Advertisement

Mite Pathogens and Their Use in Biological Control

  • Vitalis W. WekesaEmail author
  • Fabien C. C. Hountondji
  • Surendra K. Dara
Part of the Progress in Biological Control book series (PIBC, volume 19)

Abstract

An overview of infectious microorganisms associated with pest mites is presented. Many mites are major impediments to the production of food crops either in open fields or under protected environments such as greenhouses and plastic tunnels. Reliance on chemical acaricides for management of these mites is of serious concern due to the development of resistance in mite populations, environmental disturbance and effect on human health. Several pathogens play an important role in the regulation of pest mite populations through natural epizootics. The majority of these are fungi, but other pathogens include viruses, bacteria, protozoa, and nematodes. Several successful examples of pathogens that have been produced in vitro for the control of pest mites are presented. Interaction of the pathogens with beneficial arthropods such as predatory mites is also important for implementing biological control. Prospects for the application of acaropathogens in the management of mites in various agricultural systems are discussed.

Keywords

Biocontrol agents Acaropathogens Mites and IPM 

References

  1. Agboton BV, Hanna R, Hountondji FCC, Von Tiedemann A (2009) Pathogenicity and host specificity of Brazilian and African isolates of the acaropathogenic fungus Neozygites tanajoae to mite species associated with cassava. J Appl Entomol 133:651–658Google Scholar
  2. Aghajanzadeh S, Mallik B, Chandrashekar SC (2006) Bioefficacy of six isolates of Hirsutella thompsonii Fisher against citrus rust mite, Phyllocoptruta oleivora Ashmead (Acari: Eriophyidae) and twospotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). Pak J Biol Sci 9:871–875Google Scholar
  3. Agudelo-Silva P (1986) A species of Triplosporium (Zygomycetes: Entomophthorales) infecting Mononychellus progressivus (Acari: Tetranychidae) in Venezuela. Fla Entomol 69:444–446Google Scholar
  4. Al-Shanfari A, Hountondji FCC, Al-Zawamri H, Rawas H, Al-Mashiki Y, De Moraes GJ, Moore D, Gowen RS (2013) Occurrence and seasonal prevalence of the coconut mite, Aceria guerreronis (Eriophyidae), and associated arthropods in Oman. Exp Appl Acarol 60:139–151PubMedGoogle Scholar
  5. Alves SB, Rossi LS, Lopes RB, Tamai MA, Perera RM (2002) Beauveria bassiana yeast on agar medium and its pathogenicity against Diatraea saccharalis (Lepidoptera: Crambidae) and Tetranychus urticae (Acari: Tetranychidae). J Invertebr Pathol 81:70–77PubMedGoogle Scholar
  6. Anderson TE, Roberts DW (1983) Compatibility of Beauveria bassiana isolates with insecticides formulation used in Colorado potato beetle (Coleoptera: Chrysomelidae) control. J Econ Entomol 76:1437–1441Google Scholar
  7. Anderson TE, Hajek AE, Roberts DW, Preisler HK, Robertson JL (1989) Colorado potato beetle (Coleoptera: Chrysomelidae): effects of combinations of Beauveria bassiana with insecticides. J Econ Entomol 82:83–89Google Scholar
  8. Ariori S, Dara SK (2007) Predation of Neozygites tanajoae-infected cassava green mites by Typhlodromalus aripo (Acari: Phytoseiidae). Agric Conspec Sci 72:169–172Google Scholar
  9. ARSEF (ARS Collection of Entomopathogenic Fungal Cultures) (2009) Catalog of species. USDA ARS Biological Integrated Pest Management Research – US Department of Agriculture, Agricultural Research Service, Ithaca, p 435Google Scholar
  10. Bacon CW, White J (2000) Microbial endophytes. CRC Press, Roca Baton, Florida, p 500Google Scholar
  11. Bajan C, Kmitowa K, Popowska EN (1998) Reaction of various ecotypes of entomopathogenic fungus Beauveria bassiana to the botanical preparation NEEMTM and pyrethroid Fastak. Arch Phytopathol Plant Protect 31:369–375Google Scholar
  12. Bałazy S, Wiśniewski J (1984) Records on some lower fungi occurring in mites (Acarina) from Poland. Acta Mycol 20:159–172Google Scholar
  13. Bałazy S, Wiśniewski J (1989) Pathogene Pilze bei Milben. Mikrokosmos 78:299–304Google Scholar
  14. Bartkowski J, Odindo MO, Otieno WA (1988) Some fungal pathogens of the cassava green spider mite Mononychellus spp. (Tetranychidae) in Kenya. Insect Sci Appl 9:457–459Google Scholar
  15. Bartlett BR (1968) Outbreaks of twospotted spider mites and cotton aphids following pesticide treatment. Pest stimulation vs natural enemy destruction as the cause of outbreaks. J Econ Entomol 61:297–303Google Scholar
  16. Beerling EAM, Van Der Geest LPS (1991a) A microsporidium (Microspora: Pleistophoridae) in mass-rearings of the predatory mites Amblyseius cucumeris and A. barkeri (Acarina: Phytoseiidae): analysis of a problem. IOBC/WPRS Bull 14:5–8Google Scholar
  17. Beerling EAM, Van Der Geest LPS (1991b) Microsporidiosis in mass-rearings of the predatory mites Amblyseius cucumeris and A. barkeri (Acarina: Phytoseiidae). Proc Exp Appl Entomol NEV Amsterdam 2:157–162Google Scholar
  18. Bjørnson S, Steiner MY, Keddie BA (1997) Birefringent crystals and abdominal discoloration of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). J Invertebr Pathol 69:85–91Google Scholar
  19. Boucias DG, Stokes C, Storey G, Pendland JC (1996) The effects of imidacloprid on the termite Reticulitermes flavipes and its interaction with the mycopathogen Beauveria bassiana. Pflanzenschutz-Nachr Bayer 49:105–151Google Scholar
  20. Brandenburg RL, Kennedy GG (1982) Relationship of Neozygites floridana (Entomophthorales: Entomophthoraceae) to two-spotted spider mite (Acari: Tetranychidae) populations in field corn. J Econ Entomol 75:691–694Google Scholar
  21. Brandenburg RL, Kennedy GG (1983) Interactive effects of selected pesticides on the 2-spotted spider-mite and its fungal pathogen Neozygites floridana. Entomol Exp Appl 34:240–244Google Scholar
  22. Breeuwer JAJ, Jacobs G (1996) Wolbachia: intracellular manipulators of mite reproduction. Exp Appl Acarol 20:421–434PubMedGoogle Scholar
  23. Chandler D, Davidson G, Pell JG, Ball BV, Shaw K, Sunderland KD (2000) Fungal biocontrol of Acari. Biocontrol Sci Tech 10:357–384Google Scholar
  24. Crous PW, Braun U, Schubert K, Groenewald JZ (2007) Delimiting Cladosporium from 356 morphologically similar genera. Stud Mycol 58:33–56PubMedCentralPubMedGoogle Scholar
  25. da Costa GL, Sarquis MI, de Moraes AM, Bittencourt VR (2002) Isolation of Beauveria bassiana and Metarhizium anisopliae var. anisopliae from Boophilus microplus tick (Canestrini, 1887), in Rio de Janeiro State, Brazil. Mycopathologia 154:207–209PubMedGoogle Scholar
  26. Dara S (2013) Microbial control as an important component of strawberry IPM. CAPCA Adviser 16:29–32Google Scholar
  27. Dara SK (2014a) New strawberry IPM studies with chemical, botanical, and microbial solutions. CAPCA Adviser 17:34–37Google Scholar
  28. Dara SK (2014b) Beauveria bassiana and California strawberries: endophytic, mycorrhizal, and entomopathogenic interactions. Annual meetings of the Society for Invertebrate Pathology, Mainz, 3–7 Aug, p 148Google Scholar
  29. Dara SK, Dara SS (2013) Compatibility of the entomopathogenic fungus, Beauveria bassiana with some fungicides commonly used in strawberries. Univ Calif Coop Ext Strawberries and Vegetables eNewsletter. http://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=9626
  30. Dara SK, Hountondji FCC (2001) Effects of formulated imidacloprid on two mite pathogens, Neozygites floridana (Zygomycotina: Zygomycetes) and Hirsutella thompsonii (Deuteromycotina: Hyphomycetes). Insect Sci Appl 21:133–138Google Scholar
  31. Dara SK, Dara SR, Dara SS (2014a) Endophytic colonization and pest management potential of Beauveria bassiana in strawberries. J Berry Res 3:203–211Google Scholar
  32. Dara SS, Dara SSR, Dara SK (2014b) Optimal time intervals for using insect pathogenic Beauveria bassiana with fungicides. University of California Cooperative Extension Central Coast Agriculture Highlights Newsletter, Feb 2014, pp 4–5. http://cesantabarbara.ucanr.edu/newsletters/Central_Coast_Agriculture_Highlights50500.pdf
  33. Dara SSR, Dara SS, Sahoo A, Bellam H, Dara SK (2014c) Can entomopathogenic fungus, Beauveria bassiana be used for pest management when fungicides are used for disease management? University of California Cooperative Extension Strawberries and Vegetables e-Newsletter. http://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=15671
  34. Delalibera I Jr, Sosa-Gomez DR, de Moraes GJ, de Alencar JA, Farias-Araújo W (1992) Infection of Mononychellus tanajoa (Acari: Tetranychidae) by the fungus Neozygites sp. in Northeastern Brazil. Fla Entomol 75:145–147Google Scholar
  35. Delalibera I Jr, Hajek AE, Humber RA (2003) Use of cell culture media for cultivation of the mite pathogenic fungi Neozygites tanajoae and Neozygites floridana. J Invertebr Pathol 84:119–127PubMedGoogle Scholar
  36. Delalibera I Jr, Hajek AE, Humber RA (2004) Neozygites tanajoae sp. nov., a pathogen of the cassava green mite. Mycologia 96:1002–1009PubMedGoogle Scholar
  37. Delalibera I Jr, Demetrio CGB, Manly BFJ, Hajek A (2006) Effect of relative humidity and origin of isolates of Neozygites tanajoae (Zygomycetes: Entomophthorales) on production of conidia from cassava green mite, Mononychellus tanajoa (Acari: Tetranychidae) cadavers. Biol Control 39:489–496Google Scholar
  38. Delgado FX, Britton JH, Onsager JA, Swearingen W (1999) Field assessment of Beauveria bassiana (Balsamo) Vuillemin and potential synergism with diflubenzuron for control of Savanna grasshopper complex (Orthoptera) in Mali. J Invertebr Pathol 73:34–39PubMedGoogle Scholar
  39. Dresner E (1949) Culture and use of entomogenous fungi for the control of insects. Contrib Boyce Thompson Inst 15:319–335Google Scholar
  40. Fargues J, Goettel MS, Smits N, Ouedraogo A, Rougier M (1997) Effect of temperature on vegetative growth of Beauveria bassiana isolates from different origins. Mycologia 89:383–392Google Scholar
  41. Feng M-G, Poprawski TJ, Nowierski RM, Zeng Z (1999) Infectivity of Pandora neoaphidis (Zygomycetes: Entomophthorales) to Acyrthosiphon pisum (Homoptera: Aphididae) in response to varying temperature and photoperiod regimes. J Appl Entomol 123:29–35Google Scholar
  42. Filotas MJ, Hajek AE (2007) Variability in thermal responses among Furia gastropachae isolates from different geographic origins. J Invertebr Pathol 96:109–117PubMedGoogle Scholar
  43. Furtado IP, De Moraes GJ, Keller S (1996) Infection of Euseius citrifolius (Acari: Phytoseiidae) by an entomophthoralean fungus in Brazil. Rev Ecossistema 21:85–86Google Scholar
  44. 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 81–95Google Scholar
  45. Guo YL, Zuo G, Zhao JH, Wang NY, Jiang JW (1993) A laboratory test of thuringiensin to Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytoseiidae). Chin J Biol Control 9:151–155Google Scholar
  46. Hajek A (2004) Natural enemies; an introduction to biological control. Cambridge University Press, CambridgeGoogle Scholar
  47. Hajek AE, St. Leger R (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322Google Scholar
  48. Hassan AEM, Charnley AK (1989) Ultrastructural study of the penetration by Metarhizium anisopliae through Dimilin-affected cuticle of Manduca sexta. J Invertebr Pathol 54:117–124Google Scholar
  49. Hess RT, Hoy MA (1982) Microorganisms associated with the spider mite predator Metaseiulus (Typhlodromus) occidentalis: electron microscope observations. J Invertebr Pathol 40:98–106Google Scholar
  50. Hirose E, Neves PMOJ, Zequi JAC, Martins LH, Peralta CH, Moino A Jr (2001) Effect of biofertilizers and neem oil on the entomopathogenic fungi Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch.) Sorok. Braz Arch Biol Technol 44:419–423Google Scholar
  51. Hountondji FCC, Yaninek JS, de Moraes GJ, Oduor GI (2002a) Host specificity of the cassava green mite pathogen Neozygites floridana. BioControl 47:61–66Google Scholar
  52. Hountondji FCC, Lomer CJ, Hanna R, Cherry AJ, Dara SK (2002b) Field evaluation of Brazilian isolates of Neozygites floridana (Entomophthorales: Neozygitaceae) for the microbial control of cassava green mite in Benin, West Africa. Biocontrol Sci Tech 12:361–370Google Scholar
  53. Hountondji FCC, Sabelis M, Hanna R, Janssen A (2005) Herbivore-induced plant volatiles trigger spoprulation in entomopathogenic fungi: the case of Neozygites tanajaoe infecting the cassava green mite. J Chem Ecol 31:1003–1021PubMedGoogle Scholar
  54. Hountondji FCC, Hanna R, Sabelis MW (2006) Does methyl salicylate, a component of herbivore-induced plant odour, promote sporulation of the mite-pathogenic fungus Neozygites tanajoae? Exp Appl Acarol 39:63–74PubMedGoogle Scholar
  55. Hountondji FCC, Hanna R, Cherry AJ, Sabelis MW, Agboton B, Korie S (2007) Scaling-up tests on virulence of the cassava green mite fungal pathogen Neozygites tanajoae (Entomophthorales: Neozygitaceae) under controlled conditions: first observations at the population-level. Exp Appl Acarol 41:153–168PubMedGoogle Scholar
  56. Hountondji FCC, De Moraes J, Al-Zawamri H (2010) Mites (Acari) on coconut, date palm and associated plants in Oman. Syst Appl Acarol 15:228–234Google Scholar
  57. Hoy MA (1998) Myths, modes and mitigations of resistance to pesticides. Philos Trans R Soc Lond B 353:1787–1795Google Scholar
  58. Humber RA, De Moraes GJ, Dos Santos JM (1981) Natural infection of Tetranychus evansi (Acarina: Tetranychidae) by a Triplosporium sp. (Zygomycetes: Entomophthorales) in northeastern Brazil. Entomophaga 26:421–425Google Scholar
  59. Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetes fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biological control agents. CAB International, Wallingford, pp 23–27Google Scholar
  60. Irigaray FJS, Marco-Mancebón V, Pérez-Moreno I (2003) The entomopathogenic fungus Beauveria bassiana and its compatibility with triflumuron: effects on the twospotted spider mite Tetranychus urticae. Biol Control 26:168–173Google Scholar
  61. Islam MT, Olleka A, Shunxiang R (2010) Influence of neem on susceptibility of Beauveria bassiana and investigation of their combined efficacy against sweetpotato whitefly, Bemisia tabaci on eggplant. Pestic Biochem Physiol 98:45–49Google Scholar
  62. Jacobson RJ, Chandler D, Fenlon J, Russel KM (2001) Compatibility of Beuveria bassiana (Balsamo) Vuillemin with Amblyseius cucumeris Oudemans (Acarina: Phytoseiidae) to control Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) on cucumber plants. Biocontrol Sci Technol 11:391–400Google Scholar
  63. James DG, Price TS (2002) Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid. J Econ Entomol 95:729–732PubMedGoogle Scholar
  64. Johanowicz DL, Hoy MA (1998) Wolbachia in a predator–prey system: 16S ribosomal DNA analysis of two phytoseiids (Acari: Phytoseiidae) and their prey (Acari: Tetranychidae). Ann Entomol Soc Am 89:435–441Google Scholar
  65. Kaakeh W, Reid BL, Bohnert TJ, Bennett GW (1997) Toxicity of imidacloprid in the German cockroach (Dictyoptera: Blattellidae), and the synergism between imidacloprid and Metarhizium anisopliae (Imperfect fungi: Hyphomycetes). J Econ Entomol 90:473–482Google Scholar
  66. Kaaya GP, Hassan S (2001) Entomogenous fungi as promising biopesticides for tick control. Exp Appl Acarol 24:913–926Google Scholar
  67. Kassa A, Brownbridge M, Parker BL, Skinner M, Gouli V, Gouli S, Guo M, Lee F, Hata T (2008) Whey for mass production of Beauveria bassiana and Metarhizium anisopliae. Mycol Res 112:583–591PubMedGoogle Scholar
  68. Keller S (1997) The genus Neozygites (Zygomycetes: Entomophthorales) with special reference to species found in tropical regions. Sydowia 49:118–146Google Scholar
  69. Kirby C, Safford III, Allan SA (2010) Field applications of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae F52 (Hypocreales: Clavicipitaceae) for the control of Ixodes scapularis (Acari: Ixodidae). J Med Entomol 47:1107–1115Google Scholar
  70. Kumar SP, Singh L (2008) Enabling mycelial application of Hirsutella thompsonii for managing the coconut mite. Exp Appl Acarol 46:169–182Google Scholar
  71. Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens as biological control agents: do they have a future? Biol Control 21:230–248Google Scholar
  72. Leite LG, Smith L, Moraes GJ, Roberts DW (2000) In vitro production of hyphal bodies of the mite pathogenic fungus Neozygites floridana. Mycologia 92:201–207Google Scholar
  73. Lighthart B, Sewall D, Thomas DR (1988) Effect of several stress factors on the susceptibility of the predatory mite, Metaseiulus occidentalis (Acari: Phytoseiidae), to the weak bacterial pathogen Serratia marcescens. J Invertebr Pathol 52:33–42Google Scholar
  74. Maniania NK, Bugeme DM, Wekesa VW, Delalibera I Jr, Knapp M (2008) Role of entomopathogenic fungi in the control of Tetranychus evansi and Tetranychus urticae (Acari: Tetranychidae), pests of horticultural crops. Exp Appl Acarol 46:259–274PubMedGoogle Scholar
  75. McCoy CW, Kanavel RF (1969) Isolation of Hirsutella thompsonii from the citrus rust mite, Phyllocoptruta oleivora and its cultivation on various synthetic media. J Invertebr Pathol 14:386–390Google Scholar
  76. McCoy CW, Omoto C, Mazet I, Vey A (1992) Biological activity of crude filtrates and hirsutellin A to mosquitoes and phytophagous arthropods. Abstract 120 XXV annual meeting. Society of Invertebrate Pathology, HeidelbergGoogle Scholar
  77. McMurtry JA, Huffaker CB, Van de Vrie M (1970) Ecology of tetranychid mites and their natural enemies. A review on tetranychid enemies; their biological characters and the impact of spray practices. Hilgardia 40:331–370Google Scholar
  78. Messing RH, Croft BA (1996) Pesticide resistance in Eriophyoid mites, their competitors and predators. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites, their biology, natural enemies and control. Elsevier, Amsterdam, pp 689–694Google Scholar
  79. Mietkiewski RT, Balazy S, Van Deer Geest LPS (1993) Observations on a mycosis of spider mites (Acari: Tetranychidae) caused by Neozygites floridana in Poland. J Invertebr Pathol 61:317–319Google Scholar
  80. Mikunthan G, Manjunatha M (2006a) Fusarium semitectum, a potential mycopathogen against thrips and mites in chilli, Capsicum annuum. Commun Agric Appl Biol Sci 71:449–463PubMedGoogle Scholar
  81. Mikunthan G, Manjunatha M (2006b) Pathogenicity of Fusarium semitectum against crop pests and its biosafety to non-target organisms. Commun Agric Appl Biol Sci 71:465–473PubMedGoogle Scholar
  82. Milner RJ (1985) Neozygites acaridis (Petch) comb. nov. An entomophthoralean pathogen of the mite, Macrocheles peregrinus, in Australia. Trans Br Mycol Soc 85:641–647Google Scholar
  83. Mwangi EN, Kaaya GP, Essuman S (1995) Experimental infections of the tick Riphicephalus appenticulatus with pathogenic fungi, Beauveria bassiana and Metarhizium anisopliae, and natural infections of some ticks with bacteria and fungi. J Afr Zool 109:151–160Google Scholar
  84. Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, Kisimoto R, Yanase T, Matsumoto Y, Kageyama D, Noda H (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Appl Environ Microbiol 75:6757–6763PubMedCentralPubMedGoogle Scholar
  85. Oduor GI, Moraes GJ, Yaninek JS, Van Der Geest LPS (1995) Effect of temperature, humidity and photoperiod on mortality of Mononychellus tanajoa (Acari: Tetranychidae) infected by Neozygites cf. floridana (Zygomycetes: Entomophthorales). Exp Appl Acarol 19:571–579Google Scholar
  86. Oduor GI, Yaninek JS, Van Der Geest LPS, De Moraes GJ (1996a) Germination and viability of capilliconidia of Neozygites floridana (Zygomycetes: Entomophthorales) under constant temperature, humidity and light conditions. J Invertebr Pathol 67:267–278PubMedGoogle Scholar
  87. Oduor GI, De Moraes GJ, Van der Geest LPS, Yaninek JS (1996b) Production and germination of primary conidia of Neozygites floridana (Zygomycetes: Entmophthorales) under constant temperatures, relative humidities and photoperiods. J Invertebr Pathol 68:213–222PubMedGoogle Scholar
  88. Olson DL, Oetting RD (1999) Compatibility of insect growth regulators and Beauveria bassiana (Balsamo) Vuillemin in controlling green peach aphids (Homoptera: Aphididae) on greenhouse chrysanthemums. J Entomol Sci 34:286–294Google Scholar
  89. Omoto C, McCoy CW (1998) Toxicity of purified fungal toxin hirsutellin A to the citrus rust mite, Phyllocoptruta oleivora (Ash.). J Invertebr Pathol 72:319–322PubMedGoogle Scholar
  90. Papierok B, Rafanomezantsoa-Randriambololona BN, Ziat N (1993) Nouvelles donne‘es sur l’ecologie et le comportement entomopathoge’ne experimental de l’entomophthorale Conidiobolus coronatus (Zygomycetes). Entomophaga 38:299–312Google Scholar
  91. Peña JE, Mannion CM, Howard FW, Hoy MA (2006) Raoiella indica (Prostigmata: Tenuipalpidae): the red palm mite: a potential invasive pest of palms and bananas and other tropical crops in Florida. University of Florida IFAS Extension, ENY-837, 414. http://edis.ifas.ufl.edu/IN681
  92. Penman DR, Chapman RB (1988) Pesticide induced mite outbreaks: pyrethroids and spider mites. Exp Appl Acarol 4:265–276Google Scholar
  93. Poinar G Jr, Poinar R (1998) Parasites and pathogens of mites. Annu Rev Entomol 43:449–469PubMedGoogle Scholar
  94. Polar P, Kairo MTK, Moore D, Pegram R, John S, Peterkin D (2005) Assessment of fungal isolates for the development of a myco-acaricide for cattle tick control. Vector Borne Zoonotic Dis 5:276–284PubMedGoogle Scholar
  95. Quintela ED, McCoy CW (1997) Pathogenicity enhancement of Metarhizium anisopliae and Beauveria bassiana to first instars of Diaprepes abbreviatus (Coleoptera: Curculionidae) with sublethal doses of imidacloprid. Environ Entomol 26:1173–1182Google Scholar
  96. Ramaseshiah G (1971) Occurrence of an Entomophthora on tetranychid mites in India. J Invertebr Pathol 24:218–223Google Scholar
  97. Raupp MJ, Webb R, Szczepaniec A, Booth D, Ahern R (2004) Incidence, abundance, and severity of mites on hemlocks following applications of imidacloprid. J Arboric 30:108–113Google Scholar
  98. Roberts DW, Campbell AS (1977) Stability of entomopathogenic fungi. Misc Publ Entomol Soc Am 10:19–76Google Scholar
  99. Ros, VID, Fleming VM, Feil EJ, Breeuwer JAJ (2012) Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiol. http://www.biomedcentral.com/1471-2180/12/S1/S13
  100. Royalty RN, Hall FR, Taylor RAJ (1990) Effects of thuringiensin on Tetranychus urticae (Acari: Tetranychidae) mortality, fecundity and feeding. J Econ Entomol 83:792–798Google Scholar
  101. Saba F (1971) Population dynamics of tetranychids in subtropical Florida. In: Proceeding of the 3rd international congress of Acarology, Prague. Junk, The Hague, pp 237–240Google Scholar
  102. Samson RA, Rombach MC (1985) Biology of the fungi Verticilium and Aschersonia. In: Hussey NW, Scopes N (eds) Biological pest control, the glasshouse experience. Cornell University Press, Ithaca, pp 34–42Google Scholar
  103. Schütte C, Dicke M (2008) Verified and potential pathogens of predatory mites (Acari: Phytoseiidae). Exp Appl Acarol 46(1–4):307–328PubMedGoogle Scholar
  104. Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423PubMedGoogle Scholar
  105. Shi W-B, Feng M-G (2006) Field efficacy of application of Beauveria bassiana formulation and low rate pyridaben for sustainable control of citrus red mite Panonychus citri (Acari: Tetranychidae) in orchards. Biol Control 39:210–217Google Scholar
  106. Shi W-B, Jian Y, Feng M-G (2005) Compatibility of ten acaricides with Beauveria bassiana and enhancement of fungal infection to Tetranychus cinnabarinus (Acari: Tetranychidae) eggs by sublethal application rates of pyridaben. Appl Entomol Zool 40:659–666Google Scholar
  107. Smitley DR, Brooks W, Kennedy GG (1986) Environmental effects on production of primary and secondary conidia, infection, and pathogenesis of Neozygites floridana, a pathogen of the two-spotted spider mite, Tetranychus urticae. J Invertebr Pathol 47:325–332Google Scholar
  108. Smitley DR, Kennedy GG, Brooks WM (2011) Role of the entomogenous fungus, Neozygites floridana, in population declines of the twospotted spider mite, Tetranychus urticae, on field corn. Entomol Exp Appl 41:255–264Google Scholar
  109. Soper RS, Ward MG (1981) Production, formulation and application of fungi for insect control. In: Papavizas CG (ed) Biological control in crop production. Osmoun, Montclair, pp 161–180Google Scholar
  110. Sosa Gomez DR (1987) Control microbiano de Phyllocoptruta oleivora (Ashm). y Eriophyes sheldoni Ewing mediante pulverizaciones de conídios de tres variedades de Hirsutella thompsonii Fisher. XI Congr Bras Entomol Res 1:167Google Scholar
  111. Sosa Gomez DR, Moscardi F (1991) Microbial control and insect pathology in Argentina. Ciencia e Cultura 43(5):375–379Google Scholar
  112. Stacey DA, Fellowes MDE (2002) Influence of temperature on pea aphid (Acyrthosiphon pisum) resistance to natural enemy attack. Bull Entomol Res 92:351–357PubMedGoogle Scholar
  113. Steiner M (1993) Quality control requirements for pest biological control agents. Alberta Government Publication AECV93-R6, Alberta Environmental Centre, VegrevileGoogle Scholar
  114. Steinkraus DC, Boys GO (2005) Mass harvesting of the entomopathogenic fungus, Neozygites fresenii, from natural field epizootics in the cotton aphid, Aphis gossypii. J Invertebr Pathol 88:212–217PubMedGoogle Scholar
  115. Šutáková G (1988) Electron microscopic study of developmental stages of Rickettsiella phytoseiuli in Phytoseiulus persimilis Athias-Henriot (Gamasoidea: Phytoseiidae) mites. Acta Virol 32:50–54PubMedGoogle Scholar
  116. Tedders WL (1981) In vitro inhibition of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae by six fungicides used in pecan culture. Environ Entomol 10:346–349Google Scholar
  117. Trinci APJ, Lane BS, Humphreys AM (1990) Optimization of cultural conditions for production and longevity of entomopathogenic fungi. Proceeding of the Vth international colloquium on invertebrate pathology and microbial control, Adelaide, 20–24 Aug 1990, pp 121–125Google Scholar
  118. Van Der Geest LPS, Elliot SL, Breeuwer JAJ, Beerling EAM (2000) Diseases of mites. Exp Appl Acarol 24:497–560PubMedGoogle Scholar
  119. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the twospotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572PubMedGoogle Scholar
  120. Vey A, Quiot JM, Mazet I, McCoy CW (1993) Toxicity and pathology of crude broth filtrate produced by Hirsutella thompsonii var. thompsonii in shake culture. J Invertebr Pathol 61:131–137PubMedGoogle Scholar
  121. Weiser J, Muma MH (1966) Entomophthora floridana n.s. (Phycomycetes: Entomophthoraceae) a parasite of the Texas citrus mite Tetranychus banksi. Fla Entomol 49:155–159Google Scholar
  122. Wekesa VW, Delalibera I Jr (2008) Long-term preservation of Neozygites tanajoae (Entomophthorales: Neozygitaceae) in cadavers of Mononychellus tanajoa (Acari: Tetranychidae). Biocontrol Sci Technol 18:621–627Google Scholar
  123. Wekesa VW, Maniania NK, Knapp M, Boga HI (2005) Pathogenicity of Beauveria bassiana and Metarhizium anisopliae to the tobacco spider mite Tetranychus evansi. Exp Appl Acarol 36:41–50PubMedGoogle Scholar
  124. Wekesa VW, Knapp M, Maniania NK, Boga HI (2006) Effects of Beauveria bassiana and Metarhizium anisopliae on mortality, fecundity and egg fertility of Tetranychus evansi. J Appl Entomol 130:155–159Google Scholar
  125. Wekesa VW, Moraes GJ, Knapp M, Delalibera I Jr (2007) Interactions of two natural enemies of Tetranychus evansi, the fungal pathogen Neozygites floridana (Zygomycetes: Entomophthorales) and the predatory mite, Phytoseiulus longipes (Acari: Phytoseiidae). Biol Control 41:408–414Google Scholar
  126. Wekesa VW, Moraes GJ, Ortega EMM, Delalibera I Jr (2010) Effect of temperature on sporulation of Neozygites floridana isolates from different climates and their virulence against the tomato red spider mite, Tetranychus evansi. J Invertebr Pathol 103:36–42PubMedGoogle Scholar
  127. Yaninek S, Hanna R (2003) Cassava green mite in Africa—a unique example of successful classical biological control of a mite pest on a continental scale. In: Neuenschwander P, Borgemeister C, Langewald J (eds) Biological control in IPM systems in Africa. CAB International, Wallingford, pp 61–75Google Scholar
  128. Yaninek JS, Saizonou S, Onzo A, Zannou I, Gnanvossou D (1996) Seasonal and habitat variability in the fungal pathogens: Neozygites cf. floridana and Hirsutella thompsonii, associated with cassava mites in Benin. Biocontrol Sci Technol 6:23–33Google Scholar
  129. Ye SD, Dun YH, Feng M-G (2005) Time and concentration dependent interactions of Beauveria bassiana with sublethal rates of imidacloprid against the aphid pests Macrosiphoniella sanborni and Myzus persicae. Ann Appl Biol 146:459–468Google Scholar
  130. 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 Manag Sci 59:156–165PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Vitalis W. Wekesa
    • 1
    Email author
  • Fabien C. C. Hountondji
    • 2
  • Surendra K. Dara
    • 3
    • 4
  1. 1.Department of Applied and Technical BiologyTechnical University of KenyaNairobiKenya
  2. 2.Université de Parakou, Ecole Nationale Supérieure des Sciences et Techniques AgronomiquesDjougouRepublic of Benin
  3. 3.Strawberry and Vegetable Crops Advisor and Affiliated IPM AdvisorSan Luis Obispo, Santa BarbaraUSA
  4. 4.Ventura Counties, UC Cooperative ExtensionSan Luis ObispoUSA

Personalised recommendations