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Early studies
2001 PNAS Studies-- How were they funded?
Findings of the PNAS studies
Who's Who?

Several varieties of corn and cotton have been genetically engineered to resist attacks from the larvae of Lepidopteran insects-- the family that includes moths and butterflies. The larvae of monarch butterflies (and most other butterfly species) do not feed directly on corn or cotton, so USDA regulators initially had no reason to suspect that the genetically engineered varieties could cause them harm. A report published in Nature in May 1999 suggested that if corn pollen were to blow onto milkweed leaves-the sole source of food for monarch larvae-that the larvae could be harmed by inadvertently consuming the pollen (1). The Nature study demonstrated that monarch larvae, when fed milkweed leaves dusted with genetically engineered corn pollen, had reduced growth rates and were less likely to survive to adulthood.

The Nature study was widely reported. Critics of genetic engineering cited the study as an example of the potential, difficult-to-predict harms of the new technology (the monarch has become a mascot of the anti-GE movement). Others criticized the laboratory study as not particularly representative of "real world" conditions. A host of other factors might mitigate the impact on butterflies in nature: monarchs might never be exposed to the levels of pollen used in the Nature study (which were not quantified), little was known about the distribution of milkweed populations in relation to corn fields, the timing of pollen shed might not overlap with vulnerable larval stages, etc. Some even dismissed the reported harm to monarchs as "a rumor" (2). Nonetheless, a second study published in August 2000 confirmed the initial findings, this time using corn pollen naturally-deposited on milkweed (3).
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After the initial finding, in December 1999 the EPA requested researchers to submit data clarifying the risk of Bt-corn pollen to monarchs. The following February, a USDA-sponsored Monarch Research Workshop outlined research priorities, and in April a "steering committee" chosen at the workshop selected projects to be funded. The committee included Adrianna Hewings (USDA-ARS), Eldon Ortman (Purdue), Mark Scriber (Michigan State University), Eric Sachs (Monsanto), and Margaret Mellon (Union of Concerned Scientists). A grant pool to fund the chosen proposals was created from contributions by the USDA-ARS and committee representing several biotech companies (Aventis, Dow, du Pont, Monsanto, and Syngenta). Some of the researchers had additional funds from: the Canadian Food Inspection Agency, Environment Canada, the Ontario Ministry of Agriculture, Food, and Rural Affairs, the Ontario Corn Growers' Association, the Maryland Agricultural Experiment Station, and the Leopold Center for Sustainable Agriculture.

The results of these studies were published in the Proceedings of the National Academy of Science (PNAS) in September, 2001.
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• Exposure

To determine the amount of corn pollen naturally found on milkweed leaves, researchers measured pollen levels in and around corn fields in Iowa, Minnesota, Wisconsin, Ontario, and Maryland, at the time that corn plants were shedding pollen (4). Average pollen concentration within the fields was 170.6 grains per square cm, and dropped off to 14.2 grains per square cm two meters outside the field. 95% of all samples had pollen densities below 600 grains per square cm. Researchers found that one rain shower washed away 54-86% of the pollen, and because of this, upper leaves on a plant (where monarch larvae tend to feed) had 30-50% less pollen than middle leaves.

A second paper (5) demonstrated that most monarchs from the upper midwest are produced in around cornfields, as opposed to other natural habitats. In northern regions (Minnesota and Ontario), there is a substantial overlap in time between corn pollen shed and monarch growth, but less overlap in more southern regions (Iowa and Maryland), where corn sheds its pollen much earlier in the season.

• Toxicity

There are several different commercially available varieties of Bt-corn, many of which produce slightly different Bt-toxin proteins. Using both purified toxin proteins and pollen collected from every available variety, researchers measured the impact on monarch larval growth and mortality when fed a diet including these toxins (6). The toxin concentrations fed to the larvae were representative of actual pollen concentrations observed in the field (4), including samples with more than 1600 grains per cm2. Researchers discovered that, although some versions of the purified Bt-toxin were more toxic to monarch larvae than others, only one pollen source appeared to be consistently toxic to larvae: pollen from the "Event 176" hybrids. At the time of the studies, corn hybrids carrying the "Event 176" trait were grown on less than 2% of US corn acres, and have since been discontinued.

• Impact in the field

Researchers directly measured the impact of Bt-pollen on monarch larvae in the field (7). After corn pollen shed, monarch larvae were placed on milkweed plants in cornfields and which were then caged to prevent predation. Similar to the toxicity findings above, the results demonstrated that there was a significant impact on monarch larval growth and survival with Event 167 corn, but no effect was observed with other corn varieties. A second field study (8) also revealed that the pollen of Event 167 corn had a significant impact on both monarch and black swallowtail larvae, even at low pollen concentrations.

In one location (7), the pollen effect of Bt-corn was compared to a single application of the insecticide l-cyhalothrin (commonly applied to sweet corn). Bt-corn pollen had no effect, but the insecticide killed 91-100% of the monarch larvae within one hour. Considering that most monarchs live in or near corn fields (5), this observation suggests that, unlike Bt-corn, the use of commercial insecticides is likely to have a substantial impact on monarch populations.

• Overall Risk-- Putting the pieces together

The data from the studies above can be combined into a mathematical risk-assessment model to estimate the overall probability of the impact of Bt-corn pollen on monarch populations (9). As stated above, risk is a combination of toxicity and exposure. Toxicity was quantified in the study above (6). Exposure is quantified as a combination of 1) proportion of monarchs living in or near corn, 2) the overlap in time of corn pollen shed with susceptible larval stages, and 3) the adoption rate of Bt-corn varieties. Using this model, the authors estimate that no more than 0.8% of the total US monarch population is currently exposed to Bt-corn pollen. However, only 0.7% of that 0.8% would be exposed to acutely toxic levels-- a total of 0.0056% of the US monarch population or 56 in one million. The authors conclude that, even if the corn market were entirely saturated with Bt-corn varieties (currently less than 20%), the impact of Bt-corn on monarch populations is negligible.
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The following researchers contributed to one or more of the recent PNAS studies (listed by University or Research Center):

Cornell University:
John E. Losey: Dept. Entomology
Iowa State University:
Keith G. Bidne: Dept Entomology
Michael J. Daniels: Dept Statistics
Laura C. Jesse: Dept. Entomology
John Obrycki: Dept. Entomology
John M. Pleasants: Dept. Zoology & Genetics
Purdue University:
Wai-Ki F. Lam: Southwest Ag Program
University of Guelph (Ontario, Canada):
Heather R. Mattila: Dept. Environmental Biology
Mark K. Sears: Dept. Environmental Biology
Diane E. Stanley-Horn: Dept. Environmental Biology
University of Illinois, Urbana-Champaigne:
M.R. Berenbaum: Dept. Entomology
M. Carroll: Dept. Entomology
P. Ficarello: Dept. Entomology
D. McKenna: Dept. Entomology
R. Warner: Dept. Entomology
C.L. Wrait: Dept. Entomology
R. Zangerl: Dept. Entomology
University of Maryland:
Galen P. Dively: Dept. Entomology
Eric Olsen: Dept. Entomology
Robin Rose: Dept. Entomology
University of Minnesota, St. Paul:
Karen S. Oberhauser: Ecology & Evolutionary Biology
Michele D. Prysby: Ecology & Evolutionary Biology
University of Nebraska:
Thomas L Clark: Dept. Entomology
John E. Foster: Dept. Entomology
Blair D. Sigfried: Dept. Entomology
Terrence Spencer: Dept. Entomology
USDA, Agricultural Research Service:
Richard L. Hellmich (Iowa St)
Gretchen D. Jones (College Station)
Leslie C. Lewis
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1. Losey, J.E., Raynor, L.S., Carter, M.E. 1999. Transgenic pollen harms Monarch larvae. Nature 399:214.

2. Shelton, A.T. & Roush, R.T. 1999. False reports and the ears of men. Nature Biotechnology 17:832.

3. Hansen-Jesse, L.C. & Obrycki, J.J. 2000. Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125(2): 241-245.

4. Pleasants, J.M., Hellmich, R.L., Dively, G.P., Sears, M.K., Stanley-Horn, D.E., Mattila, H.R., Foster. J.E., Clark, T.C., Jones, G.D. 2001. Corn pollen deposition on milkweeds in and near cornfields. PNAS Early Edition.

5. Oberhauser, K.S., Prysby, M.D., Mattila, H.R., Stanley-Horn, D.E., Sears, M.K., Dively, G., Olson, E., Pleasants, J.M., Wai-Ki, F.L., Hellmich, R.L. 2001. Temporal and spatial overlap between monarch larvae and corn pollen. PNAS Early Edition.

6. Hellmich, R.L., Siegfried, B.D., Sears, M.K., Stanley-Horn, D.E., Daniels, M.J., Mattila, H.M., Spencer, T., Bidne, K.G., Lewis, L.C. 2001. Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. PNAS Early Edition.

7. Stanley-Horn, D.E., Dively, G.P., Hellmich, R.L., Mattila, H.R., Sears, M.K., Rose, R., Jesse, L.C.H., Losey, J.C., Obrycki, J.J., Lewis, L. 2001 Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly in field studies. PNAS Early Edition.

8. Zangerl, A.R., D. McKenna, C.L., Wraight, C.L., Carroll, M., Ficarello, P., Warner, R., Berenbaum, M.R. 2001. Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. PNAS Early Edition.

9. Sears, M.K., Hellmich, R.L., Stanley-Horn, D.E., Oberhauser, K.S., Pleasants, J.M., Mattlia, H.R., Sigfried, B.D., Dively, G.P. 2001. Impact of Bt corn pollen on monarch butterfly populations: A risk assessment. PNAS Early Edition.
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