Environmental Safety of Genetically Engineered Crops [1 ed.] 9781609172275, 9781611860085

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Copyright © 2011. Michigan State University Press. All rights reserved. Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

E n v i ro n m e n ta l S a f e t y o f

Copyright © 2011. Michigan State University Press. All rights reserved.

G e n e t i c a l l y E n g i n ee r e d C r o p s

Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

Copyright © 2011. Michigan State University Press. All rights reserved. Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

E n v i ro n m e n ta l Safety of G e n e t i c a l ly E n g i n ee r e d Crops

Copyright © 2011. Michigan State University Press. All rights reserved.

Edited by Rebecca Grumet, James F. Hancock, Karim M. Maredia, and Cholani Weebadde

Michigan State University Press East Lansing

Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

Copyright © 2011 by Michigan State University i The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-­1992 (R 1997) (Permanence of Paper). Michigan State University Press East Lansing, Michigan 48823-­5245 Printed and bound in the United States of America. 17  16  15  14  13  12  11   1  2  3  4  5  6  7  8  9  10 library of congress cataloging-­in-­publication data Environmental safety of genetically engineered crops / edited by Rebecca Grumet . . . [et al]. p. cm. Includes bibliographical references and index. ISBN 978-­1-­61186-­008-­5 (cloth : alk. paper) 1. Crops—­Genetic engineering—­Environmental aspects. 2. Crops—­Genetic engineering—­Safety measures. 3. Crops—­Genetic engineering—­Government policy. I. Grumet, Rebecca. SB123.57.E68 2010 631.5'233—­dc22

2010052158

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This book is dedicated to the Father of Green Revolution, Dr. Norman E. Borlaug (1914–­2 009), a visionary scientist and inspirational leader who dedicated his life to the development and use of new science and technology for the benefit of farmers and consumers around the world.

Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

Copyright © 2011. Michigan State University Press. All rights reserved. Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

Contents Foreword by M. S. Swaminathan

ix

Preface

xi

Part 1. Introduction to Environmental Biosafety in Relation to Genetically Engineered Crops

Production of Genetically Engineered Crops, Relationship to Conventional Plant Breeding, and Implications for Safety Assessment Rebecca Grumet

3

Environmental Issues Associated with Agricultural Production Systems Kurt D. Thelen

15

Environmental Biosafety Issues Associated with Genetically Engineered Crops Cholani Weebadde and Karim M. Maredia

21

Current Status of Genetically Engineered Crops and Assessment of Environmental Impacts

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Hector Quemada

31

Future Possible Genetically Engineered Crops and Traits and Their Potential Environmental Impacts Rebecca Grumet, LaReesa Wolfenbarger, and Alejandra Ferenczi

47

Part 2. Environmental Considerations Associated with Genetically Engineered Crops

Factors Influencing the Genetic Diversity of Plant Species and the Potential Impact of Transgene Movement James F. Hancock

61

Control and Monitoring of Gene Flow from Genetically Engineered Crops James F. Hancock and Mark Halsey

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75

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viii    Contents Evaluation of Potential Impacts of Genetically Engineered Plant-­Incorporated Protectants on Non-Target Organisms Robyn Rose

87

Pests Resistant to Pesticides and Genetically Modified Crop Plants: Theory and Management Christina DiFonzo, Edward Grafius, David E. Hillger, Chad D. Lee, and James J. Kells

105

A Problem-­Based Approach to Environmental Risk Assessment of Genetically Engineered Crops James F. Hancock and Hector Quemada

123

Part 3. Regulation of Genetically Engineered Crops with Respect to Environmental Safety

The Cartagena Protocol on Biosafety and Other International Regulations Fee Chon Low and Robert J. Frederick

131

Systems to Regulate Genetically Engineered Plants: Similarities and Differences among Countries Karen Hokanson and Alejandra Ferenczi

147

Bio-­Innovations and the Economics of Biosafety Regulatory Decision Making and Design in Developing Countries José Falck-­Zepeda and Patricia Zambrano

157

Part 4. Future Challenges and Opportunities

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Risk-­Benefit Communication for Transgenic Crops Muffy Koch and Adrianne Massey

175

Capacity Building in Biosafety Karim M. Maredia, Cholani Weebadde, John Komen, and Kakoli Ghosh

189

The Evolving International Regulatory Regime: Impact on Agricultural Development John Komen and Silvia Salazar

209

Contributors

225

Index

231

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Foreword

Copyright © 2011. Michigan State University Press. All rights reserved.

M. S. Swaminathan

Genetically engineered crops provide uncommon opportunities to breed varieties that possess novel genetic combinations capable of conferring tolerance to a wide range of biotic and abiotic stresses. With the onset of the era of climate change, we will need genetic material capable of withstanding unfavorable alterations in temperature, precipitation, and sea level. Biodiversity is the feedstock for a climate-­resilient farming system. Biodiversity is also the feedstock for the biotechnology industry. While the benefits of genetic engineering are clear, the potential risks have created public concern about the wisdom of releasing and consuming genetically modified crops. Therefore, there is need for a system of benefit-­risk analysis that inspires confidence among professions, politicians, the public, and the media. Among the risks to be assessed, environmental biosafety occupies an important place. Damage to the environment will have multiple effects on the health and well-­being of both human and animal inhabitants of an area. The present book is therefore a timely contribution. It deals with environmental biosafety in a comprehensive manner, ranging from the impact of genetic engineering on agricultural production systems to problems arising from gene flow from genetically engineered crops. The impact of herbicide-­resistant varieties on soil microflora and microfauna will have to be studied over time. Longitudinal studies are also needed to reliably assess environmental risks. The book contains chapters on scientific aspects of biosafety as well as the economics of biosafety regulatory decision-­making, and capacity building in biosafety procedures and evaluation. The evolving international regulatory regime is also described in detail. Genetic engineering techniques can help humankind to face the new challenges arising from population growth, biodiversity loss, and climate change. Therefore, every country should equip itself with the capacity to assess and manage environmental risks. This book will be of invaluable help in this task. We owe the authors deep gratitude for their comprehensive and authoritative treatment of a difficult and often emotionally charged subject. All biotechnology regulatory authorities should derive benefit from this publication.

ix

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Copyright © 2011. Michigan State University Press. All rights reserved. Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

Copyright © 2011. Michigan State University Press. All rights reserved.

Preface Humans have an enormous capacity to alter the environment around them, a fact that has become increasingly evident in recent years. With that capacity comes responsibility, and often conflicting imperatives. How do we achieve the right balance between food security, human health, nutrition, sanitation, quality of life, and environmental sustainability? To what extent can new technologies help us achieve that balance, or drive us to further, and perhaps irreparable, long-­term environmental degradation? Agriculture is one of the human activities that causes the greatest environmental impact, first and foremost through the diversion of land from natural ecosystems to food production, whether through subsistence small-­scale farming in the developing world, or large-­scale commercial production in industrialized countries. But it is agriculture that provides fundamental needs for food, fiber, and shelter, and that frees humans to achieve in other endeavors. Furthermore, without high-­yielding agriculture, despite its attendant effects on water use, soil salinization, pesticide use, and soil erosion, it would be necessary to bring additional, often agriculturally marginal, land into cultivation, thus causing even more destruction of native ecosystems. Where do biotechnology and the development of genetically engineered (GE) crops fit into this tug of priorities? Proponents argue that by producing higher yields and reduced losses to pests, such crops decrease the environmental burden of agricultural production, especially if less new land is brought into cultivation, pesticide use is reduced, and more favorable farming practices can be employed to reduce soil erosion. Opponents argue that GE crops may cause unforeseen long-­term environmental consequences and perpetuate the disruption caused by conventional farming practices. How do we balance these opposing views? In these deliberations are complex roles for science, technology, economics, and ethics that ultimately drive governmental policy and individual farmers’ choices. While science cannot stand alone in determining appropriate policies and decisions about use of new technologies, discussions of policy must be rooted in accurate information. This is especially important with respect to questions of biosafety. As a starting point in assessing validity, we can ask, Is there scientific consensus at the highest levels of available expertise? How far does the consensus extend? Where is there divergence of opinion, and what are the gaps in our knowledge? More than one hundred U.S., European, and international scientific societies from around the world have addressed the relative safety of genetically engineered and conventionally bred crops. All have reached the conclusion that properly regulated genetic engineering of crop plants does not pose new risks to human health or the environment relative to conventional plant breeding. GE crops are not inherently dangerous. This conclusion is cogently summarized by the 2005 report of the International Council for Science (ICSU—­http.iscu.org), headquartered in Paris, and representing 111 national academies of science and 29 scientific xi

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xii    Preface

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unions. The ICSU’s report was based on 50 independent scientific enquiries carried out by different groups in different parts of the world to investigate the food and environmental safety of GE crops. With respect to food safety, the conclusion was that “currently available genetically modified foods are safe to eat. This view is shared by several intergovernmental agencies, including the FAO/WHO Codex Alimentarius Commission on Food Safety, which has 162 member countries.” However, the report also states that “although currently available GM foods are considered safe to eat, this does not guarantee that no risks will be encountered as more foods are developed with novel characteristics. Ongoing evaluation of emerging agricultural products is required to ensure that new foods coming to market are safe for consumers. Food safety evaluation must be undertaken on a case-­by-case basis.” With respect to environmental safety, the appropriateness of specific technologies depends on the current agricultural system and practices, and the surrounding natural environment. The ICSU report concluded: “The effect of genetic technologies may be either positive or negative. They may either accelerate the environmentally damaging effects of agriculture, or they may contribute to more sustainable agricultural practices and the conservation of natural resources. It is a matter of application and choice.” Thus, it is not GE technologies per se, but, like virtually any technology, the manner in which they are employed that can be safe or unsafe. Scientific assessments must be coupled with the governmental and institutional frameworks and capacity to interpret and make nationally and locally appropriate choices of technologies. It is from this perspective—­that the safety of genetically engineered crops is a matter of application and choice—­that this book is written. We describe the basis for the development and use of genetically engineered crops and examine the possible impacts that such technologies may have on the environment. To make these determinations, specific genes and traits must be evaluated within the context of the environment into which they will be introduced, the manner in which they will be used, and the current agricultural system and attendant environmental impacts of the technology. Our intent is to provide the reader with a framework by which to address these issues within the context of the varying geographies and circumstances in which the adoption of GE crop technology is being considered.

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Part 1

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Introduction to Environmental Biosafety in Relation to Genetically Engineered Crops

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Production of Genetically Engineered Crops, Relationship to Conventional Plant Breeding, and Implications for Safety Assessment

Copyright © 2011. Michigan State University Press. All rights reserved.

Rebecca Grumet

Genetically engineered (GE) crops are developed using a combination of genetic engineering (recombinant DNA technologies) and conventional plant breeding methods. The novelty of techniques employed in introducing new genes and traits into these crops through genetic engineering has prompted extensive debate, and has led to the establishment of regulations at national and international levels to ensure safe deployment. As a starting point for discussions of environmental safety in subsequent chapters, this chapter will provide an introduction to GE crops and their relationship to crops produced by conventional techniques. Genetic engineering, by definition, involves genes. All living organisms (plants, animals, microbes) have genes. Genes, which are located on chromosomes, encode the hereditary information that is passed from one generation to the next, and in encoded form, provide all the instructions that are needed to produce a functional organism. The genes in a plant provide the information that enables plant cells to produce the machinery needed to take carbon dioxide from the air, absorb water and nutrients from the soil, and convert them into leaves, roots, flowers, and seeds. They also provide mechanisms that enable plants to respond to their environment in various ways, such as perceiving and growing toward light, preparing for cold weather, and producing defensive compounds against pathogens and insects. The information provided by genes is in the form of instructions for producing proteins, not the least of which are all of the enzymes necessary to perform all of the biochemical reactions in a cell. Plant cells are essentially biochemical factories that perform photosynthesis (the ultimate source of all energy in the food chain) and produce the fantastic array of compounds (sugars, starches, cellulose, proteins, oils, vitamins, flavors, fragrances, pigments, medicinal compounds) that allow plants to be sources of foods, fibers, building materials, fuels, medicines, and aesthetic beauty. A trait can result from the protein itself, but more often is the result of the products of enzymatic reactions. The coding capacity of genes is derived from their molecular structure. Genes are made of DNA, a helical molecule composed of strings of four types of nucleotides, A (adenine), T (thymine), G (guanine), and C (cytosine). The order of the nucleotides specifies the sequence of amino acids that is specific to each kind of protein. Given the range of activities, 3

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4    Rebecca Grumet

it is not surprising that the genome (total collection of genes) of a typical plant comprises 20,000–­40,000 genes (Chrispeels and Sadava 2003). It has been analogized that if all of the information contained in the genes of a rice plant (estimated 37,500 genes) were to be written out as ATGCs, it would fill 40 books, each with 1,000 pages (Lemaux 2006). Any typical gene would take up less than one page. Importantly, the language of DNA (the ability to encode the amino acid sequence of proteins) is the same regardless of the type of organism it came from. This is a critical factor underlying genetic engineering techniques, which makes it possible to move genes from one organism to another. Genetic engineering depends on two types of technologies primarily developed in the 1970s and 1980s, recombinant DNA technology and transformation technologies. Recombinant DNA technology refers to a collection of techniques used to take genes from different places and put them together in new combinations (i.e., recombinant). Transformation refers to moving the recombined gene into a new organism. The resultant organism is referred to as transformed, genetically modified, genetically engineered, or transgenic.

Production of a Genetically Engineered Crop

The process of producing a GE crop can be broadly divided into five general steps: obtain and engineer the desired gene (recombinant DNA technology); introduce the gene into individual cells/chromosomes (transformation); regenerate the transformed cell into a whole plant (tissue culture technology); verify the presence and expression of the introduced gene and desired new trait (lab, greenhouse, and field studies); and incorporate the new trait into a high-­performing variety (conventional breeding) (figure 1). Each of these steps will be discussed briefly to give a general overview of the process. More complete descriptions of the relevant technologies can be found in several texts and reviews, such as Chrispeels and Sadava (2003); Sharma et al. (2005); Thomson (2006); Watson et al. (1992).

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Step 1: Obtain the Gene of Interest and Engineer into a Form for Expression in the New Plant The length of time and sophistication of technologies needed to obtain the gene of interest varies widely, depending on the state of background knowledge. If the gene of interest is closely related to one that has already been cloned from another organism, or if the protein the gene codes for has already been isolated and characterized, obtaining the gene can be relatively easy, and relies primarily on standard recombinant DNA techniques. These include cloning (making copies of the gene of interest so it can be worked with in the laboratory), and cutting and pasting to precisely assemble the intended pieces of DNA (Watson et al. 1992). If the gene has never been cloned before, and little or nothing is known about the protein it encodes, initial cloning can be more difficult, and may require more sophisticated genomic technologies developed in the last two decades that can examine thousands of genes at the same time. Desirable genes about which little is known might include a gene coding for resistance to a specific disease, or one coding for enzymes to produce an herbal medicinal compound. Once the gene of interest is in hand, modifications may be needed to engineer the gene

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Figure 1. Steps to Produce a GE Crop: (1) obtain and engineer the desired gene (recombinant DNA technology); (2) introduce the gene into individual cells/chromosomes (transformation); (3) regenerate the transformed cell into a whole plant (tissue culture technology); (4) verify the presence and expression of the introduced gene and desired new trait (lab, greenhouse and field studies); (5) and incorporate the new trait into a high performing variety (conventional breeding).

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into a form for expression in the new plant. Generally the most important modification is adding an appropriate promoter, a piece of that tells the cell when, where, and how much of the gene should be expressed. or example, certain genes may need to be expressed everywhere, others only in the seeds, others only in response to drought.

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Step 2: ransfer the Engineered Gene into Cells of the Desired Plant

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ntroducing the gene into cells (and ultimately chromosomes) of the desired plant requires transformation technology. he two most widely used methods are Agrobacterium-mediated transformation and particle bombardment ( hrispeels and Sadava 2003; Sharma et al. 2005). T

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Production, Breeding, and Safety

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6    Rebecca Grumet

Agrobacterium-­mediated transformation uses a naturally occurring soil bacterium that, as part of its normal infection process, transfers a few of its own genes into a chromosome of the host plant cell—­it is a natural genetic engineer. Through recombinant DNA techniques, it is possible to remove the genes that the bacterium would normally transfer and substitute genes of interest for crop improvement. Agrobacterium-­mediated transformation is the preferred method because of its relative efficiency and specificity. However, it does not work well for all species. The second method, particle bombardment, uses tiny particles of tungsten or gold that are coated with the desired DNA.  The particles are then accelerated to speeds that allow them to penetrate the cells. In some cases, some of the DNA becomes incorporated into the chromosome, allowing it to be passed on through cell divisions and inherited by subsequent generations. Although less efficient, a primary advantage of this method is it can be used for any species. Step 3: Regenerate Cells with the New Gene into the Whole Plant

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In the first stage of transformation, the gene of interest becomes incorporated into a single cell. It is then necessary to culture the cell to become a whole plant. This process, called regeneration, is accomplished by placing the treated plant tissue onto a culture medium that allows the cells to divide and differentiate to form plant parts. The necessary media conditions must be developed for each species of interest. The regenerated plant is ultimately transferred to soil and used to produce progeny. Tissue culture techniques are also used for a variety of other purposes, such as propagating species that are not typically grown from seeds (i.e., clonally propagated species), or to produce disease-­free sources of planting materials (Lindsey and Jones 1990). In any transformation process, only a tiny fraction of a percent of the treated cells acquire the gene of interest. One of the challenges is to be able to separate the few transformed cells from the thousands of nontransformed cells. This is most often accomplished by introducing two genes, the desired gene (e.g., for insect resistance), and a second gene that serves as a marker to find the transformed cells (selectable marker gene) (Sharma et al. 2005). The selectable marker allows the transformed cells to grow in conditions that inhibit nontransformed cells, such as in the presence of antibiotic or herbicide resistance. In this way, only the cells that have become transformed are able to grow and divide and ultimately regenerate. Step 4: Verify Incorporation and Expression of the Gene and Performance of the New Trait The first step after regenerating a putatively transgenic plant is to verify presence and expression of the gene. Presence of the gene is determined using DNA detection techniques such as PCR or Southern analysis. Stable inheritance is verified by transfer to subsequent generations. Expression of the gene can be verified by testing for transcription to RNA or production of the desired protein. Once it is determined that the gene is present, stably inherited, and properly expressed, the plants can be tested for expression of the desired trait, (e.g., virus resistance, salt stress resistance) in greenhouse and confined field trials. At this stage, if the desired trait has been obtained, proof of concept has been established, demonstrating that the introduced gene can be potentially useful.

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Production, Breeding, and Safety    7

Step 5: Incorporate the Gene into High-­Performing Cultivars by Conventional Breeding For many, if not most crops, the plant varieties that perform well in tissue culture for transformation and regeneration are not the best varieties for performance and productivity in the field. Furthermore, even if a high-­performing cultivar can be successfully transformed, no one variety can be used everywhere. Varieties must be bred for the specific conditions in which they will be grown with respect to temperatures, availability of water, length of growing season, day length, prevalent diseases, and so forth. As an example, seed company catalogs offer hundreds of “Roundup Ready” (glyphosate resistant) soybean varieties for sale in the United States. For genes/traits being introduced into new locations, the gene will need to be transferred into locally adapted varieties. Varieties also vary depending on the use of the crop, for example, fresh market versus processing, food versus feed, specific processing characteristics (e.g., oil or starch qualities), again necessitating incorporation of the gene of interest into the types appropriate for the intended use. Controlled crosses (pollinations) are made between plants of the genetically engineered variety and the desired recipient variety, and backcrossed as needed to obtain the appropriate combination of traits. The resultant progeny are tested in small-­plot field trials to verify performance. The most promising lines are moved to more extensive multiyear, multilocation trials to be sure the crop and the new trait perform well over a range of conditions that may be encountered by the new variety.

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Comparison of Genetic Engineering and Conventional Plant Breeding Methods

When considering the biosafety of genetically engineered crops, it is important to be familiar with methods used for the alternative option, conventionally bred crops. Plant breeding began with the domestication of crops for agriculture. People have been genetically modifying plants as long as they have cultivated crops. For example, excavation of archaeological sites in Peru found beans associated with the remains of city dwellings dated 7,000–­10,000 years ago exhibiting features of domestication including markedly increased size relative to wild beans in the area, thin seed coats, and loss of the inner fibrous pod layer which in the wild expels beans from the pod (Kaplan et al. 1973). These modifications demonstrate that prehistoric plant breeders were able to make impressive gains in productivity and agricultural and culinary quality. Selection The primary tool available to the earliest plant breeders was selection, that is, choosing the best types for further propagation. Selection can occur both intentionally and inadvertently. Examples of intentional selection include selection for increased size, better flavor, or ease of cooking. Inadvertent selection plays a predominant role in local adaptation. Humans move crops from one location to another. In this process, the environmental conditions change, and

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thus the selection pressures change. or example, wheat, which originated in the ear East, became widely planted throughout the iddle East and Europe. ven time, exposure to different growing conditions (e.g., hot, dry climates in Egypt vs. short, cool growing seasons in England) leads to differential local adaptations. Selection can have dramatic effects. prime example can be seen in the cabbage family (figure 2). abbage, Brussels sprouts, broccoli, and cauliflower are members of the same species (Brassica oleracea), but have strikingly different morphologies. Broccoli and cauliflower were selected for mutations that cause delay of flower development; cabbage and Brussels sprouts were selected for mutations that inhibit stem growth between adjacent leaves on the main stem (cabbage) or lateral stems (Brussels sprouts). here are, however, limitations to what selection can do. t is not possible to select for a trait that does not already exist in the population. his can be a problem if an important trait, for example, disease resistance, does not occur in the population. isease resistance and insect resistance, for which there is often not a source within the cultivated crop, are primary challenges to plant breeders today.

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f a desired trait does not occur within the population, the plant breeder must look elsewhere to obtain the necessary genes. ncorporating a new trait can be done by hybridization— crossing with a plant with a different one that possesses the desired trait. typical example is crossing a cultivated variety with a wild relative that provides disease or insect resistance. he process of hybridization typically introduces many traits in addition to the specific target trait. or example, crossing with a wild relative can bring along undesirable characteristics such as low yield, small seeds or fruits, bitter or tart taste, or inferior growth habit. he original cross is generally followed by 5–10 generations of backcrosses to the cultivated parent to obtain a desirable crop type that has acquired the new desired trait (e.g., disease resistance). I

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Hybridization

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Figure 2. Cabbage, Brussels sprouts, broccoli, and cauliflower all members of the same species (Brassica oleracea), but have strikingly different morphologies. Each was selected during crop domestication for specific traits of interest.

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Production, Breeding, and Safety    9

Hybridization was well established by the 1700s and became formalized in the 1900s (Simmonds 1979). Selection plus hybridization formed the basis for modern plant breeding in the twentieth century and contributed to tremendous gains in crop productivity (Chrispeels and Sadava 2003). These methods are still being effectively used in plant breeding programs throughout the world. Like selection, however, there are limits to what they can achieve. Hybridization is limited to the crop species or other relatives that are sufficiently closely related to produce viable offspring (i.e., a tomato plant cannot be crossed with a corn plant). Recombinant DNA and Transformation Technologies The newest tools available to plant breeders are recombinant DNA and transformation technologies as described above. Because the language of DNA is the same regardless of organism, these tools allow the introduction of genes from any species. The breeder is no longer limited to species that are interfertile with the crop of interest. For example, researchers at the University of Wisconsin recently cloned a gene for resistance to late blight of potato from a wild species of potato that is sexually incompatible with the cultivated potato (Song et al. 2003). Late blight was the cause of the potato famine in Ireland in the 1800s and remains a major problem today. Sources of resistance available within compatible species have been of limited use, preventing development of highly resistant varieties and necessitating intensive application of fungicides. Introducing the cloned gene into cultivated potatoes could increase production and reduce pesticide use. In general, genetic engineering can be undertaken for the same reasons as conventional breeding, such as increased yields, reduced losses to pests, better adaptation to challenging environments, or improved product quality. It is also possible to introduce genes to produce new types of products, such as soybeans with new types of oils that are healthier, or have specific lubricant properties.

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Comparison of Potential Risks of Genetic Engineering and Conventional Plant Breeding

Genetic engineering can be compared to conventional plant breeding with respect to several criteria that are relevant to risk assessment: the source of genes, the extent of genetic change, and the extent of characterization of the introduced genetic material. Source of Genes As discussed earlier, the source of genes available for conventional breeding is limited to the species of interest and closely related, interfertile relatives. This in turn restricts the kinds of genes available. In contrast, with recombinant DNA technologies, the genes can come from anywhere: plants, animals, bacteria, fungi, viruses. This led scientists who were involved in the early development of molecular genetic techniques to raise questions about the safety of the technology, and as a group decide that regulatory procedures should be put in place to ensure that care was taken to prevent introduction of potentially dangerous genes (Berg et al. 1975). The process was formally initiated at a conference in Asilomar, California, in 1975

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10    Rebecca Grumet

and led to the development of safety guidelines instituted by the U.S. National Institutes of Health (NIH) to regulate recombinant DNA (rDNA) technology research. Institutions performing such research must have an institutional biosafety committee that reviews all rDNA experiments. If experiments are ready to reach the field for confined field trials, they must also receive approval from federal and state departments of agriculture. Products that a company wishes to commercialize in the United States next go through regulatory processes including United States Department of Agriculture (USDA) approval for agriculture and agroecosystem-­related concerns, Food and Drug Administration (FDA) approval for food safety, and Environmental Protection Agency (EPA) approval with respect to pesticidal or toxic traits and residues (FDA 1992; EPA 2010a; 2010b). The FDA maintains a list of completed consultations of genetically engineered foods (FDA 2010). Although consultation is voluntary on the part of developers, the legal requirements to ensure food safety are not (Bren 2003). Information on crops that have been granted “non-­regulated status” permission for open field production from the USDA can be obtained through the Animal Plant Health Inspection Service (APHIS 2007). The regulatory process typically costs several million U.S. dollars for a given crop with a given new gene (Falck-­Zepeda and Zambrano, this volume). Labeling laws vary by country. In the United States, labeling is based on the food product and not the process by which it is produced; that is, the FDA only requires labeling if the food product is substantially different from its non-­genetically engineered counterparts (FDA 1992). Key considerations include nutritional content, toxicity and allergenicity. If any of these factors is changed relative to the standard levels observed in that crop, the law requires that the GE food be labeled. No GE crop currently on the market has been altered with respect to these characteristics.

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Amount of Genetic Change When conventional crosses are made, there can be a large number of genetic changes, depending on the phenotypes and genetic distances between the two parents that are crossed. For example, resistance to the fungal disease Fusarium yellows was introduced into celery by conventional breeding by crossing with celeriac (Quiros et al. 1993). Celery is grown for its large fleshy petioles, celeriac for it bulbous root. The two crops look very different, and the resultant first-­generation hybrid had thin, brittle, stringy, and bitter petioles. Thus, in addition to the introduction of disease resistance, many other traits, including undesirable ones, were introduced by the hybridization process. Not only is it possible to introduce undesirable traits, it is possible to introduce dangerous traits. Many plants and their wild relatives are capable of producing highly toxic compounds. For example, members of the potato family, including the above-­ground parts of potato that we do not eat, produce poisonous glycoalkaloids (Valkonen et al. 1996). Many of the wild relatives of potato that are used as breeding sources for disease and insect resistance also produce toxic levels of glycoalkaloids in the tubers (the below-­ground portion that we eat). As a result, determination of glycoalkaloid composition is an important criterion for assessing new potato cultivars prior to release for production. Thus, it is evident that potential safety concerns are not unique to genetic engineering. In contrast to the amount of change that can occur with conventional breeding, with current genetic engineering technologies we can introduce only a very few genes. The potential for unintended effects is thus limited to the small number of genes introduced and the traits

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Production, Breeding, and Safety    11

those genes affect. How many traits are affected will depend on the nature of the genes that are introduced. Recent studies have compared conventional and genetically engineered crops for the extent of change that occurred as measured by changes in gene expression (mRNA) or protein production (Baudo et al. 2006; Lehesranta et al. 2005). As might be expected based on the numbers of genes involved, the genetically engineered crops showed fewer changes than the conventionally bred crops. It should be noted, though, that the extent of change can also vary with the type of gene introduced.

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Extent of Characterization of the Introduced Genetic Changes When a trait such as disease resistance is introduced by conventional plant breeding, we know that the gene comes from a closely related relative and confers disease resistance. We do not know what the gene codes for or does. Does disease resistance occur because the cells make stronger cell walls that the pathogen cannot penetrate as easily? Do the cells make enzymes that can detoxify a toxin produced by the pathogen? Does the plant make a compound that is toxic to the pathogen (and possibly also to other nontarget species as well, e.g., glycoalkaloids)? Does the plant recognize the pathogen and signal for production of defense compounds? Any of these kinds of resistances, and more, are possible; all involve very different types of genes, traits, and possible secondary effects. By contrast, when a gene is introduced by genetic engineering, it has already been isolated, cloned and sequenced. From this information it is possible to determine the kind of protein that is produced. The protein is then studied in the laboratory to analyze function; larger amounts are produced to test for possible toxicity or allergenicity. Thus it is possible to analyze relevant safety concerns associated with expression of the candidate gene. On the other hand, with current genetic engineering technologies, the site of insertion in the chromosome is not directed. Thus it is possible that the gene could become inserted into a place that could alter expression of other genes. For example, it is conceivable that a new gene could insert in a way that induces expression of a native toxin gene (e.g., glycoalkaloid). It should be emphasized, though, that the potential to express a potentially dangerous trait such as a toxin resides within the genetic capacity of the original crop, not the introduced gene. Thus, for genetic engineering, as was the case with conventional plant breeding, it is necessary to know the genetic capacity of the crop in establishing appropriate safety precautions.

Conclusions

A crop is a combination of many thousands of genes that has been refined by humans over the eons. Selection and hybridization, which have been the primary tools available for plant breeding, have led to tremendous advances in productivity, quality, adaptation to the environment, and resistance to diseases and insects. Genetic engineering technologies provide a new set of tools to facilitate crop improvement. Breeding experience and knowledge of the species demonstrate that safety precautions are important for both conventionally bred and genetically engineered crops. More than 100 scientific societies from around the world have addressed the question of relative safety of genetically engineered versus conventionally bed crops (figure 3). U.S.,

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12    Rebecca Grumet

U.S. Society of Toxicology, Sept. 2002, Consensus position statement National Research Council Institute of Medicine, Sept. 2004 National Research Council National Academy of Sciences American Medical Association Institute of Food Technologists American Dietetic Association European and International Statements France: French Academy of Medicine, 2003 Italy: Eighteen scientific associations, October 2004 (including National Academy of Science, Societies for Toxicology, Microbiology, Nutrition, Biochemistry) signed consensus statement on safety of GMO crops Food and Agriculture Organization (FAO) World Health Organization (WHO) International Council for Science, 2005 (111 National Academies of Science and 29 scientific unions) Figure 3. Examples of Safety Evaluations of Genetically Engineered Crops of National and International Scientific and Regulatory Bodies

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European, and international studies, including the report of the International Council for Science (2005), representing 111 national academies of science and 29 scientific unions, concluded that properly regulated genetic engineering of crop plants does not pose new risks relative to conventional plant breeding. Safety decisions must be made on a case-­by-­case basis depending on the crop, gene, and environment. In performing safety evaluations, the key issues that must be considered are the following: • What genes were transferred? • What do they code for? • What traits do they confer? • What crops are they put into? • In what environment will the crops be grown?

These questions will be addressed in subsequent chapters examining environmental safety assessment of transgenic crops.

References Animal and Plant Health Inspection Service (APHIS). U.S.  Food and Drug Administration. 2007. Biotechnology. November 26. http://www.aphhis.usda.gov/biotechnology/.

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Production, Breeding, and Safety    13

Baudo, M. M., R. Lyons, S. Powers, G. M. Pastori, K. F. Edwards, M. J. Holdsworth, and P. R. Shewry. 2006. Transgenesis has less impact on the transcriptome of wheat grain than conventional breeding. Plant Biotechnol. J. 4:369–­380. Berg, P., D. Baltimore, S. Brenner, R. O. Robin, and M. F. Singer. 1975. Summary statement of the Asilomar conference on recombinant DNA molecules. Proc. Natl. Acad. Sci. U.S.A. 72:1981–­1984. Bren, L. 2003. Genetic engineering: The future of foods? FDA Consumer Magazine Nov.–­Dec. http:// www.fda.gov/fdac/features/2003/603_food.html. Chrispeels, M. J., and D. E. Sadava. 2003. Plants, Genes, and Crop Biotechnology. 2nd ed. Sandbury, MA: Jones and Barlett. Environmental Protection Agency (EPA). Office of Science Coordination and Policy Biotechnology Team. 2010a. Biotechnology overview. April 22. http://www.epa.gov/scipoly/biotech/pubs/over view.htm. ———. 2010b. Regulatory framework. April 22. http://www.epa.gov/scipoly/biotech/pubs/frame work.htm. Food and Drug Administration (FDA). 1992. Statement of policy: Foods derived from new plant varieties. Fed. Regist. 57 (104). May 29. ———. 2010. Completed consultations on bioengineered foods. Center for Food Safety and Applied Nutrition, Office of Food Additive Safety. September 30. http://www.accessdata.fda.gov/scripts/ fcn/fcnNavigation.cfm?filter=&sortColumn=%2C39LOE%29%2CC1%2C+D%25@%2C%0A &rpt=bioListing&displayAll=true. Hancock, J. F. 2004. Plant Evolution and the Origin of Crop Species. Englewood Cliffs, NJ: Prentice Hall. Kaplan, L., T. F. Lynch, and C. E. Smith. 1973. Early cultivated beans (Phaseolus vulgaris) from an intermontane Peruvian valley. Science 179:76–­77. Lehesranta, S. J., H. V. Davies, L. V. T. Shepherd, N. Nunan, J. W. McNicol, S. Auriola, K. M. Koistinen, S. Soumalainen, H. I. Kokko, and S. O. Karenlampi. 2005. Comparison of tuber proteomes of potato varieties, landraces, and genetically modified lines. Plant Physiol. 138:1690–­1699. Lemaux, P. G. 2006. Introduction to genetic modification. Agricultural Biotechnology in California Series Pub. 8178. http://anrcataglog.ucdavis.edu. Lindsey, K., and M. G. K. Jones. 1990. Current applications of plant, cell and tissue culture. In Plant Biotechnology in Agriculture. Englewood Cliffs, NJ: Prentice Hall. Pp. 57–­77. Quiros, C. F., V. Dantonio, A. S. Greathead, and R. Brendler. 1993. UC8-­1, UC10-­1, and UC26-­1-­3 celery lines resistant to Fusarium yellows. HortScience 28:351–­352. Sharma, K.  K., P.  Bhatnagar-­Mathur, and T.  A.  Thorpe. 2005. Genetic transformation technology: Status and problems. In Vitro Cell Dev. Biol.–­Plant 41:102–­112. Simmonds, N. W. 1979. Principles of Crop Improvement. New York: Longman. Song, J., J. M. Bradeen, S. K. Naess, J. A. Raasch, S. M. Wielgus, G. T. Haberlach, J. Liu, H. Kuang, S. Austin-­Phillips, C. R. Buell, J. P. Helgeson, and J. Jiang. 2003. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad. Sci U.S.A. 100:9128–­9133. Thomson, J. A. 2006. Seeds for the Future: The Impact of Genetically Modified Crops on the Environment. Ithaca, NY: Cornell University Press. Valkonen, J. P. T., M. Keskitalo, T. Vasara, and L. Pietila. 1996. Potato glycoalkaloids: A burden or a blessing? Crit. Rev. Plant Sci. 15:1–­20. Watson, J.  D., M.  Gilman, J.  Witkowski, and M.  Zoller. 1992. Recombinant DNA. New York: W. H. Freeman.

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Environmental Issues Associated with Agricultural Production Systems Kurt D. Thelen

Agriculture is one of the predominant uses of land worldwide. Approximately 40% of the world’s land area, at least 1.5 billion hectares, is under cultivation, and over two-­thirds of human water use is for agriculture (FAO 2010; Millennium Ecosystem Assessment 2005). Agricultural production systems impart a significant environmental footprint on the surrounding ecosystems. The quality of soil, water, and air is affected by agricultural activities occurring on the surrounding landscape. Many of these activities adversely affect environmental quality, contributing to desertification, soil degradation, deforestation, global warming, and water scarcity (FAO 2010; Millennium Ecosystem Assessment 2005). However, improved agricultural management practices minimize the adverse environmental impacts associated with agricultural production, and in some cases can even improve the quality of soil, water, and air.

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Soil

Degradation of soil has been an issue since the onset of agriculture. Tillage disturbance of soil for seedbed preparation, weed control, and the addition of nutritional amendments is an integral part of agriculture. These practices, though historically essential for food production, have resulted in tremendous soil erosion and loss of soil productivity on a global basis. Lal (2003) estimates that water and wind erosion affect 1,094 and 549 million hectares annually, leading to loss of soil on-­site. Erosion is particularly problematic in regions with sloping land, and around 45% of the world’s agricultural land has slopes of greater than 8% (FAO 2002). Erosion also leads to off-­site damage. In the United States, the annual off-­site damage from soil erosion caused by water recreation, water storage, navigation, flooding, and municipal water treatments is estimated at $8.8 billion (CTIC 2006). Cropland erosion in the United States is estimated at 4 billion tons of soil lost from 160 million hectares of farmland annually at an estimated cost of $20 billion for replacement nutrients and $7 billion for lost water and soil depth (Pimentel et al. 1995). Adverse soil effects also include nutrient depletion and salinization. Farmers often use insufficient fertilizers to replace lost nutrients, leading to nutrient mining and lost soil productivity (FAO 2002). Salinization can result from the use of irrigation in arid and semiarid 15

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16    Kurt D. Thelen

environments where rainfall is inadequate to provide leaching needed to remove excess salts from the soil. It has been estimated that 40% of the world’s arable land is subject to this problem (Smedema and Shiati 2002). Heavy irrigation also can cause waterlogging of the soil, which brings soil-­borne salts closer to the surface. High evaporation rates remove the water and leave behind the salt, eventually leading to a salt crust on the soil surface.

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Water Use and Quality

Use of water for irrigation results in lowered water tables, increased river diversions to agricultural fields, and salinization of some water tables in arid or semiarid regions. In some areas of India and China, water tables are dropping by 1–­3 meters per year because of heavy withdrawals of water for agricultural production (FAO 2010). Agriculture is already the primary use of water, and demands for agricultural use, and possible associated shortages, are expected to increase over the next decades (FAO 2010). Agriculture is the leading source of pollutants in assessed streams, rivers, and lakes in the United States, as determined by the Environmental Protection Agency (US EPA). As an industry, agriculture adversely affects 18% of assessed streams and rivers and contributes 48% of the water quality problems in the rivers and streams classified by the US EPA as having impaired water quality. Agricultural pollution problems affect 18% of lakes assessed by the US EPA and contribute 41% of the reported quality problems in lakes characterized as impaired. Leading pollutants attributable to agriculture include siltation, dissolved solids, bacterial pathogens, habitat alterations, oxygen-­depleting substances, carried nutrients, and thermal modifications. Of these, siltation, sometimes referred to as sedimentation, and carried nutrients are generally identified as having the most extensive effect. Sediment moving from agricultural fields through erosion finds its way to streams, rivers, and lakes. Once in aquatic ecosystems, sediment can cause algal blooms and eutrophication from carried nutrients; reduce available habitat where fish lay eggs; deplete available oxygen through the biological oxygen demand of microorganisms; degrade the organic fractions carried with sediment; block sunlight penetration, reducing growth of beneficial aquatic plants; and in severe cases, abrade gills of indigenous fish. As algae die, they sink to the bottom, where microbial degradation consumes oxygen, resulting in the suffocation of fish. Nutrients are found in 22% of U.S. assessed lakes and contribute to 50% of the reported water quality problems in lakes classified as having impaired water quality (US EPA 2000). Worldwide, nutrient runoff, especially of nitrogen and phosphorus, has caused eutrophication of freshwater and coastal marine ecosystems (Millennium Ecosystem Assessment 2005).

Pesticide Use

Because of their inherent toxicity and risk to the environment, pesticides used in agricultural systems have undergone much scrutiny. Pesticide production increased globally over the second half of the twentieth century, reaching approximately 3 million tons per year (Tilman et al. 2001). Pesticides that do not degrade rapidly can bioaccumulate in food chains and have

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Environmental Issues    17

impacts on nontarget species and distant locations. The ideal fate of a pesticide in an agricultural system is for it to degrade into harmless byproducts, having exerted its toxicity on the targeted weed, insect, or plant pathogen. However, as in all biological systems, many variables influence the activity and fate of an imposed input such as a pesticide. Weather conditions, soil properties, applicator equipment, and the chemical properties of the pesticide all interact to determine its fate. When it is applied according to label directions, the risk of adverse environmental effects from pesticides is minimized. However, under adverse conditions, such as the rainfall-­induced runoff that causes pesticide contamination of surface waters in the Midwestern United States (Wauchope et al. 2002), the off-­site movement and thus the nontarget injury of the pesticide is increased. Prior to the implementation of more stringent US EPA pesticide registration requirements in the United States, several significant environmental problems occurred from commonly practiced agricultural pesticide applications. Prior to the removal of DDT from the market in 1973, these include off-­target DDT injury to avian species. Additionally, in the late 1970s, aldicarb, a broad-­spectrum insecticide, was found in numerous drinking water wells in the potato-­producing region of Long Island, New York, and DBCP (dibromochloropropane) was found in over 2,000 drinking wells in California. As a result of these environmental concerns, the US EPA revamped its pesticide registration requirements. Before a pesticide can be used in the United States, the US EPA conducts ecological risk assessments to determine what risks are posed by a pesticide and whether changes to the use or proposed use of that pesticide are necessary to protect the environment. A pesticide applicant is required by the US EPA to conduct and submit a wide range of environmental laboratory and field studies. These studies examine the ecological effects and chemical fate and transport of pesticides in the environment. Using data on environmental fates and exposure models, US EPA scientists estimate the exposure of different animals to pesticide residues in the environment. Finally, pesticide toxicity information and exposure data are evaluated to determine the ecological risk from the use of the pesticide, whether it is safe for the environment and wildlife (US EPA 2010). The US EPA, Section 305(b), Clean Water Act National Reports, compiled from state water quality assessments, does not list pesticides among the leading pollutants in streams and rivers. However, the same report implicates pesticides as a source of contamination in 4% of the U.S. assessed lake acres. Soil contamination by label-­rate applications of pesticides is not considered to be a significant environmental risk because they are eventually degraded by the soil microbial community. Currently, the predominant pesticide risk to soil quality is from point source contaminations in which applicator or transfer/loading equipment malfunctions, and large quantities of pesticide are discharged to the soil. While pesticide use declined in most developed countries during the 1990s, it increased in other parts of the world (FAO 2002). Hazardous pesticides that have been phased out in North America and Europe remain in use in other parts of the world, as pesticide sales records demonstrate (Brodesser et al. 2006). In addition to potential environmental effects of pesticide use, there are human health risks, with an estimated 3,000,000 cases of pesticide poisoning occurring worldwide annually (CGIAR 2003). The majority occur in developing countries where there is less education, regulation, and use of personal protective equipment (Brodesser et al. 2006; CGIAR 2003).

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Air Quality

The release of carbon dioxide (CO2) and other greenhouse gases (GHG) into the atmosphere is perhaps the most potentially significant air quality impairment from agriculture. However, as will be discussed later, it is potentially the area where agriculture can contribute the greatest ecosystem service to society with the plant-­based removal of CO2 from the atmosphere and subsequent sequestration of carbon into the soil system. Dust and particulate matter emanating from agricultural operations can cause allergenic and safety concerns. Finally, livestock and manure odors can be the basis for social and quality of life concerns. Since the preindustrial era, human activities have significantly changed the composition of the atmosphere. The three primary GHG, namely CO2, nitrous oxide (N2O), and methane (CH4), have all increased in the past 200 years. Atmospheric CO2 levels have risen from a background level of 280 ppm in the year 1800 to over 360 ppm today (WDGCC 2004). CH4 concentrations have more than doubled in the same time period, rising from 750 to over 1,600 ppb. On a global bases, human activity results in a net increase of 3.3. gigatons (3.6 billion tons) of carbon released into the atmosphere annually. In the United States, agriculture ranks fifth in GHG emissions behind the industrial, transportation, commercial, and residential sectors. Agricultural practices involving intensive tillage, residue removal, high erosion rates, and low productivity all contribute to GHG emissions. In more recent years, improved agricultural management practices, including conservation tillage, cover crops, erosion control methods such as vegetated filter strips, and improved rotations, have reversed the trend for GHG emissions, and if managed correctly, can even result in a net removal of GHG from the atmosphere. Indeed, agriculture can be a significant part of the mitigating of GHG emissions. However, if all the carbon released by historical land use changes could be restored to the soil system, atmospheric CO2 concentrations would only be reduced by 40 to 70 ppm. Energy conservation and replacement of fossil based fuels with renewable fuel alternatives are still necessary components in the reduction of global GHG (Lal 2004). Agriculture alone cannot be relied upon to solve the problem. A potential mitigating factor in GHG emissions from agriculture is the planting of glyphosate-­resistant crops. Bennet et al. (2004) assert that the environmental and health effects of integrating glyphosate-­resistant crops into cropping systems need to be analyzed on a case-­by-­case basis. However, their research in Europe indicated that approximately 50% less energy was required to grow glyphosate-­resistant sugar beets than to grow conventional beets, meaning lower emissions and energy consumption from herbicide manufacturing, transport, and field operations. Recent U.S. air quality standards, which exempt agricultural operations only for disease control purposes, require particulate matter emissions below derived threshold levels. Intensive tillage under dry soil conditions, harvest operations in field crops, and controlled burns of plant residue for rotational crop establishment purposes are examples of agricultural practices that can result in high particulate matter emissions. Reduced tillage systems, including no-­till, have reduced particulate matter emissions from the agricultural sector. Research on technology-­based improvements for limiting particulate matter emissions from agricultural activities continues to improve emission levels.

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Environmental Issues    19

Summary

Because of the predominance of agriculture as a major use of land, the environmental risk from agricultural activities is significant. Impacts include loss of biodiversity resulting from conversion of land to agriculture purposes, as well as effects on land, water, and air quality (Foley et al. 2005; Tilman et al. 2001). Strategies to reduce further land conversion and ameliorate the effects of agriculture include increased productivity per unit land area, reduced chemical inputs and water use, and implementation of management practices to maintain soil quality. Technological advances in agriculture can increase productivity while still protecting the environment. Recent advances in transgenic crops can contribute to this “win-­win” technology. For example, the adaptation of glyphosate-­resistant crops has contributed to minimizing erosive soil loss, reducing agricultural energy inputs, increasing carbon sequestration, and reducing greenhouse gas emissions (Cerdeira and Duke 2006; Gianessi 2005; Heimlich et al. 2000). In a comprehensive review on the environmental effects of glyphosate-­resistant crops, Cerdeira and Duke (2006) conclude that the compatibility of glyphosate-­resistant crops with reduced or no-­till systems has contributed significantly to their adoption in the Western Hemisphere. Similarly, Heimlich et al. (2000) report that glyphosate replaced herbicides that are twice as persistent in soil and three times more toxic. Furthermore, the use of glyphosate on glyphosate-­resistant crops has reduced herbicide use by 17 million kg per year in the United States (Gianessi 2005). Society will require continued improvement in agricultural conservation measures and will call for agriculture to play a major role in remediating current environmental issues such as greenhouse gas accumulation and global warming.

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References Bennett, R., R. Phipps, A. Strange, and P. Grey. 2004. Environmental and human health impacts of growing genetically modified herbicide tolerant sugar beet: A life-­cycle assessment. Plant Biotechnol. J. 2:273–­278. Brodesser, J., D. H. Byron, A. Cannavan, I. G. Ferris, K. Gross-­Helmert, J. Hendrichs, B. M. Maestroni, J.  Unsworth, G.  Vaagt, and F.  Zapata. 2006. Pesticides in developing countries and the international code of conduct on the distribution of use of pesticides. http://www-naweb.iaea.org/ nafa/fep/public/2006-AGES-CoC.pdf. Cerdeira, A. L., and S. O. Duke. 2006. The current status and environmental impacts of glyphosate-­ resistant crops: A review. J. Environ. Qual. 35:1633–­1658. Consultative Group on International Agricultural Research (CGIAR) 2003. Pesticide use and abuse in irrigated areas. http://www.iwmi.cgiar.org/health/pesticide/index.htm. Foley, J. A., R. DeFries, G. P. Asner, C. Barford, C. Bonan, G. Bonana, S. R. Carpenter, F. S. Chapin, M. T. Coe, G. C. Daily, H. K. Gibbs, J. H. Helkowski, T. Holloway, E. A. Howard, C. J. Kucharik, C. Monfreda, J. A. Patz, C. Prentice, N. Ramankutty, and P. K. Snyder. 2005. Global consequences of land use. Science 309:570–­574. Food and Agriculture Organization of the United Nations (FAO). 2002. World agriculture: Towards 2015/2030. Summary report. http://www.fao.org/docrep/004/y3557e/y3557e08.htm.

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———. 2010. AQUASTAT.  Review of agricultural water use per country. http://www.fao.org/nr/ water/aquastat/water_use/index.stm. Gianessi, L. P. 2005. Economic and herbicide use impacts of glyphosate-­resistant crops. Pest Manag. Sci. 61:241–­245. Heimlich, R. E., J. Fernandez-­Cornejo, W. McBride, J. S. Klotz-­Ingram, S. Jans, and N. Brooks. 2000. Genetically engineered crops: Has adoption reduced pesticide use? Agric. Outlook 274:13–­17. Lal, R. 2003. Soil erosion and the global carbon budget. Environ. Int. 29:437–­450. ———. 2004. Agricultural activities and the global carbon cycle. Nutr. Cycl. Agroecosyst. 70:103–­116. Millennium Ecosytem Assessment. 2005. Ecosystems and human well-­being: Synthesis. Washington, DC: Island Press. Pimentel, D., C.  Harvey, P.  Resoudatmo, K.  Sinclair, D.  Kurz, M.  McNAir, S.  Crist, I.  Shpritz, L. Fitton, R. Saffouri, and R. Blair. 1995. Environmental and economic costs of soil erosion and conservation benefits. Science 267:1117–­1127. Smedema, L. K., and K. Shiati. 2002. Irrigation and salinity: A perspective review of the salinity hazards of irrigation development in the arid zone. Irrig. Drain. Syst. 16:161–­174. Tilman, D., J.  Fargione, B.  Wolff, C.  D’Antonio, A.  Dobson, R.  Howarth, D.  Schindler, W. H. Schlesinger, D.  Simberloff, and D.  Swackhamer. 2001. Forecasting agriculturally driven global environmental change. Science 292:281–­284. U.S.  Environmental Protection Agency (US EPA). 2000. National Water Quality Inventory: 2000 Report. http://water.epa.gov/lawsregs/guidance/cwa/305b/2000report_index.cfm. ———. 2010. Pesticides: Environmental Effects. http://www.epa.gov/pesticides/ecosystem/index.htm. Wauchope, R. D., T. L. Estes, R. Allen, J. L. Baker, A. G. Hornsby, R. L. Jones, R. P. Richards, and D. I. Gustafson. 2002. Predicted impact of transgenic, herbicide-­tolerant corn on drinking water quality in vulnerable watershed of the mid-­western U.S.A. Pest Manag. Sci. 58:146–­160. World Data Center for Greenhouse Gasses (WDGCC). 2004. WMO Global Atmospheric Watch. http://gaw.kishou.go.jp/wdcgg/.

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Environmental Biosafety Issues Associated with Genetically Engineered Crops Chol ani Weebadde and Karim M. Maredia

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Biotechnological tools allow the transfer of DNA between distantly related species. These techniques have facilitated the engineering of novel traits into crops, including insect resistance, herbicide tolerance, virus resistance and nutritional enhancement. The most widely deployed genetically engineered (GE) crops today contain insect resistance and herbicide tolerance, with farmers in over 25 countries growing these crops (James 2008). Many other traits are in the pipeline, such as tolerance to drought and cold and increases in the ability to use soil nitrogen (Grumet et al., this volume). Many of these target traits have been difficult or impossible to develop using conventional crop improvement techniques. Among the key considerations that must be weighed in the release of GE crops is whether they pose an unacceptable risk to the environment and human safety. These concerns have been recognized in many countries and have led to the establishment of regulatory policies and decision-­making bodies. In this chapter we provide an introduction to the ecological concerns that have been raised with respect to GE crops and describe how those risks can be assessed.

Environmental Issues and Concerns Associated with GE Crops

Concerns about the potential environmental impacts of GE crops and approaches to evaluate these concerns have been discussed by many authors, including excellent reviews by Conner et al. (2003), Dale et al. (2002), Hancock (2003), Nickson (2008), and Snow et al. (2005). These concerns are briefly outlined here. Environmental concerns consider both natural ecosystems and agroecosystems, and primarily center around the possibility that production of GE crops might reduce the biodiversity of organisms living in or near areas where they are grown. The potential negative environmental impacts associated with transgenic crops can be grouped into the following four broad areas: (1) weediness and invasiveness, (2) gene flow, (3) nontarget effects, and (4) pest resistance.

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Weediness and Invasiveness One of the potential concerns about GE crops is that they will become agricultural weeds or invade natural habitats (Hancock, this volume). The term weediness is best applied to a species’ competiveness in agricultural fields, while invasiveness relates to how effectively a species competes in natural environments. The concern is that traits introduced by genetic engineering might increase the reproductive success or fitness of the crop and thereby increase its competitive ability. For example, if a crop was engineered for tolerance to a particular herbicide, it would be more difficult to control as a “volunteer” in subsequent plantings. Alternatively, a crop engineered for salt tolerance may be able to invade previously inaccessible environments and outcompete other wild species. It should be noted, however, that the competitive ability of a plant is a function of many characteristics regulated by numerous genes acting in concert, and most crops have been so domesticated that they have difficulty surviving in the wild (Hancock et al. 1996; Hancock and Hokanson 2003). Genes controlling traits such as reproductive effort, seed size, dormancy, germination rate, ripening periods, and fruit and seed dehiscence all act in concert to determine relative competitiveness in different environments (Hancock 2003; Keeler 1989; Baker 1974). The potential impact of any given transgene will depend on competitive characteristics of the crop or recipient population, the specific environment into which it is introduced, and fitness traits conferred by the introduced gene.

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Gene Flow The possibility that transgenes may be transferred via pollen “escape” to wild or weedy relatives growing nearby is often cited as a potential risk of GE crops. Gene flow between crops and their close wild relatives is a well-­documented natural phenomenon (Ellstrand et al. 1999). Several kinds of gene flow from GE crops to relatives are possible, including (1) gene/ pollen flow from GE crops to conventionally bred crops, (2) gene/pollen flow from GE crops to landraces and (3) gene/pollen flow from GE crops to wild relatives (Hancock, this volume; Hancock and Halsey, this volume). In the first case, there is concern that seeds and fruit of organic or conventionally grown crops will acquire transgenes from nearby GE crops. Levels of gene flow can be controlled by isolation distances, but at present, laws do restrict how close GE crops can be planted to organic ones. In the second case, pollen flow is expected to occur wherever GE crops and landraces are grown in close proximity. If farmers choose to keep the hybrids, the landraces could be dramatically altered. However, landraces are rarely static entities, and farmers routinely trade landraces and allow them to hybridize both with other landraces and with modern cultivars (Perales et al. 2003; Bellon and Berthaud 2004; Hancock, this volume). As far as the third scenario is concerned, the question is whether the fitness of a wild plant would be sufficiently enhanced through pollen flow of a transgene to make it a more noxious weed or better competitor in the natural plant community. In assessing the risk of transgene escape into natural populations via pollen flow, three factors must be considered (Hancock, this volume): (1) Is a compatible relative present in the area of deployment? (2) How invasive is the native relative or crop without the transgene? and (3) Will the engineered trait significantly affect the invasiveness of the crop or native relative? The net effect of transgenes could be neutral, advantageous, or even deleterious, and the

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Environmental Biosafety Issues    23

risk of their deployment relates to which of these effects they have (Hancock 2003; Hancock and Hokanson 2003). In addition, the transgenes move as part of a total package with the rest of the domesticated crops’ genes. In the case of traits such as herbicide resistance, their escape will have little impact on the reproductive success of plants in the natural environment, where herbicides are not used, but they could have a major impact in farmers’ fields if the previously controlled native species is a noxious weed. The effect of pest resistance genes such as Bt and virus resistance in native populations depends on whether other resistance genes are already in existence in the wild and how much pest pressure is in the natural environment. The impact of genes that broaden the adaptations of crops such as improving salinity or drought tolerance depends on whether they elevate the existing adaptations of the native species. Another concern associated with gene flow is the possibility of horizontal gene transfer (e.g., Snow et al. 2005). Transmission of DNA by nonsexual means is not uncommon among microbes under specific conditions (Snow et al. 2005). Transmission of plant DNA to microbes has also been demonstrated under specific conditions in the laboratory (Kay et al. 2002; Tepfer et al. 2003). One key feature of these laboratory experiments is that the observed DNA transfer was from transgenes incorporated into the chloroplast of the transgenic plant, not in the nuclear DNA, where all of the transgenes currently released have been inserted. They were also conducted under conditions that were meant to favor horizontal gene transfer. Therefore, these experiments established that there is the possibility of occurrence of this phenomenon. Whether such a phenomenon would occur under field conditions and with the transgenic crops currently in commerce has not been established. Conditions for such transfer from extant transgenic crops include homology of the transgene to microbial DNA and release of the DNA in close proximity to bacteria capable of taking up DNA (Gebhard and Smalla 1998; Bertolla and Simonet 1999). Attempts to detect horizontal gene transfer from plants with transgenes in the nuclear genome have thus far failed (Smalla et al. 2000; Syvanen 1999). Furthermore, it should be noted that transgenes comprise only a few genes out of the tens of thousands of genes (DNA) released by each plant into the environment on a regular basis. Thus, if horizontal gene transfer were to be considered a risk, the exposure to that risk would be several orders of magnitude greater from plant DNA other than the transgenes.

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Impacts on Nontarget Organisms Another of the concerns associated with transgenic crops is that they could have toxic effects on nontarget organisms (Rose, this volume; O’Callaghan et al. 2005). This is of particular concern in those crops engineered to produce a pesticidal compound. Deployment of pest control measures could adversely affect species that come in contact with the crop, including beneficial insects and soil organisms, and thus negatively impact ecosystem function and biodiversity. These concerns are addressed through testing toxicity of the active ingredient on indicator organisms and by monitoring for toxic effects (Andow and Hilbeck 2004). When considering the potential effects of GE crops on nontarget organisms, it is important to compare those effects with the environmental impact of conventional alternatives, including widely used chemical pesticides. Every new technology has its own risks and benefits, and it is important to evaluate its impact on the ecosystem as a whole. The appropriate comparison will depend on the current practices in the location to which the GE crop will be introduced. For example, are chemical pesticides currently in use in the local cropping

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24    Cholani Weebadde and Karim M. Maredia

systems? Are other methods being used? The list of potentially affected organisms in natural and agroecosystems is very wide, and for this reason, risk analysis of nontarget effects has to be focused on organisms closely related to the target group and representatives of other classes of organisms such as pollinators (honeybees), natural enemies (predators and parasitoids), endangered and threatened species or insects of cultural and aesthetic value (monarch butterflies) and soil-­dwelling organisms (earthworms, Collembola, microorganisms and microarthropods, protozoans) (Rose, this volume). Risk analyses of nontarget effects are generally conducted using a tiered approach (Rose, this volume). In tier 1, the toxicity of microbially derived protein mixed with diet is analyzed in the laboratory. In these “lower-­tier” laboratory studies, extremely high levels of toxin, standard testing protocols, and surrogate species are used to provide a high level of sensitivity in identifying any hazard. If potential adverse effects are noted, a tier 2 study is conducted where the toxicity of more natural routes of exposure are analyzed, such as transgenic leaf material and exposed prey. In tiers 3 and 4, long-­term, semifield (greenhouse or cages) and open field studies are undertaken to determine population level effects with more realistic levels of environmental exposure. The types of monitoring done in tier 4 include aerial/flying invertebrates, surface-­dwelling organisms, and below-­ground invertebrates and microorganisms. Although a lack of toxicity in lower-­tier tests indicates little risk to the tested organisms, higher-­tier tests are often required by regulatory agencies. Higher-­tier field studies with appropriate levels of replication become very costly and generate large datasets whose relevance to a regulatory decision is often limited. Nevertheless, field studies have been done, often postcommercialization, to confirm the precommercialization risk assessments.

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Development of Pest Resistance Pest organisms (insects, pathogens, and weeds) can develop resistance to control tactics if a high selection pressure is imposed on them. One of the concerns associated with the release of crops engineered for pest resistance is that resistance will develop over time if the transgenic crop is used as the only or primary control tactic (DiFonzo et al., this volume). This is not unlike the long-­recognized cases where resistance has evolved after continual exposure to chemical sprays (Touart and Maciorowski 1997; Knight and Norton 1989). From an environmental perspective, the primary concern is that loss of insect control through GE crops may cause a return to less benign chemical pesticide controls. To delay the appearance of resistance, a number of insect resistance management (IRM) practices have been deployed in conjunction with the release of transgenic crops (DiFonzo et al., this volume). The most common IRM practice used with Bt crops is the planting of a refuge area of non-­Bt crops (that are unsprayed) along with the Bt crops. The idea is to provide the insects with a choice to feed on the non-­Bt crops so that the selection pressure for the resistant allele in the population is reduced and the allele susceptible to the Bt toxin will be maintained in high numbers. Another common IRM strategy to delay the appearance of resistance to Bt crops is to deploy transgenic crops that carry more than one resistance gene with different modes of action. It is assumed that the evolution of resistance to more than one gene will be more difficult to achieve than to one gene only (Gould 2003). Numerous laboratory experiments have shown that Bt resistance can evolve if insects are exposed to increasing doses of Bt (Janmaat and Myers 2003; Moulton and Dennehy 2001).

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Environmental Biosafety Issues    25

The high dose and refuge strategy has been the most successfully deployed IRM strategy in the field. Although large-­scale resistance to pests in Bt fields have not been reported, there are a few reported cases where lepidopteron pests have developed resistance to the Bt toxins Cry 1Ac, Cry1F, and Cry1Ab (Tabashnik et al. 2008; Moar et al. 2008). However, as Bt crops become more and more widely deployed, it is likely to be only a matter of time until pest resistance develops. Weeds can also develop resistance to herbicides over time (DiFonzo et al., this volume). With the wide-­scale adoption of the glyphosate-­resistant or “Roundup Ready” (RR) crops, there has been increased use of the herbicide glyphosate and a reduction in the application of other herbicides. These shifts have increased selection pressure for glyphosate-­resistant weed biotypes, and resistant wild genotypes are beginning to emerge, with or without gene flow from transgenic crops (Owen and Zelaya 2005; Sandermann 2006; Powles 2008). These resistant genotypes will have little impact in the natural environment where herbicides are not used, but their existence may make future weed control in agronomic fields more difficult.

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Other Agroecological Issues With the increased use of GE crops in the developed and developing world, several additional agroecological concerns have been expressed. One of these is whether secondary pests will become more prominent when the primary pests are more effectively controlled by the transgenic insect resistant crops. In the case of Bt cotton in India, farmers have observed an increase in the secondary pests such as the mirid bugs (Creontides biseratence) and the tobacco caterpillar, Spodoptera litura (Khadi et al. 2007). The relevant question then becomes whether the benefits of yield increases and reduction of pesticides used outweigh concerns over the emergence of these secondary pests. Ideally, strategies will be developed in which Bt transgenes are used to control the primary pests and biological control methods are then used to control secondary and tertiary pests. Of particular concern to small-­scale subsistence farmers in developing countries is the impact of herbicide-­tolerant GE crops on intercropping and mixed-­cropping systems where a variety of leguminous food crops (e.g., cowpea and beans) are grown together with field crops such as maize, millet, and sorghum. Another concern sometimes expressed about the use of GE crops is that they will replace traditional landrace varieties and reduce the biodiversity of the crops grown, particularly in developing countries. While reduction in crop diversity is a legitimate concern, it is associated with the deployment of all modern crop varieties, not just GE varieties. Food Safety Concerns with GE Crops Although the focus of this book and this particular chapter is on the environmental safety aspects of GE crops, food safety is critical to any product intended for human consumption. Therefore, along with environmental safety, food safety assessments are also required as a part of the regulatory approval process of GE products (Cohen et al. 2003; Hollingworth et al. 2003). The principles of food safety assessment are well established and broadly accepted internationally (Kuiper et al. 2001; Konig et al. 2004). The Codex Alimentarius, operating under the Food and

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26    Cholani Weebadde and Karim M. Maredia

Agricultural Organization (FAO) in Rome, sets standards for food safety, quality, and labeling; the reader is referred to the Codex for further information. The key issues raised with respect to GE food products include allergenicity and toxicity of introduced proteins on humans and animals, and impact of genetic engineering on nutritional composition (Kuiper et al. 2001; Konig et al. 2004). Safety evaluation for GE foods as outlined in the Codex Alimentarius (2004) involves extensive characterization of the gene and gene product, including testing for toxicity and allergenicity, and evaluation of gene expression and biochemical composition of the transgenic plants. The International Food Safety Assessment Guidelines provided by the Codex Alimentarius use substantial equivalence as the basis of safety assessment. GE foods are compared to their conventional counterparts to determine whether they are altered in a significant way that could influence food safety (Konig et al. 2004).

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Guidelines for Environmental Risk Assessment for GE Crops

Concerns about possible impacts of GE crops on biodiversity have been addressed at both international and national levels. Three international agreements provide guidelines for assessing the environmental and food safety risk of biotechnological crops and products (see Low and Frederick, this volume). These include the Cartagena Protocol on Biosafety, the International Plant Protection Convention, and the Codex Alimentarius, as mentioned above. The primary aim of the Cartagena Protocol on Biosafety (CPB) is to protect biodiversity through responsible “development, handling, use, transfer and release of any Living Modified Organism.” The CPB provides guidelines for evaluating environmental risk and food safety, along with a central clearinghouse of information on GE crop production, export, and safety. The International Plant Protection Convention (IPPC) is a multilateral treaty administered by the IPPC Secretariat in FAO’s Plant Protection Service. Its role is to prevent the introduction and spread of plant pests and products and promote appropriate measures for their control. Risk can be best expressed in a mathematical form as Risk = probability × consequence = likelihood of event × undesired impact of the event. The undesired impact is referred to as hazard. All risk assessments should answer the following three questions (Conner et al. 2003): (1) What can go wrong (the possibility of harm)? (2) How likely is it to happen (the probability of that harm occurring)? and (3) What are the consequences if it happens (the consequence of that harm)? A number of steps are typically included in a biotechnology risk assessment (Traynor et al. 2002): (1) identifying any potential adverse effects on human health or the environment, (2) estimating the likelihood of these adverse effects occurring, (3) evaluating the consequences if the identified effects are realized, (4) considering the appropriate risk-­management strategies, and (5) estimating the overall potential environmental impact, both positive and negative. An efficient way to approach risk assessment is through “problem formulation” (Nickson 2008). It is conducted in several stages. First, assessment end points are identified that represent the ecological entities that need protection. Only those end points are recognized that are likely to be affected by the transgene/crop combination in the area where the GE crop might be deployed. A conceptual model is then developed that identifies the potential linkages between the GE crop and the ecological entity, followed by a risk hypothesis that can be tested using available information. Finally, an analysis plan is generated that identifies what data is needed and how it can be gathered.

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Environmental Biosafety Issues    27

Two general concepts have been proposed to guide ecological risk assessment—­the concept of familiarity and the precautionary principle. In the familiarity approach, the modified organism is compared to similar organisms with traits derived through classical breeding and considers whether the GE phenotype is novel in the environment (NRC 1989; OECD 1993a; 1993b). The risks of GE crop deployment are evaluated on a case-­by-­case basis depending on the crop species, the traits introduced, and the geographic location of introduction. The precautionary principle is outlined in the Cartagena Protocol on Biosafety preamble (1992): “Where there is a threat of significant reduction or loss of biological diversity, lack of full scientific certainty should not be used as a reason for postponing measures to avoid or minimize such a threat.” The intent of the precautionary principle has been understood in various ways (Goklany 2000; Wiener and Rogers 2002; Belt 2003; Cameron 2006; Recuerda 2008). In its most extreme form, it can be interpreted to mean “In case of doubt, do nothing.” However, as is evident from the prior chapter, current agricultural practices can have significant environmental impacts. Depending on the specific crop and application, and as discussed by Quemada (this volume), GE crops can help to reduce those impacts.

Summary

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Potential environmental concerns associated with GE crops include (1) weediness or invasiveness, (2) gene flow to non-­GE crops or relatives, (3) effects on nontarget organisms, and (4) evolution of pest resistance (in this volume: Hancock; Hancock and Halsey; Rose; DiFonzo et al.). In light of possible environmental impacts, countries around the world are developing or have developed biosafety guidelines, laws, and regulations for risk assessment, risk management, and risk communication (in this volume: Hancock and Quemada; Low and Frederick; Hokanson and Ferenczi; Falck-­Zepeda and Zambrano; Koch and Massey). Regardless of the underlying risk assessment concepts, prudent and safe deployment of new technologies requires safety assessment commensurate with the potential risks in the context in which those technologies will be used and managed. Both risks and benefits should be considered within the context of current-­day crops and production practices.

References Andow, D. A., and A. Hilbeck. 2004. Science-­based risk assessment for non-­target effects of transgenic crops. BioScience 54:637–­649. Baker, H. G. 1974. The evolution of weeds. Ann. Rev. Ecol. Syst. 5:1–­23. Bellon, M.  R., and J.  Berthaud. 2004. Transgenic maize and the evolution of landrace diversity in Mexico: The importance of farmers’ behavior. Plant Physiol. 134:883–­888. Belt, Henk van den. 2003. Debating the precautionary principle: “Guilty until proven innocent” or “innocent until proven guilty”? Plant Physiol. 132(3): 1122–­1126. Bertolla, F., and P. Simonet. 1999. Horizontal gene transfers in the environment: Natural transformation as a putative process for gene transfers between transgenic plants and microorganisms. Res. Microbiol. 150:375–­384. Cameron, L. 2006. Environmental Risk Management in New Zealand—­Is There Scope to Apply a

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28    Cholani Weebadde and Karim M. Maredia

More Generic Framework? New Zealand Treasury Policy Perspectives Paper 06/06. June. http:// www.treasury.govt.nz/publications/research-policy/ppp/2006/06-06/.tpp06-06.pdf. Cohen, J. I., H. Quemade, and R. Frederick. 2003. Food safety and GM crops: Implications for developing country research. Policy Brief Number 16, in Food Safety in Food Security and Food Trade, ed. L. J. Unnevehr. IFPRI, Washington, DC. 2003. Conner, A. J., T. R. Glare, and J.-­P. Nap. 2003. The release of genetically modified crops into the environment: Part II. Overview of ecological risk assessment Plant J. 33:19–­46. Dale, P. J., B. Clarke, and E. M. G. Fontes. 2002. Potential for the environmental impact of transgenic crops. Nat. Biotechnol. 20:567–­574. Ellstrand, N. C., H. C. Prentice, and J. F. Hancock. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Ann. Rev. Ecol. Syst. 30:539–­563. Gebhard, F., and K. Smalla. 1998. Transformation of Acinetobacter sp. Strain BD 413 by transgenic sugar beet DNA. Appl. Environ. Microbiol. 64:1550–­1554. Goklany, I. M. 2000. Applying the precautionary principle to genetically modified crops. Weidenbaum Center for the Study of American Business, Washington University, Working Paper No. 157. August. Gould, F. 2003. Bt-­resistance management—­theory meets data. Nat. Biotech. 21:1450–­1451. Hancock, J. F. 2003. A framework for assessing the risk of transgenic crops. BioScience 53:512–­519. Hancock, J. F., R. Grumet, and S. C. Hokanson. 1996. The opportunity for escape of engineered genes from transgenic crops. HortScience 31:1080–­1085. Hancock, J. F., and K. Hokanson. 2003. Invasiveness of transgenic versus exotic plant species: How useful is the analogy? In The Bioengineered Forest: Challenges for Science and Technology, ed. S. H. Strauss and H. D. Bradshaw. Corvallis, OR: RFF Press. Pp. 181–­189. Hollingworth, R. M., L. F. Bjeldanes, M. Bolger, I. Kimber, B. J. Meade, S. L. Taylor, and K. B. Wallace. 2003. The safety of genetically modified foods produced through biotechnology. Tox. Sci. 71: 2–­8. James, C. 2008. Global status of commercialized biotech/GM crops: 2008. International Service for the Acquisition of Agri-­biotech Applications, ISAAA Brief No. 37. http://croplife.intraspin.com/ Biotech/papers/ID_372_james.pdf. Janmaat, A.  F., and J.  Myers. 2003. Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc. R.  Soc. Lond. Ser. B 270:2263–­2270. Kay, E., T. Vogel, F. Bertola, R. Nalin, and P. Simonet. 2002. In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl. Environ. Microbiol. 68:3345–­3351. Keeler, K. H. 1989. Can genetically engineered crops become weeds? Bio/Technology 7:1134–­1139. Khadi, B. M., K. R. Kranthi, and K. C. Jain. 2007. Impact of Bt-­cotton on Agriculture in India. World Cotton Research Conference-­4, Lubbock, TX, September 10–­14. Knight, A.  L., and G.  Norton. 1989. Economics of agricultural pesticide resistance in arthropods. Annu. Rev. Entomol. 34:293–­313. Konig, A., A. Kocburn, R. W. R. Crevel, E. Debruyne, R. Grafstroem, U. Hammerling, I. Kimber, I.  Kinudsen, H.  A.  Kuiper, C.  M.  Peijnenburg, A.  H.  Penninks, M.  Paulsen, M.  Schauzu, and J. W. Wall. 2004. Assessment of the safety of foods derived from genetically modified (GM) crops. Food Chem. Toxicol. 42:1047–­1088. Kuiper, H. A., G. A. Kleter, H. P. J. M. Noteborn, and E. J. Kok. 2001. Assessment of the food safety issues related to genetically modified foods. Plant J. 27:503–­528. Moar, W., R. T. Roush, A. M. Shelton, J. Ferre, S. MacIntosh, B. R. Leonard, and C. Abel. 2008. Field-­ evolved resistance to Bt toxins. Nat. Biotechnol. 26:1072–­1074.

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Moulton, J. K., and J. T. Dennehy. 2001. University of Arizona College of Agriculture vegetable report. National Research Council (NRC). Committee on Scientific Evaluation of the Introduction of Genetically Modified Microorganisms and Plants into the Environment, Board on Biology, Commission on Life Sciences. 1989. Field Testing Genetically Modified Organisms: Framework for Decisions. Washington, DC: National Academy Press. Nickson, T. E. 2008. Planning environmental risk assessment for genetically modified crops: Problem formulation for stress tolerant crops. Plant Physiol. 147:494–­502. O’Callaghan, M., T. Glare, E. P. J. Burgess, and L. A. Malone. 2005. Effect of plants genetically modified for insect resistance on non-­target organisms. Annu. Rev. Entomol. 50:271–­292. Organization for Economic Co-­operation and Development (OECD). 1993a. Safety Considerations for Biotechnology: Scale-­up of Crop Plants. Paris: OECD. ———. 1993b. Safety Considerations of Foods Derived by Modern Biotechnology: Concepts and Principles. Paris: OECD. Owen, M. D. K., and I. A. Zelaya. 2005. Herbicide-­resistant crops and weed resistance to herbicides. Pest Manag. Sci. 61:301–­311. Perales, H. R., S. B. Brush, and C. O. Qualset. 2003. Dynamic management of maize landraces in central Mexico. Econ. Bot. 57:21–­34. Powles, S. B. 2008. Evolved glyphosate-­resistant weeds around the world: Lessons to be learnt. Pest Manag. Sci. 64:360–­365. Recuerda, M. A. 2008. Dangerous interpretations of the precautionary principle and the foundation values of the European Union food law: Risk versus risk. J. Food Law and Policy 4 (1): 1–­43. Sandermann, H. 2006. Plant biotechnology: Ecological case studies on herbicide resistance. Trends Plant Sci. 11:324–­328. Smalla, K., S. Borin, H. Heuer, F. Gebhard, J. van Elsas, and K. Neilson. 2000. Horizontal transfer of antibiotic resistance genes from transgenic plants to bacteria: Are there new data to fuel the debate? In Proceedings of the 6th International Symposium on the Biosafety of Genetically Modified Organisms, ed. G. Fairbairn, G. Scoles, and A. McHugen. Saskatchewan, Canada: University Extension Press. Pp.146–­154. Snow, A. A., D. A. Andow, P. Gepts, E. M. Hallerman, A. Power, J. M. Tiedje, and L. L. Wolfenbarger. 2005. Genetically engineered organisms and the environment: Current status and recommendations. Ecol. Appl. 15:377–­404. Syvanen, M. 1999. In search of horizontal gene transfer. Nat. Biotechnol. 17:833. Tabashnik, B. E., A. J. Gassmann, D. W. Crowder, and Y. Carriere. 2008. Insect resistance to Bt crops: Evidence versus theory. Nat. Biotechnol. 26:199–­202. Tepfer, D., R. Garcia-­Gonzales, H. Mansouri, M. Seruga, B. Message, F. Leach, and M. Perica. 2003. Homology-­dependent DNA transfer from plants to a soil bacterium under laboratory conditions: Implications in evolution and horizontal gene transfer. Transgen. Res. 12:425–­437. Touart, L. W., and A. F. Maciorowski. 1997. Information needs for pesticide registration in the United States. Ecol. Appl. 7:1086–­1093. Traynor, P. L., R. J. Frederick, and M. Koch. 2002. Biosafety and Risk Assessment in Agricultural Biotechnology: A Workbook for Technical Training. East Lansing: Agricultural Biotechnology Support Project, Institute of International Agriculture, Michigan State University. http://www.science.oas. org/Simbio/biosafety/intro_bios.pdf. Wiener, J. B., and M. D. Rogers. 2002. Comparing precaution in the United States and Europe. J. Risk Res. http://www.env.duke.edu/solutions/documents/wp01.pdf.

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Current Status of Genetically Engineered Crops and Assessment of Environmental Impacts

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Hector Quemada

Genetically engineered (GE) crops have been commercially grown since 1996, when the first such crops were planted in the United States. Since then, the adoption of these crops has been rapid. James (2009) has provided an global overview of the current status of these crops: a total of roughly 134 million hectares (330 million acres) were grown worldwide in 2008; plantings of genetically engineered crops expanded from the the United States to 25 countries; North America was the largest producer of GE crops (the United States and Canada account for 64% of the world plantings) followed by South America with at least 34% of the hectarage (primarily in Argentina, Brazil, and Paraguay); globally, 77% of the soybean, 49% of the cotton, and 26% of the corn crop was planted to GE varieties in 2009; in Asia, the leading producers were India and China, with more limited production in the Philippines; while there was some production on all continents except Antarctica, the use has been more limited in Europe, Africa, and Australia. An estimated 14 million farmers planted GE crops in 2009, but because of differences in farm size, the great majority (90%) were in developing countries. The majority of the transgenic acreage planted worldwide is composed of only a few crops and traits. Soybean, maize, cotton, and canola account for the vast majority of area planted with transgenic varieties; insect resistance, herbicide tolerance, and the combination of the two are the most prevalent traits deployed (James 2009). In all commercial products to date, insect resistance has been achieved by introduction of various insecticidal proteins from the bacterium Bacillus thuringiensis (Bt). Most of the insecticidal proteins form crystals that accumulate in the bacterial spores. When consumed by an insect, the alkaline conditions in the insect gut release the toxin, which is highly specific to different orders of insects (e.g., Lepidoptera, Coleoptera, Diptera), depending on presence of the appropriate receptor molecules for uptake of the toxin (Schnepf et al. 1998; Gill et al. 1992). Other proteins (VIP proteins) are expressed during the vegetative growth phase of the bacterium. The Bt proteins are not toxic to vertebrates, which do not possess the necessary receptors for binding of the toxin. Herbicide resistance has been achieved for several products by introducing genes that encode an herbicide-­insensitive target molecule, or an enzyme that degrades the herbicide (Sahora et al. 1998). The most widely deployed herbicide tolerance gene is one encoding a protein that allows plants to tolerate the herbicide, glyphosate, marketed under the trade name 31

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Roundup (James 2006; Brookes and Barfoot 2006). Glyphosate is a nonselective herbicide that has broad applications in many cropping systems. It is noted for its low environmental impact due to low toxicity to animals; rapid adsorption to soil particles, reducing movement in the environment; and rapid degradation by soil microbes (Cerdeira and Duke 2006). Genetically engineered virus resistance also has been developed for a few specialty crops with limited production areas, such as papaya and squash (Grumet 2002). In these cases a pathogen-­derived resistance strategy has been used wherein the resistance genes are derived from the virus and expressed to interfere with the normal viral life cycle or trigger host defenses that target incoming viral RNA for degradation (Grumet and Lanina-­Zlatkina 1996; Fuchs 2008). All products on the market thus far have obtained regulatory approval first in the United States, and a smaller number then have been submitted for regulatory approval in other countries. Slightly more than 100 transgenic products worldwide—­representing 22 different species—­have completed the necessary steps for commercial approval (Center for Environmental Risk Assessment n.d.; see also Fukuda-­Parr 2007). The various transgenic lines that have been approved have then been crossed to nontransgenic lines to create new hybrids or varieties that are locally adapted to conditions such as day length, local diseases, abiotic stresses, or speed of maturity, in order to create literally thousands of varieties. While a large number of genetically engineered transformation events have been approved, particularly in the United States, only a subset of them have been placed on the market, or continue to be on the market (Biotechnology Industry Organization 2010). For example, early entries into the market such as Flavr Savr tomatoes and NewLeaf potatoes are no longer sold or, in cases such as LL601 rice, have not been released commercially by the company that developed them. The reasons for removal from the market or failure to release are beyond the scope of the present chapter. However, it is important to point out that none of these cases has been due to a safety concern.

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Potential Positive Impacts on the Environment and Human Health

Agriculture throughout the world is subject to many problems that reduce productivity. For example, pests account for a loss of 40% of agricultural production worldwide, despite measures taken to control them (Pimentel 1998). Data from Africa indicate highly variable impacts of pests, depending upon agroecological zone, but can reach 100% (Abate et al. 2000). Plant disease causes at least 10% losses in global food production (Strange and Scott 2005). Weeds and abiotic stresses such as drought are also a major factor in the loss of crop productivity (Boyer 1982). The potential for genetically engineered crops to address these problems has led to a high level of interest in agricultural biotechnology, in both the developed and developing world and in the public as well as the private sector. Genetically engineered crops hold the promise of being helpful in achieving increased food productivity while introducing methods and inputs that have a reduced impact on the environment. For example, the insect-­resistant crops expressing Bt genes in principle allow the reduction of synthetic pesticide use by replacing those pesticides with endogenously expressed, more environmentally benign proteins. This appears to have been the case on a global basis (Brookes and Barfoot 2008). Because of the improved environmental compatibility of the

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GE Crops and Environmental Impacts    33

Bt proteins, beneficial consequences are expected. First, greater taxonomic specificity of the Bt proteins should result in benefits to biodiversity within agricultural fields, relative to synthetic pesticides that have a broader range of nontarget effects. Meta-­analyses have recently been completed, compiling the results of numerous studies, and this expectation has been confirmed (Marvier et al. 2007; Duan et al. 2008; Wolfenbarger et al. 2008). Greater in-­field biodiversity might then be reflected in benefits to biodiversity outside of agricultural fields, at least for those species that inhabit or are affected by both types of environment. However, the impact on the latter will be more difficult to demonstrate. Another anticipated benefit from the cultivation of genetically engineered crops is the reduction in use of herbicides—­or at least a reduction in the use of more harmful herbicides. The reduced environmental impact of glyphosate relative to other herbicides should result in a reduction in the ecological toxicity of herbicides sprayed to control weeds. When considered on a global basis, this expectation also appears to have been realized (Brookes and Barfoot 2008). All of these crop improvements have more efficient production of food as their goal. In order to preserve biodiversity, some have argued that future needs for food must be met by present cropland area (Trewavas 2001). Consequently, further technological improvements are required in order to achieve this goal, and genetic engineering is one approach to achieving those necessary improvements. By contributing to the efficiency of food production, genetic engineering can help to relieve the pressure to increase the area of land under cultivation, thus reducing the amount of environmental destruction that is a necessary part of agriculture. The reduction in chemical use also has potential advantages from the point of view of human health. First, the substitution of nontoxic (against mammals) methods for insect control reduces the risk of poisoning to farmworkers and others who might come in contact with these chemicals. This benefit has been shown in a few cases (see below). More importantly, the exposure of consumers to toxic pesticide residues would be reduced. The benefit to farmworkers would be especially valuable in developing countries, where literacy is low (thus reducing awareness of proper application instructions) as is the availability of safety equipment on the farm. Lower capacity to enforce regulations or to test for pesticide residues also makes developing country populations more vulnerable to exposure to unhealthy levels of agricultural chemicals. Therefore, the benefit to developing country consumers would be correspondingly greater than to consumers in developed countries, where regulatory restrictions on pesticide use are more likely to be enforced. While the potential for addressing the problems of agricultural production are great, genetic engineering also presents the opportunity to develop crops that have enhanced nutritional value, or can produce food with desired product characteristics such as improved flavor, texture, or shelf life. These traits can do much to improve the health status of people in developing countries as well as enhance the exportability of crops grown there.

Potential Negative Impacts on the Environment and Human Health

When we consider the impact of transgenic crops on the environment, it is first useful to understand that the practice of agriculture itself exerts a significant negative impact (Thelen, this volume). Practices such as tillage, water use, intercropping, crop rotation, grazing, and

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34    Hector Quemada

extensive usage of pesticides affect the biodiversity of agricultural fields as well as the environment outside of fields (McLaughlin and Mineau 1995; Tilman 1999; Tilman et al. 2002; Stoate et al. 2001; Hails 2002; Robinson and Sutherland 2002; Butler et al. 2007). Intensification of agriculture is an underlying cause of biodiversity loss worldwide (Butler et al. 2007). It is against this background of the existing impact of present agriculture on the environment and biodiversity that the concerns about the environmental impact of genetically engineered crops should be considered. The concerns connected with the release of GE crops are described by Weebadde and Maredia (this volume), and have been reviewed previously by Snow et al. (2005). While these concerns remain as issues to be considered during the risk assessment before commercial approval of a crop, as of the writing of this present chapter, only one concern—­the evolution of resistance—­appears to have been substantiated. These concerns are discussed in what follows. Transgenic organisms persist without cultivation. The trait expressed in a transgenic crop might release it from natural constraints, thus allowing it to persist and become invasive in a nonagricultural situation. If this should happen, then the crop might outcompete other wild species, and thus lead to a decrease in biodiversity. Alternatively, the trait expressed in a crop may cause it to be tolerant of current measures used to control individuals that might grow where they are unwanted. If this should happen, then the crop would present a new weed problem. Transgenic organisms interbreed with related taxa, causing those taxa to become weedy or invasive. If a genetically engineered crop were capable of crossing with a wild relative, then a transgene might be transferred to progeny of populations of the wild relative. That introgressed trait might then cause the recipient populations to be released from a natural constraint on population size. Biosafety researchers usually try to address this question by determining whether the transgene confers increased fitness to individuals expressing the transgene compared with those that do not (see, for example, Crawley et al. 1993; Snow et al. 1998; Snow et al. 1999; Snow et al. 2003). However, in the case of pathogen resistance, others have taken the approach of trying to determine whether the pathogen is responsible for limiting the size of wild populations (Raybould and Cooper 2005; Quemada et al. 2008). Nontarget and indirect effects. Nontarget and indirect effects are a concern for crops expressing compounds that protect them from pests, such as those that express Bt proteins. This concern applies equally to transgenic crops or conventional pesticides. The concern about impact on nontarget organisms arises from the possibility that the loss of biodiversity resulting from the deployment of pest control measures could adversely affect populations of insects that do not feed on the crop (and are therefore not pests) and possibly lead to the loss of beneficial ecological functions, such as pollination, nutrient cycling, and natural pest control. The impact on endangered species or species of particular cultural significance is also a consideration. Included in these considerations is the impact on nontarget organisms that might be exposed to the insect control proteins through introgression of the transgene into compatible wild relatives. It should be pointed out that indirect effects resulting from the control of the target pest are a possibility if the technology performs as intended. For example, predators that feed on the target pest may be negatively affected because pest populations decline or the quality of the pest as food is reduced. Such indirect effects are a foreseeable and accepted potential of any pest control method. Consequently, any impact of this type should not be part of a risk assessment (OECD 1993; Romeis et al. 2008), nor should it be considered as an adverse effect

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that is normally of concern. With regard to the impact of genetically engineered crops on nontarget organisms, it should be kept in mind that the use of pesticides, which is the technology that this approach seeks to replace, has already demonstrated negative impacts on nontargets. Therefore, the evaluation of the impacts of genetically engineered crops should be done in comparison to this technology. However, it is recognized that in countries where access to chemical inputs is limited, then the proper standard of comparison may indeed be no pesticides. More information on impacts of Bt crops on nontarget organisms is provided below. Evolution of resistance. Evolution of resistance by the pest to the insect or disease resistance conferred by the transgene can shorten the useful life of the genetically engineered product. This is of concern if the genetically engineered product is designed to replace chemical pesticides, because the loss of the genetically engineered product will mean the return to dependence on less environmentally benign technologies. The evolution of resistance is also a concern to the developer of the genetically engineered crop because it means a shortened period of time during which the developer can market that crop.

Have Potential Positive Impacts on the Environment and Human Health Been Realized?

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Reduction of Pesticide and Herbicide Use Several studies on the use of pesticides and herbicides connected with the use of transgenic crops have been conducted, and have been the subject of recent reviews. Herbicide use has been seen to increase or decrease, depending upon the country and agricultural system, while reduction in pesticides has been more clearly demonstrated, particularly in cotton, which is a pesticide-intensive crop (Sanvido et al. 2007). Raney (2006) reported reductions in pesticide costs on cotton (presumably reflecting reduced use) ranging from 40%–­77% for farmers in Argentina, China, India and South Africa. Cattaneo et al. (2006) reported reductions of 28%–­53% (4.7–­7.9 tons/hectare) for cotton in Arizona in 2002 and 2003. The overall reduction in pesticide use attributed to GE crops increased from 45.7 to 69.7 million pounds per year from 2001 to 2005 (Sankula and Carpenter 2006). Brookes and Barfoot (2006; 2008) aggregated the use of pesticides and herbicides, and also took into consideration the toxicity of the chemicals used, to derive an Environmental Impact Quotient. This work indicates that the environmental impact of cultivating herbicide-­ tolerant soybeans, maize, cotton, and canola, as well as insect resistant maize and cotton, has been reduced as a result of the genetically engineered traits. The reduction in environmental impact is due to the cumulative reduction of 286 million kg of chemical active ingredients applied to agricultural land worldwide (Brookes and Barfoot 2008). Studies in China revealed more far-­reaching benefits of the use of Bt cotton (Wu et al. 2008). Analyses of 3 million hectares of cotton over six provinces showed that pest pressure from cotton bollworm decreased in direct proportion to the use of Bt cotton over the past decade. The decline did not correlate with several other factors that might influence pest populations such as temperature or rainfall. In addition to these expected effects on Bt cotton fields, were unexpected benefits on neighboring fields of non-­Bt cotton; the pest pressure from cotton bollworm showed a parallel drop in non-­Bt cotton fields. Bollworm

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36    Hector Quemada

eggs deposited on Bt plants did not develop into larvae, thus reducing the population size of subsequent bollworm generations. As a result, nearby non-­Bt cotton also required less pest control. This effect extended beyond cotton. Analysis of an additional 22 million hectares of noncotton crops in the Bt cotton-­growing areas showed that the pest pressure on crops such as corn, peanuts, soybean, and vegetables also decreased in direct proportion to the use of Bt cotton over the past decade. As a result these other crops also required less pesticide to control pests, and experienced reduced crop losses.

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Enhancement of Biodiversity One report that studied the impact of GE cotton on a large scale suggests that there is no difference in the effect of nontransgenic cotton, Bt cotton, and Bt/herbicide-­resistant cotton on the density and species richness of ants and beetles in cotton fields compared to adjacent noncultivated areas (Cattaneo et al. 2006). However, the impact of Bt crops on biodiversity outside of agricultural fields has not been extensively studied; much more data have been obtained for in-­field diversity. A recent meta-­analysis of the impact of Bt crops in 42 field experiments suggests that there is an overall beneficial impact on biodiversity in comparison to spray regimes (Marvier et al. 2007). Organisms such as ladybird beetles, earthworms, and bees were more abundant in Bt fields than in conventional cotton fields, although reduction in certain nontarget taxa was observed when compared with nonsprayed treatments (Marvier et al. 2007). This study was confirmed by further meta-­analyses to determine the impact on honeybees (Duan et al. 2008) and on functional guilds of arthropods (Wolfenbarger et al. 2008). These studies illustrate that the ability of Bt crops to enhance in-­field biodiversity must be judged relative to the need for control of target pests and the current methods used to control them. Research in China has revealed interesting impacts of Bt cotton on some nontarget pests. After the cotton bollworm, aphids are one of the most important pests of cotton in China. (Wu, Peng, and Jia 2003). Because of the use of insecticides in non-­Bt cotton fields, the availability of predators to control aphids (which are resistant to the insecticides) is reduced, while the predators remaining in the Bt cotton fields are able to control the aphids. Consequently, aphids increase in numbers in the non-­Bt cotton fields, relative to Bt cotton fields (Wu and Guo 2003). Therefore, in this case, the improved control of aphids is a side-­benefit of the technology.

Other Unanticipated Benefits

Increased No-­Till and Reduced Till Practices One unanticipated benefit resulting from the planting of genetically engineered crops has been the role that herbicide tolerant crops have played in enabling the practice of no-­till or reduced-­till agriculture. The beneficial impact of this development in increased productivity, through reduction of soil erosion, has been particularly evident in Argentina, where the area of soybeans grown under no-­till agriculture has increased dramatically (Trigo and Cap 2003). Similarly, in the United States, the increased adoption of no-till agriculture has been linked

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directly to the availability of these crops, especially herbicide-tolerant cotton (Fawcett and Towery 2002; Young 2006). No-­till agriculture has been linked to several agricultural and environmental benefits, including reduced soil erosion and carbon dioxide emissions, while increasing soil health and field biodiversity (Fawcett and Towery 2002). Reduction of Health Hazards Reduction in exposure and, consequently, reduction in toxicity effects on farmers have been documented for Bt cotton grown in China (Huang et al. 2002; Pray et al. 2002; Hossain et al. 2004; Huang et al. 2005). Reduction in consumer exposure to pesticides has not been studied, but an interesting unexpected benefit has been documented. Because injury to stems and kernels of maize by pest lepidopterans provides the opportunity for secondary pathogen infections, particularly fungi, protection against these pests prevents the accumulation of mycotoxins in grain (Munkvold et al. 1999). The reduction in mycotoxins, which are highly toxic to humans, has been consistently observed in several studies, and in different countries (Dalmacio et al. 2007). Reduction in mycotoxin contamination should be of greater relative benefit in countries that have less capacity to regulate the levels of these hazards in grain.

Have Potential Negative Impacts on the Environment and Human Health Been Realized?

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The concerns regarding possible negative impacts on the environment and human health listed previously remain topics of much discussion and have fueled much of the controversy surrounding genetically engineered crops. However, after just over a decade of commercial and large-­scale deployment, there has so far been no demonstration that harm to the environment or human health has actually occurred. The specific issues of concern are individually considered in this section. Transgenic Organisms Persist without Cultivation This author has been unable to find any report where addition of the traits used to date, either herbicide tolerance or insect or virus resistance, has conferred upon the genetically engineered crop the ability to invade unmanaged habitats and outcompete wild species, or to escape some means of control currently considered part of standard agricultural practices. Transgenic Organisms Interbreed with Related Taxa, Causing Those Taxa to Become Weedy or Invasive There have been documented examples of transgenic organisms interbreeding with free-­living (i.e., non-­agriculturally managed) nontransgenic plants of the same species (Watrud et al. 2004; Warwick et al. 2008). However, in these cases, there is no evidence that the transgene

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38    Hector Quemada

has conferred increased fitness to the recipient populations. In any case, there is as yet no good evidence to implicate enhanced fitness as a necessary or sufficient condition for invasiveness. In fact, Bossdorf et al. (2004) compared the fitness of garlic mustard (Alliaria petiolata) plant populations that had evolved in North America to become invasive, with the fitness of populations from Europe that were noninvasive. In experiments where these two types of populations were allowed to compete for limited resources, the noninvasive populations outperformed the invasive populations on the parameters of fitness measured (plant height, total biomass, silique number, and silique biomass).

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Nontarget and Indirect Effects To date, Bt genes have been the only commercially applied insect protection deployed in transgenic plants. Therefore, the data on actual nontarget and indirect ecological effects is available only for these technologies. In most countries where Bt crops have been deployed, they have been intended to replace or reduce applications of conventional insecticides commonly used in agriculture. Therefore, it can be argued that the proper baseline for comparative risk assessment should be the impact of insecticides (Dale et al. 2002; Conner et al. 2003). However, there may be some cases, particularly in developing countries, where there is very little if any access to chemical insecticides. In that case, the appropriate standard of comparison would be a nonsprayed control. As described above, numerous field studies have been conducted over the years, using both types of controls for comparison. The overall conclusion that can be drawn from those studies is that there are no consistent differences between non-­Bt and Bt crops under nonsprayed conditions, but that when compared to insecticide applications, Bt cotton has been overall beneficial. The most extensive information on impacts on nontarget organisms come from studies conducted in the United States and China. A household survey of Chinese farmers conducted in 2004 found that the net revenue of Bt farmers was significantly lower than non-­Bt farmers because of the cost of additional sprays required in that year to control mirid bug species, which are secondary pests in cotton fields (Wang et al. 2006). Wu et al. (2002) showed that while there was no difference in the abundance of the mirid bug species Lygus lucorum, Adelphicoris fasciaticollis, and Adelphicoris lineolatus, between nonsprayed Bt cotton and nonsprayed, nontransgenic cotton, the amount of damage caused by these secondary pests was greater in Bt-­cotton than in nontransgenic cotton. Therefore, these authors suggested that the control of these secondary pests could require additional measures. Whether these conditions will predominate in subsequent years, leading to the emergence of secondary pests, requires further study. These results serve as reminders that the informed and proper use of Bt technology, including its incorporation into more ecologically friendly integrated pest management approaches, is important to ensure its sustained beneficial impacts. Studies from India generally corroborate results from China. Bambawale et al. (2004) described the results of a farmers’ participatory field trial in rain-­fed conditions, with the majority of the farmers having small-­to-­marginal landholdings. In this case, the Bt cotton was compared with non-­Bt cotton for its impact on performance and nontarget insects under conditions of integrated pest management (IPM) as well as non-­IPM practices. Under IPM conditions, the abundance of sucking pests—­aphids (Aphis gossypii), jassids (Amrasca biguttula biguttula), thrips (Thrips tabaci) and whiteflies (Bemisia tabaci)—­as well as two species

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of natural enemies—­green lacewing (Chrysoperla carnea) and ladybird beetles (Coccinella spp.)—­was reduced in Bt-­cotton. However, the numbers of these insects were even lower in the non-­Bt, non-­IPM cotton. The decreased abundance of sucking pests in this study is unexpected, since the Bt protein expressed by the cotton plants has been shown to be specific to lepidopterans. The decrease in the natural enemies was attributed to the decrease in target pest (prey of the sucking pests) rather than a direct toxic effect of the Bt protein itself (Bambawale et al. 2004). In Australia, Whitehouse et al. (2005) evaluated the impact of Bt cotton on over 100 species groups over three seasons. They found consistently higher numbers of the pest Helicoverpa armigera in conventional nonsprayed cotton than in nonsprayed Bt cotton. Slightly higher numbers of Chloropidae and Drosopillidae (Diptera), damsel bugs (Hemiptera, Nabidae), and jassids (Hemiptera, Cicadellidae) in conventional (sprayed and unsprayed) crops were observed, leading the authors to recommend that the effects of these small differences in the transgenic and conventional communities should be monitored over the long term to determine whether these findings are of any concern and require any action. Among the nontarget organisms of concern are soil microbes. With regard to the impact of genetically engineered crops on soil, it is important to note that agricultural practices themselves cause large changes in soil (Buckley and Schmidt 2001; Clegg et al. 2003). Furthermore, factors such variations in seasons and weather, plant growth stage, and plant varieties, independent of whether they are genetically engineered, are also responsible for significant impacts on soil microbial communities (Heuer and Smalla 1999; Griffiths et al. 2000; Lukow et al. 2000; Dunfield and Germida 2001; 2004; Lottman and Berg 2001; Gyamfi et al. 2002; Heuer et al. 2002). Most studies with genetically engineered crops have shown minor or no effects on soil microbes beyond the variation caused by the factors listed above (Kowalchuk et al. 2003). The Bt crops have been especially well studied. While no formal meta-­analysis has been conducted on the impact of these crops on soil microbial communities, the picture emerging from the many studies conducted can be summarized as follows: “Concern about Bt plants is that increased levels of insecticidal Cry proteins in soil could damage beneficial organisms, such as earthworms, collembolans, nematodes, and microorganisms, necessary for plant and soil health, litter decomposition, and nutrient cycling. In general, the Cry proteins released in root exudates and from plant residues of Bt crops appear to have no consistent, significant, and long-­term effects on the microbiota and their activities in soil” (Icoz and Stotzky 2008). Evolution of Resistance Experience with the deployment of traditional chemical pesticides throughout the world has shown that under the selection pressure exerted by the application of these pesticides, resistance will eventually develop (Georghiou and Lagunes-­Tejeda 1991). Increasing resistance of Helicoverpa armigera to insecticides had become a major problem and threatened cotton production in China (Wu et al. 1997). India, Australia, Indonesia, and Thailand have experienced similar problems (Kranthi et al. 2002; Srinivas et al. 2004) The resistance of this pest to insecticides was a major reason for introducing Bt cotton in China (Wu et al. 2002; Wu, Guo, et al. 2003; Wu and Guo 2003). Similarly, years of intensive application of pyrethroid and organophosphate insecticides in West Africa has also led to the evolution of resistance to those insecticides by H. armigera (Martin et al. 2000; Alvao 2006), thus generating the need for

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alternative control strategies such as Bt crops. Consequently, one might expect that because of the extensive deployment of Bt or herbicide-­resistant crops, evolution of resistance will occur. Studies designed to monitor for resistance in areas intensively planted with Bt crops have indicated that resistance has not become a problem yet, probably due at least in part to the implementation of resistance management policies (Tabashnik et al. 2003; Sisterson et al. 2005; Bates et al. 2005; Tabashnik et al. 2009). However, three reports have indicated that there has been an increase of resistance in field populations of some target pests. One study in South Africa has shown that larvae of Busseola fusca isolated from some field populations are able to survive in the presence of Bt maize (event MON810), although without detrimental effect on growth rate (Kruger et al. 2009). In Puerto Rico, performance failures of event TC1507 maize were determined by the U.S.  Environmental Protection Agency to be the result of resistant fall armyworm (Spodoptera frugiperda) (Matten et al. 2008). In the former case, there has been no withdrawal of the MON810 product from the South African market, and Bt maize continued to be planted from the time of the report in 2004–­2005 until the present. In the latter case, sales of TC1507 were suspended in Puerto Rico in accordance with the resistance management plan, but the EPA determined that the risk of resistance was lower in the continental United States (Matten et al. 2008). Also in the United States, there is evidence that Helicoverpa zea resistance to the Bt protein, Cry1Ac, has increased, although this has not led to widespread crop failures (Tabashnik et al. 2009). These results show that, as with other insect control measures, the evolution of resistance is a potential problem that must continue to be managed. In contrast there have been several reports of the emergence of glyphosate-­resistant weeds in recent years (Duke and Powles 2008a; Service 2007). Given the great value of this product for weed control and the highly benign environmental profile, emerging resistance to this herbicide, and possible resultant loss of its usefulness, is an important environmental and food production concern (Duke and Powles 2008a). Emerging resistance to glyphosate was the subject of an international symposium in March 2007. Documented cases of glyphosate-­ resistant weeds have been reported at an increasing rate in recent years, corresponding with the increased adoption of GE herbicide-­resistant crops (Duke and Powles 2008b).

Conclusion

The area planted with transgenic crops has increased rapidly over the decade since they were first deployed commercially. Experience has been gained with these crops in several countries, which allows us to examine concerns about their potential negative environmental impacts. To date, there have been no scientifically documented cases of negative impact on the environment, even while research into these potential impacts remains an active area of science. Potential loss of current benign pest control measures (e.g., Bt, glyphosate) due to overuse, which in turn could lead to increased use of less environmentally safe controls, underscores the importance of responsible use of these products. At the same time, there is an accumulating body of scientific literature that documents the realization of some of the hoped-­for benefits to the environment, including reduced pesticide use, reduced pest pressure, and greater biodiversity than in sprayed fields. Additional benefits include the increased adoption of reduced till cultivation practices and reduced mycotoxin contamination of corn grain. While these

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benefits may vary in magnitude and may not be realized in all geographies and agricultural systems, the overall impact of the cultivation of genetically engineered crops currently in production seems to be a positive one.

Note Portions of this chapter were previously submitted as an unpublished report to the World Bank and are used with permission.

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References Abate, T., A. van Huis, and J. Ampofo. 2000. Pest management strategies in traditional agriculture: An African perspective. Annu. Rev. Entomol. 45:631–­659. Alvao, T. 2006. Biological control agents and environmentally-­friendly compounds for the integrated management of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) on cotton: Perspectives for pyrethroid resistance management in West Africa. Arch. Phytopathol. Plant Prot. 39:105–­111. Bambawale, O., A. Singh, O. Sharma, B. Bhosle, R. Lavekar, A. Dhandapani, V. Kanwar, R. Tanwar, K. Rathod, N. Patange, and V. Pawar. 2004. Performance of Bt cotton (MECH-­162) under integrated pest management in farmers’ participatory field trial in Nanded district, central India. Curr. Sci. 86:1628–­1633. Bates, S., J. Zhao, R. Roush, and A. Shelton. 2005. Insect resistance management in GM crops: Past, present and future. Nat. Biotechnol. 23:57–­62. Biotechnology Industry Organization. 2010. Commercial status of certain agricultural biotechnology products as of June 25, 2010. http://www.biotradestatus.com/default.cfm. Bossdorf, O., D.  Prati, H.  Auge, and B.  Schmid. 2004. Reduced competitive ability in an invasive plant. Ecol. Lett. 7:346–­353. Boyer, J. S. 1982. Plant productivity and environment. Science 218:443–­448. Brookes, G., and P. Barfoot. 2006. Global impact of biotech crops: Socio-­economic and environmental effects in the first ten years of commercial use. AgBioForum 9:139–­151. ———. 2008. Global impact of biotech crops: Socio-­economic and environmental effects, 1996–­ 2006. AgBioForum 11:21–­38. Buckley, D., and T. M. Schmidt. 2001. The structure of microbial communities in soil and the lasting impact of cultivation. Microb. Ecol. 42:11–­21. Butler, S., J. Vickery, and K. Norris. 2007. Farmland biodiversity and the footprint of agriculture. Science 315:381–­384. Cattaneo, M., C. Yafuso, C. Schmidt, C. Huang, M. Rahman, C. Olson, C. Ellers-­Kirk, B. Orr, S. Marsh, L. Antilla, P. Dutilleul, and Y. Carrière. 2006. Farm-­scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use, and yield. Proc. Nat. Acad. Sci. U.S.A. 103:7571–­7576. Center for Environmental Risk Assessment. N.d. GM Crop Database. http://cera-gmc.org/index .php?action=gm_crop_database. Cerdeira, A. L., and S. O. Duke. 2006. The current status and environmental impacts of glyphosate-­ resistant crops. J. Environ. Qual. 35:1633–­1658.

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42    Hector Quemada

Clegg, C., R. Lovell, and P. Hobbs. 2003. The impact of grassland management regime on the community structure of selected bacterial groups in soils. FEMS Microbiol. Ecol. 43:263–­270. Conner, A., T. Glare, and J. Nap. 2003. The release of genetically modified crops into the environment: Part II. Overview of ecological risk assessment. Plant J. 33:19–­46. Crawley, M., R. Hails, M. Rees, D. Kohn, and J. Buxton. 1993. Ecology of transgenic oilseed rape in natural habitats. Nature 363:620–­623. Dale, P., B. Clarke, and E. Fontes. 2002. Potential for the environmental impact of transgenic crops. Nat. Biotechnol. 20:567–­574. Dalmacio, S., T. Lugod, E. Serrano, and G. Munkvold. 2007. Reduced incidence of bacterial rot on transgenic insect-­resistant maize in the Philippines. Plant Dis. 91:346–­351. Duan, J. J., M. Marvier, J. Huesing, G. Dively, and Z. Y. Huang. 2008. A meta-­analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS One 3 (1): e1415. Doi:10.1371/journal.pone.0001415. Duke, S. O., and S. B. Powles. 2008a. Glyphosate resistant weeds and crops. Pest Manag. Sci. 64:317. ———. 2008b. Glyphosate: A once-­in-­a-­century herbicide. Pest Manag. Sci. 64:319–­325. Dunfield, K., and J. J. Germida. 2001. Diversity of bacterial communities in the rhizosphere and root interior of field-­grown genetically modified Brassica napus. FEMS Microbiol. Ecol. 82:1–­9. ———. 2004. Impact of genetically modified crops on soil-­and plant-­associated microbial communities. J. Environ. Qual. 33:806–­815. Fawcett, R., and D.  Towery. 2002. Conservation tillage and plant biotechnology: How new technologies can improve the environment by reducing the need to plow. Conservation Technology Information Center, West Lafayette, IN. Fuchs, M. 2008. Transgenic plants and control of virus diseases: State of the art and prospects. Virologie 12:27–­37. Fukuda-­Parr, S. 2007. The Gene Revolution: GM Crops and Unequal Development. Sterling, VA: Earthscan. Georghiou, G., and A. Lagunes-­Tejeda. 1991. The occurrence of resistance to pesticides in arthropods. Food and Agriculture Organization of the United Nations, Rhone, Switzerland. Gill, S. S., E. A. Cowles, and P. V. Pietrantonio. 1992. The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 37:615–­636. Griffiths, B., I. Geoghegan, and W. Robertson. 2000. Testing genetically engineered potato, producing the lectins GNA and Con A, on non-­target soil organisms and processes. J. Appl. Ecol. 37:159–­170. Grumet, R. 2002. Plant biotechnology in the field—­a snapshot with emphasis on horticultural crops. HortScience 37:435–­436. Grumet, R., and T. Lanina-­Zlatkina. 1996. Molecular approaches to biological control of virus diseases of plants. In Molecular Biology of Biological Control of Pests and Diseases of plants, ed. M. Gunasekaranand and D. J. Weber. Boca Raton, FL: CRC Press. Pp. 15–­36. Gyamfi, S., U.  Pfeifer, M.  Stierschneider, and A.  Sessitsch. 2002. Effects of transgenic glufosinate-­ tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. FEMS Microbiol. Ecol. 41:181–­190. Hails, R. 2002. Assessing the risks associated with new agricultural practices. Nature 418:685–­688. Heuer, H., R. Kroppenstedt, J. Lottmann, G. Berg, and K. Smalla. 2002. Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl. Environ. Microbiol. 68:1325–­1335. Heuer, H., and K. Smalla. 1999. Bacterial phyllosphere communities of Solanum tuberosum L. and T4-­ lysozyme-­producing transgenic variants. FEMS Microbiol. Ecol. 28:357–­371. Hossain, F., C. Pray, Y. Lu, J. Huang, C. Fan, and R. Hu. 2004. Genetically modified cotton and farmers’ health in China. Int. J. Occup. Environ. Health 10:296–­303

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GE Crops and Environmental Impacts    43

Huang, J., R. Hu, C. Fan, C. Pray, and S. Rozelle. 2002. Bt cotton benefits, costs, and impacts in China. AgBioForum 5:153–­166. Huang, J., R. Hu, S. Rozelle, and C. Pray. 2005. Insect-­resistant GM rice in farmers’ fields: Assessing productivity and health effects in China. Science 308:688–­690. Icoz, I., and G. Stotzky. 2008. Fate and effects of insect-­resistant Bt crops in soil ecosystems. Soil Biol. Biochem. 40:559–­586. James, C. 2006. Global status of commercialized biotech/GM crops: 2006. International Service for the Acquisition of Agri-­biotech Applications, ISAAA Brief No. 35. http://www.isaaa.org/resources/ publications/briefs/35/default.html. ———. 2009. Global status of commercialized biotech/GM crops: 2009. International Service for the Acquisition of Agri-­biotech Applications, ISAAA Brief No. 41. http://www.isaaa.org/resources/ publications/briefs/41/executivesummary/default.asp. Kowalchuk, G., M. Bruinsma, and J. van Veen. 2003. Assessing responses of soil microorganisms to GM plants. Trends Ecol. Evol. 18:403–­410. Kranthi, K., D. Russell, R. Wanjari, M. Kherde, S. Munje, N. Lavhe, and N. Armes. 2002. In-­season changes in resistance to insecticides in Helicoverpa armigera (Lepidoptera: Noctuidae) in India. J. Econ. Entomol. 95:134–­142. Kruger, M., J. B. J. van Rensburg, and J. van den Berg. 2009. Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot. 28:684–­689. Lottmann, J., and G. Berg. 2001. Phenotypic and genotypic characterization of antagonistic bacteria associated with roots of transgenic and non-­transgenic potato plants. Microbiol. Res. 56:75–­82. Lukow, T., P. Dunfield, and W. Liesack. 2000. Use of T-­RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-­transgenic potato plants. FEMS Microbiol. Ecol. 32:241–­247. Martin, T., G. Ochou, F. Hala-­N’Klo, J. Vassal, and M. Vaissayre. 2000. Pyrethroid resistance in the cotton bollworm, Helicoverpa armigera (Hubner), in West Africa. Pest Manag. Sci. 56:549–­554. Marvier, M., C. McCreedy, J. Regetz and P. Kareiva. 2007. A meta-­analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–­1477. Matten, S. R., G. P. Head, and H. D. Quemada. 2008. How governmental regulation can help or hinder the integration of Bt crops within IPM programs. In Integration of Insect-­Resistant Genetically Modified Crops within IPM Programs, ed. J. Romeis, A. M. Shelton, and G. G. Kennedy. Berlin: Springer Science and Business Media. Pp. 27–­39. McLaughlin, A., and P. Mineau. 1995. The impact of agricultural practices on biodiversity. Agric. Ecosyst. Environ. 55:201–­212. Munkvold, G., R. Hellmich, and L. Rice. 1999. Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and nontransgenic hybrids. Plant Dis. 83:130–­138. OECD (Organisation for Economic Cooperation and Development, Paris). 1993. Safety considerations for biotechnology: scale-­up of crop plants. http://www.oecd.org/dataoecd/26/26/1958527.pdf?ch annelld=34537&homeChannelld=33703&fileTitle=Safety+Considerations+for+Biotechnology +Scale-up+of+Crop+Plants. Pimentel, D. 1998. Economic benefits of natural biota. Ecol. Econ. 25:45–­47. Pray, C., J. Huang, R. Hu, and S. Rozelle. 2002. Five years of Bt cotton in China—­the benefits continue. Plant J. 31:423–­430. Quemada, H., L. Strehlow, D. S. Decker-­Walters, and J. E. Staub. 2008. Population size and incidence of virus infection in free-­living populations of Cucurbita pepo. Environ. Biosaf. Res. 7:185–­196.

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44    Hector Quemada

Raney, T. 2006. Economic impact of transgenic crops in developing countries. Curr. Opin. Biotechnol. 17:1–­5 Raybould, A., and I. Cooper. 2005. Tiered tests to assess the environmental risk of fitness changes in hybrids between transgenic crops and wild relatives: The example of virus resistant Brassica napus. Environ. Biosaf. Res. 4:127–­140. Robinson, R., and W. Sutherland. 2002. Post-­war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39:157–­176. Romeis, J., D.  Bartsch, F.  Bigler, M.  P.  Candolfi, M.  P.  C.  Gielkens, S.  Hartley, R.  L.  Hellmich, J.  E.  Huesing, P.  C.  Jepson, R.  Layton, H.  Quemada, A.  Raybould, R.  I.  Rose, J.  Schiemann, M.  K.  Sears, A.  M. Shelton, J.  Sweet, Z.  Vaituzis, and J.  D.  Wolt. 2008. Assessment of risk of insect-­resistant transgenic crops to nontarget arthropods. Nat. Biotechnol. 26:203–­208. Sahora, M.  K., P.  Sridhar, and V.  S.  Malik. 1998. Glyphosate-­tolerant crops: Genes and enzymes. J. Plant Biochem. Biotech. 7:65–­72. Sankula, S., and J.  Carpenter. 2006. Comparative environmental impacts of biotechnology-­derived and conventional soybean. Council for Agricultural Science and Technology. http.cast-science.org. Sanvido, O., J. Romeis, and F. Bigler. 2007. Ecological impacts of genetically modified crops: Ten years of field research and commercial cultivation. Adv. Biochem. Eng./Biotechnol. 107:235–­278. Schnepf, E., N.  Crickmore, J.  Van Rie, D.  Lereclus, J.  Baum, J.  Feitelson, D.  R.  Zeigler, and D. H. Dean. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Molec. Biol. Rev. 62:775–­806. Service, R. 2007. A growing threat down on the farm. Science 316:1114—­1117. Sisterson, M.  S., Y.  Carrière, T.  J.  Dennehy, and B.  E.  Tabashnik. 2005. Evolution of resistance to transgenic crops: Interactions between insect movement and field distribution. J. Econ. Entomol. 98:1751–­1762. Snow, A., B. Andersen, and R. Jorgensen. 1999. Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa. Mol. Ecol. 8:605–­615. Snow, A., D. Andow, P. Gepts, E. Hallerman, A. Power, J. Tiedje, and L. Wolfenbarger. 2005. Genetically engineered organisms and the environment: Current status and recommendations. Ecol. Appl. 15:377–­404. Snow, A., P.  Moran-­Palma, L.  Rieseberg, A.  Wszelaki, and G.  Seiler. 1998. Fecundity, phenology, and seed dormancy of F1 crop hybrids in sunflower (Helianthus annuus, Asteraceae). Am. J. Bot. 85:794–­801. Snow, A., D. Pilson, L. Riesberg, M. Paulsen, and S. Selbo. 2003. A Bt transgene reduces herbivory and enhances fecundity in wild sunflower. BioScience 13:279–­286. Srinivas, R., S. Udikeri, S. Jayalakshmi, and K. Sreeramulu. 2004. Identification of factors responsible for insecticide resistance in Helicoverpa armigera. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 137:261–­269. Stoate, C., N. Boatman, R. Borralho, C. Carvalho, G. de Snoo, and P. Eden. 2001. Ecological impacts of arable intensification in Europe. J. Environ. Manag. 63:337–­365. Strange, R., and P. Scott. 2005. Plant disease: A threat to global food security. Annu. Rev. Phytopathol. 43:83–­116. Tabashnik, B.  E., Y.  Carrière, T.  Dennehy, S.  Morin, M.  Sisterson, R.  Roush, A.  Shelton, and J.-­Z. Zhao. 2003. Insect resistance to transgenic Bt crops: Lessons from the laboratory and field. J. Econ. Entomol. 96:1031–­1038. Tabashnik, B. E., J. B. J. van Rensburg, and Y. Carrière. 2009. Field-­evolved insect resistance to Bt crops: Definition, theory and data. J. Econ. Entomol. 102:2011–­2025.

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GE Crops and Environmental Impacts    45

Tilman, D. 1999. Global environmental impacts of agricultural expansion: The need for sustainable and efficient practices. Proc. Nat. Acad. Sci U.S.A. 96:5995–­6000. Tilman, D., K. Cassman, P. Matson, R. Naylor, and S. Polasky. 2002. Agricultural sustainability and intensive production practices. Nature 418:671–­677. Trewavas, A. 2001. The population/biodiversity paradox: Agricultural efficiency to save wilderness. Plant Physiol. 125:174–­179. Trigo, E., and E. Cap. 2003. The impact of the introduction of transgenic crops in Argentinean agriculture. AgBioForum 6:87–­94. Wang, S., D. Just, and P. Pinstrup Andersen. 2006. Tarnishing silver bullets: Bt technology adoption, bounded rationality and the outbreak of secondary pest infestations in China. Paper prepared for presentation at the American Agricultural Economics Association Annual Meeting, Long Beach, CA, July 22–­26. Warwick, S., A.  Légère, M.  Imard, and T.  James. 2008. Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population. Mol. Ecol. 17:1387–­1395 Watrud, L., E. Lee, A. Fairbrother, C. Burdick, J. Reichman, M. Bollman, M. Storm, G. King, and P. Van de Water. 2004. Evidence for landscape-­level, pollen-­mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc. Nat. Acad. Sci. U.S.A. 101:14533–­14538. Whitehouse, M., L. Wilson, and G. Fitt. 2005. A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environ. Entomol. 34:1224–­1241. Wolfenbarger, L.  L., S.  E.  Naranjo, J.  G.  Lundgren, R.  J.  Bitzer, and L.  S.  Watrud. 2008. Bt crop effects on functional guilds of non-­target arthropods: A meta-­analysis. PLoS One 3 (5): e2118. Doi:10.1371/journal.pone.0002118. Wu, K., and Y.  Guo. 2003. Influences of Bacillus thuringiensis Berliner cotton planting on population dynamics of the cotton aphid, Aphis gossypii Glover, in northern China. Environ. Entomol. 32:312–­318. Wu, K., Y. Guo, L. Nan, J. Greenplate, and R. Deaton. 2003. Efficacy of transgenic cotton containing a cry1Ac gene from Bacillus thuringiensis against Helicoverpa armigera (Lepidoptera: Noctuidae) in northern China. J. Econ. Entomol. 96:1322–­1328. Wu, K., W.  Li, H.  Feng, and Y.  Guo. 2002. Seasonal abundance of the mirids, Lygus lucorum and Adelphicoris spp. (Hemiptera: Miridae) on Bt cotton in northern China. Crop Prot. 21:997–­1002. Wu, K., G. Liang, and Y. Guo. 1997. Phoxim resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in China. J. Econ. Entomol. 90:868–­872. Wu, K. M., Y. H. Lu, H. Q. Feng, Y. Y. Jiang, and J. Z. Zhao. 2008. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-­containing cotton. Science 321:1676–­1678. Wu, K., Y. Peng, and S. Jia. 2003. What we have learnt on impacts of Bt cotton on non-­target organisms in China. AgBiotechNet 5:1–­4 Young, B.  G. 2006. Change in herbicide use patterns and production practices resulting from glyphorate-­resistant crops. Weed Technol. 20:301–­307.

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Future Possible Genetically Engineered Crops and Traits and Their Potential Environmental Impacts Rebecca Grumet, L aReesa Wolfenbarger, and Alejandra Ferenczi

The “first wave” of genetically engineered (GE) crops was focused nearly exclusively on very high acreage crops and a handful of readily cloned, highly effective genes conferring insect resistance and herbicide tolerance (table 1). There were also a few instances of genetically engineered virus resistance in squash and papaya, but together they have accounted for less than 0.1% of transgenic acreage (Brookes and Barfoot 2006; James 2006). Table 1. Genetically Engineered (GE) Crops Produced during the First Decade of Commercial GE Crop Production, 1996–­2006

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Crop

% GE crop production

Trait

First year of production

Soybean

62%

Herbicide resistance

1996

Corn

22%

Insect resistance

1996

Herbicide resistance

1997

Insect resistance

1996

Herbicide resistance

1997

Herbicide resistance

1996

Potato

Insect resistance

1996–­2000*

Cotton Canola

11% 5%

Low-­acreage crops Alfalfa

Herbicide resistance

2006

Papaya

Virus resistance

1999

Squash

Virus resistance

1996

Sources: James 2007; Brookes and Barfoot 2006. * The GE potato was only produced for a short period of time before it was removed from the market. 47

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48    Grumet, Wolfenbarger, and Ferenczi

The next decade of GE crops promises to bring a host of new crops, genes, traits, and locations, and with it, a broader range of environmental safety questions. The increase in variety is due to continually more sophisticated molecular genetic and genomic technologies that have expanded our ability to obtain new genes of value, and an increasing number of public-­and private-­sector groups developing GE crops in both developed and developing countries. In some cases we will see use of familiar genes in new crops, such as herbicide resistance in sugar beet in the United States and Bt genes in eggplant (brinjal), which is undergoing development in India, Bangladesh, and the Philippines (Ramanujan 2007). In other cases, there will be new kinds of genes and traits in previously engineered crops, such as enhanced drought stress resistance in corn, or combinations of new genes and new GE crops, such as pro-­vitamin A enhanced rice. Examples of new crops and traits in development, based on recorded field trials in the United States in 2007, are summarized in tables 2 and 3. Similarly expanded lists of crops and traits are also being developed in other locations. For example, Argentina has more than 140 transgenic events under evaluation, including crops engineered with new traits such as drought tolerance and modified oil content (table 4). Environmental safety considerations for GE crops vary with crop, gene, trait, and location and result from a complex interplay of each of the factors (figure 1). For example, modified nutritional content is less likely to provide a selective advantage to the crop or interfertile relative than is increased drought stress tolerance. In addition, the same gene or trait may have different potential impacts in different crops, depending on outcrossing rates of the crop, weediness of compatible relatives, or possible interaction with other traits in the crop that may lead to enhanced competitiveness of the crop in the wild (Hancock 2003). As mentioned in previous chapters, a given trait-­crop combination could have different potential impacts in

Table 2. Permits and Acknowledgments for Crops or Species Tested in Field Trials in the United States in 2007

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More than 10 trials Corn Soybean Cotton Loblolly pine Alfalfa Tobacco Potato Rapeseed Poplar Tomato Wheat Eucalyptus

No. Trials 255 141 48 27 24 23 19 19 15 11 11 11

Other crops/species (no. trials) Commodity and subsistence crops Barley (8), cassava (6), rice (6), sugarcane (6), peanut (5), safflower (4), sugarbeet (4), sorghum (3), cowpea (1), drybean (1), guayule (1), sweetpotato (1) Fruits, vegetables Grape (9), apple (5), grapefruit (5), papaya (3), plum (2), banana (1), melon (1), onion (1) Trees and shrubs Cottonwood (9), aspen (2), chestnut (2), sweetgum (2), walnut (1) Grasses Bahia grass (1), bent grass (1), Bermuda grass (1) Ornamentals Antherium (2), camelia (2), marigold (1), rose (1)

Source: USDA-­APHIS records, http://www.nbiap.vt.edu.

Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

1

Reduced nicotine

14

345 267 22 43 10 59 8 11 57 10 24 2 3 9 5 8 13 13 33 21 18

2001

-­

80 97 19 4 11 -­ -­ -­ 5 -­ 5 -­ 1 -­ 1 -­ 2 -­ 2 -­ -­

2007

1

24 43 1 1 -­ -­ -­ -­ 3 -­ 4 -­ 2 -­ -­ -­ -­ -­ -­ 3 -­

2001

Trials in Argentina

Modified nutrition Vitamins (5), flavenoids (3), iron (2), zinc (1)

Other abiotic stress resistances Heat (5), salt (4 U.S., 1 Argentina)

Other biotic stress resistances Nematode resistance (9)

Product quality Altered lignin (8), reduced polyphenols (7), color/ pigment (6), flavor (3), fiber quality (2), digestibility (1), modified sorbitol (1), reduced cyanogenesis (1), high antioxidants (1, Argentina), increased α amylase (3, Argentina)

Other traits tested in the U.S. (and Argentina) in 2007

Sources: Data are from USDA-­APHIS http://www.nbiap.vt.edu/data.aspx or http://www.nbiap.vt.edu and SAGPyA-CONABIA http://www.minagri .gob.ar/SAGPyA/areas/biotecnologia/.

317 278 85 72 72 58 44 43 29 28 25 18 17 15 13 11 10 10 9 7 3

Insect resistance Herbicide tolerance Modified oil composition/content Yield Drought Fungal resistance Modified growth rate Morphology/development Virus resistance Seed composition Amino acid composition Cold resistance General abiotic stress resistance Bacterial resistance Nitrogen utilization Fruit development Feed properties Fertility Modified carbohydrates Increased protein Pharmaceutical products

2007

More than 10 trials in the U.S.

Table 3. Types of Traits Tested in Field Trials of Transgenic Plants in the United States (permits and acknowledgments issued) and Argentina in 2007 and 2001

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50

Grumet, Wolfenbarger, and Ferenczi

Million hectares

% worldwide GE production

54.6

53.5

ustralia

olumbia

18.0

17.6

zech epublic

rance

11.5

11.3

6.1

5.9

ran

3.8

3.7

araguay

hina

3.5

3.4

araguay

2.0

2.0

South frica

1.4

1.4

Total

102

M

ortugal

P

A

C F

Honduras exico

Slovakia

R

ndia

A

P

C

I

C

anada

Germany R

Brazil

C

A

rgentina

I

United States

Countries producing less than 1%

P

Primary producers

P

T

able 4. Countries Producing GE Crops in 2006

hilippines omania Spain

Uruguay

Source: James 2007.

­

­

Environmental Safety of Genetically Engineered Crops, Michigan State University Press, 2011. ProQuest Ebook Central,

A

I

T

different locations, depending on the environmental conditions influencing selective advantage of the introduced trait, and presence or absence of compatible wild relatives to allow for potential gene transfer. his complex interplay of factors necessitates a case-by-case assessment of potential impacts based on the specific intended conditions of use. Ultimately, the key questions center on the following: Will this trait allow the crop to be produced in new environments? f so, will the crop become invasive? re there compatible wild relatives of the crop in the region where the crop is being planted, and if so, will the gene confer a selective advantage that could influence wild populations? Will there be nontarget impacts of the new trait? his chapter will examine some of the new locations, crops, genes, and traits expected to be deployed in the years to come. T

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Figure 1. Environmental safety considerations for GE crops result from a complex interplay of factors that vary with crop, gene, trait, and location.

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Future Crops and Traits

51

s

L

ver the past decade the number of countries producing transgenic crops has steadily increased. By 2007, 23 countries were producing transgenic crops (figure 2; table 4), including the main world producers and exporters of commodities such as soybean and corn (James 2007). his number is likely to continue to rise in the next decade in cases where this technology offers an advantage in solving specific local economic, commercial, or production problems. ncreasing numbers of countries that have not yet commercialized GE crops, such as the frican nations of Ghana, Kenya, alawi, anzania, Uganda, and Zimbabwe, have reported field trials of GE crops ( -Bio e 2008). he use of GE crop technology in one country may influence the decision of other countries to try such technologies. Success of a crop or trait in one country may drive interest in a neighboring country, as has been observed for rgentina and Brazil and ndia and akistan (Hodgson 1999; Qaim and raxler 2005; Ur ehman 2007). Where there are families with relatives residing in adjacent countries, as is the case in many frican countries, the technology may cross borders casually as a result of normal interchange of products (Eicher et al. 2006). Biosafety frameworks, which are a prerequisite for possible use of GE crops by the 143 countries that have ratified the artagena rotocol, are under development or have been completed in 132 countries in frica, sia, atin merica, and entral and Eastern Europe (U E GE 2006). While the ultimate decision to use or not use GE crops in a given country or region will result from a combination of technical, agronomic, economic, and sociopolitical T

C

D

­

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P

I

­

P

N

C

A

P

L

A

F

A

C

A

R

T

A

T

FAO

M

A

I

T

O

New

ocation

Figure 2. Countries with commercial production of GE crops as of 2007. Shading indicates GE crop production; the accompanying number indicates years of production. Countries that have planted for a few years then discontinued production (e.g., Bulgaria, Indonesia) are not shaded. Data are from derived from http://www.isaaa.org/resources/publications/ briefs/default.html.

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52    Grumet, Wolfenbarger, and Ferenczi

factors, as the number of countries that produce GE crops increases, so does the number and variety of environments into which the crops are introduced. Since environmental risk assessment is, by definition, location (i.e., environment) specific, factors to be considered include the nature of the ecosystem into which these crops will be introduced; whether it is an introduction of a new crop and cropping system (rather than a new cultivar of a currently grown crop); and the presence or absence of wild relatives for possible gene exchange. The presence of wild relatives may become a greater issue in the case where there is already an aggressive, compatible relative weed, such as occurs for sorghum in Africa (Arriola and Elstrand 1996). One possible aspect of GE crops that has not arisen to a large extent yet with the current GE crops and locations, is introduction of the crops into centers of origin of the species. Examples where this will be highly relevant are maize in Mexico, potatoes in Latin America, and rice in Southeast Asia. The concerns center on possible loss of diversity of wild, indigenous populations through genetic exchange with the GE crops (Chapman and Burke 2006; Conner et al. 2003). This possibility is explored more fully by Hancock (this volume) with respect to the factors influencing crop / wild progenitor hybridization and gene exchange; fitness effect on gene persistence and spread; and influence of relative population sizes. Hybridization has occurred between conventionally bred crops and wild relatives (Ellstrand et al. 1999), demonstrating that hybridization between GE crops and conventional cultivars and wild relatives is likely where they co-­occur. Documented environmental impacts of hybridization are less common and are not necessarily a consequence of hybridization. A challenge for biosafety assessments will be determining which new genes and traits in GE crops may increase the frequency or impacts of crop/progenitor hybridizations.

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New Crops

The number of genetically engineered crops that are being produced commercially remains very small (table 1). A combination of technical, economic, and social factors have influenced which crops are being produced. The costs of technical development, intellectual property rights (IPR), and regulatory controls are collectively so high (tens of millions of U.S. dollars per crop gene combination; Bradford et al. 2005; Falck-­Zepeda and Zambrano 2008), that typically only high-­acreage crops have been chosen for development in order to recoup investments. With very few exceptions (e.g., papaya ringspot-­resistant papaya; plum pox-­resistant plum), GE crops have been released for commercial production by large corporations with the assets to invest in production, IPR, and regulatory costs. In some cases, high-­acreage crops such as wheat or potatoes have reached the stage of development and regulatory approval that would allow for commercialization, but were either removed from the market after a very short period of time (e.g., NewLeaf potato) or prevented from going to market (e.g., herbicide-­resistant wheat) in response to marketing concerns or pressure from consumer or environmental organizations (Stokstad 2004; Thornton 2003). It will remain to be seen in the next decade which crops will reach the market, both in developed and in developing countries. Public-­sector efforts at various stages of development throughout the world include many important food security crops such as cassava, sweet potato, potato, cowpea, groundnut, banana, plantain, millet, rice, sorghum, and wheat

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Future Crops and Traits    53

(Cohen 2005). There have been a small number of field trials of several of these crops in the United States (table 3). Other research programs have targeted fruits and vegetables such as apple, citrus, grape, mango, plum, strawberry, cabbage, cucumber, eggplant, melons, peppers, squash, tomato, or commodity crops such as cotton, sugarcane, cacao, and coffee (Thompson 2004; Cohen 2005). In addition to the potential for new GE food crops is the potential for production of new kinds of genetically engineered nonfood crops for purposes of pharmaceutical production and industrial production of biofuels, wood pulp, oils, and starches (McKeon 2003). Nonfood crops are being considered as an option for pharmaceuticals to reduce the risk of inadvertent mixing of pharmaceutical crops with crops destined for food purposes (Mascia and Flavell 2004). The emerging demand for biofuel has generated research effort in species such as switchgrass, miscanthus, poplar, willow, and eucalyptus (Sims et al. 2006). Several GE tree species are under development, including loblolly pine, poplar, and eucalyptus, which were each included in at least 10 field trials in the United States in 2007 (table 2). Depending on the nature of the nonfood products, possible nontarget effects may become a more important consideration for evaluation of environmental safety. How the biosafety concerns of pharmaceutical crops will be handled is a question still in its infancy. Because of the nature of the product, the very small acreages needed to produce sufficient supplies, and the potential health risks, most recommendations call for these crops to be produced in highly isolated and contained situations (e.g., Mascia and Flavell 2004). In contrast, if biofuel production becomes an important component of energy plans, there is potential for very large-­scale production of the feedstock plant material, which could require different sorts of environmental biosafety precautions, depending on the nature of the gene products. Some of the species (e.g., switchgrass, eucalyptus) being considered for these purposes also are not as highly domesticated as our typical food crops, and may have greater propensity to become feral or invasive (Raghu et al. 2006). These types of production systems may require reevaluation of the current guidelines to be sure that they provide the necessary environmental protection. Clearly, as has been a topic of much discussion, widespread conversion to production of biofuel crops introduces many environmental safety issues in terms of land use and impacts, of which possible transgenic use is just one component. Furthermore, production of new crops or species will likely result in new locations for GE crop production, either in countries that currently grow GE crops or in new countries for which these new crops are important. Thus, the production of new crops is not isolated from the question of new locations and the associated assessment of environmental risk.

New Traits

The preceding discussion of new crops already has raised the question of new traits, especially with regard to pharmaceutical and biofuel production. Even for food crops, or conventional nonfood crops (e.g., cotton), many new types of traits are under development. Despite the continued dominance of insect resistance and herbicide tolerance traits, other categories that are receiving a good deal of attention are product quality (e.g., modified oils, seed composition, amino acid composition, feed properties, carbohydrates and proteins; 184 field trails in 2007); increased or modified yield, growth, and morphology (180 field trials in 2007); and

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54    Grumet, Wolfenbarger, and Ferenczi

disease resistance (112 field trials in 2007). The most dramatic increase in numbers of field trials in the United States in recent years has been in the area of abiotic stress tolerance, especially drought resistance. More than 115 field trials tested for resistances to drought, cold, heat, and salt in 2007, versus only 23 in 2001. From the standpoint of assessing environmental risks, those most likely to be of concern are those that provide the greatest selective advantage, or increase the potential to colonize new areas or become invasive. Morphology and growth changes could influence these characters, depending on the nature of the trait. Introduced changes are typically targeted to increased suitability for crop or managed forest production (e.g., dwarfing or earlier flowering) or product quality (e.g. reduced lignin) and so, in many cases, may be disadvantageous in wild settings. Resistances to biotic and abiotic stresses, however, are likely to be advantageous. Disease resistances could confer an advantage to wild populations if the disease is currently a limiting factor for spread of that population. Since disease pressures are often very different between intense agricultural production systems and wild populations, whether or not the resistance is a significant selective advantage in the wild will need to be determined on a case-­ by-­case basis. The area of abiotic stress resistances probably poses the most new questions, as it is conceivable that traits such as frost or salt tolerance could allow a crop or wild relative to grow in areas that it could not previously colonize. These traits raise questions of potential invasiveness. Because equivalent types of traits (disease resistance, stress resistance) have been, or are being, introduced by conventional breeding, we may be able to use information about the impact of these efforts to assess the environmental safety of genetically engineered traits. .

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New Genes

Many of the new types of traits that are being developed arise from different kinds of genes than were used for the first wave of GE crops. Genes code for proteins. The proteins, in turn, can be directly useful (i.e., they are the desired end product) or, alternatively, can play subsequent functional roles to cause the desired end product, for example, abiotic stress resistance. The first wave of transgenic crops primary used genes whose protein product was directly responsible for the desired trait (e.g., Bt proteins confer insect resistance; herbicide resistance genes encode proteins that prevent binding of the herbicide or otherwise inactivate the herbicide; Carpenter et al. 2002). These protein products are largely inert with respect to other cellular functions. In contrast, the function of many of the newer genes being tested is to initiate other changes within the cell. They may cause the cell to produce needed compounds to survive, grow, and respond to the environment. Such genes may encode transcription factors that regulate expression of other genes; they may code for signaling factors that initiate response to perceived changes in the cellular environment; or they may produce metabolic pathway enzymes that result in the production of new cellular compounds. Examples include transcription factor genes that have been used to modulate floral development or abiotic stress resistance; signaling or hormonal factor genes that have been used to initiate responses to invading pathogens or modify fruit ripening; and metabolic pathway genes that have been used to modify oil, carbohydrate, or amino acid composition (Grumet 2003).

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Future Crops and Traits    55

As a result of their downstream actions, these types of genes would be expected to have broader effects on plant metabolism, physiology, and development than genes for which the protein itself is the final end product (Little et al. 2009). Indeed, it is the ability of these kinds of genes to initiate a cascade of effects that makes them highly valuable for genetic engineering. A single gene can achieve what might otherwise take dozens of genes. At the same time, however, altered expression of a broad range of genes via introduction of regulatory, signaling, or metabolic genes also has the potential to modify nontarget phenotypes within the plant through pleitrophic or epistatic interactions (Wolfenbarger and Grumet 2003; Little et al. 2009). These changes could, in turn, influence fitness or the probability of gene flow of the introduced trait. Environmentally prudent use of these sorts of genes will require careful analysis throughout the GE crop cycle and across the range of environments in which the GE crop will be deployed.

Conclusions

The promise of future genetically engineered crops will likely expand the number of locations, traits, genes, and species for which environmental assessments will be needed. The growing number of field tests for traits associated with increased stress resistance demonstrates the strong interest and progress in developing crops with these traits. Understanding when and how these traits in specific crops affect the potential for invasiveness and gene flow will ensure that these crops increase yield and are environmentally safe. To prepare for future environmental concerns, a synthesis of existing information and an identification of information needs will facilitate the assessment process. For example, where crops and wild relatives co-­occur, questions include what level of hybridization is likely and what impacts will occur as a result. Now is the time to integrate the process of environmental assessment so that development proceeds in concert with information on biosafety.

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Note The views expressed in this chapter are those of the authors and do not reflect the views of the Ministry of Livestock, Agriculture, and Fisheries of Uruguay or the School of Agronomy of the University of Uruguay.

References Arriola, P. E., and N. C. Ellstrand. 1996. Fitness of interspecific hybrids in the genus Sorghum: Persistence of crop genes in wild populations. Ecol. Appl. 7:512–­518. Bradford, K. J., A. Van Deynze, N. Gutterson, W. Parrot, and S. H. Strauss. 2005. Regulating transgenic crops sensibly: Lessons from plant breeding, biotechnology and genomics. Nat. Biotechnol. 23:439–­444.

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Brookes, G., and P. Barfoot. 2006. GM Crops: The First Ten Years—­Global Socio-­Economic and Environmental Impacts. International Service for the Acquisition of Agri-­biotech Applications, ISAAA Brief No. 36. http://www.isaaa.org/resources/publications/briefs/36/default.html. Carpenter, J., A.  Feliot, T.  Goode, M.  Hammig, D.  Oristad, and S.  Sankula. 2002. Comparative environmental impacts of biotechnology-­derived and traditional soybean, corn, and cotton crops. Council for Agricultural Science and Technology. http.cast-science.org. Chapman, M. A., and J. M. Burke. 2006. Letting the genie out of the bottle: The population genetics of genetically modified crops. New Phytol. 170:429–­443. Cohen, J. I. 2005. Poorer nations turn to publically developed GM crops. Nat. Biotechnol. 23:27–­33. Conner, A. J., T. R. Glare, and J. Nap. 2003. The release of genetically modified crops into the environment, Part II. Overview of ecological risk assessment. Plant J. 33:19–­46. Eicher, C. K., K. Maredia, and I. Sithole-­Niang. 2006. Crop biotechnology and the African farmer. Food Policy 31:504–­527. Ellstrand, N. C., H. C. Prentice, and J. F. Hancock. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst. 30:539–­563. Falck-­Zepeda, H. and P. Zambrano. 2008. Bio-­innovations and the economics of biosafety regulatory decision making in developing countries. FAO-­BioDeC. 2008. Biotechnologies in developing countries. http://www.fao.org/biotech/inventory _admin/dep/default.asp. Grumet, R. 2003. Introduction to Proceedings of a Workshop on Criteria for Field Testing of Plants with Engineered Regulatory, Metabolic, and Signaling Pathways, June 3–­4, 2002, ed. L. L. Wolfenbarger. Blacksburg, VA: Information Systems for Biotechnology. Pp. 15–­17. Hancock, J. F. 2003. A framework for assessing the risk of transgenic crops. BioScience 53:512–­519. Hodgson, J. 1999. GMO roundup. Nat. Biotechnol. 17:1047. James, C. 2006. GM crops: The first ten years—­global socioeconomic and environmental impacts. International Service for the Acquisition of Agri-­biotech Applications, ISAAA Brief No. 36. http:// www.isaaa.org/resources/publications/briefs/36/default.html ———. 2007. Global status of commercialized biotech/GM crops 2007. International Service for the Acquisition of Agri-­biotech Applications, ISAAA Brief No. 37. http://www.isaaa.org/resources/ publications/briefs/37/default.html. Little, H.  A., R.  Grumet, and J.  F.  Hancock. 2009. Modified ethylene signaling as an example of engineering for complex traits: Secondary effects and implications for risk assessment. HortScience 44:94–­101. Mascia, P. N., and R. B. Flavell. 2004. Safe and acceptable strategies for producing foreign molecules in plants. Curr. Opin. Plant Biol. 7:189–­195. McKeon, T. 2003. Genetically modified crops for industrial products and processes and their effects on human health. Trends Food Sci. Technol. 14: 229–­241. Qaim, M., and G. Traxler. 2005. Roundup Ready soybeans in Argentina: Farm level and aggregate welfare effects. Agric. Econ. 32:73–­86. Raghu, S., R.  C.  Anderson, C.  C.  Dachler, R.  S.  Davis, R.  N.  Widenmann, D.  Simberloff, and R. N. Mack. 2006. Adding biofuels to the invasive species fire? Science 313:1742. Ramanujan, K. 2007. Cornell helps develop pest-­resistant eggplant, the first genetically modified food crop in Southeast Asia. ChronicleOnline. http://www.news.cornell.edu/stories/Sept07/EggplantBt .kr.html. Sims, R.  H., A.  Hastings, B.  Schlamadinger, G.  Taylor, and B.  Smith. 2006. Energy crops: Global status and future prospects. Global Change Biol. 12:2054–­2076.

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Stokstad, E. 2004. Monsanto pulls the plug on genetically modified wheat. Science 304:1088–­1089. Thompson, J. 2004. The status of plant biotechnology in Africa. AgBioForum 7:9–­12. Thornton, M. 2003. The rise and fall of New Leaf potatoes. In Biotechnology: Science and Society at a Crossroad, ed. A. Eaglesham, S. S. Ristow, and R. W. F. Hardy. National Agricultural Biotechnology Council Report 15. Pp. 235–­243. UNEP-­GEF Biosafety Unit. 2006. A comparative analysis of experiences and lessons from the UNEP-­GEF biosafety projects. http://www.unep.org/biosafety/Documents/UNEPGEFBiosafety _comp_analysisDec2006.pdf. Ur Rehman, M. S. 2007. Pakistan agricultural situation cotton update. USDA Foreign Agricultural Service, Global Agriculture Information Network, GAIN Report PK7026. October 2. Wolfenbarger, L. L., and R. Grumet. 2003. Executive summary. In Proceedings of a Workshop on: Criteria for Field Testing of Plants with Engineered Regulatory, Metabolic, and Signaling Pathways, June 3–­4, 2002, ed. L. L. Wolfenbarger. Blacksburg, VA: Information Systems for Biotechnology. Pp. 5–­12.

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Part 2

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Environmental Considerations Associated with Genetically Engineered Crops

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Factors Influencing the Genetic Diversity of Plant Species and the Potential Impact of Transgene Movement

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James F. Hancock

Biodiversity in native and agroecosystems is a function of species composition (number of species, relative abundance) and the genetic makeup of individual species. Biodiversity is negatively affected if there are reductions in species abundance or levels of genetic diversity within species. The potential impact of a GE crop on biodiversity will depend on the invasiveness of the crop itself and changes in the competitive ability of any relatives that receive a transgene through hybridization. Herein, I will discuss the major evolutionary forces that assort genetic variability in native species and then use this information to describe how transgene movement might affect levels of genetic diversity in native and agroecosystems. Patterns of genetic variability in natural populations are regulated by three major forces of evolution: (1) migration, (2) selection, and (3) genetic drift. Migration or gene flow is the movement of genes within and between populations via pollen or seeds. Selection is a directed change in a population’s gene frequency due to differential survival and reproduction, while genetic drift is a nondirectional change in gene frequency due to random events. Selection is often believed to be the major force shaping the diversity patterns of native populations, but in many instances migration and genetic drift play just as significant or even a more significant role. In this chapter I will discuss the impacts of these various forces on levels of genetic variability in natural populations, and then will describe how conventionally bred and genetically engineered (GE) crops have affected genetic variability in compatible relatives.

Migration

Migration between Populations Gene flow between populations can have a major impact on levels of genetic variability, if the populations carry different alleles or differ in allele frequencies. The amount of migration 61

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between populations is regulated by the type of pollen vector, the breeding system of a species, its mode of seed dispersal, and the distance between populations. The most extensive information available on the factors regulating gene movement can be extracted from the recommended isolation distances for the production of pure seed lines of crops (Levin and Kerster 1974; Ellstrand and Hoffman 1990). Most wind-­pollinated species require distances of less than 200 m, while most insect-­pollinated crops require separations of more than 500 m. The average for 35 insect-­pollinated species is 657 m, while that for wind-­ pollinated species is 244 m. Self-­fertilized species require isolation distances below 200 m, while most outcrossing species require much greater distances. The average isolation distances are 385 m for 14 predominantly selfing species, 493 m for 16 mixed-­pollination (both selfed and outcrossed) species, and 846 m for 21 outcrossed species. This is not to say that long-­distance dispersal does not occur even in the crops with the shortest isolation distances. While most pollen travels only a few hundred meters, the tails of the distribution are often very lengthy and of unspecified distance. This allows for low frequencies of gene movement to distant individuals in both insect-­and wind-­pollinated species. Long-­distance gene dispersal has been documented at distances of one kilometer or more (Klinger et al. 1991; Watrud et al. 2004; Fénart et al. 2007). The mode of dispersal of seeds can also greatly influence how far gene flow occurs and influences patterns of genetic variability (Levin and Kerster 1974; Harper 1977; Cain et al. 2000). Gravity-­dispersed seeds usually travel only a few meters, and most seeds are clumped about the mother. Seeds with explosive or plumose seeds travel a little bit further 1–­10 m with a more even distribution. Animal-­dispersed seeds are often clumped about the mother because of gravity, but can have by far the longest tails. Mammals can have territories of dozens of miles, and bird migration distances can span thousands of miles. Human beings have played a particularly important role in plant evolution by carrying both native-­collected and crop seeds long distances, planting them next to compatible native populations and providing disrupted sites for population expansion (Anderson 1948; Hancock 2004).

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Migration within Populations The distance that pollen and seeds move not only affects variation patterns between populations, but also within populations. Limited gene flow results in a highly substructured population where only adjacent plants have a high likelihood of mating. Several terms have been developed to describe the substructuring of plant populations due to limited gene flow. A deme or panmictic unit is the group within which random mating occurs (Wright 1943). A neighborhood is defined as the number of individuals in a circle with a radius twice the standard deviation of the migration distance, or the number of individuals with which a parent has a 99% certainty of crossing (Wright 1946). Neighborhood sizes have been estimated to vary from four individuals in Lithospermum caroliniense (Kerster and Levin 1968) to several hundred in Phlox pilosa (Levin and Kerster 1968) and Viola pedata (Beattie and Culver 1979). The size of a neighborhood has a strong effect on the variation patterns observed in polymorphic populations. In substructured populations with many small neighborhoods, genes will move very slowly across the total population, resulting in patchy distributions, while in large, less structured populations patterns will appear much more regular. Expected levels of heterozygosity in the population as a whole can also be reduced by small neighborhood size if

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the gene frequencies within individual subpopulations vary significantly from the populational mean (Wahlund 1928). This occurs because the expected number of heterozygotes calculated from average allele frequencies is not always the same as the average of the subpopulations. Another factor that has a strong influence on variation patterns is the breeding system of the species. Highly self-­pollinating species will be more homozygous than outcrossing ones, since heterozygote percentages are reduced by 50% with each generation of selfing. The reduction in heterozygosity occurs because half of each heterozygote’s progeny will be homozygous each generation because of Mendelian segregation, while the homozygotes continue to produce only homozygotes. Any level of inbreeding reduces the number of heterozygotes expected from random mating.

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Selection

The potential impact of migrant genes on fitness can be classified into three major classes: (1) neutral, (2) detrimental, and (3) beneficial. Genes with detrimental effects on fitness will be selected against in the natural environment and will not spread. Genes with beneficial effects will increase in frequency over time through selection. Genes with a neutral effect on fitness will spread nondirectionally in natural populations through genetic drift (as will be described below), but will not lead to directional change. There are three primary types of selection: (1) directional, (2) stabilizing, and (3) disruptive or diversifying. In directional selection, one side of a distribution is selected against, resulting in a directional change. Under stabilizing selection, both extremes are selected against, and the intermediate type becomes more prevalent. In disruptive selection, the intermediate types are selected against, resulting in the increase of divergent types. The amount of genetic variability present in a population and the strength of the selection coefficient determine how fast and how much a population will change. Numerous examples of directional selection have been presented in the evolutionary literature. Perhaps the most striking and repeatable is the evolution of heavy metal tolerance in those plant species that come in contact with mine borders (Jain and Bradshaw 1966; Antonovics 1971). In less than two hundred years, pasture species such as Anthoxanthum odoratum and Agrostis tenuis evolved distinct morphologies and means of coping with high levels of copper, lead, and zinc in the face of substantial gene flow. The domestication of corn also offers a dramatic example of directional selection. Under human guidance, the size of the ear was increased between 7,000 and 3,500 b.p. (Before Present) from less than an inch to well over half a foot. In fact, directional selection is employed by all modern plant breeders to genetically improve plant species. The fact that we recognize most species as definable entities argues that stabilizing selection is common in nature, or else species lines would be much more blurred than they are. Huether (1969) provided some of the strongest evidence of stabilizing selection when he showed that Linanthus androsaceus almost always have five lobes per flower even though their environments vary greatly and there is genetic variation for the trait at every site. Plant taxonomists often find floral traits to be the most dependable species markers, because they are generally less variable than other traits. Documentation of disruptive selection has come most frequently by correlating gene

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frequency with environmental variation. One of the most commonly cited examples is the work of Allard and coworkers (1988), who found reproducible correlations between allozyme frequencies in the oat Avena barbata and the relative moisture content of soils in California. Distinct allozyme frequencies are found on the wettest (mesic) and driest (xeric) sites. These allozymes may not have been the specific traits selected, but they were at least associated with the selected loci through genetic linkage or partial selfing (Hedrick 1980; Allard 1988). Many unique races of crops were developed by human beings through disruptive selection as they gathered and grew populations from distinct regions and habitats. Perhaps the most distinct alteration came in Brassica oleraceae, where several distinct crops were developed including kale, broccoli, cabbage, kohlrabi, and brussels sprouts (Hancock 2004). Diverse races of rice, chickpea, and chili peppers also emerged in response to isolation and differential selection pressure from humans. Plant breeders have on numerous occasions employed diversifying selection to produce differences in harvest dates and quality factors. For example, dramatic changes in the protein content of corn were produced over 60 generations by selecting repeatedly for high and low values. While directional selection can eliminate variability in a population, stabilizing and disruptive selection often act to maintain it. Dobzhansky (1970) called this maintenance of genetic polymorphism balancing selection. Disruptive selection maintains polymorphism when different genotypes are “favored” in different environments. Stabilizing selection acts to maintain polymorphisms if heterozygotes produce the favored phenotype. Disruptive selection occurs not only across spatially heterogeneous environments, but also across time. Polymorphisms can be maintained across temporarily varying environments, different life stages, and variant sexes. There are also examples of polymorphisms being maintained by differing population frequencies and genetic backgrounds. Some alleles, such as the S alleles associated with self-­incompatibility, are even favored when they are in low frequency, but disfavored at high.

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Factors Limiting the Effect of Selection

Several important factors limit the influence of selection on gene frequencies: (1) amount of genetic variability present, (2) generation time, (3) strength of the selective coefficient, (4) degree of dominance, (5) initial frequency of the advantageous allele, and (6) intragenomic interactions. The only way a population can change is if there is genetic variability present. Many a breeding program has stalled or a species has gone extinct when the genetic variability for a particular trait was extinguished. This is true for both single gene traits and for quantitative traits where more than one locus is involved. In 1930, Fisher outlined his fundamental theorem of natural selection, which stated that “the rate of increase in fitness of any organism at any time is equal to its genetic variance at that time.” The mating behavior of a species has important long-­term evolutionary ramifications. Outcrossed species often have high levels of heterozygosity, and gene combinations are continually shuffled during reproduction through crossing over and independent assortment. Selfing species are frequently very homozygous, and specific gene combinations are rarely disrupted by sexual recombination. An outcrossed, heterozygous species has a considerable amount of

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genic flexibility with which to meet environmental change, but the selfing, homozygous ones may be better adapted to specific, unchanging conditions. An intermediate strategy with variable outcrossing rates may yield the greatest long-­term success in an unpredictable world; this may be why few extreme selfers or outcrossers are found (Allard 1988). Gornall (1983) has suggested that “those colonizing species which had extraordinary flexible recombination systems, which allowed them both to store and release large amounts of variability, were in a sense pre-­adapted to successful cultivation.” The strength of selection will critically influence the rate of change in a population, as the greater the proportion of individuals being selected each year the more rapid the change. Likewise, the generation time of an organism can have a strong effect on the rate of evolution simply because the longer the period between reproductive episodes, the longer the separation between meiotic reassortments of genes and seedling selection. Generation times in higher plants vary from a few weeks in Arabidopsis to dozens of years in some tree species. The degree of dominance has an influence on rates of change because recessive alleles in the heterozygous state are masked from selection. Frequencies of a newly arisen recessive allele will therefore change very slowly in a population until its frequency is quite high. Frequencies of co-­dominant alleles or those with an intermediate effect in a heterozygote will change more rapidly than recessives, since they have a partial influence on the phenotype of heterozygotes. Frequencies of dominants will initially change more abruptly than either recessives or intermediates, but the rate of change will eventually slow as the frequency of recessives becomes so low that most are “hidden” in heterozygotes. In all cases, populations with intermediate gene frequencies change more rapidly than those with low frequencies of deleterious or advantageous alleles.

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Genetic Drift

Many people stress the importance of selection in shaping natural populations, but nondirectional forces such as genetic drift can also play an important role. The common inclination is to assume that nature is ordered and that all is optimized. The simple truth is that variation patterns are regulated to a large extent by luck. A highly adapted genotype will not predominate in a population if most of its seeds fall on a rocky outcropping where they cannot germinate or there is no pollinator activity because of cool conditions when its pollen is dehisced. To proliferate, a genotype must be both well adapted and its progeny must reach maturity before some inadvertent accident eliminates it. While it is easy to document selection by observing directional changes over time or genotype/environment correlations; drift is difficult to measure because it is nondirectional and often masked by other forces (Schemske and Bierzychudek 2001). Most demonstrations of drift have come by the process of elimination—­no apparent associations were observed between any environmental parameter and an allele’s frequency. For example, on a hillside of Liatris cylindracea in Illinois, Schaal (1975) found a substantial amount of allozyme variation in several loci that she could not associate with any environmental parameter including moisture, soil pH, nutrient content, or percentage of organic matter. Sewell Wright (1931; 1969) provided numerous models that show how drift might operate. Drift will ultimately result in the fixation of one allele in a population like directional

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66    James F. Hancock

selection, but the approach will be much more variable. Two primary factors influence the effects of drift—­allele frequency and population size. The more frequent an allele, the greater its chances of being fixed, and the smaller the population, the faster it will stumble towards fixation. The probability that an allele will be fixed is equal to its frequency in a population. In the 1980s, there was considerable debate over the relative importance of drift and selection in natural populations, particularly as they related to allozyme variation (Hedrick 1983; Nei 1987). The “selectionists” believed that most variability was maintained by selection, while the “neutralists” believed that drift was the most important force. While this debate continues to go on, a reasonable compromise is to assume that both drift and selection are important and that the relative strengths of the two forces are dictated by each individual set of circumstances. The critical point to realize is that forces other than selection can shape variation patterns. This is particularly true in plant populations, where limited migration results in most populations being effectively small. Extreme cases of random genetic drift occur when a new population is initiated by only a few individuals—­this is called the founder effect (Mayr 1942). Gene frequencies may be quite different in a few colonizers compared to the population from which they originated because of sampling errors. Chance variations in allelic frequencies can also occur when populations undergo drastic reductions in numbers (“bottlenecks”) after environmental catastrophes. The early stages of most crop domestications were probably influenced by founder effects, as the bulk of our domesticated strains are based on relatively few genotypes (Ladizinsky 1985; Tanksley and McCouch 1997).

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Interaction between Forces

The evolutionary forces of migration, drift, and selection rarely act alone. The relative importance of these forces depends on the particular circumstances at hand. Selection is directional, while drift is not. The relative influence of these two forces is tempered by the strength of the selective coefficient and the population size. Where drift is the predominant force, alleles will be fixed essentially at random; where selection is the predominant force, particular alleles will be favored. In the intermediate zones it is often difficult to predict whether drift or selection will dominate. Migration can act to supply variability to a population, but it can also act in opposition to drift and selection if the migrants are distinct to the changes being imposed. In general, very small amounts of migration can block the effects of genetic drift. Likewise, if the migration rate is greater than or equal to the selection coefficient, then the importance of selection on population differentiation becomes almost insignificant (Ellstrand and Marshall 1985). Mutation can act like migration in tempering the effects of selection and drift. However, its rate of occurrence is generally quite low (