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4 Agronomic and Environmental Effects of Genetically Engineered Crops
Pages 97-170

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From page 97...
... The committee relied primarily on that literature for much of its analysis, but it also drew on studies available from other countries that produce GE crops. Chapter 3 noted that most GE crops in production from the 1990s to 2015 were engineered with resistance to herbicides, resistance to insects, or a combination of the two; this review of agronomic and environmental effects therefore is focused on these traits.1 1 The committee recognizes that there are other approaches to managing crop pests besides GE crops; many of these, including the implementation of production systems the use agroecological principles to reduce the need for pesticides, were addressed in the 2010 National Research Council report Toward Sustainable Agricultural Systems in the 21st Century (NRC, 2010b)
From page 98...
... EFFECTS OF GENETIC ENGINEERING ON CROP YIELDS Over the course of the study, the committee heard from speakers and received public comments that indicated that GE crops and their accompanying technologies were not substantially increasing crop yields; other comments and speakers endorsed genetic engineering as a contributor to yield increase, yield stabilization, or both.3 Before examining the evidence available on the effects on crop yields, it is useful to understand the factors that influence crop yield in general. Potential versus Actual Yield The distinction between potential yield and actual yield has been discussed in an earlier National Research Council report (NRC, 2010a)
From page 99...
... Such change can be accomplished in three ways. First, the potential yield can be increased; for example, the canopy architecture of the plant can be improved FIGURE 4-1  Factors that determine crop yield.
From page 100...
... The committee could only find one example of yield enhancement, that is, an increase in potential yield through genetic engineering.
From page 101...
... Transgenic eucalyptus that expresses endoglucanase was approved for cultivation on tree plantations in Brazil in 2015. Effects of Genetically Engineered Traits versus Conventional Plant Breeding on Yield The committee heard concerns from the public and from researchers that GE crops commercialized up to 2015 had not contributed to an increase in yield as much or as effectively as conventional plant breeding had (Cotter, 2014; Goodman, 2014; Gurian-Sherman, 2014; Dever, 2015)
From page 102...
... If there was a change in the slope of increase in yield since the commercialization of GE varieties (marked by the dashed line) , it could be taken as circumstantial evidence but not proof that genetic engineering caused a more rapid increase in yields.
From page 103...
... . NOTE: Dashed line indicates when genetically engineered varieties of these crops were first introduced in the United States.
From page 104...
... EFFECTS RELATED TO THE USE OF Bt CROPS The committee examined the effects of GE insect resistance on crop yield, insecticide use, secondary insect-pest populations, and the evolution of resistance to the GE trait in targeted insect populations. Yield Effects of Genetically Engineered Insect Resistance As of 2015, IR traits had been incorporated into maize, cotton, eggplant, and poplar.
From page 105...
... With regards to maize, he reviewed six studies published in 1997–2004 and concluded that the Bt traits to resist European corn borer (­Ostrinia ­nubilalis) closed the yield gap by 7–12 percent in locations where infestation by the insect was high.6 On the basis of review of three additional studies in Iowa published in 2005–2008, he concluded that the Bt trait targeting corn rootworm (Diabrotica spp.)
From page 106...
... conducted field studies in which corn earworm was the target pest. At two sites, one in North Carolina and one in South Carolina, they planted near isolines of non-Bt maize and maize with one to three Bt traits in 2012 and 2013.
From page 107...
... Field experiments in Nebraska in 2008, 2009, and 2010 compared glyphosate-resistant maize hybrids that also had Bt traits targeting E ­ uropean corn borer and corn rootworm with genetically similar hybrids without the Bt traits "in environments with no detectable infestation [of European corn borer or corn rootworm] based upon visual observations in-season and during harvest" (Novacek et al., 2014:94)
From page 108...
... compared two sets of locally adapted maize hybrids with the same general genetic backgrounds in the growing seasons of 2008 and 2009. In each set, one hybrid had GE resistance to glyphosate and the other had the GE trait for glyphosate resistance and Bt traits for resistance to European corn borer and corn rootworm.
From page 109...
... For hybrids that had herbicide resistance, they found yield increases for maize with Bt resistance to European corn borer and for maize with Bt targeting corn rootworm compared with non-GE ­hybrids. Maize with Bt targeting European corn borer yielded 6 percent more than non-GE hybrids on the basis of data from 1999–2009 (fixed effects model)
From page 110...
... They found that varieties with Bt toxins for European corn borer and western corn rootworm had decreased "cost of risk" of 106.5 kilograms/hectare. Working with cotton farmers in India, Krishna et al.
From page 111...
... . However, ­studies performed in years after Bt cotton was introduced and widely adopted9 found yield advantages.
From page 112...
... Controlling for all other factors, they found Bt cotton that controlled cotton bollworm (Helicoverpa armigera) had a yield advantage of 51 kilograms/hectare, a 24-percent increase over non-GE cotton yields during the period of the study.
From page 113...
... There was statistical interaction between the yield advantage and the specific region; the greatest advantage was 36.6 percent and the least was 14.3 percent. The authors hypothesized that the range in yield effect was due to differences in insect pest populations among the regions.
From page 114...
... When the Bt hybrids were compared by the company with popular open-pollinated varieties of eggplant, the yield benefit grew to 179 percent. Krishna and Qaim predicted that under field conditions the yield advantage of Bt eggplant hybrids over non-Bt hybrids would be 40 percent and over open-pollinated varieties 60 percent.
From page 115...
... Thus, there is evidence that GE insect resistance ad dresses yield-reducing factors in trees. FINDING: Although results are variable, Bt traits available in commer cial crops from introduction in 1996 to 2015 have in many locations contributed to a statistically significant reduction in the gap between actual yield and potential yield when targeted insect pests caused sub stantial damage to non-GE varieties and synthetic chemicals did not provide practical control.
From page 116...
... These differences could confound the estimation of the apparent yield advantage of the Bt varieties. RECOMMENDATION: In future experimental and survey studies that compare crop varieties with IR traits with those without the traits, it is important to assess how much of the difference in yield is due to decreased insect damage and how much may be due to other factors.
From page 117...
... . The decrease for nonadopters could be due to the regional decline in European corn borer populations (see Box 4-2)
From page 118...
... 118 GENETICALLY ENGINEERED CROPS FIGURE 4-5  Rates of insecticide application by adopters and nonadopters of Bt maize in the United States from 2001 to 2010. SOURCE: Fernandez-Cornejo et al.
From page 119...
... (2008) studied the relationship between insecticide use and Bt cotton in South Africa and found that farms using Bt cotton ap plied insecticide at 1.6 liters/hectare, and those with non-Bt cotton applied 2.4 liters/hectare.
From page 120...
... Bt toxins are proteins that are insect-specific, and they are rapidly destroyed by microbial action when the remains of GE crops decompose. 13 Managing Insect Pests in Organically Certified Field Corn.
From page 121...
... In some cases, the use of Bt crop varieties has also been associated with reduced use of insecticides in fields with non-Bt varieties of the crop and other crops. Changes in Secondary Insect Pests Due to Bt Crops The control of targeted species by Bt toxins sometimes provides an opportunity for populations of "secondary" insect species to increase.
From page 122...
... They concluded that the secondary insect pests "may not be serious enough to undermine the use of the technology, but do require further exploration so that practical and economically viable advice can be given to farmers and so that regulators are aware of potential issues and risks during a crop's approval phase." Resistance Evolution and Resistance Management in Bt Crops The evolution of target insects with resistance to Bt toxins has resulted in substantial economic losses for farmers of Bt crops. The committee heard from members of the public, researchers, and farmers that such resistance is an indication that genetic-engineering technology is not sustainable, and it reviewed evidence of the problem.
From page 123...
... -- but not ­others -- for example, cotton bollworm, fall armyworm, and western corn rootworm. For cases in which a high dose was lacking, theory clearly in dicated that a much larger refuge was required to delay resistance (EPA, 2002)
From page 124...
... For example, Monsanto's SmartStax® maize variety has two Bt genes targeted at the European corn borer and other Lepidoptera and two other Bt genes aimed at the western corn rootworm. Those stacked varieties can make resistance-management approaches complicated.
From page 125...
... As described in Box 4-2, Bt crops have caused the European corn borer population to decline to the point where they are well below economic thresholds, so it often is not economically favorable for farmers to grow maize with the Bt toxins that are aimed primarily at the corn borers (Hutchison et al., 2010; Bohnenblust et al., 2014)
From page 126...
... FINDING: The high dose/refuge strategy for delaying evolution of re sistance to Bt toxins appears to have been successful, but deployment of crops with intermediate levels of Bt toxins and small refuges has sometimes resulted in the evolution of resistance in insect pests that erodes the benefits of the Bt crops. FINDING: The widespread deployment of crops with Bt toxins has decreased some insect-pest populations to the point where it is eco nomically realistic to increase plantings of crop varieties without a Bt toxin that targets these pests.
From page 127...
... Yield Effects of Genetically Engineered Herbicide Resistance As of 2015, GE herbicide resistance had been incorporated into soybean, maize, cotton, canola, sugar beet (Beta vulgaris) , and alfalfa (­Medicago sativa)
From page 128...
... and those with non-HR soybean in five of the six locations.14 When the plots with HR soybean treated with glyphosate were compared with the plots with the HR soybean treated with other herbicides, yields for the HR soybean treated with glyphosate in four of the locations were greater. When HR soybean treated with glyphosate was compared with the non-HR parent line of the HR soybean treated with other herbicides, the yields for the HR soybean were greater in three of the locations.
From page 129...
... .15 Gurian-Sherman and the National Research Council report looked at the same studies from the early 2000s16 and found evidence of yield drag and yield lag. However, more recent s­tudies, such as those reviewed above, demonstrate that yield drag and yield lag appear to have been overcome in HR soybean because the yields of HR soybean are the same as or more than the yields of non-HR soybean.
From page 130...
... In the dry season of 2007–2008, five provinces reported a yield advantage; the average yield in two other provinces was nearly equivalent between HR and non-GE maize. Two years later, in the wet season of 2010, Afidchao et al.
From page 131...
... Those yield increases were as much as 38 percent greater, which they attributed to improved weed control in some circumstances but also to higher potential yield in the germplasm of the HR varieties. In field studies conducted throughout Canada under different environmental conditions, yield of the GE and nonGE varieties was similar (Clayton et al., 2004)
From page 132...
... In Idaho, weed control and yield were comparable in plants treated with glyphosate and with the herbicides typically used in sugar beet production (Guza et al., 2002)
From page 133...
... and that only application to sugar beet increased (25.6 percent)
From page 134...
... (2010) provided a comparative environmental risk assessment of glyphosate and other herbicides.
From page 135...
... . Some of the changes in weed species at that time could also have been associated with the increase in use of no-till and reduced-till crop production practices.
From page 136...
... . FINDING: Both for insect pests and weeds, there is evidence that some species have increased in abundance as IR and HR crops have become widely planted.
From page 137...
... . In 2009, Palmer amaranth was ranked as the number one weed species in cotton production in the southern United States, mostly due to its resistance to glyphosate (Webster and Nichols, 2012)
From page 138...
... Those herbicides have different sites of action, so crops with stacked HR traits could reduce specific selection pressure from glyphosate. However, that would not be the case for all weed species because some weeds are susceptible to only one herbicide in mixed herbicide applications.
From page 139...
... , fit well with approaches to conservation tillage. In general, integrated weed management requires a detailed understanding of the weed-community ecology in a specific area.
From page 140...
... Nolan and Santos (2012) found that maize with GE traits of Bt targeting European corn borer and herbicide resistance had a yield advantage of 501 kilograms/hectare over a non-GE variety.
From page 141...
... It is expected that when an insect-pest population declines dramatically because of Bt crops, as in the case of European corn borer in the United States, there will be an accompanying decline in any host-specific parasitoid or pathogen of the pest, and the parasitoid or pathogen could even become locally extinct (Lundgren et al., 2009)
From page 142...
... When weeds were controlled by a single application of glyphosate to HR maize and soybean, there was typically greater weed diversity and abundance than when other herbicides were ­applied to the non-GE counterparts. However, in HR sugar beet treated
From page 143...
... emphasized that how the HR trait is integrated with other weed control strategies will determine the local weed composition. Effects of Genetically Engineered Traits on Crop Diversity on Farms Maintaining a diversity of crop species on farms and a diversity of varieties of each crop on a farm is generally considered to provide a b ­ uffer against outbreaks of insect pests and pathogens and insurance against year-to-year environmental fluctuations that could be especially damaging to one crop or variety (Hajjar et al., 2008; Davis et al., 2012; Mijatović et al., 2013)
From page 144...
... . At the individual farm level in the United States, there is little evidence of a substantial shift toward continuous cropping (3 or more consecutive years of a single crop)
From page 145...
... , who indicated that some farmers rely on GE varieties of row crops to control weeds and enable crop rotations that include non-GE vegetables and other non-GE crops in which weed control is otherwise prohibitively expensive or difficult. For those farmers, GE crops are enabling the maintenance of more diverse cropping systems.
From page 146...
... FINDING: Although the number of available crop varieties declined in the 20th century, there is evidence that genetic diversity among major crop varieties has not declined in the late 20th and early 21st centuries since the introduction and widespread adoption of GE crops in some countries. Effects of Genetically Engineered Crops at the Landscape and Ecosystem Levels The discussion in the section above was confined to potential effects of GE crops on biodiversity on farms themselves.
From page 147...
... Genetically Engineered Crops and the Expansion of Agriculture into Unmanaged Environments On the basis of the data presented on the effects of GE crops on bio­ diversity on farms, there is evidence of some changes in the specific weeds in fields due to herbicides used in association with GE crop varieties, although the overall plant biodiversity does not seem to change substantially (Young et al., 2013; Schwartz et al., 2015)
From page 148...
... The 2002 National Research Council report saw this portfolio of coordinated studies conducted with transparency and open access to data and supported by diverse funders as a model for dealing with controversial GE crop issues and suggested that "present public research programs, such as in Biotechnology Risk Assessment and Risk Management, will need to be expanded substantially"; the report specifically pointed to the USDA Biotechnology Risk Assessment Research Grants Program in this regard (NRC, 2002:197–198)
From page 149...
... If lower abundance of milkweed is limiting the monarch populations, there is expected to be an indication of it in their population dynamics beyond winter habitats in Mexico. A series of articles published in 2015 examined data from researchers and citizen scientists collected in 1995–2014 on ­dynamics of monarch populations as they moved north in spring and began moving south in fall (Badgett and Davis, 2015; Crewe and McCracken, 2015; Howard and Davis, 2015, Nail et al., 2015; Ries et al., 2015; Steffy, 2015; Stenoien et al., 2015)
From page 150...
... Dispersal of Genes from Genetically Engineered Crops to Wild Species Gene flow is the change in gene frequency in a population due to the introduction of a gene or genes through gametes, individuals, or groups of individuals from other populations (Slatkin, 1987)
From page 151...
... Populations of HR alfalfa, canola, and creeping bentgrass (Agrostis stolonifera) produce feral populations that survive outside cultivation, increase with selection pressure from herbicides, and continue to be a transgene pollen source (Knispel et al., 2008; Zapiola et al., 2008; Schafer et al., 2011; Bagavathiannan et al., 2012; Greene et al., 2015)
From page 152...
... FINDING: Although gene flow has occurred, no examples have dem onstrated an adverse environmental effect of gene flow from a GE crop to a wild, related plant species. Herbicide-Resistant Crops, Reduced Tillage, and Ecosystem Processes No-till and reduced-till agricultural practices are known for decreasing wind and water erosion of soil (Montgomery, 2007)
From page 153...
... That is especially evident with the adoption of HR soybean, although the conclusion also holds for cotton and maize. Those conclusions are based on aggregate trends and do not allow one to determine that the introduction of GE herbicide resistance is causing the adoption of no-till or that the increase in no-till is accompanied by adoption of GE herbicide resistance.
From page 154...
... Evolved herbicide resistance in weeds was associated with the overuse of a single herbicide. If GE crops are to be used sustainably, regulations and incentives must be provided to farmers so that more integrated and sustainable pest management approaches become economically feasible.
From page 155...
... and southwestern corn borer (Lepidoptera: Crambidae)
From page 156...
... 2002. Use of transgenic Bacillus thuringiensis Berliner corn hybrids to determine the direct economic impact of the European corn borer (Lepidoptera: Crambidae)
From page 157...
... Presentation to the National Academy of Sciences' Committee on Genetically Engineered Crops: Past Experience and Future Prospects, September 16, Washington, DC. Crawley, M.J., R.S.
From page 158...
... Webinar presentation to the National Academy of Sciences' Committee on Genetically Engineered Crops: Past Experi ence and Future Prospects, January 27. Dillehay, B.L., G.W.
From page 159...
... 2014. Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize.
From page 160...
... 2014. Remarks to the National Academy of Sciences' Committee on Genetically Engineered Crops: Past Experience and Future Prospects, September 16, Washington, DC.
From page 161...
... 2010. Area wide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers.
From page 162...
... 2008. Gene flow and mul tiple herbicide resistance in escaped canola populations.
From page 163...
... 2004. Economic evalu ation of glyphosate-resistant and conventional sugar beet.
From page 164...
... , populations in India. Pest Management Science 72:738–746.
From page 165...
... 2010a. The Impact of Genetically Engineered Crops on Farm Sustainability in the United States.
From page 166...
... 1997. European corn borer management in field corn: A survey of perceptions and practices in Iowa and Minnesota.
From page 167...
... 2013. Comparison of weed control, yield, and net income in conventional, glyphosate-resistant, and glufosinate-resistant soybean.
From page 168...
... Pest Management Science 61:246–257. Thelen, K.D., and D
From page 169...
... 2015. Susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae)
From page 170...
... 2012. Crossing the divide: Gene flow produces inter­ generic hybrid in feral transgenic creeping bentgrass population.


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