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Assessing the Risks of Insect Resistant Transgenic Plants on Entomophagous Arthropods: Bt-Maize Expressing Cry1ab As a Case Study

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Assessing the Risks of Insect Resistant Transgenic Plants on Entomophagous Arthropods: Bt-Maize Expressing Cry1ab As a Case Study BioControl 48: 611–636, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands. FORUM Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study Anna DUTTON, Jörg ROMEIS and Franz BIGLER* Swiss Federal Research Station for Agroecology and Agriculture (FAL), Reckenholzstr. 191, 8046 Zurich, Switzerland ∗ Author for correspondence; e-mail: [email protected] Received 19 December 2002; accepted in revised form 15 September 2003 Abstract. One of the primary concerns related to the adoption of insect resistant trans- genic plants in the environment is the detrimental effect that these may pose on non-target organisms, including entomophagous arthropods (parasitoids and predators) which have an important function in regulating pests. Despite the fact that regulatory bodies require informa- tion regarding the potential risk of releasing transgenic plants in the environment, to date, no specific protocols have been designed for assessing the risks of insect resistant transgenic crops on entomophagous arthropods. Here a framework for risk assessment is proposed to evaluate the effects of insect resistant plants on entomophagous arthropods. Using maize expressing the Bacillus thuringiensis gene which codes for the Cry1Ab toxin, we illustrate the procedure necessary for assessing the risks. As a first step, it is required to determine which entomo- phagous arthropods play a major role in regulating maize pests, and which may be at risk. Because the risk which transgenic plants pose to entomophagous arthropods depends on both, their exposure, and their sensitivity to the insecticidal protein, it is essential to determine, as a second step, if and at what level organisms are exposed to the transgene compound. Exposure will be associated with the feeding behaviour of phytophagous and entomophagous arthropods together with the tissue and cell specific temporal and spatial expression of the insecticidal protein. For those organisms which could potentially be exposed to the insecticidal protein, sensitivity tests, as a third step, should be performed to assess toxicity. The testing procedure and the type of tests which should be adopted to quantify the effects of insect resistant plants on natural enemies are subsequently illustrated. Taking the green lacewing Chrysoperla carnea as an example, we propose a procedure on how to perform tests and give evidence that Bt-maize poses no risk to this predator. Key words: Chrysoperla carnea, exposure, genetically engineered crops, parasitoids, preda- tors, risk assessment, test procedure, tiered system, toxicity Introduction To date, the only insect resistant transgenic plants that are commercially available are those expressing genes which code for Bacillus thuringiensis 612 ANNA DUTTON ET AL. (Bt) toxins. The amount of area being cultivated with these crops is rapidly increasing (James, 2002), and other genes coding for new Bt-toxins, lectins, proteinase or α-amylase inhibitors, and other insecticidal products have been successfully engineered in plants (Schuler et al., 1998; Jouanin et al., 1998). Some of these plants are being tested at the field scale, such as peas (Pisum sativum) expressing the gene coding for common bean α-amylase inhib- itors (αAIs) (Morton et al., 2000). Moreover, in 2002, over 200 applications for release permits to conduct field tests with 11 different transgenic crops expressing various insect resistant genes were notified in the USA alone (ISB, 2002), indicating that the adoption of various transgenic plants is likely to increase. Similar to other plant protection technology, insect resistant transgenic plants bear risks and benefits to the environment (NAS, 2002). The primary ecological concerns to the release of transgenic plants include those related to their possible invasiveness in ecosystems, out-crossing, horizontal gene transfer, development of pest resistance, and effects on non-target organisms (Conner et al., 2003). Effects of GM plants on non-target entomophagous arthropods (predators and parasitoids) have been a major concern as these organisms often play an important role in natural pest regulation, and are considered to be of economic value. Moreover, this group of organisms may be a good indicator of potential ecological impacts of transgenic plants as they belong to the third trophic level in the food chain (Groot and Dicke, 2002). Although we are aware that other non-target arthropods such as herbivores, pollen feeders (bees), soil arthropods as well as other organisms including birds, mammals, and fish could be affected by transgenic plants, here we shall limit ourselves to the assessment of the risks of transgenic plants on entomophagous arthropods. Despite the fact that regulatory bodies in different countries require a detailed environmental risk assessment for the release of transgenic plants (Nap et al., 2003), it is often debated what and how to measure (Conner et al., 2003). This is distinctively the case for the assessment of non-target organisms as these include a large number of species. Moreover, these organ- isms can potentially be affected by insect-resistant transgenic plants through various ways (Schuler et al., 1999; Groot and Dicke, 2002). For example, the impacts on non-target entomophagous arthropods can be due to direct toxic effects through exposure to the insecticidal protein, indirect effects via reduc- tion in prey/host quantity and/or quality, or indirect effects due to unintended changes of plant properties (chemical or physical) caused by the insertion of a new gene (pleotropic effects or insertional mutagenesis). Although this complexity can make testing and assessment difficult, uncertainty can be BT-MAIZE EXPRESSING CRY1AB AS A CASE STUDY 613 minimised by selecting appropriate species, and by conducting suitable tests to produce meaningful crop specific results. Despite the fact that regulatory agencies require data concerning the effects of GM crops on entomophagous arthropods, to date there is no standard procedure indicating what should be assessed and how tests should be conducted. Recently two different sequential approaches have been suggested for selecting and testing the effects of Bt-maize (Schmitz et al., 2003) and protease inhibitor-expressing crops (Cowgill and Atkinson, 2003) on non-target herbivorous arthropods. However, there is until now no sequen- tial approach to risk assessment of insect resistant transgenic plants on non-target entomophagous arthropods. In this article, we first give an overview of the current requirements to assess the risk of transgenic plants on non-target organisms for the commer- cialisation of GM plants in the US and the EU, and its shortcomings. Second, taking Bt-maize expressing the cry1Ab gene as a model system, we demon- strate the sequential steps that need to be taken in order to make a selection of entomophagous arthropods which could be at risk, and present a testing procedure for assessing the effects. Our purpose is to provide a conceptual testing framework for the selection of organisms and apply an existing testing procedure (tiered system) for assessing the effects. Moreover, we provide a review of the literature concerning the effects of Bt-maize on beneficial arthropods and make a detailed evaluation on the risks of Bt-maize on the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) which has been the only predatory insect shown to be affected by Bt-maize in laboratory and greenhouse conditions (Hilbeck et al., 1998a, b; Dutton et al., 2002). Regulatory status of test requirements for non-target organisms and their shortcomings In the US, according to the National Academy of Sciences, the trait of a GM plant should be the focus of the risk assessment, and not the process by which it has been produced (NAS, 2000). As a result the Environmental Protection Agency (EPA), requires that risk assessment tests are performed on non-target organisms to assess toxicity of so called plant-incorporated protectants. This is in contrast to EU regulatory procedures which consider GM plants as something new, for which both direct (toxic) and indirect effects should be assessed prior to their commercial release (Directive 2001/18/EC) (EC, 2001). Since in the US the major concern regarding the potential effects of GM plants expressing insecticidal proteins on non-target organisms is that related 614 ANNA DUTTON ET AL. to the toxicity of the protein contained in the plant, test requirements on non-target organisms remained similar to those required for plant protection products. This means testing the effects on a set of representative insects such as bees, ladybirds and lacewings (NAS, 2002; EPA, 2002) using a tiered testing system in which the 1st tier reflects a maximum hazard approach. Organisms are exposed to the pure insecticidal protein at a range of doses and concentrations 10 to 100 times higher than those expected in the environment (EPA, 2000). Since these tests do not provide any information on the possible non-intended indirect effects that could occur once the plants are released in the field, the EPA often requires information from field studies (EPA, 2003). Field studies, however, have often the drawback of being expensive and lack appropriate statistical power. In the EU, a more extensive procedure is required for the commercial- ization of transgenic plants. The assessment should consider the potential immediate and delayed effects resulting from direct and indirect
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