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Environmental Impact of Genetically Modified Maize Expressing Cry1 Proteins

  • Detlef BartschEmail author
  • Yann Devos
  • Rosie Hails
  • Jozsef Kiss
  • Paul Henning Krogh
  • Sylvie Mestdagh
  • Marco Nuti
  • Angela Sessitsch
  • Jeremy Sweet
  • Achim Gathmann
Chapter
Part of the Biotechnology in Agriculture and Forestry book series (AGRICULTURE, volume 64)

Abstract

For more than a decade, genes of Bacillus thuringiensis (‘Bt’) that encode lepidopteran-specific protein toxins (Cry1Ab and Cry1F) have been engineered into maize for protection against lepidopteran pests. An extensive body of research data and environmental risk assessments (ERA) has been assembled on the potential environmental impact of Cry1 expressing maize. The available literature so far suggests only minor environmental effects. The majority of laboratory studies and all the field studies reviewed did not reveal any unexpected adverse or long-term effectson the environment. Negative effects observed in the laboratory do not necessarily translate to field conditions. There are more than 10 years experience of cultivating GM maize worldwide and few long-term effects have been reported. For future research studies, modelling and monitoring are appropriate tools to investigate long-term environmental effects during GMO cultivation.

Keywords

European Union Genetically Modify Genetically Modify Crop Cry1 Protein Cry1 Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors wish to thank the Members of the EFSA GMO Panel, its Ad-Hoc Members of the Environment Working Group and the staff of EFSA GMO Unit for their contributions to several published EFSA opinions (e.g., EFSA2008b, c), which provided the basis for this review.

References

  1. Ahmad A, Wilde G, Yan Zhu K (2005) Detectability of coleopteran-specific Cry3Bb1 protein in soil and its effect on nontarget surface and below-ground arthropods. Environ Entomol 34:385–394CrossRefGoogle Scholar
  2. Alstad DA, Andow DA (1995) Managing the evolution of insect resistance to transgenic plants. Science 268:1894–1896PubMedCrossRefGoogle Scholar
  3. Alvarez-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 17:943–954PubMedCrossRefGoogle Scholar
  4. Alves AP, Spencer T, Tabashnik BE, Siegfried BD (2006) Inheritance of resistance to the Cry1Ab Bacillus thuringiensis toxin in Ostrinia nubilalis (Lepidoptera: Crambidae). J Econ Entomol 99:494–501PubMedCrossRefGoogle Scholar
  5. Andersen MN, Sausse C, Lacroix B, Caul S, Messéan A (2007) Agricultural studies of GM maize and the field experimental infrastructure of ECOGEN. Pedobiologia 51:175–184CrossRefGoogle Scholar
  6. Anderson PL, Hellmich RL, Prasifka JR, Lewis LC (2005) Effects on fitness and behavior or monarch butterfly larvae exposed to a combination of Cry1Ab-expressing corn anthers and pollen. Environ Entomol 34:944–952CrossRefGoogle Scholar
  7. Anderson PL, Hellmich RL, Sumerford DV, Lewis LC (2004) Effects of Cry1Ab-expressing corn anthers on monarch butterfly larvae. Environ Entomol 33:1109–1115CrossRefGoogle Scholar
  8. Andow DA (2008) The risk of resistance evolution in insects to transgenic insecticidal crops. Collect Biosaf Rev 4:142–199Google Scholar
  9. Andow DA, Alstad DA (1998) F2 screen for rare resistance alleles. J Econ Entomol 91:572–578Google Scholar
  10. Andow DA, Olson DM, Hellmich RL, Alstad DN, Hutchinson WD (2000) Frequency of resistance alleles to Bacillus thuringiensis toxin in an Iowa population of European corn borer. J Econ Entomol 93:26–30PubMedCrossRefGoogle Scholar
  11. Andow DA, Lövei GL, Arpaia S (2006a) Ecological risk assessment for Bt crops. Nat Biotechnol 24:749–751PubMedCrossRefGoogle Scholar
  12. Andow DA, Birch, ANE, Dusi AN, Fontes, EMG, Hilbeck A, Lang A, Lövei GL, Pires CSS, Sujii ER, Underwood E, Wheatley RE (2006b) Non-target and biodiversity risk assessment for genetically modified (GM) crops. http://www.gmoera.umn.edu/public/publications/download/Andowetal2006_ISBR.pdf. Accessed on 21 Jan 2009
  13. Andreadis SS, Alvarez-Alfageme FA, Sánchez-Ramos I, Stodola TJ, Andow DA, Milonas PG, Savopoulou-Soultani M, Castánera P (2007) Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in Greek and Spanish population of Sesamia nonagrioides (Lepidoptera: Noctuidae). J Econ Entomol 100:195–201PubMedCrossRefGoogle Scholar
  14. Anonymous (2006) Monitoring of the environmental effects of the Bt gene. Schriftenreihe Bayerische Landesanstalt Landwirtschaft 10/2006. http://www.lfl-neu.bayern.de/publikationen/daten/schriftenreihe_url_1_43.pdf. Accessed on 21 Jan 2009
  15. Aviron S, Sanvido O, Herzog F, Baudry J, Romeis J, Bigler F (2006) Monitoring effects of GM crops on butterflies: the use of multiscale approaches for general surveillance. J Consum Prot Food Saf 1[S1]:85–88Google Scholar
  16. Babendreier D, Kalberer NM, Romeis J, Fluri P, Bigler F (2004) Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants. Apidology 35:293–300CrossRefGoogle Scholar
  17. Babendreier D, Kalberer NM, Romeis J, Fluri P, Mulligan E, Bigler F (2005) Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidology 36:585–594CrossRefGoogle Scholar
  18. Bailey RI, Bourguet D, Le Pallec AH, Ponsard S (2007) Dispersal propensity and settling preferences of European corn borers in maize field borders. J Appl Ecol 44:385–394CrossRefGoogle Scholar
  19. Bakonyi G, Szira F, Kiss I, Villányi I, Seres A, Székács A (2006) Preference tests with collembolas on isogenic and Bt-maize. Eur J Soil Biol 42:S132–S135CrossRefGoogle Scholar
  20. Baltazar BM, de Jesús Sánchez-Gonzalez J, de la Cruz-Larios, Schoper JB (2005) Pollination between maize and teosinte: an important determinant of gene flow in Mexico. Theor Appl Genet 110:519–526PubMedCrossRefGoogle Scholar
  21. Bates SL, Zhao JZ, Roush RT, Shelton AM (2005) Insect resistance management in GM crops: past, present and future. Nat Biotechnol 25:57–62CrossRefGoogle Scholar
  22. Baumgarte S, Tebbe CC (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Mol Ecol 14:2539–2551PubMedCrossRefGoogle Scholar
  23. Beachy RN, Fedoroff NV, Goldberg RB, McHughen A (2008) The burden of proof: a response to Rosi-Marshall et al. Proc Natl Acad Sci USA 105:E9CrossRefGoogle Scholar
  24. BEETLE (2009) Long-term effects of genetically modified (GM) crops on health and the environment (including biodiversity): prioritization of potential risks and delimitation of uncertainties. German Federal Office of Consumer Protection and Food Safety, BLaU Umweltstudienand Genius GmbH. http://ec.europa.eu/environment/biotechnology/pdf/beetle_report.pdf. Accessed on 23 Jun 2009
  25. Birch ANE, Griffiths BS, Caul S, Thompson J, Heckmann LH, Krogh PH, Cortet J (2007) The role of laboratory, glasshouse and field scale experiments in understanding the interactions between genetically modified crops and soil ecosystems: a review of the ECOGEN project. Pedobiologia 51:251–260CrossRefGoogle Scholar
  26. Bitocchi E, Nanni L, Rossi M, Rau D, Giardini A, Bellucci E, Buonamici A, Vendramin GG, Papa R (2009) Introgression from modern hybrid varieties into landrace populations of maize (Zea mays ssp. mays L.) in central Italy. Mol Ecol 18:603–621PubMedCrossRefGoogle Scholar
  27. Blackwood CB, Buyer JS (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J Environ Qual 33:832–836PubMedCrossRefGoogle Scholar
  28. Bøhn T, Primicerio R, Hessen D, Traavik T (2008) Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch Environ Contam Tox 55:584–592CrossRefGoogle Scholar
  29. Bourguet D (2004) Resistance to Bacillus thuringiensis toxins in the European corn borer: what chance for Bt maize? Physiol Entomol 29:251–256CrossRefGoogle Scholar
  30. Bourguet D, Chaufaux J, Micoud A, Delos M, Naibo B, Bombarde F, Marque G, Eychenne N, Pagliari C (2002) Ostrinia nubilalis parasitism and the field abundance of non-target insects in transgenic Bacillus thuringiensis corn (Zea mays). Environ Biosaf Res 1:49–60CrossRefGoogle Scholar
  31. Bourguet D, Chaufaux J, Séguin M, Buisson C, Hinton JL, Stodola TJ, Porter P, Cronholm G, Buschman LL, Andow DA (2003) Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer, Ostrinia nubilalis. Theor Appl Genet 106:1225–1233PubMedGoogle Scholar
  32. Bravo A, Soberón M (2008) How to cope with insect resistance to Bt toxins? Trends Biotechnol 26:573–579PubMedCrossRefGoogle Scholar
  33. Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicology 49:423–35Google Scholar
  34. Brusetti L, Francia P, Bertolini C, Pagliuca A, Borin S, Sorlini C, Abruzzese A, Sacchi G, Viti C, Giovanetti L, Giuntini E, Bazzicalupo M, Daffonchio D (2004) Bacterial communities associated with the rhizosphere of transgenic Bt 176 maize (Zea mays) and its non transgenic counterpart. Plant Soil 266:11–21CrossRefGoogle Scholar
  35. Castaldini M, Turrini A, Sbrana C, Benedetti A, Marchionni M, Mocali S, Fagiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovanetti M (2005) Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 71:6719–6729PubMedCrossRefGoogle Scholar
  36. Chaufaux J, Séguin M, Swanson JJ, Bourguet D, Siegfried BD (2001) Chronic exposure of the European corn borer (Lepidoptera: Crambidae) to Cry1Ab Bacillus thuringiensis toxin. J Econ Entomol 94:1564–1570PubMedCrossRefGoogle Scholar
  37. Clark BW, Coats JR (2006) Subacute effects of Cry1Ab Bt corn litter on the earthworm Eisenia fetida and the springtail Folsomia candida. Environ Entomol 35:1121–1129CrossRefGoogle Scholar
  38. Clark BW, Phillips TA, Coats (2005) Environmental fate and effects of Bacillus thuringiensis (Bt) proteins from transgenic crops: a review. J Agric Food Chem 53:4643–4653PubMedCrossRefGoogle Scholar
  39. Clark BW, Prihoda KR, Coats JR (2006) Subacute effects of transgenic Cry1Ab Bacillus thuringiensis corn litter on the isopods Trachelipus rathkii and Armadillidium nasatum. Environ Tox Chem 25: 2653–2661CrossRefGoogle Scholar
  40. Cortet J, Andersen MN, Caul S, Griffiths BS, Joffre R, Lacroix B, Sausse C, Thompson J, Krogh PH (2006) Decomposition processes under Bt (Bacillus thuringiensis) maize: Results of a multi-site experiment. Soil Biol Biochem 38:195–199CrossRefGoogle Scholar
  41. Cortet J, Griffiths BS, Bohanec M, Demsar D, Andersen MN, Caul S, Birch ANE, Pernin C, Tabone E, de Vaufleury A, Xin K, Krogh PH (2007) Evaluation of effects of transgenic Bt maize on microarthropods in a European multi-site experiment. Pedobiologia 51:207–218CrossRefGoogle Scholar
  42. Crecchio C, Stotzky G (2001) Biodegradation and insecticidal activity of the toxin from Bacillus thuringiensis subsp. kurstaki bound on complexes of montmorillonite-humic acids-Al hydroxypolymers. Soil Biol Biochem 33:573–581CrossRefGoogle Scholar
  43. Dale PJ, Clarke B, Fontes EMD (2002) Potential for the environmental impact of transgenic crops. Nat Biotechnol 20:567–574PubMedCrossRefGoogle Scholar
  44. Dalecky A, Ponsard S, Bailey RI, Pélissier C, Bourguet D (2006) Resistance evolution to Bt crops: predispersal mating of European corn borers. PLoS Biol 4:1048–1057 (e181)CrossRefGoogle Scholar
  45. de la Poza M, Pons X, Farinós GP, López C, Ortego F, Eizaguirre M, Castañera P, Albajes R (2005) Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Prot 24:677–684CrossRefGoogle Scholar
  46. de Vaufleury A, Kramarz PE, Binet P, Cortet J, Caul S, Andersen MN, Plumey E, Coeurdassier M, Krogh PH (2007) Exposure and effect assessments of Bt-maize on non-target organisms (gastropods, microarthropods, mycorrhizal fungi) in microcosms. Pedobiologia 51:185–194CrossRefGoogle Scholar
  47. Delos M, Hervieu F, Folcher L, Micoud A, Eychenne N (2006) Biological surveillance programme for the monitoring of crop pests and indicators in France. J Consum Prot Food Saf 1[S1]:30–36Google Scholar
  48. Delos M, Hervieu F, Folcher L, Micoud A, Eychenne N (2007) Biological surveillance programme for the monitoring of crop pests and indicators, French devices and European approach compared. J Consum Prot Food Saf 2[S1]:16–24Google Scholar
  49. Devos Y, Demont M, Sanvido O (2008) Coexistence in the EU – return of the moratorium on GM crops? Nat Biotechnol 26:1223–1225PubMedCrossRefGoogle Scholar
  50. Devos Y, De Schrijver A, Reheul D (2009) Quantifying the introgressive hybridisation propensity between transgenic oilseed rape and its wild/weedy relatives. Environ Monit Assess 149:303–322PubMedCrossRefGoogle Scholar
  51. Dively GP, Rose R, Sears MK, Hellmich RL, Stanley-Horn DE, Calvin DD, Russo JM, Anderson PL (2004) Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis. Environ Entomol 33:1116–1125CrossRefGoogle Scholar
  52. Donegan KK, Palm CJ, Fieland VJ, Porteous LA, Ganio LM, Schaller DL, Bucao LQ, Seidler RJ (1995) Changes in levels, species, and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Appl Soil Ecol 2:111–124CrossRefGoogle Scholar
  53. Douville M, Gagné F, Masson L, McKay J, Blaise C (2005) Tracking the source of Bacillus thuringiensis Cry1Ab endotoxin in the environment. Biochem System Ecol 33:219–232CrossRefGoogle Scholar
  54. Douville M, Gagné F, Blaise C, André C (2007) Occurrence and persistence of Bacillus thuringiensis (Bt) and transgenic Bt corn cry1Ab gene from an aquatic environment. Ecotox Environ Saf 66:195–203CrossRefGoogle Scholar
  55. Douville M, Gagné F, André C, Blaise C (2009) Occurrence of the transgenic corn cry1Ab gene in freshwater mussels (Elliptio complanata) near corn fields: evidence of exposure by bacterial ingestion. Ecotox Environ Saf 72:17–25CrossRefGoogle Scholar
  56. Duan JJ, Marvier M, Huesing J, Dively G, Huang ZY (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE 3:1–6 (e1415)CrossRefGoogle Scholar
  57. Dubelman S, Ayden BR, Bader BM, Brown CR, Jiang C, Vlachos D (2005) Cry1Ab protein does not persist in soil after 3 years of sustained Bt corn use. Environ Entomol 34:915–921CrossRefGoogle Scholar
  58. Dutton A, Klein H, Romeis J, Bigler F (2002) Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol Entomol 27:441–447CrossRefGoogle Scholar
  59. Dutton A, Romeis J, Bigler F (2003) Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study. BioControl 48:611–636CrossRefGoogle Scholar
  60. Dutton A, Romeis J, Bigler F (2005) Effects of Bt maize expressing Cry1Ab and Bt spray on Spodoptera littoralis. Entomol Exp Appl 114:161–169CrossRefGoogle Scholar
  61. Eckert J, Schuphan I, Hothorn LA, Gathmann A (2006) Arthropods on maize ears for detecting impacts of Bt maize on nontarget organisms. Environ Entomol 35:554–560CrossRefGoogle Scholar
  62. EFSA (2006) Opinion of the scientific panel on genetically modified organisms on the post market environmental monitoring (PMEM) of genetically modified plants, EFSA J 319:1–27. http://www.efsa.europa.eu/cs/BlobServer/Scientific_Opinion/gmo_op_ej319_pmem_en,0.pdf. Accessed on 21 Jan 2009Google Scholar
  63. EFSA (2007a) Minutes of the 37th plenary meeting of the scientific panel on genetically modified organisms held on 22–23 November 2007 in Brussels, Belgium (adopted on 18 December 2007). http://www.efsa.europa.eu/cs/BlobServer/Event_Meeting/GMO_Minutes_37th_plenmeet.pdf. Accessed on 21 Jan2009
  64. EFSA (2007b) Statement of the scientific panel on genetically modified organisms on the safe use of the nptII antibiotic resistance marker gene in genetically modified plants. http://www.efsa.europa.eu/cs/BlobServer/Statement/gmo_statement_nptII_,0.pdf. Accessed on 21 Jan 2009
  65. EFSA (2008a) Working document of the GMO panel on the interplay between directive 2001/18/EC (GMOs) and directive 91/414/EEC (plant protection products). http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1211902125247.htm. Accessed on 21 Jan 2009
  66. EFSA (2008b) Scientific opinion of the panel on genetically modified organisms on a request from the European Commission related to the safeguard clause invoked by Austria on maize MON810 and T25 according to article 23 of directive 2001/18/EC. EFSA J 891:1–64. http://www.efsa.europa.eu/cs/BlobServer/Scientific_Opinion/gmo_op_ej891_austrian_safeg_clause_MON810_T25_maize_en.pdf. Accessed on 21 Jan 2009Google Scholar
  67. EFSA (2008c) Scientific opinion of the panel on genetically modified organisms on a request from the European Commission related to the safeguard clause invoked by France on maize MON810 according to article 23 of directive 2001/18/EC and the emergency measure according to article 34 of regulation (EC) No 1829/2003. EFSA J 850:1–45. http://www.efsa.europa.eu/cs/BlobServer/Scientific_Opinion/gmo_op_ej850_French_safeguard_clause_on_MON810_maize_en,0.pdf. Accessed on 21 Jan 2009Google Scholar
  68. EFSA (2009) Scientific Opinion of the Panel on Genetically Modified Organisms on applications (EFSA-GMO-RX-MON810) for the renewal of authorisation for the continued marketing of (1) existing food and food ingredients produced from genetically modified insect resistant maize MON810; (2) feed consisting of and/or containing maize MON810, including the use of seed for cultivation; and of (3) food and feed additives, and feed materials produced from maize MON810, all under Regulation (EC) No 1829/2003 from Monsanto. The EFSA Journal 1149, 1–85. http://www.efsa.europa.eu/cs/BlobServer/Scientific_Opinion/gmo_op_ej1149_maizeMON810_finalopinion_en_rev.pdf?ssbinary=true.Accessedon30Sep2009.
  69. Eizaguirre M, Albajes R, López C, Eras J, Lumbieres B, Pons X (2006) Six years after the commercial introduction of Bt maize in Spain: field evaluation, impact and future prospects. Transgenic Res 15:1–12PubMedCrossRefGoogle Scholar
  70. Engels H, Sinha A, Schuphan I, Eber S (2008) Small-scale dispersal of the European corn borer and its relevance for resistance management in Bt maize. J Appl Entomol 132:675–680CrossRefGoogle Scholar
  71. Escher N, Kach B, Nentwig W (2000) Decomposition of transgenic Bacillus thuringiensis maize by microorganisms and woodlice Porcello scaber (Crustacea: Isopoda). Basic Appl Entomol 1:161–169CrossRefGoogle Scholar
  72. Fang M, Kremer RJ, Motavalli PP, Davis G (2005) Bacterial diversity in rhizosphere of nontransgenic and transgenic corn. Appl Environ Microbiol 71:4132–4136PubMedCrossRefGoogle Scholar
  73. Fang M, Motavalli PP, Kremer RJ, Nelson KA (2007) Assessing changes in soil microbial communities and carbon mineralieation in Bt and non-Bt corn residue-amended soils. Appl Soil Ecol 37:150–160CrossRefGoogle Scholar
  74. Faria CA, Wäckers FL, Prichard J, Barrett DA, Turlings TCJ (2007) High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS ONE 2:1–11 (e600)CrossRefGoogle Scholar
  75. Farinós GP, de la Poza M, Hernández-Crespo P, Ortego F, Castañera P (2004) Resistance monitoring of field populations of the corn borers Sesamia nonagrioides and Ostrinia nubilalis after 5 years of Bt maize cultivation in Spain. Entomol Exp Appl 110:23–30CrossRefGoogle Scholar
  76. Farinós GP, de la Poza M, Hernández-Crespo P, Ortego F, Castañera P (2008) Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central Spain. Biol Control 44:362–371CrossRefGoogle Scholar
  77. Felke M, Langenbruch G-A (2005) Auswirkungen des Pollens von transgenem Bt-Mais auf ausgewählte Schmetterlingslarven. BfN-Skripten 157. http://www.bfn.de/fileadmin/MDB/documents/skript157.pdf. Accessed on 21 Jan 2009
  78. Felke M, Lorenz N, Langenbruch GA (2002) Laboratory studies on the effects of pollen from Bt-maize on larvae of some butterfly species. J Appl Entomol 126:320–325CrossRefGoogle Scholar
  79. Ferré J, Van Rie J, MacIntosh SC (2008) Insecticidal genetically modified crops and insect resistance management (IRM). In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer, Heidelberg, pp 41–85CrossRefGoogle Scholar
  80. Filion M (2008) Do transgenic plants affect rhizobacteria populations? Microb Biotechnol 1:463–475PubMedCrossRefGoogle Scholar
  81. Fishhoff DA (1996) Insect-resistant crop plants. In: Persley GJ (ed) Biotechnology and integrated pest management. CAB International, Wallingford, pp 214–227Google Scholar
  82. Flachowsky G, Aulrich K, Böhme H, Halle I (2007) Studies on feeds from genetically modified plants (GMP). Contributions to nutritional and safety assessment. Anim Feed Sci Technol 133:2–30CrossRefGoogle Scholar
  83. Flores S, Saxena D, Stotzky G (2005) Transgenic Bt plants decompose less in soil than non-Bt plants. Soil Biol Biochem 37:1073–1082CrossRefGoogle Scholar
  84. Gassmann AJ, Carrière Y, Tabashnik BE (2009) Fitness costs of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 54:147–163PubMedCrossRefGoogle Scholar
  85. Gathmann A, Wirooks L, Eckert J, Schuphan I (2006a). Spatial distribution of Aglais urticae (L.) and its host plant Urtica dioica (L.) in an agricultural landscape: implications for Bt maize risk assessment and post-market monitorng. Environ Biosaf Res 5:27–36CrossRefGoogle Scholar
  86. Gathmann A, Wirooks L, Hothhorn LA, Bartsch D, Schuphan I (2006b) Impact of Bt-maize pollen (MON810) on lepidopteran larvae living on accompanying weeds. Mol Ecol 15:2677–2685PubMedCrossRefGoogle Scholar
  87. Glare TR, O'Callaghan M (2000) Bacillus thuringiensis, biology, ecology and safety. Wiley, Chichester, p 350Google Scholar
  88. Gomez I, Pardo-Lopez L, Munoz-Garay C, Fernandez LE, Perez C, Sanchez J, Soberón M, Bravo A (2007) Role of receptor interaction in the mode of action of insecticidal Cry and Cyt toxins produced by Bacillus thuringiensis. Peptides 28:169–173PubMedCrossRefGoogle Scholar
  89. Gómez-Barbero M, Berbel J, Rodríguez-Cerezo E (2008) Bt corn in Spain – the performance of the EU's first GM crop. Nat Biotechnol 26:384–386PubMedCrossRefGoogle Scholar
  90. Griffiths BS, Caul S, Thompson J, Birch ANE, Scrimgeour C, Andersen MN, Cortet, J, Messean A, Sausse C, Lacroix B, Krogh PH (2005) A comparison of soil microbial community structure, protozoa, and nematodes in field plots of conventional and genetically modified maize expressing the Bacillus thuringiensis Cry1Ab toxin. Plant Soil 275:135–146CrossRefGoogle Scholar
  91. Griffiths BS, Caul S, Thompson J, Birch ANE, Scrimgeour C, Cortet J, Foggo A, Hackett CA, Krogh PH (2006) Soil microbial and faunal community responses to Bt-maize and insecticide in two soils. J Environ Qual 35:734–741PubMedCrossRefGoogle Scholar
  92. Griffiths BS, Caul S, Thompson J, Birch ANE, Cortet J, Andersen MN, Krogh PH (2007a) Microbial and microfaunal community structure in cropping systems with genetically modified plants. Pedobiologia 51:195–206CrossRefGoogle Scholar
  93. Griffiths BS, Lars-Henrik H, Caul S, Thompson J, Scrimgeour C, Krogh PH (2007b) Varietal effects of eight paired lines of transgenic Bt maize and near-isogenic non-Bt maize on soil microbial and nematode community structure. Plant Biotechnol J 5:60–68PubMedCrossRefGoogle Scholar
  94. Gruber S, Colbach N, Barbottin A, Pekrun C (2008) Post-harvest gene escape and approaches for minimizing it. CAB Rev Perspect Agric Vet Sci Nutr Nat Res 3:1–17Google Scholar
  95. Hammond BC (2008) Food safety of proteins in agricultural biotechnology. CRC, Boca Raton, p 299 Google Scholar
  96. Harwood JD, Wallin WG, Obrycki JJ (2005) Uptake of Bt endotoxins by non target herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol Ecol 14:2815–2823PubMedCrossRefGoogle Scholar
  97. Harwood JD, Samson RA, Obrycki JJ (2007) Temporal detection of Cry1Ab-endotoxins in coccinellid predators from fields of Bacillus thuringiensis. Bull Entomol Res 97:643–648PubMedCrossRefGoogle Scholar
  98. Head G, Brown CR, Groth ME, Duan JJ (2001) Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Entomol Exp Appl 99:37–45CrossRefGoogle Scholar
  99. Head G, Surber JB, Watson JA, Martin JW, Duan JJ (2002) No detection of Cry1Ac protein in soil after multiple years of transgenic Bt cotton (Bollguard) use. Environ Entomol 31:30–36CrossRefGoogle Scholar
  100. Heckmann LH, Griffiths BS, Caul S, Thompson J, Pusztai-Carey M, Moar WJ, Andersen MN, Krogh PH (2006) Consequences for Protaphorura armata (Collembola: Onychiuridae) following exposure to genetically modified Bacillus thuringiensis (Bt) maize and non-Bt maize. Environ Pollut 142:212–216PubMedCrossRefGoogle Scholar
  101. Hellmich RL, Siegfried B, Sears MK, Stanley-Horn DE, Mattila HR, Spencer T, Bidne KG, Lewis LC (2001) Monarch larvae sensitivity to Bacillus thuringiensis purified proteins and pollen. Proc Natl Acad Sci USA 98:11925–11930PubMedCrossRefGoogle Scholar
  102. Herman RA, Evans SL, Shanahan DM, Mihaliak CA, Bormett GA, Yound DL, Buehrer J (2001) Rapid degradation of Cry1F delta-endotoxin in soil. Environ Entomol 30:642–644CrossRefGoogle Scholar
  103. Herman RA, Wolt JD, Halliday WR (2002) Rapid degradation of the Cry1F insecticidal crystal protein in soil. J Agric Food Chem 50:7076–7078PubMedCrossRefGoogle Scholar
  104. Hilbeck A, Baumgartner M, Fried PM, Bigler F (1998a) Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 27:480–487Google Scholar
  105. Hilbeck A, Moar WJ, Pusztai-Carey M, Filippini A, Bigler F (1998b) Toxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 27:1255–1263Google Scholar
  106. Hilbeck A, Moar WJ, Pusztai-Carey M, Filippini A, Bigler F (1999) Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea. Entomol Exp Appl 91:305–316CrossRefGoogle Scholar
  107. Hönemann L, Zurbrügg C, Nentwig W (2008) Effects of Bt-corn decomposition on the composition of soil meso- and macrofauna. Appl Soil Ecol 40:203–209CrossRefGoogle Scholar
  108. Hopkins DW, Gregorich EG (2003) Detection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize. Eur J Soil Sci 54:793–800CrossRefGoogle Scholar
  109. Hopkins DW, Gregorich EG (2005) Decomposition of transgenic (Bt) corn (Zea mays L.) residues in soil. Can J Soil Sci 85:19–26CrossRefGoogle Scholar
  110. Höss S, Arndt M, Baumgarte S, Tebbe CC, Nguyten HT, Jehle JA (2008) Effects of transgenic corn and Cry1Ab protein on the nematode, Caenorhabditis elegans. Ecotox Environ Saf 70:334–340CrossRefGoogle Scholar
  111. Huang F, Buschman LL, Higgins RA, Li H (2002) Survival of Kansas Dipel-resistant European corn borer (Lepidoptera: Crambidae) on Bt and non Bt corn hybrids. J Econ Entomol 95:614–621PubMedCrossRefGoogle Scholar
  112. Huang F, Rogers, Leonard B, Cook DR, Lee, DR, Andow DA, Baldwin JL, Tindall KV, Wu X (2007) Frequency of alleles conferring resistance to Bacillus thuringiensis maize in Louisiana populations of the southwestern corn borer. Entomol Exp Appl 122:53–58CrossRefGoogle Scholar
  113. Hubert J, Kudlíková-Křížková I, Stejskal V (2008) Effect of MON810 Bt transgenic maize diet on stored-product moths (Lepidoptera: Pyralidae). Crop Prot 27:489–496CrossRefGoogle Scholar
  114. Hunt TE, Higley LG, Witkowski JF, Young LJ, Hellmich RL (2001) Dispersal of adult European corn borer (Lepidoptera: Crambidae) within and proximal to irrigated and non-irrigated corn. J Econ Entomol 94:1369–1377CrossRefGoogle Scholar
  115. Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586CrossRefGoogle Scholar
  116. 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 37:647–662PubMedCrossRefGoogle Scholar
  117. Ives AR, Andow DA (2002) Evolution of resistance to Bt crops: directional selection in structured environments. Ecol Lett 5:792–801CrossRefGoogle Scholar
  118. Jesse LCH, Obrycki JJ (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125:241–248CrossRefGoogle Scholar
  119. Jesse LCH, Obrycki JJ (2003) Occurrence of Danaus plexippus L. (Lepidoptera: Danaidae) on milkweeds (Asclepias syriaca) in transgenic Bt corn agroecosystems. Agric Ecosyst Environ 97:225–233CrossRefGoogle Scholar
  120. Jepson PC, Croft BA, Pratt GE (1994) Test systems to determine the ecological risks by toxin release from Bacillus thuringiensis genes in crop plants. Mol Ecol 3:81–89CrossRefGoogle Scholar
  121. Krogh PH, Griffiths BS (2007) ECOGEN – soil ecological and economic evaluation of genetically modified crops. Pedobiologia 51:171–173CrossRefGoogle Scholar
  122. Krogh PH, Griffiths BS, Demsar D, Bohanec M, Debeljak M, Andersen MN, Sausse C, Birch ANE, Caul S, Holmstrup M, Heckmann LH, Cortet J (2007) Responses by earthworms to reduced tillage in herbicide tolerant maize and Bt maize cropping systems. Pedobiologia 51:219–227CrossRefGoogle Scholar
  123. Lang A (2004) Monitoring the impact of Bt maize on butterflies in the field: estimation of required sample sizes. Environ Biosaf Res 3:55–66CrossRefGoogle Scholar
  124. Lang A, Vojtech E (2006) The effects of pollen consumption on transgenic Bt maize on the common swallowtail, Papilio machaon L. (Lepidoptera, Papilionidae). Basic Appl Ecol 7:296–306CrossRefGoogle Scholar
  125. Lang A, Ludy C, Vojtech E (2004) Dispersion and deposition of Bt maize pollen in field margins. Z Pflanzenkr Pflanzenschutz 111:417–428Google Scholar
  126. Lehman RM, Osborne SL, Rosentrater KA (2008) No differences in decomposition rates observed between Bacillus thuringiensis and non-Bacillus thuringiensis corn residue incubated soil in the field. Agron J 100:163–168CrossRefGoogle Scholar
  127. 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 3:1–8 (e2909)Google Scholar
  128. Lilley AK, Bailey MJ, Cartwright C, Turner SL, Hirsch PR (2006) Life in earth: the impact of GM plants on soil ecology? Trends Biotechnol 24:9–14PubMedCrossRefGoogle Scholar
  129. Losey JE, Rayor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399:214PubMedCrossRefGoogle Scholar
  130. Lövei GL, Arpaia S (2005) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomol Exp Appl 114:1–14CrossRefGoogle Scholar
  131. Ludy C, Lang A (2006a) A 3-year field-scale monitoring of foliage-dwelling spiders (Araneae) in transgenic Bt maize fields and adjacent field margins. Biol Control 38:314–324CrossRefGoogle Scholar
  132. Ludy C, Lang A (2006b) Bt maize pollen exposure and impact on the garden spired, Araneus diadematus. Entomol Exp Appl 118:145–156CrossRefGoogle Scholar
  133. Lumbierres B, Albajes R, Pons X (2004) Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance. Ecol Entomol 29:309–317CrossRefGoogle Scholar
  134. Lutz B, Wiedemann S, Albrecht C (2006) Degradation of transgenic Cry1Ab DNA and protein in Bt-176 maize during the ensiling process. J Anim Physiol Anim Nutr 90:116–123CrossRefGoogle Scholar
  135. Malone LA (2004) Potential effects of GM crops on honey bee health. Bee World 85:29–36Google Scholar
  136. Malone LA, Pham-Delègue MH (2001) Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.). Apidology 32:287–304CrossRefGoogle Scholar
  137. Marchetti E, Accinelli C, Talamè V, Epifani R (2007) Persistence of Cry toxins and cry genes from genetically modified plants in two agricultural soils. Agron Sustain Dev 27:231–236CrossRefGoogle Scholar
  138. Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–1477PubMedCrossRefGoogle Scholar
  139. Meissle M, Vojtech E, Poppy GM (2005) Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae). Transgenic Res 14:123–132PubMedCrossRefGoogle Scholar
  140. Melé E, Peñas G, Palaudelmàs M, Serra J, Salvia J, Pla M, Nadal A, Messeguer J, (2007) Effect of volunteers on maize gene flow. In: Stein A, Rodríguez-Cerezo E (eds) Book of abstracts, third international conference on the coexistence between genetically modified (GM) and non-GM-based agriculural supply chains. European Commission, Brussels, pp 249–250Google Scholar
  141. Mendelsohn M, Kough J, Vaituzis Z, Matthews K (2003) Are Bt crops safe? Nat Biotechnol 21:1003–1009PubMedCrossRefGoogle Scholar
  142. Moar W, Roush R, Shelton A, Ferré J, MacIntosh S, Leonard BR, Abel C (2008) Field-evolved resistance to Bt toxins. Nat Biotechnol 26:1072–1074PubMedCrossRefGoogle Scholar
  143. Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238CrossRefGoogle Scholar
  144. Mulder C, Wouterse M, Raubuch M, Roelofs W, Rutgers M (2006) Can transgenic maize affect soil microbial communities? PLoS Comput Biol 2:1165–1172 (e128)CrossRefGoogle Scholar
  145. Oberhauser KS, Rivers ERL (2003) Monarch butterfly (Danaus plexippus) larvae and Bt maize pollen: a review of ecological risk assessment for non-target species. AgBiotechNet 5:1–7Google Scholar
  146. Oberhauser KS, Prysby M, Mattila HR Stanley-Horn DE, Sears MK, Dively GP, Olson E, Pleasants JM, Lam WKF, Hellmich RL (2001) Temporal and spatial overlap between monarch larvae and corn pollen. Proc Natl Acad Sci USA 98:11913–11918PubMedCrossRefGoogle Scholar
  147. Obrist LB, Dutton A, Albajes R, Bigler F (2006a) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31:143–154CrossRefGoogle Scholar
  148. Obrist LB, Dutton A, Romeis J, Bigler F (2006b) Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea. BioControl 51:31–48CrossRefGoogle Scholar
  149. Obrist LB, Dutton A, Romeis J, Bigler F (2006c) Fate of Cry1Ab toxin expressed by Bt maize upon ingestion by herbivorous arthropods and consequences for Chrysoperla carnea. BioControl 51:31–48CrossRefGoogle Scholar
  150. OECD (2003) Consensus document on the biology of Zea mays subsp. mays (maize). Series on harmonisation of regulatory oversight in biotechnology. OECD, ParisGoogle Scholar
  151. OECD (2007) Consensus document on safety information on transgenic plants expressing Bacillus thuringiensis-derived insect control proteins. Series on Harmonisation of Regulatory Oversight in Biotechnology. OECD, ParisGoogle Scholar
  152. Palaudelmas M, Penas G, Mele E, Serra J, Salvia J, Pla M, Nadal A, Messeguer J (2009) Effect of volunteers on maize gene flow. Trans Res. doi 10.1007/s11248-009-9250-7Google Scholar
  153. Parrot W (2008) Study of Bt impact on caddisflies overstates its conclusions: response to Rosi-Marshall et al. Proc Natl Acad Sci USA 105:E10CrossRefGoogle Scholar
  154. Pigott CR, Ellar DJ (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71:255–281PubMedCrossRefGoogle Scholar
  155. Pineyro-Nelson A, Van Heerwaarden J, Perales HR, Serratos-Hernandez JA, Rangel A, Hufford MB, Gepts P, Garay-Arroyo A, Rivera-Bustamante R, Alvarez-Buylla ER (2008) Transgenes in Mexican maize: molecular evidence and methodological considerations for GMO detection in landrace populations. Mol Ecol 18:750–761PubMedCrossRefGoogle Scholar
  156. 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. Proc Natl Acad Sci USA 98:11919–11924PubMedCrossRefGoogle Scholar
  157. Pons X, Lumbierres B, Lopez C, Albajes R (2005) Abundance of non-target pests in transgenic Bt-maize: A farm scale study. Eur J Entomol 102:73–79Google Scholar
  158. Pont B, Nentwig W (2005) Quantification of Bt-protein digestion and excretion by the primary decomposer Porcellio scaber, fed with two Bt corn varieties. Biocontrol Sci Technol 15:341–352CrossRefGoogle Scholar
  159. Poppy GM (2000) GM crops: environmental risks and non-target effects. Trends Plant Sci 5:4–6PubMedCrossRefGoogle Scholar
  160. Prasifka PL, Hellmich RL, Prasifka JR, Lewis LC (2007) Effects of Cry1Ab-expressing corn anthers on the movement of monarch butterfly larvae. Environ Entomol 36:228–233PubMedCrossRefGoogle Scholar
  161. Qureshi JA, Buschman LL, Throne JE, Ramaswamy SB (2005) Adult dispersal of Ostrinia nubilalis Hübner (Lepidoptera: Crambidae) and its implications for resistance management in Bt-maize. J Appl Entomol 129:281–292CrossRefGoogle Scholar
  162. Ramirez-Romero R, Chaufaux J, Pham-Delègue MH (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidology 36:601–611CrossRefGoogle Scholar
  163. Ramirez-Romero R, Bernal JS, Chaufaux J, Kaiser L (2007) Impact assessment of Bt-maize on a moth parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae), via host exposure to purified Cry1Ab protein or Bt-plants. Crop Prot 26:953–962CrossRefGoogle Scholar
  164. Ramirez-Romero R, Desneux N, Decourtye A, Chaffiol A, Pham-Delègue MH (2008) Does Cry1Ab protein affect learning performances of the honey bee Apis mellifera L. (Hymenoptera, Apidae). Ecotox Environ Saf 70:327–333CrossRefGoogle Scholar
  165. Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry 1Ab. Mol Ecol 10:525–533PubMedCrossRefGoogle Scholar
  166. Raubuch M, Roose K, Warnstorff K, Wichern F, Joergensen RG (2007) Respiration pattern and microbial use of field-grown transgenic Bt-maize residues. Soil Biol Biochem 39:2380–2389CrossRefGoogle Scholar
  167. Rausell C, Garcia-Robles I, Sanchez J, Munoz-Garay C, Martniez-Ramirez AC, Real MD, Bravo A (2004) Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata (Say). Biochim Biophys Acta Biomembr 1660:99–105CrossRefGoogle Scholar
  168. Rodrigo-Simón A, de Maagd RA, Avilla C, Bakker PL, Molthoff J, González-Zamora JE, Ferré J (2006) Lack of detrimental effects of Bacillus thuringiensis Cry toxins on the insect predator Chrysoperla carnea: a toxicological, histopathological, and biochemical analysis. Appl Environ Microbiol 72:1595–1603PubMedCrossRefGoogle Scholar
  169. Romeis J, Dutton A, Bigler F (2004) Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewind Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). J Insect Physiol 50:175–183PubMedCrossRefGoogle Scholar
  170. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71PubMedCrossRefGoogle Scholar
  171. 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 (2008a) Nontarget arthropod risk assessment of insect-resistant GM crops. Nat Biotechnol 26:203–208PubMedCrossRefGoogle Scholar
  172. Romeis J, Van Driesche RG, Barratt BIP, Bigler F (2008b) Insect-resistant transgenic crops and biological control. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer Science + Business Media, Dordrecht, pp 87–117CrossRefGoogle Scholar
  173. Rose R, Dively GP, Pettis J (2007) Effects of Bt corn pollen on honey bees: emphasis on protocol development. Apidology 38:368–377CrossRefGoogle Scholar
  174. 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 104:16204–16208PubMedCrossRefGoogle Scholar
  175. Saeglitz C, Bartsch D, Eber S, Gathmann A, Priesnitz KU, Schupman I (2006) Monitoring the Cry1Ab susceptibility of European corn borer in Germany. J Econ Entomol 99:1768–1773PubMedCrossRefGoogle Scholar
  176. Sanvido O, Widmer F, Winzeler M, Bigler F (2005) A conceptual framework for the design of environmental post-market monitoring of genetically modified plants. Environ Biosaf Res 4:13–27CrossRefGoogle Scholar
  177. Sanvido O, Romeis J, Bigler F (2007) Ecological impacts of genetically modified crops: ten years of field research and commercial cultivation. Adv Biochem Eng Biotechnol 107:235–278PubMedGoogle Scholar
  178. Saxena D, Stotzky G (2001a) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol Biochem 33:1225–1230CrossRefGoogle Scholar
  179. Saxena D, Stotzky G (2001b) Bt corn has a higher lignin content than non-Bt corn. Am J Bot 88:1704–1706PubMedCrossRefGoogle Scholar
  180. Saxena D, Stotzky G (2002) Bt toxin is not taken up from soil or hydroponic culture by corn, carrot, radish, or turnip. Plant Soil 239:165–172CrossRefGoogle Scholar
  181. Saxena D, Flores S, Stotzky G (2002) Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biol Biochem 34:133–137CrossRefGoogle Scholar
  182. Saxena D, Stewart CN, Altosaar I, Shu Q, Stotzky G (2004) Larvicidal Cry proteins from Bacillus thuringiensis are released in root exudates of transgenic B. thuringiensis corn, potato, and rice but not of B. thuringiensis canola, cotton, and tobacco. Plant Physiol Biochem 42:383–387PubMedCrossRefGoogle Scholar
  183. Schmidt K, Wilhelm R, Schmidtke J, Beißner L, Mönkemeyer W, Böttinger P, Sweet J, Schiemann J (2008) Farm questionnaires for monitoring genetically modified crops: a case study using GM maize. Environ Biosaf Res 7:163–179CrossRefGoogle Scholar
  184. Schmitz G, Pretscher P, Bartsch D (2003) Selection of relevant non-target herbivores for monitoring the environmental effects of Bt maize pollen. Environ Biosaf Res 2:117–132CrossRefGoogle Scholar
  185. Schorling M, Freier B (2006) Six-year monitoring of non-target arthropods in Bt maize (Cry 1Ab) in the European corn borer (Ostrinia nubilalis) infestation area Oderbruch (Germany). J Consumer Prot Food Saf 1(S1):106–108Google Scholar
  186. Schrader S, Münchenberg T, Baumgarte S, Tebbe CC (2008) Earthworms of different functional groups affect the fate of the Bt-toxin Cry1Ab from transgenic maize in soil. Eur J Soil Biol 44:283–289CrossRefGoogle Scholar
  187. Schuphan I (2006) Protecting the benefits of Bt-toxins from insect resistance development by monitoring and management. RWTH Aachen http://www.bio5.rwth-aachen.de/german/downloads/EU-Review.pdf. Accessed on 21 Jan 2009
  188. Sears MK, Hellmich RL, Siegfried BD, Pleasants JM, Stanley-Horn DE, Oberhauser KS, Dively GP (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc Natl Acad Sci USA 98:11937–11942PubMedCrossRefGoogle Scholar
  189. Sims SR, Holden LR (1996) Insect bioassay for determining soil degradation of Bacillus thuringiensis subsp. kurstaki CryIA(b) protein in corn tissues. Environ Entomol 25:659–664Google Scholar
  190. Snow A (2009) Unwanted transgenes re-discovered in Oaxacan maize. Mol Ecol 18:569–571PubMedCrossRefGoogle Scholar
  191. Stanley-Horn DE, Dively GP, Hellmich RL, Mattila HR, Sears MK, Rose R, Jesse LCH, Losey JE, Obrycki JJ, Lewis LC (2001) Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. Proc Natl Acad Sci USA 98:11931–11936PubMedCrossRefGoogle Scholar
  192. Stodola TJ, Andow DA, Hyden AR, Hinton JL, Roark JJ, Buschman LL, Porter P, Cronholm GB (2006) Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in southern United States corn belt population of European corn borer (Lepidoptera: Crambidae). J Econ Entomol 99:502–507PubMedCrossRefGoogle Scholar
  193. Stotzky G (2004) Persistence and biological activity in soil of the insecticidal proteins from Bacillus thuringiensis, especially from transgenic plants. Plant Soil 266:77–89CrossRefGoogle Scholar
  194. Tabashnik BE (2008) Delaying insect resistance to transgenic crops. Proc Natl Acad Sci USA 105:19029–19030PubMedCrossRefGoogle Scholar
  195. Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y (2008a) Insect resistance to Bt crops: evidence versus theory? Nat Biotechnol 26:199–202PubMedCrossRefGoogle Scholar
  196. Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y (2008b) Reply to field-evolved resistance to Bt toxins. Nat Biotechnol 26:1074–1076CrossRefGoogle Scholar
  197. Tapp H, Stotzky G (1995) Insecticidal activity of the toxins from Bacillus thuringiensis subspecies kurstaki and tenebrionis adsorbed and bound on pure and soil clay. Appl Environ Microbiol 61:1786–1790PubMedGoogle Scholar
  198. Tapp H, Stotzky G (1998) Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biol Biochem 30:471–476CrossRefGoogle Scholar
  199. Tapp H, Calamai L, Stotzky G (1994) Adsorption and binding of the insecticidal proteins from Bacillus thuringiensis subsp. kurstaki and subsp. tenebrionis on clay minerals. Soil Biol Biochem 26:663–679CrossRefGoogle Scholar
  200. Tarkalson DD, Kachman SD, Knops JMN, Thies JE, Wortmann CS (2008) Decomposition of Bt and non-Bt corn hybrid residues in the field. Nutr Cyc Agroecosyst 80:211–222CrossRefGoogle Scholar
  201. Toschki A, Hothorn LA, Roß-Nickoll M (2007) Effects of cultivation of genetically modified Bt maize on epigeic arthropods (Araneae; Carabidae). Environ Entomol 36:967–981PubMedCrossRefGoogle Scholar
  202. Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovanetti M (2004) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266:69–75CrossRefGoogle Scholar
  203. Tyutyunov Y, Zhadanovskaya E, Bourguet D, Arditi R (2008) Landscape refuges delay resistance of the European corn borer to Bt-maize: a demo-genetic dynamic model. Theor Pop Biol 74:138–146CrossRefGoogle Scholar
  204. Van Rensburg JBJ (2007) First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. South African J. Plant Soil 24:147–151Google Scholar
  205. Vercesi ML, Krogh PH, Holmstrup M (2006) Can Bacillus thuringiensis (Bt) corn residues and Bt-corn plants affect life-history traits in the earthworm Aporrectodea caliginosa? Appl Soil Ecol 32:180–187CrossRefGoogle Scholar
  206. Vojtech E, Meissle M, Poppy GM (2005) Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). Transgenic Res 14:133–144PubMedCrossRefGoogle Scholar
  207. Wandeler H, Bahylova J, Nentwig W (2002) Consumption of two Bt and six non-Bt corn varieties by the woodlouse Porcellio scaber. Basic Appl Ecol 3:357–365CrossRefGoogle Scholar
  208. Wang H, Ye Q, Wang W, Wu L, Wu W (2006) Cry1Ab protein from Bt transgenic rice does not residue in rhizosphere soil. Environ Pollut 143:449–455PubMedCrossRefGoogle Scholar
  209. Whalon ME, Mota-Sanchez D, Hollingworth RM, Duynslager L (2008) Arthropod pesticide resistance database. Michigan State University, 2004–2008. http://www.pesticideresistance.org. Accessed on 21 Jan 2009
  210. Widmer F (2007) Assessing effects of transgenic crops on soil microbial communities. Adv Biochem Eng Biotechnol 107:207–234PubMedGoogle Scholar
  211. Wilkinson MJ, Sweet J, Poppy GM (2003) Risk assessment of GM plants: avoiding gridlock? Trends Plant Sci 8:208–212PubMedCrossRefGoogle Scholar
  212. 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 3:1–11 (e2118)CrossRefGoogle Scholar
  213. Wolt JD, Peterson RKD, Bystrak P, Maede T (2003) A screening level approach for nontarget insect risk assessment: transgenic Bt corn pollen and the monarch butterfly (Lepidoptera: Danaidae). Environ Entomol 32:237–246CrossRefGoogle Scholar
  214. Zangerl AR, McKenna D, Wraight CL, Carroll M, Ficarello P, Warner R, Berenbaum MR (2001) Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. Proc Natl Acad Sci USA 98:11908–11912PubMedCrossRefGoogle Scholar
  215. Zwahlen C, Hilbeck A, Gugerli P, Nentwig W (2003a) Degradation of the Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Mol Ecol 12:765–775PubMedCrossRefGoogle Scholar
  216. Zwahlen C, Hilbeck A, Howald R, Nentwig W (2003b) Effects of transgenic Bt corn litter on earthworm Lumbricus terrestris. Mol Ecol 12:1077–1086PubMedCrossRefGoogle Scholar
  217. Zwahlen C, Hilbeck A, Nentwig W (2007) Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates. Plant Soil 300:245–257CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Detlef Bartsch
    • 1
    Email author
  • Yann Devos
    • 2
  • Rosie Hails
    • 3
  • Jozsef Kiss
    • 4
  • Paul Henning Krogh
    • 5
  • Sylvie Mestdagh
    • 2
  • Marco Nuti
    • 6
  • Angela Sessitsch
    • 7
  • Jeremy Sweet
    • 8
  • Achim Gathmann
    • 1
  1. 1.Bundesamt für Verbraucherschutz und Lebensmittelsicherheit (BVL)BerlinGermany
  2. 2.European Food Safety Authority (EFSA), GMO UnitParmaItaly
  3. 3.Centre for Ecology and HydrologyOxfordUnited Kingdom
  4. 4.Plant Protection Institute, Szent Istvan UniversityGödöllöHungary
  5. 5.National Environmental Research Institute, University of AarhusSilkeborgDenmark
  6. 6.Department of Crop BiologyFaculty of Agriculture, University of PisaPisaItaly
  7. 7.AIT Austrian Institute of Technology GmbHViennaAustria
  8. 8.Environmental ConsultantCambridgeUnited Kingdom

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