Baseline susceptibility of different European lepidopteran and coleopteran pests to Bt proteins expressed in Bt maize: a systematic review

Background: Lepidopteran and coleopteran species are the most important pests in maize. They can be controlled using genetically modified (GM) crops expressing insecticidal Bacillus thuringiensis (Bt) proteins. The long-term success of this technology demands a pest resistance management. Important information for the successful management of resistance is the baseline susceptibility of the different target pests to the different Bt proteins. The data on baseline susceptibility should enable risk assessors and managers to assess whether a GM maize produces a Bt protein in a high-dose to specific target organisms and resistance has evolved during the commercial cultivation of this GM maize events. Methods: Our systematic search followed an a priori protocol including the database platforms Web of Science, Scopus, CAB abstracts, Science Direct and JSTOR. We additionally conducted a Google scholar search. We collated all search results and screened all retrieved articles using predetermined inclusion criteria. We identified 30 studies, which fulfilled the criteria of including a relevant Bt protein, a relevant species, an appropriate endpoint, and fieldderived pest generations reared in the laboratory no longer than three generations. We then made a quality assessment to discover if the studies considered the dose response curves with confidence intervals, described the protein source, tested the protein concentration and the protein activity via positive controls, use more than ten larvae per concentration, more than two replications, and more than five protein concentrations. Since no quantitative synthesis was possible the synthesis of the results was done in a narrative form. Results: Seventy percent of the studies fulfilled five or more criteria and 17% fulfilled four of the seven criteria. Six Bt proteins were tested on one or more of the four species Ostrinia nubilalis, Helicoverpa armigera, Sesamia nonagrioides, and Diabrotica virgifera virgifera. We extracted the baseline susceptibility for the given protein-species-combinations and the test method with the Bt protein applied either on the surface of the diet or incorporated. Although, the data displays a high heterogeneity and are thus hard to compare, they give an overview of the baseline susceptibility of lepidopteran/coleopteran pests to Bt proteins. Conclusion: Our systematic review illustrates the heterogeneity of the data and indicates the necessity of standard protocols for testing susceptibility of insect pests, which provide comparable data. The cultivation of Bt crops, as with any other plant protection measure, is likely to result in resistance evolution in the target pests. Industry, policy makers, and research should combine knowledge to protect the benefits of this technology. © The Author(s) 2016. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Open Access Environmental Evidence *Correspondence: [email protected] Kai U. Priesnitz, Anja Vaasen and Achim Gathmann contributed equally to this work Department Genetic Engineering, Unit Coexistence and GMO-Monitoring, Federal Office of Consumer Protection and Food Safety (BVL), Mauerstr. 39-42, 10117 Berlin, Germany Page 2 of 12 Priesnitz et al. Environ Evid (2016) 5:27 Background Lepidopteran and coleopteran species are the most important pests in maize. Several factors affect the effectiveness of control measures. The stem boring and root feeding life style of some pest species reduces exposure to insecticides, which creates difficulties to effectively control these species by spraying. Resistance evolution to conventional insecticides can cause ineffectiveness of treatments. Certain farming practices such as continuous or frequent maize cultivation and no tillage lead to higher pest pressure. In addition, there is a desire to reduce the environmental harm caused by insecticides. An alternative approach to control these pests is the use of genetically modified (GM) crops expressing Bacillus thuringiensis derived insecticidal proteins (Bt proteins). However, one concern in growing maize is the potential for resistance evolution against control measures, which is a well-known problem for more than 100 years [1]. This phenomenon occurs regularly where pest populations are exposed to uniform, strong and continuous selection pressure [1–3] and will evolve as a result of cultivating insect resistant GM plants. In consequence, Bt products might lose their effectiveness either as conventional spray applications or when expressed as transgenic traits in GM crops. Therefore, it is desirable that pest resistance management accompanies the cultivation of Bt crops to delay the evolution of resistance to B. thuringiensis products [4]. The regulatory risk assessment in the European Union (EU) considers impacts of the changes in management associated with the GM crop including the consequences of pest resistance evolution, and therefore also considers the efficacy of strategies by applicants delaying the expected resistance evolution. The most common strategy is the “high-dose/refuge” strategy (e.g. [1, 5]), which includes monitoring and models to forecast the evolution of resistance [6]. The principles of the high-dose/refuge strategy used in these models are that (1) the Bt protein kills most of the susceptible pest population feeding on GM plants (highdose), (2) the frequency of resistance alleles is low in the pest population, (3) the inheritance of resistance is fully recessive, (4) rare resistant pests surviving on Bt crops mate with susceptible populations from nearby refuges of non-Bt host plants [5], and (5) fitness costs are associated with the evolution of resistance [7]. Therefore, all relevant data on the biology of the target pests, the characteristics of the modified plant and the GM trait are needed to create the model. In case not all requirements for the high-dose/refuge strategies are fulfilled, a modified strategy or additional measures might be needed. One of the most important sources of information to model the potential for resistance to evolve in a pest/crop system is the baseline susceptibility of the target organisms to Bt proteins. Data on baseline susceptibility should enable risk assessors and managers to assess whether Bt maize events present a high-dose to specific target pests and whether resistance has evolved after commercial introduction of Bt maize events. Objective of the review In order to study the available information on baseline susceptible of certain pests, we formulated the following review question: How susceptible are different lepidopteran/coleopteran maize pests to Bt proteins? The research question has the following components: P = Population: the populations considered are all lepidopteran or coleopteran pest species in maize, which are intended to be controlled by Bt maize in Europe. These include Ostrinia nubilalis, Sesamia nonagrioides, and Diabrotica virgifera virgifera, which are defined as the focal target species for GM Bt maize being cultivated or developed for cultivation in the EU and elsewhere. Additionally lepidopteran or coleopteran pest species should be considered, which might be of economic relevance in maize cultivation. The selection of considered species is based on an extended review initiated by the European Food Safety Authority (EFSA) [8]. I/E = intervention/exposure: exposure to Bt proteins in the Bt crop. O = outcome: baseline susceptibility data of lepidopteran and coleopteran pest species on different Bt proteins. The goal of the systematic review (SR) was to collect as much data as possible on baseline susceptibility of different lepidopteran/coleopteran maize pests to Bt proteins expressed in Bt maize varieties, in order to have a broad data base on which to model and assess the potential for evolution of resistance of different crop-Bt protein-speciescombinations and to identify potential knowledge gaps. Methods This review was part of the EU funded project GRACE (GMO risk assessment and communication of evidence, http://www.grace-fp7.eu/) to collate available evidence