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Assessment of risk of insect-resistant transgenic crops to nontarget arthropods

Nature Biotechnology volume 26, pages 203–208 (2008)Cite this article

Abstract

An international initiative is developing a scientifically rigorous approach to evaluate the potential risks to nontarget arthropods (NTAs) posed by insect-resistant, genetically modified (IRGM) crops. It adapts the tiered approach to risk assessment that is used internationally within regulatory toxicology and environmental sciences. The approach focuses on the formulation and testing of clearly stated risk hypotheses, making maximum use of available data and using formal decision guidelines to progress between testing stages (or tiers). It is intended to provide guidance to regulatory agencies that are currently developing their own NTA risk assessment guidelines for IRGM crops and to help harmonize regulatory requirements between different countries and different regions of the world.

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Figure 1: Assessment continuum within a tiered scheme of ecological risk assessment.
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References

  1. James, C. Global status of commercialized biotech/GM crops: 2006. ISAAA Briefs No. 35 (International Service for the Acquisition of Agric.-Biotech Applications, Ithaca, NY, USA, 2005).

  2. Nap, J.P., Metz, P.L.J., Escaler, M. & Conner, A.J. The release of genetically modified crops into the environment - Part I. Overview of current status and regulations. Plant J. 33, 1–18 (2003).

    Article  Google Scholar 

  3. Conner, A.J., Glare, T.R. & Nap, J.P. The release of genetically modified crops into the environment - Part II. Overview of ecological risk assessment. Plant J. 33, 19–46 (2003).

    Article  Google Scholar 

  4. Rose, R.I. (ed.) White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target invertebrates for regulatory risk assessment (USDA-APHIS and US Environmental Protection Agency, Washington, DC, USA, 2007). <http://www.epa.gov/pesticides/biopesticides/pips/non-target-arthropods.pdf>

  5. Canadian Food Inspection Agency. Assessment criteria for determining environmental safety of plants with novel traits. Directive 94–08 (Canadian Food Inspection Agency, Government of Canada, Ottawa, Ontario, 2004).

  6. European Community (EC). Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EEC. Off. J. Eur. Commun. L 106, 1–39 (2001). <http://ec.europa.eu/environment/biotechnology/pdf/dir2001_18.pdf>

  7. European Commission (EC). Commission Decision (2002/623/EC) of 24 July 2002 establishing guidance notes supplementing Annex II to Directive 2001/18/EC of the European Parliament and of the Council of the deliberate release in to the environment of genetically modified organisms and repealing Council Directive 90/220/EEC. Off. J. Eur. Commun. L 200, 22–33 (2002). <http://ec.europa.eu/environment/biotechnology/pdf/dec2002_623.pdf>

  8. European Food Safety Authority (EFSA). Guidance document of the Scientific Panel on Genetically Modified Organisms for the risk assessment of genetically modified plants and derived food and feed. EFSA J. 99, 1–100 (2006). <http://www.efsa.europa.eu/EFSA/Scientific_Document/ gmo_guidance_gm_plants_en,0.pdf>

  9. Secretariat of the Convention on Biological Diversity. Cartagena Protocol on Biosafety to the Convention on Biological Diversity: Text and Annexes (Secretariat of the Convention on Biological Diversity, Montreal, Canada, 2000).

  10. Romeis, J. Non-target risk assessment of GM crops and regulation. IOBC WPRS Bull. 29(5), 197–200 (2006).

    Google Scholar 

  11. Wolt, J.D. & Peterson, K.D. Agricultural biotechnology and societal decision-making: the role of risk analysis. AgBioForum 3, 39–46 (2000). <http://www.agbioforum.org/v3n1/v3n1a06-wolt.htm>

    Google Scholar 

  12. Johnson, K.L., Rabould, A.F., Hudson, M.D. & Poppy, G.M. How does scientific risk assessment of GM crops fit within the wider risk analysis? Trends Plant Sci. 12, 1–5 (2007).

    Article  CAS  Google Scholar 

  13. US Environmental Protection Agency (USEPA). Guidelines for ecological risk assessment. EPA 630/R-95–002F (Environmental Protection Agency, Washington, DC, USA, 1998).

  14. Raybould, A. Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops. Environ. Biosafety Res. 5, 119–125 (2006).

    Article  Google Scholar 

  15. National Research Council (NRC). Field testing genetically modified organisms: framework for decisions (NRC Committee on Scientific Evaluation of the Introduction of Genetically Modified Microorganisms and Plants into the Environment, National Academy Press, Washington, DC, 1989).

  16. Tiedje, J.M. et al. The planned introduction of genetically modified organisms: ecological considerations and recommendations. Ecology 70, 298–315 (1989).

    Article  Google Scholar 

  17. Hokanson, K. et al. The concept of familiarity and pest resistant plants. in Proc., Ecological Effects of Pest Resistance Genes in Managed Ecosystems, January 31–February 3, 1999, Bethesda, Maryland (eds. Trayner, P.L. & Westwood, J.H.), 15–19 (Information Systems for Biotechnology, Blacksburg, Virginia, USA, 1999).

    Google Scholar 

  18. Organisation for Economic Cooperation and Development (OECD). Safety considerations for biotechnology: scale-up of crop plants (Organisation for Economic Cooperation and Development, Paris, 1993). <http://www.oecd.org/dataoecd/26/26/1958527.pdf? channelld=34537&homeChannelld=33703&file Title=Safety+Considerations+for+Biotechnology+Scale-up+of+Crop+Plants>

  19. Kuiper, H.A., Kleter, G.A., Noteborn, H.P.J.M. & Kok, E.J. Assessment of the food safety issues related to genetically modified foods. Plant J. 27, 503–528 (2001).

    Article  CAS  Google Scholar 

  20. Bradford, K.J., Van Deynze, A., Gutterson, N., Parrott, W. & Strauss, S.H. Regulating transgenic crops sensibly: lessons from plant breeding, biotechnology and genomics. Nat. Biotechnol. 23, 439–444 (2005).

    Article  CAS  Google Scholar 

  21. Glare, T.R. & O'Callaghan, M. Bacillus thuringiensis: Biology, Ecology and Safety (John Wiley & Sons Ltd, Chichester, UK, 2000).

    Google Scholar 

  22. Romeis, J., Meissle, M. & Bigler, F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24, 63–71 (2006).

    Article  CAS  Google Scholar 

  23. Hill, R.A. & Sendashonga, C. General principles for risk assessment of living modified organisms: lessons from chemical risk assessment. Environ. Biosafety Res. 2, 81–88 (2003).

    Article  Google Scholar 

  24. Touart, L.W. & Maciorowski, A.F. Information needs for pesticide registration in the United States. Ecol. Appl. 7, 1086–1093 (1997).

    Article  Google Scholar 

  25. Peters, R.H. A Critique for Ecology (Cambridge University Press, Cambridge, UK, 1991).

    Google Scholar 

  26. Marvier, M., McCreedy, C., Regetz, J. & Kareiva, P. A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316, 1475–1477 (2007).

    Article  CAS  Google Scholar 

  27. Dutton, A., Romeis, J. & Bigler, F. Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study. BioControl 48, 611–636 (2003).

    Article  CAS  Google Scholar 

  28. Barrett, K.L., Grandy, N., Harrison, E.G., Hassan, S. & Oomen, P. (eds.) Guidance document on regulatory testing procedures for pesticides with non-target arthropods. From the ESCORT workshop (European Standard Characteristics of Non-Target Arthropod Regulatory Testing) (Society of Environmental Toxicology and Chemistry Europe, Brussels, Belgium, 1994).

  29. American Society for Testing and Materials (ASTM). Standard guide for selection of resident species as test organisms for aquatic and sediment toxicity tests. Document E 1850 (American Society for Testing and Materials ASTM International, West Conshohocken, Pennsylvania, USA 2004).

  30. Scholte, E.J. & Dicke, M. Effects of insect-resistant transgenic crops on non-target arthropods: first step in pre-market risk assessment studies. A literature-based study, proposing an ecologically based first step to select non-target organisms. COGEM report CGM 2005–06 (2005). <http://www.cogem.net/ContentFiles/CGM%202005-06.pdf>

    Google Scholar 

  31. Niemi, G.J. & McDonald, M.E. Application of ecological indicators. Annu. Rev. Ecol. Evol. Syst. 35, 89–111 (2004).

    Article  Google Scholar 

  32. Candolfi, M. et al. Principles for regulatory testing and interpretation of semi-field and field studies with non-target arthropods. J. Pest Sci. 73, 141–147 (2000).

    Google Scholar 

  33. Candolfi, M.P. et al. (eds.). Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods. From the ESCORT 2 workshop (European Standard Characteristics of Non-Target Arthropod Regulatory Testing), a joint BART, EPPO/CoE, OECD and IOBC Workshop, organized in conjunction with SETAC Europe and EC (Society of Environmental Toxicology and Chemistry Office, Pensacola, Florida, USA, 2001).

  34. Levin, S.A., Harwell, M.A., Kelly, J.R. & Kimball, K.D. Ecotoxicology problems and approaches. in Ecotoxicology: Problems and Approaches. (ed. Levin, S.A.) 3–8 (Springer, New York, USA, 1989).

    Chapter  Google Scholar 

  35. Caro, T.M. & O'Doherty, G. On the use of surrogate species in conservation biology. Conserv. Biol. 13, 805–814 (1999).

    Article  Google Scholar 

  36. Duelli, P. & Obrist, M.K. Biodiversity indicators: the choice of values and measures. Agric. Ecosyst. Environ. 98, 87–98 (2003).

    Article  Google Scholar 

  37. Bates, S.L., Zhao, J.-Z., Roush, R.T. & Shelton, A.M. Insect resistance management in GM crops: past, present and future. Nat. Biotechnol. 23, 57–62 (2005).

    Article  CAS  Google Scholar 

  38. Candolfi, M.P. et al. (eds.). Guidelines to evaluate side-effects of plant protection products to non-target arthropods (IOBC/WPRS, Gent, Belgium, 2000).

  39. US Environmental Protection Agency (USEPA). Harmonized test guidelines, series 885 microbial pesticide test guidelines OPPTS (Office of Prevention, Pesticides and Toxic Substances Washington, DC, USA, February 1996 <http://www.epa.gov/opptsfrs/publications/ OPPTS_Harmonized/885_Microbial_Pesticide_Test_Guidelines/ index.html>

  40. Raybould, A. et al. Non-target organisms risk assessment of MIR604 maize expressing mCry3A for control of corn rootworms. J. Appl. Entomol. 131, 391–399 (2007).

    Article  CAS  Google Scholar 

  41. Jaffe, G. Regulatory slowdown on GM crop decisions. Nat. Biotechnol. 24, 748–749 (2006).

    Article  CAS  Google Scholar 

  42. US Environmental Protection Agency (USEPA). Biopesticide registration action document. Bacillus thuringiensis (Bt) plant-incorporated protectants. 15 October 2001. <http://www.epa.gov/oppbppd1/biopesticides/pips/bt_brad.htm>

  43. US Environmental Protection Agency (USEPA). Pesticide fact sheet for Bacillus thuringiensis ssp. kurstaki Cry1(A)b delta-endotoxin and the genetic material necessary for the production (plasmid vector pCIB4431) in corn. EPA publication no. EPA 731-F-95–004 (Environmental Protection Agency, Washington, DC, USA, 1995).

  44. Losey, J.E., Rayor, L.S. & Carter, M.E. Transgenic pollen harms monarch larvae. Nature 399, 214 (1999).

    Article  CAS  Google Scholar 

  45. Hellmich, R.L. et al. Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proc. Natl. Acad. Sci. USA 98, 11925–11930 (2001).

    Article  CAS  Google Scholar 

  46. Dively, G.P. et al. Effects on Monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expresing corn during anthesis. Environ. Entomol. 33, 1116–1125 (2004).

    Article  CAS  Google Scholar 

  47. Prasifka, J.R., Hellmich, R.L., Dively, G.P. & Lewis, L.C. Assessing the effects of pest management on nontarget arthropods: The influence of plot size and isolation. Environ. Entomol. 34, 1181–1192 (2005).

    Article  Google Scholar 

  48. Sears, M. et al. Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc. Natl. Acad. Sci. USA 98, 11937–11942 (2001).

    Article  CAS  Google Scholar 

  49. Wolt, J.D., Peterson, R.K.D., Bystrak, P. & Meade, T. A screening level approach for nontarget insect risk assessment: transgenic Bt corn pollen and the monarch butterfly (Lepidoptera: Danaidae). Environ. Entomol. 32, 237–246 (2003).

    Article  CAS  Google Scholar 

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Author information

Author notes

  1. Marco P Candolfi

    Present address: Present address: BASF SE, APD/EE, LI 425, 67117 Limburgerhof, Germany.,

Authors and Affiliations

  1. Agroscope Reckenholz-Tänikon Research Station ART, Reckenholzstr. 191, Zurich, 8046, Switzerland

    Jörg Romeis & Franz Bigler

  2. Federal Office of Consumer Protection and Food Safety (BVL), Mauerstrasse 39-42, Berlin, 10117, Germany

    Detlef Bartsch

  3. RCC Laboratories India Private Ltd., Genome Valley, Turkapally, Shameerpet, Ranga Reddy District, Hyderabad, 500078, India

    Marco P Candolfi

  4. National Institute for Public Health and the Environment, Expertise Centre for Substances, PO Box 1, Bilthoven, 3720 BA, The Netherlands

    Marco M C Gielkens

  5. Department of Biology and Environmental Science, University of Sussex, Falmer, BN1 9QG, Brighton, UK

    Susan E Hartley

  6. Corn Insects and Crop Genetics Research Unit and Department of Entomology, USDA–ARS, Iowa State University, 110 Genetics Laboratory c/o Insectary, Ames, 50011, Iowa, USA

    Richard L Hellmich

  7. Regulatory Sciences, Monsanto Company, 800 N. Lindbergh Blvd., St. Louis, 63167, Missouri, USA

    Joseph E Huesing

  8. Integrated Plant Protection Center and Department of Environmental and Molecular Toxicology, Oregon State University, Cordley Hall, Corvallis, 2040, 97331-2907, Oregon, USA

    Paul C Jepson

  9. Regulatory Sciences, DuPont Crop Genetics, 7250 NW 62nd Ave., PO Box 552, Johnston, 50131-0052, Iowa, USA

    Raymond Layton

  10. Department of Biology, Program for Biosafety Systems, Calvin College, 1726 Knollcrest Circle, S.E., Grand Rapids, 49546-4403, Michigan, USA

    Hector Quemada

  11. Syngenta, Jealott's Hill International Research Centre, Bracknell, RG42 6EY, Berkshire, UK

    Alan Raybould

  12. USDA–APHIS Biotechnology Regulatory Services, 4700 River Rd., Unit 146, Riverdale, 20737, Maryland, USA

    Robyn I Rose

  13. Julius Kuehn Institute, Federal Research Centre for Cultivated Plants (JKI), Institute for Biosafety of Genetically Modified Plants, Messeweg 11/12, Braunschweig, 38104, Germany

    Joachim Schiemann

  14. Department of Environmental Biology, University of Guelph, Guelph, N1G 2W1, Ontario, Canada

    Mark K Sears

  15. Department of Entomology, Cornell University/NYSAES, 630 W. North Street, Geneva, 14456, New York, USA

    Anthony M Shelton

  16. Environmental Consultant, The Green, Willingham, CB4 5JA, Cambridge, UK

    Jeremy Sweet

  17. Biopesticides and Pollution Prevention Division, USEPA 7511P, 1200 Pennsylvania Ave. NW, Washington, 20460, DC, USA

    Zigfridas Vaituzis

  18. Biosafety Institute for Genetically Modified Agricultural Products and Department of Agronomy, Iowa State University, 164 Seed Science Center, Ames, 50011, Iowa, USA

    Jeffrey D Wolt

Authors
  1. Jörg Romeis
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Corresponding author

Correspondence to Jörg Romeis.

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Competing interests

J.E.H., R.L. and A.R. are employed by companies that develop and sell GM plants. M.P.C. had been employed by a company that conducts regulatory risk assessment studies and works now for a plant protection company.

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Romeis, J., Bartsch, D., Bigler, F. et al. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26, 203–208 (2008). https://doi.org/10.1038/nbt1381

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