Prospective role of insecticides of fungal origin: Review

Advances in the application of microbial‐based technology in insect pest management assist us to counter problems created by the application of chemical pesticides. These are mainly strong environmental effects, resistance development and high costs. Among the microbial pesticides, fungal pesticides are now preferred as they are target specific, ecofriendly, lacking in toxic residue and are economical. Being numerous with great diversification, entomopathogenic fungi therefore have great potential to control a large variety of insect pests. Fungi are applied directly in form of spores, mycelia or blastospores or by their metabolites (mycotoxins). Both approaches have very promising roles in insect pest management. However, there are three main obstacles in the development of fungal pesticides: (i) scant production of mycotoxins; (ii) carcinogenic mycotoxicosis in non‐target organisms; and (iii) slow effectiveness. Therefore, to eliminate these problems, attention has recently been paid to a synergistic approach to combating insecticide resistance. Next to synergism, genetic manipulation is also used to enhance the pathogenicity and virulence of fungal insecticides. However, the key risk associated with the release of recombinant microorganisms into the environment is that the novel organism may have unforeseen undesirable characteristics. Therefore, the introduction of synergists in pest control could have great benefit both economically and ecologically. An ideal synergistic approach is the mixing of more than two accelerating components together, i.e. tripartite or multiple synergism to enhance effectiveness. Thus, synergistic approaches have a bright future and require further research and financial support.

[1]  J. Amler The Fifth Kingdom , 2011 .

[2]  Chengshu Wang,et al.  Insecticidal evaluation of Beauveria bassiana engineered to express a scorpion neurotoxin and a cuticle degrading protease , 2008, Applied Microbiology and Biotechnology.

[3]  H. Atamian,et al.  Isolation of Beauveria species from Lebanon and evaluation of its efficacy against the cedar web-spinning sawfly, Cephalcia tannourinensis , 2008, BioControl.

[4]  Bin Chen,et al.  Occurrence of entomopathogenic fungi in migratory alate aphids in Yunnan Province of China , 2008, BioControl.

[5]  Stephen P. Wraight,et al.  Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types ☆ , 2007 .

[6]  H. Sharma,et al.  Growth and insect assays of Beauveria bassiana with neem to test their compatibility and synergism , 2007 .

[7]  K. Hell,et al.  Farm‐scale trials to compare the entomopathogenic fungus Beauveria bassiana with pirimiphos methyl + deltamethrin and essential oil of lemon grass for protection of stored cowpea against Callosobruchus maculatus (Coleoptera: Bruchidae) , 2007 .

[8]  A. Read,et al.  Can fungal biopesticides control malaria? , 2007, Nature Reviews Microbiology.

[9]  R. Samuels,et al.  Selection of entomopathogenic fungi for use in combination with sub-lethal doses of imidacloprid: perspectives for the control of the leaf-cutting ant Atta sexdensrubropilosa Forel (Hymenoptera: Formicidae) , 2007, Mycopathologia.

[10]  R. Pegram,et al.  Assessment of fungal isolates for development of a myco-acaricide for cattle tick control. , 2005, Vector borne and zoonotic diseases.

[11]  K. Walters,et al.  Compatibility of the entomopathogenic fungus Lecanicillium muscarium and insecticides for eradication of sweetpotato whitefly, Bemisia tabaci , 2005, Mycopathologia.

[12]  T. Loughin,et al.  Efficacy of Beauveria bassiana for Red Flour Beetle When Applied with Plant Essential Oils or in Mineral Oil and Organosilicone Carriers , 2005, Journal of economic entomology.

[13]  J. Lord From Metchnikoff to Monsanto and beyond: the path of microbial control. , 2005, Journal of invertebrate pathology.

[14]  C. Ulhoa,et al.  Is there a relationship between N‐acetyl‐β‐d‐glucosaminidase activity of Metarhizium anisopliae (Metschn.) Sorokin (Hyphomycetes) isolates from peridomestic areas in Central Brazil and larvicidal effect on Aedes aegypti (L.) (Diptera, Culicidae)? , 2005 .

[15]  W. Takken,et al.  Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). , 2005, Chemical Sensors.

[16]  L. Tirry,et al.  Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus , 2004 .

[17]  R. S. St. Leger,et al.  EST analysis of genes expressed by the zygomycete pathogen Conidiobolus coronatus during growth on insect cuticle. , 2003, Microbiology.

[18]  R. James Combining azadirachtin and Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) to control Bemisia argentifolii (Homoptera: Aleyrodidae). , 2003, Journal of economic entomology.

[19]  R. B. Lopes,et al.  Potential of some Metarhizium anisopliae isolates for control of Culex quinquefasciatus (Dipt., Culicidae) , 2002 .

[20]  M. Brownbridge,et al.  Pathogenicity of Beauveria bassiana, Metarhizium anisopliae (Deuteromycotina: Hyphomycetes), and other Entomopathogenic Fungi Against Lygus lineolaris (Hemiptera: Miridae) , 2002, Journal of economic entomology.

[21]  A. B. Filho,et al.  Effect of Thiamethoxam on Entomopathogenic Microorganisms , 2001 .

[22]  R. James,et al.  Antagonism Between Beauveria bassiana and Imidacloprid When Combined for Bemisia argentifolii (Homoptera: Aleyrodidae) Control , 2001, Journal of economic entomology.

[23]  E. Groden,et al.  Evaluation of Synergistic Interactions Between the Colorado Potato Beetle (Coleoptera: Chrysomelidae) Pathogen Beauveria bassiana and the Insecticides, Imidacloprid, and Cyromazine , 2001, Journal of economic entomology.

[24]  S. Ignacimuthu,et al.  Efficacy of Beauveria bassiana for control of the rice weevil Sitophilus oryzae (L.) (Coleoptera:Curculionidae) , 2001 .

[25]  C. Lucarotti,et al.  Coelomomyces stegomyiae infection in adult female Aedes aegypti following the first, second, and third host blood meals. , 2000, Journal of invertebrate pathology.

[26]  S. Kamble,et al.  In Vivo Study on Combined Toxicity of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) Strain ESC-1 with Sublethal Doses of Chlorpyrifos, Propetamphos, and Cyfluthrin Against German Cockroach (Dictyoptera: Blattellidae) , 2000, Journal of economic entomology.

[27]  A. Tepsuwan,et al.  Effects of neem flowers, Thai and Chinese bitter gourd fruits and sweet basil leaves on hepatic monooxygenases and glutathione S-transferase activities, and in vitro metabolic activation of chemical carcinogens in rats. , 1998, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[28]  C. Mccoy,et al.  Pathogenicity enhancement of Metarhizium anisopliae and Beauveria bassiana to first instars of Diaprepes abbreviatus (Coleoptera: Curculionidae) with sublethal doses of imidacloprid , 1997 .

[29]  C. Vidal,et al.  Pathogenicity of Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) Against Bemisia argentifolii (Homoptera: Aleyrodidae) with a Description of a Bioassay Method , 1997 .

[30]  W. Kaakeh,et al.  Toxicity of Imidacloprid in the German Cockroach (Dictyoptera: Blattellidae), and the Synergism Between Imidacloprid and Metarhizium anisopliae (Imperfect Fungi: Hyphomycetes) , 1997 .

[31]  V. Sharma,et al.  Field studies on the mosquito repellent action of neem oil. , 1995, The Southeast Asian journal of tropical medicine and public health.

[32]  D. Holdom,et al.  Effects of pesticides on growth and sporulation of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) , 1994 .

[33]  J. Spatafora,et al.  MOLECULAR SYSTEMATICS OF UNITUNICATE PERITHECIAL ASCOMYCETES: THE CLAVICIPITALES-HYPOCREALES CONNECTION , 1993 .

[34]  A. Charnley,et al.  Microbial pathogens and insect pest control , 1991 .

[35]  James B. Johnson,et al.  Relative Virulence of Six Isolates of Beauveria bassiana on Diuraphis noxia (Homoptera: Aphididae) , 1990 .

[36]  J. Fuxa Fate of Released Entomopathogens with Reference to Risk Assessment of Genetically Engineered Microorganisms , 1989 .

[37]  A. Charnley Mycoinsecticides: present use and future prospects , 1989 .

[38]  L. Bernier,et al.  Transformation of the entomopathogenic fungus Metarhizium anisopliae to benomyl resistance , 1989 .

[39]  A. W. Sweeney,et al.  Crypticola clavulifera gen. et sp. nov. and Lagenidium giganteum: oomycetes pathogenic for dipterans infesting leaf axils in an Australian rain forest. , 1989, Journal of invertebrate pathology.

[40]  M. Hluchý,et al.  Comparative study on the susceptibility of adult Sitophilus granarius (L.) (Coleoptera: Curculionidae) and larval Galleria mellonella (L.) (Lepidoptera: Pyralidae) to the entomogenous fungus Beauveria bassiana (Bals.) Vuill. , 1989 .

[41]  G. L. Patourel,et al.  Infectivity of oil and water formulations of Beauveria bassiana (Deuteromycotina: Hyphomycetes) to the cocoa weevil pest Pantorhytes plutus (Coleoptera: Curculionidae) , 1988 .

[42]  T. Mcinnis,et al.  Life cycle and mode of infection of Leptolegnia chapmanii (Oomycetes) parasitizing Aedes aegypti. , 1987, Journal of invertebrate pathology.

[43]  M. Simmonds,et al.  Mycopesticidal effects of characterized extracts of Penicillium isolates and purified secondary metabolites (including mycotoxins) on Drosophila melanogaster and Spodoptora littoralis , 1987 .

[44]  F. Nelson,et al.  Compatability of Metarhizium anisopliae var. anisopliae with chemical pesticides , 1987, Mycopathologia.

[45]  D. Roberts,et al.  Infection of Rice Brown Planthopper, Nilaparvata lugens (Homoptera: Delphacidae), by Field Application of Entomopathogenic Hyphomycetes (Deuteromycotina) , 1986 .

[46]  B. Croft,et al.  The effects of microbial pesticides on non-target, beneficial arthropods , 1986 .

[47]  M. Prevost,et al.  Integumental penetration of the pea aphid, Acyrthosiphon pisum, by Conidiobolus obscurus (Entomophthoracease) , 1986 .

[48]  B. Mullens,et al.  Dynamics of Entomophthora muscae (Entomophthorales: Entomophthoraceae) Conidial Discharge from Musca domestica (Diptera: Muscidae) Cadavers , 1985 .

[49]  M. Marchal,et al.  Comparative Susceptibility of Otiorhynchus sulcatus and Sitona lineatus (Coleoptera: Curculionidae) Early Stages to Five Entomopathogenic Hyphomycetes , 1985 .

[50]  R. Samson,et al.  Entomopathogenic species of the hyphomycete genus Tolypocladium , 1984 .

[51]  T. Singh,et al.  Inducement of metabolic dysfunction by carbamate and organophosphorus compounds in a fish, Puntius conchonius , 1983 .

[52]  T. Andreadis,et al.  Erynia (= Entomophthora) aquatica in a salt-marsh mosquito, Aedes cantator , 1983 .

[53]  D. Roberts,et al.  Virulence of natural and insect-passaged strains of Metarhizium anisopliae to mosquito larvae , 1982 .

[54]  J. V. Bell,et al.  Heliothis zea larval mortality time from topical and per os dosages of Nomuraea rileyi conidia , 1980 .

[55]  P. Ferron Influence of relative humidity on the development of fungal infection caused byBeauveria bassiana [Fungi Imperfecti, Moniliales] in imagines ofAcanthoscelides obtectus [Col.: Bruchidae] , 1977, Entomophaga.

[56]  J. Fargues,et al.  Histological and ultrastructural studies of Beauveria bassiana infection in Leptinotarsa decemlineta larvae during ecdysis , 1977 .

[57]  R. Koyama,et al.  Hibernation of resting spores of Entomophthora aulicae in egg masses of the gypsy moth Porthetria dispar , 1976 .

[58]  G. Latch Studies on the susceptibility ofOryctes rhinoceros to some entomogenous fungi , 1976, Entomophaga.

[59]  P. Ferron,et al.  Susceptibility of Oryctes rhinoceros adults to Metarrhizium anisopliae , 1975 .

[60]  M. Kučera,et al.  Toxins of the entomophagous fungus Beauveria bassiana. , 1968, Journal of invertebrate pathology.

[61]  The Control of Grasshoppers , 1931, Science.

[62]  N. Jonsson,et al.  Laboratory studies on Australian isolates of Metarhizium anisopliae as a biopesticide for the cattle tick Boophilus microplus. , 2008, Journal of invertebrate pathology.

[63]  J. Grove,et al.  The insecticidal activity of some fungal dihydroisocoumarins , 2004, Mycopathologia.

[64]  Abha Sharma,et al.  Studies on physiology, zoospore morphology and entomopathogenic potential of the aquatic oomycete: Lagenidium giganteum , 2004, Mycopathologia.

[65]  G. Kaaya,et al.  Entomogenous Fungi as Promising Biopesticides for Tick Control , 1999 .

[66]  A. Charnley Fungal pathogens of insects: Cuticle degrading enzymes and toxins , 2003 .

[67]  R. S. St. Leger,et al.  Expressed sequence tag (EST) analysis of two subspecies of Metarhizium anisopliae reveals a plethora of secreted proteins with potential activity in insect hosts. , 2003, Microbiology.

[68]  N. Magan,et al.  Production, stabilization and formulation of fungal biocontrol agents. , 2001 .

[69]  L. Jeffs Physical and biochemical properties of entomopathogenic fungal spores , 1999 .

[70]  R. Bateman,et al.  Performance of Metarhizium anisopliae formulations with oil adjuvants on Tenebrio molitor. , 1998 .

[71]  N. Becker THE USE OF BACILLUS THURINGIENSIS SUBSP. ISRAELENSIS (BTI) AGAINST MOSQUITOES, WITH SPECIAL EMPHASIS ON THE ECOLOGICAL IMPACT , 1998 .

[72]  Roy Bateman,et al.  METHODS OF APPLICATION OF MICROBIAL PESTICIDE FORMULATIONS FOR THE CONTROL OF GRASSHOPPERS AND LOCUSTS , 1997 .

[73]  M. Goettel,et al.  Chapter V-3 – Fungi: Hyphomycetes , 1997 .

[74]  M. Thomas,et al.  CONTROL OF GRASSHOPPERS, PARTICULARLY HIEROGLYPHUS DAGANENSIS, IN NORTHERN BENIN USING METARHIZIUM FLAVOVIRIDE , 1997 .

[75]  George G. Khachatourians,et al.  Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status. , 1994 .

[76]  J. Zizka,et al.  Effect of beauvericin, a toxic metabolite of Beauveria bassiana, on the ultrastructure of Culex pipiens autogenicus larvae , 1993 .

[77]  H. Evans Mycopathogens of insects of epigeal and aerial habitats. , 1989 .

[78]  J. Latgé,et al.  Atlas of Entomopathogenic Fungi , 1988, Springer Berlin Heidelberg.

[79]  D. L. Haynes,et al.  Entomophthora muscae (Entomophthorales: Entomophthoracae) mycosis in the onion fly, Delia antiqua (Diptera: Anthomyiidae) , 1985 .

[80]  Tomomasa Misato,et al.  RECENT STATUS AND FUTURE ASPECTS OF AGRICULTURAL ANTIBIOTICS , 1983 .

[81]  W. Zattau,et al.  Experimental infection of mosquito larvae by a species of the aquatic fungus , 1982 .

[82]  R. Hall A bioassay of the pathogenicity of Verticillium lecanii conidiospores on the aphid, Macrosiphoniella sanborni , 1976 .

[83]  H. Chapman Biological control of mosquito larvae. , 1974, Annual review of entomology.

[84]  D. Roberts Fungal infections of mosquitoes , 1974 .