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MUSHROOMS AND MOLDS: HABITS AND HABITATS1

C. WAYNE ELLETT2 Department of Pathology, Ohio State University, Columbus, OH ^3210 Cooke, in an article in the Ohio Journal find them fascinating organisms existing of Science in 1973, describes the fungi as in an amazing variety of form and hab- "eukaryotic, nonchlorophyllous, reducer itat. The fungi have exerted a profound organisms which occupy specific niches effect on the life of man. They have in all environments." He goes on to say, been the objects of wonder and. specula- "they are integral parts of any ecosystem, tion from the time of earliest record. natural or artificial, which may be de- Pliny in the first century A.D. wrote, limited." "Among the most wonderful of all things We do not have a catalogue of Ohio is the fact that anything can spring up fungi so no one knows how many species and live without a root." It is not my actually occur in Ohio, but I have esti- intent to report details of research investi- mated, that there are 5000 to ()()()() species gations, but to indicate a few of the vari- or about twice the number of seed ous roles of fungi in our environment. (Ellett 1957). It is interesting to note The microscopic fungus, Phytophthora that Cooke (1973a) records some 138 infestans, parasitizes potato plants and species of fungi collected in his own back- sporulates on the underside of potato yard, a lot 50 x 142 feet. This number, leaflets (fig. 1). This mold devastated he admits, could be increased consider- the potato crop in Ireland and elsewhere ably through routine soil sampling and in Europe 125 years ago and caused the other studies. Reports of soil fungi in Irish famine. Montagne, Berkeley, Lind- Ohio by Huang and Schmitt (1975) and ley, and others studied this fungus and by Williams and Schmitthenner (1965) argued about whether it was the cause or and their students, support this conten- the result of the potato blight, while Sir tion. In 1955, I compiled a list of nearly Robert Peel, in a speech in the House of 1000 species of plant parasitic fungi in Commons in London, used the famine in Ohio (Ellett 1957) and during the last Ireland as an excuse for advocating repeal 20 years, have collected and identified of the Corn Laws which prohibited the dozens of previously unreported species. import of cheap grain (Large 1940). For more than 30 years, I have col- Thus, a microscopic mold was responsible, lected, studied and read about fungi and at least in part, for establishing the British policy of free trade—a happening Manuscript received May 11, 1977 and in revised form June 27, 1977 (#77-39). which some have said was the most "PRESIDENTIAL ADDRESS—Presented significant in the entire history of Britain. at the 86th Annual Meeting of the Ohio Acad- and numerous other grass species emy of Science held at Capital University, Columbus, OH, April 23, 1977. Dr. C. Wayne serve as a habitat for the fungus Claviceps Ellett, retiring president of the Ohio Academy purpurea, where it produces the ergot of Science, is a Professor of Plant Pathology sclerotia (fig. 2). Much has been written and Director of the Plant Disease Clinic at about the gangrenous and convulsive The Ohio State University. He is a specialist in ornamental plant, cereal, and forage crop ergotism that occurs in man and animals diseases. Wayne Ellett received his B.S. from after eating ergoty grain or products Kent State University in 1938 and his M.S. made from it. Ergotism was an espe- and Ph.D. degrees from Ohio State University cially serious problem in Europe from the in 1940 and 1955, respectively. Dr. Ellett's writings have appeared in many scientific and earliest times and even into the 20th professional journals and he is widely known as Century. This fungus had its impact on a speaker on mushrooms spp. He is a fellow, history when an oubtreak of ergotism in past president, and past treasurer of the Ohio the cavalry of Peter the Great in 1722 pre- Academy of Science as well as a member of the Mycological Society of America, the American vented him from undertaking a campaign Phytopathological Society, the North Ameri- against Turkey because 20,000 Russian can Mycological Association and Sigma Xi. soldiers were reported to have died from 155 156 C. WAYNE ELLETT Vol. 77

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FIGURE 1. Phytophthora infestans, a microscopic fungus that parasitizes potatoes causing late blight. FIGURE 2. Sclerotia of the ergot fungus Claviceps purpurea growing on rye inflorescences. the disease. Caporeal (1976) attempted The threat of downy mildew to the to relate the occurrence of the Salem French wine industry was so great that witchcraft trials of the 169()'s to the other Mediterranean countries made ex- ergot fungus—suggesting those accused tensive plantings of grapes, anticipating were suffering from convulsive ergotism. a wine market for the thirsty French. One of the alkaloids produced by the ergot Millardet's Bordeaux mixture solved the fungus is ; upon which mi- downy mildew problem and grape over- graine sufferers around the world depend production in these countries caused an for relief. Although rare in humans, economic crisis (Alexopoulos 1962). ergotism in animals still occurs today due Moving to modern times, in the early to grazing on diseased pasture grasses. I 197()'s the fungus Bipolaris maydis re- have identified ergot in Ohio on 19 grass duced corn yields in the USA by 10-15% species—some of which are first reports or 700 million bushels. This would be for the United States. Agropyron repens worth $1 billion or when fed to cattle (quack grass) is probably the commonest would have produced nearly 8 billion host grass in Ohio for ergot. Few have one-pound steaks. Many metropolitan seen the spore-producing stage of the newspapers wrote about corn for the first ergot fungus because it is so small and time and informed their readers on the arises from sclerotia buried in the soil. front page about Zea mays and Helmin- Downy mildew, a fungus on grapes, thosporium maydis (as the fungus was was our gift to the French in the 187()'s. then called). This resulted in the great- The resulting disease provided the est financial loss due to a plant disease groundwork for Professor Millardet's de- in the history of U.S. agriculture. It velopment of Bordeaux Mixture [O1SO4 was the first example of a cytoplasmic + Ca(OH)2]; a fungicide still widely used. factor being primarily responsible for Ohio J. Sci. MUSHROOMS AND MOLDS 157 conditioning susceptibility to a pathogen for this synthesis. The story of events which resulted in a major plant disease. leading to the discovery of the Fusarium roseum is a fungus that as the cause of death of 100,000 turkeys causes an ear and kernel rot of corn. in England in the early 196()'s reads like Under some conditions as it grows in a detective novel. Bx was re- corn , a hormone-like sub- ported to be the most carcinogenic stance, is produced which causes the naturally-occurring substance known. estrogenic syndrome in swine. The same The LD50 to various animals ranges from fungus, under other conditions, may pro- 0.3 mg/kg body weight for ducklings to duce one or more . One 9.0 mg/kg for mice. In addition to be- of these, vomitoxin, functions as an ing a carcinogen aflatoxin Bi is also a emetic and/or refusal . Hogs will teratogen and a mutagen (Ciegler 1975). starve rather than eat corn, if this my co- toxin is present. There are many other For a number of years I have observed examples in an area of research known and briefly investigated a disease of the as mycotoxicology and the extent of adderstongue fern, Ophioglossum vul- contamination of food and gatum, caused by Curvularia crepini feed has only been realized in recent years. (fig. 4). The disease and fungus were Aspergillus flavus is a very common fun- first collected in Belgium in 1859 and the gus and grows in a variety of habitats only report from the Western Hemisphere (fig. 3). Under certain conditions and is from Columbus, Ohio, where it has on some substrates such as peanuts, cot- been regularly identified during the past ton and copra, a group of toxic metabo- 20 years (Ellett 1956). From examina- lites referred to as aflatoxins are syn- tion of herbarium specimens of Ophio- thesized. Fortunately, our major feed glossum it is evident that Curvularia grains and soybeans are low risk crops blight was present in Ohio as early as

FIGURE 3. Aspergillus flavus growing on corn grains. FIGURE 4. Curvularia crepini conidia of the blight that causes Curvularia blight of the adderstongue 158 C. WAYNE ELLETT Vol. 77 1901 and this fungus may be much more the past 25 years. The inciting fungus common than reports indicate. (Ceratostomella ulmi) of the Dutch, elm Another interesting host-fungus associ- disease is efficiently transmitted by the ation is the systemic rust fungus, Chryso- bark beetle, Scolytus multistriatus. The myxa pirolata on Pyrola elliptica. It is a fungus, the bark beetle, and the disease heteroecious rust fungus with species of are now found from New England to Picea (spruce) as alternate hosts. There California and have resulted in the elimi- are no reports on record of the fungus on nation from many cities of a shade tree our present-day introduced spruces in that was once considered to be the best Ohio. Since Pyrola is the host of the repeating stage of the rust fungus, it can persist in the absence of the spruce hosts. One may speculate this rust became established on Pyrola during the most recent glacial and immediate post-glacial times when Picea species probably were numerous in central and southern Ohio, and persisting since on the Pyrola host via the uredinial phase, which is the re- peating stage in the life cycle. Although many individuals have seen the corn smut fungus (Ustilago maydis), few have seen the smut fungus that oc- curs on fire pink, a species of Silene. This smut fungus, Ustilago violacea, parasitizes several members of the Caryo- phyllaceae causing anther smut. It is detected on Silene by examining the anthers and finding smut spores instead of pollen. The only reports or collections of the fungus in Ohio are those I have made, but few of the 10 million plus Ohioans have spent much time squeezing the anthers of Silene stamens. There were several instances where rust fungi have provided valuable infor- mation to plant taxonomists. Accord- FIGURE 5. Cerotelium dicentrae: aecial stage ing to Holm (1969), the true affinities of on Dicentra (Dutchman's Breeches) leaves. the grass genera, Molinia and Spartina have been clarified by studying the rusts parasitic on them. It has been observed available. A recent report indicates 75% repeatedly that a rust fungus regularly of the American elm population has been differentiates between two species of eliminated in 12 northeastern states. Dicentra. Cerotelium dicentrae occurs on Interest in mushroom fungi in Ohio and Dutchman's breeches but not on squirrel elsewhere in the United States on the corn, even though the leaves of the two part of non-professionals has increased species are morphologically indistinguish- greatly in recent years. Mycological able. This rust has been collected over clubs and organizations have increased a period of years in Ohio in an area in number and in membership. The where both Dicentra species are common, North American Mycological Association, and I find it only on Dutchman's breeches an example of one such organization, (fig. 5). started in Ohio in 1960 with a small Insects and fungi are associated in a group meeting in Scioto County. With number of ways. One such relationship help and encouragement from several pro- resulted in the gradual elimination of the fessional mycologists, it now has a mem- American elm in the United States over bership of nearly 1000 and has annual Ohio J. Sci. MUSHROOMS AND MOLDS 159 forays with more participants than the sold at an average price of $1.50 a pound. forays of the professional Mycological At that time some 50 species were ap- Society of America. proved for sale in the Geneva markets World production of cultivated mush- (Weber 1964). A number of the wild rooms is about 1.3 billion pounds (San mushrooms are dried or canned, and Antonio 1975) and nearly 75% of this marketed in other countries. An Asso- production is Agaricus bisporus. Second ciated Press news release early in 1977 in importance is the Shiitake mushroom, reported that officials in Finland em- Lentinus edodes, which is cultivated in barked on a project to exploit their Japan on logs of Quercus (oak) and sev- naturally-occurring crop of edible mush- eral other genera. The paddy straw rooms. The report suggests the collec- mushroom, Volvariella volvacea, is culti- tion and sale of mushrooms would make a vated in southeast Asia on the sub- healthy contribution to the Finnish econ- stratum of straw. omy. Examples of some extensively col- Several .species of truffles are widely lected wild mushrooms include Boletus collected for eating and include Tuber edulis, Suillus luteus, Leccinum species melanosporum and Tuber griseum in (rig. 6), Morchella species (fig. 7), Can- southern Europe and Tirmania africana tharellus cibarius (fig. 8), certain species in northern Africa (Singer 1961). The of Tricholoma, Lactarius and Termito- black truffle of France {Tuber melano- myces. All except Termitomyces are found sporum) is a semicultivated species. It is in both Europe and the United States. apparently mycorrhizal with several tree species and in France, oak plantations Although many wild mushrooms are established for the express purpose of are food delicacies, there are many obtaining crops of truffles. In Europe, species that are toxic and no simple one can purchase young oak {Quercus) test is known for distinguishing them. and hazel {Corylus) trees that have roots There is an old saying, "There are with truffle mycelium already present, old mushroom hunters, and bold which when planted and cultivated for mushroom hunters, but there are no 8 or 10 years will yield a truffle garden. old, bold mushroom hunters." The natural distribution of the black Much has been written about poisonous truffle is mostly between 44° and 46° N mushrooms and mushroom , and latitude and primarily in France, Spain differences of opinion and misinformation and Italy. The truffles are hypogeous are easily found in the medical and Ascomycetes, not much to look at—but mycological literature. In part, these they are expensive, and reported to retail differences can be explained by problems for more than $100 a pound. Annual in the identification of certain species, production has been estimated at more and the continued republication of earlier than 3 million pounds in some earlier reports now known to be incorrect. The years but it is not likely such quantities taxonomy of some of these problem are marketed today. genera has been clarified in the last few Other mushrooms cultivated, in a more years and much has been learned in limited way, include the Ear Fungus, recent years about some of the mush- which is a species of Auricula; the oyster room toxins. The Amanita toxins ac- mushroom (a species of Pleurotus); Fla- count for nearly all deaths from eating mulina velutipes (the winter mushroom); poisonous mushrooms worldwide. The and a species of Tremella, which is one of number of deaths in the United States is the jelly fungi used extensively as food not great but reliable records are not by the Chinese people. available. The collection and use of wild mush- The mushrooms reported to contain rooms for food is extensive, especially in Amanita type toxins include A. verna, A. some European countries. Marketing virosa, A. bisporigera, A. phalloides and of edible wild species is governed in many certain species in the genera Galerina and areas by local ordinances. On the mar- Conocybe. The latter genera are not kets of Geneva, Switzerland in 1963, closely related to the Amanitas and 70,000 pounds of wild mushrooms were fortunately are not likely to attract the 160 C. WAYNE ELLETT Vol. 77 attention of those collecting edible mush- variation in the effects on consumers of rooms. Amanita bisporigera is common this mushroom when collections from in Ohio, as is A. virosa. Recent research Mexico were compared with those from indicates the toxins in A. virosa are not the Houston area. They report that P. the Amanita toxins. Amanita phalloides cubensis occurs almost exclusively in is common in Europe and has been found pastures on decomposing cow dung and in a few areas of the United States, but in early hours of the morning, cows and not in Ohio. The principle toxins in young people compete for the fresh these mushrooms are cyclo-peptides, the basidiocarps. Cows grazing on the mush- and . The lethal room are not visibly affected, but young dose of for humans is approxi- people consume it for psychedelic ex- mately 0.1 mg/kg of body weight. The periences. Any mushrooms escaping toxicity of phalloidin is much lower, the cows and people are rapidly decomposed LD50 for mice being about 2 mg/kg body by ants. In Texas there have been many weight. Some basidiocarps of A. bi- reports of individuals suffering gastro- sporigera may contain as much as 10 to intestinal discomfort after partaking of 15 mg of the amatoxins, thus one mush- P. cubensis, and one victim reported room provides enough toxin to be lethal nausea, cramps, and vomiting along with for an adult. hilarity. It seems apparent that the kind The amatoxins are hepatic toxins and and quantity of hallucinogens and/or the extent of liver injury is indicated by other toxins may vary considerably in a marked elevation in levels of serum collections of the same morphologic glutamic-oxaloacetic and glutamic-pyru- species. vate transaminases. Over the years Mushrooms containing the toxins ibo- there has been no satisfactory method of tenic acid and include the treating patients poisoned by the Ama- widely distributed Amanita muscaria nita toxins—the result being a death rate (fig. 9) and probably Amanita panthe- of nearly 50%. Recently, treatment with rina, a species common in the Pacific thioctic acid, however, has shown promise northwest. Muscarine was reported at in counteracting the effects of the ama- one time to be the principal toxin in A. toxins and has been widely used in muscaria and atropine was prescribed as Europe and more recently in this country. the antidote. It is now clear that this In Columbus last year, thioctic acid species contains physiologically insig- therapy was used for two persons who nificant amounts of muscarine, yet the dined on a mixture of Amanita bispori- early reports found their way into many gera and A. virosa and both patients of the most recent medical and toxicology survived. texts, which recommend treatment with The hallucinogenic mushrooms have atropine, which if given, complicates the received considerable attention in recent problem. years. Mushrooms with active halluci- and muscimol are iso- nogenic principles are known in the gen- xazole derivatives and have neurological era Conocybe, Psilocybe, Panaeolus and effects. Amanita muscaria was used ex- Stropharia. Most of these species are tensively in parts of Siberia and probably small and are not likely to be collected by elsewhere for its psychoactive effects. the mycophagist. Some occur in lawns The effects of this mushroom are not the and other grassy areas and could easily typical hallucinogenic syndrome seen be involved in poisoning in young child- with LSD and psilocybin. The psycho- ren. The toxins are indole derivatives, active compounds are not metabolized psilocybin and psilocin, which affect the by the body and primitive peoples were central nervous system. Some states aware they could get a psychedelic re- have passed laws prohibiting the posses- sponse by saving and drinking urine. In sion of psilocybin-containing mushrooms. a report in the Mycologia, a woman in- Psilocybe cubensis is a species occurring toxicated with Amanita pantherina was in southern Texas, Florida, Cuba, and quoted as imagining herself in hell and Mexico. In a recent study, Jackson and concluding it was not as bad a place as Alexopoulos (1976) found considerable some people would have us believe. Ohio J. Sci. MUSHROOMS AND MOLDS 101

FIGURE 6. Leccinum sp.: one of the common edible fleshy pore fungi. FIGURE 7. Morchella esculenta: an example of one of the edible morels. FIGURE 8. Cantharellus cibarius: the widely collected edible chantarelle. FIGURE 9. Amanita muscaria: the fly mushroom, an example of a poisonous mushroom. 162 C. WAYNE ELLETT Vol. 77 Often reported as deadly, the mushrooms We owe much to McKnight (1971; 1973) in this group are not highly toxic, al- for clarifying the taxonomy of this genus though I am not suggesting they are in the United States. Considering all edible. There are no specific antidotes the problems, toxicologic and taxonomic, for treating intoxication caused by these one is well advised to avoid eating false two Amanitas, but prognosis for recovery morels in spite of the many mushroom is excellent. books reporting some species as edible. Much confusion has existed relative to The muscarine-containing species of the toxins in the false morels {Gyromitra mushrooms include several species of spp.) and whether or not certain species Inocybe and Clitocybe. Some of these of the genus are poisonous or edible. The species occur in lawns or under trees near situation has been clarified somewhat due homes and therefore are likely to be eaten to better concepts of the species, and by young children. As much as 1% verification of the toxin as monomethyl muscarine on a dry weight basis is found hydrazine or its derivative; not helvellic in some species. Muscarine stimulates acid as originally thought. Monomethyl the parasympathetic nervous system. hydrazine has been used as a rocket fuel The symptoms include increased sweat- and its toxicity extensively investigated ing, salivation, lachrimation, reduced by the U.S. Air Force. It affects the cen- blood pressure, blurred vision, asthmatic tral nervous system, and the mystery of breathing, nausea and severe vomiting. why one meal of Gyromitra might cause Muscarine is not a central nervous system no effect, while the second one would toxin as sometimes reported. Atropine cause serious illness or even death, can is a specific antidote for this type of now be explained. It has been found poison. Determination of species of there is an extremely narrow limit be- Clitocybe and Inocybe is not easy and the tween a no-effect and a lethal dose of genera should be avoided by the my- monomethyl hydrazine. Gyromitra escu- cophagist. lenta has been eaten by many individuals Consumption of alcohol after a meal of and this leads one to speculate how many Coprinus atratnentarius, one of the inky persons have come close to the ragged cap mushrooms, has been repeatedly re- edge—one more bite or meal may have ported to result in symptoms resembling been disastrous. The toxin of this mush- the antabuse syndrome. There is a room is volatile and a recent report sug- substance in this mushroom which inter- gests this may explain the cases of intoxi- feres with the normal activity of enzymes cation reported from Europe in persons metabolizing ethanol, which has recently exposed to vapors during the commercial been identified as a glutamine complex processing of G. esculenta. The second and given the common name coprine. problem involved with Gyromitra is that A number of other mushrooms have it is not possible to accurately identify been identified as causing intestinal up- and separate the species with any mush- room guide available in this country. In fact, one is likely to misidentify them. I have studied the genus for a number of years and have become aware of problems of identifying the species, especially if one makes the mistake of referring to more than one book. Gross morphology cannot be relied on to separate the spe- cies—and this is, of course, what most mushroom collectors use. Characteris- tics of the ascospores must be determined and the ascospores must be mature. Spore size, shape and markings change with age, and this has been another source of error in the literature. Spores may ap- FIGURE 10. Clitocybe illudens: the Jack-O- pear to be mature when they are not. Lantern mushroom. It is bright orange and mildly poisonous. Ohio J. Sci. MUSHROOMS AND MOLDS 103 sets—mild to severe. Symptoms usually Ciegler, A. 1975 : occurrence, chemistry, biological activity. Lloydia 38: terminate within 3-4 hrs. and recovery is 21-35. complete in a day or two. Although Cooke, W. B. 1973 Some backgrounds for their toxins have not been identified, ex- an Ohio Mycobiota. Ohio J. Sci. 73: 83-88. amples include Lepiota morgani, with a Cooke, \V. B. 1973a Back-yard fungi. Ohio I. Sci. 73:88-96. greenish spore print, the beautiful Clito- Ellett, C. W. 1957 The parasitic fungi of cybe illudens (fig. 10), Russula emetica, Ohio plants. Ohio J. Sci. 57: 236-242. and Cantharellus floccosus. 1956 Curvularia blight of Ophioglos- suni. Plant Disease Rcptr. 40: 750. In conclusion, I wish to quote M. C. Holm, L. 1969 An uredinological approach to Cooke, a 19th century British mycologist, some problems in angiosperm taxonomy. who also believed the fungi to be fascinat- Nytt Mag. Bot. 10: 147-150. Huang, L.'H. and J. A. Schmitt 1975 Soil ing organisms worthy of more under- microfungi of central and southern Ohio. standing and study for either their harm- Mycotaxon 3: 55-80. ful or beneficial activities. In his book Jackson, R. E. and C. J. Alexopoulos 1970 on British Fungi, published in 18(52, he Psilocybe cubensis (Agaricales): A comparison writes, of Mexican and Texas types. Southwestern Naturalist 21: 227-233. "Let me assure the student that, all. Large, 15. C. 1940 The advance of the fungi. Henry Holt and Co., New York. 488 p. times, seasons, and localities will af- McKnight, K. H. 1971 On two species of false ford him some species for examina- morels (Gyromitra) in Utah. The Great tion; and whether he has felt in- Basin Naturalist 31: 35-47. terested in them before, or now for 1973 Two misunderstood species of Gyromitra (false morels) in North America. the first time, adopts these interest- Michigan Bot. 12: 147-162. ing plants as objects worthy of his San Antonio, J. P. 1975 Commercial and special regard, I would commend small scale cultivation of the mushroom, them to his patient and persevering Agaricus bisporus (Lange) Sing. Hort. Sci. 10:451-458. attention, in the assurance that this Singer, R. 1961. Mushrooms and truffles. pursuit will lead 'from joy to joy'." Interscience Publishers, Inc. New York. 272 p. LITERATURE CITED Weber, C. 1964 The popularity of edible mushrooms in Geneva. Econ. Botany. 254- Alexopoulos, C. J. 1962 Introductory My- 255. cology. 2nd ed. John Wiley and Sons. Williams, L. E. and A. F. Schmitthcnner 1956 Caporael, Linnda R. 1976 Ergotism: The Genera of fungi in Ohio soils. Res. Circular Satan loosed in Salem. Science 192: 21-26. No. 39. Ohio Agri. Exp. Station. 7 p.