Bt or not Bt ... Transgenic Corn vs. Monarch Butterflies

John Losey thought his Nature paper might attract some attention, but not the media "whirlwind" of "a good 60 calls" that disrupted his life for a few days. Losey, assistant professor of entomology at Cornell University, "expected to be busy, but not quite this busy." What prompted the fuss? By claiming that a gene for a Bacillus thuringiensis (Bt) toxic protein makes corn pollen poisonous to Monarch butterflies,1 Losey's team ignited another round in the volatile politics of genetically modified foods. Scientists, biotech critics, and industry spokespersons exploded with comment. Even Nature Editor Philip Campbell got into the act in an urgent E-mail message to journalists, emphasizing that the BBC notwithstanding, Losey's paper was indeed peer reviewed. Transgenic corn containing Bt genes is resistant to ravenous larvae of the European corn borer and corn earworm. The insects die when the Bt toxins in corn tissues bind to digestive tract receptors. Annual U.S. damage from corn borer alone adds up to nearly a billion dollars, so the use of Bt is a major advance. By reducing reliance on expensive conventional pesticides, Bt varieties are sweeping the U.S. corn belt, accounting for 30 percent of 1999 corn acreage, according to industry estimates. Bt use is spreading to other crops too, including cotton and potatoes. But widespread use of Bt has its downside in the form of potentially resistant insects and a threat to helpful or endangered species, including the Monarch, which calls the corn belt its summer home. That's where Losey comes in. Monarch caterpillars dine on milkweed plants growing near corn fields, so Losey's team simulated field conditions by dusting moistened milkweed leaves in the laboratory with pollen from a Bt hybrid sold by Novartis Seeds of Research Triangle Park, N.C. They then fed the leaves to caterpillars. After four days, only 56 percent of the larvae survived--high mortality compared to caterpillars munching on leaves with nontransgenic pollen or no pollen at all. And surviving caterpillars were pretty scrawny, weighing on average less than half the controls. Given the notoriety of genetically modified foods, no wonder the pollen hit the fan. Photo: Kent Loeffler, Cornell University Monarch caterpillars on a milkweed leaf dusted with pollen But how well did Losey's experiments mimic real-life field conditions? According to butterfly maven Camille Parmesan, assistant professor of integrative biology at the University of Texas in Austin, efforts are under way to preserve remaining Monarch habitat along corn belt creeks and byways. Bt-containing pollen drifting into these sites could be counterproductive. Pioneer Hi-Bred International of Des Moines, Iowa, a key player in Bt corn, maintains that "for many areas of North America, the peak feeding time for Monarch larvae occurs prior to the peak times of corn pollen shedding"--a line also taken by the Biotechnology Industry Organization (BIO) in Washington, DC. Losey himself readily points to potential problems in his study. For example, he applied pollen in amounts that "visually matched" densities seen in field material. But few data are available on how much corn pollen actually lands on milkweed plants at various distances from fields. A BIO press release noted that "ongoing monitoring of Bt corn fields ... shows that very little pollen lands on adjacent milkweed leaves." Laura Hansen and John Obrycki of Iowa State University recently reported that levels of pollen on milkweed rapidly decline only 3 meters from a Bt corn field.2 When they fed Monarch larvae leaves from the corn field's edge, 19 percent died--a lot less than Losey's 44 percent. According to Jay Pershing, research entomologist and product launch manager at Monsanto Corp. in St. Louis, which markets Bt corn and licensed the YieldGard® system used in the hybrid Losey's group tested, the company's research "made us conclude that we wouldn't have an effect on Monarchs in the field," especially since Bt toxin in pollen is below 0.1 parts per million, a level that stunts corn borers but doesn't kill them. Says Pershing, "the next step is to look at experiments in the field ...; it's absolutely certain there will be studies this summer to address this." Some want to know why intensive studies weren't already done with a product of major potential ecological significance. Bt corn has been tested on a tiny fraction of the world's insects, and many more remain to be discovered. As Bt technology spreads to other crops, including fruit and timber trees, more serious problems may arise. Still, the Monarch flap may be a tempest in a corncob. Richard Meagher, a professor of genetics at the University of Georgia who genetically modifies plants for bioremediation, thinks Bt critics "have completely lost perspective." Bt crops involve a "couple of orders of magnitude less exposure to toxins" compared to wholesale spraying of fields with conventional insecticides or Bt preparations. Adds Meagher, "There are no perfect solutions, but this is so superior ecologically." Even ecologists and butterfly people admit that Bt is not the main threat to Monarchs. Says Parmesan, "What's causing most change in numbers is habitat loss," particularly in Mexico, where the butterflies migrate. An industry spokesperson was even more blunt: More Monarchs are killed by cars and trucks than by Bt corn. Solutions? If Bt toxin poses even a small threat to biodiversity, the problem could be fixable. Michael Adang, Bt pioneer and professor of entomology at the University of Georgia, is investigating "why Bt toxins kill some insects and not others." He'd love to find "a rational way of selecting toxins based on binding sites in the insect." Scientists include a short segment of DNA called a promoter ahead of each Bt gene to control its activity in the plant. Commercial Bt genes are driven by various promoters. It may be possible to find another one that reduces or eliminates pollen expression. Meagher thinks, perhaps optimistically, that if the right promoter drives Bt, "you wouldn't see a trace in pollen." The trick is finding it. "A lot of genes on here are also on in pollen." A group from Auburn University in Alabama and North Carolina State University in Raleigh recently announced another strategy: putting Bt genes into the chloroplast genome.3 Since a leaf cell loaded with chloroplasts contains as many as 100,000 copies of the organelle's DNA, elevated toxin zaps insects that happen to take a bite. But pollen's tiny, unspecialized plastids may be relatively inactive, so toxin may be minuscule to nonexistent. Team member Henry Daniell, now professor of molecular biology and microbiology at the University of Central Florida in Orlando, seems confident that "no Bt insecticidal protein will be expressed in pollen when Bt genes are introduced via the chloroplast genome." Jeffrey Palmer, professor of biology at Indiana University in Bloomington, agrees: "I would expect very low levels, if any." Unfortunately, expression of plastid genes in pollen is still a black box. "Nobody really knows what's happening in pollen," says Joseph Mascarenhas, biology professor at the State University of New York in Albany, an opinion echoed by other researchers. That makes any biotech application still tenuous. "Right now it's not a commercially enabling technology, but it's being worked on by us and other companies," notes Monsanto's Pershing. If Monarchs will only stop eating for awhile, help may be on the way. Barry A. Palevitz is a contributing editor for The Scientist. J.E. Losey et al., "Transgenic pollen harms Monarch larvae," Nature, 399:214, May 20, 1999. L. Hansen, J. Obrycki, "Non-target effects of Bt corn pollen on the Monarch butterfly (Lepidoptera: Danaidae)," Abstract D81, Annual Meeting, North Central Branch of the Entomological Society of America, 1999. M. Kota et al., "Overexpression of the Bacillus thuringiensis (Bt) Cry2A2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects," Proceedings of the National Academy of Sciences, 96:1840-5, March 2, 1999.

Bt or not Bt ... Transgenic Corn vs. Monarch Butterflies

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