Abstract
Transgenic maize expressing the Cry1Ab and Cry2Ab protein simultaneously from Bacillus thuringiensis (Bt-maize) has been grown for farm-scale study to investigate its potential impact to non-target arthropod (NTA). The trials were conducted between Bt maize 2A-7 and its parental line (B73-329) in Beijing, China, over 3 years. Richness (C), Shannon index (H), Pielou index (J), Simpson index (D), and Bray-Curtis index were used to evaluate the population dynamics and biodiversity of the dominant arthropods from per 50 plants in crop field. The mainly abundant groups were Aphidoidea, Araneae, Coccinellidae, Anthocoridae, and Thripidae which represented about 90% of the total number of NTA. Although the abundance of NTA varied from year to year, there is no significant difference between Bt maize and non-Bt maize field. Fluctuations were found at individual sample dates, but the trend of these descriptors remained consistent. Further analysis showed the biodiversity indexes of the dominant arthropods C, H, J, D, and Bray-Curtis dissimilarity between Bt maize producing Cry1Ab and Cry2Ab toxin simultaneously and its parental line had no significant difference except for some sampling dates. These results suggested that Bt maize is compatible with the NTAs and provides further evidence of the ecological impact of genetically modified maize.
Similar content being viewed by others
References
Albajes R, Lumbierres B, Pons X, Comas J (2013) Representative taxa in field trials for environmental risk assessment of genetically modified maize. Bull Entomol Res 103:724–733
Arias-Martín M, Garcia M, Castanera P, Ortego F, Farinos GP (2018) Farm-scale evaluation of the impact of CrylAb Bt maize on canopy nontarget arthropods: a 3-year study. Insect Sci 25:87–98
Arpaia S, Baldacchino F, Bosi S, Burgio G, Errico S, Magarelli RA, Masetti A, Santorsola S (2018) Evaluation of the potential exposure of butterflies to genetically modified maize pollen in protected areas in Italy. Insect Sci 25:549–561
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349
Brookes G, Barfoot P (2015) Environmental impacts of genetically modified (GM) crop use 1996–2013: impacts on pesticide use and carbon emissions. GM Crops Food 6:103–133
Chen M, Zhao JZ, Ye GY, Fu Q, Shelton AM (2006) Impact of insect-resistant transgenic rice on target insect pests and non-target arthropods in China. Insect Sci 13:409–420
Chen HX, Yang R, Wang Y, Zhang L, Camara I, Dong XH, Liu YQ, Shi WP (2016) Efficacy of Bt maize producing the Cry1Ac protein against two important pests of corn in China. Environ Sci Pollut Res 23:21511–21516
Cohen MB, Chen M, Bentur JS, Heong KL, Ye GY (2008) Bt rice in Asia: potential benefits, impact, and sustainability. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer Science + Business, Media B.V., Dordrecht, pp 223–248
Collins SL, Micheli F, Hartt L (2000) A method to determine rates and patterns of variability in ecological communities. Oikos 91:285–293
Comas C, Lumbierres B, Pons X, Albajes R (2014) No effects of Bacillus thuringiensis maize on nontarget organisms in the field in southern Europe: a meta-analysis of 26 arthropod taxa. Transgenic Res 23:135–143
Dang C, Lu ZB, Wang L, Chang XF, Wang F, Yao HW, Peng YF, David S, Ye GY (2017) Does Bt rice pose risks to non-target arthropods? Results of a meta-analysis in China. Plant Biotechnol J 15:1047–1053
Devos Y, Schrijver AD, Clercq PD, Kiss J, Romeis J (2012) Bt-maize event Mon 88017 expressing Cry3Bb1 does not cause harm to non-target organisms. Transgenic Res 21:1191–1214
EFSA (2010) Guidance on the environmental risk assessment of genetically modified plants. EFSA J 8:1879
EFSA (2011) Guidance for risk assessment of food and feed from GM plants. EFSA J 9(5):2150
Guo YY, Feng YJ, Ge Y, Tetreau G, ChenX W, Dong XH, Shi WP (2014) The cultivation of Bt corn producing Cry1Ac toxins does not adversely affect non-target arthropods. PLoS One 9:e114228
Guo JF, He KL, Bai SX, Zhang TT, Liu YJ, Wang FX, Wang ZY (2016) Effects of transgenic cry1Ie maize on non-lepidopteran pest abundance, diversity and community composition. Transgenic Res 25:761–772
Huang JH, Jing X, Douglas AE (2015) The multi-tasking gut epithelium of insect. Insect Biochem Mol Biol 67:15–20
ISAAA (2018) Global Status of Commercialized Biotech/GM Crops in 2018 (ISAAA Brief No. 54). ISAAA, Ithaca
Kim HS, Noh S, Park Y (2017) Enhancement of Bacillus thuringiensis Cry1Ac and Cry1Ca toxicity against Spodoptera exigua (Hübner) by suppression of a chitin synthase B gene in midgut. J Asia Pac Entomol 20(1):199–205
Klumper W, Qaim M (2014) A meta-analysis of the impacts of genetically modifified crops. PLoS One 9:e111629
Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford
Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use pattern. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4:1–23
Perry JN, ter Braak CJF, Dixon PM, Duan JJ, Hails RS, Huesken A et al (2009) Statistical aspects of environmental risk assessment of GM plants for effects on non-target organisms. Environ Biosafety Res 8:65–78. https://doi.org/10.1051/ebr/2009009
Peterson JA, Lundgren JG, Harwood JD (2011) Interactions of transgenic Bacillus thuringiensis insecticidal crops with spiders (Araneae). J Arachnol 39:1–21
Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144
Prasifka JR, Hellmich RL, Dively GP, Lewis LC (2005) Assessing the effects of pest management on nontarget arthropods: the influence of plot and isolation. Environ Entomol 34:1181–1192
Priestley AL, Brownbridge M (2009) Field trials to evaluate effects of Bt-transgenic silage corn expressing the CrylAb insecticidal toxin on non-target soil arthropods in northern New England, USA. Transgenic Res 18:425–443
Qiao FB, Huang JK, Rozelle S, Wilen J (2010) Natural refuge crops, build up of resistance, and zero-refuge strategy for Bt cotton in China. Sci China Life Sci 53:1227–1238. https://doi.org/10.1007/s11427-010-4076-3
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna https://www.R-project.org/. Accessed 17 Jul 2019
Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkens MMC, Hartley SE, Hellmich RL, Huesing JE, Jepson PC, Layton R (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26:203–208
Simpson EH (1949) Measurement of diversity. Nature 163:688
Simpson BB, Cracraft J (1995) Systematics: the science of biodiversity. BioScience 45(10):670–672
Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana
Schuirmann D (1987) A comparison of the two one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. J Pharmacokinet Biopharm 15:657–680
Tabashnik BE, Gould F, Carrière Y (2004) Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. J Evol Biol. https://doi.org/10.1111/j.1420-9101.2004.00695.x
van der Voet H, Goedhart PW, Lazebnik J, Kessel GJT, Mullins E, van Loon JJA, Arpaia S (2019) Equivalence analysis to support environmental safety assessment: using nontarget organism count data from field trials with cisgenically modified potato. Ecol Evol 9:2863–2882. https://doi.org/10.1002/ece3.4964
Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS One 3:e2118
Wolt JD, Peterson RK (2010) Prospective formulation of environmental risk assessments: probabilistic screening for Cry1A(b) maize risk to aquatic insects. Ecotoxicol Environ Saf 73:1182–1188
Xing YJ, Qin ZF, Feng MY, Li AM, Zhang L, Wang Y, Dong XH, Zhang YX, Tan SQ, Shi WP (2019) The impact of Bt maize expressing the Cry1Ac protein on non-target arthropods. Environ Sci Pollut Res 26:5814–5819. https://doi.org/10.1007/s11356-018-4025-4
Zhang B, Chen M, Zhang XF, Luan HH, Tian YC, Su XH (2011) Expressing of Bt-Cry3A in transgenic Populus alba × P. glandulosa and its effects on target and non-target pests and the arthropod community. Transgenic Res 20:523–532
Funding
This research was funded by the Special Fund for Transgenic Crop Research of China (2016ZX08011-003).
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: YY, WPS, and XHD. Performed the experiments: YY, ZFQ, YDX, KLC, and XXZ. Analyzed the data: YY. Contributed reagents/materials/analysis tools: XHD and WPS. Wrote the paper: YY and WPS.
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 254 kb).
Rights and permissions
About this article
Cite this article
Yin, Y., Xu, Y., Cao, K. et al. Impact assessment of Bt maize expressing the Cry1Ab and Cry2Ab protein simultaneously on non-target arthropods. Environ Sci Pollut Res 27, 21552–21559 (2020). https://doi.org/10.1007/s11356-020-08665-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-08665-9