昆虫病原微生物对其寄主行为的调控作用研究进展
|
摘要
昆虫病原微生物是调控昆虫种群数量动态的重要因子,其作为生物防治害虫的重要手段被广泛应用。昆虫病原物往往通过调控其寄主行为来提高自身的适应性,而有些寄主行为的改变却是其应对病原物侵染的免疫反应。发烧行为被证明可抑制病原增殖并延长寄主死亡;取食行为变化影响病原物或寄主的适应性;繁殖行为主要表现在产卵力、交配行为和性信息素等方面的变化;社会性行为改变对整个社会群体的适应性或病原物传播有影响;病原物所引起的寄主防卫和群集能力下降被认为对病原传播不利;病虫趋光和趋地行为、顶峰行为和活体寄主传病行为等被认为是病原物操纵的有利于病原微生物扩散和传播的行为。明确昆虫病原物调控其寄主行为的策略和机制对于寻找到新的害虫防治方法有指导意义。
Entomopathogens are an important factor to regulate dynamics of insect population, and widely applied for biological control of pest insects. Entomopathogens increase their fitness by modifying the host behavior; some modifications of host behavior are immune response for infection of pathogens. Behavioral fever could suppress pathogen reproduction and extend the death time of host. The changes of feeding behavior affect the fitness of both host and pathogen. Reproductive behavior changes contain the modification from the fecundity, sexual attractiveness and sex pheromones. The alterations of social behavior are effective on the fitness of social crowd and transmission of pathogens. The weakness of defensive and aggregation behavior of infected host is unbeneficial to the transmission of pathogens; but the responses of phototropism and geotropism of host manipulated by pathogen are helpful for the spread and transmission of the pathogen. It is meaningful to find new methods controlling insect pests by discovering the strategy and mechanism of the pathogen regulating host behaviors.
Entomopathogens are an important factor to regulate dynamics of insect population, and widely applied for biological control of pest insects. Entomopathogens increase their fitness by modifying the host behavior; some modifications of host behavior are immune response for infection of pathogens. Behavioral fever could suppress pathogen reproduction and extend the death time of host. The changes of feeding behavior affect the fitness of both host and pathogen. Reproductive behavior changes contain the modification from the fecundity, sexual attractiveness and sex pheromones. The alterations of social behavior are effective on the fitness of social crowd and transmission of pathogens. The weakness of defensive and aggregation behavior of infected host is unbeneficial to the transmission of pathogens; but the responses of phototropism and geotropism of host manipulated by pathogen are helpful for the spread and transmission of the pathogen. It is meaningful to find new methods controlling insect pests by discovering the strategy and mechanism of the pathogen regulating host behaviors.
引文
[1]Gul HT,Saeed S,Khan FZA.Entomopathogenic fungi as effective insect pest management tactic:a review.Applied Sciences and Business Economics,2014,1(1):10-18.
[2]Fukatsu T,Sato H,Kuriyama H.Isolation,inoculation to insect host,and molecular phylogeny of an entomogenous fungus Paecilomyces tenuipes.Journal of Invertebrate Pathology,1997,70(3):203-208.
[3]Hajek AE,St.Leger RJ.Interactions between fungal pathogens and insect hosts.Annual Review of Entomology,1994,39:293-322.
[4]White Jr JF,Bacon CW,Hywel-Jones NL,Spatafora JW.Clavicipitalean Fungi:Evolutionary Biology,Chemistry,Biocontrol,and Cultural Impacts.New York:Marcel Dekker,2003.
[5]Hu G,St.Leger RJ.2002.Field studies using a recombinant mycoinsecticide(Metarhizium anisopliae)reveal that it is rhizosphere competent.Applied Environmental Microbiology,2002,68(12):6383-6387.
[6]Shah PA,Pell JK.Entomopathogenic fungi as biological control agents.Applied Microbiology and Biotechnology,2003,61(5/6):413-423.
[7]Moore J.Parasites and the Behavior of Animals.Oxford,UK:Oxford University Press,2002.
[8]Carruthers RI,Larkin TS,Firstencel H,Feng ZD.Influence of thermal ecology on the mycosis of a rangeland grasshopper.Ecology,1992,73(1):190-204.
[9]Olesen US.Effect of humidity and temperature on Entomophthora muscae infecting the house fly,Musca domestica and the increase of survival of the fly by behavioural fever.Master Dissertation of University of Copenhagen,1985.
[10]Watson DW,Mullens BA,Petersen JJ.Behavioral fever response of Musca domestica(Diptera:Muscidae)to infection by Entomophthora muscae(Zygomycetes:Entomophthorales).Journal of Invertebrate Pathology,1993,61(1):10-16.
[11]Kalsbeek V,Mullens BA,Jespersen JB.Field studies of Entomophthora(Zygomycetes:Entomophthorales)-induced behavioral fever in Musca domestica(Diptera:Muscidae)in Denmark.Biological Control,2001,21(3):264-273.
[12]Anderson RD,Blanford S,Thomas MB.House flies delay fungal infection by fevering:at a cost.Ecological Entomology,2013,38(1):1-10.
[13]Anderson RD,Blanford S,Jenkins NE,Thomas MB.Discriminating fever behavior in house flies.PLo S One,2013,8(4):e62269,doi:10.1371/journal.pone.0062269.
[14]Blanford S,Thomas MB.Host thermal biology:the key to understanding host-pathogen interactions and microbial pest control?Agricultural and Forest Entomology,1999,1(3):195-202.
[15]Blanford S,Thomas MB.Role of thermal biology in disease dynamics.Aspects of Applied Biology,1999,53:73-82.
[16]Blanford S,Thomas MB.Thermal behavior of two acridid species:effects of habitat and season on body temperature and the potential impact on biocontrol with pathogens.Environmental Entomology,2000,29(5):1060-1069.
[17]Blanford S,Thomas MB,Langewald J.Behavioural fever in the Senegalese grasshopper,Oedaleus senegalensis,and its implications for biological control using pathogens.Ecological Entomology,1998,23(1):9-14.
[18]Inglis GD,Johnson DL,Cheng KJ,Goettel MS.Use of pathogen combinations to overcome the constraints of temperature on entomopathogenic hyphomycetes against grasshoppers.Biological Control,1997,8(2):143-152.
[19]Inglis GD,Johnson DL,Goettel MS.Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers.Biological Control,1996,7(2):131-139.
[20]Ouedraogo RM,Goettel MS,Brodeur J.Behavioral thermoregulation in the migratory locust:a therapy to overcome fungal infection.Oecologia,2004,138(2):312-319.
[21]Elliot SL,Blanford S,Thomas MB.Host-pathogen interactions in a varying environment:temperature,behavioural fever and fitness.Proceedings of the Royal Society B:Biological Science,2002,269(100):1599-1607.
[22]Furlong MJ,Pell JK.The influence of environmental factors on the persistence of Zoophthora radicans conidia.Journal of Invertebrate Pathology,1997,69(3):223-233.
[23]Freimoser FM,Hu G,St.Leger RJ.Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro.Microbiology,2005,151(2):361-371.
[24]Thomas MB,Blanford S,Lomer CJ.Reduction of feeding by the variegated grasshopper,Zonocerus variegatus,following infection by the fungal pathogen,Metarhizium flavoviride.Biocontrol Science and Technology,1997,7(3):327-334.
[25]De Faria MR,Almeida DDO,Magalh?es BP.Food consumption of Rhammatocerus schistocercoides rehn(Orthoptera:Acrididae)infected by the fungus Metarhizium flavoviride gams&rozsypal.Anais da Sociedade Entomológica do Brasil,1999,28(1):91-99.
[26]Arthurs S,Thomas MB.Effects of a mycoinsecticide on feeding and fecundity of the brown locust Locustana pardalina.Biocontrol Science and Technology,2000,10(3):321-329.
[27]Ekesi S.Pathogenicity and antifeedant activity of entomopathogenic hyphomycetes to the cowpea leaf beetle,Ootheca mutabilis Shalberg.Insect Science and Its Application,2001,21(1):55-60.
[28]France A,Gerding M,Sandoval YA.Pathogenicity of Chilean isolates of Beauveria bassiana to adults of Asynonychus cervinus(Coleoptera:Curculionidae).Agricultura Técnica,2002,62(4):489-496.
[29]Tefera T,Pringle KL.Food consumption by Chilo partellus(Lepidoptera:Pyralidae)larvae infected with Beauveria bassiana and Metarhizium anisopliae and effects of feeding natural versus artificial diets on mortality and mycosis.Journal of Invertebrate Pathology,2003,84(3):220-225.
[30]Moore D,Reed M,le Patourel G,Abraham YJ,Prior C.Reduction of feeding by the desert locust,Schistocerca gregaria,after infection with Metarhizium flavoviride.Journal of Invertebrate Pathology,1992,60(3):304-307.
[31]Shi WP,Njagi PGN.Disruption of aggregation behaviour of oriental migratory locusts(Locusta migratoria manilensis)infected with Nosema locustae.Journal of Applied Entomology,2004,128(6):414-418.
[32]Mohamed AKA.Pathogenicity of Nomuraea rileyi and its effect on food consumption and utilization by Heliothis virescens larvae.Journal of the Georgia Entomological Society,1982,17:377-382.
[33]Samuels RI,Reynolds SE,Charnley AK.Calcium channel activation of insect muscle by destruxins,insecticidal compounds produced by the entomopathogenic fungus Metarhizium anisopliae.Comparative Biochemistry and Physiology Part C:Comparative Pharmacology,1988,90(2):403-412.
[34]Cheung PYK,Grula EA.In vivo events associated with entomopathology of Beauveria bassiana for the corn earworm(Heliothis zea).Journal of Invertebrate Pathology,1982,39(3):303-313.
[35]Hajek AE.Food consumption by Lymantria dispar(Lepidoptera:Lymantriidae)larvae infected with Entomophaga maimaiga(Zygomycetes:Entomophthorales).Environmental Entomology,1989,18(4):723-727.
[36]Furlong MJ,Pell JK,Reddy GVP.Premortality effects of Zoophthora radicans infection in Plutella xylostella.Journal of Invertebrate Pathology,1997,70(3):214-220.
[37]Tyrrell D.Pathogenesis of Entomophaga aulicae:I.disease symptoms and effect of infection on weight gain of infected Choristoneura fumiferana and Malacosoma disstria larvae.Journal of Invertebrate Pathology,1990,56(2):150-156.
[38]Glare TR,Milner RJ.Ecology of entomopathogenic fungi//Arora DK,Ajello L,Mukerji KG.Handbook of Applied Mycology,Vol.2:Humans,Animals,and Insects.New York:Marcel Dekker,1991.
[39]Funk CJ,Ramoska WA,Bechtel DB.Histopathology of Entomophaga grylli pathotype 2 infections in Melanoplus differentialis.Journal of Invertebrate Pathology,1993,61(2):196-202.
[40]O’Reilly DR.Baculovirus-encoded ecdysteroid UDP-glucosyltransferases.Insect Biochemistry and Molecular Biology,1995,25(5):541-550.
[41]Jensen MA,Losey JE,Hajek AE.Altered behavior and distribution of pea aphids,Acyrthosiphon pisum(Homoptera:Aphididae),infected with Pandora neoaphidis(Zygomycetes:Entomophthorales).Bio Control,2001,46(1):337-343.
[42]Roy HE,Alderson PG,Pell JK.The effect of Erynia neoaphidis infection and coccinellid foraging on the spatial distribution of aphids on plants.Journal of Invertebrate Pathology,2002,81(2):127-129.
[43]Mc Allister MK,Roitberg BD.Adaptive suicidal behaviour in pea aphids.Nature,1987,328(6133):797-799.
[44]Roditakis E,Couzin ID,Franks NR,Charnley AK.Effects of Lecanicillium longisporum infection on the behaviour of the green peach aphid Myzus persicae.Journal of Insect Physiology,2008,54(1):128-136.
[45]Blanford S,Thomas MB.Adult survival,maturation,and reproduction of the desert locust Schistocerca gregaria infected with the fungus Metarhizium anisopliae var acridum.Journal of Invertebrate Pathology,2001,78(1):1-8.
[46]Fu XJ,Hunter DM,Shi WP.Effect of Paranosema(Nosema)locustae(Microsporidia)on morphological phase transformation of Locusta migratoria manilensis(Orthoptera:Acrididae).Biocontrol Science and Technology,2010,20(7):683-693.
[47]Baverstock J,Roy HE,Clark SJ,Pell J.The effect of fungal infection on the reproductive potential of aphids and their progeny.Journal of Invertebrate Pathology,2006,91(2):136-9.
[48]Eilenberg J.Abnormal egg-laying behaviour of female carrot flies(Psila rosae)induced by the fungus Entomophthora muscae.Entomologia Experimentalis et Applicata,1987,43(1):61-65.
[49]Staudacher H,Menken SBJ,Groot AT.Effects of immune challenge on the oviposition strategy of a noctuid moth.Journal of Evolutionary Biology,2015,28(8):1568-1577.
[50]M?ller AP.A fungus infecting domestic flies manipulates sexual behaviour of its host.Behavioral Ecology and Sociobiology,1993,33(6):403-407.
[51]Zurek L,Watson DW,Krasnoff SB,Schal C.Effect of the entomopathogenic fungus,Entomophthora muscae(Zygomycetes:Entomophthoraceae),on sex pheromone and other cuticular hydrocarbons of the house fly,Musca domestica.Journal of Invertebrate Pathology,2002,80(3):171-176.
[52]Watson DW,Petersen JJ.Sexual activity of male Musca domestica(Diptera:Muscidae)infected with Entomophthora muscae(Entomophthoraceae:Entomophthorales).Biological Control,1993,3(1):22-26.
[53]Reddy GVP,Furlong MJ,Pell JK,Poppy GM.Zoophthora radicans infection inhibits the response to and production of sex pheromone in the diamondback moth.Journal of Invertebrate Pathology,1998,72(2):167-169.
[54]Moret Y,Schmid-Hempel P.Social life-history response to individual immune challenge of workers of Bombus terrestris L.:a possible new cooperative phenomenon.Ecological Letter,2004,7(2):146-152.
[55]Oi DH,Pereira RM.Ant behavior and microbial pathogens(Hymenoptera:Formicidae).The Florida entomologist,1993,76(1):63-74.
[56]Siebeneicher SR,Vinson SB,Kenerley CM.Infection of the red imported fire ant by Beauveria bassiana through various routes of exposure.Journal of Invertebrate Pathology,1992,59(3):280-285.
[57]Kramm KR,West DF,Rockenbach PG.Termite pathogens:transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp.termites.Journal of Invertebrate Pathology,1982,40(1):1-6.
[58]Febvay G,Decharme M,Kermarrec A.Digestion of chitin by the labial glands of Acromyrmex octospinosus reich(Hymenoptera:Formicidae).Canadian Journal of Zoology,1984,62(2):229-234.
[59]Hughes WOH,Eilenberg J,Boomsma JJ.Trade-offs in group living:transmission and disease resistance in leaf-cutting ants.Proceedings of the Royal Society B:Biological Science,2002,269(1502):1811-1819.
[60]Zhukovskaya M,Yanagawa A,Forschler BT.Grooming behavior as a mechanism of insect disease defense.Insects,2013,4(4):609-630.
[61]Konrad M,Grasse AV,Tragust S,Cremer S.Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host.Proceedings of the Royal Society B:Biological Science,2015,282(1799):20141976.
[62]Turnbull C,Wilson PD,Hoggard S,Gillings M,Palmer C,Smith S,Beattie D,Hussey S,Stow A,Beattie A.Primordial enemies:fungal pathogens in thrips societies.PLo S One,2012,7(11):e49737,doi:10.1371/journal.pone.0049737.
[63]Mc Allister MK,Roitberg BD,Weldon KL.Adaptive suicide in pea aphids:decisions are cost sensitive.Animal Behaviour,1990,40(1):167-175.
[64]Poulin R.Altered behaviour in parasitized bumblebees:parasite manipulation or adaptive suicide?Animal Behaviour,1992,44(1):174-176.
[65]Leclerc JB,Detrain C.Ants detect but do not discriminate diseased workers within their nest.The Science of Nature,2016,103(7/8):70.
[66]Rosengaus RB,Jordan C,Lefebvre ML,Traniello JFA.Pathogen alarm behavior in a termite:a new form of communication in social insects.Naturwissenschaften,1999,86(11):544-548
[67]Adamo SA.Parasites:evolution’s neurobiologists.Journal of Experimental Biology,2013,216(Pt 10):3-10.
[68]Feng YJ,Ge Y,Tan SQ,Zhang KQ,Ji R,Shi WP.Effect of Paranosema locustae(Microsporidia)on the behavioural phases of Locusta migratoria(Orthoptera:Acrididae)in the laboratory.Biocontrol Science and Technology,2015,25(1):48-55.
[69]Shi WP,Guo Y,Xu C,Tan SQ,Miao J,Feng YJ,Zhao H,Leger RJS,Fang WG.Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior.Proceedings of the National Academy of Sciences of the United States of America,2014,111(4):1343-1348.
[70]Tan SQ,Zhang KQ,Chen HX,Ge Y,Ji R,Shi WP.The mechanism for microsporidian parasite suppression of the hindgut bacteria of the migratory locust Locusta migratoria manilensis.Scientific Reports,2015,5:17365,doi:10.1038/srep17365.
[71]Wang YD,Yang PC,Cui F,Kang L.Altered Immunity in crowded locust reduced fungal(Metarhizium anisopliae)pathogenesis.PLo S Pathogens,2013,9(1):e1003102,doi:10.1371/journal.ppat.1003102.
[72]Arthurs S,Thomas MB.Behavioural changes in Schistocerca gregaria following infection with a fungal pathogen:implications for susceptibility to predation.Ecological Entomology,2001,26(3):227-234.
[73]Roy HE,Pell JK,Alderson PG.Effects of fungal infection on the alarm response of pea aphids.Journal of Invertebrate Pathology,1999,74(1):69-75.
[74]Fuentes CE,Pell JK,Niemeyer HM.Influence of plant resistance at the third trophic level:interactions between parasitoids and entomopathogenic fungi of cereal aphids.Oecologia,1998,117(3):426-432.
[75]Roy HE,Pell JK,Clark SJ,Alderson PG.Implications of predator foraging on aphid pathogen dynamics.Journal of Invertebrate Pathology,1998,71(3):236-247.
[76]Roy HE,Baverstock J,Chamberlain K,Pell JK.Do aphids infected with entomopathogenic fungi continue to produce and respond to alarm pheromone?Biocontrol Science and Technology,2005,15(8):859-866.
[77]Myles TG.Isolation of Metarhizium anisopliae(Deuteromycotina:Hyphomycetes)from Reticulitermes flavipes(Isoptera:Rhinotermitidae)with convenient methods for its culture and collection of conidia.Sociobiology,2002,40(2):257-264.
[78]Staples JA,Milner RJ.A laboratory evaluation of the repellency of Metarhizium anisopliae conidia to Coptotermes lacteus.Sociobiology,2000,36(1):133-148.
[79]Lord JC.Response of the wasp Cephalonomia tarsalis(Hymenoptera:Bethylidae)to Beauveria bassiana(Hyphomycetes:Moniliales)as free conidia or infection in its host,the sawtoothed grain beetle,Oryzaephilus surinamensis(Coleoptera:Silvanidae).Biological Control,2001,21(3):300-304.
[80]Mesquita ALM,Lacey LA.Interactions among the entomopathogenic fungus,Paecilomyces fumosoroseus(Deuteromycotina:Hyphomycetes),the parasitoid,Aphelinus asychis(Hymenoptera:Aphelinidae),and their aphid host.Biological Control,2001,22(1):51-59.
[81]Fransen JJ,van Lenteren JC.Host selection and survival of the parasitoid Encarsia formosa on greenhouse whitefly,Trialeurodes vaporariorum,in the presence of hosts infected with the fungus Aschersonia aleyrodis.Entomologia Experimentalis et Applicata,1993,69(3):239-249.
[82]Brobyn PJ,Clark SJ,Wilding N.Effect of fungus infection of Metopolophium dirhodum[Hom.:Aphididae]on the oviposition behaviour of the aphid parasitoid Aphidius rhopalosiphi[Hym.:Aphidiidae].Entomophaga,1988,33(3):333-338.
[83]Chow A,Dunlap CA,Jackson MA,Flores D,Patt JM,Sétamou M.Oviposition behavior and survival of Tamarixia radiata(Hymenoptera:Eulophidae),an ectoparasitoid of the Asian citrus psyllid,Diaphorina citri(Hemiptera:Liviidae),on hosts exposed to an entomopathogenic fungus,Isaria fumosorosea(Hypocreales:Cordycipitaceae),under laboratory conditions.Journal of Economic Entomology,2016,109(5):1995-2005.
[84]Ohbayashi T,Iwabuchi K.Abnormal behavior of the common armyworm Pseudaletia separate(WALKER)(Lepidoptera:Noctuidae)larvae infected with an entomogenous fungus,Entomophaga aulicae and a nuclear polyhedrosis virus.Applied Entomology and Zoology,1991,26(4):579-585.
[85]Milner RJ,Holdom DG,Glare TR.Diurnal patterns of mortality in aphids infected by entomophthoran fungi.Entomologia Experimentalis et Applicata,1984,36(1):37-42.
[86]Krasnoff SB,Watson DW,Gibson DM,Kwan EC.Behavioral effects of the entomopathogenic fungus,Entomophthora muscae on its host Musca domestica:postural changes in dying hosts and gated pattern of mortality.Journal of Insect Physiology,1995,41(10):895-903.
[87]Thomsen L,Eilenberg J.Entomophthora muscae resting spore formation in vivo in the host Delia radicum.Journal of Invertebrate Pathology,2000,76(2):127-130.
[88]Steinkraus DC,Mueller AJ,Humber RA.Furia virescens(Thaxter)Humber(Zygomycetes:Entomophthoraceae)infections in the armyworm,Pseudaletia unipuncta(Haworth)(Lepidoptera:Noctuidae)in Arkansas with notes on other natural enemies.Journal of Entomological Science,1993,28(4):376-386.
[89]Evans HC.Mycopathogens of insects of epigeal and aerial habitats//Wilding N,Collins NM,Hammond PM,Webber JF.Insect-Fungus Interactions.San Diego:Academic Press,1989,205-238.
[90]Steinkraus DC,Kramer JP.Development of resting spores of Erynia aquatica(Zygomycetes:Entomophthoraceae)in Aedes aegypti(Diptera:Culicidae).Environmental Entomology,1989,18(6):1147-1152.
[91]Duke L,Steinkraus DC,English JE,Smith KG.Infectivity of resting spores of Massospora cicadina(Entomophthorales:Entomophthoraceae),an entomopathogenic fungus of periodical cicadas(Magicicada spp.)(Homoptera:Cicadidae).Journal of Invertebrate Pathology,2002,80(1):1-6.
[92]Hutchison JA.Studies on a new Entomophthora attacking calyptrate flies.Mycologia,1962,54(3):258-271.
[93]Mac Leod DM,Müller-K?gler E.Entomogenous fungi:Entomophthora species with pear-shaped to almost spherical conidia(Entomophthorales:Entomophthoraceae).Mycologia,1993,65(4):823-893.
[94]Katsuma S.Phosphatase activity of Bombyx mori nucleopolyhedrovirus PTP is dispensable for enhanced locomotory activity in B.mori larvae.Journal of Invertebrate Pathology,2015,132:228-232.
[95]Kamita SG,Nagasaka K,Chua JW,Shimada T,Mita K,Kobayashi M,Maeda S,Hammock BD.A baculovirusencoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host.Proceedings of the National Academy of Sciences of the United States of America,2005,102(7):2584-2589.
[96]Janzen DH.When is it coevolution?Evolution,1980,34(3):611-612.
[97]Butt TM,Jackson C,Magan N.Fungi as Biocontrol Agents:Progress,Problems and Potential.Wallingford,UK:CABIPublishing,2001.
[2]Fukatsu T,Sato H,Kuriyama H.Isolation,inoculation to insect host,and molecular phylogeny of an entomogenous fungus Paecilomyces tenuipes.Journal of Invertebrate Pathology,1997,70(3):203-208.
[3]Hajek AE,St.Leger RJ.Interactions between fungal pathogens and insect hosts.Annual Review of Entomology,1994,39:293-322.
[4]White Jr JF,Bacon CW,Hywel-Jones NL,Spatafora JW.Clavicipitalean Fungi:Evolutionary Biology,Chemistry,Biocontrol,and Cultural Impacts.New York:Marcel Dekker,2003.
[5]Hu G,St.Leger RJ.2002.Field studies using a recombinant mycoinsecticide(Metarhizium anisopliae)reveal that it is rhizosphere competent.Applied Environmental Microbiology,2002,68(12):6383-6387.
[6]Shah PA,Pell JK.Entomopathogenic fungi as biological control agents.Applied Microbiology and Biotechnology,2003,61(5/6):413-423.
[7]Moore J.Parasites and the Behavior of Animals.Oxford,UK:Oxford University Press,2002.
[8]Carruthers RI,Larkin TS,Firstencel H,Feng ZD.Influence of thermal ecology on the mycosis of a rangeland grasshopper.Ecology,1992,73(1):190-204.
[9]Olesen US.Effect of humidity and temperature on Entomophthora muscae infecting the house fly,Musca domestica and the increase of survival of the fly by behavioural fever.Master Dissertation of University of Copenhagen,1985.
[10]Watson DW,Mullens BA,Petersen JJ.Behavioral fever response of Musca domestica(Diptera:Muscidae)to infection by Entomophthora muscae(Zygomycetes:Entomophthorales).Journal of Invertebrate Pathology,1993,61(1):10-16.
[11]Kalsbeek V,Mullens BA,Jespersen JB.Field studies of Entomophthora(Zygomycetes:Entomophthorales)-induced behavioral fever in Musca domestica(Diptera:Muscidae)in Denmark.Biological Control,2001,21(3):264-273.
[12]Anderson RD,Blanford S,Thomas MB.House flies delay fungal infection by fevering:at a cost.Ecological Entomology,2013,38(1):1-10.
[13]Anderson RD,Blanford S,Jenkins NE,Thomas MB.Discriminating fever behavior in house flies.PLo S One,2013,8(4):e62269,doi:10.1371/journal.pone.0062269.
[14]Blanford S,Thomas MB.Host thermal biology:the key to understanding host-pathogen interactions and microbial pest control?Agricultural and Forest Entomology,1999,1(3):195-202.
[15]Blanford S,Thomas MB.Role of thermal biology in disease dynamics.Aspects of Applied Biology,1999,53:73-82.
[16]Blanford S,Thomas MB.Thermal behavior of two acridid species:effects of habitat and season on body temperature and the potential impact on biocontrol with pathogens.Environmental Entomology,2000,29(5):1060-1069.
[17]Blanford S,Thomas MB,Langewald J.Behavioural fever in the Senegalese grasshopper,Oedaleus senegalensis,and its implications for biological control using pathogens.Ecological Entomology,1998,23(1):9-14.
[18]Inglis GD,Johnson DL,Cheng KJ,Goettel MS.Use of pathogen combinations to overcome the constraints of temperature on entomopathogenic hyphomycetes against grasshoppers.Biological Control,1997,8(2):143-152.
[19]Inglis GD,Johnson DL,Goettel MS.Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers.Biological Control,1996,7(2):131-139.
[20]Ouedraogo RM,Goettel MS,Brodeur J.Behavioral thermoregulation in the migratory locust:a therapy to overcome fungal infection.Oecologia,2004,138(2):312-319.
[21]Elliot SL,Blanford S,Thomas MB.Host-pathogen interactions in a varying environment:temperature,behavioural fever and fitness.Proceedings of the Royal Society B:Biological Science,2002,269(100):1599-1607.
[22]Furlong MJ,Pell JK.The influence of environmental factors on the persistence of Zoophthora radicans conidia.Journal of Invertebrate Pathology,1997,69(3):223-233.
[23]Freimoser FM,Hu G,St.Leger RJ.Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro.Microbiology,2005,151(2):361-371.
[24]Thomas MB,Blanford S,Lomer CJ.Reduction of feeding by the variegated grasshopper,Zonocerus variegatus,following infection by the fungal pathogen,Metarhizium flavoviride.Biocontrol Science and Technology,1997,7(3):327-334.
[25]De Faria MR,Almeida DDO,Magalh?es BP.Food consumption of Rhammatocerus schistocercoides rehn(Orthoptera:Acrididae)infected by the fungus Metarhizium flavoviride gams&rozsypal.Anais da Sociedade Entomológica do Brasil,1999,28(1):91-99.
[26]Arthurs S,Thomas MB.Effects of a mycoinsecticide on feeding and fecundity of the brown locust Locustana pardalina.Biocontrol Science and Technology,2000,10(3):321-329.
[27]Ekesi S.Pathogenicity and antifeedant activity of entomopathogenic hyphomycetes to the cowpea leaf beetle,Ootheca mutabilis Shalberg.Insect Science and Its Application,2001,21(1):55-60.
[28]France A,Gerding M,Sandoval YA.Pathogenicity of Chilean isolates of Beauveria bassiana to adults of Asynonychus cervinus(Coleoptera:Curculionidae).Agricultura Técnica,2002,62(4):489-496.
[29]Tefera T,Pringle KL.Food consumption by Chilo partellus(Lepidoptera:Pyralidae)larvae infected with Beauveria bassiana and Metarhizium anisopliae and effects of feeding natural versus artificial diets on mortality and mycosis.Journal of Invertebrate Pathology,2003,84(3):220-225.
[30]Moore D,Reed M,le Patourel G,Abraham YJ,Prior C.Reduction of feeding by the desert locust,Schistocerca gregaria,after infection with Metarhizium flavoviride.Journal of Invertebrate Pathology,1992,60(3):304-307.
[31]Shi WP,Njagi PGN.Disruption of aggregation behaviour of oriental migratory locusts(Locusta migratoria manilensis)infected with Nosema locustae.Journal of Applied Entomology,2004,128(6):414-418.
[32]Mohamed AKA.Pathogenicity of Nomuraea rileyi and its effect on food consumption and utilization by Heliothis virescens larvae.Journal of the Georgia Entomological Society,1982,17:377-382.
[33]Samuels RI,Reynolds SE,Charnley AK.Calcium channel activation of insect muscle by destruxins,insecticidal compounds produced by the entomopathogenic fungus Metarhizium anisopliae.Comparative Biochemistry and Physiology Part C:Comparative Pharmacology,1988,90(2):403-412.
[34]Cheung PYK,Grula EA.In vivo events associated with entomopathology of Beauveria bassiana for the corn earworm(Heliothis zea).Journal of Invertebrate Pathology,1982,39(3):303-313.
[35]Hajek AE.Food consumption by Lymantria dispar(Lepidoptera:Lymantriidae)larvae infected with Entomophaga maimaiga(Zygomycetes:Entomophthorales).Environmental Entomology,1989,18(4):723-727.
[36]Furlong MJ,Pell JK,Reddy GVP.Premortality effects of Zoophthora radicans infection in Plutella xylostella.Journal of Invertebrate Pathology,1997,70(3):214-220.
[37]Tyrrell D.Pathogenesis of Entomophaga aulicae:I.disease symptoms and effect of infection on weight gain of infected Choristoneura fumiferana and Malacosoma disstria larvae.Journal of Invertebrate Pathology,1990,56(2):150-156.
[38]Glare TR,Milner RJ.Ecology of entomopathogenic fungi//Arora DK,Ajello L,Mukerji KG.Handbook of Applied Mycology,Vol.2:Humans,Animals,and Insects.New York:Marcel Dekker,1991.
[39]Funk CJ,Ramoska WA,Bechtel DB.Histopathology of Entomophaga grylli pathotype 2 infections in Melanoplus differentialis.Journal of Invertebrate Pathology,1993,61(2):196-202.
[40]O’Reilly DR.Baculovirus-encoded ecdysteroid UDP-glucosyltransferases.Insect Biochemistry and Molecular Biology,1995,25(5):541-550.
[41]Jensen MA,Losey JE,Hajek AE.Altered behavior and distribution of pea aphids,Acyrthosiphon pisum(Homoptera:Aphididae),infected with Pandora neoaphidis(Zygomycetes:Entomophthorales).Bio Control,2001,46(1):337-343.
[42]Roy HE,Alderson PG,Pell JK.The effect of Erynia neoaphidis infection and coccinellid foraging on the spatial distribution of aphids on plants.Journal of Invertebrate Pathology,2002,81(2):127-129.
[43]Mc Allister MK,Roitberg BD.Adaptive suicidal behaviour in pea aphids.Nature,1987,328(6133):797-799.
[44]Roditakis E,Couzin ID,Franks NR,Charnley AK.Effects of Lecanicillium longisporum infection on the behaviour of the green peach aphid Myzus persicae.Journal of Insect Physiology,2008,54(1):128-136.
[45]Blanford S,Thomas MB.Adult survival,maturation,and reproduction of the desert locust Schistocerca gregaria infected with the fungus Metarhizium anisopliae var acridum.Journal of Invertebrate Pathology,2001,78(1):1-8.
[46]Fu XJ,Hunter DM,Shi WP.Effect of Paranosema(Nosema)locustae(Microsporidia)on morphological phase transformation of Locusta migratoria manilensis(Orthoptera:Acrididae).Biocontrol Science and Technology,2010,20(7):683-693.
[47]Baverstock J,Roy HE,Clark SJ,Pell J.The effect of fungal infection on the reproductive potential of aphids and their progeny.Journal of Invertebrate Pathology,2006,91(2):136-9.
[48]Eilenberg J.Abnormal egg-laying behaviour of female carrot flies(Psila rosae)induced by the fungus Entomophthora muscae.Entomologia Experimentalis et Applicata,1987,43(1):61-65.
[49]Staudacher H,Menken SBJ,Groot AT.Effects of immune challenge on the oviposition strategy of a noctuid moth.Journal of Evolutionary Biology,2015,28(8):1568-1577.
[50]M?ller AP.A fungus infecting domestic flies manipulates sexual behaviour of its host.Behavioral Ecology and Sociobiology,1993,33(6):403-407.
[51]Zurek L,Watson DW,Krasnoff SB,Schal C.Effect of the entomopathogenic fungus,Entomophthora muscae(Zygomycetes:Entomophthoraceae),on sex pheromone and other cuticular hydrocarbons of the house fly,Musca domestica.Journal of Invertebrate Pathology,2002,80(3):171-176.
[52]Watson DW,Petersen JJ.Sexual activity of male Musca domestica(Diptera:Muscidae)infected with Entomophthora muscae(Entomophthoraceae:Entomophthorales).Biological Control,1993,3(1):22-26.
[53]Reddy GVP,Furlong MJ,Pell JK,Poppy GM.Zoophthora radicans infection inhibits the response to and production of sex pheromone in the diamondback moth.Journal of Invertebrate Pathology,1998,72(2):167-169.
[54]Moret Y,Schmid-Hempel P.Social life-history response to individual immune challenge of workers of Bombus terrestris L.:a possible new cooperative phenomenon.Ecological Letter,2004,7(2):146-152.
[55]Oi DH,Pereira RM.Ant behavior and microbial pathogens(Hymenoptera:Formicidae).The Florida entomologist,1993,76(1):63-74.
[56]Siebeneicher SR,Vinson SB,Kenerley CM.Infection of the red imported fire ant by Beauveria bassiana through various routes of exposure.Journal of Invertebrate Pathology,1992,59(3):280-285.
[57]Kramm KR,West DF,Rockenbach PG.Termite pathogens:transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes sp.termites.Journal of Invertebrate Pathology,1982,40(1):1-6.
[58]Febvay G,Decharme M,Kermarrec A.Digestion of chitin by the labial glands of Acromyrmex octospinosus reich(Hymenoptera:Formicidae).Canadian Journal of Zoology,1984,62(2):229-234.
[59]Hughes WOH,Eilenberg J,Boomsma JJ.Trade-offs in group living:transmission and disease resistance in leaf-cutting ants.Proceedings of the Royal Society B:Biological Science,2002,269(1502):1811-1819.
[60]Zhukovskaya M,Yanagawa A,Forschler BT.Grooming behavior as a mechanism of insect disease defense.Insects,2013,4(4):609-630.
[61]Konrad M,Grasse AV,Tragust S,Cremer S.Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host.Proceedings of the Royal Society B:Biological Science,2015,282(1799):20141976.
[62]Turnbull C,Wilson PD,Hoggard S,Gillings M,Palmer C,Smith S,Beattie D,Hussey S,Stow A,Beattie A.Primordial enemies:fungal pathogens in thrips societies.PLo S One,2012,7(11):e49737,doi:10.1371/journal.pone.0049737.
[63]Mc Allister MK,Roitberg BD,Weldon KL.Adaptive suicide in pea aphids:decisions are cost sensitive.Animal Behaviour,1990,40(1):167-175.
[64]Poulin R.Altered behaviour in parasitized bumblebees:parasite manipulation or adaptive suicide?Animal Behaviour,1992,44(1):174-176.
[65]Leclerc JB,Detrain C.Ants detect but do not discriminate diseased workers within their nest.The Science of Nature,2016,103(7/8):70.
[66]Rosengaus RB,Jordan C,Lefebvre ML,Traniello JFA.Pathogen alarm behavior in a termite:a new form of communication in social insects.Naturwissenschaften,1999,86(11):544-548
[67]Adamo SA.Parasites:evolution’s neurobiologists.Journal of Experimental Biology,2013,216(Pt 10):3-10.
[68]Feng YJ,Ge Y,Tan SQ,Zhang KQ,Ji R,Shi WP.Effect of Paranosema locustae(Microsporidia)on the behavioural phases of Locusta migratoria(Orthoptera:Acrididae)in the laboratory.Biocontrol Science and Technology,2015,25(1):48-55.
[69]Shi WP,Guo Y,Xu C,Tan SQ,Miao J,Feng YJ,Zhao H,Leger RJS,Fang WG.Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior.Proceedings of the National Academy of Sciences of the United States of America,2014,111(4):1343-1348.
[70]Tan SQ,Zhang KQ,Chen HX,Ge Y,Ji R,Shi WP.The mechanism for microsporidian parasite suppression of the hindgut bacteria of the migratory locust Locusta migratoria manilensis.Scientific Reports,2015,5:17365,doi:10.1038/srep17365.
[71]Wang YD,Yang PC,Cui F,Kang L.Altered Immunity in crowded locust reduced fungal(Metarhizium anisopliae)pathogenesis.PLo S Pathogens,2013,9(1):e1003102,doi:10.1371/journal.ppat.1003102.
[72]Arthurs S,Thomas MB.Behavioural changes in Schistocerca gregaria following infection with a fungal pathogen:implications for susceptibility to predation.Ecological Entomology,2001,26(3):227-234.
[73]Roy HE,Pell JK,Alderson PG.Effects of fungal infection on the alarm response of pea aphids.Journal of Invertebrate Pathology,1999,74(1):69-75.
[74]Fuentes CE,Pell JK,Niemeyer HM.Influence of plant resistance at the third trophic level:interactions between parasitoids and entomopathogenic fungi of cereal aphids.Oecologia,1998,117(3):426-432.
[75]Roy HE,Pell JK,Clark SJ,Alderson PG.Implications of predator foraging on aphid pathogen dynamics.Journal of Invertebrate Pathology,1998,71(3):236-247.
[76]Roy HE,Baverstock J,Chamberlain K,Pell JK.Do aphids infected with entomopathogenic fungi continue to produce and respond to alarm pheromone?Biocontrol Science and Technology,2005,15(8):859-866.
[77]Myles TG.Isolation of Metarhizium anisopliae(Deuteromycotina:Hyphomycetes)from Reticulitermes flavipes(Isoptera:Rhinotermitidae)with convenient methods for its culture and collection of conidia.Sociobiology,2002,40(2):257-264.
[78]Staples JA,Milner RJ.A laboratory evaluation of the repellency of Metarhizium anisopliae conidia to Coptotermes lacteus.Sociobiology,2000,36(1):133-148.
[79]Lord JC.Response of the wasp Cephalonomia tarsalis(Hymenoptera:Bethylidae)to Beauveria bassiana(Hyphomycetes:Moniliales)as free conidia or infection in its host,the sawtoothed grain beetle,Oryzaephilus surinamensis(Coleoptera:Silvanidae).Biological Control,2001,21(3):300-304.
[80]Mesquita ALM,Lacey LA.Interactions among the entomopathogenic fungus,Paecilomyces fumosoroseus(Deuteromycotina:Hyphomycetes),the parasitoid,Aphelinus asychis(Hymenoptera:Aphelinidae),and their aphid host.Biological Control,2001,22(1):51-59.
[81]Fransen JJ,van Lenteren JC.Host selection and survival of the parasitoid Encarsia formosa on greenhouse whitefly,Trialeurodes vaporariorum,in the presence of hosts infected with the fungus Aschersonia aleyrodis.Entomologia Experimentalis et Applicata,1993,69(3):239-249.
[82]Brobyn PJ,Clark SJ,Wilding N.Effect of fungus infection of Metopolophium dirhodum[Hom.:Aphididae]on the oviposition behaviour of the aphid parasitoid Aphidius rhopalosiphi[Hym.:Aphidiidae].Entomophaga,1988,33(3):333-338.
[83]Chow A,Dunlap CA,Jackson MA,Flores D,Patt JM,Sétamou M.Oviposition behavior and survival of Tamarixia radiata(Hymenoptera:Eulophidae),an ectoparasitoid of the Asian citrus psyllid,Diaphorina citri(Hemiptera:Liviidae),on hosts exposed to an entomopathogenic fungus,Isaria fumosorosea(Hypocreales:Cordycipitaceae),under laboratory conditions.Journal of Economic Entomology,2016,109(5):1995-2005.
[84]Ohbayashi T,Iwabuchi K.Abnormal behavior of the common armyworm Pseudaletia separate(WALKER)(Lepidoptera:Noctuidae)larvae infected with an entomogenous fungus,Entomophaga aulicae and a nuclear polyhedrosis virus.Applied Entomology and Zoology,1991,26(4):579-585.
[85]Milner RJ,Holdom DG,Glare TR.Diurnal patterns of mortality in aphids infected by entomophthoran fungi.Entomologia Experimentalis et Applicata,1984,36(1):37-42.
[86]Krasnoff SB,Watson DW,Gibson DM,Kwan EC.Behavioral effects of the entomopathogenic fungus,Entomophthora muscae on its host Musca domestica:postural changes in dying hosts and gated pattern of mortality.Journal of Insect Physiology,1995,41(10):895-903.
[87]Thomsen L,Eilenberg J.Entomophthora muscae resting spore formation in vivo in the host Delia radicum.Journal of Invertebrate Pathology,2000,76(2):127-130.
[88]Steinkraus DC,Mueller AJ,Humber RA.Furia virescens(Thaxter)Humber(Zygomycetes:Entomophthoraceae)infections in the armyworm,Pseudaletia unipuncta(Haworth)(Lepidoptera:Noctuidae)in Arkansas with notes on other natural enemies.Journal of Entomological Science,1993,28(4):376-386.
[89]Evans HC.Mycopathogens of insects of epigeal and aerial habitats//Wilding N,Collins NM,Hammond PM,Webber JF.Insect-Fungus Interactions.San Diego:Academic Press,1989,205-238.
[90]Steinkraus DC,Kramer JP.Development of resting spores of Erynia aquatica(Zygomycetes:Entomophthoraceae)in Aedes aegypti(Diptera:Culicidae).Environmental Entomology,1989,18(6):1147-1152.
[91]Duke L,Steinkraus DC,English JE,Smith KG.Infectivity of resting spores of Massospora cicadina(Entomophthorales:Entomophthoraceae),an entomopathogenic fungus of periodical cicadas(Magicicada spp.)(Homoptera:Cicadidae).Journal of Invertebrate Pathology,2002,80(1):1-6.
[92]Hutchison JA.Studies on a new Entomophthora attacking calyptrate flies.Mycologia,1962,54(3):258-271.
[93]Mac Leod DM,Müller-K?gler E.Entomogenous fungi:Entomophthora species with pear-shaped to almost spherical conidia(Entomophthorales:Entomophthoraceae).Mycologia,1993,65(4):823-893.
[94]Katsuma S.Phosphatase activity of Bombyx mori nucleopolyhedrovirus PTP is dispensable for enhanced locomotory activity in B.mori larvae.Journal of Invertebrate Pathology,2015,132:228-232.
[95]Kamita SG,Nagasaka K,Chua JW,Shimada T,Mita K,Kobayashi M,Maeda S,Hammock BD.A baculovirusencoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host.Proceedings of the National Academy of Sciences of the United States of America,2005,102(7):2584-2589.
[96]Janzen DH.When is it coevolution?Evolution,1980,34(3):611-612.
[97]Butt TM,Jackson C,Magan N.Fungi as Biocontrol Agents:Progress,Problems and Potential.Wallingford,UK:CABIPublishing,2001.