BACTERIOLOGICAL REVIEWS, Sept., 1965Copyright ( 1965 American Society for Microbiology

Vol. 29, No. 3Printed in U.S.A.

Symposium on Microbial InsecticidesIII. Fungal Parasites of Insects and Nematodes'

DAVID PRAMERDepartment of Agricultural Microbiology, Rutgers, The State University, New Brunswick, New Jersey

INTRODUCTION..................... 382

INFECTIONS OF INSECTS ..................... ................................... 382Entomophthora..................... 382Cordyceps..................... 383Septobasidium..................... 383Beauveria..................... 384

INFECTIONS OF NEMATODES ..................... ............................... 384Nematode-Trapping Fungi .................................................... 384

Harposporium...................................... 385

COMMENTS CONCERNING MICROBIAL CONTROL.386LITERATURE CITED.386

INTRODUCTIONFungal parasites of insects and nematodes are

too important to be treated superficially, and cur-rent knowledge of the subject is much too exten-sive for complete coverage here. I have no alter-native, therefore, but to deal in detail withselected aspects of my topic, and to hope that inso doing, I will focus attention on a field of fasci-nation and future promise in microbiology. Here,then, are gleanings from a voluminous literaturethat pertains to fungal parasites of insects andnematodes. No claim is made for originality ofeither content or exposition. My own investiga-tions are concerned with a group of microorgan-isms known as the nematode-trapping fungi.These will be considered subsequently, but itmust be understood that the major portion of mytext describes the work of others on organismswith which I have had little or no personal ex-perience.

INFECTIONS OF INSECTSFungal parasites are unique in the history of

insect pathology (34). The very first experimentalproof that a disease of animals can be caused bya microorganism was the demonstration, in 1835,by Agostino Bassi that muscardine of the silk-worm was a fungal infection. Moreover, it was afungus parasite of the cockehafer that Metch-nikoff used, in 1879, to first demonstrate that a

1 A contribution to the symposium "MicrobialInsecticides" presented at the Annual Meeting ofthe American Society for Microbiology, Washing-ton, D.C., 7 May 1964, under the sponsorship of theDivision of Agricultural and Industrial Bacteriol-ogy, with Harlow H. Hall as convener and Consul-tant Editor. Paper of the Journal Series, NewJersey Agricultural Experiment Station.

microbial disease of an insect of economic signifi-cance can be established intentionally. Fromthese beginnings, insect pathology has developedas an experimental and applied science. Today,many representatives of the fungi are known tocause disease in insects. There are numerous para-sites of insects among the Phycomycetes, Asco-mycetes, and Deuteromycetes, but the number ofBasidiomycetes known to infect insects is rela-tively small. Varying degress of parasitism arerecognized, and many fungus-insect relationshipshave been described. It is not practical to attempthere a discussion of all of the species of fungi in-volved or the infections they cause, but some es-sential relationships will be exemplified by thefollowing consideration of a few of the more com-pletely described insect mycoses.

EntomophthoraThe Entomophthorales constitute an order of

Phycomycetes that is divided into six genera, oneof which, Entomophthora, contains more than 100species known to parasitize insects. Entomoph-thorales infections have been reviewed by Stein-haus (33) and, more recently, by MacLeod (23).Insects representative of seven different orders(Orthoptera, Homoptera, Hemiptera, Coleoptera,Lepidoptera, Diptera, and Hymenoptera) are at-tacked by Entomophthora species, and suscepti-bility to infection is shared by larvae, pupae, andadult.

Infection results when an airborne spore ger-minates and penetrates the exoskeleton of an in-sect. Vegetative growth occurs in the living host,but hyphal extension is limited, and there is frag-mentation of filaments into their component cells.These develop into hyphal bodies which are short,multinucleate, and variable in form and size.

382

on October 19, 2020 by guest

http://mm

br.asm.org/

Dow

nloaded from

VOiL. 29, 1965 FUNGAL PARASITES OF INSECTS AND NEMATODES

Hyphal bodies increase in number by fission andbudding, and, ultimately, fill the insect hemo-coele. As the infection progresses, insects becomesluggish, and eventually lose their power of loco-motion. They may drop to the ground or come torest on the underside of branches or leaves. Fre-quently, hyphae penetrate the body surface andform rhizoids which anchor the cadaver firmly tothe site at which death occurred. Shortly afterdeath of the insect, the hyphal bodies give rise tospores. These may be of the resting (chlamydo-spores), sexual (zygospores), or asexual (conidia)type, but, under optimal conditions of tempera-ture and moisture, it is conidia that are formedpredominantly. Conidiophores develop rapidly,penetrating the less resistant portions of the exo-skeleton, and conidia may be recognized exter-nally on the body surface, within a few hours ofdeath of the insect. Entomophthora conidia andconidiophores appear to absorb water differen-tially, which causes pressure to be exerted and thespores to be discharged violently into the air. Bythis mechanism the parasite is dispersed overconsiderable distances, and the probability of re-newed contact with a living host is increased.MacLeod (23) emphasized that great difficulty

is encountered by investigators who attempt toinfect healthy insects with Ertomophthora. It ap-pears that conditions which induce natural infec-tions and a highly contagious state are unknownand, therefore, cannot be reproduced at will inthe laboratory. Entomophthora organisms are notobligate parasites. They develop saprophyticallyon a variety of complex organic substrates (30).Some species have no requirement for an exoge-nous supply of vitamins or other accessory growthfactors, and can be cultivated on simple mediathat are chemically defined (31, 38). However,much remains to be revealed regarding the nutri-tion of Entomophthora. Also, information (15, 16,30) concerning the influence of environmentalfactors on growth, morphogenesis, and patho-genicity is limited, and must be extended greatlyif these fungi are to be understood, and, throughunderstanding, be exploited for the biological con-trol of insect pests.

CordycepsAscomycetes are divided into two subclasses,

the Hemiascomycetes and the Euascomycetes, inwhich ascocarps are present and absent, respec-tively. The genus Cordyceps, which is included inthe order Hypocreales, subclass Eusascomycetes,contains approximately 200 species, the majorityof which parasitize insects. Members of the genushave been isolated from seven different orders ofinsects (Diptera, Hymenoptera, Coleoptera, Lep-idoptera, Hemiptera, Isoptera, and Orthoptera)

and from spiders, and they are well characterizedtaxonomically. Insects parasitized by Cordycepsspecies are bizarre in appearance and attractedthe attention of early naturalists. Steinhaus (33)cites Torrubia, a Franciscan friar, who, in 1749,on finding some dead wasps in a field near Ha-vana, wrote, "from the belly of every wasp a plantgerminated, which grows about five spans high."It is of interest to note also that some Cordyceps-infected insects are used as food and for medicinalpurposes in China (17). Our present knowledge ofthe taxonomy, morphology, physiology, and path-ogenicity of Cordyceps was most recently reviewedby McEwen (26).

It is characteristic of Cordyceps that the scle-rotium located within the infected insect givesrise to a stroma or aerial structure, consisting ofan outer layer of short lateral hyphal branchesarising from a central core of parallel and inter-twined filaments. The sterile, erect portion of thestroma usually terminates in an enlarged fertilehead that contains perithecia and may be brightlycolored. Stromata vary in length from 1.5 to 300mm, and this exposed portion of Cordyceps wasdescribed in early writings as a plant or tree de-veloping from a "bug's belly."

If spores of Cordyceps germinate on the sur-face of a suitable host, the integument of the in-sect is penetrated, and, through a process of frag-mentation, hyphal bodies are produced in thehemocoele. The hyphal bodies multiply by bud-ding. They increase in number in the blood andeventually fill the entire body cavity. Death ofthe host occurs, but there is continued growth ofthe fungus, and the compacted hyphal strandsform the sclerotium from which the stroma arises(25, 33). Most species of Cordyceps appear to behost specific, but exceptions are known. C. mili-taris is notable in this regard, and has been re-ported as parasitic on 13 genera of Lepidoptera,on coleopterous pupae, and on some Hymenop-tera (37). There have been a limited number ofattempts to culture these fungi on laboratorymedia. Huber (18) reported that C. militaris grewwell on a medium containing glycerol as the solesource of carbon and energy. The fungus requiredno accessory growth factors and was capable ofutilizing both inorganic and organic nitrogen. Atpresent, there is great need for information re-lating nutritional and environmental conditionsto infectivity, growth, and sporulation of Cor-dyceps species.

SeptobasidiumOf the few Basidiomycetes that parasitize in-

sects, members of the genus Septobasidium arethe most noteworthy. There are approximately160 known species that live in balanced associa-

383

on October 19, 2020 by guest

http://mm

br.asm.org/

Dow

nloaded from

BACTERIOL. REV.

tion with about 20 species of scale insects. Couch(3) studied in detail this fungus-insect relation-ship, and it is from his treatise on the genus Sep-tobasidium that most present information is de-rived.The Septobasidium colony develops best on the

undersurface of the lower branches of trees, andis composed of a series of irregular concentricrings of annual growth. It can be as large as 30cm in diameter and 1.0 cm thick. Within the col-ony are numerous tunnels and chambers whichcontain the scale insects. The insects feed on thewoody host plant, and the fungus provides themwith shelter. However, some of the insects areparasitized and nourish the fungus. The youngscale insect contacts the yeastlike bud of the ger-minating basidiospore, which adheres to the bodysurface and initiates infection. Hyphae of thefungus enter the circulatory system of the livinginsect and there form numerous coiled haustoria.Growth of the fungus within the parasitized in-sect is exceedingly slow. Infected insects continueto feed on the host plant, but they are dwarfedand incapable of reproduction. Many of theyoung insects escape infection and remain to re-produce the species, while those that are parasi-tized nourish the fungus which provides shelterfor all. Unless insects are infected when young,they remain free from the fungus. Thus, fungusand insect live together interdependently.

BeauveriaBeauveria species are the best known of the

Deuteromycetes that parasitize insects. They arewidespread and frequently the most abundant offungi isolated from collections of dead insects.B. bassiana is the agent responsible for muscar-dine of the silkworm, the first disease of animalsdemonstrated to be of microbial origin, and re-ferred to previously. Although B. bassianra provedcostly to the silk industry, it can parasitize morethan 30 different insect species, including the cornborer, the codling moth, and the potato beetle,and is a favored subject for study by those con-cerned with biological control (10, 35, 36). Themorphology and taxonomy of Beauveria specieswere reviewed thoroughly by MacLeod (21), andBeauveria diseases of insects were described anddiscussed by Steinhaus (33) and Madelin (24).The infective unit in Beauveria diseases is the

spore. Tracheal openings or the digestive tractare possible routes of infection, but it appearsthat in most instances spores contaminating thesurface of the insect germinate and penetrate theintegument. Within the body cavity of the host,the fungus continues to develop. Hyphal bodiesare formed, blood cells are destroyed, and circula-tion is decreased in rate. Glandular structures and

ganglia may be invaded, and the fungus fre-quently enters tracheae, impairing respiration.An infected insect moves sluggishly and fails torespond to external stimuli. Eventually, there isgeneral paralysis, followed by death and mummi-fication of the host. Colonization of the dead in-sect culminates in the formation of a mass ofmycelium within the brittle integument. In a dryatmosphere, the fungus may lie dormant for pro-longed periods, but soon after exposure to moistair a mycelium develops over the surface of theinsect, and conidia are produced abundantlywithin 1 or 2 days. Since the conditions that favorsporulation are similar to those that favor infec-tion, the disease is transmitted from insect to in-sect and perpetuated within a population.

Beauveria species grow readily on a mediumthat contains glucose, ammonium-nitrogen, andinorganic salts only (22), and there is no diminu-tion of virulence with continued transfer of purecultures in the laboratory (19). Spore germina-tion and infection of host insects is favored byhigh humidity and is influenced by temperature(24). Penetration of the insect integument is usu-ally attributed to enzymatic mechanisms. Huber(18) demonstrated that B. bassiana hydrolyzedchitin, but in the presence of more simple sub-strates chitinase production by the fungus wassuppressed. It is possible that infectivity is a func-tion of the nutrient status of the environment.

INFECTIONS OF NEMATODESI wish now to direct your attention from fungi

that parasitize insects to those that parasitizenematodes. Nematode parasites comprise a het-erogeneous group that includes representativesfrom each of the major classes of fungi. They canbe divided arbitrarily into the nematode-trappingfungi and the endozoic fungal parasites (9).

Nematode-Trapping FungiMost of the nematode-trapping fungi are clas-

sified within the order Moniliales of the Deutero-mycetes, but some are Phycomycetes and at leastone is a Basidiomycete (6, 7). Although they aretaxonomically diverse, the nematode-trappingfungi are ecologically a natural group, united bytheir adaptation to the predaceous habit (4, 5).They are able to capture, kill, and consume wormsof microscopic dimension, and, for this purpose,produce specialized hyphal structures that aretruly remarkable. These organelles of capturevary greatly in form, but they trap nematodes byeither adhesion or occlusion.

In some species, the mycelium gives rise toone-celled processes, short branches, or sphericalknobs on aerial hyphae. In other species, brancheselongate and curl, and there may be considerable

384 PRAMER

on October 19, 2020 by guest

http://mm

br.asm.org/

Dow

nloaded from

VOL. 29, 1965 FUNGAL PARASITES OF INSECTS AND NEMATODES

anastomosis to form a three-dimensional systemof hyphal loops. In every case, these structuresare coated with a sticky secretion of unknowncomposition, and they capture nematodes by ad-hesion and entanglement. There are two types oftraps that function mechanically: the noncon-stricting and the constricting ring. Both are com-posed of three cells which join to form a closedring at the end of a short mycelial branch. Anematode entering the nonconstricting ring, andattempting to force its way through, becomesfirmly wedged and is unable to escape. Constrict-ing rings are active rather than passive. When anematode enters, the cells that comprise the ringswell to approximately three times their normalvolume, obliterating the opening and constrictingthe nematode so that it cannot escape. Ring clo-sure is a thigomotropic response and does not re-quire more than 0.1 sec. Whatever the species offungus or the trapping mechanism involved, acaptured nematode struggles for a time, dies, andis then penetrated by fungus hyphae which ram-ify throughout the carcass, digesting and absorb-ing its content. Under favorable conditions,nematodes may be captured in large numbers, butthe actual cause of death of a trapped worm isuncertain. It may be due to exhaustion or physicaldamage, but the production by the fungus of atoxin is a possibility that cannot be ignored (27,32).

Nematode-trapping fungi are not obligate par-asites. They grow readily in pure culture on avariety of laboratory media, but some species donot produce traps in the absence of prey. I havehad recent opportunity to summarize the resultsof work in my laboratory concerned with the nu-trition and biochemical basis of morphogenesis innematode-trapping fungi (29). Repetition and ex-tension here are tempting but not justified. Therehave been many laboratory, greenhouse, and fieldtrials performed in an effort to exploit the activ-ity of predaceous fungi for the control of nema-tode pests (8, 9). The results are promising, buthave never been decisive. Empirical attempts atbiological control will continue to be made, butthe work will be easier and the probability of suc-cess increased greatly if future tests have a ra-tional basis derived from fundamental investiga-tion and experimental fact (28). In testimony tothe validity of this statement, I will limit my dis-cussion of the many fungi that do not form traps,but are endozoic parasites of nematodes (9), tospecies of the genus Harposporium. The tale I tellis meant to emphasize the necessity of fundamen-tal fact as armament for the strategist who wishesto employ biological agents in a meaningful at-tack on insect and nematode pests.

HarposporiumNematodes infected with Harposporium were

first encountered by Lohde in 1874 (20), but theyoccur commonly in a variety of habitats, includ-ing soil, moss cushions, and decomposing plantand animal residues. Conidiophores of the fungusdevelop from a vegetative mycelium within thehost. They penetrate the integument, and, in air,bear crescentric or sickle-shaped spores withpointed tips. Several opinions have been expressedregarding the mechanism of infection by Har-posporium. The spores appeared too large to enterhost species by the oral route, and this possibilitywas rejected. Morphology was related to mode ofinfection, and it was suggested by some that thepointed tip, on impact, served to impale the nem-atode on the spore. However, most investigatorsagreed that a drop of mucilage secreted at thespore tip acted, on contact, to glue the spore tothe outer integument of the nematode. In 1959,with this dogma in mind, Feder and Duddington(11) decided to test the ability of Harposporiurnto control a nematode disease of plants. Their de-cision was undoubtedly based on the observationthat Harposporium species were widespread andapparently successful obligate parasites. More-over, there was need to compare endozoic fungusspecies with nematode-trapping species as agentsof biological control.An obligate parasite will develop in only living-

host tissue. Therefore, to obtain adequate suppliesof Harposporium for laboratory and field studies,Feder and Duddington (11) reared, infected, andthen lyophilized thousands of nematodes. Re-grettably, their efforts were in vain, for, as theylabored to accumulate nematode tissue infectedwith Harposporium, Aschner and Kohn (1) re-ported that the organism is not an obligate para-site, that it has no specialized nutrient require-ments, and that it will develop readily on aglucose-inorganic salts medium containing am-monium-nitrogen. Harposporium parasitizes nem-atodes of the Rhabditis group that feed on partic-ulate matter, but is unable to infect stylet-bearingspecies of the genus Dorylaimus that consumefluids only. To determine the mode of invasion ofhost by the fungus, Aschner and Kohn (1) exam-ined early stages of infection of rhabditic nema-todes. Spores did not adhere to living worms, andthe fungus was never observed to penetrate thenematode integument. Infection of nematodes byHarposporium species proceeds by the oral routeonly. Harposporium spores are long but they areslender and can be swallowed. Entrance is facil-itated by the nematode itself, for the worm mod-ifies the dimensions of its alimentary tract wheningesting particles that vary in size and shape.

38 5

on October 19, 2020 by guest

http://mm

br.asm.org/

Dow

nloaded from

BACTERIOL. REV.

These observations are of the utmost significanceand necessitate a complete re-evaluation of Har-posporium species as agents for the biological con-

trol of nematode pests. The fact that these fungiare widespread may be a reflection of their sapro-

phytic rather than their parasitic ability. More-over, most economically important species ofnematodes have mouth parts that are modifiedto form a needlelike stylet for sucking. Since thestylet opening is less than 1 Au in diameter and willnot pass spores, no successful control of a popula-tion of plant parasitic nematodes can be expectedfrom Harposporium, or from any other fungalparasite that must enter its host by the oral route.

COMMENTS CONCERNING MICROBIAL CONTROL

There is at present a great desire to direct mi-crobial parasites against economically importantagricultural pests. This interest derives in partfrom the fact that field collections of insects andnematodes frequently contain infected specimens.It is due also to recurring reports in which micro-organisms are described as responsible, in nature,for dramatic reductions in the density of insectpopulations. However, present concern must beattributed primarily to the undesirable effects ofpersisting residues of chemical pesticides and torecognition of an increase in both degree and in-cidence of resistance of pests to these chemicals.The numerous individual attempts to controlinsects and nematodes with fungal parasites can-

not be considered here. Fortunately, they havebeen compiled and recently reviewed by others(2, 8, 9, 12, 13, 14, 33, 35, 36). The usual approachto microbial control has been empirical. Fre-quently, published reports reflect a lack of thor-oughness in experimental design, procedures are

not described fully, and results are often inde-terminate or inconclusive. Nevertheless, Baird(2), after reviewing the enormous quantity ofwork that has been done in this field, cites as suc-

cessful some 41 attempts to employ fungi for thecontrol of 28 different insect pests, and the po-tentialities of many of these fungi are in the proc-ess of being reappraised (13, 14).

Microbial control has intellectual and popularappeal and support, but it is among the most dif-ficult of tasks to accomplish. The degree of success

achieved is frequently a direct function of avail-able knowledge of the system under study. Stein-haus (33) has emphasized that disease is to beregarded as a process and not a thing. It is nec-

essary that the factors which initiate and controlthis process be identified, and that investigationsbe performed to reveal the biochemical basis ofthe host-parasite relationship. This is not meantto imply that understanding will assure success,

but the cause of an applied biologist interested inusing microorganisms for the control of pests willbe advanced greatly if he bases his efforts on re-liable information concerning both parasite andhost, acting individually and as an integrated unitunder a variety of environmental conditions.Much remains to be accomplished, but I wish tostress that there is more to fungal parasites of in-sects and nematodes than their application. Theycomprise an engaging group and provide the in-terested investigator with a unique opportunityto apply the principles and techniques of con-temporary microbiology and to contribute to ourunderstanding of fungi and fungal infections.

ACKNOWLEDGMENTSThis investigation was supported by National

Science Foundation grants G19211, GB-548, andGB-1508.

LITERATURE CITED1. ASCHNER, M., AND S. KOHN. 1958. The biology

of Harposporium anquillulae. J. Gen. Mi-crobiol. 19:182-189.

2. BAIRD, R. 1958. Use of fungous diseases inbiological control of insects. Intern. Congr.Entomol. Proc., 10th, Montreal 4:689-692.

3. COUCH, J. N. 1938. The genus Septobasidium.Univ. of North Carolina Press, Chapel Hill.

4. DRECHSLER, C. 1937. Some Hyphomycetesthat prey on free-living terricolous nema-todes. Mycologia 29:447-552.

5. DRECHSLER, C. 1941. Predaceous fungi. Biol.Rev. Cambridge Phil. Soc. 16:265-290.

6. DRECHSLER, C. 1949. A nematode-capturingfungus with anastomosing clamp-bearinghyphae. Mycologia 41:369-387.

7. DUDDINGTON, C. L. 1956. The predaceousfungi: Zoopagales and Moniliales. Biol.Rev. Cambridge Phil. Soc. 31:152-193.

8. DUDDINGTON, C. L. 1960. Biological control-predaceous fungi. p. 461-465. In J. N. Sasserand W. R. Jenkins [ed.], Nematology. Univ.of North Carolina Press, Chapel Hill.

9. DUDDINGTON, C. L. 1962. Predaceous fungiand the control of eelworms, p. 151-200. InJ. D. Carthy and C. L. Duddington [ed.],Viewpoints in biology, vol. 1. Butterworthand Co., London.

10. DUTKY, S. R. 1959. Insect microbiology. Ad-van. Appl. Microbiol. 1:175-200.

11. FEDER, W. A., AND C. L. DUDDINGTON. 1959.Freeze drying of Harposporium anquillulaein its nematode host. Nature 183:767-768.

12. HALL, I. M. 1961. Some fundamental aspects ofapplied insect pathology. Advan. Pest Con-trol Res. 4:1-32.

13. HALL, I. M. 1963. Microbial control, p. 477-517. In E. A. Steinhaus [ed.], Insect pathol-ogy, vol. 2. Academic Press, Inc., New York.

14. HALL, I. M. 1963. The use of microbial agents

386 PRAMER

on October 19, 2020 by guest

http://mm

br.asm.org/

Dow

nloaded from

FUNGAL PARASITES OF INSECTS AND NEMATODES

for control of noxious insects. Develop.Ind. Microbiol. 4:148-152.

15. HALL, I. M., AND J. V. BELL. 1960. The effectof temperature on some entomophthorace-ous fungi. J. Insect. Pathol. 2:247-253.

16. HALL, I. M., AND J. V. BELL. 1961. Furtherstudies on the effect of temperature on thegrowth of some entomophthoraceous fungi.J. Insect Pathol. 3:289-296.

17. HOFFMAN, W. E. 1947. Insects as human food.Proc. Entomol. Soc. Wash. 49:233-237.

18. HUBER, J. 1958. Untersuchungen zur Physio-logie insektent6tender Pilze. Arch. Mikro-biol. 29:257-276.

19. LEFhBVRE, C. L. 1931. A destructive fungousdisease of the corn borer. Phytopathology21:124-125.

20. LOHDE, G. 1874. Ueber einige neue parasitischePilze. Ges. Deut. Naturf. Artze. Tagebl.Vers. 47:203-206.

21. MAcLEOD, D. M. 1954. Investigations on thegenera Beauveria Vuill. and TritirachiumLimber. Can. J. Botany 32:818-890.

22. MACLEOD, D. M. 1954. Natural and culturalvariation in entomogenous Fungi Imper-fecti. Ann. N.Y. Acad. Sci. 60:58-70.

23. MACLEOD, D. M. 1963. Entomophthoralesinfections, p. 189-231. In E. A. Steinhaus[ed.], Insect pathology, vol. 2. AcademicPress, Inc., New York.

24. MADELIN, M. F. 1963. Diseases caused byhyphomycetous fungi, p. 233-271. In E. A.Steinhaus [ed.], Insect pathology, vol. 2.Academic Press, Inc., New York.

25. MATHIESON, J. 1949. Cordyceps aphodii, a new

species, on pasture cockchafer grubs. Trans.Brit. Mycol. Soc. 32:113-136.

26. Mc EWEN, F. L. 1963. Cordyceps infections,

P. 273-290. In E. A. Steinhaus [ed.], Insectpathology, vol. 2. Academic Press, Inc.,New York.

27. OLTHOF, T. H. A., AND R. H. ESTEY. 1963. Anematotoxin produced by the nematopagousfungus Arthrobotrys oligospora. Nature 197:514-515.

28. PRAMER, D. 1964. Nematode-trapping fungi.Science 144:382-388.

29. PRAMER, D., AND S. KUYAMA. 1963. Nemin andthe nematode-trapping fungi. Bacteriol.Rev. 27:282-292.

30. SAWYER, W. H. 1929. Observations on someentomogenous members of the Entomoph-thoraceae in artificial culture. Am. J. Botany16:87-121.

31. SMITH, M. C. W. 1953. The nutrition and physi-ology of Entomophthora coronata. Rev. Appl.Mycol. 33:441.

32. SOPRUNON, F. F., AND Z. A. GALUILINA. 1951.Predatory Hyphomycetes from the soil ofTurkmenistan. Mikrobiologiya 20:489-499.

33. STEINHAUS, E. A. 1949. Principles of insectpathology. McGraw-Hill Book Co., Inc.,New York.

34. STEINHAUS, E. A. 1956. Microbial control-theemergence of an idea. Hilgardia 26:107-159.

35. STEINHAUS, E. A. 1957. Microbial diseases ofinsects. Ann. Rev. Microbiol. 11:165-182.

36. TANADA, Y. 1959. Microbial control of insectpests. Ann. Rev. Entomol. 4:277-302.

37. WILLIS, J. H. 1959. Australian species of thefungal genus Cordyceps with critical noteson collections in Australian herbaria. Muel-leria 1:67-89.

38. WOLF, F. T. 1951. The cultivation of twospecies of Entomophthora on synthetic media.Bull. Torrey Botan. Club 78:211-220.

387VOL. 29, 1965

on October 19, 2020 by guest

http://mm

br.asm.org/

Dow

nloaded from