Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (4): 893-899    DOI: 10.1016/S2095-3119(17)61887-2
Research Article Advanced Online Publication | Current Issue | Archive | Adv Search |
No detrimental effect of Bt maize pollen containing Cry1Ab/2Aj or Cry1Ac on adult green lacewings Chrysoperla sinica Tjeder
LIU Yan-min1, LI Yun-he1, CHEN Xiu-ping1, SONG Xin-yuan2, SHEN Ping3, PENG Yu-fa1
1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2 Jilin Academy of Agricultural Sciences, Changchun 130124, P.R.China
3 Science and Technology Development Center, Ministry of Agriculture, Beijing 100122, P.R.China
Download:  PDF (759KB) ( )  
Export:  BibTeX | EndNote (RIS)      
Adult Chrysoperla sinica Tjeder is a common pollen feeder in maize fields.  They are thus directly exposed to insecticidal proteins by consumption of genetically engineered maize pollen containing Bacillus thuringiensis (Bt) proteins.  Here we assessed the potential effects of Cry1Ab/2Aj- or Cry1Ac-containing Bt maize pollen on the fitness of adult C. sinica via a dietary-exposure assay under laboratory conditions.  Survival, pre-oviposition, fecundity and adult dry weight did not differ between adult C. sinica consuming Bt or the corresponding non-Bt maize pollen.  The stability of the Cry protein in the food sources and uptake of the Cry protein by adult C. sinica during the feeding experiment were confirmed by ELISA.  These results demonstrate that adult C. sinica are not affected by the consumption of Cry1Ab/2Aj- or Cry1Ac-containing maize pollen, suggesting that production of Bt maize expressing cry1Ab/2Aj or cry1Ac genes will pose a negligible risk to adult C. sinica.
Keywords:  non-target effect        environmental risk assessment        ELISA        dietary exposure assay  
Received: 14 September 2017   Accepted:
Fund: The study was supported by the National GMO New Variety Breeding Program of China (2015ZX08013-003).
Corresponding Authors:  Corrrespondence LI Yun-he, Tel: +86-10-62815947, Fax: +86-10-62896114, E-mail:   
About author:  LIU Yan-min, E-mail:;

Cite this article: 

LIU Yan-min, LI Yun-he, CHEN Xiu-ping, SONG Xin-yuan, SHEN Ping, PENG Yu-fa. 2019. No detrimental effect of Bt maize pollen containing Cry1Ab/2Aj or Cry1Ac on adult green lacewings Chrysoperla sinica Tjeder. Journal of Integrative Agriculture, 18(4): 893-899.

Bai Y Y, Jiang M X, Cheng J A. 2005. Effects of transgenic cry1Ab rice pollen on the oviposition and adult longevity of Chrysoperla sinica Tjeder. Acta Phytophylacica Sinica, 32, 225–230. (in Chinese)
Chang X, Liu G G, He K L, Shen Z C, Peng Y F, Ye G Y. 2013. Efficacy evaluation of two transgenic maize events expressing fused proteins to Cry1Ab-susceptible and-resistant Ostrinia furnacalis (Lepidoptera: Crambidae). Journal of Economic Entomology, 106, 2548–2556.
Devos Y, Romeis J, Luttik R, Maggiore A, Perry J N, Schoonjans R, Streissl F, Tarazona J V, Brock T C M. 2015. Optimising environmental risk assessments. EMBO Reports, 16, 1060–1063.
Garcia-Alonso M, Jacobs E, Raybould A, Nickson T E, Sowig P, Willekens H, Van Der Kouwe P, Layton R, Amijee F, Fuentes A M. 2006. A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environmental Biosafety Research, 5, 57–65.
He K L, Wang Z Y, Wen L, Bai S X, Zhou D R, Zhu Q H. 2003. Field evaluation of the Asian maize borer control inhybrid of transgenic maize event MON 810. Agricultural Sciences in China, 2, 1363–1368.
Hilbeck A, Baumgartner M, Fried P M, Bigler F. 1998a. Effects of transgenic Bacillus thuringiensis maize-fed prey on mortality and development time of immature Chrysoperla maizeea (Neuroptera: Chrysopidae). Environmental Entomology, 27, 480–487.
Hilbeck A, Moar W J, Pusztai-Carey M, Filippini A, Bigler F. 1998b. Toxicity of Bacillus thuringiensis CrylAb toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Environmental Entomology, 27, 1255–1263.
James C. 2016. Global status of commercialized biotech/GM crops: 2015. ISAAA Briefs. ISAAA, Ithaca, NY, USA.
Jiang X B, Xiao G Y. 2010. Diversity of arthropod community in the canopy of genetically modified herbicide-tolerant rice (Oryza sativa L.). Chinese Journal of Eco-Agriculture, 18, 1277–1283. (in Chinese)
Li Y H, Chen X P, Hu L, Romeis J, Peng Y F. 2014a. Bt rice producing Cry1C protein does not have direct detrimental effects on the green lacewing Chrysoperla sinica (Tjeder). Environmental Toxicology and Chemistry, 33, 1391–1397.
Li Y H, Hu L, Romeis J, Wang Y, Han L, Chen X P, Peng Y F. 2014b. Use of an artificial diet system to study the toxicity of gut-active insecticidal compounds on larvae of the green lacewing Chrysoperla sinica. Biological Control, 69, 45–51.
Li Y H, Liu Y M, Yin X M, Romeis J, Song X Y, Chen X P, Gen L L, Peng Y F, Li Y H. 2017a. Consumption of Bt maize pollen containing Cry1Ie does not negatively affect Propylea japonica (Thunberg) (Coleoptera: Coccinellidae). Toxins, 9, 108.
Li Y H, 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, e2909.
Li Y H, Meissle M, Romeis J. 2010. Use of maize pollen by adult Chrysoperla carnea (Neuroptera: Chrysopidae) and fate of Cry proteins in Bt-transgenic varieties. Journal of Insect Physiology, 56, 157–164.
Li Y H, Romeis J, Wu K M, Peng Y F. 2014c. Tier-1 assays for assessing the toxicity of insecticidal proteins produced by genetically engineered plants to non-target arthropods. Insect Science, 21, 125–134.
Li Y H, Wang Y Y, Romeis J, Liu Q S, Lin K J, Chen X P, Peng Y F. 2013. Bt rice expressing Cry2Aa does not cause direct detrimental effects on larvae of Chrysoperla sinica. Ecotoxicology, 22, 1413–1421.
Li Y H, Zhang Q L, Liu Q S, Meissle M, Yang Y, Wang Y N, Hua H X, Chen X P, Peng Y F, Romeis J. 2017b. Bt rice in China-focusing the nontarget risk assessment. Plant Biotechnology Journal, 15, 1340–1345.
Li Y H, Zhang X J, Chen X P, Romeis J, Yin X M, Peng Y F. 2015. Consumption of Bt rice pollen containing Cry1C or Cry2A does not pose a risk to Propylea japonica (Thunberg) (Coleoptera: Coccinellidae). Scientific Reports, 5, 7679.
Liu Q S, Hallerman E, Peng Y F, Li Y H. 2016. Development of Bt rice and Bt maize in China and their efficacy in target pest control. International Journal of Molecular Sciences, 17, 1561.
Liu Y M, Liu Q S, Wang Y N, Chen X P, Song X Y, Romeis J, Li Y H, Peng Y F. 2016. Ingestion of Bt maize pollen containing Cry1Ab/2Aj or Cry1Ac does not harm Propylea japonica larvae. Scientific Reports, 6, 23507.
Mason C E, Sheldon J K, Pesek J, Bacon H, Gallusser R, Radke G, Slabaugh B. 2008. Assessment of Chrysoperla plorabunda longevity, fecundity, and egg viability when adults are fed transgenic Bt maize pollen. Journal of Agricultural and Urban Entomology, 25, 265–278.
Murray D, Wesseling C, Keifer M, Corriols M, Henao S. 2002. Surveillance of pesticide-related illness in the developing world: putting the data to work. International Journal of Occupational and Environmental Health, 8, 243–248.
Pechanova O, Pechan T. 2015. Maize-pathogen interactions: An ongoing combat from a proteomics perspective. International Journal of Molecular Sciences, 16, 28429–28448.
Pusztai M, Fast P, Gringorten L, Kaplan H, Lessard T, Carey P. 1991. The mechanism of sunlight-mediated inactivation of Bacillus thuringiensis crystals. Biochemical Journal, 273, 43–47.
Romeis J, Bartsch D, Bigler F, Candolfi M P, Gielkens M M, Hartley S E, Hellmich R L, Huesing J E, Jepson P C, Layton R. 2008. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nature Biotechnology, 26, 203–208.
Romeis J, Hellmich R L, Candolfi M P, Carstens K, De Schrijver A, Gatehouse A M, Herman R A, Huesing J E, McLean M A, Raybould A. 2011. Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Research, 20, 1–22.
Romeis J, Meissle M, Naranjo S E, Li Y H, Bigler F. 2014. The end of a myth-Bt (Cry1Ab) maize does not harm green lacewings. Frontiers in Plant Science, 5, 391.
Sears M K, Hellmich R L, Stanley-Horn D E, Oberhauser K S, Pleasants J M, Mattila H R, Siegfried B D, Dively G P. 2001. Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proceedings of the National Academy of Sciences of the United States of America, 98, 11937–11942.
Sims S R, Ream J E. 1997. Soil inactivation of the Bacillus thuringiensis subsp. kurstaki CryIIA insecticidal protein within transgenic cotton tissue: Laboratory microcosm and field studies. Journal of Agricultural and Food Chemistry, 45, 1502–1505.
Wang J, Wu F C, Liu X Y, Feng S D, Song X Y. 2016. Evaluation of transgenic maize ‘Shuangkang 12–5’ with complex traits of insect-resistance and glyphosate-resistance for the resistance to Ostrinia furnacalis and tolerance to glyphosate. Plant Protection, 42, 45–50. (in Chinese)
Wang Y Q, He K L, Jiang F, Wang Y D, Zhang T T, Wang Z Y, Bai S X. 2014. Resistance of transgenic Bt maize variety BT-799 to the Asian maize borer. Chinese Journal of Applied Entomology, 3, 636–642. (in Chinese)
Wang Y Y, Dai P L, Chen X P, Romeis J, Shi J, Peng Y F, Li Y H. 2017. Ingestion of Bt rice pollen does not reduce the survival or hypopharyngeal gland development of Apis mellifera adults. Environmental Toxicology and Chemistry, 36, 1243–1248.
Wang Y Y, Li Y H, Huang Z Y, Chen X P, Romeis J, Dai P L, Peng Y F. 2015. Toxicological, biochemical, and histopathological analyses demonstrating that Cry1C and Cry2A are not toxic to larvae of the honeybee, Apis mellifera. Journal of Agricultural and Food Chemistry, 63, 6126–6132.
Wang Y Y, Li Y H, Romeis J, Chen X P, Zhang J, Chen H, Peng Y F. 2012. Consumption of Bt rice pollen expressing Cry2Aa does not cause adverse effects on adult Chrysoperla sinica Tjeder (Neuroptera: Chrysopidae). Biological Control, 61, 246–251.
Xing Z J, Wang Z Y, He K L, Bai S X. 2008. Field degradation dynamics of Cry1Ab insecticidal protein in transgenic Bacillus thuringiensis maize pollen accumulated in leaf axiles. Chinese Journal of Applied and Environmental Biology, 14, 163–166. (in Chinese)
Yang Y, Chen X P, Cheng L S, Cao F Q, Romeis J, Li Y H, Peng Y F. 2015. Toxicological and biochemical analyses demonstrate no toxic effect of Cry1C and Cry2A to Folsomia candida. Scientific Reports, 5, 15619.
Zhang B, Yang Y, Zhou X, Shen P, Peng Y F, Li Y H. 2017. A laboratory assessment of the potential effect of Cry1Ab/Cry2Aj-containing Bt maize pollen on Folsomia candida by toxicological and biochemical analyses. Environmental Pollution, 222, 94–100.
Zhang Y W, Liu Y J, Ren Y, Liu Y, Liang G M, Song F P, Bai S X, Wang J H, Wang G Y. 2013. Overexpression of a novel Cry1Ie gene confers resistance to Cry1Ac-resistant cotton bollworm in transgenic lines of maize. Plant Cell Tissue and Organ Culture, 115, 151–158.
[1] Akhtar Zunnu Raen, DANG Cong, WANG Fang, PENG Yu-fa, YE Gong-yin. Thrips-mediated impacts from transgenic rice expressing Cry1Ab on ecological fitness of non-target predator Orius tantilus (Hemiptera: Anthocoridae)[J]. >Journal of Integrative Agriculture, 2016, 15(9): 2059-2069.
[2] Akhtar Zunnu Raen, YE Gong-yin, LU Zeng-bin, CHANG Xue, SHEN Xiao-jing, PENG Yu-fa. Impact Assessments of Transgenic cry1Ab Rice on the Population Dynamics of Five Non-Target Thrips Species and Their General Predatory Flower Bug in Bt and Non-Bt Rice Fields Using Color Sticky Card Traps[J]. >Journal of Integrative Agriculture, 2013, 12(10): 1807-1815.
No Suggested Reading articles found!