红火蚁工蚁对棉蚜诱导的棉花挥发物的嗅觉和行为反应
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摘要
【目的】红火蚁Solenopsis invicta与棉蚜Aphis gossypii存在兼性共生关系,红火蚁可能利用棉蚜危害诱导棉花释放的挥发物定位棉蚜。本研究将测试红火蚁工蚁对棉花挥发物的嗅觉和行为反应。【方法】使用Y型管实验测试红火蚁工蚁对棉花气味的行为反应;以红火蚁告警信息素2-乙基-3,5(6)-二甲基吡嗪为阳性对照,测试红火蚁工蚁对不同剂量(100, 10, 1和0.1μg)的9种棉花挥发物组分[α-蒎烯、β-蒎烯、β-石竹烯、(E,E)-4,8,12-三甲基-1,3,7,11-十三碳四烯(TMTT)、(E)-4,8-二甲基-1,3,7-壬三烯(DMNT)、辛醛、6-甲基-5-庚烯-2-酮、顺-3-己烯基乙酸酯和水杨酸甲酯]的触角电位反应;再利用Y型嗅觉仪测试这些挥发物对红火蚁工蚁的行为选择影响。【结果】结果表明,受棉蚜为害的棉花较健康棉花对红火蚁工蚁具有极显著的引诱效果。红火蚁对9种挥发物组分的EAG反应随着剂量升高而升高。各化合物在100μg剂量时EAG反应值最大,其中,工蚁对水杨酸甲酯和6-甲基-5-庚烯-2-酮这两个化合物反应最强。在行为选择实验中,化合物水杨酸甲酯、6-甲基-5-庚烯-2-酮和DMNT对红火蚁工蚁均具有显著的引诱效果。【结论】棉蚜诱导的棉花挥发物中水杨酸甲酯和6-甲基-5-庚烯-2-酮对红火蚁有显著的引诱效果,这2种化合物可能在红火蚁定位棉蚜、建立共生关系中起着关键的作用。
【Aim】 There is a facultative mutualistic interaction between the red imported fire ant, Solenopsis invicta and the cotton aphid, Aphis gossypii. Fire ants may utilize cotton aphid-induced cotton volatiles to locate mutualistic partners. This study aims to test the olfactory and behavioral responses of S. invicta workers to cotton volatiles induced by cotton aphid. 【Methods】 The behavioral response of S. invicta workers to cotton odor was tested by Y-tube. The electroantennogram(EAG) responses of the fire ant workers to nine volatile compounds including(1 S)-(-)-α-pinene,(1 S)-(-)-β-pinene, β-caryophyllene,(E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene(TMTT),(E)-4,8-dimethyl 1,3,7-nonatriene(DMNT), octanal, 6-methyl-5-hepten-2-one,(Z)-(3)-hexenyl acetate, and methyl salicylate at different dosages(100, 10, 1 and 0.1 μg) were tested using fire ant alarm pheromone 2-ethyl-3,5(6)-dimethylpyrazine as the positive control, and the influence of the volatile compounds on the behavior choice of the fire ant workers was tested by Y-tube olfactometer. 【Results】 The results showed that fire ant workers were significantly attracted to the cotton plants damaged by cotton aphids over undamaged ones. The EAG responses of fire ant workers to the nine volatile compounds were dose-dependent. These compounds triggered the highest EAG response in fire ant workers at the dose of 100 μg, and methyl salicylate and 6-methyl-5-hepten-2-one caused the greatest EAG responses. In behavioral selection experiments, fire ant workers were significantly attracted to methyl salicylate, 6-methyl-5-hepten-2-one and DMNT. 【Conclusion】 Among cotton aphid-induced volatile compounds, methyl salicylate and 6-methyl-5-hepten-2-one significantly attract fire ants, and they may play a key role in locating cotton aphids by fire ants for establishment of mutualistic interaction.
【Aim】 There is a facultative mutualistic interaction between the red imported fire ant, Solenopsis invicta and the cotton aphid, Aphis gossypii. Fire ants may utilize cotton aphid-induced cotton volatiles to locate mutualistic partners. This study aims to test the olfactory and behavioral responses of S. invicta workers to cotton volatiles induced by cotton aphid. 【Methods】 The behavioral response of S. invicta workers to cotton odor was tested by Y-tube. The electroantennogram(EAG) responses of the fire ant workers to nine volatile compounds including(1 S)-(-)-α-pinene,(1 S)-(-)-β-pinene, β-caryophyllene,(E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene(TMTT),(E)-4,8-dimethyl 1,3,7-nonatriene(DMNT), octanal, 6-methyl-5-hepten-2-one,(Z)-(3)-hexenyl acetate, and methyl salicylate at different dosages(100, 10, 1 and 0.1 μg) were tested using fire ant alarm pheromone 2-ethyl-3,5(6)-dimethylpyrazine as the positive control, and the influence of the volatile compounds on the behavior choice of the fire ant workers was tested by Y-tube olfactometer. 【Results】 The results showed that fire ant workers were significantly attracted to the cotton plants damaged by cotton aphids over undamaged ones. The EAG responses of fire ant workers to the nine volatile compounds were dose-dependent. These compounds triggered the highest EAG response in fire ant workers at the dose of 100 μg, and methyl salicylate and 6-methyl-5-hepten-2-one caused the greatest EAG responses. In behavioral selection experiments, fire ant workers were significantly attracted to methyl salicylate, 6-methyl-5-hepten-2-one and DMNT. 【Conclusion】 Among cotton aphid-induced volatile compounds, methyl salicylate and 6-methyl-5-hepten-2-one significantly attract fire ants, and they may play a key role in locating cotton aphids by fire ants for establishment of mutualistic interaction.
引文
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Brindis Y,Lachaud JP,Gómez YGB,Rojas JC,Malo EA,Cruz-López L,2008.Behavioral and olfactory antennal responses of Solenopsis geminata (Fabricius) (Hymenoptera:Formicidae) workers to their dufour gland secretion.Neotrop.Entomol.,37(2):131-136.
Buckley RC,1987.Interactions involving plants,Homoptera,and ants.Annu.Rev.Ecol.Syst.,18:111-135.
de Bruyne M,Baker TC,2008.Odor detection in insects:volatile codes.J.Chem.Ecol.,34(7):882-897.
De Moraes CM,Lewis WJ,Pare PW,Alborn HT,Tumlinson JH,1998.Herbivore-infested plants selectively attract parasitoids.Nature,393(6685):570-573.
De Moraes CM,Mescher MC,Tumlinson JH,2001.Caterpillar-induced nocturnal plant volatiles repel conspecific females.Nature,410 (6828):577-580.
Delabie JHC,2001.Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha):an overview.Neotrop.Entomol.,30(4):501-516.
Dicke M,Baldwin IT,2010.The evolutionary context for herbivore-induced plant volatiles:beyond the ‘cry for help’.Trends Plant Sci.,15(3):167-175.
Feng HZ,Wang L,Yao YS,Xiong RC,2013.Analysis of volatile compounds released from cotton,induced by Aphis gossypii and methyl jasmonate.Chin.J.Appl.Entomol.,50(3):742-748.[冯宏祖,王兰,姚永生,熊仁次,2013.棉蚜和茉莉酸甲酯诱导棉花挥发物组分分析.应用昆虫学报,50(3):742-748]
Fischer CY,Detrain C,Thonart P,Haubruge E,Francis F,Verheggen FJ,Lognay GC,2017.Bacteria may contribute to distant species recognition in ant-aphid mutualistic relationships.Insect Sci.,24(2):278-284.
Fischer CY,Lognay GC,Detrain C,Heil M,Grigorescu A,Sabri A,Thonart P,Haubruge E,Verheggen FJ,2015.Bacteria may enhance species association in an ant-aphid mutualistic relationship.Chemoecology,25(5):223-232.
Gao Y,Luo LZ,2005.Antennal morphology and sensilla of the fire ants,Solenopsis invicta Buren invaded southern China observed with scanning electron microscopy.Acta Entomol.Sin.,48(6):986-992.[高艳,罗礼智,2005.红火蚁触角及其上感受器的扫描电镜观察.昆虫学报,48(6):986-992]
Guan D,Lu YY,Li XL,Wei L,Chen L,2014.Electroantennogram and behavioral responses of the imported fire ant,Solenopsis invicta Buren,to an alarm pheromone component and its analogues.J.Agric.Food Chem.,62(49):11924-11932.
Han BY,Chen ZM,2002.Behavioral and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids,Toxoptera aurantii.J.Chem.Ecol.,28(11):2203-2219.
Hao Y,Lou YG,2013.Research progress in herbivore-induced plant volatiles.J.Yangtze Univ.(Nat.Sci.Ed.),10(11):12-15.[郝娅,娄永根,2013.虫害诱导植物挥发物的研究进展.长江大学学报(自然科学版),10(11):12-15]
Hegde M,Oliveira JN,da Costa JG,Bleicher E,Santana AEG,Bruce TJA,Caulfield J,Dewhirst SY,Woodcock CM,Pickett JA,Birkett MA,2011.Identification of semiochemicals released by cotton,Gossypium hirsutum,upon infestation by the cotton aphid,Aphis gossypii.J.Chem.Ecol.,37(7):741-750.
Kessler A,Baldwin IT,2001.Defensive function of herbivore-induced plant volatile emissions in nature.Science,291(5511):2141-2144.
Krieger J,Breer H,1999.Olfactory reception in invertebrates.Science,286(5440):720-723.
Leather SR Watt AD,Forrest GI,1987.Insect-induced chemical-changes in young lodgepole pine (Pinus contorta) - the effect of previous defoliation on oviposition,growth and survival of the pine beauty moth,Panolis flammea.Ecol.Entomol.,12(3):275-281.
Liu Y,Xie DS,Hu CH,Dong WX,Zhang F,Zhang JP,Xiao C,2018.Influence of β-caryophyllene on the behaviors of female Drosophila suzukii.J.Environ.Entomol.,40(3):684-689.[刘燕,谢冬生,胡春华,董文霞,张峰,张金平,肖春,2018.β-石竹烯对斑翅果蝇雌成虫行为的影响.环境昆虫学报,40(3):684-689]
Lou YG,Cheng JA,2000.Herbivore-induced plant volatiles:primary characteristics,ecological functions and its release mechanism.Acta Ecol.Sin.,20(6):1097-1106.[娄永根,程家安,2000.虫害诱导的植物挥发物:基本特性、生态学功能及释放机制.生态学报,20(6):1097-1106]
Nault LR,Edwards LJ,Styer WE,1973.Aphid alarm pheromones:secretion and reception.Environ.Entomol.,2(1):101-105.
Oliver TH,Mashanova A,Leather SR,Cook JM,Jansen VAA,2007.Ant semiochemicals limit apterous aphid dispersal.Proc.R.Soc.B Biol.Sci.,274(1629):3127-3131.
Renthal R,Velasquez D,Olmos D,Hampton J,Wergin WP,2003.Structure and distribution of antennal sensilla of the red imported fire ant.Micron,34(8):405-413.
Rose USR,Tumlinson JH,2004.Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds.Planta,218(5):824-832.
Styrsky JD,Eubanks MD,2010.A facultative mutualism between aphids and an invasive ant increases plant reproduction.Ecol.Entomol.,35(2):190-199.
Tallamy DW,1985.Squash beetle feeding behavior:an adaptation against induced cucurbit defenses.Ecology,66(5):1574-1579.
Verheggen FJ,Diez L,Sablon L,Fischer C,Bartram S,Haubruge E,Detrain C,2012.Aphid alarm pheromone as a cue for ants to locate aphid partners.PLoS ONE,7(8):e41841.
Way MJ,1963.Mutualism between ants and honeydew-producing Homoptera.Annu.Rev.Entomol.,8:307-344.
Wilson EO,1962.Chemical communication among workers of the fire ant Solenopsis saevissima (Fr.Smith) 1.The organization of mass-foraging.Anim.Behav.,10(1/2):134-147.
Yan SC,Zhang DD,Chi DF,2003.Advances of studies on the effects of plant volatiles on insect behavior.Chin.J.Appl.Entomol.,14(2):310-313.[严善春,张丹丹,迟德富,2003.植物挥发性物质对昆虫作用的研究进展.应用生态学报,14(2):310-313]
Brindis Y,Lachaud JP,Gómez YGB,Rojas JC,Malo EA,Cruz-López L,2008.Behavioral and olfactory antennal responses of Solenopsis geminata (Fabricius) (Hymenoptera:Formicidae) workers to their dufour gland secretion.Neotrop.Entomol.,37(2):131-136.
Buckley RC,1987.Interactions involving plants,Homoptera,and ants.Annu.Rev.Ecol.Syst.,18:111-135.
de Bruyne M,Baker TC,2008.Odor detection in insects:volatile codes.J.Chem.Ecol.,34(7):882-897.
De Moraes CM,Lewis WJ,Pare PW,Alborn HT,Tumlinson JH,1998.Herbivore-infested plants selectively attract parasitoids.Nature,393(6685):570-573.
De Moraes CM,Mescher MC,Tumlinson JH,2001.Caterpillar-induced nocturnal plant volatiles repel conspecific females.Nature,410 (6828):577-580.
Delabie JHC,2001.Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha):an overview.Neotrop.Entomol.,30(4):501-516.
Dicke M,Baldwin IT,2010.The evolutionary context for herbivore-induced plant volatiles:beyond the ‘cry for help’.Trends Plant Sci.,15(3):167-175.
Feng HZ,Wang L,Yao YS,Xiong RC,2013.Analysis of volatile compounds released from cotton,induced by Aphis gossypii and methyl jasmonate.Chin.J.Appl.Entomol.,50(3):742-748.[冯宏祖,王兰,姚永生,熊仁次,2013.棉蚜和茉莉酸甲酯诱导棉花挥发物组分分析.应用昆虫学报,50(3):742-748]
Fischer CY,Detrain C,Thonart P,Haubruge E,Francis F,Verheggen FJ,Lognay GC,2017.Bacteria may contribute to distant species recognition in ant-aphid mutualistic relationships.Insect Sci.,24(2):278-284.
Fischer CY,Lognay GC,Detrain C,Heil M,Grigorescu A,Sabri A,Thonart P,Haubruge E,Verheggen FJ,2015.Bacteria may enhance species association in an ant-aphid mutualistic relationship.Chemoecology,25(5):223-232.
Gao Y,Luo LZ,2005.Antennal morphology and sensilla of the fire ants,Solenopsis invicta Buren invaded southern China observed with scanning electron microscopy.Acta Entomol.Sin.,48(6):986-992.[高艳,罗礼智,2005.红火蚁触角及其上感受器的扫描电镜观察.昆虫学报,48(6):986-992]
Guan D,Lu YY,Li XL,Wei L,Chen L,2014.Electroantennogram and behavioral responses of the imported fire ant,Solenopsis invicta Buren,to an alarm pheromone component and its analogues.J.Agric.Food Chem.,62(49):11924-11932.
Han BY,Chen ZM,2002.Behavioral and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids,Toxoptera aurantii.J.Chem.Ecol.,28(11):2203-2219.
Hao Y,Lou YG,2013.Research progress in herbivore-induced plant volatiles.J.Yangtze Univ.(Nat.Sci.Ed.),10(11):12-15.[郝娅,娄永根,2013.虫害诱导植物挥发物的研究进展.长江大学学报(自然科学版),10(11):12-15]
Hegde M,Oliveira JN,da Costa JG,Bleicher E,Santana AEG,Bruce TJA,Caulfield J,Dewhirst SY,Woodcock CM,Pickett JA,Birkett MA,2011.Identification of semiochemicals released by cotton,Gossypium hirsutum,upon infestation by the cotton aphid,Aphis gossypii.J.Chem.Ecol.,37(7):741-750.
Kessler A,Baldwin IT,2001.Defensive function of herbivore-induced plant volatile emissions in nature.Science,291(5511):2141-2144.
Krieger J,Breer H,1999.Olfactory reception in invertebrates.Science,286(5440):720-723.
Leather SR Watt AD,Forrest GI,1987.Insect-induced chemical-changes in young lodgepole pine (Pinus contorta) - the effect of previous defoliation on oviposition,growth and survival of the pine beauty moth,Panolis flammea.Ecol.Entomol.,12(3):275-281.
Liu Y,Xie DS,Hu CH,Dong WX,Zhang F,Zhang JP,Xiao C,2018.Influence of β-caryophyllene on the behaviors of female Drosophila suzukii.J.Environ.Entomol.,40(3):684-689.[刘燕,谢冬生,胡春华,董文霞,张峰,张金平,肖春,2018.β-石竹烯对斑翅果蝇雌成虫行为的影响.环境昆虫学报,40(3):684-689]
Lou YG,Cheng JA,2000.Herbivore-induced plant volatiles:primary characteristics,ecological functions and its release mechanism.Acta Ecol.Sin.,20(6):1097-1106.[娄永根,程家安,2000.虫害诱导的植物挥发物:基本特性、生态学功能及释放机制.生态学报,20(6):1097-1106]
Nault LR,Edwards LJ,Styer WE,1973.Aphid alarm pheromones:secretion and reception.Environ.Entomol.,2(1):101-105.
Oliver TH,Mashanova A,Leather SR,Cook JM,Jansen VAA,2007.Ant semiochemicals limit apterous aphid dispersal.Proc.R.Soc.B Biol.Sci.,274(1629):3127-3131.
Renthal R,Velasquez D,Olmos D,Hampton J,Wergin WP,2003.Structure and distribution of antennal sensilla of the red imported fire ant.Micron,34(8):405-413.
Rose USR,Tumlinson JH,2004.Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds.Planta,218(5):824-832.
Styrsky JD,Eubanks MD,2010.A facultative mutualism between aphids and an invasive ant increases plant reproduction.Ecol.Entomol.,35(2):190-199.
Tallamy DW,1985.Squash beetle feeding behavior:an adaptation against induced cucurbit defenses.Ecology,66(5):1574-1579.
Verheggen FJ,Diez L,Sablon L,Fischer C,Bartram S,Haubruge E,Detrain C,2012.Aphid alarm pheromone as a cue for ants to locate aphid partners.PLoS ONE,7(8):e41841.
Way MJ,1963.Mutualism between ants and honeydew-producing Homoptera.Annu.Rev.Entomol.,8:307-344.
Wilson EO,1962.Chemical communication among workers of the fire ant Solenopsis saevissima (Fr.Smith) 1.The organization of mass-foraging.Anim.Behav.,10(1/2):134-147.
Yan SC,Zhang DD,Chi DF,2003.Advances of studies on the effects of plant volatiles on insect behavior.Chin.J.Appl.Entomol.,14(2):310-313.[严善春,张丹丹,迟德富,2003.植物挥发性物质对昆虫作用的研究进展.应用生态学报,14(2):310-313]