First EFSA Experiences with Monitoring Plans

J. Verbr. Lebensm. 2 (2007) Supplement 1: 33 – 36 1661-5751/07/050033-4 Journal für Verbraucherschutz und Lebensmittelsicherheit DOI 10.1007/s00003-007-0257-9 Journal of Consumer Protection and Food Safety © Birkhäuser Verlag, Basel, 2007

First EFSA experiences with monitoring plans

D. Bartsch1, A. Gathmann1, S. Hartley2, N. B. Hendriksen3, R. Hails4, K. Lheureux5, J. Kiss6, S. Mesdagh5, G. Neemann7, J. Perry8, S. Renckens5, J. Schiemann9 and J. Sweet10 1 BVL, Federal Office of Consumer Protection and Food Safety, Berlin, Germany 2 University of Sussex, Biology and Environmental Science, Brighton, BN1 9RH, United Kingdom 3 Department of Environmental Chemistry and Microbiology, National Environmental Research Institute, University of Aarhus, Frederiksborgvej 399, DK-4000 Roskilde, Denmark 4 Pathogen Population Ecology Centre for Ecology and Hydrology Mansfield Rd OXFORD OX1 3SR, United Kingdom 5 EFSA Largo N. Palli 5/A 43100 Parma, Italy 6 Plant Protection Institute, Szent Istvan University, Pater K. street 1, Godollo, Hungary 7Blau-Umweltstudien, Göttingen, Germany 8 Oaklands Barn, Lug’s Lane, Broome, Norfolk NR35 2HT, United Kingdom 9 Federal Biological Research Centre for Agriculture and Forestry, Institute for Plant Virology, Microbiology and Biosafety, Messeweg 11/12, D-38104 Braunschweig, Germany 10 The Green, Willingham, CB4 5JA Cambridge, United Kingdom

Correspondence to: PD Dr. Detlef Bartsch, Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Referat 404, Mauerstr. 39–42, D-10117 Berlin, Germany, Tel.: +49 1888 444 40400, Fax: +49 1888 444 40009, E-Mail: [email protected]

Received: September 10, 2007

Key words: Directive 2001/18/EC, General surveillance, Case- is needed. In one case (an application for cultivation of a GM specific monitoring, GMO, Regulation (EC) 1829/2003, GMO Risk crop), the GMO Panel recommended case-specific monitoring. assessment. We explain in more detail how the environmental risk assessment of two Bt maize dossiers (maize Bt11 and 1507) were con- Abstract: A plan for Post Market Environmental Monitoring sidered by the GMO Panel in the evaluation of the PMEM plan and (PMEM) of genetically modified (GM) plants is mandatory in all the consequences for the environmental monitoring plan. As applications for deliberate release submitted under EU Directive stated in the EFSA opinion on post-market environmental mo- 2001/18/EC and EU Regulation 1829/2003. PMEM is composed of nitoring, the general surveillance plans shall, when possible, case-specific monitoring and general surveillance of GM plants. make use of existing monitoring systems in addition to more The European Food Safety Authority (EFSA) is responsible for focused monitoring systems. However, the use of these national assessing the scientific quality of PMEM plans submitted with monitoring programmes is outside of the management and each application. In a scientific opinion, the EFSA GMO Panel control of an individual applicant and thus it cannot be the task presented specific guidance for applicants for developing PMEM of an applicant alone to use, modify or improve existing sur- plans. In addition the EFSA GMO Panel explained the scientific veillance systems. The availability of biodiversity monitoring rationale for this guidance and makes a number of recommen- programmes in the EU Member States should be evaluated by dations for the management and conduct of PMEM by both applicants in close liaison with risk managers. applicants and risk managers. Until the end of March 2007, the EFSA GMO Panel gave opinions on 11 PMEM plans submitted under EU Directive 2001/18/EC and another 11 plans submitted 1. Introduction within applications under EU Regulation 1829/2003. Currently 27 applications for GM plants are still in the evaluation process and A plan for Post Market Environmental Monitoring (PMEM) of the EFSA GMO Panel sent 26 questions to the applicants for genetically modified (GM) plants is mandatory in all applica- clarification and additional information during the evaluation tions for deliberate release submitted under EU Directive 2001/ process. Sixteen of these questions were related to General 18/EC (EC, 2001) and EU Regulation 1829/2003 (EC, 2003). PMEM Surveillance (e.g. general structure, farm & operator que- is composed of case-specific monitoring and general surveil- stionnaires, integrations of identity preservation systems, use of lance of GM plants. The European Food Safety Authority (EFSA) existing surveillance systems, feral plant surveillance). Nine is responsible for assessing the scientific quality of PMEM plans questions requested clarification on the environmental risk as- submitted with each application. In a scientific opinion, the sessment, which might effect whether case-specific monitoring EFSA GMO Panel presented specific guidance for applicants for 34 D. Bartsch et al.

developing PMEM plans (EFSA, 2006a). In addition, the EFSA the USA or in Europe (Evans, 2002; Tabashnik et al., 2005; GMO Panel explained the scientific rationale for this guidance Bourguet et al., 2002; Farinós et al., 2004, Saeglitz et al., 2006, and makes a number of recommendations for the manage- Eizaguirre et al., 2006). In the Bt11 and 1507 maize notifica- ment and conduct of PMEM by both applicants and risk ma- tions, insect-resistance management (IRM) plans, including nagers (Bartsch et al., 2006). the high dose/refuge resistance management strategy, were provided by the applicants. The GMO Panel supports these approaches to minimize/delay the potential resistance deve- 2. Recent experience of applications for import and lopment of target organisms. The GMO Panel also points out processing and for cultivation of GM plants that the use of non-GM border rows as refuges would also have the effect of reducing exposure of field margin weeds (and Until the end of March 2007, the EFSA GMO Panel gave opi- hence non-target Lepidoptera, see Schmitz et al., 2003) to pol- nions on 11 PMEM plans submitted under EU Directive 2001/18/ len from Bt maize. EC and another 11 plans submitted within applications under Therefore, the GMO Panel has recommended that case- EU Regulation 1829/20031. Currently 27 applications for GM specific monitoring for resistance development in target or- plants are still under scientific evaluation by the GMO Panel ganisms is a requirement for Bt resistant genetically modified and the EFSA GMO Panel sent 26 questions to the applicants for Bt11 and 1507 maize crops cultivated in the EU (EFSA, 2005a, clarification and additional information during the evaluation 2005b). process. Sixteen of these questions were related to General Surveillance (e.g. general structure, farm & operator ques- 3.2 General Surveillance tionnaires,ACHTUNGRE integrations of identity preservation systems, use of As indicated in its earlier opinion, the EFSA GMO Panel re- existing surveillance systems, feral plant surveillance). Nine commends that General Surveillance for unanticipated ad- questions requested clarification on the environmental risk verse effects of GM plants for cultivation should be protection assessment which might influence decisions on the need for goal oriented to allow for an efficient use of potentially limited case-specific monitoring (e.g. environmental exposure of ex- resources within new and existing surveillance systems (EFSA, pressed proteins or accidental release of GM seeds). In one case 2006b). In addition, the GMO Panel recommended that gen- (an application for cultivation of a GMP), the GMO Panel re- eral surveillance in the Member States should make full use of commended case-specific monitoring. More details on the existing and on-going monitoring studies that can supply re- nature of the environmental risk assessment and its conse- levant data. Three examples are described: quences for risk management measures are given for two examples in the following chapter. (1) One of the best-known examples for connecting environmental monitoring of biodiversity to potential needs of general surveillance comes from Switzerland (not a 3. Specific comments on Bt11 and 1507 maize PMEM plans – Member of the EU). The Swiss Biodiversity Monitoring applications for cultivation Programme (BDM) has carried out measurements of biological diversity since 2001 using evenly-spread random 3.1 Case specific monitoring plots all over the country which are sampled to draw The risk assessment of Bt11 (EFSA, 2005a) and 1507 maize (EFSA, conclusions about Switzerland as a whole (Bühler, 2006). A 2005b) indicated a risk that the target organisms might de- central coordination office compiles data collection, ana- velop resistance to the Cry proteins (Cry1Ab protein expressed lysis and publication. Vascular plants, breeding birds and in Bt11 maize and Cry1F protein expressed in 1507 maize). This butterflies are assessed. From a conceptional point of view, triggered the need for specific monitoring for resistance of the the sampling strategy of BDM meets the basic principles of target species (lepidopteran pest species like Ostrinia nubilalis general surveillance (EFSA, 2006b). The BDM provides ba- (European Corn Borer, ECB), and Sesamia nonagrioides (West seline information that can be used to detect unanticipa- African Pink Borer) and implementation of risk management ted consequences of the cultivation of GM plants (Bühler, strategies to reduce the likelihood of resistance developing. 2006). The BDM uses no predictions about the changes Recent resistance monitoring measures conducted on Bt that might happen to infer a specific sampling design and maize in Spain (Eizaguirre et al., 2006) has shown no build up so is not hypothesis-driven. This is one of the main at- of resistance in pest species but has concluded that the com- tributes of general surveillance pointed out by several pulsory high-dose/refuge strategy was the most efficient tool authors (Sanvido et al., 2005; ACRE, 2004; COGEM, 2005; to minimize/delay resistance development in target orga- EFSA, 2006b). Both BDM and General Surveillance search nisms. for unanticipated adverse effects. Both lepidopteran species, Ostrinia nubilalis and Sesamia (2) A second example of a connection to general surveillance nonagrioides, are already the subject of monitoring and re- is the biological survey of the national territory of France, sistanceACHTUNGRE management studies in Europe. Up to now, resistant which consists of monitoring the evolution of crop pests O. nubilalis and S. nonagrioides have not been found in fields in and other bio-indicators linked to agricultural produc- tions (Delos et al., 2006). The annual assessments of a large number of indicators enable the detection of significant 1 overview at http://www.efsa.europa.eu/en/science/gmo/gmo_opinions.html time trends which may be linked to agricultural practices, EFSA experiences 35

new plant protection products, changes in farming prac- plement additional monitoring and inspection as laid down in tices or plant cultivars. The early detection survey of any recital 44 and Article 4(5) of Directive 2001/18/EC. significant modification was developed in accordance with the French Agricultural Orientation Law of 1999 im- plementing biovigilance activity (Loi n 99–574 d’orienta- 5. References tion agricole, 1999). Since 1998, this surveillance has been aimed at a number of pests and other animal organisms of ACRE (2004) Guidance on best practice in the design of post-market maize crops. It was extended to other environment para- monitoring plans in submissions to the advisory committee on meters: weed flora on nearly 900 fields of different crops releases to the environment. ACRE Guidance Note 16. http:// www.defra.gov.uk/environment/acre/postmarket/acre_post- in rotation since 2002, spread on the main crops areas of marketmonitor-guidance.pdf the territory, fungi of corn kernel and mycotoxins since Bartsch, D., Bigler, F., Castanera, P., Gathmann, A., Gielkens, M., 2004, soil pests and birds since 2005. In 2006, the pro- Hartley, S., Lheureux, K., Renckens, S., Schiemann, J., Sweet, J. gramme continued including all plant diseases and pests and Wilhelm, R. (2006) Concepts for General Surveillance of of crops involved in a rotation on a nine hundred fields- Genetically Modified (GM) Plants: The EFSA position. J Verbr network. Lebensm 1, Supplement 1: 15–20. (3) A third example is provided by Traxler et al. (2005) for Bourguet, D., Chaufaux, J., Micoud, A., Delos, M., Naibo, B., Bom- Austria. Here, on butterflies, 24.300 data-records are bardes, F., Marque, G., Eychenne, N. and Pagliari, C. (2002) Ost- rinia nubilalis parasitism and the field abundance of non-target available as baseline data to compare any future changes insects in transgenic Bacillus thuringiensis corn (Zea mays). En- at a landscape level. Within the 215 species of butterflies viron Biosafety Res 1: 49–60. occurring in Austria, 152 appear in agricultural landscapes Bühler, C. (2006) Biodiversity Monitoring in Switzerland: What can and therefore are in potential contact with GM crops (e.g. we learn for general surveillance of GM crops? J Verbr Lebensm pollen of Bt maize). Maps were already designed for pa- 1, Supplement 1: 37–41. rameters “pollination time from maize” and “larval de- COGEM (2005) Post-market monitoring of genetically modified velopmentACHTUNGRE of butterflies”. These baseline data could be a crops in the Netherlands. COGEM advice CGM/050414–03. Delos, M., Hervieu, F., Folcher, L., Micoud, A. and Eychenne, N. (2006) starting point for post-market surveillance of Bt maize Biological surveillance programme for the monitoring of crop cultivation in Austria. pests and indicators in France. J Verbr Lebensm 1, Supplement 1: 30–36. Following several requests from the GMO Panel to the ap- EC (2001) Directive 2001/18/EC of the European Parliament and of the plicants for clarifications and modifications of the proposed Council of 12 March 2001 on the deliberate release into the en- monitoring plans, the PMEM plans for Bt11 maize and 1507 vironment of genetically modified organisms and repealing maize were finally accepted by the GMO Panel and were Council Directive 90/220/EEC. Official J Europ Communities communicated to the risk managers (European Commission, L106: 1–38. http://europa.eu.int/eurlex/pri/en/oj/dat/2001/l_106/ l_10620010417en00010038.pdf Directorate General ‘Environment’) as part of the scientific EC (2003) Regulation (EC) 1829/2003 of the European Parliament and opinions of the GMO Panel on Bt11 maize and 1507 maize and as of the Council of 22 September 2003 on genetically modified a basis for the final authorisation process. Further information food and feed. Official J Europ Communities L 268: 1–23. http:// on the status of notifications under Directive 2001/18/EC at the europa.eu.int/eur-lex/pri/en/oj/dat/2003/l_268/l_26820031018en- European Commission is available2. 00010023.pdfACHTUNGRE EFSA (2005a) Opinion of the Scientific Panel on Genetically Modified Organisms on a request from the Commission related to the notification (Reference C/F/96/05.10) for the placing on the 4. Conclusions market of insect resistant genetically modified maize Bt11, for cultivation, feed and industrial processing, under Part C of Di- There is obviously a case-by-case learning process on best rective 2001/18/EC from Syngenta Seeds. EFSA J 213: 1–33. http:// PMEM practice and the quality of the monitoring plans pre- www.efsa.eu.int/science/gmo/gmo_opinions/922/gmo_opinion_- sented by the applicants is increasing since the publication of ej213_bt11maize_cultivation_en1.pdfACHTUNGRE the EFSA guidance document on PMEM. As stated in the EFSA EFSA (2005b) Opinion of the GMO Panel related to the notification opinion on post-market environmental monitoring (EFSA, (Reference C/ES/01/01) for the placing on the market of insect- tolerant genetically modified maize 1507 for import, feed and 2006a), the use of national monitoring programmes is outside industrial processing and cultivation, under Part C of Directive of the management and control of an individual applicant and 2001/18/EC from Pioneer Hi-Bred International/Mycogen Seeds. thus it cannot be the task of an applicant alone to use, modify (Question No EFSAQ- 2004–072). EFSA J 181: 1–33. http:// or improve existing surveillance systems. The availability of www.efsa.eu.int/science/gmo/gmo_opinions/827/op_gm08_ej181- biodiversity monitoring programmes in the EU Member States _1507_opinion_doc1_2en1.pdfACHTUNGRE should be evaluated by applicants in close liaison with risk EFSA (2006a) Opinion of the Scientific Panel on Genetically Modified managers. The GMO Panel also expresses its opinion that it Organisms on the Post Market Environmental Monitoring would be valuable if Member States would improve or adapt (PMEM) of genetically modified plants. EFSA J 319: 1–27. http:// www.efsa.europa.eu/science/gmo/gmo_opinions/1381/gmo_op_- existing national environmental monitoring systems and im- ej319_pmem_en1.pdfACHTUNGRE EFSA (2006b) Guidance document of the Scientific Panel on Gen- etically Modified Organisms for the Risk Assessment of Genetically 2 http://ec.europa.eu/environment/biotechnology/authorised_prod_2.htm. Modified Plants and Derived Food and Feed. EFSA J 374: 1–115. 36 D. Bartsch et al.

Eizaguirre, M., Albajes, R., López, C., Eras, J., Lumbieres, B. and Pons, ceptual framework for the design of environmental post-market X. (2006) Six years after the commercial introduction of Bt maize monitoring of genetically modified plants. Environm Biosafety in Spain: field evaluation, impact and future prospects. Trans- Res 4: 13–27. genic Res 15: 1–12. Schmitz, G., Pretscher, P. and Bartsch, D. (2003) Selection of relevant Evans, H. F. (2002) Environmental impact of Bt exudates from roots of non-target herbivores for monitoring the environmental effects genetically modified plants. Defra-Report (EPG 1/5/156). of Bt maize pollen. Environm Biosafety Res 2: 117–132. Farinós, G. P., de la Poza, M., Hernández-Crespo, P., Ortego, F. and Tabashnik B. E., Dennehy T. J. and Carriere Y. (2005) Delayed res- Castañera, P. (2004) Resistance monitoring of field populations istance to transgenic cotton in pink bollworm. Proc Natl Acad Sci of the corn borers Sesamia nonagrioides and Ostrinia nubilalis USA 102: 15389–15393. after 5 years of Bt maize cultivation in Spain. Entomologia Ex- Traxler, A., Minarz, E., Höttinger, H., Pennerstorfer, J., Schmatz- perimentalis et Applicata 110: 23. berger, A., Banko, G., Placer, K., Hadrobolec, M. and Gaugitsch, Loi n899–574 d’orientation agricole (1999) J.O n 158 du 10 juillet 1999 H. (2005) Hotspots of biodiversity within agricultural landscapes page 10231 http://www.legifrance.gouv.fr/WAspad/UnTexteDe- as a basis for risk assessment and monitoring of GMO (Bio- Jorf ?numjo=AGRX9800053L diversitäts-Hotspots der Agrarlandschaft als Eckpfeiler für Risi- Saeglitz, C., Bartsch, D., Eber, S. Gathmann A., Priesnitz, K. U. and koabschätzung und Monitoring von GVO). Rote Reihe des Bun- Schuphan, I. (2006) Monitoring the Cry1Ab susceptibility of Eu- desministeriums für Gesundheit und Frauen – Sektion IV. ropean Corn Borer (Ostrinia nubilalis Hbn.) in Germany. J Eco- Band 5/05. http://www.bmgf.gv.at/cms/site/attachments/4/9/0/ nomic Entomol 99: 1768–-1773. Sanvido, O., Widmer, F., Winzeler, M. and Bigler, F. (2005) A con- CH0255/CMS1134473757104/biodiv__hotspots_engl.pd

To access this journal online: http://www.birkhauser.ch/JVL