Skip to main content

Lessons from interactions within the cassava green mite fungal pathogen Neozygites tanajoae system and prospects for microbial control using Entomophthorales

  • Chapter
Diseases of Mites and Ticks

Abstract

Most fungal pathogens lack the capacity to search for their host but rather develop sit-and-wait strategies that favour contact with them. The success of these strategies depends upon the interactions of the pathogen with its host, the host plant and the environmental conditions, which altogether determine its transmissibility. Given the limited success that has characterized application of sustainable microbial control, particularly using Entomophthorales, interaction studies have been conducted with the entomophthoralean fungus Neozygites tanajoae, pathogenic to the cassava green mite (CGM), Mononychellus tanajoa, to help understand differences observed between laboratory and field performances of this pathogen. Reciprocal pathogen-host interactions as well as tritrophic interactions involving the host plant were studied. It was found that herbivory triggers the release of volatiles that promote sporulation of isolates of N. tanajoae, whereas the host mite avoids haloes of spores of this pathogen. However, the host mite does not avoid the pathogen when inside the mummified fungus-killed cadaver. The status of microbial control of CGM in Africa is reviewed and implications of these interactions are discussed for prospective application of microbial control using Entomophthorales.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Agudelo-Silva P (1986) A species of Triplosporium (Zygomycetes: Entomophthorales) infecting Mononychellus progressivus (Acari: Tetranychidae) in Venezuela. Fla Entomol 67:444–446

    Google Scholar 

  • Alvarez Afanador JM, Acosta A, Bellotti AC, Braun AR (1993) Estudios de patogenicidad de un hongo asociado con Mononychellus tanajoa (Bondar), acaro plaga de la yuca (Manihot esculenta Crantz). Rev Colomb Entomol 19:10–20

    Google Scholar 

  • Bartkowski J, Odindo MO, Otieno WA (1988) Some fungal pathogens of the cassava green spider mites Mononychellus spp. (Tetranychidae) in Kenya. Insect Sci Appl 9:457–459

    Google Scholar 

  • Baverstock J, Elliot SL, Alderson PG, Pell JK (2005) Response of the entomopathogenic fungus Pandora neoaphidis to aphid-induced plant volatiles. J Invertebr Pathol 89:157–164

    Article  PubMed  CAS  Google Scholar 

  • Bidochka MJ, Walsh SRA, Ramos ME, Leger RJ, Carruthers RI, Silver JC, Roberts DW (1997) The cloned DNA probes distinguish endemic and exotic Entomophaga grylli fungal pathotype infections in grasshopper life stages. Mol Ecol 6(4):303–308

    Article  Google Scholar 

  • Brown GC, Prochaska GL, Hildebrand DF, Nordin GL, Jackson DM (1995) Green leaf volatiles inhibit conidial germination of the entomopathogen Pandora neoaphidis (Entomopthorales: Entomophthoraceae). Environ Entomol 24(6):1637–1643

    CAS  Google Scholar 

  • Cock JH (1985) Cassava, new potential for a neglected crop. Westview Press, Boulder, p 191

    Google Scholar 

  • Cory JS, Hoover K (2006) Plant-mediated effects in insect–pathogen interactions. Trends Ecol Evol 21:278–286

    Article  PubMed  Google Scholar 

  • Dahlberg KR, van Etten JL (1982) Physiology and biochemistry of fungal sporulation. Ann Rev Phytopathol 20:281–301

    Article  CAS  Google Scholar 

  • Dara SK, Semtner PJ (1996) Artificial introduction of Pandora neoaphidis (Zygomycotina: Entomophthorales) for the control of Myzus nicotianae (Homoptera: Aphididae) on flue-cured tobacco. In: 29th Annual meeting of the Society for Invertebrate Pathology, September 1–6, 1996, Córdoba, Spain, p 18

    Google Scholar 

  • Dara SK, Lomer CJ, Hountondji FCC, Yaninek JS (2001) Seasonal incidence of two fungal pathogens Neozygites floridana (Zygomycotina: Zygomycetes) and Hirsutella thompsonii (Deuteromycotina: Hyphomycetes), in mite populations on cassava in Benin. In: Akoroda MO, Ngeve JM (eds) Root crops in the 21st century. Proceedings of the 7th triennial symposium of the International Society for Tropical Root Crops-Africa Branch (ISTRC-AB), October 11–17, 1998, Cotonou, pp 503–507

    Google Scholar 

  • de Moraes GJ, Delalibera I Jr (1992) Specificity of a strain of Neozygites sp. (Zygomycetes: Entomophthorales) to Mononychellus tanajoa (Acari: Tetranychidae). Exp Appl Acarol 14:89–94

    Article  Google Scholar 

  • Delalibera I Jr, Hajek AE (2004) Pathogenicity and specificity of Neozygites tanajoae and Neozygites floridana (Zygomycetes: Entomophthorales) isolates pathogenic to the cassava green mite. Biol Control 30:608–616

    Article  Google Scholar 

  • Delalibera I Jr, Sosa Gomez DR, de Moraes GJ, de Alencar JA, Farias Araujo W (1992) Infection of Mononychellus tanajoa (Acari: Tetranychidae) by the fungus Neozygites sp. (Entomophthorales) in Northeastern Brazil. Fla Entomol 75:145–147

    Article  Google Scholar 

  • Delalibera I Jr, Hajek AE, Humber RA (2003) Use of cell culture media for cultivation of mite pathogenic fungi Neozygites tanajoae and Neozygites floridana. J Invertebr Pathol 84:119–127

    Article  PubMed  Google Scholar 

  • Delalibera I Jr, Hajek AE, Humber RA (2004) Neozygites tanajoae sp. nov., a pathogen of the cassava green mite. Mycologia 96:1002–1009

    Article  Google Scholar 

  • Delalibera I Jr, Demétrio CGB, Manly BFJ, Hajek AE (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 39:489–496

    Article  Google Scholar 

  • Dicke M, Sabelis MW (1988) How plants obtain predatory mites as bodyguards. Neth J Zool 38:148–165

    Google Scholar 

  • Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA (1990) Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118

    Article  CAS  Google Scholar 

  • Elliot SL, Sabelis MW, Adler FR (2002a) Virulence management in biocontrol agents. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K (eds) Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge University Press, Cambridge, pp 448–459

    Google Scholar 

  • Elliot SL, Mumford JD, Moraes GJ, Sabelis MW (2002b) Age-dependent rates of infection of cassava green mites by a fungal pathogen in Brazil. Exp Appl Acarol 27:169–180

    Article  PubMed  Google Scholar 

  • Elliot SL, Mumford JD, de Moraes GJ (2002c) The role of resting spores in the survival of the mite–pathogenic fungus Neozygites floridana from Mononychellus tanajoa during dry periods in Brazil. J Invertebr Pathol 81:148–157

    Article  PubMed  Google Scholar 

  • Elliot SL, de Moraes GJ, Mumford JD (2002d) Importance of ambient saturation deficits in an epizootic of the fungus Neozygites floridana in cassava green mite (Mononychellus tanajoa). Exp Appl Acarol 27:11–25

    Article  PubMed  Google Scholar 

  • Gandon S, Michalakis Y (2002) Multiple infection and its consequences for virulence management. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K (eds) Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge University Press, Cambridge, pp 150–164

    Google Scholar 

  • Gutierrez J, Bonato O (1994) Les acariens Tetranychidae attaquant le manioc au Congo et quelques-uns de leurs prédateurs. J Afr Zool 108:191–200

    Google Scholar 

  • Hajek AE, Humber RA (1997) Formation and germination of Entomophaga maimaga azygospores. Can J Bot 75:1739–1747

    Article  Google Scholar 

  • Hajek AE, Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322

    Article  Google Scholar 

  • Hajek AE, Humber RA, Elkinton JS (1995a) Mysterious origin of Entomophaga maimaiga in North America. Am Entomol 41:31–42

    Google Scholar 

  • Hajek AE, Renwick JAA, Roberts DW (1995b) Effects of larval host-plant on the gypsy-moth (Lepidoptera: Lymantriidae) fungal pathogen, Entomophaga maimaiga (Zygomycetes: Entomophthorales). Environ Entomol 24:1307–1314

    Google Scholar 

  • Hajek AE, Butler L, Walsh SRA, Silver JC, Hain FP, Hasting FL, Odell TM, Smitley DR (1996) Host range of the gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in the field versus laboratory. Environ Entomol 25(4):709–721

    Google Scholar 

  • Hajek AE, McManus ML, Delalibera I Jr (2005) Catalogue of introductions of pathogens and nematodes for classical biological control of insects and mites. USDA, Forest Service, FHTET, Morgantown (WV), USA, 59 p

    Google Scholar 

  • Hajek AE, McManus ML, Delalibera I Jr (2007) A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biol Control 41:1–13

    Article  Google Scholar 

  • Hanna R, Toko M (2003) Africa-wide classical biological control of cassava green mite–overview, accomplishments and future action and priorities. In: Hanna R, Toko M (eds) In: Proceedings of the third inter-regional meeting of the Africa-wide cassava green mite biocontrol project. Biological Control Centre for Africa, International Institute of Tropical Agriculture, Benin, pp 4–12

    Google Scholar 

  • Hanna R, Onzo A, Lingeman R, Sabelis MW, Yaninek JS (2005) Seasonal cycles and persistence in an acarine predator-prey system on cassava in Africa. Pop Ecol 47:107–117

    Google Scholar 

  • Herren HR, Neuenschwander P (1991) Biological control of cassava pests in Africa. Annu Rev Entomol 36:257–283

    Article  Google Scholar 

  • Hountondji FCC (2005) Classical microbial control of the cassava green mite: from individual behaviour to population dynamics. PhD thesis, University of Amsterdam, p 150

    Google Scholar 

  • Hountondji FCC, Yaninek JS, de Moraes GJ, Oduor GI (2002a) Host specificity of the cassava green mite pathogen Neozygites floridana. Biocontrol 47:61–66

    Article  Google Scholar 

  • 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 Technol 12:361–363

    Article  Google Scholar 

  • Hountondji FCC, Sabelis MW, Hanna R, Janssen A (2005) Herbivore-induced plant volatiles trigger sporulation in entomopathogenic fungi: the case of Neozygites tanajoae infecting the cassava green mite. J Chem Ecol 31:1003–1021

    Article  PubMed  CAS  Google Scholar 

  • 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 39:63–74

    Article  PubMed  CAS  Google Scholar 

  • 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 41:153–168

    Article  PubMed  Google Scholar 

  • Hountondji FCC, Sabelis MW, Hanna R (in press) The role of infochemicals in the interaction between cassava green mites and its fungal pathogen Neozygites tanajoae. In: Diseases of mites and ticks symposium, International Conference of Acarology; August 2006, Amsterdam, The Netherlands

    Google Scholar 

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, pp 27–69

    Google Scholar 

  • Klingen I, Hajek A, Meadow R, Renwick JAA (2002) Effect of brassicaceous plants on the survival and infectivity of insect pathogenic fungi. BioControl 47:411–425

    Article  CAS  Google Scholar 

  • Kogan PH, Hajek AE (2000) In vitro formation of resting spores by the insect pathogenic fungus Entomophaga maimaiga. J Invertebr Pathol 75:193–201

    Article  PubMed  CAS  Google Scholar 

  • Kulkarni RD, Thon MR, Pan H, Dean RA (2005) Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol 6(R24): 1–14

    Google Scholar 

  • Leite LG, Smith L, de Moraes GJ, Roberts DW (2000) In vitro production of hyphal bodies of the mite pathogenic fungus Neozygites floridana. Mycologia 92:201–207

    Article  Google Scholar 

  • Lyon WF (1973) A plant-feeding mite Mononychellus tanajoa Bondar (Acarina: Tetranychidae) new to the african continent threatens cassava (Manihot esculenta Crantz) in Uganda, East Africa. Pest Artic News summ 19:36–37

    Google Scholar 

  • Magalhães S, Janssen A, Hanna R, Sabelis MW (2002) Flexible antipredator behaviour in herbivorous mites through vertical migration in a plant. Oecologia 132:143–149

    Article  Google Scholar 

  • Milner RJ, Soper RS, Lutton GG (1982) Field release of an Israeli strain of the fungus Zoophthora radicans (Brefeld) Batko for the biological control of Therioaphis trifolii (Monell) f. maculata. J Aust Entomol Soc 21:113–118

    Article  Google Scholar 

  • Munster M, Janssen A, Clérivet A, Heuvel J (2005) Can plants use an entomopathogenic virus as a defence against herbivores? Oecologia 143:396–401

    Article  PubMed  Google Scholar 

  • Nowak MA, Sigmund K (2002) Super- and co-infection: the two extremes. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K (eds) Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge University Press, Cambridge, pp 124–137

    Google Scholar 

  • Nyiira ZM (1972) Report of investigation of cassava mite, Mononychellus tanajoa (Bondar). Kawanda Research Station, Kampala, Uganda, p 14

    Google Scholar 

  • Oduor GI, de Moraes GJ, Yaninek JS, Van der Geest LPS (1995a) Effect of temperature, humidity and photoperiod on mortality of Mononychellus tanajoa (Acari: Tetranychidae) infected by Neozygites cf. floridana (Zygomycetes: Entomophthorales). Exp Appl Acarol 19:571–579

    Article  Google Scholar 

  • Oduor GI, Yaninek JS, Van der Geest LPS, de Moraes GJ (1995b) Survival of Neozygites cf. floridana (Zygomycetes: Entomophthorales) in mummies of cassava green mites and the viability of its primary conidia. Exp Appl Acarol 19:479–488

    Article  Google Scholar 

  • Oduor GI, de Moraes GJ, van der Geest LPS, Yaninek JS (1996) Production and germination of primary conidia of Neozygites floridana (Zygomycetes: Entomophthorales) under constant temperatures, humidities, and photoperiods. J Invertebr Pathol 68:213–222

    Article  PubMed  Google Scholar 

  • Oduor GI, Yaninek JS, de Moraes GJ, van der Geest LPS (1997a) The effect of pathogen dosage on the pathogenicity of Neozygites floridana (Zygomycetes: Entomophthorales) to Mononychellus tanajoa (Acari: Tetranychidae). J Invertebr Pathol 70:127–130

    Article  PubMed  Google Scholar 

  • Oduor GI, Sabelis MW, Lingeman R, van der Geest LPS, de Moraes GJ, Yaninek JS (1997b) Modeling fungal (Neozygites cf. floridana) epizootics among local populations of cassava green mite (Mononychellus tanajoa). Exp Appl Acarol 21:485–506

    Article  Google Scholar 

  • Olsen KM, Schaal BA (1999) Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proc Natl Acad Sci USA 96:5586–5591

    Article  PubMed  CAS  Google Scholar 

  • Onzo A, Hanna R, Zannou I, Sabelis MW, Yaninek JS (2003) Dynamics of refuge use: diurnal, vertical migration in predatory and herbivorous mites within cassava plants. Oïkos 101:59–69

    Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • Raymond B, Hails RS (2007) Variation in plant resource quality and the transmission and fitness of the winter moth, Operophtera brumata nucleopolyhedrovirus. Biol Control 41:237–245

    Article  Google Scholar 

  • Shapiro-Ilan DI, Fuxa FR, Lacey LA, Onstad DW, Kaya HK (2005) Definitions of pathogenecity and virulence in invertebrate pathology. J Invertebr Pathol 88:1–7

    Article  PubMed  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  PubMed  CAS  Google Scholar 

  • Van der Geest LPS, Elliot SL, Breeuwer JAJ, Beerling EAM (2000) Diseases of mites. Exp Appl Acarol 24:497–560

    Article  PubMed  Google Scholar 

  • Wilding N, Mardell SK, Brobyn PJ, Wratten SD, Lomas J (1990) The effect of introducing the aphid pathogenic fungus Erynia neoaphidis into populations of cereal aphids. Ann Appl Biol 117:683–691

    Article  Google Scholar 

  • Yaninek JS, Herren HR (1988) Introduction and spread of the cassava green mite, Mononychellus tanajoa Bondar (Acari: Tetranychidae), an exotic pest in Africa and the search for appropriate control methods—a review. Bull Entomol Res 78:1–13

    Article  Google Scholar 

  • Yaninek JS, Hanna R. (2003) Cassava green mite in Africa: a unique example of successful classical biological control of a mite pest on a continent scale. In: Neuenschwander P., Borgmeister C. and Langwald L. (eds.) Biological control in IPM systems in Africa. CABI Publishing, Wallingford, UK, pp 61–75

    Google Scholar 

  • Yaninek JS, Herren AR, Gutierrez AP (1989) Dynamics of Mononychellus tanajoa (Acari: Tetranychidae) in Africa: seasonal factors affecting phenology and abundance. Environ Entomol 18:625–632

    Google Scholar 

  • Yaninek JS, Baumgaertner J, Gutierrez AP (1991) Sampling Mononychellus tanajoa (Acari: Tetranychidae) on cassava in Africa. Bull Entomol Res 81:201–208

    Google Scholar 

  • Yaninek JS, Onzo A, Ojo B (1993) Continent-wide experiences releasing neotropical phytoseiids against the exotic cassava green mite in Africa. Exp Appl Acarol 16:145–160

    Google Scholar 

  • Yaninek JS, Saizonou S, Onzo A, Zannou I, Gnanvossou D (1996) Seasonal and habitat variability in the fungal pathogens: Neozygites cf. Biocontrol Sci Technol 6:23–33

    Article  Google Scholar 

  • Yaninek JS, Megevand B, Ojo B, Cudjoe AR, Abole E, Onzo A, Zannou I (1998) Establishment and spread of Typhlodromalus manihoti (Acari: Phytoseiidae), an introduced phytoseiid predator of Mononychellus tanajoa (Acari: Tetranychidae) in Africa. Environ Entomol 27:1496–1505

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabien C. C. Hountondji .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Hountondji, F.C.C. (2008). Lessons from interactions within the cassava green mite fungal pathogen Neozygites tanajoae system and prospects for microbial control using Entomophthorales. In: Bruin, J., van der Geest, L.P.S. (eds) Diseases of Mites and Ticks. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9695-2_16

Download citation

Publish with us

Policies and ethics