References
Artjariyasripong S, Mitchell JI, Hywel-Jones NL, Jones EBG (2001) Relationship of the genus Cordyceps and related genera based on parsimony and spectral analysis of partial 18S and 28S ribosomal gene sequences. Mycoscience 42:503–517
Bałazy S (1993) Entomophthorales. In: Flora of Poland, Fungi (Mycota), vol XXIV. Instytut Botaniki, Kraków, Poland
Bateman RP, Godonou I, Kpindu D, Lomer CJ, Paraïso A (1992) Development of a novel bioassay technique for assessing mycoinsecticide ULV formulations. In: Lomer CJ, Prior C (eds) Biological control of locusts and grasshoppers. CAB International, Wallingford, pp 255–262
Bateman RP, Neethling D, Oosthuizen F (1998) Green Muscle handbook for central and southern Africa. LUBILOSA/Biological Control Products SA
Bradley CA, Black WE, Kearns R, Wood P (1992) Role of production technology in mycoinsecticide development. In: Leatham GF (ed) Frontiers in industrial mycology. Chapman and Hall, New York, pp 160–173
Burges HD (1998) Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. Kluwer Academic, Dordrecht, The Netherlands
Burges HD (2000) Techniques for testing microbials for control of arthropod pests in greenhouses. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology: application and evaluation of pathogens for control of insects and other invertebrate pests. Kluwer Academic, Dordrecht, The Netherlands, pp 505–526
Butt TM, Jackson C, Magan N (2001) Fungi as biocontrol agents: progress, problems and potential. CABI International, Wallingford
Copping LG (1998) The BioPesticide manual, 1st edn. British Crop Protection Council, Farnham, Surrey
Dorworth CE (1997) Two models for the development of fungal biological control agents as instruments of ecological management. In: Chapela IH, Palm ME (eds) Mycology and sustainable development: expanding concepts, vanishing borders. Parkway, Boone, N.C., pp 211–224
Driver F, Milner RJ, Trueman JWH (2000) A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycol Res 104:134–150
Eilenberg J (2002) Biology of fungi from the order Entomophthorales, with emphasis on the genera Entomophthora, Strongwellsea and Eryniopsis. The Royal Veterinary and Agricultural University, Copenhagen, Denmark
Elkinton JS, Hajek AE, Boettner GH, Simons EE (1991) Distribution and apparent spread of Entomophaga maimaiga (Zygomycetes: Entomophthorales) in gypsy moth (Lepidoptera: Lymantriidae) populations in North America. Environ Entomol 20:1601–1605
Evans HC (1989) Mycopathogens of insects of epigeal and aerial habitats. In: Wilding N, Collins NM, Hammond PM, Weber JF (eds) Insect–fungus interactions. Academic Press, London, pp 205–238
Evans HC (2003) Use of Clavicipitalean fungi for the biological control of arthropod pests. In: White JF, et al (eds) Clavicipitalean fungi. Marcel Dekker, New York
Evans HC, Shah PA (2002) Taxonomic status of the genera Sorosporella and Syngliocladium associated with grasshoppers and locusts (Orthoptera: Acridoidea) in Africa. Mycol Res 106:737–744
Feng MG, Johnson JB, Halbert SE (1991) Natural control of cereal aphids (Homoptera: Aphididae) by entomopathogenic fungi (Zygomycetes: Entomophthorales) and parasitoids (Hymenoptera: Braconidae and Encyrtidae) on irrigated spring wheat in southwestern Idaho. Environ Entomol 20:1699–1710
Feng MG, Nowierski RM, Klein RE, Scharen AL, Sands DC (1992) Spherical hyphal bodies of Pandora neoaphidis (Remaudière and Hennebert) Humber (Zygomycetes: Entomophthorales) on Acyrthosiphon pisum Harris (Homoptera: Aphididae): a potential overwintering form. Pan-Pacific Entomol 68:100–104
Furlong MJ, Pell JK (1997) The influence of environmental factors on the persistence of Zoophthora radicans conidia. J Invert Pathol 69:223–233
Furlong MJ, Pell JK (2001) Horizontal transmission of entomopathogenic fungi by the diamondback moth. Biol Control 22:288–299
Furlong MJ, Pell JK, Ong PC, Syed AR (1995) Field and laboratory evaluation of a sex pheromone trap for the autodissemination of the fungal entomopathogen Zoophthora radicans (Entomophthorales) by the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Bull Entomol Res 85:331–337
Fuxa JR (1998) Environmental manipulation for microbial control of insects. In: Barbosa P (ed) Conservation biological control. Academic Press, San Diego, pp 255–289
Gelernter WD (1997) Resistance to microbial insecticides: the scale of the problem and how to manage it. In: Evans HF (ed) Microbial insecticides: novelty or necessity? British Crop Protection Council Symposium 68:201–214
Gelernter WD, Lomer CJ (2000) Success in biological control of above-ground insects by pathogens. In: Gurr G, Wratten S (eds) Biological control: measures of success. Kluwer Academic, Dordrecht, The Netherlands, pp 297–322
Georgis R (1997) Commercial prospects of microbial insecticides in agriculture. In: Evans HF (ed) Microbial insecticides: novelty or necessity? British Crop Protection Council Symposium 68:243–252
Glare TR, Milner RJ (1991) Ecology of entomopathogenic fungi. In: Arora DK, Ajello L, Mukerji KG (eds) Handbook of applied mycology, vol 2: humans, animals, and insects. Marcel Dekker, New York, pp 547-612
Goettel MS, Hajek AE (2000) Evaluation of non-target effects of pathogens used for management of arthropods. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, pp 81–97
Gray SN, Markham P (1997) A model to explain the growth kinetics of the aphid-pathogenic fungus Erynia neoaphidis in liquid culture. Mycol Res 101:1475–1483
Hajek AE, Humber RA, Elkinton JS, May B, Walsh SRA, Silver JC (1990) Allozyme and RFLP analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American gypsy moth populations. Proc Nat Acad Sci USA 87:6979-6982
Hajek AE, Humber RA, Elkinton JS (1995) Mysterious origin of Entomophaga maimaiga in North America. Am Entomol 41:31–42
Hajek AE, Elkinton JS, Witocosky JJ (1996) Introduction and spread of the fungal pathogen Entomophaga maimaiga along the leading edge of gypsy moth spread. Environ Entomol 25:1235–1247
Hajek AE, Bauer L, Wheeler MM, McManus ML (1998a) Distribution of resting spores of the Lymantria dispar pathogen Entomophaga maimaiga in soil and on bark. BioControl 43:189–200
Hajek AE, Tatman KM, Wanner PH, Wheeler MM (1998b) Location and persistence of gypsy moth, Lymantria dispar, cadavers containing Entomophaga maimaiga azygospores. Mycologia 90:754–760
Hajek AE, McNeil JR, Filotas MJ (2002) Using Entomophthorales for control: maturation, dormancy and survival of laboratory-produced Entomophaga maimaiga. Proceedings of the XXXIV Annual Meeting of the Society for Invertebrate Pathology, Noordwijkerhout, The Netherlands
Hall RA (1981) The fungus Verticillium lecanii as a microbial insecticide against aphids and scales. In: Burges HD (ed) Microbial control of pests and plant diseases 1970–1980. Academic Press, London, pp 483–498
Hall RA, Papierok B (1982) Fungi as biological agents of arthropods of agricultural and medical importance. Parasitology 84:205–240
Hartfield CM, Campbell CAM, Hardie J, Pickett JA, Wadhams LJ (2001) Pheromone traps for the dissemination of an entomopathogen by the damson-hop aphid, Phorodon humuli. Biocontrol Sci Technol 11:401–410
Hemmati F, Pell JK, McCartney HA, Deadman ML (2001) Airborne concentrations of conidia of Erynia neoaphidis above cereal fields. Mycol Res 105:485–489
Hockland SH, Dawson GW, Griffiths DC, Marples B, Pickett JA, Woodcock CM (1986) The use of aphid alarm pheromone ((E)-ß-farnesene) to increase effectiveness of the entomophilic fungus Verticillium lecanii in controlling aphids on chrysanthemums. Proceedings of the Fourth International Colloquium of Invertebrate Pathology, Veldhoven, The Netherlands
Humber RA (1984) Foundations for an evolutionary classification of the Entomophthorales (Zygomycetes). In: Wheeler Q, Blackwell M (eds) Fungus–insect relationships. Columbia University Press, New York, pp 166–183
Jackson TA, Alves SB, Pereira RM (2000) Success in biological control of soil-dwelling insects by pathogens and nematodes. In: Gurr G, Wratten S (eds) Biological control: measures of success. Kluwer Academic, Dordrecht, The Netherlands, pp 271–296
Jaronski ST, Lord J, Rosinska J, Bradley C, Hoelmer K, Simmons G, Osterlind R, Brown C, Staten R (1998) Effect of a Beauveria bassiana-based mycoinsecticide on beneficial insects under field conditions. Proceedings of the 1998 Brighton Conference – Pests and Diseases 2:651–657
Jenkins NE, Heviefo G, Langewald J, Cherry AJ, Lomer CJ (1998) Development of mass production technology for aerial conidia for use as mycopesticides. Biocontrol News Inform 19:21N–31N
Jung K, Gonschorrek J, Ruther J, Zimmerman G (2002) Field testing of new biocontrol strategies to decrease population density in Melolontha hippocastani, an important scarab species in Germany. Proceedings of the XXXV Annual meeting of the Society for Invertebrate Pathology, Iguassu Falls, Brazil
Keller S (1992) The Beauveria-Melolontha project: experiences with regard to locust and grasshopper control. In: Lomer CJ, Prior C (eds) Biological control of locusts and grasshoppers. CAB International, Wallingford, pp. 279–286
Keller S (1998) The role of Entomophthorales in a sustainable agriculture. IOBC Bulletin 21:13–16
Keller S, Suter H (1980) Epizootiologische Untersuchungen über das Entomophthora-Auftreten bei feldbaulich wichtigen Blattlausarten. Acta Oecol Oecol Appl 1:63–81
Keller S, Zimmerman G (1989) Mycopathogens of soil insects. In: Wilding N, Collins NM, Hammond PM, Weber JF (eds) Insect–fungus interactions. Academic Press, London, pp 239–270
Keller S, Schweizer C, Keller E, Brenner H (1997) Control of white grubs (Melolontha melolontha L.) by treating adults with the fungus Beauveria brongniartii. Biocontrol Sci Technol 7:105–116
Keller S, Schweizer C, Shah P (1999) Differential susceptibility of two Melolontha populations to infections by the fungus Beauveria brongniartii. Biocontrol Sci Technol 9:441–446
Kenneth R, Olmert I (1975) Entomopathogenic fungi and their insect hosts in Israel: additions. Israel J Entomol 10:105–112
Langewald J, Ouambama Z, Mamadou A, Peveling R, Stolz I, Bateman R, Attignon S, Blanford S, Arthurs A, Lomer C (1999) Comparison of an organophosphate insecticide with a mycoinsecticide for the control of Oedaleus senegalensis (Orthoptera: Acrididae) and other Sahelian grasshoppers at an operational scale. Biocontrol Sci Technol 9:199–214
Lomer CJ, Bateman RP, Godonou I, Kpindou D, Shah PA, Paraïso A, Prior C (1993) Field infection of Zonocerus variegatus following application of an oil-based formulation of Metarhizium flavoviride conidia. Biocontrol Sci Technol 3:337–346
Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas MB (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46:667–702
May RM (2000) The dimensions of Life on Earth. In: Raven PH, Williams T (eds) Nature and human society: the quest for a sustainable world. National Academy Press, Washington D.C., pp 30–45
McCabe D, Soper RS (1985) Preparation of an entomopathogenic fungal insect control agent. US Patent No 4530834
Mendonça AF (1992) Mass production, application and formulation of Metarhizium anisopliae for control of sugarcane froghopper Mahanarva posticata in Brazil. In: Lomer CJ, Prior C (eds) Biological control of locusts and grasshoppers. CAB International, Wallingford, pp 239–254
Milner RJ 1(1997) Prospects for biopesticides for aphid control. Entomophaga 42:227–239
Milner RJ, Teakle RE, Lutton GG, Dare FM (1980) Pathogens of the blue green aphid Acyrthosiphon kondoi Shinji and other aphids in Australia. Aust J Bot 28:601–619
Milner RJ, Soper RS, Lutton GG (1982) Field release of an Israeli strain of the fungus Zoophthora radicans (Brefeld) Batko for biological control of Therioaphis trifolii (Monell) f. maculata. J Aust Entomol Soc 21:113-118
Moore D, DouroKpindou OK, Jenkins NE, Lomer CJ (1996) Effects of moisture content and temperature on storage of Metarhizium flavoviride conidia. Biocontrol Sci Technol 6:51–61
Nikoh N, Fukatsu T (2000) Interkingdom host jumping underground: phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps. Mol Biol Evol 17:629–638
Nielsen C, Hajek AE, Humber RA, Eilenberg J (1998) Soil: a natural source of entomophthoralean fungi infecting aphids. IOBC Bull 21:45–48
Pell JK, Macaulay EDM, Wilding N (1993a) A pheromone trap for dispersal of the pathogen, Zoophthora radicans Brefeld (Zygomycetes: Entomophthorales) amongst populations of the diamondback moth, Plutella xylostella L. (Lepidoptera: Yponomeutidae). Biocontrol Sci Technol 3:315–320
Pell JK, Wilding N, Player AL, Clark SJ (1993b) Selection of an isolate of Zoophthora radicans (Zygomycetes: Entomophthorales) for biocontrol of the diamondback moth Plutella xylostella (Lepidoptera: Yponomeutidae). J Invert Pathol 61:75–80
Pell JK, Barker ADP, Clark SJ, Wilding N, Alderson PG (1998) Use of a novel sporulation monitor to quantify the effects of formulation and storage on conidia production by dried mycelia of the entomopathogenic fungus Zoophthora radicans. Biocontrol Sci Technol 8:13–21
Pell JK, Eilenberg J, Hajek AE, Steinkraus DC (2001) Biology, ecology and pest management potential of Entomophthorales. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CAB International, Wallingford, pp 71–153
Poprawski TJ, Carruthers RI, Speese J, Vacek DC, Wendel LE (1997) Early-season applications of the fungus Beauveria bassiana and introduction of the hemipteran predator Perillus bioculatus for control of Colorado potato beetle. Biol Control 10:48–57
Poprawski TJ, Parker PE, Tsai JH (1999) Laboratory and field evaluation of hyphomycete insect pathogenic fungi for control of brown citrus aphid (Homoptera: Aphididae). Environ Entomol 28:315–321
Powell W, Dean GJ, Wilding N (1986) The influence of weeds on aphid-specific natural enemies in winter wheat. Crop Prot 5:182–189
Prior C, Greathead DG (1989) Biological control of locusts: the potential for the exploitation of pathogens. FAO Plant Prot Bull 37:37–48
Roberts DR (1981) Toxins of entomopathogenic fungi. In: Burges HD (ed) Microbial control of pests and diseases, 1970–1980. Academic Press, London, pp 441–464
Roberts DR, Hajek AE (1992) Entomopathogenic fungi as bioinsecticides. In: Leatham GF (ed) Frontiers in industrial mycology. Chapman and Hall, New York, pp 144–159
Roditakis E, Couzin ID, Balrow K, Franks NR, Charnley AK (2000) Improving the secondary pick up of insect pathogen conidia by manipulating host behaviour. Ann Appl Biol 137:329–335
Roy HE, Pell JK, Alderson PG (2001) Targeted dispersal of the aphid pathogenic fungus Erynia neoaphidis by the aphid predator Coccinella septempunctata. Biocontrol Sci Technol 11:99–110
Samson RA, Evans HC, Latgé JP (1988) Atlas of entomopathogenic fungi. Springer, Berlin Heidelberg New York
Samways MJ (1981) Biological control of pests and weeds. (Studies in biology no 132) Edward Arnold, London
Shah PA, Goettel MS (1999) Directory of microbial control products and services, 2nd edn. Division on Microbial Control, Society for Invertebrate Pathology
Shah PA, Kooyman C, Paraïso A (1997) Surveys for fungal pathogens of locusts and grasshoppers in Africa and the Near East. Mem Entomol Soc Can 171:27–35
Shah PA, Aebi M, Tuor U (1998) Method to immobilise the aphid-pathogenic fungus Erynia neoaphidis in an alginate matrix for biocontrol. Appl Environ Microbiol 64:4260–4263
Shah PA, Aebi M, Tuor U (2000) Infection of Macrosiphum euphorbiae with mycelial preparations of Erynia neoaphidis in a greenhouse trial. Mycol Res 104:645–652
Shah PA, Tymon A, Pell JK (2001) Conservation biocontrol with mycopathogens: Erynia neoaphidis and agricultural field margins. Proceedings of the XXXIV Annual Meeting of the Society for Invertebrate Pathology, Noordwijkerhout, The Netherlands
Shah PA, Aebi M, Tuor U (2002) Effects of constant and fluctuating temperatures on sporulation and infection by the aphid-pathogenic fungus Pandora neoaphidis. Entomol Exp Appl 103:257–266
Shaw KE, Davidson G, Clark SJ, Ball BV, Pell JK, Chandler D, Sunderland KD (2002) Laboratory bioassays to assess the pathogenicity of mitosporic fungi to Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of the honeybee, Apis mellifera. Biol Control 24:266–276
Shelton AM, Vandenberg JD, Ramos M, Wilsey WT (1998) Efficacy and persistence of Beauveria bassiana and other fungi for control of diamondback moth (Lepidoptera: Plutellidae) on cabbage seedlings. J Entomol Sci 33:142–152
Sierotzki H, Camastral F, Shah PA, Aebi M, Tuor U (2000) Biological characteristics of selected Erynia neoaphidis isolates. Mycol Res 104:213–219
Spatafora JW, Blackwell M (1993) Molecular systematics of unitunicate perithecia ascomycetes: the Clavicipitales-Hypocreales connection. Mycologia 85:912–922
Spatafora JW, Sung G-H (2002) Evolution of inter-kingdom host-jumping of Cordyceps and the Clavicipitaceae. Proceedings of the 7th International Mycological Congress, Oslo
Steinhaus EA (1949) Principles of insect pathology. McGraw-Hill, New York
Steinhaus EA (1964) Microbial diseases of insects. In: DeBach P (ed) Biological control of insect pests and weeds. Chapman and Hall, London, pp 515–547
Steinkraus DC, Boys GO (1997) Update on prediction of epizootics with extension-based sampling service. Proceedings of the Beltwide Cotton Conferences. National Cotton Council of America, Memphis, Tenn.
Steinkraus DC, Kring TJ, Tugwell NP (1991) Neozygites fresnii in Aphis gossypii on cotton. Southwestern Entomol 16:118–122
Steinkraus DC, Hollingsworth RG, Slaymaker PH (1995) Prevalence of Neozygites fresenii (Entomopthorales: Neozygitaceae) on cotton aphids (Homoptera: Aphididae) in Arkansas cotton. Environ Entomol 24:465–474
Steinkraus DC, Boys GO, Hollingsworth RG, Bacheler JS, Durant JA, Freeman BL, Gaylor MJ, Harris FA, Knutson A, Lentz GL, Leonard BR, Luttrell R, Parker D, Powell JD, Ruberson JR, Sorenson C (1996) Multistate sampling for Neozygites fresenii in cotton. Proceedings of the Beltwide Cotton Research Conferences, Nashville, Tenn.
Steinkraus DC, Boys GO, Bagwell RD, Johnson DR, Lorenz GM, Meyers H, Layton MB, O'Leary PF (1998) Expansion of extension-based aphid fungus sampling service to Louisiana and Mississippi. Proceedings of the Beltwide Cotton Conferences, San Diego, Calif.
Tymon A, Shah PA, Pell JK (2002). Molecular studies on intra-specific variation in the aphid pathogenic fungus Erynia (= Pandora) neoaphidis. Proceedings of the XXXV Annual Meeting of the Society for Invertebrate Pathology, Iguassu Falls, Brazil
Vandenberg JD, Shelton AM, Wilsey WT, Ramos M (1998) Assessment of Beauveria bassiana sprays for control of diamondback moth (Lepidoptera: Plutellidae) on crucifers. J Econ Entomol 91:73–85
Vega FE, Dowd PF, Lacey LA, Pell JK, Jackson DM, Klein MG (2000) Dissemination of beneficial microbial agents by insects. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Kluwer Academic, Dordrecht, The Netherlands, pp 153–177
Vickers R, Pell JK, White A, Furlong MJ (2001) Proof-of-concept trials for control of DBM by auto-dissemination. Proceedings of the IV international workshop on control of diamondback moth and other cruciferous pests. Melbourne, Australia
Weiser J, Bucher GE, Poinar GO Jr (1976) Host relationships and utility of pathogens. In: Huffaker CB, Messenger PS (eds) Theory and practice of biological control. Academic Press, New York, pp 169–185
Wilding N, Brady BL (1984) CMI descriptions of pathogenic fungi and bacteria, set 82, nos 811–820. Commonwealth Agricultural Bureaux, The Cambrian News (Aberystwyth), UK
Wilding N, Latteur G (1987) The Entomophthorales: problems relative to their mass production and their utilisation. Meded Facult Landbouw Rijksuniv Gent 52:159–164
Wraight SP, Carruthers RI, Jaronski ST, Bradley CA, Garza CJ, Galaini-Wraight S (2000) Evaluation of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silverleaf whitefly, Bemisia argentifolii. J Invert Pathol 71:217–226
Wraight SP, Jackson MA, Kock SL de (2001) Production, stabilization and formulation of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CAB International, Wallingford, pp 253–287
Yeo H, Pell JK, Alderson PG, Clark SJ, Pye BJ (2003) Laboratory evaluation of temperature effects on the germination and growth of entomopathogenic fungi and on their pathogenicity to two aphid species. Pest Manage Sci 59:156–165
Acknowledgements
The authors thank J. Mitchell (University of Portsmouth, UK), D. Dent and H.C. Evans (both CABI Biosciences, UK) for advice and additional information. P.A.S. was sponsored by the Biotechnology and Biological Sciences Research Council, UK (BBSRC) through the Sustainable Arable LINK Programme with support from the following industrial partners: Home-Grown Cereals Authority, Horticulture Development Council, Processors' and Growers' Research Organisation, Sainsbury's plc, British Potato Council, and the National Institute for Agricultural Botany. J.K.P. was funded by the Department for Environment, Food and Rural Affairs, UK (DEFRA). Rothamsted Research receives grant-aided support from BBSRC.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shah, P.A., Pell, J.K. Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61, 413–423 (2003). https://doi.org/10.1007/s00253-003-1240-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-003-1240-8