Journal or Publishing Institution: Proceedings of the National Academy of Sciences
Study: https://web.archive.org/web/20180814151605/http://www.pnas.org/content/98/21/11908.full
Author(s): Zangerl, A.R., McKenna, D., Wraight, C.L., Carroll, M., Ficarello, P., Warner, R. and Berenbaum, M.R.
Article Type: Peer Reviewed Study
Record ID: 1651
Abstract: The widespread planting of corn genetically modified to produce Bacillus thuringiensisendotoxin has led to speculation that pollen from these fields might adversely affect nearby nontarget lepidopterans. A previous study of Bt corn engineered with Monsanto event 810 failed to detect an effect of pollen exposure on the black swallowtail, Papilio polyxenes, in either the field or the laboratory. Here, we report results of a field study investigating the impact of exposure to pollen from a Bt corn hybrid containing Novartis event 176 on two species of Lepidoptera, black swallowtails and monarch butterflies, Danaus plexippus. Nearly half of the 600 monarch larvae died within the first 24 h; this and subsequent mortality was not associated with proximity to Bt corn and may have been due in part to predation. Survivorship of black swallowtails was much higher than that of the monarchs and was also independent of proximity to the transgenic corn. However, despite five rainfall events that removed much of the pollen from the leaves of their host plants during the experiment, we observed a significant reduction in growth rates of black swallowtail larvae that was likely caused by pollen exposure. These results suggest that Btcorn incorporating event 176 can have adverse sublethal effects on black swallowtails in the field and underscore the importance of event selection in reducing environmental impacts of transgenic plants. With the exception of herbicide-tolerant soybeans, Bt corn (Zea mays engineered to express genes from the soil bacterium Bacillus thuringiensis that encode the insecticidal protein toxins Cry1Ac, Cry1Ab, or Cry9C) is the most widely grown transgenic crop plant in the United States. In 1999, Bt corn was planted on 9.6 million hectares. The principal target species for Bt corn is the European corn borer (ECB), Ostrinia nubilalis, one of the most damaging pests of corn in North America (http://www.extensionumn.edu/Documents/D/C/DC7055.html). Losses to ECB damage and costs of control range upward of $1 billion annually in the United States. In addition to direct damage, ECB damage leaves corn vulnerable to infection by Fusarium fungi; these pathogens can produce highly toxic fumonisins, which pose a risk to human health if ingested. Although Bt corn has been touted as an environmentally friendly alternative to the synthetic organic insecticides traditionally used for ECB control in sweet corn (including permethrin, bifenthrin, lambda-cyhalothrin, and methyl parathion), concerns have been raised that there may be adverse effects of Bt corn use on nontarget lepidopterans and their consumers. In a laboratory feeding study, Losey et al. demonstrated that exposure to Bt corn pollen can cause mortality in neonate monarch caterpillars (Danaus plexippus). Despite the fact that the authors cautioned that “it would be inappropriate to draw any conclusion about the risk to monarch populations in the field based solely on these initial results,” the study created a widespread perception of risk, particularly among nonscientists. In a second study, Hansen-Jesse and Obrycki fed milkweed foliage, which was “naturally dusted” under field conditions with pollen from Bt corn, to monarch caterpillars in laboratory feeding trials; they reported significantly greater mortality of larvae that consumed foliage contaminated with Bt pollen, although no dose-dependent effect of pollen concentration was observed. To date, the only published study done to examine the consequences of exposure to Btcorn pollen on nontarget lepidopterans in the field is Wraight et al. In this study, which dealt not with D. plexippus but rather with Papilio polyxenes, the black swallowtail, no mortality could be directly attributable to exposure to MON810 corn pollen under field conditions. How representative P. polyxenes is of nontarget lepidopterans that live alongside cornfields is an open question. In a companion laboratory experiment, however, these authors demonstrated that P. polyxenes is sensitive to pollen from Novartis event 176, which contained 40-fold higher concentrations of endotoxin than does MON810. Environmentalists as well as government regulators are calling for more detailed studies on possible nontarget impacts of Bt corn. In the Federal Insecticide, Fungicide and Rodenticide Act Scientific Advisory Panel Report No. 99-06, released February 4, 2000 (http://www.epa.gov/scipoly/sap/1999/december/report.pdf), “Characterization and non-target organism data requirements for protein plant-pesticides,” the Panel concluded that current nontarget testing requirements were inadequate, in that they were limited in terms of species numbers, and called for “additional research . . . on the various possible effects of plant pesticidal proteins on non-target insects.” Here, we report the results of a study comparing responses of two different nontarget species with larval ecologies that place them at risk of exposure; both the black swallowtail P. polyxenes and the monarch caterpillar D. plexippus feed on weedy forbs that are frequently found in or around cornfields throughout the Midwest. Moreover, for the first time, we document sublethal effects of Bt corn pollen on growth and development of P. polyxenes in the field.
Keywords: Cry1Ac, Cry1Ab, Host, Growth, Oviposition, Behaviors, Corn, Black Swallowtail (Papilio polyxenes), Plants, Pastinaca sativa (P. sativa), Monarch Butterflies (Danaus plexippus), Infection, Acetone, Protein, Water, Exposure, Mortality, Leaf; Zea mays, Transgenic Plants, Bacillus thuringiensis, Bacterial Toxins, Crystal Proteins, Gene Expression, Pollen, Nontarget Organisms, Papilio polyxenes, Field Experimentation, Adverse Effects, Illinois; Animals, Bacterial Proteins, Bacterial Toxins, Butterflies, Endotoxins, Female, Hemolysin Proteins, Biological Pest Control, Genetically Modified Plants
Citation: Zangerl, A.R., McKenna, D., Wraight, C.L., Carroll, M., Ficarello, P., Warner, R. and Berenbaum, M.R., 2001. Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. Proceedings of the National Academy of Sciences, 98(21), pp.11908-11912.