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Journal of Integrative Agriculture  2022, Vol. 21 Issue (5): 1424-1435    DOI: 10.1016/S2095-3119(20)63597-3
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Assessment of the potential toxicity of insecticidal compounds to Peristenus spretus, a parasitoid of mirid bugs
ZHAO Man1, 2, LI Yun-he1, NIU Lin-lin1, CHEN Lin1, LIANG Ge-mei1  
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 College of Plant Protection, Henan Agricultural University, Zhengzhou 450002, P.R.China 
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随着我国Bt作物种植面积的增加,绿盲蝽和其他盲蝽逐渐成为重要农业害虫因为它们对作物中的Bt蛋白不敏感。此外,Bt作物种植后杀虫剂使用量的减少也增加了盲蝽爆发的严重程度。红颈常室茧蜂是一种盲蝽若虫的寄生蜂,但它对Bt蛋白的敏感性尚不清楚。在当前研究中,我们利用添加Bt蛋白(400 µg g-1)或不添加Bt蛋白的10%蜂蜜水,发展了一种评价Bt蛋白(Cry1Ab, Cry1Ac, Cry1F, Cry2Aa和Cry2Ab)对红颈常室茧蜂成虫影响的直接暴露试验体系。结果显示,红颈常室茧蜂成虫的存活和繁殖情况能够被半胱氨酸蛋白酶抑制剂E-64(阳性对照)显著抑制,但不受供试5种Bt蛋白影响。此外,寄生蜂体内的消化酶、解毒酶和保护酶活性也不受供试Bt蛋白影响,但取食含E-64的饲料后,它们受到显著影响。然后我们建立了一种三级营养试验,来测定供试5种Bt蛋白对红颈常室茧蜂幼虫和蛹的影响,在这个试验中,以取食含有Cry蛋白饲料的盲蝽若虫作为红颈常室茧蜂的寄主昆虫。三级营养试验的结果显示,即使被寄主的绿盲蝽体内含有大量Bt蛋白,以它们为寄主的红颈常室茧蜂寄生蜂化蛹率和羽化率也没有受到显著影响。上述结果整体表明,研究中发展的这2个生物试验可以用来评价杀虫物质对红颈常室茧蜂的毒性,供试的Cry蛋白对红颈常室茧蜂无毒性

Abstract  With the increased cultivation of Bt crops in China, Apolygus lucorum and other mirid bugs have emerged as important agricultural pests because they are insensitive to the Bt proteins.  In addition, the reduction of pesticide applications after planting Bt crops also increases the severity of mirid bug outbreaks.  Peristenus spretus is a parasitoid of mirid nymphs, but its sensitivity to Bt proteins is not known.  In the current study, we developed a dietary exposure assay to assess the effects of Bt proteins (Cry1Ab, Cry1Ac, Cry1F, Cry2Aa, and Cry2Ab) on P. spretus adults using a diet consisting of a 10% honey solution with or without Bt proteins at 400 µg g–1 diet.  The results showed that the survival and reproduction of P. spretus adults were reduced by the cysteine protease inhibitor E-64 (a positive control) but were not affected by any of the five Bt proteins.  The activities of digestive, detoxifying, and antioxidant enzymes in P. spretus were also unaffected by diets containing the Cry proteins, but they were significantly affected by the diet containing E-64.  We then developed a tri-trophic bioassay to determine the effects of the five Bt proteins on P. spretus larvae and pupae.  In this assay, A. lucorum nymphs fed an artificial diet containing Cry proteins were used as the hosts for P. spretus.  The results of the tri-trophic assay indicated that neither the pupation rate nor the eclosion rate of the P. spretus parasitoids were significantly affected by the presence of high concentrations of Bt proteins in the parasitized A. lucorum nymphs.  The overall results indicate that these two assays can be used to evaluate the toxicity of insecticidal compounds to P. spretus and that the tested Cry proteins are not toxic to P. spretus.  
Keywords:  transgenic crops       plant bugs        parasitic natural enemy        Cry proteins        non-target risk assessment
Received: 19 August 2020   Accepted: 17 December 2020
Fund: This research was supported by the Key Project for Breeding Genetically Modified Organisms, China (2016ZX08011-002) and China’s Donation to the CABI Development Fund.
About author:  ZHAO Man, Mobile: +86-13693160661, E-mail: zhaoman821; Correspondence LIANG Ge-mei, Tel: +86-10-62815929, E-mail:

Cite this article: 

ZHAO Man, LI Yun-he, NIU Lin-lin, CHEN Lin, LIANG Ge-mei . 2022. Assessment of the potential toxicity of insecticidal compounds to Peristenus spretus, a parasitoid of mirid bugs. Journal of Integrative Agriculture, 21(5): 1424-1435.

Bai S X, Zhang H G, Ge X, Wang Z Y. 2011. Effects of Bt-corn expressing Cry1F on the survival and fecundity of the parasitoid Macrocentrus cingulum. Plant Protection, 37, 82–85. (in Chinese)
Bortolotto O C, Silva G V, Bueno A F, Pomari A F, Martinelli S, Head G P, Carvalho R A, Barbosa G C. 2014. Development and reproduction of Spodoptera eridania (Lepidoptera: Noctuidae) and its egg parasitoid Telenomus remus (Hymenoptera: Platygastridae) on the genetically modified soybean (Bt) MON 87701×MON 89788. Bulletin of Entomological Research, 104, 724–730.
Bradford M M. 1976. A rapid and sensitive method for the quantitation on microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–256.
Carpenter J E. 2010. Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nature Biotechnology, 28, 319–321. 
Chen M, Zhao J Z, Collins H L, Earle E D, Cao J, Shelton A M. 2008. A critical assessment of the effects of Bt transgenic plants on parasitoids. PLoS ONE, 3, e2284.
Clark B W, Coats J R. 2006. Subacute effects of Cry1Ab Bt corn litter on the earthworm Eisenia fetida and the springtail Folsomia candida. Environmental Entomology, 35, 1121–1129.
Digilio M C, Sasso R, Di Leo M G, Iodice L, Monti M M, Santeramo R, Arpaia S, Guerrieri E. 2012. Interactions between Bt-expressing tomato and non-target insects: The aphid Macrosiphum euphorbiae and its natural enemies. Journal of Plant Interactions, 7, 71–77.
Edgerton M D, Fridgen J, Anderson J R, Ahlgrim J, Criswell M, Dhungana P, Gocken T, Li Z, Mariappan S, Pilcher C D, Rosielle A, Stark S B. 2012. Transgenic insect resistance traits increase corn yield and yield stability. Nature Biotechnology, 30, 493–496.
Feng H Q, Jin Y L, Li G P, Feng H Y. 2012. Establishment of an artificial diet for successive rearing of Apolygus lucorum (Hemiptera: Miridae). Journal of Economic Entomology, 105, 1921–1928.
Haye T, Kuhlmann U, Goulet H, Mason P. 2007. Controlling Lygus plant bugs (Heteroptera: Miridae) with European Peristenus relictus (Hymenoptera: Braconidae) in Canada - risky or not? Bulletin of Entomological Research, 96, 187–196.
James C. 2018. Global status of commercialized biotech/GM crops in 2017: Biotech crop adoption surges as economic benefits accumulate in 22 years. In: International Service for the Acquisition of Agri-biotech Applications. Ithaca, NY.
Li Y H, Hallerman E M, Peng Y F. 2018. How can China prepare for the domestic cultivation of Bt maize? Trends Food Science Technology, 73, 87–88.
Li Y H, Peng Y F, Hallerman E M, Wu K M. 2014. Biosafety management and commercial use of genetically modified crops in China. Plant Cell Reports, 33, 565–573.
Li Y H, Romeis J, Wang P, Peng Y F, Shelton A M. 2011. A comprehensive assessment of the effects of Bt cotton on Coleomegilla maculata demonstrates no detrimental effects by Cry1Ac and Cry2Ab. PLoS ONE, 6, e22185.
Li Y H, Romeis J, Wu K M, Peng Y F. 2013. 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, 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, 07679.
Liang G M, Tan W J, Guo Y Y. 1999. An improvement in the technique of artificial rearing cotton bollworm. Plant Protection, 2, 15–17. (in Chinese)
Liu X X, Chen M, Onstad D, Roush R, Shelton A M. 2011. Effect of Bt broccoli and resistant genotype of Plutella xylostella (Lepidoptera: Plutellidae) on development and host acceptance of the parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae). Transgenic Research, 20, 887–897.
Liu X X, Zhang Q W, Cai Q N, Li J C, Dong J. 2004. Effects of Bt protein on development of different strains of the cotton bollworm, Helicoverpa armigera (Hübner) and the parasitoid, Microplitis mediator (Haliday). Acta Entomologica Sinica, 47, 461–466. (in Chinese)
Lövei G L, Andow D A, Arpaia S. 2009. Transgenic insecticidal crops and natural enemies: A detailed review of laboratory studies. Environmental Entomology, 38, 293–306.
Lu Y H, Wu K M, Cai X M, Liu Y Q. 2008. A rearing method for mirids using the green bean, Phaseolus vulgaris in the laboratory. Acta Phytophylacica Sinica, 35, 215–219. (in Chinese)
Lu Y H, Wu K M, Jiang Y Y, Xia B, Li P, Feng H Q, Wyckhuys K A, Guo Y Y. 2010. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science, 328, 1151–1154.
Luo S P, Li H M, Lu Y H, Zhang F, Haye T, Kuhlmann U, Wu K M. 2014. Functional response and mutual interference of Peristenus spretus (Hymenoptera: Braconidae), a parasitoid of Apolygus lucorum (Heteroptera: Miridae). Biocontrol Science and Technology, 24, 247–256.
Luo S P, Zhang F, Wu K M. 2015. Effect of temperature on the reproductive biology of Peristenus spretus (Hymenoptera: Braconidae), a biological control agent of the plant bug Apolygus lucorum (Hemiptera: Miridae). Biocontrol Science and Technology, 25, 1410–1425.
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.
Perry J N, Devos Y, Arpaia S, Bartsch D, Ehlert C, Gathmann A, Hails R S, Hendriksen N B, Kiss J, Messean A, Mestdagh S, Neemann G, Nuti M, Sweet J B, Tebbe C C. 2012. Estimating the effects of Cry1F Bt-maize pollen on non-target Lepidoptera using a mathematical model of exposure. Journal of Applied Ecology, 49, 29–37.
Raybould A, Kilby P, Graser G. 2013. Characterising microbial protein test substances and establishing their equivalence with plant-produced proteins for use in risk assessments of transgenic crops. Transgenic Research, 22, 445–460.
Romeis J, Bartsch D, Bigler F, Candolfi P, Gielkens M M C, Hartley S E, Hellmich R L, Huesing J E, Jepson P C, Layton R, Quemada H, Raybould A, Rose R I, Schiemann J, Sears M K, Shelton A M, Sweet J, Vaituzis Z, Wolt J D. 2008. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nature Biotechnology, 26, 203–208.
Sharma H C, Dhillon M K, Arora R. 2008. Effects of Bacillus thuringiensis δ-endotoxin-fed Helicoverpa armigera on the survival and development of the parasitoid Campoletis chlorideae. Entomologia Experimentalis et Applicata, 126, 1–8.
Sivasupramaniam S, Moar W J, Ruschke L G, Osborn J A, Jiang C, Sebaugh J L, Brown G R, Shappley Z W, Oppenhutzen M E, Mullins J W, Greenplate J T. 2008. Toxicity and characterization of cotton expressing Bacillus thuringiensis Cry1Ac and Cry2Ab2 proteins for control of Lepidopteran pests. Journal of Economic Entomology, 101, 546–554.
Tian J C, Romeis J, Liu K, Zhang F C, Zheng X S, Xu H X, Chen G H, He X C, Lu Z X. 2017. Assessing the effects of Cry1C rice and Cry2A rice to Pseudogonatopus flavifemur, a parasitoid of rice planthoppers. Scientific Reports, 7, 7838.
Tian J C, Wang X P, Long L P, Romeis J, Naranjo S E, Hellmich R L, Shelton A M. 2014. Eliminating host-mediated effects demonstrates Bt maize producing Cry1F has no adverse effects on the parasitoid Cotesia marginiventris. Transgenic Research, 23, 257–264.
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 Y, 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.
Wei J Z, Guo Y Y, Liang G M, Wu K M, Zhang J, Tabashnik B E, Li X C. 2015. Cross-resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against the cotton bollworm. Scientific Reports, 5, 07714.
Wolfenbarger L L, Naranjo S E, Lundgren J G, Bitzer R J, Watrud L S. 2008. Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS ONE, 3, e2118.
Wu K M, Lu Y H. 2008. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. China Basic Science, 321, 1676–1677. (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.
Yu H L, Li Y H, Wu K M. 2011. Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms. Journal of Integrative Plant Biology, 53, 520–538.
Yuan Y Y, Ke X, Chen F J, Krogh P H, Ge F. 2011. Decrease in catalase activity of Folsomia candida fed a Bt rice diet. Environmental Pollution, 159, 3714–3720.
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 L, Jiang S J, Jiang X F, Yang H X, Luo L Z. 2011. The influence of Cry1Ab toxin on the growth and development of Microplitis pallidipes. Plant Protection, 37, 107–111. (in Chinese)
Zhang X J, Li Y H, Romeis J, Yin X M, Wu K M, Peng Y F. 2014. Use of a pollen-based diet to expose the ladybird beetle Propylea japonica to insecticidal proteins. PLoS ONE, 9, e85395.
Zhao M, Li Y H, Yuan X D, Liang G M, Wang B J, Liu C, Khaing M M. 2018. Establishment of a dietary exposure assay for evaluating the toxicity of insecticidal compounds to Apolygus lucorum (Hemiptera: Miridae). Environmental Pollution, 237, 414–423.
Zhao Y, Zhang S, Luo J Y, Wang C Y, Lv L M, Wang X P, Cui J J, Lei C L. 2016. Bt proteins Cry1Ah and Cry2Ab do not affect cotton aphid Aphis gossypii and ladybeetle Propylea japonica. Scientific Reports, 6, 20368.
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