Skip to main content

Natural parasites and biological control

  • Chapter
The Cyst Nematodes

Abstract

Widespread concern about the hazards of pesticides to human health and the environment has led to considerable international efforts to reduce their use (Dinham, 1993; Zedan, 1994). In this regard, nematicides are no exception and this has stimulated the search for alternative approaches to nematode management (Thomason, 1987) of which biological control is one amongst others such as the development of resistant cultivars. The introduction of one organism to control another has a history going back to the 1920s and the first studies using natural enemies to control plant parasitic nematodes date from the mid-1930s (Linford, 1937; Linford, Yap and Oliveira, 1938). The research, since the mid-1930s, has been thoroughly reviewed by Stirling (1991). The results of using natural enemies to control nematodes has been inconsistent which has led many nematologists to be sceptical about their use to control plant parasitic nematodes; indeed, at present there are no reliable commercial products available. However, the increase and subsequent decline of cereal cyst nematodes in monocropped cereals reported between 1955 and 1968 by Gair, Mathias and Harvey (1969) has been attributed to the effects of two main species of nematophagous fungi Nematophthora gynophila and Verticillium chlamydosporium (Kerry, 1975). The evidence for the involvement of these fungi in suppressing nematode populations below the economic threshold comes from a number of studies in which: (1) H. avenue failed to increase where spores of V. chlamydosporium and N. gynophila were numerous (Crump and Kerry, 1981; Kerry, Crump and Mullen, 1982a), (2) the numbers of H. avenae were inversely related to the level of fungal parasitism (Kerry, Crump and Mullen, 1982b), (3) the reduction in the number of nematophagus fungi induced by the application of formalin resulted in an increase in nematode multiplication (Kerry, Crump and Mullen, 1980, 1982a, b; Crump and Kerry, 1981) and this effect was only observed in soils where V. chlamydosporium and N. gynophila were present and not where they were absent (Kerry, Crump and Mullen, 1980), and (4) watering only increased fungal parasitism and reduced the numbers of H. avenae in untreated soil and not in soil treated with formalin, where there was no effect on nematode numbers (Kerry, Crump and Mullen, 1980). These studies are the first example of density dependency in the biological control of plant pathogens but since then other examples of density dependence in the biological control of soil borne pests and diseases have been reported (Jaffee, 1993). Although suppressive soils have provided an insight and significant levels of nematode control in some soils, the use of microbial agents to control plant parasitic nematodes has produced highly variable results and the successful use of microbial agents will require a deep knowledge of the interrelationships between agent, pest and plant and the environmental factors which influence them (Kerry, 1993). The purpose of this chapter will therefore be to focus on the use of the natural parasites of cyst nematodes in nematode biomanagement and review the work that has accumulated with respect to these organisms since the publication of Stirling’s book the Biological Control of Plant Parasitic Nematodes (1991), and to examine the research strategies available to understand the nematode/hyperparasite interactions at the population and molecular level as a way forward.

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 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

  • Afolabi, P., Davies, K. G. and O’Shea, P. (1995) The electrostatic nature of the spore surface of Pasteuria penetrans, the bacterial parasite of root-knot nematodes. Journal of Applied Bacteriology, 79, 244–49.

    Google Scholar 

  • Arora, D. K., Hirsch, P. R. and Kerry, B. R. (1996) PCR-based molecular discrimination of Verticillium chlamydosporium isolates. Mycological Research, 100, 801–9.

    CAS  Google Scholar 

  • Carder, J. H., Segers, R, Butt, T. M., Barbara, D. J., Von Mende, N. and Coosemans, J. (1993) Taxonomy of the nematophagus fungi Verticillium chlamydosporium and V. suchlasporium based on secreted enzymes and RFLP analysis. Journal of Invertebrate Pathology, 62, 178–84.

    CAS  Google Scholar 

  • Caswell-Chen, E. P., Williamson, V. M. and Westerdahl, B. B. (1993) Applied biotechnology in nematology. Journal of Nematology, 25, 719–30.

    PubMed  CAS  Google Scholar 

  • Charmer, A. G. De R. and Gowen, S. R. (1992) Selection for increased host resistance and increased pathogen specificity in the Meloidogyne-Pasteuria penetrans interaction. Fundamental and Applied Nematology, 15, 331–39.

    Google Scholar 

  • Chen, S. Y. and Dickson, D. W. (1996) Fungal penetration of the cyst wall of Heterodera glycines. Phytopathology, 86, 319–27.

    Google Scholar 

  • Chen, S. Y., Dickson, D. W., Kimbrough, J. W., McSorley, R. and Mitchell, D. J. (1994) Fungi associated with females and cysts of Heterodera glycines in a Florida soybean field. Journal of Nematology, 26, 296–303.

    PubMed  CAS  Google Scholar 

  • Chen, S. Y., Dickson, D. W. and Mitchell, D. J. (1996a) Population development of Heterodera glycines in response to mycoflora in soil from florida. Biological Control, 6, 226–31.

    Google Scholar 

  • Chen, S. Y., Dickson, D. W. and Mitchell, D. J. (1996b) Pathogenicity of fungi to eggs of Heterodera glycines. Journal of Nematology, 28, 148–58.

    PubMed  CAS  Google Scholar 

  • Ciancio, A. (1995) Phenotypic adaptations in Pasteuria spp nematode parasites. Journal of Nematology, 27, 328–38.

    PubMed  CAS  Google Scholar 

  • Ciancio, A., Bonsignore, R., Vovlas, N. and Lamberti, F. (1994) Host records and spore morphometrics of Pasteuria penetrans group parasites of nematodes. Journal of Invertebrate Pathology, 63, 260–67.

    Google Scholar 

  • Claridge, M. F. (1996) Biochemical approaches to understanding agricultural pests, in The Ecology of Agricultural Pests (eds W.O.C. Symondson and J.E. Liddell), Chapman and Hall, London, pp. 1–5.

    Google Scholar 

  • Cook, R and Evans, K. (1987) Resistance and tolerance, in Principles and Practice of Nematode Control in Crops (eds R. H. Brown and B. R. Kerry), Academic Press, Australia, pp. 179–766.

    Google Scholar 

  • Cook, R. J. and Baker, K. F. (1983) The Nature and Practice of Biological Control of Plant Pathogens. The American Phytopathological Society, St. Paul, Minnesota.

    Google Scholar 

  • Cooke, R. C. and Rayner, A. D. M. (1984) Ecology of Saprotrophic Fungi. Longman, London.

    Google Scholar 

  • Crump, D. H. (1987) Effect of time sampling, method of isolation and age of nematode on the species of fungi isolated from females of Heterodera schachtii and H. avenae. Revue de Nematologie, 10, 369–73.

    Google Scholar 

  • Crump, D. H. and Flynn, C. A. (1995) Isolation and screening of fungi for the biological control of potato cyst nematodes. Nematologica, 41, 628–38.

    Google Scholar 

  • Crump, D. H. and Irving, F. (1992) Selection of isolates and methods of culturing Verticillium chlamydosporium and its efficacy as a biological control agent of beet and potato cyst nematodes. Nematologica, 38, 367–74.

    Google Scholar 

  • Crump, D. H. and Kerry, B. R. (1981) A quantitative method for extracting resting spores of two nematophagus fungi, Verticillium chlamydosporium and Cylindrocarpon destructans. Nematologica, 32, 363–66.

    Google Scholar 

  • Crute, I. R. (1994) Gene-for-gene recognition in plant-pathogen interactions. Philosophical Transactions of the Royal Society London. Section B 346, 345–49.

    Google Scholar 

  • Curl, E.A. and Truelove, B. (1986) The Rhizosphere. Springer Verlag, Berlin and New York.

    Google Scholar 

  • Davies, K. G., Afolabi, P. and O’Shea, P. S. (1996) Adhesion of Pasteuria penetrans to the cuticle of root-knot nematodes (Meloidogyne spp) inhibited by fibronectin: a study of electrostatic and hydrophobic interactions. Parasitology, 112, 553–59.

    CAS  Google Scholar 

  • Davies, K. G., De Leij, F. A. A. M. and Kerry, B. R. (1991) Microbial agents for the biological control of plant-parasitic nematodes in tropical agriculture. Tropical Pest Management, 37, 303–20.

    Google Scholar 

  • Davies, K. G., Flynn, C. A., Laird, V. and Kerry, B. R. (1990) The life-cycle, population dynamics and host specificity of a parasite of Heterodera avenae, similar to Pasteuria penetrans. Revue de NĂ©matologie, 13, 303–9.

    Google Scholar 

  • Davies, K. G., Kerry, B. R. and Flynn, C. A. (1988) Observations on the pathogenicity of Pasteuria penetrans, a parasite of root-knot nematodes. Annals of Applied Biology, 112, 491–501.

    Google Scholar 

  • Davies, K. G., Laird, V. and Kerry, B. R. (1991) The motility, development and infection of Meloidogyne incognita encumbered with spores of the obligate hyperparasite Pasteuria penetrans. Revue de NĂ©matologie, 14, 611–18.

    Google Scholar 

  • Davies, K. G. and Redden, M. (1997) Diversity and partial characterisation of putative virulence determinants in Pasteuria penetrans, the hyperparasitic bacterium of root-knot nematodes (Meloidogyne spp.). Journal of Applied Microbiology, 83, 227–235.

    PubMed  CAS  Google Scholar 

  • Davies, K. G., Redden, M. and T. K. Pearson, (1994) Endospore heterogeneity in Pasteuria penetrans related to attachment to plant-parasitic nematodes. Letters in Applied Microbiology, 19, 370–73.

    Google Scholar 

  • Dinham, B. (1993) The Pesticide Hazard: A Global Health and Environmental Audit, Zed Books, London and New Jersey.

    Google Scholar 

  • Espanol, M., Verdejo-Lucas, S., Davies, K. G. and Kerry, B. R. (1997) Compatibility between Pasteuria penetrans and Meloidogyne populations. Biocontrol Science and Technology, 7, 219–230.

    Google Scholar 

  • Evans, K. (1995) Closing the gap between molecular biologists and traditional nematologists. Nematologica, 41, 385–94.

    Google Scholar 

  • Flor, H.H. (1956) The complementary genic systems in flax and flax rust. Advances in Genetics, 8, 29–54.

    Google Scholar 

  • Flor, H.H. (1971) The current status of the gene-for-gene concept. Annual Review of Phytopathology, 9, 275–96.

    Google Scholar 

  • Frank, S. A. (1994) Recognition and polymorphism in host-parasite genetics. Philosophical Transactions of the Royal Society London, Section B 346, 283–93.

    CAS  Google Scholar 

  • Frankland, J. C. (1992) Mechanisms of fungal succession, in The Fungal Community (eds G. C. Carrol and D. T. Wicklow), Marcel Dekker, New York, pp. 383–401.

    Google Scholar 

  • Gair, R., Mathias, P. L. and Harvey, P. N. (1969) Studies of cereal nematode populations and cereal yields under continuous or intensive culture. Annals of Applied Biology, 63, 503–12.

    Google Scholar 

  • Garrett, S. D. (1963) Soil Fungi and Soil Fertility. Pergamon Press, New York.

    Google Scholar 

  • Haldane, J. B. S. (1949) Disease and evolution. La Ricerca Scientifica Supplemento, 19, 1–11.

    Google Scholar 

  • Hay, F. S. and Skipp, R. A. (1993) Fungi and actinomycetes associated with cysts of Heterodera trifolii Goffart (Nematoda, Tylenchida) in pasture soils in New Zealand. Nematologica, 39, 376–84.

    Google Scholar 

  • Heijbroek, W. (1983) Some effects of fungal parasites on the population development of the beet cyst nematode (Heterodera schachtii Schm.) Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent, 48, 433–39.

    Google Scholar 

  • Himmelhoch, S., Kisiel, M. J. and Zuckerman, B. M. (1977) Caenorhabditis briggsae: electron microscope analysis of changes in negative charge density of the outer cuticle membrane. Experimental Parasitology, 41, 118–23.

    PubMed  CAS  Google Scholar 

  • Jaffee, B. A. (1993) Density-dependent parasitism in biological control of soilborne insects, nematodes, fungi and bacteria. Biocontrol Science and Technology, 3, 235–46.

    Google Scholar 

  • Jaffee, B. A., Muldoon, A. E. and Westerdahl, B. B. (1996) Failure of a mycelial formulation of the nematophagous fungus Hirsutella rhossiliensis to suppress the nematode Heterodera schachtii. Journal of Biological Control, 6, 340–46.

    Google Scholar 

  • Jaffee, B. A. Muldoon, A. E. and Tedford, E. C. (1992) Trap production by nematophagous fungi growing from parasitized nematodes. Phytopathology, 82, 615–20.

    Google Scholar 

  • Jaffee, B. A., Phillips, R., Muldoon, A. E. and Mangel, M. (1993) Density-dependent host pathogen dynamics in soil microcosms. Ecology, 73, 495–506.

    Google Scholar 

  • Kamra, A. and Dhawan, S. C. (1994) Effect of storage temperature on viability of Pasteuria penetrans spores infecting Heterodera avenae. Indian Journal of Nematology, 24, 116–19.

    Google Scholar 

  • Kerry, B. R. (1995) Ecological considerations for the use of the nematophagous fungus, Verticillium chlamydosporium, to control plant-parasitic nematodes. Canadian Journal of Botany, 73, 65–70.

    Google Scholar 

  • Kerry, B. R. (1993) The use of microbial agents for the biological control of plant parasitic nematodes, in Exploitation of Microorganisms (ed D Gareth Jones), Chapman and Hall, London, pp. 81–104.

    Google Scholar 

  • Kerry, B. R., (1975) Fungi and the decrease of cereal cyst-nematode populations in cereal monoculture. EPPO Bulletin, 5, 353–61.

    Google Scholar 

  • Kerry, B. R. and Bourne, J. M. (1996) The importance of rhizosphere interactions in the biological control of plant parasitic nematodes — a case study using Verticillium chlamydosporium. Pesticide Science, 47, 69–75.

    CAS  Google Scholar 

  • Kerry, B. R., Crump, D. H. and Mullen, L. A. (1980) Parasitic fungi, soil moisture and multiplication of the cereal cyst nematode, Heterodera avenae. Nematologica, 26, 57–68.

    Google Scholar 

  • Kerry, B. R., Crump, D. H. and Mullen, L. A. (1982a) Studies of the cereal cystnematode Heterodera avanae under continuous cereals, 1975–1978. II Fungal parasitism of nematode eggs and females. Annals of Applied Biology, 100, 489–99.

    Google Scholar 

  • Kerry, B. R., Crump, D. H. and Mullen, L. A. (1982b) Natural control of the cereal cyst nematode, Heterodera avanae Woll., by soil fungi at three sites. Crop Protection, 1, 99–109.

    Google Scholar 

  • Kerry, B. R., Kirkwood, I. A., Deleij, F. A. A. M, Barba, J., Leijdens, M. B. and Brookes, P.C. (1993) Growth and survival of Verticillium chlamydosporium goddard, a parasite of nematodes, in soil. Biocontrol Science and Technology, 3, 355–65.

    Google Scholar 

  • Kim, D. G., Riggs, R. D. and Kim, K. S. (1992) Ultrastructure of Heterodera glycines parasitized by Arkansas fungus-18. Phytopathology, 82, 429–33.

    Google Scholar 

  • Kim, D. G. and Riggs, R. D. (1995) Efficacy of the nematophagous fungus ARFL8 in alginate-clay pellet formulations against Heterodera glycines. Journal of Nematology, 27, 602–8.

    PubMed  CAS  Google Scholar 

  • Kim, D. G. and Riggs, R. D. (1991) Characteristics and efficacy of a sterile hyphomycete (ARFL8), a new biocontrol agent for Heterodera glycines and other nematodes. Journal of Nematology, 23, 275–82.

    PubMed  CAS  Google Scholar 

  • Lackey, B. A. Jaffee, B. A. and Muldoon, A. E. (1994) Effect of nematode inoculum on suppression of root-knot and cyst nematodes by the nematophagous fungus Hirsutella rhossiliensis. Phytopathology, 84, 415–20.

    Google Scholar 

  • Lackey, B. A., Jaffee, B. A. and Muldoon, A.E. (1992) Sporulation of the nematophagous fungus Hirsutella rhossiliensis from hyphae produced in vitro and added to soil. Phytopathology, 82, 1326–30.

    Google Scholar 

  • Lackey, B. A. Muldoon, A. E. and Jaffee, B. A. (1993) Alginate pellet formulation of Hirsutella rhossiliensis for biological control of plant-parasitic nematodes. Biological Control, 3, 155–60.

    Google Scholar 

  • Last, F. T., Mason, P. A., Wilson, J. and Deacon, J. W. (1983) Fine roots and sheathing mycorrhizas: their formation, function and dynamics. Plant and Soil, 71, 9–21.

    Google Scholar 

  • Last, F. T., Mason, P. A., Ingleby, K. and Fleming, L. V. (1984) Succession of fruit bodies of sheathing mycorrhizal fungi associated with Betula pendula. Forest Ecology and Management, 9, 229–234.

    Google Scholar 

  • Linford, M. B. (1937) Stimulated activity of natural enemies of nematodes. Science, 85, 123–24.

    PubMed  CAS  Google Scholar 

  • Linford, M. B., Yap, F. and Oliveira, J. M. (1938) Reduction of soil populations of the root-knot nematode during decomposition of organic matter. Soil Science, 45, 127–41.

    Google Scholar 

  • Mason, P. A., Last, F. T., Wilson, J., Deacon, J. W., Fleming, L. V. and Fox, F. M. (1988) Fruiting and succession of ectomycorhizal fungi, in Fungal Infection of Plants (eds G.F. Pegg and P.G. Ayres), Cambridge University Press, New York, pp 253–68.

    Google Scholar 

  • Mateille, T., Duponnois, R. and Diop, M. T. (1995) Influence of abiotic soil factors and host-plant on the infection of phytoparasitic nematodes of the genus Meloidogyne by the actinomycete parasitiod Pasteuria penetrans. Agronomie, 15, 581–91.

    Google Scholar 

  • May, R.M. and Hassell, M.P. (1988) Population dynamics and biological control. Philosophical Transactions of the Royal Society London, Section B, 318, 129–69.

    Google Scholar 

  • Maynard Smith, J. (1986) The Problems of Biology. Oxford University Press.

    Google Scholar 

  • Meyer, S. L. F. and Meyer, R. J. (1992) Induction of increased benomyl tolerance in Verticillium lecanii, a fungus antagonistic to plant-parasitic nematodes. Journal of the Helminthological Society of Washington, 59, 237–39.

    Google Scholar 

  • Meyer, S. L. F. and Huettel, R. N. (1996) Application of a sex pheromone, pheromone analogs, and Erticillium lecanii for management of Heterodera glycines. Journal of Nematology, 28, 36–

    PubMed  CAS  Google Scholar 

  • Meyer, S. L. F. and Meyer, R. J. (1996a) Greenhouse studies comparing strains of the fungus Verticillium lecanii for activity against the nematode Heterodera glycines. Fundamental and Applied Nematology, 19, 305–8.

    Google Scholar 

  • Meyer, S. L. F. and Meyer, R. J. (1996b) Survival of the nematode-antagonistic fungus Verticillium lecanii in alginate prills. Nematologica, 42, 114–23.

    Google Scholar 

  • Meyer, S. L. F. and Meyer, R. J. (1995) Effects of a mutant strain and a wild-type strain of Verticillium lecanii on Heterodera glycines populations in the greenhouse. Journal of Nematology, 27, 409–17.

    PubMed  CAS  Google Scholar 

  • Meyer, S. L. F., Sayre, R. M. and Huettel, R. N. (1991) Benomyl tolerance of 10 fungi antagonistic to plant-parasitic nematodes. Journal of Nematology, 23, 402–8.

    PubMed  CAS  Google Scholar 

  • Noel, G. R. and Stanger, B. A. (1994) First report of pasteuria sp attacking Heterodera glycines in North America. Journal of Nematology, 26, 612–15.

    PubMed  CAS  Google Scholar 

  • Powers, T. (1992) Biological control of plant parasitic nematodes: progress, problems and prospects. Parasitology Today, 8, 320.

    Google Scholar 

  • Sayre, R. M., Wergin, W. P., Schmidt, J. M. and Starr, M. P. (1991) Pasteuria nishizawae sp-nov, a mycelial and endospore-forming bacterium parasitic on cyst nematodes of genera Heterodera and Globodera. Research in Microbiology, 142, 551–64.

    PubMed  CAS  Google Scholar 

  • Segers, R., Butt, T. M., Kerry, B. R., Beckett, A. and Peberdy, J.F. (1996) The role of the proteinase VCP1 produced by the nematophagous Verticillium chlamydosporium in the infection process of nematode eggs. Mycological Research, 100, 421–28.

    CAS  Google Scholar 

  • Segers, R. Butt, T. M., Keen, J.N., Kerry, B. R. and Peberdy, J.F. (1995) The subtilisins of invertebrate mycopathogens Verticillium chlamydosporium and Metarhizium anisopliae are serologically and functionally related. FEMS Microbiology Letters, 126, 227–32.

    PubMed  CAS  Google Scholar 

  • Segers, R. Butt, T. M., Kerry, B. R. and Peberdy, J. F. (1994) The nematophagous fungus Verticillium chlamydosporium produces a chymoelastase-like protease that hydrolyses host nematode proteins in situ. Microbiology, 140, 2715–23.

    PubMed  CAS  Google Scholar 

  • Sharma, S. B. and Davies, K. G. (1996a) Characterization of Pasteuria isolated from Heterodera cajani using morphology, pathology and serology of endospores. Systematic and Applied Microbiology, 19, 106–12.

    Google Scholar 

  • Sharma, S. B. and Davies, K. G. (1996b) Comparison of two sympatric Pasteuria populations isolated from a tropical vertisol soil. World Journal of Microbiology and Biotechnology, 12, 361–66.

    Google Scholar 

  • Siddiqui, Z. A. and Mahmood, I. (1995) Biological control of Heterodera cajani and Fusarium udum by Bacillus subtilis, Bradyrhizobium japonicum and Glomus fasciculatum on pigeonpea. Fundamental and Applied Nematology, 18, 559–66.

    Google Scholar 

  • Singh, B. and Dhawan, S. C. (1990) A new bacterial strain of Pasteuria penetrans its host range and effect of temperature on spore attachment to second-stage juveniles of pigeon pea cyst nematode Heterodera cajani. Indian Journal of Nematology, 20, 161–66.

    Google Scholar 

  • Singh, M., Sharma, S. B. and Sharma, R. (1998) Fusarium solani — a natural parasite of pigeonpea cyst nematode, Heterodera cajani. Indian Journal of Nematology, 26, 189–196.

    Google Scholar 

  • Spaull, V. W. (1984) Observations on Bacillus penetrans infecting meloidogyne in sugar cane fields in South Africa. Revue de Nematologie, 7, 277–82.

    Google Scholar 

  • Stein, B. and Grabert, D. (1992) Isolation of fungi from Heterodera avenae Wollenberger cysts and eggs and their pathogenicity for nematodes. Nematologica, 38, 375–84.

    Google Scholar 

  • Stiles, C. M., Glawe, D. A., Noel, G. R. and Pataky, J. K. (1993) Reproduction of Heterodera glycines on soybean in nonsterile soil infested with cyst-colonizing fungi. Nematropica, 23, 81–89.

    Google Scholar 

  • Stirling, G. R. (1991) Biological Control of Plant Parasitic Nematodes, CAB International, Wallingford, UK.

    Google Scholar 

  • Stirling, G. R. (1985) Host specificity of Pasteuria penetrans within the genus Meloidogyne. Nematologica, 31, 203–9.

    Google Scholar 

  • Stirling, G. R. and White, A. M. (1982) Distribution of a parasite of root-knot nematodes in South Australian vineyards. Plant Disease, 66, 52–53.

    Google Scholar 

  • Stone, A. R. (1979) Co-evolution of nematodes and plants. Symbolae Botanicae Upsaliensis, 22, 46–61.

    Google Scholar 

  • Tedford, E. C. and Jaffee, B. A. (1995) In vitro parasitism of Rotylenchus robustus by isolates of Hirsutella rhossiliensis. Journal of Nematology, 27, 486–89.

    PubMed  CAS  Google Scholar 

  • Tedford, E. C., Jaffee, B. A. and Muldoon, A. E. (1992) Effect of soil moisture and texture on transmission of the nematophagous fungus Hirsutella rhossiliensis to cyst and root-knot nematodes. Phytopathology, 82, 1002–7.

    Google Scholar 

  • Tedford, E. C., Jaffee, B. A. and Muldoon, A. E. (1995a) Effect of temperature on infection of the cyst nematode Heterodera schachtii by the nematophagous fungus Hirsutella rhossiliensis. Journal of Invertebrate Pathology, 66, 6–10.

    Google Scholar 

  • Tedford, E. C., Jaffee, B. A. and Muldoon, A. E. (1995b) Suppression of the nematode Heterodera schachtii by the fungus Hirsutella rhossiliensis as affected by fungus population density and nematode movement. Phytopathology, 85, 613–17.

    Google Scholar 

  • Tedford, E. C., Jaffee, B. A., Muldoon, A. E., Anderson, C. E. and Westerdahl, B. B. (1993) Parasitism of Heterodera schachtii and meloidogyne-javanica by Hirsutella rhossiliensis in microplots over 2 growing seasons. Journal of Nematology, 25, 427–33.

    PubMed  CAS  Google Scholar 

  • Thomason, I. J. (1987) Challenges facing nematology: environmental risks with nematicides and the need for new approaches, in Vistas on Nematology (eds J. A. Veech and D. W. Dickson), Society of Nematologists, Hyattsville, Maryland, pp. 469–76.

    Google Scholar 

  • Thompson, J. N. and Burdon, J. J. (1992) Gene-for-gene coevolution between plants and parasites. Nature, 360, 121–25.

    Google Scholar 

  • Tribe, H. T. (1957) Ecology of micro-organisms in soils as observed during their development upon buried cellulose film, in Microbial Ecology (eds R. E. O. Williams and C. C. Spicer), Cambridge University Press, New York, pp. 287–98.

    Google Scholar 

  • Trudgill, D. L. (1991) Resistance to and tolerance of plant parasitic nematodes in plants. Annual Review of Phytopathology, 29, 167–92.

    Google Scholar 

  • Uziel, A. and Sikora, R. A. (1992) Use of nontarget isolates of the entomopathogen Verticillium lecanii (Zimm) viegas to control the potato cyst nematode, Globodera pallida (Stone). Nematologica, 38, 123–30.

    Google Scholar 

  • Vanderplank, J. E. (1978) Genetic and Molecular Basis of Plant Pathogenesis. Springer-Verlag, Berlin, Heidelberg, New York.

    Google Scholar 

  • Velivis, H. and Kemp, P. (1995) Suppression of potato cyst nematode root penetration by the endoparasitic nematophagous fungus Hirsutella rhossiliensis. European Journal of Plant Pathology, 102, 115–122.

    Google Scholar 

  • Verdejo-Lucas, S. (1992) Seasonal populational fluctuations of Meloidogyne spp. and the Pasteuria penetrans group in Kiwi Orchards. Plant Disease, 76, 1275–79.

    Google Scholar 

  • Zadoks, J. C. and Schein, R. D. (1979) Epidemiology and Plant Disease Management, Oxford University Press, New York, Oxford.

    Google Scholar 

  • Zedan, H. (1994) Pest organisms: numbers, ecosystem impact, and developing country needs, in The Identification and Characterisation of Pest Organisms (ed. D. L. Hawksworth), CAB International, Wallingford, UK, pp. 17–34.

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Davies, K.G. (1998). Natural parasites and biological control. In: Sharma, S.B. (eds) The Cyst Nematodes. Springer, Dordrecht. https://doi.org/10.1007/978-94-015-9018-1_15

Download citation

  • DOI: https://doi.org/10.1007/978-94-015-9018-1_15

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-4021-3

  • Online ISBN: 978-94-015-9018-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics