Why we use insecticides?

Why Bt GM crops has had a spectacular success?

Dangers hidden under the use of Bt crops

Strategies to reduce risks in using Bt crops

Farming and economic burdens of using Bt crops

Failures and hints in reducing risks of Bt crops

(modified from: Nina V. Fedoroff and Nancy Marie Brown - Mendel in the kitchen - The National Academies Press, 2004)

Bt-based pesticides

Bt-based pesticides [E1] [E2] have been used for more than 30 years to control a variety of insects, including gypsy moths. They are especially favored by organic farmers, who consider them natural, not synthetic. The toxins, which break down when exposed to sunlight, heat, or drying, come from a bacterium, Bacillus thuringiensis. While commonly referred to in the singular as ‘Bt,’ B. thuringiensis is actually a large group of subspecies. More than 70 subspecies (also called varieties or strains) have been identified. Each produces one or more types of “Cry” (for crystal-like) proteins in its spores. These proteins are not toxic until they come into contact with an insect’s digestive juices.

Eaten by an insect larva, the crystal dissolves. The protein is then broken apart, producing a toxic fragment. The fragment binds to a receptor on the lining of the insect’s gut. If the insect doesn’t have such a receptor, nothing happens. In insects that have these receptors, on the other hand, the cell immediately begins to swell until it bursts. The active toxin binds to proteins on the epithelial cells lining the insect’s midgut, forming pores that let potassium ions escape. Lacking potassium, the insect’s gut cells take up too much water. Within two hours the insect stops feeding; if it has eaten enough of the toxin it becomes paralyzed and soon dies. The bacterium in this way prepares its own habitat. After the larva is dead, the bacterium feeds off its body, reproduces, and makes millions of spores.

The toxin has no effect on humans because of the differences between our digestive system and that of an insect. A human’s digestive juices are highly acidic, so the crystal is not dissolved and the toxic fragment is not released.

The genes that encode Cry proteins are on a large plasmid that B. thuringiensis strains carry. And, today, several varieties of corn have been genetically engineered to incorporate a Bt gene.

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Why we use insecticides?

Plants and insects, as entomologists well know, wage ongoing chemical battles for survival. Plants produce toxic chemicals in an effort to keep insects from eating them. Insects evolve ways to evade the chemical tricks of plants. The interests of humans are generally aligned with those of the plants—we don’t want bugs getting to our food first—with one rather large exception. The chemicals that plants make to protect themselves sometimes irritate us as well. In this context, crop breeding can be seen as a means of controlling unwanted wild traits, such as toxin production, in plants destined for the table. Unfortunately, selected traits that make a plant desirable as human food also make it desirable to insects. This, in fact, is why synthetic pesticides are used: they replace the naturally occurring pesticides and related survival traits that have been bred out of food plants.

Chemical insecticides are, from an insect’s point of view, no different from the plant’s own toxins. And their widespread use in modern agriculture has had a highly predictable result: the emergence of insects that are resistant to certain pesticides. How? Through mutation. Although a mutation in just the right gene to make an insect proof against a toxin is very rare, the number of insects in nature is very large—so large that the heavy use of insecticides rapidly selects for the ones with the right kinds of mutations. All the others die, and only the few that are resistant reproduce and multiply. But those few are enough. Insects breed geometrically and, with populations that go from hundreds to billions in only days, farmers must spray a different poison from the old one, for these billions of resistant bugs.

Why Bt GM crops has had a spectacular success?

Bt crops [E3] (GMO crops), in theory, can make farming safer for farmers (and, incidentally, for insects not dangerous to crops). Because the Bt genes protect plants from within, the use of the spray rig, and the accidents that accompany that use, should be less. But farm safety is not, in fact, behind the spectacular success of Bt corn. As professors at Colorado State University explain in their handbook on transgenic crops, “Field corn is not usually sprayed with insecticides because there is some market tolerance for insect damage on this kind of corn.” It is either fed to animals or ground and processed into corn chips, cornflakes, and cornmeal, so wormholes and other blemishes are not generally noticed. Worm-eaten sweet corn, on the other hand, is hard to sell. “Sweet corn is sprayed with insecticides frequently, sometimes every two or three days, to ensure that the ears will be attractive at harvest.” But while Bt sweet corn has been approved by the EPA, it is not being grown.

Instead of replacing the chemical pesticides, Bt field corn has shown farmers the true cost of the damage done by the European corn borer. In its moth stage, the corn borer lays eggs on young corn plants, where the larvae hatch. They feed briefly on the leaves, then, as their name implies, bore into the cornstalk. The damage their tunnels do goes unseen and unchecked until, in a heavy rain or wind, the riddled cornstalk topples. Unless a farmer scouts his fields often, an infestation is easily overlooked until too late. Even the efforts of the 5 to 8 percent of farmers who did try to spray against corn borers were often without effect. Once the worm is in the corn, the poison cannot reach it. The corn borer can produce from two to four generations in each crop cycle. The only sure way to control it is to stop planting corn altogether.

Bt corn first went on sale in 1996; as of June 2002 more than a third of the field corn in the U.S. were Bt crops. Bt varieties were sold not only by Monsanto, but by Syngenta, Aventis, Mycogen (owned by Dow AgroSciences), and Pioneer Hi-Bred (owned by DuPont). Bt corn did not immediately reduce farmers’ pesticide use. As the 2000 report to Congress on the benefits, safety, and oversight of agricultural biotechnology noted, this fact “is often cited by critics of biotechnology as an example of a bioengineered crop that has not met expectations.” Rebecca Goldburg of the Environmental Defense Fund, for example, complained to Congress that “Bt corn largely supplements rather than substitutes for insecticide use on field corn.” And yet few farmers had expected Bt corn to cut their use of sprays. According to a study by Iowa State University in 1998, 82 percent of the farmers in the Midwest who had planted Bt corn that year said their primary reason for doing so was to prevent losses from the corn borer. Those losses, according to the National Center for Food and Agricultural Policy, a nonprofit research organization, were equal to 3.5 billion pounds of corn by 2001, an amount worth $125 million.

Now that the enemy has shown its face, farmers are unlikely to ignore it once again if, for any reason, Bt corn becomes unavailable. Having seen how much more corn each acre yields when corn borers are eliminated, the National Center for Food and Agricultural Policy study suggests, farmers “would be likely to take the pest more seriously and apply insecticides more frequently than in prior years.” In a typical year, the study calculates, farmers would spray an additional 2.6 million pounds of pesticide to kill corn borers if Bt corn were not available.

Dangers hidden under the use of Bt crops

Why would Bt corn become unavailable? Because of its spectacular success, entomologists have argued. Just like a chemical insecticide, Bt kills sensitive insects. Those insects with rare mutations that make them resistant to the toxin will be a larger fraction of the survivors. With the introduction of Bt genes into so many different kinds of plants (by 1999 18 crop varieties had been approved for field testing, and 16 companies were at work developing more), and with the acreage being planted in Bt crops expanding so rapidly, entomologists feared that Bt crops would select for resistance faster than anyone anticipated. An early estimate was that insects might become resistant in no more than five to seven years—or even less.

Because there are more than 170 different toxic Cry proteins, some scientists suggest that saying insects will become resistant to Bt is like crying wolf.

And yet for the company that has developed a Bt corn variety, these argument is little solace. Once insects become resistant to its toxin, a Bt crop would have no advantage over another, less expensive variety; both would need to be sprayed to protect them against the corn borer. Because developing and testing new Bt crops is fiercely expensive, it was important for companies to invest in strategies that would extend the useful life span of each Bt variety.

The EPA was also concerned. Part of its mission is to limit the environmental risks of pesticides and to promote safer means of pest management. Bt, used by home gardeners and organic farmers for decades, has a reputation for being a benign and environmentally friendly insecticide.

Bt, in fact, is the safest insecticide on the market, one that farmers are not even required to wash off of their produce before selling it. The loss of one Bt toxin, like the loss of one antibiotic, might not matter. Yet many of the Cry proteins engineered into plants are also found in Bt sprays. A bug that became resistant to the plant would also be unharmed by the spray. Consequently, a 2001 EPA report noted that the loss of a popular Bt toxin, if insects did become resistant to it, could have “serious adverse consequences for the environment”: conventional growers would have to shift to more-toxic pesticides and organic farmers would lose a valuable tool. Keeping pests susceptible to Bt, the EPA decided, was “in the public good.”

Resistance breeding is an ongoing effort for crops just to stay ahead of the ever-evolving populations of pest species. But the costs of creating a new cultivar are particularly high, in particular if it is a genetically engineered variety, like Bt corn. A four-year life span cannot recoup a company’s outlay.

Strategies to reduce risks in using Bt crops

To delay—or if possible, to avoid altogether—the onset of resistance to Bt crops, the solution followed, studied by Anthony Shelton, an entomologist at Cornell University, was the establishment of insect refuges or refugia, areas planted in conventional, non-Bt crops, within or adjacent to each cornfield.

In a refuge the pests—the corn borers in this case—are allowed to multiply. Most of them are sensitive, susceptible to the Bt toxin. A larva with the lucky mutation that makes it resistant to Bt enjoys no advantage there in the refuge, because it is never exposed to Bt. It takes its chances along with its kin and might or might not live long enough to metamorphose into a moth, fly away, and mate.

Next door in the Bt fields, however, most insects die before reaching maturity. Among those few that survive and transform into moths, there’s a much greater chance that one is resistant—simply because the others have succumbed to the toxin. But with all the normal, sensitive moths now emerging from the nearby refuge, the odds are that this resistant survivor will mate with one of them. The offspring of such a mating should be sensitive to the toxin, having one resistance allele (the gene from the resistant parent) and one sensitivity allele (from the parent from the refuge). When such a heterozygote eats a bt plant, it dies, eliminating the resistant allele from the population.

It dies, that is, if the resistance trait is recessive. This assumption has been tested by a number of researchers. They selected Bt-resistant insects and allowed them to breed in the laboratory. In almost all of the experiments, the resistance trait was, indeed, recessive. One report in 1999, however, suggested that a kind of resistance that is dominant—which wouldn’t be controlled through the use of refuges—can occasionally arise.

To test the refugia strategy under true field conditions, Shelton and his colleagues at Cornell University released diamondback moths into plots of broccoli plants carrying a Bt toxin gene. Shelton chose diamondback moths instead of corn borers for two reasons. First, the diamondback had already shown some resistance to Bt and the trait was known to be recessive. (Because the resistance was apparent by 1993, three years before any Bt crops were on the market, it was clearly a response to the Bt sprays that organic gardeners and others had used for decades.) Second, the diamondback is a warm-climate moth. The harsh New York winters would act like the walls of a greenhouse to contain the experiment: any moths that escaped the test plots would die when the cold weather came.

In 1996 and 1997 Shelton and his colleagues monitored the diamondbacks in their Bt broccoli fields. As they reported in 2000, the refuge strategy worked very well—if it was used carefully. In pure stands of Bt broccoli, with no refuge set aside, the moths quickly became highly resistant to Bt. But the larger the refuge, the longer it took for that resistance to develop. It also mattered where the refuge was. A separate, well-defined refuge, around the edges of the field or even up to a half mile away, was more effective in keeping the level of resistance in the moth population low than one created, for example, by planting every other row with the Bt crop.

The separate refuges worked as expected because although diamondbacks travel only short distances in their leaf-eating larval stage, they cover a much wider territory as winged moths looking for mates. When the two types of plants, Bt and non-Bt, were mixed together randomly in a single plot, the diamondback larvae naturally wandered from one plant to the next. The ordinary, sensitive larvae that moved onto a Bt plant and started to munch quickly died. The resistant larvae that found the same plant lived. The result was that only the resistant larvae lived long enough to become moths and breed, passing on their resistance genes. If, on the other hand, a patch of non-Bt broccoli were planted far enough away from the Bt broccoli that the larvae could not wriggle from one to the other, many sensitive larvae also lived to adulthood. Once winged, these sought out and mated with their resistant cousins in the Bt broccoli patch and, following Mendel’s laws, the recessive resistance trait was found in many fewer of their offspring. In 2001 the EPA included Shelton’s and other scientists’ recommendations in its rules for registering Bt corn.

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Farming and economic burdens of using Bt crops

In order to buy Bt corn seed, farmers must sign grower agreements or stewardship agreements, which “impose binding contractual obligations on the grower to comply with the refuge requirements”—that is, farmers who plant Bt corn but fail to establish proper insect refuges can be sued. The onus for educating farmers about proper stewardship—and for ensuring their compliance—falls on the seed company. Any company selling Bt corn seed has to monitor the success of its stewardship plan and report to EPA any “statistically significant and biologically relevant” changes in the corn borer’s susceptibility to the Bt toxin its variety expresses. It has to have ready a “remedial action plan” in case resistant insects are detected. And finally, it must submit annual reports to the EPA on its sales, its educational programs, the results of its stewardship plan, and the extent to which its farmers complied with that plan.

In the Corn Belt, the stewardship agreements between the seed company and the farmer specify a refuge that covers at least 20 percent of the farmer’s cornfields (it’s 50 percent in the South). This refuge can be laid out as whole fields, as blocks within fields (for instance, as a border along the edges), or as strips, at least four rows wide, across the field. If whole fields, they must be within half a mile (closer is better) of a Bt field.

A refuge can be sprayed for European corn borer and similar pests “only if economic thresholds are reached”; these thresholds are to be determined “using methods recommended by local or regional professionals” such as Cooperative Extension Service agents or crop consultants. Under no circumstances can the spray be any form of Bt. No conventional pesticide has such extensive—and expensive—requirements for managing insect resistance, yet as the case of the diamondback moth shows, insects respond to dusts, powders, and sprays by becoming resistant to the pesticide just as they do when eating Bt corn.

Leaving the refuge unsprayed means farmers must stand by and watch while pests eat 20 percent or more of their cornfields. This kind of compromise, between a short-term sacrifice and a long-term gain, can be hard for a farmer to make.

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Failures and hints in reducing risks of Bt crops

In 2000 a telephone survey commissioned by the major seed companies, Aventis, Dow, DuPont, Monsanto, and Syngenta, found that 29 percent of the farmers growing Bt corn “broke the rules.” The refuges they planted were either too small or too far away. Many farmers pleaded ignorance of the rules. A third of the Bt corn growers in the Midwest and more than half of those in the South couldn’t say what size of refuge was required in their area; 60 percent couldn’t say how far away the refuge should be; and two-thirds said they didn’t know they couldn’t spray it with Bt. In 2001 the situation improved somewhat: 13 percent of farmers in the Midwest’s Corn Belt and 23 percent of farmers in the South (where the restrictions are tighter because of the proximity of Bt cotton) were “out of compliance.” Still, only just over a third, when quizzed, knew the rules for making a refuge in their area. The 2002 growing season saw a closing of the knowledge gap—only 12 percent of the 550 Bt corn farmers surveyed remained unaware of the rules—but 14 percent still didn’t comply.

An independent survey by the Center for Science in the Public Interest found that 19 percent of farms did not comply. Thirteen percent planted no refuge at all. “One reason for the discrepancy,” noted the New York Times, “was that the industry surveyed only large farms. The center also looked at small farms, which had a higher rate of non-compliance.” Those small farms accounted for only 8 percent of the Bt corn grown. Yet, as the Center insisted, the requirement is for each farm, not for each county or region.

Before the Center’s report came out—and before seeds were sold in 2003—the EPA stiffened the rules. Seed companies are now required to enforce the stewardship agreements the farmers sign by conducting on-farm visits. They are required to help the farmer design an appropriate refuge, and they are required to check, the next growing season, to see if the farmer complied. Farmers who are “significantly out of compliance” for two years will no longer be allowed to buy Bt corn.

In spite of the numbers of farmers who have broken the Bt corn rules, the crop is still winning the chemical battle for survival. Approving the re-registrations of five varieties of Bt corn in 2001, the EPA noted, “Available data indicate that after six years of commercialization, no reported insect resistance has occurred to the Bt toxins expressed either in Bt potato, Bt corn, or Bt cotton products.” If the refugia rules are followed, scientists predict that the corn borer will not evolve to be resistant to Bt corn for at least 99 years. One of Shelton’s collaborators, Richard T. Roush, now at the University of California at Davis, suggests designing plants that express Bt toxins only when they are turned on by an otherwise environmentally harmless chemical spray. Or that express Bt only in certain parts of the plant.

But even without these enhancements “the success of Bt crops exceeds expectations,” concluded a study published in 2003. In laboratory and greenhouse tests, three pests have been found that are completely resistant, able to live and reproduce on Bt crops. None of these have yet been found in the field. Even pests living in Bt crop fields that have been continuously monitored for five and six years have shown no signs of an increase in the frequency of resistance.

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