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Now or Never: 
Serious New Plans to Save Natural Pest Control

Contributions by:

David Andow, Ph.D.
David Ferro, Ph.D.
Fred Gould, Ph.D.
William Hutchison, Ph.D.
Bruce Tabashnik, Ph.D.
Mark Whalon, Ph.D.

Union of Concerned Scientists

Chapter 1 Introduction and Chapter 2 Contributors Introduction are included in this file at mindfully.org
The remaining chapters in PDF format can be downloaded from the UCS website using the following links:

3. Bt-Corn Resistance Management (pdf)
4. Bt-Cotton Resistance Management (pdf)
5. Bt-Potato Resistance Management (pdf)
Appendices (pdf)
    A. Bt Crops Approved for Field Testing by USDA, 1987-1997
    B. Microbial Bt Insecticide Use in US Crop Production, by Crop and State, 1992
    C. Microbial Bt Insecticide Use in US Crop Production, by Crop, 1992

Two Brattle Square
Cambridge, Massachusetts 02238
Copyright 1998 by the Union of Concerned Scientists
All rights reserved.

The Union of Concerned Scientists (UCS), an independent nonprofit organization, is dedicated to advancing responsible public policies in areas where science and technology play a critical role. Established in 1969, UCS works in partnership with scientists and citizens to address serious environmental and security threats facing humanity.

UCS is currently working to encourage responsible stewardship of the global environment and life-sustaining resources; promote energy technologies that are renewable, safe, and cost effective; reform transportation policy; curtail weapons proliferation; and promote sustainable agriculture.

Recognizing the impacts of agricultural practices on food security, environmental protection, and economic prosperity, the UCS Agriculture and Biotechnology Program advocates sustainable agriculture policies. The program promotes agricultural methods that minimize pesticide, fertilizer, and energy use, and evaluates the risks and benefits of biotechnology in agriculture.

More information on UCS and the Agriculture and Biotechnology Program is available at the UCS Web site at www.ucsusa.org .

Copies of Now or Never: Serious New Plans to Save a Natural Pest Control are available for $14.95 plus 20% shipping and handling from UCS Publications Department N, Two Brattle Square, Cambridge, MA 02238-9105; or call 617-547- 5552. UCS Sponsors may purchase copies for $11.95 plus 20% shipping and handling.

We are grateful to the six contributors for their hard work and commitment to this project. In midsummer, the Union of Concerned Scientists (UCS) asked them to analyze existing resistance management plans and write first-class plans for Bt corn, cotton, and potato in time to be implemented before the 1998 growing season. In late September, the contributors and UCS staff met in Washington to discuss early drafts and solidify plans for the final report. Over the following months, the scientists, working in pairs, exchanged several drafts of their chapters with UCS and each other. One draft was reviewed by twelve other scientists, who are listed below.

The scientists are the sole authors of their chapters. UCS placed no constraints on the substance of their analysis or recommendations. The six contributors do not necessarily agree with or endorse UCS's observations and recommendations. Among the many other people who contributed to this report, we extend special thanks to Cheryl Siebert and Teri Grimwood for producing the final report for printing, Anita Spiess for editing the final draft, and Yuri Kant for performing the myriad tasks necessary to complete this project. Eason Associates, Inc., designed the cover.

We are grateful to the following persons who reviewed all or parts of the three chapters on crop-specific management plans: Brian Baker, Michael Caprio, Rebecca Goldburg, Richard Hellmich, George Kennedy, Randy Luttrell, William McGaughey, Richard Roush, and Eric Sideman. Three industry reviewers requested anonymity. While we appreciate the valuable advice and information provided by the reviewers, this report does not necessarily reflect their opinions. UCS and the six contributors are responsible for any errors in their respective chapters.

The project to save Bt and the other work of the UCS Agriculture and Biotechnology Program are supported by grants from the C.S. Fund, The Educational Foundation of America, Clarence E. Heller Charitable Foundation, HKH Foundation, The Joyce Foundation, Mary R. Morgan, and Newman's Own; and by contributions from UCS sponsors and the UCS Solutions Capital Campaign.

Margaret Mellon, Ph.D., J.D.
Jane Rissler, Ph.D.
Union of Concerned Scientists
January 1998.

Chapter 1 UCS Introduction (below)
Margaret Mellon

Chapter 2 Contributors' Introduction (below)
Fred Gould, Bruce Tabashnik, William Hutchison, David Ferro, David Andow, Mark Whalon

Chapter 3 Bt-Corn Resistance Management (PDF at UCS website)
David Andow and William Hutchison

Chapter 4 Bt-Cotton Resistance Management (PDF at UCS website)
Fred Gould and Bruce Tabashnik

Chapter 5 Bt-Potato Resistance Management (PDF at UCS website)
Mark Whalon and David Ferro

Appendices (PDF at UCS website)

Chapter 1 UCS Introduction

Margaret Mellon

About two years ago, the Union of Concerned Scientists (UCS) inaugurated a campaign to save important valuable natural pest control products, the so-called Bt toxins. The toxins are a family of related molecules produced in nature by a soil bacterium, Bacillus thuringiensis (Bt). Farmers and gardeners have used the microorganisms in spray form to control insects for more than 50 years. Now, they risk losing Bt through the development of resistance in target insect populations. This report is one in a series of actions UCS is carrying out to save Bt by delaying the development of resistance.

Insect resistance could develop because of widespread use of crops genetically engineered to produce Bt toxins. Such crops are referred to as "transgenic" because they contain genes from unrelated sources-in this case, bacteria and plants. Genetic engineering provides the artificial gene transfer techniques that move genes across natural boundaries. So far, three transgenic Bt crops have been approved for commercial use in the United States-corn, cotton, and potato-with many more under development (see Appendix A). In 1997 nearly 9 million acres of Bt crops were planted in the United States- about 7 million acres of Bt corn, 1.7 million acres of Bt cotton, and 25 thousand acres of Bt potato. With millions of acres already devoted to Bt crops, the issue is urgent. We need to adopt effective plans to delay resistance now-or lose our chance, perhaps forever.

Transgenic crops are a threat to Bt because they produce toxin throughout much, if not all, of their lives. Constant long-term exposure of pest populations to Bt encourages survival of individual pests that are resistant to that toxin. Over time, the proportion of resistant individuals in pest populations can increase, reducing the efficacy of the Bt toxin as a pesticide. If resistance develops, Bt toxins will cease to be effective both for the users of the new transgenic plants and for those who have relied on Bt sprays for decades. Scientists have estimated that widespread use of Bt crops could lead to the loss of Bt's efficacy against certain pest populations in as few as two to four years.

Bt is a natural pest control product that provides an extraordinary combination of safety and effectiveness. Bt toxins are highly effective against many economically important agricultural pests, but are generally safe for mammals and other nontarget organisms, including beneficial insects like ladybugs. In addition, the toxins break down rapidly in the environment and do not accumulate in water or through food chains.

Bt toxins appear in nature as large crystals enclosed within sporulating Bacillus thuringiensis bacteria. Because the crystal occupies much of the spore, semipurified preparations of the bacteria can be used as pest-control products. Different Bt toxins act against different pests. Some Bts are toxic to moth and butterfly larvae, others to beetles, and still others to flies.

Because of their safety record and natural origin, Bt sprays have long been approved for use by organic farmers. Vegetable growers, orchardists, and foresters also rely on them. In 1992, over 2 million acres of US crops were treated with Bt sprays, including many high-value crops like strawberries, apples, and sweet peppers (see Appendices B and C). On many vegetable farms and orchards, Bt is an important component of integrated pest management (IPM) systems that use chemicals only as a last resort.

Despite an exemplary safety record, Bt sprays have never been widely used on commodity crops because their relatively rapid breakdown requires precise timing in application and more intensive management than most large industrialized farms are willing to provide.

Genetically engineered Bt crops offer conventional farmers the option of taking advantage of Bt's safety and efficacy without major changes in their management practices. US farmers are consequently adopting them rapidly where they can realize cost savings compared with current pest control regimes. Most of these savings result from farmers' ability to reduce the number of pesticide applications. In systems that currently depend on multiple applications of chemical insecticides, e.g., cotton, some farmers can cut their applications of pesticides from six to three. Such foregone pesticide applications represent a considerable environmental benefit for high acreage commodity crops like cotton.

In addition, the narrow spectrum of insects affected by various Bt toxins allows beneficial insects to emerge in fields. Under the right circumstances, these beneficial insects can provide an additional measure of pest control that further reduces the need for chemical pesticides.

The cost savings and environmental benefits of Bt crops will last only as long as Bt does. If resistance develops, as has happened with many insecticides in the past, farmers will again increase their applications of chemical pesticides, incurring higher costs and inflicting damage on the environment.

The benefits of transgenic Bt crops are also limited in other ways. Much of the potential cost saving to farmers is captured by the company that created the crop in the form of a technology fee, reducing the likelihood that the products will translate into substantially lower prices to consumers. Also, environmental benefits materialize only where chemicals are already in use. That is not the case in Bt field corn, for example, where losses from the target pest (European corn borer) are often considered small and variable enough that farmers generally elect not to treat with chemicals. In those situations, Bt crops offer few environmental benefits. On the other hand, new data discussed in this report suggest that the losses to corn borer may be large enough that farmers will begin to treat field corn with insecticides. This would increase the environmental benefit of using Bt corn.

While in some cases the narrow spectrum of Bt leads to reduced pesticide applications by sparing beneficial insects, in others it can have the opposite effect. In some potato regions, for example, the European corn borer, previously suppressed by broad-spectrum chemical pesticides, is emerging in Bt-potato fields. Where the corn borer occurs at high enough levels, growers may treat Bt potatoes with added applications of chemical pesticides, reducing the net environmental benefit of the Bt crop.

The benefits of Bt crops to conventional agriculture may also be offset by environmental risks. Among these are negative impacts on beneficial organisms, changes in the composition of soil biota, and the movement of Bt genes from crops via pollen to nearby wild or weedy plant relatives. Studies on environmental effects of Bt crops are just getting under way.

Finally, while the reduced applications of pesticides that accompany Bt crops are real and welcome, their introduction does not represent a fundamental shift toward an environmentally sound agriculture. They are an improvement in the current cropping system, which is based on growing large acreages of the same crop year after year on the same ground or alternated annually with one other crop. That style of agriculture encourages the growth of pest populations by assuring them adequate food. Agricultural systems based on multiyear crop rotations would reduce pest pressure-and the concomitant demand for chemical use-from the outset. Reorientation of US agriculture in this direction is an enormous undertaking that will require deep and sweeping changes. To the extent that Bt crops further entrench the current system, they impede that important transition.

Bt toxins are the only protein toxins currently in commercial use by genetic engineers. So far, Bt genes have been put in numerous crops, vegetables, and trees, of which 18 have already been granted field-test permits (see Appendix A). At this stage, we do not know whether scientists will be able to discover other insect-resistance genes with the same favorable combination of efficacy and safety as Bt toxins. Although intensive research is underway, finding insect resistance genes for use in transgenic plants is proving difficult. At this point, it seems unlikely that pesticidal proteins will be forthcoming at anything like the rate that chemical pesticides emerged from laboratories in the 1950s and 1960s. Even if it turns out to be possible to develop new genes to replace the Bt toxins, that prospect would not justify squandering a gene as valuable as Bt. But the fact that replacements are apparently difficult to come by should increase the value society places on Bt and strengthen the determination to use it wisely.

Questions about the ownership of genes and gene products are well beyond the scope of this report. But Bt illustrates the complexity of the issues and need for new policies. If nothing else, Bt highlights problems associated with considering genes simply the property of private companies. That approach might provide incentives for private sector research to use the new genes, but it ignores the effects on others in the society. In this case, organic and IPM farmers may well lose Bt as the result of the use of transgenic crops. The loss would deprive them of a valuable tool, undermining to some extent their prospects for success. Yet society has an interest in these farmers' abilities to develop high-yield agricultural systems based on techniques of soil culture, systems management, and biocontrol. Also IPM and organic farmers would lose this tool without any compensation. In a fair system, the interests of all parties-conventional farmers, organic and IPM farmers, and the public at large-would be factored into decisions about the lifespan of a valuable genetic resource like the Bt toxins.

There is little dispute that saving Bt for as long as possible would be in the long-term interest of agriculture, the environment, and the biotechnology companies that have invested in the development of Bt crops. Indeed, the biotechnology industry, high officials in the US Department of Agriculture (USDA) and the Environmental Protection Agency (EPA), and many scientists are on record to that effect. All this might lead to the conclusion that Bt resistance management will be easy to accomplish. Not so.

Resistance management plans often require farmers to use on-farm practices and planting arrangements that they do not find appealing. For example, they could be required to leave certain fields unprotected from insect pests. Farmers whose practices are not already geared to the long term are often unwilling to take on short-term pain for long-term gain. This is especially true if farmers perceive themselves to be incurring costs their neighbors are avoiding. Resistance management also runs counter to the short-term interests of companies, which need to recoup the investment for expensive research and to perform well on quarterly profit reports. Companies' short-term incentives favor aggressive marketing of transgenic crops. The combination of companies' and farmers' short-term interests is often deadly for resistance management. A company that is willing to sidestep refuge requirements, for example, will find plenty of buyers for its products. These competitive pressures make it unrealistic to expect companies to voluntarily go the full distance to achieve resistance management goals.

In truth, most farmers and most pesticide companies are accustomed to losing pesticides to resistance and replacing them with other products. This pattern is embedded in the fabric of conventional agriculture. To be successful, resistance management for Bt will have to overcome this ingrained attitude. Difficult does not mean impossible, however. Delaying resistance can be achieved, but only if everyone understands the magnitude of the task. In particular, resistance management regimes will have to be established in ways that blunt the competitive pressures on both farmers and companies. That requires a judicious mix of education, and voluntary and enforceable requirements.

Prolonging the life of Bt may also have deeper implications for the use of pesticides. The slower rate of introduction and the increasing cost of new chemical pesticides in recent years suggest that science may have an increasingly difficult time providing replacements for pesticides lost to resistance. If the stream of new products continues to slow, resistance management will move from being an option to a necessity. In that case, any success achieved with Bt-resistance management will be even more important than its impact on a single pest-control option.

This report-aimed at strengthening the resistance management plans for the three Bt crops currently commercialized in the United States-is only one part of the overall strategy to save Bt. A complete strategy for Bt-resistance management would include an adequately funded research base, new legal tools to blunt competitive pressures on both farmers and companies, and scientifically credible resistance management plans. It would also encompass all Bt crops in all the countries where they will be used.

Also, while the millions of acres of transgenic crops represent the largest threat, it is necessary to keep an eye on the use of Bt sprays. Although Bt sprays have been in use for over fifty years, Bt resistance did not arise until recently. The successful avoidance of resistance was probably due to a combination of factors, including relatively low levels of use, lack of persistence in the environment, and the preference in IPM and organic systems for selective rather than prophylactic use of pesticides. But recent reports confirm that resistance can develop to Bt sprays, particularly where farmers employ the sprays in the same way they have used synthetic pesticides-in multiple, short-interval applications over a long period. Intensive use of Bt sprays may increase in the future as farmers lose other pesticides.

Scientifically credible resistance management plans are the key element of any strategy to save Bt. These plans consist of coordinated measures by industry, government, and farmers to delay or prevent resistance. Plans typically contain three major elements: farm-level practices to delay or prevent resistance, monitoring for early detection of resistance, and response to the emergence of resistant populations. In general, the strategies recommended in resistance management plans are based on computer models that predict the changes in the genetic makeup of populations of pests over time. The accuracy of the models depends heavily on a thorough understanding of how pests behave in their environment.

Currently, EPA endorses or requires some sort of resistance management plan for the three approved Bt crops. The agency has developed those plans in cooperation with industry in the context of approvals of the Bt crops under the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA). The current plans are a mixed bag in terms of both legal status and provisions. Legally, the resistance management plan for potato, the first to be adopted, is completely voluntary. Although it is not required to do so, the one company that currently sells Bt potatoes, NatureMark, a subsidiary of Monsanto, has developed a resistance management plan that it imposes on purchasers of its potatoes by means of one-on-one contracts.

The measures that make up the corn and cotton plans, by contrast, are imposed on the companies as enforceable conditions of the pesticide registrations issued under FIFRA. If sellers of Bt cotton and Bt corn fail to comply with the terms of the conditions, EPA could rescind their permission to sell the Bt crops. Delta and Pine Land, under license to Monsanto, is the major seller of Bt cotton. Many companies, including Novartis, DeKalb Genetics, and Pioneer Hi-Bred, sell several versions of Bt corn derived from different so-called "events." Bt-corn events result from separate operations transferring genes into corn tissue. They can differ from one another in the level, timing, and tissue location of toxin production.

The provisions of resistance plans are found in different documents for different crops. NatureMark, for example, describes the current potato plan in the educational materials it sends to farmers and in the provisions of its contracts. This relatively detailed plan requires crop rotation and specifies the size of plantings of non-Bt potatoes.

The provisions of the corn and cotton plans, on other hand, are found primarily in the Pesticide Fact Sheets that accompany EPA's registration of the Bt crops and in correspondence and internal decision documents prepared by EPA. Currently, the cotton plan contains detailed acreage requirements for non-Bt cotton, while the corn plan gives companies until the end of the 1998 growing season to develop specific plans.

A signal feature of all the plans is that they rely on a scientific strategy that combines transgenic plants producing very high doses of toxin with the presence of nearby non-Bt plants or refuges-the so-called "high-dose/refuge" strategy. While theoretically sound, the strategy was adopted before its major assumptions were confirmed. Since its adoption, new data have come to light demonstrating that not all crops produce a "high" dose and that new strategies are required for such crops. Furthermore, new data suggest that even where transgenic crops produce a relatively high dose of toxin, adjustments in the size and placement of the refuges are appropriate. Moreover, several key assumptions still remain unconfirmed.

The purpose of this report is to present new plans to manage the evolution of resistance to Bt in transgenic Bt corn, Bt cotton, and Bt potato. These plans were developed independently by six university scientists all of whom are recognized experts in the field of insect resistance. Working in pairs on the three crops, these scientists developed recommendations for "state-of-the-art" resistance management plans that in their view would substantially delay the evolution of resistance to Bt. These plans take into account new research, as well as the latest field experience with the transgenic crops. The scientists' recommendations for refuge sizes, placement, and spray choices are intended to be effective options for farmers in conventional systems. The scientists have also jointly prepared a chapter introducing their work.

The views and opinions expressed by the scientists in their chapters are completely their own, as are their recommendations for action. UCS brought the six scientists together for a one-day meeting, facilitated the subsequent exchanges of drafts, and produced and published the report. UCS had no substantive role in developing the plans or recommendations found in the scientists' chapters.

The scientists' recommendations in this report are considerably stronger than plans currently endorsed by EPA. For example, they recommend that all resistance management plans be enforceable. In addition, although the plans differ in detail from crop to crop, they all recommend relatively large refuges and specify the spatial relationships of the refuges and Bt crops. They also recommend detailed monitoring and response plans for Bt.

UCS objects to the EPA's approval of transgenic Bt crops because the agency did not require validation in the field of the high-dose/refuge strategy. We believe that the approvals were premature. Scientists should have been given the resources to test their assumptions and perfect resistance strategies. Then, the commercial Bt products should have been introduced gradually. Now that this option is no longer available, the United States needs plans that can be used immediately on millions of acres of transgenic crops. These plans must have a substantial chance of delaying the development of resistance to Bt and must also be capable of implementation by farmers, often conflicting goals. The scientists' plans presented in this report are first-rate efforts in that direction.

Among the many important contributions these plans make is a thorough analysis of the strengths and weaknesses of the high-dose/refuge strategy. The scientists offer criteria for determining whether Bt crops produce high doses and note that Bt cotton does not produce a high dose for at least one target pest and that one of the Bt corn events also fails to meet the criteria. Where plants do not produce high doses, the scientists have recommended that EPA take a conservative approach and require large refuges.

The scientists' plans acknowledge the considerable scientific uncertainty surrounding these issues. Indeed, the science is imperfect enough that there is at least some possibility that resistance would not develop even in the absence of specific measures like those found in the plans. In that case, "Now or Never" might turn out to be an overly pessimistic dichotomy. But public decisions must often be made on the best available scientific information, even if that information is incomplete. As the chapters in this report demonstrate, scientists have confidence that large, structured refuges will delay resistance and that small refuges will work only where the transgenic crops deliver genuinely "high" doses of toxin. This is a sufficient base on which to develop a conservative strategy for the deployment of Bt crops.

EPA needs to adopt plans as strong as the scientists' plans as soon as possible. The agency has already put Bt at risk by allowing the planting of millions of acres of Bt crops. It first approved Bt potato for commercial use in 1995 and followed rapidly with Bt cotton and Bt corn. This flurry of approvals occurred over the objections of many agricultural and environmental groups-including UCS. But EPA went ahead under heavy pressure from the biotechnology industry.

EPA's hurried approvals mean agriculture is already two years into a several million-acre experiment on resistance development and transgenic Bt crops. EPA's actions have put Bt on a high trapeze before the nets have been installed. If the nets are strong and put up in time, we will all be lucky. If they are too weak, so much for Bt. Resistance management, like trapeze acrobatics, is a game with few second chances.

Bt is a valuable gift of nature with benefits for many: organic and IPM farmers, conventional farmers, and the biotechnology industry. To lose it within a few years would be a tragic waste. The six scientists who prepared this report have laid out the path to keep that from happening. EPA should now heed their warnings and swiftly translate their recommendations into action.

As part of an overall strategy to save the valuable Bt toxin for use in sprays and transgenic plants for as long as possible, UCS recommends that the EPA take the following actions:

1. EPA should act immediately to adopt Bt-corn, Bt-cotton, and Bt-potato plans at least as strong as those presented in this report in time for the 1998 planting season, including

2. EPA should not approve any new transgenic Bt crops until field-validated strategies for resistance management have been developed for those crops.

3. EPA should develop flexible means to update resistance management plans as new information emerges, including a strategy to cancel Bt crop registrations in a timely manner if Bt resistance develops. 4. EPA should compile all the elements of the resistance management plans into readily accessible documents that can be updated as needed.

Bt Corn

David Andow and William Hutchison

1. Mandatory resistance management plans are necessary for Bt corn. Separate plans may be needed for different transformation events and/or where other lepidopteran pests are important.

2. Growers should plant no more than 50 percent of their corn acreage in Bt corn. The non-Bt corn can be managed to control pests, but cannot be exposed to Bt insecticide. This conservative refuge requirement is necessary given the current knowledge gaps regarding European corn borer and concerns that not all Bt-corn events meet the high-dose assumption throughout the growing season.

3. If effective implementation and enforcement of a 25 percent untreated non-Bt corn refuge can be guaranteed, then a grower can expand the Bt-corn acreage to 75 percent of the total corn acreage.

4. The non-Bt corn refuge should be planted adjacent to or within Bt-corn fields. Specifically, non-Bt corn refuges should be planted on every 320 acres (1/2 section) of corn.

5. EPA, USDA, and the seed industry should support substantially more research on estimating initial gene frequencies for resistance, improving sensitivity and cost-effectiveness of monitoring methods, developing and validating refuge options, and characterizing movement and ecology of the European corn borer.

Bt Cotton

Fred Gould and Bruce Tabashnik

1. EPA should establish two separate mandatory resistance management plans for Bt cotton, one for areas with pink bollworm and one for areas without this insect pest. Because of the limited mobility of pink bollworm, non-Bt cotton should be closer to Bt cotton in areas where this pest occurs.

2. In areas with or without the pink bollworm, growers should plant Bt cotton on less than 84 percent of their total cotton acreage.

3. Growers who wish to treat their non-Bt cotton with insecticides that kill caterpillar pests should plant Bt cotton on 50 percent or less of their total cotton acreage.

4. Non-Bt cotton should be planted close enough to Bt cotton to encourage mating between moths emerging from Bt and non-Bt cotton.

Bt Potato

Mark Whalon and David Ferro

1. EPA should require a mandatory resistance management plan for Bt potato.

2. The plan should require a 20 percent refuge of non-Bt potato arranged either in strips throughout the field, as a single block at the end of the field, or in center pivot operations, reasonably close by. In no case should Bt-potato refuges be planted further than 500 meters from the Bt-potato fields.

3. Growers should rotate another crop through the potato acreage at least every third year and avoid the use of in-furrow and foliar imidacloprid in non-Bt refuges. Potato beetles in refuges should be managed under IPM principles and not treated with pesticides until they reach economic thresholds.

4. Baseline susceptibility data should be developed on the easily observable, lateinstar larvae that farmers are most likely to detect in their fields. Monitoring programs should be redesigned to encourage the detection of both early- and late-instar larvae.

5. Monsanto should offer growers a substantial reward of perhaps $5,000 for the discovery of Bt-resistant Colorado potato beetles.

6. The company should have a local eradication plan in the grower agreements that provides "step-by-step" directions for collecting, shipping, and eradicating beetles when survivors are found on Bt potatoes.

Chapter 2 Contributors Introduction

Recommendations for Developing and Implementing Resistance Management Plans for Bt-Toxin Producing Crops

Fred Gould, Bruce Tabashnick, William Hutchison, David Ferro, David Andow, Mark Whalon

In formulating action plans to deal with major environmental issues (e.g., global climate change, species' extinctions), policymakers must often develop regulations in the absence of comprehensive data. In such situations, there are usually some groups who argue that no regulatory action should be taken until it can be conclusively proven that there is a problem and an action plan to alleviate the problem. At the opposite extreme are those who feel that any evidence of an environmental problem should be responded to with moratoria on use of processes or products that could be causing the problem.

Recently commercialized, genetically engineered crops produce toxins derived from the bacterium Bacillus thuringiensis (commonly called Bt). Although use of Bt crops is new, the bacterium has been used for decades as a pest control spray by organic and conventional farmers. The toxins in the bacterial sprays and the Bt crops kill certain insect pests without harm to wildlife, people, and even most other insects. While the use of Bt sprays has always been limited, Bt corn, cotton, and potatoes have already been grown on millions of acres of US farmland. Because acreage planted to Bt crops is likely to dramatically increase and because Bt crops are defended against some of the worst agricultural pests, they should provide immediate environmental benefits by reducing use of conventional insecticides.

Although Bt crops can yield significant environmental and economic benefits, their success will be short lived if pests quickly adapt to the toxins they produce. More than 500 species of pests have already evolved resistance to conventional insecticides, and pests can also evolve resistance to Bt toxins (Tabashnik 1994). Susceptibility to Bt toxins can therefore be viewed as a natural resource that could be quickly depleted by inappropriate use of Bt crops. However, cautiously restricted use of these crops should substantially delay the evolution of resistance and result in greater long-term benefits from Bt crops. As with the major environmental issues mentioned above, efforts to avoid rapid pest adaptation to Bt crops will require that decisions be made with less than comprehensive data and theory. It has been argued that because scientists cannot predict exactly when or if resistance to Bt cultivars will occur and because scientists cannot prove, conclusively, that resistance management plans will have significant environmental benefits, the US government should not promulgate action plans aimed at decreasing the rate at which pest populations become resistant. Based on the same observations about our predictive capabilities, others advocate a moratorium on any commercial use of Bt crops until more scientifically accurate plans can be developed for delaying resistance.

We conclude from an examination of available data and theory that use of genetically engineered Bt crops should return to following the general guidelines put forth by the US National Academy of Sciences (National Research Council 1989, 1993) for work with genetically engineered organisms. The guidelines state clearly that we should be using a step-by-step approach. After each step, we are to examine the new information and decide whether a next step is appropriate. These guidelines were initially followed closely in developing Bt crops. First, tests were conducted in carefully monitored laboratories. Plants were then taken to confined greenhouses, to confined field plots, and finally to partially confined commercial-size fields. US regulatory authorities then took a leap from allowing the planting of a small set of carefully monitored fields to allowing almost all cotton, corn and potato production in most of the United States to be based on Bt-toxin-producing cultivars. Not only does this leap push the limits of our ability to manage pest adaptation (Tabashnik and Croft 1982; McGaughey and Whalon 1992; Gould 1998), it is not clear that such high proportions of Bt-producing plants are necessary for long-term suppression of the target pests (Painter 1951; Luginbill and Knipling 1969; Roush 1996; Alstad and Andow 1996; Riggin-Bucci and Gould 1997). In the following three chapters, we develop resistance management plans that conservatively match our level of confidence in available data and theory. Our goal is to avoid early misuse of the technology that could significantly damage the potential of Bt crops.

The chapters present resistance risk assessments and management recommendations for Bt-toxin-producing corn, cotton, and potato separately because each crop is unique in terms of its pests, ecology, and agronomy. Although recommendations are tailored to each crop, we agree that the following recommendations fit all three crops:

1. Mandatory resistance management plans must be implemented for each Bt crop.

2. The high-dose/refuge strategy is currently the most promising approach, if implemented with sufficiently large refuges.

3. Non-Bt refuges must be near the Bt crops, with distances specified for each crop.

4. The susceptibility of pest populations must continue to be monitored to evaluate the success of resistance management plans.

5. Plans should be modified, if necessary, as additional information is acquired through research and experience in the field.

The high-dose/refuge approach, which the Environmental Protection Agency (EPA) (1997) and industry (Fishhoff 1996) have also advocated, involves exposing one portion of the pest population to plants with an extremely high concentration of toxin, while maintaining another part of the population in a refuge where the pests do not encounter any of the toxin. By maintaining the refuges in close proximity to the toxin-producing crop, susceptible pests that survive in the refuge are expected to mate with any toxin-resistant individuals that survive on the engineered plants. The offspring from these matings are expected to have only a low or moderate level of toxin resistance and should not be able to survive on plants with high Bt-toxin levels. Carefully explored population genetic theory (e.g., Tabashnik and Croft 1982; Gould 1986; Mallet and Porter 1992; Alstad and Andow 1996) and laboratory experiments (Liu and Tabashnik 1996; Roush et al., in preparation) predict that this approach will substantially delay evolution of resistance, if it is appropriately implemented and its assumptions are met.

Although the EPA/industry plans for implementing the high-dose/refuge approach are headed in the right direction, we find that, for each of the three crops, there are deficiencies in the current resistance management plans that make achievement of a successful, high-dose/refuge approach unlikely. We conclude that in all three cropping systems, too few susceptible insects will usually be produced in the currently recommended minimum refuges. Furthermore, the lack of regulations on refuge placement could seriously reduce the probability of mating between susceptible and resistant pests. Therefore, we offer recommendations for improving refuge size and placement in each of the cropping systems. When more data are collected on the movement and mating patterns of the target pests, it should be possible to refine our recommendations. A critical problem in corn and cotton systems is that for at least some of the major target pests, currently available Bt cultivars do not produce toxin concentrations that are expected to kill offspring from the mating of resistant and susceptible insects. In the case of cotton, for example, the current Bt cultivars typically cause high mortality of such hybrid offspring (Gould et al. 1997) in one target pest (tobacco budworm) that is very sensitive to the toxin. However, another major cotton pest (cotton bollworm) is not as sensitive to the toxin, so 10-40 percent of caterpillars, with only average tolerance, survive on these Bt plants. There is no way to justify use of these plants in a high-dose/ refuge strategy. For such cultivars, only large refuges could delay resistance. In some geographical areas, refuges from natural vegetation and crops other than cotton are not available. In areas where such refuges could exist, they have not been carefully quantified. Until the effective size of noncotton refuges is documented, we recommend that much larger percentages of cotton acreage be planted with non-Bt cultivars. Requiring larger refuges for cultivars that do not produce a high dose for the cotton bollworm will delay resistance evolution, and it will also offer incentives for companies to produce high-dose plants that could be approved for use on more acreage.

As researchers continue to amass experimental and survey data and carefully test current assumptions about appropriate refuge size and placement, it will be possible to develop more robust resistance management plans. However, even with more data, long-term predictions regarding pest evolution will always be subject to some uncertainty. We therefore recommend that target pest populations be carefully monitored as the acreage planted to Bt cultivars expands. The information from monitoring will enable unexpected ecological or genetic changes in pest populations to be detected. Resistance management plans could then be adjusted to deal with these findings.

We are convinced that our recommendations for 1998 offer an improvement over the current resistance management plans. However, we hope that in the coming months, rigorous, targeted discussions involving all stakeholders can lead to improvements in our 1998 recommendations regarding both short- and long-term concerns.

Some of the restrictions in our recommendations are necessitated by the current lack of detailed survey and experimental evidence from the field. Therefore, as we work to put forth acceptable resistance management plans for 1998 based on currently available data, we must concentrate efforts and resources to obtain the essential data on the ecology and genetics of target pests. Monitoring and evaluation of strategies in place and large-scale field tests of alternative strategies must be performed.

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