GMOs in Integrated Plant Production IOBC-WPRS Bulletin Vol. 114, 2016 pp. 31-35 Arthropod communities in European arable crops a database Michael Meissle 1, Judith Riedel 1, Adalbert Balog 2, Paweł Bereś 3, Marcin Grabowski 4, David A. Bohan 5, Xavier Pons 6, Jörg Romeis 1 1 Agroscope, Institute for Sustainability Sciences, Reckenholzstrasse 191, 8046 Zürich, Switzerland; 2 Sapientia Hungarian University of Transylvania, Faculty of Technical and Human Sciences, 540485 Târgu-Mureş, Romania; 3 Institute of Plant Protection National Research Institute, Regional Experimental Station Rzeszów, Gen. Langiewicza 28 St., 35-101 Rzeszów, Poland; 4 Department of Applied Entomology, Faculty of Horticulture, Biotechnology and Landscape Architecture, Warsaw University of Life Sciences, Nowoursynowska 159 St., 02-776 Warsaw, Poland; 5 Agroécologie, INRA Centre de Dijon, 17 Rue Sully, 21065 Dijon, France; 6 Department of Crop and Forest Sciences, Agrotecnio Center, Universitat de Lleida, Avinguda Rovira Roure 191, 25198 Lleida, Spain E-mail: michael.meissle@agroscope.admin.ch Abstract: Knowledge of the arthropod fauna found within and around agricultural fields is a basis for the non-target risk assessment of plant protection technologies, including genetically modified (GM) crops. Test species for laboratory experiments should be suitable representatives of field populations that are likely to be exposed and sensitive to the stressor of concern. Moreover, species monitored in field trials should be representative for the growing area of the crop for which the risk assessment is conducted. Building on systematic literature searches, a database of bio-ecological information of arthropod species found in arable crops across Europe was established. This database, commissioned by the European Food Safety Authority (EFSA), contains referenced descriptions of the ecological function and the taxonomy of > 4000 arthropod species derived from > 27000 records and > 2000 publications across the European continent. The database covers major European crops, such as small grain cereals, maize, oilseed rape, potato and beet, as well as minor crops including rice, cotton, and soybean. The database gives a comprehensive overview of the arthropod communities in European agro-ecosystems and can assist in the identification of relevant non-target species to be addressed in the risk assessment of GM crops. It can also help to assess the similarities and differences in the arthropod communities across crops and environmental regions and thus contribute to the transportability of risk assessment data. Key words: genetically modified crops, risk assessment, systematic literature searches Background Before new genetically modified (GM) plants can be released into the environment, an environmental risk assessment needs to be conducted. For the European Union, guidance is provided by the European Food Safety Authority (EFSA, 2010). Part of this assessment is the evaluation of potentially adverse effects on non-target organisms (NTOs). Arthropods are an important group of NTOs as they provide a range of different ecosystem services, such as biological control, pollination, decomposition, and herbivory (which is undesired for crop hosts and beneficial for weed hosts). To be able to build relevant risk hypotheses in the problem formulation phase of the risk assessment, it is important to know which arthropods inhabit the crop in the region where the GM crop is expected to be released. Knowledge of 31
32 arthropod abundance in a range of European arable crops has been collected to construct a database commissioned by EFSA, which is presented here. European arable crops Statistical data on agricultural production in the European Union (EU) is available from Eurostat (http://ec.europa.eu/eurostat/data/database). Cereals dominate the agricultural land in Europe. The largest areas are cropped with wheat, followed by maize and barley (Figure 1). Other important cereals include triticale, oats, and rye. Cereals for the production of grain covered 58 million hectares of agricultural land in the EU in 2015. Fodder crops covered 21 million hectares in 2014, including temporary grasses and grazing land, leguminous plants, green maize, and other cereals harvested green. Oilseed crops were grown on more than 11 million hectares, mainly represented by oilseed/turnip rape and sunflower, and on a much smaller area, soybeans. Permanent crops, such as fruits, berries, and nuts were cultivated on 11 million hectares. Fresh vegetables covered 2 million hectares in 2014. Finally, fibre crops, such as flax, hemp, and cotton, are of minor importance in European agriculture (< 0.5 million hectares). Figure 1: Most important crops grown on the agricultural land in the European Union. Black bars represent crops that are covered by the arthropod database. Data from Eurostat (http://ec.europa.eu/eurostat/data/database), table apro_acs_a. Whenever available, data from 2015 were used, otherwise from 2014.
33 The arthropod database The first arthropod database was established in 2009 and contained information on arthropods collected in European maize crops (Knecht et al., 2009). Maize was selected because insecticidal maize transformed with genes from Bacillus thuringiensis (Bt) has been cultivated in Europe since 1996. It is currently the only GM crop grown commercially in Europe (James, 2014; Meissle et al., 2013). Subsequently, EFSA commissioned the establishment of an arthropod database including data from a range of important European crops, such as maize, potato, oilseed rape, and beet (Meissle et al., 2012). It also included minor crops, such as rice, cotton, and soybean. All of those crops have been genetically engineered, either for herbicide tolerance (maize, oilseed rape, beet, cotton, soy) or insect resistance (maize, potato, rice, cotton), and have been commercialized or are close to commercialization in other parts of the world. Between 2010 and 2012, almost 14000 records of 2900 species were entered from ca. 1000 scientific publications. Literature was searched and screened systematically for relevant publications, from which data on species taxonomy and ecology, collection locations and methods, and arthropod abundance were extracted. In a follow-up project also funded by EFSA, arthropod data on small grain cereals have been entered and the database was updated for the previous crops (Riedel et al., 2015). Small grain cereals have been the target of genetic improvements in the recent years, even through no plants are commercially grown yet (Parisi et al., 2016). GM traits include e.g. herbicide tolerance, disease resistance or drought and salinity tolerance. The extended and updated database comprises more than 27000 records of more than 4000 species derived from over 2000 publications. Arthropod communities in arable crops Most of the arthropod records in the database come from the functional groups of herbivores and predators. Relatively few records are available for decomposers, parasitoids, and pollinators. Because herbivores are often specialized to certain crops, the taxonomic composition of this functional group differs among the crops. However, most herbivore species across all crops belong to the taxonomic orders of Hemiptera, Coleoptera, Lepidoptera, and Diptera. Similarly, parasitoids are specialized on certain host arthropods and the communities consist of different species in the different crops. Most parasitoids belong to the order of Hymenoptera, while some Diptera and Coleoptera (Staphylinidae) species have also been identified. In contrast, predators are often generalists and a number of species can be found in all crops. Predators mainly comprise species from the orders Coleoptera (mainly Carabidae and Staphylinidae), Araneae, and Diptera. Similarly, decomposers inhabit the soil more or less independently from the crop that is grown. Decomposer records were mainly available for Collembola and Diptera, while few records comprise Coleoptera and Acari species. Finally, records of pollinators are dominated by bees (Hymenoptera: Apidae). However, a range of different flying arthropods from the orders of Diptera, Lepidoptera, and Coleoptera is likely to contribute to pollination.
34 Using the database for risk assessment Because it is not feasable to assess the risk for all species potentially present in the field explicitly, risk assessment focuses on important representatives of the arthropod community that are likely to be exposed to the stressor of concern (EFSA, 2010). Thus species have to be selected for the assessment and eventually for experimental testing (Romeis et al., 2012). Test species for laboratory experiments should be suitable representatives of field populations. Moreover, species monitored in field trials should be representative for the growing area of the crop for which the risk assessment is conducted. This growing area may cover different environmental regions with different arthropod communities. Romeis et al. (2014) demonstrate how the arthropod database can assist in the selection of species for risk assessment: - Step 1: Identify the ecosystem services (and functional groups) hypothesized to be provided by non-target arthropods - Step 2: Identify the main taxonomic groups and species associated with the different functional groups - Step 3: Prioritise non-target species based on potential risk considering ecological criteria (abundance, geographic distribution, likely exposure) and likely sensitivity to the GM trait - Step 4: If assessment requires additional experiments, practical considerations help to identify the selection of species most suitable to test the risk hypothesis (e.g. availability of test protocols, commercial sources, collectability, etc.) The database provides generic information for steps 1 and 2. It can further contribute to step 3, which has to be done on a case-by-case basis, by providing abundance and geographic distribution data (Romeis et al., 2014). The database can also contribute to data transportability among crops and among geographic regions. This is important because the European continent covers several environmental zones, such as the atlantic, boreal, continental, and mediteranean zone, with potentially different arthropod communities. While some species occur in all zones, there are also more local species restricted to particular zones. For laboratory testing and monitoring, choosing more ubiquitous species will ensure that the obtained results are widely applicable. Furthermore, arthropod data of a particular crop (e.g. a minor crop in Europe, such as cotton or soybean) might be scarce, while data of other crops are available. For generalist species (e.g. predators or decomposers), species lists from other crops might be applicable also for the crop in question. Using statistical methods, such as rarefaction and extrapolation, the similarity of the species composition of different crops or geographic regions can be compared. Prerequisite for such comparisons, however, is the availability of a number of comprehensive species lists covering a certain taxonomic group. Candidate groups for statistical comparisons are carabid beetles, linyphiid and lycosid spiders, aphids, and aphid parasitoids. Rarefaction curves also give an indication how comprehensive the database is for certain taxonomic groups. Finally, the database might also be useful for the risk assessment of other agricultural technologies, such as chemical and biological pesticides or biological control agents.
35 Acknowledgements The database was established with funding from the European Food Safety Authority (EFSA), grant numbers CT-EFSA-GMO-2010-2 and OC-EFSA-GMO-2013-02. References EFSA 2010: Guidance on the environmental risk assessment of genetically modified plants. EFSA Panel on Genetically Modified Organisms (GMO). EFSA J. 8: 1879. URL: http://www.efsa.europa.eu/it/scdocs/doc/1879.pdf James, C. 2014: Global status of commercialized biotech/gm crops: 2014. ISAAA Brief No. 49, ISAAA, Ithaca, NY. Knecht, S., Romeis, J., Malone, L. A., Candolfi, M. P., Garcia-Alonso, M., Habuštová, O., Huesing, J. E., Kiss, J. & Nentwig, W. 2010: A faunistic database as a tool for identification and selection of potential non-target arthropod species for regulatory risk assessment of GM maize. IOBC-WPRS Bull. 52: 65-69. Meissle, M., Álvarez-Alfageme, F., Bigler, F., Bohan, D. A., Devos, Y., Malone, L. A., Pons, X., Rauschen, S. & Romeis, J. 2013: Arthropods in European maize fields Describing the receiving environment for the risk assessment of GM crops. IOBC-WPRS Bulletin 97: 81-87. Meissle, M., Álvarez-Alfageme, F., Malone, L. A. & Romeis, J. 2012: Establishing a database of bio-ecological information on non-target arthropod species to support the environmental risk assessment of genetically modified crops in the EU. EFSA supporting publications 2012: EN-334. European Food Safety Authority (EFSA), Parma, Italy. URL: http://www.efsa.europa.eu/en/supporting/pub/334e Parisi, C., Tillie, P. & Rodriguez-Cerezo, E. 2016: The global pipeline of GM crops out to 2020. Nature Biotechnology 34: 31-36. Riedel, J., Romeis, J. & Meissle, M. 2015: Update and expansion of the database of bioecological information on non-target arthropod species established to support the environmental risk assessment of genetically modified crops in the EU. EFSA supporting publication 2016: EN-956. European Food Safety Authority (EFSA), Parma, Italy. URL: http://www.efsa.europa.eu/de/supporting/pub/956e Romeis, J., Raybould, A., Bigler, F., Candolfi, M. P., Hellmich, R. L., Huesing, J. E. & Shelton, A. M. 2012: Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops. Chemosphere 90: 901-909. Romeis, J., Meissle, M., Álvarez-Alfageme, F., Bigler, F., Bohan, D. A., Devos, Y., Malone, L. A., Pons, X. & Rauschen, S. 2014: Potential use of an arthropod database to support the nontarget risk assessment and monitoring of transgenic plants. Transgenic Research 23: 995-1013.
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