Plant and Soil

, Volume 300, Issue 1–2, pp 245–257 | Cite as

Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates

  • C. ZwahlenEmail author
  • A. Hilbeck
  • W. Nentwig
Regular Article


Genetically modified Bacillus thuringiensis Berliner (Bt) maize (Zea mays L.) expressing Cry toxins against various target pests is now grown on more than 16 million hectares worldwide, but its potential effects on the soil ecosystem need to be further investigated. In an 8-month field study, we investigated the effects of Bt maize expressing the Cry1Ab protein on both the soil community and maize residue decomposition. We used litterbags with three different mesh sizes (20, 125, and 5,000 μm) to investigate potential effects of different soil organism groups on the decomposition processes. Litterbags were incorporated into the soil in fall into a field that had previously been planted with non-Bt maize and subsamples were removed monthly. The dry weight of the remaining residue was measured for all bags. Bt and non-Bt maize decomposed similarly in large mesh bags, which allowed the whole soil organism community to enter and interact with each other. In contrast, Bt maize decomposed significantly faster than non-Bt maize at some sample dates in winter in bags with small and medium mesh sizes. At the end of the experiment in late spring, however, there was no significant difference in the amount of maize plant residues remaining for any of these three mesh sizes. Additionally, soil organisms from bags with the largest mesh size were identified. The most frequent taxa extracted were collembolans (Isotomidae, Tullbergiidae, Entomobryidae), mites (Gamasina, Oribatida), and annelids (Enchytraeidae). Three of these taxa were extracted in higher numbers from non-Bt than Bt residue (Tullbergiidae, Gamasina, Enchytraeidae), while there was no difference in the number of individuals extracted for the remaining three taxa. Our results do not show major changes in the decomposition of Bt maize residue and in the composition of the soil organism community. However, further studies are needed that assess the impact of the continuous release of Cry1Ab via root exudates and plant biomass on the soil ecosystem.


Transgenic Bt corn Decomposition process Risk assessment Collembola Acarina Annelida 



We would like to thank R. Howald (University of Bern, Switzerland) and K. Barmettler (ETH Zurich, Switzerland) for technical assistance and K. Jost for providing the field. We are grateful to D.A. Andow (University of Minnesota, USA), R. Liesch, H.-R. Roth (ETH Zurich), J.-P. Airoldi, and H. Wandeler (University of Bern), J. Zimmerman (University of Minnesota), S. Kenyon (University of Neuchâtel) and two anonymous reviewers for helpful discussions, advice in statistics, and comments on earlier versions of this manuscript. Many thanks to J. Zettel (University of Bern) for help in the identification of the soil organisms.


  1. Addison JA (1993) Persistence and nontarget effects of Bacillus thuringiensis in soil: a review. Can J For Res 23:2329–2342CrossRefGoogle Scholar
  2. Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecol Lett 9:196–214PubMedCrossRefGoogle Scholar
  3. Atlavinyté O, Galvelis A, Dačiulyté J, Lugauskas A (1982) Effects of entobacterin on earthworm activity. Pedobiologia 23:372–379Google Scholar
  4. Baumgarte S, Tebbe C (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on eubacterial communities in the maize rhizosphere. Mol Ecol 14:2539–2551PubMedCrossRefGoogle Scholar
  5. Bitzer RJ, Rice ME, Pilcher CD, Pilcher CL, Frankie Lam WK (2005) Biodiversity and community structure of epedaphic and euedaphic springtails (Collembola) in transgenic rootworm Bt corn. Environ Entomol 34:1346–1376CrossRefGoogle Scholar
  6. 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
  7. Bottjer KP, Bone LW, Gill SS (1985) Nematoda: Susceptibility of the egg to Bacillus thuringiensis toxins. Exp Parasitol 60:239–244PubMedCrossRefGoogle Scholar
  8. Bradford MA, Tordoff GM, Eggers T, Jones TH, Newington JE (2002) Microbiota, fauna, and mesh size interactions in litter decomposition. Oikos 99:317–323CrossRefGoogle Scholar
  9. Castaldini M, Turrini A, Sbrana C, Benedetti A, Marchionni M, Mocali S, Fabiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovannetti 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
  10. Chapman M, Hoy MA (1991) Relative toxicity of Bacillus thuringiensis var. tenebrionis on the two-spotted spider mite (Tetranychus urticae Koch) and its predator Metaseiulus occidentalis (Nesbitt) (Acari, Tetranychidae and Phytoseiidae). J Appl Entomol 111:147–154CrossRefGoogle Scholar
  11. Clark BW, Coats JR (2006) Subacute effects of transgenic Cry1Ab Bt corn litter on the earthworm Eisenia fetida and the springtail Folsomia candida. Environ Entomol 35:1121–1129CrossRefGoogle Scholar
  12. 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 Toxicol Chem 25:2653–2661PubMedCrossRefGoogle Scholar
  13. DeLucca AJ, Simonson JG, Larson AD (1981) Bacillus thuringiensis distribution in soils of the United States. Can J Microbiol 28:452–456Google Scholar
  14. De Ruiter PC, Neutel AM, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260PubMedCrossRefGoogle Scholar
  15. Didden WAM (1993) Ecology of terrestrial Enchytraeidae. Pedobiologia 37:2–29Google Scholar
  16. 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
  17. Escher N, Käch B, Nentwig W (2000) Decomposition of transgenic Bacillus thuringiensis maize by microorganisms and woodlice Porcellio scaber. Basic Appl Ecol 1:161–169CrossRefGoogle Scholar
  18. Fearing PL, Brown D, Vlachos D, Meghji M, Privalle L (1997) Quantitative analysis of Cry1A(b) expression in Bt maize plants, tissues, and silage and stability of expression over successive generations. Mol Breed 3:169–176CrossRefGoogle Scholar
  19. Fierer N, Craine JM, McLauchlan K, Schimel JP (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326CrossRefGoogle Scholar
  20. 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
  21. Gisi U, Schenker R, Schulin R, Stadelmann FX, Sticher H (1997) Bodenökologie. Thieme, Stuttgart, p 350Google Scholar
  22. Griffiths BS, Caul S, Thompson J, Birch ANE, Scrimgeour C, Andersen MN, Cortet J, Messéan 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
  23. Griffiths BS, Heckmann LH, Caul S, Thompson J, Scrimgeour C, Krogh PH (2007) 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
  24. Heal OW, Anderson JM, Swift MJ (1997) Plant litter quality and decomposition: an historical overview. In: Cadisch G, Giller KE (eds) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, pp 3–29Google Scholar
  25. 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
  26. Hedlund K, Öhrn MS (2000) Tritrophic interactions in a soil community enhance decomposition rates. Oikos 88:585–591CrossRefGoogle Scholar
  27. Hendrix PF, Parmelee RW, Crossley DA, Coleman DC, Odum EP, Groffman PM (1986) Detritus food webs in conventional and no-tillage agroecosystems. BioScience 36:374–380CrossRefGoogle Scholar
  28. 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
  29. House GJ, Stinner RE (1987) Decomposition of plant residues in no-tillage agroecosystems: Influence of litterbag mesh size and soil arthropods. Pedobiologia 30:351–360Google Scholar
  30. James RR, Difazio SP, Brunner AM, Strauss SH (1998) Environmental effects of genetically engineered woody biomass crops. Biomass Bioenergy 14:403–414CrossRefGoogle Scholar
  31. Jung HG, Scheaffer CC (2004) Influence of Bt transgenes on cell wall lignification and digestibility of maize stover for silage. Crop Sci 44:1781–1789CrossRefGoogle Scholar
  32. Koehler HH (1999) Predatory mites (Gamasina, Mesostigmata). Agric Ecosyst Environ 74:395–410CrossRefGoogle Scholar
  33. Laakso J, Setälä H (1999) Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87:57–64CrossRefGoogle Scholar
  34. Lachnicht SL, Hendrix PF, Potter RL, Coleman DC, Crossley Jr D (2004) Winter decomposition of transgenic cotton residue in conventional-till and no-till systems. Appl Soil Ecol 27:135–142CrossRefGoogle Scholar
  35. MacFadyen A (1961) Improved funnel-type extractors for soil arthropods. J Anim Ecol 30:171–184CrossRefGoogle Scholar
  36. MacFadyen A (1962) Soil arthropod sampling. Adv Ecol Res 1:1–34CrossRefGoogle Scholar
  37. Martin PAW, Travers S (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl Environ Microbiol 55:2437–2442PubMedGoogle Scholar
  38. Masoero F, Moschini M, Rossi F, Prantini A, Pietri A (1999) Nutritive value, mycotoxin contamination and in-vitro rumen fermentation of normal and genetically modified corn (Cry1Ab) grown in northern Italy. Maydica 44:205–209Google Scholar
  39. Meadows J, Gill SS, Bone LW (1990) Bacillus thuringiensis strains affect population growth of the free-living nematode Turbatrix aceti. Invertebr Reprod Dev 17:73–76Google Scholar
  40. 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
  41. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  42. Moore JC, Walter DE, Hunt HW (1988) Arthropod regulation of microbiota and mesobiota in belowground detrital food webs. Annu Rev Entomol 33:419–439Google Scholar
  43. Mungai NW, Motavalli PP, Nelson KA, Kremer RJ (2005) Differences in yields, residue composition and N mineralization dynamics of Bt and non-Bt maize. Nutr Cycl Agroecosyst 71:101–109CrossRefGoogle Scholar
  44. Oatman ER (1965) The effect of Bacillus thuringiensis on some lepidopterous larval pests, apple aphid and predators, and on phytophagous and predaceous mites on young apple trees. J Econ Entomol 58:1144–1147Google Scholar
  45. Ohba M, Aizawa K (1986) Distribution of Bacillus thuringiensis in soils of Japan. J Invertebr Pathol 47:277–282CrossRefGoogle Scholar
  46. Poerschmann J, Gathmann A, Augustin J, Langer U, Górecki T (2005) Molecular composition of leaves and stems of genetically modified Bt and near-isogenic non-Bt maize – characterization of lignin patterns. J Environ Qual 34:1508–1518PubMedCrossRefGoogle Scholar
  47. 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
  48. SAS Institute Inc (2004) SAS/STAT® 9.1. SAS Institute Inc., Cary, NCGoogle Scholar
  49. SAS Institute Inc (2006) The GLIMMIX procedure. SAS Institute Inc. Available from: +Software
  50. Saxena D, Stotzky G (2000) Insecticidal toxin from Bacillus thuringiensis is released from roots of transgenic Bt corn in vitro and in situ. FEMS Microbiol Ecol 33:35–39PubMedCrossRefGoogle Scholar
  51. 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
  52. Saxena D, Stotzky G (2001b) Bt toxin uptake from soil by plants. Nat Biotechnol 19:199PubMedCrossRefGoogle Scholar
  53. Saxena D, Stotzky G (2001c) Bt corn has a higher lignin content than non-Bt corn. Am J Bot 88:1704–1706CrossRefGoogle Scholar
  54. Saxena D, Stotzky G (2003) Fate and effects in soil of insecticidal toxins from Bacillus thuringiensis in transgenic plants. In Collection of biosafety reviews, vol. 1. International Centre for Genetic Engineering and Biotechnology, Trieste, pp 7–83Google Scholar
  55. Saxena D, Flores S, Stotzky G (1999) Insecticidal toxin in root exudates from Bt corn. Nature 402:480PubMedGoogle Scholar
  56. Saxena D, Flores S, Stotzky G (2002) Vertical movement in soil of insecticidal Cry1Ab protein from Bacillus thuringiensis. Soil Biol Biochem 34:111–120CrossRefGoogle Scholar
  57. Scheffer F, Schachtschabel P (1989) Lehrbuch der Bodenkunde. Enke, Stuttgart, p 491Google Scholar
  58. Sims SR, Martin JW (1997) Effect of the Bacillus thuringiensis insecticidal proteins CryIA(b), CryIIA, and CryIIIA on Folsomia candida and Xenylla grisea (Insecta: Collembola). Pedobiologia 41:412–416Google Scholar
  59. Smirnoff WA, Heimpel AM (1961) Notes on the pathogenicity of Bacillus thuringiensis var. thuringiensis Berliner for the earthworm, Lumbricus terrestris Linnaeus. J Insect Pathol 3:403–408Google Scholar
  60. Smith RA, Couché GA (1991) The phylloplane as a source of Bacillus thuringiensis variants. Appl Environ Microbiol 57:311–331PubMedGoogle Scholar
  61. Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70:97–104CrossRefGoogle Scholar
  62. Turlings TCJ, Jeanbourquin PM, Held M, Degen T (2005) Evaluating the induced-odour emission of a Bt maize and its attractiveness to parasitic wasps. Transgenic Res 14:807–816PubMedCrossRefGoogle Scholar
  63. US Environmental Protection Agency (US-EPA) (1997) Pesticide fact sheet. Bacillus thuringiensis CryIA(b) delta-endotoxin and the genetic material necessary for its production (plasmid vector pZ01502) in corn. Office of Prevention, Pesticides and Toxic Substances (7501C)Google Scholar
  64. US Environmental Protection Agency (US-EPA) (2001) Biopesticides registration action document - Bacillus thuringiensis plant-incorporated protectants. 16 October 2001. [online] URL:
  65. 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
  66. Vreeken-Buijs MJ, Brussaard L (1996) Soil mesofauna dynamics, wheat residue decomposition and nitrogen mineralization in buried litterbags. Biol Fert Soils 23:374–381CrossRefGoogle Scholar
  67. 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
  68. Yu L, Berry RE, Croft BA (1997) Effects of Bacillus thuringiensis toxins in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Oribatidae). J Econ Entomol 90:113–118Google Scholar
  69. Zettel J (1999) Blick in die Unterwelt. Ein illustrierter Bestimmungsschlüssel zur Bodenfauna. Agrarökologie, Bern, p 110Google Scholar
  70. Zscheischler J, Estler MC, Staudacher W, Gross F, Burgstaller G (1984) Handbuch Mais. Anbau – Verwertung – Fütterung. Verlagsunion Agrar, Frankfurt am Main, p 253Google Scholar
  71. Zwahlen C, Andow DA (2005) Field evidence for the exposure of ground beetles to Cry1Ab from transgenic corn. Environ Biosafety Res 4:113–117PubMedCrossRefGoogle Scholar
  72. Zwahlen C, Hilbeck A, Gugerli P, Nentwig W (2003a) Degradation of Cry1Ab protein within transgenic Bacillus thuringiensis corn tissue in the field. Mol Ecol 12:765–775PubMedCrossRefGoogle Scholar
  73. Zwahlen C, Hilbeck A, Howald R, Nentwig W (2003b) Effects of transgenic Bt corn litter on the earthworm Lumbricus terrestris. Mol Ecol 12:1077–1086PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland
  2. 2.Zoological InstituteUniversity of BernBernSwitzerland
  3. 3.Institute of Integrative BiologyETH ZurichZurichSwitzerland

Personalised recommendations