The Effect of BT-Maize on Butterflies – Reckoning the Risk

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Abstract:

Insect-resistant genetically-modified (GM) crops have been developed to provide protection against target pests by the introduction of a Bacillus thuringiensis (Bt) gene encoding various insecticidal Cry proteins. Such is the pervasiveness of this technology that the global area planted commercially with these genetically-modified Bt crops exceeded 50 million hectares in 2010. Bt maize crops engineered for toxicity to the larvae of lepidopteran pests such as the European corn borer, Ostrinia nubilalis, present a potential risk to the larvae of non-target butterflies that are not pests, but that feed in the vicinity of the crop and that might therefore be affected by toxic maize pollen. The hazard is from contact with the Bt protein by ingestion of maize pollen adhering to host plants. In North America, such a potential hazard was highlighted by a laboratory assay of Monarch butterfly larvae (Danaus plexippus) that consumed Bt maize pollen on milkweed (Asclepias syriaca) and led to extensive exposure assessments in the field in the USA. However, these found that that the amounts of maize pollen potentially ingested by monarch larvae on their host-plants in and around Bt-maize fields are unlikely to adversely affect a significant proportion of this species. However, extrapolating the monarch butterfly results to other species is problematic because of between-species variability in acute sensitivity to specific Cry1 proteins, differences in host-plants and other ecological factors. Within Europe, although lethal and sub-lethal effects of Bt-maize pollen consumption by lepidopteran larvae have now been reported for several non-target lepidopteran species under laboratory conditions, there have been few intensive field-based studies of exposure on prominent non-target butterflies of conservation concern. Only a minority of lepidopteran species live in habitats inside arable maize ecosystems, and the larvae of those that do are often found in greater numbers on host-plants in field margins, rather than in the crop itself, because host-plant densities are usually much greater in margins than in the crop. However, the intensification of agriculture over the last 50 years has been associated with substantial losses of biodiversity in arable ecosystems. Butterflies are popular indicators of biodiversity and are in decline in arable ecosystems throughout Europe, partly as a result of farming practice. In addition, genetic modification remains a controversial area for environmental policy in Europe, where public acceptance of genetically-engineered plants is much weaker than in North America. For example, in January 2005 Hungary invoked an emergency 'safeguard clause' to attempt to ban the cultivation of the Bt-maize event MON810 (which expresses the Cry1Ab protein). Despite its lack of success, this was followed in 2008 and 2009 by other EU states, including France and Germany; these safeguard clauses currently remain in place but are being challenged legally. MON810 is the only GM crop currently cultivated on a wide scale (c. 105 ha) in Europe, mainly in Spain, but also in the Czech Republic, Poland, Portugal, Romania and Slovakia. Obtaining direct data on the mortality of non-target Lepidoptera is difficult because there are many species potentially at risk; these have different host-plants; exposure studies require good estimates of population densities of both lepidopteran species and host-plant, in both crop, margin and alternative habitats; the species at risk may be rare and have a low population density; larvae may be difficult to find in the field; and the period over which pollen is shed is relatively short. Such difficulties were discussed by Aviron et al. (2009), who calculated that to detect a change in abundance of 20% with adequate statistical power would require more than 100 pairs of fields or field margins. Furthermore, there are restrictions due to limited resources and time limitations for largescale agro-ecological experiments (Perry et al., 2003). Additional problems include refusals to grant permission for trials in many EU member states and the risk of damage by activists. The body responsible for providing independent scientific advice to the European Commission and Parliament on GM crops is the European Food Safety Authority (EFSA). EFSA has a panel of 21 experts, seven of whom specialize in environmental risk assessment (ERA). The Directive 2001/18/EC provides the legal framework for assessment and states that: "The objective of an ERA is, on a case by case basis, to identify and evaluate potential adverse effects of the GMO, either direct and indirect, immediate or delayed, on human health and the environment". Note that potential advantages, such as the decrease of pesticide applications widely reported for GM crops, are legally excluded from consideration through the wording of the Directive. In response to the 2005 safeguard clause invoked by Hungary, EFSA concluded that there was no new scientific evidence presented and called for future safeguard clauses to supply an appropriate ERA with data of a quality which can be subjected to detailed scientific scrutiny. Also that: "considering toxicity and exposure of Cry1Ab, the risk of exposure of non-target Lepidoptera to harmful toxin concentrations via Mon 810 maize pollen is negligible and that adverse impacts on populations are very unlikely." However, whilst developing its own opinion on the risk of renewal of the license to cultivate MON810 in early May 2009, EFSA received a letter signed personally by sixteen EU Member State Environment Ministers specifically requesting that EFSA consider the impact of MON810 crops on non-target European Lepidoptera. The situation appeared something of an impasse; whilst there was no specific data demonstrating serious levels of mortality in the field in Europe, NGOs and some EU Member States claimed that the previous EFSA opinions had not taken sufficient note of the uncertainty engendered by the lack of such quantified estimates of mortality. Clearly, a new approach was required, if the risk was to be described in more than vague and purely qualitative terms.

Keywords: BT; ENVIRONMENTAL RISK ASSESSMENT; GENETICALLY-MODIFIED MAIZE; MATHEMATICAL MODEL; NON-TARGET LEPIDOPTERA

Document Type: Research Article

DOI: http://dx.doi.org/10.1564/22oct02

Publication date: October 1, 2011

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