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Genetically Engineered Crops: Experiences and Prospects


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This consensus report examines a range of questions and opinions about the economic, agronomic, health, safety, or other effects of genetically engineered (GE) crops and food. Claims and research that extol both the benefits and risks of GE crops have created a confusing landscape for the public and for policy makers. This report is intended to provide an independent, objective examination of what has been learned since the introduction of GE crops, based on current evidence.

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Responses to Public Comments

Appendix F – Summarized Comments Received from Members of the Public

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Errata

The prepublication version of Genetically Engineered Crops: Experiences and Prospects released on May 17, was provided to the public to facilitate timely access to the report. Although the substance of the report is final, editorial changes were made throughout the text and citations were checked prior to final publication. Notices of factual errors in the prepublication version from the public were submitted to National Academies staff until September 30, 2016.

The following factual errors in the prepublication version are corrected in the final text.

 

Page Error Correction
10 Incorrect sentence: In 2015, the International Agency for Research on Cancer (IARC) of the World Health Organization (WHO) issued a monograph in which it changed its classification of glyphosate from Group 2B (possibly carcinogenic to humans) to Group 2A (probably carcinogenic to humans). Correction: In 2015, the International Agency for Research on Cancer (IARC) of the World Health Organization (WHO) issued a monograph in which it classified glyphosate in Group 2A (probably carcinogenic to humans).
11 Incorrect word: Virus-resistant papaya is an example of a GE crop that is conducive to adoption by small-scale farmers because it addresses an agronomic problem but does not require concomitant purchase of such inputs as fertilizer or insecticides. Correction: Virus-resistant papaya is an example of a GE crop that is conducive to adoption by small-scale farmers because it addresses an agronomic problem but does not require concomitant purchase of such inputs as fertilizer or pesticides.
38 Incorrect reference: De Schutter, O. and S. Deakin. 2003. Reflexive governance and the dilemmas of social regulation. European Law Review 28:814. Correction: De Schutter, O., and S. Deakin. 2005. Reflexive governance and the dilemmas of social regulation. In Social Rights and Market Forces: Is the Open Coordination of Employment and Social Policies the Future of Social Europe? O. De Schutter and S. Deakin, eds. Brussels: Bruylant.
48  Errors in Table 3-1 Correction: Table 3-1 has been corrected to reflect the list of petitions to USDA–APHIS for determination of nonregulated status as of December 2015.
68 Footnote clarification: An isogenic line has closely related genotypes of a crop that differ by one or a few genes and are therefore expected to perform similarly on farms. A near isogenic line (or near isoline) is more vaguely defined and can have similar varieties, but they may have differences in performance under some farm conditions. Correction: An isogenic line has closely related genotypes of a crop that differ by one or a few genes and are therefore expected to perform similarly on farms. Near isogenic lines (or near isolines) are more vaguely defined and can have multiple genes differing between them and thus may have differences in performance under some farm conditions.
74 Footnote clarification: Thus, about 50 percent of cropland in the United States was producing GE crops (Fernandez-Cornejo et al., 2014). Correction: Seventy million hectares is roughly half of all U.S. cropland. Thus, about 50 percent of cropland in the United States was producing GE crops when the committee was writing its report (Fernandez-Cornejo et al., 2014).
77 Sentence clarification:  Douglas and Tooker (2015) provided a detailed assessment of U.S. data on the increase in use from the 1990s until 2011. It is clear that the increase was as dramatic in soybean as in maize. Commercial soybean in the United States has not been engineered to produce Bt toxins, so the increase in neonicotinoid use in this crop clearly was not associated with the use of Bt varieties. Correction: Douglas and Tooker (2015) provided a detailed assessment of U.S. data on the increase in use of neonicotinoids from the 1990s until 2011. It is clear that the increase was as dramatic in soybean as in maize. As of 2015, commercial soybean in the United States had not been engineered to produce Bt toxins, so the increase in neonicotinoid use in this crop clearly was not associated with the use of Bt varieties.
86 Incorrect acronym: EIC Correction: EIQ
98 Incorrect sentence: In one research study, transfer of the Bt trait from GE sunflowers to wild sunflowers reduced insect feeding injury on the wild sunflowers and increased their fecundity, though the results were not statistically significant (Snow et al., 2003).
Correction: In one research study, transfer of the Bt trait from GE sunflowers to wild sunflowers reduced insect feeding injury on the wild sunflowers and increased their fecundity (Snow et al., 2003).
99 Missing citation: Unlike previous researchers, they found that “HR soybean adoption has a positive and highly significant (P < 0.0001) impact on the adoption of conservation tillage” in the United States. Correction: Unlike previous researchers, they found that “HR soybean adoption has a positive and highly significant (P < 0.0001) impact on the adoption of conservation tillage” in the United States (Fernandez-Cornejo et al., 2012:236–237).
 101 Incorrect reference title: Barfoot, P. and G. Brookes. 2014. Key global economic and environmental impacts of genetically modified (GM) crop use 1996-2012. GM Crops and Food: Biotechnology in Agricultural and the Food Chain 5:149–160. Corrected reference title: Barfoot, P. and G. Brookes. 2014. Key global environmental impacts of genetically modified (GM) crop use 1996-2012. GM Crops and Food: Biotechnology in Agricultural and the Food Chain 5:149–160.
128 Missing reference: Magana-Gomez and de la Barca (2009), Snell et al. (2012), and Ricroch et al. (2013b) reviewed the studies. Correction: Magana-Gomez and de la Barca (2009), Domingo and Bordonaba (2011), Snell et al. (2012), and Ricroch et al. (2013b) reviewed the studies.
131 Delete paragraph: Herman and Price (2013) argued that, because biologically relevant unintended compositional changes have not been found in GE crops over a 20-year period, such testing is not justifiable. The current compositional analyses have not assessed whether the components measured are the appropriate ones to examine or whether differences found in measured components are indicators that there are differences in other unmeasured components. Reason: Deleted to correct implication that identifying the compositional components for analysis is not given sufficient forethought to ensure that the components most relevant to safety and nutrition are being measured.
133 Delete sentence: In the year of seeding and the following year, the two systems were similar in yield and forage quality. In a research trial conducted over 5 years, glyphosate-resistant and non-GE alfalfa had similar yield when herbicides typically used in non-GE production were applied Reason: Incorrect statement.
133 Clarification to sentence: The latter factor comes from research demonstrating that proteins already known to be food allergens are resistant to digestion by gut fluids. Correction: The latter factor comes from research demonstrating that some, but not all, proteins already known to be food allergens are resistant to digestion by gut fluids.
134 Clarification to sentence: In the second case, EPA allowed a Bt maize variety with a potential for allergenicity (due to decreased digestion of the protein Cry9c in simulated gastric fluid) to be sold as cattle feed; because of the potential for allergenicity, the variety was not approved for direct human consumption. Correction: In the second case, EPA allowed a Bt maize variety developed by Aventis CropScience with a potential for allergenicity (due to decreased digestion of the protein Cry9c in simulated gastric fluid) to be sold as cattle feed under the name StarLink™; because of the potential for allergenicity, the variety was not approved for direct human consumption.
137 Incorrect reference: Assessment of glyphosate is relevant to the committee’s report because it is the principal herbicide used on HR crops (Landrigan and Benbrook, 2015; Guyton et al., 2015), and it has been shown that there are higher residues of glyphosate in HR soybean treated with glyphosate than in non-GE soybean (Duke et al., 2003; Bøhn et al., 2014). Correction: Assessment of glyphosate is relevant to the committee’s report because it is the principal herbicide used on HR crops (Livingston, et al. 2015), and it has been shown that there are higher residues of glyphosate in HR soybean treated with glyphosate than in non-GE soybean (Duke et al., 2003; Bøhn et al., 2014).
138 Incorrect sentences: In the monograph, IARC changed its classification of glyphosate from Group 2B (possibly carcinogenic to humans) to Group 2A (probably carcinogenic to humans). A summary and reasons for the change in classification were published in Lancet Oncology (Guyton et al., 2015). Correction: In the monograph, IARC classified glyphosate in Group 2A (probably carcinogenic to humans). A summary and reasons for the classification were published in Lancet Oncology (Guyton et al., 2015).
143 Missing citation: They concluded that “diversification of the weed community, both in the weed seedbank and aboveground, is reflective of geographic region, cropping system being implemented and crop rotation, but not frequency of the use [of] the [glyphosate-resistant] crop trait.” They emphasized that how the HR trait is integrated with other weed control strategies will determine the local weed composition. Correction: Schwartz et al. (2015:437) concluded that “diversification of the weed community, both in the weed seedbank and aboveground, is reflective of geographic region, cropping system being implemented and crop rotation, but not frequency of the use [of] the [glyphosate-resistant] crop trait.” Schwartz et al. emphasized that how the HR trait is integrated with other weed control strategies will determine the local weed composition.
146 Missing citation: The CDC report stated that “the extent to which this variation might be attributable to diagnostic practices, under recognition of ASD symptoms in some racial/ethnic groups, socioeconomic disparities in access to services, and regional differences in clinical or school-based practices that might influence the findings in this report is unclear.” Correction: The CDC report stated that “the extent to which this variation might be attributable to diagnostic practices, under-recognition of ASD symptoms in some racial/ethnic groups, socioeconomic disparities in access to services, and regional differences in clinical or school-based practices that might influence the findings in this report is unclear” (CDC, 2014:1).
147 Missing citation: These similarities between countries as well as within different locations in each country point to a common etiology for this extraordinary medical case.” Correction: These similarities between countries as well as within different locations in each country point to a common etiology for this extraordinary medical case” (Taylor et al., 2013:5).
154 Missing citation: They reviewed cohort, case–control, and cross-sectional studies within the AHS study and found “no evidence of a consistent pattern of positive associations indicating a causal relationship between any disease and exposure to glyphosate.” Correction: They reviewed cohort, case–control, and cross-sectional studies within the AHS study and found “no evidence of a consistent pattern of positive associations indicating a causal relationship between any disease and exposure to glyphosate” (Mink et al., 2011:172).
173 Clarification to footnote: Argentina, Australia, Canada, Chile, China, Czech Republic, France, India, Mexico, Mozambique, Philippines, Portugal, Romania, South Africa, Spain, and the United States. Correction: Klümper and Qaim (2014) included ex-ante and ex-post studies conducted in Argentina, Australia, Brazil, Burkina Faso, Canada, Chile, China, Colombia, Czech Republic, Germany, India, Mali, Pakistan, Philippines, Portugal, Romania, South Africa, Spain, and the United States.
175 Added reference: They also included data on Bt maize in 10 countries; most of the studies were conducted in Germany, Spain, South Africa, and Argentina. Correction: They also included data on Bt maize in 10 countries; most of the studies were conducted in Germany, Spain, South Africa, and Argentina (Finger et al., 2011).
177 Delete sentence: The authors concluded that Bt maize needed more fertilizer to promote the production of the Bt toxin and that farmers’ concerns about Asian corn borer (Ostrinia furnacalis [Guenée]) caused them to continue to spray insecticides even when Bt maize was planted. Average net income and return on investment did not differ between non-GE growers and Bt growers. The authors concluded that “Bt and Bt/HT corn hybrids containing the Cry1Ab protein performed well in Isabela Province. Reduced cob damage by Asian corn borer on Bt fields could mean smaller economic losses even with Asian corn borer infestation. Correction: The authors concluded that Bt maize needed more fertilizer to promote the production of the Bt toxin and that farmers’ concerns about insect pests other than Asian corn borer (Ostrinia furnacalis [Guenée]) caused them to continue to spray insecticides even when Bt maize was planted. Average net income and return on investment did not differ between non-GE growers and Bt growers.
181 Incorrect sentences: Studies conducted in Canada, Australia, and the European Union (EU) provide evidence on the economic benefits to adopters of HR canola (see Phillips 2003; Beckie et al., 2006; Gusta et al., 2011; Smyth et al., 2014a) and of HR sugar beet (Dillen et al., 2013; Nichterlein et al., 2013; Tillie et al., 2014). Studies of income effects after adoption of more recently commercialized crops, such as Bt eggplant or drought-tolerant maize, have yet to be done. Correction: Studies conducted in Canada provide evidence on the economic benefits to adopters of HR canola (see
Phillips, 2003; Beckie et al., 2006; Gusta et al., 2011; Smyth et al., 2014a). Studies of income effects after adoption of more recently commercialized crops, such as Bt eggplant or drought tolerant maize, have yet to be done.
183 Incorrect sentence: In the case of cotton, a substantial body of evidence shows that countries who have become world leaders in cotton production (India, China, and Pakistan) use Bt and Bt-HR cotton and that the use of those varieties has created benefits to smallholder farmers. Correction: In the case of cotton, a substantial body of evidence shows that countries who have become world leaders in cotton production (India, China, and Pakistan) use Bt cotton and that the use of those varieties has created benefits to smallholder farmers.
185 Incorrect sentence: About 25 percent of survey respondents who adopted maize with Bt and HR traits said that they did not find GE maize to have been worth the investment, whereas 75 percent did find it worthwhile Correction: About 25 percent of survey respondents who adopted maize with Bt and HR traits said that they no longer agreed with the statements that GE maize is worth investing in and could improve farmer livelihoods.
186 Incorrect sentence: Other farmers continued to use insecticides that were redundant to the insects targeted by Bt; this indicated a lack of facility with the technology. Correction: Other farmers continued to use insecticides to control insect pests not targeted by Bt.
186 Incorrect statement: They concluded that the social and economic conditions observed with respect to seed costs and lending costs, the lack of familiarity with the technology, and the inability to exploit the technology’s potential could keep GE maize varieties from being economically advantageous compared with non-GE varieties for resource-poor farmers in the Philippines. Correction: They concluded that the social and economic conditions observed with respect to seed costs and lending costs and the inability to exploit the technology’s potential could keep GE maize varieties from being economically advantageous compared with non-GE varieties for resource-poor farmers in the Philippines.
198 Clarification: Coexistence has appeared not only since GE crops were commercialized. Correction: Coexistence is not an issue that has only appeared since GE crops were commercialized.
198 Incorrect sentence: Seeds with GE traits left over from the previous season can germinate in a field that has been planted with organic or non-GE seed in the following season. Correction: Seeds with GE traits left over from the previous season can germinate in a field that has been planted with non-GE seed in the following season.
204 Clarification: The consequence of asynchronous approval is that exporters of crops with GE traits must segregate from exports so that they only send non-GE crops or GE crops that have been approved into the importing jurisdiction. Correction: The consequence of asynchronous approval is that exports of crops with GE traits must be segregated from exports of non-GE crops so that exporters only send non-GE crops or GE crops that have been approved into the importing jurisdiction.
207 Clarification: Aventis, the maker of Starlink, paid over $120 million to settle various lawsuits (Cowan, 2013). Correction: Aventis CropScience, the maker of StarLink™ maize, paid over $120 million to settle various lawsuits (Cowan, 2013; see “Food Allergenicity Testing and Prediction” section in Chapter 5.
209 Clarification:  The reason for that difference is that, although compositional analyses are performed on all new varieties to demonstrate that they are safe and within normal genetic variation, toxicity tests and environmental assessments that are not performed on conventionally bred crops are performed on GE crops. Correction: The reason for that difference is that, although compositional analyses are often performed on new varieties to demonstrate that they are within normal genetic variation, toxicity tests and environmental assessments that are not performed on conventionally bred crops are performed on GE crops.
216 Clarification: For example, a farmer might want only the HR trait in a maize variety but be unable to find a maize variety that does not also include Bt traits (see Chapter 4); this may lead to higher seed costs for the farmer in that the farmer does not need the added trait but is paying for it. Correction: For example, a farmer might want only the HR trait in a maize variety but be unable to find a maize variety that does not also include Bt traits (see discussion of resistance evolution and resistance management in Chapter 4); this may lead to higher seed costs for the farmer in that the farmer does not need the added trait but is paying for it.
223 Missing reference Correction: Busch, L., W. Lacy, J. Burkhardt, and L. Lacy. 1991. Plants, Power, and Profits: Social, Economic, and Ethical Consequences of the New Biotechnologies. Oxford, UK: Basil Blackwell.
227 Missing reference Correction: Graff, G., and D. Zilberman. 2016. How the IP–Regulatory Complex affects incentives to develop socially beneficial products from agricultural genomics. Pp. 68–101 in The Intellectual Property—Regulatory Complex: Overcoming Barriers to Innovation in Agricultural Genomics, E. Marden, R.N. Godfrey, and R. Manion, eds. Vancouver: UBC Press.
227 Missing reference Correction: Heinemann, J.A., M. Massaro, D.S. Coray, S.Z. Agapito-Tenfen, and J.D. Wen. 2014. Sustainability and innovation in staple crop production in the US Midwest. International Journal of Agricultural Sustainability 12:71–88.
228 Missing reference Correction: Jefferson, R. 2006. Science as social enterprise: The CAMBIA BiOS initiative. Innovations 1:13–44.
229 Missing reference Correction: Kolady, D.E., D.J. Spielman, and A. Cavalieri. 2012. The impact of seed policy reforms and intellectual property rights on crop productivity in India. Journal of Agricultural Economics 63:361–384.
229 Missing reference Correction: Krishna, V.V., M. Qaim, and D. Zilberman. 2016. Transgenic crops, production risk, and agrobiodiversity. European Review of Agricultural Economics 43:137–164.
230 Missing reference Correction: Mohan, K.S., K.C. Ravi, P.J. Suresh, D. Sumerford, and G.P. Head. 2016. Field resistance to the Bacillus thuringiensis protein CrylAc expressed in Bollgard® hybrid cotton in pink bollworm, Pectinophora gossypiella (Saunders), populations in India. Pest Management Science 72:738–746.
231 Missing reference Correction: Parentoni, S.N., R. Augusto de Miranda, and J.C. Garcia. 2013. Implications on the introduction of transgenics in Brazilian maize breeding programs. Crop Breeding and Applied Biotechnology 13:9–22.
233 Missing reference Correction: Smale, M., and J. Falck-Zepeda. 2012. Farmers and researchers discovering biotech crops: Experiences measuring economic impacts among new adopters. A Special Issue of AgBioForum 15.
235 Missing reference Correction: Van Brunt, J. 1985. Ex parte Hibberd: Another landmark decision. Nature Biotechnology 3:1059–1060.
240 Clarification: When the backwards gene is transcribed, the messenger RNA (mRNA) produced from the transgene interferes with the translation into protein of complementary mRNA of the gene to be silenced in the plant or pest (or it can lead to RNA interference, described below). Correction: When the backwards gene is transcribed, the messenger RNA (mRNA) produced from the transgene interferes with the translation of complementary mRNA of the gene to be silenced in the plant or pest into protein (or it can lead to RNA interference, described below).
251 Clarification: The following example considers the selection of gain-of-function strategies for increasing the amounts of a beneficial chemical component (such as a nutrient or useful pharmaceutical compound) in a plant. Correction: There are both conventional-breeding and genetic-engineering approaches for the selection of gain-of-function traits such as increasing the amount of a beneficial component (for example, a nutrient or useful pharmaceutical compound).
265 Missing reference Correction: Fraser, C.M., J.D. Gocayne, O. White, M.D. Adams, R.A. Clayton, R.D. Fleischmann, C.J. Butt, A.R. Kerlavge, G. Sutton, J.M. Kelley, J.L. Fritchman, J.F. Weidman, K.V. Small, M. Sandusky, J. Fuhrmann, D. Nguyen, T.R. Utterback, D.M. Saudek, C.A. Phillips, J.M. Merrick, J.F. Tomb, B.A. Dougherty, K.F. Bott, P.C. Hu, T.S. Lucier, S.N. Peterson, H.O. Smith, C.A. Hutchison, and J.C. Venter. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397–403.
277 Incorrect sentence: According to the American Chestnut Research and Restoration Project, the GE trees will be initially introduced in areas currently devoid of trees, in botanical gardens, and on private land (Powell, 2015). Correction: According to the American Chestnut Research and Restoration Project, should the GE chestnut be submitted to and ultimately approved by EPA (and any other regulatory agencies if needed), the GE trees will be initially introduced in areas currently devoid of trees, in botanical gardens, and on private land (Powell, 2015).
278 Incorrect word: Lack of gossypol detoxification as a result of RNAi-targeted silencing of CYP6AE1 expression led to drastic reduction of bollworm larval growth on cotton plants that were engineered to express the CYP6AE14 dsRNA (Mao et al., 2011b). Correction: Lack of gossypol detoxification as a result of RNAi-targeted silencing of CYP6AE14 expression led to drastic reduction of bollworm larval growth on cotton plants that were engineered to express the CYP6AE14 dsRNA (Mao et al., 2011b).
279 Incorrect word: Another report described the expression of dsRNA against the gossypoldetoxifying CYP6AE1 and other targets in tobacco chloroplasts (Jin et al., 2015) and concluded that the strategy was effective for insect control. Correction: Another report described the expression of dsRNA against the gossypoldetoxifying CYP6AE14 and other targets in tobacco chloroplasts (Jin et al., 2015) and concluded that the strategy was effective for insect control.
313 Incorrect sentences: The first GE whole food to receive FDA approval, the FLAVR SAVR™ tomato, was approved under a food-additive approval process in 1994. At the manufacturer’s request, FDA approved a kanamycin-resistant marker gene in the transformed tomato as a food additive (FDA, 1994). Correction: In 1994, the FLAVR-SAVR tomato was the first whole food from a genetically engineered plant to be reviewed by FDA under its voluntary consultation process. At the same time, at the developer’s request, the FDA approved an enzyme (aminoglycoside 3’ phosphotransferase II) encoded by the kanamycin resistance gene in the FLAVR SAVR tomato as a food additive (FDA, 1994).
336 Clarification to sentence: In particular, the committee was aware that the lack of public access to the health and safety data submitted by developers creates distrust in some stakeholders. Add Footnote: With respect to FDA’s consultation process, interested parties are able to obtain the developer submissions and related data that are not trade secrets or confidential commercial information from the agency by submitting a Freedom of Information Act request. Health and safety data submitted to FDA as part of final consultations are typically available to the public upon request.
338 Incorrect footnote: In addition to the unintended changes in the plant itself, risk assessors need to consider unexpected or unintended effects of the trait that has been intentionally introduced into the plant. In the environmental assessment, for example, regulators would need to consider whether organisms other than the intended target organism of a plant-incorporated protectant would be unintentionally harmed, whether through direct action (for example, toxicity) or indirect action (for example, loss of habitat). Correction: In addition to the unintended changes in the plant itself, risk assessors need to consider unexpected or unintended effects of the trait that has been intentionally introduced into the plant. In the environmental assessment, for example, regulators would need to consider whether organisms other than the intended target organism of a plant-incorporated protectant would be unintentionally harmed, whether through direct action (for example, toxicity) or indirect action (for example, loss of habitat).
346 Incorrect reference: NRC (National Research Council). 2004. Biological Confinement of Genetically Engineered Organisms. Washington, DC: National Academies Press. Correction: NRC (National Research Council). 2004. Safety of Genetically Engineered Foods: Approaches to Assessing Unintended Health Effects. Washington, DC: National Academies Press.

 

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