Chemical insecticides in agriculture have a tarnished history, despite their promotion as magic bullets by some commercial manufacturers. In 1948, Paul Müller won a Nobel Prize for his 1939 discovery that DDT killed insects, and in the 1950s this and other synthetic toxins saw their first widespread deployment to control agricultural pests. The initial euphoria was misguided, however, as the destructive ecological effects of this broad-spectrum neurotoxin eventually became too great to ignore. Long-lasting residues from DDT become concentrated as they move up food chains, often killing songbirds and other animals as well as insects. In the 1960s, some of North America's most spectacular native species including brown pelicans, peregrine falcons, and bald eagles were driven to the brink of extinction when DDT products accumulated in their tissues and caused massive reproductive failures. Thank goodness Rachel Carson sounded her eloquent alarm in 1962, and the United States later banned this poisonous chemical, or else we might forever be facing "silent springs."
Every year, U.S. crops are showered with nearly 1 billion pounds of various pesticides, mostly for the control of insects, weeds, and fungi. Although these synthetic toxins effectively reduce populations of many crop-destructive pests, at least temporarily, most are blunt instruments of pest control. They can devastate desirable creatures, cause health concerns for humans, promote the evolution of insecticide resistance in pest species (some houseflies already had evolved DDT resistance before Paul Müller won his 1948 Nobel Prize), wreak environmental havoc, and in general divert attention from integrative, multifaceted pest-management protocols with sounder ecological footings.
For these reasons a quest began for natural biopesticides as alternatives to synthetic chemical pesticides. This effort got a huge boost with the characterization of pathogenic strains of Bacillus thuringiensis (Bt), a widely distributed soil bacterium. Known to science since 1911, this microbe houses plasmids carrying genes that produce a wide variety of natural biological toxins, each deadly to a particular insect group. For example, protein toxins fostered by the Cryl gene kill the larvae of some butterfly and moth species (Lepidoptera), those from CryIII act primarily against beetles (Coleoptera), and those from CrylV affect flies (Diptera). These toxins activate only in the special conditions of the insect gut, so they normally remain physiologically harmless to other creatures.
Because different Bt toxins kill different types of insects, they permit relatively focused biocontrol of specific agricultural pests. The traditional Bt agronomic products are powders or suspensions, sold under such trade names as Biobit, Raven, and Skeetal. They contain mixtures of bacterial spores and toxin crystals, applied to leaves or other environmental surfaces where the harmful insects feed. These Bt concoctions constitute about 1% of the total world market for agrochemicals (insecticides, fungicides, and herbicides), and they have been used in diverse applications ranging from suppression of the Colorado potato beetle to attacks on the blackfly vectors of some tropical human diseases such as river blindness (onchocerciasis).
Bt powders have revolutionized pest-control practices in agriculture, but these biological agents have some drawbacks. First, Bt toxins applied to external surfaces are ineffective against insects that bore into plant tissues or attack roots. Second, Bt powders can contaminate nontarget surfaces, affecting other insect species. Third, pest populations can evolve resistance to Bt toxins, especially when the latter are applied one toxin at a time and in low doses. For example, mosquitoes in some tropical countries evolved resistance to Bt toxins within one or two years of their widespread application, as did diamondback moths (a serious crop pest) in Hawaii and Florida. Resistance to Bt toxins also has emerged in experimental laboratory populations of more than 25 insect pest species.
In attempts to overcome some of these shortcomings, genetic engineers have inserted various Bt-toxin genes into a wide range of crops such as corn, cotton, potatoes, and soybeans. More than 100 patents now exist for such GMOs. In each transgenic crop, the production and deployment of Bt toxins in effect are shifted from an exogenous source (a chemical factory) to an endogenous source (the living plant itself). The Bt toxins expressed in the tissues of transgenic crops have proved effective against numerous pest species.
All of which brings us to Bt-engineered corn and its role in efforts to control the European cornborer, Ostriwia «wbf/a/ii. This moth species probably arrived in the United States in the early 1900s, inside Hungarian or Italian cornstalks used to make brooms. It has become North America's leading corn pest, reducing total yields by as much as 25% and causing annual losses exceeding $1 billion. Uncontested, the moth larvae bore into a plant's tissues, breaking stalks and producing poor cob growth and dropped ears. However, a larva that takes even a few bites from a Bt-transgenic plant soon dies of intestinal obstruction.
Bt-engineered corn offers several advantages over traditional Bt powders. First, the transgenic toxin is perfused throughout the plant's tissues, so it attacks cornborer larvae where they live and feed. Second, the toxin is displayed continually (although this is a mixed blessing; see below), so the time and expense associated with the reapplication of powders to the crop are avoided. Third, transgenic plants display the toxin at higher and more effective doses than Bt powders. So, overall, Bt corn can pay significant dividends to farm productivity, particularly in years of heavy corn borer infestation.
In addition to the direct production boosts, the environmental promises of Bt-engineered corn are staggering. Currently, about 250 million pounds of chemical pesticides—more than for any other crop—are applied annually to corn fields in the United States. To the extent that transgenic strains or culti-vars of Bt-engineered corn diminish the need for these environmental poisons, the GM plants could be a wonderful step toward ecologically sound agricultural practices. According to the EPA, some Bt-engineered crops have significantly reduced the amount of chemical insecticides sprayed on the American landscape. However, a recent assessment of agricultural practices in the American Midwest revealed that corn farmers used just as much chemical insecticide on Bt corn as on regular corn, apparently seeing the Bt corn merely as a safety net in the event of a cornborer outbreak.
There are some other potential concerns as well. One is a flipside of the aforementioned benefit that Bt toxins are expressed constitutively in transgenic corn. Unlike Bt powders that have a short halflife and can be sprayed to coincide with pest outbreaks, the endogenous toxins in a field of Bt-engineered corn are present continually, and this can have ramifications for the evolution of Bt resistance in corn borers. Inevitably, insect pests exposed continually to high doses of Bt are under strong selection pressure to evolve Bt resistance. The threat is not merely academic; some laboratory populations of corn borers exposed to Bt proteins for several generations have evolved a capacity to withstand Bt toxins at levels 30—60 times greater than their non-resistant ancestors.
At the time of this writing, full-blown resistance has not emerged in natural populations of corn borers, but this eventuality is feared deeply, especially by organic farmers who long have relied on the periodic application of Bt powders as a highly successful means of biocontrol. If pest resistance to endogenous Bt toxins emerges in GM crops that are planted widely, this could compromise not only the entire transgenic Bt approach, but also the proven use of exogenous (non-GM) Bt powders as effective biopesticides.
A second concern about Bt-engineered corn emerged in 2000, when approximately 800 retail corn products (such as taco shells) were recalled from U.S. grocery shelves. The culprit was StarLink corn, engineered by Aventis CropScience to contain a CrylX Bt toxin. Because StarLink contained a transgenic protein that might elicit an allergic reaction in some people, this strain had been approved only for use as animal feed. However, the CrylX protein somehow made its way into the human food supply. Whether this occurred via seed-lot contamination or as a hybrid-mediated movement of the CrylX gene into other corn strains was unclear, but either way the economic repercussions were huge (exceeding $1 billion total). Later, the EPA ruled that Bt corn is safe for human consumption, but the StarLink name was tarnished and, most likely, the strain will never again be planted.
A third concern is that corn-delivered Bt toxins might kill nontarget insects both on and off the plant. Most available varieties of transgenic corn express Bt toxins in pollen as well as in ears and stalks. These pollen grains disperse widely and may be consumed, intentionally or inadvertently, by other insects. Thus, beneficial insects might be impacted by Bt pollen from transgenic corn, as might populations of some insect-eating birds or other insectivorous species if their food supplies thereby were diminished.
In 1999, a short research note generated much media attention. It showed experimentally that larvae of the monarch butterfly (Danaus plexippus) may die when fed milkweed leaves dusted by pollen from Bt corn. Monarchs specialize on milkweed plants, which are common near corn fields throughout the central United States. However, follow-up studies on the larvae of this and other butterfly species revealed no significant mortality effects of Bt corn pollen under more realistic field conditions. The authors of these latter studies concluded that any impacts of Bt corn pollen on nontarget insect species are likely to be negligible when compared to other mortality factors.
Despite great promise (and ardent promotion by agribusiness), it remains to be seen whether Bt-transgenic corn will be a lasting panacea for control of corn borers and other maize pests. Any long-term success may depend in large measure on the extent to which the approach is adopted not in isolation, but rather as one ingredient of integrated pest management.
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