Bt corn pollen impacts on nontarget lepidoptera: assessment of effects in nature.

T demonstrations by Losey et al. (1) and Hansen and Obrycki (www.ent. iastate.eduyentsocynch 99yprogyabsy D81.html) that milkweed leaves dusted with heavy concentrations of Bt corn pollen are toxic to Monarch butterfly larvae (Danaus plexippus) feeding on them were consistent with the known toxicity of Bt endotoxin to Lepidoptera in general and the expression of Bt endotoxins in the pollen of the strains of corn they studied. Much speculation and some investigations followed, concerning the extent to which the poisoning of Monarch butterflies and other nontarget Lepidoptera might be significant contributors to the mortality of these insects in nature. For example, Shelton and Roush (2) were critical of the two earlier findings, but did not provide any data from nature, despite the fact that Losey et al. (1), in the original report, stated ‘‘it would be inappropriate to draw any conclusions about the risk to Monarch populations in the field based solely on these initial results.’’ In a recent issue of PNAS, Wraight et al. (3) reported their experiments with populations of black swallowtail larvae (Papilio polyxenes) under field conditions. The food plants were located at varying distances from plantings of Bt corn; the authors found no effects on the mortality of the larvae. These results demonstrated that Bt corn pollen from this corn strain is not toxic to this species of butterfly at levels observed in the field no matter how close the larval food plants were to the pollen-shedding corn plants. It has not been demonstrated, however, that Monarch butterflies and black swallowtails are equally susceptible to Bt endotoxins. Further, the pollen of the corn strain 176 used by Hansen and Obrycki (www.ent. iastate.eduyentsocynch 99yprogyabsy D81.html) in their experiments with Monarch butterf lies was demonstrated by Wraight et al. (3) to be lethal to black swallowtail larvae in the laboratory, whereas the pollen of the strain they used in their field experiments, with 1y40 of the Bt endotoxin level of strain 176, was not. Studies of the effects of corn strain 176 pollen on both black swallowtails and Monarch butterflies in the field are underway in the summer of 2000. For their original report, Losey et al. (1) used still a different corn strain, N4640. At any event, the level of Bt endotoxin in the pollen of the particular corn strain, as expected, has a direct effect on the survival of black swallowtail larvae in the laboratory and presumably on the larvae of other butterf ly species as well. It has not been demonstrated whether different species of butterflies have varying levels of tolerance to Bt toxin, but they probably do, as demonstrated with other toxins. Taking the overall picture into account, the effect on the survival of butterfly populations of Bt corn pollen dusting their larval food plants appears to be relatively insignificant compared with other factors. For example, the high productivity of U.S. agriculture is made possible by the application of insecticides, herbicides, and fungicides. Despite the yearly application of about 115 million kilograms of pesticides to control insect pests, other plant pathogens, and weeds on corn, these pests continue to reduce potential corn yields by nearly one-third (4). Consequently, corn receives more pesticide treatments than any other U.S. crop. If untreated, corn rootworm can reduce corn yields by 45% and the European corn borer by as much as 20%. The corn rootworm can be controlled with insecticides by rotating corn with non-corn crops, or by newly developed genetically modified strains of corn that have not yet reached the market. The corn borer, however, is a difficult pest to control with contact insecticides, because once the larvae have burrowed into the corn stalks, they are impossible to kill by conventional spraying techniques (5), the basic reason that Bt corn has so rapidly become popular in the U.S. and to a limited extent elsewhere. Using Bt corn makes it possible for farmers to avoid the critical timing of the insecticide applications that is necessary to control corn borers (5). In evaluating the use of Bt corn and its possible environmental damage, it is important to take into account the serious public health and environmental damage caused by the use of pesticides in U.S. agriculture generally. Human pesticide poisonings are a major health concern, with a reported 110,000 nonfatal pesticide poisonings reported each year (6), together with an estimated 10,000 cases of cancer and numerous other public health problems (7). Although 97–99% of the foods sampled in supermarkets in the U.S. have acceptable or tolerable pesticide residue levels that for the most part do not constitute health hazards, approximately 35% of such foods do have detectable pesticide residues (7), a condition that most of us would wish to avoid. In addition to the demonstrated and potential health problems associated with their use, pesticides cause widespread and serious environmental effects. An estimated 70 million birds are killed each year in the U.S. alone as a result of pesticide use (7), and billions of insects, beneficial and harmful, are also killed. These include incalculable numbers of insects that are vital to our fruit and vegetable pollination, useful biological control agents, and many others. It has been estimated that such environmental losses cost the public about $1 billion each year; they are without doubt a major factor in determining the population levels of the insects concerned. Considering the enormous damage caused to human health and to biodiversity through the application of pesticides, it is clear that all efforts should continue to improve crop productivity while reducing the amounts of pesticides applied. In this connection, plants genetically modified to produce Bt endotoxin or other toxins clearly have an important role to play. The environmental effects of Bt endotoxin, freely sprayed or produced by genetically modified corn and other crops, have been assessed for many years, should continue to be evaluated. Many steps can be taken to ameliorate the potential prob-