Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

References

  • Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotechnol 25(4):195–203

    CAS  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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):417–430

    CAS  Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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)

    CAS  Google Scholar 

  • 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 13:409–420

    CAS  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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 18:230–238

    CAS  Article  PubMed  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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):1821

    Article  Google Scholar 

  • 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 

  • 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 60:251–261

    CAS  Google Scholar 

  • 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):454–460

    Google Scholar 

  • 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 10:299–314

    Article  PubMed  Google Scholar 

  • Li FF, Ye GY, Wu Q et al (2007) Arthropod abundance and diversity in Bt and Non-Bt rice fields. Environ Entomol 36(3):646–654

    CAS  Article  PubMed  Google Scholar 

  • 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 

  • 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)

    CAS  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects: the Achilles’heel of biological control? Annu Rev Entomol 48:365–396

    CAS  Article  PubMed  Google Scholar 

  • Lu YH, Wu KG, Jiang YY et al (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487(7407):362–365

    CAS  Article  PubMed  Google Scholar 

  • Ludy C, Lang A (2006) Bt maize pollen exposure and impact on the garden spider, Araneus diadematus. Entomol Exp Appl 118:145–156

    CAS  Article  Google Scholar 

  • Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A Meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–1477

    CAS  Article  PubMed  Google Scholar 

  • Meissle M (2013) Side effects of Bacillus thuringiensis toxins on spiders. In: Nentwig W (ed) Spider ecophysiology. Springer-Verlag, Berlin, pp 429–439

    Chapter  Google Scholar 

  • Meissle M, Lang A (2005) Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages. Agric Ecosyst Environ 107:359–370

    Article  Google Scholar 

  • Meissle M, Romeis J (2009) The web-building spiderTheridion impressum(Araneae: Theridiidae) is not adversely affected byBtmaize resistant to corn rootworms. Plant Biotechnol J 7:645–656

    CAS  Article  Google Scholar 

  • Meissle M, Romeis J (2012) No accumulation of Bt protein in Phylloneta impressa (Araneae: Theridiidae) and pre y arthropods in Bt maize. Environ Entomol 41:1037–1042

    Article  Google Scholar 

  • 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. 21–25

  • Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 4:011

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 34:77–88

    CAS  Article  PubMed  Google Scholar 

  • Peterson JA, Lundgren JG, Harwood JD (2011) In teractions of transgenic Bacillus thuringiensis in secticidal crops with spiders (Araneae). Journal of Arachnology 39:1–21

    Article  Google Scholar 

  • 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 9:1–42

    Google Scholar 

  • Pu D, Shi M, Wu Q et al (2014) Flower-visiting insects and their potential impact on transgene flow in rice. J Appl Ecol 51:1357–1365

    Article  Google Scholar 

  • 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 

  • 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):217–223

    Article  Google Scholar 

  • Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71

    CAS  Article  PubMed  Google Scholar 

  • Romeis J, Bartsch D, Bigler F et al (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26(2):203–208

    CAS  Article  PubMed  Google Scholar 

  • 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 90:901–909

    CAS  Article  PubMed  Google Scholar 

  • 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 2:181–206

    Article  PubMed  Google Scholar 

  • 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):1–17

    Article  Google Scholar 

  • Sunderland KD (1999) Mechanisms underlying the effects of spiders on pest populations. J Arachnol 27:308–316

    Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    CAS  Article  PubMed  Google Scholar 

  • 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):1369–1377

    CAS  Article  PubMed  Google Scholar 

  • 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 

  • 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):e35164

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tian YX, Zhou Y, Xiao KF, et al (2013) Effect of Cry1Ab protein on hemocytes of the wolf spider Pardosa pseudoannulata. Biocontrol Sci Techn 1:423–432

    Article  Google Scholar 

  • Touart LW, Maciorowski AF (1997) Information needs for pesticide registration in the United States. Ecol Appl 7(4):1086–1093

    Article  Google Scholar 

  • 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, DC

    Google Scholar 

  • 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 51:609–634

    Article  PubMed  Google Scholar 

  • 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(:):1–7

    CAS  PubMed  Google Scholar 

  • 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):e2118

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):1019–1028

    CAS  Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 75:1059

    Article  Google Scholar 

  • 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):271–276

    CAS  Article  PubMed  Google Scholar 

  • 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):819–827

    Article  Google Scholar 

  • 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):e84724

    Article  PubMed  PubMed Central  Google Scholar 

  • Zurbrügg C, Nentwig W (2009) Ingestion and excretion of two transgenic Bt corn varieties by slugs. Transgenic Res 4:18(2):215–225

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The study was supported by the Nature Science Foundation of China (Grants Nos. 31472017 and 31272339) and the Agricultural Science and Technology Innovation Program of China (CAAS-ASTIP-IBFC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhi Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Communicated by Neal Stewart.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, H., Peng, Y., Tian, J. et al. Review: biosafety assessment of Bt rice and other Bt crops using spiders as example for non-target arthropods in China. Plant Cell Rep 36, 505–517 (2017). https://doi.org/10.1007/s00299-017-2108-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2108-1

Keywords

  • Spiders
  • Bt rice
  • Non-target effects
  • GM crops
  • Spider ecology