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Bt-maize event MON 88017 expressing Cry3Bb1 does not cause harm to non-target organisms

Abstract

This review paper explores whether the cultivation of the genetically modified Bt-maize transformation event MON 88017, expressing the insecticidal Cry3Bb1 protein against corn rootworms (Coleoptera: Chrysomelidae), causes adverse effects to non-target organisms (NTOs) and the ecological and anthropocentric functions they provide. Available data do not reveal adverse effects of Cry3Bb1 on various NTOs that are representative of potentially exposed taxonomic and functional groups, confirming that the insecticidal activity of the Cry3Bb1 protein is limited to species belonging to the coleopteran family of Chrysomelidae. The potential risk to non-target chrysomelid larvae ingesting maize MON 88017 pollen deposited on host plants is minimal, as their abundance in maize fields and the likelihood of encountering harmful amounts of pollen in and around maize MON 88017 fields are low. Non-target adult chrysomelids, which may occasionally feed on maize MON 88017 plants, are not expected to be affected due to the low activity of the Cry3Bb1 protein on adults. Impacts on NTOs caused by potential unintended changes in maize MON 88017 are not expected to occur, as no differences in composition, phenotypic characteristics and plant-NTO interactions were observed between maize MON 88017 and its near-isogenic line.

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References

  1. Ahmad A, Wilde GE, Zhu KY (2005) Detectability of coleopteran-specific Cry3Bb1 protein in soil and its effect on nontarget surface and below-ground arthropods. Environ Entomol 34:385–394

    CAS  Article  Google Scholar 

  2. Ahmad A, Wilde GE, Whitworth RJ, Zolnerowich G (2006a) Effect of corn hybrids expressing the coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators. J Econ Entomol 99:1085–1095

    PubMed  CAS  Article  Google Scholar 

  3. Ahmad A, Wilde GE, Zhu KY (2006b) Evaluation of effects of coleopteran-specific Cry3Bb1 protein on earthworms exposed to soil containing corn roots or biomass. Environ Entomol 35:976–985

    Article  Google Scholar 

  4. Albajes R, Lumbierres B, Madeira F, Pons X (2012) Field trials to assess risks to transgenic crops for non-target arthropods: power analysis and surrogate arthropods in Spain. IOBC/wprs Bull 73:1–7

    Google Scholar 

  5. Al-Deeb MA, Wilde GE (2003) Effect of Bt corn expressing the Cry3Bb1 toxin for corn rootworm control on aboveground nontarget arthropods. Environ Entomol 32:1164–1170

    Article  Google Scholar 

  6. Al-Deeb MA, Wilde GE, Blair JM, Todd TC (2003) Effect of Bt corn for corn rootworm control on nontarget soil microarthropods and nematodes. Environ Entomol 32:859–865

    Article  Google Scholar 

  7. Álvarez-Alfageme F, Bigler F, Romeis J (2011) Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res 20:476–479

    Article  CAS  Google Scholar 

  8. Arpaia S (1996) Ecological impact of Bt-transgenic plants: 1. Assessing possible effects of CryIIIB toxin on honey bee (Apis mellifera L.) colonies. J Genet Breeding 50:315–319

    CAS  Google Scholar 

  9. Astwood JD, Hileman RE, McKee MJ, Rydel TJ, Seale JW, English L (2001) Safety assessment of Cry3Bb1 variants in corn rootworm protected corn. Unpublished study performed by Monsanto Company [as reviewed in US EPA 2010]

  10. BAC (2010) Evaluation of the environmental risk assessment of application EFSA/GMO/CZ/2008/54 (maize line MON 88017) submitted under Regulation (EC) No. 1829/2003. Final evaluation report of the Belgian Biosafety Advisory Council (Reference BAC_2010_0928), http://www.bio-council.be/docs/BAC_2010_0928_CONSOLIDE.pdf

  11. Bhakta NS, Hartmann AJ, Jennings JC (2003) Cry3Bb1 and CP4 EPSPS protein levels in corn tissues collected from MON88017 corn produced in U.S. field trials conducted in 2002. Unpublished study performed by Monsanto Company [as reviewed in EFSA 2009, 2011]

  12. Bhatti MA, Duan JJ, Head GP, Jiang C, McKee MJ, Nickson TE, Pilcher CL, Pilcher CP (2005a) Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on ground-dwelling invertebrates. Environ Entomol 34:1325–1335

    Article  Google Scholar 

  13. Bhatti MA, Duan JJ, Head GP, Jiang C, McKee MJ, Nickson TE, Pilcher CL, Pilcher CP (2005b) Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on foliage-dwelling arthropods. Environ Entomol 34:1336–1345

    Article  Google Scholar 

  14. Bitzer R, Rice M, Pilcher C, Pilcher C, Lam WKF (2005) Biodiversity and community structure of epedaphic and euedaphic springtails (Collembola) in transgenic rootworm Bt corn. Environ Entomol 34:1346–1375

    Article  Google Scholar 

  15. Boriani M, Agosti M, Kiss J, Edwards CR (2006) Sustainable management of the western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), in infested areas: experiences in Italy, Hungary and the USA. EPPO Bull 36:531–537

    Article  Google Scholar 

  16. Bryan RL, Porch JR, Krueger HO (2001) Dietary effects of transgenic Bacillus thuringiensis (Bt) corn pollen expressing a variant of Cry3Bb1 protein on the ladybird beetle, Hippodamia convergens. Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2002b]

  17. Candolfi M, Bigler F, Campbell P, Heimbach U, Schmuck R, Angeli G, Bakker F, Brown K, Carli G, Dinter A, Forti D, Forster R, Gathmann A, Hassan S, Mead-Briggs M, Melandri M, Neumann P, Pasqualini E, Powell W, Reboulet JN, Romijn K, Sechser B, Thieme T, Ufer A, Vergnet C, Vogt H (2000) Principles for regulatory testing and interpretation of semi-field and field studies with non-target arthropods. J Pest Sci 73:141–147

    Google Scholar 

  18. Carrasco LR, Harwood TD, Toepfer S, MacLeod A, Levay N, Kiss J, Baker RHA, Mumford JD, Knight JD (2010) Dispersal kernels of the invasive alien western corn rootworm and the effectiveness of buffer zones in eradication programmes in Europe. Ann Appl Biol 156:63–77

    Article  Google Scholar 

  19. Carstens K, Anderson J, Bachman B, De Schrijver A, Dively G, Federici B, Hamer M, Gielkins M, Jensen P, Lamp W, Rauschen S, Ridley G, Romeis J, Waggoner A (2011) Genetically modified crops and aquatic ecosystems: considerations for environmental risk assessment and non-target organism testing. Transgenic Res. doi:10.1007/s11248-011-9569-8

    Google Scholar 

  20. Carter ME, Villani MG, Allee LL, Losey JE (2004) Absence of nontarget effects of two Bacillus thuringiensis coleopteran active delta-endotoxin on the bulb mite, Rhizoglypus robini (Claparède) (Acari, Acaridae). J Appl Entomol 128:56–63

    CAS  Article  Google Scholar 

  21. CERA (2012) GM crop database. ILSI Research Foundation, Washington D.C., http://cera-gmc.org/index.php?action=gm_crop_database

  22. CFIA (2006) DD2006-57: determination of the safety of Monsanto Canada Inc.’s glyphosate-tolerant, corn-rootworm-protected corn (Zea mays L) event MON88017, http://www.inspection.gc.ca/plants/plants-with-novel-traits/approved-under-review/decision-documents/dd2006-57/eng/1311618259264/1311618485252

  23. Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    PubMed  CAS  Article  Google Scholar 

  24. COGEM (2011) Additional advice on cultivation of maize MON88017 (CGM/111209-01), http://www.cogem.net/index.cfm/en/publications/publicatie/additional-advice-on-cultivation-of-maize-mon88017

  25. Cummins KW, Wilzbach MA, Gates DM, Perry JB, Taliaferro WB (1989) Shredders and riparian vegetation. Bioscience 39:24–30

    Article  Google Scholar 

  26. Curry JP, Schmidt O (2006) The feeding ecology of earthworms: a review. Pedobiologia 50:463–477

    CAS  Article  Google Scholar 

  27. Devare MH, Jones CM, Thies JE (2004) Effect of Cry3Bb transgenic corn and tefluthrin on the soil microbial community: biomass, activity and diversity. J Environ Qual 33:837–843

    PubMed  CAS  Article  Google Scholar 

  28. Devare MH, Londoño RLM, Thies JE (2007) Neither transgenic Bt maize (MON863) nor tefluthrin insecticide affect soil microbial activity or biomass: a 3-year field analysis. Soil Biol Biochem 39:2038–2047

    CAS  Article  Google Scholar 

  29. Dewar A (2010) Endangered European coleoptera: a report on the vulnerability of species listed under Council Directive 92/43/EEC to the introduction of GM crops. Unpublished study commissioned by Monsanto Company [as referred to in EFSA 2011]

  30. Didden W (1993) Ecology of terrestrial enchytraeidae. Pedobiologia 37:2–29

    Google Scholar 

  31. Donovan WP, Rupar MJ, Slaney AC, Malvar T, Gawron-Burke MC, Johnson TB (1992) Characterization of two genes encoding Bacillus thuringiensis insecticidal crystal proteins toxic to Coleoptera species. Appl Environ Microbiol 58:3921–3927

    PubMed  CAS  Google Scholar 

  32. Drottar K, Krueger H (1999) Bacillus thuringiensis protein 11098 in corn pollen: a 48-hour static-renewal acute toxicity test with the cladoceran (Daphnia magna). Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2010]

  33. Duan JJ, Head GP, McKee M, Nickson TE (2001a) Dietary effects of transgenic Bacillus thuringiensis (Bt) corn pollen expressing a variant of the Cry3Bb1 protein on adults of the ladybird beetle, Coleomegilla maculata. Unpublished study performed by Monsanto Company [as reviewed in US EPA 2002b]

  34. Duan JJ, McKee M, Nickson TE (2001b) Dietary effects of transgenic Bacillus thuringiensis (Bt) corn pollen expressing a variant of Cry3Bb1 protein on larvae of the ladybird beetle, Coleomegilla maculata. Unpublished study performed by Monsanto Company [as reviewed in US EPA 2002a]

  35. Duan JJ, Head GP, McKee MJ, Nickson TE, Martin JW, Sayegh FS (2002) Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bb1 protein on a non-target ladybird beetle, Coleomegilla maculata. Entomol Exp Appl 104:271–280

    CAS  Article  Google Scholar 

  36. Duan JJ, Paradise M, Jiang C (2003) Evaluation of the functional equivalence of two Cry3Bb1 protein variants against susceptible coleopteran species. Unpublished study performed by Monsanto Company [as reviewed in US EPA 2002c]

  37. Duan JJ, Jiang C, Head GP, Bhatti MA, Ward DP, Levine SL, Nickson TE, Nemeth MA (2006a) Statistical power analysis of a 2-year field study and design of experiments to evaluate non-target effects of genetically modified Bacillus thuringiensis corn. Ecol Entomol 31:521–531

    Article  Google Scholar 

  38. Duan JJ, Paradise MS, Lundgren JG, Bookout JT, Jiang C, Wiedenmann RN (2006b) Assessing nontarget impacts of Bt corn resistant to corn rootworms: tier-1 testing with larvae of Poecilus chalcites (Coleoptera: Carabidae). Environ Entomol 35:135–142

    CAS  Article  Google Scholar 

  39. Duan JJ, Huesing JE, Teixeira D (2007) Development of tier-I toxicity assays for Orius insidiosus (Heteroptera: Anthocoridae) for assessing the risk of plant-incorporated protectants to nontarget heteropterans. Environ Entomol 36:982–988

    PubMed  CAS  Article  Google Scholar 

  40. Duan JJ, Marvier M, Huesing J, Dively G, Huang ZY (2008a) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE 3:e1415

    PubMed  Article  Google Scholar 

  41. Duan JJ, Teixeira D, Huesing JE, Jiang CJ (2008b) Assessing the risk to nontarget organisms from Bt corn resistant to corn rootworms (Coleoptera: Chrysomelidae): Tier-I testing with Orius insidiosus (Heteroptera: Anthocoridae). Environ Entomol 37:838–844

    PubMed  CAS  Article  Google Scholar 

  42. Duan JJ, Lundgren JG, Naranjo S, Marvier M (2010) Extrapolating non-target risk of Bt crops from laboratory to field. Biol Lett 6:74–77

    PubMed  Article  Google Scholar 

  43. Dudin YA, Tonnu B, Albee LD, Lirette RP (2001) Amended report for MSL16559: B.t. Cry3Bb1.11098 and NPTII protein levels in samples tissue collected from corn event MON863 grown in 1999 field trials. Unpublished study performed by Monsanto Company [as reviewed in EFSA 2009, 2011]

  44. EFSA (2007) EFSA review of statistical analyses conducted for the assessment of the MON 863 90-day rat feeding study, http://www.efsa.europa.eu/en/efsajournal/doc/19r.pdf

  45. EFSA (2009) Scientific opinion of the panel on genetically modified organisms on an application (Reference EFSA-GMO-CZ-2005-27) for the placing on the market of the insect-resistant and herbicide-tolerant genetically modified maize MON 88017, for food and feed uses, import and processing under Regulation (EC) No 1829/2003 from Monsanto. EFSA J 1075:1–28, http://www.efsa.europa.eu/en/scdocs/doc/1075.pdf

  46. EFSA (2010) Guidance on the environmental risk assessment of genetically modified plants. EFSA J 1879:1-111, http://www.efsa.europa.eu/en/efsajournal/doc/1879.pdf

    Google Scholar 

  47. EFSA (2011) Scientific Opinion on application (EFSA-GMO-CZ-2008-54) for placing on the market of genetically modified insect resistant and herbicide tolerant maize MON 88017 for cultivation under Regulation (EC) No 1829/2003 from Monsanto. EFSA J 2428:1–152, http://www.efsa.europa.eu/en/efsajournal/doc/2428.pdf

  48. FCEC (2009) Analysis of the economic, social and environmental impacts of options for the long-term EU strategy against Diabrotica virgifera virgifera (western corn rootworm), a regulated harmful organism of maize, http://ec.europa.eu/food/plant/organisms/emergency/final_report_Diabrotica_study.pdf

  49. Gallagher SP, Grimes J, Beavers JB (1999) Bacillus thuringiensis protein 11231 in corn grain: a dietary toxicity study with the northern bobwhite. Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2010]

  50. García M, Ortego F, Castañera P, Farinós GP (2011) Assessment of prey-mediated effects of the coleopteran-specific toxin Cry3Bb1 on the generalist predator Atheta coriaria (Coleoptera: Staphylinidae). Bull Entomol Res. doi:10.1017/S0007485311000666

    PubMed  Google Scholar 

  51. Garcia-Alonso M, Jacobs E, Raybould A, Nickson TE, Sowig P, Willekens H, Van der Kouwe P, Layton R, Amijee F, Fuentes AM, Tencalla F (2006) A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environ Biosafety Res 5:57–65

    PubMed  Article  Google Scholar 

  52. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6:e22629

    PubMed  CAS  Article  Google Scholar 

  53. Gathmann A, Wirooks L, Hothorn LA, Bartsch D, Schuphan I (2006) Impact of Bt maize pollen (MON810) on lepidopteran larvae living on accompanying weeds. Mol Ecol 15:2677–2685

    PubMed  CAS  Article  Google Scholar 

  54. Hammond BG, Dudek R, Lemen JK, Nemeth MA (2006) Results of a 90-day safety assurance study with rats fed grain from corn borer-protected corn. Food Chem Toxicol 44:1092–1099

    PubMed  CAS  Article  Google Scholar 

  55. Head GP, Pleau M, Sivausupramanian S, Vaughn T (2001) Insecticidal spectrum of activity for Cry3Bb protein in vitro. Unpublished study performed by Monsanto Company [as reviewed in US EPA 2002c]

  56. Hendriksma HP, Härtel S, Steffan-Dewenter I (2011) Testing pollen of single and stacked insect-resistant Bt-maize on in vitro reared honey bee larvae. PLoS ONE 6:e28174

    PubMed  CAS  Article  Google Scholar 

  57. Hendriksma HP, Härtel S, Babendreier D, von der Ohe W, Steffan-Dewenter I (2012) Effects of multiple Bt proteins and GNA lectin on in vitro-reared honey bee larvae. Apidologie. doi:10.1007/s13592-012-0123-3

    Google Scholar 

  58. Hilbeck A, McMillan J, Meier M, Humbel A, Schlaepfer-Miller J, Trtikova M (2012) A controversy re-visited: Is the coccinellid Adalia bipunctata adversely affected by Bt toxins? Environ Sci Europe 24:10

    CAS  Article  Google Scholar 

  59. Höfte H, Whiteley HR (1989) Insecticidal crystal proteins of Bacillus tburingiensis. Microbiol Rev 53:242–255

    PubMed  Google Scholar 

  60. Hönemann L, Nentwig W (2009) Are survival and reproduction of Enchytraeus albidus (Annelida: Enchytraeidae) at risk by feeding on Bt-maize litter? Eur J Soil Biol 45:351–355

    Article  CAS  Google Scholar 

  61. Hönemann L, Nentwig W (2010) Does feeding on Bt-maize affect the slug Arion vulgaris (Mollusca: Arionidae)? Biocontrol Sci Technol 20:13–18

    Article  Google Scholar 

  62. Hönemann L, Zurbrügg C, Nentwig W (2008) Effects of Bt-corn decomposition on the composition of the soil meso- and macrofauna. Appl Soil Ecol 40:203–209

    Article  Google Scholar 

  63. Höss S, Nguyen HT, Menzel R, Pagel-Wieder S, Miethling-Graf R, Tebbe CC, Jehle JA, Traunspurger W (2011) Assessing the risk posed to free-living soil nematodes by genetically modified maize expressing the insecticidal Cry3Bb1 protein. Sci Total Environ 409:2674–2684

    PubMed  Article  CAS  Google Scholar 

  64. Huber J, Langenbruch GA (2008) Freisetzungsbegleitende Untersuchungen zur Aktivität von Bt-Toxinen bei Ziel- und Nicht-Ziel-Organismen, sowie im Boden–Teilprojekt: untersuchungen zu Nebenwirkungen von Cry3Bb-Mais auf epigäische Nicht-Ziel-Organimen. TIB/UB Hannover 0313279D:59

    Google Scholar 

  65. Icoz I, Stotzky G (2007) Cry3Bb1 protein from Bacillus thuringiensis in root exudates and biomass of transgenic corn does not persist in soil. Transgenic Res 17:609–620

    PubMed  Article  CAS  Google Scholar 

  66. Icoz I, Saxena D, Andow D, Zwahlen C, Stotzky G (2008) Microbial populations and enzyme activities in soil in situ under transgenic corn expressing Cry proteins from Bacillus thuringiensis. J Environ Qual 37:647–662

    PubMed  CAS  Article  Google Scholar 

  67. Isenhour DJ, Yeargan KV (1981) Effect of temperature on the development of Orius insidiosus, with notes on laboratory rearing. Ann Entomol Soc Am 74:114–116

    Google Scholar 

  68. Jensen PD, Dively GP, Swan CM, Lamp WO (2010) Exposure and nontarget effects of transgenic Bt corn debris in streams. Environ Entomol 39:707–714

    PubMed  CAS  Article  Google Scholar 

  69. Kiman ZB, Yeargan KV (1985) Development and reproduction of the predator Orius insidiosus (Hemiptera: Anthocoridae) reared on diets of selected plant material and arthropod prey. Ann Entomol Soc Am 78:464–467

    Google Scholar 

  70. Kiss J, Szentkirályi F, Szénási A, Tóth F, Szekeres D, Kádár F, Árpás K, Edwards CR (2004) Effect of transgenic Bt-corn on biodiversity of non-target insects in corn fields. Report on contract number QLK3-CT-2000-00547 (project “Bt-BioNoTa”) within the 5th EU framework programme. Report was provided by József Kiss

  71. Kiss J, Szentkirályi F, Tóth F, Szénási A, Kádár F, Arpás K, Szekeres D, Edwards CR (2002) Bt corn: impact on non-targets and adjusting to local IPM systems. In: Lelley T, Balázs E, Tepfer M (eds) Ecological impact of GMO dissemination in agro-ecosystems. Facultas, Wien, pp 157–172

    Google Scholar 

  72. Kiss J, Komáromi J, Bayar JK, Edwards CR, Hatala-Zsellér I (2005) Western corn rootworm (Diabrotica virgifera virgifera LeConte) and the crop rotation systems in Europe. In: Vidal S, Kuhlmann U, Edwards CR (eds) Western corn rootworm: ecology and management. CABI Publishing, Wallingford, pp 189–220

    Chapter  Google Scholar 

  73. Knecht S, Nentwig W (2010) Effect of Bt maize on the reproduction and development of saprophagous Diptera over multiple generations. Basic Appl Ecol 11:346–353

    CAS  Article  Google Scholar 

  74. Knecht S, Romeis J, Malone LA, Candolfi MP, Garcia-Alonso M, Habustova O, Huesing JE, Kiss J, Nentwig W, Pons X, Rauschen S, Szénási A, Bigler F (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

    Google Scholar 

  75. Lawhorn CN, Neher DA, Dively GP (2009) Impact of coleopteran targeting toxin (Cry3Bb1) of Bt corn on microbially mediated decomposition. Appl Soil Ecol 41:364–368

    Article  Google Scholar 

  76. Lehman RM, Osborne SL, Rosentrater KA (2008a) No differences in decomposition rates observed between Bacillus thuringiensis and non-Bacillus thuringiensis corn residue incubated soil in the field. Agron J 100:163–168

    Article  Google Scholar 

  77. Lehman RM, Osborne SL, Rosentrater KA (2008b) No evidence that Bacillus thuringiensis genes and their products influence the susceptibility of corn residue to decomposition. Agron J 100:1687–1693

    Article  Google Scholar 

  78. Lehman RM, Osborne SL, Prischmann-Voldseth DA, Rosentrater KA (2010) Insect-damaged corn stalks decompose at rates similar to Bt-protected, non-damaged corn stalks. Plant Soil 333:481–490

    CAS  Article  Google Scholar 

  79. Li Y, Romeis J (2010) Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol Control 52:337–344

    Article  CAS  Google Scholar 

  80. Li Y, Meissle M, Romeis J (2008) Consumption of Bt maize pollen expressing Cry1Ab or Cry3Bb1 does not harm adult green lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae). PLoS ONE 3:e2909

    PubMed  Article  CAS  Google Scholar 

  81. Li Y, Meissle M, Romeis J (2010) Use of maize pollen by adult Chrysoperla carnea (Neuroptera: Chrysopidae) and fate of Cry proteins in Bt-transgenic varieties. J Insect Physiol 56:157–164

    PubMed  CAS  Article  Google Scholar 

  82. Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer Science + Business Media BV

  83. Lundgren JG, Wiedenmann RN (2002) Coleopteran-specific Cry3Bb toxin from transgenic corn pollen does not affect the fitness of a nontarget species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae). Environ Entomol 31:1213–1218

    CAS  Article  Google Scholar 

  84. Lundgren JG, Wiedenmann RN (2005) Tritrophic interactions among Bt (Cry3Bb1) corn, aphid prey, and the predator Coleomegilla maculata (Coleoptera: Coccinellidae). Environ Entomol 34:1621–1625

    Article  Google Scholar 

  85. Maggi VL (1999a) Evaluation of the dietary effects of purified Bacillus thuringiensis protein 11231 on honey bee larvae. Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2002a]

  86. Maggi VL (1999b) Evaluation of the dietary effect(s) of purified Bacillus thuringiensis protein 11231 on adult honey bees (Apis mellifera L.). Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2002a]

  87. Maggi VL (2002) Evaluation of dietary effect(s) of a Cry3Bb1 protein variant on honey bee larvae (Apis mellifera L). Unpublished study commissioned by Monsanto Company [as referred to in Duan et al. 2008a]

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

    PubMed  CAS  Article  Google Scholar 

  89. Mattila HR, Sears MK, Duan JJ (2005) Response of Danaus plexippus to pollen of two new Bt corn events via laboratory bioassay. Entomol Exp Appl 116:31–41

    Article  Google Scholar 

  90. McCann MC, Trujillo WA, Riordan SG, Sorbet R, Bogdanova NN, Sidhu RS (2007) Comparison of the forage and grain composition from insect-protected and glyphosate-tolerant MON88017 corn to conventional corn (Zea mays L.). J Agri Food Chem 55:4034–4042

    CAS  Article  Google Scholar 

  91. McManus BL, Fuller BW, Boetel MA, French BW, Ellsbury MM, Head GP (2005) Abundance of Coleomegilla maculata (Coleoptera: Coccinellidae) in corn-rootworm-resistant Cry3Bb1 maize. J Econ Entomol 98:1992–1998

    PubMed  CAS  Article  Google Scholar 

  92. Meinke LJ, Sappington TW, Onstad DW, Guillemaud T, Miller NJ, Komáromi J, Levay N, Furlan L, Kiss J, Toth F (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agri Forest Entomol 11:29–46

    Article  Google Scholar 

  93. Meissle M, Romeis J (2008) Compatibility of biological control with Bt maize expressing Cry3Bb1 in controlling corn rootworms. In: Mason PG, Gillespie DR, Vincent C (eds) Proceedings of the third symposium on biological control of arthropods. Christchurch, New Zealand, pp 146–160

    Google Scholar 

  94. Meissle M, Romeis J (2009a) Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 131:308–319

    CAS  Article  Google Scholar 

  95. Meissle M, Romeis J (2009b) The web-building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotechnol J 7:645–656

    CAS  Article  Google Scholar 

  96. Meissle M, Pilz C, Romeis J (2009) Susceptibility of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to the entomopathogenic fungus Metarhizium anisopliae when feeding on Bacillus thuringiensis Cry3Bb1-expressing maize. Appl Environ Microbiol 75:3937–3943

    PubMed  CAS  Article  Google Scholar 

  97. Meissle M, Hellmich RL, Romeis J (2011a) Impact of Cry3Bb1-expressing Bt maize on adults of the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Pest Manag Sci 67:807–814

    PubMed  CAS  Article  Google Scholar 

  98. Meissle M, Romeis J, Bigler F (2011b) Bt maize and integrated pest management: a European perspective. Pest Manag Sci 67:1049–1058

    CAS  Article  Google Scholar 

  99. Meissle M, Knecht S, Waldburger M, Romeis J (2012) Sensitivity of the cereal leaf beetle Oulema melanopus (Coleoptera: Chrysomelidae) to Bt maize-expressed Cry3Bb1 and Cry1Ab. Arthropod Plant Int. doi:10.1007/s11829-011-9178-8

    Google Scholar 

  100. Metcalf ER (1986) Foreword. In: Krysan JL, Miller TA (eds) Methods for the study of pest Diabrotica. Springer, New York

    Google Scholar 

  101. Miethling-Graff R, Dockhorn S, Tebbe CC (2010) Release of the recombinant Cry3Bb1 protein of Bt maize MON88017 into field soil and detection of effects on the diversity of rhizosphere bacteria. Eur J Soil Biol 46:41–48

    CAS  Article  Google Scholar 

  102. Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992

    PubMed  CAS  Article  Google Scholar 

  103. Moonen AC, Bàrberi P (2008) Functional biodiversity: an agroecosystem approach. Agri Ecosyst Environ 127:7–21

    Article  Google Scholar 

  104. Mullin CA, Saunders MC, Leslie TW, Biddinger DJ, Fleischer SJ (2005) Toxic and behavioural effects to Carabidae of seed treatments used on Cry3Bb1- and Cry1Ab/c-protected corn. Environ Entomol 34:1626–1636

    CAS  Article  Google Scholar 

  105. Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev: Perspect Agric Vet Sci Nut Nat Resour 4:No 011

  106. Nguyen HT, Jehle JA (2009a) Expression of Cry3Bb1 in transgenic corn MON88017. J Agri Food Chem 57:9990–9996

    CAS  Article  Google Scholar 

  107. Nguyen HT, Jehle JA (2009b) Stability of Cry1Ab protein during long-term storage for standardization of insect bioassays. Environ Biosafety Res 8:113–119

    PubMed  CAS  Article  Google Scholar 

  108. Niemeyer KE, Silvanovich A (2007) Assessment of the Cry3Bb1 and CP4 EPSPS protein levels in tissues of corn MON 88017 produced in 2006 European trial fields. Unpublished study performed by Monsanto Company [as reviewed in EFSA 2009, 2011]

  109. Nowatzki TM, Zhou X, Meinke LJ, Vaughn T, Siegfried BD (2006) Effect of Bacillus thuringiensis Cry3Bb1 protein on the feeding behaviour and longevity of adult western corn rootworms (Coleoptera: Chrysomelidae). J Econ Entomol 99:927–930

    PubMed  CAS  Article  Google Scholar 

  110. Palmer SJ, Krueger HO (1999a) Bacillus thuringiensis protein 11231: a dietary toxicity study with the ladybird beetle (Hippodamia convergens). Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2000]

  111. Palmer SJ, Krueger HO (1999b) Bacillus thuringiensis protein 11231: a dietary toxicity study with green lacewing larvae (Chrysoperla carnea). Unpublished study commissioned by Monsanto Company [as reviewed in US EPA, 2002a]

  112. Palmer SJ, Krueger HO (1999c) Bacillus thuringiensis protein 11231: a dietary toxicity study with the parasitic Hymenoptera (Nasonia vitripennis). Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2002a]

  113. Park Y, Abdullah MAF, Taylor MD, Rahman K, Adang MJ (2009) Enhancement of Bacillus thuringiensis Cry3Aa and Cry3Bb toxicities to coleopteran larvae by a toxin-binding fragment of an insect cadherin. Appl Environ Microbiol 75:3086–3092

    PubMed  CAS  Article  Google Scholar 

  114. Perry JN, ter Braak CJF, Dixon PM, Duan JJ, Hails RS, Huesken A, Lavielle A, Marvier M, Scardi M, Schmidt K, Tothmeresz B, Schaarschmidt F, van der Voet H (2009) Statistical aspects of environmental risk assessment of GM plants for effects on non-target organisms. Environ Biosafety Res 8:65–78

    PubMed  Article  Google Scholar 

  115. Pilcher CD, Obrycki JJ, Rice ME, Lewis LC (1997) Preimaginal development, survival, and field abundance of insect predators on transgenic Bacillus thuringiensis corn. Environ Entomol 26:446–454

    Google Scholar 

  116. Pleasants JM, Hellmich RL, Dively GP, Sears MK, Stanley-Horn DE, Mattila HR, Foster JE, Clark P, Jones GD (2001) Corn pollen deposition on milkweeds in and near cornfields. Proc Natl Acad Sci USA 98:11919–11924

    PubMed  CAS  Article  Google Scholar 

  117. Poerschmann J, Rauschen S, Langer U, Augustin J, Gorecki T (2009) Fatty acid patterns of genetically modified Cry3Bb1 expressing Bt-maize MON88017 and its near-isogenic line. J Agri Food Chem 57:127–132

    CAS  Article  Google Scholar 

  118. Priesnitz KU (2010) Potential impact of Diabrotica resistant Bt-maize expressing Cry3Bb1 on ground beetles (Coleoptera: Carabidae). PhD Thesis, RWTH Aachen, Germany

  119. Prihoda KR, Coats JR (2008a) Aquatic fate and effects of Bacillus thuringiensis Cry3Bb1 protein: toward risk assessment. Environ Toxicol Chem 27:793–798

    PubMed  CAS  Article  Google Scholar 

  120. Prihoda KR, Coats JR (2008b) Fate of Bacillus thuringiensis (Bt) Cry3Bb1 protein in a soil microcosm. Chemosphere 73:1102–1107

    PubMed  CAS  Article  Google Scholar 

  121. Rauschen S (2010) A case of “pseudo science”? A study claiming effects of the Cry1Ab protein on larvae of the two-spotted ladybird is reminiscent of the case of the green lacewing. Transgenic Res 19:13–16

    PubMed  CAS  Article  Google Scholar 

  122. Rauschen S, Schuphan I, Eber S (2008) Assessment of possible non-target impacts of the novel Bt-maize event MON88017 resistant against the western corn rootworm Diabrotica virgifera virgifera (LeConte). IOBC/wprs Bull 33:93–99

    Google Scholar 

  123. Rauschen S, Schultheis E, Pagel-Wieder S, Schuphan I, Eber S (2009) Impact of Bt-corn MON88017 in comparison to three conventional lines on Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae) field densities. Transgenic Res 18:203–214

    PubMed  CAS  Article  Google Scholar 

  124. Rauschen S, Schaarmschmidt F, Gathmann A (2010a) Occurrence and field densities of Coleoptera in the maize herb layer: implications for environmental risk assessment of genetically modified Bt-maize. Transgenic Res 19:727–744

    PubMed  CAS  Article  Google Scholar 

  125. Rauschen S, Schultheis E, Hunfeld H, Schaarschmidt F, Schuphan I, Eber S (2010b) Diabrotica-resistant Bt-maize DKc5143 event MON88017 has no impact on the field densities of the leafhopper Zyginidia scutellaris. Environ Biosafety Res 9:87–99

    PubMed  Article  Google Scholar 

  126. Raybould A, Tuttle A, Shore S, Stone T (2010) Environmental risk assessment for transgenic crops producing output trait enzymes. Transgenic Res 19:595–609

    PubMed  CAS  Article  Google Scholar 

  127. Richards KB (2011a) Evaluation of the potential for dietary effect(s) of pollen from corn product MON 88017 on honey bee larvae (Apis mellifera L.) development. Unpublished study commissioned by Monsanto Company [as reviewed in COGEM 2011 and EFSA 2011]

  128. Richards KB (2011b) Evaluation of the potential for dietary effect(s) of pollen from corn product MON 88017 on honey bee adults (Apis mellifera L.). Unpublished study commissioned by Monsanto Company [as reviewed in COGEM 2011 and EFSA 2011]

  129. Ricroch A, Bergé JB, Kuntz M (2010) Is the German suspension of MON810 maize cultivation scientifically justified? Transgenic Res 19:1–12

    PubMed  CAS  Article  Google Scholar 

  130. Romeis J, Meissle M (2011) Non-target risk assessment of Bt crops: Cry protein uptake by aphids. J Appl Entomol 135:1–6

    CAS  Article  Google Scholar 

  131. Romeis J, Álvarez-Alfageme F, Bigler F (2012) Putative effects of Cry1Ab to larvae of Adalia bipunctata – reply to Hilbeck et al. (2012). Environ Sci Europe 24 (in press)

  132. Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkens M, Hartley SE, Hellmich RL, Huesing JE, Jepson PC, Layton R, Quemada H, Raybould A, Rose RI, Schiemann J, Sears MK, Shelton AM, Sweet J, Vaituzis Z, Wolt JD (2008) Nontarget arthropod risk assessment of insect-resistant GM crops. Nat Biotechnol 26:203–208

    PubMed  CAS  Article  Google Scholar 

  133. Romeis J, Van Driesche RG, Barratt BIP, Bigler F (2009) Insect-resistant transgenic crops and biological control. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-restistant genetically modified crops within IPM programs. Springer Science + Business Media BV, pp 87–117

  134. Romeis J, Hellmich RL, Candolfi MP, Carstens K, De Schrijver A, Gatehouse AMR, Herman RA, Huesing JE, McLean MA, Raybould A, Shelton AM, Waggoner A (2011) Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Res 20:1–22

    PubMed  CAS  Article  Google Scholar 

  135. Rosca I, Cagan L (2012a) Research on the influence of genetically modified maize on the Coccinellidae fauna. IOBC/wprs Bull 73:83–88

    Google Scholar 

  136. Rosca I, Cagan L (2012b) Research on the influence of genetically modified maize on the Neuroptera fauna. IOBC/wprs Bull 73:89–94

    Google Scholar 

  137. Rose RI (2007) 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, http://www.epa.gov/pesticides/biopesticides/pips/non-target-arthropods.pdf

  138. Rosi-Marshall EJ, Tank JL, Royer TV, Whiles MR, Evans-White M, Chambers C, Griffiths NA, Pokelsek J, Stephen ML (2007) Toxins in transgenic crop by products may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104:16204–16208

    PubMed  CAS  Article  Google Scholar 

  139. Sanahuja G, Banakar R, Twyman RM, Capelle T, Christou P (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J 9:283–300

    PubMed  CAS  Article  Google Scholar 

  140. Sanvido O, Romeis J, Bigler F (2009) An approach for post-market monitoring of potential environmental effects of Bt-maize expressing Cry1Ab on natural enemies. J Appl Entomol 133:236–248

    Article  Google Scholar 

  141. Sanvido O, Romeis J, Gathmann A, Gielkens M, Raybould A, Bigler F (2012) Evaluating environmental risks of genetically modified crops: ecological harm criteria for regulatory decision-making. Environ Sci Pol 15:82–91

    Article  Google Scholar 

  142. Schmidt JEU, Braun CU, Whitehouse LP, Hilbeck A (2009) Effects of activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adalia bipunctata in laboratory ecotoxicity testing. Arch Environ Con Toxicol 56:221–228

    CAS  Article  Google Scholar 

  143. Sears M, Mattila H (2001) Determination of the toxicity of corn pollen expressing a Cry3Bb1 variant protein to first instar monarch butterfly larvae (Danaus plexippus) via laboratory bioassay. Unpublished study commissioned by Monsanto Company [as reviewed in US EPA, 2002a]

  144. Shirai Y (2006) Laboratory evaluation of effects of transgenic Bt corn pollen on two non-target herbivorous beetles, Epilachna vigintioctopunctata (Coccinellidae) and Galerucella vittaticollis (Chrysomelidae). Appl Entomol Zool 41:607–611

    CAS  Article  Google Scholar 

  145. Sindermann AB, Porch JR, Krueger HO (2002a) Evaluation of a Cry3Bb1 protein variant in an acute toxicity study with the earthworm in an artificial soil substrate. Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2010]

  146. Sindermann AB, Porch JR, Krueger HO (2002b) Evaluation of a Cry3Bb1 protein variant in a dietary toxicity study with parasitic Hymenoptera (Nasonia vitripennis). Unpublished study commissioned by Monsanto Company [as referred to in http://www.monsanto.com/products/Documents/safety-summaries/yieldgard_rw_pss.pdf]

  147. Sochova I, Hofman J, Holoubek I (2006) Using nematodes in soil ecotoxicology. Environ Int 32:374–383

    PubMed  CAS  Article  Google Scholar 

  148. Svobodová Z, Habuštova O, Hussein HM, Půža V, Sehnal F (2012a) Impact of genetically modified maize expressing Cry3Bb1 on non-target arthropods: first year results of a field study. IOBC/wprs Bull 73:107–120

    Google Scholar 

  149. Svobodová Z, Habuštova O, Sehnal F, Holec M, Hussein HM (2012b) Epigeic spiders are not affected by the genetically modified maize MON 88017. J Appl Entomol. doi:10.1111/j.1439-0418.2012.01727.x

  150. Symondson WOC, Cesarini S, Dodd PW, Harper GL, Bruford MW, Glen DM, Wiltshire CW, Harwood JD (2006) Biodiversity versus biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles. Bull Entomol Res 96:637–645

    PubMed  CAS  Article  Google Scholar 

  151. Tan J, Paradise MS, Levine SL, Bachman PM, Uffman JP, Jiang C, Carson DB (2011) Development and survival of Orius insidiosus (Say) nymphs on encapsulated bee pollen-based diet in a Tier-I toxicity assay. Environ Entomol 40:1613–1621

    PubMed  Article  Google Scholar 

  152. Tank JL, Rosi-Marshall EJ, Royer TV, Whiles MR, Griffiths NA, Frauendorf TC, Treering DJ (2010) Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape. Proc Natl Acad Sci USA 107:17645–17650

    PubMed  CAS  Article  Google Scholar 

  153. Teixeira D (1999) Assessment of chronic toxicity of corn tissue containing the Bacillus thuringiensis protein 11098 to Collembola (Folsomia candida). Unpublished study commissioned by Monsanto Company [as reviewed in US EPA 2002a]

  154. US EPA (2000) Review of ecological non-target lady beetle effects for Monsanto’s EUP request to allow testing and further development of their Bacillus thuringiensis Cry3Bb1 field corn (EPA Reg. No. 524-LRA; Barcode No. D262045; Case No. 066221; Submission No. S572997), http://www.epa.gov/scipoly/sap/meetings/2002/August/3-10-2000_lady_beetle_review_mon_863_corn.pdf

  155. US EPA (2002a) Review of ecological non-target insect studies for Bacillus thuringiensis Cry3Bb1 protein. EPA Reg. No. 524-LRA; Barcode No. D262045; Case No. 066221; Submission No. S572997. MRID Nos 449043-10, 449043-11, 449043-12, 449043-13, 449043-17, 455382-04, 455382-05, 455382-06, 455770-03, http://www.epa.gov/scipoly/sap/meetings/2002/August/5-20-2002_non-target_insect_review_mon_863_corn.pdf

  156. US EPA (2002b) Review of laboratory pollen feeding studies on two species of lady beetles (Coleomegilla maculata and Hippodamia convergens) in support of Monsanto’s request to register Bacillus thuringiensis (Bt) Cry3Bb1 protein (event MON 863) expressed in field corn pollen. EPA Reg.No: 524-LRA, DP Barcode No. 282664, PC Code No 006484, MRID Nos. 453613-01 and 453613-02, http://www.epa.gov/scipoly/sap/meetings/2002/August/7-11-2002_lady_beetle_review_mon_863_corn.pdf

  157. US EPA (2002c) Review of efficacy and insecticidal activity data for event MON863: corn rootworm protected corn (vector ZMIR13L); Permit No. 524-LEI; Chemical No 006484; DP Barcode No D275903, D280086; Case No 065182; MRID #453613-03, 455382-07, 455382-08, http://www.epa.gov/scipoly/sap/meetings/2002/August/6-25-2002_efficacy_and_insect_act_rev_mon_863_corn.pdf

  158. US EPA (2007) Biopesticide Registration Action Document: Bacillus thuringiensis Cry3Bb1 corn: environmental assessment, http://www.epa.gov/oppbppd1/biopesticides/ingredients/tech_docs/cry3bb1/2_c_cry3bb1_environl.pdf

  159. US EPA (2010) Biopesticides registration action document: Bacillus thuringiensis Cry3Bb1 protein and the genetic material necessary for its production (vector PV-ZMIR13L) in MON 863 corn (OECD Unique Identifier: MON-ØØ863-5) PC code: 006484 and Bacillus thuringiensis Cry3Bb1 protein and the genetic material necessary for its production (vector PV-ZMIR39) in MON 88017 corn (OECD Unique Identifier: MON-88Ø17-3) PC code: 006498, http://www.epa.gov/oppbppd1/biopesticides/pips/cry3bb1-brad.pdf

  160. van Rozen K, Ester A (2010) Chemical control of Diabrotica virgifera virgifera LeConte. J Appl Entomol 134:376–384

    Article  CAS  Google Scholar 

  161. Vaughn T, Cavato T, Brar G, Coombe T, DeGooyer T, Ford S, Groth M, Howe A, Johnson S, Kolacz K, Pilcher C, Purcell J, Romano C, English L, Pershing J (2005) A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci 45:931–938

    CAS  Article  Google Scholar 

  162. Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe – the ‘no control’. J Appl Entomol 134:385–394

    Article  Google Scholar 

  163. WHO (2009) Handbook: good laboratory practice (GLP): quality practices for regulated non-clinical research and development, http://apps.who.int/tdr/publications/training-guideline-publications/good-laboratory-practice-handbook/pdf/glp-handbook.pdf

  164. WIL-50283 (2005) A 90-day feeding study in rats with MON 88017 corn grain. Unpublished study commissioned by Monsanto Company [as reviewed in EFSA 2010]

  165. WIL-50284 (2005) A 90-day feeding study in rats with six different reference corn varieties. Unpublished study commissioned by Monsanto Company [as reviewed in EFSA 2010]

  166. Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crop effecs on functional guilds of non-target arthropods: a meta-analysis. PLoS ONE 3:e2118

    PubMed  Article  CAS  Google Scholar 

  167. Wolt JD, Keese P, Raybould A, Fitzpatrick JW, Burachik M, Gray A, Olin SS, Schiemann J, Sears M, Wu F (2010) Problem formulation in the environmental risk assessment for genetically modified plants. Transgenic Res 19:425–436

    PubMed  CAS  Article  Google Scholar 

  168. Xue K, Serohijos RC, Devare M, Thies JE (2011) Decomposition rates and residue-colonizing microbial communities of Bacillus thuringiensis insecticidal protein Cry3Bb-expressing (Bt) and non-Bt corn hybrids in the field. Appl Environ Microbiol 77:839–846

    PubMed  CAS  Article  Google Scholar 

  169. Zeilinger AR, Andow DA, Zwahlen C, Stotzky G (2010) Earthworm populations in a northern US cornbelt soil are not affected by long-term cultivation of Bt maize expressing Cry1Ab and Cry3Bb1 proteins. Soil Biol Biochem 42:1284–1292

    CAS  Article  Google Scholar 

  170. ZKBS (2009) Statement of the ZKBS on the risk assessment of MON810–New studies on the environmental impact of MON810, Federal Office of Consumer Protection and Food Safety, Germany, Ref. No. 6788-02-13, http://www.bvl.bund.de/EN/06_Genetic_Engineering/ZKBS/01_Allg_Stellungnahmen/05_plants/zkbs_plants_maize_MON810_2009.pdf?__blob=publicationFile&v=1

  171. ZKBS (2011) Statement of the Central Commission on Biological Safety (ZKBS) on the latest scientific publications on the risk assessment of the maize line MON810, Federal Office of Consumer Protection and Food Safety, Germany, Az. 6790-02-0013, http://www.bvl.bund.de/EN/06_Genetic_Engineering/ZKBS/01_Allg_Stellungnahmen/05_plants/zkbs_plants_maize_MON810_statement_2011.pdf?__blob=publicationFile&v=4

  172. Zurbrügg C, Nentwig W (2009) Ingestion and excretion of two transgenic Bt corn varieties by slugs. Transgenic Res 18:215–225

    PubMed  Article  CAS  Google Scholar 

  173. Zurbrügg C, Hönemann L, Meissle M, Romeis J, Nentwig W (2010) Decomposition dynamics and structural plant components of genetically modified Bt maize. Transgenic Res 19:257–267

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

We thank Patrick du Jardin, Michael Meissle, Stefan Rauschen and the experts of the Environment Working Group on GMO applications of the EFSA GMO Panel for inspiring discussions that helped to develop this paper.

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Correspondence to Yann Devos or Adinda De Schrijver.

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Yann Devos and Adinda De Schrijver contributed equally to the work and should be considered co-first authors.

Opinions and views (if any) expressed in the present paper do not necessarily reflect those of the European Food Safety Authority (EFSA). This paper does not disclose any confidential information or data. Mention of proprietary products does not constitute an endorsement or a recommendation by EFSA for their use.

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Devos, Y., De Schrijver, A., De Clercq, P. et al. Bt-maize event MON 88017 expressing Cry3Bb1 does not cause harm to non-target organisms. Transgenic Res 21, 1191–1214 (2012). https://doi.org/10.1007/s11248-012-9617-z

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Keywords

  • Genetically modified maize
  • MON 88017
  • MON 863
  • Insect resistance
  • Cry3Bb1
  • Non-target organisms
  • Adverse effects
  • Environmental risk assessment
  • Tiered approach