EVALUATION OF PARASITES AND PREDATORS OF PLANT PARASITIC NEMATODES'
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1 EVALUATION OF PARASITES AND PREDATORS OF PLANT PARASITIC NEMATODES' Eldon I. Zehr Department of Plant Pathology and Physiology Clemson University Clemson, BC Abstract: Fungi and other organisms that llre I>nrasites of plant-parasitic nematodes have been described and some ha\'e been used to help suprress nematode populations. Generally, the biology of these organisms is poorly understood. Potential applications of certain parasites and predators for biological control and the need for additional research on the biology of these organisms are discussed. Key Words: Nematode parasitic fungi, biological control, soil biology. J. Agric. EntomoL 2(1): L (January L985) Soil-inhabiting nematodes are a Large and diverse group of organisms. In the complexity of the soil environment many kinds of predators and parasites interact with the nematode population. Many kinds of fungi limit populations of nematodes in most soil environments. Excellent reviews of fungi as biocontrol agents have been written by Barron (l977), Mankau (1980), and Kerry (1980). Certain bacterial parasites of nematodes also have been described by Sayre (1980), and predacious nematodes may contribute to population limitations of soil-inhabiting nematodes. Plant-parasitic nematodes do not differ from other nematodes in sensitivity to biological agents that limit nematode populations in soil. Their numbers, too, are reduced by the parasitic and predacious activity of many organisms. Difficulties of investigating the biology of nematodes and potential parasites or predators that might be useful for control of plant. parasites slow the advance of knowledge that might allow us to capitalize upon such organisms to control plant-parasitic nematodes in the field. In this brief discussion I shall not attempt to add to the information already reviewed thoroughly by others_ I wish to describe very briefly the kinds of organisms that attack plant-parasitic nematodes, describe some procedures that have been used to test the effectiveness of certain of these organisms for suppression of nematode populations, and, finally, suggest some lines of investigation that might be used to enhance the activity of these organisms in biological control. KINDS OF PARASITES AND PREDATORS Nematode-trapping fungi. This variable, soil-inhabiting group of organisms consists of vigorous saprophytes that are not entirely dependent upon living 01' dead nematodes for their growth or sulvival. They grow on many organic substrates and compete well in the soil environment.. The distinguishing features of these I Contribution No or the South Cprolinl A~riculturlll E:::~periment St.lltion. Received for Ilu!Jlicalion 22 May 1984; accepted I November
2 ZEHR: Parasites and Predators of Plant. Parasitic Nematodes 131 fungi are the adhesive hyphae, nets, rings or other structures that capture and destroy nematodes passing in the soil (Barron 1977). Since some nematodetrapping fungi often are abundant near plant roots (Mankau 1980), these fungi have significant potential for trapping plant-parasitic nematodes as well as freeliving nematodes in the soil. Endoparasitic organisms. Endoparasites of nematodes include certain fungi that invade tissues of nematodes and have relatively little external mycelium other than the hyphae that produce spores. A parasitic bacterium described as Bacillus penetrans Mankau (Sayre 1980) invades nematodes through the body wall. This organism, of uncertain taxonomic classification (Sayre et a ), may be an important agent for biological control of the nematodes it infects. It appears to be an obligate parasite and studies of its behavior have been restricted by difficulties of experimental manipulations. Spores of some endoparasitic fungi may be ingested by nematodes, with infection following spore gennination in the alimentary canal. However, these fungi have little potential for control of plant-parasitic nematodes because the spores are not ingested by stylet-bearing nematodes. Hirsutella rhossi/iensis Minter and Brady, a parasitic fungus described in Great Britain (Minter and Brady 1980), may have more potential to control some plant-parasitic nematodes. Jaffee and Zehr (1982) found this organism to be widespread in South Carolina peach orchard soils, sometimes infecting large numbers of the nematode Criconemella xenoplax (RaskO Luc and Raski. Egg-destroying fungi. The fungus Catenaria auxiliaris (Kuhn) Tribe was discovered in cysts of the sugar beet cyst nematode, Heterodera schachtti Schm. (Stone 1983). The fungus attacks nematode eggs in the cysts. This fungus has not successfully controlled populations of H. schachtii in the field (Stirling et al. 1979), but it can reduce populations of the cereal cyst nematode, Helero([era avenae \Voll., to levels that do not cause economic damage (Kerry and Crump 1977). Another egg parasite, Dactylella uuiparasitica Stiding and Mankau, has been found in egg masses of root-knot nematodes (Meloidogyne sp.) in California (Stirling 1979). Although the fungus appeared to suppress root-knot populations in some peach orchards, attempts to use the fungus to advantage for root-knot suppression have not been unsuccessful. Other nematode parasites and predators. There is a notable absence of infonnation about the importance of other agents for controlling nematodes. Nematodes in t.he genus Mononchus are predators of other nematodes, but little is known of their potential importance for nematode suppression. There is little infonnation about viruses that may infect plant-parasitic nematodes, or of the effects of arthropods in the soil that may be nematode predators. Presumably, there are bacterial diseases and perhaps additional diseases caused by fungi that may be of importance for nematode suppression. Additional studies of these agents may yield infol1'nation that would be valuable for biological control. PROBLEM AREAS Because parasites and predators are diverse and numerous in the soil environment, t.hey exert pressure on the nematode population in most soils. If these organisms were not present, populations of plant parasites might increase more rapidly and become more numerous than are observed in most environments.
3 132 J. Agric. Entomol. Vol. 2. No. I (1985) However, with occasional exceptions, parasitism is insufficient to suppress populations enough to avoid crop injury. One notable exception is suppression of Heterodera avenae by Catenaria auxiliaris, which is sufficient to reduce injury of oats by this nematode (Kerry and Crump 1977). A major problem is the lack of information about the behavior, survival, and competitive capabilities of nematode parasites in soil. Despite the prevalence of parasites in soil they are difficult to study because interactions of organisms in soil are very complex. Introduction of parasites or predators into soil is difficult because they must become established in soil in order to become an important factor in nematode suppression. Some, such as Bacil/us penetruns, cannot be grown easily in culture and are, therefore, very difficult to introduce in suitable numbers into soil. These problems are important, but they suggest that investigations of the biology of parasites and predators might produce new information that could be used to enhance parasitism of plant-parasitic nematodes. Further understanding of the nature of parasitism, spore production and survival of fungal parasites in soil, competition with other soil inhabitants, and the potential for modifications of cultural practices to influence parasitism will enhance the opportunities for control of plant parasitic nematodes by organisms in soil. EXPERIMENTAL APPROACHES FOR RESEARCH There are a few examples of nematode-parasite or predator interactions where research has progressed beyond a description of the organisms and their interactions to the point of utilizing these agents in the field. Attempts to introduce fungal parasites into soil for control of plant parasitic nematodes generally have not been very successful. These organisms are generally poor saprophytes that do not compete well with other soil inhabitants. However, some of these studies provide a basis for optimism that organisms might be used as an aid in nematode control. Parasitism of females and eggs of the cereal nematode Heterodera auenae by the fungus Nematophthora gynophila Kerry and Crump was sufficient to reduce damage from this nematode to minor significance (Kerry and Crump 1977). Eggs and females of the sugar beet nematode Heterodera schuctii also were parasitized by N. gynophila to the extent that the population was reduced; however, the amount of population reduction was insufficient to prevent a large population from developing and the only effect was a delay in population build-up (Stirling 1979). A similar situation appears to exist with root-knot nematodes. (Meloidogyne spp.) in California. The fungus Dacty/eUa ouiparasilica, an egg parasite of Meloidogyne spp., was active in peach orchards and appeared to partially suppress root-knot in peach (Stirling 1979). Suppression of root knot was not observed on grape, perhaps because the nematode produces large numbers of eggs and for a longer period on this host than on peach. In another nematode-fungus interaction the fungus Hirsulella rhossiliensis is a parasite of the nematode Criconemella xenoplax. The fungus invades the nematode through the cuticle after spores adhere to the body of the nematode and germinate (Jaffee and Zehr 1982). Hirsutella rhossiliensis may be an important parasite because it is widespread in South Carolina peach orchard soils and large numbers of parasitized C. xenoplcl'( occasionally are found. However, the nematode populations
4 ZEHR: Pa.rasites and Predators of Plant Parasitic Nematodes 133 remain large enough to cause significant injury to peach trees even in the presence of t.he fungus. The fungus may be partially responsible for the rapid fluctuations of C. xenoplax populations often observed in peach orchards (Jaffee and Zehr 1982; Nesmith et al. 1981), and might be involved in the occasional collapse of nematode populations observed in some orchards. Parasitism by H. rhossiliensis is affected by cerlain em'ironmental factors. Exposure of C. xenopla:r, to 40 Q C for two hours increases the nematode's susceptibility to invasion by the fungus (Jaffee and Zehr 1982). Since such temperatures are common in the soil in peach orchards in summer months, iernperature may exert an important effect upon the parasite-host interaction in nature. Certain cations act to enhance parasitism, while the sulfate anion appears to inhibit parasitism (Jaffee and Zehr J 983). Thus, certain constituents of the soil solution may hove important influences upon the activity of parasitic organisms in the soil (Jaffee and Zehr 1983). These examples illustrate the need for a thorough understanding of the behavior and biology of both host and parasite so that the parasitic interaction may be enhanced or appropriately regulated for maximum benefit in biological control. Techniques for introducing biological control agents into soil are poorly developed. Stirling et al. (1983) used infected cut roots to introduce D. parasitica inco soil in greenhouse tests of suppression. They also successfully introduced the fungus mycelium into autoclaved soil in which biological control of Meloidogyne was tested. Eayre, Jaffee, and Zehr (unpublished) grew H. rhossiliensis on vermiculite impregnated with a suitable growth medium and introduced the fungus into steamed soil in greenhouse tests. These methods may not be satisfactory for use in the field. However, Jaffee et al (unpublished data) have successfully introduced H. rhossiliensis into the field by adding the fungus to nematode infested soil containing peach seedlings before the seedlings were transplanted to the field. Cayrol and Frankowski, cited in Mankau (1980), utilized an oat seed medium to grow Arthrobotrys and introduce it into the soil to control root~knot of tomato. This technique was successful for satisfactory control unless the nematode population was very large. The partial successes of these attempts suggest that further study into the biology of parasites and predators may lead to successful innovations for biological control of plant-parasitic nematodes. Until much more is known ahout the biology of such organisms and their soil ecology, rapid progress is unlikely. Biological agents as controls for plant parasites may become economically important as techniques are developed for their introduction and maintenance in the soil environment. REI'ERENCES CITED Barron, G. L The nematode-destroying fungi. Topics in Mycobiology No.1, Can, BioI. Pub.: Guelph. 140 pp. Jaffee, B. A.. and E. I. Zehr Parasitism of the nematode CricOTlemelia xerwplax by the fungus flirsutclfa rhqssiliensrs. Phytopathology 72: Jaffee, B. A., and E. L Zehr Effects of certain solutes, osmotic potential, and soil solutions on parasitism of Criconemella xenoplax by flirsutella rhossiliells;'<;. Phytopathology 73: 54' Kerry. B Biocontrol: fungal parasites of female cyst nematodes. J. :"Jematol. 12: _
5 134 J. Agric. Entomol. Vol. 2, 1\0. 1 (1985) Kerry, B. R., and D. H. Crump Observations on ruugnl parasit.es of females and eggs of the cereul cyst-nematode, Heterodera avenoe, and other cyst-nematode. Nematologica 26: Mankau. R Bioconi..rol: fungi as nematode collirol agents. J. Nemal.ol. 12: Minter, D. W., and B. L. Brady Mononematous species of flirsutella. Trans. Br. Mycol. Soc. 74: Nesmith, W. C.. E. I. Zehr. and W. M. Dowler Association of Macroposlhotlia xcnoplax and Scuteilollcma brachyurum with the peach tree short life syndrome. J. Nematol. 13: Sayre, H. M Biocont.rol: Bw.:ilItls pcnclnl1ls and related parasiies of nematodes.,j. Nemllwl. 12: Sayre. R. M. H. L. Cherna. and W. P. Wergin Morphological lind laxonomic reevaluat.ion of Pasteuria ramosn Metchnikofr 1888 and "l3acillu,,, penetrluls" ~18nkau Int. J. Syst. Bacteriol. 33: 636-6,19. Stirling, G. R., M. V. McKenry, and R. :\ofankau Biological control of root-knot nematodes (Meloidogyne spp.) on peach. Phytopathology 69: 809. Stone. A. R Integrated control of the beet cyst-nematode. Rept. Rothnmsted Exp. Stu., Nematology Dept., p. 165.
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