Advertisement

Transgenic Research

, Volume 25, Issue 4, pp 395–411 | Cite as

Quality of laboratory studies assessing effects of Bt-proteins on non-target organisms: minimal criteria for acceptability

  • Adinda De SchrijverEmail author
  • Yann Devos
  • Patrick De Clercq
  • Achim Gathmann
  • Jörg Romeis
Review

Abstract

The potential risks that genetically modified plants may pose to non-target organisms and the ecosystem services they contribute to are assessed as part of pre-market risk assessments. This paper reviews the early tier studies testing the hypothesis whether exposure to plant-produced Cry34/35Ab1 proteins as a result of cultivation of maize 59122 is harmful to valued non-target organisms, in particular Arthropoda and Annelida. The available studies were assessed for their scientific quality by considering a set of criteria determining their relevance and reliability. As a case-study, this exercise revealed that when not all quality criteria are met, weighing the robustness of the study and its relevance for risk assessment is not obvious. Applying a worst-case expected environmental concentration of bioactive toxins equivalent to that present in the transgenic crop, confirming exposure of the test species to the test substance, and the use of a negative control were identified as minimum criteria to be met to guarantee sufficiently reliable data. This exercise stresses the importance of conducting studies meeting certain quality standards as this minimises the probability of erroneous or inconclusive results and increases confidence in the results and adds certainty to the conclusions drawn.

Keywords

Bt-maize DAS-59122-7 Cry34/35Ab1 Non-target effects Environmental risk assessment 

Notes

Acknowledgments

We thank the experts of the Environmental Risk Assessment Working Group on GMO applications of the GMO Panel of the European Food Safety Authority (EFSA) for inspiring discussions that helped to develop this publication, Elisabeth Waigmann and two anonymous reviewers for insightful comments that helped to improve this paper.

Supplementary material

11248_2016_9950_MOESM1_ESM.docx (50 kb)
Supplementary material 1 (DOCX 49 kb)

References

  1. Abraham R (1985) Nasonia vitripennis an insect from birds’ nests (Hymenoptera, Chalcidoidea, Pteromalidae). Entomol Gen 10:121–124CrossRefGoogle Scholar
  2. Álvarez-Alfageme F, Ferry N, Castañera P, Ortego F, Gatehouse AMR (2008) Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res 17:943–954CrossRefPubMedGoogle Scholar
  3. Aragón P, Lobo JM (2012) Predicted effect of climate change on the invasibility and distribution of the western corn rootworm. Agric For Entomol 14:13–18CrossRefGoogle Scholar
  4. Babendreier D, Kalberer N, Romeis J, Fluri P, Bigler F (2004) Pollen consumption in honey bee larvae: a 343 step forward in the risk assessment of transgenic plants. Apidologie 35:293–300CrossRefGoogle Scholar
  5. Bryan RL, Porch JR, Krueger HO (2000a) PS149B1 binary insecticidal crystal protein: a dietary toxicity study with the ladybird beetle. Unpublished study commissioned by Dow AgroSciences LLC [as referred to in US EPA 2005, 2010a; CERA 2013; EFSA 2013a]Google Scholar
  6. Bryan RL, Porch JR, Krueger HO (2000b) PS149B1 binary insecticidal crystal protein: acute toxicity to the earthworm in an artificial substrate. Unpublished study commissioned by Dow AgroSciences LLC [as referred to in APHIS 2004; US EPA 2005, 2010a; CERA 2013; EFSA 2013a]Google Scholar
  7. Califf K, Ostrem J (2009) Evaluation of seven-spotted ladybird beetle (Coccinella septempunctata) response to maize pollen containing event DAS-59122-7 incorporated into artificial diet. Unpublished study performed by Pioneer Hi-Bred International [as referred to in EFSA, 2013a]Google Scholar
  8. Carstens K, Anderson J, Bachman B, De Schrijver A, Dively G, Federici B, Hamer M, Gielkens M, Jensen P, Lamp W, Rauschen S, Ridley G, Romeis J, Waggoner A (2012) Genetically modified crops and aquatic ecosystems: considerations for environmental risk assessment and non-target organism testing. Transgenic Res 21:813–842CrossRefPubMedGoogle Scholar
  9. Carstens K, Cayabyab B, De Schrijver A, Gadaleta PG, Hellmich RL, Romeis J, Storer N, Valicente FH, Wach M (2014) Surrogate species selection for assessing potential adverse environmental impacts of genetically engineered insect-resistant plants on non-target organisms. GM Crops and Food 5:11–15CrossRefPubMedGoogle Scholar
  10. CERA (2013) A review of the environmental safety of the Cry34Ab1 and Cry35Ab1 proteins, Center for Environmental Risk Assessment (CERA), ILSI Research Foundation, Washington DC. http://www.cera-gmc.org/files/cera/uploads/Cry3435_en_rev1.pdf
  11. CFIA (2005) DD2005-55: Determination of the safety of Dow AgroSciences Canada Inc. and Pioneer Hi-Bred Production INc.’s insect resistant and glufosinate-ammonium herbicide tolerant corn (Zea mays L.) line 59122. Canadian Food Inspection Agency, Ottawa. http://www.inspection.gc.ca/plants/plants-with-novel-traits/approved-under-review/decision-documents/dd2005-55/eng/1311629475402/1311629546153#a4
  12. Chambers CP, Whiles MR, Rosi-Marshall EJ, Tank JL, Royer TV, Griffiths NA, Evans-White MA, Stojak AR (2010) Responses of stream macroinvertebrates to Bt maize leaf detritus. Ecol Appl 20:1949–1960CrossRefPubMedGoogle Scholar
  13. COGEM (2008) Cultivation of genetically modified maize line 59122. COGEM advice CGM/080207-02. http://www.cogem.net/index.cfm/nl/publicaties/publicatie/cultivation-of-genetically-modified-maize-line-1507x59122
  14. Dunville C, Sosa M, Herman R (2010) Soil accumulations of Cry34Ab1 and Cry35Ab1 proteins after three years of cropping with DAS-59122-7 corn. Unpublished study performed by Dow AgroSciences LLC [as referred to in US EPA, 2010a; EFSA, 2013a]Google Scholar
  15. EC (2012) Survey results for the presence of Diabrotica virgifera Le Conte in the European Union in 2011. Report from the Health & Consumers Directorate-General of the European Commission (Reference: Ares(2012)564532 - 08/05/2012)Google Scholar
  16. EFSA (2007) Opinion of the Scientific Panel on genetically modified organisms [GMO] on an application (Reference EFSA-GMO-NL-2005–12) for the placing on the market of insect-resistant genetically modified maize 59122, for food and feed uses, import and processing under Regulation (EC) No 1829/2003, from Pioneer Hi-Bred International, Inc. and Mycogen Seeds, c/o Dow Agrosciences LLC. EFSA J 470:1–25Google Scholar
  17. EFSA (2010) Guidance on the environmental risk assessment of genetically modified plants. EFSA J 8:1–111Google Scholar
  18. EFSA (2013a) Scientific Opinion on an application from Pioneer Hi-Bred International and Dow AgroSciences LLC (EFSA-GMO-NL-2005-23) for placing on the market of genetically modified maize 59122 for food and feed uses, import, processing and cultivation under Regulation (EC) No 1829/2003. EFSA J 11:1–103Google Scholar
  19. EFSA (2013b) Statement supplementing the environmental risk assessment conclusions and risk management recommendations on genetically modified insect-resistant maize 59122 for cultivation in the light of new scientific information on non-target organisms and regionally sensitive areas. EFSA J 11:3443CrossRefGoogle Scholar
  20. Ellis RT, Stockhoff BA, Stamp L, Schnepf HE, Schwab GE, Knuth M, Russell J, Cardineau GA, Narva KE (2002) Novel Bacillus thuringiensis binary insecticidal crystal proteins active on western corn rootworm, Diabrotica virgifera virgifera LeConte. Appl Environ Microbiol 68:1137–1145CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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
  22. Federici BA, Park H-W, Bideshi DK, Wirth MC, Johnson JJ (2003) Recombinant bacteria for mosquito control. J Exp Biol 206:3877–3885CrossRefPubMedGoogle Scholar
  23. Fisher T, Kong X, Boeckman C (2012) Observations of potential larval mortality of Culex quinquefasciatus after forty-eight hour exposure to Cry34Ab1 and Cry35Ab1 proteins. Unpublished study performed by Pioneer Hi-Bred International [as referred to in EFSA 2013a]Google Scholar
  24. Fonseca AE, Westgate ME, Grass L, Dornbos DL (2003) Tassel morphology as an indicator of potential pollen production in maize. Crop Manag. doi: 10.1094/CM-2003-0804-01-RS Google Scholar
  25. Gao Y, Schafer BW, Collins RA, Herman RA, Xu X, Gilbert JR, Ni W, Langer VL, Tagliani LA (2004) Characterization of Cry34Ab1 and Cry35Ab1 insecticidal crystal proteins expressed in transgenic corn plants and Pseudomonas fluorescens. J Agr Food Chem 52:8057–8065CrossRefGoogle Scholar
  26. 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 Biosaf Res 5:57–65CrossRefGoogle Scholar
  27. Gathmann A, Wirooks L, Hothhorn LA, Bartsch D, Schuphan I (2006) Impact of Bt-maize pollen (MON810) on lepidopteran larvae living on accompanying weeds. Mol Ecol 15:2677–2685CrossRefPubMedGoogle Scholar
  28. Hellmich RL, Siegfried BD, Sears MK, Stanley-Horn DE, Daniels MJ, Mattila HR, Spencer T, Bidne KG, Lewis LC (2001) Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. PNAS 98:11925–11930CrossRefPubMedPubMedCentralGoogle Scholar
  29. Herman RA, Scherer PN, Wolt JD (2002a) Rapid degradation of a binary, PS149B1, delta-endotoxin of Bacillus thuringiensis in soil, and a novel mathematical model for fitting curve-linear decay. Physiol Chem Ecol 31:208–214Google Scholar
  30. Herman RA, Scherer PN, Young DL, Mihaliak CA, Meade T, Woodsworth AT, Stockhoff BA, Narva KE (2002b) Binary insecticidal crystal protein from Bacillus thuringiensis, strain PS149B1: effects of individual protein components and mixtures in laboratory bioassays. J Econ Entomol 95:635–639CrossRefPubMedGoogle Scholar
  31. Higgins L (2000) The tri-trophic interaction between PS149B1 transformed maize, corn leaf aphid and ladybird beetle. Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in US EPA 2010a]Google Scholar
  32. Higgins L (2003) The effect of Cry34Ab1/35Ab1 proteins on the development and mortality of the ladybird beetle Coleomegilla maculata DeGeer. Unpublished study performed by Pioneer Hi-Bred International [as referred to in COGEM 2008; US EPA 2005, 2010a; CERA 2013; EFSA 2013a]Google Scholar
  33. Hong B (2009) Statistical analysis. Unpublished study performed by Pioneer Hi-Bred International [as referred to in EFSA 2013a, b]Google Scholar
  34. Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586CrossRefGoogle Scholar
  35. Krauss A (2011) Evaluation of the amino acid sequence similarities of the Cry34Ab1 and Cry35Ab1 proteins to the NCBI protein sequence datasets. Unpublished study performed by Pioneer Hi-Bred International [as referred to in EFSA, 2013a]Google Scholar
  36. 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 56:157–164CrossRefPubMedGoogle Scholar
  37. Li H, Olson M, Lin G, Hey T, Tan SY, Narva KE (2013) Bacillus thuringiensis Cry34Ab1/35Ab1 interactions with western corn rootworm midgut membrane binding sites. PLoS ONE 8:e53079CrossRefPubMedPubMedCentralGoogle Scholar
  38. Luna SV, Figueroa JM, Baltazar BM, Gomez RL, Townsend R, Schoper JB (2001) Maize pollen longevity and distance isolation requirements for effective pollen control. Crop Sci 41:1551–1557CrossRefGoogle Scholar
  39. Lundgren JG (2009) Relationships of natural enemies and nonprey foods. Springer, BerlinGoogle Scholar
  40. Maggi VL (2001) Microbial PS149B1 binary insecticidal crystal protein, pollen expressing PS149B1 binary ICP, and individual PS149B1 14 kDa and 44 kDa ICPs: evaluation of dietary exposure on honeybee development. Unpublished study commissioned by Dow AgroSciences LLC [as referred to in US EPA 2005, 2010a; CERA 2013; EFSA 2013a, b]Google Scholar
  41. Marino TA, Yaroch AM (2001) 149B1 binary insecticidal crystal protein: acute toxicity study with the dahnid, Daphnia Magna Straus. Unpublished study commissioned by Dow AgroSciences LLC [as referred to in US EPA 2005, 2010a; CERA 2013; EFSA 2013a]Google Scholar
  42. Măruţescu A (2012) A brief survey regarding fate of Bt proteins synthesized by transgenic maize in soil. J Hortic For Biotech 16:126–130Google Scholar
  43. Masson L, Schwab G, Mazza A, Brousseau R, Potvin L, Schwartz JL (2004) A novel Bacillus thuringiensis (PS149B1) containing a Cry34Ab1/35Ab1 binary toxin specific for western corn rootworm Diabrotica virgifera virgifera LeConte forms ion channels in lipid membranes. Biochemistry 43:12349–12357CrossRefPubMedGoogle Scholar
  44. 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. Agric For Entomol 11:29–46CrossRefGoogle Scholar
  45. Meissle M, Romeis J (2009) Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Entomol Exp Appl 131:308–319CrossRefGoogle Scholar
  46. Meissle M, Romeis J, Bigler F (2011) Bt maize and integrated pest management—a European perspective. Pest Manag Sci 67:1049–1058CrossRefPubMedGoogle Scholar
  47. Meissle M, Álvarez-Alfageme F, Malone LA, 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. Supporting Publications 2012:EN-334, European Food Safety Authority (EFSA), Parma, Italy (170 pp). http://www.efsa.europa.eu/en/publications.htm
  48. Nguyen HT, Jehle JA (2009) Stability of Cry1Ab protein during long-term storage for standardization of insect bioassays. Environ Biosaf Res 8:113–119CrossRefGoogle Scholar
  49. Obrist LB, Dutton A, Albajes R, Bigler F (2006) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31:143–154CrossRefGoogle Scholar
  50. Patnaude M (2008) Evaluation of potential dietary effects of Cry34/35Ab1 protein on insidious flower bugs, Orius insidiosus (Hemiptera: Anthocoridae). Project Number: 13855/6105, PHI/2004/099, 092705/OPPTS/PIONEER. Unpublished study prepared by Springborn Smithers Laboratories, 41 pages [as referred to in US EPA 2010]Google Scholar
  51. Perry JN, Arpaia S, Bartsch D, Birch ANE, Devos Y, Gathmann A, Gennaro A, Kiss J, Messéan A, Mestdagh S, Nuti M, Sweet JB, Tebbe CC (2013) No evidence requiring change in the risk assessment of Inachis io larvae. Ecol Model 268:103–122CrossRefGoogle Scholar
  52. Pleasants JM, Hellmich RL, Dively GP, Sears MK, Stanley-Horn DE, Mattila HR, Foster JE, Clark TL, Jones GD (2001) Corn pollen deposition on milkweeds in or near corn field. PNAS 98:11919–11924CrossRefPubMedPubMedCentralGoogle Scholar
  53. Porch JR, Krueger HO (2001) PS149B1 binary insecticidal crystal protein: dietary toxicity to parasitic Hymenoptera (Nasonia vitripennis). Unpublished study commissioned by Dow AgroSciences LLC [as referred to in COGEM 2008; US EPA 2005, 2010a; EFSA 2013a]Google Scholar
  54. Raybould A, Stacey D, Vlachos D, Graser G, Li X, Joseph R (2007) Non-target organism risk assessment of MIR604 maize expressing mCry3A for control of corn rootworm. J Appl Entomol 131:391–399CrossRefGoogle Scholar
  55. Raybould A, Kilby P, Graser G (2013) Characterising microbial protein test substances and establishing their equivalence with plant-produced proteins for use in risk assessments of transgenic crops. Transgenic Res 22:445–460CrossRefPubMedGoogle Scholar
  56. Romeis J, Meissle M (2011) Non-target risk assessment of Bt crops—cry protein uptake by aphids. J Appl Entomol 135:1–6CrossRefGoogle Scholar
  57. 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 26:203–208CrossRefPubMedGoogle Scholar
  58. 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 20:1–22CrossRefPubMedGoogle Scholar
  59. Romeis J, Raybould A, Bigler F, Candolfi MP, Hellmich RL, Huesing JE, Shelton AM (2013) Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops. Chemosphere 90:901–909CrossRefPubMedGoogle Scholar
  60. Romeis J, Meissle M, Álvarez-Alfageme F, Bigler F, Bohan DA, Devos Y, Malone LA, Pons X, Rauschen S (2014) Potential use of an arthropod database to support the non-target risk assessment and monitoring of transgenic plants. Transgenic Res 23:995–1013CrossRefPubMedGoogle Scholar
  61. 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
  62. 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. PNAS 104:16204–16208CrossRefPubMedPubMedCentralGoogle Scholar
  63. Schafer B (2002) Characterization of Cry34Ab1 and Cry35Ab1 from recombinant Pseudomonas fluorescens and transgenic maize. Unpublished study performed by Dow AgroSciences LLC [as referred to in US EPA 2010]Google Scholar
  64. Schnepf HE, Lee S, Dojillo JJ, Burmeister P, Fencil K, Morera L, Nygaard L, Narva KE, Wolt JD (2005) Characterization of Cry34/Cry35 binary insecticidal proteins from diverse Bacillus thuringiensis strain collections. Appl Environ Microbiol 71:1765–1774CrossRefPubMedPubMedCentralGoogle Scholar
  65. Sears M, Rempel S (2003) Final report on the laboratory bioassay assessment of Bt corn pollen and its effect on the larvae of the monarch butterfly. Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in US EPA 2005; EFSA 2013a]Google Scholar
  66. Shan G, Embrey SK (2009a) Determination of Cry34Ab1 insecticidal crystal protein in soils by enzyme-linked immunosorbent assay. Unpublished study performed by Dow AgroSciences LLC [as referred to in EFSA 2013a]Google Scholar
  67. Shan G, Embrey SK (2009b) Determination of Cry35Ab1 insecticidal crystal protein in soils by enzyme-linked immunosorbent assay. Unpublished study performed by Dow AgroSciences LLC [as referred to in EFSA, 2013a]Google Scholar
  68. Sheldon JK, MacLeod EG (1971) Studies on the biology of the Chrysopidae. II. The feeding behavior of the adult of Chrysopa carnea (Neuroptera). Psyche 78:107–121CrossRefGoogle Scholar
  69. Sindermann AB, Porch JR, Krueger HO (2001) PS149B1 insecticidal crystal protein: dietary toxicity to green lacewing larvae (Chrysoperla carnea). Unpublished study commissioned by Dow AgroSciences LLC [as referred to in US EPA 2005, 2010; CERA 2013; EFSA 2013a]Google Scholar
  70. Swanckaert J, Pannecoucque J, Van Waes J, De Cauwer D, Latre J, Haesaert G, Reheul D (2016) Harvest date do not influence variety ranking in Belgian forage maize variety trials. J Agric Sci. doi: 10.1017/s0021859615000994
  71. Székács A, Kong X (2011) Evaluation of the effects of pollen of transgenic maize containing event DAS-59122-7 on the non-target species, green dock leaf beetle (Gastrophysa viridula) fed on Rumex spp. in a direct exposure system under laboratory conditions. Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in EFSA 2013a]Google Scholar
  72. Takács E, Bánáti H, Fónagy A, Darvas B (2010) Short term study of DAS-59122-7 maize on L1 and L2 larvae of seven-spotted ladybird (Coccinella septempunctata) feeding on the bird cherry-oat aphid (Rhopalosiphum padi). Növénytermesztés 59S:625–628Google Scholar
  73. Takács E, Fónagy A, Juracsek J, Kugler N, Székács A (2012) Characterisation of tritrophic effects of DAS-59122-7 maize on the seven-spotted ladybird (Coccinella septempunctata) feeding on the bird cherry-oat aphid (Rhopalosiphum padi). IOBC/WPRS Bull 73:121–134Google Scholar
  74. 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. PNAS 107:17645–17650CrossRefPubMedPubMedCentralGoogle Scholar
  75. Teixeira D (2001) Assessment of chronic toxicity of diet containing Bacillus thuringiensis PS149B1 insecticidal crystal protein to Collembola (Folsomia candida). Unpublished study commissioned by Dow AgroSciences LLC [as referred to in US EPA 2005, 2010; EFSA 2013a]Google Scholar
  76. Teixeira D (2006a) Acute toxicity to earthworms (Eisenia fetida) using lyophilized transgenic maize (DAS-59122-7) whole plant material containing Cry34Ab1 and Cry35Ab1. Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in EFSA 2013a]Google Scholar
  77. Teixeira D (2006b) Chronic toxicity to Collembola (Folsomia candida) using lyophilized transgenic maize (DAS-59122-7) whole plant material containing Cry34Ab1 and Cry35Ab1. Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in EFSA 2013a]Google Scholar
  78. Tinsley NA, Estes RE, Gray ME (2013) Validation of a nested error component model to estimate damage caused by corn rootworm larvae. J Appl Entomol 137:161–169CrossRefGoogle Scholar
  79. US EPA (2010) Biopesticides registration action document: Bacillus thuringiensis Cry34Ab1 and Cry35Ab1 proteins and the genetic material necessary for their production (PHP17662 T-DNA) in event DAS-59122–7 corn (OECD Unique Identifier: DAS-59122–7), PC code: 006490. http://www.epa.gov/oppbppd1/biopesticides/pips/cry3435ab1-brad.pdf
  80. USDA (2004) Application for the determination of nonregulated status for B.t. Cry34/35Ab1 insect-resistant, glufosinate-tolerant corn: corn line 59122. http://www.aphis.usda.gov/brs/aphisdocs/03_35301p.pdf
  81. van Rozen K, Ester A (2010) Chemical control of Diabrotica virgifera virgifera LeConte. J Appl Entomol 134:376–384CrossRefGoogle Scholar
  82. Vinall S (2005) A laboratory toxicity test of the Cry34Ab1 and Cry35Ab1 proteins to larvae of the ground-dwelling beetle, Poecilus cupreus (Coleoptera: Carabidae). Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in US EPA 2010; EFSA 2013a]Google Scholar
  83. Vinall S (2011a) Cry34Ab1 and Cry35Ab1—a laboratory bioassay of the effects on the predatory bug, Orius laevigatus (Hemiptera: Anthocoridae). Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in EFSA 2013a]Google Scholar
  84. Vinall S (2011b) Laboratory bioassay of the effects of pollen from hybrid maize containing the combined trait product DAS-59122-7xDASØ15Ø7-1xMON-ØØ6Ø3-6 on ladybird beetle, Coccinella septempunctata (Coleoptera: Coccinellidae). Unpublished study commissioned by Pioneer Hi-Bred International [as referred to in EFSA 2013b]Google Scholar
  85. Vogt H, Bigler F, Brown K, Candolfi MP, Kemmeter F, Kühner C, Moll M, Travis A, Ufer A, Viñuela E, Waldburger M, Waltersdorfer A (2000) Laboratory method to test effects of plant protection products on larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). In: Candolfi MP et al (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. Reinheim, IOBC/WPRS, pp 27–44Google Scholar
  86. Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe—the ‘no control’. J Appl Entomol 134:385–394CrossRefGoogle Scholar
  87. WHO (2009) Handbook: good laboratory practice (GLP): quality practices for regulated non-clinical research and development. http://www.who.int/tdr/publications/documents/glp-handbook-old.pdf?ua=1
  88. Yang Y, Chen X, Cheng L, Cao F, Romeis J, Li Y, Peng Y (2015) Toxicological and biochemical analyses demonstrate no toxic effect of Cry1C and Cry2A to Folsomia candida. Scientific Reports 5:15619CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Adinda De Schrijver
    • 1
    Email author
  • Yann Devos
    • 2
  • Patrick De Clercq
    • 3
  • Achim Gathmann
    • 4
  • Jörg Romeis
    • 5
  1. 1.Biosafety and Biotechnology UnitScientific Institute of Public HealthBrusselsBelgium
  2. 2.GMO UnitEuropean Food Safety Authority (EFSA)ParmaItaly
  3. 3.Department of Crop ProtectionGhent UniversityGhentBelgium
  4. 4.Unit 404: Coexistence, GMO-MonitoringFederal Office of Consumer Protection and Food Safety (BVL)BerlinGermany
  5. 5.Institute for Sustainability SciencesAgroscopeZurichSwitzerland

Personalised recommendations