CO_2浓度倍增影响转Bt水稻非靶标害虫褐飞虱的生长发育及取食行为
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摘要
近年来,大气CO_2浓度升高等全球气候变化和转Bt作物非靶标害虫抗虫性等问题备受关注.大气CO_2浓度升高直接或间接地影响植食性昆虫,而迄今为止有关大气CO_2浓度升高对刺吸式昆虫(同时也是转Bt作物的非靶标害虫)的影响结论不一,且对其刺吸取食行为的影响研究少有报道.本研究利用智能人工气候箱设置CO_2浓度,研究大气CO_2浓度倍增(800μL·L-1)对转Bt水稻的非靶标害虫褐飞虱取食行为及其生长发育和繁殖等的影响.结果表明:大气CO_2浓度倍增对褐飞虱卵和若虫历期、成虫体质量和寿命,以及4龄和5龄若虫的刺吸取食行为等都具有显著影响,但对其繁殖力影响不显著.与对照CO_2浓度(400μL·L-1)相比,倍增CO_2浓度处理下褐飞虱的卵和若虫历期及雌成虫寿命分别显著缩短了4.0%、4.2%和6.6%;长翅型成虫比例显著增加了11.6%;初羽化成虫体质量降低,且雌成虫体质量显著降低了2.2%;此外,倍增CO_2浓度处理下褐飞虱4龄和5龄若虫口针的刺探效率都显著增加;其中,N4b波的持续时间分别显著延长了60.0%和50.1%,频次分别显著增加了230.0%和155.9%.可见,CO_2浓度倍增可通过提高褐飞虱的刺吸取食而促进其生长发育,并缩短其世代历期、提高长翅成虫比例,最终导致大气CO_2浓度升高下转Bt水稻的非靶标害虫褐飞虱发生危害严重,并面临其迁飞扩散为害加重的风险.
In recent years,the two issues of climate change including elevated CO_2 etc.,and resistance of transgenic Bt crops against non-target insect pests have received widespread attention.Elevated CO_2 can affect the herbivorous insects. To date,there is no consensus about the effect of elevated CO_2 on the suck-feeding insect pests( non-target insect pests of transgenic Bt crops). Its effects on the suck-feeding behavior have rarely been reported. In this study,CO_2 levels were set up in artificial climate chamber to examined the effects of ambient( 400 μL·L-1) and double-ambient( 800 μL·L-1) CO_2 levels on the suck-feeding behavior,growth,development,and reproduction of the non-target insect pest of transgenic Bt rice,brown planthopper,Nilaparvata lugens. The results showed that CO_2 level significantly affected the egg and nymph duration,longevity and body mass of adults,and feeding behavior of the 4 th and 5 th instar nymphs,while had no effect on the fecundity of N. lugens. The duration of eggs and nymphs,and the longevity of female adults were significantly shortened by 4.0%,4.2% and 6.6% respectively,the proportion of the macropterous adults was significantly increased by 11.6%,and the body mass of newly hatched female adults wassignificantly decreased by 2.2% by elevated CO_2. In addition,elevated CO_2 significantly enhanced the stylet puncturing efficiency of the 4 th and 5 th instar nymphs of N. lugens. The duration of phloem ingestion of the N4b waveform was significantly prolonged by 60. 0% and 50. 1%,and the frequency significantly was increased by 230.0% and 155.9% for the 4 th and 5 th instar nymphs of N. lugens by elevated CO_2,respectively. It was concluded that double-ambient CO_2 could promote the growth and development of N. lugens through enhancing its suck-feeding,shorten the generation life-span and increase the macropertous adults' proportion of N. lugens. Thus,it could result in the occurrence of non-target rice planthopper N. lugens and make the transgenic Bt crops face with harm risk due to migration and diffusion of N. lugens under elevated CO_2.
In recent years,the two issues of climate change including elevated CO_2 etc.,and resistance of transgenic Bt crops against non-target insect pests have received widespread attention.Elevated CO_2 can affect the herbivorous insects. To date,there is no consensus about the effect of elevated CO_2 on the suck-feeding insect pests( non-target insect pests of transgenic Bt crops). Its effects on the suck-feeding behavior have rarely been reported. In this study,CO_2 levels were set up in artificial climate chamber to examined the effects of ambient( 400 μL·L-1) and double-ambient( 800 μL·L-1) CO_2 levels on the suck-feeding behavior,growth,development,and reproduction of the non-target insect pest of transgenic Bt rice,brown planthopper,Nilaparvata lugens. The results showed that CO_2 level significantly affected the egg and nymph duration,longevity and body mass of adults,and feeding behavior of the 4 th and 5 th instar nymphs,while had no effect on the fecundity of N. lugens. The duration of eggs and nymphs,and the longevity of female adults were significantly shortened by 4.0%,4.2% and 6.6% respectively,the proportion of the macropterous adults was significantly increased by 11.6%,and the body mass of newly hatched female adults wassignificantly decreased by 2.2% by elevated CO_2. In addition,elevated CO_2 significantly enhanced the stylet puncturing efficiency of the 4 th and 5 th instar nymphs of N. lugens. The duration of phloem ingestion of the N4b waveform was significantly prolonged by 60. 0% and 50. 1%,and the frequency significantly was increased by 230.0% and 155.9% for the 4 th and 5 th instar nymphs of N. lugens by elevated CO_2,respectively. It was concluded that double-ambient CO_2 could promote the growth and development of N. lugens through enhancing its suck-feeding,shorten the generation life-span and increase the macropertous adults' proportion of N. lugens. Thus,it could result in the occurrence of non-target rice planthopper N. lugens and make the transgenic Bt crops face with harm risk due to migration and diffusion of N. lugens under elevated CO_2.
引文
[1]IPCC.Climate change 2007:The physical science basis//Solomon S,Qin D,Manning M,eds.Contribution of Working GroupⅠto the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge,UK:Cambridge University Press,2007
[2]Ainsworth EA,Long SP.What have we learned from 15years of free-air CO2enrichment(FACE)?A metaanalytic review of the responses of photosynthesis,canopy properties and plant production to rising CO2.New Phytologist,2005,165:351-371
[3]Ainsworth EA,Rogers A,Leakey AD,et al.Does elevated atmospheric[CO2]alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves?Journal of Experimental Botany,2007,58:579-591
[4]Long SP,Ainsworth EA,Leakey AD,et al.Global food insecurity.Treatment of major food crops with elevated carbon dioxide or ozone under large-scale fully open-air conditions suggests recent models may have overestimated future yields.Philosophical Transactions of the Royal Society of London,2005,360:2011-2020
[5]Stacey DA,Fellowes ME.Influence of elevated CO2on interspecfic interactions at higher trophic levels.Global Change Biology,2002,8:668-678
[6]Ge F(戈峰),Chen F-J(陈法军).Impacts of elevated CO2on insects.Acta Ecologica Sinica(生态学报),2006,26(3):935-944(in Chinese)
[7]Chen F-J(陈法军),Ge F(戈峰),Liu X-H(刘向辉).Responses of cotton to elevated CO2and the effects on cotton aphid occurrences.Acta Ecologica Sinica(生态学报),2004,24(5):991-996(in Chinese)
[8]Chen F-J(陈法军),Wu G(吴刚),Ge F(戈峰).Responses of spring wheat to elevated CO2and their effects on Sitobion avenae aphid growth,development and reproduction.Chinese Journal of Applied Ecology(应用生态学报),2006,17(1):91-96(in Chinese)
[9]Guo HJ,Sun YC,Li YF,et al.Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2.Global Change Biology,2013,19:3210-3223
[10]Sun YC,Guo HJ,Yuan L,et al.Plant stomatal closure improves aphid feeding under elevated CO2.Global Change Biology,2015,21:2739-2748
[11]Chen FJ,Wu G,Ge F.Impacts of elevated CO2on the population abundance and reproductive activity of aphid Sitobion avenae Fabricius feeding on spring wheat.Journal of Applied Entomology,2004,128:723-730
[12]Jiang SL,Liu TJ,Yu FL,et al.Feeding behavioral response of cotton aphid,Aphis gossypii,to elevated CO2:EPG test with leaf microstructure and leaf chemistry.Entomologia Experimentalis et Applicata,2016,160:219-228
[13]Bezemer TM,Jones TH.Plant-insect herbivore interactions in elevated atmospheric CO2:Quantitative analyses and guild effects.Oikos,1998,82:212-222
[14]Guo HJ,Sun YC,Li YF,et al.Elevated CO2decreases the response of the ethylene signaling pathway in Medicago truncatula and increases the abundance of the pea aphid.New Phytologist,2014,201:279-291
[15]Chen FJ,Wu G,Ge F,et al.Effects of elevated CO2and transgenic Bt cotton on plant chemistry,performance,and feeding of an insect herbivore,the cotton bollworm.Entomologia Experimentalis et Applicata,2005,115:341-350
[16]Chen F-J(陈法军),Wu G(吴刚),Ge F(戈峰).Impacts of elevated CO2on the growth,development,and reproduction of cotton aphid Aphis gossypii(Glover).Acta Ecologica Sinica(生态学报),2005,25(10):2601-2607(in Chinese)
[17]Mendelsohn M,Kough JL,Vaituzis Z,et al.Are Bt crops safe.Nature Biotechnology,2003,21:1003-1009
[18]Bernal CC,Aguda RM,Cohen MB.Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis.Entomologia Experimentalis et Applicata,2010,102:21-28
[19]Ramirez-Romero R,Desneux N,Chaufaux J,et al.Bt-maize effects on biological parameters of the nontarget aphid Sitobion avenae,(Homoptera:Aphididae)and Cry1Ab toxin detection.Pesticide Biochemistry&Physiology,2008,91:110-115
[20]Torres JB,Ruberson JR.Interactions of Bt-cotton and the omnivorous big-eyed bug Geocoris punctipes(Say),a key predator in cotton fields.Biological Control,2006,39:47-57
[21]Zhang GF,Wan FH,Murphy ST,et al.Reproductive biology of two nontarget insect species,Aphis gossypii(Homoptera:Aphididae)and Orius sauteri(Hemiptera:Anthocoridae),on Bt and non-Bt cotton cultivars.Environmental Entomology,2008,37:1035-1042
[22]Obrist LB,Klein H,Dutton A,et al.Assessing the effects of Bt maize on the predatory mite Neoseiulus cucumeris.Experimental&Applied Acarology,2006,38:125-139
[23]Chen FJ,Wu G,Parajulee MN,et al.Long-term impacts of elevated carbon dioxide and transgenic Bt cotton on performance and feeding of three generations of cotton bollworm.Entomologia Experimentalis et Applicata,2007,124:27-35
[24]Han L-Z(韩兰芝),Wu K-M(吴孔明),Peng Y-F(彭于发),et al.Research advance in ecological safety of insect-resistant transgenic rice.Chinese Journal of Applied&Environmental Biology(应用与环境生物学报),2006,12(3):431-436(in Chinese)
[25]Han L-Z(韩兰芝),Bai S-X(白树雄),Zhao J-Z(赵建周),et al.Progress in ecological biosafety of insectresistant transgenic cotton and corn in relation to arthropods.Acta Entomologica Sinica(昆虫学报),2007,50(7):727-736(in Chinese)
[26]Chen M,Shelton A,Ye GY.Insect-resistant genetically modified rice in China:From research to commercialization.Annual Review of Entomology,2011,56:81-101
[27]Sui H(隋贺),Li Z-Y(李志毅),Xu Y-B(徐艳博),et al.Occurrence dynamics of migratory pest insects Cnaphalocrocis medinalis and Sogatella furcifera in transgenic Bt rice field in Xing’an County of Guangxi Province.Chinese Journal of Applied Ecology(应用生态学报),2011,22(11):3021-3025(in Chinese)
[28]Pritchard SG,Rogers HH,Prior SA,et al.Elevated CO2and plant structure:A review.Global Change Biology,1999,5:807-837
[29]Khan ZR,Saxena RC.Probing behavior of three biotypes of Nilaparvata lugens(Homoptera:Delphacidae)on different resistant and susceptible rice varieties.Journal of Economic Entomology,1988,81:1338-1345
[30]Kimmins FM.Electrical penetration graphs from Nilaparvata lugens on resistant and susceptible rice varieties.Entomologia Experimentalis et Applicata,1988,50:69-79
[31]Chen Y(陈燕),Wu B-Q(吴碧球),Huang S-S(黄所生),et al.Geographical populations of brown planthopper in Nanning of South China and in Vietnam:A comparative study.Chinese Journal of Applied Ecology(应用生态学报),2013,24(1):190-196(in Chinese)
[32]Seo BY,Kwon YH,Jung JK,et al.Electrical penetration graphic waveforms in relation to the actual positions of the stylet tips of Nilaparvata lugens in rice tissue.Journal of Asia-Pacific Entomology,2009,12:89-95
[33]Pan J-H(潘建红),Chen F(陈峰),He J-C(何伎春),et al.Comparison on electrical penetration graph(EPG)of two populations of Nilaparvata lugens with different virulence.Chinese Journal of Rice Science(中国水稻科学),2011,25(1):86-90(in Chinese)
[34]Jiang S-L(江守林),He H(何花),Qu Y(屈勇),et al.A comparative study of three methods using to fix insects for electrical penetration graph experiments.Chinese Journal of Applied Entomology(应用昆虫学报),2015,52(4):1049-1057(in Chinese)
[35]Kumar A,Silim SN,Okamoto M,et al.Differential expression of three members of the AMT1 gene family encoding putative high-affinity NH4+transporters in roots of Oryza sativa subspecies indica.Plant,Cell&Environment,2003,26:907-914
[36]Lu ZX,Heong KL,Yu XP,et al.Effects of nitrogen on the tolerance of brown planthopper,Nilaparvata lugens,to adverse environmental factors.Insect Science,2005,12:121-128
[37]Peter S,Tatiana C.How does elevated carbon dioxide(CO2)affect plant-herbivore interactions?A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance.Global Change Biology,2007,13:1823-1842
[38]Yin J,Sun YC,Wu G,et al.No effects of elevated CO2on the population relationship between cotton bollworm,Helicoverpa armigera Hübner(Lepidoptera:Noctuidae),and its parasitoid,Microplitis mediator Haliday(Hymenoptera:Braconidae).Agriculture,Ecosystems and Environment,2009,132:267-275
[39]Braun S,Thomas VF,Quiring R,et al.Does nitrogen deposition increase forest production?The role of phosphorus.Environmental Pollution,2010,6:2043-2052
[40]Tao LL,Hunter MD.Effects of insect herbivores on the nitrogen economy of plants//Polacco JC,Todd CD,eds.Ecological Aspects of Nitrogen Metabolism in Plants.London:Wiley-Blackwell,2011:255-279
[41]Liu G-J(刘光杰),Han C-Y-C(寒川一成),Shen L-L(沈丽丽).Study on wing-type differentiation of brown planthopper.Entomological Knowledge(昆虫知识),2000,37(3):186-190(in Chinese)
[42]Chang XN,Wei H,Xiao NW,et al.Effects of elevated CO2and transgenic Bt rice on yeast-like endosymbiote and its host brown planthopper.Journal of Applied Entomology,2011,135:333-342
[43]Guo HJ,Sun YC,Li Y,et al.Elevated CO2alters the feeding behaviour of the pea aphid by modifying the physical and chemical resistance of Medicago truncatula.Plant,Cell&Environment,2014,37:2158-2168
[44]Sun YC,Jing BB,Ge F,et al.Response of amino acid changes in Aphis gossypii(Glover)to elevated CO2levels.Journal of Applied Entomology,2009,133:189-197
[45]Peng X-H(彭新红),Liu Z-Y(刘志源),Guo H-J(郭慧娟),et al.Feeding behavior of the peach aphid under elevated CO2levels.Chinese Journal of Applied Entomology(应用昆虫学报),2016,53(1):103-111(in Chinese)
[46]Suzuki Y,Koyama T,Hiruma K,et al.A molt timer is involved in the metamorphic molt in Manduca sexta larvae.Proceedings of the National Academy of Sciences of the United States of America,2013,110:12518-12525
[2]Ainsworth EA,Long SP.What have we learned from 15years of free-air CO2enrichment(FACE)?A metaanalytic review of the responses of photosynthesis,canopy properties and plant production to rising CO2.New Phytologist,2005,165:351-371
[3]Ainsworth EA,Rogers A,Leakey AD,et al.Does elevated atmospheric[CO2]alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves?Journal of Experimental Botany,2007,58:579-591
[4]Long SP,Ainsworth EA,Leakey AD,et al.Global food insecurity.Treatment of major food crops with elevated carbon dioxide or ozone under large-scale fully open-air conditions suggests recent models may have overestimated future yields.Philosophical Transactions of the Royal Society of London,2005,360:2011-2020
[5]Stacey DA,Fellowes ME.Influence of elevated CO2on interspecfic interactions at higher trophic levels.Global Change Biology,2002,8:668-678
[6]Ge F(戈峰),Chen F-J(陈法军).Impacts of elevated CO2on insects.Acta Ecologica Sinica(生态学报),2006,26(3):935-944(in Chinese)
[7]Chen F-J(陈法军),Ge F(戈峰),Liu X-H(刘向辉).Responses of cotton to elevated CO2and the effects on cotton aphid occurrences.Acta Ecologica Sinica(生态学报),2004,24(5):991-996(in Chinese)
[8]Chen F-J(陈法军),Wu G(吴刚),Ge F(戈峰).Responses of spring wheat to elevated CO2and their effects on Sitobion avenae aphid growth,development and reproduction.Chinese Journal of Applied Ecology(应用生态学报),2006,17(1):91-96(in Chinese)
[9]Guo HJ,Sun YC,Li YF,et al.Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2.Global Change Biology,2013,19:3210-3223
[10]Sun YC,Guo HJ,Yuan L,et al.Plant stomatal closure improves aphid feeding under elevated CO2.Global Change Biology,2015,21:2739-2748
[11]Chen FJ,Wu G,Ge F.Impacts of elevated CO2on the population abundance and reproductive activity of aphid Sitobion avenae Fabricius feeding on spring wheat.Journal of Applied Entomology,2004,128:723-730
[12]Jiang SL,Liu TJ,Yu FL,et al.Feeding behavioral response of cotton aphid,Aphis gossypii,to elevated CO2:EPG test with leaf microstructure and leaf chemistry.Entomologia Experimentalis et Applicata,2016,160:219-228
[13]Bezemer TM,Jones TH.Plant-insect herbivore interactions in elevated atmospheric CO2:Quantitative analyses and guild effects.Oikos,1998,82:212-222
[14]Guo HJ,Sun YC,Li YF,et al.Elevated CO2decreases the response of the ethylene signaling pathway in Medicago truncatula and increases the abundance of the pea aphid.New Phytologist,2014,201:279-291
[15]Chen FJ,Wu G,Ge F,et al.Effects of elevated CO2and transgenic Bt cotton on plant chemistry,performance,and feeding of an insect herbivore,the cotton bollworm.Entomologia Experimentalis et Applicata,2005,115:341-350
[16]Chen F-J(陈法军),Wu G(吴刚),Ge F(戈峰).Impacts of elevated CO2on the growth,development,and reproduction of cotton aphid Aphis gossypii(Glover).Acta Ecologica Sinica(生态学报),2005,25(10):2601-2607(in Chinese)
[17]Mendelsohn M,Kough JL,Vaituzis Z,et al.Are Bt crops safe.Nature Biotechnology,2003,21:1003-1009
[18]Bernal CC,Aguda RM,Cohen MB.Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis.Entomologia Experimentalis et Applicata,2010,102:21-28
[19]Ramirez-Romero R,Desneux N,Chaufaux J,et al.Bt-maize effects on biological parameters of the nontarget aphid Sitobion avenae,(Homoptera:Aphididae)and Cry1Ab toxin detection.Pesticide Biochemistry&Physiology,2008,91:110-115
[20]Torres JB,Ruberson JR.Interactions of Bt-cotton and the omnivorous big-eyed bug Geocoris punctipes(Say),a key predator in cotton fields.Biological Control,2006,39:47-57
[21]Zhang GF,Wan FH,Murphy ST,et al.Reproductive biology of two nontarget insect species,Aphis gossypii(Homoptera:Aphididae)and Orius sauteri(Hemiptera:Anthocoridae),on Bt and non-Bt cotton cultivars.Environmental Entomology,2008,37:1035-1042
[22]Obrist LB,Klein H,Dutton A,et al.Assessing the effects of Bt maize on the predatory mite Neoseiulus cucumeris.Experimental&Applied Acarology,2006,38:125-139
[23]Chen FJ,Wu G,Parajulee MN,et al.Long-term impacts of elevated carbon dioxide and transgenic Bt cotton on performance and feeding of three generations of cotton bollworm.Entomologia Experimentalis et Applicata,2007,124:27-35
[24]Han L-Z(韩兰芝),Wu K-M(吴孔明),Peng Y-F(彭于发),et al.Research advance in ecological safety of insect-resistant transgenic rice.Chinese Journal of Applied&Environmental Biology(应用与环境生物学报),2006,12(3):431-436(in Chinese)
[25]Han L-Z(韩兰芝),Bai S-X(白树雄),Zhao J-Z(赵建周),et al.Progress in ecological biosafety of insectresistant transgenic cotton and corn in relation to arthropods.Acta Entomologica Sinica(昆虫学报),2007,50(7):727-736(in Chinese)
[26]Chen M,Shelton A,Ye GY.Insect-resistant genetically modified rice in China:From research to commercialization.Annual Review of Entomology,2011,56:81-101
[27]Sui H(隋贺),Li Z-Y(李志毅),Xu Y-B(徐艳博),et al.Occurrence dynamics of migratory pest insects Cnaphalocrocis medinalis and Sogatella furcifera in transgenic Bt rice field in Xing’an County of Guangxi Province.Chinese Journal of Applied Ecology(应用生态学报),2011,22(11):3021-3025(in Chinese)
[28]Pritchard SG,Rogers HH,Prior SA,et al.Elevated CO2and plant structure:A review.Global Change Biology,1999,5:807-837
[29]Khan ZR,Saxena RC.Probing behavior of three biotypes of Nilaparvata lugens(Homoptera:Delphacidae)on different resistant and susceptible rice varieties.Journal of Economic Entomology,1988,81:1338-1345
[30]Kimmins FM.Electrical penetration graphs from Nilaparvata lugens on resistant and susceptible rice varieties.Entomologia Experimentalis et Applicata,1988,50:69-79
[31]Chen Y(陈燕),Wu B-Q(吴碧球),Huang S-S(黄所生),et al.Geographical populations of brown planthopper in Nanning of South China and in Vietnam:A comparative study.Chinese Journal of Applied Ecology(应用生态学报),2013,24(1):190-196(in Chinese)
[32]Seo BY,Kwon YH,Jung JK,et al.Electrical penetration graphic waveforms in relation to the actual positions of the stylet tips of Nilaparvata lugens in rice tissue.Journal of Asia-Pacific Entomology,2009,12:89-95
[33]Pan J-H(潘建红),Chen F(陈峰),He J-C(何伎春),et al.Comparison on electrical penetration graph(EPG)of two populations of Nilaparvata lugens with different virulence.Chinese Journal of Rice Science(中国水稻科学),2011,25(1):86-90(in Chinese)
[34]Jiang S-L(江守林),He H(何花),Qu Y(屈勇),et al.A comparative study of three methods using to fix insects for electrical penetration graph experiments.Chinese Journal of Applied Entomology(应用昆虫学报),2015,52(4):1049-1057(in Chinese)
[35]Kumar A,Silim SN,Okamoto M,et al.Differential expression of three members of the AMT1 gene family encoding putative high-affinity NH4+transporters in roots of Oryza sativa subspecies indica.Plant,Cell&Environment,2003,26:907-914
[36]Lu ZX,Heong KL,Yu XP,et al.Effects of nitrogen on the tolerance of brown planthopper,Nilaparvata lugens,to adverse environmental factors.Insect Science,2005,12:121-128
[37]Peter S,Tatiana C.How does elevated carbon dioxide(CO2)affect plant-herbivore interactions?A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance.Global Change Biology,2007,13:1823-1842
[38]Yin J,Sun YC,Wu G,et al.No effects of elevated CO2on the population relationship between cotton bollworm,Helicoverpa armigera Hübner(Lepidoptera:Noctuidae),and its parasitoid,Microplitis mediator Haliday(Hymenoptera:Braconidae).Agriculture,Ecosystems and Environment,2009,132:267-275
[39]Braun S,Thomas VF,Quiring R,et al.Does nitrogen deposition increase forest production?The role of phosphorus.Environmental Pollution,2010,6:2043-2052
[40]Tao LL,Hunter MD.Effects of insect herbivores on the nitrogen economy of plants//Polacco JC,Todd CD,eds.Ecological Aspects of Nitrogen Metabolism in Plants.London:Wiley-Blackwell,2011:255-279
[41]Liu G-J(刘光杰),Han C-Y-C(寒川一成),Shen L-L(沈丽丽).Study on wing-type differentiation of brown planthopper.Entomological Knowledge(昆虫知识),2000,37(3):186-190(in Chinese)
[42]Chang XN,Wei H,Xiao NW,et al.Effects of elevated CO2and transgenic Bt rice on yeast-like endosymbiote and its host brown planthopper.Journal of Applied Entomology,2011,135:333-342
[43]Guo HJ,Sun YC,Li Y,et al.Elevated CO2alters the feeding behaviour of the pea aphid by modifying the physical and chemical resistance of Medicago truncatula.Plant,Cell&Environment,2014,37:2158-2168
[44]Sun YC,Jing BB,Ge F,et al.Response of amino acid changes in Aphis gossypii(Glover)to elevated CO2levels.Journal of Applied Entomology,2009,133:189-197
[45]Peng X-H(彭新红),Liu Z-Y(刘志源),Guo H-J(郭慧娟),et al.Feeding behavior of the peach aphid under elevated CO2levels.Chinese Journal of Applied Entomology(应用昆虫学报),2016,53(1):103-111(in Chinese)
[46]Suzuki Y,Koyama T,Hiruma K,et al.A molt timer is involved in the metamorphic molt in Manduca sexta larvae.Proceedings of the National Academy of Sciences of the United States of America,2013,110:12518-12525