Original article by Charles M Benbook
Public debate over genetically engineered (GE) crops is intensifying in the United States (U.S.), driven by new science on the possible adverse health impacts associated with herbicide-resistant (HR) crop pesticide use, and the rapid spread of glyphosate-resistant weeds. Still, many experts and organizations assert that GE crops have reduced, and continue to reduce herbicide, insecticide, and overall pesticide use. Fortunately, high quality and publically accessible U.S. Department of Agriculture (USDA) pesticide use data are available and can be used to track changes in pesticide use on crops containing GE traits. Moreover, the impacts of these traits on U.S. pesticide use trends are substantial and obvious, especially in recent years as a result of the growing number and geographical spread of glyphosate-resistant (GR) weeds.
Stable reductions in insecticide use in Bt-transgenic corn are also now in jeopardy as a result of the emergence of corn rootworm (CRW) populations resistant to the Cry 3Bb1 toxins expressed in several corn hybrids [1,2]. To combat this ominous development, some seed and pesticide companies are recommending a return to use of corn soil insecticides as a resistance management tool. There is a degree of irony in such recommendations, given that the purpose of Cry 3Bb1 corn was to eliminate the need for corn soil insecticides.
The emergence of herbicide-resistant genetically engineered crops in 1996 made it possible for farmers to use a broad-spectrum herbicide, glyphosate, in ways that were previously impossible. From 1996 through 2011, 0.55 billion hectares of HR corn (Zea mays), soybeans (Glycine max), and cotton (Gossypium hirsutum) were grown in the U.S. [Additional file 1: Table S7]. In 2011, an estimated 94% of the soybean area planted, 72% of corn, and 96% of cotton were planted to HR varieties, respectively, while about 65% of corn and 75% of cotton hectares in the U.S. were planted to Bt varieties [Additional file 1: Table S6].
Additional file 1. The projection model used is composed of a series of linked worksheets in a Microsoft Excel workbook. Each table within the workbook appears below in pdf as sequentially numbered Additional file 1: Table S1 (e.g., ST 1). The pesticide use data incorporated in the model were originally reported by U.S. government agencies in pounds of active ingredient, and/or pounds of a.i./acre, and so these units are used throughout the Additional files to report data on herbicide use. Convert pounds to kgs by multiplying by 0.454; to convert pounds/acre to kg/ha, multiply by 1.12. (XLSX 1068 kb)
Format: XLSX Size: 1MB Download file
Glyphosate-resistant, Roundup Ready (RR) crops now comprise the overwhelming majority of HR crops. RR crops were rapidly adopted because they provided farmers a simple, flexible, and forgiving weed management system, especially compared to systems reliant on the low-dose, persistent herbicide chemistries on the market in the late 1990s, such as imazethapyr (43% soybean hectares treated in 1996) and chlorimuron-ethyl (14% treated). From 1996 through 2008, HR crops resistant to herbicides other than glyphosate either disappeared from the market (e.g. bromoxynil HR cotton), or have been planted on relatively few hectares (e.g. glufosinate HR, LibertyLink cotton and corn).
Net reductions in pesticide use, encompassing changes in both herbicide and insecticide kilograms/pounds applied, are among the purported claims of GE crops [3–5]. Analysts assessing the impacts of Bt crops on insecticide use report reductions, or displacement, in the range of 25% to 50% per hectare . A more recent study reports a 24% reduction . On GE and non-GE corn since 1996, the volume of insecticides applied has declined, because of the pesticide industry-wide trend toward more biologically active insecticides applied at incrementally lower application rates.
The corn rootworm (CRW) has been the target of the majority of corn insecticide applications the last several decades. The average corn insecticide application rate in 1996 was about 0.76 kilograms of active ingredient per hectare (kgs/ha) (0.7 pounds/acre) and is less than 0.2 kgs/ha today (0.18 pounds a.i./acre) [Additional file 1: Table S12]. The two contemporary corn soil insecticide market leaders – tebupirimiphos and tefluthrin – are applied at average rates around 0.13 kgs/ha (0.12 pounds/acre). In 1996, the market leaders were chlorpyrifos and terbufos, insecticides applied at rates above 1.12 kgs/ha (1.0 pounds/acre) [Additional file 1: Table S12]. Obviously, planting Bt corn in 2011 reduced insecticide use less significantly compared to land planted to Bt corn in the late 1990s.
Few comprehensive estimates have been made of the impacts of HR crops on herbicide use. The USDA has not issued a new estimate in well over a decade; the USDA’s Economic Research Service (ERS) reported an 3.7 million kg (8.2 million pound) decrease in pesticide use in 1998 as a result of GE corn, soybeans, and cotton , an estimate that is comparable to the present study’s estimate of a 4.4 million kg (9.6 million pound) reduction [Additional file 1: Table S15]. A series of unpublished simulation studies have been carried out by the National Center for Food and Agriculture Policy (NCFAP). In a report covering crop year 2005, NCFAP projected that HR corn, soybean, and cotton reduced total herbicide use by 25.6 million kgs, compared to hectares planted to non-HR varieties . Sankula’s herbicide use estimates are based on observations of mostly university experts regarding “typical” herbicide use rates on farms planting HR versus non-HR varieties. The rates incorporated in Sankula’s estimates often differ from those published for the same year by USDA’s National Agricultural Statistics Service (NASS) . NASS reported that an average 1.5 applications of glyphosate were made on HR soybeans in 2005, while Sankula assumes only 1.18 applications. Sankula’s estimate of total herbicide use on RR soybeans in 2005, 1.15 kgs/ha (1.03 pounds/acre), is less than the NASS figure for glyphosate alone, 1.23 kgs/ha (1.1 pounds/acre). If true, Sankula’s data suggests that essentially no other herbicides were applied to RR soybeans in 2005, when in fact the average soybean hectare in 2002 was treated with 1.66 herbicides according to NASS data.
This paper quantifies the impacts of GE crops on the kilograms of pesticides applied per hectare and across all GE hectares, drawing upon publicly accessible USDA data. The pesticide use impacts of the six major, commercial GE pest-management traits are modeled and then aggregated over the 16 years since commercial introduction. While most of the pesticide use data incorporated in the model were originally reported by U.S. government agencies in pounds of active ingredient, and/or pounds of a.i./acre, results are reported herein in SI units (kilograms of active ingredient and kg/ha). Some key results are also reported in pounds/acre. Convert kilograms to pounds by multiplying by 2.205, and pounds to kgs by multiplying by 0.454. To convert from kg/ha to pounds/acre, multiply by 0.893; to convert from pounds/acre to kg/ha, multiply by 1.12.
Results and discussion
Farmers planted 0.55 billion hectares (1.37 billion acres) of HR corn, soybeans, and cotton from 1996 through 2011, with HR soybeans accounting for 60% of these hectares [Additional file 1: Table S7]. In terms of overall herbicide use per hectare based on NASS data, substantial increases have occurred from 1996 through 2011. In soybeans, USDA reported herbicide applications totaling 1.3 kgs/ha (1.17 pounds/acre) in 1996, and 1.6 kgs/ha (1.42 pounds/acre) in 2006, the last year soybeans were surveyed by USDA. In cotton, herbicide use has risen from 2.1 kgs/ha (1.88 pounds/acre) in 1996 to 3.0 kgs/ha (2.69 pounds/acre) in 2010, the year of the most recent USDA survey. In the case of corn, herbicide use has fallen marginally from 3.0 kgs/ha (2.66 pounds/acre) in 1996 to 2.5 kgs/ha (2.26 pounds/acre) in 2010, largely as a result of lessened reliance on older, high-rate herbicides.
Compared to herbicide use rates per hectare on non-HR hectares, HR crops increased herbicide use in the U.S. by an estimated 239 million kgs (527 million pounds) in the 1996–2011 period, with HR soybeans accounting for 70% of the total increase across the three HR crops. Rising reliance on glyphosate accounted for most of this increase.
In light of its generally favorable environmental and toxicological properties, especially compared to some of the herbicides displaced by glyphosate, the dramatic increase in glyphosate use has likely not markedly increased human health risks. Because glyphosate cannot be sprayed on most actively growing, non-GE plants, residues of glyphosate in food have been rare, at least until the expansion ~ 2006 in the number of late-season glyphosate applications on wheat and barley as a harvest aid and/or to control escaped weeds. Presumably as a result of such uses, 5.6% of 107 bread samples tested in 2010 by the U.K. Food Standards Agency contained glyphosate residues . Three samples had 0.5 parts per million of glyphosate , a relatively high level compared to the other pesticides found in these bread samples.
Budget pressures have forced the U.S. Department of Agriculture to reduce the number of crops included in its annual NASS pesticide use survey. Soybean pesticide use has not been surveyed since 2006, about when the spread of glyphosate-resistant weeds began to significantly increase herbicide use in selected areas. Herein, total herbicide use on HR hectares is projected to rise 13.5% from 2006–2011 (about 2.7% annually), compared to a 6.6% (1.3% annually) increase on conventional soybean hectares. By way of contrast, the NASS-reported glyphosate rate of application per crop year on the average hectare of soybeans increased 8.9% per annum from 2000–2006 (see Table 1). So, despite the significant and widespread challenges inherent in managing glyphosate-resistant weeds in the 2006–2011 period, a substantial decrease is projected in the rate of increase in glyphosate applications per hectare of HR soybeans. The justification for this projected fall in the rate of increase is recognition by farmers that further increases in glyphosate use will likely not prove cost-effective, coupled with positive responses by farmers to the near-universal recommendation that corn-soybean farmers incorporate into their spray programs herbicides that work through modes of action other than glyphosate’s [10–15].
Table 1. Projected rates of change in herbicide use since the most recent USDA survey, relative to recent annual percent changes in rates
Since 1996, about 317 million trait hectares (782 million trait acres) have been planted to the three major Bt traits – Bt corn for European corn borer (ECB) and CRW, and Bt cotton. Bt corn and cotton have delivered consistent reductions in insecticide applications totaling 56 million kgs (123 million pounds) over 16 years of commercial use. Bt corn reduced insecticide use by 41 million kgs (90 million pounds), while Bt cotton displaced 15 million kgs (34 million pounds) of insecticide use.
Taking into account applications of all pesticides targeted by the traits embedded in the three major GE crops, pesticide use in the U.S. was reduced in each of the first six years of commercial use (1996–2001). But in 2002, herbicide use on HR soybeans increased 8.6 million kgs (19 million pounds), driven by a 0.2 kgs/ha (0.18 pounds/acre), increase in the glyphosate rate per crop year, a 21% increase. Overall in 2002, GE traits increased pesticide use by 6.9 million kgs (15.2 million pounds), or by about 5%. Incrementally greater annual increases in the kilograms/pounds of herbicides applied to HR hectares have continued nearly every year since, leading to progressively larger annual increases in overall pesticide use on GE hectares/acres compared to non-GE hectares/acres. The increase just in 2011 was 35.3 million kgs (77.9 million pounds), a quantity exceeding by a wide margin the cumulative, total 14 million kg (31 million pound) reduction from 1996 through 2002.
Total pesticide use has been driven upward by 183 million kgs (404 million pounds) in the U.S. since 1996 by GE crops, compared to what pesticide use would likely have been in the absence of HR and Bt cultivars. This increase represents, on average, an additional ~0.21 kgs/ha (~0.19 pounds/acre) of pesticide active ingredient for every GE-trait hectare planted. The estimated overall increase of 183 million kgs (404 million pounds) applied over the past 16 years represents about a 7% increase in total pesticide use.
There are two major factors driving the upward trend in herbicide use on HR hectares compared to hectares planted to non-HR crops: incremental reductions in the application rate of herbicides other than glyphosate applied on non-HR crop hectares, and second, the emergence and rapid spread of glyphosate-resistant weeds. The first factor is driven by progress made by the pesticide industry in discovering more potent herbicidal active ingredients effective at progressively lower rates of application.
Twenty-seven percent of U.S. soybean hectares in 1996 were treated with pendimethalin at an average rate of 1.1 kgs/ha and another 22% were sprayed with trifluralin at a rate of 0.99 kgs/ha, while the market leader (imazethapyr) was applied to 43% of hectares planted at a rate of 0.07 kgs/ha . By 2002 the combined percentage of soybean hectares treated with these two high-dose herbicides had dropped from 49% to 16% , and just 5% were treated in 2006 . Between 1996 and 2006, the number of registered soybean herbicides applied at rates below 0.11 kgs/ha increased from nine to 17. As a result, the amount of herbicides applied to conventional crops has steadily fallen since 1996. In contrast, glyphosate is a relatively high-dose herbicide that is usually applied at a rate between 0.67 to 0.9 kgs per hectare.
The emergence and spread of glyphosate-resistant weeds is the second, and by far most important factor driving up herbicide use on land planted to herbicide-resistant varieties. Glyphosate resistant (GR) weeds were practically unknown before the introduction of RR crops in 1996. The first glyphosate-resistant weed (Lolium rigidum) emerged in Australia in 1996 from canola, cereal crop, and fence line applications . In the mid-1990s, as the first glyphosate-resistant crops were moving toward commercialization and gaining market share, Monsanto scientists wrote or were co-authors on several papers arguing that the evolution of GR weeds was unlikely, citing the herbicide’s long history of use (~20 years) and relative absence of resistant weeds [20,21].
Other scientists, however, challenged this assertion . Dr. Ian Heap, long-time manager of the international database on resistant weeds, warned in a 1997 conference presentation that to limit glyphosate selection pressure in Roundup Ready cropping systems, the herbicide would need to be used in conjunction with proven resistance-management practices and with non-chemical weed control methods . A 1996 report by Consumers Union stated that HR crops are “custom-made” for accelerating resistance and called for the Environmental Protection Agency (EPA) to revoke approval of HR crops when and where credible evidence of resistance emerges .
Today, the Weed Science Society of America (WSSA) website lists 22 GR weed species in the U.S. . Over two-thirds of the approximate 70 state-GR weed combinations listed by WSSA have been documented since 2005, reflecting the rapidly spreading nature of the GR-weed problem. According to the WSSA, over 5.7 million hectares (14 million acres) are now infested by GR weeds, an estimate that substantially underestimates the actual spread of resistant weeds [16,22], [and personal communication, Dr. Ian Heap]. Dow AgroSciences carried out a recent survey on the percent of crop acres/hectares in the U.S. impacted by glyphosate-resistant weeds . Findings from the survey were provided to USDA in support of Dow AgroSciences’s petition for deregulation of 2,4-D herbicide-resistant corn, and suggest that around 40 million hectares (100 million acres) are already impacted by glyphosate-resistant weeds, an estimate that Heap considers inflated [personal communication]. The true extent of spread in the U.S. likely lies around the midpoint between the WSSA and Dow AgroSciences estimates (i.e., 20–25 million hectares), and by all accounts, will continue to rise rapidly for several years.
Why have GR weeds become such a serious problem? Heavy reliance on a single herbicide – glyphosate (Roundup) — has placed weed populations under progressively intense, and indeed unprecedented, selection pressure . HR crops make it possible to extend the glyphosate application window to most of the growing season, instead of just the pre-plant and post-harvest periods. HR technology allows multiple applications of glyphosate in the same crop year. The common Midwestern rotation of HR corn-HR soybeans, or HR soybeans-HR cotton in the South, exposes weed populations to annual and repetitive glyphosate-selection pressure.
These factors trigger a perfect storm for the emergence of GR weeds. Research has traced the resistance mechanism in Palmer amaranth (Amaranthus palmeri) to 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene amplification. Resistant weed populations from Georgia contained 5-fold to 160-fold more copies of the EPSPS gene, compared to susceptible plants . Moreover, EPSPS gene amplification is heritable, leading Gaines et al. to warn that the emergence of GR weeds “endangers the continued success of transgenic glyphosate-resistant crops and the sustainability of glyphosate as the world’s most important herbicide.”
Resistant Palmer amaranth (Amaranthus palmeri) has spread dramatically across southern states since the first resistant populations were confirmed in 2005, and already poses a major economic threat to U.S. cotton production. Some infestations are so severe that cotton farmers have been forced to leave some crops unharvested.