Mathias Otto

A synthesis of laboratory and field studies on the effects of transgenic Bacillus thuringiensis (Bt) maize on non‐target Lepidoptera

One of the major applications of transgenic crops in agriculture are the so‐called Bacillus thuringiensis Berliner (Bt) plants, in particular Bt maizes, which produce insecticidal Cry proteins that target specific orders, such as the Lepidoptera or Coleoptera. We reviewed publications that reported on the direct toxic effects of Bt‐maize and/or Cry proteins of current Bt‐maize events on larvae of non‐target butterflies and moths (Lepidoptera). In total, 20 peer‐reviewed publications were identified, of which 16 papers contributed laboratory‐based data and seven field‐based data. An adverse effect on caterpillars was recorded in 52% of all laboratory‐based and in 21% of all field‐based observations. The variables most often studied and having the highest occurrence of effects were larval survival, body mass, and developmental time. Parameters of the adult stage were under‐represented in the studies. Overall, 11 lepidopteran species were tested. The majority of the studies originated from the USA, with the Monarch butterfly being the most studied, whereas other species and other parts of the world were widely neglected. Laboratory experiments were often run under unrealistic conditions from an ecological point of view. Although the papers we reviewed indicated a potential hazard for Lepidoptera that are exposed to and feed on lepidopteran‐specific Bt‐maize pollen, a general conclusion on the level of risk for butterflies and moths cannot as yet be drawn. A comprehensive risk characterization would require thorough hazard identification, exposure assessment, and impact assessment. However, our review showed that even the basic level of hazard characterization is as yet incomplete. Reasons for this are the still‐limited numbers of publications and concurrent lack of knowledge, the restriction of data to only a few species, the over‐representation of North American species, and the identified limitations of both laboratory and field experiments. The findings of this review suggest that more realistic, ecologically meaningful, and detailed experiments and analyses are crucial to improve the present assessment of Bt‐maize cultivation effects on Lepidoptera.

Maize pollen deposition in relation to distance from the nearest pollen source under common cultivation - results of 10 years of monitoring (2001 to 2010)

BackgroundInformation on pollen dispersal is essential for the risk assessment and management of genetically modified organisms (GMOs) such as Bt maize. We analyzed data on maize pollen deposition at 216 sites in Germany, Switzerland, and Belgium from 2001 to 2010. All data were collected using the same standardized sampling method. The distances between sampling site and the nearest maize field ranged from within the field to 4.45 km.ResultsMaize pollen deposition was negatively correlated with distance from the nearest pollen source. The highest pollen deposition was within the field, but depositions of several thousand pollen grains per square meter were recorded over the kilometer range. A power function model most accurately described the relationship between deposition and distance from the nearest pollen source, rather than the exponential model currently used in EU risk assessment and management, which underestimates exposure for distances greater than 10 m. Regression analysis confirmed the high significance of the power relationship. The large variation in pollen deposition at a given distance reflected the influences of wind direction and other meteorological and site conditions. Plausible variations of single values and the predicted mean pollen count at a given distance were expressed by confidence intervals.ConclusionsThe model described here allows estimations of pollen deposition in relation to distance from the nearest field; therefore, it will be valuable for the risk assessment and management of GMOs. Our results indicate that buffer zones in the kilometer range are required to prevent harmful exposure of non-target organisms to GMOs.

Scrutinizing the current practice of the environmental risk assessment of GM maize applications for cultivation in the EU

PurposeThe prevailing controversies on the potential environmental risks of genetically modified organisms [GMOs] still fuel ongoing discussions among European Union [EU] member states, risk assessors, applicants and scientists, even several years after the commercial introduction of GMOs. The disagreements mainly derive from the current risk assessment practice of GMOs and differences in the perceived environmental risks. Against this background, the aim of this study was to scrutinize the current practice of environmental risk assessment [ERA] of several GMO applications currently pending for authorisation in the EU.MethodsWe analysed the data presented for three assessment categories of the ERA of genetically modified [GM] maize applications for cultivation in the European Union: the agronomic evaluations and the assessments of the effects of GM maize on target organisms and of its potential adverse effects on non-target organisms.ResultsMajor shortcomings causing considerable uncertainties related to the risk assessment were identified in all three categories. In addition, two principles of Directive 2001/18/EC are largely not fulfilled - the consideration of the receiving environment and the indirect effects, as mediated, e.g. by the application of the complementary herbicide in the case of herbicide-tolerant GM maize.ConclusionsWe conclude that the current practice of ERA does not comprehensively fulfil the scientific and legal requirements of Directive 2001/18/EC, and we propose improvements and needs for further guidance and development of standards. The recommendations address likewise applicants, risk assessors as well as decision makers.

Modelling in the light of uncertainty of key parameters: a call to exercise caution in field predictions of Bt-maize effects

Perry et al . [[1][1]] developed a model to simulate the field exposure and adverse effects for three European non-target Lepidoptera species ( Inachis io L., Vanessa atalanta L., and Plutella xylostella L.) to pollen of the Bacillus thuringiensis ( Bt ) maize MON810 containing lepidopteran-

A New Method for in Situ Measurement of Bt-Maize Pollen Deposition on Host-Plant Leaves.

Maize is wind pollinated and produces huge amounts of pollen. In consequence, the Cry toxins expressed in the pollen of Bt maize will be dispersed by wind in the surrounding vegetation leading to exposure of non-target organisms (NTO). NTO like lepidopteran larvae may be affected by the uptake of Bt-pollen deposited on their host plants. Although some information is available to estimate pollen deposition on host plants, recorded data are based on indirect measurements such as shaking or washing off pollen, or removing pollen with adhesive tapes. These methods often lack precision and they do not include the necessary information such as the spatial and temporal variation of pollen deposition on the leaves. Here, we present a new method for recording in situ the amount and the distribution of Bt-maize pollen deposited on host plant leaves. The method is based on the use of a mobile digital microscope (Dino-Lite Pro, including DinoCapture software), which can be used in combination with a notebook in the field. The method was evaluated during experiments in 2008 to 2010. Maize pollen could be correctly identified and pollen deposition as well as the spatial heterogeneity of maize pollen deposition was recorded on maize and different lepidopteran host plants (Centaurea scabiosa, Chenopodium album, Rumex spp., Succina pratensis and Urtica dioica) growing adjacent to maize fields.

Feeding behaviour on host plants may influence potential exposure to Bt maize pollen of Aglais urticae larvae (Lepidoptera, Nymphalidae)

Non-target butterfly larvae may be harmed by feeding on host plants dusted with Bt maize pollen. Feeding patterns of larvae and their utilization of host plants can affect the adverse Bt impact because the maize pollen is distributed unequally on the plant. In a field study, we investigated the feeding of larvae of the Small Tortoiseshell, Aglais urticae, on nettles, Urtica dioica. Young larvae used smaller host plants than older larvae. In general, the position of the larvae was in the top part of the host plant, but older larvae showed a broader vertical distribution on the nettles. Leaf blades and leaf tips were the plant parts most often consumed. Leaf veins were consumed but midribs were fed on to a lesser extent than other plant veins, particularly by young larvae. The feeding behavior of the larvae may increase possible exposure to Bt maize pollen because pollen densities are expected to be higher on the top parts and along leaf veins of nettles.

Prioritizing stream types according to their potential risk to receive crop plant material — A GIS-based procedure to assist in the risk assessment of genetically modified crops and systemic insecticide residues

Crop plant residues may enter aquatic ecosystems via wind deposition or surface runoff. In the case of genetically modified crops or crops treated with systemic pesticides, these materials may contain insecticidal Bt toxins or pesticides that potentially affect aquatic life. However, the particular exposure pattern of aquatic ecosystems (i.e., via plant material) is not properly reflected in current risk assessment schemes, which primarily focus on waterborne toxicity and not on plant material as the route of uptake. To assist in risk assessment, the present study proposes a prioritization procedure of stream types based on the freshwater network and crop-specific cultivation data using maize in Germany as a model system. To identify stream types with a high probability of receiving crop materials, we developed a formalized, criteria-based and thus transparent procedure that considers the exposure-related parameters, ecological status--an estimate of the diversity and potential vulnerability of local communities towards anthropogenic stress--and availability of uncontaminated reference sections. By applying the procedure to maize, ten stream types out of 38 are expected to be the most relevant if the ecological effects from plant-incorporated pesticides need to be evaluated. This information is an important first step to identifying habitats within these stream types with a high probability of receiving crop plant material at a more local scale, including accumulation areas. Moreover, the prioritization procedure developed in the present study may support the selection of aquatic species for ecotoxicological testing based on their probability of occurrence in stream types having a higher chance of exposure. Finally, this procedure can be adapted to any geographical region or crop of interest and is, therefore, a valuable tool for a site-specific risk assessment of crop plants carrying systemic pesticides or novel proteins, such as insecticidal Bt toxins, expressed in genetically modified crops.

Procedure to select test organisms for environmental risk assessment of genetically modified crops in aquatic systems

For a long time, the environmental risk assessment (ERA) of genetically modified (GM) crops focused mainly on terrestrial ecosystems. This changed when it was scientifically established that aquatic ecosystems are exposed to GM crop residues that may negatively affect aquatic species. To assist the risk assessment process, we present a tool to identify ecologically relevant species usable in tiered testing prior to authorization or for biological monitoring in the field. The tool is derived from a selection procedure for terrestrial ecosystems with substantial but necessary changes to adequately consider the differences in the type of ecosystems. By using available information from the Water Framework Directive (2000/60/EC), the procedure can draw upon existing biological data on aquatic systems. The proposed procedure for aquatic ecosystems was tested for the first time during an expert workshop in 2013, using the cultivation of Bacillus thuringiensis (Bt) maize as the GM crop and 1 stream type as the receiving environment in the model system. During this workshop, species executing important ecological functions in aquatic environments were identified in a stepwise procedure according to predefined ecological criteria. By doing so, we demonstrated that the procedure is practicable with regard to its goal: From the initial long list of 141 potentially exposed aquatic species, 7 species and 1 genus were identified as the most suitable candidates for nontarget testing programs. Integr Environ Assess Manag 2017;13:974-979.

Impact of genetically modified organisms on aquatic environments: Review of available data for the risk assessment

The aquatic environment is strongly connected to the surrounding agricultural landscapes, which regularly serve as sources of stressors such as agrochemicals. Genetically modified crops, which are cultivated on a large scale in many countries, may also act as stressors. Despite the commercial use of genetically modified organisms (GMOs) for over 20years, their impact on the aquatic environment came into focus only 10years ago. We present the status quo of the available scientific data in order to provide an input for informed aquatic risk assessment of GMOs. We could identify only 39 publications, including 84 studies, dealing with GMOs in the aquatic environment, and our analysis shows substantial knowledge gaps. The available information is restricted to a small number of crop plants, traits, events, and test organisms. The analysis of effect studies reveals that only a narrow range of organisms has been tested and that studies on combinatorial actions of stressors are virtually absent. The analysis of fate studies shows that many aspects, such as the fate of leached toxins, degradation of plant material, and distribution of crop residues in the aquatic habitat, are insufficiently investigated. Together with these research needs, we identify standardization of test methods as an issue of high priority, both for research and risk assessment needed for GMO regulation.

Synthetic gene drive: between continuity and novelty: Crucial differences between gene drive and genetically modified organisms require an adapted risk assessment for their use

Gene drive organisms differ from “classical” genetically modified organisms in several crucial aspects. It would require new approaches for risk assessment to gauge their potential impact on the environment.