Bt Crops and the Environment

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COMMENTARY | Bt CORN POLLEN IMPACTS ON NONTARGET LEPIDOPTERA: ASSESSMENT OF EFFECTS IN NATURE Proceedings of the National Academy of Sciences (2000) David S. Pimentel - and Peter H. Raven*

The demonstrations by Losey et al. and Hansen and Obrycki 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., 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. 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 in their experiments with Monarch butterfies was demonstrated by Wraight et al. to be lethal to black swallowtail larvae in the laboratory, whereas the pollen of the strain they used in their field experiments, with 1 y 40 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. 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 butterfly 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.
. . . 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.


The ubiquitous nature of Bacillus thuringiensis (Bt), a Gram-positive bacterium capable of producing crystal proteins with insecticidal activity during sporulation, is now being mirrored in major crops plants that have been engineered through recombinant DNA to carry genes responsible for producing these crystal proteins and providing host plant resistance to major lepidopteran and coleopteran pests. In 2007, the 11th year of commercial production, Bt maize and Bt cotton were commercially produced on a total of 42 million hectares in 20 countries. Assessment of environmental safety has been and continues to be a key element of transgenic crop technology.
This review focuses on two environmental elements, effects on non-target invertebrates and changes in insecticide use patterns since the adoption of Bt maize and cotton. Meta-analyses of the extant literature on invertebrate non-target effects reveals that the pattern and extent of impact varies in relation to taxonomy, ecological or anthropomorphic guild, route of exposure and the non-Bt control against which effects are gauged. Hazards identified in the laboratory may not always manifest in the field and the minor negative effects of Bt crops demonstrated in the field pale in comparison with alternative pest suppression measures based on insecticides.
The efficacy of Bt maize and cotton against major pest species has been associated with an estimated 136.6million kg global reduction in insecticide active ingredient used between 1996 and 2006 (29.9% reduction). Benefits vary by country and region and are heavily weighted towards cotton production, which has historically been one of the largest users of insecticides in the world.


Effects at the overall community structure and nematode genera varied more by seasonal phenology than corn treatment. The isoline with insecticide had more non-target effects on nematode communities than the Bt hybrid.


In total, 29 species in 23 genera and nine families were identified from the 4,937 spiders collected, and both Bt and non-Bt rice fields showed a typical Korean spider assemblage. The temporal patterns of spider species richness and spider abundance were very similar between Bt and non-Bt rice, although significant differences in species richness were observed on a few occasions. Overall, spider community structure, including diversity, the dominant species, and abundance did not differ between Bt and non-Bt rice. The results of the study indicated that the transgenic Cry1Ac rice lines tested in this study had no adverse effects on the spider community structure of the rice fields.


Reduced Use of Insecticides Bt maize offers both economic and environmental advantages and grower responses indicate an awareness of both types of these benefits. Many growers cite unique opportunities to protect yield and reduce handling (and use) of insecticides to explain their rapid adoption of Bt maize (Pilcher et al. 2002). Brookes and Barfoot (2010) estimated that from 1996 to 2008 the cumulative decrease in insecticide active ingredient (a.i.) use on Bt maize was 35% (29.9 million kg) globally. Much of the reduction in insecticide a.i. was probably due to coleopteran-active Bt maize, as insecticides used against Diabrotica spp. comprise 25–30% of the global total in maize (James 2003, Rice 2004).

Possible Effects on Non-target Organisms

There have been no surprising effects on non-target organisms observed with Bt maize, which confirms the specificity of the Bt proteins. Most studies suggest Bt maize has little if any impact on predators and parasitoids and, when compared with maize treated with chemical insecticides, Bt maize often results in increased biodiversity [for general reviews see (O'Callaghan et al. 2005, Romeis et al. 2008)]. Specialist insects that depend on target pests are the exception to the generalization that Bt maize does not impact non-target organisms. This is particularly true for some parasitoids, which may become less abundant along with their herbivorous hosts (Pilcher et al. 2005, Romeis et al. 2008, Storer et al. 2008). Also, fewer saprophagous dipterans (i.e., fly larvae that feed on decaying organic matter) have been observed in Bt maize fields, which has been attributed to the indirect effect of reduced lepidopteran plant injury (Candolfi et al. 2004, Dively et al. 2004). Studies with monarch butterfly caterpillars, Danaus plexippus, suggested monarch butterfly populations would be reduced from feeding on milkweed leaves coated with Bt maize pollen (Jesse & Obrycki 2000, Losey et al. 1999). Follow-up studies, however, indicated that the impact was negligible because of limited exposure and low toxicity of Bt maize pollen to monarch caterpillars (Dively et al. 2004, Hellmich et al. 2001, Sears et al. 2001, Stanley-Horn et al. 2001).