Key words: biodiversity, GM crops, GMO, sustainability

Introduction

Agriculture is associated with several critical societal issues, including carbon footprint and climate change, water use, biodiversity, food security, early childhood nutrition and food vs. feed vs. fuel. As an industry, agricul-ture needs to do a better job communicating with a public that in industrial-ized countries has become too distant from current agricultural practices. Improvements in animal productivity (growth rates, milk production, etc.) are critical to increasing the efficiency of animal production and reducing the footprint of animal agriculture. These improvements have largely come from dilution of maintenance (Capper, 2011) while other improvements can come from increased digestibility or nutrient availability from feeds (Jung and Allen, 1995), reduced non-productive days for dairy (Meyer et al., 2006; Klusmeyer et al., 2009), or genetic selection for feed efficiency (Connor, 2015). Since feed is a large portion of the inputs in animal agriculture, its impact on the overall footprint of animal agriculture, as well as on the labor and profitability of farms, needs to be well understood. Since the adoption of genetically modified (GM) crops more than 20 yr ago, they have been widely adopted in the U.S. and other regions, resulting in a reduced carbon footprint of crop production. This paper will discuss the development, ben-efits, and some of the controversies of GM crops fed to livestock.

Conventional Crop Breeding

Domestication of crops and conventional breeding has been practiced for thousands of years by selecting phenotypes such as yield, grain quality, dis-ease resistance, etc. Teosinte, the ancestor of corn, illustrates how this type of selection can result in a significant change in phenotype that results in a major, yet beneficial change in a crop. Teosinte is a multi-stalked grass that produces up to 12 kernels encased in a hard covering that makes it relatively inedible, in contrast to today’s modern single-stalk corn varieties that have 500 highly digestible kernels. One theory is that teosinte could not have been developed by man because it would offer little or no encouragement as a food source (Beadle, 1939). The goal of traditional plant breeding is to develop newer, better varieties by mating two parents that have desirable qualities and selecting the best progeny. This seems to be very simple on face value, but commercial-scale production of seed that competes in a global marketplace is an incredibly complex process (Glenn et al., 2017). In the case of corn, new hybrids are developed by breeding inbred lines selected for specific traits. The first generation will contain the desired trait but also will contain some undesirable genetic changes. Undesirable genetic changes occur during plant breeding by several mechanisms including: combining genes from one inbred that might have been lost in the other line, random or purposefully induced mutations, and by chromosomal rearrangements. The undesirable genetic changes are selected against through at least six generations of back-crossing in which progeny with the undesirable characteristics are eliminated while retaining plants with the desired trait(s). To ensure that the intended genes are moved and undesirable genes are not in the commercialized prod-uct, it takes more than six seasons and thousands of test plots in multiple geographies to develop new hybrids, most of which never reach commercial-ization. Throughout the process, plants are selected for advancement based on the traditional method of identifying phenotypes as well as by newer ge-nomic approaches such as marker-assisted selection (Eathington et al., 2007). Marker-assisted selection al-lows for testing new inbreds or hybrids with fewer plots, which reduces the footprint of seed production.

Just as with animals, crop breeders depend on germ-plasm diversity for breed-ing improved crop varieties. Random mutations were introduced into crop germ-plasm by treating with chem-icals or placing them near a radiation source—tech-niques known as chemical or irradiation mutagenesis, respectively. There are more

GMO crops in animal nutritionJ.L. Vicini

Regulatory Policy and Scientific Affairs, Monsanto Co., St. Louis, MO 63167

Implications

• Genetically modified (GM or GMO) crops have been widely ad-opted by growers and are a significant source of feed for animal agriculture.

• Most GMO crops commercialized for animal feed have input traits that do not change their composition or nutritional value for animals.

• Feeding GMO crops does not result in detection of transgenic DNA or their translated proteins in meat, milk, or eggs.

• Genetically modified crops help reduce greenhouse gases, de-crease agricultural chemical use, and increase farmer incomes.

• Genetically modified crops provide better pest protection and weed control, which increases yields and preserves more land for wildlife and biodiversity.

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than 3,000 known plant varieties that are commonly consumed by humans or animals, mostly vegetables and cereals, that have been developed using mutagenesis (IAEA, 2016). Plants improved through mutagenesis are ac-ceptable for organic agriculture.

Conventional breeding has been responsible for significant improve-ments in yields throughout the years. In spite of these greater yields, Ray et al. (2013) examined rates of increases for crop yields back to 1961 (when world populations were ~ 3 billion) and determined that this rate has not been sufficient to meet crop requirements for 2050 when the world population is predicted to approach 10 billion. Clearly, more technological breakthroughs are needed to improve agricultural productivity to supply affordable feed. An additional major goal of plant and animal agriculture should be to avoid conversion of forests, wetlands, and prairies to agricul-ture to preserve land for wildlife and support biodiversity.

GM Crops

GM crops (also known as GMOs) are crops that have had at least one gene for a desired trait that was derived from a different plant or organ-ism. The inserted gene, or transgene, can be introduced to the donor plant

by biolistic or Agrobacterium tumefaciens mediated approaches. The first GMO row crop was soybean developed to be resistant to glyphosate (active ingredient in Roundup® herbicide) and was commercialized in 1996. Since then, GM varieties of many other row crops have been commercialized (Pa-risi et al., 2016). Detailed information on approvals of major GM crops is maintained by CERA (2016). Currently, there are eight crops commercial-ized in the U.S. (corn, soybean, cotton, canola, alfalfa, sugar beets, papaya, and some squash varieties) and, with the exception of papaya and squash, these are all significant crops for animal feeds. One criticism of these traits is that farmers derive the benefit from them, and although consumers get benefits (discussed later), they might not recognize them (Herring and Paarlberg, 2016). These crops have genetic modifications that result in one or a combination of traits that include herbicide tolerance, insect resistance, drought tolerance, disease resistance, or reduced lignin (Table 1). Recently approved varieties of non-browning (apple and potato) and reduced aspara-gine (potato) are not yet in stores and will provide direct consumer benefits such as reduced food waste and lowered acrylamide, a carcinogen, after frying. Other traits in the pipeline intended to provide consumer benefits are soybeans with oil that contain stearidonic acid or oil that is higher in oleic acid. Fatty acid composition changes are most notable because these

Table 1. Commercial and pipeline traits by categories for GM crops in the U.S.

Trait

BenefitsFarmer End use consumer

Commercialized1

Herbicide tolerance Corn, soybean, canola, cotton, sugar beet, alfalfa, sweet corn

Weed control, yield, reduced pesticides, reduced input costs, maintain topsoil

Reduced greenhouse gasses, reduced sediment in surface waters

Insect resistance Corn, cotton, sweet corn Insect control, yield, reduced losses, reduced input costs, reduced pesticides

Reduced greenhouse gasses

Drought tolerant Corn Yield, water conservation Commodity price stabilityDisease resistance Papaya, summer squash Grow crop in infected regions, reduced waste Availability, reduced waste, more appealingHybridization System Canola Improved yield, reduced labor Commodity price stability

Pipeline2

Hybridization system Corn Reduced labor costsHerbicide resistance Corn, soybean, cotton.

canola, sugar beetNew mode of action for weed resistance

Insect Resistance Corn, cotton, rice New mode of action for insect resistance managementInsect Resistance Rice, soybean Insect control, yield, reduced losses, reduced input costs,

reduced pesticides

Nematode resistance Soybean Pest controlReduced lignin Alfalfa Flexible harvest windowImproved fatty acid profile Soybean Price premium Reduced waste, Healthier fatty acid profileDisease resistance Chestnut Grow trees in infected regions Forest restoration, lumberDisease resistance Oranges and other citrus Grow crop in infected regions Crop availabilityNon-browning Potato3, apple Reduced waste, more appealingDisease control Corn, sugar beet Yield, Reduced fungicide use (beet)Fungal resistance Soybean Yield, reduced fungicide useYield Soybean YieldYield Sugar beet YieldYield Wheat YieldDrought tolerance Soybean Yield, water conservation Commodity price stability1Commercialized prior to 2016.2From: https://croplife.org/?s = pipeline; Drought tolerant soy also added. For pipeline products only newer expected benefits are listed.3Potato also has reduced potential for acrylamide after frying, which is a carcinogen.

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products were developed to primarily benefit human health. One example of a trait that has a direct human benefit is soybean that makes stearidonic acid (SDA). Stearidonic acid is a precursor of eicosapentaenoic acid (EPA), one of the long-chain omega-3 fatty acids that provides heart healthy benefits of fish oil. Unlike α-linolenic acid (ALA), it is converted to EPA, and it does not have the fishy taste of EPA or fish oil, allowing it to be supplemented into everyday foods. Supplementing foods with SDA results in increased EPA in red blood cell membranes (Lemke et al., 2013), and this magnitude of change has been demonstrated to reduce sudden cardiac death. Moreover, SDA represents a land-based solution to providing needed nutrition without depleting fisheries. Considering these benefits to people and the environ-ment, this will be an interesting GM product in regards to consumer accep-tance. The refined oil does not contain DNA or protein from the transgene; however, food companies will have to be willing to market this as a GM product sold and consumed directly by consumers.

Development and global regulatory approvals of GMOs take consid-erable time and resources (Prado et al., 2014). Although many products have been developed by independent researchers, the majority of the regu-latory approvals have been by large agricultural companies likely due to the burden of time and money excluding smaller companies (Parisi et al., 2016; Ricroch and Hénard-Damave, 2016). Extensive data requirements by global regulatory agencies focus on: 1) the safety of introduced proteins and/or RNA from the inserted DNA; 2) the environmental and/or food/feed safety of the intended trait(s) of the GM crop; and 3) the safety and nutritional quality of the food/feed from the GM crop. The safety and nu-tritional assessment of each GM crop includes a conventional variety as a comparator that has a history of safe use. This does not mean that the non-GM crop is 100% safe as most foods contain undesirable compound(s) (i.e., lectins in soybean, solanine in potato, etc.). The standard for compari-son of the new GM crop is that it is as safe as the comparator that has been commonly consumed. The safety of the differences between the food or feed from a GMO crop and its conventional counterpart is assessed before commercialization. Studies are conducted to examine relevant aspects of the recipient crop itself, the transgene and its insertion, the gene product, and safety assessment of the new crop (Fig. 1). Data that are particularly notable for animal production systems come from composition analyses that are further confirmed by animal feeding studies.

Composition studiesCrop composition studies are conducted

with samples that come from replicated field sites in multiple geographic locations (Brune et al., 2013). Nutrient composition, anti-nutri-tional factors and known toxins of grain and/or forage samples come from the new GM crop grown in the same field sites as its conventional counterpart variety. The analytes are from a crop-specific list provided by OECD, and addi-tional analytes are based on the metabolic path-ways resulting from the transgene (Chassy et al., 2008). Animal nutritionists are very famil-iar with the variability in forage composition, but non-pooled grains from individual fields, or even locations within fields, also have consider-able compositional variability. For instance, ac-cording to the ILSI Crop Composition Database (ILSI, 2016), crude protein from 186 field corn samples collected from conventional samples in

U.S. studies during 2014 had a range of 6.51 to 12.50% DM. This vari-ability is attributable to genetic differences from conventional breeding and environmental factors and not the transgene (Harrigan et al., 2010; Venkatesh et al., 2015). Genetically modified crops with traits that do not intentionally affect composition have been shown through numerous stud-ies to be compositionally equivalent to their conventional comparators (Herman and Price, 2013), allowing animal nutritionists to use standard composition tables, such as in NRC’s publications on nutrient require-ments for diet formulation.

Animal testing of GM cropsThere are three major types of animal testing of GM crops, two are labo-

ratory rodent studies, and the third is livestock studies. Acute oral gavage studies in rodents test purified components (usually the introduced protein) and typically follow OECD guidelines. The tested dosage is often thousands to millions of times the amount that a human or farm animal could possibly consume since the foods from GM crops would contain the protein and there is no route to direct exposure of the protein. It is usually conducted after evidence for the safety of the newly expressed protein already exists. The protein is dosed one time, and clinical signs are observed for 14 d prior to a gross necropsy. This is an appropriate study design since dietary pro-teins are usually digested to amino acids and according to Hammond et al. (2013) “because proteins known to be toxic to mammals and other organ-isms generally work through specific mechanisms to cause adverse acute effects, testing can often be performed using acute toxicity tests.”

The 90-d, sub-chronic toxicity study involves rodents fed either grain or meal from GM crops at the highest reasonable amount while maintaining a balanced diet. A review of nearly 20 yr of whole-food toxicology studies with numerous GM crops concluded that these studies did not add to the in-formation from agronomic and compositional analyses to demonstrate toxi-cological concern or otherwise question the weight of evidence for the GM crops when compared with their conventional counterpart (Bartholomaeus et al., 2013). Moreover, Bartholomaeus et al. (2013) stated that this conclu-sion is consistent with the results from a 10-yr program of > 500 research groups and costing the European Commission > €300 million that concluded

Figure 1. Components for assessing the safety of GM crops. Reprinted with permission from Konig et al. (2004).

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in 2010 that “…biotechnology, and in par-ticular GMOs, are not per se more risky than conventional plant breeding technologies.”

The third type of animal testing is feed-ing whole feeds to target poultry or livestock. For the first GM soybean approval, a series of studies of this kind were conducted that included individual experiments with broiler chickens, catfish, and dairy cattle (Ham-mond et al., 1996) that were not conducted as required studies, but instead were done to answer concerns from animal producers who wanted to know if the nutrition and feed efficiencies would be altered. For most animal production operations, feed costs are their greatest expense, and even a small dif-ference in productivity, either due to nutrient availability, effects on voluntary feed intake, or as a result of health maladies, would have a major influence on profitability. Billions of broilers are grown globally each year, and even a small change in the ration cost per bird would be a significant economic impact. Hundreds of in vivo studies have been done, and they have been the subject of several re-views (Snell et al., 2012; Flachowsky, 2013; Ricroch, 2013; Ricroch et al., 2013). In gen-eral, these studies demonstrate that animal productivity is unaffected by feeding GM crops. Van Eenennaam and Young (2014) used a different approach by examining re-cords from public databases for more than a 100-billion animals in the U.S., and per-formance of broilers, swine, beef cattle and dairy cows apparently have been unaffected by the widespread adoption of GM crops.

Future of biotech cropsSeveral recent statements from well-

respected scientific organizations may prove to be persuasive to public acceptance of GM crops. Not only has the recent report of the National Academies of Science found that there were no health concerns from the pro-cess of genetic modification, but a letter was issued by 110 Nobel Laureates to criticize Greenpeace’s stance on GMOs. They “urge Greenpeace and its supporters to re-examine the experience of farmers and consumers worldwide with crops and foods improved through biotechnology, recognize the find-ings of authoritative scientific bodies and regulatory agencies, and abandon their cam-paign against “GMOs” in general and Gold-en Rice in particular.” Products that are cur-rently in the process of obtaining regulatory

Genetically modified crops in the 20+ years since their commercialization have predominantly benefited farmers and the environment. Although transgenes have not been introduced to directly improve yields, there have been yield gains that were realized due to effective control of weeds, insects, and, most recently, drought stress. Society at large benefits from yield gains attributable to GM crops because harvesting more crops per hectare creates the potential to use less cropland and increase habitat for biodiversity and wildlife without impacting food security. In 2014, without the crop gains due to GM, 20.7 million hectare of additional land would have been needed (Brookes and Barfoot, 2016b), which is equivalent to all of the farmland in Iowa and Missouri. Likewise, for 2014, there have been reductions in greenhouse gas emissions (equivalent to 10 million cars for 1 yr) and pesticide use (Brookes and Barfoot, 2016a). A meta-analysis by Klumper and Qaim (2014) also concluded that GM crops have reduced chemical pesticide use by 37%, increased crop yields by 22%, and increased farmer profits by 68%. Their data also demonstrated that yield and profit gains were actually greater for developing countries than developed countries.

Recently, the National Academies of Science conducted a comprehensive review of GM crops and concluded that there was no evidence of a risk to human health from GM crops compared with conventional crops (NAS, 2016). In spite of this relevant conclusion, for many critics and consumers, scientific findings are unconvincing in light of alternative preferences and biases. One member of Greenpeace, Mark Lynas, admits to destroying GM crop field trials in the EU and now publicly states that GM crops have science-based safety assessments. A former leader of Green-peace International, Gerd Leipold, said in a BBC interview, “We as a pressure group have to emo-tionalize issues. We are not ashamed of emotionalizing issues” (Adler, 2016). Part of the blame might be due to companies that did not see the coming impact of social media and the internet and therefore failed to communicate with consumers (Ryan, 2014). One internet rumor was that cattle preferentially ate from stover fields that had been planted previously with conventional compared with GM Bt corn. Feed intake differences had never been seen in test/control studies, so some theorized that cows taste a difference or somehow sensed it was toxic. Investigation revealed the simple answer that the conventional fields had more insect damage, resulting in weak stalks and more kernels on the ground. Unfortunately, many consumers are not able to discern accurate from faulty studies, and many controversial studies now end up in predatory journals or other journals that do not have an adequate peer review (Ryan and Vicini, 2016). One example for animals is a swine paper published in a journal (Carman et al., 2013) with editors that don’t list backgrounds in animal or veterinary sciences. The design and analysis of the study had several flaws that would have been caught if reviewed by experts in animal health and pathology. To magnify this issue, articles in predatory journals end up as references in research papers, meta-analyses, and review papers with the appearance of having been peer reviewed.

Until recently in the U.S., food items containing GMOs have not had a mandatory requirement for food labeling; however, states legislatures or statewide ballot initiatives were being consid-ered to force mandatory labeling. Voluntary labeling has always been available but some voters saw this as unnecessary and costly while others saw it as hiding something. Due to the confusion that could be created with state by state labeling regulations, the federal government passed a mandatory labeling bill. The bill made it clear that this legislation is about marketing and not food safety. Recently, a yogurt processor asked dairy farmers to eliminate feeding crops derived from GM crops to produce milk for their yogurt. This not only puts these farmers at an economic disadvantage, but it is purely a marketing scheme since feeding GM crops to animals does not change meat, milk, and eggs. Many studies have been conducted that fail to detect the DNA and/or protein from GM crops in animal products (Phipps et al., 2006; Chassy et al., 2008; Rizzi et al., 2012). Therefore, food companies currently cannot test animal products to determine if animals were fed feeds derived from GM crops such that claims that they can are highly questionable.

Controversies

Benefits

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approvals are a departure from the pattern of the typical GM products currently in the market-place. These include technologies such as a RNAi-based products to protect plants from corn rootworm damage, reduce lignin in alfal-fa, or increase oleic acid in low-linolenic soybean while reducing saturated fats (Table 1).

Gene editing is a technology that uses specific nucleases to make targeted changes to the genome and products using this technology could enter the market-place in the near future, and regulators are evaluating what information/studies they will want to see. The tools used are CRISPR, TALEN, and zinc-finger nucleases, and they make it possible for scientists to enhance (edit) beneficial traits or remove undesired characteristics as well as allow for the site-directed inte-gration of specific genes. One interesting product from gene editing is being developed by Recombinetics, Inc. (St. Paul, MN) to edit the genome of cattle to a natural mutation that results in polled cattle. Previous at-tempts to breed for this have reduced milk production, but this technique may uncouple those phenotypes. Therefore, using gene editing to replace the current practice of dehorning dairy cows could provide the opportu-nity to bring together groups that currently oppose the concept of “big ag” biotechnology since this has clear welfare benefits over current practices; however, recently the National Organic Standards Board recommended against allowing gene editing, suggesting that milk from these humanely hornless animals will not be considered organic. Hopefully some critics of animal agriculture that are opposed to the current methods of dehorn-ing cattle may find this technology acceptable (McGowan, 2015). This illustrates that, when a product is safe, benefits might be more important than the process and that other intangibles such as corporate ownership and perception of food security (Herring and Paarlberg, 2016) may affect resistance to new technologies as the planet heads closer to 10 billion people.

Conclusion

Genetically modified crops have been widely adopted by growers be-cause they benefit from the introduced traits that help protect plants from insect damage, allow no-till methods of weed control, and other means to maximize yield on minimal acreage. In spite of the fact that every major global regulatory group has approved the safety of the crops they have re-viewed, there continues to be some concerns. Consumers often deal with confusing information that does not explain the benefits of biotechnology; therefore, GM seed providers and agricultural scientists need to be able to provide accurate information to make science-based decisions and to understand their benefits to reducing the impact of agriculture on use of land and other resources.

ACknOwLedGMenTS

The author is grateful to Ray Dobert, Kevin Glenn, Aimee Hood, Tracey Reynolds, and Eric Sachs for their constructive comments about the paper.

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About the AuthorJohn Vicini received a Ph.D. from the University of Illinois in 1986. Since then, he has worked at the Monsanto Company where he has conducted numerous studies assessing safety of Monsanto’s products, including bST and genetically modified crops. Throughout his scientific career, he has worked with teams that have devel-oped products for improving productivity of farms to enhance animal and human nutrition. He is a member of the American Society of Animal Science, the American Dairy Science Association, and is on the

Board of Representatives for the Council for Agricultural Science and Tech-nology (CAST). Apart from research papers, he has also written articles on predatory publishing and use of natural language processing in biology. Vicini is a Senior Editor for the Journal of Dairy Science, and in his spare time, enjoys fishing in the arctic. Correspondence: john.l.vicini@monsanto.com.

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