Transgenic Research

, Volume 25, Issue 6, pp 761–772 | Cite as

Effects of transgenic cry1Ie maize on non-lepidopteran pest abundance, diversity and community composition

  • Jingfei Guo
  • Kanglai He
  • Shuxiong Bai
  • Tiantao Zhang
  • Yunjun Liu
  • Fuxin Wang
  • Zhenying Wang
Original Paper


Non-lepidopteran pests are exposed to, and may be influenced by, Bt toxins when feeding on Bt maize that express insecticidal Cry proteins derived from Bacillus thuringiensis (Bt). In order to assess the potential effects of transgenic cry1Ie maize on non-lepidopteran pest species and ecological communities, a 2-year field study was conducted to compare the non-lepidopteran pest abundance, diversity and community composition between transgenic cry1Ie maize (Event IE09S034, Bt maize) and its near isoline (Zong 31, non-Bt maize) by whole plant inspections. Results showed that Bt maize had no effects on non-lepidopteran pest abundance and diversity (Shannon–Wiener diversity index, Simpson’s diversity index, species richness, and Pielou’s index). There was a significant effect of year and sampling time on those indices analyzed. Redundancy analysis indicated maize type, sampling time and year totally explained 20.43 % of the variance in the non-lepidopteran pest community composition, but no association was presented between maize type (Bt maize and non-Bt maize) and the variance. Nonmetric multidimensional scaling analysis showed that sampling time and year, rather than maize type had close relationship with the non-lepidopteran pest community composition. These results corroborated the hypothesis that, at least in the short-term, the transgenic cry1Ie maize had negligible effects on the non-lepidopteran pest abundance, diversity and community composition.


Transgenic cry1Ie maize Non-lepidopteran pest Abundance Diversity Community composition 

Supplementary material

11248_2016_9968_MOESM1_ESM.doc (130 kb)
Supplementary material 1 (DOC 130 kb)


  1. Afidchao MM, Musters CJM, de Snoo GR (2013) Asian corn borer (ACB) and non-ACB pests in GM corn (Zea mays L.) in the Philippines. Pest Manag Sci 69:792–801CrossRefPubMedGoogle Scholar
  2. Balog A, Kiss J, Szekeres D, Szénási Á, Markó V (2010) Rove beetle (Coleoptera: Staphylinidae) communities in transgenic Bt (MON810) and near isogenic maize. Crop Prot 29:567–571CrossRefGoogle Scholar
  3. Bernal CC, Aguda RM, Cohen MB (2002) Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis. Entomol Exp Appl 102:21–28CrossRefGoogle Scholar
  4. Bourguet D et al (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
  5. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  6. Burgio G, Lanzoni A, Accinelli G, Dinelli G, Bonetti A, Marotti I, Ramilli F (2007) Evaluation of Bt-toxin uptake by the non-target herbivore, Myzus persicae (Hemiptera: Aphididae), feeding on transgenic oilseed rape. Bull Entomol Res 97:211–215CrossRefPubMedGoogle Scholar
  7. Chen M et al (2007) Impacts of transgenic cry1Ab rice on non-target planthoppers and their main predator Cyrtorhinus lividipennis (Hemiptera: Miridae)—a case study of the compatibility of Bt rice with biological control. Biol Control 42:242–250CrossRefGoogle Scholar
  8. Chen M, Ye GY, Liu ZC, Fang Q, Hu C, Peng YF, Shelton AM (2009) Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology 18:230–238CrossRefPubMedGoogle Scholar
  9. Chen Y et al (2012) Bt rice expressing Cry1Ab does not stimulate an outbreak of its non-target herbivore, Nilaparvata lugens. Transgenic Res 21:279–291CrossRefPubMedGoogle Scholar
  10. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  11. Clergue B, Amiaud B, Pervanchon F, Lasserre-Joulin F, Plantureux S (2005) Biodiversity: function and assessment in agricultural areas. A review. Agron Sustain Dev 25:1–15CrossRefGoogle Scholar
  12. Crawley MJ (1999) Bollworms, genes and ecologists. Nature 400:501–502CrossRefPubMedGoogle Scholar
  13. de la Poza M et al (2005) Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Prot 24:677–684CrossRefGoogle Scholar
  14. Devos Y, De Schrijver A, De Clercq P, Kiss J, Romeis J (2012) Bt-maize event MON 88017 expressing Cry3Bb1 does not cause harm to non-target organisms. Transgenic Res 21:1191–1214CrossRefPubMedGoogle Scholar
  15. Digby PGN, Kempton RA (1987) Multivariate analysis of ecological communities. Chapman and Hall, LondonCrossRefGoogle Scholar
  16. Duan JJ et al (2010) Extrapolating non-target risk of Bt crops from laboratory to field. Biol Lett 6:74–77CrossRefPubMedGoogle Scholar
  17. 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
  18. Faith D, Minchin P, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68CrossRefGoogle Scholar
  19. Faria CA, Wäckers FL, Pritchard J, Barrett DA, Turlings TC (2007) High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. Plos One 2:e600CrossRefPubMedPubMedCentralGoogle Scholar
  20. Foulquier A, Volat B, Neyra M, Bornette G, Montuelle B (2013) Long-term impact of hydrological regime on structure and functions of microbial communities in riverine wetland sediments. FEMS Microbiol Ecol 85:211–226CrossRefPubMedGoogle Scholar
  21. Groot AT, Dicke M (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant J 31:387–406CrossRefPubMedGoogle Scholar
  22. Guo YY, Feng YJ, Ge Y, Tetreau G, Chen XW, Dong XH, Shi WP (2014) The cultivation of Bt corn producing Cry1Ac toxins does not adversely affect non-target arthropods. Plos One 9:e114228CrossRefPubMedPubMedCentralGoogle Scholar
  23. Habuštová O, Doležal P, Spitzer L, Svobodová Z, Hussein H, Sehnal F (2014) Impact of Cry1Ab toxin expression on the non-target insects dwelling on maize plants. J Appl Entomol 138:164–172CrossRefGoogle Scholar
  24. Han HL, Li GT, Wang ZY, Zhang J, He KL (2009) Cross-resistance of Cry1Ac-selected Asian corn borer to other Bt toxins. Acta Phytophylacica Sin 36:329–334Google Scholar
  25. He KL, Wang ZY, Zhou DR, Wen LP, Song YY, Yao Z (2003) Evaluation of transgenic Bt corn for resistance to the Asian corn borer (Lepidoptera: Pyralidae). J Econ Entomol 96:935–940CrossRefPubMedGoogle Scholar
  26. He MX, He KL, Wang ZY, Wang XY, Li Q (2013) Selection for Cry1Ie resistance and cross-resistance of the selected strain to other Cry toxins in the Asian corn borer, Ostrinia furnacalis (Lepidoptera: Crambidae). Acta Entomol Sin 56:1135–1142Google Scholar
  27. Houlahan JE et al (2006) The effects of adjacent land use on wetland species richness and community composition. Wetlands 26:79–96CrossRefGoogle Scholar
  28. Huang J, Hu R, Rozelle S, Pray C (2005) Insect-resistant GM rice in farmers’ fields: assessing productivity and health effects in China. Science 308:688–690CrossRefPubMedGoogle Scholar
  29. James C (2014) Global status of commercialized biotech/GM crops: 2014. ISAAA Brief. 49. ISAAA, IthacaGoogle Scholar
  30. Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–26CrossRefGoogle Scholar
  31. Kruskal J, Whish M (1978) Multidimensional scaling. Sage, Beverly HillsCrossRefGoogle Scholar
  32. Li X, Liu B (2013) A 2-year field study shows little evidence that the long-term planting of transgenic insect-resistant cotton affects the community structure of soil nematodes. Plos One 8:e61670CrossRefPubMedPubMedCentralGoogle Scholar
  33. Li Y, Romeis J (2010) Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol Control 53:337–344CrossRefGoogle Scholar
  34. Li LL, Wang ZY, He KL, Bai SX, Hua L (2007) Effects of transgenic corn expressing Bacillus thuringiensis CrylAb toxin on population increase of Rhopalosiphum maidis Fitch. J Appl Ecol 18:1077–1080Google Scholar
  35. 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:e2909CrossRefPubMedPubMedCentralGoogle Scholar
  36. Liu XD, Zhai BP, Zhang XX, Zong JM (2005) Impact of transgenic cotton plants on a non-target pest, Aphis gossypii glover. Ecol Entomol 30:307–315CrossRefGoogle Scholar
  37. Lu YH et al (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328:1151–1154CrossRefPubMedGoogle Scholar
  38. Lu ZB et al (2014) No direct effects of two transgenic Bt rice lines, T1C-19 and T2A-1, on the arthropod communities. Environ Entomol 43:1453–1463CrossRefPubMedGoogle Scholar
  39. Lundgren JG, Gassmann AJ, Bernal J, Duan JJ, Ruberson J (2009) Ecological compatibility of GM crops and biological control. Crop Prot 28:1017–1030CrossRefGoogle Scholar
  40. Luo TH, Yu XD, Zhou HZ (2013) Effects of reforestation practices on staphylinid beetles (Coleoptera: Staphylinidae) in southwestern China forests. Environ Entomol 42:7–16CrossRefPubMedGoogle Scholar
  41. Meyer C, Gilbert D, Gillet F, Moskura M, Franchi M, Bernard N (2012) Using “bryophytes and their associated testate amoeba” microsystems as indicators of atmospheric pollution. Ecol Indic 13:144–151CrossRefGoogle Scholar
  42. Nafus DM, Schreiner IH (1991) Review of the biology and control of the Asian corn borer, Ostrinia furnacalis (Lep: Pyralidae). Trop Pest Manag 37:41–56CrossRefGoogle Scholar
  43. Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 4:1–11Google Scholar
  44. Nielsen UN et al (2010) The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. J Biogeogr 37:1317–1328CrossRefGoogle Scholar
  45. Oksanen J et al Vegan: community ecology package R package version 2.2-1. Accessed: 20th Jan 2015
  46. Palmer MW (1993) Putting things in even better order: The advantages of canonical correspondence analysis. Ecology 74:2215–2230CrossRefGoogle Scholar
  47. Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144CrossRefGoogle Scholar
  48. Piepho HP, Büchse A, Richter C (2004) A mixed modelling approach for randomized experiments with repeated measures. J Agron Crop Sci 190:230–247CrossRefGoogle Scholar
  49. Pons X, Lumbierres B, Lopez C, Albajes R (2005) Abundance of non-target herbivores in transgenic Bt-maize: a farm scale study. Eurep J Entomol 102:73–79CrossRefGoogle Scholar
  50. Prasifka JR, Hellmich RL, Dively GP, Lewis LC (2005) Assessing the effects of pest management on nontarget arthropods: the influence of plot size and isolation. Environ Entomol 34:1181–1192CrossRefGoogle Scholar
  51. Priestley A, Brownbridge M (2009) Field trials to evaluate effects of Bt-transgenic silage corn expressing the Cry1Ab insecticidal toxin on non-target soil arthropods in northern New England, USA. Transgenic Res 18:425–443CrossRefPubMedGoogle Scholar
  52. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rao CR (1964) The use and interpretation of principal component analysis in applied research. Sankhyā Indian J Stat Ser A, pp 329–358. Indian Statistical InstituteGoogle Scholar
  54. Rauschen S et al (2009) Impact of Bt-corn MON88017 in comparison to three conventional lines on Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae) field densities. Transgenic Res 18:203–214CrossRefPubMedGoogle Scholar
  55. Rauschen S, Schultheis E, Hunfeld H, Schaarschmidt F, Schuphan I, Eber S (2010) Diabrotica-resistant Bt-maize DKc5143 event MON88017 has no impact on the field densities of the leafhopper Zyginidia scutellaris. Environ Biosaf Res 9:87–99CrossRefGoogle Scholar
  56. R Development Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. Accessed: 10th Dec 2015
  57. Romeis J et al (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26:203–208CrossRefPubMedGoogle Scholar
  58. Romeis J et al (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 et al (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. SAS Institute (2009) Base SAS® 9.2 procedures guide. SAS Institute, CaryGoogle Scholar
  62. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  63. Shepard RN (1962) The analysis of proximities: multidimensional scaling with an unknown distance function. Psychometrika 27:125–139CrossRefGoogle Scholar
  64. Simpson EH (1949) Measurement of diversit. Nature 163:688CrossRefGoogle Scholar
  65. Slade NA, Blair SM (2000) An empirical test of using counts of individuals captured as indices of population size. J Mammal 81:1035–1045CrossRefGoogle Scholar
  66. Song FP et al (2003) Identification of cry1I-Type genes from Bacillus thuringiensis strains and characterization of a novel cry1I-Type Gene. Appl Environ Microb 69:5207–5211CrossRefGoogle Scholar
  67. Svobodová Z, Habuštová O, Sehnal F, Holec M, Hussein HM (2013) Epigeic spiders are not affected by the genetically modified maize MON 88017. J Appl Entomol 137:56–67CrossRefGoogle Scholar
  68. Svobodová Z, Skoková Habuštová O, Hutchison WD, Hussein HM, Sehnal F (2015) Risk assessment of genetically engineered maize resistant to Diabrotica spp.: influence on above-ground arthropods in the Czech Republic. Plos One 10:e0130656CrossRefPubMedPubMedCentralGoogle Scholar
  69. Svobodová Z, Skoková Habuštová O, Boháč J, Sehnal F (2016) Functional diversity of staphylinid beetles (Coleoptera: Staphylinidae) in maize fields: testing the possible effect of genetically modified, insect resistant maize. Bull Entomol Res 106:1–14CrossRefGoogle Scholar
  70. Szenasi A, Palinkas Z, Zalai M, Schmitz OJ, Balog A (2014) Short-term effects of different genetically modified maize varieties on arthropod food web properties: an experimental field assessment. Sci Rep. doi:10.1038/srep05315 PubMedPubMedCentralGoogle Scholar
  71. Ter Braak CJ (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179CrossRefGoogle Scholar
  72. Virla EG, Casuso M, Frias EA (2010) A preliminary study on the effects of a transgenic corn event on the non-target pest Dalbulus maidis (Hemiptera: Cicadellidae). Crop Prot 29:635–638CrossRefGoogle Scholar
  73. Wang ZY et al (2005) Effects of transgenic corn hybrids expressing Bacillus thuringiensis Cry1Ab toxin on survival and growth of the beet armyworm, Spodoptera exigua (Hübner). Acta Entomol Sin 48:214–220Google Scholar
  74. Wang YM, Zhang GA, Du JP, Liu B, Wang MC (2010) Influence of transgenic hybrid rice expressing a fused gene derived from cry1Ab and cry1Ac on primary insect pests and rice yield. Crop Prot 29:128–133CrossRefGoogle Scholar
  75. Wells GF, Park HD, Eggleston B, Francis CA, Criddle CS (2011) Fine-scale bacterial community dynamics and the taxa–time relationship within a full-scale activated sludge bioreactor. Water Res 45:5476–5488CrossRefPubMedGoogle Scholar
  76. Wimp GW, Martinsen GD, Floate KD, Bangert RK, Whitham TG (2005) Plant genetic determinants of arthropod community structure and diversity. Evolution 59:61–69CrossRefPubMedGoogle Scholar
  77. Wolt J et al (2010) Problem formulation in the environmental risk assessment for genetically modified plants. Transgenic Res 19:425–436CrossRefPubMedGoogle Scholar
  78. Wu K, Li W, Feng H, Guo Y (2002) Seasonal abundance of the mirids, Lygus lucorum and Adelphocoris spp. (Hemiptera: Miridae) on Bt cotton in northern China. Crop Prot 21:997–1002CrossRefGoogle Scholar
  79. Xu L, Ferry N, Wang Z, Zhang J, Edwards MG, Gatehouse AMR, He K (2013) A proteomic approach to study the mechanism of tolerance to Bt toxins in Ostrinia furnacalis larvae selected for resistance to Cry1Ab. Transgenic Res 22:1155–1166CrossRefPubMedGoogle Scholar
  80. Yang ZJ, Lang ZH, Zhang J, Song FP, He KL, Huang DF (2012) Studies on insect-resistant transgenic maize (Zea mays L.) harboring Bt cry1Ah and cry1Ie genes. J Agric Sci Technol (Beijing) 14:39–45Google Scholar
  81. Zeilinger AR, Olson DM, Andow DA (2015) Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton. Ecol Appl. doi:10.1890/15-1314.1 Google Scholar
  82. Zhang B, Chen M, Zhang X, Luan H, Tian Y, Su X (2011) Expression of Bt-Cry3A in transgenic Populus alba × P. glandulosa and its effects on target and non-target herbivores and the arthropod community. Transgenic Res 20:523–532CrossRefPubMedGoogle Scholar
  83. Zhang YW et al (2013) Overexpression of a novel cry1Ie gene confers resistance to Cry1Ac-resistant cotton bollworm in transgenic lines of maize. Plant Cell Tiss Org 115:151–158CrossRefGoogle Scholar
  84. Zhang TT, He MX, Gatehouse AMR, Wang ZY, Edwards MG, Li Q, He KL (2014) Inheritance patterns, dominance and cross-resistance of Cry1Ab-and Cry1Ac-selected Ostrinia furnacalis (Guenée). Toxins 6:2694–2707CrossRefPubMedPubMedCentralGoogle Scholar
  85. Zurbrügg C, Nentwig W (2009) Ingestion and excretion of two transgenic Bt corn varieties by slugs. Transgenic Res 18:215–225CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Jingfei Guo
    • 1
  • Kanglai He
    • 1
  • Shuxiong Bai
    • 1
  • Tiantao Zhang
    • 1
  • Yunjun Liu
    • 2
  • Fuxin Wang
    • 1
  • Zhenying Wang
    • 1
  1. 1.State Key Laboratory for Biology of Plant Diseases and Insect Pests, MOA – CABI Joint Laboratory for Bio-Safety, Institute of Plant ProtectionChinese Academy of Agricultural SciencesBeijingChina
  2. 2.Institute of Crop SciencesChinese Academy of Agricultural SciencesBeijingChina

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