Bt Corn & European Corn BorerLong-Term Success Through Resistance ManagementCopyright © 2002 Regents of the University of Minnesota. All rights reserved. Contents
Authors Editors: K.R. Ostlie, W.D. Hutchison, & R. L. Hellmich. The editors express their appreciation to J.F. Witkowski for hosting key discussions on publication content. We greatly acknowledge the encouragement and support provided by R.A. Higgins (current chair), and E.E. Ortman, (Administrative Advisor), NC-205. DedicationIn recognition of his lifelong research contributions to improved understanding of European corn borer ecology and management, the authors respectfully dedicate this inter-regional bulletin to W.B. (Bill) Showers, emeritus member, NC-205 research committee. "Bt Corn and European Corn Borer" was co-authored and sponsored by members of the North Central Regional Technical Committee on "Ecology and Management of the European Corn Borer and Other Stalk-Boring Lepidop-tera," NC-205, including: Experiment Stations and Extension Services of Colorado, Delaware, Illinois, Indiana, Iowa, Kansas, Maryland, Massachusetts, Michigan, Minnesota, Missouri, Nebraska, New York, North Carolina, North Dakota, Ohio, Pennsylvania, South Carolina, South Dakota and Wisconsin, and the USDA Agricultural Research Service, Ames, Iowa. AcknowledgmentsIndividuals from the following companies and U.S. government agencies provided invaluable input during multiple reviews of this publication's content and technical accuracy: AgrEvo (Plant Genetic Systems), Monsanto Co., DowElanco, DEKALB Genetics Corp., Garst Seeds, Mycogen Seeds, Novartis Seeds (Ciba Seeds, Northrup King), Pioneer Hi-Bred International, Inc., US Environmental Protection Agency and USDA Cooperative States Research, Education and Extension Service. Our sincere appreciation for their ongoing contributions. This publication represents a collaborative inter-regional effort to provide timely guidelines for growers, crop consultants, cooperative extension educators and industry personnel about how best to use Bt corn technology. Because of the dynamic nature of this technology, and ongoing research, this publication will be updated frequently. Updated versions will be available on the World Wide Web at the Northern Plains Crop Base at http://www.mnipm.umn.edu/ Bt Corn & European Corn BorerSeed companies are now marketing Bt corn, one of the first tangible fruits of biotechnology that has practical implications for U.S. and Canadian corn farmers. Bt corn hybrids produce an insecticidal protein derived from the bacterium Bacillus thuringiensis, commonly called Bt. These hybrids provide protection against the European corn borer equal to, and usually far greater than, optimally timed insecticides. Rapid introduction of Bt corn hybrids creates uncertainty about the technology and new questions about its use. What is Bt corn? How is it made? How does it work? What is the best way to use it? Is it worth the added cost? This publication provides an overview of Bt corn, an innovative technology for managing European corn borer, and discusses how to use this technology for long-term profitability. Why manage European corn borer?European corn borer, Ostrinia nubilalis, is the most damaging insect pest of corn throughout the United States and Canada (Figs. 1 & 2). Losses resulting from European corn borer damage and control costs exceed $1 billion each year. For example, losses during a 1995 outbreak in Minnesota alone exceeded $285 million. A recent four-year study in Iowa indicated average losses near 13 bushels per acre in both first and second generations of European corn borer, for total losses of about 25 bushels per acre.
Despite consistent losses to European corn borer, many growers are reluctant to use current integrated pest management (IPM) methods for this pest. Historically, this reluctance stems from several factors:
One geographical exception, to the prevailing attitude of "benign neglect" toward European corn borer, occurs in the intensively managed irrigated corn of the high-plains states, such as Texas, western Kansas, eastern Colorado, and Nebraska. Irrigated corn with its higher yields is monitored closely for insect pests, such as European corn borer and the southwestern corn borer, and is treated frequently with insecticides. These farmers have a history of aggressive management of European corn borer. Bt corn provides a new management tool for all corn producers. Ciba Seeds (now Novartis Seeds) and Mycogen Seeds introduced the first Bt corn hybrids in 1996. Several seed companies have incorporated this technology into their best inbred lines. Availability of Bt corn hybrids will increase dramatically as additional companies receive registrations and Bt corn seed production increases. Bt corn hybrids have one common feature. They each have a gene from Bacillus thuringiensis. Because these hybrids contain an exotic gene, they are commonly called transgenic plants. The Bt gene in these plants produces a protein that kills European corn borer larvae. Most larvae die after taking only a few bites. Consequently, Bt corn provides high levels of yield protection even during heavy infestations of European corn borer (Fig. 3). What is Bt?Bt is a naturally-occurring soilborne bacterium that is found worldwide. A unique feature of this bacterium is its production of crystal-like proteins that selectively kill specific groups of insects. These crystal proteins (Cry proteins) are insect stomach poisons that must be eaten to kill the insect. Once eaten, an insect's own digestive enzymes activate the toxic form of the protein. The Cry proteins bind to specific "receptors" on the intestinal lining and rupture the cells. Insects stop feeding within two hours of a first bite and, if enough toxin is eaten, die within two or three days (Fig. 4). For more than 30 years, various liquid and granular formulations of Bt have been used successfully against European corn borer and other insect pests on a variety of crops. There are several strains of Bt, each with differing Cry proteins. Scientists have identified more than 60 Cry proteins. Proteins have been found with insecticidal activity against the Colorado potato beetle (for example, Cry3A, Cry3C), corn earworm (Cry1Ac, Cry1Ab), tobacco budworm (Cry1Ab) and European corn borer (Cry1Ab, Cry1Ac, Cry9C). Most of the Bt corn hybrids, targeted against European corn borer, produce only the Cry1Ab protein; a few produce the Cry1Ac protein or the Cry9C protein. Why create Bt corn?Although conventional Bt insecticides may perform as well as synthetic insecticides, their performance is not always consistent. Erratic performance of Bt insecticides is attributed to:
Modifying a corn plant to produce its own Bt protein overcomes these liabilities. The protein is protected from rapid environmental degradation. Plants produce the protein in tissues where larvae feed, so coverage is not an issue. Finally, the protein is present whenever newly-hatched larvae try to feed, so the timing of Bt application is not a problem. The result is an efficient and consistent built-in system to deliver Bt proteins to the target pest (Figs. 4 & 5). How is Bt corn created?Plant geneticists create Bt corn by inserting selected exotic DNA into the corn plant's own DNA. DNA is the genetic material that controls expression of a plant's or animal's traits. Seed companies select elite hybrids for the Bt transformation in order to retain important agronomic qualities for yield, harvestability and disease resistance. Three primary components of the genetic package inserted into corn include: This genetic package is inserted into corn through a variety of plant transformation techniques (Fig. 6). Successful transformations, called "events," vary in the components of the genetic package and where this DNA is inserted into the corn DNA. The insertion site may affect Bt protein production and could affect other plant functions. Consequently, seed companies carefully scrutinize transformation events to ensure adequate production of Bt protein and no negative effects on agronomic traits. As of September 1997, the Environmental Protection Agency (EPA) has registered four unique events for commercial use: 176 (Novartis Seeds and Mycogen Seeds), BT11 (Northrup King/Novartis Seeds), MON810 (Monsanto) and DBT418 (DEKALB Genetics Corp.). Event 176 is trademarked as "KnockOut" by Novartis and "NatureGard" by Mycogen. Both the BT11 and MON810 events are trademarked as "YieldGard" and the DBT418 event is trademarked as "Bt-Xtra." Various seed companies license each event, so when purchasing seed, note which trademark is present on the seed tag and bag. The number of events is likely to increase rapidly. Understanding these events and how they affect performance is critical to the wise selection of corn hybrids. Does Bt corn work against European corn borer?Bt corn has the potential to improve European corn borer control dramatically, compared with current IPM options. Chemical insecticides, if timed well, typically provide control from 60-95% of first generation larvae and 40-80% of second generation larvae. As indicated in Fig. 7, performance of Bt corn can be dramatic when compared with non-Bt versions of the same hybrid. In field tests against natural and supplemented European corn borer infestations, Bt corn hybrids (regardless of event) provide more than 99% control of first generation European corn borer larvae in whorl-stage corn. However, the level of European corn borer control against late-season European corn borer infestations differs between Bt events. Under heavy European corn borer pressure, events BT11 and MON810 provide a higher level of control than event 176. Why? Event 176 hybrids produce Bt protein only in green tissues and pollen, whereas BT11 and MON810 events produce Bt protein throughout the plant. Because some hatching larvae initially colonize ears to feed on silks and developing kernels (Fig. 8), these larvae may survive on event 176 and may tunnel later into stalks and ear shanks. Are Bt expression differences important? Presence of late-season European corn borer in ears in event 176 can be unsettling to growers, who expect complete control of European corn borer, and is a topic of debate in resistance management discussions. Control with event 176, nonetheless, is better than insecticide options. Survival differences between events may be more critical where other late-season caterpillars (for example, southwestern corn borer and corn earworm) are serious pests. A case in point: Kansas State University trials during 1996 showed that BT11 and MON810 events provided 93% control of southwestern corn borer, while event 176 afforded only 19% control. In this situation the full-season Bt expression provided by the YieldGard[TM] events gave better control of southwestern corn borer. The Bt gene is only one of several thousand genes that affect a hybrid's yield. Growers should carefully consider all the hybrid's characteristics, particularly its yield performance. Primarily, growers should select hybrids that have consistently performed well in yield trials, especially when corn borer pressure is low. Maturity, standability, harvest moisture and disease resistance are just a few examples of other traits that growers should consider when selecting hybrids. How safe is Bt and Bt corn?The EPA considered 20 years of human and animal safety data before registering Bt corn. Bt proteins are not toxic to people, domestic animals, fish, or wildlife; and they have no negative impacts on the environment. The Food and Drug Administration (FDA) exempts Bt Cry proteins from residue analyses because of Bt's history of safety and because these proteins degrade rapidly. Are other insect pests or mites controlled by Bt corn?European corn borer is not the only insect pest attacking corn (Fig. 9). Will Bt control other corn insects? The following summary reflects known toxicity of current Bt proteins plus field and laboratory studies of Bt corn in Iowa and Kansas. Current Bt corn hybrids have virtually no activity on the following pests: aphids, spider mites, black cutworm, western bean cutworm and soil insects such as corn rootworms, wireworms, white grubs, seedcorn maggots and seedcorn beetles. Bt corn might suppress, but not control, foliar feeding pests, such as stalk borers and armyworm. Although some events have good activity on armyworm, fall armyworm and corn earworm, field studies on these pests are limited. Finally, Bt corn protection from the southwestern corn borer differs markedly between events (see discussion on Bt events). If southwestern corn borer, armyworm or corn earworm are consistent pests, ask about the availability of hybrids with specific activity on these pests. Future Bt corn hybrids may include new Bt proteins or other novel toxins that will control more pests. Indirect impacts of Bt corn on pests might occur. For example, Bt corn does not have activity on spider mites. Yet a reduction in pyrethroid use for corn borers might minimize outbreaks of spider mites. Although puzzling at first, this makes sense when one considers that natural enemies of mites are not reduced by insecticide applications in Bt corn fields. In contrast, minor pests may become more predominant, such as the western bean cutworm in western Kansas, eastern Colorado and Nebraska. Beginning with the widespread use of foliar insecticides, this insect has been a minor pest of corn. Pest status of this insect could change, though, when foliar insecticides are reduced and if this insect is not controlled by current Bt events or natural enemies. Does Bt corn affect beneficial insects and natural enemies?Many studies have shown that Bt Cry proteins are highly selective in killing larvae of moths. Bt corn, however, does not affect beneficial insects including honey bees, lady beetles, green lacewing larvae, spiders, pirate bugs or parasitic wasps (Fig. 10). Indirect effects on natural enemies of European corn borer, however, could occur. Predators, parasites and pathogens of the corn borer might decline as corn borer populations decline. Refuge areas, discussed below, may moderate these indirect effects. Unfortunately, little data on the subject exists. Bt corn fits into and complements an integrated pest management approach to farming that includes conservation of biological control agents. What are the economical benefits of Bt corn?Bt corn technology is so new that performance data from research and extension entomologists are limited. Also, few studies have compared Bt corn with other management options. Many questions remain concerning benefits of Bt corn, and whether these benefits are worth the extra cost for seed. An economic analysis of historical corn borer infestation and yield-loss data provides insight into the potential benefits of Bt corn. The following analysis examines the comparative performance of four different management strategies: do nothing, use insecticides based on scouting and economic thresholds (Fig. 11), plant Bt corn event 176, or plant Bt corn events BT11 or MON810. Net gain for each management strategy is calculated by subtracting management costs from expected benefits. Expected benefits are based on the following assumptions:
This study includes data on insecticide and Bt corn performance from several states.
Benign neglect of European corn borer costs U.S. growers about $6.57 and $12.90 per acre for first and second generation borers, respectively. An IPM approach, basing insecticide use on scouting and economic thresholds, was profitable against both first and second generation borers, $0.38 and $4.07 per acre, respectively (Fig. 12). Bt corn, however, offered much better economic advantage with returns of $2.79 per acre for all events against first generation borers. The 176 and BT11/MON810 events returned $5.74 and $8.72 per acre, respectively, against second generation borers. Analysis of historical European corn borer damage in Minnesota from 1988 to 1995 gave similar results. Estimated yield protection by Bt corn was $5.61 and $11.63 for first and second generation European corn borer control, respectively. The projected benefits, totaling $17.24 per acre, significantly exceed the current price premium for Bt corn of $7 to $10 per acre. Both the national and Minnesota projections clearly suggest that Bt corn offers a sound economic return, under the assumptions listed above. European corn borer populations fluctuate over the years and from one field to the next. Similarly, corn yields and market prices often are volatile. This variability raises concerns about fluctuations in yearly economic benefits of Bt corn. To illustrate this point, the risk of investing in Bt corn was scrutinized for southern Minnesota over an eight-year period 1988-1995. This period included three outbreak (high) years for European corn borer and five endemic (low) years. The average benefit for this period, $17.24 per acre, was very close to the national estimate of Bt value, but returns varied considerably between endemic and outbreak years (Table 1). During the endemic years, the yield protection offered by Bt corn barely covered the price premium for seed, currently $7 to $10 per acre. During outbreak years, yield savings were four to five times the added seed cost ($28 to $50 per acre). The bottom line: Do not expect an economic return every year or in every field. As with any type of natural resistance, Bt corn only delivers an economic benefit when European corn borer outbreaks occur. Unfortunately, no predictive tools for European corn borer outbreaks are currently available. Yield data on Bt corn are available from university entomologists and agronomists, and seed companies, who are conducting studies in nearly every state that grows corn (Fig. 13). As mentioned previously, yield results will depend on Bt events, specific hybrids and European corn borer infestation levels. Are there indirect benefits from Bt corn?Bt corn reduces the European corn borer population in a field and, depending on prevalence of Bt corn in the area, influences the local European corn borer population. For example, if 50% of the corn acreage is planted to Bt corn, then the corn borer population in the area could be reduced by 50%. Conceptually, this population suppression should be greatest nearer Bt corn than farther away. Neighboring corn fields could experience reduced attack by European corn borer. Movement of adult moths during each generation will influence the area and magnitude of this neighborhood effect. Conceivably, planting non-Bt corn near Bt corn could be beneficial because European corn borer populations near Bt corn fields should be suppressed. Indirect benefits may also occur through decreased incidence of corn disease. Bt corn reduces European corn borer tunnels that provide entryways for plant pathogens. Thus, stem rots and ear rots could be reduced along with mycotoxin production. Fewer dropped ears with Bt corn will mean less volunteer corn in the following year's crop. Can European corn borer develop resistance to Bt corn?European corn borer may have the potential to develop resistance to Bt Cry proteins. Insects are known for their ability to rapidly develop resistance to certain insecticides. Resistance occurs particularly when insecticides are used repeatedly and at high concentrations. More than 500 species of insects and mites have developed resistance to insecticides and miticides. A recent Midwestern example in corn includes adult western corn rootworm resistance to Penncap-M in Nebraska. In addition, laboratory colonies of more than 15 different insect pests have developed resistance to Bt proteins, including Indian meal moth, tobacco budworm, beet armyworm, pink bollworm and Colorado potato beetle. Moreover, the diamondback moth, a worldwide pest of cole crops, has developed high levels of resistance to Bt insecticide in field populations in Hawaii and Florida. Many factors contribute to the development of resistance. Some of these factors for the European corn borer include: predictions for widespread use of Bt corn, high season-long mortality, and two or more generations per year. Recent laboratory studies in Minnesota, Kansas and Delaware confirm that European corn borers (collected from Minnesota, Iowa and Kansas corn fields) can develop moderate levels of resistance to Bt insecticides or Bt Cry proteins (Fig. 14). Resistant European corn borer strains in these studies require 30-60 times more toxin (resistance ratio) to kill 50% of a test population of young borers compared with nonresistant European corn borer strains. This modest level of Bt resistance developed in relatively small lab populations after seven to nine generations of exposure. Although these results confirm the genetic potential of European corn borer to develop resistance, laboratory studies do not prove resistance will develop under field conditions. Bt corn and European corn borers in the field pose a dramatically different situation than larvae feeding on Bt insecticides in laboratory diet. How does resistance develop?Scenarios of resistance development by European corn borer are suggested by studies of insecticide resistance in many insects and by resistance to Bt insecticides by tobacco budworm and diamondback moth. In any population of European corn borers, a few of the borers will have two copies of genes for resistance (rr), some will have one copy of the gene (rs) and most will have none (ss). Resistance genes are likely to be rare. On Bt corn, European corn borer with one or more copies of resistance genes (rr or rs) could survive and produce more offspring (Fig. 15). Improved survival or reproductive success results in a "selective advantage." As the Bt corn acreage increases, and with it the proportion of the European corn borer population exposed to Bt corn, more larvae carrying resistance genes could survive to adulthood. The overall population of Bt-resistant individuals increases with each generation. At some point, control failure could occur with resistant larvae reaching infestation levels in Bt corn fields similar to levels found in non-Bt corn fields. What are the implications of European corn borer developing resistance to Bt corn?Growers and seed companies will face the primary impacts of European corn borer resistance to Bt corn. Initially, while seed companies and entomologists develop strategies for countering European corn borer resistance, producers in problem areas might lose the option to use Bt corn. Organic growers who rely on Bt insecticides also could lose a valuable management option in these areas. Resistance effects could be minor, though, if hybrids that express alternative Cry proteins are effective and if they are introduced rapidly into problem areas. European corn borers, however, could develop cross resistance to two or more of the Cry proteins. If entire groups of Cry proteins are neutralized by resistance development, growers could permanently lose Bt corn and Bt insecticides as valuable management tools. This loss would be unfortunate for organic growers and other producers who rely on Bt insecticides. In addition, the failure of a voluntary, proactive resistance management plan could create more regulatory pressure for future transgenic crop technologies. This could limit the use of a transgenic Bt approach for other high-value crops, such as sweet corn. Can development of European corn borer resistance to Bt corn be managed?The potential threat of resistance by European corn borer to Bt corn necessitates a management plan to delay or avoid the risk of resistance. Resistance management is a key element of good IPM practices. Consequently, the EPA has issued conditional registrations that require companies selling Bt corn to develop and carry out resistance management plans by 2001. Resistance management in Bt corn is currently based on two complementary principles: high dose and refuge. Plant geneticists designed Bt corn to produce very high levels of Bt Cry proteins, much higher than levels found on corn treated with Bt insecticides. The intent is to kill all European corn borer larvae with no genes for resistance (ss), plus those with one copy of a resistance gene (rs). The assumption inherent in this resistance management approach is that Bt hybrids have achieved this high-dose objective. If a high-dose objective is not achieved, then corn borer larvae with one copy of a resistance gene may survive to adulthood and mate with other resistant moths. Most of the offspring from these matings would be resistant to Bt corn. The second principle of the resistance management plan is the use of refuges. The purpose of the refuge is to provide a source of European corn borers, not exposed to Bt corn or Bt insecticides, that could mate with potential resistant moths emerging from nearby Bt corn. The goal is to produce an overwhelming number of susceptible moths to every resistant moth (Fig. 16). A refuge is any non-Bt host of European corn borer, including non-Bt corn, potatoes, sweet corn, cotton or native weeds that occur near Bt corn (within the same 1/2 section, 320 acres). The question is, "How large a refuge is needed to provide enough susceptible moths?" In any given year, approximately 20-30% of European corn borer larvae should not be exposed to Bt Cry proteins. This estimate is based on current knowledge of European corn borer biology, pesticide resistance studies and computer simulation models. To be effective, European corn borer moths must emerge from the refuge at the same time as resistant moths and be close enough to mate with resistant moths. Although some European corn borer moths can fly substantial distances, many moths fly less than a mile from their emergence site. Consequently, each farm should have one or more refuge areas next to Bt corn. Examples of possible refuge configurations are illustrated in Fig. 17. The actual amount of refuge required will vary among regions, farms, and corn production systems. Always the goal is to prevent Bt protein exposure to 20-30% of the larval population. In continuous corn and corn-soybean rotations, the primary available refuge is non-Bt corn, so 20-30% of the corn acreage should be non-Bt corn. In continuous corn areas where European corn borers are typically sprayed with insecticides, the refuge should be increased to 40% to compensate for larval mortality. Where the total corn acreage is small and much of the local European corn borer population is associated with alternative hosts that do not contain Bt proteins, a smaller refuge may be suitable. This reduction in refuge size assumes that corn borers from alternative hosts emerge at similar times as corn borers from corn. When the proportion of the local European corn borer population that flows through non-Bt hosts is unknown, a refuge of 20-30% non-Bt corn may be the simplest and best insurance to delay resistance. For specific refuge recommendations, contact local extension entomologists. Can resistance development be monitored?Monitoring for the development of resistance to transgenic plants provides information essential to managing European corn borer resistance (Fig. 18). Monitoring is necessary to learn whether a field control failure resulted from resistance or other factors that might inhibit expression of the Bt Cry protein. The extent and distribution of resistant populations can be mapped so that alternative control strategies can be adopted in areas where resistance has become prevalent. Finally, detecting resistance may be possible before control failures occur, if monitoring techniques are sensitive enough to provide complete discrimination between resistant and susceptible individuals (See Sidebar). What is the best strategy for using Bt corn?Insect control by Bt expression is only one trait that farmers need to consider in their selection of hybrids. Bt genes only protect the yield potential inherent in the hybrid. Because corn borer populations fluctuate, looking at hybrid performance over several years is important (Fig. 19). Expect yield protection with Bt hybrids when European corn borer infestations are heavy, and little to no yield protection when infestations are light. Sound preliminary choices might be Bt versions of commercial hybrids that are proven performers. Like other plant-resistance strategies, the decision to purchase Bt corn seed is made before pest population levels are known. Unfortunately, predicting when and where heavy European corn borer infestations will occur is not possible. Producers should consider using Bt corn only in areas where the economic risk from European or southwestern corn borer justifies the price premium for Bt corn. Watch Bt corn fields closely. Learn about the level of European or southwestern corn borer protection achieved with Bt corn. The best strategy for using Bt corn may be to protect fields likely to bear the heaviest brunt of European corn borer attack or fields with the highest yield potential. For example, in northern areas, the best choice may be earlier planted fields with their higher yield potential and heavier first generation European corn borer attack. Conversely, using Bt corn in later-planted, later-pollinated fields provides optimal protection against second-generation or late-season infestations. In southern areas where multiple generations of European corn borer can contribute to yield loss, protecting hybrids throughout the season may be desirable. Regional and local strategies for using Bt corn will become more refined as producers and agricultural scientists gain experience with the product. Future versions of this publication will bring together this knowledge. Transgenic crops, such as Bt corn, are at the forefront of a revolution in pest management. The concept of managing insects by a simple seed choice is a powerful one. As with any new technology, Bt corn brings mixed feelings: excitement of using new technology, desire to know more about it, apprehension about its wise use, and uncertainty about its value. In the next few years, much will be learned about how to use this powerful new tool wisely. Hopefully this new approach toward corn borer management will not falter because of resistance problems. By working together, producers, seed companies, scientists and regulators can better ensure the longevity of Bt corn.
Glossary
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