Nematophagous Fungi

 

Koon-Hui Wang, Robert McSorley

University of Florida, Department of Entomology and Nematology, P.O. Box 110620, Gainesville, FL 32611-0620, U.S.A.

(Last updated September 2003)

 


* What are nematophagous fungi?

* A key to commonly occurring nematophagous fungi

* Ecology of nematophagous fungi

* Protocol to quantify nematophagous fungi

* Examples of use of cover crop for enhancement of nematophagous fungi

* Factors affecting cover crops for nematophagous fungi

* Duration of cover crop for enhancing nematophagous fungi in field conditions

* Selected references

 

What are nematophagous fungi?

Nematophagous fungi are fungi that feed on nematodes. These fungi can be fungal egg-parasites, nematode-trapping fungi that capture nematodes using modified hyphal traps, or endoparasites that parasitize the nematode by means of small conidia or zoospores. There are various ways for soil-borne fungi to suppress nematode multiplication. A detailed review of fungi as biocontrol agents against plant-parasitic nematodes has been published (Kerry and Jaffee, 1997). In summary, there are five mechanisms that fungi use to suppress nematodes. Some of these interactions are direct whereas others are indirect. The direct mechanism is performed by 1) fungi that feed on nematodes directly, known as nematophagous fungi; fungi interact with nematodes in an indirect manner by several mechanisms including: 2) fungi that kill nematodes by mycotoxin (Barron and Thorne, 1987) or 3) through the destruction of the feeding sites of sedentary nematodes in roots (Glawe and Stiles, 1989); 4) fungi that are nonpathogenic to plants, but compete with nematodes in roots and significantly reduce nematode multiplication (Sikora, 1992). Many of these fungi are used as potential nematode biocontrol agents; 5) Mycorrhizal fungi improve the growth of nematode infected plants and may also affect nematode development (Hussey and Roncadori, 1982).

 

According to a survey of nematophagous fungi in Ireland by Gray (1983), nematophagous fungi were found in all of the habitats examined, among which, permanent pasture, coniferous leaf litter, and coastal vegetation had the most frequent incidence of nematophagous fungi. Other habitats examined by Gray included coniferous leaf litter, old and partly revegetated dung, permanent grassland pasture, cultivated land, moss cushions, decaying vegetation and compost, and peatland (Gray, 1983). In addition, many other studies (Barron, 1977) also supported the hypothesis that nematophagous fungi are widely distributed and have great potential to be explored as biocontrol agents.

 

 However, as stated by Kerry (1988): “The successful introduction of such an agent depends on whether a suitable niche for the microorganism exists or can be created and until we know much more about the factors that affect the activity of nematophagous fungi in soil, their full potential as control agents for nematodes will not be realized.”

 

 

This article summarizes groups of nematophagous fungi according to their feeding habits:

 

A)   Nematode-trapping fungi

Facultative fungi that form trapping structure to trap nematodes. There are 6 types of traps reported by Barron (1977).

*  adhesive hyphae:

                 eg. Zygomycotina

                        Stylopage

                        Cystopage

*  adhesive traps:

                      eg. Deuteromycota

                             Monacrosporium cionopagum (branches)

                             M. ellipsosporum (knobs)

  Arthrobotrys oligospora (networks)

*  non-adhesive traps

                      eg. Deuteromycota

  Arthrobotrys dactyloides (constricting ring)

  Dactylella leptospora (non-constricting ring)

 

B)    Facultative parasitic fungi attacking sedentary stages of nematodes (Kerry and Jaffee, 1997)

These are facultative fungi that are commonly soil saprophytes, and are opportunistic fungi isolated from the sedentary stages (female and egg stages) of sedentary nematodes such as Heterodera, Globodera, and Meloidogyne. They do not form specialized infection structures except appressoria. They can survive and proliferate in soil in the absence of nematodes.

                 eg. Hyphomycotina

                          Acremonium

                          Cylindrocarpon

                          Fusarium

                          Paecilomyces

                          Verticillium

 

C)    Endoparasitic fungi (Kerry and Jaffee, 1997)

These are obligate parasitic fungi that have limited growth in soil outside the colonized nematode cadaver.

*  They can infect vermiform nematodes by producing adhesive spores attached to cuticle of passing nematodes.

            eg. Hyphomycotina

                      Hirsutella rhossiliensis

                      Drechmeria coniospora

                      Verticillium spp.

*  Some can infect vermiform nematodes by producing conidia spores that can be ingested by nematodes.

                      Harposporium anguillulae

*  Some can infect vermiform nematodes by producing motile zoospores that encyst on the nematode’s surface.

            eg. Oomycota

                      Myzocytium spp.

                      Lagenidium spp.

                 Chytridiomycota

                      Catenaria anguillulae

*  Some can infect sedentary nematodes when the nematodes were exposed on the root surface.

            eg. Oomycota

                      Nematophthora gynophila

 

A Key To Commonly Occurring Nematophagous Fungi 5

 

Ecology of Nematophagous Fungi

 

An ecology study of nematophagous fungi conducted by Gray (1985) revealed that different types of nematophagous fungi have different edaphic preferences. The saprophytic NTF (formed adhesive nets) are found in soil with low organic matter and low moisture due to their saprophytic nature. When nutrients or moisture condition improved, the saprophytic NTF are able to compete with other soil organisms by feeding on the expanding nematode population. In contrast, NTF that form rings are more common in soil with high organic matter and moisture. Endoparasitic fungi that produce conidia are strongly influenced by organic matter. While most of the NTF (except those that formed adhesive branches) are not affected by nematode densities, endoparasitic fungi that form ingestive spores are nematode-density dependent. In general, the conidia-forming endoparasites were isolated from samples with comparatively high soil moisture and low pH. Little is known about edaphic preference of the nematophagous fungi with unmodified adhesive hyphae, except that they are more frequently recovered from soils with higher pH. Table 1-1 summarizes soil factors affecting different nematophagous fungi.

 

Table 1. Effect of soil edaphic factors on distribution of nematophagous fungi (Gray, 1985).

 

Nematophagous fungi

Organic matter

pH

Moisture

Nematode densities

Nematode-trapping

NSz

low

NS

NS

         net

lowy

low

low

NS

         ring

highx

low

high

NS

        adhesive hyphae

NS

high

NS

NS

        adhesive branch

NS

NS

NS

high

        adhesive knobs

NS

low

NS

NS

Endoparasites

high

low

high

high

 

zNS = effects of the edaphic factors is not significant.

ylow = lower value of the edaphic factor is preferred by the group of nematophagous fungi.

xhigh = higher value of the edaphic factor is preferred by the group of nematophagous fungi.

 

Base on their ecological preferences, nematode-trapping fungi (NTF) are separated into two groups: saprophytic and parasitic NTF (Cooke, 1963). 

*   Saprophytic NTF—form 3-dimensional-network traps in response to the presence of nematodes. Under low nematode population densities, they remain saprophytic. Therefore, they are regarded as inefficient nematode-trappers.

*   Parasitic NTF—have low saprophytic ability, but form traps spontaneously. This group consists of NTF that form constricting rings, adhesive branches and are more effective nematode trappers than the saprophytic NTF (Jasson, 1982).

 

 

Further information on nematode-antagonistic fungi can be obtained through:

http://sacs.cpes.peachnet.edu/nemabc/

http://www.area.ba.cnr.it/~e085ac01/bkfair3444.html

http://www.ag.auburn.edu/bci/nematolo.htm

 

 

Protocol to Quantify Nematophagous Fungi

Examples of Use of Cover Crop for Enhancement of Nematophagous Fungi

Factors affecting Cover Crops for Nematophagous Fungi

Duration of Cover Crop for Enhancing Nematophagous Fungi in Field Conditions

 

Selected References

*  Alexander, M. 1982. Most probable number method for microbial populations. Pp. 815-820. A. L. Page (ed.). In Methods of soil analysis, part 2. Chemical and microbiological properties. Agronomy Monograph No. 9 (2 nd edition). ASA-SSSA, Madison, Wisconsin.

*  Barron, G. L. 1977. The nematode-destroying fungi. Canadian Biological Publications. Ontaria, Canada. 140 pp.

*  Barron, G. L., and R. G. Thorne. 1987. Destruction of nematodes species of Pleurotus. Canadian Journal of Botany 65: 774-778.

*  Cooke, R. C. 1963. Ecological characteristics of nematode-trapping fungi Hyphomycetes. Annual Review of Applied Biology 52: 431-437.

*  Cooke, R. C. and B. E. S. Godfrey. 1964. A key to the nematode-destroying fungi. Trans. Brit. Mycol. Soc. 47: 61-74.

*  Esser, R. P. 1976. Haptoglossa heterospora Drechsler, a fungus parasite of Florida nematodes. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 23. 2 pp.

*  Esser, R. P. and T. S. Schubert. 1981. Fungi that entrap and assimilate nematodes employing mucilaginous, hyphal, 3-dimensional traps. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 80. 3 pp.

*  Esser, R. P. and T. S. Schubert. 1982. Fungi employing mucilaginous, undifferentiated hyphae that entrap and assimilate nematodes. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 86. 2 pp.

*  Esser, R. P. and T. S. Schubert. 1982. Fungi employing mucilaginoushyphal, sessile, or stalked globose cells to entrap nematodes. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 94. 4 pp.

*  Esser, R. P. and T. S. Schubert. 1983. Fungi that entrap nematodes by mucilaginous droplets borne on glandular cells. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 95. 2 pp.

*  Esser, R. P. and T. S. Schubert. 1983. Fungi that utilize zoospores to parasitize nematodes. Fla.Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 101. 4 pp.

*  Esser, R. P. 1987. Biology of Arthrobotrys dactyloides, a fungal parasite of nematodes. Soil and Crop Science Society of Florida 47: 243-249.

*  Esser, R. P., N. E . El-Gholl, and M. Price. 1990. Biology of Dactylella megalospora Drechs., a nematophagous fungus. Crop Science Society of Florida 50: 173-180.

*  Esser, R. P. and T. S. Schubert. 1983. Fungi that entrap nematodes utilizing non-constricting rings. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 103. 2 pp.

*  Esser, R. P. and T. S. Schubert. 1991. Fungi that entrap and assimilate nematodes by employing constricting rings. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 192. 3 pp.

*  Esser, R. P. and N. E . El-Gholl. 1992. Harposporium, a fungus that parasitizes and kills nematodes utilizing conidia swallowed by or sticking to its prey. Fla. Dept. Agric. & Consumer Services, Division of Plant Industry. Nematology Circular No. 200. 6 pp.

*  Glawe, D. A., and C. M. Stiles. 1989. Colonization of soybean roots by fungi isolated from cysts of Heterodera glycines. Mycologia 81: 797-799.

*  Gray, N. F. 1985. Ecology of nematophagous fungi:distribution and habitat. Annual Review of Applied Biology 102: 501-509.

*  Gray, N. F. 1985. Ecology of nematophagous fungi: effect of soil moisture, organic matter, pH and nematode density on distribution. Soil Biol. Biochem. 17: 499-507.

*  Hussey, R. S., and R. W. Roncadori. 1982. Vesicular-arbuscular mycorrhizae may limit nematode activity and improve plant growth. Plant Disease 66: 9-14.

*  Jaffee, B. A., D. R. Strong, and A. E. Muldoon. 1996. Nematode-trapping fungi of a natural shrubland: Tests for food chain involvement. Mycologia 88: 554-564.

*  Jasson, H. B. 1982. Predacity by nematophagous fungi and its relation to the attraction of nematodes. Microbial Ecology 8: 233-240.

*  Kerry, B. 1988. fungal parasites of cyst nematodes. Agriculture, ecosystems, and environment 24:293-305.

*  Kerry, B. R., and B. A. Jaffee. 1997. Fungi as biological control agents for plant parasitic nematodes. in The Mycota K. Esser and P. A. Lemke, eds., Vol. IV, pp. 204-218. Springer, Verlag Berlin Heidelberg.

*  Sikora, R. A. 1992. Management of the antagonistic potential in agricultural ecosystems for the biological control of plant parasitic nematodes. Annual Review of Phytopathology 30: 245-247.

*  Wang, K.-H., B. S. Sipes, and D. P. Schmitt. 2001. Suppression of Rotylenchulus reniformis by Crotalaria juncea, Brassica napus, and Tagetes erecta. Nematropica 31: 235-249.

*  Wang, K.-H., B. S. Sipes, and D. P. Schmitt. 2002. Management of Rotylenchulus reniformis in pineapple, Ananas comosus, by intercycle cover crops. J. Nematol. 34: 106-114.

*  Wang, K.-H., B. S. Sipes, and D. P. Schmitt. 2003. Suppression of Rotylenchulus reniformis enhanced by Crotalaria juncea amendment in pineapple field soil. Agri. Eco. Environ. 94: 197-203.

*  Woodring, J. L. and H. K. Kaya. 1988. Steinernematid and Heterorhabditid nematodes: a handbook of techniques. Southern Cooperative Series Bulletin 331. Arkansas Agricultural Experimental Station, Fayetteville, Arkansas. 30 pp.