice was only surveyed six times over the last 25 yr, but since the surveys were conducted near the beginning and end of the period, they still provide valuable information on herbicide use trends. The number of herbicide area-treatments increased from 2.25 or fewer in 1990 through 1992 to 3.75 in 2013 ( Figure 6 ). In 1990, only two herbicide SOAs (Group 7 and Group 8) made up 78% of rice herbicide area-treatments ( Figure 6 ). Herbicide SOA diversity and evenness were greater in the last 3 yr surveyed (2000, 2006, and 2013) than in the 3-yr period from 1990 to 1992 ( Figure 6 ). At least a portion of the increased SOA diversity in rice is due to adoption of herbicide-resistant varieties. Use of Group 2 herbicides increased substantially beginning in 2000, so that by 2013, this SOA made up 37% of area-treatments in rice. The increase in Group 2 herbicides corresponds with introduction of imidazolinone-resistant (IR) rice cultivars in 2002. IR rice was conventionally bred to be resistant to this group of herbicides, which would normally be lethal to the crop. By 2006, IR rice cultivars were planted on a substantial number of rice fields in the United States, and adoption increased again between 2006 and 2013 (Anonymous 2016 ).

Herbicide SOA diversity in cotton increased steadily from 1990 until 1999, peaking at 7.6 ( Figure 5 ), then declined as glyphosate use became a more dominant component of cotton herbicide programs. Glyphosate became a major component of herbicide use in cotton in the early 2000s. By 2005, glyphosate accounted for 2 area-treatments, which represented 54% of total cotton area-treatments. In 2015, SOA diversity was similar to the value in 1990 (6 and 5.9, respectively). Glyphosate use still accounted for 2 area-treatments in 2015, but due to increases in use of other herbicide SOAs, glyphosate represented only 45% of total area-treatments. Similar to soybean, the increase in non-glyphosate herbicide use in cotton was likely a response to evolution of glyphosate-resistant weeds, most notably, Palmer amaranth (Amaranthus palmeri S. Wats.). The first documented case of glyphosate-resistant Palmer amaranth arose from cotton fields in Georgia in 2004, where glyphosate failed to control this species (Culpepper et al. Reference Culpepper, Grey, Vencill, Kichler, Webster, Brown, York, Davis and Hanna2006 ). Since that time, Palmer amaranth resistant to multiple herbicide SOAs has become widespread throughout cotton-growing states (Heap Reference Heap2017 ).

Cotton herbicide area-treatments increased from 2.57 in 1990 to 3.93 in 2015 ( Figure 5 ). A trend for increasing area-treatments was evident before the introduction of glyphosate-resistant crop cultivars, reaching 3.33 in 1997, the first year of glyphosate-resistant cotton availability. Herbicide area-treatments remained relatively steady through 2005, when 3.14 area-treatments were made. The USDA did not collect cotton herbicide use data in 2006 through 2009. In 2010 and 2015, the last 2 yr of USDA data collection in cotton, area-treatments had increased to more than 3.9. The greatest reduction in cotton herbicide use over this time period was observed in Group 17 herbicides, which are the organic arsenicals. Organic arsenical herbicide use peaked at 0.45 area-treatments and declined to 0.03 area-treatments by 2015. MSMA, the most prominent herbicide in this group, has been reviewed by the U.S. Environmental Protection Agency, but as of the writing of this paper, MSMA still has an active registration for use on cotton in the United States. Mitosis inhibitor herbicides (WSSA Group 3) and photosystem II inhibitors (WSSA Groups 5 and 7) have also remained important components of cotton weed control over time.

By 2012 herbicide SOA diversity in soybean had increased to levels similar to those observed in 2001 ( Figure 4 ). Although glyphosate use remained steady during the period of 2005 to 2015 (area-treatments ranged between 1.35 to 1.60), the near-exclusive reliance on glyphosate in soybean decreased due to increased use of other herbicides; glyphosate represented 43% of total area-treatments in 2015, and herbicide area-treatments increased to reach an all-time high of 3.23 in 2015. The first documented case of a glyphosate-resistant weed in GE crops (and the second case overall in the United States) was collected from a soybean field in Delaware in 2000 (Heap Reference Heap2017 ; VanGessel Reference VanGessel2001 ). It is likely that glyphosate-resistant weeds were responsible for the increase in non-glyphosate herbicide use and the corresponding increase in area-treatments and herbicide diversity between 2006 and 2012, although a causal relationship cannot be confirmed from this data.

In soybean, herbicide area-treatments reached a peak in 1994 of 3.03 before decreasing steadily to 1.78 area-treatments in 2005 ( Figure 4 ). This reduction corresponded with an increase in glyphosate use (Group 9) and a reduction in all other herbicide SOAs due to adoption of glyphosate-resistant soybean cultivars. Herbicide diversity in soybean declined rapidly beginning in 1999 and continued a downward trend until 2006. Evenness of herbicide SOAs in soybean followed a trend similar to SOA diversity. The reduction in herbicide diversity corresponded with heavy use of glyphosate in glyphosate-resistant soybean. By 2005, glyphosate represented 76% of all area-treatments. USDA-NASS did not collect herbicide use data for soybean between 2006 and 2012.

Herbicide area-treatments increased from 2.04 in 1990 to 3.47 in 2014 ( Figure 3 ). Herbicide SOA diversity also steadily increased in corn until 2005, reaching a peak SOA diversity of 6.8 ( Figure 3 ). Evenness of herbicide SOAs remained relatively consistent over the same period. This suggests that the potential for herbicide-resistant weed evolution became less likely in corn in the decade following GE corn introduction. Several changes in herbicide use patterns during this time are responsible for the increase in herbicide diversity. Glyphosate (the only herbicide that inhibits the 5-enolpyruvylshikimate-3-phosphate synthase enzyme, WSSA Group 9) began to increase substantially in corn after 2002, due to adoption of glyphosate-resistant hybrids. Group 27 herbicides (4-hydroxyphenylpyruvate dioxygenase inhibitors) were introduced commercially around the same time (in 1999) and have also increased steadily to reach 0.48 area-treatments in 2014. Group 5 herbicides, which include atrazine, once made up 46% of total corn area-treatments, but have decreased steadily in corn from 0.94 area-treatments in 1990 to 0.64 in 2014. Group 2 herbicide use has fluctuated somewhat over time, reaching a maximum of 0.59 area-treatments, but has averaged 0.29 area-treatments over the entire time period. Group 4 herbicide use has been mostly steady, averaging 0.36 area-treatments, but ranging between 0.23 and 0.46 area-treatments.

Interpretation of SOA diversity and evenness is intuitive; greater values mean greater diversity and evenness, respectively. It is presumed that as SOA diversity increases, the selection pressure for herbicide-resistant weeds decreases, because as diversity of herbicide SOA increases, the likelihood that any particular field received multiple effective SOAs also increases.

Rate of Herbicide-Resistant Weed Evolution

New herbicide-resistant weed species have increased rapidly over the last few decades, averaging approximately 5 new cases year−1 between 1990 and 2015 (Figure 9). However, break-point analysis suggests that the confirmation of new herbicide-resistant weed species has slowed since 2002 (Davies’ test P-value<0.001), averaging more than 6 new species year−1 before 2002, compared with 4 new species year−1 after 2002. Similarly, of the three herbicide SOAs with at least 10 resistant weed species since 1990, the confirmation of new resistant weed species has also slowed. For Group 1 and Group 2 herbicides, the change in slope occurred around 2002 and 2000, respectively, with the number of new confirmed resistant species dropping 78% and 65%, respectively.

Between 1990 and 2015, 17 different weed species evolved resistance to glyphosate in the United States, and glyphosate had been applied approximately 3 billion times to the 6 crops in this analysis (Figure 10). For comparison, there were 27 species resistant to Group 5 herbicides (photosystem II inhibitors), and 51 species resistant to Group 2 herbicides (ALS inhibitors), even though those herbicides were applied a combined 3.2 billion times over the same time period. This suggests that weeds have relatively less capacity to evolve resistance to glyphosate compared with some other commonly used classes of herbicides. This is consistent with previous analyses by Beckie (Reference Beckie2006) and Gustafson (Reference Gustafson2008).

There are several herbicide groups with a lower rate of resistance evolution than glyphosate (Figure 10). Group 15 herbicides are of particular note, since only 1 weed species has evolved resistance to this SOA, even after 1.3 billion herbicide applications. Auxin herbicides (Group 4) appear similar to glyphosate in the rate at which resistant species have evolved (0.9 new resistant species year−1; 0.0059 species per million area-treatments). Looking exclusively from a resistant weed management perspective, these herbicide groups would be preferred options for reducing the likelihood of herbicide-resistant weed development compared with SOAs with higher resistance evolution rates like Group 1 (acetyl-CoA carboxylase inhibitors) or Group 2 (ALS inhibitors).

Although a great deal of recent coverage in the media and scientific literature has focused on herbicide increases in GE crops, herbicide treatments have actually increased faster in the non-GE crops rice and wheat compared with the three major GE crops (Kniss Reference Kniss2017). The herbicide that has generated most recent public interest is glyphosate, which has become heavily used in GE glyphosate-resistant crops. The relationship between glyphosate use and continued use of other herbicides differed among the three GE glyphosate-resistant crops, and glyphosate use has also increased in non-GE crops over the last 25 yr. The rate of new glyphosate-resistant species evolution, however, has remained relatively modest compared with other herbicide SOAs, even in the face of unprecedented selection pressure for resistance.

Evolved weed resistance to glyphosate continues to increase, and this is certainly a problem for farmers who rely on this herbicide for weed control. When viewed broadly, however, the available data suggest that the evolution of herbicide-resistant weeds has not accelerated since the adoption of GE glyphosate-resistant crops. Rather, the rate of new resistant weed species has progressed at a similar or even slightly reduced rate over time. Although GE herbicide-resistant crops are typically discussed as a single entity, the impact this technology had on herbicide use differed depending on the crop. In corn, where many other effective herbicide options are available, increasing glyphosate use did not reduce application of other herbicides. This finding is similar to that of Livingston et al. (Reference Livingston, Fernandez-Cornejo, Unger, Osteen, Schimmelpfennig, Park and Lambert2015), who used a similar data set and reported that less than 15% of corn area received glyphosate-only treatments in 2005 and 2010, and more than 40% of corn area received combinations of glyphosate plus other herbicides in 2010. Purely in the context of herbicide-resistant weeds, the introduction of glyphosate and GE corn varieties has probably had a positive effect, since an additional SOA was introduced and herbicide diversity did not decrease. Similarly, herbicide diversity in the non-GE crops rice and wheat increased during the 25-yr time period of this analysis, although diversity in wheat remains low compared with all GE crops.

A different trend was observed in cotton and soybean, however, where the introduction of GE crops resistant to glyphosate caused a rapid reduction in herbicide diversity by replacing alternative herbicide chemistries. Livingston et al. (Reference Livingston, Fernandez-Cornejo, Unger, Osteen, Schimmelpfennig, Park and Lambert2015) similarly estimated that in 2006, more than 50% of soybean area received only glyphosate without the use of other herbicides. While this may have exacerbated the problem of herbicide-resistant weeds, glyphosate appears to have at least partially displaced three herbicide SOAs (Groups 2, 5, and 7) which are more likely to select for herbicide-resistant weeds compared with glyphosate (Figure 10). It is possible that because glyphosate appears less likely to select for resistant weeds, the overall impact of reduced herbicide diversity may have been at least partially mitigated with respect to herbicide-resistant weed evolution in GE soybean and cotton. This is further supported by the reduced rate of herbicide-resistant weed evolution observed for all SOAs combined, as well as for Group 1 and Group 2 herbicides (Figure 9).

It is important to note that the reduced rate of herbicide resistance that occurred as glyphosate use increased, while suggestive, is not necessarily a causal relationship. It is possible that there are simply fewer remaining weed species with the ability to evolve herbicide resistance to these SOAs, and this decreased rate of resistance might have been observed regardless of the herbicide SOA used. This illustrates the primary weakness in the analysis presented here; one simply cannot estimate with certainty what would have happened if GE crops had not been adopted. The available data suggest that at the very least, the problem of herbicide-resistant weeds has not been accelerated or exacerbated by the adoption of GE herbicide-resistant crops. This does not mean that this trend will continue, however. If continued development of herbicide-resistant crops reduces herbicide diversity in the future, or increases use of herbicide SOAs that are prone to resistance evolution, the herbicide-resistance problem could accelerate. And the current pace at which new herbicide-resistant weeds are evolving, even if it has not been accelerated by GE crops, is unsustainable, given the lack of new herbicide SOAs (Davis and Frisvold Reference Davis and Frisvold2017; Duke Reference Duke2012).

There is also a risk that continued focus on breeding herbicide-resistant crops to manage herbicide-resistant weeds is slowing the development and adoption of new nonchemical weed control strategies and practices. Maintaining or increasing herbicide diversity will certainly play an important role in the management of herbicide-resistant weeds, but it would be naive to think that this problem will be solved by herbicide diversity alone. Using diverse crop and weed management practices is the most important consideration for proactive management of herbicide-resistant weeds (Beckie and Harker 2017; Harker et al Reference Harker, O’Donovan, Blackshaw, Beckie, Mallory-Smith and Maxwell2012; Norsworthy et al. Reference Norsworthy, Ward, Shaw, Llewellyn, Nichols, Webster, Bradley, Frisvold, Powles, Burgos, Witt and Barrett2012). A broad view of weed management diversity that includes nonchemical weed control practices such as new robotics technologies (Slaughter et al. Reference Slaughter, Giles and Downey2008), as well as older, proven practices like tillage and crop rotation, will undoubtedly be required to minimize the impacts of herbicide-resistant weeds in the future.