ROOT ROT OF THE GRAPEVINE IN MISSOURI CAUSED BY CLITOCYBE TABES GENS (SCOP.) BRES.12

By ARTHUR S. RHOADS Assistant Plant Pathologist, Agricultural Experiment Station of the 'University of Florida; formerly Pathologist, Missouri State Fruit Experiment Station

INTRODUCTION Australia and some other countries "white-rot. " According to Verge (Ô6)4 Shortly after the writer had as- the cause of pourridié in Europe is at- sumed his duties at the Missouri tributed to several of the higher fungi, State Fruit Experiment Station in 1922 among them being Armillaria mellea his attention was directed to reports (Fries) Quel., Dematophora necatrix received from several localities of the Hartig, Vibrissea (Roesleria) hypogaea destruction of grapevines caused by Ch. Richon and Le Monnier, and some- root rot. The first opportunity to in- times Psathyrella ampelina Foex and vestigate this disease was afforded by a Viala. In the United States the dis- trip to Knobview, Mo., on May 30, ease has sometimes been attributed to 1922, where, in the vineyard from these fungi and also to Phymatotrichum which the trouble was reported, a (Ozonium) omnivorum (Shear) Duggar. number of vines that had recently died Most American writers, however, have were carefully dug up. All exhibited generally believed that the disease in the same symptoms, namely, an abund- this country is caused by Armillaria ant growth of characteristic whitish to mellea and Dematophora necatrix {51 y isabelline mycelial sheets or mats oc- p. 172-17Jf), although as a rule on as- curring between the layers of the immer sumption rather than from definite bark and between the bark and the evidence. wood of the roots and root crown, oc- Root rot of the grapevine was first casionally accompanied by black rhizo- reported in this country in Missouri, morphic strands. These symptoms in- Scribner (46, p. 137) stating that it dicated that the disease was caused was discovered in a vineyard at Bush- by a mushroom root rot, although no berg, about 25 miles south of St. Louis, fruiting bodies could be found to verify by the eminent French viticulturist the supposition. Cultures and further Viala, in 1887, while the two were field studies were made which afforded making a tour of the principal grape- a basis for the conclusions herein growing regions of the United States. reported.3 The same author also states (Jft, p. 12; 48, p. 64) that they found the disease HISTORICAL REVIEW later in northeastern Texas and again in Napa Valley, Calif. He records the Although grapevines are known to be fact that he has seen a number of vines attacked by several different root rot- nearly or quite dead from the same ting fungi, especially when the root disease in the vicinity of Knoxville, systems have become weakened or in- Tenn. jured, comparatively few investigations In 1892 Pierce (38 p., 153-161), dis- have been made in this country of cussing the relation of root-attacking the resulting diseases. fungi to the California vine disease, Root rot of the grapevine has long states that Dematophora, although been known in Europe, where it has found in several places in the United been investigated extensively. In States, had not been seen in California; France it is called "blanc des racines" that Armillaria mellea has been re- or, more commonly, "pourridié;" in ported in northern California; and Germany " Weinstock-fäule;" and in that Vibrissea hypogaea was found in

i Received for publication May 19, 1924; issued April, 1925. 2 Commonly known in this country under the names Clitocybe monadelpha (Morg.) Sacc, Armillaria mellea exannulata Peck, Clitocybe parasítica Wilcox, and Monadelphus caespitosus (Berk.) Murrill. 3 The writer gratefully acknowledges helpful advice and suggestions concerning the taxonomic treat- ment of the fungus under discussion from Dr. E. A. Burt of the Missouri Botanical Garden, Dr. L. O. Overholts of the Pennsylvania State College, and C. G. Lloyd of the Lloyd Library and Museum at Cincinnati. Grateful acknowledgment is made of the invaluable services rendered by the libraries of the Missouri Botanical Garden and the U. S. Department of Agriculture. 4 Reference is made by number (italic) to "Literature cited," p. 364.

Journal of Agricultural Research, Vol. XXX, No. 4 Washington, D. C. Feb. 15, 1925 Key No. Fla.-2 (341) 342 Journal oj Agricultural Research Vol. XXX, No. 4 the Santa Ana Valley on the roots of that all of these were affected by root vines which had been brought from rot, they believe that the greater part Missouri. He also reports the oc- of them died from this cause. These currence of a species of Graphium in- authors conclude that the Herbemont festing diseased vine roots in the and Rulander varieties are immune Santa Ana Valley but thinks that it and that the Delaware is very resistant bore no relation to the cause of the to mortalitv from root rot. disease in question. In 190r Wilcox (58) described a Between this date and 1900 a few rhizomorphic root rot of fruit trees additional reports were made of grape- which was causing widespread destruc- vine root rot. McCarthy {251 p. 122), tion of orchards in Oklahoma and ad- discussing the disease in North Caro- jacent States. He demonstrates that lina, and Starnes (50, p. 282), in this disease is caused by a species of Georgia, both arbitrarily attribute it Clitocybe, which he describes as a new to Dematophora necatrix and Armillaria species, Clitocybe parasitica. In addi- (Agaricus) mellea, merely because the tion to its occurrence on fruit trees, he same disease in Europe was commonly finds the fungus to be a common para- attributed to attacks by these fungi. sitic and saprophytic form on four species of oaks in Oklahoma. A rhizo- Underwood and Earle "(54, p. 272), T discussing root rot of the grapevine in morphic root rot, w hich Wilcox as- Alabama, state that it seems to be sumes was caused by this species of identical with the disease known as Clitocybe, is reported as occurring also "pourridié" in France. They believe in Texas, Missouri, southern Illinois, that it is quite prevalent and often Indiana, and to some extent in Ohio, does serious damage, as evidence of Georgia, California, and Oregon. Ex- which they mention the fact that out cept for a few references in the bibli- of the 584 vines in the station vineyard ography appended, Wilcox makes no all but 83 showed evident signs of the mention whatever of this disease on disease, and that many died during the the grapevine, which, in some cases, late summer and fall. They note that undoubtedly is caused by the same fun- the character of the soil apparently has gus as that with which he was working. much to do with the prevalence of the Walker (57, p. 30) and Hewitt and disease, that vines may live many years Hayhurst (21, p. 424) reported that while more or less affected by it, and root rot of fruit trees is widespread in that some varieties are evidently much Arkansas and causes serious damage more resistant than others. Earle in some localities. The first author and Austin (Í4), writing four years says that, "besides the apple it affects later, give a much more detailed ac- probably all of the commonly culti- count of grapevine root rot in Alabama vated fruit trees, the grape as well as a and question the earlier statement of number of forest trees," and states that Underwood and Earle (54, V- 272) the disease is caused by toadstool that this disease is the same as the fungi, "two of the forms concerned be- "pourridié" of the French, which they ing Clitocybe parasitica and Armillaria say is caused by Dematophora necatrix. mellea." Repeated attempts to isolate and Duggar (13, p. 471) mentioned the culture the organism causing the abundant occurrence of Clitocybe para- whitish mycelial growth under the bark sitica at Columbia, Mo., during favor- of diseased roots were unsuccessful able seasons on roots of hickory and and further observations led Earle other deciduous trees, but failed to and Austin to conclude that the dis- observe its occurrence in orchards, ease works much more slowly than the despite special effort to find it. The European root rot. These authors suggestion by some observers that state that the mycelial whitening can Armillaria mellea is responsible for often be found on old Scuppernong the root rot of fruit trees attributed to vines and on wild grapevines in the Clitocybe parasitica is refuted by Dug- woods, although these are seldom if gar, who states that he has never ever killed by it, and that its presence detected this fungus associated with on the roots of cultivated vines is by the typical disease in Missouri. Al- no means a sure sign of immediate though Armillaria mellea may occur in death. From an examination of the Missouri, and in this case be responsi- statistics on grape planting at the ble for some of the root rot reported, Alabama station these authors con- the writer has never seen it in the State clude that the disease is a very serious even in forests where in favorable sea- one. They state that of the 651 vines sons Clitocybe parasitica often abounds. alive or planted in 1894, a loss of 483, Butler (8, p. 24-29), in his account of or 75 per cent, was sustained in six root rot of grapevines in California, years and, although there was no proof describes a slow and a rapid form of Peb. is, 1925 Root Rot of Grapevine Caused by Olitocybe Tabescens 343 the disease, but contributes nothing to its greatest development in the medul^ the identity of the causal organisms lary rays, probably by reason of the involved. The vineyard in which an fact that these are centers for the stor- exceptionally severe form of root rot age of reserve food materials. This was observed was planted on a slope great growth of mycelium within the shortly after the land had been cleared larger medullary rays soon leads to the of its oak timber, and the lower part formation of radial cracks in the wood, was poorly drained. From his experi- which become stuffed with light tan- ence with California conditions, the colored sheets or feltlike mats of my- writer would attribute the form of root celium often extending into the pith. rot prevailing there to Armillaria This tendency of the mycelium to mellea. develop most abundantly within the larger medullary rays explains why the decay first appears as whitish more or SYMPTOMS OF THE DISEASE less delignified radial streaks. Within the centers of decay the cell walls fail Often, without any cause apparent to respond to microchemical tests for to the vineyardist, the vines will lignin and various stages of dissolution exhibit a sickly appearance which are to be seen there. Within the becomes quite evident in midsummer, individual cell the dissolution proceeds when the demand for water conduction outward from the laminae bordering is greatest. At this time the margins on the lumen, the middle lamella or of the leaves on diseased vines suddenly primary layer being the last part to turn brown, usually shortly before the disappear. Contrary to the statement ripening of the fruit. Later the leaves by Wilcox (58, p. 15) that the hyphae may dry up entirely and the vine sud- find their way into the cells only denly die, leaving the fruit to shrivel through the pits, the writer finds that in the sun (pi. 1), or the crop may they may penetrate the walls regardless mature and the vine linger until fall, of the presence of pits, as is the case in being entirely dead at the winter prun- virtually all fungi causing an enzymatic ing. In other cases only a part of the digestion of the wood elements and the vine will die, some branches putting consequent decay of the wood. forth a feeble growth for two or three The mycelial growth through the seasons longer. inner bark is by no means confined to The root crowns and larger roots of vines in which the foliage has shown diseased vines, when dug up and the signs of disease, but frequently may be outer fibrous bark peeled off, invariably found on those that are still making a show a whitish to creamy white or fairly strong growth and on which the isabelline mycelial coating or sheet, the foliage is perfectly healthy. This point marginal portions of which spread out can be determined readily in an in- in a fan-shaped manner, the older parts fected vineyard by making a slicing often forming a feltlike layer of fungous cut down through the outer bark at the tissue between the outer bark and the ground line. The presence of the my- wood (pi. 2). Often there is present celium in the inner bark of the roots also a number of more or less flattened, is by no means an indication of speedy black rhizomorphs. The inner living death, however, for the disease works bark has been killed by the mycelium, comparatively slowly and vines may which usually can be traced from 1 to 3 be affected for a number of years before inches above the ground line and down they succumb. Although the writer to all the larger roots. In well- has no definite figures on this point, it advanced cases the smaller fibrous is believed that at least from two to roots may be rotted away, although four years are required for this root rot in less advanced cases only the crown fungus to kill a well-established vine. and the larger roots may be affected, When the mycelium has progressed the smaller ones remaining for the most sufficiently through the wood and the part healthy. There is comparatively inner living bark to cut off, either wholly little decay of the wood of the root or in part, the water supply, the vine crown or larger roots until after the dies more or less suddenly. death of the vine, in which case trans- During the late summer and autumn, verse sections through the root crown in favorable years, one often finds in or larger roots exhibit whitish radial vineyards and orchards suffering from streaks of more or less delignified wood. root rot clusters of the mushrooms The course and nature of the decay fruiting from the root crowns of vines are essentially the same as those and fruit trees. These may be found described by Wilcox (58) for fruit trees. even more abundantly in forests, espe- Within the wood the mycelium attains cially in oak stands (pi. 3). Root Rot of the Grapevine Caused by Clitocybe Tabescens. Plate 1

Concord grapevine killed by Clitocybe root rot. All the leaves and fruit dried up shortly before the harvest. The living leaves showing in the background are on the vine in the next row 3^

Root Rot o the Grapevine Caused by Clitocybe Tabescens. Plate 2

Eootstock of Concord vine recently killed by Clitocybe root rot. The outer fibrous bark has been peeled away to show the whitish to bufl colored mycelial mat and the branching blackish rhizo- morph at the point marked R. The level at the top of the picture was but a short distance below the ground line. Three-fourths natural size Root Rot of the Grapevine Caused by Clltocybe Tabescens. Plate 3

Clusters of sporophores of Clitocybe tahescens in woods consisting largely of oak. Hundreds of these clusters of mushrooms occurred in one section of woods, most of them growing from the bases and roots of dead trees and stumps, or from buried wood, while a few others grew from the bases of living trees. The cluster at the left was placed in the field of view to show the character of the under side Feb. 15,1925 Root Rot of Grapevine Caused by Glitocybe Tabescens 347

CULTURAL STUDIES cultures a group of little hornlike processes—the primordia of clusters of Cultures made from the mycelial mushrooms—often developed from the sheets on the roots of grapevines central part of the culture, but never affected by root rot invariably yielded developed further on account of the a very characteristic, slow-growing drying up of the cultures. organism. Very scant growth of the On July 19, 1922, the fungus was fungus or none was obtained on corn- inoculated on 4-inch lengths of roots meal agar, and cultures on plain agar of wild grape (Vitis cordifolia Michx.), resulted in but weak growth. A much autoclaved in large test tubes contain- better growth was secured on prune ing a small quantity of water. From agar and a very satisfactory growth on the mycelial transfer, which was placed both maltose agar (30 gm. maltose per on the top of the root length, the lifer) and raisin agar (50 gm. seeded mycelium quickly grew down through raisins per liter). The growth of the the inner bark, even to the bases fungus on these different media indi- standing in water. At a few points cates that it does best on media rich it pierced the bark and developed super- in sugar. ficial masses of mycelium, a few light Since this organism develops rhizo- tan-colored nodules forming on the morphs that grow down into the agar, tops. it was found highly desirable early in Just a few days before the fruiting the work to have the culture media as of one of these sets of cultures, the clear as possible in order to best writer, while making a study of the observe the development and morpho- grape diseases at Neosho, Mo., during logical characters of these structures. the picking season, found several clus- In order to clarify the agar, the whites ters of a caespitose species of mushroom of two eggs were added to each liter developing from the bases of Moore's and the whole boiled prior to tubing Early and Concord vines which had and sterilization. been killed by root rot in a badly The initial mycelial growth was infected vineyard. Large numbers of whitish, the marginal growth in most clusters of the same fungus were ob- cases being rather sparse and downy- served also in one section of an oak appressed, although in a few instances forest (pi. 2) several miles distant, a rather dense white marginal growth growing from the bases of dead oak occurred (pi. 4, A). In all cases the trees and from roots beneath the sur- mycelial growth eventually became face of the ground. One large cluster thickened at the center, so that it was also observed growing from the presented a convex outline, the older superficial roots of an old silver maple portion near the center soon becoming shade tree in Neosho. The mor- a dirty white and later changing to phological characters and spore mea- isabelline or light buff. Often the surements of these specimens agreed immediate central part would appear perfectly with those of Clitocybe tabe- as an irregular, light tan-colored lump. scens (Scop.) Bres., of which Morgan's In the case of cultures made on raisin Agaricus monadelphus, Wilcox's Cli- agar the agar invariably became dis- tocybe parasítica, and Murrill's Mon- colored, showing dark brown immedi- adelphus caespitosus represent the ately beneath the mycelial mat and for American forms. A representative some distance in advance of it. No specimen from both the vineyard and such discoloration was noted, however, the oak forest was sent to Murrill, in any of the cultures on maltose agar. who identified both as Monadelphus After the lapse of from two to three caespitosus. weeks, rarely longer, there would grow Upon the writer's return from Neosho down into the agar, from the central he was agreeably surprised to find one part of the culture, peculiar, tortuous of the series of cultures on the lengths whitish strands, which constitute the of grape roots beginning to develop beginning of rhizomorph formation fruiting bodies. On August 10, a (pi. 4, B). The plate cultures invari- group of hornlike processes appeared ably dried up before the fungus on the top of the root length in one attained any great development, so of the tubes. By August 17 this had that their use was abandoned early in developed into a miniature cluster of the work. Even tube cultures made in mushrooms that was reasonably typi- the size of tubes commonly used dried cal of those collected in the field a up as a rule before fruiting bodies few days before. With the lapse of developed. The best results with this four more days the mushrooms of slow-growing organism were obtained this cluster had attained their full by making the cultures in large tubes development (pi. 4, C) and had cast and flasks. In some of the small-tube on the side of the tube a print of white Root Rot of the Grapevine Caused by Clitocybe Tabescens. Plate 4

A.—One-month-old Petri dish culture of Clitocybe root rot, isolated from a recently killed vine, on raisin agar. The marginal mycelium is whiter and more superficial than in the case of cultures on other agars used. About 1H natural size B.—Under side of same culture showing the dark-brown discoloration of the agar and the character- istic whitish rhizomorphs beginning to develop beneath the surface of the agar. About IK natural size C—Cluster of sporophores of Clitocybe tabescens developed in artificial culture made by inoculating a sterilized length of root of Vitis cordifolia in a large test tube. This cluster of sporophores developed to maturity and cast a print of white spores on the side of the tube within one month and three days from the time the length of root was inoculated- About natural size Feb. is, 1025 Root Rot of Grapevine Caused by Clitocybe Tabescens 349 spores typical of Clitocybe tabescens. rhizomorphs and fruiting bodies where Thus mature fruiting bodies shedding a large quantity of the substratum and spores were developed within approxi- a larger space for growth were pro- mately one month from a mycelial vided. Six cultures were made in 500 transfer.5 c. c. flasks containing a quantity of None of the other cultures of the small pieces of roots of a wild grape- series on lengths of wild grape roots vine ( Vitis aestivalis Michx.). Twelve fruited, some becoming contaminated other cultures were made in 150 c. c. with molds and others drying up. No flasks filled to a depth of three-quarters rhizomorph formation was noted on of an inch with agar. Six of these con- any of the lengths of roots, but, when tained maltose agar, the other six the bark was peeled off, all exhibited raisin agar. One of each of these three the whitish fan-shaped mycelial sheets sets of six flasks was inoculated with a characteristic of the root rot of grape- pure culture of the Florida form caus- vines found in the field. The source ing root rot of eucalyptus, which was of the inoculum for this set of cultures kindly furnished by Miss C. Audrey was the rotted vine roots collected at Richards, of the Madison branch of the Knobview in the early part of the Office of Investigations in Forest summer, at which time no fruiting Pathology, Bureau of Plant Industry, bodies were in evidence. United States Department of Agri- The type of the root rot, including culture. The remaining five flasks in the fan-shaped mycelial sheets and the each of the three sets of six were rhizomorphs, of the vines at Neosho inoculated with pure cultures of the was identical with that of the Knob- grapevine root-rot fungus secured by view vines first studied, and cultures the writer at Knobview, Mo. secured from the rotted vine roots bear- All the cultures made a slow but ing sporophores at Neosho agreed in steady growth after the lapse of a few every way with those secured from the days. The different cultures presented Knobview material. Although the certain minor variations in the appear- writer has had no opportunity to ance of the superficial mycelium, but attempt the reproduction of this root- no greater difference appeared between rot disease of grapevines by inocula- the two root-rot fungi than occurred tions with pure cultures of the fungus in any one group of the three different isolated from infected vines, he is substrata. The cultures all exhibited thoroughly convinced that it is caused the same general appearance in so far by this rhizomorph-producing fungus. as the aerial mycelium was concerned. In this connection it is of interest to The marginal growth, as a rule, was note that Knobview, where the writer rather sparse and downy-appressed. obtained his first cultures of the grape At the center of the cultures the my- root-rot fungus, from which material celium developed into thickened com- he succeeded in rearing the fruiting pact masses which sometimes were bodies of Clitocybe tabescens^ is but quite nodular at first. In some in- about 70 miles by air line from Bush- stances the downy-appressed marginal berg, where Scribner (46, p. 137) re- growth was lacking, the feltlike my- ported the discovery of grape root rot celial growth being thickened and con- in this country in 1887. The evidence vex clear up to the margin. The my- at hand strongly indicates that the celium was white at first, but soon organism isolated by the writer, which turned to a dirty white, later changing causes a more or less serious root rot to isabelline or light buff, and eventu- of grapevines in many sections of ally becoming light tan in the older southern Missouri, was likewise the portions. cause of the root rot reported 38 years After the lapse of from ten days to ago, rather than Ar miliaria mellea, as is two weeks it was noted that in all of generally believed according to Piper the six cultures on raisin agar the agar and Fletcher (39, p. 7) and Hesler and had become strikingly discolored, be- Whetzel (20, p. 97). coming dark brown in advance of the On June 12, 1923, a series of cultures mycelium, whereas such a discolora- in Erlenmeyer flasks was begun with a tion did not occur in any of the cul- view to observing the production of tures on maltose agar. When but a

5 In this connection it is of interest to note that Totten (53) reported cultural studies of this fungus (as- Clitocybe cespitosa), but made no mention of the production of fruiting bodies. A report of the writer's successful rearing of the sporophores of this fungus was given in the following: RHOADS, A. S. CLITOCYBE PARASíTICA AS A CAUSE OF ROOT ROT OF GRAPEVINES. Paper presented at 17th Annual Meeting, Bot. Soc. Amer. (Mycol. Sect.), Cambridge, Mass., December, 1922. [Not published. Title in program,, p. 13.] On the same program there also appeared an abstract of a paper by Miss C. Audrey Richards (40 in which report was made of the rearing of sporophores of the latter fungus isolated from a piece of rotted eucalyptus root sent from Florida. Clitocybe monadelpha is but one of the several synonyms of Clitocybe tabescens, the discussion of the history and nomenclature of which will be deferred until later. These joint reports constitute the first record of the development of sporophores of this fungus in artificial cultures. 350 Journal oj Agricultural Research Vol. XXX, No. 4 week old the cultures of eucalyptus much more minute and dense in com- root rot, on both maltose and raisin parison. Other rhizomorphs without agars, quickly developed a number of this root hairlike development of deli- light-brown branching rhizomorphs cate radiating mycelial filaments had with whitish tips. These extended numerous little white branches from downward and outward from the cen- 1 to 3 mm. long that developed out of tral portion of the mycelial growth. the old brown rhizomorph at more or The appearance of these structures was less of a right angle, like the aerial somewhat varied, but perhaps can be roots along the stem of the English ivy. described best as at first antlerlike, Sometimes there would be one every closely resembling the branches of cer- millimeter or two, or a space of several tain Clavarias. In some cases the millimeters might occur without them. ends were pointed; in others they were In other cases these branches would blunt and flattened. develop in pairs or even in tufts of When the cultures of the eucalyptus several, some of which were branched. root-rot fungus were 2 weeks old, it Eventually these numerous, short, was noticed that in both those on mal- more or less radially disposed lateral tose and on raisin agar the ends of branches of the rhizomorphs also be- some of the rhizomorphs had turned came brown. This is truly a remark- upward and had continued growth in able fungus that is well worth an this position until they reached slightly intensive cultural study. above the surface of the agar. That In a number of the cultures in this the upward growth of these submerged series, chiefly those of the Florida form, organs was the result of their own clusters of mushrooms made their volition and that they were not de- appearance after a more or less definite flected upward by the walls of the period of time and attained a more or flasks were clearly evident. The ex- less perfect stage of development. The posed ends were whitish and at their first evidence of sporophore formation junction with the surface of the agar was the development of a little group of there soon developed outward a downy- hornlike processes which quickly dif- appressed mycelial growth. In this ferentiated into a cluster of embryonic way the growth of the fungus might be mushrooms. The time at which fruit- started anew at several points on the ing began is based in the tables upon surface of the agar in advance of the the appearance of the latter. In prac- superficial mycelium developed out- tically every case the clusters of fruiting ward from the original point of inocu- bodies developed first from the central lation. After reaching the surface of portion, or oldest part, of the culture. the agar the rhizomorphs grew but After one cluster of mushrooms had little longer. They rarely protruded started its development at this point, above the surface of the agar more from one to five others sometimes than from one-sixteenth to one-eighth appeared, developing beside the first inch. one, or at the periphery of the central With the increased age of the cul- mycelial mass, or at points farther out tures the rhizomorphs gradually ac- from the central mycelial mass, such as quired a darker coloring until they be- the ends of the rhizomorphs which had came dark brown. When about 4 turned upward and reached the surface weeks old, it was noted on viewing the of the agar, or from the mycelial growth cultures by transmitted light that there developed where the ends of the radiated from many of the rhizomorphs rhizomorphs appeared at the surface of a dense but delicate growth of whitish the agar. As a rule, only the cluster of mycelium having an opalescent ap- mushrooms first appearing attained full pearance, like the growth of certain bac- development, and only a few of the teria in stab cultures. So dense was sporophores within this cluster attained this halo of radiating mycelial growth any great size. In a few cases, how- that its filamentous character could be ever, a second, and even a third, cluster distinguished only at the periphery, of mushrooms developed in more or less even with a hand lens. Beginning at rapid succession. The caps were hemi- the ends of the rhizomorphs, or prac- spherical at first, but quickly became tically so, this radiating halo of my- more or less sharply centrally depressed celium gradually became broader, pro- or depressed-umbonate as they ex- ceeding away from the end until it panded to their full development. The had attained a length of as much as 5 young sporophores presented a consid- mm., measured radially from the erable variation in color, ranging from a rhizomorphs. The appearance called creamy white when very young to buff to mind the root-hair development on or fawn color as they became somewhat a radish seedling, except for the fact older. As they approached maturity that the radiating mycelial threads were the marginal portion of the pileus Feb. is, 1925 Root Rot of Grapevine Caused by Glitocybe Tabescens 351

became yellowish white to buff and the of cultures and in other miscellaneous central part darker and often orna- ones were an exact counterpart of these mented with brownish fibrils. The developed by cultures of the Florida gills were pure white at first and dis- form, and the writer is convinced that tinctly decurrent. No evidence what- these twTo forms of root rot represent ever of an annulus was seen. As a rule, simply two different strains of the same about a week was required for the fungus, namely, Clitocybe tabescens. The embryonic sporophores to develop to more luxuriant development of rhizo- maturity and shed spores, after which morphs and stronger tendency to de- they quickly became sodden and dis- velop sporophores exhibited by the colored. Occasionally, the develop- Florida form may possibly be an ac- ment of the sporophores was checked, quired environmental character. and they dried up before shedding On June 30, 1923, a series of cultures spores. of the Florida form was started from The Missouri form causing the basidiospores taken from a spore print grapevine root rot behaved essentially cast on the side of the tube in which a the same in culture as did the euca- group of mushrooms had developed in a lyptus form from Florida described in former culture. This series was made

TABLE I.—Flask cultures for comparison of the Florida and Missouri strains of Clitocybe root rot

Number of days required for—

Dif- Culture medium and number of Source of organism Appear- Matura- culture ferentia- tion of ance of tion of rhizo- sporo- sporo- phores morphs phores

Pieces of Vitis aestimlis root: 1 Eucalyptus from Florida _ 22 44 50 2 . . Grapevine from Missouri 15 3 do . 31 76 83 4 do 33 5 do ... 37 6 do 37 Maltose agar: 1 Eucalyptus from Florida 7 37 50 2 Grapevine from Missouri 22 75 86 3 do ._ 35 4 do 35 77 87 5 do -.-- 37 6. do 37 Raisin agar: 1 Eucalyptus from Florida _ 36 42 Grapevine from Missouri 18 §::::::::::::::::::::::::::::::: do - 18 4 _. do 18 5 do - 21 6 do 35

the four preceding paragraphs, differing with a view to determining the length only in that it gave a very meager and of time required to run this fungus more delayed development of rhizo- through its full life cycle from spore to morphs as compared with the latter. spore and to compare this with the The Missouri form likewise developed length of time required for mycelial fruiting bodies in the cultures much transfers of the same form to produce more slowly and with much more diffi- fruiting bodies. Unfortunately, spores culty than the Florida form. The of the Missouri form were not available development of these two forms of at this time, nor was the opportunity Clitocybe tabescens may be compared in afforded the writer of collecting material Table I, which shows the length of in the field to furnish spores; so that no time required for each to reach certain comparison can be made between the definite stages of development on three two forms of Clitocybe tabescens grown different substrata. Inasmuch as the from the basidiospores. writer left Missouri, the cultures were The results of the experiment with abandoned after the lapse of 110 days. the Florida form, presented in Table The fruiting bodies which the writer II, indicate that it makes no difference succeeded in developing from the cul- in the length of time required for this tures of the Missouri form in this series form to develop fruiting bodies, 352 Journal oj Agricultural Research Vol. XXX, No. 4 whether the cultures are started from made an extensive survey of the liter- freshly cast basidiospores or mycelial ature on this subject, has deemed it transfers. In all cases the basidio- advisable and highly desirable, there- spores quickly gave rise to a sparse, fore, to review the history, nomen- downy-appressed mycelium, the central clature and geographic distribution of part of which developed into a tough, this fungus with the hope that its convex, light tan mycelial mass, the exact status and the relation of its surface of which was very finely and numerous synonyms may be definitely densely nodular. The marginal growth settled and established. about this initial mycelial mass was a Clitocybe tabescens (Scop.) Bres. is sparse, downy-appressed fawn to tan- based upon Scopoli's description of colored mycelium. In their subsequent Agaricus tabescens in 1772 (4£, p. 446), growth and behavior these cultures of Bresadola having decided that Sco- the Florida form started from basidio- poli's species represents the earliest spores (pi. 5) agreed exactly with those authentic description of this much- of the same form started from my- named plant. Although the history celial transfers. of the plant in question appears per-

TABLE II.—Growth of the Florida strain of Clitocybe root rot in cultures made from basidiospores

\ Number of days required for-

Differ- Culture medium and number of culture Appear- entia- Matur- ance of tion of ation of rhizo- sporo- sporo- morphs phores phores

Raisin agar (three small test tubes): 1 7 31 37 2 .. . 7 31 37 3 8 32 38 Maltose agar (three large test tubes): 7 31 38 2 . 8 31 38 3 9 31 38 Maltose agar, (three 150 c. c. flasks): 1 . 8 33 38 2 ...... 9 34 41 3 . 9 36 43

HISTORY, NOMENCLATURE, AND fectly clear since that date, the status GEOGRAPHIC DISTRIBUTION OF of Scopoli's species and its relation to the species described by certain con- FUNGUS temporaneous writers is somewhat of a Early in the course of the investi- mystery and probably will always gation it became evident that although remain so. the species of Clitocybe causing the As a synonym of his Agaricus tabe- root rot of grapevines in Missouri was scens, Scopoli cites Haller's "Fungus identical with Morgan's Agaricus mon- siccior, pulvinatus, rufus, lamellis rario- adelphus {27, p. 69), this was but one of ribus," with the note "huic proximus, " several names that had been given to Scopoli's citation of the number of the same plant in the United States. Haller's species, however, should have Moreover, Bresadola's decision in 1900 been 74 instead of 47. As synonyms (6, p. 84-85) that the plant which we of his species Haller (19, p. 49, no. 74) have known best in the United States cites Micheli's "Fungusparvus, esculen- as Clitocybe monadelpha is the same as tus, odoratus, coriaceus, rufus, la- Clitocybe tabescens of Europe, which is mellis inter se longe distantibus" accepted by practically all American {26, p. I48, no. 3), with a question mark mycologists who are familiar with this and the note, "Non répugnât," and plant, adds still more to the multi- Vaillant's "Fungus multiplex sordide plicity of names for it. carneus" (55, p. 66, no. 36), with the While various writers have from note, " Non recedit. " time to time given a partial list of the Agaricus gymnopodius illustrated by synonyms of this fungus, each has Bulliard (7, pi. 601) in 1780 and A. included but a small portion of the socialis described by De Candolle large total. The present writer, having (9, p. 48) in 1815 are accepted by Root Rot of the Grapevine Caused by Clitooybe Tabescens Plate 5

ite*

Lower figure—Cultures oí ClUocybe tabescens (Florida form causing root rot of Eucalyptus) de- velojwd on maltose agar 19 days after inoculation with basidiospores, showing the production of rhizomorphs. About natural size Upper figure—Cultures of Clitoct/be tabescens (Florida form causing root rot of Eucalyptus) de- veloped on maltose agar 38 days after inoculation with basidiospores, showing the production of rhizomorphs and mature sporophores. About natural size 354 Journal oj Agricultural Research Vol. XXX, No. 4

Bresadola {6) and others as synonyms of A. tabescens, it appears that he of Scopoli's A. tabescens. A. glomera- disagrees with Scopoli's use of this as tus described and illustrated in 1824 by a basis of his species, for on page 704, Pollini (40, p. 679), which, as he states, under addenda, he says: "P. 319. A, is an "Agaricus gymnop. aggregatus tabescens. Hic diversus est a supra n. caespitosus saepius ramoso-connatus,,, 344 citato. Utri synonymon Scopolii etc., is not included as a synonym by sit referendum, dubium." Even if Bresadola, although in Saccardo's Syl- this be so, the writer can not see any loge Fungorum (43, p. 385) it is in- justification for Fries's making two cluded in the list of illustrations of kinds of A. tabescens out of Scopoli's Clitocybe tabescens, or Collybia tabe- brief description. scens as he calls it, following Fries. From the foregoing it is evident that With allowances for poor drawing, there is considerable confusion and Pollini's illustration might pass for a uncertainty as to just what species cluster of the sporophores of Clitocybe authors writing before Scopoli in 1772 tabescens in which the bases of the considered as synonyms of his Agaricus stipes had anastomosed as a result of tabescens. However, it is virtually of growth conditions. no taxonomic value, and is even futile Fries, who clearly had but little from the standpoint of accuracy to familarity with the plant or plants attempt to trace this species back to which we now know as Clitocybe the days before the existence of bino- tabescens, added greatly to the con- mial nomenclature. fusion. In his "Epicrisis" in 1836 to Owing to the universal acceptance 1838 (17) he described, without having of Fries's work, the views held by him seen either of them, Agaricus tabescens have been perpetuated in subsequent under Tricholoma (17, p. 33) and A. writings. Thus, in Saccardo's "Sylloge gymnopodius, which he knew only Fungorum" (43, p. 385), which follows from Bulliard's illustration, under Fries, Micheli's figure of his " Fungus Flammula (17, p. 183), assuming that pileolo desuper lacero, etc.," is cited as the spores were colored because the an illustration of Collybia tabescens, as gills were. As synonyms of A. tabe- Saccardo calls it, although in the scens, Fries cited Scopoli's description writer's opinion Micheli's figure does and illustrations by Battarra, Larber not even resemble the species. Per- and Micheli, the latter being Micheli's soon's Agaricus buxeus (37), which was Plate 74, Figure 2, on which Persoon based upon this illustrated species of based his A. buxeus. None of these Micheli's, is accepted as a synonym of illustrations cited by Fries bears the Agaricus (Collybia) tabescens by Win- slightest resemblance to Clitocybe ter (59, p. 852), and doubtfully so in tabescens as understood by Bresadola. Saccardo's "Sylloge Fungorum" (42, In a later work in 1874 (18) Fries p. 12). exhibited no greater familiarity with In the middle of the nineteenth these species, retaining A. gymnodius century the history of the American under Flammula (18, p. 244) and plant which we know to-day as Cli- transferring A. tabescens to Collybia tocybe tabescens began. It was col- (18, p. Ill), although uncertain as lected first in Ohio by Lea, who sent it to whether or not the gills were de- to Berkeley. In 1847 the latter pub- current and whether the spores were lished a description of it (1), calling it colorless or colored. His account of Lentinus caespitosus. In 1868, sup- the latter species is especially confusing. plemented by additional specimens of After its description as No. 344 on page the plant collected by Ravenel in 111, in which he cites only Scopoli's South Carolina, it was renamed Agari- description and A. socialis in the sense cus (Pleurotus) caespitosus by Berkeley of De Candolle (9) and Se3mes (49), and Curtis (2), apparently on the he describes it again but differently in advice of the latter, who stated that his appendix to Agaricus on page 319, "this is certainly an agaric." again citing Scopoli's description but One year previous to this, however, adding this time Micheli's Plate 74, Curtis (11, p. 85), in his catalogue of Figure 2, on which Persoon (37, p. 190) the indigenous and naturalized plants based his A. buxeus in 1828. This of North Carolina, lists "Clitocybe illustration of Micheli represents his caespitosus, M. A. C." under Agaricus. ''Fungus pileolo desuper lacero," etc. Although Totten (53), on the strength (26, p. 158), which is a different of Curtis' citation, used the name species from that mentioned above as Clitocybe cespitosa for the plant we now having been cited by Haller and upon know as Clitocybe tabescens, Curtis's which Scopoli based his A, tabescens. name must be regarded as a nomen Since Fries does not cite the synonym nudum. Neither Clitocybe caespitosa which Scopoli gives in his description Peck (31, p. 61) nor Clitocybe caespitosa Feb. 15,1925 Root Rot of Grapevine Caused by Clitocybe Tabescens 355

Pat. (50, p. 248) should be confused produced here as Plate 6. It is typical with Curtis's name, for they represent of our plants. entirely different species. In his paper on a rhizomorphic root In 1883, Schulzer von Muggenburg rot of fruit trees in Oklahoma caused (44, V' 256) described as a new species by a caespitose species of Clitocybe, a plant occurring in Hungary, Poland, Wilcox (58) states that this species of and Transylvania, which he had had Clitocybe is closely related to C. mona- under observation for several years and delpha Morgan and to Armillaria mel- regarded as an exannulate form of lea exannulata Peck, but he describes Agaricus {Armiliaria) melleus, naming it as a new species, C. parasitica, since it Agaricus (Collybia) inarmillatus. he believed that it differed from these This was regarded as a synonym of two species in certain morphological Clitocybe tabescens by Bresadola (6). characters and in its parasitic habit of In the same year Morgan (27) growth. described from Ohio a plant which Unfortunately, the writer has not closely resembled Agaricus (Armiliaria) been able to see the type of Wilcox's melleus, but which lacked an annulus. species. Specimens do not occur This he called Agaricus monadelphus, either at the Missouri Botanical placing it under Clitocybe. Garden, where he spent a few weeks In 1892 Peck (32, p. 180-181) pub- in examination of the literature, or lished Miss Banning's description of at the Oklahoma Agricultural and Clitocybe aquatica, based upon speci- Mechanical College, where, if any were mens from Maryland. A year later deposited, they probably were de- Peck (33, p. 134) under his description stroyed in the 1914 fire which con- of Ar miliaria mellea, mentions the sumed the herbarium and all records receipt from Brooklyn, N. Y., and pertaining thereto. Washington, D. C, of a densely Almost the only points in which caespitose, slender-stemmed form with Wilcox's description of his species no annulus, which he called var. differs from Morgan's are these: In exannulata. The following remark by Wilcox's plant the pileus is roughened him is of interest: "It is scarcely dis- with small scales from the first instead tinguishable from Clitocybe aquatica of being at first glabrous and then Banning, and Clitocybe monadelpha scaly; the stipes are never twisted, and Morg., which, I suspect, will yet have it "is always parasitic in habit." to be referred to this species. Accord- According to the observations of the ing to Quelet, Clitocybe socialis DC, writer on the plants in both Missouri and Agaricus gymnopodius Bull, also and Florida, Wilcox's morphological belong here." distinctions are based on rather vari- In 1895 Peck (34, p. 265) described able characters. It is obvious that Armillaria mellea var. exannulata in fungi never can be stereotyped crea- greater detail. In 1898 he reported tions and that mycologists must for the first time the occurrence of allow a certain amount of latitude in Clitocybe monadelpha in New York the species concept, which, in this (35, p. 284) and described and illus- case at least, is but arbitrarily defined. trated the species (35, p. 302-303, Citing a statement in one of Morgan's pi. 51, figs. 1 to 5). In his report on letters to him, written in 1901, that the edible fungi of New York in 1900, C. monadelpha is never a parasite, Peck (36) reproduced the same de- Wilcox reports (58, p. 18) that "our scription of Clitocybe monadelpha, the species is always parasitic in habit," illustrations being changed somewhat. and at the bottom of the same page In 1900 appeared Bresadola's work further states that "the species grows (6), in which he pointed out that the in dense clusters from the crowns of plant we have known best in the United living trees and the stumps of dead States as Clitocybe monadelpha is but trees but is strictly a parasitic form in a synonym of Clitocybe tabescens of both cases." In his summary on page Europe. It is generally conceded by 22 he says: "The same fungus is a most American mycologists familiar common parasitic and saprophytic with this plant that Bresadola was form on four species of oak in Okla- correct in considering the American homa." It is obvious, therefore, that plant to be the same as the European. neither the distinctions made by Boudier's excellent illustration, ap- Wilcox in the morphological characters pearing as Plate 61 (51a) in his " Icones nor those in the habit of growth of Mycologicae ou Iconographie des these two fungi hold good. Champignons de France" and repro- Wilcox regarded the Oklahoma form duced with slight modification as as distinct from Peck's Armillaria Plate 197 of Bresadola's work, is re- mella exannulata because the plants Root Rot of the Grapev.ne Caused by Clitocybe Tabescens Plate 6

Eeproduotion of Boudier's illustration of Clitocybe tabescens given as Plate 61 (51a) in his "Icones Mycologicae ou Iconographie des Champignons de France," (5). Reduced to about % size of original plate Feb. is, 1925 Boot Rot of Grapevine Caused by Glitocybe Tabescens 357

were larger and the caps not smooth, SYNONOMY OF CLITOCYBE TABESCENS as Peck mentions in one place for his (SCOP.) BRES. species, and because it never exhibited any evidence of an annulus even in Agaricus tabescens Scop., Fl. Carn. ed. the young stages, Peck's plant having 2. 2: 446. 1772. occasionally had an evanescent annulus. Agaricus gymnopodius Bull., Herb. Fr., These points of difference again clearly PL 601, Fig. 1. 1793. are variable characters and the writer Agaricus socialis DC, Fl. Fr. 6: 48. is of the opinion that both plants 1815. Not A. socialis Fr., Ic. Hy- should be included as synonyms of men. 1: PI. 49, Fig. 2. 1871; Hy- Clitocybe tabescens in the sense of men. Eur., p. 83. 1874. Bresadola. ?Agaricus glomeratus Pollini, Fl. Ver. 3 : Murrill, in his monograph of the 679. 1824. Agaricaceae of tropical North America Lentinus caespitosus Berk., Lond. Jour. (28) and in his monograph of the genera Bot. 6: 317. 1847. Clitocybe and Monadelphus in the Agaricus (Pleurotus) caespitosus Berk. North American Flora (29, p. 420-421), & Curt., Jour. Linn. Soc. 10: 287. retains in Clitocybe the nonwood- 1868. loving caespitose species of Clitocybe Flammula gymnopodius (Bull.) Quel., and restricts the genus Monadelphus 6 Champ. Jura Vosg. 2: 346. 1873. founded by Earle (15, p. 432) to re- Clitocybe gymnopodia (Bull.) Gill., ceive the caespitose species of Clito- Champ. Fr., p. 162. 1874. cybe, to include only those that are Agaricus (Collybia) inarmillatus Schul- wood-loving.7 Murrill makes no men- zer, Oesterr. Bot. Ztschr. 33: 256. tion of Clitocybe tabescens, and Bresa- 1883. dola's determination that the plant we Agaricus monadelphus Morgan, Jour. have known best in the United States Cine. Soc. Nat. Hist. 6: 69. 1883. as Clitocybe monadelpha is but a syno- Clitocybe monadelpha (Morgan) Sacc, nym of this species appears to have Syll. Fung. 5: 164. 1887. been overlooked entirely by him. The Collybia tabescens (Scop.) Sacc, Syll. plant which is the subject of this Fung. 5: 206. 1887. paper is treated as Monadelphus caespi- Pleurotus caespitosus (Berk, and Curt.) tosus, based upon Berkeley's Lentinus Sacc, Syll. Fung. 5: 352. 1887. caespitosus. Morgan's Agaricus mona- Clitocybe aquatica Banning and Peck, delphus, Miss Banning's Clitocybe aqua- Ann. Rpt. N. Y. State Mus. 44: 180. tica published by Peck, Peck's Armil- 1892. laria mellea exannulata, and Wilcox's Ar miliaria mellea exannulata Peck, Ann. Clitocybe parasitica are all given as Rpt. N.Y.State Mus. 46:134. 1893. synonyms, although the latter is pref- Clitocybe tabescens (Scop.) Bres., Fungi aced with a question mark. Trid. 2: 84. 1900. Various other synonyms of Clito- Clitocybe parasitica Wilcox, Okla. Agr. cybe tabescens not discussed here result Exp. Sta. Bui. 49: 18. 1901. from the raising of the older sub- Monadelphus caespitosus (Berk.) Mur- genera to full generic rank or the rill, Mycologia 3: 192. 1911. transfer of a species to various other genera. Taxonomic notes of historical interest are given on this species by ILLUSTRATIONS OF CLITOCYBE TABES- Lloyd (23, 24). The treatment of this CENS (SCOP.) BRES. species by Kauffman (22, p. 723) and by Coker and Beardsley (10, p. 106- BuUiard, Herb. Fr., PI. 601, Fig. 1. 107) is also of interest. 1793. (As Agaricus gymnopodius.) There follows a chronological list of ?Pollini, Fl. Ver. 3: PI. 2, Fig. 6. 1824. all the synonyms of Clitocybe tabescens (As Agaricus glomeratus.) in so far as they are known to the Sicard, Hist. Nat. Champ., PI. 31, Fig. writer, those prefaced with a question 163. 1883. (As Agaricus gymno- mark being doubtful. Following this podius.) is a chronological list of all the illustra- Morgan, Jour. Cine. Soc. Nat. Hist. 6: tions of this species as far as they are PI. 4. 1883. (As Agaricus mona- known to the writer and believed to delphus) ; also reproduced by Wilcox, be correct, those prefaced with a Okla. Agr. Exp. Sta. Bui. 49: PI. 6. question mark being doubtful. 1901.

6 It is of interest to note that this genus was given the variant spelling of "Monodelphus" by Earle in his generic description on page 432. This appears to be a typographic error, however, for it was spelled the usual way in his key on page 403. 7 This is truly a superficial distinction for placing a group of species with the same general character in different genera. Even when collected carefully, it is not always clear whether these plants are growing from the ground alone or from buried wood, and, in case this point is not noted by the collector, the diffi- culty of making a correct determination of the species by these keys is increased. 13952—25t- 358 Journal oj Agricultural Research Vol. XXX, No. 4

Banning, Fungi of Maryland (MS. in occurrence of Clitocybe monadelpha in Herbarium N. Y. State Mus.), PI. 46. Michigan, and Fawcett (16, p. Ixvi) re- 1889. (As Clitocybe aquatica.) ported Clitocybe parasitica as causing Peck, Ann. Rpt. N. Y. State Mus. 51: a root rot of peach in Florida. The PI. 51, Figs. 1 to 5. 1898. (As cultures of Clitocybe root rot men- Clitocybe monadelpha.) tioned above as furnished by Miss Peck, Mem. N. Y. State Mus. 3: PL 46, Richards were also from Florida, having Figs. 7 to 12. 1900. (As Clitocybe been isolated from a rotted eucalyptus monadelpha.) root. Since coming to Florida in 1923 Mcllvaine, Amer. Fungi, PI. 27. 1900. the writer has collected specimens of (As Clitocybe monadelpha.) In Plate Clitocybe tabescens growing at the bases 16, Fig. 2, a poor illustration is given of stumps of Washingtonia robusta and of Peck's Armillaria mellea exannu- Ilex opaca at Gainesville, and at the lata, which is reproduced by Wilcox, base of a living oak tree at Cocoa. He Okla. Agr. Exp. Sta. Bui. 49: PL 4, has also observed two instances of this Fig. 4. 1901. fungus causing a root rot of guava Bresadola, Fungi Trid. 2: PL 197. (As (Psidium guajàva), one at Cocoa and Clitocybe tabescens.) the other near Courtenay on Merritt's Wilcox, Okla. Agr. Exp. Sta. Bui. 49: Island.8 Pis. 1 to 3, 5, 7 to 9; Figs. 10, 11, 14 Murrill (28, p. 198) states that the to 16,19. 1901. (As Clitocybe para- species also occurs in Mexico and sifica ) British Honduras. According to the Boudier, Ic. Myc. 1: PL 61 (51a). taxonomic literature previously cited 1905-10. (As Clitocybe tabescens.) in this paper, the plant has a wide dis- Hard, Mushr., PL 12 (fig. 75). 1908. tribution in Europe. Nowhere in the (As Clitocybe monadelpha.) European literature, however, has the Duggar, Fungous Diseases of Plants, writer seen any mention of its causing Fig. 234. 1909. (As Clitocybe para- a rhizomorphic root rot of woody sttica ) plants. In fact, even the cultural Rolland, Atlas, PL 25. 1910. (As characters of the European form appear Clitocybe gymnopodia.) to be unknown. Coker and Beardslee, Jour. Elisha In the United States the range of Mitchell Sei. Soc. 38: PL 12; 33, Clitocybe tabescens, which extends from Fig. 7. 1922. (As Clitocybe tabes- New York south to Florida and west to cens.) Michigan, Kansas, and Texas, over- On his map in Plate 11, Wilcox {58) laps to a large extent the range of the shows the localities in which occurs the closely related Armillaria mellea, which rhizomorphic root rot described by him likewise causes a rhizomorphic root rot. as found in Texas, Oklahoma, Missouri, Except for a few middle-eastern States, Illinois, Indiana, Ohio, and Georgia, however, root rot caused by Clitocybe and adds that California and Oregon tabescens has been reported only from should have been marked as States the southern part of the United States, from which the same disease had been where it is of most widespread occur- reported. The rhizomorphic root rot rence. reported by Wilcox from the two latter States, and assumed by him to RELATION OF CLITOCYBE ROOT be due to Clitocybe parasitica, was in all probability caused by Armillaria ROT TO TIMBERED LANDS AND mellea, which the writer knows from DRAINAGE personal observation is of widespread occurrence on the Pacific coast. So far The root rot of grapevines and fruit as the writer's information extends, trees caused by Clitocybe tabescens is there never has been an authentic re- associated with lands which were port of Clitocybe root rot occurring on formerly covered with hardwood tim- the Pacific coast or in the Pacific North- ber, especially oak. This disease ap- west. pears to be practically unknown in From the reports of Peck we know strictly prairie soils and in old land, that the species of Clitocybe that we except at the margins in close proximity now call C. tabescens occurs as far to timbered land. Men who have had north as New York on the Atlantic no experience with the disease on old coast. Kauifman (##) reported the land have found that it quickly made

8 Thus far the writer has not found grapevines attacked by Clitocybe root rot in Florida, but has had virtually no opportunity to investigate this problem since coming to this State. In a case of root rot observed on a single Herbemont vine at Bartow the fungus associated with the root rot did not appear to be Clitocybe nor did the one isolated prove to be a rhizomorph-producing fungus. Al- though cultures have been maintained for several months, neither spores nor fruiting-bodies have been secured. Feb. is, 1925 Root Rot of Grapevine Caused by Glitocyle Tabescens 359 its appearance upon extending their palliatives. In selecting a site for vine- plantings into ground more recently yard planting, newly cleared land, espe- cleared. cially in a region of oak forests, should In all cases where the writer has had be avoided, since the fungus may live the opportunity to observe Clitocybe in the soil as a saprophyte on deadwood, root rot, both of grapevines and fruit such as stumps and roots. The charac- trees in Missouri, it has occurred in the ter of the disease suggests the need for low and poorly drained parts of vine- thorough preparation of cleared lands, yards and orchards where water is liable including the removal of all roots, and to stand in the soil, although it may cultivation for at least three years in also occur in soils underlaid with an im- other crops before setting out to grape- pervious subsoil or hardpan, where vines or fruit trees. In any case, land natural drainage is poor. In Florida, which promises poor natural drainage however, Clitocybe root rot has been should be avoided unless artificial observed in sandy soils that appeared drainage can be assured at a reasonable to be well drained. The relation of cost. Care should also be taken to Clitocybe root rot to inadequate drain- prevent barking or otherwise injuring age was illustrated in very striking the roots of vines when cultivating the fashion in a vineyard about 18 years vineyard, since such injuries favor in- old at Neosho. This was planted in fection by root-rotting fungi. Control Moore's Early grapes on one side and of the grapevine root borer is also Concord on the other. The land was essential for the same reason. practically level. Immediately adjoin- After Clitocybe root rot appears in a ing one end of the vineyard was a sor- vineyard the vines that have been ghum field in which, close to the end of seriously attacked can not be saved; the vineyard, lay a large, slightly de- however, measures can be taken to pressed area where water stood for long check the spread of the disease and to periods during the early summer. save those recently attacked. Inas- Even the sorghum in this vicinity had much as an excess of moisture in the made but poor growth and appeared soil, either as a result of a natural de- stunted and pallid. The grapevines at pression or being underlaid by an im- this end of the vineyard were weak and pervious substratum, is one of the chief unthrifty. Large numbers had died conditions favoring the development of out and been removed (pi. 7, upper Clitocybe root rot, adequate drainage figure), and still others were dying or is, and will always be, the most val- were practically dead. Several of the uable preventive and corrective meas- dying vines were dug up and found to ure. Unless this precaution is taken have the mycelium characteristic of all others are useless, for vineyards Clitocybe root rot. Clusters of the that have become infected with this mushrooms had even developed from root-rot fungus are, unless drained, the root crowns in some cases. In always subject to attack by it. The addition, it was determined by the low or otherwise poorly drained places cutting method previously referred to in the vineyard where water is liable to that many of the living vines which stand in the soil should receive most appeared to be at least moderately careful attention in this respect, for it healthy were infected by the fungus. is at these points that root rot is most At the other end of the vineyard, which likely to occur. As soon as the root was 520 feet in length and contained rot is discovered in a vineyard all vines but 52 vines, there was a full stand that have been killed by it and all vines growing vigorously (pi. 7, lower figure). badly diseased, that is, those whose The losses occasioned to vineyards scanty growth shows that their root by Clitocybe root rot vary greatly. In system is seriously attacked, should be mild cases perhaps just a few vines will removed. These should be excavated die from year to year, but in severer carefully, care being taken to remove cases they may die quite rapidly until all the roots, which should be burned. within a few years parts of the vineyard Then, if the hole is left exposed to the may be heavily depleted, as in the case air and sun for a few weeks or disinfec- just cited. tion of the soil is accomplished by the use of chemicals, and the drainage of the soil has been assured, it should be CONTROL OF CLITOCYBE ROOT ROT safe to replant. OF GRAPEVINES In European practice a number of chemicals have been applied to the A little attention directed to preven- soil to destroy the mycelium and spores tive measures will obviate the necessity of Dematophora necatrix and other root- of applying remedial measures in com- rot fungi in the soil or to destroy the bating root rot which at best are but fungus on recently infected vines with- Root Rot of the Grapevine Caused by Clitocybe Tabescens. Piale 7

(Above).—Depletion of Toncord vines by Clitocybe root rot in poorly drained end of vineyard. These vines continue to die out from year to year v tt (Below) —Full stand of thrifty Concord vines in well-drained end of vineyard shown above, the undrained end being in the background. The rows are 620 feet in length and contain only 52 vines. The transition between the sickly vines at one end and the vigorous ones at the other was rather abrupt Feb. is, 1925 Root Rot of Grapevine Caused by Clitocybe Tabescens 361 out injuring the vine itself. Bonjour sufficient to destroy the old foci of (4) recommends the use of a 7 per cent infection represented by the roots of solution of green vitriol (ferrous sul- the once existing trees, and repeated phate). Beniling and Behaix likewise and stronger doses endangered the recommend green vitriol against rot of vines. According to the same author, vine roots where carbon bisulphide and ferrous sulphate applied each winter sodium fluoride had no action. Dufour for three successive years at the rate (12), however, who has conducted ex- of 8, 16, and 16 ounces, respectively, periments to control pourridié of the to each vine was sufficient to restore all grapevine for a number of years, tested but two vines in which the root rot comparatively the action of green vitriol yielded to a further and slightly modi- and blue vitriol on the causal fungus fied treatment consisting of daubing (Dematophora necatrix) and found the the infected part of the stem with a latter much superior. He recommends solution made up of 10 per cent by a 3 per cent solution of blue vitriol weight of sulphuric acid and 50 per (bluestone or copper sulphate) as a soil cent of ferrous sulphate. The ferrous disinfectant. This is applied by ex- sulphate was used in preference to cavating a small basin around the trunk copper sulphate because it was much of the vine and pouring into it a gallon cheaper. It was applied in the usual or so of the solution, the exact quantity way by digging a hole around the stem being determined by the nature of the 6 inches deep with a radius of 12 soil and the supposed extent of the root inches, at the bottom of which the system. Before planting new vines, 1 chemical was scattered and the soil to 2 quarts of the same solution are then replaced. This salt was thought poured into the holes. Vines adjoining to act not only as a fungicide but also those known to be attacked are also as a vigorous stimulant to growth. laid bare in the spring and watered freely with the solution; 3 to 5 ounces Szigethi-Gyula (52) states that ex- of granulated bluestone per stock may periments in a vineyard located in a likewise be spread over the ground. rather moist situation showed that the The result is not always completely application of lime at the rate of 2 visible the first year, and it is some- kg., or 10 liters of milk of lime, to a times necessary to repeat the treatment vine was efficient in preventing pour- for two years in succession, in which ridié. case the results obtained are claimed Inasmuch as the mycelium of the to be very positive. root-rot fungi is often more resistant Dufour likewise tried ammonium sul- to toxic substances than the host phide, hyposulphite of soda and sul- plant, considerable experimentation phite of lime against Dematophora neca- will be necessary before there will be trix without securing any promising found for the control of root-rot fungi results. Potassium sulphocarbonate, an efficient and satisfactory fungicide which Dufour and Mouillefert tried, that can be recommended for general also proved disappointing. Narbonne use with safety to the vine. It seems experimented with sulphur and advises to the writer that paradichlorobenzene, laying bare the less badly attacked which has proved so successful in the stocks as deep as possible and dusting control of the peach-tree borer, would the roots abundantly with sulphur, re- be well worth a trial for the control of peating the dusting several times be- root-rot fungi. So far as is known, this fore the stocks are covered again. chemical is not especially injurious to Carbon bisulphide has been tested grapevines. The above-mentioned fun- extensively by numerous investigators gicides are not recommended for gen- for the control of insects and root rot eral use, but are merely suggested for in vineyards. Dufour made applica- those who may wish to experiment in tions at the rate of 200 gm. per square a small way with them. meter, after having removed the dis- The comparatively simple method eased roots. According to this eminent of aeration and exposure to sunlight investigator, carbon bisulphide destroys also has shown encouraging results in the mycelium of the fungus to a large the control of root rot, both on grape- extent. Blunno (3), experimenting vines in Europe and on fruit trees in later in Australia, states that carbon this country. In this method the dirt bisulphide applied at the rate of 1 is carefully excavated from about the ounce per vine, divided into five root crown and larger roots and these partial injections made within 6 to 8 are left exposed to the sun during the inches from the stem, was effective in remainder of the summer, either with killing the mycelium living externally, or without the application of a fungi- that is, during the first stage of infec- cidal wash. The soil is replaced be- tion. Such a dose, however, was not fore the advent of winter. 362 Journal oj Agricultural Research Vol. XXX, No. 4

SUMMARY Although Clitocybe tabescens in the United States is known to occur from A mushroom root rot of grapevines, New York south to Florida and west of rather common occurrence in various to Michigan, Kansas, and Texas, localities in the Ozark section of Mis- cases of root rot caused by this fungus, souri, is reported and described in de- with the exception of those in a few tail. The organism isolated from the middle eastern States, have been roots of the diseased vines proved to reported only from the southern part be a very slow-growing but distinctive of the country, where it appears to be one, developing characteristic sub- of most widespread occurrence. The merged rhizomorphs in the cultures. losses occasioned to vineyards in Fruiting bodies, w^hile not associated Missouri by Clitocybe root rot, which with the diseased vines first studied appears to be a comparatively slow- in the field, were subsequently de- working disease, vary from the death veloped in some of the cultures. But of a few vines each year in cases of a few days before the first fruiting mild attack to such rapid destruction bodies were secured in the cultures a that within a few years parts of the species of Clitocybe was observed vineyard may be heavily depleted. fruiting abundantly at the bases of Clitocybe root rot is a disease rotted grapevines in a vineyard in associated with lands which formerly another section of the State and in an were covered by hardwood timber, oak forest a few miles distant. Cul- especially oak. The disease appears tures of the fungus isolated from the to be practically unknown in strictly roots of these vines yielded a rhizo- prairie soils and in old land, except at morph-producing organism identical the margins in close proximity to with the one isolated from the first timbered lands. It has been found to material studied. Although no oppor- attack grapevines and fruit trees tunity of reproducing this root-rot chiefly in places where the soil is disease by inoculations with pure cul- poorly drained, either as the result of tures of the fungus isolated from in- natural depressions in contour or in fected vines has been afforded, it is places underlaid with a more or less believed that beyond all doubt the impervious soil or hardpan. disease in question is caused by this Attention directed in the selection rhizomorph-producing organism. of vineyard sites to the thorough prep- The fungus which is believed to be aration of newly cleared timberlands, the causal organism is a species of adequate drainage of any spots in need Clitocybe described by various writers of it, and prevention of barking or in this country under the names C. other injury of the vine roots when monadelpha, C. aquatica, Armillaria cultivating the vineyard, will prove mellea exannulata, and C. parasítica, valuable measures in preventing at- all of which are clearly different tack by Clitocybe root rot. In case names for the same plant and identical the disease is observed in vineyards with Clitocybe iabescens of Europe. already established, adequate drain- A detailed discussion is given of the age, which is and will always remain history, nomenclature, and geographic the most valuable remedial measure, distribution of this fungus, together should be assured, and the spread of with complete lists of the synonyms the disease may then be checked by and illustrations believed to be au- the prompt removal of all badly thentic. diseased and dead vines, the chemical A detailed description is given of the treatment of adjacent vines, and the characteristics and behavior of the disinfection of the soil before replant- Clitocybe root-rot fungus in pure cul- ing. The various methods for the tures and a comparison is made be- destruction of the fungus on newly tween the form isolated from grape- infected vines and in the soil are vine roots in Missouri and one secured briefly reviewed and the need for from a eucalyptus root from Florida. further experimentation is pointed out. Although the writer's cultures of the Comparatively little study has been Missouri form of Clitocybe root rot made of the fungi causing root rot of were generally much slower in their grapevines in this country. Although development and in the production cases of this disease have been reported of fruiting bodies than the Florida in various sections since its discovery form, the two agreed so closely in in Missouri in 1887, it has, with few their morphological characters that he exceptions, been attributed to Armil- is of the opinion that these two forms laria mellea and Dematophora necatrix, represent but two rather widely dif- as a rule on assumption, however, fering strains of the same fungus. rather than from definite knowledge. Feb. is, 1925 Root Rot of Grapevine Caused by Olitocybe Tabescens 363

The present investigation affords very (18) FRIES, E. M. 1874. HYMENOMYCETES EUROPAEI SIVE EPICRIS- definite evidence that Clitocybe root EOS SYSTEMATIS MYCOLOGICI EDITIO ALTERA. rot, which hitherto has been certainly 755 p. Upsaliae. known to attack only fruit, forest, and (19) HALLER, A. VON 1742. ENUMERATIO METHODICA STIRPIUM HEL- shade trees, is responsible for a con- VETIAE INDIGENARUM. 794 p., illUS. Got- siderable quantity of root rot of grape- tingae. vines, at least in Missouri, and prob- (20) HESLER, L. R., and WHETZEL, H. H. 1920. MANUAL OF FRUIT DISEASES. 462 p., illUS. ably also in other southern States. New York. The isolation of this fungus by the (21) HEWITT, J. L., and HAYHURST, P. writer from the roots of recently 1911. DISEASES OF APPLE TREES AND FRUIT CAUSED BY FUNGI AND INSECTS. Ark. Agr. Exp. Sta. killed vines but 70 miles from the point Bui. 109: 411-445. where root rot of the grapevine was (22) KAUFFMAN, C. H. first discovered in this country indi- 1918. THE AGARICACEAE OF MICHIGAN. V. 1. Lansing, Mich. (Mich. Geol. and Biol. Surv. cates that Clitocybe tabescens was the Pub. 26.) cause of the case first reported rather (23) LLOYD, C. G. than Armillaria mellea, as is generally 1899. CUTOCYBE MONADELPHA. Mycol. Notes 1:17. believed. (24) 1901. CLITOCYBE TABESCENS. MyCOl. Notes 1: 54. LITERATURE CITED (25) MCCARTHY, G. 1893. THE DISEASES AND INSECTS AFFECTING (1) BERKELEY, M. J. FRUIT TREES AND PLANTS, WITH REMEDIES FOR 1847. DECADES OF FUNGI. DEC. XII-XIV. OHIO THEIR DESTRUCTION. N, C. Agr. Exp. Sta. FUNGI. Lond. Jour. Bot. 6: 312-326. Bul. 92, p. 65-144, illus. (2) and CURTIS, M. A. (26) MICHELI, P. A. 1868. FUNGI CUBENSES(HYMENOMYCETES). Jour. 1729. NOVA PLANTARUM GENERA. 234 p., illUS. Linn. Soc. Bot. 10: 280-392. Floren tiae. (3) BLUNNO, M. (27) MORGAN, A. P. 1911. ON THE PROPORTION OF FERROUS SULPHATE 1883. THE MYCOLOGIC FLORA OF THE MIAMI VALLEY. USED AGAINST THE "WHITE ROT" OF GRAPE Jour. Cincinnati Soc. Nat. Hist. 6: 54-81, 97- VINES. Rpt. Austral. Assoc. Adv. Sei. 13: 117, 173-199, illus. 562-566. (28) MURRILL, W. A. (4) BONJOUR, J. 1911. THE AGARICACEAE OF TROPICAL NORTH 1891. MANUEL PRATIQUE DU VIGNERON. Avec AMERICA—HI. Mycologia 3: 189-199. figures, chez Eugène Vodoz, à Vevey. [Not (29) seen. Commented on by "S. B." in Chron. 1916. AGARICACEAE. No. Amer. Flora 9: 163-421. Agr., Vit. et Forest Vaud. 4: 272. 1891.] (30) PATOUILLARD, N. (5) BOUDIER, E. 1909. ADDITIONS AU CATALOGUE DES CHAMPIG- 1905-10. ICONES MYCOLOGICAE, OU ICONOGRAPHIE NONS DE LA TUNISIE. Compt. Rend. Cong. DES CHAMPIGNONS DE FRANCE, t. 1, illUS. Soc. Savantes (Sect. Sei.) 1908: 242-257. Paris. (31) PECK, C. H. (6) BRESADOLA, G. 1888. REPORT OF THE BOTANIST. Ann. Rpt. 1900. FUNGI TRIDENTINI NOVI, VEL NONDUM N. Y. State Mus. Nat. Hist. (1887) 41: 51-122. DELINEATI, DESCRIPTI, ET ICONIBUS ILLUSTRATI. (32) v. 2, illus. Tridenti. 1892. REPORT OF THE STATE BOTANIST. Ann. (7) BULLIARD, P. Rpt. N. Y. State Mus. Nat. Hist. (1890) 44: 1780. HERBIER DE LA FRANCE. 602 COl. pi. Paris. 177-187, ülus. (8) BUTLER, O. (33) 1905. OBSERVATIONS ON SOME VINE DISEASES IN 1893. REPORT OF THE STATE BOTANIST. Ann. SONOMA COUNTY, CALIFORNIA. Calif. Agr. Rpt. N. Y. State Mus. Nat. Hist. (1892) 46: Exp. Sta. Bui. 168, 29 p., illus. 83-149. (9) CANDOLLE, AUG. DE (34) 1815. FLORE FRANçAISE, t. 5 (v. 6). Paris. 1895. REPORT OF THE STATE BOTANIST. Ann. (10) COKER, W. C, and BEARDSLEY, H. C. Rpt. N. Y. State Mus. Nat. Hist. (1894) 48 (1): 1922. THE LACCARIAS AND CLITOCYBES OF NORTH 101-337. CAROLINA. Jour. Elisha Mitchell Sei. Soc. (35) 38: 9&-126, illus. 1899. REPORT OF THE STATE BOTANIST. Ann. (11) CURTIS, M. A Rpt. N. Y. State Mus. Nat. Hist. (1897) 51 (1): 1867. BOTANY; CONTAINING A CATALOGUE OF THE 267-317, illus. INDIGENOUS AND NATURALIZED PLANTS OF THE (36) STATE. Geol. and Nat. Hist. Surv. N. C, v. 2, 1900. REPORT OF THE STATE BOTANIST ON EDIBLE pt. 3, 156 p. FUNGI OF NEW YORK, 1895-99. Mem. N. Y. (12) DUFOUR, J. State Mus. 3 (4): 140-141, illus. 1894. NOTE SUR L'EMPLOY DU VITRIOL BLEU (37) PERSOON, C. H. CONTRE LE POURRIDIé. Rev. Internat. Vit. et 1828. MYCOLOGIA EUROPAEA. V. 3, illUS. Er Oenol. 1: 75-77 langae. (13) DUGGAR, B. M. (38) PIERCE, N. B. [1909]. FUNGOUS DISEASES OF PLANTS, WITH CHAP* 1892. THE CALIFORNIA VINE DISEASE; A PRELIMI- TERS ON PHYSIOLOGY, CULTURE METHODS AND NARY REPORT OF INVESTIGATIONS. U. S. Dept. TECHNIOUE. 508 p., illus. Boston, New York Agr., Div. Veg. Path. Bui. 2, 222 p., illus. [etc.]. (39) PIPER, C. V., and FLETCHER, S. W. (14) EARLE, F. S., and AUSTIN, C F. 1903. ROOT DISEASES OF FRUIT AND OTHER TREES 1900. GRAPES. Ala. Agr. Exp. Sta. Bui. 110, CAUSED BY TOADSTOOLS. Wash. Agr. Exp. Sta. p. 55-91, illus. Bui. 59, 14 p. (15) . (40) POLLINI, C. 1909. THE GENERA OF NORTH AMERICAN GILL 1824. FLORA VERONENSis. v. 3, illus. Veronae. FUNGI. N. Y. Bot. Gard. Bul. 5: 373-451. (41) RICHARDS, C. A. (16) FAWCETT, H. S. 1923. CULTURAL STUDIES OF ARMILLARIA MELLEA 1912. REPORT OF THE PLANT PATHOLOGIST. Fla. FR., AND CLITOCYBE MONODELPHA MORG. (Ab- Agr. Exp. Sta. Ann. Rpt. 1911: Iviii-lxvii. stract) Science 57: 156. (17) FRIES, E. M. (42) SACCARDO, P. A. 1836-38. EPICRISIS SYSTEMATIS MYCOLOGICI, SEU 1901. SYLLOGE FUNGORUM. V. 15. PataVÜ. SYNOPSIS HYMENOMYCETUM. 610 p., illus. (43) Upsaliae. 1910. SYLLOGE FUNGORUM. V. 19. PataVÜ. 364 Journal of Agricultural Research Vol. XXX, No. 4

(44) SCHULZER VON MÜGGENBURG, S. (52) SZIGETHI-GYULA, A. 1883. MYKOLOGISCHES. EINIGE, MEIN ERSTES 1908. TRAITEMENT DU POURRIDIÉ. Bul. Inst. GROSSES AN DIE UNGARISCHE AKADEMIE DER Cent. Ampélol. Roy. Hongrois (1906) 1: 16. WISSENSCHAFTEN ABGETRETENES BILDERWERK (53) TOTTEN, H. R. BETREFFENDE BERICHTIGUNGEN. OeSteiT. 1917. ARMILLARIA MELLEA, CLITOCYBE CESPITOSA, Bot. Ztschr. 33: 255-257. PLEUROTUS SAPID US, AND CLAUDOPUS NIDULANS (45) SCOPOLI, G. A. IN PURE CULTURE. (Abstract) Jour. Elisha 1772. FLORA CARNIOLICA; EXHIBENS PLANTAS Mitchell Sei. Soc. 33: 96. CARNIOLIAE INDÍGENAS ET DISTRIBUTAS IN (54) UNDERWOOD, L. M., and EARLE, F. S. CLASSES, GENERA, SPECIES, VARIETATES ORDINE 1896. TREATMENT OF SOME FUNGOUS DISEASES. LiNNAEANO. Ed. 2, t. 2, illus. [Vindobonae] Ala. Agr. Exp. Sta. Bui. 69: 245-272. (46) SCRIBNER, F. L. 1888. OBSERVATIONS THE PAST SEASON WITH (55) VAILLANT, S. GRAPE ROT AND MILDEW. PlOC. N. J. Hort. 1727. BOTANICON PARISIENSE. 205 p., illus. Leide Soc. 1887: 133-146. and Amsterdam. (47) (56) VERGE, G. 1890. ROOT-ROT OF THE VINE. Orchard and 1912. LE POURRIDIé. Prog. Agr. et Vit. 57:132- Garden 12:12-13, illus. 136, illus. (48) (57) WALKER, E. 1890. FUNGUS DISEASES OF THE GRAPE AND OTHER 1902. WHY APPLE TREES FAIL. Ark. Agr. Exp. PLANTS AND THEIR TREATMENT. 134 p., ÜIUS. Sta. Bui. 71, 32 p., illus. Little Silver, N. J. (49) SEYNES, J. DE (58) WILCOX, E. M. 1863. ESSAI D'UNE FLORE MYCOLOGIQUE DE LA 1901. A RHIZOMORPHIC ROOT-ROT OF FRUIT TREES. RÉGION DE MONTPELLIER ET DU GARD. 156 p., Okla. Agr. Exp. Sta. Bui. 49, 32 p., illus. illus. Paris. (59) WINTER, G. (50) STARNES, H. N. 1884. DIE PILZE DEUTSCHLANDS, OESTERREICHS 1895. GRAPE CULTURE. Ga. Agr. Exp. Sta. Bul. UND DER SCHWEIZ. ABT. 1. SCHIZOMYCETEN, 28: 229-294, illus; SACCHAROMYCETEN UND BASIDIOMYCETEN. (51) STEVENS, F. L., and HALL, J. G. (Rabenhorst, L. Kryptogamen-Flora von 1910. DISEASES OF ECONOMIC PLANTS. 5l3p.,illuS. Deutschland, Oesterreich und der Schweiz. New York. Aufl. 2, Bd. 1, Abt. 1. Leipzig.)