Biodiversity Science ›› 2018, Vol. 26 ›› Issue (6): 636-644.doi: 10.17520/biods.2017315

• Review • Previous Article     Next Article

Effects of Bt crops on non-target insect pests

Zhengjun Guan1, Shunbao Lu2, Yanlin Huo3, Haoyong Hao3, Jianbin Cao1, Wei Wei4, *(), Biao Liu5, *()   

  1. 1 Department of Biological Sciences, Yuncheng University, Yuncheng, Shanxi 044000
    2 College of Biosciences, Jiangxi Normal University, Nanchang 330022
    3 Science Experimental Center, Yuncheng University, Yuncheng, Shanxi 044000
    4 State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093
    5 Nanjing Institute of Environmental Sciences of the Ministry of Environmental Protection, Nanjing 210042
  • Received:2018-04-04 Accepted:2018-04-17 Online:2018-09-11
  • Wei Wei,Liu Biao E-mail:weiwei@ibcas.ac.cn;liubiao@nies.org
  • About author:

    # Co-first authors

The long-term large-scale planting of genetically modified (GM) crops may have potential impacts on the health and stability of agricultural ecosystems while benefitting agricultural production. Bt proteins expressed in Bt crops have a good control on target pests. However, non-target insects that are not susceptible to Bt toxins may have increased populations rapidly, causing significant damage to crops. With the long-term continued cultivation of insect-resistant GM crops, different reports and views on the amounts of pesticide applications have been reported. Based on existing research, we reviewed the characteristics and status of non-target insect pest outbreaks and analyzed the main causes of the outbreaks (such as insecticide use, decrease of natural enemies, and species replacement). In addition, we discussed the effects of GM crops on non-target pests over long-term cultivation using Bt corn and cotton as examples. Given the existing problems of non-target insect outbreaks due to commercial applications of Bt crops, further studies on monitoring the efficacies of insect-resistant GM crops are necessary to prevent outbreaks of non-target pests needed for sustainable agriculture.

Key words: insect-resistanceBt crops, non-target pests, outbreak, risk assessment

[1] Andow DA, Lövei GL, Arpaia S (2006) Ecological risk assessment for Bt crops. Nature Biotechnology, 24, 749-751.
[2] Andow DA, Lövei GL, Arpaia S (2009) Cry toxins and proteinase inhibitors in transgenic plants do have non-zero effects on natural enemies in the laboratory: Rebuttal to Shelton et al. 2009. Environmental Entomology, 38, 1528-1532.
[3] Areal FJ, Riesgo L (2015) Probability functions to build composite indicators: A methodology to measure environmental impacts of genetically modified crops. Ecological Indicators, 52, 498-516.
[4] Areal FJ, Riesgo L, Rodriguez-Cerezo E (2013) Economic and agronomic impact of commercialized GM crops: A meta-analysis. Journal of Agricultural Science, 151, 7-33.
[5] Arpaia S (2010) Genetically modified plants and non-target organisms: Analysing the functioning of the agro-ecosystem. Collection of Biosafety Reviews, 5, 12-80.
[6] Arpaia S, Birch ANE, Kiss J, Loon JJAV, Messéan A (2017) Assessing environmental impacts of genetically modified plants on non-target organisms: The relevance of in planta studies. Science of the Total Environment, 583, 123-132.
[7] Benbrook CM (2012) Impacts of genetically engineered crops on pesticide use in the U.S. —the first sixteen years. Environmental Sciences Europe, 24, 24.
[8] Brévault T, Heuberger S, Zhang M, Ellers-Kirk C, Ni X, Masson L, Li X, Tabashnik BE, Carrière Y (2013) Potential shortfall of pyramided transgenic cotton for insect resistance management. Proceedings of the National Academy of Sciences, USA, 110, 5806-5811.
[9] Brookes G, Barfoot P (2016) GM Crops: Global Socio-Economic and Environmental Impacts 1996-2014. PG Economics Ltd., UK.
[10] Campos RC, Hernandez MIM (2015) Changes in the dynamics of functional groups in communities of dung beetles in Atlantic forest fragments adjacent to transgenic maize crops. Ecological Indicators, 49, 216-227.
[11] Carrière Y, Crowder DW, Tabashnik BE (2010) Evolutionary ecology of insect adaptation to Bt crops. Evolutionary Applications, 3, 561-573.
[12] Catangui MA, Berg RK (2006) Western bean cutworm, Striacosta albicosta (Smith) (Lepidoptera: Noctuidae), as a potential pest of transgenic Cry1Ab Bacillus thuringiensis corn hybrids in South Dakota. Environmental Entomology, 35, 1439-1452.
[13] Catarino R, Ceddia G, Areal FJ, Park J (2015) The impact of secondary pests on Bacillus thuringiensis (Bt) crops. Plant Biotechnology Journal, 13, 601-612.
[14] Chen M, Ye G, Liu Z, Fang Q, Hu C, Peng YF, Shelton AM (2009) Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology, 18, 230-238.
[15] Dorhout DL, Rice ME (2010) Intraguild competition and enhanced survival of western bean cutworm (Lepidoptera: Noctuidae) on transgenic Cry1Ab (MON810) Bacillus thuringiensis corn. Journal of Economic Entomology, 103, 54-62.
[16] Dowd-Uribe B (2014) Engineering yields and inequality? How institutions and agro-ecology shape Bt cotton outcomes in Burkina Faso. Geoforum, 53, 161-171.
[17] EFSA (2010) EFSA Panel on genetically modified organisms (GMO): Scientific opinion on the assessment of potential impacts of genetically modified plants on non-target organisms. EFSA Journal, 8, 73.
[18] Eizaguirre M, Madeira F, López C (2010) Effects of Bt maize on non-target Lepidopteran pests. IOBC/WPRS Betin, 52, 49-55.
[19] Fu Q, Lai FX, Chen Y, Li KL (2013) A review of the ecological safety of the insect-resistant transgenic rices to non-target organisms. Plant Physiology Journal, 49, 655-663. (in Chinese)
[傅强, 赖凤香, 陈洋, 李凯龙 (2013) 抗虫转基因水稻对非靶标生物的生态安全性研究进展. 植物生理学报, 49, 655-663.]
[20] Gassmann AJ, Carrière Y, Tabashnik BE (2009) Fitness costs of insect resistance to Bacillus thuringiensis. Annual Review of Entomology, 54, 147-163.
[21] González-Cabrera J, García M, Hernández-Crespo P, Farinós GP, Ortego F, Castanera P (2013) Resistance to Bt maize in Mythimna unipuncta (Lepidoptera: Noctuidae) is mediated by alteration in Cry1Ab protein activation. Insect Biochemistry and Molecular Biology, 43, 635-643.
[22] Gressel J, Gassmann AJ, Owen MD (2016) How well will stacked transgenic pest/herbicide resistances delay pests from evolving resistance? Pest Management Science, 73, 22.
[23] Gross K, Rosenheim JA (2011) Quantifying secondary pest outbreaks in cotton and their monetary cost with causal-inference statistics. Ecological Applications, 21, 2770-2780.
[24] Guan ZJ, Lu SB, Huo YL, Guan ZP, Liu B, Wei W (2016) Do genetically modified plants affect adversely on soil microbial communities? Agriculture, Ecosystems and Environment, 235, 289-305.
[25] Guedes RNC, Cutler GC (2014) Insecticide-induced hormesis and arthropod pest management. Pest Management Science, 70, 690-697.
[26] Hagenbucher S, Wackers FL, Wettstein FE, Olson DM, Ruberson JR, Romeis J (2013) Pest trade-offs in technology: Reduced damage by caterpillars in Bt cotton benefits aphids. Proceedings of the Royal Society B, 280, 1-8.
[27] Han LZ, Bai SX, Zhao JZ, Wang ZY, Wu KM (2007) Progress in ecological biosafety of insect-resistant transgenic cotton and corn in relation to arthropods. Acta Entomologica Sinica, 50, 727-736. (in Chinese with English abstract)
[韩兰芝, 白树雄, 赵建周, 王振营, 吴孔明 (2007) 转基因抗虫棉花和玉米与节肢动物相关的生态安全性研究进展. 昆虫学报, 50, 727-736.]
[28] Han P, Niu CY, Desneux N (2013) Identification of top-down forces regulating cotton aphid population growth in transgenic Bt cotton in central China. PLoS ONE, 9, e102980.
[29] Hardke JT, Leonard BR, Huang F, Jackson RE (2011) Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Protection, 30, 168-172.
[30] Huang J, Rozelle S, Pray C, Wang Q (2002) Plant biotechnology in China. Science, 295, 674-676.
[31] Hutchison WD, Burkness EC, Mitchell PD (2010) Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science, 330, 222-225.
[32] Hutchison WD, Hunt TE, Hein GL (2011) Genetically engineered Bt corn and range expansion of the western bean cutworm (Lepidoptera: Noctuidae) in the United States: A response to Greenpeace Germany. Journal of Integrated Pest Management, 2, B1-B8.
[33] ISAAA (2016) Global Status of Commercialized Biotech/GM Crops: 2016. ISAAA Brief No. 52. ISAAA: Ithaca, NY.
[34] Kilic A, Akay MT (2008) A three generation study with genetically modified Bt corn in rats: Biochemical and histopathological investigation. Food & Chemical Toxicology, 46, 1164-1170.
[35] Krishna VV, Qaim M (2012) Bt cotton and sustainability of pesticide reductions in India. Agricultural Systems, 107, 47-55.
[36] Kruger M, Van Rensburg JBJ, Van den Berg J (2012) Transgenic Bt maize: Farmers’ perceptions, refuge compliance and reports of stem borer resistance in South Africa. Journal of Applied Entomology, 136, 38-50.
[37] Kumar R, Tian JC, Naranjo SE, Shelton AM (2014) Effects of Bt cotton on Thrips tabaci (Thysanoptera: Thripidae) and its predator, Orius insidiosus (Hemiptera: Anthocoridae). Journal of Economic Entomology, 107, 927.
[38] Ladics GS, Bartholomaeus A, Bregitzer P, Doerrer NG, Gray A, Holzhauser T, Jordan M, Keese P, Kok E, Macdonald P, Parrott W, Privalle L, Raybould A, Rhee SY, Rice E, Romeis J, Vaughn J, Wal JM, Glenn K (2015) Genetic basis and detection of unintended effects in genetically modified crop plants. Transgenic Research, 24, 587-603.
[39] Lin ZF, Chen HY, Ji XC (2015) Insect resistance to Bt crops: Possible mechanism and resistance management strategy. Journal of Tropical Biology, 6, 497-503. (in Chinese with English abstract)
[林珠凤, 陈海燕, 吉训聪 (2015) 害虫对转Bt基因作物的抗性及治理. 热带生物学报, 6, 497-503.]
[40] Lindroth E, Hunt TE, Skoda SR, Culy MD, Lee D, Foster JE (2012) Population genetics of the western bean cutworm (Lepidoptera: Noctuidae) across the United States. Annals of the Entomological Society of America, 105, 685-692.
[41] Liu B (2016) Research progresses on the environmental safety of transgenic Bt plants with insect-resistant trait. Journal of Nanjing Normal University (Natural Science Edition), 39, 1025-1030. (in Chinese with English abstract)
[刘标 (2016) 抗虫转Bt基因植物的环境安全研究进展. 南京师大学报(自然科学版), 39, 1025-1030.]
[42] Lövei GL, Andow DA, Arpaia S (2009) Transgenic insecticidal crops and natural enemies: A detailed review of laboratory studies. Environmental Entomology, 38, 293-306.
[43] Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature, 487, 362-365.
[44] Lu Y, Wu K, Jiang Y, Xia B, Li P, Feng H, Wyckhuys KA, Guo Y (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science, 328, 1151-1154.
[45] Lu YH (2012) Advance in insect pest management in Bt cotton worldwide Chinese. Chinese Journal of Applied Entomology, 49, 809-819. (in Chinese with English abstract)
[陆宴辉 (2012) Bt棉花害虫综合治理研究前沿. 应用昆虫学报, 49, 809-819.]
[46] Lu YH, Liang GM (2016) Research advance on the succession of insect pest complex in Bt crop ecosystem. Plant Protection, 42, 7-11. (in Chinese with English abstract)
[陆宴辉, 梁革梅 (2016) Bt作物系统害虫发生演替研究进展. 植物保护, 42, 7-11.]
[47] Lu YH, Qiu F, Feng HQ, Li HB, Yang ZC, Wyckhuys KAG, Wu KM (2008) Species composition and seasonal abundance of pestiferous plant bugs (Hemiptera: Miridae) on Bt cotton in China. Crop Protection, 27, 465-472.
[48] Luttrell RG, Teague TG, Brewer MJ (2015) Cotton insect pest management. In: Cotton, 2nd edn (eds David DF, Richard GP). Agronomy Monograph 57.pp. 509-546. ASA, CSSA, and SSSA, Madison, WI .
[49] Ma H, Xia XM, Zhou Y, Zhao M, Wang HY (2009) Impact of transgenic Bt cotton on non-target insects. Chinese Agricultural Science Bulletin, 25, 214-218. (in Chinese with English abstract)
[马惠, 夏晓明, 周玉, 赵鸣, 王红艳 (2009) 转Bt基因抗虫棉对非靶标昆虫的影响. 中国农学通报, 25, 214-218.]
[50] 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.
[51] Mccoll SA, Khan M, Umina PA (2011) Review of the biology and control of Creontiades dilutus (Stål) (Hemiptera: Miridae). Austral Entomology, 50, 107-117.
[52] Meissle M, Mouron P, Musa T, Bigler F, Pons X (2010) Pests, pesticide use and alternative options in European maize production: Current status and future prospects. Journal of Applied Entomology, 134, 357-375.
[53] Naranjo SE (2005) Long-term assessment of the effects of transgenic Bt cotton on the abundance of non-target arthropod natural enemies. Environmental Entomology, 34, 1193-1210.
[54] Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Reviews, 4(11), 1-23.
[55] Naranjo SE (2010) Impacts of Bt transgenic cotton on integrated pest management. Journal of Agricultural and Food Chemistry, 59, 5842-5851.
[56] Naranjo SE (2014) Effects of GM crops on non-target organisms. In: Plant Biotechnology (ed Naranjo SE), pp. 129-142, Springer International Publishing, New York.
[57] Naranjo SE, Ellsworth PC (2009) The contribution of conservation biological control to integrated control of Bemisia tabaci in cotton. Biological Control, 51, 458-470.
[58] Naranjo SE, Ruberson JR, Sharma HC, Wilson L, Wu KM (2008) The present and future role of insect-resistant GM cotton in IPM. In: Integration of Insect-Resistant Genetically Modified Crops Within IPM Programs (eds Romeis J, Shelton AM, Kennedy GG), pp. 159-194. Springer International Publishing, New York.
[59] National Academies of Sciences, Engineering, and Medicine(2016) Genetically Engineered Crops: Experiences and Prospects. The National Academies Press, Washington, DC.
[60] Pemsl DE, Voelker M, Wu L, Waibel H (2011) Long-term impact of Bt cotton: Findings from a case study in China using panel data. International Journal of Agricultural Sustainability, 9, 508-521.
[61] Pérez-Hedo M, López C, Albajes R, Eizaguierre M (2012) Low susceptibility of non-target Lepidopteran maize pests to the Bt protein Cry1Ab. Bulletin of Entomological Research, 102, 737-743.
[62] Razze JM, Mason CE (2012) Dispersal behavior of neonate European corn borer (Lepidoptera: Crambidae) on Bt corn. Journal of Economic Entomology, 105, 1214-1223.
[63] Ricroch A, Chopra S, Fleischer S (2014) Plant Biotechnology: Experience and Future Prospects. Springer International Publishing, New York.
[64] Shahid AA, Bano S, Khalid S, Samiullah TR, Bajwa KS, Ali MA (2016) Biosafety assessment of transgenic Bt cotton on model animals. Advancements in Life Sciences, 3(3), 97-108.
[65] Shi G, Chavas JP, Lauer J (2013) Commercialized transgenic traits, maize productivity and yield risk. Nature Biotechnology, 31, 111-114.
[66] Snow AA, Andow DA, Gepts P, Hallerman E, Power A, Tiedje J, Wolfenbarger L (2005) Genetically engineered organisms and the environment: Current status and recommendations. Ecological Applications, 15, 377-404.
[67] Stephens EJ, Losey JE, Allee LL, DiTommaso A Bodner C, Breyre A (2012) The impact of Cry3Bb Bt-maize on two guilds of beneficial beetles. Agriculture, Ecosystems and Environment, 156, 72-81.
[68] Tanwar RK, Jeyakumar P, Singh A, Jafri AA, Bambawale OM (2011) Survey for cotton mealybug, Phenacoccus solenopsis (Tinsley) and its natural enemies. Journal of Environmental Biology, 32, 381-384.
[69] Tindall KV, Siebert MW, Leonard BR, All J, Haile FJ (2009) Efficacy of Cry1Ac: Cry1F proteins in cotton leaf tissue against fall armyworm, beet armyworm, and soybean looper (Lepidoptera: Noctuidae). Journal of Economic Entomology, 102, 1497-1505.
[70] Virla EG, Casuso M, Frias EA (2010) A preliminary study on the effects of a transgenic corn event on the non-target pest Dalbulus maidis (Hemiptera: Cicadellidae). Crop Protection, 29, 635-638.
[71] Wang YY, Li YH, Chen XP, Wu HJ, Peng YF (2011) Progress in the assessment of ecological effects of insect-resistant plants on non-target arthropods. Journal of Biosafety, 20, 100-107. (in Chinese with English abstract)
[王园园, 李云河, 陈秀萍, 武红巾, 彭于发 (2011) 抗虫转基因植物对非靶标节肢动物生态影响的研究进展. 生物安全学报, 20, 100-107.]
[72] Wei W, Guan ZJ, Ma KP (2016) Advances on ecological risk assessment of genetically modified crops. In: New Biology Yearbook 2015(ed. the Editorial Board of New Biology Yearbook 2015), pp. 137-155. Science Press, Beijing. (in Chinese)
[魏伟, 关正君, 马克平 (2016) 转基因作物的生态风险评价研究进展. 见: 新生物学年鉴2015 (新生物学年鉴2015编委会主编), 137-155页. 科学出版社, 北京.]
[73] Wei W, Ma KP (2016) Transgenic organisms and biosafety. Bulletin of Chinese Academy of Sciences, 31, 405-413. (in Chinese with English abstract)
[魏伟, 马克平 (2016) 转基因与生物安全. 中国科学院院刊, 31, 405-413.]
[74] Wei W, Schuler TH, Clark SJ, Stewart CN, Poppy GM (2008) Movement of transgenic plant-expressed Bt Cry1Ac proteins through high trophic levels. Journal of Applied Entomology, 132, 1-11.
[75] Wolfenbarger LLR, 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.
[76] Wu KM, Guo YY (2005) The evolution of cotton pest management practices in China. Annual Review of Entomology, 50, 31-52.
[77] Xu N, Fok M, Bai L, Zhou L (2008) Effectiveness and chemical pest control of Bt-cotton in the Yangtze River Valley, China. Crop Protection, 27, 1269-1276.
[78] Yan LZ, Zhao CY, Liu XY, Lv FC, Guan X, Liu MH, Li JS (2011) Influence and mechanism of transgenic Bt crops on the food chain: Plant-pest-predator. Plant Protection, 37(6), 27-31. (in Chinese with English abstract)
[闫亮珍, 赵彩云, 柳晓燕, 吕凤春, 关潇, 刘茂华, 李俊生 (2011) 转Bt基因作物对植物-害虫-天敌食物链的影响. 植物保护, 37(6), 27-31.]
[79] Yang H, Peng Y, Tian J, Wang J, Song Q, Wang Z (2017) Review: Biosafety assessment of Bt rice and other Bt crops using spiders as example for non-target arthropods in China. Plant Cell Reports, 36(4), 1-13.
[80] Yang Y, Li YH, Cao FQ, Cheng LS, Peng YF (2014) Progress in the assessment of ecological effects of insect-resistant Bt crops on non-target of Lepidopteran insects. Journal of Biosafety, 23, 224-237. (in Chinese with English abstract)
[杨艳, 李云河, 曹凤勤, 程立生, 彭于发 (2014) 转Bt基因抗虫作物对鳞翅目非靶标昆虫生态影响的研究进展. 生物安全学报, 23, 224-237.]
[81] Ye GY, Chen Y, Tian JC, Peng YF (2011) The effects of transgenic Bt insect-resistant crops on non-target organisms. Plant Protection, 37(6), 1-10. (in Chinese with English abstract)
[叶恭银, 陈洋, 田俊策, 彭于发 (2011) 转Bt基因抗虫作物对非靶标生物的影响. 植物保护, 37(6), 1-10.]
[82] Yuan YY, Ge F (2010) Effects of transgenic Bt crops on non-target soil animals. Chinese Journal of Applied Ecology, 21, 1339-1345. (in Chinese with English abstract)
[袁一杨, 戈峰 (2010) 转Bt基因作物对非靶标土壤动物的影响. 应用生态学报, 21, 1339-1345.]
[83] Zeilinger AR, Olson DM, Andow DA (2016) Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton. Ecological Applications, 26, 1047-1054.
[84] Zeng RS, Sun ZX, Song YY, Lu K, Zhu KY (2016) The mechanism of phytophagous insects accommodating protease inhibitors. In: New Biology Yearbook 2015(ed. the Editorial Board of New biology Yearbook 2015). Science Press, Beijing. 117-137. (in Chinese)
[曾任森, 孙仲享, 宋圆圆, 卢凯, 朱克岩 (2016) 植食性昆虫适应植物蛋白酶抑制剂的机制. 见: 新生物学年鉴2015 (新生物学年鉴2015编委会主编) , 117-137页. 科学出版社, 北京.]
[85] Zhao JH, Ho P, Azadi H (2011) Benefits of Bt cotton counterbalanced by secondary pests? Perceptions of ecological change in China. Environmental Monitoring and Assessment, 173, 985-994.
[1] Haining Qin, Lina Zhao, Shengxiang Yu, Huiyuan Liu, Bo Liu, Nianhe Xia, Hua Peng, Zhenyu Li, Zhixiang Zhang, Xingjin He, Linke Yin, Yulin Lin, Quanru Liu, Yuantong Hou, Yan Liu, Qixin Liu, Wei Cao, Jianqiang Li, Shilong Chen, Xiaohua Jin, Tiangang Gao, Wenli Chen, Haiying Ma, Yuying Geng, Xiaofeng Jin, Chaoyang Chang, Hong Jiang, Lei Cai, Chunxin Zang, Jianyong Wu, Jianfei Ye, Yangjun Lai, Bing Liu, Qinwen Lin, Naxin Xue. Evaluating the endangerment status of China’s angiosperms through the red list assessment [J]. Biodiv Sci, 2017, 25(7): 745-757.
[2] Shan Li,Jiakuan Chen,Xiaoming Wang. Global distribution, entry routes, mechanisms and consequences of invasive freshwater fish [J]. Biodiv Sci, 2016, 24(6): 672-685.
[3] Minghao Qiu,Yue Huang,Jieqing Zhang,Yi Huang. International negotiations on synthetic biology and China’s implementation strategies within the Convention on Biological Diversity framework [J]. Biodiv Sci, 2016, 24(1): 114-120.
[4] Weichang Huang,Xiangyu Zhou,Ziyi Ni,Li Shao. An assessment of the extinction risk of Calanthe from China based on specimens and field observations [J]. Biodiv Sci, 2015, 23(4): 493-498.
[5] Zhengjun Guan, Lei Pei, Markus Schmidt, Wei Wei. Assessment and management of biosafety in synthetic biology [J]. Biodiv Sci, 2012, 20(2): 138-150.
[6] Ruiting Ju, Bo Li. A risk analysis system for alien species in urban green spaces and application to the 2010 Expo, Shanghai [J]. Biodiv Sci, 2012, 20(1): 12-23.
[7] Lei Wang, Chao Yang, Bao-Rong Lu. Establishing diagnostic platform for environmental biosafety assessment of genetically modified plants based on the decision-tree method [J]. Biodiv Sci, 2010, 18(3): 215-226.
[8] Bao-Rong Lu, Hui Xia, Xiao Yang, Xin Jin, Ping Liu, Wei Wang. Evolutionary theory of hybridization-introgression: its implication in en-vironmental risk assessment and research of transgene escape [J]. Biodiv Sci, 2009, 17(4): 362-377.
[9] LI Jian, MA Jian-Hua, SONG Bo. HEAVY METAL ACCUMULATION AND HEALTH RISK ASSESSMENT IN THE ROADSIDE SOIL-WHEAT SYSTEM ALONG ZHENGZHOU-KAIFENG HIGHWAY, CHINA [J]. Chin J Plan Ecolo, 2009, 33(3): 624-628.
[10] LI Yi-Ming. Population viability analysis in conservation biology: precision and uses [J]. Biodiv Sci, 2003, 11(4): 340-350.
[11] WAN Fang-Hao, GUO Jian-Ying, WANG De-Hui. Alien invasive species in China: their damages and management strategies [J]. Biodiv Sci, 2002, 10(1): 119-125.
[12] Qian Yingqian, Tian Yan, Wei Wei. Ecological Risk Assessment of Transgenic Plant [J]. Chin J Plan Ecolo, 1998, 22(4): 289-299.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Yong-Chang SONG, En-Rong YAN, Kun SONG. An update of the vegetation classification in China[J]. Chin J Plan Ecolo, 2017, 41(2): 269 -278 .
[2] Xinjun LiaoGenetic diversity of five native Chinese yak breeds based on microsatel-lite DNA markers[J]. Biodiv Sci, 2008, 16(2): 156 -165 .
[3] He He, Jin Chen. Visiting motivation and satisfaction of visitors to Chinese botanical gardens[J]. Biodiv Sci, 2011, 19(5): 589 -596 .
[4] YAN Zheng-Bing, KIM Nam-Young, HAN Ting-Shen, FANG Jing-Yun, and HAN Wen-Xuan. Effects of nitrogen and phosphorus fertilization on leaf carbon, nitrogen and phosphorus stoichiometry of Arabidopsis thaliana[J]. Chin J Plan Ecolo, 2013, 37(6): 551 -557 .
[5] . [J]. Chin J Plan Ecolo, 2006, 30(6): 968 .
[6] Zhao Hui-Ru, Yang Ya-Ling. New Taxa and New Combinations of Indocalamus from China[J]. J Syst Evol, 1985, 23(6): 460 -465 .
[7] ZHAO Yun-Yun ZHOU Xiao-Mei YANG Cai. Production of Hybrid F1 Between Avena magna and Avena nuda and It''s Identification[J]. Chin Bull Bot, 2003, 20(03): 302 -306 .
[8] Huang Quan, Li Yi-de, Zheng De-zhang, Zhang Jia-cheng, Wang Li-li, Jiang You-xu, Zhao Yan-min. Study of Tropical Vegetation Series in Jianfengling Region, Hainan Island[J]. Chin J Plan Ecolo, 1986, 10(2): 90 -105 .
[9] LIU Jian-Fu, YANG Dao-Mao, OUYANG Ming-An, WANG Li-Na, ZHANG Yong, ZENG Ming. INFLUENCE OF METHANOL ELUATES FRACTIONATED FROM MACADAMIA INTEGRIFOLIAROOTS ON SPORE GERMINATION AND HYPHAL GROWTH OF AM FUNGI[J]. Chin J Plan Ecolo, 2005, 29(6): 1038 -1042 .
[10] Lu Qingguang. The importance of classical biological control to biodiversity protection[J]. Biodiv Sci, 1997, 05(3): 224 -230 .