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Biocontrol: Fungi As Nematode Control Agents

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Biocontrol: Fungi As Nematode Control Agents Biocontroh Fungi as Nematode Control Agents 1 R. Mankau 2 Abstract: The fungal antagonists of nematodes consist of a great variety of organisms belonging to widely divergent orders and families of fungi. They include the nematode-trapping fungi, endoparasitic fungi, parasites of nematode eggs and cysts, and fungi which produce metabolites toxic to nematodes. The diversity, adaptations, and distribution of nematode-destroying fungi and taxonomic problems encountered in their study are reviewed. The importance of nemato- phagous fungi in soil biology, with special emphasis on their relationship to populations of plant- parasitic nematodes, is considered. While predacious fungi have long been investigated as possible biocontrol agents and have often exhibited spectacular results in vitro, their performance in field studies has generated little enthusiasm among nematologists. To date no species has demonstrated control of any plant pest to a degree achieved with nematicides, but recent studies have provided a much clearer concept of possibilities and problems in the applied use of fungal antagonists. The discovery of new species, which appear to control certain pests effectively under specific conditions, holds out some promise that fungi may be utilized as alternatives to chemical control after a more thorough and expanded study of their biology and ecology. Key Words: Nematode- trapping fungi, nematode-destroying fungi, nematode egg parasites, nematode antagonists, nema- tode parasites, nematophagous fungi. The fungal antagonists of nematodes cause of the complexities of the soil habitat. consist of a great variety of organisms which Specialized techniques are required to ex- include the nematode-trapping or preda- tract, count, and isolate the fungal antago- cious fungi, endoparasitic fungi, parasites of nists, and many of the fungi concerned are nematode eggs, parasites of nematode cysts, obligate parasites or do not sporulate read- and fungi which produce metabolites toxic ily. to nematodes. It is remarkable that fungi Nematode-destroying fungi play a major belonging to widely divergent orders and role in recycling the carbon, nitrogen, and families occur in each of these groups. Pre- other important elements from the rather dacious, parasitic, and biochemical relation- substantial biomass of nematodes which ships with nematodes have evolved among browse on microbial primary decomposers. almost all major groups of soil fungi from Virtually every population expansion of the Phycomycetes to the Basidiomycetes. microbivorous nematodes occurring in the Considering the long co-evolution of nema- soil is accompanied by epizootics of fungal todes and fungi which obviously occurred in antagonists. Thus, fungi help convert the the close confines of the soil habitat, it is reservoir of materials in the rather extensive not surprising that a great variety of inter- nematode biomass back into microbial bio- relationships have developed between tlle mass, making basic materials available to two groups. A complete and readable ac- plants. Phytophagus nematodes, migrating count of these interesting organisms was in soil to new host plants or deprived of recently published in a small book on the proper hosts, face survival in an environ- nematode-destroying fungi by G. L. Barron ment abundantly populated with fungal (4). enemies. Once within plant tissue they are It is important to recognize the fact that probably isolated from most antagonists. fungi continuously destroy nematodes in The attention of investigators is often virtually all soils. Microbial and fungal con- focused on plant-parasitic nematodes. How- trol of nematodes is of great biological im- ever, other types which are often far more portance. In some circumstances it may be numerous have very important roles in the of considerable economic importance. How- biology of soil. It is with these groups of ever, we are presented with great technical nematodes that many, if not most, of the problems in the observation and assessment nematode-destroying fungi interact. Some of the importance of these organisms be- fungus species, for example, have spores which must be ingested by the nematode Received for publication 19 December 1979. host. These spores then germinate in the 1Symposium paper presented at the annual meeting of the Society of Nematologists, Salt Lake City, Utah, 23-26 esophagus to develop and consume the nem- July 1979. atode (1). Such fungi generally have no rela- 2Professor of Nematology, Department of Nematology, University of California, Riverside, CA 92521. tionship with plant-parasitic nematodes 244 Fungal Control of Nematodes: Mankau 245 which feed through a stylet whose aperture there is no need to redescribe them here, but is too small to admit fungal spores. Such recent studies have revealed the interesting fungi cannot play any role in biological con- fact that in many species the traps, or infec- trol of economically important nematodes. tion pegs, which penetrate captured nema- Species of Harposporium and similar genera todes give off a toxin which immobilizes a fall into that category. However, other fungi nematode almost immediately (3,16,24). have evolved spores specialized for adhesion There are also fungi that apparently im- to, or penetration of, the nematode cuticle, mobilize nematodes without any direct con- making them possible antagonists of plant- tact with the hyphae (11,12). Whether this parasitic nematodes. could occur in the soil would be difficult to determine. These fungi have a variety of FUNGAL ADAPTATIONS trapping organs: some coated with a muci- The fungal spore has undergone some laginous material from which an average- remarkable adaptation and specialization to sized soil nematode rarely escapes, some capture or penetrate nematodes. Among the with constricting rings triggered by complex lower fungi, motile zoospores appear to physiological processes, some whose traps have positive tropisms toward nematodes. have a fail-safe chemical system which in- Catenaria anguillulae spores most often ac- toxicates a nematode, and others whose trap- cumulate around the natural body orifices ping organs give off substances attractive to of the nematode cuticle. The many species nematodes (3,10,15). with nonmotile zoospores have special ad- There is also evidence that the assimila- hesive properties to adhere instantaneously tive or haustorial hyphae of some trapping to the cuticles of passing nematodes. The fungi release antibiotic inside the nematode most specialized and spectacular spore which prevents the development of com- adaptation occurs in Haptoglossa hetero- peting microorganisms (4). Secondary mi- spora, where spherical nonmotile spores are croorganisms enter moribund nematodes expelled through an exit tube from a zoo- through the buccal cavity, excretory pore, sporangium within a parasitized nematode. vulva, and anus; however, in nematodes The spores germinate to produce another captured in the hyphal traps of most species oddly shaped, nonmotile spore which has a of predacious fungi, secondary microorga- tonguelike lobe containing a minute pro- nisms seldom or never develop. The body jectile under tension. The spores inject the contents of captured nematodes are con- infective cell particle through the cuticle of sumed, leaving an empty cuticle filled with passing nematodes upon mechanostimula- assimilative hyphae which eventually lyse. tion. Davidson and Barron have described No other organisms develop in the victim. the process in detail (8). Many fungi with The conidia of nematode-trapping fungi spores that adhere to the nematode cuticle are much larger than those of most soil may have some specificity toward different saprophytes. They have food reserves which groups or even species of nematode, but we can be utilized to produce quickly one or have little information on the subject. more traps upon which the fungus relies for Scutellonema cavenessi was observed to re- nutrition and development in a predatory peatedly pass through clumps of the ad- mode. The conidia of most of these fungi do hesive spores of Meristracum asterospermum not tolerate dessication and therefore do not without any spores attaching, while various survive adverse conditions in the soil. They rhabditid and cephalobid nematodes had are easily lysed. The conidia apparently many spores per individual attach to their provide a short-term method of propagation cuticles (Mankau, unpubl, observations). and may be the stage at which a fungus can Even the spores of predacious hyphomycetes most conveniently switch from a saprophytic are remarkable in that they can germinate to a predacious nutritional mode or vice directly into a capture organ, or a vegetative versa. Little is known about sporulation of hypha, depending on external stimuli. nematode-trapping fungi in soil or about Most nematologists are quite familiar development of resistant structures. Many with the unique hyphal adaptations which species have chlamydospores, but no in- make up the traps of predacious fungi, and formation exists on their survival or germi- 246 jou~'nai of Nematology, Volume i2, No. 4, October 1~80 nation in soil or on their role in the biology fungi have been observed (18), but most of these fungi: Some species produce thick- species appear to occur in the top 10-20 cm walled storage hyphae, others produce mi- of any given soil. A few species can be iso- crosclerotia (Mankau, unpubl, observa- lated at relatively great depths. tions), and still others have no resistant Some
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