Yann Devos

Coexistence of genetically modified (GM) and non-GM crops in the European Union. A review

The adoption of genetically modified (GM) crops in the European Union (EU) raises questions on the feasibility of coexistence between GM and non-GM crops. Regulations to ensure that different cropping systems can develop side-by-side without excluding any agricultural option are currently implemented or developed by member states. The aim of this review is to explore whether nationally or regionally proposed coexistence strategies comply with the general principles established by the European Commission that ask for science-based and proportionate coexistence measures. In the first part, existing legal requirements and potential sources of adventitious mixing are reviewed. It is discussed what type of coexistence measures might be necessary to keep GM inputs below the legal tolerance threshold of 0.9%. Concentrating on cross-fertilisation as the major biological source of adventitious mixing in maize, it is then assessed to which extent available scientific data on cross-fertilisation can explain the diversity of currently proposed isolation distances by several member states. In the second part, it is analysed whether currently proposed isolation distances reflect contending policy objectives towards GM crops that largely exceed the economic scope of coexistence. It is investigated how coexistence is intersecting with a wider debate about the role of GM crops in agriculture. Based on the analysis of existing cross-fertilisation data, it is concluded that some of the currently proposed isolation distances are not in line with the coexistence principles laid down by the European Commission: they are (i) excessive from a scientific point of view; (ii) difficult to implement in practice; (iii) rarely proportional to the regional heterogeneity in the agricultural landscape; and (iv) not proportional to the farmers’ basic economic incentives for coexistence. Hence, the range of proposed isolation distances cannot simply be explained by different interpretations of available scientific data, possible error intervals and remaining uncertainties inherent in the scientific process. It is argued that other than scientific issues must be at play. One might thus claim that coexistence has become an arena of contending values and visions on the future of agriculture and on the role GM crops might play therein.

A mathematical model of exposure of non- target Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe

Genetically modified (GM) maize MON810 expresses a Cry1Ab insecticidal protein, derived from Bacillus thuringiensis (Bt), toxic to lepidopteran target pests such as Ostrinia nubilalis. An environmental risk to non-target Lepidoptera from this GM crop is exposure to harmful amounts of Bt-containing pollen deposited on host plants in or near MON810 fields. An 11-parameter mathematical model analysed exposure of larvae of three non-target species: the butterflies Inachis io (L.), Vanessa atalanta (L.) and moth Plutella xylostella (L.), in 11 representative maize cultivation regions in four European countries. A mortality–dose relationship was integrated with a dose–distance relationship to estimate mortality both within the maize MON810 crop and within the field margin at varying distances from the crop edge. Mortality estimates were adjusted to allow for physical effects; the lack of temporal coincidence between the susceptible larval stage concerned and the period over which maize MON810 pollen is shed; and seven further parameters concerned with maize agronomy and host-plant ecology. Sublethal effects were estimated and allowance made for aggregated pollen deposition. Estimated environmental impact was low: in all regions, the calculated mortality rate for worst-case scenarios was less than one individual in every 1572 for the butterflies and one in 392 for the moth.

Regulating coexistence of GM and non-GM crops without jeopardizing economic incentives

The ongoing debate about the coexistence of genetically modified (GM) and non-GM crops in the European Union (EU) mainly focuses on preventive measures needed to keep the adventitious presence of GM material in non-GM products below established tolerance thresholds, as well as on issues covering questions of liability and the duty to redress the incurred economic harm once adventitious mixing in non-GM products has occurred. By contrast, the interplay between the economic incentives and costs of coexistence has attracted little attention. The current overemphasis on the technical aspects and cost of coexistence over its economic incentives might lead EU policy-makers to adopt too stringent and rigid regulations on coexistence. Therefore, we argue for flexible coexistence regulations that explicitly take into account the economic incentives for coexistence. Our arguments provide a timely and important framework for EU policy-makers, who are currently struggling to implement coherent coexistence regulations in all member states.

Transgenic or not? No simple answer!: New biotechnology-based plant breeding techniques and the regulatory landscape

The global cultivation area of genetically modified plants (GMPs) includ‐ing soybean, maize, cotton, canola (oilseed rape) and sugar beet has been increasing consistently since they were first cultivated commercially in 1996, reaching 160 million hectares (ha) in 2011 [[1]]. By 2011, the global area of planted insect‐resistant crops was 66 million ha. The rapid adoption of insect‐resistant crops indicates that they have become a primary tool for managing lepidopteran and coleopteran target pest species in cotton and maize [[2]]. Herbicide‐resistant GMPs have changed weed management practices and made an important contribution to the global production of commodity crops [[3]]. Yet, most of these GMPs were created by using first‐generation transgenic technologies: particle bombardment or Agrobacterium ‐mediated genetic engineering techniques. As such, they typically carry recombinant DNA from organisms including bacteria and viruses, as well as other plants, to provide resistance against pests or herbicides. > The main rationales behind the creation of NPPs are to accelerate the breeding process and to address consumer concerns about GMPs… In the meantime, plant science has made considerable progress both in identifying genetic factors for traits conferring improved disease resistance, drought tolerance, nutrient use and nutritional value, but also in developing new biotechnology‐based plant breeding techniques to alter genetic and epigenetic factors more efficiently [[4]]. These new techniques enable the transfer of limited amounts of DNA between related genotypes from the ‘breeders’ gene pool’, as well as the introduction of specific modifications to plant genomes through targeted mutagenesis by using zinc‐finger nucleases or oligonucleotide‐directed mutagenesis. Although in some cases (for example, zinc finger nuclease type 3; see Sidebar A) DNA from outwith the breeders’ gene pool can be inserted, the insert is highly targeted within the plant genome, unlike in transgenesis. They also allow breeders to modify …

Feral genetically modified herbicide tolerant oilseed rape from seed import spills: are concerns scientifically justified?

One of the concerns surrounding the import (for food and feed uses or processing) of genetically modified herbicide tolerant (GMHT) oilseed rape is that, through seed spillage, the herbicide tolerance (HT) trait will escape into agricultural or semi-natural habitats, causing environmental or economic problems. Based on these concerns, three EU countries have invoked national safeguard clauses to ban the marketing of specific GMHT oilseed rape events on their territory. However, the scientific basis for the environmental and economic concerns posed by feral GMHT oilseed rape resulting from seed import spills is debatable. While oilseed rape has characteristics such as secondary dormancy and small seed size that enable it to persist and be redistributed in the landscape, the presence of ferals is not in itself an environmental or economic problem. Crucially, feral oilseed rape has not become invasive outside cultivated and ruderal habitats, and HT traits are not likely to result in increased invasiveness. Feral GMHT oilseed rape has the potential to introduce HT traits to volunteer weeds in agricultural fields, but would only be amplified if the herbicides to which HT volunteers are tolerant were used routinely in the field. However, this worst-case scenario is most unlikely, as seed import spills are mostly confined to port areas. Economic concerns revolve around the potential for feral GMHT oilseed rape to contribute to GM admixtures in non-GM crops. Since feral plants derived from cultivation (as distinct from import) occur at too low a frequency to affect the coexistence threshold of 0.9% in the EU, it can be concluded that feral GMHT plants resulting from seed import spills will have little relevance as a potential source of pollen or seed for GM admixture. This paper concludes that feral oilseed rape in Europe should not be routinely managed, and certainly not in semi-natural habitats, as the benefits of such action would not outweigh the negative effects of management.

Environmental impact of herbicide regimes used with genetically modified herbicide-resistant maize

With the potential advent of genetically modified herbicide-resistant (GMHR) crops in the European Union, changes in patterns of herbicide use are predicted. Broad-spectrum, non-selective herbicides used with GMHR crops are expected to substitute for a set of currently used herbicides, which might alter the agro-environmental footprint from crop production. To test this hypothesis, the environmental impact of various herbicide regimes currently used with non-GMHR maize in Belgium was calculated and compared with that of possible herbicide regimes applied in GMHR maize. Impacts on human health and the environment were calculated through the pesticide occupational and environmental risk (POCER) indicator. Results showed that the environmental impact of herbicide regimes solely relying on the active ingredients glyphosate (GLY) or glufosinate-ammonium (GLU) is lower than that of herbicide regimes applied in non-GMHR maize. Due to the lower potential of GLY and GLU to contaminate ground water and their lower acute toxicity to aquatic organisms, the POCER exceedence factor values for the environment were reduced approximately by a sixth when GLY or GLU is used alone. However, the environmental impact of novel herbicide regimes tested may be underestimated due to the assumption that active ingredients used with GMHR maize would be used alone. Data retrieved from literature suggest that weed control efficacy is increased and resistance development delayed when GLY or GLU is used together with other herbicides in the GMHR system. Due to the partial instead of complete replacement of currently used herbicide regimes, the beneficial environmental impact of novel herbicide regimes might sometimes be reduced or counterbalanced. Despite the high weed control efficacy provided by the biotechnology-based weed management strategy, neither indirect harmful effects on farmland biodiversity through losses in food resources and shelter, nor shifts in weed communities have been demonstrated in GMHR maize yet. However, with the increasing adoption rate of GMHR maize and their associated novel herbicide regimes, this situation is expected to change in the short-term.

Estimating the effects of Cry1F Bt‐maize pollen on non‐target Lepidoptera using a mathematical model of exposure

Summary 1. In farmland biodiversity, a potential risk to the larvae of non‐target Lepidoptera from genetically modified (GM) Bt‐maize expressing insecticidal Cry1 proteins is the ingestion of harmful amounts of pollen deposited on their host plants. A previous mathematical model of exposure quantified this risk for Cry1Ab protein. We extend this model to quantify the risk for sensitive species exposed to pollen containing Cry1F protein from maize event 1507 and to provide recommendations for management to mitigate this risk. 2. A 14‐parameter mathematical model integrating small‐ and large‐scale exposure was used to estimate the larval mortality of hypothetical species with a range of sensitivities, and under a range of simulated mitigation measures consisting of non‐Bt maize strips of different widths placed around the field edge. 3. The greatest source of variability in estimated mortality was species sensitivity. Before allowance for effects of large‐scale exposure, with moderate within‐crop host‐plant density and with no mitigation, estimated mortality locally was <10% for species of average sensitivity. For the worst‐case extreme sensitivity considered, estimated mortality locally was 99·6% with no mitigation, although this estimate was reduced to below 40% with mitigation of 24‐m‐wide strips of non‐Bt maize. For highly sensitive species, a 12‐m‐wide strip reduced estimated local mortality under 1·5%, when within‐crop host‐plant density was zero. Allowance for large‐scale exposure effects would reduce these estimates of local mortality by a highly variable amount, but typically of the order of 50‐fold. 4. Mitigation efficacy depended critically on assumed within‐crop host‐plant density; if this could be assumed negligible, then the estimated effect of mitigation would reduce local mortality below 1% even for very highly sensitive species. 5.  Synthesis and applications. Mitigation measures of risks of Bt‐maize to sensitive larvae of non‐target lepidopteran species can be effective, but depend on host‐plant densities which are in turn affected by weed‐management regimes. We discuss the relevance for management of maize events where cry1F is combined (stacked) with a herbicide‐tolerance trait. This exemplifies how interactions between biota may occur when different traits are stacked irrespective of interactions between the proteins themselves and highlights the importance of accounting for crop management in the assessment of the ecological impact of GM plants.

Quantifying the introgressive hybridisation propensity between transgenic oilseed rape and its wild/weedy relatives.

In order to estimate the introgressive hybridisation propensity (IHP) between genetically modified (GM) oilseed rape (Brassica napus) and certain of its cross-compatible wild/weedy relatives at the landscape level, a conceptual approach was developed. A gene flow index was established enclosing the successive steps to successfully achieve introgressive hybridisation: wild/weedy relatives and oilseed rape should co-occur, have overlapping flowering periods, be compatible, produce viable and fertile progeny, and the transgenes should persist in natural/weedy populations. Each step was described and scored, resulting in an IHP value for each cross-compatible oilseed rape wild/weedy relative. The gene flow index revealed that Brassica rapa has the highest introgressive hybridisation propensity (IHP value = 11.5), followed by Hirschfeldia incana and Raphanus raphanistrum (IHP = 6.7), Brassica juncea (IHP = 5.1), Diplotaxis tenuifolia and Sinapis arvensis (IHP = 4.5) in Flanders. Based on the IHP values, monitoring priorities can be defined within the pool of cross-compatible wild/weedy oilseed rape relatives. Moreover, the developed approach enables to select areas where case-specific monitoring of GM oilseed rape could be done in order to detect potential adverse effects on cross-compatible wild/weedy relatives resulting from vertical gene flow. The implementation of the proposed oilseed rape–wild relative gene flow index revealed that the survey design of existing botanical survey networks does not suit general surveillance needs of GM crops in Belgium. The encountered hurdles to implement the gene flow index and proposals to acquire the missing data are discussed.

Towards a more open debate about values in decision-making on agricultural biotechnology

Regulatory decision-making over the use of products of new technology aims to be based on science-based risk assessment. In some jurisdictions, decision-making about the cultivation of genetically modified (GM) plants is blocked supposedly because of scientific uncertainty about risks to the environment. However, disagreement about the acceptability of risks is primarily a dispute over normative values, which is not resolvable through natural sciences. Natural sciences may improve the quality and relevance of the scientific information used to support environmental risk assessments and make scientific uncertainties explicit, but offer little to resolve differences about values. Decisions about cultivating GM plants will thus not necessarily be eased by performing more research to reduce scientific uncertainty in environmental risk assessments, but by clarifying the debate over values. We suggest several approaches to reveal values in decision-making: (1) clarifying policy objectives; (2) determining what constitutes environmental harm; (3) making explicit the factual and normative premises on which risk assessments are based; (4) better demarcating environmental risk assessment studies from ecological research; (5) weighing the potential for environmental benefits (i.e., opportunities) as well as the potential for environmental harms (i.e., risks); and (6) expanding participation in the risk governance of GM plants. Recognising and openly debating differences about values will not remove controversy about the cultivation of GM plants. However, by revealing what is truly in dispute, debates about values will clarify decision-making criteria.

Potential use of an arthropod database to support the non-target risk assessment and monitoring of transgenic plants

Abstract Worldwide, plants obtained through genetic modification are subject to a risk analysis and regulatory approval before they can enter the market. An area of concern addressed in environmental risk assessments is the potential of genetically modified (GM) plants to adversely affect non-target arthropods and the valued ecosystem services they provide. Environmental risk assessments are conducted case-by-case for each GM plant taking into account the plant species, its trait(s), the receiving environments into which the GM plant is to be released and its intended uses, and the combination of these characteristics. To facilitate the non-target risk assessment of GM plants, information on arthropods found in relevant agro-ecosystems in Europe has been compiled in a publicly available database of bio-ecological information during a project commissioned by the European Food Safety Authority (EFSA). Using different hypothetical GM maize case studies, we demonstrate how the information contained in the database can assist in identifying valued species that may be at risk and in selecting suitable species for laboratory testing, higher-tier studies, as well as post-market environmental monitoring.