2
Environmental Impacts of Genetically Engineered Crops at the Farm Level

The environmental impacts of planting genetically engineered (GE) crops occur within the context of agriculture’s general contribution to environmental change. Agriculture has historically converted biologically diverse natural grasslands, wetlands, and native forests into less diverse agroecosystems to produce food, feed, and fiber. Effects on the environment depend on the intensity of cultivation over time and space; the inputs applied, including water, fertilizer, and pesticides; and the management of inputs, crop residue, and tillage. With 18 percent of the land area in the United States planted to crops and another 26 percent devoted to pastures (FAO, 2008), the huge scale of these impacts becomes obvious. In general, tillage, crop monoculture, fertilizers, and pesticide use often have adverse effects on soil, water, and biodiversity. Agriculture is the leading cause of water-quality impairment in the United States (USDA-ERS, 2006). No-tillage systems, crop rotations, integrated pest management, and other environmentally friendly management practices may ameliorate some of the adverse impacts, but the tradeoff between agricultural production and the environment remains. With agricultural lands approaching 50 percent of U.S. land, developing more ecologically and environmentally sound agricultural management practices for crops, soil, and water is a central challenge for the future (Hanson et al., 2008). Against that backdrop, we evaluate the impact of GE crops on the environmental sustainability of U.S. farms.

This chapter examines the changes in farm practices that have accompanied the adoption of GE crops and the evidence on how such adop-



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2 Environmental Impacts of Genetically Engineered Crops at the Farm Level T he environmental impacts of planting genetically engineered (GE) crops occur within the context of agriculture’s general contribution to environmental change. Agriculture has historically converted biologically diverse natural grasslands, wetlands, and native forests into less diverse agroecosystems to produce food, feed, and fiber. Effects on the environment depend on the intensity of cultivation over time and space; the inputs applied, including water, fertilizer, and pesticides; and the management of inputs, crop residue, and tillage. With 18 percent of the land area in the United States planted to crops and another 26 percent devoted to pastures (FAO, 2008), the huge scale of these impacts becomes obvious. In general, tillage, crop monoculture, fertilizers, and pesticide use often have adverse effects on soil, water, and biodiversity. Agriculture is the leading cause of water-quality impairment in the United States (USDA-ERS, 2006). No-tillage systems, crop rotations, integrated pest management, and other environmentally friendly management practices may ameliorate some of the adverse impacts, but the tradeoff between agricultural production and the environment remains. With agricultural lands approaching 50 percent of U.S. land, developing more ecologically and environmentally sound agricultural management practices for crops, soil, and water is a central challenge for the future (Hanson et al., 2008). Against that backdrop, we evaluate the impact of GE crops on the envi- ronmental sustainability of U.S. farms. This chapter examines the changes in farm practices that have accom- panied the adoption of GE crops and the evidence on how such adop- 

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0 THE IMPACT OF GE CROPS ON FARM SUSTAINABILITY tion affects the environment. It addresses impacts at the individual farm level and also at the landscape level, given that impacts from individual farms accumulate and affect other farms and their access to communal natural resources in the region. The use of GE crops has altered farmers’ agronomic practices, such as tillage, herbicides, and insecticides; these alterations have implications for environmental sustainability both on and off the farm, which are evaluated to the extent possible at this point in time (Box 2-1). In particular, we examine the effects of the adoption of GE crops on soil quality, biodiversity, and water quality. ENVIRONMENTAL IMPACTS OF HERBICIDE-RESISTANT CROPS The adoption of herbicide-resistant (HR) crops has affected the types and number of herbicides and the amount of active ingredient applied to soybean, corn, and cotton. This section first examines the substitu - tion of glyphosate for other herbicides that has taken place and how the use of HR crops has interacted with tillage practices. It then assesses eco - logical effects of those changes on soil quality, water quality, arthropod biodiversity, and weed communities. Lastly, the implications for weed management in cropping systems with HR crops are considered, espe- cially for systems in which glyphosate-resistant weeds evolve. Herbicide Substitution A higher proportion of herbicide-resistant GE soybean has been planted than of any other GE crop in the United States. Adoption has exceeded 90 percent of the acres planted to soybean by U.S. farmers (Figure 2-1). HR cotton acreage reached 71 percent in 2009 (Figure 2-2), while planted HR corn acres were 68 percent that year (Figure 2-3). The HR crops planted thus far have altered the mix of herbicides used in cropping systems and allowed the substitution of glyphosate for other herbicides.1 Figures 2-1 through 2-3 summarize the trends in the use of glyphosate and other herbicides on soybean, cotton, and corn (expressed in pounds of active ingredient per planted acre of these crops) and the adoption of HR soybean, cotton, and corn (Fernandez-Cornejo et al., 2009). It is important to recognize that, depending on the metrics used, the substitution of glyphosate for other herbicides has resulted in the use of fewer alternative herbicides by growers of HR crops. However, glyphosate is often applied in higher doses and with greater frequency than the herbicides it replaced. Thus, the actual amount of active ingredi - 1A list of herbicides for which glyphosate is a common substitute can be found in Appendix A.

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 ENVIRONMENTAL IMPACTS OF GE CROPS AT THE FARM LEVEL BOX 2-1 Limitations to Evaluating the Magnitude of Environmental Effects Although environmental risk assessment is conducted for all GE varieties before regulatory approval, in some cases the absence of environmental monitoring at the landscape level prevents calculating the magnitude of effects (e.g., water quality) following commercializa- tion. Where monitoring data on agricultural practices are available (e.g., tillage practices, pesticide use), simple correlations of the adoption rates with trends in agricultural practices do not capture the complexity required to quantify the magnitude of any environmental effect. The lack of spatially explicit data linking the use of GE crops with data-monitoring agricultural practices stymies any accurate calculation of the magnitude of environmental effects at national or even regional levels (NRC, 2002). Environmental consequences of agricultural practices can vary greatly at a subregional scale. For example, the adoption of a herbicide-resistant crop may facilitate use of no-till practices, but the environmental effects of no-till practices depend on existing soil texture, structure, and erosion potential for each individual farm. Though models may exist to quantify soil retention given erosion potential, what amount of retention can be attributed to HR crops requires two additional calculations: 1. Quantifying to what extent HR crops caused the adoption of conservation tillage practices, given that there is a two-way relationship, and 2. Spatially linking the adoption of HR crops with data on the occur- rence of Highly Erodible Land, something not feasible without spatially- explicit data. Similarly, weed and pest control measures fluctuate from year to year and crop to crop, as have the choices of active ingredients. Determining the extent to which adoption of GE crops replaced specific pesticides over time requires incorporating a suite of factors, such as changes in pest pressure or pest-management strategies (e.g., see footnote on boll weevil eradication program), tillage practices, technology, and public policy (e.g., pesticide regulation, government programs) (Fernandez-Cornejo et al., 2009). Spatial data on the evolution of weed resistance are also lacking, thus preventing any calculation of environmental consequences of the declining effectiveness of glyphosate with glyphosate-resistant crops.

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 THE IMPACT OF GE CROPS ON FARM SUSTAINABILITY 1.4 100 1.2 80 Pounds of ac tiv e ingredient per Perc ent of soybean acres 1 planted ac re 60 0.8 0.6 40 0.4 20 0.2 0 0 1996 1998 2000 2002 2004 2006 2008 Year Gly phos ate Other herbic ides Perc ent ac res HR FIGURE 2-1 Application of herbicide to soybean and percentage of acres of herbicide-resistant soybean. NOTE: The strong correlation between the rising percentage of HR soybean acres planted over time, the increased applications of glyphosate, and the decreased use of other herbicides suggests but does not confirm causation between these variables. SOURCE: USDA-NASS, 2001, 2003, 2005, 2007, 2009a, 2009b; Fernandez-Cornejo et al., 2009. ents (glyphosate and other herbicides) applied per acre actually increased from 1996 to 2007 in soybean (Figure 2-1) and cotton (Figure 2-2) but decreased over the same period in corn (Figure 2-3). Glyphosate is reported to be more environmentally benign than the herbicides that it has replaced (Fernandez-Cornejo and McBride, 2002; Cerdeira and Duke, 2006). It binds to soil rapidly (preventing leaching), it is biodegraded by soil bacteria, and it has a very low toxicity to mammals, birds, and fish (Malik et al., 1989). Glyphosate can be detected in the soil for a relatively short period of time compared to many other herbicides, but is essentially biologically unavailable (Wauchope et al., 1992). Formulations that contain the surfactant polyoxyethylene amine can be toxic to some amphibians at environmentally expected concentrations and may affect aquatic organisms under some environmental conditions (Folmar et al., 1979; Tsui and Chu, 2003; Relyea and Jones, 2009); however, these formu- lations are labeled for terrestrial uses only with restrictions with respect to waterways. The greater use of postemergence glyphosate applications has been accompanied by modifications of agronomic practices, particularly

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 ENVIRONMENTAL IMPACTS OF GE CROPS AT THE FARM LEVEL 2. 5 100 Pounds of active ingredient 2 80 Perc ent of cotton acres per planted acre 1. 5 60 1 40 0. 5 20 0 0 1996 1998 2000 2002 2004 2006 2008 Year Gly phos ate Other herbic ides Perc ent ac res HR FIGURE 2-2 Application of herbicide to cotton and percentage of acres of herbicide-resistant cotton. NOTE: The strong correlation between the rising percentage of HR cotton acres planted over time, the increased applications of glyphosate, and the decreased use of other herbicides suggests but does not confirm causation between these variables. SOURCE: USDA-NASS, 2001, 2003, 2005, 2007, 2009a, 2009b; Fernandez-Cornejo et al., 2009. with regards to weed management and tillage. The interactions of those practices have implications for environmental sustainability. Tillage Practices Tillage is one process used by farmers to prepare the soil before planting. In conventional tillage, all postharvest residue is plowed into the soil to prepare a clean seedbed for planting and to reduce the growth of weeds; in conservation tillage, at least 30 percent of the soil surface is left covered with crop residue after planting. In the 1970s and 1980s, innovations in cultivators and seeders enabled farmers to plant seeds at a reasonable cost with residue remaining on the field. Those developments encouraged the adoption of one form of conservation tillage called no-till, in which the soil and surface residue from the previously harvested crop are left undisturbed as the next crop is seeded directly into the soil with - out tillage. After soil-conservation policy was incorporated into the Food Security Act of 1985, conservation tillage accelerated in the 1990s. The

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 THE IMPACT OF GE CROPS ON FARM SUSTAINABILITY 3 100 2.5 80 Pounds of ac tiv e ingredient 2 per planted ac re Perc ent of corn acres 60 1.5 40 1 20 0.5 0 0 1996 1998 2000 2002 2004 2006 2008 Year Gly phos ate Other herbic ides Perc ent ac res HR FIGURE 2-3 Application of herbicide to corn and percentage of herbicide-resistant corn. NOTE: The strong correlation between the rising percentage of HR corn acres planted over time, the increased applications of glyphosate, and the decreased use of other herbicides suggests but does not confirm causation between these variables. SOURCE: USDA-NASS, 2001, 2003, 2005, 2007, 2009a, 2009b; Fernandez-Cornejo et al., 2009. introduction of HR soybean and cotton has supported the trend because the use of glyphosate allowed weeds to be controlled after crop emergence without the need for tillage to disrupt weed development before or after planting. Indeed, in the last 10 years, the use of conservation tillage has continued to increase, with the exception that it has remained constant in the case of corn (Figure 2-4).2 The adoption of conservation tillage practices by U.S. soybean growers increased from 51 percent of planted acres in 1996 to 63 percent in 2008, or an addition of 12 million acres. The adoption of no-till prac - tices accounted for most of the increase and was used on 85 percent of these additional 12 million acres. Over the same time period, the acreage planted to soybean increased at most nine million acres. In cotton there was a doubling of the percentage of acres managed using conservation tillage from 1996 to 2008, and no-till is the predominant conservation tillage practice. Cotton acreage declined over the same time period. For 2 More information on different types of tillage systems can be found in Appendix B.

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Figure 2-4  ENVIRONMENTAL IMPACTS OF GE CROPS AT THE FARM LEVEL Soybeans 80 60 Ac res plant ed (million) 40 20 0 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 Year Cons ervation t illage: ≥30% res idue Tillage leaving < 30% res idue No-t ill HR s oy beans 20 Cotton 15 Ac res planted (million) 10 5 0 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 Year Cons ervat ion t illage: ≥30% res idue Tillage leaving < 30% res idue No-t ill HR c ott on Corn 80 Ac res planted (million) 60 40 20 0 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008 Year Cons ervat ion t illage: ≥30% res idue Tillage leaving < 30% res idue No-t ill HR c orn FIGURE 2-4 Trends in conservation tillage practices and no-till for soybean, cot - ton, and corn, and adoption of herbicide-resistant crops since their introduction in 1996. SOURCE: CTIC, 2009; USDA-ERS, 2009.

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 THE IMPACT OF GE CROPS ON FARM SUSTAINABILITY corn between 1996 and 2008, an additional 4.8 million acres of corn were planted. At the same time, the use of conservation tillage practices remained at a fairly constant 40 percent of planted acreage. No-till prac - tices increased by 4 percent over the same time period (4.3 million acres), but this was disproportionate relative to overall increases in conservation tillage practices (1.9 million acres), indicating that farmers converted from other conservation tillage practices to no-till. According to U.S. Department of Agriculture (USDA) survey data for 1997, a larger share of acreages planted to HR soybean was man- aged with conservation tillage than was planted to conventional soy - bean (Fernandez-Cornejo and McBride, 2002)—about 60 percent versus about 40 percent (Figure 2-5). The difference in the use of no-till between adopters and nonadopters of HR soybean was even more pronounced: 40 percent of acres planted with HR soybean were under no-till, double the corresponding share of acres of non-GE soybean under no-till man - agement practices (Fernandez-Cornejo and McBride, 2002). From the perspective of farmer decision making, the availability of herbicide-resistance technology may affect the adoption of conservation tillage, and the use of conservation tillage may affect the decision to adopt HR crops. Several economists have tried to understand how closely the two decisions are linked. An econometric model developed to address the simultaneous nature of the decisions was used to determine the nature of the relationship between the adoption of GE crops with HR traits and no- till practices on the basis of 1997 national survey data on soybean farmers (Fernandez-Cornejo et al., 2003). Farmers using no-till were found to have a higher probability of adopting HR cultivars than farmers using conven - tional tillage, but using HR cultivars did not significantly affect no-till adoption. That result suggested that farmers already using no-till incor- porated HR cultivars seamlessly into their weed-management program; but the commercialization of HR soybean did not seem to encourage the adoption of no-till, at least at the time of the survey. More recently, however, Mensah (2007) found a two-way causal rela- tionship on the basis of more recent data. Using a simultaneous-adoption model and 2002 survey data on soybean farmers, Mensah found that farmers who adopted no-till were more likely to adopt HR soybeans and that farmers who adopted herbicide-resistance technology were more likely to adopt no-till practices. In the case of cotton, the evidence also points toward a two-way causal relationship. Roberts et al. (2006) evaluated the relationship between adoption of HR cotton and conservation tillage practices in Tennessee from 1992 to 2004. Using two methods,3 they found that the adoption of 3 An application of Bayes’s theorem and a two-equation logit model.

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 ENVIRONMENTAL IMPACTS OF GE CROPS AT THE FARM LEVEL 10 0 Conventional tillage 80 Percent of Acres 60 C ons ervation tillage 40 No-till 20 0 Herbicide-resistant Conventional varieties varieties FIGURE 2-5 Soybean acreage under conventional tillage, conservation tillage, and no-till, 1997. SOURCE: Adapted from Fernandez-Cornejo and McBride, 2002. HR cotton increased the probability that farmers would adopt conser- vation tillage and conversely that farmers that had previously adopted conservation tillage practices were more likely to adopt HR cotton. Thus, the adoption of no-till and the adoption of HR cotton are complementary practices. Kalaitzandonakes and Suntornpithug (2003) also studied the simul - taneous adoption of HR and stacked cotton varieties and conservation tillage practices on the basis of farm-level data. They concluded that conservation tillage practices both encouraged the adoption of HR and stacked cotton varieties and were encouraged by their adoption. Using state-level data for 1997–2002 and using a simultaneous-equation econo - metric model, Frisvold et al. (2007) studied the diffusion of HR cotton and conservation tillage. They found strong complementarity between the two practices and rejected the null hypothesis that the diffusion of one is inde- pendent of the diffusion of the other. They also observed that an increase in the probability of adoption of HR cotton increased the probability of adoption of conservation tillage and vice versa. Thus, most empirical evidence points to a two-way causal relation- ship between the adoption of HR crops and conservation tillage.4 Farmers using conservation tillage practices are more likely to adopt HR crop varieties than those using conventional tillage, and those adopting HR crop varieties are more likely to change to conservation tillage practices than those who use non-HR cultivars. The analytical techniques used do 4 Most published evidence is for the cases of soybean and cotton given that extensive adoption of HR corn is relatively more recent (HR corn adoption only exceeded 20 percent of corn acreage in 2005).

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 THE IMPACT OF GE CROPS ON FARM SUSTAINABILITY not reveal the relative strength of each causal linkage, so it is not clear which factor (adoption of HR varieties or use of conservation tillage) has a greater influence on the other. Soil Quality The relationship between the adoption of conservation tillage practices and the adoption of HR crops is relevant to farm sustainability because conservation tillage has fewer adverse environmental impacts than con - ventional tillage (reviewed by Uri et al., 1999). On the farm, conservation tillage reduces soil loss from erosion, increases water infiltration, and can improve soil quality and moisture retention (reviewed by Uri et al., 1999; Holland, 2004). Corn and soybean are grown in regions where highly erodible land is common, and conversion to conservation tillage for these crops results in substantial reduction in soil loss and wind erosion even on non-highly erodible land (Uri et al., 1999). Leaving more crop residue on fields strengthens nutrient cycling and increases soil organic matter, a key component of soil quality (reviewed by Blanco-Canqui and Lal, 2009). Soil organisms decompose plant residue, and this, in turn, cycles nutrients and improves soil structure. In general, soil organisms have greater abun- dance or biomass in no-till systems than in conventional tillage systems because soil is disturbed less (reviewed by Wardle, 1995; Kladivko, 2001; Liebig et al., 2004). In addition to tillage, the use of herbicides can affect soil quality through their impact on soil organisms, so interpreting the effects of HR crops on soil quality requires an understanding of how tillage prac - tices interact with herbicide use to influence the soil microorganism community. In laboratory studies, glyphosate can inhibit or stimulate microbial activity, depending on soil type and glyphosate formulation (Carlisle and Trevors, 1986, and references therein). Some microorganisms can use glyphosate as a substrate for metabolism (increased activity), whereas others are susceptible to the herbicide because they have an enzyme 5-enolpyruvyl-shikimate-3-phosphate synthase pathway that glyphosate inhibits. When species-level responses were measured, roots of glyphosate-resistant soybean and corn treated with glyphosate had significantly more colonies of the fungus Fusarium than did non-HR cul- tivars or HR cultivars not treated with glyphosate (Kremer and Means, 2009). In contrast, fluorescent Pseudomonas populations, an antagonist of fungal pathogens like Fusarium, were significantly lower in soybean that were both glyphosate resistant and treated with glyphosate compared to untreated HR cultivars or a non-HR cultivar treated with other herbi- cides (Kremer and Means, 2009). Those results indicate a change in the antagonistic relationship between Fusarium and Pseudomonas attributable

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 ENVIRONMENTAL IMPACTS OF GE CROPS AT THE FARM LEVEL to the formulation of glyphosate used. Whether magnitude of change in this antagonistic relationship would have consequences on soil quality of disease control was not a part of the study. With respect to general microbial activity, three studies in the United States have detected no uniform changes in soil organism profiles in asso- ciation with tillage or with the use of glyphosate on glyphosate-resistant cropping systems (Liphadzi et al., 2005; Weaver et al., 2007; Locke et al., 2008). Soil microorganisms in fields planted with glyphosate-resistant corn and soybean varieties were similar with and without tillage (Liphadzi et al., 2005). HR fields treated with glyphosate and non-GE fields treated with other herbicides were also similar in soil microbe activity (Liphadzi et al., 2005). On tilled, experimental plots of glyphosate-resistant soybean, transient changes in the soil microbial community were detected in the first few days after application of glyphosate compared to no application (Weaver et al., 2007), but the differences disappeared after 7 days. When there was continuous cotton cropping, soil quality did not differ between HR and non-HR systems. In contrast, soil under continuous HR-corn cropping contained more carbon and nitrogen than soil with non-HR corn (Locke et al., 2008), which would be considered a benign change. Differ- ences in carbon and nitrogen contents could have been due to glyphosate use, but they were also probably influenced by changes in the detrital food web associated with the higher biomass of winter weeds in the HR- corn cropping system (Locke et al., 2008). Subtle differences in the struc- ture of the soil microbial community were also detectable in those same experiments; the significance of the differences for soil quality were not discussed. Thus, species-level studies suggest that glyphosate can alter the microbial composition in the rhizosphere. General studies of the inter- action of tillage and glyphosate use in HR crops have indicated transient benign effects of glyphosate and neutral, or in one case favorable, effects of conservation tillage on the soil communities in HR crops. Water Quality Conservation tillage practices can have off-farm benefits for water quality that are potentially more important than onsite productivity effects (Foster and Dabney, 1995). Because conservation tillage practices improve soil-water infiltration, the volume of runoff is less than when conventional tillage is used. Reduced tillage and no-till practices can improve water quality by reducing the amounts of sediments and sediment-associated chemicals in runoff from farm fields into surface water. Similarly, lower volumes of runoff can decrease the transport of soil nutrients and agri- cultural inputs, such as fertilizers and pesticides, although the decrease will vary with soil type, tillage practice, and nutrient or pesticide input.

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