Chapter 3
Genetic Engineering and Yield: What Has the Technology Accomplished So Far?Many have claimed that current GE crops increase yield (for example, Biotechnology Industry Organization 2009; Fernandez-Cornejo and Caswell 2006; McLaren 2005; Barboza 1999; Ibrahim 1996). To evaluate these claims we need to be clear on whether they apply to potential or operational yield, and we need to examine GE crops for which there are sufficiently robust data to draw reliable conclusions. Several Bt genes—insecticidal genes from the bacterium Bacillus thuringiensis—for achieving insect resistance in corn, as well as GE methods for instilling herbicide tolerance (HT) in corn and soybeans, have been widely commercialized for up to 13 years in the United States. These crops provide the best available test for the impact on yield of GE technology.
In addition to these few currently commercialized GE traits, many transgenes (genes transferred from one organism to another through GE) have been tested at various times over the past 20 years in field trials regulated by the USDA. Many of these latter genes encode traits that are typically aimed at improving yield. The number of field trials for these traits indicates the industry’s determination to develop transgenic crops with higher yields, and the number of these experimental genes that go on to commercialization reveals the rate of success.
Intrinsic or Potential YieldAs discussed above, the two major types of traits now present in transgenic crops—insect resistance and herbicide tolerance—are often classic contributors to operational yield. Neither trait would be expected to enhance potential or intrinsic yield, and indeed there is virtually no evidence that they have done so.
Thus commercial GE crops have made no inroads so far into raising the intrinsic or potential yield of any crop. By contrast, traditional breeding has been spectacularly successful in this regard; it can be solely credited with the intrinsic-yield increases in the United States and other parts of the world that characterized the agriculture of the twentieth century.
Operational Yield: Comparative Studies on Commercialized Genetically Engineered Food and Feed CropsWhile GE crops have been commercialized since the mid-1990s, only two types have been widely grown—corn and cotton containing Bt insecticidal genes, and corn, cotton, canola, and soybeans containing genes for herbicide tolerance. Bt genes in corn have targeted either Lepidoptera (primarily the larvae of the European corn-borer moth) or, more recently, the larvae of the corn rootworm beetles (Coleoptera). As of 2008, transgenic HT soybeans contained genes for tolerance to glyphosate-containing herbicides while transgenic HT corn contained genes for glyphosate or glufosinate tolerance.
Evaluation of Comparative Studies: The Importance of Appropriate DataBy design, Bt and HT—the two major transgenes in GE crops—would be expected to produce increases in operational yield in crops despite the presence of insect pests or weeds. To determine the contribution of these transgenes to yield, research must be able to isolate their effects from the many other factors that influence yield. These factors include the overall genetic makeup of the crop variety—often, as the result of conventional breeding—along with specific growing conditions and practices such as pesticide use, crop rotations, irrigation, soil quality, and weather. For studies to accurately attribute yield increases to transgenes, they must try to control or account for these factors.
There are many approaches to measuring yield and to comparing the yield performance of one agricultural production method or technology to another. Different methods vary in their ability to accurately assess the contribution of the transgene—as opposed to other factors—to the yield of the crop. It is therefore important to consider the methodologies used in studies that measure and compare yield in GE crops.
Claims about the yield impact of transgenic crops have often been made based on inappropriate data. For example, substantial yield increase from GE has been suggested based on observations of broad yield trends (McLaren 2005) that do not adequately consider the many other important influences on yield, such as the varying impact of weather and the continuing advances from conventional breeding.
For this report we have searched for the most reliable and best-controlled studies we could find. Most of the studies selected were based on comparative field trials that attempted to control for non-GE variables.
One important such variable reflects the background genetic differences (other than the transgene) between crop varieties. Several studies have actually found that background genetics is often more critical than the transgene for determining yield (Jost et al. 2008; Meredith 2006). But when high-yielding varieties also contain a transgene, higher yield may be inaccurately attributed to GE if care is not taken in designing the experiments. The converse situation may also occur. Ideally, the background genetics of the GE and non-GE varieties should be identical except for the presence or absence of the transgene. In practice, however, such complete genetic identity is not possible, though it can be approximated in so-called “near-isogenic” (NI) varieties.5
In addition to an inherent lack of complete identity, further breeding may cause the NI varieties to differ from their first-developed versions. Research conducted in Iowa, for example, found that one type of Bt corn resistant to corn rootworm had higher yields than the NI variety in the absence of pest infestation (Tollefson 2006). This suggests that further breeding of the Bt variety had produced higher yields independent of the transgenes. In general, however, use of NI varieties provides better control for genetic background than use of varieties that are not near-isogenic.
Field trials have their own limitations for predicting commercial-scale yield. Their limited duration and small size often do not adequately account for variability in weather, local pest species and amounts, crop rotations, and other factors that differ with place and time. For these reasons, multiple field trials at different locations and at different times are most useful, but remain only an approximation of the actual conditions of commercial agriculture.
To be of greatest practical value, the methods typically practiced by farmers should be used in field trials for comparison with the GE crop (Jost et al. 2008). For example, because conventional farmers sometimes use chemical insecticides to control moderate to heavy infestations of corn borer, it is most useful to compare a Bt crop to an untreated, NI, non-Bt control crop and also to treatments using typical corn borer insecticides. This would be representative of in-use farming methods and therefore would more accurately reflect yield benefits on actual farms. Organic farmers, meanwhile, rely on crop rotation, soil quality, and other cultural methods to control insect pests, and therefore it is not accurate to consider an untreated non-Bt control crop that is otherwise grown using conventional industrial farming practices as a stand-in for organic farming.
In field trials that test traits expected to control pests, it is important to compare crops challenged with sufficient levels of the pest in at least some of the trials. Low levels of pests often do not provide a stringent-enough challenge to enable differentiation between methods.
Although there are no methods that are free from limitations, those that are likely to be hampered by the fewest problems are emphasized in this report where possible.
Herbicide-Tolerant Soybeans: Operational Yield in the Presence of WeedsSoybeans tolerant of the herbicide glyphosate were introduced to U.S. farmers in 1996 and rapidly gained market share. Glyphosate-tolerant (GT) soybeans now constitute over 90 percent of all soybeans planted in the United States and represent the greatest proportion among GE crops. It is widely agreed that the ability to apply glyphosate to soybeans has provided greater convenience to farmers and reduced the time and costs relative to those of the herbicides previously used. But is any of this success attributable to increased yields in glyphosate-tolerant soy?
A number of studies have examined the yield of GT soybeans, several of which were included by the USDA in a recent report (Fernandez-Cornejo and Caswell 2006). Three of the studies compared yield for GT soybeans to non-GT, with two showing some increase and one a small decrease in yields. The report did not attempt to quantify yield differences.
One study not included in the USDA report deserves special mention, however, because it controlled for variables other than the GT gene that could affect yield. This research shows that when comparing several sets of GT and non-GT NI varieties, those with GT yielded about 5 percent less than conventional NI varieties (Elmore et al. 2001). The study concluded that the presence of the glyphosate tolerance gene was responsible for the yield reduction—an effect called yield drag. This work, conducted over a two-year period at several sites using several NI varieties and their counterparts, is probably among the best available for determining the effect of the GT gene on yield. Because special efforts were made to keep fields weed-free (hand weeding in addition to herbicides), these experiments do not necessarily reveal how different varieties of soybeans would respond to typical herbicide treatments on commercial farms.
Field trials conducted over a period of three years (1995–1997) in Tennessee used GT soybeans treated either with conventional herbicides or glyphosate (Roberts, Pendergrass, and Hayes 1999). These experiments would not account for the yield drag effects on GT soybeans noted by Elmore at al. (2001) because all varieties contain the GT gene, but these trials do compare the efficacy of different herbicide treatments. Seven of 11 non-GE herbicide combinations provided yields as high as glyphosate. All of the better-performing combinations of conventional herbicides are widely available. The authors note that higher infestations of grass weeds than those observed in their trials may reduce yields where non-glyphosate herbicides are used. On the other hand, shifts to more GT weeds and the development of glyphosate-resistant weeds could reduce the efficacy of glyphosate.
Over the past eight years, several weed species have developed resistance to glyphosate due to the overuse of this herbicide on GE crops, and these weeds now infest several million acres of farmland (International Survey of Herbicide Resistant Weeds 2009). Control of glyphosate-resistant weeds requires the use of different herbicides, while glyphosate may continue to be used to control weeds that remain susceptible. The emergence of glyphosate-resistant weeds therefore may be eroding the convenience and efficacy of GT soybeans, as well as contributing to increased herbicide use.
In a summary of several hundred field trials, Raymer and Grey (2003) found that in the mid-1990s, on average, non-GT varieties and herbicide treatments out-yielded GT varieties where glyphosate was used. These yield differences appeared to be less in later field trials, suggesting that they were due at least in part to variety differences, including lower disease resistance, that were diminishing. The authors suggest that these trends may make GT varieties competitive in yield with non-GT varieties over time.
Overall, studies have reported both increases and decreases in yield of GT compared to non-GT soybeans, but the best-controlled studies suggest that GT has not increased—and may even have decreased—soybean yield. This is not necessarily surprising. The typical pesticide regimes and combinations of several herbicides used prior to the introduction of GT soybeans were generally effective, if inconvenient, in controlling weeds. Glyphosate has been effective against many species of weeds, and therefore more convenient because farmers can often avoid using several different herbicides and spraying schedules, but it does not necessarily provide better weed control than several other herbicides combined.
Recently, Monsanto Co. announced the release of a new GT soybean, called Roundup Ready 2 Yield (RR2Y), that is claimed to increase yield by 7–11 percent over previous GT soybeans. Significantly, increased yield is the result of insertion of the gene for glyphosate tolerance in a way that avoids the negative yield effect of the original GT soybeans, and the use of a soybean variety that provides high yield due to conventional breeding methods (Meyer et al. 2006). GE in this case does not increase yields, but merely eliminates the previous yield reduction associated with the original HT-engineered soybeans, such as was observed by Elmore et al. (2001).
Herbicide-Tolerant Corn: Operational Yield in the Presence of WeedsFarmers have adopted transgenic HT varieties of corn more slowly than soybeans. This is probably due to the availability of effective herbicides, including ones to which corn is naturally tolerant. In the past six years, however, adoption of HT corn has greatly increased, reaching 63 percent of the corn crop in 2008 (Economic Research Service 2008b).
Switching to glyphosate from other systems might be of short-lived benefit, however, if measures are not taken to prevent the rise in glyphosate-resistant weeds. Several important corn weeds have already developed such resistance in several parts of the country because of the overuse of glyphosate in GT soybeans and cotton. These weeds include Palmer’s amaranth (Amaranthus palmeri), ragweeds (Ambrosia subspecies), and johnsongrass (Sorghum halapense) (International Survey of Herbicide Resistant Weeds 2009). Another important weed of corn, goosegrass (Eleusine indica), has developed resistance to glyphosate outside the United States.
Several recent studies have compared yields achieved by transgenic and conventional corn-herbicide systems. In tests in North Carolina, all systems, conventional or transgenic, produced statistically equivalent yields if they incorporated post-crop-emergence herbicide applications, usually spread over the crop (Burke et al. 2008). None of the tested systems used atrazine, an herbicide with a controversial safety profile. Although more effective or less effective in controlling different individual weed species, combinations of herbicides used in non-transgenic corn were as effective overall as herbicides used with transgenic corn. This research apparently did not use NI varieties to compare either glyphosate- or glufosinate-tolerant varieties, so the possibility that differences in genetic background could have had an effect cannot be ruled out.
In other experiments carried out in North Carolina in 2004, all transgenic and non-transgenic systems that incorporated over-the-crop application of herbicides provided high levels of weed control compared to herbicide applications applied in other ways, such as before crop emergence (Thomas et al. 2007). At several test sites, yields of the transgenic and non-transgenic corn varieties did not differ significantly, but overall the GT transgenic varieties produced the highest yields most often. The tested corn varieties were not near-isogenic, however, and the authors noted that yield differences may be explained by the genetics of the different varieties rather than by weed control.
Studies done in Kentucky at two locations over two years compared several non-transgenic herbicide systems and GT corn in tests that resulted in statistically equivalent weed control, although apparently using varieties that were not near-isogenic (Ferrell and Witt 2002). Glyphosate used with GT varieties provided better weed control than several of the herbicides used with non-transgenic corn but did not show statistically significant differences in yield. The authors noted that the low level of surviving weeds in the less effective non-GT systems was not sufficient to lower yield significantly. Similar results were found in research conducted over two years at two sites in Missouri and Illinois (Johnson et al. 2000).
In summary, based on the reviewed research, it does not appear that transgenic HT corn provides any consistent yield advantage over several non-transgenic herbicide systems. Transgenic corn generally achieves weed control equivalent to that of non-transgenic systems, but the weed control does not necessarily translate into higher yields. In some instances, when GT varieties produced a higher yield than did the non-transgenic systems, that yield advantage may have been the result of the different background genetics of the varieties used. As with other GE crops, motivations other than increased yield are more likely to be encouraging farmers to adopt HT corn.
Insect-Resistant Corn: Operational Yield in the Presence of InsectsSoil organisms produce a wide variety of Bt toxins that are effective against different types of insect pests. Corn varieties containing the gene Cry1Ab were first commercialized in the United States in 1996. This gene is mainly intended to control the larvae of a moth, the European corn borer (ECB, Ostrinia nubilalis), that damage the corn plant’s leaves, bore into the stalks of corn, or attack the cob. The ECB can complete one to three generations during a growing season in different parts of the Corn Belt, with differences in impact between generations. The Southwestern corn borer, a problem in some areas, is also controlled by this variety of Bt corn. Several similar Bt genes have also been approved, including Cry1F, which in addition to controlling corn borers also provides some protection against several other insects—black cutworm (Agrotis ipsilon) and fall armyworm (Spodoptera frugiperda)—that are generally of less commercial importance. In 2004, corn containing a Cry3Bb1 gene was introduced to control a different kind of corn pest, corn rootworm (Diabrotica species)—beetles whose larval stage damages corn roots—and a new Bt-based corn rootworm gene, Cry34 /35 , was recently approved by the U.S. Environmental Protection Agency.
Yield Effects of Bt Corn for Control of the European Corn Borer:Comparisons of Bt and Non-Bt CropsSeveral research studies, which report yield data on a per-unit-area (e.g., per-acre) basis, provide a measure of the yield contribution of Bt transgenes to control of the corn borer. It is possible to use these data to estimate the overall impact of Bt transgenes on corn-crop yield at the national level. Such productivity information is invaluable in assessing the ability of Bt crops to contribute to food security on the international scale as well.
Field trials using NI varieties were conducted at several locations with differing levels of corn borer infestation. Dillehay and colleagues (2004) compared Bt and NI varieties over a period of three years in Pennsylvania and Maryland, where ECB infestation levels varied from low to high. The non-Bt NI varieties that were not treated with insecticide to control ECB averaged 5.8 percent lower yield than the Bt varieties for all locations and dates. There were no yield differences between varieties when ECB levels were low, and there was no apparent yield lag for the Bt varieties compared to popular non-Bt, non-NI varieties.6
A three-year field trial in South Dakota compared several Bt corn varieties with NI non-Bt varieties, either treated twice with insecticide (permethrin)—for first- and second-generation ECB—or with no insecticide treatment for the NI variety (Catangui and Berg 2002). First- and second-generation ECB levels were high during one year (1997), and there was no significant difference in yield between the Bt varieties and the insecticide-treated non-Bt NI. Meanwhile, the Bt varieties had an 8 percent higher yield than untreated NI non-Bt varieties. For the two years when first-generation borer activity was very low and second-generation levels were moderate, there were no statistically significant differences in yield between varieties or treatments, including NI with no insecticide use. A three-year (2000–2002) study in Ottawa, Canada, using several pairs of Bt and NI varieties under low- to moderate-ECB levels, showed no significant differences in yields compared to no insecticide use (Ma and Subedi 2005).
Rice and Pilcher (1998) summarized 1997 results from 14 Iowa field trials, where Bt corn averaged 5 percent higher yields than NI varieties. At three locations in Minnesota in 1997, yield from Bt corn averaged 12 percent higher than yield from non-Bt NI varieties (Rice and Pilcher 1998).
Research performed in Wisconsin in 1995 and 1996 using Bt and corresponding NI varieties reported severe first-generation ECB infestation. The Bt varieties averaged about 7.5 percent higher yields than the NI varieties under standard farming practices (Lauer and Wedberg 1999).7 In other research, infestation was relatively low in Indiana in 1994, and there was no significant difference in yield between Bt and NI varieties (Graeber, Nafziger, and Mies 1999). The non-Bt corn was treated with a microbial Bt for first- and second generation ECB, although microbial Bt is not recommended for treating second-generation ECB and is not the best available insecticide (Lauer and Wedberg 1999). Some of the crop was also artificially infested with large numbers of ECB larvae (60 larvae simulating each generation per plant). Only NI plants untreated with insecticide and artificially infested with both first- and second-generation larvae had lower yields, reduced by 6.6 percent, compared to Bt counterparts.
Yield data from crops raised prior to Bt corn’s introduction can be useful in determining potential yield losses from ECB that are preventable by Bt. In 1991 an outbreak of ECB caused substantial losses in Minnesota and Iowa; the average loss for Minnesota was 14 bushels per acre (Rice and Ostlie 1997). This amounted to about a 12 percent yield loss (based on USDA corn-yield data for Minnesota in 1991), which could have been avoided had Bt corn been available.
In summary, when levels of ECB infestation are low or even moderate, most research reviewed here suggests that there is typically little or no significant yield difference between Bt varieties and their NI counterparts, even without insecticide treatment of the NI. When infestation levels are high, Bt corn provides yield advantages of about 7–12 percent compared to typical alternative practices used by conventional (non-organic) farmers.
The lack of yield advantage for Bt corn when there are low infestations of ECB contrasts with the often-cited report by the National Center for Agriculture Policy (NCFAP) (Gianessi, Sankula, and Reigner 2002), which estimated a substantial yield advantage for Bt corn on a state-by-state basis even at low levels of ECB infestation, but without providing supporting experimental data. Those estimates of yield loss at low ECB incidence ranged from zero to eight bushels per acre, averaging 4.4 bushels per acre (not weighted for corn acres per state). For some of the states considered by the NCFAP, field trial data have since been produced. For example, in Maryland and South Dakota, where the NCFAP estimated that low ECB infestations caused losses of eight and five bushels per acre, respectively, data from subsequent field trials showed no yield advantage for Bt corn when infestations were low (Dillehay et al. 2004; Catangui and Berg 2002).
By contrast, when ECB infestation levels are high, Bt varieties often provide higher yield than NI varieties, especially when the NI varieties are not treated with insecticides. Infestation levels alone are not predictive of yield loss, however, because pest damage is affected by environmental conditions and the stage of crop growth when the larvae are present. Therefore significant losses may sometimes occur even with low infestation levels, or minimal damage may occur with higher levels of infestation. Overall, the cited data suggest that when infestation levels are high, the yield advantage of the Bt gene is often about 10 percent compared to typical farmer practices used with non-Bt varieties. By comparison, Mitchell, Hurley, and Rice (2004) arrived at an average yield advantage of 2.8–6.6 percent on all Bt corn acres, based on modeling informed by field trial data for five states.
Although yield is the subject of this report, it must be noted that yield is not the only possible advantage of Bt corn. Reductions in chemical insecticide use through the substitution of Bt is generally considered to be beneficial to farm workers’ health and the environment; this effect has been cited by farmers as being among the most important reasons to use Bt corn (Rice and Pilcher 1998).
National Yield Advantage: Aggregate Yield Attributable to Bt Corn Borer CornHow do the yield data from individual experiments on Bt crops translate into impacts on nationwide corn yields? Estimating these impacts requires information on acres infested with ECB and the percentages of acres planted with Bt varieties or treated with insecticides. Such numbers are not easy to come by, first because ECB is an episodic pest that only emerges as a big problem every four to eight years and second because there have been two classes of Bt corn products on the market since 2004—one directed at corn borers and the other at rootworms.
One possible way to estimate the percentage of corn farmers that use Bt corn is to determine how many of them used insecticides to control ECB prior to the advent of Bt corn. But only a minority of U.S. farmers treated their corn to control ECB in a typical year. For example, despite an outbreak in Minnesota in 1991, just 5 percent of corn farmers used insecticides to control ECB despite substantial yield losses (Rice and Pilcher 1998). Surveys of farmers taken during the 1990s provide other measures of insecticide use. For example, studies done in 1995 by Rice and Ostlie (1997) found that during the year before the introduction of Bt corn, only about 28 percent of farmers in Iowa and Minnesota reported ever having used insecticide for ECB. This was in part because it was not economical to treat moderate infestation levels of ECB, given the limited effectiveness and cost of available insecticides. Because insecticides for ECB are used on only a small percentage of acres, yield differences between Bt corn and insecticide-treated non-Bt corn are a relatively minor factor overall.
More farmers use Bt corn than previously used insecticides because Bt corn may provide better ECB control. However, it is only economical for farmers to use the transgenic varieties when the value of added yield exceeds the additional cost of Bt seed; such eventualities occur primarily during years of heavy, and sometimes moderate, infestation. The need to make seed-purchasing decisions prior to the growing season, however, may increase the amount of Bt seed purchased. Because it is difficult to accurately predict infestation and damage levels prior to growing the crop, many farmers buy Bt seed as “insurance” in case ECB reaches harmful levels.
Economically damaging outbreaks of ECB, based on insecticide efficacy and cost, typically occur in the upper Midwest—a primary corn-growing region—during only one year out of four to eight (Rice and Ostlie 1997), or between about 12 and 25 percent of growing seasons. But because of its greater efficacy, somewhat greater acreage may be economically justified for Bt corn, depending on the price of the seed.
Adoption of Bt corn reached about 26 percent by 1999, only three years after commercialization, but increased only an additional 6 percent the next five years, to a total of 32 percent (Economic Research Service 2008a). Bt corn directed at rootworm pests entered the market in 2004, and much of the increase in Bt corn acres since then is likely due to use of that class of products (Economic Research Service 2008c). Under current costs of Bt seed and prices for corn, it seems reasonable to estimate that about 30–35 percent of corn acres may be devoted to Bt corn for ECB or to stacked varieties that contain additional transgenes as well.
Yield data for Bt corn, compared to that of non-Bt corn produced from typical farm practices, can be used along with estimates of corn acreage infested with high and low levels of ECB to estimate national yield advantages for Bt corn. The published data are not extensive enough to arrive at precise yield data across years and regions of the United States (especially because the Southwestern corn borer can be a factor in some regions), but the data can still provide a rough estimate.
As noted above, Bt corn provides about a 7–12 percent yield advantage compared to non-Bt varieties for high ECB infestations and little or no yield advantage for most low- to moderate-infestation levels. Multiplying the acres infested with high or low levels of ECB by the corresponding typical Bt yield advantages, and then dividing by total corn acres, provides an estimated range of the total yield advantage for ECB Bt corn. If about 12–25 percent of corn acres have high infestation levels on average (based on Rice and Ostlie 1997), then about 10-23 percent of Bt corn acres are planted where ECB infestation would otherwise be low to moderate.
A low estimate of Bt yield effects (assuming a 7 percent yield advantage on 12 percent of corn acres with high infestation) and no yield advantage on an additional 23 percent of Bt acres (averaged across all U.S. corn acres) results in a yield advantage of about 0.8 percent. A high estimate can be calculated by assuming a yield advantage of 12 percent on all Bt acres (that is, assuming high infestation levels on all Bt acres, and also assuming that about 33 percent of corn acres planted with Bt corn are aimed at the corn borer). In that case, Bt corn would provide about a 4.0 percent yield advantage averaged over all U.S. corn acres.
A more reasonable scenario is about a 10 percent yield advantage on 20 percent of Bt ECB corn acres (assuming heavy infestation once every five years) and a 2 percent advantage on another 15 percent of Bt acres (assuming a small yield advantage for light to moderate infestations), which gives a 2.3 percent yield advantage averaged over all U.S. corn acres. This estimate is in line with a calculation of 6.6 percent yield advantage for Bt in Iowa, using the highest estimate from the range of values of Mitchell, Hurley, and Rice (2004). When applied to all corn-growing states, and assuming 33 percent of acres devoted to Bt corn, this gives a 2.2 percent yield increase averaged over all corn acres.
Yield Effects of Bt Corn for Control of the Corn RootwormAside from ECB, the other major insect pests of corn are species of corn rootworm, which collectively cause an estimated $1 billion in damages annually (Rice 2004). Rootworm larvae feed on corn roots, thereby reducing the uptake of water and nutrients and making the plants more susceptible to toppling (lodging) in the fields. Adult beetles feed on corn tassels, but this does not usually cause a substantial problem.
Several studies have examined the yield impacts of Bt corn aimed at rootworm control. As with ECB, current data do not allow a precise determination of yield benefit from the Bt gene, but they are sufficient for ballpark estimates. National yield impact is considered here as well as yield per unit area. The latter is important to individual farmers, who need to maximize production on the limited acreage under their control, while the national data provide an assessment of the impact of Bt corn for rootworm on the overall productivity of the corn crop.
A complication when considering rootworm is that some populations of Northern and Western corn rootworm have adapted to the corn-soybean biennial crop rotations common in the Midwest. Until the 1990s, damage from rootworm could be avoided by alternating the planting of corn and another crop—in particular, soybeans. Rootworm beetles laid their eggs in corn during the fall, but they did not lay many eggs in soybeans. Corn following soybeans thus had few rootworms, and any eggs laid after the corn harvest would hatch in soybean fields, where the larvae could not survive. Rootworm was a problem only where corn followed corn. But over the past two decades, some corn rootworms have developed ways to evade this form of cultural control. For example, some Western corn rootworms now lay eggs in soybeans (or other rotation crops), and they hatch the following year into corn. In areas where these rootworms are found, especially parts of Illinois and Indiana, corn-soy rotations no longer adequately prevent rootworm damage. Another type of adaptation allows eggs laid in corn to hatch in the corn crop that follows the intervening soybean crop. In this report, such pests are collectively referred to as rotation-adapted rootworms.
There are fewer published data on the yield impact of Bt corn for rootworm than for ECB. One widely cited study on the benefits of Bt rootworm corn cites modeling data based on an index that correlates root damage with yield loss (Mitchell, Hurley, and Rice 2004; Rice 2004; Mitchell 2002). Yield advantage for Bt rootworm corn compared to insecticide use was estimated on average to be about 1.5-4.5 percent.
Iowa State University has been conducting field experiments comparing Bt rootworm varieties with either untreated NI controls or NIs treated with various insecticides. These insecticides include organophosphates, carbamates, and synthetic pyrethroids, which can cause considerable harm to the environment and human health. The experimental plots are located in different parts of Iowa, and they often use corn as a trap crop in years prior to the test in order to increase rootworm populations. Rootworm infestations are typically moderate to high, with damage to untreated controls often high to severe.
When feeding damage is low to moderate, several of the insecticide treatments typically perform as well as the Bt variety. But when damage in the untreated controls is high, Bt corn can show a significant yield advantage, although this result in not consistent across tests. For example, at a 2008 test site comparing many different Bt rootworm varieties and various insecticide-treatment plots, there was no significant yield difference between insecticide treatments and Bt crops. At Sutherland, Iowa, the single Bt rootworm variety that did not receive an insecticide application (most were treated with insecticide despite containing Bt) yielded about 3 percent more than the non-Bt NIs treated with insecticide (Gassmann and Weber 2008). In 2006, there were no statistically significant yield differences between Bt rootworm corn and insecticide treatments at several sites (Tollefson 2006) though at one site with a number of different insecticide treatments one Bt variety averaged 11 percent higher yield than the next five best insecticide treatments.
In 2005, rootworm injury and crop loss was often severe on untreated controls, and Bt corn provided significantly higher yields than insecticide treatments (Tollefson and Oleson 2005). The authors note, for example, a 30-bushel or greater benefit from Bt rootworm varieties compared to insecticide—a yield advantage of at least 14 percent. At a site experiencing serious drought, the yield advantage was at least 69 percent.
In sum, these tests suggest that Bt rootworm corn can provide substantially higher yields than insecticides under very high rootworm pressures and especially under unfavorable weather conditions. But the effect is not consistent, and in many tests insecticides performed about as well as Bt corn.
Several experiments in 2006 (Tollefson 2006) tested whether a variety of Bt rootworm corn and the NI variety had the same yield when there was no pest pressure—a test of whether the yield potential was, as would be expected, the same for the Bt and NI varieties. Surprisingly, the data showed that the Bt variety had a significantly higher yield—by about 8 percent. This result suggests that the tested Bt rootworm variety had a genetic yield advantage compared to its NI control. Such a bias may help account for some observed difference in tests. For example, subtracting 8 percent from the 11 or 14 percent yield advantages noted above leaves a 3–6 percent yield advantage for the transgene. As with any single study showing a new finding, additional studies should be performed to confirm it.
National Yield Advantage: Aggregate Yield Attributable to Bt Rootworm CornAlthough the yield differences between Bt corn and the better insecticide treatments tested in Iowa were generally positive, it is difficult to arrive at typical yield difference. While in some cases they were in the range of 10–20 percent for Bt rootworm corn (or even higher when drought occurred), in others there was no significant difference. We therefore use the estimate of Mitchell (2002) to determine national average yield gains for Bt rootworm corn compared to insecticide—about 1.5–4.5 percent—which takes a range of conditions into account.
National Bt corn usage data (Economic Research Service 2008a; Economic Research Service 2008c) suggest that if ECB Bt corn acreage is about 33 percent, then most of the rest of the 57 percent of corn acres using Bt varieties are for rootworm, or 24 percent. In addition, Bt rootworm gene is found in stacked varieties that contain several transgenes. Estimates of insecticide use for controlling rootworms prior to Bt corn vary from about 13.3 million to 25 million acres (Rice 2004), or about 15–33 percent of corn acres (depending on acres planted, which varies by year). Using the yield advantage data of 1.5–4.5 percent, assuming that 33 percent of corn contains Bt rootworm varieties (at the high end of estimated treated corn acres), and averaging over the entire corn crop, the national yield advantage for Bt rootworm corn is about 0.5–1.5 percent. An average value, using 24 percent of acres planted with Bt rootworm varieties, gives about 0.4–1.1 percent yield advantage.
National Aggregate Yield Advantage of Bt Rootworm and Bt Corn Borer CornAn estimate of the yield advantage provided by all Bt corn currently grown in the United States combines the yield advantages of ECB and rootworm Bt varieties taken separately. A low estimate, using the ECB yield advantage of 0.8 percent combined with the rootworm yield advantage of 0.5 percent, amounts to a total yield advantage of 1.3 percent. At the upper end, a 4.0 percent yield advantage for ECB added to a 1.5 percent yield advantage for rootworm gives a 5.5 percent yield advantage for the national corn crop. A 2.3 percent yield advantage for ECB is probably more realistic (see p. 20), which, added to the mean for rootworm of about 1 percent, gives an estimate of 3.3 percent.8 Because of the uncertainties, a 3–4 percent yield advantage for Bt corn is probably reasonable.
It is relevant to ask whether the acreage planted with Bt corn may increase in the future. Bt corn for ECB may be near a roughly constant percentage of the crop, depending on economic factors and infestation levels. Earlier in the decade, the USDA suggested a leveling of demand at about 25 percent of acres planted with ECB Bt varieties (Fernandez-Cornejo and McBride 2002). Although this estimate was not projected past 2002, barring significant changes in some of the underlying parameters these numbers may remain reasonable for a number of years to come. Mitchell and others found that in addition to ECB control, Bt corn for ECB provided a 1.65 percent “yield boost” of unknown cause (Mitchell, Hurley, and Rice 2004), which may partly explain an adoption rate—around 35 percent—somewhat higher than what was predicted by the USDA. Given these considerations, a substantial increase in the percentage of ECB Bt acres beyond current levels is not expected.
The amount of future corn acreage planted with Bt rootworm varieties depends in part on the spread of rotation-adapted rootworm variants that defeat the beneficial effects of the corn-soybean rotation, and in part on the use of alternative strategies where these rootworms already exist.9 Onstad et al. (2003b) determined that further evolution of rotation-resistant variant Western corn rootworm could be halted, even assuming a dominant allele (a variant of a gene) for rotation adaptation, by widely planting three-year rotations that include wheat preceding corn. Because of the currently lower profitability of wheat, however, this scenario may not be economically feasible. Other modeling suggests that landscape diversity (land not planted with corn or rotated soybeans) could slow the spread of rotation-resistant rootworm (Onstad et al. 2003a). We therefore use current acres for rootworm Bt corn, with the understanding that if two-crop rotations continue to dominate in the Corn Belt, this acreage could increase.
Other Transgenes for Increased Yield: Field Trials of Experimental GenesAll crops containing transgenes are tested in field trials, usually for several years, before being approved for commercialization. Comparison of the number of field trials of transgenes intended to increase yield with the number of commercially successful yield-enhancing transgenic crops therefore provides another, albeit rough, measure of the degree of GE’s success at realizing this goal. Meanwhile, the total number of these field trials suggests the accompanying level of effort to increase yield.
Since 1987, all field trials in which GE plants were to be propagated have required approval from the USDA. A publicly available record of approved field trial applications (Animal and Plant Health Inspection Service 2008) provides data on the genes, traits, and crops that have been investigated for the past 21 years.
Several limitations in the field trial database should be noted. First, the identities of a large percentage of genes are not revealed because the GE crop developer has claimed the gene as confidential business information (CBI). Although this practice greatly reduces the public’s ability to identify the genes under investigation, the alternative used in this report entails examination of the phenotypes, or traits, expected in the engineered crops, which tend to be disclosed in the database. This approach does not allow an accurate determination of the number of different genes intended to increase yield; a particular gene is often used in several field trials, including in multiple crops and by multiple institutions, while other field trials include several different genes for a single phenotype. Nevertheless, the approach does establish the magnitude of genes that have been tested for yield improvement.
In general, we assume that genes intended to provide pest resistance or abiotic tolerance are also intended to increase yield rather than, for example, simply reduce costs, although this is not always the case. For genes that are intended to increase yield potential, as opposed to operational yield, the purpose of the genes is rarely ambiguous.
We also note that several phenotype categories listed by the USDA may sometimes be intended to increase yields but primarily serve other purposes. For example, genes for nitrogen-use efficiency or nitrogen uptake may increase yield for a given amount of applied nitrogen fertilizer, but their primary mission is to reduce the need for applied nitrogen. Such categories are not included in the discussion below.
Table 1 shows the numbers of field-tested traits in categories typically intended to increase yields. The two categories from which crops have been successfully commercialized—insect resistance and HT—are listed separately. The intention here is to examine as-yet-uncommercialized genes. In particular, it should be noted that many insect resistance genes other than Bt have been tested, none of which have been commercialized. For example, there have been 15 non-Bt field trials for several genes intended to impart resistance to aphids. Excluding all HT and insect resistance genes therefore underestimates the number of operational-yield genes.
The table lists 1,787 field trials for resistance to plant pathogens (bacterial, fungal, viral, and nematode-related), including numerous genes. So far, only about five of these genes have been used commercially—virus resistance in papaya, squash (three genes), and plums—and comprise less than 1 percent of total GE acres. Only the gene for resistance to papaya ringspot virus can be considered a commercial success, and so far it has been used only in Hawaii.
None of the other categories has produced any commercial successes. Although there have been 583 field trials for abiotic stress tolerance—phenotypes include cold, heat, drought, shade, salt, and metal tolerances, among others—none of these genes have been used commercially.
There have been 652 field trials with yield listed in the database as the phenotype. Most of them were likely aimed at intrinsic-yield increase, and none of these transgenic crops have yet been commercialized.
In summary, beyond the category of virus resistance (for a very few virus-tolerant traits), none of the 3,022 field trials—which do not include HT and insect resistance—have led to commercialized varieties with significant impact on national yield. Virus-resistant papaya, however, has helped conventional farmers in Hawaii continue growing that crop.
The very low percentage of commercial transgenes for increased yield raises the question of why more of these transgenes have not been successful. No study that we are aware of has tried to answer this question, and therefore we consider several possibilities.
Table 1. Field Trials of Genetically Engineered Crops Having Traits Associated with Increased Yield Note: Numbers in parentheses indicate field trial numbers minus HT and IR. Source: Data from Animal and Plant Health Inspection Service 2008.A trivial answer is that sometimes the field trials were not intended to lead to commercialization. This may have been the case if the gene was being used only for basic research, such as in trying to understand how the gene functions in the plant, or in the few field trials using non-crop research species such as Arabidopsis. This explanation is likely to apply, however, only to a small minority of the field trials included in Table 1. Most field trials, about 82 percent, were conducted by companies or other entities that were motivated primarily by commercialization of the transgenic crop, with almost all of the rest conducted by universities.10 And because companies and universities alike have strong interests in eventual commercialization, only a small percentage of the field trials included in Table 1 were conducted without that goal.
Some of these transgenes may simply not be ready for commercialization. It typically takes several years of field trials and safety testing to acquire enough data about the crop, both for safety purposes and to make sure it performs as intended, before a transgenic crop is approved. However, as seen in Table 1, 1,108 of these field trials—not including those aimed at herbicide tolerance or insect resistance—were approved prior to 2000. Most of these earlier transgenic crops could have been ready for commercialization by the time of this report, but none have been submitted to the USDA for approval as of February 2009.
One possible reason for the lack of commercialization of some GE crops may be insufficient consumer acceptance. This would be especially true for food crops. But the field trial record includes numerous experimental yield-enhancing genes of a subset of transgenic crops that have already been widely commercialized—canola, corn, cotton, and soybeans—and thus it is unlikely that these genes’ lack of commercialization was caused by consumer rejection.
The most likely explanation for many of the failures to achieve commercial success are:
(1) technical challenges inherent in the unpredictable interaction of transgenes in the imperfectly understood genetic environment of the crop; or
(2) limited knowledge of the new trait’s efficacy prior to growing the transgenic crop in the field. Unpredicted properties of the transgene may result in deleterious unintended side effects, common in transgenic crops, that could reduce their agronomic performance or safety. For example, Bt corn varieties containing Cry1Ab genes have been reported to have elevated levels of lignin (a structural component of stems) compared to NI non-Bt varieties (Poersch-mann et al. 2005)—an unexpected and poorly understood result. Some of these side effects may have little agronomic or safety impact, but others may make the transgenic crop unmarketable or unsafe.
Whatever the reasons, the record of GE has not kept pace with yield increases accomplished by other means, such as traditional breeding or newer methods that enhance selective breeding with molecular-marker technology such as marker-assisted selection. As noted earlier, corn yield has been increasing on average by about 1 percent per year over the past several decades.
Looking at yield increases more closely with the aid of the USDA national data, we find that the contribution of GE continues to be greatly overshadowed by other methods. Average yields for the five years prior to the introduction of GE crops, 1991–1995, can be compared to the yields of the five most recent years of 2004–2008.11 Corn, soybeans, and wheat averaged 118.6, 36.2, and 37 bushels per acre, respectively, during the earlier five years and 152.4, 41.9, and 41.8 during 2004–2008. These changes amounted to yield increases of 28 percent for corn, 16 percent for soybeans, and 13 percent for wheat. A 4 percent yield enhancement from Bt corn accounted for about 14 percent of the increase in corn yields over the past 14 years. And GE has not contributed to the yield increases that have occurred in soybeans, wheat, and other crops.
