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 predacious fungi appear to be structures at all. Most attempts to produce rhizosphere organisms, while others occur inoculum on a commercial scale, as well as mainly in nonrhizosphere soil. The rela- most experimental soil colonizations, have tionships to plant rhizospheres may be im- concentrated on the production of mycelia portant aspects of the biological control and conidia, but these may have very lim- capacity of these fungi. Species occurring in ited survival when introduced into soil. Pre- tile rhizosphere appear better situated to dacious fungi tend to be poor saprophytic influence plant-parasitic nematode popula- competitors and some soils are fungistatic tions. In my experience, Arthrobotrys to them (17). dactyloides, Dactylaria brochopaga, Mona- crosporium ellipsosporum, and M. gephy- DISTRIBUTION ropagum, which are among species with Studies in several areas of the world show restricted saprophytic capability, are con- that the majority of species of nematode- sistently associated closely with plant roots trapping fungi and endoparasitic fungi and thus in a favorable position to prey are cosmopolitan. Surveys for nematode- upon economically important nematodes. trapping fungi in Canada, the United States, TAXONOMIC PROBLEMS Western Europe, Russia, New Zealand, Australia, Taiwan, and India have revealed Most of the endoparasitic fungi belong similar flora in each area. A few recently to groups little known by most mycologists. described species are controversial because They are minute and mainly obligate para- they are close variants of already well-known sites, thus difficult subjects for study. Species species. I have isolated some unusual species must be separated largely on minute differ- (unpublished) from a few specialized areas ences in spores, zoosporangia, or other such as arid desert soils and coastal dunes, aspects of their rather simple thalli. Barron but the flora of agricultural soils generally (4) recently has described a number of new appears similar almost everywhere. species and organized our knowledge of this Recently I surveyed the nematode- group so that many of the biological and destroying fungus flora of portions of West taxonomic problems are now apparent. Africa and found, for the most part, species Species identification of both parasitic identical to those occurring in southern and nematode-trapping fungi is important California soils. Barron's extensive examina- if we are to advance our understanding of tion of the flora of the soils of Ontario, their biology and importance as biological Canada, (4) revealed that those temperate control agents. Taxonomic characters are soils with long winter-dormant periods con- based on extremely simple morphological tain essentially the same flora we have ob- features whose subtle differences require a served in the sub-tropical soils of southern considerable commitment of time and en- California. It may be that not many re- ergy from nematologists interested in de- markably different or exotic species remain veloping expertise in their differentiation. to be found. However, information on the Nevertheless, some fundamental and fruit- occurrence of nematode-destroying fungi in [ul studies of these interesting organisms can the tropics is notably lacking, and the trop- be undertaken by nematologists without em- ics may prove to be unique areas for these barking on additional careers as mycologists. fungi. The major genera of predacious fungi, We now need investigations of the rela- Arthrobotrys, Dactylaria, Dactylella, and tionships of various species of nematode- Monacrosporium, probably contain more destroying fungi to biotic and abiotic fac- than 100 species. Many of these have been tors in soil, to cropping sequences, to differ- described by Charles Drechsler (9) whose ent soil types, and to microhabitats. Some meticulous work delineated differences be- differences in vertical distribution of these tween most species in these genera. As one Fungal Control of Nematodes: Mankau 247 collects more and more isolates, however, it the fungi he tested rapidly colonized or ex- becomes evident that there are continuums ploited the soil microhabitat. They were of gradations in the characteristics between poor competitive saprophytes, susceptible to most species, and it often becomes impossi- antagonisms from other soil organisms. ble to assign an isolate to a given species or Added mycelia were nonpersistent in soil to clearly focus on characteristics designat- even in the presence of energy sources. ing it a new species. A genus such as Cooke concluded that it may be possible to Arthrobotrys may, in fact, be as varied and alter the soil environment in favor of complex as Penicillium and its relatives. nematode-trapping fungi, but the means of We have collected approximately 50 geo- doing so (or even the directions to pursue) graphic isolates which could be placed in are beyond present knowledge. the species A. conoides, yet most of the iso- Cooke (7) reviewed some of the ecolog- lates were unique and could be separated ical relationships in which fungal predators from any of the others on some physiolog- were involved and identified some of the ical, morphological, ecological, or biochem- problems associated with using them as bio- ical basis (Mankau, unpublished data). logical control agents. Before predation can They exhibited different patterns of sporu- occur, mycelial growth and trap formation lation and chlamydospore production, dif- must occur. Both these processes require ferent responses and growth rates on a energy, which can be supplied by a readily variety of comparative media, and different available carbon source. Consequently, the degrees of predaciousness or response to addition of organic amendments to soil is trap-stimulatory factors. What constitutes a usually followed by a short period in which species among these fungi is, or should be, the activity of nematode-trapping fungi in- a matter of controversy and a subject for a creases. Cooke suggested that nematode great deal of painstaking study. capture may have been a means of escaping competition during phases of intense micro- NEMATODE CONTROL bial activity in microhabitats with readily Nematode-trapping fungi have long been available organic substrates. He also noted considered promising biological agents for that, although the addition of organic control of nematodes. Their spectacular amendments to soil results in an increase in predacious behavior on agar plates made the population of free-living nematodes, them intriguing organisms for study and predation is apparently not related to the speculation. Some of the early tests in green- density of the nematode population. In fact, house pots and in the field were not de- an increasing amount of amendment may signed to evaluate critically their effects on result in a reduction in the predacious activ- target nematodes and probably tended to ity of a fungus. This occurs because of an exaggerate their potential. Most such ex- intensification in the activity of the soil periments involved adding one fungus to microbes competing with the predacious soil which had been amended with organic fungi for nutrients. Obviously complex in- matter on the assumption that the fungus teractions between predacious fungi, de- would increase on the amendment and turn composing organic substances, and the re- to predation on nematodes, hopefully the mainder of the soil microbial population plant-parasites. All that was generally determine the final level of each in the known about the test fungus was that it had soil. The dual nutritional capability of trapped nematodes while under observation nematode-trapping fungi remains a puzzling or culture in the laboratory. The criteria aspect of their biology which requires fur- generally used in choosing the fungal agent ther investigation to understand what initi- were ready availability and easy culture, ates predacious activity and how long it can characteristics which may have some in- be sustained. herent value but are not necessarily those of The factors which initiate trap forma- a good natural enemy. tion in these fungi have been reviewed and Cooke (7) showed that the chance of investigated, most recently by Nordbring- establishing "alien" nematophagous species Hertz and her co-workers (20,22). Although in the predacious phase is small. None of she has isolated a few valyl-peptides which 248 Journal of Nematology, Volume 12, No. 4, October 1980 effectively trigger trap formation in one nistic biological agents increase to a point fungal isolate, such compounds still do not where their activity is noticeable and eco- appear to elicit as strong and rapid a re- nomically advantageous. This is more apt to sponse as do living nematodes (21). A bio- be true for perennial crops than for annual chemical complex may be involved, and it crops, may be quite different for various species A salient consideration in the use of and isolates. Many species form traps fungi as applied biological control agents spontaneously and consistently even in pure against nematodes is the soil habitat in culture, while others produce traps only which most plant-parasitic nematodes exist. feebly even in the presence of nematodes An average fertile field soil contains ap- (Mankau, unpublished data). There is a proximately 10 9 bacteria, 10 5-s actinomycete, wide range of facultative saprophytism and 10 5-G fungus, and 10 4-5 protozoa reproduc- predation among different closely related tive units per gram, plus a large number of isolates and certainly among different spe- fungivorous nematodes, tardigrades, Col- cies. Nordbring-Hertz and Mattiasson (23) lembola, mites, and other assorted micro- have just presented evidence for the pres- fauna and meiofauna. To believe that ence of a lectin on the traps of A. oligospora adding one additional organism will have which binds to a carbohydrate on the nema- an immediate measurable effect requires tode surface leading to penetration of the credulity. But biological antagonisms are cuticle by a hypha. These interesting find- common in tile soil, and biological control ings open the possibility of solutions to has often occurred there (2). The fungi the problem of specificity in these host- under consideration are highly specialized microorganism interrelationships. A method in their roles as nematode consumers, and it to assess the variable predacity of nematode- would be unfortunate if we did not pursue trapping fungi in vitro in order to select the our investigations of their biology and im- most predacious ones for soil and field tests pact in the soil until we understand most of was developed by Heintz (13). After several tile possibilities and problems inherent in decades of study we still have relatively their use as biological control agents. little knowledge about the predacious habit The introduction of predacious fungi of these fungi, but some is now accumulat- into soil to effect biological control should ing on the physiology of trap formation. probably be attempted with those organisms With the exception of a few Arthrobotrys that research has demonstrated to be in- species, which are nearly always present, herently effective in regulating target prey trapping fungi usually appear after intense populations. They may not already be doing microbial activity on organic substrates has this in given areas because of controllable subsided and secondary microbial browsers, environmental factors, because they are not such as nematodes, predominate. On agar synchronized with susceptible stages of the plates seeded with soil one frequently ob- host, or because they do not occur in the serves a succession of species, with some ap- problem area. The nonspecific nature of pearing as much as several weeks to several nematode predation by most fungi may be a months after the earliest species. The eco- serious hindrance to their use as biological logical relationships of nematode-destroying control agents. Most predacious and some fungi are exceedingly variable and complex, parasitic species can be cultured easily and and we are a long way from an adequate produced commercially. It is likely that the understanding of how effective they are in more effective biological control agents will reducing specific nematode populations. It be difficult to culture because of obligate may be that under some agricultural condi- parasitism or predation and will be some- tions the reproductive capability of certain what specific for tylenchid nematodes. nematode pests far exceeds all of the com- Despite the generally equivocal per- bined biotic factors limiting population ex- formance of predacious fungi in applied bio- pansion, but there is not conclusive evidence logical control in the past, a few recent that this is true. If we could tolerate nema- examples of successful results promotes some tode damage or population expansions for optimism. By systematically testing a group longer periods, we might find that antago- of predacious fungi for compatibility with Fungal Control of Nematodes: Mankau 249 ,4garicus bispora, Cayrol et al. (6) developed Rhopalomyces elegans to be a confirmed egg the use of a commercially prepared isolate parasite; however, it has never been asso- Arthrobotrys to protect the commercial ciated with the eggs of a crop pest. The mushroom from attack by the destructive difficulty of observing nematode eggs in mycophagous nematode Ditylenchus my- soil, or of extracting them from soil, had celiophagus. They tested six fungi com- led to few observations of egg parasites. The monly found in the horse manure used for sugar-flotation methods commonly used to mushroom compost in the south of France extract eggs from soil generally halt any for compatibility with A. bisporus. Three further development of fungal antagonists species stopped the growth of the mushroom present in or on the eggs. Most of the fungi mycelium, and one eventually destroyed it attacking eggs appear to produce quite sim- completely, but two species, M. doedycoides ilar internal hyphae, and they can only be and A. robusta (antipoIis), had no effect on identified after isolation and subsequent development of the mushroom mycelium. sporulation. Because of their importance They chose the latter, more rapidly growing as major plant parasites, and also their species for development as a biological con- easy recovery, the eggs of the root-knot trol agent (Royal 300). Trials with the (Meloidogyne spp.) and cyst nematodes fungus seeded simultaneously with .4. bi- (Heterodera spp.) have been examined most sporus into mushroom compost at a rate at frequently. Occasionally they have been 1% each increased harvests of mushroom by found to be parasitized. more than 20% and reduced Ditylenchus The viability of Heterodera eggs gen- populations in the compost by about 40%. erally declines over time as the cyst remains Substantial numbers of nematodes still re- in the soil, and fungi are suspected to be mained in the compost, and a second trial involved. Tribe (32) reviewed the relation- had less response; nevertheless, the authors ship of fungi to cyst pathology and listed were convinced that the results justified Verticillium chlamydosporium and another commercial use of the fungus for nematode nonsporulating "contortion fungus" as the control in mushroom culture. major pathogens of eggs within H. schachtii Cayrol and Frankowski (5) had another and H. avenae cysts. Cylindrocarpon de- isolate of Arthrobotrys grown commercially structans and several unidentified fungi (Royal 350) and developed it as a biological were listed as minor pathogens, but the control agent against a root-knot nematode status of this group was considered unclear problem in tomato. Trials in fields of several without further study of the ecology of vegetable growers in the Alpes-Maritimes cysts in soil over a long period of time. Departement utilized the fungus on gran- Tribe also discussed the relationship of a ules of oat seed medium at a rate of 140 number of relatively common soil fungi g/m °~ incorporated 1 month in advance of which are often reported associated with the crop. This rate was tile maximum that Heterodera cysts. was economically feasible, and it resulted Tribe (33) analyzed 112 populations of in good protection of tomato against H. schachtii from several countries; slightly Meloidogyne and satisfactory colonization over a fourth of this population was com- of tlle soil by the fungus. In the case of prised of females and cysts taken from roots. heavy populations of Meloidogyne, however, Fourteen percent of full cysts taken from Cayrol and Frankowski indicated that the soil were diseased, but under some condi- Royal 350 fungus would be more appropri- tions of monoculture with sugar beet, ate as a secondary control measure after an slightly over 50% were diseased. Tribe ob- initial (presumably nematicide) treatment. served great variability in infection, with If the experience of these researchers is re- some samples containing no diseased cysts. peatable, then even the less specific nema- A similar percentage of females taken from tode antagonists may show some promise roots were attacked by flmgi, but these under proper conditions. fungi were specific, probably obligate para- Tile discovery of fungi parasitic on the sites; in their absence infection of cysts was eggs of plant-parasitic nematodes has been very low. Catenaria auxiliaris and some of very recent. Barron (4) considered only the egg parasites already mentioned were 250 Journal oI Nematology, Volume 12, No. 4, October 1980 the principal fungi involved. Tribe recog- cited as a likely area for potentially useful nized two phases of fungal attack on cysts antagonists by Baker and Cook (2). It was and eggs; the first occurs on the roots of the suspected that the nematode was under host among females and young cysts, and natural biological control in these orchards, the second among cysts in soil over a long and close examination of the egg masses period of time. revealed that a substantial percentage of the Strains of Acremonium stricture and eggs were parasitized by a new fungus, Fusarium oxysporum were isolated from Dactylella oviparasitica Stirling and Man- eggs in H. schachtii cysts from a majority of kau (29). The fungus appeared to keep sugar beet soils examined by Nigh in Cali- Meloidogyne populations in the orchards at fornia (19). Both fungi readily attacked a level which had little or no economic im- eggs of several nematode species offered on pact on the crop. Nematode-trapping fungi, agar in vitro or mixed with the fungi in however, appeared to play no more than a amended soils, and they also grew saprophy- minor role (31). tically on dead eggs. It was concluded that D. oviparasitica required special en- these common facultative saprophytes were riched laboratory media for growth and responsible for the destruction of some H. sporulation (29) and had many attributes of schachtii eggs under certain conditions in a successful biological control agent against the fields studied. Meloidogyne. The fungus (i) actively para- It is possible that many other strains of sitized Meloidogyne eggs, which were more facultative saprophytes are able to attack vulnerable to attack than were the larvae cyst nematode eggs under circumstances (28); (ii) occasionally parasitized Mel- where the eggs are accessible to fungi before oidogyne females, particularly on hosts completion of the first molt and possibly where the nematode produced eggs rela- also under some stress. Second-stage larvae tively slowly; (iii) occurred in the rhizo- within eggs generally appear to be resistant sphere close to its nematode host; and (iv) to attack by any of the fungi thus far re- was able to survive periods when the nema- ported to be associated with cysts. Some of tode was absent by growing saprophytically the weakly pathogenic root-inhabiting fungi on dead roots (27) or by parasitizing eggs and mycorhizal fungi may be capable of in- of other nematodes (30). vading sedentary nematode endoparasites in The specific host-parasite relationship root tissue. Such fungi invaded Sarisodera of Lovell peach and Meloidogyne influenced africanus cysts in fixed and sectioned the dynamics of the parasitism. The some- Panicum roots from West Africa (D. P. what restricted capacity of Meloidogyne Taylor, personal comm.). Close examination females to produce eggs on Lovell peach of cyst nematodes in late stages of develop- allowed the parasite to destroy a large per- ment within roots, and further meticulous centage of them. Stirling et al. (31) ob- study of the degradation of cysts remaining served that on plants such as grape and in the soil, may eventually establish con- tomato, where Meloidogyne females pro- sistent fungal-egg interactions among the duce eggs over a longer period and egg many fungi isolated from cysts. A number masses contain large numbers of eggs, some of nonsporulating fungi present special egg parasitism occurs. However, this para- problems in determining their roles and sitism is not sufficient to decrease nematode importance. Much more work is required to populations unless a particular virulent understand the importance of fungal attack isolate of the fungus is present or environ- on cyst nematode population dynamics. In mental conditions favor the parasite or are some cases there appears to be a significant unsuitable for the nematode. D. ovipara- amount of biological control occurring. sitica, although capable of limited sapro- Stirling (26) examined some peach or- phytic growth, appears to be one of the most chards on Lovell rootstock in California's specialized hyphomycete parasites of nema- San Joaquin valley which had relatively low todes yet discovered. root-knot nematode populations despite sus- CONCLUSIONS ceptible host and ideal conditions for de- velopment of the nematode pest, a situation Nematophagus fungi have interested a Fungal Control of Nematodes: Mankau 251 number of researchers for several decades as periods (14). While these characteristics interesting subjects for study and as po- require some modification in consideration tential biological control agents. To date, of the soil habitat, they should apply however, not a single fungal strain has equally to the natural enemies of nema- demonstrated any sustained capacity to con- todes. As has already been noted, many of trol nematodes as effectively as chemicals. the known fungal enemies of nematodes are Perhaps this is an unrealistic comparison, inadequate with regard to at least some of and such levels of control are unattainable these characteristics, and this may explain by fungal agents. All of the commonly used why they have rarely been used successfully nematicides have been broad spectrum gen- against plant-parasitic nematodes. Now we eral biocides with which a large variety of have the example of a recently discovered soil organisms were killed to reduce and fungus, D. oviparasitica, which has more of control target nematodes. Nematode antag- the desirable attributes than most other onists have seldom been considered in ap- fungi, and this will stimulate continued plying nematicides, and use of nematode diligence in the search for more effective antagonists often resulted in increased dis- agents. Bacillus penetrans, discussed else- ease problems in subsequent seasons. Bio- where in this symposium (25), is another logical agents have very limited activities example of an organism with most of the and generally operate from a highly variable apparent characteristics of an effective bio- population base which is difficult to control logical control agent. and sustain after their addition to soil. They We still know so little about the fungal must also interact with hundreds of active antagonists of nematodes that we can afford soil organisms, other than hosts and prey, in a good deal of optimism about biological many complex ways. control. The search for antagonists and the Any biological control accomplished attempt to understand the total soil com- with fungi will probably be slow and erratic munity with respect to nematode popula- and may never completely suppress pest tions never has been pursued systematically. populations to the economically effective, With the demise of one of our most impor- albeit temporary, levels attained with nema- tant nematicides and the threatened loss of ticides. On the other hand, enough informa- others, there is some urgency in this search. tion might be gathered on the natural We have never really searched the original control already operating under certain habitats of nematode parasites for antago- conditions to develop practices enhancing nists as have the entomologists, nor have we biological control. We also may be able to imported agents for trial in problem areas. tolerate higher economic threshold levels of There is obviously no lack of research op- pest damage related to long-term biological portunity in this area. control and accept some short-term losses if they are balanced by longer term benefits LITERATURE CITED in reduced pesticide costs and pollution problems. There is always the hope that the 1. Aschner, M., and S. Kohn. 1958. The biology of Harposporium anguillulae. J. Gen. Microbiol. right organism, or combination of organ- 19:182-189. isms, will be found to provide an almost 2. Baker, K. F., and R. J. Cook. 1974. Biological permanent population balance of a nema- control of plant pathogens. W. H. Freeman g: Co., tode pest to a degree which would never be San Francisco. 3. Balan, J., and N. N. Gerber. 1972. Attraction attainable with chemicals. 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