近十年全球小型寄生蜂滞育研究的新进展
|
摘要
滞育现象在多种小型寄生蜂中存在。通过滞育调控技术,可实现蜂种的长期贮存、延长防控作用时间、提高产品的抗逆性,对寄生蜂工厂化生产及应用具有重要意义。本文总结了2007年以来国内外小型寄生蜂滞育研究文献,统计出开展滞育研究的寄生蜂37种,分属10科21属。研究内容涉及滞育特征、滞育诱导因素、亲代效应、滞育后发育、滞育的分子机制等。小型寄生蜂滞育时间较长,一般为数月,最多可达4年;光周期和温度是诱导滞育的主要因子,亲代效应对于部分寄生蜂的滞育亦有重要影响;滞育对于寄生蜂成虫寿命、生殖能力等有显著影响,这种影响既有正面的也有负面的;滞育期间寄生蜂体内代谢途径和蛋白质表达量有明显变化,运用蛋白质组学技术已发现大量滞育关联蛋白,但具体蛋白质和基因的功能分析以及滞育的激素调控等问题尚待进一步研究。
Diapause exists in a variety of small parasitic wasps.By means of diapause control,the longterm storage of the species can be realized,the time of prevention and control can be prolonged,the resistance of the products can be improved,which is significant to the production and application of parasitic wasps.This paper summarizes the literatures on the diapause of small parasitic wasps at home and abroad since 2007,and collects 37 species of parasitic wasps,which belong to 10 families and 21 genera.The study involves diapause characteristics,diapause induction factors,maternal influence,post-diapause development,and molecular mechanisms of diapause.Small parasitic wasps have longer duration,usually for several months,up to 4 years; photoperiod and temperature are the main factors that induce diapause,and the maternal influence has a significant effect on the diapause of some parasitic bees.Diapause had a significant effect on the life and reproductive capacity of parasitic wasps,which had both positive and negative effects; During the process of diapause,the in vivo metabolic pathway andprotein expression have been significantly changed,and because of the use of proteomics technology,we have found a large number of diapause-associated protein,but the specific protein and gene function analysis and diapause hormone regulation and other issues need to be further studied.
Diapause exists in a variety of small parasitic wasps.By means of diapause control,the longterm storage of the species can be realized,the time of prevention and control can be prolonged,the resistance of the products can be improved,which is significant to the production and application of parasitic wasps.This paper summarizes the literatures on the diapause of small parasitic wasps at home and abroad since 2007,and collects 37 species of parasitic wasps,which belong to 10 families and 21 genera.The study involves diapause characteristics,diapause induction factors,maternal influence,post-diapause development,and molecular mechanisms of diapause.Small parasitic wasps have longer duration,usually for several months,up to 4 years; photoperiod and temperature are the main factors that induce diapause,and the maternal influence has a significant effect on the diapause of some parasitic bees.Diapause had a significant effect on the life and reproductive capacity of parasitic wasps,which had both positive and negative effects; During the process of diapause,the in vivo metabolic pathway andprotein expression have been significantly changed,and because of the use of proteomics technology,we have found a large number of diapause-associated protein,but the specific protein and gene function analysis and diapause hormone regulation and other issues need to be further studied.
引文
Ahmed UAM,Shi Z,Guo Y,et al.Maternal photoperiod effect on and geographic variation of diapause incidence in Cotesia plutellae(Hymenoptera:Braconidae)from China[J].Applied Entomology and Zoology,2007,42(3):383-389.
Arbab A.Spatial Distribution and minimum sample size for overwintering larvae of the rice stem borer Chilo suppressalis(Walker)in Paddy Fields[J].Neotropical Entomology,2014,43(5):415-420.
Chen H,Zhang H,Throne J,et al.Transcript analysis and expression profiling of three heat shock protein 70 genes in the ectoparasitoid Habrobracon hebetor[J].Insect Science,2014,21(4):415-428.
Chen H,Zhang H,Zhu KY,et al.Performance of diapausing parasitoid wasps,Habrobracon hebetor,after cold storage[J].Biological Control,2013,64(3):186-194.
Chen H,Zhang H,Zhu KY,et al.Induction of reproductive diapause in Habrobracon hebetor(Hymenoptera:Braconidae)when reared at different photoperiods[J].Environmental Entomology,2012,41(3):697-705.
Colinet H,Muratori F,Hance T.Cold-induced expression of diapause in Praon volucre:Fitness cost and morpho-physiological characterization[J].Physiological Entomology,2010,35:301-307.
Colinet H,Renault D,Charoyguevel B,et al.Metabolic and proteomic profiling of diapause in the aphid parasitoid Praon volucre[J].PLo S ONE,2012,7(2):e23606.
Ferracini C,Gonella E,Ferrari E,et al.Novel insight in the life cycle of Torymus sinensis,biocontrol agent of the chestnut gall wasp[J].Bio Control,2015,60(2):169-177.
Garcia PV,Pereira N,Oliveira LM.Side-effects of organic and synthetic pesticides on cold-stored diapausing prepupae of Trichogramma cordubensis[J].Bio Control,2009,54:451-458.
Gardner J,Yong TH,Pitcher SA,et al.Overwintering of Trichogramma ostriniae(Hymenoptera:Trichogrammatidae)within target and non-target host eggs[J].Biocontrol Science and Technology,2013,23(4):367-380.
Gariepy V,Boivin G,Brodeur J,Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions[J].Biological Control,2015,80:1-7.
Gerling D,Erel E,Guershon M,et al.Bionomics of Encarsia scapeata Rivnay(Hymenoptera:Aphelinidae),tritrophic relationships and host-induced diapause[J].Biological Control,2009,49(3):201-206.
Hanson AA,Venette RC,Lelito JP.Cold tolerance of Chinese emerald ash borer parasitoids:Spathius agrili Yang(Hymenoptera:Braconidae),Tetrastichus planipennisi Yang(Hymenoptera:Eulophidae),and Oobius agrili Zhang and Huang(Hymenoptera:Encyrtidae)[J].Biological Control,2013,67:516-529.
Hao Z,Zhao J,Yuan Z,et al.Influence of photoperiod on hydrogen peroxide metabolism during diapause induction in Cotesia vestalis(Haliday)(Hymenoptera:Braconidae)[J].Journal of the Kansas Entomological Society,2012,85(3):206-218.
Hoban J,Duan JJ,Houghgoldstein J.Effects of temperature and photoperiod on the reproductive biology and diapause of Oobius agrili(Hymenoptera:Encyrtidae),an egg parasitoid of emerald ash borer(Coleoptera:Buprestidae)[J].Environmental Entomology,2016,3:726-731.
Huang FX,Jiang S,Ren XY,et al.Differential expression of proteins associated with lipid metabolism in diapausing Aphidius gifuensis Ashmaed[J].Chinese Journal of Biological Control,2015,31(6):811-820.[黄凤霞,蒋莎,任小云,等.烟蚜茧蜂脂代谢相关的滞育相关蛋白差异表达分析[J].中国生物防治学报,2015,31(6):811-820]
Hughes GE,Sterk G,Bale JS.Thermal biology and establishment potential in temperate climates of the aphid parasitoid,Lysiphlebus testaceipes[J].Bio Control,2011,56(1):19-33.
Ishii M,Sato Y,Tagawa J.Diapause in the braconid wasp,Cotesia glomerata(L.)ii.factors inducing and terminating diapause[J].Entomological Science,2000,3(1):201-206.
Larios GLB,Ohno K.Larval summer diapause of Chrysocharis pubicornis(Zetterstedt)(Hymenoptera:Eulophidae),a pupal parasitoid of agromyzid leafminers:Sensitive stage for diapause induction and effects of cool exposure on diapause termination[J].Applied Entomology and Zoology,2007,42(4):587-594.
Larios GLB,Ohno K,Fukuhara F.Effects of photoperiod and temperature on preimaginal development and summer diapause of Chrysocharis pubicornis(Zetterstedt)(Hymenoptera:Eulophidae),a pupal parasitoid of leafminers(Diptera:Agromyzidae[J].Applied Entomology and Zoology,2007,42(2):189-197.
Larson KM,Duan JJ.Differences in the reproductive biology and diapause of two congeneric species of egg parasitoids(Hymenoptera:Encyrtidae)from northeast Asia:Implications for biological control of the invasive emerald ash borer(Coleoptera:Buprestidae)[J].Biological Control,2016,103:39-45.
Legault S,Hébert C,Blais J,et al.Seasonal ecology and thermal constraints of Telenomus spp.(Hymenoptera:Scelionidae),egg parasitoids of the Hemlock Looper(Lepidoptera:Geometridae)[J].Environmental Entomology,2012,41(6):1290-1301.
Lehmann P,Lyytinen A,Piiroinen S,et al.Latitudinal differences in diapause related photoperiodic responses of European Colorado potato beetles(Leptinotarsa decemlineata)[J].Evolutionary Ecology,2015,29(2):269-282.
Li WX,Li JC,Lu ZY,et al.Critial photoperiod and sensitive stage of diapause induction in Microplitis mediator(Haliday)(Hymenoptera:Braconidae)[J].Acta Entomoogica Sinica,2008,6(51):635-639.[李文香,李建成,路子云,等.中红侧沟茧蜂滞育临界光周期和敏感光照虫态的测定[J].昆虫学报,2008,51(6):635-639]
Li YY,Zhang LS,Chen HY.Research advances in diapause in braconids[J].Acta Entomoogica Sinica,2010a,53(10):1167-1178.[李玉艳,张礼生,陈红印.茧蜂滞育的研究进展[J],2010a.昆虫学报,53(10):1167-1178]
Li YY,Zhang LS,Chen HY.Effect of biotic factors on diapause of parasitic wasps[J].Chinese Bulletin of Entomology,2010b,47(4):638-645.[李玉艳,张礼生,陈红印.生物因子对寄生蜂滞育的影响[J].昆虫知识,2010b,47(4):638-645]
Li YY,Zhang LS,Chen HY,et al.Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid's diapause,host diapause and host diet augme[J].Inset Biochemistry and Molecular Biology,2015,63:34-46.
Li YY,Zhang LS,Chen HY,et al.Temperature and photoperiodic response of diapause induction in Aphidius gifuensis[J].Chinese Journal of Applied Entomology,2013,50(3):718-726.[李玉艳,张礼生,陈红印,等.烟蚜茧蜂滞育诱导的温光周期反应[J].应用昆虫学报,2013,50(3):718-726]
Li YY,Zhang LS,Zhang QR,et al.Host diapause status and host diets augmented with cryoprotectants enhance cold hardiness in the parasitoid Nasonia vitripennis[J].Journal of Insect Physiology,2014,70:8-14.
Liao DX,Li XL,Pang XF.Economic Insect Fauna of China,Volume34,Hymenoptera:Chalcidoidea[M].Beijing:Science Press,1987.107.[廖定喜,李学骝,庞雄飞.中国经济昆虫志,第三十四册分册---膜翅目小蜂科[M].北京:科学出版社,1987,107]
Lu ZY,Ran HF,Liu WX,et al.Effects of photoperiod and temperature on diapause induction in Microplitis tuberculifer(Hymenoptera:Braconidea)and the cold storage of its diapause pupae[J].Acta Entomoogica Sinica,2014,57(10):1206-1212.[路子云,冉红凡,刘文旭,等.温度和光周期对管侧沟茧蜂滞育诱导及滞育茧的低温冷藏[J].昆虫学报,2014,57(10):1206-1212]
Menu F,Desouhant E.Bet-hedging for variability in life cycle duration:Bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause[J].Oecologia,2002,132(2):167-174.
Mukai A,Goto SG.The clock gene period is essential for the photoperiodic response in the jewel wasp Nasonia vitripennis(Hymenoptera:Pteromalidae)[J].Applied Entomology and Zoology,2016,51(2):185-194.
Murata Y,Ideo S,Watada M,et al.Genetic and physiological variation among sexual and parthenogenetic populations of Asobara japonica(Hymenoptera:Braconidae),a larval parasitoid of drosophilid flies[J].European Journal of Entomology,2009,106(2):171-178.
Paolucci S,Zande VD,Beukeboom LW.Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe[J].Journal of Evolutionary Biology,2013,26(4):705-718.
Paolucci S,Salis L,Vermeulen CJ,et al.QTL analysis of the photoperiodic response and clinal distribution of period alleles in Nasonia vitripennis[J].Molecular Ecology,2016,25(19):4805-4817.
Pizzol J,Pintureau B.Effect of photoperiod experienced by parents on diapause induction in Trichogramma cacoeciae[J].Entomologia Experimentalis et Applicata,2008,127(1):72-77.
Qiang CK,Du YZ,Qin YH,et al.Overwintering physiology of the rice stem borer larvae,Chilo suppressalis Walker(Lepidoptera:Pyralidae):Roles of glycerol,amino acids,low-molecular weight carbohydrates and antioxidant enzymes[J].African Journal of Biotechnology,2012,11(66):13030-13039.
Ren XY,Qi XY,An T,et al.Research on the accumulation,transformation and regulation of nutrients in diapause insects[J].Chinese Journal of Applied Entomology,2016,53(4):685-695.[任小云,齐晓阳,安涛,等.滞育昆虫营养物质的积累、转化与调控[J].应用昆虫学报,2016,53(4):685-695]
Reznik SY,Vaghina NP,Voinovich ND.Diapause induction in Trichogramma embryophagum Htg.(Hym.,Trichogrammatidae):The dynamics of thermosensitivity[J].Journal of Applied Entomology,2008,132:502-509.
Reznik SY,Vaghina NP,Voinovich ND.Multigenerational maternal effect on diapause induction in Trichogramma species(Hymenoptera:Trichogrammatidae)[J].Biocontrol Science and Technology,2012,22(4):429-445.
Reznik SY,Vaghina NP,Voinovich ND.Maternal influence on diapause induction in Trichogramma(Hymenoptera:Trichogrammatidae):The dynamics of photosen-sitivity[J].Journal of Applied Entomology,2011a,135:438-445.
Reznik SY,Vaghina NP,Voinovich ND.Variations in the tendency to diapause among successive generations of laboratory strains of Trichogramma species(Hymenoptera,Trichogrammatidae):Endogenous or exogenous[J].Entomological Review,2015,95(2):157-165.
Reznik SY,Vaghina AP,Vasiljev L.Photo-thermal regulation of siapause in Trichogramma piceum Djur.(Hymenoptera:Trichogrammatidae)[J].Entomological Review,2013,93(1):9-13.
Reznik SY,Voinovich ND,Vaghina NP.Maternal regulation of Trichogramma embryophagum Htg.(Hymenoptera:Trichogrammatidae)diapause:Photoperiodic sensitivity of adult females[J].Biological Control,2011b,57(2):158-162.
Reznik SY,Samartsev KG.Multigenerational maternal inhibition of prepupal diapause in two Trichogramma species(Hymenoptera:Trichogrammatidae)[J].Journal of Insect Physiology,2015,81:14-20.
Reznik SY,Voinovich ND.Diapause induction in Trichogramma telengai:The dynamics of maternal thermosensitivity[J].Physiological Entomology,2016,41(4):335-343.
Reznik S,Ecological and evolutionary aspects of photothermal regulation of diapause in Trichogramma[J].Zhurnal Evoliutsionno Biokhimii I Fiziologii,2011,47(6):434-443.
Seyahooei MA,Smit FK,Kraaijeveld K,et al.Closely related parasitoids induce different pupation and foraging responses in Drosophila larvae[J].Oikos,2009,118:1148-1157.
Solbreck C,Widenfalk O.Very long diapause and extreme resistance to population disturbance in a galling insect[J].Ecological Entomology,2012,37(1):51-55.
Sun SH,Zhao LW,Qi JY.Diapause induction and post-diapause developement in Chouioia cune Yang(Hymecnoptera:Eulophidac)[J].Acta Entomoogica Sinica,2009,52(12):1307-1311.[孙守慧,赵利伟,祁金玉.白蛾周氏啮小蜂滞育诱导及滞育后发育[J].昆虫学报,2009,52(12):1307-1311]
Vaghina NP,Voinovich ND,Reznik SY.Maternal thermal and photoperiodic effects on the progeny diapause in Trichogramma telengai Sorokina(Hymenoptera:Trichogrammatidae)[J].Entomological Science,2014,17(2):198-206.
Voinovich ND,Reznik SY,Vaghina NP.Maternal thermal effect on diapause in Trichogramma species(Hymenoptera:Trichogrammatidae)[J].Journal of Applied Entomology,2015,139(10):783-790.
Xiao HJ,Mou FC,Zhu XF,et al.Diapause induction,maintenance and termination in the rice stem borer Chilo suppressalis(Walker)[J].Journal of Insect Physiology,2010,56(11):1558-1564.
Xiao L,Xue FS.Ecological and physiology stages of insect's diapause[J].Jiangxi Plant Protection,2009,32(1):3-9.[肖岚,薛芳森.昆虫滞育的生态生理阶段[J].江西植保,2009,32(1):3-9]
Xu WH.Advances in insect diapause[J].Chinese Bulletin of Entomology,2008,54(4):512-517.[徐卫华.昆虫滞育研究进展.昆虫知识,2008,54(4):512-517]
Xu ZB,Liu AP,Xu LB,et al.Diapause induction and cold storage of diapause cocoons in Agrypon flexorium(Hymenoptera:Ochneumonidae)[J].Acta Entomoogica Sinica,2013,56(10):1160-1165.[徐忠宝,刘爱萍,徐林波,等.草地螟阿格姬蜂的滞育诱导和滞育茧的低温贮藏[J].昆虫学报,2013,56(10):1160-1165]
Yang ZQ,Wang XY,Gould JR,et al.Biology and behavior of Spathius agrili,a parasitoid of the emerald ash borer,Agrilus planipennis,in China[J].Journal of Insect Science,2010,10:30.
Yao YX,Duan JJ,Hopper KP,et al.A new species of Oobius trjapitzin(Hymenoptera:Encyrtidae)from the Russian far east that parasitizes eggs of emerald ssh borer(Coleoptera:Buprestidae)[J].Annals of the Entomological Society of America,2016,109(4):629-638.
Yocum GD,Rinehart JP,Larson ML.Monitoring diapause development in the Colorado potato beetle,Leptinotarsa decemlineata,under field conditions using molecular biomarkers[J].Journal of Insect Physiology,2011,57(5):645-652.
Zhang LS.Application of diapause and dormancy in insect breeding.In:Zeng FR,Chen HY,eds.The Sysetem Engineering for Rearing Insect Natural Enemies[C].Beijing:China Agricultural Science and Technology Press,2009:54-89.[张礼生.滞育和休眠在昆虫饲养中的应用.见:曾凡荣,陈红印,主编.天敌昆虫饲养系统工程[C].北京:中国农业科学院技术出版社,2009:54-89]
Zhang LS.Several problems in study of diapause in small parasitic wasps.In:Wu KM,eds.Proceedings of Plant Protection Science and Technology Innovation and Specialization of Prevention and Control of Diseases and Pests[C].Beijing:China Agricultural Press,2011:334-345.[张礼生.小型寄生蜂滞育研究中的几个问题.见:吴孔明主编.植保科技创新与病虫防控专业化[C].北京:中国农业科技出版社,2011:334-345.]
Zhang LS,Chen HY,Wang MQ.Study and application of diapause in natural enemies of insects.In:Cheng ZM,eds.Proceedings of Food Security and Plant Protection Science and Technology Innovation[C].Beijing:China Agricultural Science and Technology Press,2009:548-552.[张礼生,陈红印,王孟卿.天敌昆虫的滞育研究及其应用.见:成卓敏主编.粮食安全与植保科技创新[C].北京:中国农业科技出版社,2009:548-552.]
Zhang LS,Chen HY,Wang MQ,et al.Research prospects in diapause of parasitoid wasp[J].Chinese Journal of Biological Control,2014,30(2):149-164.[张礼生,陈红印,王孟卿,等.寄生蜂的滞育研究进展[J].中国生物防治学报,2014,30(2):149-164]
Zhang LS,Chen HY,Zhang J,et al.Maternal effect of diapause in Aphidius gifuensis Ashmead[J].Chinese Journal of Applied Entomology,2014,51(1):35-44.[张礼生,陈红印,张洁,等.滞育烟蚜茧蜂的亲代效应评价[J].应用昆虫学报,2014,51(1):35-44]
Zhang LS,Ren XY,Qi XY,et al.Advances in diapause associated protein of natural enemies of insects.In:Chen WQ,eds.Proceedings of Control of Pests and Diseases and Quality Safety of Agricultural Products[C].Beijing:China Agricultural Science and Technology Press,2015:617.[张礼生,任小云,齐晓阳,等.天敌昆虫滞育关联蛋白的研究进展.见:陈万全主编.病虫害绿色防控与农产品质量安全[C].北京:中国农业科技出版社,2015:617]
Arbab A.Spatial Distribution and minimum sample size for overwintering larvae of the rice stem borer Chilo suppressalis(Walker)in Paddy Fields[J].Neotropical Entomology,2014,43(5):415-420.
Chen H,Zhang H,Throne J,et al.Transcript analysis and expression profiling of three heat shock protein 70 genes in the ectoparasitoid Habrobracon hebetor[J].Insect Science,2014,21(4):415-428.
Chen H,Zhang H,Zhu KY,et al.Performance of diapausing parasitoid wasps,Habrobracon hebetor,after cold storage[J].Biological Control,2013,64(3):186-194.
Chen H,Zhang H,Zhu KY,et al.Induction of reproductive diapause in Habrobracon hebetor(Hymenoptera:Braconidae)when reared at different photoperiods[J].Environmental Entomology,2012,41(3):697-705.
Colinet H,Muratori F,Hance T.Cold-induced expression of diapause in Praon volucre:Fitness cost and morpho-physiological characterization[J].Physiological Entomology,2010,35:301-307.
Colinet H,Renault D,Charoyguevel B,et al.Metabolic and proteomic profiling of diapause in the aphid parasitoid Praon volucre[J].PLo S ONE,2012,7(2):e23606.
Ferracini C,Gonella E,Ferrari E,et al.Novel insight in the life cycle of Torymus sinensis,biocontrol agent of the chestnut gall wasp[J].Bio Control,2015,60(2):169-177.
Garcia PV,Pereira N,Oliveira LM.Side-effects of organic and synthetic pesticides on cold-stored diapausing prepupae of Trichogramma cordubensis[J].Bio Control,2009,54:451-458.
Gardner J,Yong TH,Pitcher SA,et al.Overwintering of Trichogramma ostriniae(Hymenoptera:Trichogrammatidae)within target and non-target host eggs[J].Biocontrol Science and Technology,2013,23(4):367-380.
Gariepy V,Boivin G,Brodeur J,Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions[J].Biological Control,2015,80:1-7.
Gerling D,Erel E,Guershon M,et al.Bionomics of Encarsia scapeata Rivnay(Hymenoptera:Aphelinidae),tritrophic relationships and host-induced diapause[J].Biological Control,2009,49(3):201-206.
Hanson AA,Venette RC,Lelito JP.Cold tolerance of Chinese emerald ash borer parasitoids:Spathius agrili Yang(Hymenoptera:Braconidae),Tetrastichus planipennisi Yang(Hymenoptera:Eulophidae),and Oobius agrili Zhang and Huang(Hymenoptera:Encyrtidae)[J].Biological Control,2013,67:516-529.
Hao Z,Zhao J,Yuan Z,et al.Influence of photoperiod on hydrogen peroxide metabolism during diapause induction in Cotesia vestalis(Haliday)(Hymenoptera:Braconidae)[J].Journal of the Kansas Entomological Society,2012,85(3):206-218.
Hoban J,Duan JJ,Houghgoldstein J.Effects of temperature and photoperiod on the reproductive biology and diapause of Oobius agrili(Hymenoptera:Encyrtidae),an egg parasitoid of emerald ash borer(Coleoptera:Buprestidae)[J].Environmental Entomology,2016,3:726-731.
Huang FX,Jiang S,Ren XY,et al.Differential expression of proteins associated with lipid metabolism in diapausing Aphidius gifuensis Ashmaed[J].Chinese Journal of Biological Control,2015,31(6):811-820.[黄凤霞,蒋莎,任小云,等.烟蚜茧蜂脂代谢相关的滞育相关蛋白差异表达分析[J].中国生物防治学报,2015,31(6):811-820]
Hughes GE,Sterk G,Bale JS.Thermal biology and establishment potential in temperate climates of the aphid parasitoid,Lysiphlebus testaceipes[J].Bio Control,2011,56(1):19-33.
Ishii M,Sato Y,Tagawa J.Diapause in the braconid wasp,Cotesia glomerata(L.)ii.factors inducing and terminating diapause[J].Entomological Science,2000,3(1):201-206.
Larios GLB,Ohno K.Larval summer diapause of Chrysocharis pubicornis(Zetterstedt)(Hymenoptera:Eulophidae),a pupal parasitoid of agromyzid leafminers:Sensitive stage for diapause induction and effects of cool exposure on diapause termination[J].Applied Entomology and Zoology,2007,42(4):587-594.
Larios GLB,Ohno K,Fukuhara F.Effects of photoperiod and temperature on preimaginal development and summer diapause of Chrysocharis pubicornis(Zetterstedt)(Hymenoptera:Eulophidae),a pupal parasitoid of leafminers(Diptera:Agromyzidae[J].Applied Entomology and Zoology,2007,42(2):189-197.
Larson KM,Duan JJ.Differences in the reproductive biology and diapause of two congeneric species of egg parasitoids(Hymenoptera:Encyrtidae)from northeast Asia:Implications for biological control of the invasive emerald ash borer(Coleoptera:Buprestidae)[J].Biological Control,2016,103:39-45.
Legault S,Hébert C,Blais J,et al.Seasonal ecology and thermal constraints of Telenomus spp.(Hymenoptera:Scelionidae),egg parasitoids of the Hemlock Looper(Lepidoptera:Geometridae)[J].Environmental Entomology,2012,41(6):1290-1301.
Lehmann P,Lyytinen A,Piiroinen S,et al.Latitudinal differences in diapause related photoperiodic responses of European Colorado potato beetles(Leptinotarsa decemlineata)[J].Evolutionary Ecology,2015,29(2):269-282.
Li WX,Li JC,Lu ZY,et al.Critial photoperiod and sensitive stage of diapause induction in Microplitis mediator(Haliday)(Hymenoptera:Braconidae)[J].Acta Entomoogica Sinica,2008,6(51):635-639.[李文香,李建成,路子云,等.中红侧沟茧蜂滞育临界光周期和敏感光照虫态的测定[J].昆虫学报,2008,51(6):635-639]
Li YY,Zhang LS,Chen HY.Research advances in diapause in braconids[J].Acta Entomoogica Sinica,2010a,53(10):1167-1178.[李玉艳,张礼生,陈红印.茧蜂滞育的研究进展[J],2010a.昆虫学报,53(10):1167-1178]
Li YY,Zhang LS,Chen HY.Effect of biotic factors on diapause of parasitic wasps[J].Chinese Bulletin of Entomology,2010b,47(4):638-645.[李玉艳,张礼生,陈红印.生物因子对寄生蜂滞育的影响[J].昆虫知识,2010b,47(4):638-645]
Li YY,Zhang LS,Chen HY,et al.Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid's diapause,host diapause and host diet augme[J].Inset Biochemistry and Molecular Biology,2015,63:34-46.
Li YY,Zhang LS,Chen HY,et al.Temperature and photoperiodic response of diapause induction in Aphidius gifuensis[J].Chinese Journal of Applied Entomology,2013,50(3):718-726.[李玉艳,张礼生,陈红印,等.烟蚜茧蜂滞育诱导的温光周期反应[J].应用昆虫学报,2013,50(3):718-726]
Li YY,Zhang LS,Zhang QR,et al.Host diapause status and host diets augmented with cryoprotectants enhance cold hardiness in the parasitoid Nasonia vitripennis[J].Journal of Insect Physiology,2014,70:8-14.
Liao DX,Li XL,Pang XF.Economic Insect Fauna of China,Volume34,Hymenoptera:Chalcidoidea[M].Beijing:Science Press,1987.107.[廖定喜,李学骝,庞雄飞.中国经济昆虫志,第三十四册分册---膜翅目小蜂科[M].北京:科学出版社,1987,107]
Lu ZY,Ran HF,Liu WX,et al.Effects of photoperiod and temperature on diapause induction in Microplitis tuberculifer(Hymenoptera:Braconidea)and the cold storage of its diapause pupae[J].Acta Entomoogica Sinica,2014,57(10):1206-1212.[路子云,冉红凡,刘文旭,等.温度和光周期对管侧沟茧蜂滞育诱导及滞育茧的低温冷藏[J].昆虫学报,2014,57(10):1206-1212]
Menu F,Desouhant E.Bet-hedging for variability in life cycle duration:Bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause[J].Oecologia,2002,132(2):167-174.
Mukai A,Goto SG.The clock gene period is essential for the photoperiodic response in the jewel wasp Nasonia vitripennis(Hymenoptera:Pteromalidae)[J].Applied Entomology and Zoology,2016,51(2):185-194.
Murata Y,Ideo S,Watada M,et al.Genetic and physiological variation among sexual and parthenogenetic populations of Asobara japonica(Hymenoptera:Braconidae),a larval parasitoid of drosophilid flies[J].European Journal of Entomology,2009,106(2):171-178.
Paolucci S,Zande VD,Beukeboom LW.Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe[J].Journal of Evolutionary Biology,2013,26(4):705-718.
Paolucci S,Salis L,Vermeulen CJ,et al.QTL analysis of the photoperiodic response and clinal distribution of period alleles in Nasonia vitripennis[J].Molecular Ecology,2016,25(19):4805-4817.
Pizzol J,Pintureau B.Effect of photoperiod experienced by parents on diapause induction in Trichogramma cacoeciae[J].Entomologia Experimentalis et Applicata,2008,127(1):72-77.
Qiang CK,Du YZ,Qin YH,et al.Overwintering physiology of the rice stem borer larvae,Chilo suppressalis Walker(Lepidoptera:Pyralidae):Roles of glycerol,amino acids,low-molecular weight carbohydrates and antioxidant enzymes[J].African Journal of Biotechnology,2012,11(66):13030-13039.
Ren XY,Qi XY,An T,et al.Research on the accumulation,transformation and regulation of nutrients in diapause insects[J].Chinese Journal of Applied Entomology,2016,53(4):685-695.[任小云,齐晓阳,安涛,等.滞育昆虫营养物质的积累、转化与调控[J].应用昆虫学报,2016,53(4):685-695]
Reznik SY,Vaghina NP,Voinovich ND.Diapause induction in Trichogramma embryophagum Htg.(Hym.,Trichogrammatidae):The dynamics of thermosensitivity[J].Journal of Applied Entomology,2008,132:502-509.
Reznik SY,Vaghina NP,Voinovich ND.Multigenerational maternal effect on diapause induction in Trichogramma species(Hymenoptera:Trichogrammatidae)[J].Biocontrol Science and Technology,2012,22(4):429-445.
Reznik SY,Vaghina NP,Voinovich ND.Maternal influence on diapause induction in Trichogramma(Hymenoptera:Trichogrammatidae):The dynamics of photosen-sitivity[J].Journal of Applied Entomology,2011a,135:438-445.
Reznik SY,Vaghina NP,Voinovich ND.Variations in the tendency to diapause among successive generations of laboratory strains of Trichogramma species(Hymenoptera,Trichogrammatidae):Endogenous or exogenous[J].Entomological Review,2015,95(2):157-165.
Reznik SY,Vaghina AP,Vasiljev L.Photo-thermal regulation of siapause in Trichogramma piceum Djur.(Hymenoptera:Trichogrammatidae)[J].Entomological Review,2013,93(1):9-13.
Reznik SY,Voinovich ND,Vaghina NP.Maternal regulation of Trichogramma embryophagum Htg.(Hymenoptera:Trichogrammatidae)diapause:Photoperiodic sensitivity of adult females[J].Biological Control,2011b,57(2):158-162.
Reznik SY,Samartsev KG.Multigenerational maternal inhibition of prepupal diapause in two Trichogramma species(Hymenoptera:Trichogrammatidae)[J].Journal of Insect Physiology,2015,81:14-20.
Reznik SY,Voinovich ND.Diapause induction in Trichogramma telengai:The dynamics of maternal thermosensitivity[J].Physiological Entomology,2016,41(4):335-343.
Reznik S,Ecological and evolutionary aspects of photothermal regulation of diapause in Trichogramma[J].Zhurnal Evoliutsionno Biokhimii I Fiziologii,2011,47(6):434-443.
Seyahooei MA,Smit FK,Kraaijeveld K,et al.Closely related parasitoids induce different pupation and foraging responses in Drosophila larvae[J].Oikos,2009,118:1148-1157.
Solbreck C,Widenfalk O.Very long diapause and extreme resistance to population disturbance in a galling insect[J].Ecological Entomology,2012,37(1):51-55.
Sun SH,Zhao LW,Qi JY.Diapause induction and post-diapause developement in Chouioia cune Yang(Hymecnoptera:Eulophidac)[J].Acta Entomoogica Sinica,2009,52(12):1307-1311.[孙守慧,赵利伟,祁金玉.白蛾周氏啮小蜂滞育诱导及滞育后发育[J].昆虫学报,2009,52(12):1307-1311]
Vaghina NP,Voinovich ND,Reznik SY.Maternal thermal and photoperiodic effects on the progeny diapause in Trichogramma telengai Sorokina(Hymenoptera:Trichogrammatidae)[J].Entomological Science,2014,17(2):198-206.
Voinovich ND,Reznik SY,Vaghina NP.Maternal thermal effect on diapause in Trichogramma species(Hymenoptera:Trichogrammatidae)[J].Journal of Applied Entomology,2015,139(10):783-790.
Xiao HJ,Mou FC,Zhu XF,et al.Diapause induction,maintenance and termination in the rice stem borer Chilo suppressalis(Walker)[J].Journal of Insect Physiology,2010,56(11):1558-1564.
Xiao L,Xue FS.Ecological and physiology stages of insect's diapause[J].Jiangxi Plant Protection,2009,32(1):3-9.[肖岚,薛芳森.昆虫滞育的生态生理阶段[J].江西植保,2009,32(1):3-9]
Xu WH.Advances in insect diapause[J].Chinese Bulletin of Entomology,2008,54(4):512-517.[徐卫华.昆虫滞育研究进展.昆虫知识,2008,54(4):512-517]
Xu ZB,Liu AP,Xu LB,et al.Diapause induction and cold storage of diapause cocoons in Agrypon flexorium(Hymenoptera:Ochneumonidae)[J].Acta Entomoogica Sinica,2013,56(10):1160-1165.[徐忠宝,刘爱萍,徐林波,等.草地螟阿格姬蜂的滞育诱导和滞育茧的低温贮藏[J].昆虫学报,2013,56(10):1160-1165]
Yang ZQ,Wang XY,Gould JR,et al.Biology and behavior of Spathius agrili,a parasitoid of the emerald ash borer,Agrilus planipennis,in China[J].Journal of Insect Science,2010,10:30.
Yao YX,Duan JJ,Hopper KP,et al.A new species of Oobius trjapitzin(Hymenoptera:Encyrtidae)from the Russian far east that parasitizes eggs of emerald ssh borer(Coleoptera:Buprestidae)[J].Annals of the Entomological Society of America,2016,109(4):629-638.
Yocum GD,Rinehart JP,Larson ML.Monitoring diapause development in the Colorado potato beetle,Leptinotarsa decemlineata,under field conditions using molecular biomarkers[J].Journal of Insect Physiology,2011,57(5):645-652.
Zhang LS.Application of diapause and dormancy in insect breeding.In:Zeng FR,Chen HY,eds.The Sysetem Engineering for Rearing Insect Natural Enemies[C].Beijing:China Agricultural Science and Technology Press,2009:54-89.[张礼生.滞育和休眠在昆虫饲养中的应用.见:曾凡荣,陈红印,主编.天敌昆虫饲养系统工程[C].北京:中国农业科学院技术出版社,2009:54-89]
Zhang LS.Several problems in study of diapause in small parasitic wasps.In:Wu KM,eds.Proceedings of Plant Protection Science and Technology Innovation and Specialization of Prevention and Control of Diseases and Pests[C].Beijing:China Agricultural Press,2011:334-345.[张礼生.小型寄生蜂滞育研究中的几个问题.见:吴孔明主编.植保科技创新与病虫防控专业化[C].北京:中国农业科技出版社,2011:334-345.]
Zhang LS,Chen HY,Wang MQ.Study and application of diapause in natural enemies of insects.In:Cheng ZM,eds.Proceedings of Food Security and Plant Protection Science and Technology Innovation[C].Beijing:China Agricultural Science and Technology Press,2009:548-552.[张礼生,陈红印,王孟卿.天敌昆虫的滞育研究及其应用.见:成卓敏主编.粮食安全与植保科技创新[C].北京:中国农业科技出版社,2009:548-552.]
Zhang LS,Chen HY,Wang MQ,et al.Research prospects in diapause of parasitoid wasp[J].Chinese Journal of Biological Control,2014,30(2):149-164.[张礼生,陈红印,王孟卿,等.寄生蜂的滞育研究进展[J].中国生物防治学报,2014,30(2):149-164]
Zhang LS,Chen HY,Zhang J,et al.Maternal effect of diapause in Aphidius gifuensis Ashmead[J].Chinese Journal of Applied Entomology,2014,51(1):35-44.[张礼生,陈红印,张洁,等.滞育烟蚜茧蜂的亲代效应评价[J].应用昆虫学报,2014,51(1):35-44]
Zhang LS,Ren XY,Qi XY,et al.Advances in diapause associated protein of natural enemies of insects.In:Chen WQ,eds.Proceedings of Control of Pests and Diseases and Quality Safety of Agricultural Products[C].Beijing:China Agricultural Science and Technology Press,2015:617.[张礼生,任小云,齐晓阳,等.天敌昆虫滞育关联蛋白的研究进展.见:陈万全主编.病虫害绿色防控与农产品质量安全[C].北京:中国农业科技出版社,2015:617]