Australasian Association of Nematologists

Background

Although the use of nematophagous fungi as ‘a new approach to the eelworm problem’ was advocated in C.L. Duddington’s (1957) The Friendly Fungi, their application to plant pathogenic nematodes has not proved easy. In 1991 Graham Stirling (1991 p9) wrote ‘there are still no widely accepted examples of the contrived use of an antagonist to control a plant parasitic nematode’, and neither Evans et al. (1993) nor Perry & Wright (1998) described practical examples. While fungal pathogens of cyst-forming nematodes have provided more fertile ground (e.g. Kerry, 1995; Bourne & Kerry, 1999; Pyrowolakis et al., 1999) that area, like the use of nematode-trapping fungi for migratory stages, has not seen any generalised, practical application. In population terms, the problem is one of dispersing, and maintaining, adequate numbers of infective propagules of the nematophagous agent throughout the potential range of the target species.

Practical use of entomopathogenic nematodes has been more successful, but according to Kondo & Kaya (1998: p77) "... although nematode infection may successfully occur, the insect cadavers do not always produce nematode progeny, and the nematodes fail to establish and recycle in the soil environment." "Reapplication is often needed," and "... their use will be restricted to high value crops or to areas where chemical pesticides cannot be used due to environmental or human health concerns."

In both these groups of potential biological control agents, small populations are present in the environment but successive, inundative releases appear to be needed for successful biological control. That is, to over-ride the barriers which have evolved.

The Duddingtonia flagrans story to date

Duddingtonia flagrans is a predacious fungus for which isolations have been reported from the environment in Australia (NSW, Queensland, WA, SA), Canada (Ontario, Nova Scotia), England, Denmark, France, India, Malaysia, Mexico, Russia and the USA (California). Some systematists place D. flagrans in the genus Arthrobotrys, a widely studied genus of the nematophagous hyphomycetes. They trap nematodes by means of specialised hyphal structures. D. flagrans forms adhesive three-dimensional hyphal nets in which nematodes are trapped, and produces large numbers of thick walled resting spores (chlamydospores).

D. flagrans can be cultured on appropriate substrates, the chlamydospores extracted and fed to sheep, cattle, horses and other grazing animals by incorporation with various feed supplements. The chlamydospores pass through the intestinal tract, apparently unscathed, and germinate once the faecal material is deposited. The resulting mycelium with its ‘traps’ has proved effective in reducing the number of ‘infective larvae’ of gastro-intestinal nematodes which survive to migrate to herbage and thence to re-infect grazing animals. An introductory account of such applications of nematophagous fungi is given by Larsen & Faedo (1998).

In a grazing trial in New South Wales, delivery of D. flagrans to sheep via salt-licks provided control of gastro-intestinal nematodes comparable with that from a conventional drenching regime (Dick, 1996). There are several publications describing successful control of nematode parasites of calves, cattle, horses and sheep. (e.g. Wolstrup et al., 1994; Dick, 1996; Fernández et al., 1997, 1999). In August and September 1999, I visited trials using D. flagrans for control of gastro-intestinal nematodes of sheep and cattle presently being conducted in Denmark and Sweden.

Systems for delivering chlamydospores to grazing animals have to be developed for a range of farming systems and the efficacy of parasite control confirmed under diverse climates, stock management and parasite burdens. However, use of D. flagrans to overcome both environmental concerns about anthelmintic use and the rapidly emergence of nematode resistance to the three currently used families of anthelmintics certainly looks promising.

• If the trapping is essentially a physical, density-dependent process, as long as chlamydospores continue to be administered, it seems that significant reduction of ‘infective larvae’ on herbage and thus of parasite burden will continue to be achieved.

• Inclusion in a livestock management regime should permit relaxation of the parasite control component of grazing patterns that were part of farm management before the advent of drenches.

• Duddingtonia could affect populations of other nematodes and organisms. A study of the New South Wales trial mentioned above showed no detectable changes in the taxonomic or functional composition of the soil nematode fauna during the first year of that trial (Yeates et al., 1997). Such studies need to be repeated under different soil and grazing regimes. As such trials will in effect normally be on sites with a history of drench use, it will be necessary to distinguish between those effects due to application of Duddingtonia and those due to the withdrawal of drenches.

• That D. flagrans has already been reported from 10 countries suggests that it is already widespread in the environment and that its use as a biocontrol agent is unlikely to have any additional impact on non-target organisms.

• As long as repeated inundative release is required there seems little potential problem.

• If farm management practices are modified to achieve ‘natural on-farm cycling’ of D. flagrans, those conditions are likely to be so specific that they do not present an environmental risk. Any ‘escape’ would presumably just merge into the low-level population already present.

• Successful biological control can be achieved when resistant propagules (chlamydospores) are delivered (per os), thoroughly mixed with the media (in the gastro-intestinal tract) and germinate in the medium (dung) before competing saprophytic fungi arrive.

• Perhaps, the ‘thermal treatment’ in the gut puts D. flagrans at a temporary competitive advantage in organic-rich substrates. Manipulation of the microflora in seedbeds and rooting media may be worth investigating. Although it has not yet been reported from mineral soils, incorporation of D. flagrans chlamydospores into pasteurised propagating mix could be a starting point.

Bourne, J. M.; Kerry, B. R. 1999: Effect of host plant on the efficacy of Verticillium chlamydosporium as a biological control agent of root-knot nematodes at different nematode densities and fungal application rates. Soil Biology and Biochemistry 31: 75–84.

Dick, A. 1996: New weapon in fight against sheep parasites. CSIRO Rural Research 171: 13–15.

Duddington, C. L. 1957: The friendly fungi – a new approach to the eelworm problem. Faber and Faber, London. 188 p.

Evans, K., Trudgill, D. L. & Webster, J. M. (eds) 1993: Plant Parasitic Nematodes in Temperate Agriculture. CAB International, Wallingford, 648 p.

Fernández, A. S.; Larsen, M.; Nansen, P.; Grønvold, J.; Henriksen, S. A.; Wolstrup, J. 1997: Effect of the nematode-trapping fungus Duddingtonia flagrans on the free-living stages of horse parasitic nematodes: a plot study. Veterinary Parasitology 73: 257–266.

Fernández, A. S.; Larsen, M.; Henningsen, E.; Nansen, P.; Grønvold, J.; Bjørn, H.; Wolstrup, J. 1999: Effect of Duddingtonia flagrans against Ostertagia ostertagi in cattle grazing at different stocking rates. Parasitology 119: 105–111.

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 (supplement): 65–70.

Kondo, E., Kaya, H. K. 1998: Recent development of biological control by beneficial nematodes: synopsis and discussion. Japanese Journal of Nematology 28 (special issue): 75–78.

Larsen, M., Faedo, M. 1998: Nematophagous fungi, new agents for biological control of nematode parasites of livestock – ecology, identification and cultivation. Pp 15–22 in: Biological control of gastro-intestinal nematodes or ruminants using predacious fungi. FAO Animal Production and Health Paper 141, 94 pp. (FAO, Rome)

Perry, R. N. & Wright, D. J. (eds) 1998: Physiology and Biochemistry of Free-living and Plant-parasitic nematodes. CAB International, Wallingford, 438 p.

Pyrowolakis, A.; Schuster, R. P.; Sikora, R. A. 1999: Effect of cropping pattern and green manure on the antagonistic potential and the diversity of egg pathogenic fungi in fields with Heterodera schachtii infection. Nematology 1: 165–171.

Stirling, G. R. 1991: Biological control of plant parasitic nematodes: progress, problems and prospects. CAB International, Wallingford, 282 p.

Wolstrup, J.; Grønvold, J., Henriksen, S. A.; Nansen, P.; Larsen, M., Bøgh, H. O.; Ilsøe, B. 1994: An attempt to implement the nematode-trapping fungus Duddingtonia flagrans in biological control of trichostrongyle infections of first year grazing calves. Journal of Helminthology 68: 175–180.

Yeates, G. W.; Waller, P. J.; King, K. L. 1997: Soil nematodes as indicators of the effect of management of grasslands in the New England Tablelands (NSW): effect of measures for control of parasites of sheep. Pedobiologia 41: 537–548.