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A Report on a Paper Concerning the Effect of Genetically Modified Bt Maize on Monarch Butterflies

Advice of the Advisory Committee on Releases to the Environment under Section 124 of the Environmental Protection Act 1990

January 2002

ACRE was asked to review a suite of work resulting from collaborative research by scientists from universities and research institutions in the United States and Canada. The work was published as six peer reviewed papers in the Proceedings of the National Academy of Sciences USA (14 September 2001). Each of the six studies deals with a specific research area to address the potential risk of Bt maize to monarch butterflies (Danaus plexippus) under natural field conditions. The maize lines used in this study were genetically modified for resistance to larvae of the European Corn Borer moth (Ostrinia nubilalis) which is an important pest of maize crops. Resistance to the corn borer is achieved by inserting a gene into the maize from the soil bacterium Bacillus thuringiensis. The gene codes for an insecticidal protein (Bt toxin) that is preferentially toxic to insects of the order Lepidoptera (butterflies and moths).

Each study in this collection investigated a different characteristic which might affect the environmental interaction between the Bt maize and the monarch butterflies.

The research of Oberhauser et al., (2001) 1 investigated the temporal and spatial overlap between development of monarch larvae and maize pollen. The study showed that there was overlap but the extent of this depended upon interacting factors. The authors concluded that agricultural practices such as weed control and foliar insecticide could have large impacts on monarch populations, regardless of the effect of GM crops.

Pleasants et al., (2001) 2 investigated the deposition of maize pollen onto the preferred food of monarch butterflies, milkweed, a weed commonly found in maize fields. They derived values for pollen deposition under various conditions and concluded that rain events in the field are an important determinant of level of pollen deposition.

Three of the papers investigated the effects of Bt maize pollen or purified proteins. Stanley-Horn et al., (2001) 3 performed an assessment of the effect of Bt maize pollen on monarch butterfly larvae in the field, using the Cry1Ab version of the Bt protein and comparing between different transformation events such as Bt 11, MON810 and event 176. Hellmich et al., (2001) 4 studied the sensitivity of monarch larvae to different purified Bt proteins and to the corresponding pollen in a laboratory-based study. Zangerl et al., (2001) 5 investigated the effects of maize pollen expressing event 176 on black swallowtail caterpillars (the monarch caterpillars which were to have been used were devastated by predation in the field and so had to be omitted from the study). The conclusion was that only event 176 showing a consistent negative effect with otherwise negligible effects of Bt maize pollen on monarch butterflies.

The work was drawn together in an overarching paper by Sears et al., (2001) 6 describing a conceptual model of a risk assessment derived from the collective research. In this they offer the conclusion that the impact of Bt maize pollen from the hybrids tested on monarch butterfly populations is negligible.

ACRE considered whether these results altered the Committee's previous advice on Bt pollen 7 and whether there are any implications for the risk assessment of genetically modified plants for release in the UK.

ACRE's advice:

ACRE welcomes the research from this collaborative group of scientists as a conspicuous example of the way in which science can shed light on the panoply of factors affecting interactions within the living environment and inform risk assessment. In particular, in this case, by helping to define the factors responsible for interactions between Bt maize and monarch butterflies and clarify the distinction between hazard and risk.

This work is an excellent addition to the research into this subject, forming an important step forward in rational risk assessment and an advance on the preliminary laboratory based work by Hansen & Obrycki (2000) 8 and Losey et al., (1999) 9 considered recently. In particular, this work includes field based experiments which are important in determining the effect of environmental conditions on exposure of the monarch butterflies to Bt maize.

The approach of this work is consistent with advice ACRE has issued previously. The paper by Sears et al., is a useful and comprehensive risk assessment and several of the papers demonstrate clearly the key role of spatial and temporal variation in exposure to pollen. Environmental factors such as rain have dramatic effects and this work serves only to emphasise the need for field analysis. There are also clear differences in toxicity between different transformation events. ACRE notes that event 176 is an outdated variety and that no re-registration is planned for this product. The work also confirms that the wider changes in agricultural practices are important determinants of monarch survival, in addition to the dangers from predation.

ACRE will continue to monitor closely this area of research. Bt maize or other insect resistant GM crops are not currently being grown in the UK. ACRE reminds applicants wishing to release GM plants, in particular those modified for insect resistance, that they will need to give more prominence in the risk assessment to any effects of GM pollen on non-target invertebrates.

Confidence in the environmental safety of GM plants can best be gained by proper evaluation in the field. Although several aspects of the interactions between Bt maize and monarch butterflies were investigated there remains a need for continued research to investigate the possible non-target effects of GM crops and how the risks from these are to be evaluated.

1 Oberhauser, KS., Prysby, MD., Mattila, HR., Stanley-Horn, DE., Sears, MK., Dively, G., Olson, E., Pleasants, JM., Lam, W-KF. & Hellmich, RL., (2001) Temporal and spatial overlap between monarch larvae and corn pollen. PNAS 98 pp 11913-11918

2 Pleasants, JM., Hellmich, RL., Dively, GP., Sears, MK., Stanley-Horn, DE., Mattila, HR., Foster, JE., Clark, P. & Jones, GD., (2001) Corn pollen deposition on milkweeds in and near cornfields. PNAS 98 pp 11919-11924

3 Stanley-Horn, DE., Dively, DP., Hellmich, RL., Mattila, HR., Sears, MK., Rose, R., Jesse, LCH., Losey, JE., Obrycki, JJ., & Lewis, L., (2001) Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. PNAS 98 pp 11931-11936

4 Hellmich, RL., Siegfried, BD., Sears, MK., Stanley-Horn, DE., Daniels, MJ., Mattila, HR., Spencer, T., Bidne, KG. & Lewis, LC., (2001) Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. PNAS 98 pp 11925-11930

5 Zangerl, AR., McKenna, D., Wraight, CL., Carroll, M., Ficarello, P., Warner, R. & Berenbaum, MR., (2001) Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. PNAS 98 pp 11908-11912

6 Sears, MK., Hellmich, RL., Stanley-Horn, DE., Oberhauser, KS., Pleasants, JM., Mattila, HR., Siegfried, BD. & Dively, G., (2001) Impact of Bt corn pollen on monarch butterfly populations: A risk assessment. PNAS 98 pp 11937-11942

7 www.defra.gov.uk/environment/acre/advice.htm

8 Hansen, L. C., & Obrycki, J., (2000). Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia, Published online: August 19, 2000.

9 Losey, JE., Raynor, LS., & Carter, ME., (1999). Transgenic Pollen Harms Monarch Larvae. Nature 399 pp 214.


    Page published 6 February 2002; last modified 11 November, 2002