Response from Obrycki and colleagues:
We agree with our colleagues (Ortman et al.) that the appropriate use of Bt transgenic corn can be one component in an economically and ecologically sound management program for lepidopteran corn pests. However, we disagree that the current use of Bt corn represents ecologically based management of lepidopteran pests of corn. We argue that planting 20%–30% of the corn acreage with Bt corn as a prophylatic treatment for lepidopteran pests is not ecologically based management. This approach is analogous to continuous spraying of up to 30% of the field corn in the United States with a selective insecticide every year, just in case there is an infestation by a lepidopteran pest.
We acknowledge that this technology is relatively new, and that data being collected will provide a clearer understanding of the benefits and risks of transgenic Bt corn. For example, a recent study has determined that nine transgenic Bt corn hybrids, developed from two separate transformation events, have significantly higher lignin levels than isogenic hybrids (Saxena and Stotzky 2001). We welcome the engagement of our colleagues in meaningful discussions of this technology and its role in pest management. We respond to several aspects of the letter from Ortman and colleagues to clarify points made in our original paper.
In Obrycki et al. (2001) we stated that “most corn hybrids already have substantial resistance to corn borers.” We do not believe that this statement means that we “claim that traditional plant breeding has developed corn plants that adequately protect against European corn borer.” Unfortunately, shooting at a straw man that has very little relation to original statements is all too common a tactic in scientific discourse (Collins and Pinch 1998), and it is of particular concern regarding an issue as important as the appropriate use of biotechnology (Shelton and Roush 1999). Corn plants express varying levels of resistance at different life stages, a fact that plays a vital role in the management of corn borers. In addition, modern corn hybrids have relatively high levels of tolerance to corn borer feeding. The combination of partial resistance and tolerance in modern corn hybrids contrasts with “the nearly complete protection provided by Bt corn.” Is complete protection—virtually 100% mortality of corn borers—a goal of ecologically based pest management?
Human-derived selective forces have been identified as one of the most important evolutionary factors on the planet (Palumbi 2001). Recently, the molecular bases of two different Bt resistance mechanisms were identified (Gahan et al. 2001, Griffitts et al. 2001). Planting approximately 25% of the corn in the United States with Bt corn that causes almost 100% mortality of corn borers does not appear to be a wise use of this biotechnology from either an ecologically based approach for population management or an evolutionary perspective relative to maintaining suseceptible genotypes of the pest.
Ortman and colleagues state that the use of Bt corn over the last 5 years has reduced the level of insecticide use. This is puzzling, because Carpenter and Gianessi (2001) state that “attributing any observed changes in insecticide since 1995 to the introduction of Bt corn is necessarily problematic for several reasons.” One difficulty in demonstrating any difference in insecticide use is that the level of insecticide use before the introduction of Bt corn was minimal (Rice and Ostlie 1997, Wintersteen and Hartzler 1997, Carpenter and Gianessi 2001). For example, from 1995 to 1998, 1%–2% of the corn grown in Iowa was treated with insecticides for corn borer infestations. If Bt corn is replacing insecticides, we might expect 2% of the corn to be planted to transgenic Bt corn. Furthermore, Ortman and colleagues cite data that indicate only 26% of growers who planted Bt corn in 1998 actually used less insecticide to control the European corn borer (Hellmich et al. 2000).
As stated by Rice and Pilcher (1998), the economic benefits of this technology will vary with a number of factors related to levels of corn borer infestations, value of field corn, and cost of transgenic Bt seed. Ortman and colleagues cited the following from the National Center for Food and Agricultural Policy Web site (Carpenter and Gianessi 2001): In “10 of the 13 years between 1986 and 1998, European corn borer infestations…were such that corn growers would have realized a gain from planting Bt corn.”Extracting this single phrase out of context presents several potential misconceptions. If data for 1999 are added, then some farmers would have made a profit in 10 of 14 years. We emphasize the word “some,” because even in years with relatively high European corn borer levels, many fields will not exceed economically damaging levels. Recent evaluations of Bt transgenic corn have not demonstrated consistent economic benefits (Hyde et al. 1999, Archer et al. 2000). We believe that the data collected over 2 years in replicated field studies under natural infestations of corn borers (Rice 1998, Farnham and Pilcher 1998), as cited in our paper, are some of the best data to evaluate the performance of transgenic Bt corn hybrids in comparison with nontransgenic lines. Carpenter and Gianessi (2001) summarize data showing that in 1997 there was a net benefit for Bt corn, but in 1998 and 1999, when the percentage of Bt corn planted increased from 18% to 26 %, there was an aggregate net loss for growers who planted transgenic Bt corn.
Ortman and colleagues state that Bt corn hybrids that are being widely planted do not appear to have major effects on monarchs outside of corn fields because of the relatively low expressions of Bt toxins in their pollen. The conclusion that Bt corn poses negligible risk to monarchs rests on the assumption that monarchs consume only pollen and not other corn tissue (Hellmich et al. 2001). However, within cornfields both pollen and anthers are deposited on milkweeds, which are relatively common in cornfields (Hartzler and Buhler 2000, Oberhauser et al. 2001). Milkweeds growing in agricultural fields are a major food source for monarchs in the midwestern United States (Oberhauser et al. 2001). Corn anthers contain higher levels of Bt toxins compared to pollen, and when studies have considered mixtures of pollen and anthers, negative effects on monarch larvae have been reported (Losey et al. 1999, Jesse and Obrycki 2000, Hellmich et al. 2001). Field observations and experimental evidence suggest that monarchs may be exposed to higher levels of corn anther material than previously assumed. The incidence of transgenic Bt corn anthers on milkweed plants in cornfields and previous studies demonstrating detrimental effects of pollen–anther mixes on monarch larval survival and development (Losey et al. 1999, Jesse and Obrycki 2000) suggest to us that questions about the nontarget effects on monarchs and other lepidopteran species require further examination.
Ortman and colleagues list species included in EPA nontarget testing of transgenic Bt corn. We note that the monarch butterfly, Danaus plexippus, and the black swallowtail, Papilio polyxenes, two species that occur in and near cornfields in the midwestern United States, were not included in the initial EPA tests. These omissions demonstrate the need to broaden EPA testing to consider organisms in a more ecologically based approach that goes beyond a strict toxicological view of potential nontarget effects. In addition, we question a registration process that approved event 176 transgenic Bt corn, which produces relatively high levels of Bt toxin in pollen. Studies have shown negative effects of this pollen on the survival and development of monarch larvae and sublethal effects on growth of black swallowtail larvae (Jesse and Obrycki 2000, Hellmich et al. 2001, Zangerl et al. 2001). Fortunately, event 176 has not been widely planted because of temporal reductions in expression of the Bt toxin in leaves and stems. Does this example show that the EPA system works, because event 176 will probably not be re-registered, or that the EPA system failed to identify potential nontarget effects from relatively high levels of Bt toxin expression in event 176 pollen?
Finally, although the letter above has numerous signatories, it is important to note that there is not, as Ortman and colleagues state, “concurrence within the scientific community that there are real benefits” stemming from the use of Bt corn to control the European corn borer. While we readily agree that there are some potential benefits, we also believe, along with other scientists, that more research is necessary before concluding that potential benefits outweigh potential risks (Hails 2000, Wolfenberger and Phifer 2000, Marvier 2001, Letourneau and Burrows 2001). We conclude by restating the final two sentences of our article (Obrycki et al. 2001): “We are not advocating the elimination of Bt corn, nor do we discount the potential benefits of biotechnology for agriculture. We do argue, however, that a balanced examination of Bt corn suggests ways to improve the regulatory process and to incorporate this technology into an integrated control framework, and we caution against the acceptance of yet another silver bullet for pest management.”
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