A paper from Cornell University (Losey et. al 1999) was the first to report toxicity of Bt corn pollen to monarch butterflies. Although there was wide discussion in the scientific community that the study was preliminary and flawed in terms of how well it represented real-world issues (Berringer 1999, Hodgson 1999, Rice 1999, Shelton and Rousch 1999), it received wide distribution in the popular press and used as an argument against further development and release of transgenic crops.
An Iowa State University study by Hansen and Obrycki (2000) was reported to corroborate Loseyís study, and under field conditions. Although a portion of the experiment was conducted in the field (unlike the laboratory study by Losey), critics contend that the study did not truly represent field conditions and didnít accurately portray risks of Bt pollen in natural field settings. As was true for the Losey study, the results were widely circulated by the popular press, while criticisms of the experimental design and conclusions drawn by the authors were not mentioned by the media. Conversely, a study by Wraight et al (2000) demonstrating an absence of toxicity of Bt pollen to black swallowtails under field conditions, received little or no circulation in the popular press. Additionally, numerous ongoing field studies showing minimal impact of Bt pollen on monarch butterflies have received no mention in the popular press.
This paper is not intended as further criticism of research conducted by Losey et. al, and Hansen and Obrycki. It is intended as a summary of those results, reasons why they may not be representative of field conditions and potential hazards of the pollen to monarch butterflies, and to point out the kinds of field research that are still needed.
Losey et. al (1999). It is not surprising that monarch mortality resulted in this lab trial. It was already known prior to this study that the Bt stain (Cry 1Ab) used for control of European corn borer was toxic to other Lepidoptera, whether used as a spray or delivered in transgenic form. If lepidopteran larvae fed on the material, some degree of mortality would result. Losey et. al coated milkweed leaves with Bt corn pollen and allowed the larvae to feed. After 4 days, 44% of the larvae receiving Bt corn pollen died, whereas there was no larval mortality when the milkweed leaves were dusted with non-Bt pollen. Larvae that survived feeding on Bt-pollen were smaller than larvae that received no Bt. Although the trial was preliminary, it received wide circulation in the national media who drew conclusions that were beyond the scope of the experiment. Those opposed to biotechnology continue to use these data in attempts to stop all development of transgenic plants intended for insect pest management.
One of the criticisms of the Losey study resulted from their failure to report
the dosage of Bt placed on the milkweed leaves, and if this represented what
would happen in the field. Additionally, the leaves were coated with Bt
pollen and larvae had no choice but to feed on these artificially coated leaves.
At a monarch vs. Bt symposium conducted during August 2000 there were arguments
suggesting that a complex series of at least 5 events must occur before significant
mortality will occur in the field:
Hansen and Obrycki (2000). Potted milkweed plants were placed in, or at various distances from the edge of, corn fields during pollen shed in attempts to assess the deposition of corn pollen on milkweed leaves. Samples of milkweed leaves were brought to the laboratory and newly hatched larvae of monarch butterflies were placed on leaf disks cut from the milkweed leaves and fed for 48 hours. Another set of experiments was conducted to assess the pollen dose required to cause mortality of neonate (newly hatched) larvae. Pollen was collected in the field and applied to leaves in the laboratory at rates of 14, 135, and 1300 grains per cm2 . Neonates were placed on disks and allowed to feed for 48 hours and observed for mortality, development and growth characteristics. Although the results were widely circulated by the media as a ìfield studyî, critics contend that the only field portion of the study involved pollen collection. By removing the leaves and conducting the trials in the laboratory, the results would be affected by factors such as variation in temperature and humidity; degradation of pollen by sunlight, moisture, microorganisms, rainfall, wind; moisture on leaf surfaces; natural dispersal and behavior of larvae, and numerous other ecological factors. The study also ignored the possibility of monarch butterflies choosing whether or not to lay eggs on pollen-infested plants (i.e. the possibility of being repelled by the Bt pollen). Without ìtrueî field studies where all aspects of the trails are conducted in the monarchís natural surroundings, it is not possible to understand the nature of pollen deposition on milkweed plants and the possible effects on monarchs or other species of caterpillars. Monarch larvae were essentially force-fed pollen-coated leaves in the laboratory, whereas in the field they would have an opportunity to move to leaves with lower levels of pollen. Larvae were placed on the upper sides of leaves in the study, but in the field they normally feed on the lower side of leaves. Because the pollen was deposited primarily on the upper leaf surfaces, feral larvae may experience considerably lower levels of pollen when feeding.
Critics of the study also contend that statements in the media and by the authors were misleading in that they implied the results implicated all Bt hybrid events expressing Cry 1Ab toxin. However, only Event 176 Bt corn resulted in consistent lethal effects. Event 176 comprised only about 2% of the total Bt corn acreage planted in North America during 1999, and was estimated to be only about 1% of the total acreage during 2000. Event 176 pollen is higher in Bt concentration than the more common Bt11 or Mon810, the leading Bt events. Thus critics contend it is misleading to imply that toxicity associated with 176 is representative of Bt hybrids planted by the majority of corn growers. Sears and Shelton (2000) suggest that the conclusions of the authors go beyond the extent of the data presented. The Hansen and Obrycki paper implies that significant amounts of pollen could be distributed within and up to 10 meters outside of cornfields such that significant mortality to monarch larvae would occur. Sears and Shelton state that the data from the experiment do not support this speculation. Hansen and Obrycki did not report the density of milkweed plants in or around fields or in different habitats in the area, nor did they provide information on the phenology of the monarch populations in relation to the pollen shed period of the Bt corn hybrids. In other words, what is the relative timing of pollen shed periods and peak egg laying by adults?
Sears and Shelton provide a detailed discussion of study findings, proceedings and conclusions, some of which raise questions:
Wraight, C.L. et. al (2000). The eastern black swallowtail was used in this field study to evaluate the potential toxicity of Bt corn pollen when placed on plants in the carrot family (Apiaceae). The larvae feed on a variety of hosts in this family, including Queen Anneís lace and parsley. With the onset of pollen shed, potted plants were infested with first-instar swallowtail larvae and placed at various intervals from the edge of a field of Bt corn (MON810, Monsanto event). Although larvae died during the course of the experiment, there was no relationship between mortality and proximity to the field, or to pollen deposition on the host plants. Pollen from these corn plants failed to cause mortality in the laboratory at the highest pollen dose tested (10,000 grains/cm2). The authors concluded that pollen from this even is unlikely to affect wild populations of black swallowtail, which is one of the key non-target lepidopteran species in the Midwest. This study received no circulation in the popular press.
1. Professor and Extension Entomologist, University of Wisconsin College of Agricultural and Life Sciences
Beringer, J. E. 1999. Cautionary tale on safety on GM crops. Nature (Lond.) 399:405
Losey, J. E., L. S. Rayor, & M. E. Carter. 1999. Transgenic pollen harms monarch larvae. Nature (London) 399: 214.
Hansen-Jesse, L. C. and J. J. Obrycki. 2000. Field deposition of Bt transgenic pollen: lethal effects on the monarch butterfly. Oecologia
Hodgson, J. 1999. Monarch Bt-corn paper questioned. Nature Biotechnology 17:627
Rice, M. E. 1999. Monarchs and Bt corn: questions and answers. Integrated crop management IC-482 (14):93-95.
Shelton, A. M. and R. T. Rousch. 1999. False reports and the ears of men. Nature Biotechnology 17:832.
Sears, M.. and A. M.. Shelton. 2000. Questionable conclusions from latest monarch study. http://www.agbioworld.org. Archived at http://agvioview.listbot.com
C. L. Wraight, A. R. Zangerl, M. L. Carrol, and M. R. Berenbaum. 2000. Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proc. Natl. Acad. Sci. USA.
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