Plant Cell Reports

, Volume 36, Issue 4, pp 505–517 | Cite as

Review: biosafety assessment of Bt rice and other Bt crops using spiders as example for non-target arthropods in China

  • Huilin Yang
  • Yuande Peng
  • Jianxiang Tian
  • Juan Wang
  • Jilin Hu
  • Qisheng Song
  • Zhi Wang


Since the birth of transgenic crops expressing Bacillus thuringiensis (Bt) toxin for pest control, the public debate regarding ecological and environmental risks as well as benefits of Bt crops has continued unabated. The impact of Bt crops, especially on non-target invertebrates, has received particular attention. In this review, we summarize and analyze evidences for non-target effects of Bt rice on spiders, major predators in rice fields. Bt rice has been genetically modified to express the Bt protein, which has been shown to be transferred and accumulate in spiders as part of their food chain. Moreover, the Bt protein exhibits unintended effects on the physiology of spiders and spreads to higher trophic levels. Spiders possess unique physiological and ecological characteristics, revealing traits of surrogate species, and are thus considered to be excellent non-target arthropod model systems for study of Bt protein impacts. Due to the complexities of Bt protein transfer and accumulation mechanisms, as well as the apparent lack of information about resulting physiological, biochemical, and ecological effects on spiders, we raise questions and provide recommendations for promising further research.


Spiders Bt rice Non-target effects GM crops Spider ecology 


  1. Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotechnol 25(4):195–203CrossRefGoogle Scholar
  2. 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 Expe Appl 102: 21–28.CrossRefGoogle Scholar
  3. Breitler JC, Vassal JM, Catala MD, Meynard D et al (2004) Bt rice harbouring cry genes controlled by a constitutive or wound-inducible promoter: protection and transgene expression under Mediterranean field conditions. Plant Biotechnol J 2(5):417–430CrossRefPubMedGoogle Scholar
  4. Chen M, Ye GY, Hu C et al (2003a) Effects of transgenic Bt indica rice on the feeding and oviposition behavior of the brown planthopper, Nilaparvata lugens. Acta Phytophylacica Sinica 30:366–370 (in Chinese with English summary) Google Scholar
  5. Chen M, Ye GY, Hu C et al (2003b) Effects of transgenic Bt rice on the dispersal of planthoppers and leafhoppers as well as their egg parasitic wasps. J Zhejiang Univ (Agriculture Life Science 29:29–33 (Chinese with English summary) Google Scholar
  6. Chen XJ, He SL, Cheng KL, Ren GJ (2003c) Effect of Bt-transgenic rice on organism community in paddy-field. J Sichuan Agric Univ 21(2):185–186 (Chinese with English summary) Google Scholar
  7. Chen M, Ye GY, Liu XM et al (2005) Biotransfer and bioaccumulation of CrylAb insecticidal protein in rice plant-brown planthopper-wolf spider food chain. Actor Entomologica Sinica 48(2):208–213 (in Chinese with English summary) Google Scholar
  8. Chen M, Zhao JZ, Ye, GY et al (2006) Impact of insect-resistant transgenic rice on target insect pests and non-target arthropods in China. Insect. Science 13:409–420Google Scholar
  9. Chen WB, Liu FJ, Lin S, You MS (2007) Effects of insect-resistant hybrid rice on bionomical characteristics of Tetrgnatha nitens. Entomol J East China 16(1):13–17 (Chinese with English summary) Google Scholar
  10. Chen M, Ye GY, Liu ZC et al (2009) Analysis of Cry1Ab Toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology 18:230–238CrossRefPubMedGoogle Scholar
  11. Cui XH, Jiao XG, Zhang GA et al (2002) Effect of Bt transgenic Rice to leafhoppers and spiders in field. J Huazhong Agric Univ 21(4):356–358 (Chinese with English summary) Google Scholar
  12. European Food Safety Authority (EFSA) (2010a) EFSA Panel on Plant Protection Products and their Residues (PPR); Scientific Opinion on the development of specific protection goal options for environmental risk assessment of pesticides, in particular in relation to the revision of the Guidance Documents on Aquatic and Terrestrial Ecotoxicology (SANCO/3268/2001 and SANCO/10329/2002). EFSA J 8(10):1821CrossRefGoogle Scholar
  13. Fei R, Yang Y, Zhang LJ et al (2004) Advance research and application of spider venom. J Jilin Univ (Med Edit ion) 06:994–1003 (in Chinese with English summary) Google Scholar
  14. Han Y, Chen J, Wang H et al (2015) Prey-mediated effects of transgenic cry2Aa rice on the spider Hylyphantes graminicola, a generalist predator of Nilapavarta lugens. Bio Control 60:251–261Google Scholar
  15. Jiang YH, Fu Q, Cheng JA et al (2004) Dynamics of Cry1Ab protein from transgenic Bt rice in herbivores and their Predators. Acta Entomologica Sinica 47(4):454–460Google Scholar
  16. Kremen C, Williams N, Aizen MA et al (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314CrossRefPubMedGoogle Scholar
  17. Li FF, Ye GY, Wu Q et al (2007) Arthropod abundance and diversity in Bt and Non-Bt rice fields. Environ Entomol 36(3):646–654CrossRefPubMedGoogle Scholar
  18. Liu ZC, Ye GY, Hu C, Swapan KD (2002) Effects of Bt transgenic rice on population dynamics of main non-target insect pests and dominant spider species in rice paddies. Acta Phytophylacica Sinica 29(2):138–144 (in Chinese with English summary) Google Scholar
  19. Liu ZC, YE GY, Fu Q, Zhang ZT, Hu C (2003) Indirect impact assessment of transgenic rice with Cry1Ab gene on predations by the Wolf Spider, Pirata subpiraticus. Chin J Rice Sci 17(2):175–178 (Chinese with English summary)Google Scholar
  20. Liu LJ, Huang Y, Duan YH et al (2011) Effects of Bt protein expressed by transgenic rice on the development of wolf spider (Pardosa pseudoannulata). Acta Laser Biol Sinica 20(1):45–49 (in Chinese with English summary) Google Scholar
  21. Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects: the Achilles’heel of biological control? Annu Rev Entomol 48:365–396CrossRefPubMedGoogle Scholar
  22. Lu YH, Wu KG, Jiang YY et al (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487(7407):362–365CrossRefPubMedGoogle Scholar
  23. Ludy C, Lang A (2006) Bt maize pollen exposure and impact on the garden spider, Araneus diadematus. Entomol Exp Appl 118:145–156CrossRefGoogle Scholar
  24. Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A Meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–1477CrossRefPubMedGoogle Scholar
  25. Meissle M (2013) Side effects of Bacillus thuringiensis toxins on spiders. In: Nentwig W (ed) Spider ecophysiology. Springer-Verlag, Berlin, pp 429–439CrossRefGoogle Scholar
  26. Meissle M, Lang A (2005) Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages. Agric Ecosyst Environ 107:359–370CrossRefGoogle Scholar
  27. Meissle M, Romeis J (2009) The web-building spiderTheridion impressum(Araneae: Theridiidae) is not adversely affected byBtmaize resistant to corn rootworms. Plant Biotechnol J 7:645–656CrossRefGoogle Scholar
  28. Meissle M, Romeis J (2012) No accumulation of Bt protein in Phylloneta impressa (Araneae: Theridiidae) and pre y arthropods in Bt maize. Environ Entomol 41:1037–1042CrossRefGoogle Scholar
  29. Milofsky TS (2006) Environmental risk assessment process for Bt crops. In: U.S.-China Agricultural Biotechnology Exchange Workshop II: Environmental Risk Assessment. Sponsored by U.S. Trade and Development Agency. Beijing, China. 21–25Google Scholar
  30. Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 4:011Google Scholar
  31. Naranjo Steven E (2005) Long-tTerm aAssessment of the eEffects of tTransgenic Bt cCotton on the aAbundance of nNon-target aArthropod nNatural eEnemies. Environ Entomol 34(5):1193–1210.CrossRefGoogle Scholar
  32. Nicolia A, Manzo A, Veronesi F, Rosellini D (2014) An overview of the last 10 years of genetically engineered crop safety research. Crit Rev Biotechnol 34:77–88CrossRefPubMedGoogle Scholar
  33. Peterson JA, Lundgren JG, Harwood JD (2011) In teractions of transgenic Bacillus thuringiensis in secticidal crops with spiders (Araneae). Journal of Arachnology 39:1–21CrossRefGoogle Scholar
  34. Peterson JA, Obrycki JJ, Harwood JD (2016) Spiders from multiple functional guilds are exposed to Bt-endotoxins in transgenic corn fields via prey and pollen consumption. Biocontrol Sci Technol 9:1–42Google Scholar
  35. Pu D, Shi M, Wu Q et al (2014) Flower-visiting insects and their potential impact on transgene flow in rice. J Appl Ecol 51:1357–1365CrossRefGoogle Scholar
  36. Qiu HM, Dong B, Wu JC et al (2005) Effect of transgenic rice on the growth, fecundity and predation of spiders. J Yangzhou Univ (Agric Life Sci Ed) 3(26):79–82 (Chinese with English summary)Google Scholar
  37. Riaz N, Husnain T, Fatima T, Makhdoom R, Bashir K et al (2006) Development of Indica Basmati rice harboring two insecticidal genes for sustainable resistance against lepidopteran insects. S Afr J Bot 72(2):217–223CrossRefGoogle Scholar
  38. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71CrossRefPubMedGoogle Scholar
  39. Romeis J, Bartsch D, Bigler F et al (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26(2):203–208CrossRefPubMedGoogle Scholar
  40. Romeis J, Raybould A, Bigler F et al (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
  41. Schoenly KG, Cohen MB, Barrion AT et al (2003) Effects of Bacillus thuringiensis on non-target herbivore and natural enemy assemblages in tropical irrigated rice. Environ Biosafety Res 2:181–206CrossRefPubMedGoogle Scholar
  42. Schrijver AD, Devos Y, Clercq PD, Gathmann A et al (2016) Quality of laboratory studies assessing effects of Bt-proteins on non-target organisms: minimal criteria for acceptability. Transgenic Res 25(4):1–17CrossRefGoogle Scholar
  43. Sunderland KD (1999) Mechanisms underlying the effects of spiders on pest populations. J Arachnol 27:308–316Google Scholar
  44. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594CrossRefPubMedGoogle Scholar
  45. Tian JC, Liu ZC, Chen M et al (2010) Laboratory and field field assessments assessments of pPrey-mMediated eEffects of tTransgenic Bt rRice on Ummeliata insecticeps (Araneida: Linyphiidae). Environ Entomol 39(4):1369–1377CrossRefPubMedGoogle Scholar
  46. Tian JC, Chen Y, Li ZL et al (2011) Assessment of effect of transgenic rice with cry1Ab gene and two insecticides on immune of non-target natural enemy, Pardosa pseudoannulata. Chin J Biol Control 27(4):559–563 (Chinese with English summary) Google Scholar
  47. Tian JC, Chen Y, Li ZL et al (2012) Transgenic Cry1Ab rice does not impact ecological fitness and predation of a generalist spider. PLoS One 7(4):e35164CrossRefPubMedPubMedCentralGoogle Scholar
  48. Tian YX, Zhou Y, Xiao KF, et al (2013) Effect of Cry1Ab protein on hemocytes of the wolf spider Pardosa pseudoannulata. Biocontrol Sci Techn 1:423–432CrossRefGoogle Scholar
  49. Touart LW, Maciorowski AF (1997) Information needs for pesticide registration in the United States. Ecol Appl 7(4):1086–1093CrossRefGoogle Scholar
  50. United States Environmental Protection Agency (USEPA) (2007) White paper on tier-based testing for the effects of proteinaceous insecticeidal plant-incorporated protectants on non-target arthropods for regulatory risk assessment. US Environmental Protection Agency, Washington, DCGoogle Scholar
  51. Van Lenteren JC, Bale J, Bigler F et al (2006) Assessing the risks of releasing exotic biological control agents of arthropod pets. Annu Rev Entomol 51:609–634CrossRefPubMedGoogle Scholar
  52. Wang J, Peng YD, He C et al (2016) Cry1Ab-expressing rice did not influence expression of fecundity-related genes in the wolf spider Pardosa pseudoannulata. Gene 592(:):1–7PubMedGoogle Scholar
  53. Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ et al (2008) Bt crop effects on functional guilds of non-target arthropods: A meta-analysis. PLoS One 3(5):e2118CrossRefPubMedPubMedCentralGoogle Scholar
  54. Xu XL, Han Y, Wu G et al (2011) Field evaluation of effects of transgenic cry1Ab/cry1Ac, cry1C and cry2A rice on Ccnaphalocrocis medinalis and its arthropod predators. Sci China Life Sci 54(11):1019–1028CrossRefPubMedGoogle Scholar
  55. Yang YY, Xiao NW (2013) Laboratory assessment of the impacts of transgenic Bt rice on the ecological fitness of the soil non-target arthropod, Folsomia candida (Collembola: Isotomidae). Tansgenic Res 22:791–803.CrossRefGoogle Scholar
  56. Yang HL, Peng YD, Tian JX et al (2016) Spiders as excellent experimental models for investigation of heavy metal impacts on the environment: a review. Environ Earth Sci 75:1059CrossRefGoogle Scholar
  57. Ye GY, Shu QY, Yao HW, Cui HR et al (2001) Field evaluation of resistance of transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to two stem borers. J Econ Entomol 94(1):271–276CrossRefPubMedGoogle Scholar
  58. Yeonlee S, Taekim S, Kookjung J et al (2014) A comparison of spider communities in Bt and non-Bt rice fields. Environ Entomol 43(3):819–827CrossRefGoogle Scholar
  59. Zhou J, Xiao K, Wei B, Wang Z, Tian Y et al (2014) Bioaccumulation of Cry1Ab protein from an herbivore reduces anti-oxidant enzyme activities in two spider species. PLoS One 9(1):e84724CrossRefPubMedPubMedCentralGoogle Scholar
  60. Zurbrügg C, Nentwig W (2009) Ingestion and excretion of two transgenic Bt corn varieties by slugs. Transgenic Res 4:18(2):215–225CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Huilin Yang
    • 1
    • 2
  • Yuande Peng
    • 3
  • Jianxiang Tian
    • 4
  • Juan Wang
    • 1
  • Jilin Hu
    • 1
  • Qisheng Song
    • 5
  • Zhi Wang
    • 1
  1. 1.College of Bioscience and BiotechnologyHunan Agriculture UniversityChangshaChina
  2. 2.College of Orient Science & TechnologyHunan Agriculture UniversityChangshaChina
  3. 3.Institute of Bast Fiber CropsChinese Academy of Agricultural SciencesChangshaChina
  4. 4.College of Continuing EducationHunan Agriculture UniversityChangshaChina
  5. 5.Division of Plant SciencesUniversity of MissouriColumbiaUSA

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