TlHll TlJWi VNDVIIIOIITY 13 A I THE FUNGI The father of American mycology. THE FUNGI IN TWO VOLUMES Volume I By Frederick A. Wolf and Frederick T. Wolf DEPARTMENT OF BOTANY DEPARTMENT OF BOTANY DUKE UNIVERSITY VANDERBILT UNIVERSITY /' New York: JOHN WILEY & SONS, Inc. Chapman 6> Hall, Limited London / Copyright, 1947 BY John Wiley & Sons, Inc. All Rights Reserved This book, or any part thereof, must not be reproduced in any form without the written permission of the publishers. PRINTED IN THE UNITED STATES OF AMERICA PREFACE This treatise on fungi is intended as a reference and textbook. Its content falls naturally into two portions. The first portion, included in Volume I, is a consideration of the developmental morphology and taxonomy of fungi and is basic to any compre- hensive study of the fungi. The second portion, included in Volume II, deals more specifically with the activities of fungi. It must be borne in mind, however, that we have attempted throughout the treatise to stress the need for more emphasis on problems relating to fungus activities. Much of the mvcological teaching and research of the past has centered around taxonomy and classification. Some em- phasis has necessarily been placed on morphology and cytology, but this phase of inquiry has been largely an adjunct to taxonomy and classification. It is, of course, essential that one should be able to name a given fungus correctly, to place it in a suitable packet, and to arrange it in some phvlogenetic category in an herbarium. This should, however, not be the end, as it all too commonly is, but rather the beginning of interest in the particular fungus. It would appear to be much more stimulating if, after having received a more or less "formal" introduction to a fungus, one were to turn his attention to its activities. To determine what a fungus does and how it does it and to attempt to approxi- mate an answer to why it reacts in a certain manner have always appealed to us as of more concern than its name. The primary purpose of Volume II is therefore to direct attention away from time-honored and well-beaten paths of mycological thinking and to focus it on this different point of view. To stress the activities of fungi with a minimum of considera- tion to taxonomic aspects has been no easy task. It has required, first of all, a fusion of the mycological concepts of two genera- tions. This in itself was a departure from tradition; although it presented very real difficulties, thev have not been insurmount- able. Another disconcerting factor which entered into the con- siderations of how to emphasize the problems of fungus behavior VI PREFACE was that, as all older mycologists appreciate, much which was once regarded as truth has been and is being supplanted. To un- learn seems no less difficult a task than to learn. It must be re- membered, too, that it is a prodigious task to become conversant with new truths, which must be sifted from voluminous myco- logical literature. Information about a particular fungus is conveyed most satis- factorily if one is able to orient it as to its structure and its rela- tionship with other species. This orientation is best achieved by using its name under standingly. For each order and family, the barest essentials of morphology and development are given. So far as possible, species of economic importance have been chosen for this purpose. Certain families have been omitted, mainly because they are so little known. This deficiency may incite adverse criticism, some of which is conceded to have real merit. A conscious effort has been made to de-emphasize phylogeny, so that the teacher with definite convictions on relationships among fungi will not be handicapped or inhibited by our opinions, expressed or im- plied. The value of present-day interpretations of phylogeny among fungi, in our opinion, still remains largely open to question. In some instances the most acceptable binomials have not been used; instead we have used the name employed by the writer of the report cited. This practice should not create any serious difficulties for the person interested in synonomy. Except in a few instances, we have not cited the authoritv^ for the binomials employed, for two reasons: (1) the correct authority can be had from Saccardo's Sylloge Fiingonim or from some mono- graph, and (2) valuable space is saved throughout by these omissions. We have arbitrarily chosen to give no consideration to lichens. Mycologists may eventually agree that they should be dispersed among the Eurotiales, Sphaeriales, Hypocreales, Hysteriales, in- operculate Discomycetes, and other groups. It seems to us that, if and when this is done, it will be the result of overemphasis of the morphology of reproductive structures and of underemphasis of a very specialized structure, the lichen thallus. It would appear that the structure of the thallus and its correlated, sym- PREFACE vii biotic, fungus-alga relationship are of much more importance than the morphology of reproductive parts. If it is borne in mind that this specialized thallus makes possible specialized func- tional relationships, it is appreciated that the lichen thallus is neither an als^a nor a fune^us, but is a lichen. Moreover one can best appreciate the possible complexities that may arise in this speciaHzed dual relationship by consideration of such a species as Strigula coviplanata. Its algal component, Cephaleiiros vires- cens, widely parasitizes the foliage of broad-leaved evergreens in tropical and subtropical regions and may be found living happily apart from the pyrenomycetous component. On the other hand, the two may form a lichen, and each component may reproduce itself in its own characteristic fashion. Most of the illustrations are adapted from those of others. If the author of the original drawing has not been mentioned, the omission is unintentional. The degree of magnification is not stated for the reason that the drawings are intended only to con- vey some idea of appearance and relationship of parts. It is intended that the illustrations and explanatory legends will serve to help define terms and thus to provide an understanding of the general morphology of representative genera or species. References to illustrations are omitted from the text. In this way all explanations occur as legends and remain concise. Nearly all the drawings and graphs are the result of our own efforts, ably supplemented by those of Mary H. Wolf. Certain cuts, drawings, and photographs were, however, provided by others; and, even though their sources are mentioned in the legends, we herewith acknowledge again, with grateful appre- ciation, these kindnesses. We are indebted also to Dr. L. E. Weh- meyer, who carefully read the entire manuscript, for his criti- cisms and suggestions and to Mrs. Fred T. Wolf for assistance in proofreading and indexing. These volumes are dedicated to Lewis David de Schweinitz (1780-1834), a distinguished pioneer in American mycology, whose achievements were the results of a labor of love during the spare moments of an otherwise all-too-busy life that was consecrated to official duties in the Moravian church. His best- known contribution. Synopsis Fiingomvi in America Boreali Media Degentium, lists 3098 species of North American fungi. vm PREFACE approximately 1200 of which had not previously been described. Were this his only accomplishment, it would constitute an ever- enduring monument and an inspiration to students of fungi in all parts of the world. His wood-cut picture, appearing as the frontispiece, was supplied by his great-granddaughter. Dr. Ade- laide L. Fries, and it is our special pleasure to acknowledge this courtesy. F. A. Wolf F. T. Wolf February, 1947 CONTENTS 1. THE FOUNDING OF MYCOLOGY 2. ISOLATION AND CULTIVATION OF FUNGI .... 14 Isolation methods, 15. Cultivation, 21. Implications, 27. 3. CLASSIFICATION AND TAXONOMY OF FUNGI ... 29 The classes of fungi, 34. The orders of fungi, 35. 4. THE MYXOMYCETES 40 5. THE PHYCOMYCETES 57 Chytridiales, 63. Doubtful Chytrids, 74. Lagenidiales, 74. Blastocladiales, 77. Monoblepharidales, 83. Lepto- mitales, 88. Saprolegniales, 92. Pythiales, 98. Albuginales, 105. Peronosporales, 108. Mucorales, 116. Entomoph- thorales, 128. Doubtful Zygomycetes, 133. Eccrinales, 134. 6. THE ASCOMYCETES 137 Hemiascomycetes, 139. Endomycetales, 140. Taphrinales, 146. Euascomycetes, 150. Plectomycetes, 152. Euro- tiales, 152. Myriangiales, 163. Erysiphales, 171. Pyreno- mycetes, 179. Dothideales, 180. Hypocreales, 186. Sphae- riales, 198. Laboulbeniales, 233. Hemisphaeriales, 236. Hysteriales, 243. Discomycetes, 245. Helotiales (Inoper- culates), 251. Ostropales, 267. Pezizales (Operculates), 268. Tuberales, 272. 7. THE BASIDIOMYCETES 276 Heterobasidiomvcetes, 284. Dacryomycetales, 284. Trem- ellales, 287. Auriculariales, 291. Ijstilaginales, 299. Ured- inales, 309. Sori and spore forms, 315. Keteroecism, 328. Sexuality of the Uredinales, 332. The Mycoplasm hy- pothesis, 333. Specialization, 334. Classification of Ured- inales, 335. Important species of rusts, 335. Homobasidio- mycetes, 341. Hymenomycetes (Agaricales), 341. Exo- IX X CONTENTS basidiaceae, 341. Thelephoraceae, 343. Clavariaceae, 345. Hydnaceae, 346. Polyporaceae, 347. Agaricaceae, 353. Gastronivcetes, 364. Hymenogastrales, 367. Podaxales, 369. Sclerodermatales, 372. Ly coper dales, 374. Phallales, 377. Nidulariales, 380. 8. THE DEUTEROMYCETES (FUNGI IMPERFECTI) ... 383 Sphaeropsidales, 390. Melanconiales, 392. Moniliales, 394. Mycelia Sterila, 401. AUTHOR INDEX 405 SUBJECT INDEX 412 Chapter 1 THE FOUNDING OF MYCOLOGY Mycology, the study of fungi, had its beginning along with the study of other kinds of living organisms. Knowledge concerning fungi, however, has advanced somewhat more slowly than that of seed plants and larger animals. Nevertheless, if the influence of discoveries in any particular field of biology upon those in other fields is traced, it is apparent that the findings in each field have tended to promote a parallel advance in every other phase of biologic knowledge. Despite this fact, knowledge of microbic hfe lagged from the beginning of historic time until at least well into the nineteenth century. Phenomena connected with the nature, origin, and develop- ment of fungi remained for a long time completely invested in superstition and mysticism. No doubt even in prehistoric times man had, through tests of their edibility, some familiarity^ with such larger kinds of fungi as mushrooms and puffballs, and he may have concerned himself with philosophical musings on their nature. Abundant evidence, dating back to the beginning of historical records, shows man's interest in fungi. For several reasons, however, appreciation of their true nature was gained very slowly. In the first place, self-constituted authority was revered for nearly 2000 years, records indicate, in all matters pertaining to church, state, and secular education. Under such a regimen experimentation was prohibited and might be at- tempted only at the risk of severe punishment, or even execu- tion, if the offender was apprehended. Even today, the influ- ence of the teachings and beliefs of "authorities" on advances in science is still very potent. Perhaps, however, the time will come \\ hen facts in science, no matter by whom they are brought to light, will themselves be "authority," and self-constituted hu- man authorities will dominate thinking to a lesser degree. In the second place, microscopic aids to vision began in 1590 with 1 2 THE FOUNDING OF MYCOLOGY Zacharias Janssen's compound microscope. This microscope and those made during the succeeding period of approximately 200 years were little more than toys or objects of curiosity. Third, there had early come into being a belief that microscopic life originated by spontaneous generation. According to this theory, all sorts of non-living materials might become transformed into living matter, an idea that dominated biologic thinking from the time of ancient Greek civilization until the classic researches of Pasteur in approximately 1860. The experiments of Pasteur con- firmed in part the observations of Leeuwenhoek, Redi, Spallan- zani, and others and established once and for all that living creatures give rise to other living^ thingrs like themselves. It should be clearly comprehended, however, that these workers did not settle the problem of the origin of life. Fourth, fer- micntations were long held to be purely chemical decomposi- tions, a concept fostered by Berzelius and Liebig. A series of researches, culminating in those of Pasteur, however, established that the agencies which induce fermentations are living microbes. There were no doubt other factors which militated against the development of mycology, but all of them contributed in some manner to the impact of the four just discussed. In the brief historical sketch that follows passing mention is made of the more important landmarks in the development of present- day concepts of mycology. Early acquaintance with fungi. Man's early knowledge of the higher plants, the beginnings of which are lost in antiquity, undoubtedly centered around their use for food and medicine. The same stimuli may be assumed to have prompted man to em- ploy fungi similarly, and the kno\\'ledge thus gained ^\'as cer- tainly transmitted to others. The preservation and widespread dissemination of such information, however, wxre seriously handicapped until the fifteenth century, \\'hen printing came into use. Abundant evidence from the wTitings of the Greeks and the Romans shows that they \^'ere able to distinguish edible and poisonous mushrooms. The high esteem in which they held these plants is indicated by a painting, identified as representing Lactarms deliciosiis, found buried beneath volcanic ash among the ruins of Pompeii. Biblical accounts indicate a familiarity among the people of that time with the diseases of crop plants, PREMODERN KNOWLEDGE OF FUNGI 3 notably with cereal rusts, the cause of which they ascribed to offended deities. The Romans, in fact. Instituted festivals to appease these deities, for by so doing they hoped to avert from Fig. 1. Professor Carlos Spegazzini (1858-1926), the foremost student of South American fungi. His studies, while professor of botany at the National University of La Plata, Buenos Aires, Argentina, were primarily taxonomic and dealt with approximately 4000 species. their grain crops the ravages of disease. During the period of about 1000 years after the fall of the Roman Empire in a.d. 476 little was accomplished to increase man's knowledge of fungi. Premodern knowledge of fungi. The invention of printing marks the beginning of a period when interest in plants was re- newed and greatly stimulated, and special consideration was given to the identification of food and medicinal plants. As a conse- 4 THE FOUNDING OF MYCOLOGY quence, herbalists collected, described, and made illustrations of not only seed plants but also many fungi. Among these early herbalists was Bauhin, \\'ho in 1623 listed in his Pinax Theatri Botanici nearly 100 species of fungi. Generic and specific names, as now employed, had not yet come into usage, so that under his group name Fungus are included species belonging in A^arica- ceae, Polyporaceae, Boletaceae, Clavariaceae, Auriculariaceae, Ly- coperdaceae, Phallaceae, and Pezizaceae. His Agaricum Fungus includes sessile Polyporaceae; and his Tubera, truffles and related forms. In Tournefort's Elemens de Botaniqiie (1694) the fungi are arranged in the following 6 groups: (1) Fungus, including all centrally stalked agarics, boletes, and polypores; (2) Boletus, in- cluding Clathrus, Morchella, and Phallus; (3) Agaricus, includ- ing Auricularia and all laterally attached polypores; (4) Lycoper- don, including the various Lycoperdaceae and certaiii slime molds; (5) Coralloides, including the coral fungi and other branched fungi; and (6) Tubera, including subterranean fungi. Mention should also be made of the results of Hooke's observa- tions on fungi, recorded and illustrated in Micrographia and pre- sented to the Royal Society in 1667. Two of the microfungi care- fully studied by him were undoubtedly Phragmidium, a rose rust, and the common mold, Mucor. He decided that both were plants but held to the idea that they were generated by the plant tissues. The outstanding student of fungi of this period was Alicheli, whose classical Nova Plantarinn Genera, published in 1729, stands as a monument to his botanical devotion and zeal. He used such group names as Clathrus, Clavaria, Geaster, Lycoperdon, Phallus, and Tuber, and his illustrations and descriptions are so accurate that specific identifications can be made. In his classification Boletus includes members of the Genus Morchella, as now under- stood; and Puccinia, as he used it, includes Gymnosporangium. He devoted special attention to the larger fungi, grouping them into Fungi lamellati (Agaricaceae), Fungi porosi (Polyporaceae), Fungi ramosi (Clavariaceae), and Fungi pulverentes (puffballs). He also cultivated a number of microfungi in approximately pure culture. These fungi included species of Botrytis and Rhizopus, whose developmental cycle from "seed" he traced, thus proving that each fungus produces its own kind. MODERN HISTORY OF FUNGI S The next landmark in progress was Linnaeus' Species Flanta- rum, published in 1753. This work is mentioned, not because it contributed to a better understanding of fungi, but because it established the binomial system, whereby each plant was given a generic and a specific name. Linnaeus assembled the then- described fungi under the Class Cryptogamia Fungi. Modern history of fungi. After Linnaeus' Species Plantanmt there occurred a period, which may be said to extend to the present day, in which mycology was mainly concerned with the collection and description of fungi. Although the larger, more conspicuous fungi received major attention at first, the microscope was early used to determine morphologic charac- teristics not discernible to the unaided eye. Specimens were preserved, exchanged, and assembled in herbaria. As a result of these practices some workers conducted monographic studies of certain groups, but unfortunately their knowledge of fungi was restricted too closely to those found in herbaria. Such students, as a consequence of this monastic seclusion, possessed little knowledge of the habitats, life histories, or range of variation of fungi, and therefore they described many new genera and species on the basis of minor, inconsequential differences. A few of the older, more important works of this period may be mentioned. Of these, Bulliard's Champignons de France (1791) is outstanding. It contains descriptions and accurate drawings of many of the microfungi, especially Discomycetes, Pyrenomycetes, Mucorales, and Mycetozoa. There followed the taxonomic treatises of Persoon, his Synopsis Methodica Fiin- gorum, in 1801, and his comprehensive Mycologia Europaea, a three-volume work that appeared between 1822 and 1828. He divided the fungi into 2 classes, 6 orders and 71 genera and was the first to establish a usable system for the classification of fungi. Probably the fundamental contribution of all time to my- cologic knowledge is Elias Fries's Systevia Mycologicum, con- sisting of three volumes published between 1821 and 1832. The Sy sterna is the basis of our present-day system of classification and constitutes the starting point of classification of many major groups of fungi. At the same time that Fries, working in Sweden, was laying the foundation for the classification of fungi, pioneer work in North America was being carried out by de Schweinitz, who 6 THE FOUNDING OF MYCOLOGY richly desen^es the title, Father of American Mycology. He collected about 3000 species of fungi in North Carolina and Pennsylvania, 1200 of which he described as new in Synopsis Fimgorinn Carolinae Sitperioris and in Synopsis Fungonim in America Boreali Media Degentiiim. Fig. 2. Professor George F. Atkinson (1854-1918), under whose guidance at Cornell University many mycologists were trained. His researches primarily involved problems in developmental morphology and taxonomy of fungi. Corda's Icones Fiingonmi Hiiciisqiie Cognitonmt, appearing in six volumes published from 1837 to 1854, contains drawings and descriptions of all fungi found in Austria and known to Corda. Of a similar nature, the Tulasne brothers' Selecta Fimgonini Carpologia, published in 1861 to 1865 in three volumes, remains unequalled and unsurpassed in beauty of illustrations. CONCEPTS OF ORIGIN OF FUNGI 7 Mention should be made also of such other excellent and in- dispensable treatises of a purely taxonomic and classificatory nature as those of Patouillard (1887), Quelet (1888), Cooke (1871-1883), Massee (1892-1895), and Bresadola (1927-1932), as well as Engler and Prantl's Die natiirlichen Pfla7ize?ifa?7nlien, Rabenhorst's Kryptogtmicn Flora, the Sydows' Monogvaphia Uredinearimi, Oudemans' Eninneratio Systematica Fimgorimi, and Seymour's Host Index of the Fungi of North America. This list of essential works is incomplete without Saccardo's Sylloge Fimgonim, which now comprises twenty-five volumes, the first having appeared in 1882. This work purports to contain brief descriptions in Latin of all known fungi, about 80,000 species, only an occasional description being inadvertently omitted. Concepts of origin of fungi. Throughout the period extend- ing to the middle of the nineteenth century the theory of spon- taneous generation dominated all explanations of the origin of microscopic life. Fungi were supposed to be generated by the substratum upon which they were found; it seemed impossible to overcome the influence of this ancient dogma. Persons inter- ested in the classification of fungi continued meanwhile to de- scribe and name them as separate entities. Observations that fungi occur on the surface of living seed plants continued to be recorded, and proofs of the ability of fungi to produce disease accumulated. Fontana's observations (1767) on Puccinia graiii- ijiis convinced him that the rust is an independent plant that probably produces "seed." Prevost (1807) proved that the "globules" in bunted wheat are the spores of the pathogen. Nevertheless Unger (1833), among others, insisted that the tis- sues of the plant underwent a metamorphosis to become the fungus. The evidence of Prevost, Fontana, and other workers, in its entirety, failed to shake the foundation of belief in spon- taneous generation. The change in point of view came primarily as the result of the brilliant and convincing experiments of Pas- teur, in which he demonstrated that microbes are air-borne, that they reproduce, giving rise to others like themselves when grown in culture, and that their activities induce fermentations. During the period in which Pasteur was making these revolu- tionary experiments that led to the discoveries of microbes as causal agencies of human and animal diseases, the foundations of knowledge regarding fungi as the cause of plant diseases were 8 THE FOUNDING OF MYCOLOGY also laid, especially by Berkeley (1837), Kiihn (1858), de Bary (1866), Hartig (1874), Woronin (1878), and Brefeld (1884- FiG. 3. Professor William G. Farlow (1858-1926), the first to occupy a chair of cryptogamic botany in the United States. His influence, although centered at Harvard University, radiated widely, for he and his students have been a major influence in guiding the course of mycological de- velopment. 1912). These investigators established such now generally ac- cepted facts as that Phytophthora infestmis is causally related to late blight of potatoes, that the aecia on barberry are genetically CHANGE IN APPROACH TO STUDY OF FUNGI 9 related to the rust on wheat, that the hyphae in wood are the assimilatory stage of the conks which form at the surface of standing trees or logs, that Flasmodiophora brassicae causes club root of crucifers, and that different cereal smuts accomplish in- fection at definite critical periods only. This type of research stimulated an appreciation of the economic importance of fungi and led to wide interest in applied mycology and plant pathology. A summary of this work is contained in Whetzel's History of Phytopathology (1918). As an outgrowth of the establishment of the fact that mi- crobes cause fermentations came Hansen's researches on the mor- phology and physiology of yeasts and the assemblage of studies on the industrial' usage of fungi in Lafar's Technische Mykologie (1904-1907). This phase of mycologic interest, in its recent developments, is more fully discussed in Chapter 4, Volume II, where its results are briefly summarized. 'Change in approach to study of fungi. Gross morphologic similarities and differences constituted the bases for groupings in the early attempts to classify fungi. Then, as microscopes came into use as aids in elucidating details of structure, more and more attention was devoted to microscopic features. Characteristic structural features found by examination with the microscope were employed increasingly to supplement those observable by the unaided eye, but for a long time the purpose of such studies, as the numerous monographs that have appeared indicate, w^as purely taxonomic and classificatory. Gradually there came into being an appreciation of detailed structure and a grasp of its im- portance, as portrayed in Bulliard's Champignons de France and the Tulasnes' Selecta Fimgonim Carpologia. This new point of interest eventually resulted in de Bary's Morphologic imd Physio- logic der Pilze, Flechten, iind Myxomyceten (1866), which my- cologists everywhere regard as a basic w^ork in the study of fungi. In it developmental morphology is emphasized, and the taxonomic approach may with fairness be said to be deempha- sized. At any rate, the investigations by de Bary and similar stud- ies by his students have securely established the morphologic approach to mycologic knowledge, ^^^here the primary interest remains to this day. In fact, de Bary is universally conceded to be the father of modern mycology. 10 THE FOUNDING OF MYCOLOGY In general, much of recent mycological investigation has not distressed too A\idely from the paths laid out by de Bary. Some of the recent contributions are recorded in the chapters that Fig. 4. Professor Robert A. Harper (1862-1946). His researches and those of his students at the University of Wisconsin and Columbia University on cytology and morphology are fundamental in the entire field of mycology. follow; to avoid repetition, it seems best not to discuss them at this point. The impact of certain ones upon current mycologic thinking, however, has been of great significance, and attention is directed therefore to a few of the more noteworthy contribu- tions. Thev include: 1. iMycorrhizae and their structure, by Frank. 2. The need for "bios" in nutrition of yeasts, by Wildiers. CHANGE IN APPROACH TO STUDY OF FUNGI 11 3. Plus and minus strains of black molds, by Blakeslee. 4. Cytology of the ascus, by Harper. 5. The function of rust pvcniospores (spermatia), by Craigie. 6. Self-sterility and cross-fertility in Pleurage, by Ames. 7. Microconidia (spermatia) and fertilization in Sclerotinia, by Drayton. 8. Clamp connections among Hymenomycetes, by Kniep and Bensaude. 9. Genetics of yeasts, by Lindegren. 10. Production of new races of rusts and smuts, by Stakman and his associates. 11. The mycoplasm hypothesis, by Eriksson. 12. The genetics of Neurospora, by Dodge. Several investigators, however, have blazed entirely new my- cologic trails. Among these are: (1) Duller, whose Researches on Fungi explains how the principles of physics may be used to further an understanding of the structure and function of fungi; (2) Sabouraud, whose researches, described in Les Teignes, are basic to an understanding of the skin fungi (Dermatophytes) and other fungi that are pathogenic to man; (3) Wehmer in Ger- many, Raistrick and his associates in Great Britain, Chrzaszcz and his associates in Poland, and Iwanoff and his associates in Russia, whose contributions stress the ability of fungi to synthesize a va- riety of chemical products of industrial use; and (4) Fleming and his associates, best known for their work in penicillin, from which study has come the use of antibiotics of microbial origin. The origins of plant pathology, as Chapter 18, Volume II, will point out, are in mycology, and the two subjects have much in common in recent researches. Unfortunately, however, their interdependence is not fully appreciated, and w-ork in each field would undoubtedly be strengthened if mycologists and plant pathologists were conversant with basic facts in both fields. In summary, this brief historical account has established that mycology began with taxonomy and classification, the basic point of departure in any field of biology. Gradually the morphologic point of view, supplementing taxonomy, developed. At the same time it became established that certain fungi are pathogenic, and as an outgrowth emphasis has been placed in increasing propor- tions upon the economic and industrial aspects of fungal activity. 12 THE FOUNDING OF MYCOLOGY Truth in mvcologv has emerged slowly. Students in this field of learning keenly appreciate that "those who seek for gold dig up much earth, perchance to find a little." LITERATURE CITED Bary, Anton de, Morphologie imd Physiologie der Pilze, Flechten, und Myxoviyceten. Engelmann, Leipzig. 1884. (Translated by Garnsey. Clarendon Press. 1887.) Bauhin, Gaspard, F'max theatri botanici. xviii + 522 pp. Ludovicius Rex, Basel. 1623. Berkeley, AI. J., Introduction to cryptogamic botany. 1857. Brefeld, Oscar, Untersiichungen aus devi Gesmmntgebiet der Mykologie, Hefte 6-15. Heinrich Schoningh, Miinster. 1884-1912. Bresadola, J., Iconograpbia mycologica, Vols. 1-24, Milan. 1927-1932. BuLLiARD, P., Histoire des chmnpig72ons de la France. 386 pp. Paris. 1791- 1798. Cooke, AI. C, Handbook of British fimgi, ivith fidl descriptions of all the species and illustrations of all the genera, Vols. I-II. Alacmillan and Company, London. 1871-1883. Cord A, A. C. I., I cones fiingorimt hiicusqiie cognitorimi, Vols. I-VI. J. G. Calve (Vols. I-IV) and F. Ehrlich (Vols. V-VI). 1837-1854. Engler, a., and K. Prantl, Die natiirlichen Pfianzenfa77tiliejj. I. Teil, Abteil. 1: 1-513, 1897. I. Teil, Abteil. 1**: 1-570, 1900. Engelmann, Leipzig. FoNTANA, Felice, "Observations on the rust of grain, in Lucca, 1767," Phy- topath. Classics, 2. 40 pp. 1932. (Translated by P. P. Pirone.) Fries, Elias, Systema tnycologicwn, sistens fungorimi ordines, genera, et species hucusque cognitas. Vols. I-III. Ernest Alauritius, Grief swald. 1821-1832. Hartig, Robert, Wichtige Krankheiten der Waldbaimie. Ill pp. Julius Springer, Berlin. 1874. HooKE, Robert, Micrograpbia, or some physiological descriptions of minute bodies made by magnifying glasses, with observations and i?jquiries thereupon. 246 pp. J. Allestry, London. 1667. KiJHN, Julius, Die Krankheiten der Kidturgewdchse, ihre Ursachen und ihre Verhiitung. 312 pp. 1858. Lafar, Franz, Technische Mykologie, Vols. I-V. Gustav Fischer, Jena. 1904-1914. (Translated by Salter, 1903-1910). Linnaeus, Carl, Species plantarum. x+ 1200 pp. L. Salvius, Stockholm. 1753. A'Iassee, George, British fungus flora, a classified textbook of Tnycology. Vols. I-IV. Geo. Bell and Sons, London. 1892-1895. Micheli, p. a., Nova plantaru?n genera, xxii + 234 pp. Bernardi Paperini, Florence. 1729. OuDEMANs, C. A. J. A., Emimeratio systematica fungorum. Vols. I-V. Alar- tin Nijhoff, The Hague. 1919-1924. LITERATURE CITED IB Patouillard, N., Les Hy77ie?iomycetes d'Eiirope. Anatoinie generale et classification des champignons superieiirs. 166 pp. Paul Klincksieck, Paris. 1887. Persoon, C. H., Synopsis methodic a fimgonmt. xxx + 706 pp. H. Dieter- ich, Gottingen. 1801. Mycologia Europaea, Vols. I-III. 852 pp. Jacob Palm, Erlangen. 1822- 1828. Prevost, B., Me?noir on the irmnediate cause of bimt or sitmt of wheat, and of several other diseases of plants, and on preventives of bunt. 80 pp. 1807. (Translated by G. W. Keitt.) QuELET, LuciEN, Flore JTtycologique de la France et des pays liviitrophes. xviii + 492 pp. O. Doin, Paris. 1888. Rabenhorst, L., Kryptogamen Flora von Deiitschland, Oesterreich und der Schiveiz, Vols. I-X. Edward Kummer, Leipzig. 1884-1920. Saccardo, p. a., Sylloge fiingorimi omnium hucusque cognitonmi, Vols. 1-25. 1882-1931. ScHAVEiNiTZ, L. D. DE, "Synopsis fungorum in America boreali media de- gentium," Trans. Am. Phil. Soc. Philadelphia, 4: 141-318, 1831. Synopsis fungorum Carolinae superioris. 105 pp. 1918. Seymour, A. B., Host index of the fungi of North A?nerica. xiii + 732 pp. Harvard University Press. 1929. Sydow, p. and H., Monographia Uredineanmi, Vols. I-III. Gebriider Born- trager, Leipzig. 1904-1915. Tournefort, Joseph P. de, Elhitens de botanique, on methode pour con- nditre les plantes, I. 562 pp. L'Imprimiere royale, Paris. 1694. TuLASNE, L. R. and C, Selecta fungonmt carpologia, Vols. I-III. 792 pp. Typographic Imperiale, Paris. 1861-1865. Unger, Franz, Die ExantheiJie der PflanzeJi iind einige mit die sen ver- ivandete Krankheiten der Gewdchse, pathogenetisch und nosographisch dargestellt. 421 pp. Gerold, Wien. 1833. Whetzel, H. H., An outline of the history of phytopathology, 130 pp. W. B. Saunders Co., Philadelphia. 1918. Woronin, M., ''''Plasmodiophora brassicae, the cause of cabbage hernia," Jahrb. wiss. Bota?i., ii;548-574, 1878. (Reprinted in Phytopathol. Classics, no. 4. 32 pp. 1934. Translated by Charles Chupp.) Chapter 2 ISOLATION AND CULTIVATION OF FUNGI The isolation and cultivation of fungi in pure culture consti- tute an essential procedure in studies involving their structure, developmental history, pathogenesis, and physiological activities. A student of fungi must appreciate at the outset, however, that, even though pure culture techniques are useful in the enrich- ment of knowledge, the results of such studies of responses and activities in artificial environments always require judicious in- terpretation. The underlying reasons for this fact, which gen- erally are not sufficiently emphasized, are that fungi may be quite abnormal when grown on substrata entirely unlike those en- countered in nature, and of necessity they react abnormally when entirely separated from the associative effects of other organisms. These influences might be expected to be more pronounced among pathogenic species, having restricted host relations, than among saprophilous species. It should also be borne in mind that in nature pure cultures seldom occur and, if they do, are not maintained for appreciable periods. Many different procedures have been developed for isolating funo-i in pure culture. The choice of method is conditioned by several factors, among them being the kind of fungus, the stage of development of the fungus, the kind of culture (monosporic or gross) which is desired, the judgment of the investigator, and finally the degree of manual skill, dexterity, and painstaking de- votion to detail which the investigator possesses. In some studies it is essential to secure monosporic cultures. Monosporic isolates, however, may be "half fungi," if the fungus is heterothallic or also if it is hermaphroditic, and at the same time self -incompatible and hence self -sterile. It may be advantageous to make a con- siderable number of isolations, using as sources material obtained from different areas or from different host species, in order prop- 14 ISOLATION METHODS IS erlv to appreciate and evaluate the variation that exists within the given species of fungus. ISOLATION METHODS In all the methods that are described in the following account the ul^iquitous presence of contaminants is presupposed. For this reason culture media, glassware, scalpels, needles, forceps, and other laboratory materials and apparatus must be sterilized be- fore being used. The atmosphere of laboratories always contains bacteria and spores of fungi, and they may contaminate plates of media during pouring or planting, or during the transfer of cultures. In order to avoid contamination from this source, isola- tions and transfers are sometimes made by use of special transfer hoods or culture chambers. Their use, however, is unnecessar\^ and constitutes a form of "self-inflicted inquisition" or "purpose- less purgatory," since contamination mav be avoided in the open laboratory if reasonable care is exercised. Surface disinfection. Isolation from diseased tissues or from the interior of fruit bodies of the larger fungi is usually accom- pHshed by planting bits of tissues directly on the surface of agar- poured plates or of tubes of slanted agar. Generally it is advan- tageous to disinfect the surface of such tissues before using frag- ments for planting, for the reason that contaminants occur at the surface. With care the action of the disinfectant may be limited to destruction of those organisms at the surface. Surface disinfection may be accomplished by the use of:. (a) 95% alcohol applied for a few seconds and removed by flaming or by washing; (b) 1 : 1000 solution of HgCU applied for 15 to 45 seconds and removed by washing; (c) a solution of calcium hypochlorite applied for about 1 minute and removed by washing; (d) a 50% solution of H2O2 appHed for 15 seconds to 5 minutes and removed by washing. In all cases washing con- sists in placing the tissues for about 5 minutes in several changes of sterile water, thus removing the disinfectant. It is entirely possible with thick or massive tissues to obviate surface disin- fection, for instead the outer tissues may be removed \\ith a sterilized scalpel. The underlying tissues can then be transferred directly to the surface of appropriate media. After incubation, transplants can be made from the marginal growth of colonies. 16 ISOLATION AND CULTIVATION OF FUNGI Spores as inoculum. If the fungus to be isolated produces spores in sufficient abundance, concentrated suspensions of spores in water can be made and either of two general methods of iso- lation can be employed: (1) the streak method, or (2) the dilu- tion method. The streak method is the oldest and simplest procedure. A needle, bearing a loopful of spores suspended in water, can be Fig. 5. Materials used in isolating single spores by streaking. A. Poured agar plate over whose surface a droplet containing spores in suspension has been spread with a zigzag stroke. B. Needle with flattened tip employed to pick up disk of agar, bearing a spore, cut out by means of loop C. D. Disk, with adhering spore transferred to slanted tube of agar. spread with a zigzag stroke over the surface of a hardened agar plate, care being taken not to break the surface of the agar. In this way most of the spores are brushed off at first, but toward the end of the stroke a few remain. When these few germinate, the colonies are discrete and may be transferred intact to fresh media. If tubes of sterile water are available, a series of increasingly less concentrated suspensions of spores can be made as a first step in isolation by the dilution method. The proper amount of dilution is entirely a matter of choice. A small quantity of inocu- lum from the first tube should be placed in a tube of melted agar cooled to about 45° C. The contents of this tube should be MONOSPORIC ISOLATIONS 11 poured immediately into a Petri dish. Similarly poured plates should be made from the remainder of the series of suspensions. After incubation some of the Petri dishes may bear a few widely separated colonies that are suitable for transfer to other media. With either of these methods difficulties may be encountered in separating the desired fungus from bacterial contaminants. Several techniques have been developed to overcome this diffi- culty. The fungus may be of a t\^pe that will leave the bacteria behind as it grows awav from the original inoculum. Advantage may be taken of this fact by cutting off portions of the hyphal tips when making transfers to new substrata. In other studies the medium upon which the inoculum was first planted or the medium in subcultures may be acidulated with a drop of 25 or 50% lactic acid. By this means media may be so acidified as to in- hibit bacterial growth and at the same time to permit the fungus to grow at the usual rate. Brown (1924) described a procedure which appHes generally in freeing fungal cultures from bacteria. Its basis is the fact that hyphae tend to penetrate the medium. After the colonies have grovv^n for 1 to 5 days, the medium is cut through wdth a sterile knife in advance of the grrowiuCT colony. The colony can then be inverted, and bits of material from the undersurface can be carefully cut away in making transfers. The same principle underlies a method recently successfully employed by Raper (1937) in isolating species of Achlya. He fused glass beads % to % mm in diameter on one rim of a van Tieghem ring and placed the beaded rim downward in a Petri dish. Agar was poured into the dish to bring the medium well up on the ring. The mixed inoculum was placed inside the ring, and as growth proceeded the hyphae extended under the ring and into the agar lyinsr beyond. The bacteria, however, remained confined within the ring. The hyphae outside the ring therefore provided inocu- lum for pure cultures. AIoxospoRic ISOLATIONS. Numerous methods are available for single-spore isolations of fungi. The techniques involved have been assembled in a recent report by Hildebrand (1938). Among these methods may be mentioned those of Barber (1914), Edger- ton (1914), Keitt (1915), LaRue (1920), Dunn (1924), Brown (1924), Hanna (1924, 1928), and Ezekiel (1930). With each technique, practice greatly facihtates successful operation. That 18 ISOLATION AND CULTIVATION OF FUNGI of Barber (1914) is among the early methods employing micro- manipulation. He used a microscope equipped with special mechanical devices to control the movement of capillary pi- pettes by means of which spores suspended in liquids were picked up for transfer. Edgerton (1914) also used capillaries attached to the substage to pick up the spores. The upper end of the capillary tube was sealed. Looking through the microscope, the operator lowered the capillary point until it came into contact with the spore in suspension. A drop of ether was then applied to the closed end of the capillary, causing the spore to be drawn up into the capillary. The spore could be expelled subsequently onto the surface of a Petri-dish culture by gently heating the closed end of the capillary. The methods employed by Keitt (1915), LaRue (1920), Dunn (1924), and Ezekiel (1930) were basically quite similar. The spores were separated in agar plates by the streak method or the dilution miethod. LaRue then located the spore in the agar or upon its surface by direct microscopic examination. When he had found the spore, he lowered a special marker on the nosepiece to cut out a disk of agar containing the desired spore and then trans- ferred this disk with a flattened needle. Ezekiel located the spore to be isolated by inverting the bottom half of the Petri dish, selected the spore or sporeling, and with India ink marked its position on the bottom of the dish. The dish was next righted, and a disk of ag^ar immediately above the marked area was cut out and removed. If the dot of ink is placed while the operator is looking through the microscope, it can be accurately located. This method has much to commend it, especially if spores are well spaced and if it is desired to make numerous isolations. Brown (1924) employed a mechanical appliance to bring a capillar)^ tube near the hyphal tips in a colony arising from germination of a well-isolated spore. The tips were then drawn into the capillary and expelled upon another plate. After a day or two on the new medium the tips were well spaced, and a single hyphal tip could be cut off. Hanna (1924), in isolating single spores of Hymenomycetes, placed a generous fragment of the hymenial surface on a sterile microscopic slide, permitting the basidiospores to be discharged. After discharge, and during observation through the microscope, OTHER ISOLATION TECHNIQUES 19 he brought a needlepoint, held in the hand, near a spore. The spore could be seen to attach itself to the needle and could then be planted on agar to permit germination and subsequent growth. Other isolation techniques. In isolating aquatic fungi, notably Saprolegniales, a small quantity of swarm spores or en- cysted spores may be suspended in water and put into an atom- izer. Some of these spores may then be forced througrh the atomizer, so that they are deposited in tiny droplets on the surface of agar plates. Here they germinate, and marked spore- lings can be transferred to slanted tubes of agar. The isolation of Chytridiales may require a more elaborate technique. Couch (1939) recently isolated certain chytrids, including Rhizidiomyces apophysaWs, Rhizophidiiun carpo- phihmi, and R. imiltipormu. He placed the materials containing these chytrids, namely, decayingr leaves and s^rass, in distilled water to \\hich activated charcoal had been added. Into this were placed, as bait, boiled bits of corn leaves or grass blades. After 2 or 3 days the bait was examined, and, if chytrids occurred within the tissues, the fragment of leaf Mas \\ashed in a stronsf Stream of w^ater. A fragment containing chytrids w^as then ex- cised and placed in a drop of water in a Petri dish. With the aid of a binocular single sporangia were dissected out and placed in a fresh drop of water baited with a fresh bit of leaf frag- ment, and again a single sporangium could be dissected out and dragged over agar to free it from bacteria, or zoospores could be picked up by means of capillary pipettes. Eventually pure cultures could be isolated by these procedures. Berdan (1941) employed this procedure in isolating Cladochytrhnn hyalimim in pure culture on agar. The ascospores are explosively discharged by many species of Pyrenomycetes and Discomycetes. Advantage may be taken of this fact in isolating them in pure culture. The tissues, bearins^ perithecia or apothecia, should be placed in the tops of inverted poured plates of agar. Bits of wet paper toweling or other absorbent paper placed beneath the plant tissues will serve to keep the tissues moist, provide a high relative humidit\% and brincT the fruit bodies sufficiently near the surface of the aijar above to be within range of the ascospores when dischars^ed. If proper conditions are provided, the ascospores on expulsion, singly or en masse, adhere to the agar, and are free from con- 20 ISOLATION AXD CULTIVATION OF FUNGI taminants. Bv means of this simple procedure they essentially isolate themselves in pure culture. If an attempt is made to isolate these same species occurring in decaying leaves and twigs by using macerated tissues as inoculum, there is difficulrv^ in separating the organism sought from protozoa, bacteria, and other fungi present. In isolating Hymenomycetes advantage may be taken of their ability to discharsre their ba- sidiospores. In such studies the spores to be used as inocu- lum can best be collected on a sterile microscopic slide. By methods previously described they can then be transferred directly to a^ar tubes or plates. Instead of this pro- cedure the sporophores may be placed above the surface of agar plates, so that the ba- sidiospores can fall upon the surface of the agar. One of the difficulties that attend efforts to isolate plant- pathogenic fungi is early oc- cupation of lesions by second- ary invaders, both bacteria and fungi. Under these conditions special techniques may be re- quired to isolate the primary organism. This situation is exem- plified by a study of the citrus melanose pathogen, Diaporthe citri. \\^hen infected leaves, fruits, or t\vigs were dipped into alcohol and flamed, and lesions were excised and planted on agar, the pathogen soon became overgro\^n by Colletotrichinn gloeo- sporioides unless subcultures were made as soon as hyphae appeared [Bach and Wolf (1928)]. Similarly other species of fungi may act as "weeds" and stifle the growth of the organism to be isolated. Observation of pure cultures. Two essentially different pro- cedures are available for the study of pure cultures: (a) cultiva- tion in test tubes or in Petri dishes, or (b) cultivation in hanging T^nr r^ T-j III Fig. 6. Diagrammatic arrangement of Van Tieghem cells attached within Petri dish, for repeated observations on germination of spores and subse- quent development. A. Surface view. B. Side view. CULTIVATION 21 drops. Each has its advantages and disadvantages. With the first method the cultures can be kept indefinitely, and subcul- tures can be made at such intervals as maintenance of viability demands. Observations are necessarily intermittent. With the second method cultivation in van Tieghem cells makes continu- ous observations possible as growth proceeds. Although usually the period of observation is limited to a few hours, by governing atmospheric humidity and availability of oxygen in van Tieghem cultures the period may be extended, and much information re- garding the developmental history of the fungus may be gained. CULTIVATION The substrata upon which fungi are cultivated in the labora- tory are called media. Many different kinds of media have been compounded or synthesized. All are made up according to standard specifications, which are usually included in laboratory manuals. Although these media may contain all the essential food substances, namely, carbohydrates, proteins, fats, amino acids, vita- mins, minerals, air, and water, none of them constitutes an ideal substratum. Their deficiency is evidenced by the fact that the mycologist has thus far been unable by use of artificial media to cultivate certain fungi, notably the rusts, downy mildews, and powdery mildews. Furthermore, numerous fungi remain sterile in culture, others cannot be induced to complete their normal developmental cycle in the test tube, and some are manifestly teratological. For these reasons many different kinds of media not Hsted as standard are continually being devised and tested. The mycologist realizes all too keenly that there is no one best medium. The ideal medium is, perforce, most nearly like the substratum on which the specific fungus occurs in nature. Until more fundamental knowledge has been acquired regarding the nutrition of fungi, the investigator will continue to depend upon empirical methods for their artificial cultivation. On the basis of their composition, media may be regarded as of two kinds: synthetic (mineral) and non-synthetic (organic), and they may be either Hquid or semisohd. Agar in the proportion of about 2% is used almost exclusively in making the media semi- solid. 22 ISOLATION AND CULTIVATION OF FUNGI Fungi generally grow best in media abundantly supplied with carbohydrates. Another requisite is that the pH be within the ranc^e of 5 to 6. Since carbohydrates and proteins are decomposed by heat, especially if the medium is acid or alkaline, they should be steri- lized separately and added to the other constituents, care being taken to prevent contamination. Agar media enriched by the addition of fruit juices may not solidify unless the fruit juices are sterilized separately and then aseptically added after the constituents have been cooled to about 50° C. Wolf and Shunk (1921) demonstrated that, if agar or gelatin media are cooled before being made acid or alka- line, they will jellify at hydrogen- or hydroxyl-ion concentra- tions far greater than those permitting growth of microorganisms. In manuals [Rawlins (1933), Riker and Riker (1936)] con- taining formulae for compounding various kinds of media may be found instructions regarding such essential matters as clearing of media, filtration, adjustment of reaction, and steriHzation. For this reason these subjects will not be given consideration here. Most kinds of organic media contain meat extract and peptone as essential constituents. The meat extract supplies mainly the ash constituents, organic nitrogen, and certain organic acids. Peptone supplies decomposable proteins that can be cleaved by many fungi to yield essential amino acids. When media con- taining these materials are enriched by the addition of plant sub- stances extracted by boiling, like those from potatoes, corn meal, or fresh beans, they constitute satisfactory substrata for the cul- tivation of a large number of different species of fungi. Such media, in fact, are widely used in mycological and phytopatho- logical laboratories. Mineral nutrient media have a more limited usage than organic media. They are employed especially in physiological studies of the suitability of a single carbohydrate, amino acid, or mineral. A mixture of mineral salts in liquid cultures or jellified with agar furnishes the basis for such media. In the cultivation of certain groups of fungi specific media have come to be used quite generally. Members of the Sapro- legniales and related orders, for example, are commonly culti- vated on boiled hempseeds placed in water. The Polyporaceae and Thelephoraceae usually grow well and may be made to fruit CULTIVATION 23 on malt agar or on sterilized sawdust or blocks of wood. Etter (1929), using a mixture of malt liquid, wood powder, corn meal and starch in flasks, secured typical pileate sporophores of such species as Lenwius lepideuSy Pleurotiis ostreatiis, Coprinus atra- mentarhiSy C. Tnicaceiis, Polyporus pereniiis, P. farloivii, Gano- derjna ciirtisii, and Trametes peckii. The incorporation of extracts from various fruits and vege- tables into media may also stimulate fruiting by wood-rotting fungi, but the sporophores on such substrata are sometimes ab- normal. Long and Harsch (1918) used such media in studies with wood-rotting species and concluded that the nature of the substrate is of minor importance in stimulating the formation of sporophores. They secured fruiting on plant-extract media by the following species: Dae dale a juniper ina, Forties applanatus^ F. pinicola, F. roseiis, F. robineae, F. texaniis, Irpex lacteiis, Len- zites saepiaria, Pleurotiis ostreatus, Polyporus ajiceps, P. cinjia- barinuSy P. dryophilus, P. farloiuii, P. obtusus, P. sulphur eus, Poly- stictus hirsutuSy P. versicoloTy Trametes peckiiy and T. serialis. The studies by Badcock (1943) indicate, moreover, that the nature of the substrate is a vital factor in the production of sporo- phores in culture. He used sawdust as a basic material supple- mented by readily available nutrients. As additional factors there should be a plentiful supply of moisture in the substratum, an atmosphere of high relative humidity, and exposure to dif- fuse Hght of moderate intensity. Under these conditions Bad- cock secured fructifications of 82 of the 92 species tested. The spores of many species, notably of the downy mildew^s, powdery mildews, and rusts, can be germinated in w^ater, where they will continue to grow until their reserve of stored food is exhausted. Even though development is determinate under these artificial conditions, observations of grow^th changes in water contribute materially to the sum total of useful information. For example, the oospores of downy mildews are notoriously refrac- tory to germination, and hence an understanding of the necessary environmental conditions, except for a few species, has not been achieved. Hiura (1930), however, described a method for ger- minating the oospores of Sclerospora graittmicola. A layer of moistened cotton is placed in the top of a Petri dish and another in the bottom, ample space being left between the layers. Moist 24 ISOLATION AND CULTIVATION OF FUNGI B filter paper is then placed lightly in the bottom part, and on it are sprinkled small amounts of well-macerated tissues contain- ing oospores. Blocks of 2% agar on which spore powder is sprinkled can be substituted for moist filter paper. Using this procedure, Hiura was able to study phenomena of infection, as circumscribed by tempera- ture and moisture [Hiura (1935)]. In the artificial cultivation of various fungi of the downy and powdery mildews and the rusts it is necessary to trans- fer them from living plants to living plants growing in a more or less controlled en- vironment. Determination of heteroeciousness in rusts is for the most part accomplished by such techniques. Clinton and McCormick (1924), however, floated green leaves on w^ater in Petri dishes and by this pro- cedure successfully accom- plished infection by 28 species of rusts from 12 genera. Experiences w^ith Perono- spora tabacina indicate that it can be maintained in culture on living tobacco plants, pro- vided the inoculated plants are maintained in an artificial environment in which the temperature does not exceed 65° F, the relative humidity is at the point of saturation, and the light is diffuse. Under such conditions crops of sporangia have been produced during every month of the year. Presumably other downy mildews would behave similarly in a suitable artificial environment. Maintenance of cultures. Much can be learned about a given fungus if it is maintained in pure culture on a chosen mm :ii!ii!iiiiiiiiiiiiiiiiiiiiiiiiif 1 Fig. 7. Schematic arrangement to show method for isolating Ascomy- cetes that forcibly expel their asco- spores. A. Poured agar plates, sur- face view, over infested leaf that rests upon pad of moist filter paper; B, side view. The tissues in which the ascocarps are embedded are ele- vated on the pad to permit the spores, when discharged, to reach the agar surface above them. MAINTENANCE OF CULTURES 25 medium, regardless of the nutritional defects of that substrate and of whether the organism is pathogenic or saprogenic in its natural state. First of all, a modicum of skill and good judgment is required to keep a fungus alive by transfer at sufficiently fre- quent intervals. Not only must it be kept alive, but also as a result of manipulation and examination each fungus will come to be recognized as having a distinctive appearance. If, then, numer- ous isolates of that species are assembled and their appearance on different substrates is compared, it will be evident that charac- teristic differences between isolates exist. Some isolates may reproduce more abundantly than others, their myceha may dif- fer in color, the mycelial mass may vary in laxness or floccose- ness and also in growth rate or in other features that do not lend themselves well to description. Eventually the observer is forced to conclude that each individual isolate must be regarded as a specimen, and that the species consists of an assemblage of closely related individuals. The frequency of subculturing will depend upon several fac- tors, including (1) the peculiarities of the fungus, (2) the culture medium, and (3) the temperature and humidity of the storage cabinet. Fungi that produce sclerotia, such as Rhizoctonia solani and Sclerotium rolfsiij will remain alive for several years even though the medium has dried up and shrunken to a corneous mass. The result of transfer of mycelium or spores from old cultures that are thoroughly desiccated may indicate that the culture is dead. It may be possible, however, to revive such an old culture by flooding its surface with a liquid medium and then incubating for a day or two before again attempting to subculture. Species that produce spores in such abundance that spore clouds may be formed even when the culture is jarred only slightly are difficult to maintain in a state of purity, and they may become contaminants in the whole culture collection unless the utmost care and faultless technique are employed during sub- culturing. Monilia sitophila and members of the genera Asper- gillus, Penicillium, Mucor, and Trichoderma are included in a group having this peculiarity. If the temperature of the culture cabinet can be maintained at about 20° C, most species of fungi need be transferred only two or three times a year. Even when transfers are infrequently 26 ISOLATION AND CULTIVATION OF FUNGI made, however, the task of subculturing becomes onerous, a situation which constitutes an argument for the estabhshment and maintenance of "bureaus of culture collections." With certain species it may be found advantageous to incubate them for a few days at a temperature favorable for rapid development and then to place them in storage at 10° C. Efforts to retard the drying out of the medium by the use of paraffin on the cotton stoppers or of waxed paper caps or rubber thimbles are quite uniformly unsuccessful because they promote contamination. Spores lodged in or on the cotton stoppers are thereby provided with sufficient moisture to permit them to germinate and the organism to employ the cotton fibers as a nutrient substrate. Because of lack of detailed knowledge regarding the nutri- tional requirements of fungi, a choice of culture medium is quite arbitrary. Potato agar, bean agar, corn-meal agar, wort agar, malt agar, and Sabouraud's agar are among those commonly used to maintain cultures. Some fungi appear to require comparison with type cultures for certain identification. This situation becomes complex in dealing with an organism which does not remain true to type. In culture, certain fungi gradually vary in mycelial color, texture of the colony, and in sporulation or other characters. Moreover, others gradually lose their vigor, dwindling until they become so depauperate and so different from their appearance when first isolated as to be unrecognizable as the same species. Some mu- tate without known reason and become clearly distinct in ap- pearance from normal colonies. Finally, some pathogenic fungi lose virulence in culture, and no basis has been established for re- storing their aggressiveness. On the other hand, others, such as Taphrwa dejormans and Ustilago zeae, have been maintained in culture for years without apparent loss of virulence. Until more basic knowledge can be gained of the influence of nutritional and environmental factors each mycologist who maintains fungi in culture must be guided largely by his o^vn experiences in culti- vating them. Another serious difficulty that will be encountered sooner or later by anyone who maintains cultures of fungi is infestation by mites. These pests devour the fungi and, in crawling from one IMPLICATIONS 27 culture to another, contaminate all of them. jVIites cannot be excluded no matter how tight the stoppers are. To guard against infestation the strictest vigilance and the most stringent sanitary measures must be employed at all times. Before infestation is widespread, fumigation with carbon tetrachloride or pyridine can be effectively employed. These chemicals are allowed to evaporate from shallow dishes placed in the culture cabinets. After 3 or 4 days a second fumigation is necessary because the egg stage and an encysted stage of the young mite are more resistant to vapors of these chemicals than are adult mites. All cultures should be transferred early after fumigation. IMPLICATIONS Certain principles underlie the techniques of isolation and cul- tivation of fungi. Following routine directions and procedures may cause failure to isolate or to grow a specific fungus arti- ficially. Failure may be attributable to use of the improper kind of substrate. Fungi should be expected to respond in a most nearly normal manner if food and environmental influences ap- proximate those that they encounter in their natural habitat. It is of course impossible in many studies to duplicate these condi- tions artificially, but a knowledge of these facts about a given fungus may prevent loss of time in attempts to isolate it and mis- interpretation of results of its responses when grow^n in culture. It follows, therefore, that the fungus in culture may be quite pathologic and that a study of its physiology in culture may in reality be a study of its pathology. LITERATURE CITED Bach, W. J., and F. A. Wolf, "The isolation of the fungus that causes citrus melanose and the pathological anatomy of the host," /. Agr. Research, 57; 243-252, 1928. Badcock, E. C, "Methods for obtaining fructifications of wood-rotting fungi in culture," Trails. Brit. Mycol. Soc, 26: 127-132, 1943. Barber, M. A., "The pipette method in the isolation of single microorgan- isms and in the inoculation of substances into living cells," Philippine J. Sci., B, 307-360, 1914. Berdan, Helen B., "A developmental study of three saphrophytic chytrids. I. Cladochytriimi hyalimim, sp. nov.," Am. J. Botany, 28: ^22-A}8, 1941. 28 ISOLATION AND CULTIVATION OF FUNGI Brown, W., "Two mycological methods. I. A simple method of freeing fungal cultures from bacteria. II. A method of isolating single strains ,of fungi by cutting out a hyphal tip," An?!. Botany, 3^:401-404, 1924. Clinton, G. P., and F. A. McCormick, "Rust infection of leaves in Petri dishes," Con??. Agr. Expt. Sta. Bull., 250:475-501, 1924. Couch, J. N., "Technic for collection, isolation, and culture of chytrids," /. Elisha Mitchell ScL Soc, 55: 208-214, 1939. Dunn, M. S., "The micro-loop. A rapid method for isolating single spores," Phytopathology, i^: 338-340, 1924. Edgerton, C. W., "A method of picking up single spores," Phytopathology, 4:115-117, 1914. Etter, Bessie E., "New media for developing sporophores of wood-rot fungi," MycoL, 21: 197-203, 1929. EzEKiEL, W. N., "Modified procedure with the Keitt single-spore method," Phytopathology, 20: 583-586, 1930. Hanna, W. p., "The dry-needle method of making monosporous cultures of Hymenomycetes and other fungi," An??. Botany, 38: 791-795, 1924. "A simple apparatus for isolating single spores," Phytopathology, 18: 1017- 1021, 1928. Hildebrand, E. M., "Techniques for the isolation of single microorganisms," Botan. Rev., 4: 611-66^, 1938. HiURA, M., "A simple method for the germination of oospores of Sclero- spora graminicola,^'' Science, n.s., 12: 95, 1930. "Mycological and pathological studies on the downy mildew of Italian millet," Giju Inip." College Research Bull, 35: 121-283, 1935. Keitt, G. W., "Simple technique for isolating single-spore strains of cer- tain types of fungi," Phytopathology, 5: 266-269, 1915. LaRue, C. D., "Isolating single spores," Bota?i. Gaz., 70:319-320, 1920. Long, W. H., and R. M. Harsch, "Cultures of wood-rotting fungi on arti- ficial media," /. Agr. Research, 12: 33-82, 1918. Raper, J. R., "A method of freeing fungi from bacterial contamination," Sciejjce, n.s., 85: 342, 1937. Rawlins, T. E., Phytopathological and botanical research methods. 156 pp. John Wiley and Sons, New York. 1933. RiKER, A. J. AND R. S., Introduction to research on plant diseases. 117 pp. J. S. Swift Co. 1936. Wolf, F. A., and I. V. Shunk, "Solid culture media with a wide range of hydrogen-ion or hydroxyl-ion concentration," /. Bact., (J: 325-330, 1921. Chapter 3 CLASSIFICATION AND TAXONOMY OF FUNGI If the fungi are among the "simplest of organisms" or the "humblest of plants," as some writers maintain, their classifica- tion should not present any great difficulties. As far as the first phrase is concerned, however, the student is ultimately forced to conclude that there is nothing simple about fungi except our knowledge of them. And as for their "humbleness"— well, that is only the estimation of man, and who would gainsay that he is among the humblest of animals? Moreover so many problems arise in classifyinsf fun^i that volumes have already been written on this subject. It is of primary importance in dealing with any group of bio- logical materials that they be organized or classified and named; otherwise all is chaos. "By the classification of any series of objects," Huxley says, "is meant the actual or ideal arrangement together of those things which are alike and the separation of those which are unlike, the purpose of the arrangement being, primarily, to disclose the correlations or laws of union of proper- ties and circumstances and, secondarily, to facihtate the opera- tions of the mind in clearly conceiving and retaining in memory the characters of the objects in question." x\ll classifications of fungi are man-made, and none is without flaws. Comparison of them indicates that, as more information has been obtained, the systems of classification which have from time to time been proposed have become increasingly more ade- quate and comprehensive. The ideal classification has not yet been proposed, however, and indeed it could be perfected only after a vast amount of intensive study, much more than has been accomplished to date or that has likelihood of being accomplished within the next few centuries. When such a classification is perfected, it should accurately reveal morphological similarities and differences between any and all species and hence should 29 30 CLASSIFICATION AND TAXONOMY OF FUNGI indicate their evolutionary position and genealogical relationship. Such a system could appropriately be designated the natural sys- tevi. In lieu of a natural system, purely artificial or predomi- nantly artificial systems are in general use. In any scheme of classification the worker must deal with units, each of which must have a designation, such as phylum, class, order, family, genus, and species. Definition of these terms is a vexatious academic problem upon which systematists are not in accord but have a variety of opinions. Nomenclature. As a natural consequence of attempts by dif- ferent persons to apply names to plants and of difficulties at- tendant on printing and exchanging information on this subject, the same organism often came to bear more than one name. This situation of course could lead only to confusion. Moreover a name at first was either a single word or a brief descriptive phrase. Since the publication of Linnaeus' Species Plaiitarum in 1753, however, each species bears two names, the first being that of the genus to which it belongs, and the second being that of the species. Subsequently, as new^ organisms were described, the principle of priority came to be accepted in determining the proper binomial. According to this principle, the oldest bino- mial used is the accepted one. If this principle is regarded as sacrosanct and its strict application is insisted upon in spite of general usage and common sense, there is little chance of estab- lishing stability in nomenclature, especially for certain old and well-known genera. Other problems in nomenclature meanwhile arose, and the machinery for their settlement was created at the International Congress of Paris in 1900. The codes and rules agreed upon by committees then and at subsequent International Congresses constitute a working basis for the solution of all such problems. A composite statement of these international rules was published as a supplement to The Journal of Botany (British and Foreign) for June, 1934, and should be carefully perused by all biologists. Among the facts important to mycologists in these rules are: {a) the nomenclature of the Myxomycetes begins with Linnaeus' Species Plantarzim, 1753; (b) the nomenclature of the Uredinales, Ustilaginales, and Gastromycetes begins with Persoon's Synopsis Methodica Fungoruvi^ 1801; and {c) the nomenclature of all other fungi is based on Fries's Sy sterna Mycologiciim, 1821-1832. NOMENCLATURE Bl The starting point of classification of all Basidiomycetes, except the TremeUineae, is Volume 1 (1821) of the Systeiiia. The classification of the TremeUineae and of the Discomycetes begins in Volume 2, Part 1 (1822). The classification of the Pyreno- mycetes and Sphaeropsidaceae starts in Volume 2, Part 2 (1823); that of the Phy corny cetes and Hyphomycetes, in Volume 3, Part 2 (1832). ' . The generic name is a noun or substantive, the initial letter of which is always capitalized; the species name is adjectival, agrees in gender with the generic name, is either nominative or genitive in case, and normally is not capitalized. Some specific names are bestowed in honor of persons or places, and some authorities capitalize all such names, whereas others consistently begin them with a lowxr-case letter. Accord in this matter is of little real consequence, certainly not to the extent of fancying that an ant- hill is a mountain. It is quite unfortunate, however, that generic names of hosts have been used as specific names, especially of pathogenic fungi, for the reason that experimentation reveals a wide host range for some species. In consequence many such specific names must eventually be reduced to synonymy. For the purpose of precision the name of the person who first pub- lished the binomial follows the name of the organism. If the name is subsequently changed, this fact is indicated by placing in parentheses the name of the person who published the first de- scription and following it immediately with the name of the person who changed the name. One excellent rule requires the description of all species in Latin. Latin has the advantages of being a dead language, of being exact in meaning of terms, and of being a tool of all scholars. Objections to its employment would vanish like "a cloud of mist smitten by the sun" if the objector were compelled to translate descriptions of fungi from the Arabic, Slavic, or some of the less frequently encountered Oriental languages. Another very important provision in the rules deals with the naming of fungi with pleomorphic life cycles. Naturally the different states or stages of the same species have been given dif- ferent names. It has been agreed that pleomorphic fungi can bear only one binomial, and the earliest name given to the perfect form, beginning with Persoon's Synopsis or Fries's Systeuw, is the accepted one. The perfect form is indicated to be that 52 CLASSIFICATION AND TAXONOMY OF FUNGI Globose Cylindrical which ends in the ascus stage in Ascomycetes, in the basidium in Basidiomycetes, and in the teHospore in Uredinales and Ustilagi- nales. Changes in systems of classification. An appreciation of the need for changes in nomenclature and taxonomy that may arise in the classification of fungi can be gained if it is borne in mind that 10 genera contain- ing fe\\'er than 100 species are included in Linnaeus' Species Pla32tarii772, and that now, ac- cording to Saccardo's Sylloge Fungorwn, there are approxi- mately 5000 genera contain- ing more than 80,000 named species. Linnaeus included in Cryp- togamia Fungi 27 species of Agaricus, 12 of Boletus, 4 of Hydnum, 2 of Phallus, 3 of Clathrus, 2 of Elvela, 8 of Peziza, 8 of Clavaria, 9 of Lycoperdon, and 1 1 of Mucor. In Syjwpsis Methodica Fim- gonmi Persoon divided all fungi into 2 classes, Angio- thecium and Gvmnothecium. These two classes included 6 orders and 71 genera. In Fries's Sy sterna Mycologiciim expansion and changes were provided for by grouping the fungi into four classes: Coniomy- cetes, Hyphomycetes, Gastromvcetes, and Hymenomvcetes, and then further dividing these classes. The Coniomycetes, for ex- ample, were eventually subdivided into Ordo I, Tubercularini; Ordo II, Stilbosporei; Ordo III, Sporodesmiei; and Ordo I\", Hypo- dermii seu Entophyti. At the present time it is estimated that more than 50 orders have come to be recognized. On the basis of Saccardo's Sylloge Fiingorum the fungi are classified into the following classes: Schizomycetes, Myxomy- cetes, Phycomycetes, Ascomycetes, Basidiomycetes, and the form-class Deuteromycetes or Fungi Imperfecti. Bisby and Ainsworth (1943) report that the approximate number of Myxo- Muriform 0 Bacilliform Echinulate Setose Filiform Fig. 8. Types of spores and the terms used to designate each kind. CHANGES IN SYSTEMS OF CLASSIFICATION 33 mycetes is 450, of Phycomycetes 1000, of Ascomycetes 12,120, Basidiomycetes 13,430, and Fungi Imperfecti 10,500, making a total of 37,500 species. They further indicate that only about one-third of all species have been described. So far as informa- tion warrants, in all present-day systems the division of each of these classes into orders, families, tribes, and similar subdivisions indicates phyletic relationships and evolutionary developments, the simplest being placed first and the more complex following in an ascending series. All of them therefore are ordinarily re- garded as natural systems, but there remains much in classifica- tion that is arbitrary or has been devised by man for his mental convenience, and hence is purely artificial. For example, the Agaricaceae are divided into tribes on the basis of color of spores en masse, tribal names being Leucosporae, Rhodosporae, Phaeo- sporae, Ochrosporae, and xMelanosporae. Similarly color, shape, and septation of spores, either as separate characters or in com- bination, especially among the Ascomycetes and Deuteromy- cetes, furnish the basis for such groupings as Amerosporae, AI- lantosporae, Hyalodidymae, Phaeodidymae, Hyalophragmeae, Phaeophragmeae, Dictyosporae, Scolecosporae, and HeHco- sporae. Any system of classification is successful only if its use will enable the worker to identify an unknown organism conveniently and accurately and at the same time relate it to known organisms. Years must still elapse, however, before the vast expanse of ig- norance will be sufficiently carefully charted to enable the stu- dent to know that he has closely approximated a natural system. Meanwhile evidence will have accumulated to clarify the ques- tion of \\ hether the fungi are a monophyletic series derived from filamentous green algae, whether they are a polyphyletic as- semblage derived from different groups of green and red algae, or whether they are a distinct phylum derived from protozoan an- cestry. This third hypothesis, voiced by Martin (1941), appears to fit present-day facts most nearly. Although many systems of classification have been proposed, the few examples which have been mentioned indicate the evo- lution of present-day systems. Certain investigators would now exclude bacteria and slime molds from the Fungi. Many would separate the Fungi from the Algae, giving each a coordinate S4 CLASSIFICATION AND TAXONOMY OF FUNGI rank as a phylum. The reasons for these proposals need not be stressed. Keys are useful as aids in the identification of fungi, but in the present imperfect state of knowledge no generally satisfac- tory keys are possible. Those of Clements and Shear (1931) are based upon Saccardo's groupings. The recent ones by Martin (1936, 1941) are most service- able in determining the family in which a given unknown or- ganism belongs. Many mono- graphic treatments of specific orders and families that con- tain keys are available and W'ill be mentioned subse- quently. The class and or- dinal key that follow^s pro- vides an introduction to the major groups of fungi and gives some indication of their interrelation. That these keys are neces- sarily artificial cannot be too strongly emphasized. Experi- ence is an irreplaceable asset in the use of these keys or, for that matter, of any others. Terms must be understood, Stavirospore Allantospore and a glossary may prove Fig. 9. Artificial groupings within families are based in part upon shape of spores and septation. The names given apply to the characteristics of spores. helpful, although not wholly satisfactory. Exceptions will be encountered, and it must be appreciated that the taxonomic position of many species has not yet been established wdth finahty. This conclusion is all too apparent even among groups of fungi that have been excellently monographed or are best known. THE CLASSES OF FUNGI 1. Vegetative or assimilatory stage plasmodial Class Myxomycetes 4 1. Vegetative or assimilatory stage usually filamentous 2 2. Mycelium usually non-septate throughout Class Phycomycetes 11 2. Mycelium septate throughout THE ORDERS OF FUNGI 3S 3. Spores of perfect or sexual stage borne in asci Class Ascomycetes 21 3. Spores of perfect or sexual stage borne on basidia Class Basidiomycetes 34 3. Lacking asci and basidia but usually possessing asexual spores Class Fungi Imperfecti 43 THE ORDERS OF FUNGI Class Myxomycetes 4. True plasmodiuni not formed, swarm spores amoeboid but not flagellate ^ 5. Swarm spores retaining individual identity, encyst at tip of "^^ss Order Acrasiales 5. Swarm spores connected by long pseudopodia into chains or ^^^^ Order Labyrinthulales 4. True plasmodium formed, swarm spores amoeboid and flagellate 6. All parasitic on vascular plants " Order Plasmodiophorales 6. Saprophytic y 7. Spores borne externally on thallus, each producing eight swarm cells on germination Subclass Exosporeae (Alyxogastres, in part) 7. Spores borne within fructification, each producing one or two swarm cells on germination Subclass Endosporeae (Alyxogastres, in part) 8 8. Spores in mass typically violaceous or black, lime pres- ent or absent 9 9. Peridium, capillitium, or both calcareous Order Phvsarales 9. Neither peridium nor capillitium calcareous, lime usu- ally present on stipe and columella Order Stemonitales 8. Spores in mass typically pallid, yellow, brown, or rosy, lime never present 10 10. True capillitium lacking or only scantily developed Order Liceales 10. Capillitium well developed, thread-like, sculptured Order Trichiales Class Phycomycetes 11. Mycelium lacking or poorly developed (a rhizomycelium), en- tire thallus or its parts functional in reproduction 12 12. Thallus microscopic, unicellular, becoming a single sporan- gium, a sorus of sporangia, or a gametangium; sexual repro- duction unknown or of various kinds; zoospores uniciliate or biciliate Subclass Archimycetes 13 B6 CLASSIFICATION AND TAXONOMY OF FUNGI 13. Mycelium lacking, or consisting of delicate rhizoid-like threads Order Chytridiales 14 14. Mycelium lacking, thallus at first naked and amoeboid; holocarpic, parasitic Suborder Alyxochytridineae 14. Mycelium of delicate threads, thallus with cell wall from the first, sterile and fertile portions distinct Suborder Alycochytridineae 13. Mycelium a chain of cells, each a functional sporangium, antheridium, or oogonium; zoospores biciliate Order Lagenidiales 11. Mycehum well developed, for the most part remaining vegeta- tive; reproductive parts separated from assimilatory by septa 15 15. Sporangia of two kinds: thin-walled and thick-walled, re- sistant; sexual reproduction lacking or involving fusion of motile gametes forming motile zygote; zoospores uniciliate Order Blastocladiales 15. Thin-walled sporangia only; sexual spores thick-walled 16 16. Gametangia dissimilar; fertihzation heterogamous to form oospore, asexual spores motile Subclass Oomycetes 17 17. Antherozoids and zoospores uniciliate Order Monoblepharidales 17. Antherozoids absent; fertilization tube extends from antheridium to oosphere 18 18, Oospheres 1 to several in each oogonium, peri- plasm absent; zoospores biciliate, commonly di- planetic Order Saproleginales 18. Oospheres 1 in each oogonium, periplasm present; zoospores biciliate 19 19. Thallus aquatic, saprophytic, arbusculate, branches constricted Order Leptomitales 19. Thallus aquatic, not arbusculate nor con- stricted, parasitic, zoospores extruded in a vesicle Order Pythiales 19. Thallus terrestrial, parasites on seed plants; sporangia germinating by zoospores or germ tube; oospores within host Order Peronosporales 16. Gametangia morphologically similar, fertilization isog- amous to form zygospore; asexual spores conidia Subclass Zygomycetes 20 20. Saprophytes; sporangia from one to many-spored; conidia not forcibly liberated Order Alucorales 20. Mostly parasites on insects; conidia forcibly dis- charged; zygospores formed within hosts Order Entomophthorales THE ORDERS OF FUNGI 57 Class Ascomycetes 21. Asci not aggregated in ascocarps, that is, naked and formed singly or in loose clusters Subclass Hemiascomycetes 22 21. Asci aggregated, enclosed in well-developed ascocarps Subclass Euascomycetes 23 22. Saprobic, ascus formed directly from zygote, mycelium not well developed, cells usually bud Order Endomycetales (Saccharomycetales) 22. Strictly parasitic on vascular plants, apical cells become asci, mycelium not well developed, budding very common Order Taphrinales (Exoascales) 23. Ascocarps lack definite ostioles, hence are cleistothecia 24 24. Asci irregularly arranged Plectomycetes 25 25. Stroma lacking, asci filling interior of ascocarp Order Eurotiales (Aspergillales) 25. Stroma present, asci borne singly in locules Order Myriangiales 24. Asci regularly arranged Order Erysiphales (Perisporiales) 23. Ascocarps provided with ostioles or cupulate, asci ar- ranged in parallel series 26 26. Ascocarps with neck-like ostioles, hence perithecia 27 27. Perithecia borne on a receptacle, minute parasites on insects and arachnids Order Laboulbeniales 27. Perithecia not borne on a receptacle 28 28. Perithecia globose, ostiole typically circular in cross-section Pyrenomycetes 29 29. Perithecia borne singly or in a stroma, black or dark colored 30 30. Perithecia provided with definite wall Order Sphaeriales 30. Differentiated perithecial walls lacking, asci borne in stromatic locules Order Dothideales 29. Perithecia borne singly or in a stroma but always bright colored— red, yellow, purple Order Hypocreales 28. Perithecia elongated with a slit-like ostiole Order Hysteriales 28. Perithecia dimidiate, opening with a pore or irregular rift Order Hemisphaeriales 26. Ascocarps wide open, discoid, hence apothecia Discomycetes 31 31. Asci inoperculate 32 32. Apothecia superficial, mostly small, fleshy, or waxy Order Helotiales 32. Apothecia innate, mostly small, carbonaceous Order Phacidiales 38 CLASSIFICATION AND TAXONOMY OF FUNGI 31. Asci operculate 33 33. Apothecia epigeic, variable in size, fleshy; stalk inconspicuous Order Pezizales 33. Apothecia epigeic; large, fleshy; stalk promi- nent Order Helvellales 33. Apothecia hypogeic, fleshy, remaining closed Order Tuberales Class Basidiomycetes 34. Basidia septate longitudinally or transversely, or arising from a teliospore or probasidium; or if non-septate, basidiocarp gelat- inous; basidiospores commonly bud on germination 35 35. Basidiocarp lacking, basidia arising from teliospores 36 36. Teliospore (chlamydospore) on germination produces tubes (basidia) septate or not, bearing sessile sporidia that bud Order Ustilaginales 36. Teliospore on germination produces tubular four-celled basidium, each cell bearing a single sporidium on a ste- rigma; sporidia produce germ tube on germination Order Uredinales 35. Basidiocarp present, mostly gelatinous 37 37. Basidia septate 38 38. Septations transverse Order Auriculariales 38. Septations longitudinal, two- or four-divided Order Tremellales 37. Basidia non-septate, with two blunt terminal sterigmata Order Dacryomycetales 34. Basidia always non-septate, cylindrical or broadly clavate; pro- basidium lacking; basidiospores usually form hyphae on germina- tion Subclass Homobasidiomycetes 39 39. Hymenium exposed before maturity of spores % Order Agaricales (Hymeniales) 39. Hymenium remaining closed or opening only after basidio- spores have been liberated from basidia (Gastromycetes) 40 .js 40. Hymenium present and lining labyrinthiform chambers of gleba 41 41. Gleba fleshy or wax\^ or sometimes slimy and fetid at maturity, but if so not exposed Order Hymenogastrales 41. Gleba fleshy, borne on lower surface of centrally stipi- tate pileus-like structure, angiocarpous or gymno- carpous Order Podaxales 41. Gleba fleshy or waxy or slimy and fetid and always exposed at maturity Order Phallales 41. Gleba powdery and dry at maturity Order Lycoperdales THE ORDERS OF FUNGI 39 40. Hymenium lacking or indistinct 42 42. Glebal chambers at maturity not separating from peridium nor from each other; gleba powdery and dry Order Sclerodermatales 42. Glebal chambers enclosed within peridioles which serve as disseminules Order Nidulariales Class Fungi Imperfecti 43. Conidia produced in globose, cupulate, or hysteroid pycnidia Order Sphaeropsidales (Phomales, Phyllostictales) 43. Conidia not formed in pycnidia 44. Fructification consisting of a plane stromatic layer of closely compacted conidiophores, an acervulus, usually innate Order Melanconiales 44. Fructification consisting of separate conidiophores or loosely compacted conidiophores, forming synnemata or sporodochia Order Moniliales (Hyphomycetes) 43. Conidia lacking Mycelia Sterila LITERATURE CITED BiSBY, G. R., AND G. C. AixswoRTH, "The numbers of fungi," Trans. Brit. Mycol. Soc, 26: 16-19, 1943. ClexMENts, F. E., and C. L. Shear, The geiiera of fungi, iv + 496 pp. H. V. Wilson Co., New York. 1931. Fifth Internatiox.\l Botanical Congress, 1930, "International rules of botanical nomenclature." 39 pp. (Published as supplement to /. Botany, June, 1934.) Fries, Elias, Syste?7ia inycologiciim, Vols. I-III. Ernest Mauritius, Griefs- wald. 1821-1832. Linnaeus, Carl, Species plantarzmi. 1200 pp. L. Salvius, Stockholm. 1753. Martin, G. W., "A key to the families of fungi exclusive of the lichens," Univ. loiva Studies, 27:83-115. University of low^a, Iowa City. 1936. "Outline of the fungi," Univ. Iowa Studies, 28. 64 pp. University of Iowa, Iowa City. 1941. Persoon, C. H., Synopsis methodica fimgonmi. xxx + 706 pp. H. Diet- erich, Gottingen. 1801. Saccardo, p. a., Sylloge fujigorum omniimi hiicusque (fognitorum, Vols. 1-25. 1882-1931. Chapter 4 THE MYXOMYCETES . The Myxomycetes, or slime molds, are fungus-like organisms which, in their vegetative or assimilatory phase, consist of a naked, multinucleate mass of protoplasm called a plasmodium, and in their reproductive phase consist of encased spores. Their relationship to fungi and to animals has long been a much-dis- cussed subject, as is indicated by the name Mycetozoa, which is frequently applied to them. Such early workers as Micheli and Fries placed them among the puffballs, and it is easily understand- able that such well-known species as Lycogala epideiidnim and Fiiligo septica should have been regarded as puffballs. The development of a slime mold is typified by that of F. septica. It is cosmopolitan, and its fruit bodies may be found on logs, around stumps, or on lawns and flowerbeds. They are yel- lowish, tawny, cushion-like structures about 3 to 6 cm in largest diameter and 2 to 3 cm thick. The cortex is friable, foamy, and calcareous. The interior is filled with violaceous, spherical spores with knotted threads (capillitia) interspersed. The spores are usually disseminated bv winds. In moist weather the spore walls open to emit swarm cells (myxamoebae), which ingest bacteria and fungus spores, assimilate them, and grow to become a large, multinucleate, naked mass of protoplasm (plasmodium). The Plasmodium moves in amoeboid fashion to the surface of the sub- stratum and in its entirety becomes a fruit body (aethalium). Each nucleus is invested with a wall during the transformation of a Plasmodium into an aethalium, and the inert materials (left- overs) become the cortex and capillitium. Present-day knowledge of the slime molds began with a series of studies by de Bary covering a period of 10 years, which were assembled in his monograph in 1864. He early observed that the spores of Hemitrichia vesparhim give rise not to germ tubes, as do those of fungi proper, but to amoeboid flagellates. For 40 ACRASIALES 41 this reason he gave slime molds the name Mycetozoa and placed them outside the plant kingdom. Meantime Cienkowski (1863, 1863a) turned his attention to this group, and as an outcome of his studies, together with those of de Bary, thoroughly estab- lished the fact that spores of slime molds germinate by the for- mation of swarm cells, that these swarm cells fuse to initiate the Plasmodium (apparently this term was first employed by Cien- kowski), and that the plasmodium eventually ceases to grow and becomes transformed into the fructification. A series of taxonomic treatises on this group have appeared, beginning with that of Rostafinski (1873), a pupil of de Bary. His studies are the basis of present-day classification. Then fol- lowed the classification of Massee (1892) and the monograph of Lister (1894), which has undergone two revisions by his daugh- ter. Meanwhile a treatise by Macbride (1899) of the North American slime molds appeared and was completely revised in 1934 [Macbride and Martin (1934)]. In the present account the Myxomycetes are regarded as including the three orders, Acrasiales, Labyrinthulales, and Plasmodiophorales, that are out- side the subclass of true slime molds, Myxogastres. This is done arbitrarily and not on the basis of evidence of relationship to the Myxobacteriales, the flagellate Protozoa, or the Myxochytridiales. Acrasiales. The Acrasiales comprise a group of approxi- mately 20 species that occur on dung and on decaying leaves and wood. There is reason to beheve that they are of general oc- currence in soils containing organic matter of any sort. They are characterized by abrupt separation into vegetative and fruit- ing stages. On germination their spores produce naked amoe- boid cells, called myxamoebae. Each cell is uninucleate and, in the presence of available food (bacteria), is capable of giving rise to an indefinite number of cells like itself. Dictyostelhim dis- coideum, as observed by Raper (1940), typifies the developmental structure of this order. He found that each amoeboid cell re- mains a distinct entity and that the cells aggregate, without fusing, to constitute the pseudoplasmodium. That they are all separate may be shown, as Raper demonstrated, by placing a pseudoplasmodium in water. As growth proceeds, the pseudo- plasmodium becomes a cylindrical body that migrates as a unit throughout the substratum or over its surface. Eventually it becomes transformed into a fruiting structure, a sporocarp, con- 42 THE MYXOMYCETES sisting of a basal disk that supports a stalk which in turn is sur- mounted by the spore mass. The construction of the sporocarp is a communal enterprise. How this division of labor among so many distinct entities is directed and controlled remains entirely- unexplained. The sporocarp of D. discoideiim is always of the same pattern. Similarly, whatever the pattern is for each other species, it is always the same. Skupienski (1920) maintained that the amoeboid cells fuse in pairs, a phenomenon that is known to occur among the true slime molds. It seems highly probable that Skupienski is correct as regards fusion among Acrasiales, but this point requires con- firmation. The ability of pseudoplasmodia to maintain their specific iden- tities is strikingly demonstrated by the experiments of Raper and Thom (1941). They crushed and thoroughly mixed the pseudo- plasmodia of Dictyosteliimi discoideiim and D. piirpiireiim, and of D. discoideimi and Folysphojidyliinn piirpureum, and from each pair of the mixture typical sorocarps of each species were eventually organized. If these investigators withheld food (bac- teria), the colonies resulting from a mixture of pseudoplasmodia of the two species of Dictyostelium produced sorocarps in which were combined the characters of each species. The combinations were not hybrids, however, but physical mixtures. The body of the fructification or sorocarp consists of inert material, and the living portion becomes encysted as multinu- cleate, walled spores that accumulate in a globular body at the tip of the mass. The Acrasiales were monographed by Olive (1902) and in- clude three families, the Guttulinaceae, Acrasiaceae, and Dictyo- steliaceae, differing mainly in structure of the sorocarps. The best-known member is the Genus Dictyostelium, investigated by Pinoy (1907), Skupienski (1920), and Raper (1937, 1940). Raper grew Dictyosteliimi discoideum and D. ?mic oroides on a variety of agar media in "pure-mixed culture" with various spe- cies of bacteria, especially Escherichia colt and Serratia mar- cescens. Cohen (1939) grew D. discoideimi in pure culture and in "two-membered" cultures. These species commonly utilize bacteria as food, as was first indicated by Pinoy (1907), and as other slime molds are known to do. They continue to ingest bac- teria so long as bacteria are available and environmental factors are PLASMODIOPHORALES 43 favorable. Raper (1940) found that 20 to 24° C is the optimum temperature and that pH S.S to 7.0 is a favorable reaction for D. discoideum. Decreased relative humidity, increased temperature, and change in light promote fruiting. In summary, the Acrasiales are distinct from the slime molds proper in that the swarm cells lack flagella, are not known to fuse, and hence do not form true plasmodia but form pseudo- plasmodia instead. Labyrinthulales. The Labyrinthulales are an aberrant, little- known group, mostly parasitic on algae of both fresh-water and marine species, Cladophora and Vaucheria being common hosts. They consist of naked, amoeboid cells connected by pseudopodial processes to form chains or nets, long ago described by Zopf as "net plasmodia." Each net plasmodium increases in size by the formation of new cells. Spores arise by rounding up and encyst- ment of the cells. On germination a single, naked, amoeboid cell is liberated from each spore. These essential features were early determined by Cienkowski (1867). Recently Dangeard (1932) described reproduction of another kind, occurring by formation from the net plasmodium of a hol- low sphere of cells aggregated around debris within the host cell. From each cell of the sphere 4 to 8 naked swarm cells escaped by rupture of the wall. This number of swarmers coming from each cell indicates that sexuality and reductional division may be involved in this reproductive process. Attention has been focused on the Labyrinthulales in recent years because of the outbreak of a disease, called "wasting disease," of Zostera inarma. This is a marine seed plant of enormous importance as a source of food for wild ducks, geese, and other water fow4 and for many marine animals. Associated with diseased plants is LabyrintJnila 77jacrocystiSy which is re- garded by some workers as the causal agent of the w^asting dis- ease. The reports by Renn (1936) and Young (1938) will ac- quaint the reader with evidences of its parasitism and with the status of this problem. Plasmodiophorales. The members of this order, containing approximately only a score of species, are all endoparasites of vascular plants. They involve roots and underground stems and cause the formation of excrescences or galls. Upon disintegra- tion of the host tissues the spores are liberated in the soil. The 44 . THE MYXOMYCETES germinating spore then liberates a naked, amoeboid swarmer pro- vided with a pair of unequal flagella, anteriorly attached, as shown by Ledingham (1934), Karling (1942), and others. Wo- ronin (1878) in his classical studies of Plasmodiophora brassicae and Cook and Schwartz (1930) described a single anterior flagel- lum, \\-hich is clearly erroneous. The swarm cells are said to fuse in pairs, settle on the epidermis or root hairs, and effect entrance as naked, amoeboid zygotes. Actual fusion of swarm cells in liv- inor material among Plasmodiophorales has been observed only in Spongospora siibterranea. Once this parasitic relationship has become established, the zygote increases in volume, with accom- panying increase in number of nuclei, to become a naked plas- modium. As the host cells divide, the plasmodium may be cut in two and may appear in each daughter cell. All divisions in the same plasmodium are simultaneous [Cook (1928)]. Finally, just before sporulation, meiosis takes place, and the uninucleate spores are walled off and remain separate or ad- here in groups characteristic of the genus or species. In Plasmodio- phora and Ligniera the spores remain separate in the host cells; in Tetramyxa they cling in tetrads; in Spongospora they remain in a spongy mass; in Sorosphaera they form a hollow sphere; and in Sorodiscus they aggregate into two layers. Flasjiwdiophora brassicae, the cause of club root of cabbage and other cruciferous plants, is the best-known member of the Plasmodiophorales, especially from the studies of Woronin (1878), Maire and Tison (1909, 1911), Lutman (1913), Schwartz (1914), Chupp (1917), Cook (1928), and Cook and Schwartz (1930). Little that is new has been added, however, to the find- ings by Woronin, so accurate were his observations and so pains- taking his attention to details. The swarm cell loses its flagella during penetration, w^hich is accomplished, according to Chupp (1917), by piercing the wall of the root hair. Then the nucleus divides repeatedly, and after 2 or 3 days the plasmodium is of a size to cleave into uninucleate protoplasts. Each protoplast next becomes enclosed in a wall and functions as a gametangium, form- ing 4 to 8 swarmers [Cook and Schwartz (1930)]. These swarmers fuse in pairs, initiating the plasmodium, which increases in size, with repeated simultaneous divisions of its nuclei. Mean- while the invaded cells become hypertrophied. All nuclear di- MYXOGASTRES 45 visions are equational except the penultimate one [Lutman (1913), Cook and Schwartz (1930), and Cook (1933)]. Spongospora siibterranea, the cause of powdery scab of potato tubers and of lesions on the underground portions of tomato stems, is the only other species of this order that is of economic importance. It has been known in Europe for approximately 100 years and was apparently introduced from the Andean home of the potato. The spores of S. subterranea germinate readily, each forming a single uninucleate amoeba. Infection is accomplished at or near the "eyes." Some workers have maintained that infection is ac- complished by separate amoebae, but Kunkel (1915) presented evidence that invasion comes from the action of a plasmodium (zygote). Osborn (1911), on the other hand, has described uni- nucleate amoebae in young potato cells. His studies show the manner of enlargement of plasmodia and the formation of the sponge-like mass of spores. While proof of sexuality is lacking, there is evidence that nuclei fuse and that reductional division occurs just before sporulation. Information concerning Sorosphaera can be gained from the report of Blomfield and Schwartz (1910), concerning Ligniera from the report of Cook (1926), and concerning Sorodiscus from the report of Wernham (1935). Generic differences among the Plasmodiophorales are insuffi- cient and too slight in taxonomic value to incline Palm and Burk (1933) to retain the six usually recognized genera. On the other hand. Cook (1933) in his taxonomic treatment of the group rec- ognizes 6 genera and 14 species. He emphasizes the importance of fusion of swarm cells by their anterior end among Plasmo- diophorales rather than by their posterior end, as occurs in the slime molds proper. Karling (1942) employs 8 genera in his monograph of the order, which includes a complete host index and bibliography. Maire and Tison (1909) stressed the point that the Plasmo- diophorales are a distinct group, an opinion with which most my- cologists are in accord, but whether they should be placed phy- logenetically between the Sporozoa and the Myxogastrales or considered primitive chytrids remains a controversial question. Myxogastres. This subclass comprises the orders Physarales, Stemonitales, Liceales, and Trichiales. It includes about 400 spe- 46 THE MYXOMYCETES cies of true slime molds. As their name implies, they were first placed among the Gastromycetes and, in fact, were so retained by Fries. Their most common habitat is rotten logs or wood and decaying leaves. Many possess unusual architectural beauty and vividly striking colors. The majority of known species grow in temperate regions and are quite cosmopolitan. Some, however, appear to be restricted to the tropics. The shme molds are characterized by having, in their assimila- tory phase, naked, amoeboid, multinucleate plasmodia that are quite mobile and that vary in size from microscopic units to masses several centimeters in diameter. These plasmodia are hyaline and white, yellow, orange, red, violet, blue, green, or brown. The colors are imparted by anthracene pigments, and a change in reaction results in a change of color. The plasmodia occur largely within or beneath decaying vegetation, but at the time of reproduction they migrate to the exposed surface of the substrate or creep up on near-by green herbs or the bases of trees. The migration of the plasmodium never fails to charm the observer. In his Sy sterna Mycologicwn Fries writes, "At one time I deposited the plasmodium of Diachaea in my hat and within the space of an hour it had covered the greater part of it w'lxh its elegant white network. ... I find nothing more won- derful than slime molds in all the world of plants." The fructifications are of several general types, all possessing an outer membranous covering of inert material, the peridium. If the entire plasmodium becomes transformed, as in Fiiligo sep- tica, into a fructification without the delimitation of separate sporangia, the reproductive structure is of the type termed an aethalium. If the plasmodium aggregates at the loci of a few of the larger veins and retains somewhat the netted form of the plas- modium, as in Hemitrichia serpiila, the fructification is termed a plasmodiocarp. If the plasmodium becomes separated into grouped, erect clusters of fructifications of definite form, with remnants of inert material remaining at the base, the fructifica- tions are termed sporangia. Sporangia are of many patterns, some being marvels of delicacy and intricacy. Fruiting may be induced by exhaustion of nutriment [Camp (1937)]. Doubtless other environmental influences stimulate transformation of the plasmodia into fructifications. SPORE GERMINATION 47 Spore germination. De Bary (1864), it has previously been stated, first noted that on germination swarm cells, rather than germ tubes, emerge from the spore membranes. Jahn (1905) ob- FiG. 10. Types of spore germination and initiation of plasmodia among slime molds. (Adapted from Gilbert.) A to F. Ceratiomyxa fructiculosa. Aj uninucleate spore; B, the same spore, which has become four-nucleate; C and D, segmentation into four bodies; E and F, fusion of cells to form Plasmodium. G to M. Physanmi polycephalnm. G, uninucleate spore; H and /, the wall has ruptured, the nucleus has divided, and the swarm cells have begun to emerge; / and K, motile swarm cells; L, fusion of swarm cells; M, plasmodium. served that the membrane may be cracked open in some species, whereas in others a circular, jagged pore is formed. In either case, he believed, rupture resulted from increased osmotic pres- sure. The change of stored glycogen within the spore into os- motically active sugar resulted in increased osmotic pressure. 48 THE MYXOMYCETES Skupienski (1920), on the other hand, believed that enzyme ac- tion did not in any way account for increased osmotic pressure. After observing germination among 56 species Gilbert (1928) expressed the opinion that local enzyme action may soften the wall in species \\'hose membrane opens by a jagged pore, as in Dicty diaethaliinii phnnbeinn. The wedge-shaped cleft charac- teristic of the other type of opening is t\^pified by Fiiligo septica. As in the germination of spores of other organisms, environ- mental factors exert a controlling influence. Nearly all species terminate best in decoctions of the substrata on which they nat- urally occur. Smart (1937, 1938) found that all but four of the 70 species and varieties which he employed could be made to o^erminate in water alone. Some slime molds retain their viability for incredibly long pe- riods. Smith (1929) germinated the spores of 21 species after thev had remained in the laboratory for periods of 5 to 35 years. Some are capable of immediate germination, as are Arcyria de- midata, Dictydhmi cmicellatinn, Dicty diaethalhmi phmibeinn, and Fiiligo septica. . Others, such as Hemitrichia serpida, do not ger- minate until they have aged a year or more. There are two types of germination among Myxogastres, each characteristic of the subclass, Exosporae or Endosporae, of this order to which the species belongs. A few species of Ceratio- myxa comprise the first subclass, and all other species the second. In Ceratiomyxa the spores (protospores) on dehmitation con- tain a single nucleus, but at maturity they become four-nucleate by two equational divisions. Upon germination the entire con- tent emerges as an amoeboid, naked body or as a four-lobed mass in which the nuclei again divide, and the protoplast then sepa- rates into eight uninucleate portions, each a flagellate, pyriform swarm cell. These swarmers fuse in pairs to form the zygote, which increases in volume to become the plasmodium. Just be- fore the delimitation of protospores, reductional division is ac- complished as shown by Jahn (1908) and verified by Gilbert (1935). In the Endosporae, many of which have been studied, the spores on germination form 1 to 4 swarm cells. Gilbert (1928b) studied 18 species, finding that Badhamia lilacina, B. iiiagna, Fhysannn connatimi, Leocarpiis fragilis, and Miicilago spongiosa form 1 to 4 swarm cells and that Physanim compressimi^ P. leu- FEEDING HABITS 49 copiis, P. serpida, and P. virescens form 1 to 2 swarm cells. Each swarm cell is amoeboid on emergence, but soon an anterior flagel- lum develops. The swarmers fuse in pairs by apposition of their posterior ends [Howard (1931)1, and nuclear fusion soon fol- lows. As the Plasmodium increases in size, the fusion nucleus repeatedly divides equationally and simultaneously. Fig. 11. Types of fructification among slime molds. Aethalium, as in Fuligo septic a, the entire plasmodium becoming a sporocarp; plasmodio- carp, as in Heitiitrichia serptda, plasmodium somewhat reticulate; sporangia, as in most species, plasmodium becoming separated into groups of fructi- fications. In Physannn poly cephahnn from 20 to 40 minutes is required for the completion of mitosis [Howard (1932)]. There is lack of accord concerning the exact point at which reduction division occurs. It may take place just before cleavage of the plas- modium into spores, or the spore may be diploid, in which case 3 of the 4 nuclei arising by meiosis within the spore may disinte- grate. Feeding habits. The plasmodia ingest a variety of materials, even those which are utterly useless as food. In nature they 50 THE MYXOMYCETES subsist largely on fungi and bacteria. Lister early noted that Badhamia iitriciilaris can attack living species of Corticium. Skupienski (1920) recorded the fact that Didymhim difforme utilizes the spores of such common molds as Aspergillus and Penicillium, as well as yeasts and bacteria. Gilbert (1928b) sup- plied the swarm cells of twenty species of Myxomycetes with spores of certain Agaricaceae, Polyporaceae, Mucorales, Pyreno- mycetes, Discomvcetes, and Fungi Imperfecti, and found that ali could be used by each of the slime molds, provided that the spores were not too large to be engulfed by the swarmer. He used Arcyria demidata, A. incarnata, Badhamia magna, B. lilacma, Comatrichia typhoides, Dicty diaethalhim plinnhemn, Didymhim. mgripes var. xajithopiis, Enteridiiim splendens, Fidigo septica, Hemitrichia clavata, H. vespariiim, Leo carpus fragilis, Lycogola epidendnim, Fhysanim viride, Reticidaria lycoperdon, Stemoiii- tis jerniginea, S. jiisca, S. splendejis var. flaccida, and Trichia fioriforims. Howard and Currie (1932) grew various agarics and polypores on agar media fortified with decoctions of corn, rolled oats, pota- toes, or Vicia faba and found that 2 1 species of slime molds were parasitic upon the mvcelia of the various Hymenomycetes. By making a series of motion pictures of feeding plasmodia at inten^als of 5 to 10 minutes and then projecting them at the usual rate, Howard was able to show that the plasmodium flows and recedes as do the waves on a beach, and in so doing breaks into fragments the fungal hvphae or hymenomycete sporophores upon which it is feeding. Artificial culture. Several methods have been devised whereby slime molds can be grown and maintained in artificial culture. Many workers have cultivated them on the sporophores of Hymenomycetes. Howard (1931) noted that Fhysanim poly- cephahnn could digest a large pileus of Ajnanita imiscaria within 24 hours. He utilized oat agar as a medium for artificial cultures, placing near the edge of the dish a fragment of plasmodium of F. polycephalum. After the plasmodium migrated from its origi- nal place of lodgment, a fragment was transferred to another dish, and by means of several transfers the plasmodium was essen- tially freed from contaminants. Camp (1936) placed the plas- modial or sclerotial fragments of this same species on a gauze or CAPILLITIAL FORMATION SI filter paper, kept moist by capillarity, in a damp chamber. Pul- verized rolled oats were sprinkled sparingly over the mobile plas- modium. After feeding on the oats, the plasmodium spread to Fig. 12. Stages in growth of plasmodium and transformation into masses of spores in Spongospora subterrajiea within cells of potato tuber. (Adapted from Osbom.) A. Young plasmodium. B. Multinucleate plasmodium at a somewhat later date. C. Aggregation of plasmodium before spore for- mation. D. Mature soral masses of spores. the walls of the culture vessel, where it could be removed and daily started anew. Capillitial formation. The capillitium and sporanglal wall are constituted of inert material deposited by the plasmodium during transformation into the fructification. Capillitial forma- 52 THE MYXOMYCETES tion has been studied by Harper and Dodge (1914) and by Bisby ( 1914) , among others. True capillitium in Fhysarella mirabilis and Stemonitis jiisca [Bisby (1914)] arises during sporangia! cleav- as^e among tubular spaces formed from invaginations. The plasma membrane lining these spaces progressively deposits sub- FiG. 13. Plamiodiopbora brassicae. A. Young plasmodia within root hair. B. Mass of spores that have come from mature plasmodium. C. Stages in germination of spores and escape of myxamoebae. {A and B after Chupp, C after Woronin.) stance that becomes the walls of capillitial threads. In S. fiisca these threads are continuous with the sporangial wall and with the columella. Some genera, such as Enteridium and Lycogala, form pseudocapillitia, which are products of protoplasmic de- generation. In Comatrichia and Lamproderma the capillitium, as in Stemo- nitis, is continuous with the columella. In Hemitrichia and Arcyria the capillitial threads are elaborately provided with spines and spiral thickenings. In Badhamia there is a network of lime-containing tubes; in Phvsarum the lime is aggregated into CLASSIFICATION S3 knots. Other genera, such as Licea and Cribraria, possess no capillitium. Classification. The classifications that have been proposed, including those of Lister (1925), Jahn (1928), and Macbride and Martin (1934), are all highly artificial. Different ordinal names are given by each worker. Color of spores and presence of capillitium and of lime are given great emphasis in ordinal group- ings. Genera apparently closely related are often widely sepa- rated, as must happen when characters whose significance is not yet evaluated are employed in classification. In spite of these limitations identification is not a difficult task, and the group must be regarded as very inviting to the taxonomist. Implications. The many unsolved problems concerning Myxomycetes are clearly stated in a recent review by Martin (1940). These problems involve, among other factors, the ques- tion of whether plasmodia fuse, the sexuality of representative genera (only a few of which have been studied), the uncertainty whether + and — swarmers exist, the nature of the pigments and of color changes in plasmodia, the stimulus of fruiting, mor- phogenic mechanisms, the factors governing endemism, the causes of protoplasmic streaming and of amoeboid movement, and the relationship of slime molds to other organisms. LITERATURE CITED Bary, Anton de, Die Mycetozoen (Schlemipilze) . Em Beitrag zur Kennt- nis der niedersten Orga?jis?7ie72. Leipzig. 1864. BisBY, G. R., "Some observ^ations on the formation of the capillitium and the development of Physarella mirabilis and Stejiionitis fiisca,'' Am. J. Botany, i; 274-288, 1914. Blomfield, J. E., AND E. T. Schwartz, "Some observations on the tumors of Vero?jica chmiaedrys caused by Sorosphaera veronicae,'' Ann. Bot- any, 24: 35-43, 1910. Camp, W. G., "A method of cultivating m)^omycete plasmodia," Bidl. Torrey Bota?j. Club, 55:205-210, 1936. "The fruiting of Physanmi polycephahmi in relation to nutrition," Am. J. Botany, 24: 300-303, 1937. Chupp, Charles, "Studies on clubroot of cruciferous plants," Cornell Agr. Expt. Sta. Bidl, 5re, which mav at marurit\- become trans- formed into a single sporangium, as occurs in the Olpidiaceae. In the S\-nch\-triaceae the thallus fragments become a sorus or cluster of sporangia. Organisms in which the entire thallus is modified into a fructification, as it is in the Olpidiaceae and S\-nch\-triaceae, are spoken of as holocarpic. If. on the other l^d. the thallus is differentiated into sterile and fertile portions, it is eucarpic. Eucarpic thalli with a single reproductive rudi- ment are monocentric; w"ith more than one. polycentric. The Rhizidiaceae possess discoid, -bulbous, or tenuously branched rhizoids bv means of which nutrients are absorbed. Among the aadoch\Triaceae the assimilator\- portion is mycelioid at first but is quite evanescent and is eventually transformed into repro- ductive structures. All the higher Phvcomvcetes, on the other hand, possess richlv branched thalli that course over or through- out the substrata. The parasitic species among them are topically intracellular or else are intercellular, absorption of food in inter- cellular species beinor accomplished by haustoria, as in the Albur oinaceae and the Peronosporaceae. The sporaxgium. Asexual reproduction among most Phy- comvcetes is accomplished bv sporangiospores that are borne endosenouslv w-ithin sporangia. They are formed by cleavage of the contents of the sporangium and may be either motile or non-motile, depending mainly upon the species. Motile spores are commonlv called zoospores or planospores; non-motile spores, aplanospores. In aquatic species the zoospores are emitted and swim away in the water. In terrestrial species, such as those of the Perono- sporaceae and Albueinaceae. the sporangia are detachable and are dispersed in toto, mainly by air currents; whereas in other species, for example, those of the Mucorales. the sporangia burst and the sporangiospores are themselves disseminated. Shape of sporangia is rather generally employed as a generic character in this group. In some genera, such as Leptolegnia, the sporangia are little different from the vegetative hyphae. In Saprolegnia, Achlva, and Dict\-uchus they are broadly clavate; in . Olpidium, Mucor. Thamnidium, and Choanephora, spherical; in Ph\-tophthora, Pxthium, and P\-thiopsis, pyriform. REPETITION AL OR PROLIFER.4TIVE DEVELOPMEST 59 Amons: filamentous species the sporangia are usuallv formed terminallv, a single sporangium constituting the terminus of the hypha. In Albugo. Svncephalis, and PiptocephaUs the sporangia appear as chains. In Blakeslea the sporangia are aggregated over the surface of the head-like tips of the sporangiophores. Fig. 14. Repetitional development among Phycomycetes. A. Repeated formation of sporanaria, each \\-ithin the one previously formed, in Sapro- legnia nwnoica. (After Pringsheim.) B. Sporangia] proliferation to form chains of sporangia in Pytkiimi proliferzcm. (After Butier./ C. Nest-like and chain- 'ike sporangia in Pytbiomorpka gonapodioides. (After Peter- sen.; D. Sporanffium of Peronospori tabacina proliferating to become diminutive sporan^iophore or to form one or more secondar\" sporangLi. £. SporangM renewal in Pkytopktkori palmh-ora from germinating oospore. (After de Bar\-.) F. Proliferation of sporangia in Genaopodyi proliferi. Re PETITION AL OR PROLIFER.\TrVE DE\TLOPMEXT OF SPORAXGL\ AXD SPORES. Sporanoial proliferation is of usual occurrence among certain species of the higher Phycomycetes. It is accom- plished bv seriate formation of sporangia at the apex of the re- productive h\~pha. Proliferation mav be an entirely normal pro- cedure, but in some species it is apparently an abnormality-. By 60 THE PHYCOMYCETES repeated growtn through the base of the old empty sporangium the fertile hvphae may give rise to a chain of sporangia, as occurs in Fythiimi prolijerinn or in Fythiovwrpha gonapodioides. If the axis does not elongate, the successively formed sporangia remain one within the other in a nest-like arrangement. In another type of proliferation, exhibited by Achlya raceviosa and Phytophthora injestans, the new branches arise laterally immediately below the sporangium and near the tip of the fertile hypha, and a sympo- dially arranged series of sporangia is thereby produced. Sporangiospores may also proHferate, giving rise to series of successively smaller spores, sporangia, or sporangiophores. Repe- titional development of this type has been recorded for Achlya racemosa, Fythhmi prolifenmi, P. diacarpinn, Phytophthora phase oH, P. cactorimi, P. mfestaiis, and Dictyiichiis sp. by vari- ous workers and for Peronospora tabacina by Wolf and McLean (1940). Another manifestation* of what appears to be the same phe- nomenon is exhibited by the Saprolegniales and is known as diplanetism. In certain genera of this order two motile or planetic stages are a more or less fixed character. The zoospores are pyriform in the first motile stage and, after encystment, emerge a second time and are reniform. Sexual spores. Diversity in the sexual process is as great among Phycomycetes as in the asexual processes. The thallus arising from a single spore may produce both kinds of gametes, that is, may be homothallic. Instead thalli from two spores, each producing only one kind of gamete, may be required for zygote formation; that is, the species is heterothallic. The gametangia are differentiated in most genera, but in a few instances they are undifferentiated cells. Two morphologically similar gametes may fuse (isogamy) or the gametes may be quite dissimilar (heterogamy). This feature is the basis for separating the Phyco- mycetes into the subclasses Zygomycetes (isogamous) and Oomycetes (heterogamous). Some species regarded as Oomy- cetes, however, are isogamous, as are Synchytrmm endobioti- cum and Olpidhnn viciae, and similarly some species regarded as Zygomycetes, such as Zy gorhynchiis heterogavms, have unlike gametes. Both gametes may be flagellated, as in Alloviyces ar- biiscida and A. javaniciis; the male gamete only may be flagel- CLASSIFICATION 61 lated, as in Monoblepharis; or the gametes may be brought into contact by passage of the male gamete through a fertihzation tube into the oogonium. In Polyphagus both gametes pass into a swelling in the fertilization tube, and this swelling becomes transformed into the zygote membrane. In Rhizopiis nigricans the two gametangia become transformed into the zygote wall. In the Saprolegniales and Peronosporales the antheridial con- tents flow into the oogonium, and the oogonial wall remains as a cyst for the developing oospores. Both gametes may be uninucleate, as they are in Synchytrium and Monoblepharis. In other species one gamete is uninucleate and the other multinucleate, and in still others, as in the AIu- corales and some species of Albugo, both are multinucleate. Organs of locomotion of zoospores. Among aquatic Phyco- mvcetes motility is induced by organs called cilia. The studies of Couch (1941) show^ that there are two distinct structural types of ciha: the "whip-lash" type and the "tinsel" type. The whip- lash type consists of a long, quite rigid, basal portion, the handle, and a short, thin, upper portion, the lash. The tinsel type con- sists of a central axis, from w^hich extend short lateral hairs. Among true chytrids the ^\'hip-lash cilium is situated posteriorly. The zoospore may rotate on its own axis, as seen by dark-field il- lumination, and the cilium will then appear alternately as a single and a double image. If the image is single, the cilium is undulat- ing in a plane vertical to the observer; if it is double, in a plane horizontal to the observer. In Rhizidioinyces apophysatiis there is a single anterior tinsel cilium. In species of Olpidiopsis, Lagenidium, Saprolegnia, and Pythium, wdth biciliate zoospores, the anterior cilium is of the tinsel type and the posterior cilium of the whip-lash type. Classification. The most recent comprehensive monograph of aquatic Phycomycetes is that of Sparrow (1943). In it are descriptions of 475 species and 10 varieties, belonging in 112 genera. It does not include the Peronosporales, as described in this book, nor the Alucorales and Entomophthorales, all species of which are terrestrial. Sparrow's excellent treatise will serve for years as a taxonomic handbook for students of aquatic fungi. The number of flagella and the place of their attachment are basic in the separation of orders in his keys. 62 THE PHYCOMYCETES In the present account the Phycomycetes are divided into 11 orders: Chytridiales, Lagenidiales, Blastocladiales, Monoblephari- dales, Leptomitales, Saprolegniales, Pythiales, Albuginales, Per- onosporalesj Mucorales, and Entomophthorales. Some workers do not recognize all these as of ordinal rank, although no one questions that all are Phycomycetes. Some students would include in addition the Endogonales and Eccrinales, but the classification of both of these orders in the Phycomycetes remains of doubtful justification. Origin of the Phycomycetes. There are three points of view among botanists regarding the origin of the Phycomycetes. The first of these, which is the oldest, is that they are degenerate algae and that consequently in classifications they should be in- cluded among the Algae. Some of the workers who hold to this concept treat the Phycomycetes and Algae as taxonomically dis- tinct, largely as a matter of convenience. This viewpoint was elaborated by Professor Charles E. Bessey. The second point of view is that the Algae and Fungi have evolved as two parallel series, a phylogenetic approach advocated by Professor G. F. Atkinson. For the student who is interested in phylogeny the evidence and arguments for and against both of these opposed viewpoints are succinctly presented in a paper by Atkinson (1909). The third viewpoint is that the Phycomycetes are derived from the Protozoa and should be placed in a phylum distinct from the Algae. Arguments for the validity of any of these points of view rest seemingly upon somewhat the same sort of founda- tion as do those for political or religious beHefs. LITERATURE CITED Atkinson, G. F., "Some problems in the evolution of the lower fungi," A?i?j. My col, 1:^^\-An, 1909. Couch, J. N., "The structure and action of the cilia in some aquatic Phy- comycetes," Am. J. Botany, 25:704-713, 1941. Sparrow, F. K., Aquatic Phycomycetes, exclusive of the Saprolegniaceae and Pythium. xx + 785 pp. The University of Michigan Press. 1943. Wolf, F. A., and Ruth M. McLean. "Sporangial proliferation in Perono- spora tabacina,'' Phytopathology, 30: 264-268, 1940. CHYTRIDIALES 63 CHYTRIDIALES The Chytridiales, commonly called chytrids, include parasitic and saprophytic fungi that are mainly aquatic. They occur on ?c?^>^^^'^^^^ •-i...: ;•.■•,'• •-'•.•,■■•••'. •; Ji"'»'-.>- ^i^Jiv.*--*' ■ Fig. 15. Stages in the development of Olpidiopsis. A. Biciliate zoospores. B. Encysted stage that has settled upon a filament of Aphanomyces. C. Migration of protoplast from cyst into filament of Aphanomyces. D. Swollen tip of host hypha containing several zoosporangia, two of which have formed exit tubes for escape of zoospores. E. Mature oospore of O. luxiirians with two empty antheridia attached. (After Barrett.) fresh water algae, other aquatic fungi, microscopic animals, and decaying tissues of seed plants. Some few marine species have been described. A few are important pathogens on seed plants. The feature of primary importance in the order is the produc- 64 THE PHYCOMYCETES tion within sporangia of anteriorly uniflagellate zoospores. Un- fortunately this feature is not easy to determine. Sparrow (1943) divides the chytrids into two groups, Inoper- culatae and Operculatae. The sporangia of the Operculatae open by means of a lid or operculum, while those of the Ino- perculatae lack this device to free the uniflagellate zoospores. The Inoperculatae include the Olpidiaceae, Achlvogetonaceae, Svnchvtriaceae, Phlyctidiaceae, Rhizidiaceae, Cladochvtriaceae, and Physodermataceae; the Operculatae include the Chytri- diaceae and Megachytriaceae. The thallus either (1) is naked at first (plasmodial), later be- coming walled, and is entirely transformed into a sporangium or a cluster (sorus) of sporangia, or else (2) is walled from the first and differentiated into a vegetative and a fertile portion. The vegetative portion is a delicate, branched structure of rhizoidal appearance and has been appropriately designated a rhizomycelium. Among older systems of chytrid classification and on the basis of these two types of thaUi the Chytridiales are divided into the suborders Myxochytridiales and Mycochytri- diales. In the Myxochytridiales are the Olpidiaceae, Synchytria- ceae, and (doubtfully) Woroninaceae; in the Alycochytridiales, the Rhizidiaceae, Cladochytriaceae, and Hyphochytriaceae. Amoncr the older taxonomic treatises are those of Schroeter (1892) and von Minden (1911). Although these r^vo works are basic, numerous species have been described subsequently, and these publications, especially the ones by Scherffel (1925) and Sparrow (1935, 1943), and the numerous reports by Couch, should be consulted in connection with the taxonomy of chy- trids. Occurrence and cultivation. A large proportion of the re- ports on chytrids have been concerned with the description of new species. Although many occur on algae, flowering plants, and other fungi, some are free-living in the soil. Recent evidence [Whiff en (1941)] from growth in culture on cellulose indicates that they may function in cellulose decomposition in the soil. Inability to isolate chytrids in pure culture has been a material obstacle in the acquisition of knowledge of their activities. For a time Sparrow (1931) cultivated Cladochytrhnn noivako^Li'skiu mixed with bacteria, on bacto-corn-meal agar. Butler and Humphries (1932) grew Catenaria migidlhdae, parasitic on the OCCURRENCE AND CULTIVATION 65 CQ > d o Oh o 4-1 p Q-, O o < '3 w ^— SI p. » CJ Ui 5^ rt ^ r-| 4-1 '5d c C3 o O 4-1 C/5 • flj c ^ si c E c T3 M-i r-; 'a 0 g > ^ C5 ^ ^" r- !<1 5 ^ "cS o 4-1 o S to C/5 ■T3 55 -S 1j rz ^ 7 'Eh •^ <^ -Q U( ^ 4> U r^ ^ ^ 5u 4-1 to >. on o CU o "rt u TS 5 "Hh , , - ^^ 4-1 V5 • 1-H C SI - 1— ( rt bii C u >>-T3 r- 3 4—* be C C rt • O u • ^^ rN c «-(-l C^^ c t/5 k-' o ^ o 4-» ^ 4-1 so r— 1 It 2 d « u Lh ::: < Q ^ 66 THE FHYCOMYCETES o/ o ova of liver fluke of sheep, on boiled fluke eggs and on 0.25/ agar fortified with fluke-ova extract. Karling (1938) grew Cate- naria sphaerocarpa on cooked root tips of corn and onion. In pure culture on 3% plain agar Couch (1939) isolated Rhizidio- myces apophysatiis, Rhizophidhim carpopbihmi, and R. midti- porinn and cultivated them through several transfers. Cox (1939), using the same technique as Couch, isolated Clavochy- tridiw7i stomophihnn. Whiff en (1941) grew Neph'ochytridhnn auranthnn on boiled leaves of corn and on filter paper. The fact that these investigators have succeeded to a certain degree in cul- tivatingr some of the chvtrids has contributed materially to under- standing their activities and stimulatinor interest in them. Reproduction. In some species two types of sporangia are developed: thin-walled, or temporary, sporangia and thick- walled, or resting, sporangia. The latter type is capable of hiber- nating and probably arises after fusion of gametes. The sporan- giospores, except in the Woroninaceae, are uniflagellate. Cyto- logical details are largely wanting and, among the few species that have been examined, are quite contradictory. Nuclei have been described as arising by amitosis, nuclear budding, and frag- mentation. Cell-plate formation has been described as it occurs during cell division (delimitation of spores). Others have con- cluded that cell division arises either by progressive cleavage of the sporangium or by fragmentation of the protoplast. Mei- osis has been described in connection with only a single species. Amoncr the cytological studies dealing with reproduction are those of Curtis (1920) on Synchytrhim endobioticimi, Kusano (1930) on Synchytrhim fidgens, Karling (1937) on Cladochy- trhim replicatimi, and AIcLarty (1941) on Olpidiopsis achlyae. Olpidiaceae. The Olpidiaceae include approximately 50 spe- cies, of which Olpidiimi brassicae, parasitic on the roots of vari- ous seedlings, including cabbage and tobacco, is typical of the family. Its uniciliate swarm spores settle upon the host, creep over its surface in amoeboid fashion, come to rest, and produce a thin wall. This wall is soon pierced by a narrow pore, the host wall is also penetrated, and the spore content escapes. Then the naked protoplast enlarges, and finally a wall is formed around the mature thallus. At this point the entire thallus becomes a sporangium; that is, it is holocarpic. During this process the content of the thallus cleaves into a group of zoospores that SYNCHYTRIACEAE a escape to the exterior through an exit tube. According to Ku- sano (1912), motile biflagellate zygotes arise in O. viciae by fusion in pairs of zoospores (gametes). The zygotes soon come to rest and produce a wall, and their contents escape into the host to become thick-walled, resting sporangia. Presumably the first divisions of the zygote nuclei are reductional. Fig. 17. Olpidium brassicae from roots of cabbage seedlings. A. Sporangia. B. Zoospores. C and D. Mature resting spores. {A and B after Woronin, C and D after Bensaude.) SYNCHYTRIACEAE. Approximately 75 species comprise the Synchytriaceae. Nearly all are parasitic on seed plants, causing excrescences. Two species, Synchytrhnn vaccmiiy on the leaves and fruits of cranberry, and S. endobioticiim, on potato tubers, are of especial interest. The latter causes excrescences to form, whence the name potato wart. These excrescences vary from small growths the size of a pea to enlargements exceeding the size of the tuber from which they arise. The disease was first discovered in upper Hungary and is now known to occur throughout Europe and Great Britain; it appeared in the United States in 1918. The causal organism was given the name Chrysophlyctis endobiotica by Schilberszky (1896). 68 THE PHYCOMYCETES In section of diseased tissues it may be noted that the outer host cells are occupied by the pathogen in the vegetative phase. It is an unwalled protoplast (plasmodium) that is able to pene- trate host-cell walls, meanwhile increasing in volume. This protoplast then forms a wall about itself and cleaves into a cluster (sorus) of sporangia. These sporangia are of two kinds: thin- FiG. 18. A to C. Stages in liberation of zoospores by Macrochytrmm bo- try dioides. (After von Mindcn.) walled ones that can grerminate at once, and thick-walled ones, called resting sporangia, that can germinate only after a pe- riod of dormancy. Under favorable conditions each kind of sporangium organizes \\'ithin itself numerous uniciliate swarm spores that escape into the soil. Swarm spores have an actively amoeboid movement and behave either as s^^'arm spores or as gametes. These single or mated swarm spores are able to initi- ate new infections bv penetrating the "eves" of the young tubers. Studies by Percival (1910) and Curtis (1921) contain detailed accounts of the structure and developmental history of Synchy- trhim evdobioticinn. RHIZIDIACEAE 69 WoROxixACEAE. This family is represented by 15 species of endoparasites of Saproleginales and Pvthiales. They differ from all other chytrids in that their zoospores are biflagellate. Olpidi- opsis and Rozella commonly cause the hyphae of Saprolegnia, Achlya, and Allomyces to be swollen. Asexual spores, formed in ellipsoidal sporangia, are emitted through exit tubes. Thick- walled, spiny oospores arise by migration of multinucleate proto- plasts from small antheridia into multinucleate oogonia formed on closely juxtaposed thalli. Sexuality in Olpidiopsis saprolegniae was studied by Barrett (1912) and Diehl (1935), in O. hixiir'nvis by Barrett (1912), and in O. achlyae by iMcLarty (1941). The germination of the oospores has not been observed. Sparrow (1943) places Olpidiopsis in the Lagenidiales, Rozella in the Olpidiaceae, and Woronina in the Plasmodiophorales. This fact shows that the Woroninaceae, as formerly understood, are not chytrids and are not a group of similar forms. In fact, in a recent study, Karling (1942) monographed a heterogeneous group of 80 biflagellate species, which he divided more or less arbitrarily into five families: Woroninaceae, Ectrogellaceae, Ol- pidiopsidaceae, Sirolpidiaceae, and Lagenidiaceae. The fact that these species possess a pair of flagella, whereas all chytrids are uniflagellate, constitutes an adequate basis for regarding them as non-chytrids. He therefore regards them as a distinct group of Phycomycetes and does not place all of them in a single order. Rhizidiaceae. The Rhizidiaceae constitute a group of ap- proximately 100 species, mostly ectoparasites. They possess globular or elongated plant bodies attached by rhizoidal branches. They may be found on various algae, both marine and fresh- water species, and upon aquatic fungi and insects. The best- known species occur on Spirogyra, Oedogonium, and various des- mids and diatoms. Rhizophidhim pollinis-pini is common on pollen grains floating in water. The swarm cells are uniflagellate and may function either as asexual spores or as gametes. Couch's (1935) account of sexu- ality in R. ovatinn states that the male gamete settles on a fila- ment of Stigeoclonium and attaches itself by a delicate rhizoid. Soon thereafter a female s^amete becomes attached to the male, both increase in volume, the protoplasmic content of the male cell passes over to the female cell, and the two nuclei unite. The zygote formed is capable of germination within a few days. 10 THE PHYCOMYCETES In Polyphagiis euglenae, frequent on Euglena that forms a green film on puddles in pigsties and corrals, a conjugation tube is formed between the uninucleate gametangia. A swelling ap- FiG. 19. Physoder77ia zeae-maydis, causing brown spot on com. A. Mature resting sporangium, surface view, with circumscissile lid from which zoo- spores escape, as in B. C. Amoeboid zoospores provided with a single flagellum. D. Rhizomycelium within epidermis of com. E. Segmentation of rhizomycelium to form thick-walled resting sporangia. pears on the conjugation tube, into which the protoplasts mi- grate. A spiny, thick-walled zygote, which remains dormant for a few months, results. On o-ermination a tube is formed; into it the two nuclei misstate and fuse; nuclear diyision follows; and many swarm cells are set free to repeat the developmental cycle. CLADOCHYTRIACEAE 11 CLADOCHYTRIACEAE. This Small family contains species para- sitic on algae, aquatic seed plants, and such economic plants as corn, beets, and alfalfa. It is characterized by the possession of Fig. 20. Synchytriiim endobioticiim, causing potato wart. A. Young uni- nucleate thallus with characteristic clear zone near periphery. B. The thallus has segmented, each segment being multinucleate and each becom- ing a sporangium. C. Sorus of mature sporangia, each of which has rounded up. D. A pair of zoospores in preparation for fusion. E. Zygote that has not yet settled down. F. Zygotes lodged on surface of pcKato in preparation for penetration. G. Early stage in penetration. a rhizomycelium, which is typically limited to a single host cell. In Physoderma zeae-maydis, causing brown-spot disease of corn and teosinte, the rhizomvcehum becomes segmented and trans- 12 THE PHYCOMYCETES formed into resting sporangia. Tisdale (1919) noted that the resting sporangia hibernate within leaves and stalks and that each emits 20 to 30 swarm cells through a circumscissile pore. Ac- cording to Sparrow (1934), these swarmers produce ecto- sporangia (temporary sporangia), which are anchored to the host; from them come what may be presumed to be true gametes. These gametes fuse in pairs, the zygote infects the corn, and resting sporangia eventually are again formed. Urophlyctis alfalfae induces the formation of galls near the eround level on alfalfa and burr clover. The thallus consists of a series of top-shaped, thick-walled cells, each provided with a crown of haustoria. Each cell is a resting sporangiuni that germi- nates when conditions are favorable. The zoospores escape through a papilla; each is provided with two flagella, one about 5 i-i long and the other about 10 times as long. These zoospores are presumed to conjugate before infections of suitable host tis- sues. The morphology and pathogenicity of this organism were carefully studied by" Wilson (1920) and Jones and Dreschler (1920).' Since so few Cladochytriaceae have been studied in- tensively, the development and sexuality of its members are not well understood. Hyphochytriaceae. The Hyphochytriaceae include a few species of doubtful relationships. The rhizomycelium is coarse, and the apical portion becomes the zoosporangium. Macrochy- trhim botrydioides, first found growing on decaying apple, typi- fies the family. When its sporangia are mature, each opens with a Hd, quite as in the resting sporangia of Physoderma and Cla- dochytrium, and the contents escape in a vesicle or are freed directly. Resting sporangia, however, are unknown in AL botry- dioides. Alacrochytrium has somewhat the appearance of the Rhizi- diaceae and the Leptomitales and may well be a link between the Chytridiales and Leptomitales. LITERATURE CITED Barrett, J. T., "Development and sexuality of some species of Olpidiopsis (Cornu) Fischer," Ann. Botany, 26: 209-238, 1912. Butler, J. B., and A. Humphries, "On the cultivation in artificial media of Catenaria angiiilhdae, a Chytridiacean parasite of the ova of the liver fluke, Fasciola hepatica;' ScL Proc. Roy, Dublin Soc, 20: 301, 1932. LITERATURE CITED 75 Couch, J. N., "New or little-known Chytridiales," MycoL, 27: 160-175, 1935. "Technic for collection, isolation, and culture of Chytrids," /. Elisba Mitchell Sci. Soc, 55:208-214, 1939. Cox, H. T., "A new genus of Rhizidiaceae," /. Elisba Mitchell Sci. Soc, 55:389-397, 1939. Curtis, K. M., "The life history and cytology of Synchytriwn endobioti- cimi (Schilb.) Perc, the cause of wart disease of potato," Phil. Trans. Roy. Soc. London, B, 270:409^79, 1921. DiEHL, H., "Beitrage zur Biologic von Olpidiopsis saprolegniae Barrett," Zentr. Bakt. Parasitenk., 92: 119-1¥), 1935. Jones, F. R., and C. Dreschler, "Crown wart of alfalfa caused by Uro~ pblyctis alfalfae;' J. Agr. Research, 20: 295-325, 1920. Karling, J. S., "The cytology of the Chytridiales, with special reference to Cladochytriinn replicatimz,'" Mein. Torrey Botan. Club, 19: 5-92, 1937. "A further study of Catenaria," Ain. J. Botany, 25:328-335, 1938. Simple holocarpic biflagellate Pbycoinycetes. 123 pp. Published by the author. New York. 1942. KusANO, S., "On the life history and cytolog}^ of a new Olpidium, with special reference to the copulation of motile isogametes," /. Coll. Agr. Univ. Tokyo, 4: 141-199, 1912. "Cytology of Synchytriinn fidgens Schroet.," /. Coll. Agr. Univ. Tokyo, 70:347-388, 1930. AIcLarty, D. a., "Studies in the Woroninaceae. II. The cytology of Olpi- diopsis achlyae, sp. nov.," Bidl. Torrey Botan. Club, 68: 75-99, 1941. MiNDEN, M. VON, "Chytridineae," in Kryptogamenflora der Mark Branden- burg, 5:209-422, 1911. Percival, J., "Potato-wart disease: the life history and cytology of Syn- chytriinn ejidobioticwn (Schilb.) Perc," Zentr. Bakt. Parasitenk., II Abt., 2S:440-A47, 1910. ScHERFFEL, A., "Zur Scxualitat der Chytrideen," Arch. Protistenk., 55: 1-58, 1925. ScHiLBERSZKY, K., "Ein neuer Schorfparasit der Kartoffelknollen," Ber. dent, botaji. Ges., 14: 36-37, 1896. ScHROETER , J., "Chytridineae." In Engler and Prantl, Die natiirlichen Pflanze7ifa77iilien, Vol. I, pp. 63-92. 1892. Sparrow, F. K., "Two new chytridiaceous fungi from Cold Spring Harbor," A?fi. J. Botany, 18:615-623, 1931. "The occurrence of true sporangia in the Phvsoderma disease of corn," Science, n.s., 79: 563-564, 1934. "Recent contributions to our knowledge of the aquatic Phycomycetes," Biol. Rev., 10: 150-186, 1935. Aquatic Phycomycetes exclusive of the Saprolegniaceae and Pytbiimt. XX -|- 785 pp. The University of Michigan Press. 1943. TiSDALE, W. H., "Physoderma disease of corn," /. Agr. Research, 16: 137- 154, 1919. 14 THE FHYCOMYCETES Whiffex, Alma J., "A new species of Nephrochytrium, Nephrochytrmm aiiranthmi,'' Am. J. Botany, 2.?; 41-44, 1941. "Cellulose decomposition by the saprophytic chytrids," /. Elisha Mitchell ScL Soc, 57:321-329, 1941a. Wilson, O. T., "Crown gall of alfalfa," Botaji. Gaz., 70:51-68, 1920. Doubtful Chytrids The most interesting ors^anism amoncr those whose relation- ship with chytrids is doubtful is Rhodochytrhnn spilanthidis. This organism is abundantly prevalent every season in North Carolina as a parasite on the leaves, stems, and flowers of rag- weed, Ambrosia artemisiijoUa. It forms bright-red pustules, the color being imparted by the presence of haematochrome. In gross appearance it resembles the members of the Genus Ento- phlyctis among the Rhizidiaceae. The zoospores, however, are biflagellate and contain starch grains [Griggs (1912)]. The pos- session of starch lars^ely influenced Grisras to relate it to the Protococcoideae (Algae). Its ability to transform absorbed sugars into starch does not appear to present an unsurmountable obstacle, however, to regarding this organism as a fungus. Be- cause of its biflagellate zoospores it is not a chytrid. LITERATURE CITED Griggs, R. P., "The development and cytology of Rhodochytrium," Botan. Gaz., 53: 127-172, 1912. LAGENIDIALES This group of fungi ^\•as previously known to mycologists as the Ancylistales. It has long been recognized, however, that the type genus, Ancylistes, which includes three species, differs rather widely from other members of the order. Ancylistes closteriiy the most thoroughly studied form, is an intracellular parasite of Closterium. Zoospore formation has never been observed WTthin the numerous hyphae which project from infected host cells. It has recently been found [Berdan (1938)1, however, that the extramatrical hyphae of AncyHstes function as conidiophores and prodlice conidia, \\hich are forcibly discharged. This fact has necessitated the removal of Ancylistes to the Order Ento- mophthorales. LAGENIDIALES IS With the removal of the type genus there is left a more uni- fied group of 3 genera, Lagenidium, Myzocytium, and Achlyoge- ton, all of which were originally described by Schenk (1857, 1858, 1859). Lagenidium is the largest genus, having about 15 species [Cook (1936)]; Achlyogeton is monotypic. The group Fig. 21. A. Portion of thallus of Lagenidiimt rabeiiborstii, showing swarm spores in vesicle, an empty sporangium, and two cells, an antheridium and oogonium. B. Lagenidhnn mnericaninn. (After Atkinson.) has been monographed by Schroter (1893) and von Minden (1915), and the Japanese forms have recently been studied by Tokunaga (1934). The species for the most part are obligate parasites of desmids, diatoms, and filamentous green algae. A single representative, hageiiidhnn giganteinn, has been grown in pure culture [Couch (1935)]. The thallus throughout the order is not extensive, being usually confined to a single host cell. A young thallus generally takes the form of a unicellular cylindrical tube, which later becomes di- 16 THE PHYCOMYCETES vided bv septa into a number of cells. The thallus is unbranched in Achlvos^eton and Myzocvtium, whereas in Las^enidium it is more or less profusely branched. Each cell of the thallus eventu- ally becomes transformed into a sporangium, an oogonium, or an antheridium. In asexual reproduction an exit tube from the sporangium penetrates the cell ^^•all of the host, and eventually the laterally biciliate zoospores are formed. In Lagenidium and Myzocytium a vesicle may or may not be present; in Achlyoe^e- ton the zoospores are fully delimited within the sporangium but encyst at its mouth. Sexual reproduction is unkno^^■n in Achlyogeton. In the re- maininor genera, the plant body is homothallic, adjacent cells functioning as antheridia and oogonia. The antheridium is usually cylindrical, whereas the oogonium is spherical in shape, but the o-ametanoria are not so well differentiated as in the higher Oomycetes. The contents of the antheridium are dischargred into the oogonium through a conjugation tube, and the oogonial contents become transformed into thick-walled oospores. Oospores may occasionally be formed parthenogenetically. The conjucration tube is persistent, remaining attached to the wall of the oospore. Germination of the oospore occurs by the forma- tion either of a germ tube or of zoospores. Sexual reproduction has been studied cytologically in only a single species, Myzo- cythmi vermicohim, by Dangeard (1906), and further work is necessary to clarify all the details. Probably also to be considered as belonging to this order is Lagena radicicola [Vanterpool and Ledingham (1930)], a para- site of cereal roots, reported from Canada. The taxonomic account of Sparrow (1943) is most useful as a guide in classification of this order. The possession through- out the order of an oomycetous type of sexual reproduction, together with simpUcity in thallus structure, suggests that the order is intermediate between the chytrids and the higj^her fila- mentous oomycetes, such as the Saprolegniales [Scherffel (1925), Cook (1936)]. » LITERATURE CITED Berdax, H., "Revision of the genus Ancylistes," MycoL, SO: 396-415, 1938. Cook, W. R. I., "The genus Lagenidium Schenk, with special reference to L. Rabenhorstii Zopf and L. entophytinn Zopf, Arch. Protistenk., 86: 58-59, 1936. BLASTOCLADIALES 77 Couch, J. N., "A new saprophytic species of Lagcnidium, with notes on other forms," Alycol., 21: 376-387, 1935. Dangeard, p. a., "Recherches sur le developpenient du perithecc chez les Ascomycetes. I. Les ancetres des champignons superieurs," Botciniste, 5>: 207-226, 1906. MiNDEN, M. VON, "Ancylistineae," in Kryptogavienfiora der Mark Branden- burg, 5:423-461, 1915. ScHENK, A., "Algologische Alittheilungen," Verband. Pbys.-med. Ges. Wiirzbiirg, 9: 12, 1857. Uber das Vorkovmien Kontraktiler Zellen ivi Fftanzenreiche. 20 pp. Wiirzburg. 1858. j "Achlyogeton, eine neue Gattung der Mycophyceae," Botan. Ztg., 11: 398^00, 1859. ScHERFFEL, A., "Endophytischc Phycomyceten-parasiten der Bacillariaceen und einige neue iMonadinen. Ein Beitrag zur Phylogenie der Oomyce- ten," Arch. Frotistenk., 52: 1-141, 1925. ScHROTER, J., "Ancylistineae." In Engler and Prantl, Die natiirlichen PflanzenfaiJiilien, I. Teil, Abteil. 7:8^92, 1893. Sparrow, F. K., Aquatic Fhycoviycetes exclusive of the Saprolegniaceae and Fythium. xx + 785 pp. The University of Michigan Press. 1943. ToKuxAGA, Y., "Notes on the Lagendiaceae in Japan," Trans. Sapporo Nat. Hist. Soc, 75:227-232, 1934. Vanterpool, T. C, and G. A. Ledingham, "Studies on 'Browning' root rot of cereals. I. The association of Lagena radicicola, n.g., n. sp., with root injur\^ of wheat," Can. J. Research, 2: 171-194, 1930. BLASTOCLADIALES The Order Blastocladiales includes about 15 species belonging to 4 orenera. All are filamentous aquatic fungi with a more or less well-developed m\xelium. In this group the cell walls do not stain blue w^ith zinc chloroiodide, an indication of the absence of cellulose. Asexual reproduction occurs by means of thin- walled zoosporangia and zoospores, which are characteristically uniciliate, as they are in the Monoblepharidales and certain of the chvtrids. All representatives of the order produce, in addition to the thin-walled sporangia, thick-walled resistant sporangia of a type not known elsewhere among the fungi. From these persistent structures with pitted walls there are produced after a dormant period zoospores similar to those formed in the thin-walled sporangia. The Genus Blastocladia contains about seven species, of which the best knowil is B. pr'mgsheimii. Species of Blastocladia occur 18 THE PHYCOMYCETES saprophytically on submerged plant materials, fruits of rose, Crataegus, and tomato being especially preferred. Methods of collection of these fungi and a taxonomic account of the genus are given by Kanouse (1925, 1927). The thallus of Blastocladia consists of a rhizoidal system within the substratum, from which arises a main trunk or axis that branches repeatedly. At the ends of the branches are borne the thin-walled sporangia which pro- duce zoospores. The resistant sporangia are also produced apically. Search for sexual reproduction in connection with the s^ermination of the resistant sporangia has produced only nes^ative results. The resistant sporangia of B. pringsheimii have recently been germinated bv Blackwell (1940). She states that after a rest period of several months they germinate, producing zoospores which develop into asexual plants, just as do zoospores from ordinary thin-walled sporangia. Thus sexuality is not known in the Genus Blastocladia. The Genus AUomyces, recently monographed by Emerson (1941), contains five species, all apparently of rather wide distri- bution in soil. This extensive distribution in soil throughout the world is stressed by Wolf (1939, 1941) and Emerson (1941), but the function therein of these species is unknown, and no one appears to have attempted to explain their wide dissemina- tion. The structure of the thallus of AUomyces is quite similar to that of Blastocladia. From the basal portion or trunk, attached by rhizoids, arise numerous slender branches, which are separated into segments by pseudosepta. On the branches are borne thin- \\'alled zoosporangia and resistant sporangia similar to those of Blastocladia. Interest attaches to two species of the genus, A. arbiisciila [But- ler (1911)] and A. javamciis [Kniep (1929, 1930)], by reason of the nature of their sexual reproduction and life cycle. In both of these species there is a distinct morphological alternation of sexual and asexual phases [Kniep (1930), Hatch (1935)]. On germination of the resistant sporangia, the zoospores develop into thalli bearing paired male and female gametangia. Both male and female gametes are motile, the female being considerably the larger and unpigmented, A\hereas the smaller gametangium is orano-e in color. This pigmentation has been shown to be due to the presence of y-carotene [Emerson and Fox (1940)]. The BLASTOCLADIALES 79 Fig. 22. Blastocladia pringshemiii. sketch of an entire plant. A. Resistant sporangium. B. Habit (Adapted from Blackwell.) 80 THE PHYCOMYCETES anisos^ametes (unequal in size) are liberated and fuse in the water to form a motile, biciliate zygote. The zygote soon comes to rest and develops into a thallus bearing sporangia. On germination these sporangia produce motile spores that develop, in turn, into Fig. 23. Life cycle of Allomyces arbiiscula. A. Germinating resistant sporangium with outer wall split. B. Zoospores emerging from germinat- ing resistant sporangium. C. Germination of one of these zoospores. D. Young plant of gamete-producing phase. E. Hypha bearing male and female e^ametangia. F. Emergence of male and female gametes. G. Copu- lation of gametes. H. Motile zygote. /. Germination of zygote. /. Young plant of sporangium-producing phase. K. Mature hypha bearing both thin-walled and thick-walled zoosporangia. L. Emergence of zoospores from zoosporangium, M. Germinating zoospores. R. Resistant sporan- gium. Z. Thin-walled zoosporangium. (Courtesy of Ralph Emerson.) thalli, each of which bears male and female gametangia, thus con- tinuing the alternation. Some \\orkers regard this sequence of sporogenic and gametogenic phases as an "alternation of sporo- phyte and gametophyte generations," w^hereas others interpret BLAST OCLADl ALES 81 the phenomerxon as sexual and asexual phases of a single gener- ation. In A. cy St 0 genus the resistant sporangium cracks open on ger- mination, and the content becomes a group of encysted cells at the point of discharge [AlcCranie (1942)]. After a period semi- amoeboid srametes, each with a sins^le flafjellum, emerg^e from these cysts. They conjugate in pairs, forming biflagellate, motile zygotes of a size like that of the uniflagellate zoospores from the thin-\valled sporangia. Conjugation in this species is therefore isos^amous. Presumably, the life cycle of A. vwnilifoiims is similar to that of A. cystogemis. There is no alternation of sexual and asexual phases as in ^. javaniciis or A. arbiisciila; instead, the hyphae bear both thin-\yalled and resistant sporangia, the btter s^erminating to produce isogamous gametes. In the remaining species, A. miomahis, there is no indication of gamete or cyst formation, the zoospores from resistant sporangia deyeloping directly into plants bearing thin-\yalled and thick- \yalled sporangia. Sorgel (1937) has reported this occurrence in A. arbitsciila as \yell, so perhaps this life cycle is a mere yariant; at any rate three distinct life cycles are known in the genus. A precise eyaluation of this situation is at present impossible in the face of such complexities as the occasional presence of resistant sporangia on the gamete-bearing plants [Sorgel (1937), Indoh (1940), Emerson (1941)] and the discrepancies in the yarious cytoloorical accounts of the Hfe history [Hatch (1938)]. Two additional genera of somewhat greater simplicity in thal- lus structure haye recently been described; they are Blastocla- diella [Matthews (1937)]' and Sphaerocladia [Stiiben (1939)]. In these genera the thallus is much reduced, bearing^ but a single sporangium, either a zoosporangium or a resistant sporangium. Likewise the male and female gametangia are borne on separate thalli, so that these genera are heterothallic, whereas Allomyces is homothallic. The gametes themselyes are isogamous [Harder and Sorgel (1938)]. The simpHcit)^ of thallus structure and sexuality in Blasto- cladiella and Sphaerocladia suggests their relationship with the chytrids. It is therefore possible to postulate an ascending series from the chytrids through these isogamous forms to Allomyces, 82 THE PHYCOMYCETES which is anisogamous, culminating in the oogamous Monoble- pharis of the next order. LITERATURE CITED Blackwell, E., "A life cycle of Blastocladia pringshemiii Reinsch," Trans. Brit. Mycol. Soc, 24: 68-96, 1940. Butler, E. J., "On Allomyces, a new aquatic fungus," Ann. Bota?iy, 25: 1023-1035, 1911. Emersox, R.\lph, "An experimental study of the life cycles and taxonomy of Allomyces," Lloydia, ^; 77-144, 1941. Emersox, Ralph, axd D. L. Fox, "7-Carotene in the sexual phase of the aquatic fungus Allomyces," Proc. Roy. Soc. London, Ser. B., 128: 275- 293, 1940. H.'UiDER, R., AXD Georg Sorgel, "Ubcr einen neuen planoisogamen Phyco- myceten mit Generationswechsel und seine phylogenetische Bedeutung," Nachr. Ges. Wiss. Gottingen, N. F., VI: Biol., 3: 119-127, 1938. Hatch, W. R., "Gametogenesis in Allomyces arbuscida,'" Aim. Botany, 49: 623-650, 1935. "Conjugation and zygote germination in Allomyces arbuscula,'' Aim. Botany, N. S., 2; 583-614, 1938. Indoh, H., "Studies on Japanese aquatic fungi. II. The Blastocladiaceae," Science Repts. Tokyo Bunrika Daigaku, Sec. B, 4: 237-284, 1940. K,\xousE, B. B., "On the distribution of the water molds with notes on the occurrence in Michigan of members of the Leptomitaceae and Blasto- cladiaceae," Papers Mich. Acad. Sci., S: 105-114, 1925. "A monographic study of special groups of the water molds. I. Blasto- cladiaceae," Am. J. Botany, 14: 287-306, 1927. KxiEP, H., Allomyces javaniciis, n.sp., ein anisogamer Phycomycet mit Planogameten," Ber. dent, botan. Ges., 41: 199-212, 1929. "Uber den Generationswechsel yon Allomyces," Z. Botan., 22:433-441, 1930. Matthews, V. D., "A new genus of the Blastocladiaceae," /. Elisha Mitchell Sci. Soc, S3: 191-195, 1937. McCraxie, James, "Sexuality in Allomyces cystogemis,'' My col, 34: 209-213, 1942. Sorgel, Georg, "Untersuchungen iiber den Generationswechsel yon Allo- myces," Z. Botan., 5i: 401-446, 1937. Stubex, H., Uber Entwicklungsgeschichte und Ernahrungsphysiologie eines neuen niederen Phycomyceten mit Generationswechsel," Planta, 50:353-383, 1939. Wolf, F. T., "A study of some aquatic Phycomycetes isolated from Mexi- can soils," Mycoi., 31: 376-387, 1939. "A contribution to the life history and geographic distribution of the genus Allomyces," Mycol., 55:158-173, 1941. MONOBLEFH ARID ALES 83 MONOBLEPHARIDALES The Order Monoblepharidales includes a small number of aquatic fungi of rather unique characteristics, the outstanding of which is that in sexual reproduction a large non-motile t^g is fertilized by a small motile antherozoid. This situation is un- known elsewhere among the filamentous fungi. Asexual repro- duction throughout the group is accomplished by means of zoo- sporangia producing uniciliate zoospores. In this order the cell walls do not turn blue with zinc chloroiodide, an indication of the absence of cellulose. Monoblepharis, the largest genus and the one most completely known, contains about eight species, the first of which was de- scribed by Cornu (1871) in France. The characteristics of Monoblepharis are so different from those of other phycomyce- tous fungi that some doubt as to the existence of these forms remained in the minds of most mycologists until Thaxter (1895) rediscovered representatives of the group in America. Shortly thereafter, as the result of the studies of Lagerheim (1900) in Sweden and Woronin (1904) in Finland, Monoblepharis became better known. The most recent monograph of the group is that of Sparrow (1933). - Monoblepharis is found most frequently on dead submerged twigs in quiet, clear, fresh-water pools. The genus appears to have been found most often in cool waters, early in spring, in the countries of northern Europe and in the northeastern United States. It is seldom recognized in the field but will develop readily when the twigs are placed in aquarium jars in the labora- tory. In cool waters (8 to 11° C) only sporangia will develop; higher temperatures (21° C) are required for the production of sexual organs. The tufts of delicate hyphae protruding from the lenticels of the twists consist of a rhizoidal system, which anchors the plant to the substratum, and a series of slender branches. The protoplasmic contents of the hyphae include regu- larly arranged vacuoles and oil globules, which impart a charac- teristic foamy appearance to the hyphae. The sporangia are borne terminally, containing a single row of zoospores, and are cylindrical, to spherical, to more or less 84 THE PHYCOMYCETES ovate in shape. At maturity a pore is formed at the tip of the sporangium; the zoospores creep through the pore in an amoe- boid fashion, adhering to the mouth of the sporangium for a time, and finally swim away. The zoospores are provided with a single slender cilium, posterior in position. Both in its ciliation and internal structure, the zoospores of Monoblepharis are very similar to those of the Blastocladiales. Each germinates by two germ tubes, one of which forms the rhizoidal system and the other the main hvphae. Fig. 24. Fertilization and emergence of the oospore of Monoblepharis polymorpha. A. The small uniciliate sperm lodged at the receptive spot on the oogonium. B. Fusion has begun. C. Fusion has been completed. (This process, A to C, may require less than 10 minutes.) D. Mature thick-walled oospore, such as may be noted after several hours. (Adapted from Barnes and Melville.) Considerable specific variation occurs in connection with the sexual reproductive structures. In M. polymorpha, for example, the antheridia are exserted on the oogonia (epigynous); whereas in M. sphaerica and M. mcicrandra the antheridia are hypogynous. The development of the antheridia and the maturation of the antherozoids occur in a manner very similar to those of the zoo- spores; the antherozoids are smaller than the zoospores and have a more pronounced amoeboid movement but otherwise resemble them very closely. The content of the oog^onium becomes a sins^le egrg. When it is mature, a receptive papilla is formed on the wall of the oogoni- um, providing a point of entrance for the sperm. Immediately after fertilization the t^g becomes extruded from the oogonium MONOBLEPH ARID ALES 8$ in some species. According to the observations of Barnes and Melville (1932) on M. polyjnorpha, only 8 minutes was required from the time of contact of the sperm A\ith the oogonial wall until fertilization had been completed and the oospore had been completely extruded from the oogonium. In M. jasciciilata and M. msigjiis the oospores are not extruded but are retained within the oogonium. After fertilization the oospore becomes sur- rounded with a heavy wall, which may be either smooth or bul- late in nature. The cytological studies of Laibach (1927) have shown that the oogonium is uninucleate from the time of its formation. After the fusion of Qgg and sperm nuclei, nuclear divisions occur in the oospore during germination, in the course of which meiosis probably occurs. The generic name Monoblepharopsis was created by Laibach to include two species, M. regignens and M. ovigera, differing from Monoblepharis in the more slender hyphae, proliferating sporangia, and absence of sexual organs. In view of the relative unimportance of these characters, Sparrow (1933) does not ac- cept the genus as valid and would reunite these species with iVIonoblepharis. Monoblepharella [Sparrow (1939, 1940)] consists of two species, M. taylori, which was recently found in soil from Trini- dad and other parts of tropical America, and M. viexicana [Shan- or (1942)] from Mexico. Asexually it is similar to Monobleph- aris; the distinctive characters of the genus lie in the behavior of the tgg. When the fertilized tgg is extruded from the oogoni- um, as in certain species of Monoblepharis, it swims away by means of a single cilium derived from the male gamete. The similarity of the reproductive structures of Monoblepharis and of the green aka Oedooronium has been stressed in connec- ^ O c-- tion with the views of those who maintain the algal ancestry of fungi. The discoverv^ of such forms as Monoblepharella has tended to discredit this view in favor of the probability of a close relationship of the Monoblepharidales with the Blasto- cladiales and Chytridiales, all of which have uniciliate zoospores. It has been maintained that Monoblepharella and Monoblepharis form an ascending series from an anisogamous ancestor, such as Allomyces javaiiicus. 86 THE PHYCOMYCETES Fig. 25. A. Monoblepharis polymorpha, showing mature oospores with empty dwarf antheridia borne on the empty oogonia. B. M. sphaerica, empty antheridia occurring at the base of the empty oogonia. (Both after Sparrow.) C. A segment of the thaUus of Gonopodya siliquaefor?im. MOyOBLEPH ARID ALES 81 Somewhat different from these genera is Gonapodva, which occurs on submerged fruits of apple, rose, or Crataegus, in asso- ciation with Blastocladia and various members of the Lepto- mitales. There are t\\o described species: G. prolifera var. sili- quaejorims and G. polyinorpha. The thallus is filamentous, be- ing composed of short segments of hvphae, which are frequently constricted. The constrictions are provided with cellulin plugs, like those in Leptomitus, but Gonapodva has uniciliate zoospores and is thus not related to the Leptomitales. Gonapodva has been placed in the Blastocladiales [Fitzpatrick (1930), Coker and .Matthews (1937)], but it lacks the characteristic resistant sporangia of that order. A proper disposition of the genus must await knowledge of its sexual reproduction. It has been strongly suspected, ho\\'ever, that if the proper environmental conditions were provided, the fungus would be found to pro- duce sexual organs similar to those of Alonoblepharis. Gona- podva is included in the Alonoblepharidales bv Sparrow^ (1933). The sporangia are terminal and more or less oval but taper at the apices to a blunt tip, thus resembling a lamp mantle. Young sporangia frequently proUferate within older ones. Sporangia of the t\vo species of Gonapodva differ greatly in size. In struc- ture and behavior of zoospores, Gonapodva is similar to Alono- blepharis. This order is rather poorly known to most mycologists. The literature gives no indication that anv representative of the group has ever been gro\\n in pure culture. Because of lack of under- standing of proper methods of collection and of cultural require- ments there is a current notion that these forms are very rare. Sparrow, however, has found practically all the species in a single favorable location, and future work will doubtless show that they are far more widespread than has previously been supposed. LITERATURE CITED B.\RNES, B., AND R. Melville, "Notes on British aquatic fungi," Trans. Brit. My col. Soc, 11: 82-96, 1932. Coker, W. C, and V. D. Matthews, "Monoblepharidales," North Avi. Flora, 2 (1):1^7, 1937. CoRNU, M., "Note sur deux genres nouveaux de la famille des Saprolegniees," Bull. soc. bot. France, 18: 5S-59, 1871. 88 THE FHYCOMYCETES FiTZPATRicK, H. M., The lower fungi: Phyco??iycetes. 331 pp. McGraw- Hill, New York. 1930. Lagerheim, G., "AUxologische Studien II. Untersuchungen iiber die Monoblepharideen," Beibang t. K. Svensk. Vet. Akad. Handl., 25: Afd. Ill (8): 3-^2, 1900. Laibach, F., "Zytologische Untersuchungen iiber die Monoblepharideen," Jahrb. iviss.' Botan., 66: 596-630, 1927. Shanor, L., "A new Monoblepharella from Mexico," MycoL, 34: 1'M-l^l, 1942. Sparrow, F. K., Jr., "The Monoblepharidales," Ann. Botany, -^7: 517-542, 1933. '''Monoblepbaris taylori, a remarkable soil fungus from Trinidad," MycoL, 57:737-738, 1939. "Aquatic Phycomycetes recovered from soil samples collected by W. R. Taylor on the Allan Hancock 1939 Expedition," Allan Hancock Pacific Exped., 5:101-113, 1940. Thaxter, R., "New or peculiar aquatic fungi. I. xMonoblepharis," Botan. Gaz., 20:433-440, 1895. II. "Gonapodya Fischer and Myrioblepharis, nov. gen.," Botan. Gaz., 20: 477^85, 1895. Woronin, M., "Beitrag zur Kenntnis der Monoblepharideen," Menx. Acad. St. Petersburg (Phys. Math. CI.), i 5: 1-24, 1904. LEPTOMITALES The group Leptomitales is one of the smaller orders of aquatic fungi, including 7 genera and approximately 20 species. Throughout the group the zoospores are biciliate, and the cell walls are invariably composed of cellulose. The group differs from the Saprolegniales chiefly in the constriction of the hyphae to form a chain of segments. Large granules of cellulin, a carbo- hydrate related to cellulose, occur within the hvphae near the constrictions and may form plugs resembling septa. There is a great diversity of form among the various genera. Some workers, including Indoh (1939), recognize two distinct groups: (1) a "filamentous" group, including Leptomiras and Apodachlya, and (2) an "arbusculate" group, including Sapro- myces, Araiospora, and Rhipidium. The appearance of the ar- busculate forms, with their basal cell crivino- off numerous slender branches above, is reminiscent of the Blastocladiales, with which they are frequently found associated in nature. The usual method of collection [Kanouse (1925)] is to leave a "bait" of fruit or twigs in the water for some time. The group has been little studied and appears to be of rather infrequent oc- LEPTOMITALES 89 currence. The only monographic treatment is that of Kanouse (1927). Leptomitus, the type genus, contains but a single species, L. lacteus. It occurs in se\va2;e effluents in waters containing Indus- trial wastes of various kinds and may occasionally be found grow- ing en Jimsse in clogged drains and similar places. Detailed stud- ies of the nutrition of this species have recently been made by Schade (1940), and Schade anci Thimann (1940). The thallus of Leptomitus is filamentous and constricted, and sporangia are not differentiated as such. The segments become transformed into sporangia in basipetal succession and liberate the biciliate zoospores either through a pore in the terminal seg- ment or through a number of pores, one in each segment. Sex- ual reproduction is unkno\\'n in the genus. Apodachlya bears considerable resemblance vegetatively to Leptomitus, but the segmented hyphae bear pyriform sporangia, whose zoospores may either s\\ im away directly or remain en- cysted for a time at the mouth of the sporangium. Sexual repro- duction occurs by means of a terminal oos^onium subtended by a hypogynous antheridial cell [Kevorkian (1935)]. The devel- opment of the oogonium differs from that of other representa- tives of the order in that no definite periplasm is formed. It has therefore been suggested that Apodachlya and the aUied Lepto- mitus are more closely related to the Saprolegniales than are the remaining genera of this group. In the Genus Sapromyces the thallus is of the arbusculate type, consisting of a trunk or basal cell and numerous branches, but there is very little difference in size between trunk and branches. Sporangia, lobate to cylindrical in shape, occur terminally or near the constrictions of the branches and liberate the biciliate zoospores. The genus has two species, S. audrogymiSy which is homothallic, and S". reinschii, which is heterothallic. In both species the oogonia are pyriform and contain a single oospore surrounded by periplasm, according to cytological investigations of Kevorkian (1935). Bishop (1940) has recently demonstrated the occurrence of relative sexuahty in 5. reinschii and has grown this organism in pure culture. In Araiospora and_ Rhipidium, both of which have several species, there is a stout trunk with rather slender, constricted branches. As in Sapromyces, the trunk is attached to the sub- 90 THE FHYCOMYCETES Fig. 26. A. Habit sketch of Sapromyces androgymis, bearing sexual organs and empty swarm sporangia. B. Fragment of Leptoviinis lacteiis, some of the sporangia being empty. C. Bicihate swarm spore. LITERATURE CITED 91 Stratum by numerous rhizoids. In Rhipidium the sporangium discharges its zoospores into a vesicle. Sexual reproduction in Rhipidium is not unlike that in Sapromyces. Fertilization in R. europaeimi has been studied by Behrens (1931), who reports the formation of a definite exospore from the periplasm. In Araiospora there mav be indications of a vesicle, but when formed it is ephemeral. In this genus two kinds of sporangia are present, one smooth-walled, the other provided with conspicuous spines. In A. pidchra, according to King (1903), the nuclei of the periplasm do not degenerate but become enclosed within cell walls, so that a layer of cells comes to surround the oospore ^\•ithin the oogonium. Although possessing a superficial resemblance to the Blasto- cladiales, the arbusculate representatives of the Leptomitales can- not be considered as closely related to that group because of differences in- the structure of the zoospores and composition of the cell wall. They perhaps form an ascending series from such a filamentous form as Apodachlya to the Pythiales or Perono- sporales, which they resemble closely in the structure of sexual reproductive organs. LITERATURE CITED Behrens, A., "Zytologische Untersuchungen an Rhipidhmi eiiropaeum (Cornu) von' Alinden," Planta, UilV^-lll, 1931. Bishop, H., "A study of sexuality in Sapromyces Reinschii," MycoL, 32: 505-529, 1940. IxDOH, H., "Studies on the Japanese aquatic fungi. I. On Apodachlyella completa, sp. nov., with revision of the Leptomitaceae," Science Repts. Tokyo Bwirika Daigaku, B, ^: 43-50, 1939. Kanouse, B. B., "On the distribution of the water molds, with notes on the occurrence in Michigan of members of the Leptomitaceae and Blas- tocladiaceae," Papers Mich. Acad. Sci. Arts Letters, S: 105-114, 1925. "A monographic study of special groups of the water molds. II. Lep- tomitaceae and Pythiomorphaceae," Am. J. Botany, 14:3^5-357, 1927. Kevorkian, A. G., "Studies in the Leptomitaceae. II. Cytology of Apo- dachlya brachynenia and Saproviyces Reinschii,'^ My col., 21: 274-285, 1935. King, C, "Observations on the cytology of Araiospora pidchra Thaxter," Proc. Boston Soc. Nat. Hist.,' 31:2X1-2^5, 1903. ScHADE, A. L., "The nutrition of Leptomitus," An?. J. Botany, 27:376-384, 1940. ScHADE, A. L., AND K. V. Thi.mann, "The metabolism of the water mold, Leptoviitiis lacteiis,^'' Am. J. Botany, 21: 659-670, 1940. 92 THE PHYCOMYCETES SAPROLEGNIALES Members of this order are commonly termed "water molds." The group includes about 15 genera and approximately 120 species, of which a number are of rather common occurrence. All members of the order are characterized by a well-developed mv- ceHum, the hvphae of which have cell walls composed of cellu- lose. The zoospores, produced in zoosporangia of various t\"pes, are invariably biflagellate. Sexual reproduction occurs by means of antheridia and oogonia containing one to several oospores; periplasm is lacking. The characteristic habitat of the Saprolegniales includes all kinds of fresh water, in which they exist as saprophytes on vari- ous kinds of organic materials. Practicallv all the species mav be readily grown in pure culture, either on solid media or in \^ater cultures on hempseed. Because of the great variability dis- played by many species, the hempseed medium has been rather extensively used as a basis for taxonomic work. The most w^ork- able monographs of the group are those of Coker (1923) and Coker and Matthews (1937). When Saprolegniales are cultivated in water culture on hemp- seeds, the hyphae radiate in a white mat that surrounds the seed. Typically hyphal tips are delimited by cross walls, and each such terminal segment becomes a zoosporangium. As observed with low magnification under a microscope, young sporangia are densely filled ^\•ith protoplasm, whereas the remainder of the hypha seems empty. If the stale water is replaced by fresh w^ater, spore formation and emergence, a fascinating spectacle, may be observed. As the zoospores take shape, the apex of the sporangium softens; at the critical moment it opens, and the zoo- spores rapidly emerge. Within 10 to 20 seconds they may all have come to the exterior and may be dispersed quickly. Although most Saprolegniales are aquatic, the discovery by Harvey (1925) that certain of them can readily be isolated from the soil has resulted in the finding of many previously known forms in this habitat and in the description of a number of new genera and species [Coker (1927), Harvey (1928), Cook and Morgan (1934)]. SAPROLEGNIALES 93 ^^O^G^^i-p i^ c CJ CO CO o rt to u O Cm C/3 O o 4-> u 4-< r-; r-l O r-. O o N So 'C c o « Cm o C-TJ 4-1 C3 :^ 4-> t/5 ^ U5 a 4-> .S M-l U1 4-1 3 y to •M r^ o rt J3 4-1 U o 4-1 to 4-1 o "blj CJ C) y^ ^^ r-* 4-' r- 4-1 U> rt fc- > 3 ri :h > I-* ^ O r" CJ • O CJ t/5 4-1 (-1 4-> 4-< t/3 CJ 4-1 S-( CJ '5i CI. C/5 u til 3 O O CU o 4) G u n o hn o C3 'r- 3 CJ 4-1 ri Sh 1-^ U Ci u bn rt 4-1 «-l-l CJ 4-1 4-) c rt o En" f- C 4-1 'to o a. CD 1-! C) 13 175 4-1 o C/5 r- ri rt • 1-H 4-1 OJ 3 4-1 ^ bxi C a. on a o 0 3 CJ S-I O Sh O t« CJ C3 o r" ?■> t/5 C/2 to U f^ (—1 t/5 O bx) c o i-i O O 4-1 > on O (/3 4-1 • U v; CJ to CJ C/5 CJ o r- C 4-1 > U < C/2 • 4-1 0 4-1 to 3 C/5 < CJ Q CJ bJQ 'o to /^ C/5 3 ri Sh r" • CQ ^3 o o CJ c/: "u 3 ^ C o o CJ 4-> CJ • en w ^ rt 8-1 r^ '■^ a o 4-1 O r-" 173 f ) 13 C O rt 4-1 CJ '4-< o d C3 n Ch f ) O o C) c CJ t/5 C3 vm rt t/3 c O, rt J^ (-1 CJ >. CJ 3 bX) u 4-" C/5 CJ C/1 CLh U 4-1 O r^ Sh o * ^^ < t/5 CJ ex XI r-" c o 4-< 3 J2 <-l-l o "So c O CX 4-1 C o • • c 3 '5n c "sh >^ cu OJ S-i H bb u rt c ca i-i yO CJ to CJ o Uh c 4-> c CJ 4-1 c C/J "3 ri C/5 o u • C3 o C/5 o 4-1 to CJ S-i CJ CJ 1-^ C- O C/5 • t-H CJ r* 4-1 >^ CJ ^ CJ c U o bxj r3 r-* ID fe c 4-1 yn ^ 94 THE PHYCOMYCETES As an important exception to the saprophytic mode of life of these fungi may be mentioned Saprolegnia parasitica, \vhich causes a serious disease of fishes and fish fry [Tiffney (1939)]. Like- \\'ise, yarious species of Aphanomyces are known as parasites on the roots of such higher plants as peas, radish, and beets [Ken- drick (1927), Drechsler (1929)] and on Spirogyra and other aquatic fungi. Asexual reproduction. A number of species reproduce asexually by means of gemmae of various size and shape, usually formed in terminal chains. After a dormant period the gemma may form a germ tube, produce sporangia, and give rise to oospores. The regular means of asexual reproduction, however, is by sporangia and zoospores. The young sporangium is multinu- cleate and cut off from its parent hypha by a septum. Cleavage planes, which appear in the protoplasm, gradually branch and divide the sporangial content into a number of uninucleate masses, each of which will eventually form a zoospore. It is principally by means of variations in the structure and behavior of the zoo- spores that the various genera are delimited. Other character- istics of importance in this connection include the method of renewal of the sporangia, whether by proliferation or by cymose branching from below, the shape of the sporangium, and the number of eggs within the oogonium [Coker and Mat^iews (1937)]. In the rather uncommon Genus Pythiopsis the sporangia are spherical to pyriform in shape, and the zoospores are mono- planetic; that is, there is but a single period of motilit\'. The zoospore itself is pyriform and has two apical cilia. All the remaining genera have sporangia \\hich are cyhndrical, fusiform, or clavate in shape. In Aplanes sporangia are rarely produced; but when they are developed, the spores germinate in situ within the sporangium, and the germ tubes protrude through the sporangial wall. In Saprolegnia, Isoachlya, and Leptolegnia the spores are di- planetic, that is, have two motile phases. On discharge from the sporangium the pyriform "primary" zoospores are motile by means of two apical cilia. After a brief motile period they encyst and then give rise to "secondary" zoospores that are reniform and possess two lateral cilia. SEXUAL REPRODUCTION . 9S In Achlya, Protoachlya, Sommerstorffia, Aphanomyces, and Plectospira the first swimming stage is almost completely sup- pressed. The spores, on discharge, come to rest at the mouth of the sporangium and encyst, and the reniform or "secondary" zoospores escape from the cysts. In Dictyuchus encystment of the zoospores occurs within the sporangium, and each reniform zoospore escapes individually through its own pore in the sporangial wall. In Thraustotheca, Brevilegnia, and Geolegnia the spores, hav- ing encysted within the sporangium, are gradually liberated by a dissolution of the sporangial wall. In some species of Brevileg- nia and in the genus Geolegnia zoospores are not formed as such. The spores are non-motile and may even be multinucleate. This phenomenon has been interpreted [Hohnk (1935)] as an adapta- tion for life in the soil. The occurrence of two distinct types of zoospores in the Saprolegniales is a feature for which no satis- factory explanation has yet been offered. Sexual reproduction. Sexual reproduction, involving the for- mation of antheridia and oogonia, generally occurs in water cul- tures upon the exhaustion of the nutrient supply. Except in occasional instances the sex organs are not readily produced on solid media. When a single hypha gives rise to both oogonia and antheridia, the species is said to be androgynous (homo- thallic). To other species, in which antheridia and oogonia may be formed on hyphae at some distance from each other, the term diclinous has been applied. In Dictyuchus monosporiis [Couch (1926)], Achlya biseximlis [Raper (1936)], and A. mnbisexiialis [Raper (1940)] true heterothallism has been demonstrated. Working with A. aiJibisexualis, Raper has clearly shown the existence of relative sexuality; that is, a strain which produces antheridia in one cross may produce oogonia instead when crossed with a different isolate. The young oogonium, which generally appears as a lateral branch of a main hypha, is multinucleate. After nuclear division there occurs a degeneration of many nuclei and a reorganization of the oogonial contents into a number of uninucleate eggs (oospheres). In a number of genera, including Leptolegnia, Aphanomyces, Dicrv^uchus, Brevilegnia, and Geolegnia, only a single Qgg is formed \\ithin the oogonium. In most of the re- maining genera more than one egg is produced, but the number oospheres, .vkb nucleus iusrrfth ^f°'P^"' formation. D. Uninucleate with gamete nuclei n contact t'r " ""''""™ '"''^- ^- O^P^-e visible G. Two nearly mat^'te " ^"^""= ""<='^'= ^""^ ""^1^°'' luo nearly mature oospores, one with large fusion nucleus. 96 LITERATURE CITED 97 formed may vary considerably within a single species. As many as thirty eggs may be formed in certain species. The development of the antheridiiim, paralleling that of the oogonium, culminates in the formation of fertilization tubes, which penetrate the oogonial wall and enter the eggs. Fertihza- tion has been demonstrated in a considerable number of species of Achlya [Patterson (1927), Wolf (1938)], Saprolegnia [Claus- sen (1908), Hohnk (1935a)], Aphanomyces [Kasanowsky (1911)], Brevilegnia [Cooper (1929)], Leptolegnia [Couch (1932)], and Thraustotheca [Shanor (1937)], and doubtless it occurs whenever antheridia are present. It has been known since the time of de Bary that antheridia may not be present on all the oogonia produced, and in certain forms oospores may be pro- duced parthenogenetically. The mature oospore is surrounded by a heavy wall. After a rest period of several months, the oospore eventually germinates by forming a short germ tube bearing a sporangium. It has re- cently been shown [Schrader (1938)] that meiosis occurs dur- ing oospore germination. LITERATURE CITED Claussen, p., "Uber Eientwickelung und Befruchtung bei Saprolegnia mo- noica^'' Ber. dent, botmi. Ges., 26: 144—161, 1908. CoKER, W. C, The Saprolegniaceae, with notes on other ivater molds. 201 pp. University of North Carolina Press, Chapel Hill. 1923. "Other water molds from the soil," /. Elisha Mitchell Sci. Soc, 42: 207- 226, 1927. CoKER, W. C, AND V. D. Matthews, "Saprolegniales (Saprolegniaceae, Ec- trogellaceae, Leptomitaceae)," North Am. Flora, 2, Part 1: 15-67, 1937. Cook, W. R. I., and Enid Morgan, "Some observations on the Saproleg- niaceae of the soils of Wales," /. Botany, 72: 345-349, 1934. Cooper, G. O., "Cvtoiogical studies on the sporange development and gametogenesis in Brevilegnia diclina Harvey," Trans. Wis. Acad. Sci.j 2-^:309-322, 1929. Couch, J. N., "Heterothallism in Dictyuchus, a genus of the water molds," Ann. Botany, ^0:849-881, 1926. "The development of the sexual organs in Leptolegnia caudata,^'' Am. J. Botany, 19: 584-599, 1932. Drechsler, C, "The beet-water mold and several related root parasites," /. Agr. Research, 5^pes, as is indicated bv the names Sphaerosporangium and Nema- tosporangium, more appropriately regarded as names of sub- genera. The development of oogonia and antheridia has been studied repeatedly, and essential features in Fythiinn de baryamim were determined long ago bv Aliyake (1901). The hyphal tips first become inflated, are multinucleate, and are set off by septa. As the oogonium enlarges, the central portion becomes the oosphere; and the peripheral portion, the periplasm. All the nuclei but one migrate into the peripheral laver, where they disintegrate. Meanwhile all but one of the antheridial nuclei disintegrate also, and a wide pore forms at the point of contact of the antheridium with the oogonium. This stage is followed by the migration of the antheridial nucleus and a portion of the cytoplasmic content through the periplasm to contact the centrally located tgg nu- cleus and cytoplasm. These two nuclei then fuse, and a thick wall, a modification of the periplasm, is developed around the zygote. In respect to position of antheridia with respect to oogonia, there are two general tvpes of Pythiales: paragvnous and amphi- gynous. In the first type the antheridia are applied at the side of the oogonia; in the second they are appUed as a doughnut- shaped collar around the oogonial stalk. The Pythiales grow readily on a wide variety of artificial sub- strata. Alany of them can be induced to form both sporangia and sexual spores on agar, whereas others remain sterile or form sporangia only. Emergence of swarm spores often takes place if fresh water is applied or if the sporangia are placed in fresh water. Boiled hempseeds placed in ^\•ater are very satisfactory in isolating Pythiales from soil samples. Pythium. The Genus Pythium is extensively treated by But- ler (1907), Matthews (1931), and Middleton (i943). As mono- graphed by Matthews (1931), it contains approximately 40 species, whereas Middleton (1943) recognizes 66 species as valid. Perhaps the best known among them is P. de haryamnn, which causes damping off of seedlings, both herbaceous and woody. It is especially destructive to coniferous seedlings in nurseries and PYTHIUM 101 to such crop plants as tobacco, cabbage, and tomatoes being grown in seed beds. It is probable that P. idtiimm?, when isolated from diseased seedlings, has been wrongly identified in some in- stances as P. de baryamnn. Although P. idtlmiim does not form zoospores, its sporangia germinate directly, that is, by germ tubes, and its antheridia are androgynous. Fig. 30. Sonmierstorffia sp'inosa, parasitizing the rotifer Monostyla attached to a filament of the alga Rhizoclonium. (Adapted from Sparrow.) Pythiimiaphajjiderinatinn, described by Edson (1915) as Rheo- sporangknn aphaniderviatum, is the cause of a seedling- and root- rot disease of sugar beets and radishes. It has been found to attack also the seedlings of various other species. Its cytology and developmental history, as reported by Edson, agree with that known to characterize Pythium. Similarly Zoophagiis insidians, described by Sommerstorff (1911) as a predator on rotifers, ap- pears to belong to the Genus Pythium instead. In Pythium, as usually encountered, the protoplasm passes in an undifferentiated state into a vesicle at the tip of the exit tube, 102 THE PHYCOMYCETES which is approximately as long as the diameter of the sporangium. This vesicle is the inner sporangial wall. After 10 to 15 minutes the zoospores become differentiated \\ithin the vesicle and move about within it, at first sluggishly and then ^\•ith increasing rapidity. At length the vesicle ruptures, and the zoospores da'rt aw^ay at high speed. After a few minutes they come to rest, en- cyst, and then orerminate by the formation of a tube. Phytophthora. The Genus Phytophthora (the name signifies "plant destroyer"), well known to all plant pathologists, includes 17 species and 1 variety, according to the monograph by Tucker (1931). The name was first employed by de Bary in 1876 as a result of his studies of P. infestavs, \\hich causes late blight and tuber rot of potatoes. This organism \\as introduced into Eu- rope, where it has produced serious losses year after year. How it hibernates remained a controversial question for years, but the mycelium is now known to survive within the "seed" tubers. Smith (1875) early maintained that it forms, within the potato foliage, oospores by means of \\hich it survives from year to year, but de Bary demonstrated that the oospores observed by Smith were those of Pythium. Jones, Giddings, and Lutman (1912) obtained oogonium-like structures in pure cultures. An- theridia were not observed, however, and Clinton (1911), who secured ooo-onia and antheridia on oat acjar, believed the struc- tures seen by Jones and his associates might as well have been chlamydospores. Microscopic examination of diseased potato foliage shows that the mycelium of P. injestans is intercellular and that haustoria penetrate the host cells. Slender, sparsely branched hyphae in small groups, the sporangiophores, emerge from the stomata. Ovoid to pear-shaped sporangia are formed at the tips of the sporangiophores, after which the hyphae continue to elongate, thus causing the sporangia to appear laterally attached. Sporangia are readily detachable and may be carried by rain-splash or air currents to other leaves to initiate new infections. The rv^pe of germination of sporangia is determined by tem- perature and moisture. The sporangium may form a germ tube that penetrates the host directly, or else its content becomes divided to form biciliate zoospores. Zoospores escape through an apical pore, and after 2 or 3 hours, have settled, produced a germ tube, and penetrated new host tissue. Entrance occurs PHYTOPHTHORA 103 1 ^- s p ^ U o Sd.2 r^ r- ri Ji o ^^ ■£d CJ 5 5fi y r- r- w ^y* ^\ rt •— ' y ^ rt Ui vi- ^>^ O fS .. '^ s 5 "^ i ^- VJ^ f p u r- o M_i rt •-§ 'u^ y ■£:: 13 >-. '^' ~ y y 0^ 4-1 • r- •t; CQ o o . ^ 5 u r^ >.o .b^ o ~u w^ »*-.. "^kl •^ '^ >M « ^ ^ -^ "3 ^ 5 rt 4J !5 ,C C/2 2 t^ '5 a fcX) ^ -Ci i*^ B -1 •1^ O-I 7 - N -^ a: d u ^ ^ c "^^ ' = 1 r" ^' "^ IE r- '^ ••^ 1;^ ' jn !"• 3 1 -^ y _ — ' ■y 'e 3 o « y _o C 'T ^ '1 y > >. c y C y 3 z £ "" in 4— ' ^ c •^ c c: • ^H C 3 ^^^ r- .M t^ CI- y c 3 'E y ^^ y w 4-1 y r- r- 4-1 ri o c '5d < C 5 ^ 5^ y <1 C3 y u-~ -^ ^ 4-> ■ ^ ^ • — E y r5 < 4^ rt E ^ ^^ >. ^- CX y c < c 'r> .2 ^ o -2 P • ^H ^ *-4 4—' • ^« 4-< o C/- s .s u r*. ^ 3 4-1 '•M ^ CT) a ki s • . r-; c« ^ c/; 3 «^^ >^ y y • r^ °1 4-1 b « t/5 C 104 THE PHYCOMYCETES either through the stomata or through unbroken epidermis. Soon lesions are formed, and after 3 to 5 days of favorable weather P. infestans will again be sporulating. The short sporangial cycle makes possible the rapid development of potato-foliage blight in epiphytotic proportions. Presumably zoospores are transferred through the soil and gain entrance through the lenticels, and thus tuber decay is initiated. There are other very destructive species of Phytophthora. Amon^ the better known are F. palmivora, studied by Seal (1928) in connection with bud rot of coconut and other tropical plants. Nearly 50 years ago van Breda de Haan (1896) recorded a disease of tobacco in Sumatra, the cause of which he identified as P. nicotianae. The fungus has since spread throughout the tropics, and about 15 years ago it appeared in the flue-cured to- bacco district of North Carolina. Tucker (1931) regards it as specifically identical with P. parasitica and uses nicotianae as a varietal name. Phytophthora citrophthora, causing brown rot and orummosis of lemons, was first described by Smith and Smith (1906) as Pythiacystis citrophthora. Petersen's (1910) mono- tA'pic Pythiomorpha gonapodioides, growing on twigs and fruits immersed in water, has been indicated to be a Phytophthora. The Genus Phytophthora differs from Pythium in that on germination the zoospores are fully formed within the sporangium and escape through an opening at the papilla. In Phytophthora palniivora, however, a vesicle may at times be formed; at others the swarm spores escape directly. The taxonomy of both Phytophthora and Pythium is difficult, since so much deoends on cultural characteristics and host rela- tionships. LITERATURE CITED Breda de H.\.\x, J. van, "De bibitziekte in de Deli tabak veroorzaakt door Phytophthora nicotianae,'' Mededeel. s'Lands Plantentiiin, 15: 107 pp., 1896. Butler, E. J., "An account of the genus Pythium and some Chytridiaceae," Mein. Dept. Agr. India, Bot. Ser., 1: 1-160, 1907. Clinton, G. P., "Oospores of the potato-blight fungus, Phytophthora in- jestmisr Kept. Conn. Agr. Expt. Sta., 1909-1910: 151-11^, 1911. Edson, H. a., ''Rheosporangiinn aphanidermatiim, a new genus and species of fungus parasitic on sugar beets and radishes," /. Agr. Research, 4: 279-291, 1915. ALBU GIN ALES 10$ Jones, L. R., N. J. Giddings, and B. F. Lutmax, "Investigations of the po- tato fungus, Fhytopbthora infestans,^'' U. S. Dept. Agr. Bur. Plant bid. Bull, 245. 100 pp. 1912. Matthews, Velma D., Studies on the genus Pytbiwu. 136 pp. The Uni- versity of North Carolina Press. 1931. MiDDLETON, J. T., "The taxonomy, host range, and geographic distribution of the genus Pvthium," Mem. Torrey Botan. Club, 20: 1-171, 1943. MiYAKE, K., "The fertilization of Pytbiwu de haryanmn^'' Ann. Botany, l)':65y-666, 1901. Petersen, H. E., "An account of Danish fresh-water Phvcomvcetes, with • biological and systematic remarks," Ann. MycoL, 5': 494-560, 1910. Seal, J. L., "Coconut bud rot in Florida," Fla. Agr, Expt. Sta. Bidl., 199: 87 pp. 1928. Smith, R. E. and Elizabeth H., "A new fungus of economic importance," Botan Gaz. ^2; 215-221, 1906. SxMith, Worthington G., "The resting spores of the potato fungus," Gard. Cbron., n.s., ^; 68-70, 1875. Somaierstorff, H., "Eine Tiere fangender Pilz (Zoopbagus insidians, nov. gen., nov. sp.)," Oest. Bot. Z., 61:361-373, 1911. Tucker, C. AL, "Taxonomy of the ^enus Phytophthora de Barv," Mo. Agr. Expt. Sta. Researcb Bidl, 153. 208 pp. 1931. ALBUGINALES The Albuginales, commonly called "white rusts," comprise a single genus, Albugo, having approximately 25 species. All are obligate parasites of flowering plants, and none has been cul- tivated on artificial media. They are an aberrant group, dis- tinguishable mainly on the basis of their host relations. For example, A. Candida is limited to various species of crucifers, A. bliti to species of Amaranthus, A. ipovweae-paiiduraiiae to morning-glory, sweet potato, and other Convolvulaceae, A. tragopogonis to salsify and other Composites, and A. portidacae to Portidaca oleracea. Usually none occurs in epidemic pro- portions on crop plants, except perhaps A. Occident alls, recently reported [Wiant, Ivanoff, and Stevenson (1939)] on spinach. Whether this pathogen occasions real harm is questionable. Certain of these species comprise rather \\'idely different mor- phological groups of entities that have been regarded as biological species. By means of biometrical studies Togashi, Sibasaki, and Sugano (1930) were able to show that the sporangia of A. Can- dida on Brassica and Raphanus have measurements approximately 25% greater than those on Arabis, Capsella, and Draba. Their 106 THE PHYCOMYCETES i< c « o O CLu-< a ^ a O ° 5 O 3 5^ D o K* -o W5 C/5 o t-> Tl o > f= c 1 0- u *w o (73 ^ en Ui So o 3 o 3 O O r: c^ r^ "73 tH w t: .5 cu CI. t£i G 'O ^ iJ ^ o O C3 ^ = ^ e <-i-i ""t-* -— ; w « IS r" " - r- G 4-> 3 "^ .3 a." •r C C « .S|.= a o OJ "" C3 O 3 '-^.^i • y5 O C bO _ rt C r- N ' S '^ ^ « C« j_, o > t; o °Q .2 O « t: rt o 3 ?^ u ^ K«: — 3 ■^ r- ^ 3 t^ C S-i C "^ -3 O 3 fcO •-• **i , ^ 3 • o ■3 a b C3 c O p C bx) C V5 ^ 3 3 CJ aj CJ J= CJ u o CO c ALBUGINALES 101 examination of sporangia from 42 cruciferous genera led them to divide A. Candida into two groups, viacrospora and viicrospora. A monograph by Wilson (1907, 1908, 1908a) deals with the classification of species known to occur in North America. Albugo is characterized by the possession of sporangiophores arranged in a palisade-like layer, thus forming pustules beneath the epidermis of the host. The sporangiophores are broadly clavate, and the sporangia are abstricted in basipetal succession and adhere in chains. The sporangia have the appearance of be- ing separated by intercalary cells, but instead the outer sporangial wall partly gelatinizes at the point of contact of adjacent sporangia, forming disks ^^•hich, when gelatinization is complete, permit the sporangia to fall apart. Pressure exerted on the super- imposed epidermis by the accumulation of sporangia finally causes the leaf tissues to rupture and permits the powder\' mass of sporangia to be disseminated by the wind. Germination of the sporangium results in the formation of 12 to 20 zoospores. The zoospores are reniform and bifiagellate. After a brief period of swarming, they encyst, and further de- velopment consists in the formation of a germ tube which is capable of penetrating a suitable host by way of the stoma. Melhus (1911) found that direct germination may also occur, governed by temperature. Palm (1932) observed that sporangia of A. portidacae, A. bliti, and A. spimilosa, on germination, may commonly form germ tubes. Antheridia and oogonia of white rusts begin to appear when the production of sporangia is ceasing. They arise within the host tissues. De Bary first described the sexual orgrans of x\lbuCTO, and Wager (1896) gave a correct account of the details of fer- tilization. The oogonia are globular, multinucleate cells, and one or more small sflobular antheridia arise near the oocronium. Gradually the oogonial content becomes differentiated into the tq^^ cell, or ooplasm, and a peripheral layer, the periplasm. The details which accompany these changes are carefully delineated in a series of papers by Stevens (1899, 1901). He found that there are essentially three types of fertilization. In the first, represented in A. bliti and A. portidacae, \\hich he records as the most primitive, there are many functional nuclei, a large recep- tive papilla and a small coenocentrum. In A. tragopogonis, rep- resenting the second type, all but one male and one female 108 THE PHYCOMYCETES nucleus disintegrate after migration into the periplasm, and this species possesses a small papilla and a large coenocentrum. In A. Candida, typifying the third type, a pair of functional nuclei fuse after disintegration of all supernumerary nuclei, and the size of both papilla and coenocentrum is intermediate between those of the other two types. According to Wager (1896), the fusion nucleus soon divides in A. Candida, and after five simultaneous divisions of the nuclei the oospore becomes dormant. Evidence indicates that the first divisions are reductional. Meanwhile a thickened, variously sculptured, three-lavered wall is formed. The oospores of each species appear to have a distinctive pattern of sculpturing, ten of which are illustrated in Wilson's (1907) monograph. After over- wintering, more divisions occur, the wall cracks open, the inner wall slips out as a vesicle containing about 100 zoospores, the vesicle bursts, and the zoospores swim away. LITERATURE CITED Melhus, I. E., "Experiments on spore germination and infection in certain species of Oomycetes," Wis. Agr. Expt. Sta. Research Bull, 15: 25-91, 1911. Palm, B. T., "Biological notes on Albugo," Ann. MycoL, 50:421-426, 1932. Stevens, F. L., "The compound oosphere of Albugo bliti,'' Botan. Gaz., 28: 149-176, 225-245, 1899. "Gametogenesis and fertilization in Albugo," Botan. Gaz., 52:77-98, 157- 169, 238-261, 1901. ToGASHi, K., Y. SiBASAKi, AND Y. SuGANo, "Morphological studies of white- rust fungi in the cruciferous plants," Agr. Hon., 5: 859-882, 1930. Wager, H., "On the structure and reproduction of Cystopiis candidiis Lev.," Ann. Botany, 10: 295-342, 1896. WiANT, J. S., S. S. IvANOFF, AND J. A. Stevenson, "White rust of spinach," Phytopathology, 29:616-623, 1939. Wilson, G. W., "Studies in North American Peronosporales. I. The genus Albugo," Bidl. Torrey Botan. Club, 34: 61-84, 1907. III. "New or noteworthy species," Bidl Torrey Botan. Club, 5S: 361-365, 1908. IV. "Host index," Bull. Torrey Botan. Club, 55:543-554, 1908a. PERONOSPORALES Approximately 300 species of fungi, commonly called downy mildews, are included in the Peronosporales. All are obligate ASEXUAL REPRODUCTION 109 parasites, and none has been grown on artificial media. Their sporangiophores project from the host, forming en masse a downy, whitish, gray, or violet coating, whence the name, downy mildews. Many of them occur on crop plants and are very destructive. The best kno^n among them are Flasmopara viti- cola on grapes [Arens (1929, 1929a)], Feronospora destructior on onion [Cook (1932)], Feronoplasfnopara ciibensis on cucur- bits [Clinton (1905)], Feronospora tabacina on tobacco, Bremia lactiicae on lettuce, Feronoplasfnopara hinniili on hop, and Sclerospora graminicola on cereals [Weston (1924), Weston and Weber (1928), Melhus, van Haltern, and Bliss (1928)]. Mycelium. The mycelium courses through the intercellular spaces, and haustoria penetrate the host cells. In many species the haustoria are vesicular, but in others they are branched and filamentous. Some few species, among which' are Feronospora schachtii on Beta vulgaris ^ F. alsinearinn on Stellaria media, F. effiisa on Spinacea oleracea, F. viciae on Vicia sepiimi, and Flas- mopara viticola on Vitis viiiifera, are known to perennate as mycelium [Melhus (1915)]. Asexual reproduction. The sporangiophores of downy mil- dews are distinctive and constitute the most important basis for identification of genera. Those of Basidiophora are club- shaped, and the sporangia are borne in a cluster at the enlarged tip; those of Bremia are branched with saucer-shaped terminal enlargements. Usually 4 to 6 branchlets (sterigmata), bearing sporangia, project from the rim of the saucer. The sporangio- phores of Plasmopara are irregularly branched, as are also the blunt-tipped branchlets. The branches of Feronospora terminate dichotomously, and the branchlets are of equal length. Each sporangiophore of Sclerospora simulates a thick-handled, com- pact brush. Species, on the other hand, are distinguished largely on the basis of host relationships. Sporangiophores emerge from the stomata singly or in small groups and appear usually on the lower leaf surface. The sporangia are borne singly at the tips of branchlets. Sporangial formation usually occurs at night and, at least in Sclerospora graminicola and Feronospora tabacina, is con- ditioned by temperature and relative humidity [Weston (1924), Wolf et al. (1934) ] . In S. graminicola the formation of sporangia begins near midnight, if there is a film of moisture on the corn no THE PHYCOMYCETES SEXUAL REPRODUCTION 111 leaves. Within 1 % hours the sporangia ^^ill mature, and they are then dispersed. Several crops of sporangia are produced during the night as the spent sporangiophores collapse and new ones emerge in their places. This process will be repeated night after night, except on dry nights. In P. tabacina, however, a single crop of sporangiophores and sporangia is developed during the period between daybreak and sunrise" The dependence of this organism upon temperature and high relative humidity is indicated by the fact that epidemics are suddenly checked with the advent of hot weather and that it has been possible to induce fructification, under controlled condi- tions, at any time throughout the year. Indeed, in North Caro- lina sporangia were caused to be formed on 2 1 nights during the month of August. Germination of the sporangia and infection are usually accom- plished during the early morning. In all downy mildews, except species of Peronospora, zoospores are normally produced. In Peronospora, however, representing the most advanced terrestrial habit, germ tubes are formed. In Peronoplasmopara, germination of both types occurs, temperature being an important factor in conditioning the type. Usually the zoospores are emitted singly through a papillar opening, swim around for a brief period, encyst, and then germinate by production of germ tubes. Sexual reproduction. The oogonia and antheridia form within the tissues, arising on closely adjoining hyphal tips. De- tails of their formation and of fertilization are contained in the accounts of Wager (1900), Kruger (1910), Arens (1929, 1929a), and McDonough (1937). Each organ is multinucleate after seg- mentation from the supporting mycelium. Gradually the cyto- plasm of the oogonium becomes differentiated into a central uni- nucleate t^g and a peripheral periplasm containing the super- numerary nuclei. All disintegrate except the t^^ nucleus. Meanwhile, within the adjacent antheridium the nucleus of the male gamete becomes differentiated, and the other nuclei, about a dozen, disintegrate. A fertilization tube that pierces the oogonial wall and periplasm is then produced. The male-gamete nucleus passes through the fertilization tube into the ooplasm. Nuclear fusion follows, whereupon a thick, resistant wall is formed around the zygote. 112 THE PHYCOMYCETES Opinions differ regarding the time of occurrence of reduc- tional division. Wager (1900) maintains that it takes place just before fertilization, and Kriiger (1910) and Arens (1929, 1929a) at the time of the first division of the zygote nucleus. It is prob- able that Kriiger and Arens are correct, but this point requires elucidation. In most downy mildews the oospores constitute the hibernat- ing stage. They usually form within necrotic tissues near the end of the pathogenic cycle and are liberated by decay of the host tissues. InPla^jiopara vkicola [Arens (1929, 1929a)], how- ever, they form all summer long. In Peronoplasmopara ciibensis they form most abundantly in the youngest host tissues. In Sclerospora graminicola they continue to fall to the ground as the leaf parenchyma disintegrates [Weston and Weber (1928)]. In Peronospora tabachia they form only in tissues that have been dead a week or more. Essentially nothinsr is known about the influence of environmental factors on oospore formation among any of the downy mildews. The essentiality of oospores in the hibernation of P. tabacina was established by Dixon et al. (1935). By epidemiological methods they determined that this pathogen overwinters as oospores in North Carolina. Primary infections in all areas ap- peared in seed beds sown on the sites of old beds. These in- fections antedated by 7 to 19 days those in near-by seed beds located on new sites. Furthermore sporulation occurred in beds located on old sites before the time when sporangia could be entrapped from the air in the same locality. Oospore germination has been observed in a few species. Greg- ory (1912) and Arens (1929, 1929a) noted that a short germ tube arises from the oospore of Plasmopara viticola and that a sporangium forms at the end of this tube. Swarm spores emitted from this germ sporangium are capable of inducing primary in- fection. In Sclerospora graininicola Hiura (1935) observed germ- tube formation, which may be assumed to cause infection after penetration of the grass host. In respect to the factors which favor oospore germination, temperatures of 20 to 25° C have been found to be optimum for both P. viticola and S. graminicola. Manifestly because of the paucity of observational data the germination of oospores of downy mildews is \\'orthy of ex- tensive investigation. SEXUAL REPRODUCTION 113 I F.0 34 Structural features of Peronospora tabacina. A. Dendritic spo- r::-;:phore at .hose ^^::::zi:: ^z'^z.^T^J^s S— ^s r^ar ^^^S^^st f^nlL of spor/,. D. Entrant of germ tube into stomate. (Penetration may also be direct.) ^'J'^^ l!T Stages in formation and maturation of oospores, as d'ssected from the inierior of leaves. /. Branched haustorium, by means of x.hich the intercellular hyphae absorb nutriment. 114 THE PHYCOMYCETES Classification. No recent comprehensive monographic treat- ments of downv mildews exist. That of Berlese (1903) now has a Hmited usefulness. Wilson's (1907, 1914) accounts deal only with approximately 40 North American species. Gaumann's (1923) monograph of Peronospora treats of 140 species occurring' in Switzerland. He divided the oenus into two subgenera, Leiotheca and Calotheca, on the basis of whether the oospores have smooth or verrucose walls, respectively. Each subgenus contains 2 groups. In Leiotheca the parasiticae include 36 thick- \Aalled species, and the effusae, 72 thin-walled species. In Calo- theca the verrucosae include 5 species with hemispherical warts, and the reticulatae, 28 species wdth a netw^ork of anastomosing ridges. Species are separated largely on the basis of biometrical measurements of sporangia and of the results of cross-inoculation trials. In identifying downy mildews the mycologist depends almost wholly upon the use of a host index. Such a procedure has little to commend it and indicates the urgent need of a usable mono- graph. General considerations. It may be of more than passing in- terest to point out that all the dozen or more known species of Sclerospora, with one doubtful exception, appear to be confined to grasses. Sclerospora gi-aminicola attacks not only corn and suorar cane but also a larg^e number of other grrasses. Several Other species are known to attack corn in the tropics. Sclero- spora viacrospora also attacks a wide variety of grass species, in- cluding rice, oats, and wheat. Some species are known only in the conidial stages and appear to lack the ability to form oospores. Bremia lactiicae, common on lettuce, seems to be a monotypic species. Downy mildews are of rare occurrence on trees and shrubs. Feronoplasmopara celtidis on hackberry (Celtis spp.) and P. meliae on chinaberry (Melia azadarrach) are notable exceptions. The discovery in 1882 of the fungicidal value of Bordeaux mix- ture by Millardet (1933), marking the beginning of spraying, is a landmark in the history of plant pathology. This discovery may be attributed to two circumstances: (1) the outbreaks of downy mildew in the vineyards of France, and (2) the propen- sity of boys, on certain occasions, to pilfer fruit. It is an interesting coincidence that the use of volatile fungi- LITERATURE CITED 11$ cides to control diseases of plants had its beginning in attempts to control another downv-mildew disease, namely, that induced by Feronospora tabacbia. The fundamental principles involved in the use of two volatile materials, benzol and paradichloro- benzene, and related compounds are presented in reports by Wolf et al. (1940), Pinckard et al. (1940), and McLean et al. (1940). LITERATURE CITED Arens, K., "Untersuchungen liber Keimung und Zvtologie der Oosporen von Flasiiiopara viticola (Berl. et de Toni)," Jahrb. iviss. Botan., 10: 57-92, 1929. "Physiologische Untersuchungen an PlcisTnopm\i i-iticola, unter besond- erer Berucksichtigung der Infektionsbedingungen," Jahrb. iviss. Botcvi., 70:93-157, 1929a. Berlese, a. N., Saggio di una vionografia delle Feronosporaceae. 311 pp. 1903. Clinton, G. P., "Downy mildew or blight of muskmelons and cucumbers," Conn. Agr. Expt. Sta. Ann. Rept., 1904: 329-362, 1905. Cook, H. T., "Studies on the downy mildew of onions and the causal or- ganism, Feronospora destriictior (Berk.) Casparv," Cornell Agr. Expt. Sta. Mem., i-/5. 40 pp. 1932. Dixon, L. F., Ruth McLean, and F. A. Wolf, "The initiation of downv mildew in North Carolina in 1934," Fbytopatbology, 25: 628-639, 1935. Gaumann, E., "Beitrage zu einer Monographie der Gattung Peronospora Corda," Beitr. Kryptogamenfi. der Scbiveiz, S: 1-360, 1923. Gregory, C. T., "Spore germination and infection with Flasmopara viti- cola'' Fhytopatbology, 2: 235-249, 1912. Hiura, M., "iMycological and pathological studies on the downy mildew of Italian millet," Giju Imp. Coll. Agr., Research Bidl., 55:121-283, 1935. Kruger, F., "Beitrag zur Kenntnis der Kernverhaltnisse von Albugo Candida und Feronospora ficariae,'' Zentr. Bakt. Farasitenk., II Abt., 21: 186-205, 1910. McDoNouGH, E. S., "The nuclear histor}^ of Sclerospora graminicola,''' My- col., 25>: 151-173, 1937. McLean, Ruth, J. A. Pinckard, F. R. Darkis, F. A. Wolf, and P. M. Gross, "The use of paradichlorobenzene in seedbeds to control tobacco downy mildew," Phytopathology, 50:495-506, 1940. Melhus, I. E., "Perennial mycelium in species of Feronosporaceae related to Fhytophthora infestans,'' J. Agr. Research, 5: 59-69, 1915. Melhus, I. E., F. H. van Haltern, and D. E. Bliss, "A study of Sclero- spora graminicola (Sacc.) Schroet. on Setaria I'iridis (L.) Beauv. and Zea mays (L.)," Iowa Agr. Expt. Sta. Res. Bull., //7: 297-338, 1928. Millardet, p. a., "The discovery of Bordeaux mixture." 25 pp. Fhyto- path. Classics, 5, 1933. (Translated by F. J. Schneiderhan.) ' 116 THE PHYCOMYCETES PiNCKARD, J. A., Ruth McLean, F. R. Darkis, P. i\I. Gross, and F. A. Wolf, "Toxicity of paradichlorobenzene in relation to control of to- bacco downy mildew," Phytopathology, 50:485-495, 1940. Wager, H., "On the fertilization of Peronospora parasitica,'^ Ami. Botany, i^; 263-279, 1900. Weston, W. H., "Nocturnal production of conidia by Sclerospora graiJii- nicola;' J. Agr. Research, 21:111-1%^, 1924. Weston, W. H., and G. F. Weber, "Downy mildew {Sclerospora gramini- cola) on everglade millet in Florida," /. Agr. Research, 55:935-963, 1928. Wilson, G. W., "Studies in North American Peronosporales. II, Phytoph- thoreae and Rhvsotheceae," Bull. Torrey Botan. Club, 34: 387-416, 1907. VI. "Notes on miscellaneous species," My col., 6: 192-210, 1914. Wolf, F. A., L. F. Dixon, Ruth AIcLean, and F. R. Darkis, "Downy mil- dew of tobacco," Phytopathology, 24: 337-363, 1934. Wolf, F. A., Ruth A. McLean, J. A. Pinckard, F. R. Darkis, and P. M. Gross, "Volatile fungicides, benzol, and related compounds, and the principles involved in their use," Phytopathology, 50:213-227, 1940. iMUCORALES The Mucorales, commonly called "black molds," comprise about 30 genera and 450 species. They are mostly saprophytic on plant or animal tissues. Although a few species are pathogenic, others are of considerable importance in the decay of fruits and vegetables, and several are utilized in industrial processes. Absidia corymbifera is associated with human bronchomycosis, A. cor- nealis with lesions of the cornea, and Aiortierella niveo-velutina with inflamed, intensely prurient, papular skin lesions; Rhizopiis nigricajis produces a destructive decay of sweet potatoes that have not been properly cured before being placed in storage. These mentioned species and a number of other Mucorales are pathogenic to laboratory animals. Choanephora ciiciirbharinn is widely parasitic on squash flowers and fruits and also on cow- pea. Rhizopiis oryzae and Ahicor javaniciis saccharify starch and can be used in alcoholic fermentation. Several species of Rhizo- pus are employed in lactic fermentation. Aiortierella bainieri, Fiptocephalis freseniana, Dlspira cormita, and Farasitella (Aliicor) simplex are parasitic on other Mucorales. Their parasitism is generally regarded as restricted to other Mucorales, but Dobbs (1942) reported that a species of Fiptocephalis, near P. tieg- hemiana, is parasitic on Fenicilliinn notatiim, P. roqiieforti, P. glabrum, P. pfefferiamim, and Aspergillus mger, as well as Ahicor miicedo and Al. hiemalis. Species of Pilobolus are coprophilous. MUCORALES 111 s «*» o •4^ £*■ s o 4-1 o N c o CL, O 4-> bX) u Vi (U 3 (U ^ P 3 o t-i ta 4-> •^ C/^ « ft u "rt U 3 4-1 OJ U > o -O s-" c -^ o • 1-H O -^ C/2 E bx) o o c p-^ u •- JZ "^^ t? u a C rt J-( •-; a O != Oh C- C C O t/2 O bo r- O c - S J-^ c 'c S • ^H ^ "^ fl^ ^ O _. U ct or iz; C3 C3 t^ Ui U g 3 t;i f^ t ^ K ^ f— "^ == -5 53 ^ rsi '- •?; J^ — « r^ ^v . — 4— ' ~~^ , ,^3 o > hi U '' >. a o' ?: bo 't- ^^ S-i ;/s ^ - 2 n tlH . 148 THE ASCOMYCETES a few species. Haustoria are lacking. Sadebeck (1893) placed in Magnusiella those species having intracellular hyphae. Reproduction. Reproduction among Taphrinaceae is accom- plished bv the formation of a palisade-like layer of asci that arise as terminations of the internal mycelium. Before ascus formation a compact mycelial layer, one cell thick, is formed subcuticularly in most species. In Taphr'wopsis laiirencia the ascus-bearing layer develops within the epidermal cells. All the cells of this layer are binucleate. As they elongate, the nuclei fuse, after which, in most species, a short stalk is cut off at the base of the ascus. In Taphrhm carnea stalk cells are not formed [Juel (1921)], but the cell containing the fused nucleus becomes the ascus. Juel (1921) states that the basal cell nucleus migrates into the cell that is to become the ascus before the cross wall is formed. In T. coryli [Martin (1924)] the fusion nucleus divides reductionally; as a result, the nucleus of the stalk cell and that of the ascus contain n chromosomes. The nucleus in the stalk cell soon degenerates, but that in the ascus divides and redivides to form eight daughter nuclei. Eight ascospores are then formed. In Taphina de- joinmvs the ascospores on discharge germinate by yeast-like bud- ding [Martin (1925), Mix (1924)], but in certain other species, such as T. johansonii, budding takes place while the spores are still confined within the ascus. , Circumstantial evidence has long indicated that the ascospores of T. dejoTJiians or the conidia formed by budding lodge be- tween the bud scales and overwinter there. The fact that peach- leaf curl can be very successfully eliminated by the application of a dormant spray [Pierce (1900)] constitutes evidence of how this organism hibernates. In fact, the discovery of lime-sulphur sprays was made as the result of drenching peach trees with lime- sulphur solutions used as sheep dip. The trees adjacent to vats were covered \\ith dip ^\•hile the solution was being changed in the vats. As a consequence trees that were drenched remained leaf -curl free. More direct evidence of hibernation of spores on peach buds was secured by Mix (1924) as the result of bagging and of inoculation experiments. In regard to the origin of the binucleate condition of the hyphal cells Martin (1940) states that in T. dejorvians, when the ascospores, buds, or thick-walled spores from culture germinate CLASSIFICATION 149 to form hyphae, two nuclei arise bv mitosis and pass into the germ tube, and that all subsequent divisions are conjugate. If the spores bud to form secondary spores, however, the cells re- main uninucleate whether the cultures originate from monosporic or polysporic cultures. Wieben (1927) reported that buds con- jugate in cultures of T. epiphylla and T. klebahni, thus resulting in paired nuclei. Wieben (1927) showed that infection of the host is possible by T. epiphylla and T. klebahni only if the penetration tube arises from tw^o spores that have fused. Fitzpatrick (1934), however, found that a single spore of T. deformans can cause infection. These divergent results may be interpreted to indicate that some species of Taphrina are homothallic, others heterothallic. Artificial cultivation. Among the older mycologists to re- port growth by budding in liquid media are Brefeld and Sade- beck (1893). Pierce (1900) grew T. dejormmis on malt extract, beer, and various sugar solutions. Klebahn (1923) grew T. tosqiimetii, T. epiphylla, T. sadebeckii, and T. aiirea on agar fortified with salep. Mix (1924) grew T. defonnans on agar media containing decoctions of potatoes, carrots, corn meal, rice, or beets, and also on those containing the common carbohydrates. Martin (1940) also grew this leaf -curl fungus on a variety of media. On these artificial media the fungus growls in veast-like fashion, and some of the cells in old cultures become thick-walled (chlamydospores). Mix (1924) kept T. deforma?is in culture for 22 months without loss of its virulence. Classification. There are no comprehensive recent treatises on the taxonomy and classification of the Taphrinaceae. Sade- beck (1893) placed in Exoascus those species with a subcuticular ascogenous layer and perennial mycelium, and in Taphrina those whose mycelium is annual but which are otherwise like Exoas- cus. In Magnusiella he placed those whose asci arise from inter- cellular mycelium without the formation of a subcuticular layer. Giesenhagen (1895) distinguished four types on the basis of the shape of the ascus: (a) filicina type, with slender cylindrical asci; (b) betulae type, with plump cylindrical asci; (c) pruni type, with long clavate asci; and (d) magnusiella t>^pe, with large globular, oval, or saccate asci. Since asci in which the spores bud profusely change shape, good morphologic features to distinguish 150 THE ASCOMYCETES gencm are lacking. Perhaps all may as well be regarded as Taphrina, ^\■ith host relationship as the basis for specific sepa- rations. LITERATURE CITED FiTZPATRicK, R. E., "The life history and parasitism of Taphrina deforrnans,'' Sci. Agr., 14: 305-326, 1934. GiESENHAGEN, K., "Die Entwicklungsreihen der parasitischen Exoasceen," Flora, 81:267-361, 1895. Ju£L, H. O., "Cytologische Pilzstudicn. II. Zur Kenntnis einiger Hemi- asceen," Ncrca Acta Regiae Soc. Sci. Upsaliensis, IV, S: 1-43, 1921. Klebahn, H., ''Infektionsversuche mit Taphrijia tosquinetii,^'' Ber. dent. botan. Ges., ^7:108-113, 1923. .Martin, Ella M., "Studies on the morphology and cytology of Taphrina coryli Nishida," Trans. Wis. Acad. Sci., 2i: 345-356, 1924. "Cultural and morphological studies of some species of Taphrina," Phytopathology, 15:61-16, 1925. "The morphology and cytology of Taphrina defor?77a77s,^'' Am. J. Botany, 27:743-751, 1940. Mix, a. J., "Biological and cultural studies of Exoasciis deformans,^'' Phy- topathology, 14:211-233, 1924. Pierce, N. B., "Peach-leaf curl. Its nature and treatment," U. S. Dept. Agr., Div. Veg. Physiol. Path., Bull. 20: 11-204, 1900. Sadebeck, R., "Die parasitischen Exoasceen, eine Monographic," Jahrb. Hamburg iviss. Anst., 10: 5-110, 1893. Wiebex, Magdalene, "Die Infektion, die Myceluber\yinterung, und die Kopulation bei Exoasceen," Forsch. Gebiete Pfianzenk. limmmi. Pflanz- enr., 3: 139-176, 1927. EUASCOMYCETES For convenience the Euascomycetes may be arbitrarily sub- divided into the Plectomycetes, Pyrenomycetes, and Discomy- cetes. The Plectomycetes include those in which the asci are irregularly arranged within a closed ascocarp or cleistothecium; the Pyrenomycetes, those with asci reg^ularly arranged within an ostiolate ascocarp or perithecium; and the Discomycetes, those with asci regularly arranged within a widely opened or discoid ascocarp or apothecium. Groups of Ascomycetes occur, to be sure, that are intermediate between these arbitrary groupings or that are in some respects aberrant. The fact that such groupings are arbitrary becomes all too apparent when an attempt is made to locate in keys certain of the Perisporiales, some of which are said to be ostiolate; the r EUASCOMYCETES 151 152 THE ASCOMVCETES Myriangiales, which are stromatic but some of ^\•hich have asci borne at different levels, and others asci all borne at the same level; and the Hemisphaeriales, Laboulbeniales, and Tuberales, each of which contains a miscellaneous aggregation. The student eventually comes to recognize ^\■hether his unknown species oc- curs in these orders and meantime becomes further convinced that present-day keys are not necessarily based on natural affini- ties. Proper classification of Ascomycetes would seem to require that more detailed research be performed on the origin and de- velopmental anatomy of ascocarps and the origin of stromatic locules, paraphyses, and periphyses. It may well be that more significance should be attached to whether the paraphyses {a) arise from the floor of the locule and remain free above, (b) arise from the ceiling of the locule and remain pendant, or (c) are attached at each end. Plectomycetes EiiTotiales This group includes the Order Eurotiales, also called the Asper- gillales and Plectascales, an assemblage of approximately 800 species. They are arranged in 5 or more families, including the Gymnoascaceae, Aspergillaceae, Onygenaceae, Elaphomyceta- ceae, and Terfeziaceae. Gymnoascaceae The Gymnoascaceae are primitive fungi, many of which grow saprophytically on dung, feathers, dead grass, puparia of moths, leather, paper, and garbage. Others are important pathogens of men and animals, if the dermatophytes, or Trichophytoneae, are imperfect forms of Gymnoascaceae, as some mycologists be- lieve. Evidence that Achorion gypseum, causing favus, pos- sesses a Gymnoascus stage was presented by Nannizzi (1927). These findings, however, remain unconfirmed. Eidajitella spinosa is associated with skin lesions in dogs. Cteno77jyces serratiis oc- curs on decaying chicken feathers. Its spiral hyphae, aleuro- GYMNOASCACEAE 153 spores, and pectinate h\ phae very closely resemble those of der- matophytes. Gyvinoascus reesii has been collected on badly de- composed twigs. The developmental cycle of members of this family is typified by that of Amaiiroascus vernicosiis, occurring on soil and dung, Fig. 51. Amaiiroascus z'errncostts. (After Dangeard.) A. Antheridium and ascogonium by which the binucleate condition is initiated. B. Hyphal segment. C. Ascospore. D. Segment of ascocarp, showing stages of ascus formation. The asci are enveloped within a loose tangle of hyphae. which forms a profuse arachnoid covering over the substrate. According to Dangeard (1907), pairs of erect branches coil around each other, one an antheridium, the other an ascoeonium. Nuclear fusions have not been observed, but the ascoffones con- tinue to grow, become branched, and eventually are segmented into binucleate cells. These cells become enlarged and finally are the eight-spored asci. Meanwhile a loose, hyphal tangle en- velops the asci and ascogenous hyphae. This loose envelope con- stitutes the peridium, the forerunner of the compact-walled rind of higher cleistocarpous forms. A quite similar course of devel- opment takes place in Gyvinoascus reesii^ G. setosus, and G. candidiis, according to Dale (1903). 154 THE ASCOMYCETES Aspergillaceae Everyone M'ho has attempted to gro^^• organisms on artificial media has encountered x\spergillus and PeniciUium, both of which genera are cosmopolitan. Many members of each are adapted, by virtue of their enzyme-producing ability, to gro\\' on a va- riety of substrata. Aspergillus. Aspergillus is usually encountered as a conidial fungus. The conidial apparatus consists of globose or elliptical heads borne singly on erect stalks. The heads are covered with radiately arranged bottle-shaped sterigmata that bear conidia in chains. If the sterigmata are branched, the species are considered by some workers to belong to Sterigmatocvstis. In a few species the cleistothecial stage has been observed. This stage w^as first described as belonging to Eurotium, before the connection with the conidial stage had been established, and de Bary proved that E. herbarionnn and Aspergillus glaiiciis are genetically connected. Aspergillus herbarionnn, common on bread, forms its cleisto- thecia on this substrate. Zikes (1922) secured these structures from A. oryzae in gelatin cultures enriched with 1% asparagine, 0.5% K2HPO4, 0.25% MgS04, and 7.5% sucrose. Members of the A. niditlans group commonly form cleistothecia. Sexual reproduction. The essential features of cleistothecial formation were long ago observed by de Bary (1854) and were verified by Eraser and Chambers (1907) and Dale (1909). In Aspergillus repens and A. herbarionnn the ascogonium develops as a hyphal branch. It becomes septate, the terminal portion be- ing the trichogyne, and each cell is multinucleate. At the same time a multinucleate antheridium, formed on another branch, winds spirally around the ascogonium. The antheridium may fuse with the trichogyne and become paired, with an antheridial and an ascogonial nucleus in each pair. If fusion does not occur, the ascogonial nuclei become paired. In any event ascogenous hyphae grow out from the ascogonium and eventually bear ir- regular clusters of asci. Dangeard (1907) found no antheridium in A. flavus and A. fischeri. In these species the cells of the ascogonium become binucleate, and pairs of nuclei migrate into the ascogenous hyphae as they form. Classification. Classification of species of Aspergillus is diffi- PENICILLIUM 15$ cult. Thorn and Church (1926) divided them into the following groups: (a) A. glaiiciis group, {b) A. nidiilans group, {c) A. jimiigants group, {d) A. niger group, {e) A. flavus-oryzae group, (/) A. clavatiis group, (g) A. oclyraceiis group, {h) A. njcentii group, (i) A, flavipes group, and (j) A. versicolor group. Color ■>■. L- .' -' •" • ' ' "- ■•'■•■•••■ ■■■'■■•^'■rr--:i^,^; ■..,■■ ■■'■■■• I ■ ^.^v^;- ■■ -Q y ■(- V'V < *• .:•.••.< •;■••• ^: - .•#.••.'•>■•■•:• ':r♦•!?; Fig. 52. Aspergillus repens. A. Segment of multinucleate hypha. B. Sec- tional view of conidiophore, which is multinucleate throughout. C. Asco- spore in optical section, which is also multinucleate and has thick verrucose wall. D. Section of young sclerotium showing ascogonial coil. E. Same section as D in surface view. F. Ascus. {A and C after Dale, B after Fraser and Chambers, others after de Bary.) of Stalks and heads, shape of heads, shape of conidia, smoothness or roughness of stalks, and one or two series of sterigmata con- stitute the features employed in separating these groups. In a recent account [Thom and Raper (1945)] the genus is divided into 14 groups, and the synonymy of all valid species is recorded. Important species and their activities. Aspergillus niger is as- sociated with a rot of pomegranates [iMacAIurran (1912)] and of figs [Hodgson (1918)1 and dates. It also causes decay of stored tobaccos and cigars. Aspergillus glaitcm, A. flavtis, A. oryzae, and A. ■iventii are all associated with the spoilage of walnuts, Fig. 53. Ascospores of different species of Aspergillus. A. A. mdidans. B. A. qiiadrilineatus. C. A. nigulosiis. D. A. variitecolor. (Courtesy K. B. Raper.) 156 PENICILLIUM 151 pecans, Brazil nuts, and chestnuts. Aspergillus glaitciis occurs on stale bread and on gloves, shoes, or soiled clothes that are stored under conditions of high relative humidity. Aspergillus oryzae is utilized in the saccharification of rice starch in making alcohol. It is also used, as is ^. niger, in commercial production of citric acid and other organic acids. Aspergillus jinuigatiis, A. flavus, A. niger, and A. nidiilans occur within the human ear, causing otomycosis. Aspergillus jinnigatiis causes involvement of the lungs of persons occupied as hair combers or feather dress- ers or employed in force-feeding fowls or preparing furs for clothing. The same organism causes pneumonic symptoms in canaries, grouse, and other birds, appearing at times in epidemic proportions. Penicillium. There are about 600 named species of Penicil- lium, many of which are synonymous. Thom (1930) would re- duce the number of species to less than 200. These organisms are commonly known as "blue mold" or "green mold" and are universally present on decaying organic matter. The conidio- phores have the appearance of tiny brooms, with chains of conidia as the tips of the brooms. The branches of the broom divide and redivide several times and terminate in verticels of sterigmata. The sterigmata, because of their bottle-shape, are termed phialides. The conidia adhere in long chains, sometimes of 100 or more elements. Sexual reproduction. Bref eld's (1874) account of ascocarpic development in Penicillium, presumably P. glauciim, has been verified in essential details by subsequent investigations. Pairs of short hyphae spirally coiled about each other are the antheridia and ascogonia. These are invested by yellowish sclerotia con- stituted of three or four layers of cells. Three kinds of hyphal elements make up the sclerotial interior: (1) large septate hy- phae, the ascogonia; (2) ascogenous hyphae with short lateral branches originating from the ascogonia; and (3) very slender hyphae that Brefeld thought functioned to nourish the asci. Dodge (1933) observed these hyphal types in P. brejeldianiim but found that asci may also arise from the tips of the slender hyphae. The cells of the ascogenous hyphae swell to become asci, and for this reason the asci have the appearance of being in monilioid chains. In mounts made by crushing cleistothecia, ag- gregates of asci may be readily obtained. 158 THE ASCOMYCETES Although cleistothecial formation is not known to occur gen- erallv among species of Penicillium, it is of rather common oc- currence in certain ones, notably P. avellaneinn, P. spiciilisponmi, P. liiteiim, P. glaiiciim, P. brejeldianimi, and P. javaniciim. Fig. 54. Development of Penicillium. A, B, and C. Conidiophores and conidia of P. roqueforti. D, E, F, and G. P. criistacenm. (Adapted from Brefeld.) D. Coiled antheridial and ascogonial hyphae. E. Ascospores. F. Cleistothecium in surface view. G. Clusters of asci. Classification. The treatises by Thorn (1910, 1930) bring tos^ether for the svstematist means for identification of this diffi- cult group of species. He treats Penicillium as a form genus, for the reason that so few species are known to possess a perfect stage. The nature of the colonies (whether, for example, they are velvety, compact, or arachnoid), the type of branching of conidiophores, the production of sclerotia, the degree of spread- ing or compactness of the penicillus, and the color of conidia PENICILLIUM 159 en masse, are among the characteristics employed in separating the assemblage into groups of species. hnportant species and their activities. Fenicilliiim expanswn is responsible for a great deal of the spoilage of apples, pears, and grapes in storage. Two species of Penicillium, P. italicum, a Fig. 55. A and B. Stages in endoconidial formation by Thielaviopsis bast- cola. C. Chlamydospores of T. basicola. (After Brierley.) D. Cleisto- thecium of Thielavia basicola. E. Ascospores. F. Ascus. blue-green mold, and P. digitatiim, an olive-green mold, occur on citrus fruits in storage. Fenicilliinn piirpiirogemmt spots priat paper, books, and engravings. Textile fibers, paper pulp, and lumber are stained and discolored, and consequently lowered in market value, by species of Penicillium. Frequently P. criista- ceum has been isolated in chronic pulmonary disorders in man, but its etiolomc role in human disease has not been established. By hydrolyzing the butter fats which produce such volatile acids as caproic, acetic, butyric, and capric, P. roqiieforti imparts to cheese a piquant flavor. FeiiicilUimi camemberti flavors camem- bert cheese by means of the products of hydrolysis of casein. 160 THE ASCOMYCETFS Venicilliinn iiotatiiTn is used in the preparation of the best-known antibiotic, peniciUin. Thielavia. The several species of Thielavia appear to be closely related to Aspergillus and Penicillium. The best-known member is T. basicola, considered by Gilbert (1909) and others the cause of black-root rot of tobacco and various leguminous plants. iMcCormick (1925) presented evidence, however, that T. basicola is not genetically connected with a conidium- and chlamydospore-producing fungus, Thielaviopsis basicola, with which it is associated in nature. This genetic relationship, or lack of it, might well be given further consideration. The development of ascocarps in Thielavia terricola and T. sepedojiium was studied by Emmons (1932). Cultures from single spores give rise to ascocarps, which begin as hyphal coils. The distal ends of these hyphae recurve, and cross walls are laid down. The tip or ultimate cell of each is just beyond the one that makes up the crook or crosier. This crosier is therefore penultimate. Each cell of the ascogenous hypha is uninucleate except the penultimate one, which has two nuclei. Such binu- cleate cells enlarge, and each becomes an ascus. During this process there is first a fusion of the two nuclei, f ollow^ed by three nuclear divisions, and the cutting out of ascospores. The production of so-called "endoconidia" w^as studied by Brierley (1915). He found that the first conidia are formed endogenously, but that the tip of the conidiophore bursts to lib- erate these conidia. The conidium-producing cell is therefore endogenous and produces chains of conidia. Onygenaceae One genus, Onygena, with 6 species comprises this family. Its habitat is hair, hoofs, fur, feathers, horns, claw s, and other animal materials. The ascocarps of 4 species are stalked and capitate. A powdery coating of gemmae may cover the young heads. When they are mature, sterile hairs occur, interspersed with the asci, which disintegrate. The heads open irregularly, so that the ascocarps look like tiny puffballs or else like sporangia of slime molds. Little is known about the developmental history of Ony- gena beyond the information contributed long ago by Ward (1899). TERFEZIACEAE 161 Elaphomy cetaceae Dodge (1929) states that 2 genera containing about 30 species comprise thiis family. The yellow to brown ascocarps are hypo- geal, resembling truffles, although the asci are scattered or clus- tered in nests rather than in layers, as thev are in truffles. The peridium is thick and verrucose, and at maturity a powdery mass of spores fills the interior. Fig. 56. Elaphomyces cervinus. A. Surface view of ascocarp. B. Ascocarp in section. The veins are covered with asci. C. Spherical ascus with thick- walled ascospores. (After Rees and Fisch.) Some species of Elaphomyces, notably E. cervinus and E. granulatus, are known to be mycorrhizal and are associated with the roots of pines, oaks, and beeches. The ascocarps of several are parasitized by species of Cordvceps. In fact, species of Ela- phomyces are found only by accident, unless the clavae of the Cordyceps parasitizing them come to the surface of the ground. Terfeziaceae The Terfeziaceae are subterranean fungi, presumably my- corrhizal and apparently Hmited in range to the Mediterranean region. Their peridium is a thin layer, much narrower than that of the Elaphomycetaceae. The spore mass is not powdery at maturity. According to Lindau, there are eight genera, but many of the species included in them have been found to be truffles and accordingly have been transferred to the Tuberales. 162 THE ASCOMYCETES LITERATURE CITED Bary, Anton de, "Uber die Entwickelung und den Zusammenhang von Aspergillus glaiiciis und Eurotium," Bot. Zeit., 12:A1S-M>^, 465-471, 1854. Brefeld, O., "Die Entwickelungsgeschichte von Penicillium," Botan. Unter- siich. Schmmielpilze, 2: 1-98, 1874. Brierley, W. B., "The 'endoconidia' of Tbielavia basic ola Zopf," Ann. Botany, 25': 483-493, 1915. Dale, E., "Observations on the Gymnoascaceae," Ann. Botany, 17:571-596, 1903. "On the morphology and cytology of Aspergilhis re pens de Bary," Ann. My col, 7:215-225, 1909. ' Dangeard, p. a., "L'origine du perithece chez les Ascomycetes," Botaniste, 10: 1-385, 1907. Dodge, B. O., "The perithecium and ascus of Penicillium," MycoL, 25:90- 104, 1933. Dodge, C. W., "The higher Plectascales," Ann. MycoL, 27: 145-184, 1929. Emmons, C. W., "The development of the ascocarp in two species of Thielavia," Bull. Torrey Botan. Club, 5i>: 415-422, 1932. Eraser, H. C. I., and H. S. Chambers, "The morphology of Aspergillus berbariorum,'''' Ann. MycoL, 5:419-431, 1907. Gilbert, W. W., "The root rot of tobacco caused by Tbielavia basicola (B. and Br.) Zopf," U. S. Dept. Agr., Bur. Plant Industry Bull., 158. 55 pp. 1909. Hodgson, R. W., "A Sterigmatocystis smut of figs," Pbytopatbology, 8: 545-546, 1918. MacMurran, S. M., "A new internal rot of pomegranate," Phytopathology, 2: 125-126, 1912. McCoRMicK, Florence A., "Perithecia of Tbielavia basicola Zopf in culture and the stimulation of their production by extracts from other fungi," Conn. Agr. Exp. Sta. Bull., 269: 539-544, 1925. Nannizzi, a., "Richerche suU'origine saprofitica dei funghi delle tigne. II. Gymnoascus gypsetim, sp. n., forma ascofora del Sabouraudites {Acborion) gypseum (Bodin) Ota et Langeron," Atti accad. fisiocritici Siena, X, 2:89-97, 1927. Thom, Charles, "Cultural studies of species of Penicillium," U. S. Dept. Agr., Bur. Aiiimal Ind. Bull., 118. 109 pp. 1910. The Penicillia. xi + 644 pp. Williams and Wilkins Co. 1930. Thom, Charles, and M. B. Church, The Aspergilli. ix + 272 pp. Williams and Wilkins Co. 1926. Thom, Charles, and K. B. Raper, Manual of the Aspergilli. 373 pp. Wil- liams and Wilkins Co. 1945. Ward, H. M., ''Onygena equina Willd., a horn-destroying fungus," Phil. Tram. Roy. Soc. London, B, 191:269-291, 1899. ZiKES, H., "Uber die Perithecienbildung bej Aspergillus oryzae," Zentr. Bakt. II Abt., 55:339-343, 1922. MYRIANGIALES 163 Myriangiales The Alyriangiales are stromatic angiocarpous fungi. The stromata are cushion-shaped in many of them, and the asci are borne irregularly dispersed, either singly or in layers within chambers or locules. Many of these fungi occur on leaves, fruits, and bark, and some are parasitic upon insects, especially in the tropics. Relatively few species have been thoroughly studied; hence mycologists are not in accord on which species properly belong in the Alyriangiales. Speculations concerning relationships to other orders and to phylogeny are believed to be quite futile because of this lack of kno^\•ledge.. For the present purpose the following families are regarded as comprising the order: Alyr- iangiaceae, Elsinoeaceae, Saccardiaceae, Dothioraceae, and Pseudosphaeriaceae. These may be separated as follows: 1. Asci arising at different levels 2. Stroma massive, of homogeneous texture, without a rind Alyriangiaceae 2. Stroma effuse, interior gelatinous, exterior crustose Elsinoeaceae 1. Asci arising at one level 3 3. Stroma naked Saccardiaceae 3. Stroma with crustose rind 4 4. Multiloculate Dothioraceae 4. Uniloculate or perithecium-like Pseudosphaeriaceae AIyriangiaceae. a recent study by Aliller (1938) on the morphology and cytology of Alyriangium diiriaei and M. ciirtisii provides the basis for an understanding of this family. Both of these species occur as parasites on scale insects that attack Nyssa syhatica, Carya illiiweusis, and other broad-leaved trees in the southeastern United States. Both species of Alyriangium possess cushion-like stromata, from the upper surface of which extend aggregates of black cupules. The interior of the cupules consists of thin-walled fungus parenchyma, in which asci are dispersed, one ascus in each locule. As the interascal tissues are weathered away, the asci become exposed, and spores are liberated. Young ascocarps contain multicellular, coiled ascogones that extend to the surface of the stromata. From the archicarps numerous ascogenous hyphae arise and bud off binucleate cells that are to become asci. In Myrianghnn diiriaei there is a single 164 THE ASCOMYCETES bo n3 c • t-H t/5 O 4-> c u c U O 4-> ^ • -H rs U CU ly) '% fcw ^ ''V c ..J j: "3? 3 o. ^ u Oh « U C (J C o J2 o in ir ^ CJ G 1 r-" OS »— ' ^ u rk <-M c « -a U M c X3 ^ o c C/2 r^ CO G ^-^ 3 O rt U M o t/2 VM J^ a Ul n3 4-> 0-, 3 rt CQ c C/5 Q cq c TS U CO 3 G o u U c/3 3 C/3 rt rt o <■!-( k-( • C 3 CO 4-1 . >% X! s Ul U 'ts rt >Jk "3 ?5 Si « 4-> • *** M-i 5^ o ?S c« u I— fa ^ ELSINOEACEAE 165 archicarp in each of the thirty to fifty cupules on each stroma, whereas in M. ciirtisii there are many in each archicarp. Miller (1938) is uncertain whether antheridia are associated with the coiled ascogones. Fig. 58. Pyrenophora tritici-repejitis. A. Perithecium in surface view, im- mersed within tissues of wheat leaf. B. Mature ascus. C. Conidium of the Helminthosporium stage. D. Germinating ascospore. E. Germinating conidium. F. Conidiophores extending from the surface of leaf of wheat. They may emerge through the stomata. (Adapted from Drechsler.) The morphological characteristics presented by the Myrian- giaceae indicate that they should be placed close to the Aspergil- lales. Elsixoeaceae. This family, also called Plectodiscellaceae, con- tains several very important plant pathogens. Woroninchin 166 THE ASCOMYCETES o rt u *—• Vi < Ui O u-, 09 . "rt ^3 ^6 r" u c 5 ^3 £ Q Cu X • «-^ cJ C/3 bo 3 t/; V3 ''^ rt rt r^ £ 2 'on CJ "-* c: 'U rt r- -^ r^ CQ u r- ^ o r-' C C ^ 4-' o r- .M J= o CLh u t-( rt ol 4-* n3 o y; ^ r; ^^ ' ^^ •T^. V3 s-> . (U 'S rt •■^H 3 o 3 u u r- ^ <-l-l \^ o o o c rt u o E CD *-> o , .£ t-i 4-1 U t/2 U-i • a C o C '■u • c 1^ t-> ^M (J (U ^- • W5 S Uh ^^ 3 4-1 rt _y c 3 O T^ *^H S c • ^ o ^ 4-» • — i ns 1 ■Ki 4-> ?> >% ^ Ci u s O MH ~-» (il >. rt • C CN •^ Ui 6 O fa a, CO DOTHIORACEAE 161 (1914) established the Plectodiscellaceae, using as the type Flec- todiscella piri, which causes a leaf spot of apple and pear in the Caucasus. Three years later Burkholder (1917, 1917a) described the ascogenous stage of the raspberry anthracnose pathogen, designating it Plectodiscella veiieta, which had previously been known in its conidial aspect as Gloeosporhnn venetinn. Burk- holder showed that monascous locules occur in the stromata which form within the decaying tissues. These stromata become erumpent at maturity and the asci are freed by the wearing away of overlyinsf stromatic tissues, which readily become gelatinous. In 1932 Jenkins (1932) pointed out that the genus Plectodi- scella is synonymous with Elsinoe, previously established, and for this reason she changed the name of Woroninchin's Plecto- discella pin to Elsinoe piri. She also established that the conid- ial stages of species of Elsinoe belong to Sphaceloma and not to Gloeosporium, Cladosporium, and other form genera to which they had been assigned. As a result of these findings, Jenkins turned to a critical examination of various related species. She found that the "scab" of Fhaseoliis hinatiis hova Cuba is caused by Elsinoe canavaliae [Jenkins (1931)] and is identical with an organism attacking species of Canavalia in Java, Ceylon, the Malay Peninsula, and the Philippines. Avocado scab is caused by Sphaceloma perseae [Jenkins (1935)]. The scab disease of lemons, sour oranges, and certain other citrus fruits [Bitancourt and Jenkins (1936)] occurring throughout all citrus-growing regions, is induced by Elsinoe fanjccetti {Cladosporium citri), whereas that of sweet orange is caused by E. aiistralis [Bitancourt and Jenkins (1937)]. Although the type of angiocarpous development in the Elsi- noeaceae apparently is quite like that in the iVIyriangiaceae, cyto- logic details are still lacking^, and nothingr is known of their sexuality. DoTHiORACEAE. The structure of members of this family, in- cluding Dothiora, Bagnisiella, Bagnisiopsis, and Botryosphaeria, was established by Theissen (1916) largely from a study of Botryosphaeria. He found wide structural variation in this genus. In B. ijjflata the locules are scattered throughout the stromatic tissue. In B. mascarensis they are seated upon the surface of the stroma at maturity. In B. ribis the locules are left standing on stipes, and each one is perithecium-like. 168 THE ASCOMYCETES B Fig. 60. Botryosphaeria ribis. A. Young ascus containing the primary ascus nucleus. B. Binucleate ascus. C. Ascus in the four-nucleate stage. D. Ascus containing eight free nuclei. E. Eight uninucleate ascospores have been delimited. F. Uninucleate and binucleate ascospore. G. Mature ascus with multinucleate ascospores. H and /. The uninucleate cells from the inner pycnidial wall of the Dothiorella stage function as conidiophores. Various stages in the formation and abstriction of multinucleate conidia are shown. /, K, and L. Stages in multinucleate condition of ascospores. PSEUDOSPHAERIACEAE 169 Botryosphaeria ribis, first described as the cause of currant- cane blight, is now known to parasitize the stems of over 50 species of woody plants. Its pycnidial stage, Macrophoma, ap- pears on recently formed lesions. Accompanying the pycnidia is another stage, Dothiorella, bearing minute spores in stromatic locules. These microconidia are beheved to be spermatia [Wolf Fig. 61. Stroma in section showing pycnidium of Dothiorella stage of Botryosphaeria ribis with conidiophoral cells and conidia. and Wolf (1939)]. Perithecial locules are initiated at the same time that spermatia are being produced. This fungus produces multinucleate conidia and multinucleate ascospores [Wolf and Wolf (1939)], a condition like that described years ago for Aspergillus repens by de Bary. IPsEUDOSPHAERiACEAE. The Pseudosphaeriaceac comprise or- ganisms that have until recently been regarded as Sphaeriales. Interthecal tissues remain, however, after the asci have matured. These tissues are compressed as the asci enlarge and have been designated pseudoparaphyses. Their stromata are spatially sepa- rated, that is, are not fused, and are therefore perithecium-like in appearance. no THE ASCOMYCETES Included in the Pseudosphaeriaceae are such genera as Pleo- spora, having approximately 300 species, Didymella, having over 200 species, ^Leptosphaeria, having over 500 species, and Pyre- FiG. 62. Section of stroma of Botryosphaeria ribis, showing a perithecial locule with asci and paraphyses. nophora. Most of them are saprophytic on plants. Some species of Pleospora have been shown to possess conidia belonging to Alternaria and iMacrosporium, in both of which imperfect genera are many plant pathogens. Various grasses are parasitized by ERYSIPHALES 111 species of Helminthosporium, several of \\hich, as Drechsler (1923) established, are genetically related to Pyrenophora. LITERATURE CITED BiTANcouRT, A. A., AND A. E. Jenkins, ''Elsiuoe fcTivcetti, the perfect stage of the citrus-scab fungus," Phytopathology, 26: 393-396, 1936. "Sweet-orange-fruit scab caused by Elsinoe mistralisj'^ J. Agr. Research, 5^:1-18, 1937. BuRKHOLDER, W. H., "The anthracnose disease of the raspberry and re- lated plants," Cornell Agr. Expt. Sta. Bull., 395: 157-183, 1917. "The perfect stage of Gloeosporhnn Venetian,''' Phytopathology, 7; 83-91, 1917a. Drechsler, C, "Some graminicolous species of Helminthosporium, I," /. Agr. Research, 2-/; 641-740, 1923. Jenkins, A. E., "Lima-bean scab caused by Elsinoe," /. Agr. Research, 42: 13-23, 1931. "Elsinoe on apple and pear," /. Agr. Research, 44: 6S9-7 00, 1932. ''''Sphaceloma perseae, the cause of avocado scab," /. Agr. Research, 49: 859-869, 1935. Miller, J. H., "Studies in the development of two Myriangium species and the systematic position of the Myriangiales," Mycol., 30: 158-181, 1938. Theissen, F., "Studien iiber Botryosphaeria," Ami. Mycol., 14: 297-340, 1916. Wolf, F. T., and F. A. Wolf, "A study of Botryosphaeria ribis on wil- low," Mycol, 31:1X1-111, 1939. Woroninchin, N. N., ^'Plectodiscella piri, der \^ertreter eines neuen Ascomyceten-Gruppe," Mycol. Centrb., ^; 225-233, 1914. Erysiphales Among the Erysiphales, also called the Perisporiales, are two important families: Erysiphaceae, or po\ydery milde\\s, and MeHolaceae (Perisporiaceae), or sooty molds. Essentially all are limited in habitat to the surface of green plants, and none appears to have been cultivated on artificial media. Their ascocarps are cleistothecia in which the asci are arranged in an orderly layer, rather than being dispersed as in the Eurotiales. Erysiphaceae. The powdery mildew^s, except Erysiphe graiiii- nis on various grasses, are limited in host range to dicotyledonous angiosperms. The monograph of Salmon (1900) lists 49 species and 11 varieties, occurring on about 1500 host species. Many of those listed in Saccardo's Sylloge Fiingorinn have been re- duced to synonymy by Salmon. Six genera, Erysiphe, Micro- 112 THE ASCOMYCETES sphaera, Podosphaera, Phvllactinia, Sphaerotheca, and Uncinula, are generally recognized. They are separated on the bases of type of cleistothecial appendages and number of asci within each cleistocarp. Fig. 63. Stages in the initiation of cleistocarps in Erysiphaceae. A to F, Sphaerotheca himnili. A. Antheridial and oogonial branches. B. Large oogonium and small antheridium at apex of antheridial branch. C. Migra- tion and association of nuclei of opposite sex; branches at base of oogonium starting to form envelope. D. A later stage in which oogonium is enclosed within wall. E. Oogonium has become a series of cells, the penultimate of which is to become an ascus; contains a pair of nuclei that will fuse. F. Young ascus containing fusion nucleus. Peripheral cells are nurse tissue. G. Section of young cleistocarp of Erysiphe polygoni. (Adapted from Harper.) The appendages are flexuous, unbranched hvphae in Erysiphe, Sphaerotheca, and Leveillula; they are unbranched but hooked or coiled at the tip in Uncinula, dichotomously branched at least at the tips in Microsphaera and Podosphaera, and needle-shaped with bulbous bases in Phvllactinia. Each cleistothecium of Podosphaera and Sphaerotheca contains only a single ascus. Mycelhmt and conidial stage. The name powdery mildew ap- propriately describes the white, mealy appearance of affected leaves, stems, flowers, and fruits, the whiteness being imparted ERYSIPHACEAE 173 by the profusion of external mycelium and conidia. The arach- noid mycelium, composed of uninucleate cells, with few excep- tions is external to the host tissues. The host cells are penetrated by haustoria, one or more entering each epidermal cell. In Uji- cimila salicis the penetrating tubes may also pass through the epi- dermal cells and form haustorial expansions within the cells of the mesophyll [Smith (1900)]. In most species the haustoria are bulbous and uninucleate. In Erysiphe graj/imis, however, and in certain other species of Erysiphe, notably E. galiopsidis and E. dehor acearimty they are ellipsoid, with digitate processes at the ends [Smith (1900)]. Some species of powdery mildews perennate as mycelium. Apple powdery mildews, caused by Podosphaera leucotricha and F. oxyacajithae, have been reported to hibernate between the bud scales [Ballard (1914)]. Similarly a series of observations has convinced the writers that the powdery-mildew fungus of crepe myrtle, Lagerstroemia indica, perhaps JJjicimda lagerstroemiae, overwinters as mycelium within the buds. Oidiopsis (Leveilhda) taiirica is of particular interest because its mycelium is wholly endophytic [Salmon (1906)]. This fungus is endemic to Asia Minor and northern Africa, occurring on many species of plants. This endophytic habit is believed to be an xerophytic adaptation. Its conidiophores emerge through the stomata. In like manner a portion of the mycelium of Fhyl- lactinia corylea occurs between the mesophyll of its numerous hosts. The conidial stage of most powdery mildews belongs to the form Genus Oidium. Special hyphal branches arise from the leaf surface, and near the tip of each a septum is formed. This apical cell becomes the first conidium in a chain of basipetally abstricted conidia. Each conidium is at first cylindrical, then becomes barrel-shaped, and finally, when ready for dissemina- tion, is elliptical. If moisture is provided, conidia germinate by formation of one or more germ tubes, and within 3 or 4 days new mycelium has grown to the extent of being capable of forming a crop of conidia. Cleistothecial stage. The origin of cleistocarps of powdery mildews was properly traced and their structure correctly de- scribed by de Bary as long ago as 1863. He employed Sphae- rotheca castagnei growing on dandelion and noted that at the 114 THE ASCOMYCETES point of contact of two hvphae a pair of erect branches arises. Each is separated from its parent hypha by a septum. One branch, the oogonium, becomes ellipsoidal; the other remains cylindrical and becomes closely applied to the oogonium, and a cell, the antheridium, is cut off at its apex. The walls at the Fig. 64. Structural features of Erysiphaceae. A. Bulbous haustorium, a type common among powdery mildews, in epidermal cell. B. Digitately branched haustorium of Erysiphe graminis. C and D. Conidiophore and conidia, the Oidium stage of powdery mildews. E. Types of dichoto- mously branched tips of appendages. F. Types of uncinate or hooked tips of appendages. G. Types of asci. H. Surface view of cleistocarp wall. /. Appendage with bulbous base as in Fhyllactinia corylea. ]. Flexuous appendage as among species of Erysiphe. {A and B adapted from Smith.) ERYSIPHACEAE US point of contact of the oogonium and antheridium open by a broad pore, after wliich the protoplasts intermingle. In Sphae- rotheca, bearingr a single ascus, there are two cells formed from the oogonial structure, the upper of which becomes the ascus and the lower skives rise to the nurse tissue and wall of the cleistocarp. Harper (1895, 1905) verified these observations of de Bary and contributed many additional cytologic facts in studies based on the same species and on Phyllactinia cor y lea and species of Erv- siphe. He traced the development of antheridia and oogonia, the fusion of nuclei, one from each ors^an, and the cytologic fea- tures that accompany nuclear division ^\•ithin the ascus and de- limitation of ascospores. The development in powdery mildews producing more than a single ascus differs mainly in that the oogonium becomes transformed into a row of cells. Each of these cells becomes an ascus or else gives rise to short branches (ascogenous hyphae), whose penultimate cells become asci. Certain mycologists, among them Eftimiu (1929), maintain that there is no migration of antheridial protoplast into the oogonium in powdery mildews. In Eftimiu's observations were included Erysiphe galeopsidis, E. tortilis. Uncimila chvidestiua, and Microsphaera herberidis.. Colson (1938) concluded that the cleistothecia of Phyllactmia corylea, growing on Cory his avel- lana, develop apogamously. The antheridial nucleus degenerates within the antheridium. The oog^onium becomes four-nucleate by division of its single nucleus. These four nuclei become separated by walls, with two nuclei in the middle cell. After further nuclear divisions the ascogenous hyphae grow out from this middle cell. By septation these hyphae become rows of bi- nucleate cells, the terminals being uninucleate. The asci then arise directly from these binucleate cells, nuclear fusion follows, and eventually several uninucleate ascospores are delimited within each ascus. Distribution of pou'dery viildeii's. Most of this group of fungi are known to occur in the North Temperate Zone, perhaps because more collectors of fungi live in this region. Approxi- mately one-third of all known species is confined to Europe, and one-third is common to both Europe and North America. Thir- teen species and 5 varieties of those listed by Salmon (1900) occur in North America. Phyllactinia corylea is essentially 116 THE ASCOMYCETES world-wide in range. Moreover Salmon (1900) lists it as having 140 hosts belonging to 36 families. Other widely dispersed species are Erysiphe polygoni^ having 355 hosts belonging to 42 families, and E. cichoraceariim, having 280 hosts belonging to 27 families [Reed (1913)]. On the other hand, Fodosphaera bi- iincmata is limited to \\'itch hazel, Hamamelis virgijiiana; and Un- cinula gemcidata, to red mulberry. Moms rubra. Uncimda cir- chiata is confined to maples. Infrequently, several species of mildews occur on a single host; on Ribes grossularia, for example, Sphaerotheca mors-uvae is most common, but Microsphaera grossidariae and Fhyllactinia corylea may also occur. liJiportant species and their activities. Since these fungi are all obhgate parasites, they can be expected to cause a great deal of damage if they appear on plants of economic importance. Among destructive pathogens are Uncimda necator on grape, known in Europe since 1847 as Oidium tuckeri. Its cleistothecial stage was not found there for over 40 years, hibernation being accomplished by means of special resistant mycehal cells. Cleis- tothecia are commonly developed, however, in California. Sphaerotheca mors-uvae is very destructive to gooseberries, S. humidi to hops [Blodgett (1913)], and 5. pannosa to roses, especially climbing varieties. Erysiphe graminis is widespread on oats, wheat, barley, rye, and bluegrass; E. polygoni is very prevalent on clovers but seldom, if ever, forms cleistothecia in the southeastern United States. Erysiphe cichoracearinn seriously attacks cucumbers and squashes, especially those grown in green- houses. Fodosphaera oxyacanthae is very damaging to cherries and may also attack apples and peaches, especially when the trees are grown in nursery io\ys. Meliolaceae. The Meliolaceae, or sooty molds, resemble the Erysiphaceae closely in structural features, but, as the common name implies, the mycelium is dark in color instead of being white. The hyphae may be so profuse as to form crusts. They may adhere to the epidermal cells so intimately as to absorb their food, may attach themselves by means of holdfasts, hyphopodia, or may send haustoria into the host tissues. Lasiobotrys is sub- cuticular. Stomatogene and Pihne form foot-like structures within the substomatal cavities. Sooty molds occur most abundantly in the tropics. Conidia are lacking in most species. Conidia of the Helminthosporium MELIOLACEAE 111 type are commonly associated with Meliola, but Stevens (1916) omitted them in his classification of approximately 100 Puerto Rican species of Meliola for the reason that he was uncertain of their genetic connection. Fig. 6S. Structural features of Meliola, a sooty mold. A. Young cleisto- thecium of Meliola circinajis at surface of Carex leaf, surface view. B. Vertical section of A enlarged, showing ascogenous hyphae filling center of stroma. C. Mature cleistocarp of Meliola corallina with basal hyphae and hvphopodia. D. Mature ascospore of M. circinans. E. Germinating ascospore of M. coralVma with hyphopodia on germ tube. {A, B, and D adapted from Graff, C and E from Gaillard.) The cleistothecia are unappendaged but may have setae or be partly invested with hyphae. They are usually coal-black. De- tails of their development are quite unknown. In Meliola circi- nans, however, Graff (1932) found that essentially the same proc- esses as in the Erysiphaceae lead to cleistocarp formation. Hy- 118 THE ASCOMYCETES phal branches that are in approximate contact bear oval oogonia and slender, somewhat spirally wound antheridia. Each organ is borne on a stalk cell, and each is uninucleate. After the opening of their adjoining tips, the antheridial protoplast passes into the oosfonium. The oojronium then elons^ates and divides into sev- eral uninucleate cells, \\hich send out ascogenous hvphae. After crosier formation asci are formed. In each ascus eiq;ht nuclei are produced, but onlv four ascospores are formed. The group has been rather extensively monographed. The studies of Stevens (1916, 1928) deal with Puerto Rican and Ha- waiian species, those of Doidge (1920) with South African species, and those of Fraser (1933, 1934, 1935, 1935a) with Aus- tralian species. Theissen and Sydow (1917) divide the family into 19 genera. Other Erysiphales. Two other families, Englerulaceae and Capnodiaceae, are included by Theissen and Sydow (1917) in this order. Both are sooty molds, the Englerulaceae containing about 30 species of parasites on tropical plants and the Capnodi- aceae 25 genera and hundreds of species that live mostly on excre- tions of aphids and scale insects. Among the best-known species is Capnodhnn citri, causing sooty mold of citrus. This fungus may be so profuse as to inter- fere with photosynthesis, and the fruits must be cleansed before beingr marketed. Scorias spongiosa occurs on beech twigs, making sponge-like masses several inches in diameter. They are carbonaceous and brittle when dry but pliable when moist, and can absorb and hold water quite like a sponge. Attention has been called to the occurrence of Adelopiis Qrawnavni on Doug-las fir in Switzerland and in the north- eastern United States [Boyce (1940)]. This capnodiaceous fungus is associated with a leaf-cast disease that may be so severe as to result in the death of affected trees. LITERATURE CITED Ballard, W. S., "Apple powdery mildew and its control in the Pajoro Valley," U. S. Dept. Agr., Bur. Plant hid. Bull., 120. 16 pp. 1914. Blodgett,'f. AI., "Hop mildew," Cornell Agr. Exp. Sta. Bull., 52^:281-310, 1913. PYRENOMYCETES 179 BoYCE, J. S., "A needle-cast of Douglas fir associated with Adelopus gaimi 072711,^^ Phytopathology, 30: 649-659, 1940. CoLsoN, Barbara, "The cytology and development of Phyllact'ma corylea Lev.," Ann. Botany, n.s., 2:381-401, 1938. DoiDcE, Ethel M.., "South African Perisporiaceae, III," Trans. Roy. Soc. South Africa, 8:235-282, 1920. Eftimiu, Panca, "Contribution a I'etude de revolution nucleaire chez cer- taines Erysiphacees," Bull. bot. soc. France, 16: 10-20, 1929. Eraser, Lillian, ''An investigation of the sooty moulds of New South Wales, I," Proc. Lmnean Soc. N. S. Wales', J^"; 375-395, 1933; II, )9: 123-142, 1934; III, 50:97-118, 1935; IV, 50:159-178, 1935a. Graff, P. W., "The morphological and cvtological development of Meliola circmans,^'' Bull. Torrey Botan. Club, JP: 241-266, 1932. Harper, R. A., "Die Entwickelung des Peritheciums bei Sphaerotheca castagnei," Ber. deutsch. botan. Ges., 75:475-481, 1895. "Sexual reproduction and the organization of the nucleus in certain mildews," Carnegie Inst. Wash. Pub., 31. 104 pp. 1905. Reed, G. AL, "The powdery mildews— Erysiphaceae," Trans. Am. Micr. Soc, 52:219-258, 1913. Salmon, E. S., "A monograph of the Erysiphaceae," Mevt. Torrey Botan. Club, 9: 1-292, 1900. "On Oidiopsis taurica Lev., an endophvtic member of the Erysiphaceae," ^7272. Botany, 20: 187-200, 1906. Smith, Grant, "The haustoria of the Erysipheae," Botan. Gaz., 29: 153- 184, 1900. Stevens, F. L., "The genus iMeliola in Porto Rico, III," Biol. Monogr., 2: 475-554, 1916. "The Meliolineae, I," A7in. MycoL, 25:405-469, 1923; II, 25:165-383, 1928. Theissen, F., and H. Sydow, "Synoptische Tafeln," Ami. MycoL, 15: 389- 491, 1917. Pyrenomycetes The Pyrenomycetes include a large assemblage of fungi vari- ously estimated to number between 10,000 and 20,000 species. They possess perithecia the wall of which opens by an ostiolum or pore. The asci are typically arranged in a parallel series over the inner basal wall of the perithecium. This group of Ascomy- cetes is usually regarded as being comprised of four orders, Dothideales, Hypocreales, Sphaeriales, and Laboulbeniales, the last-named of \\'hich is an aberrant assemblage. The orders may be distinguished as follows: Perithecial wall differentiated from stroma Stromata, if present, and perithecia bright colored, red, yellow, purple, etc. Hypocreales 180 THE ASCOMYCETES Stromata, if present, and perithecia carbonaceous Sphaeriales Perithecial wall not differentiated from stroma, but perithecia mere locules in the dark-colored stromata Dothideales Minute external parasites of insects; ascocarps borne on a receptacle that may be appendaged Laboulbeniales Dothideales As described by Lindau in Die naturlichen Fflanzenjamilien, the Dothideales comprise 24 genera and 400 species, all included in the one family Dothideaceae. In their monographic treatment Theissen and Sydow (1915) set up the order with 4 families hav- ing 140 genera and containing a total of about 8000 species, a large proportion of which are tropical. They later reduced the order to two famihes, Dothideaceae and Phyllachoraceae. In the Dothideaceae the stromata are immersed within the host and be- come erumpent at maturity; in the Phyllachoraceae they remain covered by host tissues. Members of the two remaining families, as first used by Theissen and Sydow, have been distributed among the iVIyriangiales, Hemisphaeriales, and Sphaeriales. There has even been some question as to whether the Dothideales con- stitute a natural order. The foregoing statements convincingly indicate the confused status of the Dothideales, a chaos largely traceable to the fact that the Hfe histories of less than a half- dozen dothideaceous species are known. As employed in this work, the Dothideales are pyrenomyce- tous fungi, possessing black stromata within which perithecial cavities, lacking independent perithecial walls, are developed. Whether the stromata remain endogenous (innate) or become exogenous (erumpent) at maturity is the basis for separating the two families, Phyllachoraceae and Dothideaceae. Dibotryon (Ploivrightia) viorbosinn, the cause of black knot of" plums and cherries, is widely known, but its ordinal position is not yet established. It has been placed in older accounts among the Dothideales, but Theissen and Sydow (1915) regard it as nearly related to Botryosphaeria, which some mycologists place among the Myriangiales. Undoubtedly it is not a member of the Phyllachoraceae. To shift it from the Dothideales on the basis of present knowledge would only add to existing confusion. A study of the life history of D. morhosinn was early made by Farlow (1876), and similar recent studies include those of Koch DOTHIDEALES 181 (1934, 1935). Infection takes place in the spring; and, when the host resumes growth the next spring, the invaded tissues rapidly become enlarged, a velvety layer of conidiophores appearing Fig. 66. Dibotryon (Plowrightia) morbosum. A. Habit sketch of stroma on branch of cherry. B. Portion of perithecial stroma in vertical section. C. Conidiophores and conidia of the Hormodendrum stage. D. Ascus, un- equally two-celled ascospores, and paraphyses. E. Conidia. F. Germmat- ing ascospores. over the surface of the swollen tissues. This conidial stage be- longs to the form Genus Hormodendrum. After midsummer, black stromata develop, covering the affected tissues, and by the 182 THE ASCOMYCETES succeeding spring the perithecia are mature. Koch (1935) iso- lated ascospores in culture and produced from them the Hormo- dendrum stage. Farlow (1876) and Koch (1934) call attention to an associated Coniothyrium (pycnidial) stage, which Koch states is not genetically connected. Since details of the initiation of ascocarps are lacking, this familiar organism should be rein- vestigated. Phyllachoraceae. Phyllachora graininis and related species on various grasses are the most' commonly encountered repre- sentatives of this family. Phyllachora graininis produces its stromata within the leaves of many grasses. It may prove to be a composite of many species, but this hypothesis can be proved only by comparative morphologic studies and by reciprocal cross- inoculations. Phyllachora grajnwis has not been artificially cul- tivated, does not possess a conidial stage, and has been stated to have perithecial walls like those of the Sphaeriales. For this reason Orton (1924) is of the opinion that all species of Phyl- lachora and perhaps the entire family Phyllachoraceae should be removed to the Sphaeriales. DoTHiDEACEAE. The several members of the Dothideaceae in- vestigated include Systrevi7na iilmiy parasitic on elm, Cyiimdothea trifolii, causing sooty blotch of clovers, and Systrejinna acicola* the cause of brown-spot needle disease of pines. KilHan (1920) found that ascospores of Systrenmia uhni initiate the primary in- fections in the spring. As a result, a subcuticular stroma, from * The organism was given the name Scirrhia acicola (Dearness) by Siggers in 1939 (Phytopatb., 29: 1076-1077, 1939), and this name is retained by him in a later report {Tech. Bull. U. S. Dept. Agr., 810, 36 pp., 1944). His photographs in Plate 1 are manifestly those of an immature stroma (Fig. C) and immature ascospores (Fig. D). Mature stromata are exposed and prominently protrude and hence (Fig. D) are not those of the Phyllachoraceae. Discharged ascospores have brown walls as well as brown cell content. The ascospores of the Genus Scirrhia, as delimited and accepted, are colorless. In this connection it may be well to reflect upon the fact that the conidia of the brown-spot fungus are brown-walled, that the stromata (conidial, spermogonial, carpogonial, and perithecial) are composed of brown-walled cells, and that the mycelium in culture is col- ored and produces smokv to black colonies. WTiat, then, is the likelihood of "uncolored" ascospores? It seems unthinkable that this brown-spot fungus could be properly placed in the Genus Scirrhia. DOTHIDEACEAE 183 Fig. 67. Cymadothea trifolii. A. Conidial pustule in section of the stage known as Folythrinciinn trifolii. The nodose, wavy conidiophores bear scars from which the two-celled conidia are abstricted. B. Diagrams show- ing stages in production of conidia such as might occur on a single conidio- phore. The undulate appearance is the result of sympodial branching. C. Nodose conidiophore bearing a series of scars from which conidia were abstricted. D. Conidia, some of which are germinating. E. Portion of wall of spermogonial locule, with spermatiophores and spermatia. F. Young perithecial locule in section. The trichogyne projects to the surface and the multinucleate cells belong to the basal part of the carpogonium. G. Edge of perithecial stroma, showing locule in section with one mature ascus and others all immature. H. Ascospores, one germinating. 184 THE ASCOMYCETES which conidia are abstricted, is developed. After conidial pro- duction ceases, these conidial stromata disappear, and the deeper- seated hyphae develop pads of fungus tissue beneath the epi- dermis. Within these pads are certain deeply staining cells, each of which abjoint three or four daughter cells that become two- to three-nucleate. Pairs of these cells fuse, and from the fused cells ascogenous hyphae arise. The type of sexuality in Systreirmia iilmi is quite unlike that recently described for S. acicola by Wolf and Barbour (1941). This fungus forms coincidentally on dead needles conceptacles of two kinds. In one, small rod-shaped spermatia are produced in profusion from rows of spermatium mother cells. In the other, several ascogonial coils occur, surrounded by loosely packed nurse cells. The trichogynes project well above the surface of the stromata. Presumably the spermatia lodge upon the tricho- gynes and effect fertilization. About 6 to 8 weeks thereafter the perithecia are mature, having been transformed from the locules containing ascogonial coils. The conidial stage, Lecanosticta acicola, develops both on green needles and on dry ones. Cultures isolated from conidia produce conidia on artificial media. Furthermore cultures iso- lated from ascospores produce the conidial stage on artificial media. The development of perithecia by Cymadothea trifolii [Wolf (1935)] is quite like that described for 5. acicola. Both sperma- tial and ascogonial locules may occur within the same stroma. If moisture is available, the spermatia ooze out and lodge on the several projecting trichogynes during the autumn. By the fol- lowing spring the perithecia will have matured. The conidial stage, Folythrinciiim trifolii, possesses nodose, wavy conidiophores, which were first noted about 125 years ago. This wavy characteristic, a type of sympodial branching, arises as the result of elongation of the conidiophore after each conidium is matured and dislodged in succession. The mature stromata of Dothideales have been examined by Orton (1924) and Blain (1927). Until more studies of similar nature, involving a goodly number of species and elucidating de- velopment of the stromata, have been made, exact knowledge of this order is essentially non-existent. DOTHIDEACEAE 185 Fig 68. Systrenmia acicola. A. Vertical section of stroma showing struc- ture of the conidial stage, Lecanosticta acicola. B. In section, a carpogonia locule formed concurrently with the spermogonial locule. C. Spermogonial locule. D. Chain of spermatiferous cells and spermatia. E. Cross-section of elongate perithecial stroma. F. Conidia. G. Ascospores. H. Mature ascus. 186 THE ASCOMYCETES Classification. The monograph by de Jaczewski (1895) of the Dothideaceae of Switzerland and that by Theissen and Sydow (1915) constitute the most important ones available to present- day students. LITERATURE CITED Blaix, W. L., "Comparative morphology of Dothideaceous and kindred stromata," MycoL, 19: 1-20, 1927. Farlow, W. G., "Black knot," Bull. Bussey hut., i; 440-453, 1876. Jaczewski, A. de, "Les Dothideacees de la Suisse," Bull. soc. mycol. France, 11: 155-195, 1895. KiLLiAN, C, "Le developpement du Dothidella uhiii (Duv.) Wint.," Rev. gen. botan., 52:534^551, 1920. Koch, L. W., "Investigations on black knot of plums and cherries. II. The occurrence and significance of certain fungi found in association with Dibotryon morbosinn (Schw.) T. and S.," Sci. Agr., 13: 80-95, 1934. III. "Symptomatology, life history, and cultural studies of Dibotryon morbosinn (Schw.) T. and S.," Sci. Agr., 25:411^23, 1935. Orton, C. R., "Studies in the morphology of the Ascomycetes. I. The stroma and compound fructification of the Dothideaceae and other groups," MycoL, 16:49-95, 1924. THErssEN, F., AND H. Sydow, "Die Dothideales," Ann. MycoL, 13: 149-746, 1915. Wolf, F. A., "iMorphology of Polythrincium, causing sooty blotch of clover," MycoL, 21: 58-73, 1935. ' Wolf, F. A., and W. J. Barbour, "Brown-spot needle disease of pines," Phytopathology, 52:61-74, 1941. Hypocreales The Order Hypocreales comprises those Pyrenomycetes whose perithecia are soft textured and brightly colored. xApproximately 1750 species, distributed among over 60 genera, are included in this group. Nearly all of them subsist on plant tissues, either as parasites or saprophytes; certain genera, however, notably Cor- dyceps and Sphaerostilbe, contain entomogenous species. In Hvpomyces are included species that parasitize Hymenomycetes; and in Claviceps, species that transform the ovaries of various grasses into sclerotia that, if consumed, are poisonous to man or domestic animals. No satisfactory classification of Hypocreales is possible at this time. Some workers regard the group as belonging to 1 family, some to 2 families, and some to 3 families. Seaver (1910) em- ASEXUAL REPRODUCTION 181 ployed 2 families: Nectriaceae, having solitary perithecia, and Hvpocreaceae, having perithecia seated within a stroma and there- fore partially or wholly immersed. In some instances, as in the Genus Nectria, the stroma is so meager as to invest only the basal E Fig. 69. Nectria and associated conidial stages. A. Nectria coccinea, habit sketch. B. Sporodochium (diagrammatic) of Tiibercularia vulgaris, in vertical section. C. Conidiophores and conidia of T. vulgaris. D. Conidia of Cylindrocarpon. E. Ascus and ascospores of Nectria coccinea. portion of the perithecia, whereas other species have completely discrete perithecia. Septation of ascospores provides a workable, although \\holly artificial, basis of generic classification. Asexual reproduction. Many of the Hypocreales possess conidial or chlamydospore stages. The conidial stage of Nectria cinnabarina on currants, pear, basswood, maple, elm, and oak is Tiibercularia vulgaris. Nectria coccinea on beech [Ehrlich (1934)] has a macroconidial stage belonging to the Genus Cylin- drocarpon. Other species of Nectria, including N. ipoinoeae on 188 THE ASCOMYCETES sweet potatoes, have been connected with Fusarium. Isaria con- stitutes the conidial stage of Cordvceps, Sphacelia that of Clavi- ceps, Fusarium tliat of Neocosmospora, and \>rticillium that of Hypoiiiyces ochraceus and H. chrysosper?mis. Diplocladhim vibms is connected with Hypomyces later itms, and Trichothe- chnn cand'idimi with H. roselhis. My co gone perniciosa and M. rosea parasitize mushrooms and are chlamydosporic stages of Hypomyces. Sepedoniimi chrysospervmvi is the chlamydosporic staore of Hypomyces chryso- speiiims, \\'hich attacks Bole- tus. Gibberella saiLbinettii (G. zeae) appears late in the sea- son on cereals whose heads (inflorescences) are blighted by the Fusarium stage. Ephelis constitutes the conidial stage of Epichloe, Dothichloe, and Balansia. V erticilliiim globii- Ug-erinJi is connected ^^'ith Fodocrea ahitacea. Representative forms. In the accounts that follow brief mention will be made of a few species regarded as representa- tive of this rather large group. In Nectria, containing over 250 species, are some very important plant pathogens. Nectria galUgena causes a canker disease of pomaceous trees in Europe and has been reported to attack pears in the Pacific Northwest [Zeller and Owens (1921)]. Cayley (1921) found ascogonial coils in developing perithecia but was of the opinion that they do not function to produce ascogenous hy- phae. She also observed pvcnidia, which may well have been spermogonia. In the eastern United States N, ditiss'nna causes "target-spot" cankers on basswood, red maple, birches, ^\'alnut, and yellow poplar. In the Maritime Provinces of Canada N. coc- cinea is associated with the scale insect, Cryptococciis jagh in the destruction of beech [Ehrlich (1934)]. The Genus Thyronectria, monographed by Seeler (1940), con- tains species having muriform ascospores. In some species these Fig. 70. Neocosmospora vasiniecta. A. Surface view of perithecium, B. Ascus contains thick-walled 'asco- spores. HYPOCREALES 189 ascospores, while still within the ascus, bud to form myriads of hyaline spores. Conidial stages, so far as is known, belong to Gvrostroma, Dendrochium, and Stilbella. Thyronectria mistro- americana causes a wilt disease of Gleditsia japonica and a canker disease of G. triacanthos [Seeler (1940, 1940a)]. Fig. 71. Cordyceps claviilata on Lecanium sp. on Morus rubra. Neocosmospora vasinfecta is of common occurrence in the southeastern United States on the roots of cotton, cowpeas, pea- nuts, and soybeans. This organism was reported to be connected with Fiisarmm vasinfectiim, the cause of cotton wilt. Butler (1910), working in India with this fungus on chickpea, Cicer arietmimi, disproved genetic association with a parasitic Fusarium but showed that it is connected \\ith a saprophytic species of Fusarium. 190 THE ASCOMYCETES Species of Hvpomyces are of interest because they are parasitic on various agarics and boletes. At times they are serious enemies of mushroom culture, attacking the sporocarps in the button stage and covering them with bright red or orange perithecia. The ascospores are hvahne, two-celled, and fusiform. Folystigvm nibnnn causes a red-spot disease of Prunus, es- pecially cherry, in Europe. Its development has been described Fig. 72. Volystigvia riihrinn. A. Basal portion of ascogonial coil, tricho- gyne not shown. B. Wall between two ascogonial cells partly absorbed. C. Complete plasmogamy. (After Nienburg.) by Blackman and Welsford (1912) and Nienburg (1914). In- fections are initiated by ascospores. Five or six weeks later bright-red stromata have formed ^\■ithin the leaves. Within these stromata two types of conceptacles arise. One is flask-shaped and bears slender, hooked spores that have been termed spermatia. The other is filled with a loose tangle of hyphae, in which a coiled, septate ascogonium is embedded. Filaments extend from the ascogonium to the leaf surface. During damp weather in late summer the spermatia ooze out in a slimy mass and adhere to the trichogyne, but they have not been proved to function in fertilization. Nienburg recorded the absorption of the wall be- tween certain cells of the ascogonium, permitting a pair of sister nuclei to be associated and plasmogamy to occur. Ascogenous hyphae arise from this ascogonial cell. HYPOCREALES . 191 Epichloe typh'ma forms cream-colored sheaths around the stems of Phleum, Poa, Dactvlis, and other meadow grasses. Enormous numbers of hyahne, ovate conidia cover the young stromata. The perithecia are eventually seated within these stromata, superseding the conidial or Ephelis stage. The peri- thecial initials contain three- to five-celled ascogonia, each cell being multinucleate. The protoplasts of a pair of these cells fuse; ascogenous hyphae then form and eventually produce the asci. The ascospores are hyaline and thread-like. Other closely related genera, occurring on grasses and having similar conidial stages but purplish black stromata, are Balansia and Dothichloe. Each also produces filamentous ascospores that in Dothichloe separate into segments. The fertile stromata of Balansia hy poxy Ion are cushion-shaped and sclerotium-like, and they are elevated above the stroma that invests the grass stems. Early studies of these genera within the United States were made by Atkinson (1894, 1905) and more recent ones by Diehl (1930). The Genus Cordyceps was early monographed by Massee (1895). It contains about 200 species, nearly all of which para- sitize insects, transforming their tissues into sclerotia. The most commonly encountered entomophthorous species are C. capitata on scale insects and C. sphingiim and C. militaris on larvae and pupae of various Lepidoptera. The remainder parasitize Elapho- myces, especially E. cervimis and E. gramilatns. The develop- ment and cytology of one of this second group, Cordyceps agar- icijonnia, were studied by Jenkins (1934) and found to be quite like those of Epichloe, Claviceps, and Polystigma. The stromata of Cordyceps, or clavae, are stalked, and the perithecia are pro- duced in the capitate tips. Shanor (1936), using as media living lepidopteran pupae placed on sphagnum in moist chambers, grew Cordyceps jiiilitaris to maturity. Claviceps purpurea and related species parasitize grasses, especially the cereals, transforming the ovaries into sclerotia, commonly called ergot grains. Monographic treatises by Atana- soff (1920) and Barger (1931) summarize the numerous papers dealing with this genus and with ergotism, the disease which re- sults from ingestion of ergot grains or sclerotia. These sclerotia are grayish violet externally and grayish white to white within. Their size, which varies, is dependent upon that of the ovaries 192 THE ASCOMYCETES from which they arise. On rye, they are 1 to 3 cm long; on MoUjiia coenilea, 4 to 6 mm; on Foa pratensis, 6 mm; on Elynms canadensis, the same size as on rye. The sclerotia mature at harvest time and normally fall to the ground, where they hibernate. If they are harvested and stored with the threshed grain, they may be returned to the field wdth the seed. Tulasne (1853) found that the minimum dormant period is 3 months. Kirchhoff (1929) reported that after several weeks' exposure to cold, followed by a similar period of higher temperature, germination may ensue. He secured 60 to 80% germination after 4 to 8 weeks' exposure at 15° C. If the period of exposure was short, germination proceeded tardily. If the sclerotia w^ere stored in the cold, at a temperature near freezing, for 2 months, satisfactory germination ensued after 3 to 4 weeks' exposure at the higher temperatures. Burial in moist sand consti- tuted a favorable substratum for germination. Zimmerman (1906) noted that sclerotia usually germinate dur- ing May of the year following that in which they were formed. They may remain dormant, however, until the second year and then germinate at the normal season. Germination is first evi- dent as bulges in the sclerotial cortex. These bulges burst through the rind and develop into the clavate stromata, which consist of slender stalks surmounted by spherical heads, 1 to 1.5 mm in diameter. The entire stroma is yellowish white at first but changes to grayish violet. The stromata that arise from a sclero- tium may vary in number from a few to more than a score. At maturity the head of each is covered with wart-like projections that mark the position of the innate, pear-shaped, perithecial locules with orifices at the tip. Details of the formation of perithecia were first elucidated by Killian (1919). He described pairs of branches, one an antherid- ium, the other an ascogonium, which formed on the top of pe- culiar voluminous cells and became the primordia of ascogenous hyphae. The antheridia and ascogonia are surrounded by fun- gous parenchyma that fills the locules. Eventually the paren- chyma cells are entirely replaced by asci and paraphyses. Each ascus contains 8 filamentous spores 50 to 75 \i long and 0.6 to 0.7 |i in diameter. Numerous paraphyses are interspersed among the asci. HYPOCREALES 193 According to Falck (1911), the ascospores are violently dis- charged into the air and then are carried by convection currents to grass flowers. This method of spore dispersal has been verified by several observers by means of the beam-of-light method. Stager (1903), however, maintains that the spores are slowly exuded from the perithecia to form a sHmy layer. Then dispersal is facilitated by insect visitors, especially flies and beetles. Some idea of the profligacy of ascospore production can be gained from Kiinn's calculation [Atanasoff (1920), p. 29] that a scle- rotium with fifteen stromata will produce over a million asco- spores. The exact manner in which the ovary becomes infected is not known. There is reason to beheve that germ tubes from asco- spores lodged on the glumes cannot penetrate them. If the glumes are open so that the ascospores lodge on the stigmata or in the nectar, they should germinate, and the germ tube should extend into the ovary. Experiments by Stager (1903) indicate that infection takes place both in polHnated and non-pollinated flowers. When he inoculated the ovaries 3 or 4 days before flowering, he found that infection developed very rapidly. In- fection is indicated by the investment of the ovary with a super- ficial weft of mycelium. The ovarian tissues are penetrated, how- ever, and become completely replaced by a furrowed, porous mass that will eventually be the sclerotium. Meanwhile the sur- face of the mass is densely covered with elongated cells from whose apices conidia are abstricted. This constitutes the spha- celial stage. The conidia are formed in great numbers and col- lect in droplets that appear at the edges of the glumes. These droplets are the "honey dew" which is sweet to the taste, and, if examined microscopically, will be found to be teeming with mil- lions of ellipsoidal hyaline conidia. Honey dew is attractive to flies and other insects that incidentally aid in disseminating the conidia to cause secondary infections. Dew and rain also serve to convey conidia to other grass flowers. Different explanations have been given to account for the origin of honey dew. Some workers believe that it is secreted by the sphacelial hyphae, and others that it is secreted by the nectaries in response to stimulation by the ergot fungus. The time required for the formation of sclerotia is correlated with the weather. In moist weather sclerotia may first be appar- 194 THE ASCOMYCETES Fig. 73. Various Hypocreales. A. Cross-section of stroma of Epicbloe typbina. The stroma invests the leaf sheath and cuhn, and the pinkish perithecia are seated in the stroma. B. Ascus of E. typbina containing eight thread-Uke ascospores. C. Habit sketch of Cordyceps claviilata on Lecanium on twig of mulberry. D. Tip of clava enlarged, indicating ar- rangement of perithecia. E. Single, segmented, filamentous ascospore. F. Sepedonium or chlamydospore stage of Hypomyces. G. Ascospores of Hypomyces, parasitizing Russula. H. Ascospores of Gibberella saubinettii, from wheat. /. Conidia of the Fusarium stage of the wheat-scab pathogen. SPECIES OF CLAVICEPS 195 ent 1 week after the first appearance of honey dew, whereas in dry weather 2 weeks may elapse. Sclerotial formation progresses gradually, and the sclerotia normally reach maturity by the time the rye is ready to be harvested. Ordinarily young ovarian tissues are completely destroyed and are replaced by the sphacelial mycelium. Sometimes, however, the upper portion of the ovary remains. At any rate, a rather densely interwoven mass of hyphae replaces the normal grain, which it exceeds by several times in bulk. These hyphae become densely compacted at the exterior of the mass, forming the scle- rotium. These sclerotia are yellowish brown and cartilaginous when they first attain their mature size, but on drying they be- come grayish violet and are corneous. Hosts. Claviceps piirptirea is world-wide in distribution and occurs on approximately 200 species and varieties of grasses, a list of which appears in the monograph of Barger (1931, pp. 117- 122). In w^et seasons it causes an important disease of r^^e but is of less consequence on wheat, oats, and barley. Cases are on record in which 20 to S0°/o of rye heads have been ergotized. More commonly the losses in yield of rye are less than 1%. The injury to forage grasses is greater than that to cereals. Single heads of Agropyron Occident ale are known to produce 40 ergot grains, 5 or 6% by weight of the seed being ergot. Rostrup [Atanasoff (1920), p. 5] found 2700 sclerotia in a sample pound of Festuca seed, 5600 in one of Poa, 500 in one of Holcus, and 2500 in one and 2700 in another of two samples of Agrostis alba seed. Species of Claviceps. Of the 20 named species of Claviceps, 8 are indigenous to Europe, and 12 to America. Those recorded for Australia appear to have been introduced into that continent. Undoubtedly unnamed species occur in Asia and Africa. Species are separated on the bases of shape, size, color and dimensions of stromata, and dimensions of perithecia, asci, ascospores, and co- nidia. Paraphyses are present in some species but lacking in others. These morphological characteristics, although useful in spe- cific identification, may not always be sufficient criteria. This appears to be the situation ^^'hen Claviceps paspali and C. rolfsii must be distinguished, the reported dimensions of the former be- 196 THE ASCOMYCETES ing essentially half those of the latter. For several seasons the writers have collected sclerotia from the inflorescences of Pas- pahim laeve, P. dilatatinn, and P. ftoridamnji. The sclerotia borne on the heads of each of these grasses differ in average size. Scle- rotial size is found to be proportional to the normal size of the ripened ovaries in each of these species of grass. The perithecia, asci, and ascospores, however, are all alike and correspond with measurements for C. paspali. The complete host range of species of Claviceps can be known only by means of reciprocal inoculations. Stager (1903) alone conducted such studies during a period of 10 years, but his re- sults should be verified and the experiments extended. He ap- plied dilute suspensions of honey dew by means of an atomizer to flowering grasses grown under controlled conditions. Conidia of Claviceps uoilsoni from Glyceria fliiitans failed to produce in- fection upon any other species, although they were applied to seventeen other kinds of grass. Similarly C. sesleriae failed to produce infection except on Sesleria coenilea. Claviceps pur- purea itself he found to consist of several biological races. For example, the Claviceps of Anthoxanthinn odoratu?n, although morphologically indistinguishable from C. purpurea of rye, pro- duces abundant sclerotia if used to inoculate A. odoratiiin. If, on the other hand, Claviceps of rye is used as inoculum for A. odoratwn^ sclerotia are almost never found, and, if they are found, are very abnormal and small. The Claviceps of Brachypodiinn silvaticwn is also a distinct biological race of C. purpurea. Br achy podium silvaticmn comes into flower too late to be infected by ascospores originating from sclerotia borne on this grass during the previous summer. Such ascospores readily infect Milium effiisimi, however, and abundant honey-dew formation results. Meanwhile B. silvaticinn comes into flower and can be readily infected with conidia produced on M. effusum. Numerous sclerotia develop on B. silvaticinn but are very seldom formed on M. effusimi. Apparently under nor- mal conditions this variety of C. purpurea requires two hosts, B, silvaticinn and M. effusum. Barger's (1931) account deals extensively with ergot poisoning through the eating of bread, especially that made from ergotized rye. Numerous epidemics originating from eating bread made from such rye flour have been reported. The disease results in LITERATURE CITED 191 gangrenous loss of extremities, paralysis, and death. Domestic animals are also poisoned from eating cereal grains admixed with ergot grains. Poisoning by species of Claviceps is more fully , considered in Chapter 15, Volume II. LITERATURE CITED Atanasoff, D., "Ergot of grains and grasses," U. S. Dept. Agr., Bur. Plant hid. (mimeographed). 107 pp. 1920. Atkinson, G. P., "Steps toward a revision of the linosporous species of North American graminicolous Hypocreaceae," Bull. Torrey Botaji. Club, 21:222-225, 1894. "The genera Balansia and Dothichloe in the United States, with a con- sideration of their economic importance," /. MycoL, 11: 248-267, 1905. Barger, G., "Ergot and ergotism, a monograph based on the Dohme lec- tures delivered in Johns Hopkins University." 279 pp. Gurney and Jackson, London. 1931. Blackman, V. H., AND E. J. Welsford, "The development of the perithe- cium of Folystigina rubrinn,^'' Ann. Botany, 26: 761-767, 1912. Butler, E. J., "The wilt disease of pigeon pea and the parasitism of Neo~ cosmospora vasinfecta Smith," Me77i. Dept. Agr. hidia, Botan. Series, 2: 1-^4, 1910. Cayley, Dorothy M., "Some obser\^ations on the life history of Nectria galligena Bres.," Ajm. Botany, 35:19-92, 1921. DiEHL, W. W., "Conidial fructifications in Balansia and Dothichloe," /. Agr. Research, 41:161-166, 1930. Ehrlich, John, "The beech-bark disease; a Nectria disease of Fagus follow- ing Cryptococcus fagi (Baer)," Can. J. Research, 10:593-692, 1934. Falck, K., "Uber die Luftinfektion des Mutterkorns (Claviceps fnirpurea) und die Verbreitung pflanzlicher Infektionskrankheiten durch Tem- peraturstromungen," Z. Forst.- u. Jagdiu., 43:202-221, 1911. Jenkins, W. A., "The development of Cordyceps agaricijormia,^'' MycoL, 25:220-243, 1934. Killian, C, "Sur la sexualite de I'ergot de seigle, le Claviceps purpurea Tulasne," Bidl. soc. mycol. France, 3$: 182-197, 1919. Kirchhoff, H., "Beitrage zur Biologic und Physiologic des Mutterkorns," Xentr. Bakt. Farasitenk., II Abt., 77:310-369, 1929. Massee, George, "A revision of the genus Cordyceps," Ann. Botany, 9: 1-44, 1895. NiENBURG, W., "Zur Entwicklungsgeschichte von Folystigma rubrimt D.C.," Z. Botan., 5:369-400, 1914. Seaver, F. J., "Hypocreales," N. Am. Flora, 3: 1-56, 1910. Seeler, E. v., Jr., "A monographic study of the genus Thyronectria," /. Arnold Arboretimi, 27:429-460, 1940. "Two diseases of Gleditsia caused bv a species of Thyronectria," /. Arnold Arboretum, 27:405-426, 1940a. 198 THE ASCOMYCETES Shanor, L., "The production of mature perithecia of Cordyceps militaris (L.) Link in laboratory culture," /. Elisba Mitchell Sci. Soc, 52:99- 104, 1936. - Stager, R., "Infektionsversuche niit Graniineen bewohnenden Claviceps- Arten," Botan. Z., ^ or carbonaceous d d. Perithecia with papillate ostiole Sphaeriaceae d. Perithecia with beak-like ostiolar region Ceratostomataceae a. Perithecia partly embedded in substratum or in stroma e SPHAERIALES 199 e. Perithecia at maturity completely emergent from stroma Cucurbitariaceae e. Basal portions of perithecia persistently immersed in substrate f f. Ostioles circular Amphisphaeriaceae f. Ostioles compressed, appearing elongate-elliptical in cross- section Lophiostomataceae a. Perithecia embedded in substratum or in stroma, but with ostiolar neck only protruding g g. Immersed in substratum, but well-defined stromata not formed h h. Perithecia papillate, asci not usually thickened apically Mycosphaerellaceae h. Perithecia beaked, asci thickened apically Gnomoniaceae g. Immersed in stromata i i. Stromata pulvinate, composed of fungus and host elements j ]. Asci short-stalked and ephemeral Diaporthaceae j. Asci long-stalked, spores allantoid Allantosphaeriaceae i. Stromata pulvinate or erect, composed wholly of fungal ele- ments; spores dark Xylariaceae Throughout the order the asci A\'ithin any perithecium are of different ages. In the larger proportion of species the asco- spores are forcibly expelled. In certain of them, such as the Ceratostomataceae and Fimetariaceae, however, the asci are eva- nescent; and the ascospores are extruded in mucoid droplets, or else the asci break away and are forced intact toward the ostiolar neck, where they rupture. The asci are elongate-clavate, quite generally with ascospores arranged biseriately, obliquely, and in a single row, or else lacking special arrangement. The number of ascospores is mostly 8, but occasional species, such as Neurospora tetraspemia and Fleurage anserina, have 4, or even 2, as in Gno- vionia dispora. Fleurage zygospora bears 16 spores; P. caenileo- tecta, 128; and some species of Sporormia form 256, 512, or even 1024. Many genera lack paraphyses; in others they are commonly intermingled with the asci. In many species sterile hyphae, periphyses, occur at the periphery of the hymenial area and may also line the ostiolar orifice. Conidial production is of common occurrence among the Sphaeriales. Usually the same type of conidia is produced by all species of a given genus, but some genera, as at present delimited, possess as conidial stages a wide variety of conidial types. Quite commonly, too, among plant pathogens the conidial stage occurs during pathogenesis, and the ascogenous stage during sapro- genesis. 200 THE ASCOMYCETES Chaetomiaceae. As their name indicates, the members of this family are distinguished by fructifications the exteriors of which are partly or completely beset with hairs. They occur on paper, straw, dung, and decaying plant tissues and are known to be capable of digesting cellulose and therefore of functioning in the formation of humus. Chivers (1915) in his monograph recog- nizes 114 species and 14 varieties of Chaetomium and 2 species of Ascotricha. Species of Bommerella are regarded as belonging to Chaetomium. Chaetomidium lacks an ostiole and thus shows affinity with the Plectascales. The ascospores, which are freed by early deliquescence of the asci, are brown to black and t\^pically lemon-shaped. Conidia are commonly borne on the hairs which adorn the perithecia. Various conidial forms have been observed, most of them belonging to the form Genera Sporotrichum and Verticil- Hum. In Ascotricha chartamm there occur not only a Spor- otrichum stage but also a peculiar chlamydospore stage, which was described as Die y ma ampidlijera. FiMETARiACEAE (Sordariaceae) . The Fimetariaceae are sapro- phytic species, most of them occurring on dung. Some are lim- ited rather closely to the dung of certain species of herbivors. Their perithecia are flask-shaped, the perithecial walls being membranaceous. The ascospores are typically unicellular and are provided with a gelatinous sheath or one or two gelatinous appendages. By means of this gelatinous coating the ascospores, which are forcibly discharged, adhere to vegetation. They are ingested by browsing animals and hence disseminated by them. Conidial stages are rarely found. Among the better-known representative species is Pleurage anserina. This species is normally four-spored, but occasionally five-spored asci are seen. In four-spored asci the spores are bi- nucleate; in five-spored asci the spores differ in size, two of them being small and uninucleate. The binucleate spores, when grown in monosporic culture, are hermaphroditic and self-fertile, as found by Ames (1934), whereas the small spores are of two classes, which Ames called A and B. Monosporic cultures from these small ascospores bear both ascogonia and spermatia but are self-sterile, although, when reciprocally crossed, they are fertile. In regard to this fungus, therefore, it is not proper to speak FIMETARIACEAE (SORDARIACEAE) 201 of a plus strain or class and a minus strain or class, for each strain produces both male and female organs and is thus bisexual or hermaphroditic. Obviously the difference between strains must be based on compatibility. A ^. D ^ ■1 B Fig. 74. Pleurage anserina. A. Peritherium in silhouette. B. Tip of trichogyne with spermatium attached. C. Mature ascus containing three normal and two dwarf spores. D. Ascogonium before fertilization. E. Clusters of spermatia. (After Ames.) In Pleurage zygospora, which has 16 spores, Lewis (1911) found that the typical 8 free nuclei are formed; each then be- comes delimited by a membrane. Additional nuclear divisions to form a sporogenous filament follow. A functional spore is cut off from each end of each filament, thus making 16 asco- spores. In Philocopra {Sporonnia) coeriileotecta [Jolivette-Sax (1918)], on the other hand, free nuclear divisions occur until 128 nuclei are formed, whereupon the ascospore membranes are developed. 202 THE ASCOMYCETES Another ^^'ell-kno^^-n genus, which many mycologists place among the Fimetariaceae, is Neurospora. Its conidial stage is monilioid. The pink bakery mold, N. sitophila, has 8 spores, ^\•hereas N. tetrasperma has 4. Kno\\'ledge of sexuality in these species comes from the accounts by Dodge (1927, 1932, 1935), Colson (1934), and Backus (1939). By isolating each of the ascospores from individual asci of N. sitophila and mating their mvcelia in cultures, Dodge (1927) showed that the species is heterothallic. Similarly, each ascospore of N. tetrasperma nor- mally contains two nuclei differing from each other in compati- bility. When this species is grown in monosporic cultures, there- fore, it is found to be hermaphroditic. Occasionally, however, it forms dwarf ascospores, each having only one nucleus, and these are not totipotent. They are of either class A or class B in their sex reaction, and thalli of both classes must be grown together to produce perithecia. Both N. sitophila and N. tetrasperma form coiled ascogonia with branched trichogynal hyphae, although Colson (1934) con- cluded that they may not be formed in heterothaUic races of N. tetrasperma. Both also form spermatia. Dodge (1935) appHed spermatia from class A cultures of N. tetrasperma to cultures of class B and secured perithecia in the loci of application, indicating that spermatia function in fertilization. He also found that monilioid conidia can function in fertilization, or that "young aerial hyphae or even trichogynes or trichogynous hyphae, if they come in contact with trichogynous elements of the opposite sex reaction, are capable of effecting fertilization." This tend- ency of "substitute sexuality," as denominated by Backus (1939), was verified in Backus's experiments, in which the archi- carpic stromata became transformed into perithecia after contact with germinated conidia, germinated ascospores, or myceHal mats of the complementary^ sexual strain of N. sitophila. . Moreover, a small group of perithecia was induced to form near the site where a single ungerminated conidium was deposited, just be- yond the advancing margin of the mycelium. The performance of sexual functions is therefore regulated by compatibility factors which prevent self-fertilization. It has been suggested that Acanthorhynchiis vaccijiii, causing a rot of cranberries, also belongs in this family. This fungus normally produces perithecia in decaying leaves of its host, and CERATOSTOMATACEAE 203 perithecia develop also in culture. The ascospores are peculiar for the reason that on germination appressoria develop. The monographic treatment bv Griffith (1901), although old, is very useful in any taxonomic study of the Fimetariaceae. That by Seaver (1910) should also be employed. Sphaeriaceae. The Sphaeriaceae comprise some 20 or more genera. The perithecia stand singly or in small groups, and their bases may be immersed in a felt-like mesh or subiculum. The perithecial walls are firm, and the ostiolar region is papillate. Most of the numerous species are saprophytes on plant tissues, especially Avood and bark, but a few are destructive pathogens. Rosellinia deserves mention as typifying the parasitic species. Rosellhiia qiiercina attacks oaks throughout Europe, being especially destructive to seedlings and young trees in nurseries. It forms strands of hyphae, rhizomorphs, characteristic of the form Genus Dematophora. These strands ramify throughout the cortex of the roots and extend throus^h the soil to contact the roots of near-by seedHn^s. Black sclerotia, by means of which the pathogen hibernates, also develop, both within the root tis- sues that have been killed and at the exterior. Durino- the sum- mer, conidia and perithecia form at the surface of affected roots or on the soil. Details of perithecial development are wanting, as they are for all other Sphaeriaceae. Rosellinia clavariae parasitizes Clavaria cinerea and other species, giving to the bases of these coral fungi a blackened ap- pearance. Its conidial stage has been identified as Helmintho- sporiinn clavariorimi. Ceratostomataceae. The distinguishing feature of this family is the presence of long, ostiolar beaks on the perithecia. Other- wise the Ceratostomataceae resemble the Sphaeriaceae. Most species are saprophytic. In the Genus Ceratostomella, however, are several very destructive pathogens, as \\t\\ as certain others commercially important because they stain lumber or logs that have not yet been made into lumber. The most notable of the pathogens is Ceratostomella iihni, the cause of Dutch elm disease. This disease was first recognized in Holland and its causal agent described as Graphiinn iihiti, the conidial stage, in 1922. Eight years later it was discovered on elms in Cleveland, Ohio, and in Cincinnati, Ohio. Soon afterwards it was located in the area surroundinij New York City, ^^ here it Fig. 75. The conidial stage of Ceratostomella fimbriata. A and B. The first-formed oHve-brown conidium is double-walled. B and C. The subse- quently formed conidia are single-walled. D. Olive-brown conidium. E to L. Hyaline conidia. E to G. Stages in formation of hyaline conidia which are developed endogenously. H to L. Germination of hyaline conidia, which in turn are forming endoconidia. (Andrus and Harter.) 204 CERATOSTOMATACEAE 205 has continued to spread at an alarming rate and threatens to ehminate the American elm. In 1932 Buisman (1932) found, bv growing together on sterilized elm twigs certain stains isolated from conidia, that perithecia characteristic of Ceratostomella are produced. She also secured perithecia by inoculating elm branches with paired strains; this evidence in its entirety is in- terpreted to show that C. ztlmi is heterothallic. An account of this disease and the developmental history of its causal fungus, to which the student is referred, is available from the researches of Clinton and McCormick (1936). Ahrens and his associates (1935) have prepared a complete list of references to studies of this disease, especially studies conducted in Europe. Ceratostomella fimbriata causes black rot of sweet potatoes. Its "asci" are ephemeral; consequently the perithecial stage was long regarded as the conidial fungus, Sphaeronenia fimbriata, as Elliott (1925) has shown. The true conidial sta^e consists of endog-- enously formed conidia that adhere in chains. An understand- ing of the details attendant on perithecial formation has come from studies by Elliott (1925) and Andrus and Harter (1933, 1937). Although a pair of closely associated organs is produced to initiate the perithecia, it is not definitely determined that a fusion of antheridium and ascoo^onium involving nuclear mio-ra- ton occurs. Apparently by a crosier device a binucleate cell arises from the subterminal cell of the ascogonium. As soon as the hyphae have formed an envelope around the original asco- gonium, its walls disintegrate, and the ascogonium appears as a naked protoplast. The initial binucleate cell then proliferates, and soon the interior of the perithecial cavity is filled wdth naked cells or vesicles. Eventually paired nuclei in these unwalled cells fuse to make the primary nucleus of the ascus. There then fol- low three successive nuclear divisions. The immature spores are delimited by a layer of cytoplasm, and all appear to have a com- mon base of attachment. They are thus clustered; and, since no well-defined ascus wall ever appears, there is none to be dis- solved. The periphery of the ascus is merely a cytoplasmic layer. Among the organisms responsible for blue stain of wood the world over are several species of Ceratostomella, notably C. pil- ifera, C. ips, C. phiriaimzdata, C. minor, C. pseiidotsiigae, and C. piceaperda. They may penetrate sapwood by way of the rays; Fig. 76. Formation of perithecia by Ceratostomella fivibriata and C. vtonili- jormis. A to N . C. iiiomlijormis. A to H. Initiation of perithecia from primordium consisting of an antheridium and an ascogonium. /. Uninucle- ate protoplasts of antheridium and oogonium before plasmogamy. / to N. Binucleate cells or ascogonial cells within young perithecia. O to U. C. -fivibriata. O. Somewhat later development of perithecium, showing beak formation, and arrangement of ascogenous cells within the perithecial cavity. P. Nuclear fusion to make the primary ascus nucleus, 0- ^' Binu- cleate ascus. S. Quadrinucleate ascus. T. Early and late stages in forma- tion of eight ascospores. U. Habit sketch of mature perithecium. (Andrus and Harter.) 206 AMPHISPHAERIACEAE 201 and, although there is no evidence that they weaken the wood, they cause enormous losses by degrading the kimber. Conditions favoring the development of these fungi and methods for pre- venting losses are fully discussed in a report by Scheffer and Lindgren (1940). Ophioceras albicedrae is of more than passing interest, for the reason that it is commonly present on Jimipenis mexicana, pro- ducing conspicuous white patches on the trunk and limbs. [Heald and Wolf (1910)]. These patches are regarded as a specific characteristic to be employed in identifying the tree. CucuRBiTARiACEAE. The Cucurbitariaccae are characterized by the possession of stromata varying from a thin subiculum to a rather thick pulvinate layer, upon which the perithecia are seated, usually in caespitose aggregates. Most of them are saprophytic, occurring on the stems of woody plants. The Cucurbitariaceae are quite like the Sphaeriaceae, and Fitz- patrick (1923) has suggested that the two families be merged. This suggestion arises from his critical study of the Subfamily Nitschkieae, in which, within a single species, as among members of the Genus Calyculosphaeria, there may be found an intergrad- ing transition between a well-defined stroma and stromata con- sisting of a loose, hyphoid subiculum. Furthermore the perithecia of the Nitschkieae are all turbinate to cupulate in shape with a tapering, sterile base. The closely related Genus Fracchiaea is not cupulate but seems to be intermediate between the Cucurbi- tariaceae, as delimited by Lindau, and the Nitschkieae. Amphisphaeriaceae. The perithecia of members of this fam- ily are partly sunken in the substratum, with the upper portions free. Among its representatives of ^^'orld-wide occurrence is Caryospora piitamimim, commonly found on old pits of prunes and peaches. This organism, recently studied by Jeffers (1940), has large conical perithecia, and its asci usually contain three large, fusoid, two-celled ascospores. He found that the five nu- clei remaining within the young ascus after spore formation dis- integrate. Spermogonia containing spermatia developed in cul- tures on pea-extract agar, but Jeffers did not regard them as essential for sexual reproduction. The problem of how this organism thrives on sclerenchyma tissues is of more than passing interest. 208 THE ASCOMYCETES Another member of special interest is Pleosphaeria citri, oc- curring on citrus and oleander in the Mediterranean area. It is epiphytic, subsisting on the honey dew of plant Uce. Both peri- thecial and pycnidial stages are embedded in a thin but well- defined, loosely woven stroma. LoPHiosTOMATACEAE. As the name of this family indicates, the perithecial ostioles of its members are laterally compressed and have slit-like openings. For this reason the Lophiostomata- ceae are regarded as a link connecting the Sphaeriales with the Hysteriales. All of them seem to be saprophytic on herbaceous or woody stems. No detailed studies of any of them appear to have been made. Mycosphaerellaceae. This family is beyond all doubt the most unwieldy assemblage of Pyrenomycetes. As employed in this book, it includes the Pleosporaceae, as used by Lin- FiG. 77. Caryospora putaminiim. A. dau, excepting those members Half of peach pit, at the surface of belonging to the Pseudosphae- which are numerous black perithecia. riaceae, which were included B. Perithecium, in oudine, indicating ^^ ^^^ Myriangiales. The shape and attachment to the pit. C. ^. ' • • r A/r 11 J r.1 ,,.,vi, Pleosporaceae remaming arter Mature two-celled ascospore with ^ r & thick envelope. D. Typical ascus. this arrangement resemble Mycosphaerellaceae in all fea- tures except that they possess paraphyses. Such a characteristic seems scarcely worthy to constitute a basis for familial rank. In the Mycosphaerellaceae the genera Mycosphaerella, Guignardia, Venturia, Physalospora, and Ophiobolus deserve attention, partly for the reason that they contain so many plant pathogens, some of which are very destructive to crop plants. Mycosphaerella. Mycosphaerella, as at present delimited, contains well over 1000 species. Many of them possess a conidial stage that has been classified as belonging to such form genera as Phyllosticta, Phoma, Ascochyta, Septoria, Phleospora, Ramu- MYCOSPHAERELLACEAE 209 laria, Cercospora, Cercosporella, Ovularia, and Marssonia. Mani- festly the type of imperfect stage could be employed as a criterion for separating this large group into sections, as was suggested by Klebahn (1918). On this basis he proposed such names as Septoriosphaerella, Cercosphaerella, and Ramularisphae- rella. Some species do not possess conidial stages, for example, Fig. 78. Formation of spermatia by Mycosphaerella bolleana. A. Uni- nucleate spermatiferous cell just before first nuclear division. B. Binucleate spermatiferous cell. C. Quadrinucleate cell, only three of the cells shown. D. Sterigma being formed and protoplast from one quadrant migrating into the sterigma and forming a spermatium. E. Spermatium formation nearly completed. F. Spermatium with relatively large nucleus. (After Higgins.) Mycosphaerella fraxhiicola [Wolf (1939)] and M. nyssaecola [Wolf (1940, 1940a)]. Mycosphaerella jraxinicola is associated with Phyllosticta viridis and M. nyssaecola with P. nyssae; both of these species of Phyllosticta proyed to be not conidial stages but spermogonial stages. The conidial stage of species of xAIycosphaerella generally ap- pears during the pathogenic portion of their deyelopmental cycle, and the perithecial stage is initiated during late summer or fall and becomes mature during the follo^^'ing spring. Two distinct stromatic structures are concerned in perithecial formation, and both are initiated concurrently. One of these is the spermo- gonium, containing spermatia; the other is the perithecial primor- dium, containing within it one or more coiled ascogonia. Each 210 THE ASCOMYCETES ascofronium consists of a basal ascoo^onial cell and a terminal trichogynal portion that projects to the exterior. Whether the spermatia function in fertilization has not been determined, but indirect evidence indicates that they are necessary. For example, Fig. 79. Development of Mycosphaerella bolleana. A. Conidiophore fas- cicle of Cercospora bolleana. B. Variation in shape and septation of conidia. C. Young spermogonium just beginning to form spermatia. The stroma is still a loose tangle of hvphae without an outer wall of thick- walled cells. D. Young carpogonial locule with coiled ascogonium devel- oping coincidentallv with the spermogonium. Conidia of the Cercospora stage may be formed on both kinds of young stromata. E. Portion of base of mature carpogonial stroma with ascogenous hyphae and asci borne on ascogonium. (After Higgins.) the spermatia collect in a film or droplet at the spermogonial ori- fice, and, unless moisture is present to make possible their trans- fer to the archicarpic locules, perithecia are not produced. Furthermore, if material bearing the conidial stage is collected and kept indoors to dry for a month or more before being placed outdoors to hibernate, in most instances the perithecial stage will not develop, because of the lack of moisture in the form of dew or rain at the critical stage when spermatization should have been MYCOSPHAERELLACEAE 211 accomplished. If the leaves are occasionally moistened while they are maintained indoors, however, perithecia will develop. An ever-increasing body of evidence is available ^hich indi- cates that spermatia are commonly produced in iMycosphaerella. Some of the species known to possess spermatia are listed in Table 1, and spermatia have been observed in a number of others whose life histories are being elucidated. TABLE 1 Species of Mycosphaerella Known to Possess Spermatia Organism Host Observer Mycosphaerella Primus cerasus, Higgins (1914) nigerristigma '' P. pennsyhanica Klebahn (1918) Klebahn (1918)" Mycosphaerella Hier actum hieracii boreale Mycosphaerella Tilia cordata punctijormis f. tiliae Mycosphaerella Aesculus hippo- Klebahn (1918) hippocastani castanum Mycosphaerella Ficus carica Higgins (1920) bolleana Mycosphaerella lythr ace arum Mycosphaerella personata Punica grana- tum Vitis spp. Wolf (1927) Higgins (1929) Mycosphaerella Prunus cerasus Jenkins (1930) cerasella Remarks Spermogonia pycnidia- like and associated in late summer with the Septoria stage, often in same pycnidia. Micropycnidia associ- ated with the Ramu- laria stage. Bacteria-like conidia pro- duced in old stromata of the Cercospora stage or in separate pycnidia of Phyllosticta type. Called microconidia. Oc- cur interspersed with Septoria stages, and also produced in pure culture. Associated with Cercos- pora bolleana at close of season. Spermo- gonia pycnidia-like. Associated late in season with Cercospora lythra- cearum. Associated with Cercos- pora viticola during au- tumn. Spermogonia are pycnidia-like. Spermogonia are pyc- nidia-like and occur late, associated with the Cercospora stage in bases of conidial stromata. 212 THE ASCOMYCETES TABLE 1 (Confinuecf) Species of Mvcosphaerella Known to Possess Spermatia Organism Mycosphaerella areola Mycosphaerella cruenta Mycosphaerella berkeleyi Mycosphaerella arachidicola Mycosphaerella confusa Mycosphaerella arachnoidea Mycosphaerella per sic ae Mycosphaerella Jraxinicola Mycosphaerella cercidicola Mycosphaerella nyssaecola Mycosphaerella effigurata Mycosphaerella polymorpha Host Gossypium spp. Observer Ehrlich and Wolf (1932) Vigna sinensis Latham (1934) Arachis hypo- gaea Arachis hypo- gaea Rubus spp. Morus rubra Prunus persica Fraxinus spp. Cercis canaden- sis Nyssa spp. Fraxinus spp. Jenkins (1935) Plat anus occi- d en talis Jenkins (1935) Wolf (1935) W^olf (1936) Higgins and Wolf (1937) W^olf (1939) Wolf (1940, 1940a) Wolf (1940, 1940a) Wolf and David- son (1941) Smith and Smith (1941) Remarks Associated with Ramu- laria areola. Spermatia also developed in cul- ture. Associated with Cerco- spora cruenta at bases of old conidial stro- mata. Pycnidia-like spermogo- nia formed during au- tumn on lesions formed by Cercospora stage. Quite as the previous species. Associated with Cerco- spora rubi. Associated with Cerco- spora arachnoidea. Associated with Cerco- spora persica. Spermogonial stage had been identified as Phyl- losticta viridis. Associated with Cerco- spora cercidicola. Spermogonial stage has been called Phyllosticta nyssae. Associated with Mars- sonia Jraxini. Sper- mogonial stage identi- fied as Piggotia Jraxini. Associated with Stigmina polymorpha. The details of spermatial formation in this genus were first recorded by Higgins (1920). He found that the uninucleate spermatium mother cells, occurring in chains, become quadrinu- cleate; the protoplast then separates into four units but without wall formation. These units then migrate one at a time into a sterigma and are abstricted from its tip. After the mother cell is empty, its wall dissolves to become part of the mucoid matrix MYCOSPHAERELLACEAE 213 Fig. 80. Mycosphaerella jraxinicola. A. Mature spermogonium, in section, of "multilocular" appearance. This appearance may be accounted for be- cause, in spermatial formation, all chains of spermatiferous cells do not bear spermatia at the same time. B. Spermatium mother-cell whose content is quadrinucleate. Spermatia are abstricted as the mother-cell contents migrate into the sterigma seriatim. C. Multicellular ascogonium. D. Uninucleate nurse cells from the interior of the young perithecial locule. E. Mature ascus. F. Young perithecial locule containing three ascogonia. Both spermogonial and ascogonial locules develop coincidentally. 214 THE ASCOMYCETES which invests the entire mass of Hberated spermatia. This matrix swells in the presence of moisture, and as a result the spermatia are forced to the exterior of the spermogonium. Their germina- FiG. 81. Mycosphaerella cercidicola. A and B. Fascicles of conidiophores, the conidiophores tending to be coremioid. C. Germinating conidiophore. D. Germinating conidia. E. Vertical section of mature spermogonium. F. Vertical section of perithecial primordium with single archicarp. G. Ascus after elongation by rupture of outer ascal membrane. H. Mature ascospores. 7. Germinating ascospores. tion has not been observed. Each spermatium contains a single nucleus, so large that it practically fills the cell. These charac- teristics are interpreted to indicate that spermatia are male cells. Giiignardia. The best-known species of Guignardia is G. bid- ivelliiy causing black rot of grapes, endemic to North America and introduced into Europe about 1885. It was first described MYCOSPHAERELLACEAE 215 by Ellis in 1880 as Sphaeria bidwellii, and about a dozen other binomials have subsequently been applied to it. The most ex- tensive studies of this fungus are those of Reddick (1911). Its pvcnidial stage belongs to Phvllostictina and is characterized by large spherical to ellipsoidal hyaline but granular pvcnidiospores. These appear in lesions on leaves, canes, and berries. Reddick noted microconidia, produced in pycnosclerotia, which occurred among the true pycnidia, especially on shrivelled berries. These undoubtedly are spermogonia, and archicarpic sclerotia should be looked for, interspersed among the pycnosclerotia. In the spring, in the leaves and berries that have overwintered on the ground, are mature perithecia. They contain hyaline, unequally two- celled ascospores that become septate at time of maturing. Giiignardia baccae, possessing larger ascospores than those of G. bidnxeUii, is regarded as the cause of grape black rot in the Caucasus region. Undoubtedly still other species are responsible for diseases of muscadine grapes native to the southeastern United States. Ventiiria. Several species of \^enturia are concerned with scab diseases of pomaceous fruits. Of these V, inaeqiialis of apples, involving leaves, flowers, fruits, and twigs, is the most widely known. Its conidial stage, Fiisicladiinn dendriticiim, forms stro- matic cushions beneath the cuticle, and from their surface conidia are abstricted. The pathogen may hibernate in the conidial stage on twigs, but more commonly its survival is accomplished by the perithecial stage, which develops throughout the winter and matures in the spring in decaying leaves. The initiation of perithecia was described by Killian (1917) and has been confirmed in essential features by several investiga- tors. A coiled hypha arises within a fungus stroma. The cells at the periphery of this stroma are uninucleate, and their walls become thickened, v/hereas the inner cells remain thin-walled and multinucleate. One of these thin-walled cells produces a chain of cells, the ascogonium, each cell of which is bi- to quadrinu- cleate. The apical cell becomes clavate and is the trichogyne. Meanwhile, near the developing ascogonium another hyphal tip thickens and becomes lobate, and paired nuclei migrate into its lobes. This structure is the antheridium. Its growth continues until the lobes contact the trichogyne and become closely appHed to it. A pore then forms, and the antheridial content empties 216 THE ASCOMYCETES Fig. 82. Mycosphaerella mori. A. Conidia of Cercosporella stage. B. Germinating conidia. C. Fascicle of conidiophores. D. Perithecium in vertical section. E. Mature ascospores. F. Germinating ascospores. MYCOSPHAERELLACEAE 211 into the trichogyne. Septations in the ascogonial chain are then dissolved, whereupon the antheridial nuclei migrate to the asco- gonium and become associated in pafi's with the ascogonial nu- clei. After this stage ascogenous hyphae are developed as out- growths from the ascogonium. Meanwhile the uninucleate perid- FiG. 83. Ventiiria inaeqiialis. A. Edge of conidial stroma in vertical section. The conidial stage is commonly known as Fiisicladiiim dendriticiim. B. Section of perithecium innate in tissues of decaying leaves. C. Ascospores. D. The fertilized ascogonium (diagrammatic), showing the multinucleate condition after migration of nuclei from the antheridium. The septa of the ascogonium have been dissolved. (After Killian.) ial cells have multiplied to form the wall of the developing perithecium and the nurse tissue for the developing asci and paraphvses. Physalospora. Several species of Physalospora are involved in the production of important crop-plant diseases. These include P. cydoniae on pomaceous fruits [Hesler (1916)] and P. jiisca and P. rbodina on citrus [Stevens (1926)]. Physalospora cy- doniae, the cause of apple black rot, leaf spot, and canker, was shown by Hesler to possess a wide host range, including other 218 THE ASCOMYCETES pomaceous species and about a score of forest trees and shrubs. Its conidial stage is Sphaeropsis rimlonim. Physalospora fzisca and P. rhodina are associated with the imperfect Genus Diplodia. Fig. 84. Physalospora cydomae. A. Perithecium in section. B. Ascus and paraphvses. C. Ascospores. D. Pycnidium, in section, of Sphaeropsis ?nalorn7?2, the conidial stage. E. Conidia. F. Stages in conidial formation. (Adapted from Hesler.) Diplodia natalensis, a cause of stem-end rot of citrus, is the conid- ial stage of P. rhodina. Stevens (1926) regards P. gossypina, with its associated Diplodia gossypina, as synonymous with P. GNOMONIACEAE 219 rhodina. Sexuality in species of Physalospora has never been investigated. Attention may well be directed to the fact that the ascospores of some species of Phvsalospora have been described as hyaline and those of other species as yellowish. Hesler (1916) states that those of P. cydoniae are yellowish. There remains the likeHhood that all species having Sphaeropsis, Diplodia, or other conidial stages with dark spores will be found to have pigmented asco- spores. Mature ascospores must be examined. Ophiobohis. The most important member of the Genus Ophi- obolus is O. cariceti var. graviiniSy causing take-all disease of cereals and grasses. This disease was first reported in the United States in 1920 but was known long before that date in Australia, Europe, and Africa. Its causal fungus was first described as Sphaeria cariceti from England in 1861. Essential facts regarding the disease are contained in a report by Kirby (1925) and regard- ing the development of the pathogen in a report by Jones (1926). Ophiobohis cariceti produces spermatia, which Jones regards as functionless, in association with perithecial primordia contain- ing coiled ascos^onia. Thev too are regarded as abortive, and fertilization is apogamous, involving vegetative cells. From these conjugated vegetative cells the ascogenous hyphae arise. Nuclear fusion is not antecedent to ascus formation, and meiosis occurs with the first division of the primary nucleus of the ascus. Since Gjiomojiia erythrostoma has a similar type of development, Jones suggested that O. cariceti be placed among the Gnomoniaceae. In the opinion of the present authors both of these organisms should be reinvestigated in regard to the function of spermatia. Gnomoniaceae. The Gnomoniaceae resemble the Myco- sphaerellaceae in that their perithecial walls are of similar texture; the perithecia of both are embedded within the substratum, but those of the Gnomoniaceae have ostiolar necks that project much more prominently. The asci of Gnomoniaceae possess thick apices provided with a canal. Gnomonia and Glomerella, both of which contain a considerable number of destructive plant pathogens, have been extensively studied and are worthy of more than passing mention. Their conidial stages, belonging to the imperfect genera Gloeosporium, Colletotrichum, and xMarssonia, produce diseases known as anthracnoses. The conidia of anthrac- 220 THE ASCOMYCETES *nose fungi usually become uniseptate as an initial step in germina- tion. At the apex of the germ tube, moreover, a thick-walled, dark organ of attachment, called an appressorium, develops. The appressoria anchor the organism during host penetration. Ap- pressoria are developed in culture and on the host in Glomerella but have never been observed in Gnomonia. A few of the best-known members of this family include Gnomo7iia erythrostoma on cherry [Brooks (1910)], G. lep- FiG. 85. . Diaporthe chri. A. Pycnidial stage (diagrammatic) of Fhomopsis citri, in section, bearing two kinds of spores, oval ones that germinate and thread-like ones, stylospores or scolecospores, that have not been found capable of germination. B. Conidia. C. Stylospores. D. Germinating conidia. E. Diagram of perithecial stroma in section bearing long-beaked perithecia. F. Ascus with thickened apex. G. Germinating ascospores. tostyla on w^alnut, G. veneta on sycamore [Klebahn (1905, 1918), Edgerton (1908)], G. iilmea on elms [iMiles (1921), Pomerleau (1938)], Glomerella cingiilata on apple [von Schrenck and Spaulding (1903), Shear and Wood (1913)], G. gossypii on cotton, G. lagenaria on melons, G. Undeumthimia on beans, and G. glycines on soybeans. Details of perithecial development among the species just men- tioned are best known for Giwmonia erythrostoma. Brooks (1910) observed that this organism possesses filamentous sper- matia, borne in pycnidia, W'hich he deemed functionless. Asco- gones bearing trichogynes are also formed, but the trichogynes GNOMONIACEAE 221 do not function in fertilization. Brooks suggested that instead thev mav serve as respiratory channels. His evidence led him to doubt that the ascogonia give rise to ascogenous hyphae. D E m00mm Mwm Fig. 86. Endothia parasitica. A. Diagrammatic section of pycnidial stroma. B. Section of the inner wall of pycnidium, showing conidiophores and conidia. C. Perithecial stroma of E. parasitica in section. D. Ascus of E. parc.dtica. E. Ascospores. (A and C from Heald, B, D, and E from Anderson and Rankin.) x\scoCTonial coils in Gno7noma iilmea were observed by Miles (1921) and Pomerleau (1938), but these workers did not account for the manner in which the ascogonial cells become binucleate. 222 THE ASCOMYCETES Gnomonia leptostyla produces bacillar spermatia in acervuli con- currently with the conidial stage, Marssoiiia jiiglmidis. Klebahn (1905) first connected a Gloeosporium with Gno- monia in his study of the sycamore-blight pathogen. The conid- ial stage, causing the buds to blight and necrotizing strips on either side of the veins of older leaves, is known as Gloeosporimn nerviseqinim. The stage blighting the twigs is known as Myxo- sporiimi valsoideiim. On fallen leaves cleistocarpous pycnidia are produced and are known as Sporonema platani. This last- named stage may prove to be spermogonial. Klebahn listed six- teen names in synonvmy of Gnovwma veneta, and Edgerton (1908) added two others. The sycamore-blight pathogen grown on oaks, which Stoneman (1898) and Edgerton (1908) regarded as hosts, has much longer perithecial beaks than when it is grown on sycamore. Stoneman (1898) determined that Gloeosporium cingiilatinn occurring on privet has a perithecial stage for which she em- ployed the generic name Gnomoniopsis. Von Schrenck and Spaulding (1903), in connection with studies on apple bitter rot, found that the perithecial stage occurs on limb cankers and on decaying fruits. They found furthermore that the apple pathogen belongs in the Genus Gnomoniopsis, as described by Stoneman, but, because of preoccupation of Gnomoniopsis, they established in its stead the Genus Glomerella. Some regard the organism on privet and that on apple as specifically identical; support for this belief comes from extensive studies by Shear and Wood (1913). They found it on avocado, cinnamon, coffee, cocoa, cranberry, dewberry, ebony, fig, grape, guava, loquat, mango, and tea. Other workers contend that species of Glomerella have greater host specificity than is indicated by Shear and Wood's studies. Edgerton (1914) secured evidence of heterothallism in strains of Glomerella, isolated from Fopiihis deltoides and Ipomoea pur- purea. These isolates appeared indistinguishable from the apple- bitter-rot fungus. By mating strains he secured rows of perithe- cia on the boundary Hne between colonies cultured in Petri dishes. The perithecial stage of certain species of Glomerella has never been observed except on host tissues. Others, however, such as the bean-anthracnose fungus and the watermelon-anthracnose fungus, appear never to have been observed except in artificial GNOMONIACEAE 223 Fig. 87. Initiation of perithecia in Endothia parasitica. (From Anderson and Rankin.) A, B, and C. Coiled ascogonia, invested with loosely ar- ranged fungous tissue that makes up the central portion of the primordium. Many primordia occur within each stroma. D, E, and F. Densely staining multinucleate cells composing the basal portion of the ascogonia. G. Multi- cellular, multinuclear ascogonium, viewed laterally, the upper portion being a part of the slender trichogyne. H. Stroma with ascogonium at center, viewed from above. /, /, and K. Degeneration of ascogonial base and trich- ogyne with no evidence of formation of ascogenous hvphae. L. Young perithecium, a complex of fungus cells all quite alike. 224 THE ASCOAIYCETES culture. The genus is therefore well adapted to cytologic and genetic studies, matters on which essentially nothing is at present known. Fig. 88. Structure of Gloinerella glycmes. A. Diagram of three perithecia borne innately on dead stems of soybean. B. Ascus. C. Germinating ascospores with resultant formation of appressoria. D. Conidia (Colleto- trichinn glycines) from pustules on living pods and stems. E. Appressoria formed from germinating conidia. F. Infection from conidium. The in- fection hypha penetrates the host cell wall by a narrow tube formed immediately below the appressorium. DiAPORTHACEAE. The Diapotthaceac comprise a group of over 1000 species of stromatic Sphaeriales. Most of them are sapro- phytic, but in this family is Endothia parasitica, ^\ hich, within a period of about 30 years, spread throughout the entire Appa- lachian region and practically accomplished the extinction of DIAPORTHACEAE 22S American chestnut. Other important pathogenic species are in- ckided in Diaporthe and \^alsa. Of these species Diaporthe citri, D. phaseolonmi, D. sojae, and Valsa leiicostovm are of interest. The conidial stages of species of Diaporthe belong to Phomopsis; of \^alsa, to Cytospora. Fig. 89. The svcamore-blight fungus, Gnovwnia veneta. A. Perithecium in section. B. Ascus and ascospores. C. Conidial stage, commonly desig- nated Gloeosporhmi nerviseqimni, on young leaves. D and E. Secondary spore stages that mav prove to be spermogonia. D, on rotting leaves, re- garded as Myxosporhnn valsoidewn (Discella platani) ; E, on t\vigs, desig- nated Sporojievia platani. {A, C, D, and E adapted from Klebahn.) Diaporthe citri [Wolf (1926)] causes melanose, dieback, and stem-end rot of citrus. Perithecia have been observed only on twigs lying on the ground. The conidial stage of this species is known as Fhoinopsis citri. Diaporthe phaseolonnn [Harter (1917)] attacks stems, pods, and leaves of Lima bean. Perithecia mature on old pods in the late summer. The conidial stage has been designated Fhoina 226 THE ASCOMYCETES siibcincta and Fhyllosticta phase olina, but Harter showed that this stage properly belongs with Phomopsis, since both ellipsoidal conidia and stylospores are produced. Diaporthe sojae was found bv Lehman (1923) to be seed-borne and to involve leaves, pods, and stems of soybean. Its ascigerous stage has been developed in pure culture. Valsa leiico St 0777a produces its stromata within the bark of the trunk and twigs of stone fruits. The stromata protrude at ma- uirity and in coming to the surface cause the host to appear silvery. Rolfs (1910) found that this organism attacks trees weakened bv freezing, bv drought, and by lack of an adequate supply of minerals. Although numerous reports of studies of Endothia parasitica have been published, adequate acquaintance with this organism can be gained by perusal of those by Anderson (1914), Ander- son and Rankin (1914), and Shear, Stevens, and Tiller (1917). This organism was described as Diaporthe parasitica by Murrill in 1906, although Alerkel reported its presence in New York 2 years earher. In 1913 the plant explorer Aleyer found it in northern China, whence it had probably been imported to the United States. Endothia parasitica causes the formation of cankers on twigs, larger branches, and trunk. The mycelium spreads within the cambium of these parts, girdling and killing them. The pycnidia arise from a loose tangle of hvphae, the central branches of \\'hich become conidiophores. This hyphal mass becomes stromatic, and pycnidia are produced near the surface. Conidia are ex- truded in tendrils if moisture is present. The perithecia form from more deeply seated parts of the same stromata. First there is a coiled ascos^onium with a functionless trichooryne. Around this ascogonium are enveloping hvphae, whose cells are deeply staining. These enveloping hyphae produce the perithecial loc- uli, the innermost of which nourish the developing asci. De- tails re^ardin^ fertilization are unknown. The taxonomic monograph by Wehmever (1933) is a basis for study of the Genus Diaporthe; that by Shear, Stevens, and Tiller (1917), for study of Endothia. The closely related genera Melanconis, Pseudovalsa, Prosthecium, and Titania are taxonom- ically treated by Wehmeyer (1941). ALLANTOSPHAERIACEAE 221 ALLANTOSPHAERIACEAE. This family is also stromatic; some of its members are to be found among the Valsaceae and Diatry- paceae, as used in older literature. They occur as saprophytes or weak parasites on woody plants. As the family name indicates, i^?Z^^ D Fig. 90. Nimmmlaria discreta, the apple blister-canker fungus. A. Diagram showing disk-shaped black stromata that protrude through fissures in the bark. B. Sectional diagram of perithecial stroma; the outer rind is compact and dark, and a black ring remains in the wood when a stroma is broken off. The flask-shaped perithecia open to the surface by pores. C. Ascus and dark ascospores. D. Laver of conidiophores and conidia at surface near a perithecial pore. (After J. R. Cooper.) the ascospores are allantoid. The asci are long-stalked. The paraphvses usually jellify at maturity. The family may further be characterized as havingf ectostroma that is usually deciduous and a persistent entostroma. The ectostroma develops at the sur- face and within the periderm and consists of fungus elements and remnants of periderm. The entostroma develops within the cortex or woody tissues and contains remnants of these tissues. 228 THE ASCOMYCETES Usually the ectostroma is deciduous and may bear the conidial stage. When it is thrown off, the entostroma is exposed. The perithecia are sunken in the entostroma, the ostiolar necks ex- tending to the surface. The ostioles may be separate or may open collectively into a few passages. The stromata are cushion- shaped or even broadly effuse. In some species the substratum is not greatly modified in the formation of the entostroma, and its periphery is indicated by a definite dark line. Diatrype and Diatrvpella are the most commonly encountered representatives of this family. They differ mainly in that Dia- trype has eight-spored asci, whereas the asci of Diatrypella are polysporous. Acquaintance with this family and its relationship with the Diaporthaceae may be gained from the work of Weh- meyer (1926, 1933, 1941). Xylariaceae. The stromata of Xylariaceae are well developed and are entirely fungal in composition. They are nearly always exposed from the beginning and in youth are covered by a conid- ial layer. The stromata are cushion-shaped or crustose in such representative genera as Hypoxylon and Daldinia but are erect and club-shaped or variously branched in Xylaria. Nearly all are saprophytic on woody substrata. A few, how- ever, cause important diseases of trees, notably Xylaria mali^ which produces a black root-rot disease of apples [Fromme (1928)] and Nimnmilaria discreta, which causes apple-tree canker [Cooper (1917)]. Hypoxylon, with broadly effuse to hemispherical stromata, is the largest genus, containing over 200 species. Daldinia, mono- graphed by Child (1932), has concentrically zonate stromata that may be 3 to 5 cm In diameter. Niinnmdavia discreta forms stro- matic cushions 3 to 6 mm across, which are seated on the wood but protrude through the bark. When the stromata break away, a black ring remains in the wood. Xylaria polymorpha forms thick, black clubs 6 to 8 cm tall, and X. hypoxylon forms stag- horn-shaped stromata 3 to 4 cm tall. Little is known about the development of any members of this family, although the grosser features of X. polymorpha and X. hypoxylon were studied by Fisch as long ago as 1882 [Brown (1913)]. Xylaria tentaciilata was found by Brown (1913) to be parthenogenetic. Ascogonial coils form in the young stromata, XYLARIACEAE 229 Fig. 91. Ophiobohts cariceti, cause of take-all of wheat. A. Spermogonium in section. Speimatia are pear-shaped and curved. B. Portion of initial of perithecium. The hyphae make a loose aggregate, in the center of which are coiled ascogonia with deeply staining cells. C. Mature perithecium, in diagram, lying obliquely and entirely immersed within the tissues, except for the tip of the beak. D. Mature ascus. The asci are extruded intact during wet periods and collect in a mass at the tip of the beak. (A and B adapted from Jones.) 230 ' THE ASCOMYCETES and the ascogonium, uninucleate at first, comes to have twenty or more nuclei. The ascogenous hyphae arise as outgrowths from the ascogonium. LITERATURE CITED Ahrexs, W. E., et al., "A list of references to literature on the Dutch elm disease." 29 pp. (iMimeographed.) U. S. Dept. Agr., Dutch Elm Disease Laboratory. Morristown, N. J. 1935. Ames, L. M., "Hermaphroditism involving self-sterility and cross-fertility in the Ascomycete, Pleiirage anserina,^' MycoL, 26: 392-414, 1934. Anderson, P. J., 'The morphology and life history of the chestnut-blight fungus," Co77mtisswn for the Investigation and Control of the Chestnut- Tree-Blight Disease in Peiinsyhajiia, Bull. 7. 44 pp. 1914. Anderson, P. J., and W. H. Rankin, "Endothia canker of chestnut," Cor- nell Agr. Expt. Sta. Bull., 341: 530-618, 1914. Andrus, C. p., and L. L. Harter, "Alorphology and reproduction in Cera- tostoiJiella fivibriata,^'' J. Agr. Research, 46: 1059-1078, 1933. "Organization of the unwalled ascus in two species of Ceratostomella," /. Agr. Research, 54: 19-46, 1937. Backus, M. P., "The mechanics of conidial fertilization in Neiirospora sitophila,^'' Bull. Torrey Botan. Club, 66: 6}-76, 1939. Brooks, F. T., "The development of Gnomonia erythrostoma^'' Ann. Bot- any, 24: 585-603, 1910. Brown, H. B., "Studies in the development of Xylaria," Ann. MycoL, 11: 1-13, 1913. BuiSMAN, Christine, ^^Ceratostomella iilnii, de geschlachtelijke vorm van Graphiimi ulmi Schwarz," Tijdschr. over Phvitenziekteji, 38: 1-5, 1932. Child, Marion, "The genus Daldinia," Ann. Mo. Botan. Garden, 19:^29- 496, 1932. Chivers, a. H., "A monograph of the genera Chaetomium and Ascotricha," Me77i. Torrey Botan. Club, 14: 155-240, 1915. Clinton, G. P., and Florence A. McCormick, "Dutch elm disease, Graphium idmi;' Conn. Agr. Expt. Sta. Bull, 389: 701-752, 1936. CoLSON, B., "The cytology and morphology of Neurospora tetrasperma Dodge," Ann. Botany', 48: 211-22^, 1934. Cooper, J. R., "Studies of the etiology and control of blister canker on apple trees," Nebr. Agr. Expt. Sta. Bidl, 12. 117 pp. 1917. Dodge, B. O., "Nuclear phenomena associated with heterothallism and homothallism in the ascomycete Neurospora," /. Agr. Research, 35: 289-305, 1927. "The non-sexual and sexual functions of microconidia of Neurospora," Bidl. Torrey Botan. Club, 5P: 347-360, 1932. "The mechanics of sexual reproduction in Neurospora," MycoL, 27:418- 438, 1935. Edgerton, C. W., "The physiology and development of some anthracnoses," Botan. Gaz., 45: 367-407, 1908. LITERATURE CITED 231 "Plus and minus strains in the genus Glomerella," Am. J. Botan., 1: 244- 254, 1914. Ehrlich, John, and F. A. Wolf, "Areolate mildew of cotton," Phytopa- thology, 22:229-240, 1932. Elliott, J. A., "A cytological study of Ceratostoviella fijubriata (E. and H.) Elliott," Phytopathology, iJ; 417-422, 1925. FiTZPATRicK, H. M., "Monograph of the Nitschkieae," MycoL, iJ; 23-44, 45-67, 1923. Fromme, F. D., "The black-root-rot disease of apple," Va. Agr. Expt. Sta. Bull., 34: 5-52, 1928. Griffith, D., "The North American Sordariaceae," Meui. Torrey Botan. Club, 11: 1-134, 1901. Harter, L. L., "Pod blight of the Lima bean caused by Diaporthe phase- oloritm,'' J. Agr. Research, ii: 473-504, 1917. Heald, F. D., and F. a. Wolf, "The whitening of the mountain cedar, Sabma sabinoides (H.B.K.) Small," Mycol., 2:205-211, 1910. Hesler, L. R., "Black rot, leaf spot, and canker of pomaceous fruits," Cor- jiell Agr. Expt. Sta. Bull., 575^:51-148, 1916. HiGGiNs, B. B., "Life history of a new species of Sphaerella," Mycol. Centrb., 4: 187-193, 1914. "Morphology and life history of some of the Ascomycetes, with special reference to the presence and function of spemiatia," Am. J. Botany, 7:435^H4, 1920. "Morphology and life history of some Ascomycetes, with special ref- • erence to the presence and function of spermatia, II," Am. J. Botany, id: 287-296, 1929. HiGGiNS, B. B., AND F. A. Wolf, "Frosty mildew of peach," Phytopa- thology, 27:690-696, 1937. Jeffers, W. F., "Studies on Caryospora putaminum,^'' Mycol., 32: 550-566, 1940. Jenkins, W. A., "The cherry-leaf-spot fungus, Mycosphaerella cerasella Aderh., its morphology and life history^" Phytopathology, 20:329-337, 1930. "Two fungi causing leaf spot of peanut," /. Agr. Research, S6: 317-322, 1935. Jolivette-Sax, H. D. M., "Spore formation in Philocopra coeruleotecta^'' Am. J. Botany, J: 61-78, 1918. Jones, S. G., "The development of the perithecium of Ophiobolus gra^ninis Sacc," Ann. Botany, 40:607-629, 1926. Killian, C, "Uber die Sexualitat von Venturia inaequalis,^'' Z. Botan., 9: 353-398, 1917. KiRBY, R. S., "The take-all disease of cereals and grasses caused by Ophi- obolus cariceti (Berkeley and Broome) Saccardo," Cornell Agr. Expt. Sta. Mem., 88. 44 pp. 1925. Klebahn, H., "Untersuchungen iiber einige Fungi Imperfect! und die zuge- horigen Ascomycetenformen," Jahrb. iviss. Botan., 41: 515-55S, 1905. Haupt- und N ebeiTJruchtformen der Ascomyceteri. 395 pp. Gebr. Borntrager, Leipzig. 1918. 232 THE ASCOMYCETES Latham, D. H., "Life history of a Cercospora leaf-spot fungus on cow- pea," My col, 26:S\6-Sll\ 1934. Lehman, S. G., "Pod and stem blight of soybean," Ajin. Mo. Botan. Gar- den, 10: 111-178, 1923. Lewis, L M., "The development of spores of Fleurage zygospora," Bota?i. Gaz., SI: 369-373, 1911. AL\RTiN, G. W., "A key to the families of fungi, exclusive of the lichens," Uuiv. loiva Studies, 27:83-115, 1936. .Miles, L. E., "Leaf spots of the elm," Botan. Gaz., 77:161-196, 1921. Po-merleau, R., "Recherches sur le Gnovionia iduiea (Schw.) Thiim," Con- trib. inst. hot. Univ. Montreal, 31. 139 pp. 1938. Reddick, D., "The black-rot disease of grapes," Cornell Agr. Expt. Sta. Bidl., 293:289-36^, 1911. Rolfs, F. AL, "Winter killing of twigs, cankers, and sun scald of peach," Mo. Fruit Sta. Bidl, 77:9-101, 1910. ScHEFFER, T. C, AND R. M. LiNDGREN, "Stains of sapwood and sapwood products and their control," U. S. Dept. Agr. Tech. Bidl., 114. 123 pp. 1940. ScHRENCK, H. VON, AND P. Spaulding, "The bitter rot of apples," U. S. Dept. Agr., Biir. Plant hid. Bull., 44. 54 pp. 1905. Seaver, F. J., "Fimetariales," North Am. Flora, 3: 57-88, 1910. Shear, C. L., N. E. Stevens, and Ruby J. Tiller, ''Endothia parasitica and related species," U. S. Dept. Agr. Professional Paper Series, Bull. 380. 82 pp. 1917. Shear, C. L., and Anna K. Wood, "Studies of fungous parasites belonging to the genus Glomerella," Bur. Plant hid. Bidl., 252. 110 pp. 1913. Smith, D. J., and C. O. Smith, "Species of Stigmina and Stigmella occurring on Platanus," HUgardia, 14:205-231, 1941. Stevens, N. E., "Two species of Phvsalospora on Citrus and other hosts," My col., 18:206-217, 1926. Stoneman, Bertha J\L, "The comparative development of some anthrac- noses," Botan. Gaz., 26:69-120, 1898. Wehmeyer, L. E., "A biologic and phvlogenetic study of stromatic Sphaeri- ales," A?7i. }. Botany, 13: 574-645, 1926. "The genus Diaporthe Nitschke and its segregates," Univ. Mich. Studies, Sci. Ser., 9. 349 pp. University of .Michigan Press, Ann Arbor, Mich. 1933. A revision of Melanconis, Pseudovalsa, Prosthecium, and Titania. viii -|- 161 pp. University of Michigan Press, Ann Arbor, Mich. 1941. Wolf, F. A., "The perfect stage of the fungus which causes melanose of citrus," /. Agr. Research, 33:621-625, 1926. "Pomegranate blotch," /. Agr. Research, 55:465-469, 1927. "The perfect stage of Cercospora rubi,'" MycoL, 27: 347-356, 1935. "False mildews of red mulberry," MycoL, 28: 268-277, 1936. "Leaf spot of ash and Phyllosticta viridis," MycoL, 31: 258-266, 1939. "Cercospora leaf spot of red bud," MycoL, 32: 129-136, 1940. "A leaf-spot fungus on Nyssa," MycoL, 52:331-335, 1940a. A'S^OLF, F. A., AND R. W. Davidson, "Life cycle of Piggotia fraxini, causing leaf disease of ash," MycoL, 55:526-539, 1941. LABOULBENIALES 2S3 Laboulbeniales The Laboulbeniales comprise a group of peculiar pyrenomyce- tous fungi that are obligate parasites of insects. Knowledge of the group, in which some 50 genera and 1250 species are known at present, is almost entirely the result of the researches of Thax- ter (1895, 1908, 1924, 1926, 1931). Although most members of the order are parasitic upon Coleoptera, a few are to be found upon Hymenoptera, Diptera, and other groups of insects. The Laboulbeniales are characteristically ectoparasites upon the chitinous exoskeleton or integument of their hosts. The various species of fungi are limited not only to definite host genera and species, but also in a few instances to a definite and restricted area upon its host; for example, some species occurring upon the right wing cover of a beetle are not to be found in a corresponding position upon the left elytron. The plant body is attached to the chitinous integument by means of a "foot," which in the vast majority of species does not penetrate within the body cavity of the insect. Hence, unlike most other ento- mogenous fungi, the Laboulbeniales are not fatal to their hosts, which suffer little injury from infection. The role of the foot in the nutrition of the fungus is a question much in dispute. The plant body consists essentially of a row of cells, arising from the foot, bearing a female reproductive branch and giving rise laterally to filamentous appendages on which are borne the antheridia. Reproduction. Sterile appendages similar to those bearing an- theridia may occur throughout the order. It is upon the basis of the antheridia that the Laboulbeniales have been classified. Uninucleate spermatia are produced throughout the order. In the primitive Family Ceratomycetaceae the spermatia are borne exogenously on the antheridial branches. In the Laboulbeniaceae the spermatia are formed endogenously within flask-shaped an- theridia. In the Peyritschiellaceae the antheridia are compound, and the endogenous spermatia are discharged into a common cavity. The female reproductive branch, or archicarp, consists of a trichogyne, trichophore cell, and carpogenic cell. The carpo- genic cell produces from 1 to 32 ascogenous cells; ascogenous 234 THE ASCOMYCETES RELATIONSHIP 23$ hyphae, as such, are absent. Eventually each ascogenous cell becomes an ascus and forms 4 to 8 ascospores. Although the attachment of the spermatia to the trichogynes has been observed in many species, the details of fertilization are unknown. The cytological investigations of Faull (1911, 1912) were unfortunately made upon two parthenogenetic species, La- boitlbenia chaetophora and L. gyrwidanmi, in w^hich nuclear fusion was observed to occur in the young ascus. Although 3 nuclear divisions give rise to 8 nuclei, 4 of these soon degenerate, and the mature ascus contains 4 ascospores. The mature ascospore has 2 unequal cells; the larger is cov- ered with a gelatinous material which attaches the spore to its host. No conidia or other spore forms are to be found. A num- ber of genera and species of the group are dioecious; in these forms the ascospores are discharged in pairs and develop into separate male and female plants growing close together on the host. Relationship. The Laboulbeniales have been prominently mentioned by those who support the red-algal theory of the origin of the Ascomycetes. The presence of spermatia and trichogynes and of sterile cells surrounding the procarp (archi- carp) in both groups is certainly a striking instance of parallel development, if nothing more. Furthermore, the protoplasts of adjacent vegetative cells are frequently connected through pores. Yet the difficulty of homologizing the asci with any structure in the Rhodophyceae and the differences in chemical composition of the cell ^^•alls in the two groups are strong arguments against the supposed relationship. It is perhaps better to regard the Fig. 92. Various Laboulbeniales. A. Mature plant of Stigviatomyces baeri, having both antheridial and ascogonial branches. The spermatia are being shed and some are attached to the trichogyne. B. Two mature plants of Amorphomyces falagriae, the one at the left ascogonial, at the right anthe- rial. C. Ascus of Stigmatoinyces baeri. D. Ascospore of S. baeri, with gelatinous envelope. E. Early development from the ascospore in which foot-like attachment disk has formed. F. Young thallus of 5. baeri, with foot, stalk cell (from basal cell of ascospore) and three vegetative cells from upper cell of ascospore. G. Amorpboviyces africanus, illustrating spermatial formation among the Ceratomycetaceae. H. Rhynchophoro- Tnyces rostratiis, illustrating spermatial formation among the Laboul- beniaceae. /. Stig7nato77iyces baeri, illustrating spermatial formation among the Pevritschiellaceae. (Adapted from Thaxter.) 236 THE ASCOMYCETES Laboulbeniales as reduced and specialized forms, differing rather widely from other Ascomycetes. LITERATURE CITED Faull, J. H., "The cytology of the Laboulbeniales," Aim. Botany, 25: 649- 654, 1911. "The cytology of Laboitlbenia cbaetopbora and L. Gyrmidanmi,^'' Ann. Botany, 26:125-155, 1912. Thaxter, R., "Contribution to\vard a monograph of the Laboulbeniaceae," Part 1, Mem. Am. Acad. Arts Sci., 12^95-^29, 1895; Part 2, i5;219- 469, 1908; Part 3, i-/; 309-426, 1924; Part 4, 2 T; 427-580, 1926; Part 5, 16: 1-435, 1931. Heijjisphaeriales The Hemisphaeriales comprise an artificial assemblage of five families which resemble both Pyrenomycetes and Phacidiales and are therefore regarded as intermediate between the pyreno- mycetous and discomycetous fungi. Their fructifications are shield-shaped, lack ostiola, and hence rupture irregularly, and their supporting hyphae are for the most part radiately arranged. Certain mycologists have res^arded such fructifications as the lower half of inverted perithecia, the morphologic base being attached to the hyphae above and the upper part having atro- phied in response to protection afforded by attachment to the host tissues. To such structures, the name thyriothecia has been applied. The Hemisphaeriales generally are parasitic on leaves of plants. The larger number are tropical, but collectors familiar with the order are finding them not uncommon in the Temperate zones. Relatively few are known to possess conidial stages. In their monographic treatment Theissen and Sydow (1917) recognize over 300 species in 111 genera, arranged in 5 famihes and dis- tributed as follows: Stigmateaceae, 11 genera; Polystomellaceae, 39; Microthyriaceae, 36; Trichopeltaceae, 6; and Hemisphaeria- ceae, 19. In the arrangement of Theissen and Sydow the families are separated on the following bases: 1. Fructification (shield) radially constructed 2 2. Mycelium thread-like, either not abundant or else wanting 3 3. Ascomata largely internal 4 4. Ascomata subcuticular Stigmateaceae 4. Ascomata superficial but hypostromata internal Polystomellaceae MICROTHYRIACEAE 237 3. Ascomata and assimilatorv hvphae superficial Alicrothyriaceae 2. Mycelium membranaceous and radially anastomosed Trichopeltaceae 1. Fructification (shield) not composed of radially arranged elements Hemisphaeriaceae Little regarding the developmental history of Hemisphaeriales is known, and generalizations concerning them will be possible only when a reasonably large number have been adequately studied. Studies of their gross structure, such as those of Arnaud (1918), have been made by using herbarium specimens. Al- though such studies are very valuable, they are not sufficient to establish relationships ^\'ithin the order or to determine their phylogeny. Stigmateaceae. The Genus Stigmatea is the best-known rep- resentative of this family. Klebahn (1918) studied several species, including S. robertiani, occurring on Geraniiini roberti- animt. He noted that this species forms leaf spots during late summer and fall and that the pathogen forms a membranaceous layer beneath the cuticle. During the winter this layer thickens at certain points, these thickened areas (stromata) becoming fructifications that mature in the spring. Killian (1922) described the occurrence within youns^ stromata of a uninucleate anther- idial cell and a uninucleate ascogonial cell whose protoplasts fused through a papillar passage. After several divisions of each of the nuclei, fusion in pairs took place; the diploid nuclei then migrated into ascogenous hyphae arising from the ascos^onium. Several functional asco^onia may be formed within each stroma. It is probable that this type of sexual apparatus does not occur in all species of Stigmatea, for in S. potentillae conceptacles that appear to be spermogonia have been observed. MicROTHYRiACEAE. In this family the radiate nature of the fructifications is best developed. The position of the family has been much in dispute, however, as is indicated by the fact that in Sylloge Fiingonnn Saccardo placed it first among the Dothi- deales; then it was shifted among the Ervsiphales; and finally Theissen (1913, 1913a) and Theissen and Sydow (1917) included it in their new order, Hemisphaeriales. Doidge (1920) and Ryan (1926) accept this classification among the Hemisphaeriales, but Arnaud (1918) would place it near the Myriangiales. Ryan (1926) found that the ascocarps of Microthyriaceae may arise either from a mycelial cell, a hyphopodium, a lateral my- 238 THE ASCOMYCETES Fig. 93. Morenoella qiierci?ja. A. Spermogonia and young ascocarps formed on the mycelium occurring on the upper surface of oak leaves. B. A voung shield-shaped ascocarp, together with supporting mycelium. C. Cross-section of ascocarp, showing asci forming singly within the super- ficial stroma. D. Mature two-celled ascospores. E. Mature spermogonium bearing rod-shaped spermatia. The spermatiophores form a layer at the base of the spermogonium. F. Spermatiophores and spermatia. G. Vertical section of mature ascocarp. Ascocarp superficial, nutritive hyphae sub- cuticular. (Courtesy of E. S. Luttrell.) MICROTHYRIACEAE 239 celial branch, or a nodulate cell. Her data on this point are summarized in Table 2. TABLE 2 Origin of Ascocarps Among Microthyriaceae Development from Genus Mycelial cell Hyphopodium Lateral branch 1 Nodulate cell Asterina 35 3 2 2 Asterinella 6 1 1 Amazonia 1 1 Aulographum 1 Caulothyriopeltis 3 Echidnodes 3 Echidnodella 5 Englerulaster 2 1 Lembosia 10 Morenoella 16 Questieria 1 1 The cells of the fructification are dark brown, being lighter at the periphery, and are laid down in rows. This radiate charac- teristic persists but may not be discernible in some genera unless the material is cleared by boiling in potassium hydroxide. In other genera the color is so dense as to be carbonaceous, making it impossible, even by use of a clearing reagent, to determine the arrangement of cells. In still other genera the central cells gelatinize. Aloreijoella qiiercina, commonly occurring in the southeastern United States on the foliage of various species of red oaks and black oaks, is the most thoroughly known species of Micro- thyriaceae. Luttrell (1940) observed that its mycelium is en- tirely superficial during the early summer and that the hyphae may fragment in a toruloid manner, each element being presum- ably capable of functioning as a conidium. By late summer sub- cuticular hyphae are present. By the time the leaves are shed, spermogonia and ascocarp initials are produced coincidentally in separate structures on the same superficial mycelium. Both structures are dimidiate, with a flat cushion of fertile cells formed beneath the shield. The spermogonia are ostiolate and shed spermatia through the pore. Whether the spermatia function is not known, and ascogenous hyphae have not been observed. Each ascus arises individually and creates a loculus within the 240 THE ASCOMYCETES rt O^ « tin S REMAINING FAMILIES 241 Stroma by absorbing or crushing adjacent cells. By spring the asci are mature; then the shield becomes fissured and the asci are thereby exposed. MoreiweUa vioUemdeae is represented by Arnaud (1918) as possessing spermogonia resembling those described by Luttrell (1940). Such spermogonia have been shown to occur also among species of Asterina. More should be learned regarding their possible role in fertilization. Remainixg families. The Polystomellaceae possess ascocarps that expose the asci through a linear aperture, and for this reason the family has been regarded as related to the Hysteriales. Ap- parently all genera are tropical as are also the Hemisphaeriaceae. Theissen (1913, 1913a) divided the Hemisphaeriaceae into two tribes, using the structure of the shield, whether net-like or knotted, as the basis for separation. In this family the asci are scattered, one in each loculus. The Trichothyriaceae, monographed by Theissen (1914), are typified by Trichothyrhim sarcinijenim, described by Spegaz- zini in 1889. This species grows upon Aleliola, one of the genera of sooty molds. Certain other members of the family parasitize stromatic Sphaeriales. Approximately a score of species, all tropical, have been described. LITERATURE CITED Arnaud, G., Les Asterinees. Theses presentes a la Faculte des Sciences de Paris. 288 pp. 1918. DoiDGE, Ethel AI., "South African Alicrothyriaceae," Trans. Roy. Soc. South Africa, 8: 235-282, 1920. KiLLiAN, C, "Le developpement du Stiginatea robertiani Fries," Rev. gen. hotam, 34:511-5^^, 1922. Klebahn, H., Haiipt- and N ehenfrncbtforvien der Ascomyceten. 395 pp. Gebr. Borntrager, Leipzig. 1918. Luttrell, E. S., ''Morenoella qiiercina, cause of leaf spot of oaks," MycoL, 32:652-666, 1940. Ryan, Ruth W., "The development of the perithecia in the Alicrothy- riaceae and a comparison with Alehola," MycoL, 7.?; 100-110, 1926. Theissen, P., "Hemisphaeriales," Aijn. MycoL, 77:468-469, 1913. "Uber Alembranstrukturen bei den Alicrothvriaceen als Grundlacre fiir den Ausbau der Hemisphaeriales," MycoL Centrb., 5:273-286, 1913a. "Die Trichothyriaceen," Beih. Bot. Centrb., Abt. 2, 32: 1-16, 1914. Theissen, F., and H. Sydow, "Synoptische Tafeln," Aim. MycoL, IS: 389- 491, 1917. 242 THE ASCOMYCETES ►Si 5^ 5 1 u, OQ s ^ I'*' C O d • u •«~» .<-i o r^ «-) *>. u S S: s « ;r p a. s: • d ^ "<** Q o V3 d Ui S <5j -s. «-kH O (-1 >i o o ^^ "^>» o 4-> v. o u p c c u o c o (A > u u > ►Q c Uh r-' o .S2 c u u d ^ .2 Q u o t/5 a. c a C o > 03 u ^ ^ 5 OS '5; u o o u fa "ts ji: HYSTERIALES 243 Hy St er tales The Hysteriales include a group of some 670 species of asco- mycetous fungi characterized by the possession of a distinctive type of ascocarp called a hysterothecium. The fruiting body is a small, black, elongate structure of hard or leathery texture, which opens by a single narrow slit at maturity. The hystero- thecium has been variously interpreted as an elongated perithe- cium and as a compressed apothecium. Consequently the Hysteriales have been classified by various systematists with both the Pyrenomycetes and the Discomycetes. According to Bisby (1913), this indicates clearly that they form a transitional group, a fact which was first recognized by Rehm. Hohnel (1918), in a rather radical classification of the group, would emphasize the similarities between the Hysteriales and the family Lophiostoma- taceae of the Sphaeriales. The similarity of the Hysteriales and the Phacidiales has been pointed out by a number of workers. The Hysteriales include both parasitic forms and saprophytes that produce the fruiting bodies on dead wood and bark. In the customarily accepted classification [Lindau (1896)1, the group is divided into 5 families, of which 2 will be considered here. In the Hypodermataceae, which has been monographed by Darker (1932), the hysterothecia are embedded within the substratum and are overgrown by host tissue to form a clypeus above; in the Hysteriaceae, the carbonaceous hysterothecia are freely ex- posed. Elytroderma {Hypodemm) defomians, a typical representa- tive of the Hypodermataceae, is parasitic on the needles and stem tips of Finns ponderosa in the Pacific Northwest [Weir (1916)]. Witches' brooms may be formed as the result of in- volvement of the terminal shoots by this fungus. The needles become browned at the tips and turn yello\\ ish where the black, elongate hysterothecia are produced. A spermogonial stage also is known, but the developmental history of the fungus has not been followed. The asci, intermingled with paraphyses, contain two-celled, fusiform ascospores. Closely related to Hypoderma is the Genus Lophodermium, which differs only in the fiHform nature of its ascospores [Tehon (1935)]. Lophodemninn pinastri is a serious parasite of pines, 244 THE ASCOMYCETES causing a destructive disease called needle cast. The disease is world-wide in its distribution and is especially serious on young trees in the nursery. The characteristic symptom of infection is premature shedding of the needles; in severe attacks all the green needles may fall before May. Infection of the needles occurs from germinating ascospores by penetration of the stomata. There follows the formation of a Fig. 96. Various Hysteriales. A. Habit sketch of Hysteriwn piilicare as it occurs on birch bark. B. Single hvsterothecium, surface view. C. Ascus and paraphysis. D. Ascospore. E. Habit sketch of Hysterograph'nnu ■fraxini. F. Ascus and paraphysis. G. Ascospore. H. Conidial or Septo- nema stage. /, /, and K. Mytilidion scolecosporwji. (Adapted from Loh- man.) /. End view of section of hvsterothecium. /. Ascospores. K. Conidial or Septonema stage. subcuticular or subepidermal stroma; in this are developed spores which have been shown [Jones (1935)] to function as spermatia. Jones describes the initiation of ascogonia as occurring in the summer, whereas the hysterothecia become evident during the winter, and ascospores are discharged the following spring. The most extensive studies of the disease and of the growth of the fungus in pure culture are those of Haack (1911). In the family Hysteriaceae, which includes saprophytic forms, the fruiting bodies are freely exposed at maturity and are formed singly or are united in a stroma. The hysterothecia throughout the family are black and carbonaceous. The group has been DISCOMYCETES 245 Studied extensively by Lohman (1933). The genus Glonium [Lohman (1937)1, including forms with two-celled, fusiform, and hyaline ascospores, is common on wood of various kinds throughout Europe and North America. Hvsterographium, with brown muriform ascospores, is also of rather common occur- rence. Among imperfect stages found associated with members of the group are Septonema, Sporodesmium, and Papulospora. Unfor- tunately the details of sexual reproduction are almost completely unknown. Spermogonia should be sought, especially amono- species having pycnidial stages. LITERATURE CITED BiSBY, G. R., "The literature on the classification of the Hysteriales," Trans. Brit. Mycol. Soc, 8: 176-189, 1913. Darker, G. D., "The Hypodermataceae of conifers," Contrib. Arnold Ar- boretinn, 1: 1-131, 1932. Haack, G., "Die Schuttepilz der Kiefer," 2. Forst-u. JagdiD., 43:329-357, 402-423, 481-505, 1911. HoHNEL, F, VON, "Mycologische Fragmente 272. tjber die Hvsteriaceen," ^777z. Mycol., 16: 145-154, 1918. Jones, S. G., "The structure of Lophoderjnium pinastri (Schrad.) Lev.," Ann. Botany, 49:699-12^, 1935. LiNDAu, G., ''Hysterimeae.'" In Engler and Prantl, Die natiirlicben Pflanz- enjamiilien, 1: (1) 265-278, 1896^ Lohman, M. L., "Hysteriaceae: Life histories of certain species," Papers Mich. Acad., 11 (1932): 229-288, 1933. "Studies in the genus Glonium as represented in the southeast," Bidl. Torrey Botan. Club, 64:57-72, 1937. Tehon, L. R., "A monographic rearrangement of Lophodermium," ///. Biol. Monogr., 13:1-151, 1935. Weir, J. R., ''Hypodenna deformans, an undescribed needle fungus of the ■ western yellow pine," /. Agr. Research, 6: 277-288, 1916. DiSCOMYCETES The Discomycetes comprise those ascomycetous fungi which have disk-like or cup-like fructifications. The fructifications are given various appellations, such as disks, ascomata, discocarps, and apothecia. More than 5000 species are included in this major groupinij. They may be separated into two sections, the Operculates and 246 THE ASCOMYCETES the Inoperculates. In the first, the asci open by means of a Hd or, more rarely, a transverse slit; in the second, no special mecha- nism for dehiscence of the asci is provided. Seaver (1928, 1942) monographed the Operculates and included therein the Pezizales, which embrace the two famihes, Pezizaceae and Elvellaceae (Hel- vellaceae). The Pezizaceae contain the cup-shaped or discoid Peridium Paraphyses Ascogonium Ascogenous hyphae Antheridium Fig. 97. Fyronevm confliiens. A. Cluster of paired oogonia and antheridia. B. Multinucleate oogonium, antheridium, and trichogyne. C. Diagram- matic representation of parts of ascocarp of P. confitieiis. forms; and Elvellaceae, the pileate ones. Nannfeldt (1932) mono- graphed the Inoperculates, including two orders, Ostropales and the Helotiales. In Nannfeldt's arrangement the Ostropales con- tain a single family, Ostropaceae, and the Helotiales contain the Dermateaceae, Phacidiaceae, Orbiliaceae, Hyalocyphaceae, Helo- tiaceae, and Geoglossaceae. The tip of the ascus in the Ostropales is thickened and is pierced by a narrow canal. The ascospores are filamentous and readily fall apart into cvHndrical elements, whereas those of the Helo- tiales are never filamentous and do not break up into cylindrical cells. DISCOMYCETES 241 An older, more commonly employed system of classification considers the Discomycetes to be comprised of the Pezizales, Helvellales, Helotiales, and Phacidiales. The Phacidiales includes Fig. 98. Diagram of the development of a gymnocarpous apothecium. (After Corner.) The circle indicates the position of the ascogonium within the apothecial initial. A. Branched hyphae surround the ascogo- nium. B. Ascogenous hyphae arise from the ascogonium and are separated by sterile hyphae. C. A layer of asci (hymenial layer) forms exposed at the upper surface of the young apothecium. D. A fully formed apothe- cium with poorly developed rim. those with leathery and carbonaceous ascomata, whereas the Others are fleshy. The operculate genera are included in the Pezizales and the Helvellales. There are approximately 20 genera and 300 species of Helvellales, and 100 genera and 3300 species of Pezizales. Among the larger genera are Helotium with 280 species, Humaria and Dasyscypha with 220 each, Mollisia with 248 THE ASCOMYCETES 210, Lachnea with 180, Peziza with 160, Pezizella with 140, Pyre- nopeziza with 100, Sclerotinia with 80, Ascobolus, Ascophanus, Geopyxis, and Lachnella with 60 each, and iVlorchella, Elvella, Sarcoscypha, and Geoglossum, \\'ith about 40 each. Apothecial development. The development of apothecia is tv^pified by that in Pyronema confliiejis, which is among the better-known representatives of cup fungi that may be found in the greenhouse at the surface of pots of sterilized soil or at sites of campfires or of burned brush piles. It may be recognized by the groups of fiesh-colored apothecia 1 to 3 mm broad. The apothecial initials are first recognizable as small hyphal tufts. Within each of these tufts are thickened, erect branches, one of which will become the antheridium and the other the ascogonium. The ascogonial branch is slightly more precocious in develop- ment, and the antheridium arises from a stipe cell beneath it. While differentiating, each becomes multinucleate. At the apex of the antheridium a multinucleate papilla, the trichogyne, is delimited; its tip curves to come in contact with the tip of the ascogonium, and its nuclei gradually degenerate. Then the antheridial nuclei migrate into the trichooryne. The partition between the trichogyne and the ascogonium next dis- solves, and the antheridial and ascogonial nuclei pair. Shortly thereafter a score or more of ascogenous hyphae grow out from the ascogonium, and the penultimate cell at each recurved tip (crosier) becomes the ascus. Meanwhile paraphyses arise from cells that are adjacent to the ascogonium. Among Discomycetes there are t\vo types of apothecial de- velopment, gymnocarpic and angiocarpic. Differences in cor- tical or marginal gro^^'th of the primordia during early develop- ment account for the two types, as Corner (1929) has shown that both kinds may occur \\ithin the Genus Ascobolus. Inter- mediate between these t\^pes is one which Corner designates as hemiangiocarpic. In these genera the marginal hyphae arch over the ascogonium, but their growth is limited, in consequence of which a closed sheath is not produced. Corner lists Cheiy?nenia stercorea, Anthracobia melaloiiia, Ascophanus granidifonnis, and Peziza aiiraiitia as hemiangiocarpic, and Ciliaria sciitellata, Ascoph- miiis carneiis, Ascobolus st ere or arms , A. citrinus, A. magiiif- icus, Pyronerna confluens, and Saccobohis violascens as angio- carpic. APOTHECIAL DEVELOPMENT 249 .^A^IA .^•' . >^ D Fig. 99, Diagram of the development of an angiocarpous apothecium. (After Corner.) The circle indicates the position of the ascogonium within the apothecial initial. A. Branched hyphae rising from the stalk cells of the archicarp invest the ascogonium. B. Tissue differentiation be- gins within the spherical mass (apothecial initial) ; cortex is thick-walled, internal tissues thin-walled; ascogenous hyphae appear as protrusions diverg- ing from the ascogonium. C. Mucilage cavity appears in upper portion by dissolution of internal tissues, a palisade of hyphae forms floor of cavitv, coming in part from hyphae that ascend with ascogenous hyphae, which together form hymenium. D, Pressure from expanding hvmenium ruptures cortex above hymenium; as asci enlarge, the disk expands laterallv. Asci at center of disk first to mature, and maturation continues centrifugally. 250 THE ASCOMYCETES Corner (1930, 1930a) also studied the development of certain stipitate discomycetes, including Mitriila pnsilla, Geoglossinn dif- jorme^ Trichoglossinn hirsiitiim, and Microglossinn viride, the last of which is angiocarpic, and the others gymnocarpic. The shaft arises is a result of greater growth of the medulla than of the cortical region. Correlation between size of apothecia, rate of development, and duration of the period of ascospore discharge is shown in data by Corner (1930) in Table 3. TABLE 3 Size, Age, and Sporing of Certain Discomycetes Diameter of Apotheciur?i {mm) f When sporing 1 Duration of Species begins Ai maturity sporing {days) Rhizina inflata 20 80-100 40-50 Peziza aurantia 12-20 40-60 40 Galactinia proteana 10-15 30-40 35-46 Galactinia saniosa 8-10 12-15 18-24 Ciliaria asperior 5-6 9-13 Pulvinula constellatio 1-2 4-5 12-15 Anthracobia maurilabra 0.5-1 3-4 10-21 Coprobia granulata 1.5 3 9-12 Within the temperature range 14° C to 22° C these disk fungi shed scores incessantly day and night. LITERATURE CITED Corner, E. J. H., "Studies in the morphologv of Discomvcetes. II. The structure and development of the ascocarp," Trans. Brit. Mycol. Soc, 14:275-291, 1929. m. "The clavulae," Trans. Brit. Mycol. Soc, i5; 107-120, 1930. IV. "The evolution of the ascocarp," Trails. Brit. Mycol. Soc, IS: 121-134, 1930a. Nannfeldt, J. A., "Studien iiber die Morphologic und Systematik der nicht- lichenisierten inoperculaten Discomvceten," Nova Acta Regiae Soc Sci. Upsalensis, Ser. IX, 8: 1-368, 1932. Seaver, F. J., The North Aniericaji ciip-fiingi {Operciilates). 284 pp. New York. Published bv the author, 1928. The North American ciip-jiingi, Supplemented ed. 375 pp. New York. Published by the author, 1942. HELOTIALES (INOPERCULATES) 251 Helotiales {Ino per dilates) The Helotiales include nearly all the inoperculate Discomy- cetes, except those that are symbiotically associated in the Liche- nes. Nannfeldt (1932), it has been pointed out, divided this order into 6 families, and in the present account brief mention will be made of representative members of 4 of these families, namely, Dermateaceae, Phacidiaceae, Helotiaceae, and Geoglos- saceae. Nannfeldt characterizes the Dermateaceae as having apothecia that are leathery to fleshy and typically dark. They arise either at the surface or within the substratum and are sessile or, at most, have a short stipe. They are paraphysate, and the ascospores are hyaline and filamentous. The apothecia of the Phacidiaceae arise within a well-devel- oped stroma that is usually dark. They open by an irregular rup- ture of the stromatic covering. The ascospores are elongate to needle-shaped. The excipulum is poorly developed. The conid- ial stages of many of the Phacidiaceae belong to the Lepto- stromataceae. In the Helotiaceae the apothecia are typically soft, fleshy to corneous, superficial, and stalked. The excipulum is thick. The ascospores are elliptical to elongate. Paraphyses are present. The conidia belong to various form genera. The apothecia of the Geoglossaceae are club-shaped or stalked, w^th a capitate hymenial surface. The ascospores are elongate to thread-like, simple or septate, and none is known to possess a conidial stage. Dermateaceae. This family is divided by Nannfeldt (1932) into 9 tribes. The apothecia of all arise innately and at maturity rupture the overlying tissues. They are corneous to leathery in texture, and the excipulum is thick, being composed of dark, thick-walled cells. Among the Mollisioideae is the Genus Pvrenopeziza, of which one species, P. inedicaginis, produces the yellow leaf blotch of alfalfa [Jones (1918)]. Its conidial stage was first described by Desmazieres in 1 847 as Sporonema phacidioides. It appears rather to be Phyllosticta. Jones was able to establish the genetic con- nections of conidial and ascigerous stages, both of which devel- oped in cultures on alfalfa stems and on oatmeal agar. 252 THE ASCOMYCETES Fig. 100. CoccojJiyces hiemalis, the cause of cherry shot-hole. A. Conid- ium of the Cylindrosporium stage, which on germination formed spermatia. B. Branched spermatiophore from conidial acervulus. C. Basal portion of coiled archicarp from interior of stroma, at exterior of which spermatia and conidia are being produced. D. Semidiagrammatic representation of a portion of stroma, showing spermatia adhering in great numbers to the trichogvne that protrudes well above the surface of the young apothecial stroma. E. Host cell with intercellular hypha and bulbous haustoria. F. Mature ascospores. G. Ascus and branched paraphysis. H. Segment of acervulus, showing conidia and conidiophores. At times conidia are borne among the asci within the apothecium. {A, B, C, and D adapted from Backus, E, F, G, and H adapted from Higgins.) DERMATEACEAE 253 Among the Drepanapezizoideae are the several species of Coccomvces that cause shot-hole diseases of Prunus. These in- clude C. hievialis on cherries, especially Pnimis cerasits, P. aviiirn^ and P. pennsylvaiiica, C. pninophorae on plums, especially P. doinestica and F. americana, and C. lutescens on chokecherry, P. virg'miana, and on black cherry, P. serotina. These species were described by Higgins (1914) and were assigned by Nannfeldt (1932) to the new Genus Higginsia. Their conidial stage is Cylindrosporium. Higgins (1914) established that spermatia are formed in late summer within conidial acervuli and among the conidia. At the same time, within the stromata beneath the spermatiferous layer, archicarps are produced, a dozen or more in each stroma. Septate trichogynes project well above the leaf surface. Spermatia adhere in great profusion to the trichogynes. There seems little reason to doubt, both from Higgins' observa- tions and from those of Backus (1934), that the spermatia func- tion in fertilization. By spring, the apothecia have matured on fallen leaves. Higgins (1914) also made the interesting observation that the shot-hole effect is the result of cleavage of the glucoside amygda- lin, by emulsin within invaded cells. In this cleavage of the amygdahn molecule, two molecules of glucose, one of benzalde- hyde, and one of prussic acid are formed. The increased osmotic pressure resulting from the presence of glucose causes water to be drawn from cells at the periphery of invaded ones, which swell in consequence, and a line of abscission is developed. Nannfeldt also placed Diplocarpon in the tribe of Drepanape- zizoideae. Among the species included in this genus are D. rosae, causing black spot of roses, D. earliaiia, causing strawberry-leaf scorch, and D. (Entojnopeziza) soraueri, causing pear-leaf spot. Diplocarpon rosae is commonly known in its conidial stage as Actinonevia rosae. Its morphology, however, is that of the form Genus Alarssonia. The ascis^erous staore was first described [Wolf (1912)] in 1912 and improperly assigned to the Micro- thyriaceae. In late summer spermatia are produced in the conid- ial acervuli [Wolf (1926)]. Coincidentally several ascogones are developed in each apothecial initial. By spring the apothecia have matured within decaying leaves. Occasional apothecia have been noted to bear conidia, as has been recorded also [Backus (1934)] for Higginsia hievialis. A similar course of develop- 2S4 THE ASCOMYCETES Fig 101 Diplocarpon earliajia causing leaf scorch of strawberry. A,^ B, F and H Stages in progressive development of apothecmm, in vertical section. C. Group of conidia of Marssonia stage. D. Spermatia that may be borne in acervulus with conidia. E. Ascospores. G. Ascus and paraphyses. DERMATEACEAE 25S ment has been shown to exist in the strawberry-leaf-scorch patho- gen [Wolf (1924, 1926)]. In pure culture each species develops conidia, whether the isolations are from ascospores or from conidia. Fig. 102. Other stages in development of Diplocarpon. A. Young apothe- cial stroma of Diplocarpon earliana, in vertical section, showing septate archicarps projecting to the leaf surface. B. Bulbous haustoria that arise from intercellular mycelium. C. Intertwining ascogenous hyphae of D. rosae that develop similarly in D. earliana. D. Vertical section of acervulus of D. earliana. The pear-leaf-spot fungus, whose peculiar conidial stage is known as EntoTnosporium maculatimt, was confirmed by Kle- bahn (1918) as a discomycetous species. He placed it in Ento- mopeziza. It had long ago been placed in Stigmatea, among the 2S6 THE ASCOMYCETES d t^ c ^ --S C/5 <>- Vi f-^i f^ a u ^ »<» CJ >-— ^ > C »^ , rt C) ^.' J3 •C5, y t-i ^■^ t«4 t?v «r: o ki o n3 ^ n r^ • i-H ^3 C •**>* <^ o e^ U ^ O bxi •Ki Ui • u CJ O u. M-i ^ Vt-H (« C C/5 *-> 1^ c p C CL > (73 V) u U4 (U rt «+-! 'O CU rt r: OJ TD C bo « rt ri ".u- C/5 CA. Q 3 J3 f ) cfl C) C/5 Cfl CJ on O ta < *\ n3 o Q s u ?s r^ 5^ 1^ •»« O ?«. «^ V4-I 0.) •^ i !?? r" s^ K) -^ o "r^ t^ 6( •M «J r ) m ^ O CJ C/2 Q o !»^ -M tli p S > ■a CQ o ;^ n « rt v> o C) tn ■a u , c r«~i a O fcr) T— ( o r^ u 4-< fa o^ PHACIDIACEAE 2S1 Pyrenomycetes, and Atkinson (1909) was the first to note that it is a disk fungus which, on closing, looks like a perithecial one. Among the Pseudopezizoideae are Fseudopeziza medicaginisy occurring on alfalfa, and P. trifolii, occurring on clovers, each causing leaf-spot diseases. Jones (1919) observed that conidial stages are lacking in both species and that the apothecia may be mature before the leaves are shed. Nothing is known about the events leading to the initiation of apothecia. Some mycologists include in the Dermateaceae the white-pine- canker fungus, Tympanis piiiastri [Hansbrough (1936)]. Its po- sition among the Discomycetes is not given, however, by Nann- feldt (1932). It attacks also red pine, producing cankers on the main stem. The apothecia are most common on cankers several years old. The disks occur in clusters, are dull-black, short- stalked, and about 1 mm broad. The ascospores are elongate, 3- to 9-septate, and hyaline; they bud while still within the ascus. Protruding stromata bear pycnidial loculi having tiny conidia 2 to 4 by 1 |.i. Very probably this stage will prove to be spermatial, rather than conidial. Phacidiaceae. Many mycologists regard the Phacidiaceae as of ordinal rank and as a distinct group intermediate between the Pyrenomycetes and the Pezizales. In this family the genera Rhy- tisma, Keithia, and Cryptomycina are worthy of mention. The best-known representative of Rhytisma, which includes about 25 species, all causing tar-spot diseases, is R. acerinum on maples. The conidial stage of Rhytisma belongs to the form Genus Me- lasmia, which may well be regarded as a spermatial stage. Jones (1925) found that the black, innate, conidial stromata shed spores during the summer. Deeply seated within these stromata may be ascogonia, each consisting of an ascogonial cell surmounted by several trichogynal cells and supported below by a more slender filament. Adjacent trichogynal cell walls become perforate, and the nuclei become paired in the ascogone. Ascogenous hyphae arise from the ascogone. Crooks may form at the termini of these hyphae, and the penultimate cell either becomes the ascus or else, if it contains more than a single pair of nuclei, proliferates eventually to form asci. Jones (1925) regarded the conidia (spermatia) as functionless. The five known species of Keithia are restricted to conifers. ■Keithia tetraspora occurs on Jiniipenis connmmis, and K. jiinip- 2S8 THE ASCOMYCETES eri on /. virginiana. The asci of K. tetraspora contain 4 asco- spores; those of K. juniper i, 8. Keithia tsiigae on Tsiiga canaden- sis also has asci with 4 spores. The asci of K. thujina on Tbiija occidentalis and K. chamaecyparissi on Chavmecyparis thyoides, however, contain 2 spores. The black apothecia usually occur Fig. 104. Rhytimia acerininn, causing tar-spot on maple. A. Apothecial sorus with a variously contoured surface that ruptures irregularly. B. Melasmia or conidial stage in vertical section. C. Conidiophore and conidia enlarged. This stage may be spermatiophore and spermatia, instead. D. Archicarp with three "trichogyne" cells borne on slender stalk. The asco- gonium cell is basal, septa are perforate, and nuclei are migrating into ascogonium cell. E. Ascogenous hypha arising from ascogonium, nuclei paired; penultimate cell has two pairs of nuclei and may again hook and branch. F. Vertical section of apothecial stroma in diagram. A mucilagi- nous cavity at apex aids in rupture and the freeing of ascospores. G. Single ascus enlarged. (Adapted from Jones.) HELOTIACEAE 259 singly and may mature on green leaves. Their development has not been studied. None possesses a conidial stage. Cryptofny cilia pteridis, widely distributed in Europe and North America, causes leaf roll of bracken fern, Pteridiwn lathis cidimi. Recent studies by Bache-Wiig (1940) show that the mycelium perennates in the buds. The conidial stage is of the Cylindro- sporium type. Young tissues, even those of prothallia, became infected after artificial inoculation. Helotiaceae. This family contains numerous parasitic and saprophytic species, arranged by Nannfeldt (1932) into 9 tribes. Their apothecia generally are superficial from the beginning and are fleshy, leathery, or corneous in texture with rather thick excipula. Among the Trichocyphelloideae is Dasyscypha, called Tricho- cyphella by Nannfeldt, characterized by apothecia the outer sur- face of which is densely covered with long white hairs. Accord- ing to Saccardo's Sylloge Fiingorimi, this genus contains approxi- mately 150 species. Its best-known member is D. ivUlkoijmiii, causing larch canker in Europe. This fungus was introduced into Europe early in the eighteenth century, and the literature on for- est pathology contains many controversial articles regarding it. Recently it was introduced into New England but was eradi- cated by the destruction of all infected larch trees. At the same time a great deal of confusion arose from the finding of a species of Dasyscypha, at first thought to be the larch-canker pathogen, on Douglas fir, Fseiidotsiiga taxifoUa. Hahn and Ayers (1934a), however, determined that the organism on Douglas fir is D. elli- siana, an indigenous species, commonly occurring as a saprophyte on pines. They (1934b) also determined that D. pini occurs on species of five-needled pines in the Pacific Northwest. In 1892 this fungus was first described as Lachnella pini from collections on Scots pine in Scandinavia. The details of these studies by Hahn and Ayers are contained in the reports just mentioned (1934a, 1934b) and those on other species of Dasyscypha in an earlier report (1934). Sclerotinia. None of the Discomycetes is of greater economic importance than are those usually included in Sclerotinia, belong- ing in the Tribe Ciborioideae. In Engler and Prantl's Die natiir- lichen Pflauzenfajjiilien, Schroeter divided Sclerotinia into 2 sub- genera, Stromatinia and Eusclerotinia. In Stromatinia he placed 260 THE ASCOMYCETES the fungi having pseudosclerotia and conidia of the Monilia type, and in Eusclerotinia those having well-developed sclerotia and conidia of the Botrytis type. Nannfeldt (1932) employed Moni- FiG. 105. Conidia and spermatia of Sclerotinia. A. Conidial chain from conidial pustule or Monilia stage of Sclerotinia iirmila. Each conidium is freed by a disjunctor mechanism. B. Germinating conidium from whose hyphae spermatia are being produced. C. Spermatial formation by Sclero- tinia trifolionmz. D. Conidia of Botrytis cinerea. E. Conidial head of Botrytis cinerea, from diseased tobacco seedlings. {A and B, from Woro- nin.) linia, a generic name proposed by Honev, for the fungi Schroeter placed in Stromatinia, and Sclerotinia for those Schroeter placed in Eusclerotinia; he placed in Ciboria those species lacking co- nidia. Sclerotinia {Ciboria) trifolionm?, causing stem rot of clovers, and Ciboria ficariae on Rammciihis ficaria are representa- tive of this group. In addition account must be taken of the fact HELOTIACEAE 261 that conidial stages alone are known in some species, as in Monilia laxa (probably M. cinerea of Europe), occurring on cherries in the Pacific Northwest. Similarly detached conidial forms of Botrytis exist, such as B. cinerea, one form of which was recently found by Groves and Drayton (1939) to have a Sclerotinia stage. Among the better-known species usually placed in Sclerotinia are 5. jnicticola on stone fruits, S". jnictigena on pome fruits (not known to occur in North America), S. rtcini on castor bean {Riciniis connmmis), S. inimla on Vaccinium vitis-idaea, S. scle- rotionmi on lettuce, cucumber, potato, and various other garden plants, and S. heteroica on Ledum paliistre and V accinhim uligi- 7? o Sinn. Honey (1928) created the name Monilinia for the monilioid species of Sclerotinia, with S. jnicticola as the type. The tax- onomy of this organism has been greatly confused, a subject dis- cussed in detail by Roberts and Dunegan (1924, 1927). Its dis- comycetous stage, which matures on mummified fruits lying partly buried on the ground during the period when the flower buds are opening, was first described as Ciboria in 1883 but was rediscovered in 1902, when it was thought to be identical with S. jnictigena. Other names applied to it include S. cinerea and S. americana. Sclerotinia {Monilinia) jnicticola is most widely known in its conidial or Monilia stage as it occurs on decaying plums and peaches. From the mycelium within the fruits are produced grayish tufts of hyphal branches, which extend through the cuticle. These tufts are conidiophores that form chains of lemon- shaped or moniliform conidia. When the end walls between co- nidia are first formed, they are plane, and the cells are then barrel- shaped. Later the septa split into two layers, and a fusiform plug is formed between the tAvo layers. This plug, the disjunctor, serves to detach the conidia from each other. While the dis- junctor is forming, the conidia increase in size, become lemon- shaped, and are then easily dislodged to inoculate other fruits. When the fruits have decayed and have fallen to the ground, they become mummified. Within the mummified tissues, apo- thecial stromata are produced throughout the summer and the succeeding fall and winter. In the spring brownish apothecia, 1 to 1.5 cm broad, with stipes 1 to 10 cm long, emerge from the 262 THE ASCOMYCETES surface of the mummified fruits. They are capable of explosively shedding ascospores by the time the flower buds are beginning to open. The flowers become infected thereby and are blighted. Such blighted flowers constitute a means of keeping the fungus alive until the fruits begin to ripen. The classical studies on Sclerotinia gladioli by Drayton (1934) are fundamental to an understanding of the development of this genus and presumably of related cup-fungi. Drayton grew this fungus in culture. Microconidia (spermatia) were developed in abundance; stromatic masses were also produced. When these stromatic masses were placed on moist sand and kept at a favor- able temperature, columnar pilose structures developed. These structures proved to be receptive bodies, for when Drayton placed spermatia on them the columns elongated and eventually were transformed into mature stalked apothecia. On sectioning the columnar structures, Drayton found that each contained a coiled ascogone, larger and more deeply staining than the sur- rounding filaments. Drayton furthermore found that monospore cultures yielded isolates that could be divided into two groups on the basis of compatibility. Each produced microconidia that were functional [Drayton (1932)], and also each produced archicarps. Indi- vidually the monosporic cultures w ere sterile. When Drayton crossed a member of one group of isolates with a member of the other, however, apothecia were developed. By crossings he dem- onstrated that the members of either group were cross-incom- patible and intragroup sterile, but intergroup compatible and fertile. Among the many others who have contributed to an under- standing of Sclerotinia are Woronin (1896), Godfrey (1923) and Whetzel (1926, 1929, 1945). Perhaps the most remarkable Monilinia is one whose pseudo- sclerotia form on fruits of Ledum pahistre, where apothecia are produced. The ascospores initiate infection on the foliage of Vacciiiiimt uliginosimt, where conidia form to reinfect the fruits of L. paliistre [Woronin and Nawaschin (1896)]. This Moni- linia is thus heteroecious, a phenomenon that is otherwise re- stricted, among fungi, to the Uredinales. Other Ciborioideae. Other genera of the Ciborioideae of more than passing interest are Ovulinia, Rutstroemia, Septotinia, and HELOTIACEAE 263 Lambertella. Ovulinia produces conidia singly on simple co- nidiophores, but otherwise it closely resembles Sclerotinia [Weiss (1940)]. Ovulinia azaleae causes flower spot in destructive pro- portions on cultivated azaleas and rhododendron. Rutstroemia, Fig. 106. Sclerotifiia gladioli. A. Multinucleate cells from vertical section of ascogonial coil that has not been spermatized. B. Ascogonial cells, 3 days after spermatization, showing paired nuclei and initiation of asco- genous hyphae. C. Ascogonial cells, 4 days after spermatization. D. Asco- gonial hyphae, 6 days after spermatization. E, F, and G. Stages in conju- gate division in ascogenous hyphae. H. Conjugate nuclei ready for fusion. /. Fusion of nuclei in young ascus. /. First division of fusion nucleus. (Courtesy of F. L. Drayton.) 264 THE ASCOMYCETES Fig. 107. Morchella hybrida (above), M. esciilenta (below), ascocarps, ascal tips, and ascospores. (Courtesy of F. J. Seaver.) HELOTIACEAE 26S recently monographed by White (1941), lacks a conidial stage and has ascospores that are one- to several-septate. Septotima podophyllinay the generic type of Septotinia, possesses elongate, septate conidia borne on sporodochia, but its other structures are like those of Sclerotinia [Whetzel (1937)]. Lambertella, having brown ascospores, but otherwise quite like Rutstroemia, has been monographed by Whetzel (1943). Certain members of the Ciborioideae (Sclerotiniaceae, accord- ing to Whetzel) are known to possess ascospores enclosed by gelatinous envelopes. These envelopes constitute adaptive de- FiG. 108. Some Geoglossaceae showing differences in discocarps, asci, asco- spores, and paraphyses in three representative genera. A. Leotia. B. Geoglossum. C. Spathularia. vices to cause ascospores to adhere to the suscept and to retain and supply moisture during germination. Attention was re- cently directed to these structures occurring in Ciboria canincu- loides and Monilima friicticola [Whetzel and Wolf (1945)]. Fungi of other tribes of Helotiaceae. In the Tribe Ombro- philoideae is Cenangiinn abietis, the cause of dieback of twigs of pines, especially on trees whose vigor has been reduced by drought or other factors. Clusters of brown to black apothecia break through dead bark in the late summer and autumn. The hymenial surface is greenish. The ascospores are hyaline and elliptical. A conidial stage is unknown. In the same tribe occurs Chlorospleiiiinn aeniginosiim, which occurs on the decorticated slash of hardwoods and stains the wood a brilliant verdig^ris screen. 266 THE ASCOMYCETES Scleroderis ribis on Ribes and S. abieticola on white firs, mem- bers of the Scleroderridoideae, produce inconspicuous, short- stalked, black apothecia on the bark of killed twigs. Their asco- spores are several-septate and hyaline. Geoglossaceae. The Geoglossaceae, or "earth tongues," are saprophytes, occurring in moist locations or in shady woods. Some are restricted to certain kinds of decaying wood, leaves, or mosses, as, for example, Cudonia hitea to beech litter, Mitrula ciicidlata to coniferous leaves, and Mitrida miiscicola to moss litter among living mosses. The family is divided into two tribes on the basis of the form of the stalked ascomata: Geoglosseae, with clavate or spathulate ascomata, and Cudonieae, with pileate ascomata. The shape and color of ascopores serve as bases for separating genera. Conidial stages are unknown. The monographic treatise by Durand (1908) is indispensable in the identification of North American species. LITERATURE CITED Atkinson, G. F., 'The perfect stage of leaf spot of pear and quince," Science, n.s., 50; 452, 1909. Bache-Wiig, Sara, "Contributions to the life history of a systemic fungous parasite, Cryptoviychm pteridis,'" My col., 52:214-250, 1940. Backus, M. P., "Initiation of the ascocarp and associated phenomena in Cocco77iyces bie?nalis,''' Contrib. Boyce Thompson Inst., 6: 339-379, 1934. Drayton, F. D., "The sexual function of the microconidia in certain dis- comycetes," Mycol., 24: 345-348, 1932, "The sexual mechanism of Sclerotinia gladioli,'''' Mycol., 25:46-72, 1934. "The perfect stage of Botrytis cojivoluta,'' Mycol., 2P: 305-318, 1937. Durand, E. J., "A monograph of the Geoglossaceae," Ajin. Mycol., 6: 387- 477, 1908. Godfrey, G. H., "Gray mold of castor bean," /. Agr. Research, 23:619- 716, 1923. Groves, J. W., and F. L. Drayton, "The perfect stage of Botrytis cinerea^^ Mycol, 57:485-489, 1939. Hahn, G. G., and T. E. x\yers, "Dasyscvphae on conifers in North America. I. The large-spored white-excipled species," Mycol., 26: 73- 101, 1934. II. ''Dasyscypha ellisiana,'' Mycol, 26: 167-180, 1934a. III. "Dasyscypha piiii;' Mycol, 25:479-501, 1934b. Hansbrough, J. R., "The Tympanis canker of red pine," Yale Univ., Sch. Forestry Bidl, 43: 1-58, 1936. OSTROPALES 267 HiGGiNS, B. B., "Contribution to tlie life history and physiology of Cylin- drosporium on stone fruits," A77z. /. Botany, 1: 145-173, 1914. Honey, E. E., "The monilioid species of Sclerotinia," MycoL, 20: 127-157, 1928. Jones, F. R., "Yellow leaf blotch of alfalfa caused by the fungus Pyrenope- ziza fnedicagmis," J. Agr. Research, 13: 307-330, 1918. "The leaf-spot diseases of alfalfa and red clover caused by the fungi Pseudopeziza medicaginis and Pseudopeziza trifolii, respectively," U. S. Dept. Agr. Bidl, 159. 38 pp. 1919. Jones, S. G., "Life history and cytolog}^ of Rhytimia acerina (Pers.) Fr.," Ann. Botany, 39:^1-75, 1925. Klebahn, H., Hanpt- iind Nebenfruchtjonnen der AscomyceteJi. 395 pp. Gebr. Borntrager, Leipzig. 1918. Nannfeldt, J. A., "Studien iiber die Morphologie und Systematik der nichtlichenisierten operculaten Discomvceten," Nova Acta Regiae Soc. Sci. Upsalensis, Ser. IV, 8: 1-368, 1932. Roberts, J. W., and J. C. Dunegan, "The fungus causing the common brown rot of fruits in America," /. Agr. Research, 28: 955-960, 1924. "Critical remarks on certain species of Sclerotinia and Monilia associated with diseases of fruits," MycoL, 19: 195-205, 1927. Weiss, Freeman, "Ovulinia, a new generic segregate from Sclerotinia," Phytopathology, 30: 236-244, 1940. Whetzel, H. H., "North American species of Sclerotinia, I," MycoL, 18: 224-235, 1926; II, 21: 5-32, 1929. "Septotinia, a new genus of the Ciborioideae," MycoL, 29: 128-146, 1937. "A monograph of Lambertella, a genus of brown-spored inoperculate Discomycetes," Lloydia, 6: 18-52, 1943. "A synopsis of the genera and species of the Sclerotiniaceae, a family of stromatic inoperculate Discomvcetes," MycoL, 57:648-714, 1945. Whetzel, H. H., and F. A. Wolf, "The cup-fungus, Ciboria carimcu- loides, pathogenic on mulberry fruits," MycoL, 37: ^76-A9l, 1945. White, W. L., "A monograph of the genus Rutstroemia (Discomvcetes)," Lloydia, 4: 153-200, 1941. Wolf, F. A., "The perfect stage of Actinonema rosae^'' Botan. Gaz., 54: 218- 234, 1912. "Strawberry-leaf scorch," /. Elisha Mitchell Sci. Soc, 39: 141-163, 1924. "The leaf-scorch disease of strawberries," N. C. Agr. Expt. Sta. Tech. Bull., 28:1-16, 1926. Woronin, M., "Uber die Sclerotinia-krankheit der Vaccinieenbeeren," Mem. Acad. hnp. Sci. Petersbourg, 7 ser., 36: 1-49, 1888. Woronin, M., and S. Nawaschin, ^''Sclerotinia heteroica," Z. Pflanzen- krankh. Gallejikunde, 6: 129-140, 199-207, 1896. Ostropales This order, according to Nannfeldt (1932), contains the single family Ostropaceae. Its ascospores, as has been indicated, are 268 THE ASCOMYCETES thread-like and septate, and the cells separate into cylindrical ele- ments. In this order Nannfeldt assembled Ostropa and Robergea, formerly placed among the Hysteriales, \^ibrissea from the Geoglossaceae, Apostemidium, variously placed among the Geoglossaceae, Mollisiaceae, and Helotiaceae, and Stictis and Schizoxylon from the Stictidaceae. Durand (1908) placed Apos- temidium among the Geoglossaceae. None of the species are known to possess conidia, with the possible exception of Schiz- oxylon sepincola and members of Apostemidium. LITERATURE CITED Durand, E. J., "A monograph of the Geoglossaceae," Ann. My col., 6: 387- 477, 1908. Nannfeldt, J. A., "Studien iiber die Morphologic und Svstematik der nichdichenisierten operculaten Discomvceten," Nova Acta Regiae Soc. Sci. Upsalensis, Ser. I\", 8: 1-368, 1932. Pezizales (Operciilates) The Pezizales consist of 2 families, the Pezizaceae and Elvella- ceae. Seaver (1942) divided the Pezizaceae into 8 tribes: Sphae- rosporeae, Ascoboleae, Aleurieae, Humarieae, Lachneeae, Oti- deeae, Sarcoscypheae, and Pezizeae. The characteristics used as bases for separation are shape, color, and surface markings of spores and size, consistency, and nature of apothecia— whether stipitate or sessile, and whether hairy or smooth. These 8 tribes contain 39 genera. The Elvellaceae are constituted of 5 genera, distinguished primarily on the shape of the hymenial portion. The Pezizales are all saprophytic. Their fructifications vary in size from barely visible disks, such as those in Streptotheca, Ryparobius, and Fyronevia conflnens, to stipitate structures 8 to 10 cm tall, as in Morchella crassipes, M. esciilenta, and Urmila geastei', or even considerably larger, as in Diirandioviyces phil- lipsii. The disks are discrete in nearly all species. In Morchella, however, the hymenial surface is alveolate, being compounded of many disks laterally united, and in Elvella it reposes saddle- wise or variously convoluted at the top of the stipe. The asci typically have 8 spores, but those of species of Strep- totheca, Ryparobius, and Theotheca are polysporous, containing 16, 64, or more ascospores. PEZIZALES (OPERCULATES) 269 Fig. 109. Ascospores of Pezizales. A. Fseiidoplectania nigrella, common on decayed pine wood among mosses. B. Boiidieria areolata, on damp soil in swampy situations. C. Laviprospora areolata, on damp soil among moss. D. Pitbya ctipressi, common on twigs and leaves of recently killed Juniperus and related conifers. E. Ascodesmis ?mcroscopica, on excreta of dogs. F. Ascobohis viridis. G. Aleuria aiirantia, common on damp earth in woods. H. Ascophamis isabellmits, on mud from corrals. /. Streptotheca crouaui grows on a variety of dung. The asci are polysporous. /. Patella sciitel- lata, widely prevalent on badly decomposed wood. K. Paxina fiisicarpa, on soil in woods. L. Uniida geaster, on decaying wood of Ulmiis crassifolia. M. Rhizina inflata, on burned-over ground. N. Peziza vesicjdosa, on heav- ily manured soils. O. Elvella elastica, on soil. P. Underivoodia colwnimiris, on soil. Q. Wynnea americana, on soil in rich woods. 210 THE ASCOMYCETES Conidial stages are uncommon, but Peziza repaiida, P. vesicu- losa, and Patella abiindans are reported to posses^ conidia. In P. abiindans the conidia are of the Botrvtis type. The Pezizales generally are not restricted to a particular sub- strate, most of them occurring on moist soil high in organic con- tent or on decaying wood. Some species, however, are quite restricted in substrate and range. Pyronevm cojifluens is com- monly found on burnt ground at the sites of campfires and has been observed to produce a copious pinkish cover upon the surface of pots of soil sterilized by steam. Corner (1930) records having seen millions of apothecia of AntJoracobia nmiirilabra on several acres of burnt ground in England. During rainy weather Pithy a ciipressi may densely occupy the recently killed branches of Juniperus and related conifers. Urnula geaster is limited to the vicinity of decaying stumps of Ulvnis crassifolia. Some species are coprophilous, and species of Ascobolus, Asco- desmis, Ascophanus, and Ryparobius are limited to the dung of certain animals; Ascodesmis porcina, for example, occurs only on pig dung. Apothecial development. Sexuality and the development of apothecia among Pezizales have been extensively studied by Harper (1900), Dangeard (1907), Claussen (1912), Dodge (1912), Dowding (1931), Schweitzer (1931), and Gwynne- Vaughan and Williamson (1932). Pyronema confluens and sev- eral species of Ascobolus have been employed in these studies. Pyroneina confluens has large vesiculate, multinucleate ascogonia. Clavate, multinucleate antheridia arise near the ascogonia, each surmounted by a curved hypha, the trichogyne. The multinu- cleate protoplast from the antheridium empties, by way of the trichogyne, into the ascogonium. Soon ascogenous hyphae arise from the surface of the ascogonium, from the penultimate cells of whose recurved tips the asci are developed. Two opposed views are held concerning nuclear activities. Harper (1900) maintained that the nuclei fuse in pairs within the ascogonium and again in the base of the developing ascus, thus making the primary nucleus of the ascus tetraploid. This view is supported by Gwynne-Vaughan and Williamson (1932), who found that the chromosome number in spore nuclei and in the nuclei of sterile tissue is 6, whereas that in nuclei of the ascog- enous hyphae is 12. Moreover, they found that the number of PEZIZALES (OPERCULATES) 211 nuclei in the antheridium varies from 100 to 200, with a similar variation in the ascogone. Then, when the ascogenous hyphae start to protrude, the average number in the ascogone is 160. The opposing theory was proposed bv Claussen (1912), who maintained that the nuclei merely became associated in pairs in the ascogonium and that fusion is delayed until the formation of the primary nucleus of the ascus. This view has a great deal of support, the most striking of which comes from the observations of Schweitzer (1931). He noted that the antheridial nuclei of Ascoboliis strobilinus are smaller than the ascogonial nuclei. They do not fuse in the ascogonium but migrate in pairs, a small one and a large one, into the ascogenous hyphae. Dangeard (1907) found that the antheridium did not open into the trichogyne in Fyronema confliienSy and hence he de- duced that this species is apogamous, a conclusion that has been supported by several subsequent investigators. Common species of Pezizaceae and Elvellaceae. Members of both these families are essentially cosmopolitan and are always of interest to the student of fungi. Patella sciitellata, occurring on decaying ^\'ood, has bright red disks with a fringe of dark hairs. Peziza vesiculosa occurs in clumps in richly manured gar- dens or on manure piles. Its cups are brown, 2 to 3 in. broad, and are commonly contorted and crimped. Peziza venosa and P, badia are common on the ground in deciduous woods. The hy- menial surface of P. vejiosa is convoluted, Plectania coccinea grows on partly buried sticks. Its funnel-shaped fruit bodies are about 1 in. broad, and its hymenial surface is scarlet. In the spring the stalked clusters of dark cups of Uiimla craterium, 1 to 2 in. broad, are common on partly buried oak branches. The base of the stipes and the mycelium from which they arise are coal black. The gyrosely folded hymenia of Morchella and El- vella give them the appearance of sponges. LITERATURE CITED Claussen", p., "Zur Entwickelungsgeschichte der Ascomyceten, Fyronema cojifiiieijs" Z. Botan., 4: 1-63, 1912. Corner, E. J. H., "Studies in rhe morphology of Discomycetes. IV. The evolution of the ascocarp," Trans. Brit. My col. Soc, 15: 121-134, 1930. Dangeard, P. A., "L'origine du perithece chez les Ascomycetes," Botaniste, 10: 1-385, 1907. 272 THE ASCOMYCETES Dodge, B. O., "Methods of culture and the morphology of the archicarp in certain species of the Ascobolaccac," Bull. Torrey Botan. Club, 39: 139-197, 1912. DowDiNG, E. S., "The sexuality of Ascobohts stercorarhis and the trans- portation of the oidia bv^ mites and flies," Ami. Botan., ^5; 621-637, 1931. Gwynne-Vaughan, H. C. I., and H. S. Williamson, "The cytology and development of Ascobolus incigjiificus,'" A?J7i. Botmiy, 46: 65y-670, 1932. Harper, R. A., "Sexual reproduction in Fyroneiiia confliiens and the morphology of the ascocarp," Ann. Botany, i^; 321-400, 1900. Schweitzer, G., "Zur Entwickelungsgeschichte von Ascobolus strobilimis, n.s.," Planta, 72:588-602, 1931. ^ Seaver, F. J., The North Ainerican cup-fimgi (Opercidates) , Supplemented ed. 377 pp. Published by the author. New York, 1942. Tiiberales The Tuberales, commonlv called truffles, are tvpicallv sub- terranean, although a few species are imperfectly buried or grow quite near the surface among decaying leaves. At least some of them grow only in association with certain species of trees, especially oaks and beeches. It was this constant association with trees, in fact, which led Frank long ago to postulate that truffles may establish the symbiotic relationship which he designated as mycorrhizal. Evidence of this preference for particular tree species is contained in the report of Parks (1920) that in Cali- fornia he unearthed ascocarps of 7 genera, including 1 1 species, in an area 10 ft square beneath an oak tree, Qiierciis agrifolia. The gross appearance of fruit bodies of truffles would lead the observer to suspect them of being Gastromycetes, among which they were, in fact, placed by early investigators. The ascocarps are globular structures varying in size from 0.5 cm to about 8 cm. They are brownish in color, and their surface may be smooth or warty. The rind or peridium is a compact, resistant layer composed of thick-walled tissue. The interior consists of elaborate folds or chambers lined with a palisade of asci, inter- spersed with loose fungus tissue. The Tuberales comprise a relatively small assemblage, having 27 genera and approximately 200 species. Four species were de- scribed in Persoon's Synopsis Alethodica Fiingonnn. Thirty years later, with the appearance of Vittadini's classical Mono- graphia Tiiberaceannn, the known forms increased to 13 genera and 73 species. Massee (1909) lists 11 genera and 32 species as TUBERALES 273 Fig. 110. Truffles. A. Ascocarp of Genea verrucosa, in section. B. Ascus and ascospores of G. verrucosa. C. Ascocarp of Tuber bruviale, in sec- tion. D. Ascus and ascospores of T. bruviale. (Adapted from Tulasne.) E. Ascospore of Hydnobolites californicus. (Adapted from Gilkey.) F. Ascospore of Hydnotrya tidasnei. (Adapted from Massee.) G. Ascospore of Viersonia alveolata. (Adapted from Gilkey.) 214 THE ASCOMYCETES occurring in England; and Gilkey (1916), 37 species in California. In a later monograph Gilkey (1939) lists and describes 58 species, included in 19 genera, as occurring in North America. All are edible, some species being highly prized as food, especially Tuber aestivimi, T. brwnale, T. inelaiiosponnn, T. viagnatimi, and T. 7iitidum. Although the number of known species of truffles is not large, edible ones may occur so abundantly as to make their collection commercially profitable. Persons who collect truffles commercially, especially in France and Italy, work with the help of trained dos^s or hogs that locate the truffles by scent. Reproduction. No asexual or conidial stage is known to oc- cur anions^ Tuberales, with the possible exception of one species of Tuber found to form conidia in culture. Their only known reproductiye stage is ascospores. Unfortunately the early devel- opm.ent of ascocarps, has not been obseryed; hence little is known about their sexuality. Dangeard (1894) found that crosiers are formed in T. bnniiale and T. dryophihnn and that the customary number of free nuclei is produced within each ascus. The num- ber of ascospores, howeyer, yaries from 1 to 8 per ascus, and the wall of the ascospores at maturity is ornamented with spines, warts, or reticulations. Ascospore dispersal is accomplished only after decay of the rind or through the agency of animals, especially rodents, that utilize truffles for food. Classification and relationship. The truffles are divided into two families: Eutuberaceae, with hymenial chambers that open to the outside, and Balsamiaceae, with closed chambers. It re- mains questionable whether this basis is adequate for separation. Evidence presented by Bucholtz (1897) shows that Tuber exca- vatinn, typifying the Eutuberaceae, is at first gymnocarpous. In Genea, too, the ascocarps are initially closed, and they open apothecium-like at maturitv^ These observations incline some mycologists to regard the Tuberales as discomycetous. The find- ings of Bucholtz (1903, 1910) indicate that the convolutions which are to become the hymenium arise as invasrinations from the upper surface of the ascocarp. Bucholtz (1910) regards the Balsamiaceae as intermediate between Pezizales and Helvellales. On further study, as has been indicated, certain of the species formerly placed among the Elaphomycetaceae and Terfeziaceae have been found to belong among the Tuberales. Relationships TUBERALES 21S among all these subterranean fungi can be established only after further investigation with access to ascocarps in immature stages. LITERATURE CITED BucHOLTZ, F., "Zur Entwickelungsgeschichte der Tuberaceen," Ber. deut. botan. Ges., 75:211-226, 1897. "Zur Morphologic und Systematik der Fungi hypogaee," Ann. Mycol.y i; 152-174, 1903. "Zur Entwickelungsgeschichte des Balsamieenfruchtkorpers, nebst Bemerk- ungen zu \"er\vandschaft der Tuberineen," Ann. My col., 8: 121-141, 1910. Dangeard, p. a., "La truffe," Botaniste, 4:63-87, 1894. GiLKEY, Helen AL, "A revision of the Tuberales of California," Ufiiv. Calif. Fiibl. Bot., 6:275-356, 1916. "Tuberales of North America," Oregon State Monographs, 1. 63 pp. 1939. Massee, George, "The structure and affinities of the British Tuberaceae," Ann. Botany, 23: 243-263, 1909. Parks, H. E., "California hypogaeous fungi-Tuberaceae," Mycol., 13: 301- 314, 1920. Chapter 7 THE BASIDIOAiYCETES The Basidiomycetes, a group of 20,000 to 25,000 species, in- clude the fungi that bear their spores exogenously on basidia. The basidia may occur singly or be variously arranged on hy- menia. On the basis of the shape and structure of basidia and of their arranofement, the Basidiomycetes are divided into two groupings, the Heterobasidiomycetes and Homobasidiomycetes. The Heterobasidiomycetes include the fungi commonly known as smuts, rusts, and jelly fungi, and the Homobasidiomycetes all others, including the gill, pore, leathery, and coral fungi, puff- balls, stinkhorns, and bird's-nest fungi. Essentially all the Hetero- basidiomycetes are gymnocarpous; that is, their basidia arise on the free surface of the fructification. The Homobasidiomycetes are further commonly divided into two subclasses, Hymenomycetes and Gastromycetes. The Gastromycetes include those fungi whose hymenia are formed within the fructification; hence they are spoken of as angiocarpous. Transitional conditions of gym- nocarpy and hemiangiocarpy exist among the Hymenomycetes. Among pileate species the sporiferous layer is generally differ- entiated on the interior of tuberous or "button-like" fundaments, and the hymenium is eventually exposed by expansion and rup- ture. These fungi are spoken of as hemiangiocarpous. Among leathery funo-i and pore fungri crenerally, the basidia from their beginning comprise a free hymenial layer. The basidium, the characteristic structural feature of the Basid- iomycetes, is typically club-shaped and non-segmented and bears exogenously a complement of four basidiospores. The shape and structure of basidia, as will be pointed out, vary. Initially they are the ends of hyphae composed of dicaryotic (two- nucleate) cells. As each terminal cell enlarges, the two nuclei enlarge also. These nuclei soon fuse to form a diploid fusion nucleus, that is, one with 2x number of chromosomes, which 275 THE BASIDIOMYCETES 211 then undergoes 2 divisions to form 4 daughter nuclei. Each of these nuclei has x number of chromosomes and is therefore hap- loid. Next, from the apex of the enlarging basidium 4 protru- sions (sterigmata) arise. These protrusions expand terminally, and a nucleus passes into each inflated tip. When delimited, the Fig. 111. Common genera of so-called mushrooms, nearly all of which are Basidiomycetes. (Courtesy, General Biological Supply House, Inc., Chicago, Illinois.) A. Agaricus. B. Amanita. C. Boletus. D. Geaster. £. Coprinus. F. Pleurotus. G. Alorchella (Discomycete). H. Lycoperdon. /. Clavaria. 21S THE BASIDIOMYCETES enlarged tip is the uninucleate basidiospore. Sometimes only 2 sterigmata are produced; then each of the 2 spores may receive 2 nuclei, or 2 nuclei may remain unused within the basidium. On germination the basidiospores, which are almost universally uninucleate (monocaryotic), give rise to hyphae with uninucleate cells, which constitute the primary mycelium. Soon the primary mycelium gives rise to binucleate (dicaryotic) cells that com- pose the secondary mycelium. The process of mating in which haploid myceha become diploid is called diploidization. It is very commonly accomplished by clamp connections. These are buckle-like devices, formed at the septa, that permit a pair of nuclei to be walled off in each cell. All subsequent nuclear divisions of this pair of nuclei or of their progeny are conjugate; that is, they divide coincidentally. As a result the vesfetative mycelium remains dicaryotic through- out. Eventually fruit bodies are produced from fundaments laid down by the dicaryotic mycelium. When the hymenial layer is differentiated in the fruit body, the terminal cells that are to be- come basidia are dicaryotic. The cycle of development may then be initiated anew by fusion (final stage of diploidization) of the pair of nuclei within each young basidium. Types of basidia. Basidia, as has been indicated, vary widely in structure and development. In the Uredinales and Ustila- ginales the teliospore, a uninucleate but diploid thick-walled structure, is the probasidium. On germination it gives rise to a tubular basidium, sometimes called a promycelium. Meanwhile meiotic nuclear division has taken place, after which, by trans- verse septation, the basidium becomes a row of cells, usually 4, each containing a haploid nucleus. Each nucleus then migrates into a laterally or terminally formed bud, which becomes ab- stricted and is the basidiospore. Among the Ustilaginaceae, the primary haploid nuclei within the basidium may continue to divide, and as a result many basidiospores may be produced. Quite the same type of basidial structure occurs among all Auriculariales. The cell from which the so-called epibasidium (promycelium) arises is commonly designated the hypobasidium (probasidium). After the first nuclear division in the hypo- basidium, a cross wall is formed in the elongating epibasidium; after the next division other cross walls are laid down to form a row of superimposed cells. From each epibasidial cell in TYPES OF BASIDIA 279 Auricularia slender sterigmata arise that bear the basidiospores at the same level. In Phleogena (Pilacre) basidiospores are pro- duced in a row down one side of the epibasidium. In Septo- basidium the probasidium is thick-walled, quite as in the rusts, and the slender septate epibasidium bears its basidiospores on rather long sterigmata. In this type of basidium with its several minor modifications the nuclear spindles are longitudinally oriented, and such basidia are said to be of the stichobasidial type. The Tremellales are characterized by another basidial type. The spherical or elongate basidium becomes divided by a vertical septum after division of the primary diploid nucleus. After di- vision of each of these nuclei another vertical septum at right angles to the first is laid down, so that the basidium, as seen from above, is cruciately divided. Each quadrant then bears a slender sterigma on which a single haploid basidiospore is apically pro- duced. The nuclear spindles among Tremellales are oriented transversely to the longitudinal axis of the basidium, such basidia being therefore regarded as of the chiastobasidial type. Among the Heterobasidiomycetes there exists still another type of basidium. Here the primary diploid nucleus divides twice, the spindles being longitudinally placed. Then a tuning- fork-shaped process arises at the apex of the basidium. Two of the nuclei pass into basidiospores, 1 at each tip of the fork, and the other 2 nuclei eventually disintegrate. This type occurs among the Dacryomycetales. The basidia of the Hymenomycetes and Gastromycetes repre- sent another type. In general they are slender, clavate to broadly clavate in the Hymenomycetes, and nearly globular in the Gas- tromycetes. The fusion nucleus characteristically undergoes 2 divisions to make 4 haploid nuclei. Sometimes there are 1 or more additional divisions. Usually 4 slender sterigmata arise from the basidial apex, and a uninucleate basidiospore is borne on each sterigma. In Tulostoma the sterigmata may be somewhat lateral. In certain gill fungi, such as Ama?iita bisporigera, Cama- TOphylhis virgmeiis, Cantharellus cornucopioides, Mycena metata, and Psalliota campestris [Bauch (1927), Buhr (1932), Smith (1934), and Colson (1935)], and in the coral fungi, Clavaria ci- nerea and C. cristata, 2 basidiospores, instead of 4, are regularly produced on each basidium. Bauch (1927) has shown that such basidiospores are rarely binucleate, although they are known 280 THE BASIDIOMYCETES to possess 2 nuclei in Cantharellus corimcopioides, Coprimis ephemerus, HydnaiJghini carneimt, Myceiia nmrina, and FsaUiota campestris. In some species that produce only 2 uninucleate ba- sidiospores, the 2 residual nuclei disintegrate in the basidium. In species that have 4 spores, such as Mycena atkinsoni, M. alca- Una, M. heviisphaerica, M. leptocephalay M. sanguineolenta, M. stannea, and M. viscosa, there may be 4 residual nuclei to dis- integrate [Smith (1934)]. Alycena citrinoinargijiata, M. dis- siliens, M. leptocephala, M. polygi'amma var. albida [Smith (1934)] and Naiicoria lenticeps may produce 2, 3, or 4 spores on different basidia in a single pileus. Galera silignea is said to have monosporous basidia. Smith (1934) also noted that the young basidia of Mycena capillaris, M. cholea, AI. citrinomarginata, M. dissUienSy M. lasiosperrna, M. leptocephala, M. poly gravmia var. albida, M. roseo-pallens, M. riibromarginata var. laricis, and M. vitilis have a single nucleus, instead of 2, in the young basidium. These species are considered parthenogenetic. Spindle orientation in basidia of Hymenomycetes and Gastro- mycetes may be transitional between stichobasidial and chiasto- basidial, as noted by Levine (1913) in Boletus, or each kind may occur in adjacent basidia in the same hymenium, as in Exoba- sidhim rhododendri [Eftimiu and Kharbush (1927)]. Basidiospores. The basidiospores of Basidiomycetes generally, except among the Gastromycetes, are inaequilateral, unicellular, uninucleate, thin-walled structures. They may vary in color en masse, being hyaline, pink, yellow, brown, or black, but other- wise are monotonously alike. Their wall is almost universally smooth, echinulations being common in a few genera, such as Lactarius and Russula. In Ganoderma the walls are peculiarly thickened. In Auricularia, Dacryomyces, and related genera the basidiospores may become several times transversely septate. The basidiospores of many Gastromycetes have thick walls that are variously ornamented,, and the spore mass may be yellow, brown, purple, or black. Mycelium. The conspicuous part of most species of Basidio- mycetes is the fructification. The mycelium is usually en- sconced within the leaf mold, decaying wood, dung, or other organic matter of the soil or within plant tissues. Here it exists as an interlacing, anastomosing weft of hyphae, as delicate my- celial strands, or as conspicuous rhizomorphs or sclerotia. The DIPLOIDIZATION 281 mycelium of parasitic species is intercellular, entrance to the host cells being accomplished by haustoria in the rusts. Bensaude (1918) pointed out that the mycelium from a single basidiospore may be incapable of giving rise to fructifications, but that two mycelia of opposite potentialities may be adequate. She regarded such species as heterothallic, in contrast to other species in which a single basidiospore is totipotent and which are therefore homothallic. These fundamental differences have been studied and further elaborated by Mounce (1922), Vandendries (1925), Hanna (1925), Newton (1926), Kniep (1928), and others. Coprimis lagopits, C. iiarcoticiis, C. iiiveits, and C. stercorarius are among the species found to be homothallic; Armillaria inu- cida, Coprimis fimetar'ms^ certain varieties of C. lagopiis, C. mi- caceiis, Cortichnn poly gomiim, Fomes roseiis, F. sitbroseiis, Len- zites saepiarja, L. trabea, Faneohis campamilatiis^ Schizophyllwn covnmine, and Trametes americaria are heterothallic. Mycelia arising from the germination of basidiospores of dif- ferent species differ rather fundamentally. Mycelium from most of the rusts and from Cortic 121771 varians, Colly bia conigena^ and Feniophora sambuci [Kniep (1915, 1917)] consists of uninucleate cells. Mycelium from basidiospores of Feniophora gigantea is also uninucleate, although the basidiospores are themselves bi- nucleate. In this instance one nucleus remains within the spore membrane, and the other migrates into the developing germ tube. The mycelium from basidiospores of Armillaria mucida, Copri- mis fimetariiis, Hypholoma perplexiim, and Fholiota praecox is coenocytic, becoming so by failure of septations to form as the nuclei are undergoing divisions. In Corticiinn bomby cimim (Hy- pochmis terrestris) and in most Gastromycetes the basidiospores are binucleate, and all divisions are conjugate, resulting in di- caryotic mycelium. DiPLOiDiZATiON. One peculiarity of the mycelium of the ma- jorits^ of Basidiomycetes is the presence of buckle joints or clamp connections, first noted by Hoffman in 1856 and called "Schnal- lenzellen."- Accord has not been reached on their function and significance. Usually they occur in connection with dicaryotic mycelium only. They are always present at all septa in Daedalea imicolor, Fistiilina hepatica, Lejizites abietimis, and Meniliiis lacrymans and occur at only occasional septa in Coniophora cere- 282 THE BASIDIOMYCETES Bella, Clitocybe expallens, and Lycoperdon pyriforme. A whorl of clamps may be developed in Coniophora cerebella. Clamp connections are commonly present also among the jelly fungi. In Armillaria mellea and Corticmm bombycimimy although the cells are dicaryotic, clamps are absent. They occur in the mono- caryotic mycelium of Stereiim hirsiitinn and in the coenocytic mycelium of Copriniis narcoticiis. The essentials of the process of clamp formation among the higher Basidiomycetes are as follows: A bowed pouch-like pro- trusion arises from the wall medianly between a pair of nuclei. The nuclei divide conjugately, and one of the daughter nuclei passes into the pouch. A septum is formed near the base of the pouch, producing a uninucleate clamp cell. At the same time another septum is laid down to separate two of the nuclei in the terminal cell from the fourth nucleus in the basal cell. After a time the tip of the clamp cell fuses with the basal cell, and the nucleus of the clamp cell passes out into the basal cell, thus making it binucleate. Evidently diploidization may be initiated in several ways. De- tails of the process in Ustilaginales and Uredinales will be con- sidered later in connection with these orders. Among Hymeno- mycetes it may be initiated by the fusion of monocaryotic hy- phae of opposite sexual phases. It may also result by fusion of an oidium borne on a hypha of one sexual phase with the hyphae of the opposite phase [Brodie (1931)], or oidial mycelia of op- posite sexual phase may unite [Brodie (1931)]. Some cases of diploidization are not so readily explained and appear to involve factors for compatibility and their disjunction, and the existence of "geographic races." Newton (1926) found among 25 mono- sporous mycehal cultures of Coprimis rostrupiamis that 11 re- mained haploid, whereas 14 spontaneously became diploid. At any rate mycelial cells once diploid remain diploid throughout the greater period of the developmental cycle, and fusion takes place in the young basidia, whereupon reductional division fol- lows to form haploid basidiospores in the majority of species. The development of present-day concepts of diploidization and an interpretation of its significance are comprehensively pre- sented in a report by Buller (1941). CoNiDiA. The production of conidia among Basidiomycetes cannot be regarded as of common occurrence'. The basidiospores CONIDIA 283 of many smuts bud indefinitely in yeast-like fashion, and these buds, like conidia, may eventually serve to initiate infection. The urediniospores of rusts are like conidia in their origin, and, since they function in dissemination, may in a sense be considered conidia. The basidiospores of many jelly fungi germinate by formation of sprout cells that may eventually develop mycelia. In Copmms lagopiis [Brodie (1931)] lateral oidiophores arise from the mycelium. These become segmented basipetally into ellipsoidal oidia that cling together in balls at the apices of short branches, the remnants of the oidiophores. These oidia may function as conidia or else in diploidization, as has been men- tioned. Chlamydospores may form as a powdery layer at the upper surface of pilei of certain mushrooms, notably Nyctalis aster o- phora and N. parasitica. These mushrooms parasitize species of Armillaria, Clitocybe, Cantharellus, Lactarius, and Russula. Gemmae have been noted to arise as propagative devices in several Hymenomycetes. Perhaps the most striking of these is Ornphalia flavida [Buller (1934)], whose stalked gemmae are formed on the leaves of coffee and other tropical species. This stage produces leaf spots, and the gemmiferous structures, which are like those in Stilbum, cover the lesions. True conidia, belonging to the form Genus Oedocephalum, occur in Corticiimt effiiscatiim, C. roseo-pallens, Fonies annosiis, Peniophora allescheri, Tomentella flava, and T. gramdata [Nobles (1935)]. They are uninucleate in P. allescheri, according to Nobles, whether they are produced on haploid or diploid my- celia. Conidia from the haploid mycelium are of the same sexual phase as the mycelium from which they are derived, whereas those from the diploid mycelium are of two kinds, some of one sexual phase and the remainder of the other. Fleiirotiis pinsitus, P. corticatiis, and Corticiiim calceimi are also said to form conidia. LITERATURE CITED Bauch, R., "Untersuchungen iiber zweisporige Hymenomyceten. II. Kern- degeneration bei einigen Clavaria-arten," Arch. Protistenk., 58: 285-299, 1927. Bensaude, M., Recherches sur le cycle evohitif et la sexiialite chez les Ba- sidioinycetes. These (Paris). 153 pp. 1918. 284 THE BASIDIOMYCETES Brodie, H. J., "The oidia of Coprimis lagopiis and their relation to insects," Ami. Botany, ^5:315-344, 1931. BuHR, H., "Untersuchungen iiber zweisporige Hymenomyceten," Arch. Protisteiik., 77:125-131, 1932. BuLLER, A. H. R., Researches on Fungi, Vol. 6: 397-443. Longmans, Green and Company, London. 1934. "The diploid cell and the diploidization process in plants and animals, with special reference to the higher fungi," Botan. Rev., 7:335-431, 1941. CoLSON, Barbara, "The cytology of the mushroom FsalUota cavipestris Quel.," Ann. Botany,' 49: \-\%, 1935. Eftimiu, p., and S. Kharbush, "Recherches histologiques sur les Exoba- sidiees," Rev. path, vegetale entomol. agr. France, i-/: 62-88, 1927. Hanna, W. F., "The problem of sex in Coprimis lagopiis,'" Ann. Botany, 39:^3l-A57, 1925. Kniep, Hans, "Beitrage zur Kenntnis der Hymenomyceten. I, II," Z. Botan., J: 593-637, 1913; III, 7:369-398, 1915; IV, . 2 — w U t/i 0 Oh ^ •^x 0 tc 0 Ui n »— ^ 1/1 • -^ u 0 .R >^ > Vi 0 "c Vi t> > I^ r" r« a^ -M • •H M-i ^ f) 0 4-) Ij . u ^^ u >. X c; 0 r- Lh 4-1 fl) /-v <+-! ^^^ • -^ C 0 • ^H x Ui h 3 U Ov 0 T— 1 4-> rt • (U u J3 :i. ^ DEVELOPMENTAL CYCLE OF PUCCINIA GRAMINIS 311 produced on the interior of pycnia and are extruded to the leaf surface. While the pycnia are forming, other hyphal aggregates, the initials of the aecia (cluster-cups), are being formed at points more deeply embedded within the leaf tissues. Special hyphae that protrude in tufts from the orifices of the pycnia are con- nected with the young aecia beneath. These protruding hyphae function as trichogynes. Evidence for such functioning rests in part upon the fact that all the cells composing the aecia are uni- nucleate, except the basal cells that initiate aeciospores (cluster- cup spores). The aeciospore initials or aeciospore mother cells, however, are binucleate (dicaryotic). By successive divisions of the aeciospore mother cells chains of aeciospores are produced. Pressure exerted on overlying leaf tissues by the developing aeciospores causes the aecia to open, whereupon they have the appearance of cups. The aeciospores, thus liberated, are dis- tributed by winds. Those that lodge on a suitable host (wheat) may germinate, and the germ tube enters the host tissues through a stoma. An intercellular mycelium of dicaryotic cells will give rise within a few weeks thereafter to uredinia (red-rust-stage pustules), containing stalked, rust-colored, eUipsoidal, 1 -celled but binucleate urediniospores. Urediniospores are air-borne, are capable of immediate germination on wheat, and thus serve to spread and increase the red-rust stage. The mycelium arising from the germination of urediniospores is dicaryotic throughout. The same mycelium that gave rise to urediniospores eventually produces 2-celled teliospores. Each young tehospore cell is bi- nucleate, but before germination, during the succeeding spring, the 2 nuclei fuse; thus the fusion nucleus becomes diploid. By 2 successive nuclear divisions that occur during the formation of the probasidium, 4 haploid nuclei are again formed. These hap- loid nuclei migrate singly into the sporidia, and the sporidia are thus ready to start again the developmental cycle. The outstanding features of rusts are ( 1 ) their polymorphism, as expressed by the production of 5 spore forms in the complete life cycle; and (2) the necessity, for many species, of 2 unre- lated hosts for the completion of their developmental cycle. In the complete cycle of rusts there are teliospores, basidiospores or sporidia, pycniospores (spermatia), aeciospores, and uredinio- spores, formed in sequence. In some species 1 or more stages 312 THE BASIDIOMYCETES are regularly omitted in the developmental cycle. In others, such as Fuccinia vexans, and certain other grass and sedge rusts from arid or semiarid regions [Arthur (1905)] an additional spore form, known as an amphiospore, is produced. In reality such spores are urediniospores with thickened walls and hence are capable of hibernating. As might be anticipated, much con- fusion on taxonomic problems of rusts arose before their poly- morphic nature was understood, and for that matter it still exists. Confusion is also causally related to the fact that some rusts are heteroecious; that is, certain spore forms are produced on 1 host species, and the other spore forms on a wholly unrelated species. The teliospores (teleutospores), as indicated by their name, constitute the ultimate or last stage in the cycle. They are characteristically thick-walled, germinate after a dormant period in all except a few genera, and are formed in pustules or sori (telia), sometimes associated in the same sorus with uredinio- spores. On germination, teliospores produce a germinal tube (promycelium or basidium) that is generally transversely 4-celled, and each cell bears on a lateral sterigma a sporidium or basidio- spore. Sporidia are capable of immediate germination by germ- tube formation. These germ tubes enter the host and produce mycelia that bear: (1) aeciospores, urediniospores, and telio- spores in sequence. If the rust is heteroecious, the urediniospores and teliospores or the teliospores only are borne on a different host from that on which the aeciospores are produced. Pycnio- spores may precede or accompany the aeciospores; (2) uredinio- spores and subsequently teliospores; or (3) teliospores only. Even within the same genus rusts are so variable in their de- velopmental cycle that generalizations are made \\ith difficulty, and exceptions are known to practically all such generalizations. General aspect of rust-affected plants. Rusts, as has been indicated, cause the formation of pustular rust-colored out- growths on any or all of the plant parts above ground. The invaded tissues may be discolored, usually paler green than nor- mal, or necrotic lesions may surround the sori. Quite generally rust-affected plants are stunted, but in some instances the invaded tissues are hypertrophic. Gyimw sporangium jiiniperi-virgwianae may modify the scale leaves of Jwiipenis virginiana to the extent that galls 2 to 4 cm in diameter are formed. Uromycladmm notabile and U. tepperiamim form galls 6 to 9 cm across on Aca- MYCELIUM 313 cia in Australia. The woody galls on various pines produced by Cronarthnn qiiercinnn may be 2 or 3 times the diameter of the stems on which they are formed. Some rusts cause the branch axes to be foreshortened, resulting in the formation of witches' brooms. Among such rusts are Gymnospormigmm nidiis-avis on Juniperus, Ravenelia pygviea on tropical species of Euphorbia, R. volkesnii on species of Acacia in Africa, Piiccinia caricis on Urtica parviflora in central Asia, and Calyptospora goeppertiana on \^accinium. Mycelium. The mycelium of rusts consists of branched hy- phae that with a few notable exceptions are intercellular. Inti- mate contact with invaded tissues is made by means of haustoria. Thev are usually bulbous but sometimes variously branched and knotted. The opinion that the haustoria may not penetrate the protoplast was expressed by Colley (1918) from observations on Cronarthnn ribicola and by Rice (1934), who studied Uro- viyces caladii. In these species, and presumably in rusts gen- erally, the haustoria are invaginations, and the ratio of their sur- face area to host-cell volume establishes a nutritional balance that does not result in the death of the invaded cells. Pady (1935) has shown that the mycelium of the short-cycled form of Gym- noconia interstitialis on Rubus is intracellular. Goplaiia mirab- ilis on the foliage of Michelia velutina in Java is said to have a superficial mycelium. The mycelium may be short-lived or perennial. Klebahn (1904) lists 44 species in which the mycelium perennates. Among fungi with perennating mycelium are such well-known species as Cranarthmi ribicola, C. querciiimi, C. coleosporoides, attack- ing conifers, Gyvmosporaiigiinn clavipes and G. iiidiis-avis on Juniperus, Fhragmidiimi siibcorticimim on roses, Uromyces tri- folii on clovers, Kitnkelia nitens on Rubus spp., Melampsora pini- t or qua, Chrysomyxa abietis, and Endophylliim eiiphorbiae-syl- vatici. Rust mycelia consists of two well-marked phases that alternate, a monocaryotic phase and a dicaryotic phase. All too commonly this alternation has been erroneously interpreted as alternation of generations. Mature teliospores, promycelial cells, sporidia, the mycelium arising from the germination of sporidia, and pycnio- spores are monocaryotic. Aeciospore mother cells, aeciospores, the mycelial cells resultant from germination of aeciospores, ure- 314 THE BASIDIOAiVCETES diniospores, the mycelial cells resultant from germination of urediniospores, and young teliospores are dicaryotic. The mono- carvotic phase is usually of short duration among species attack- ing herbaceous plants but may persist for several years among parasites on woody plants. Developmental cycles and types. For the reason that the names applied to sori and spore forms of rusts are somewhat long and cumbersome, Karsten in 1879 first suggested that the aecial stage be designated bv I, the uredinial by II, the telial by III. Subsequently O was used to designate the pycnial stage, and IV the sporidial. Arthur and many students of rusts have adopted these symbols. As has been indicated, rusts may have the com- plete cycle, that is, O, I, II, III, and IV stages in sequence; such rusts are called En forms. If I is omitted from the cycle, the rusts are brachy forms; if II is omitted, they are op sis forms; if O and I are omitted, they are heiin forms; if only III is produced, they are either micro or lepto forms. Micro and lepto forms are dis- tinguished on the basis of whether the teliospores germinate only after a period of rest (micro forms) or immediately after ma- turity (lepto forms). The I stage is rarely absent among rusts. If O and I occur on the same host as III, the rust is autoecious; if they occur on a totally different species, it is heteroecious. In arctic and alpine regions the micro and lepto forms predominate. The develop- mental cycles of many species have not yet been determined; hence they are known in the aecial stage alone or in the uredinial stage alone. Many others are known in the uredinial and telial stages but have not been connected with an aecial stage. Klebahn (1904) grouped heteroecious rusts into six develop- mental types as follows: 1. Teliospores that form near the close of the growing season hibernate, and aecia are formed in the spring that give rise to urediniospores which act as a propagative stage. Adost species of Uromyces, Puccinia, Melampsora, and Pucciniastrum are in- cluded in this group. Example: Fiiccijiia graviinis. 2. Telial mycelium hibernates and forms teliospores in the spring. Sporidia are therefore distributed in the spring, where- upon aecia soon develop. Examples: Clyijsomyxa rhododendri and C. ledi. SORI AND SPORE FORMS 315 3. Mycelium perennates and produces teliospores in the spring in Gymnosporangium spp. Such teliospores germinate immedi- ately in situ, and the sporidia are dispersed to infect the alternate host. 4. Aecial mycelium hibernates, that of Coleosporium for 1 year, of Cronartium for several years. Aecia appear in the spring, and aeciospores infect the telial host. Teliospores are formed during the summer that infect the aecial host immedi- ately, and aecial mycelium again hibernates. 5. Both aecial and telial mycelia perennate. In spring aecia arise from mycelium, and the aeciospores infect the telial host. From telial mycelium teliospores also form in the spring, which germinate immediately, and the sporidia initiate infection of the aecial host. Urediniospores arise in the summer from the same mycelium as bore teHospores. Example: Melampsorella caryo- phyllacearinn. 6. Both urediniospores and teliospores form in the late sum- mer. The teliospores germinate immediately and infect Anchusa, upon which pycnia and aecia form. The aeciospores can infect rye during the autumn, but it is not known whether the uredinio- spores can survive the winter. Example: Fiiccinia dispersa. Sori and Spore Forms Pycnia or spermogonia. In the usual course of events, pycnia are the first structures formed as the result of infections initiated by basidiospores. Moreover they usually precede the aecia but may be formed simultaneously with them. Arthur (1904) re- gards them as of importance in foretelling the length of the de- velopmental cycle. Pycnia do not repeat themselves but occur only once in the life cycle. If pycnia and urediniospores arise from the same mycelium, aecia are absent from the cycle. If pycnia and teliospores are associated, neither aecia nor uredinia exist in the cycle. Occasional species exist, such as Uromy- cladium maritinnnn, U. notabile, and U. robinsoni, in which the pycnia are associated with both uredinia and telia. If the telio- spores germinate immediately upon becoming mature and pycnia are associated with them, other spore forms are absent. In Piic- cinia malvacearinn on various mallows, Alelampsora farloivii on Tsiiga canadensis, Gallowaya pinicola on Pimis virginiana, 316 THE BASIDIOMYCETES Chryso77iyxa abietis on Picea sp., and Piicciiiia vivipari on Polygo- niim vivipannn, pvcnia are unknown. In Cronarthnn ribicola the pycnia are usually produced a year before the formation of the aecial stage. Fig. 120. Acerv^ular and pycnidial types of pycnia. A. Pycnium of Gyut- nosporanghnn clavariaeforme, in section, beneath epidermis on leaf of Crataegus. B. Subcuticular pvcnium of Phragviidiwn violaceinn on leaf of Rubus. C. Portion of vertical section of pvcnium of Cronarthnu ribicola on white-pine twig. D. Subepidermal pycnium of Milesia marginalis on needle of Abies balsaviea. {A and B adapted from Blackman, C from Collev, and D from Hunter.) The position, size, color, and form of pvcnia are worth noting. In most species they appear on the surface opposite that on which the other stage or stages occur. Occasionally, as in Gyjnnocoma inter stitialis, they are produced on both leaf surfaces. Pycnia vary in form from hemispherical or acervular to globu- lar or pycnidial. Subcuticular or subepidermal forms are usually acervular, whereas pycnidial forms are more deeply seated. Rusts PYCNIA OR SPERMOGONIA 311 attackino- Rosaceae and Ranunculaceae have acervular or hemi- spherical pvcnia. All pvcnia consist of a palisade of slender sporophores that arise from a pseudoparenchymatous tissue. Toward the upper part or the periphery sterile sporophores or paraphvses form a column that extends beyond the surface of the host. In species of Alilesia, however, paraphyses are wanting. Spherical to oval spores (spermatia) are abstricted in series from the apices of the sporophores. The mass of spermatia accumulates to the extent of rupturing the overlving host tissues or of effecting an ostiole, through which the spermatia ooze. The ooze is sugary and sometimes gives off a fragrant odor. \^arious insects are in con- sequence attracted to the exudate and serve as vectors in the dis- persion of the spermatia. The spermatia are uninucleate, the nucleus being proportion- ally large. They may germinate by forming a germ tube or by budding, as was observed by Cornu as long ago as 1876. Opinions concerning the function of spermatia have been in conflict since 1833, when Unger placed all rust spermogonia under one genus and species, Aecidiohnn exanthematimi. In 1841 Meven regarded them as male structures but maintained that there is no sexuality among rusts. Later, as the result of cyto- lo^ical studies involving the formation of aeciospore mother cells, a subject given more attention at another point in the discussion, the opinion became established that spermogonia are vestigial and non-functional. In 1927, however, Craigie (1927) observed that spermogonia and aecial primordia develop from infection by a single basidiospore, but that aeciospores never develop in such primordia unless spermatia from one lesion are transferred from one sorus to another. In these studies Craigie employed Fiiccinia grmnims on barberry and P. helianthi on sunflower. Later (1931) he demonstrated that the 4 basidiospores arising from any basidium of these rusts are of 2 sexual phases, and that the spermatia arising from 1 phase w^ill fertilize the sorus of the opposite sexual phase, and vice versa. He noticed a similar situa- tion in Fiiccinia coronata, P. pringsheimiana, and a species of Gymnosporangium; therefore in some rusts, presumably all which form spermogonia, the spermatia are functional. Attention has also been called by several workers [Andrus (1931), Pierson (1933)] to the presence of receptive hyphae 318 THE BASIDIOMYCETES (trichogynes) among rusts. Furthermore they are produced from the same haploid mvceHum as bears spermatia. Self-fertili- zation does not occur, but, as would be anticipated, the thalli are cross-fertile and cross-compatible. Heterothallism is now defi- nitely known in Puccinia gramwiSy P. helianthi, P. tritichia, P. coronata, P. sorghi, P. pr'mgsheimiana, Melavipsora lini, Crojiar- tium ribicola, Uromyces appendiciilatiis, U. fabae, U. trifolii- hybridi, U. vignae, and Gyvmocoma biterstitialis. It must by no means be inferred that all rusts are heterothallic. Brown (1939) offers evidence that a single sporidium of Puccinia coro- nata-elaeagm, P. grindeliae, and P. xanthi gives rise spontaneously to binucleate mycelium that is homothallic. The receptive hyphae are composed of uninucleate cells, ac- cording to Andrus (1931), Pierson (1933), and Allen (1934a), and they extend out from uninucleate basal cells of the aecial primordium. Craigie (1931), using Puccinia helianthi, Allen (1934a), using F. sorghi, and Buller (1938), using P. graminis, have shown that receptive hyphae extend from the ostiole of the spermogonium. The spermatium has been shown to fuse with the receptive hvpha (paraphysis or trichogyne) and to pass down through the hypha to the basal cell {&<^^ cell). There the two nuclei associate in what is regarded as the aeciospore mother cell. Here they divide conjugately and repeatedly, and the mother cell gives rise to a series of dicaryotic aeciospores. Allen (1932) has shown in Puccinia triticina that hyphae other than those near the spermogonial orifice may serve as receptors. Instead recep- tive hvphae may emerge from stomatal openings or may even penetrate to the surface between epidermal cells. Diploidization may be accomplished otherwise, as is indicated by Brown (1935), who found evidence that hyphal fusions may occur in P. helianthi w^hen two haploid pustules of opposite sex phases coalesce. In this case the spermatia did not function, but there is reason to believe that the dicaryotic condition in rusts is quite generally achieved through the agency of spermatia. Aecia. The aecia are of four form types: aecidium, caeoma, roestelia, and peridermium. These terms are sometimes used as generic names to designate the aecial stages. If the chains of aeciospores are formed compactly within a membrane or pe- ridium that, on opening, is cup-like, the structure is spoken of as an aecidium. If the peridium is lacking and the chains of aecio- AECIA 319 spores are loosely compacted, the structure is called a caeoma. If the peridium is strongly developed and extends prominently above the chains of aeciospores, the structure is spoken of as a roestelium or a peridermium. In general, the term roestelia is limited to the aecial stage of species of Gymnosporangium, whereas peridermium applies to the aecial stage of Coleosporium, Cronartium, Melampsora, and various other genera having non- pedicellate teliospores. Another very peculiar type of aecium occurs in Dasyspora faveolata. A much-branched hyphal mass protrudes from the host stomata. Each branch bears at its apex a verrucose aecio- spore that is abstricted by a narrow stalk cell. The aeciospores, it has been pointed out, arise in series from a binucleate mother cell. First the mother cell elongates, and conjugate division occurs; then by a transverse septum a terminal cell containing a pair of nuclei is cut off. This terminal cell again divides transversely. Usually the upper cell so formed is the larger and becomes the aeciospore; the smaller cell is a buffer or intercalary cell. Sometimes the first cell formed by the mother cell becomes a peridial cell. At any rate the basal mother cell repeats the process of conjugate nuclear division and delimitation of the upper portion, and eventually chains of aeciospores and intercalary cells are formed. The intercalary cells serve as dis- junctors and may early become disorganized. The aeciospores are always unicellular, and their wall is hyaline and two-layered. Sometimes the outer membrane is echinulate. Mutual pressure causes the aeciospores to be polygo- nal. Their content is orange-colored. The germ tubes usually emerge through one or the other of the thin places in the spore wall. Fromme (1914) studied the development of the aecia of Piic- ciiiia claytoniata. He observed that the primordium is at first a tangled globular mass of hyphae. Near the basal portion a layer of mother cells is differentiated. Sporulation begins first with the mother cells near the center of the hymenium and extends outward in a centrifugal manner. The first cells abstricted ad- here laterally and constitute the upper and lateral walls of the peridium. In some instances the young peridial cells divide to form intercalary cells, but such a procedure is exceptional. Since the mother cells near the center of the hymenium sporulate first. 320 THE BASIDIOMYCETES Qi f- O M ^ « S ^ o P • is _r I 1^ c/3 C C Cl. c •- C- UREDINIA 321 the aecial sorus becomes dome-shaped. As the pressure increases from repeated dehmitation of the aeciospores in chains, the pe- ridium is ruptured, thus Hberating the aeciospores. The surface markings or sculpturing of the walls of the pe- ridial cells in species of Roestelia (Gvmnosporangium) has been employed to distinguish species. Kern (1910) used this criterion in a study involving 16 species of Roestelia. Hedgcock (1928) separated the needle-inhabiting peridermiums on pines, which be- FiG. 122. Germination of apogamous aeciospores of Endophyllinn euphor- biaesylvaticae. (Adapted from Moreau.) long to the Genus Coleosporium, by using structural features and color. Infection resulting from germinating aeciospores produces my- celia on which urediniospores or teliospores or both are formed. In a few species repeated aecium formation has been observed. Secondary aeciospores have been noted, for example, in Fiiccinia senecionis and in Uro7/iyces cminijigh ami amis, the latter occur- ring on Jas77nmmi grandiflonim in India and appearing to consti- tute the first known case of repeating aecia [Barclay (1891)]. Uredinia. The urediniospores are borne on the same host as aeciospores in autoecious rusts but on a different species in heter- oecious rusts. Urediniospores originate from mycelium, arising from: (1) germination of aeciospores, (2) germination of spo- ridia, or (3) germination of other urediniospores. Urediniospores normally constitute the repeating spore forms, and many succes- sive crops may be produced during a season. They are unicel- lular and ovate to elliptical; the Mall is echinulate, and, except for S22 THE BASIDIOMYCETES Fig 12. Stages in development of the uredinium of Cronartinm ribicola. (Adapted from Colley.) A. Subepidermal primordium composed of bi- nucleate cells B. Layer of cells, destined to become urediniospores, formed on outer surface of primordium. C. Urediniospores liberated by rupture of overlying host tissue. UREDINIA 323 Puccifiia monopora, they possess more than one germ pore. They are commonly borne singly on stalks. Their color varies from orange to brown, and the pigment may occur in the protoplast or in the wall. The development of uredinia and urediniospores has been stud- ied by Moss (1926). Since the cells from which the sorus arises are dicaryotic, the soral cells are also dicaryotic. Urediniospores are delimited from basal cells of the sorus in quite the same way as aeciospores are produced. Buffer cells form in some species. In some, the urediniospores are catenulate, especially in Coleo- sporium and Chrysomyxa, and in others pedicellate. In HeiJtileia vastatrix the sori arise beneath the stomata of the coffee leaves, and the urediniospores form singly at the apices of the fascicle of stalk cells. They also protrude from the stomata in Olivea capitulijonnis, Aplospora nyssae, Prospodium plagiopus, and P. bahamiejise, in w^hich species a circle of incurved paraphyses sur- rounds the uredinial pustules. Paraphyses accompany uredinio- spores in a number of other rusts, such as Tranzschelia pnini- spinosae, Fiiccinia poanim, P. perplexans, Uromyces dactylidis, and Phraginidhnn siibcorticimmi, and they may not form a pe- ripheral ring but instead occur interspersed, as in Melampsora lini. In this last-named species the paraphyses are metamorphosed stalked urediniospores. Among the genera Hyalospora, Milesia, and Uredinopsis, all of which are fern rusts, and among Cronartium, Melampsorella, Melampsoridium, and Puccinastrum, the uredinia possess peridia. Urediniospores may be dimorphic, as in the genera Uredinop- sis, Hyalospora, and Alilesia, and in Triphragmiiim zdjjiariae, oc- curring on Spiraea. The primary uredinia in T. idmariae^ formed on petioles and veins, are large and abundant, and the secondary ones are quite small and sparsely dispersed on the laminar tissues. Although urediniospores and aeciospores are generally quite different, they are known to resemble each other very closely in certain species, as in Piiccinia fraxijiata, having aecia on ash and uredinia on Spartina spp., in P. seymoiiriana, having aecia on Cephalanthus and uredinia on Spartina spp., and in P. verbemcola, having aecia on Verbena spp. and uredinia on Sporobohis spp. In some portions of the world, species that are normally heter- oecious are perpetuated year after year in the uredinial stage. Such is the situation wdth Piiccinia graminis in Australia, where 324 THE BASIDIOMYCETES barberry is absent, and with P. coronata in Andean regions of South America, where Rhamnus is absent. Such rusts may sur- vive the winter by migration in the autumn from colder to warmer portions of the country, multiplying there during win- ter, and again migrating to colder regions in the spring. Stakman and his associates have amassed abundant evidence to show that Fig. 124. Urediniospores of various rusts, in surface view and in optical section. (Adapted from Arthur.) A. Uredinopsis mirabilis. B. Milesla polypodophila. C. Cronarthmi ribicola. D. Coleosporhnn solidaginis. E. Melcmipsora abietis-canadensis. F. Physopella fici. G. Pileolaria toxi- codendri. H. Fiiccinia grmninis. I. Tranzschelici pnmi-spinosae. J. Kuebne- ola uredinis. there is a seasonal migration of P. graminis of this kind in the Great Plains area of the United States. There is also abundant evidence that this rust and other orrain rusts cannot survive the winter as urediniospores in the Northern United States or in northern Europe. In Australia viable urediniospores of P. gravii- 72ts, P. trkicinay and P. chry santhemi have been taken from sori at various times during the winter by McAlpine. Certain autoecious species also persist and perpetuate them- selves in the uredinial stage. Such is reported to be the situation with Uromyces fabae in Ecuador, whereas this same species in Europe produces aecia and also telia. Plasticity among rusts may find expression in other ways, such as the occurrence of short- cycled forms like Kiinkelia nitens and Fiiccinia podophyUi. TELIA 325 Telia. Teliospores arise from mycelium, originating ( 1 ) from aeciospores, (2) from urediniospores, or (3) from sporidia. They c a^ Fig. 125. A. Vertical section of uredinial pustule of Coleosporhim soUdagi- nis. The ''buffer" peridial cells are lacking. Intercalar\^ cells separate the urediniospores that are produced in chains. The basal cells give rise in acropetal succession to urediniospores and buffer cells alternately. (Adapted from xMoss.) B. Portion of mature uredinium of Melampsora lini. The capitate structure at the left is a paraphysis. The urediniospore at the right is long-stalked. The remaining stalks exhibit stages in ure- diniospore delimitation. (Adapted from Fromme.) C. Section of young uredinial pustule of Melampsorella elatma. Buffer cells constitute a layer immediately beneath the epidermis. Beneath them are immature uredinio- spores. Clear binucleate cells beneath the urediniospores separate them from the basal urediniospore-mother cells. (Adapted from Moss.) are rv^picallv thick-walled resting spores that normally have a period of dormancy, but in lepto forms teliospores are capable of germination as soon as they reach maturity. The arrangement 326 THE BASIDIOMYCETES of teliospores, their shape, and their septation are among the characters used in generic separations. In the Pucciniaceae the tehospores are borne on a stalk or pedicel, whereas in the Alelamp- soraceae they are sessile and arranged in layers or in columns. The feature that most strikingly separates teliospores from other types of rust spores is their method of germination. Among many pedicellate species each cell of the teliospore has a single germ pore, through which a short germ tube emerges. This germ tube has a limited growth and is called a promycelium or ba- sidiuni. It usually becomes 4-celled by transyerse septa. It never functions as an infection hypha. From each basidial cell a sterigma arises, supporting a sporidium or basidiospore that is discharged at maturity and is air-borne. Among certain melampsoraceous species germination of telio- spores follows a somewhat different plan. In Coleosporium, Ochrospora, Trichospora, and Chrysopsora, for example, mature teliospores are single-celled but on germination become 4 super- imposed cells, each of which bears a long sterigma that abstricts a sporidium. In certain other genera, such as Melampsora, Chrysomyxa, and Cronartium, each superimposed cell forms a 4-celled promycelium and 4 sporidia. This same type of germi- nation occurs in Phragmidium, which has pedicellate spores. The basidia of Ravenelia may bear only a single sporidium. Another unusual kind of germination occurs in Barclay ella dejonnans on Ficea morinda in the Himalayas; in this species each cell of the tehospores forms a promycelium, each segment of which rounds up and is the sporidium. Other noteworthy teliospore types occur in certain short- cycled rusts. In species of Endophyllum the teliospores are borne in cupulate structures in aecioid chains and are morphologically like aeciospores. In fact, they were regarded as aeciospores by early workers. On germination, however, the Moreaus (1919) have shown, promycelia and sporidia are produced. Sappin-Trouffy (1896) showed that E. sempervivi and E. eiiphorbiae-sylvaticae have binucleate tehospores and that their nuclei divide conju- gately. This condition may not occur invariably, and other species of Endophyllum may behave differently [Ashworth (1934)]. Kimkelia nitejis produces caeomoid telia. Kunkel (1913, 1914) and Dodge and Gaiser (1926) have given considera- TELIA 321 tion to the phenomena of germination and nuclear activities. Other aecioid telial rusts are Fiiccinia grindeliae, Uromyces sciitel- latiiSy and U. levis [Arthur et al. (1929)], but these species are aecioid only in the sense that the aecial sori and telial sori look quite alike. Fig. 126. Teliospores of various rusts. A. Surface view of epidermal cell of Folypodhnn virginianuin that is occupied by teliospores of Milesia poly- podophila. B. Uredinopsis osmimdae in epidermal cell of Osinunda cin- namomea. C. Chrysoinyxa arctostaphyli, margin of sorus. D. Portion of telial column of Cronarthnn ribicola. E. Portion of telial sorus of Melcnnp- sora medusae on Populus. F. Ravenelia cassiaecola from Cassia cbamae- crista. G. Uropyxis amorphae from Amorpha. H. Fhragmidium aiueri- caninn from Rosa. /. Xeiiodochus carbojiarms from Sangiiisorba micro- cephala. J. Nyssopsora echmata from Oefianthe californica. K. Endo- phylhmi sentpervivi from Sempervivum. L. Fuccinia podophylU from Fodo- phyllum peltatimt. M. Fuccinia coronata from Avena sativa. N. Gymno- sporangimn clavipes from Juniperus virginimm. O. Uromyces caryophyl- linus from Dianthus caryophyllus. {Ay C, E, G, I, adapted from Arthur.) 328 ' THE BASIDIOMYCETES Kursanov [Arthur et al. (1929)] has studied the development of telia among several genera, and his accounts indicate that the developmental features resemble those of aecia and uredinia gen- erally. Occasional genera are exceptional, such as Cystopsora, in which the sori protrude from stomata and the teliospores appear to be superficial, and Goplana mirabilis, occurring on Michelia vehit'ma in Java, the teliospores of which are borne on a super- ficial mycelium. Heteroecisin It is easily understandable that the early students of rusts should regard the different spore forms as distinct genera, although in 1807 de CandoUe expressed the opinion that IJredo linearis and Fiiccinia granmiis on wheat were one and the same but that they chanored aspect with age. Persoon also suspected that the two were stages of the same species. The Tulasnes {Ann. Sci. Nat. Bot., ser. 4, 2:77-196) in 1854 decided that Uredo and Puccinia were one and the same. They had noted several years earlier, in connection with rose rust, the curious fact that Uredo rosae and FhragiJiidiinn incrassatimi occur in the same sorus. Corda (Icones Fimgorum Hiiciisqiie Cognitoriim 419, 1840) and Fries {Sinmm Veg. Scand. 507, 1849) regarded the Phragmidium stage as parasitic upon the Uredo stage. That the existence of a relationship between cereal rusts and the presence of barberry had become thoroughly established in the minds of farmers Ions: before de Barv's classical demonstra- tion (1865) is shown by the fact that a law was enacted in France in 1660 for the eradication of barberry, and that similar laws \\'ere passed in several New England States between 1726 and 1766. Moreover in 1818 Schoeler in Denmark [Arthur et al. (1929)] transplanted barberry bushes in rye fields and found that rust became abundant, especially on those plants on the lee- ward side of the barberry bushes. He also applied aeciospores to rye leaves; after 5 days infections were evident, whereas his control plants were rust-free. Nevertheless botanists were not convinced of the genetic connections and continued to regard the aecial stage as a different genus. In 1863 de Bary (1863) sowed sporidia of Uromyces appen- diciilatiis on beans grown in the laboratory. Lesions appeared on inoculated plants after 5 or 6 days, and spermogonia were ma- HETEROECISM ' 329 ture 3 days later. After an additional period of 8 to 12 days aeciospores were produced, and a month later urediniospores and teliospores. By sowing aeciospores on other beans, he se- FiG. 127. Germination of teliospores. A. Section of sorus of Coleospor- ium sonchi-arvensis. The one-celled teliospores, in situ, become trans- formed into four superimposed cells (the promycelium or basidium), each of which bears a sterigma at whose tip the basidiospore is produced. B. Typical germination of teliospore of Uromyces appendicidatiis. C. Ger- mination of one-celled teliospores in telial column of Cronartiinn quercmim. D. Section of telial sorus of Thekopsora areolata. Stages in germination of teliospores. The promycelium extends to the exterior of the host. (After Sappin-Trouffy.) E. Piiccinia malvacearum; at left, normal germina- tion, in middle, when teliospores are submerged, and at right, when pres- sure of Oo is reduced. (After Sappin-Trouffy.) F. Ravenelia sp. G. Bar- clayella sp. cured uredinia, followed by telia. Having thus established that the bean-rust fungus is polymorphic, de Bary devoted himself to similar sowings of spores from rust pustules on barberr\^ and on wheat. Again he found that one polymorphic species was in- volved on both hosts, that the different spore forms appeared in sequence, that the aecial and pycnial stages occurred on barberry 330 THE BASIDIOMYCETES and the uredinial and telial ones on wheat, that the stages on barberry could infect wheat but could not infect barberry and vice versa, and, as a consequence, that both hosts were required for the polymorphic rust to complete its cycle of development. In spite of these experimentally established results, the heter- oecism of rusts was not immediately accepted among mycologists, at least not without temeritv^ 0rsted [Arthur et al. (1929)] during the summer of 1865 showed the connection of Gymno- sporangiinn sabijiae with Roestelia cmicellata. By 1880 it had been established that 16 rusts are heteroecious, and during the next 10-year period the list was extended to include about 100 species. Klebahn (1904) lists 153 species, distributed among the genera as follows: Chrysomyxa 2, Coleosporium 14, Cronartium 3, Gymnosporangium 13, Melampsora 21, Melampsorella 1, Melampsoridum 1, Puccinia 85, Pucciniastrum 3, and Uromyces 10. The list compiled by Dietel (1918) contains 264 species, and since 1918 many additional ones have been demonstrated to be heteroecious. The origin of the heteroecious habit among rusts has long been a fertile field for speculation, and, as on all such topics, accord is lacking. Acquaintance with this problem, with the views of those who have contributed to its solution, and with the difficul- ties involved can be gained from the accounts by Olive (1911), Grove (1913), Orton (1927), and Jackson (1931). In general two diametrically opposed views are held: (1) that the ancestral forms were autoecious but able to live plurivorously; that is, they were at least able to pass their entire developmental cycle on either of two hosts; or (2) that ancestral rusts were heteroecious, as well as heterothallic and polymorphic. Fischer is among those who assume that heteroecious species once lived on either host autoeciously, and that host specialization is a recent development. Such a species as Fiiccinia graminella, with both aecia and telia on Stipa, might be regarded as evidence of this point of view. This species is not plurivorous, however, and there is no evidence that it ever was. Other evidence for this point of view is that the host for the monocaryotic phase is the more primitive and that the stimulus imparted by the dicaryotic condition results in invigoration. It would therefore follow that aeciospores pos- sess greater vigor, and hence greater capacity for infecting, than do other spore forms. The fact that aeciospores of some species HETEROECISM 331 act as a bridge supports this argument. For example, the aecio- spores of Cronartium asclepiadmm, formed on Piims syhestris, infect and produce teha on members of 4 families of flowering plants: Asclepiadaceae, Verbenaceae, Scrophulariaceae, and Ra- nunculaceae. Again, the aeciospores of Melampsorella caryo- phyllaceariim initiate infection on species among distinct genera of Caryophyllaceae. On the other hand, quite the opposite con- dition may result, as it does with 7 species of heteroecious Puc- cinia that bear aeciospores on members of 3 or 4 families of monocots but that all produce teliospores on Phalaris arimdi- nacea. The opinion of Jackson (1931) and nearly all present-day stu- dents of rusts is not only that the autoecious species have been developed from heteroecious species but also that all species with a reduced cycle typify present-day trends among rusts. These short-cycled species are therefore derived from autoecious species. Olive (1911) and a group of other workers, such as Klebahn, Magnus, and Dietel, regarded lepto and micro forms as the ancestors of heteroecious rusts. They would argue that Piic- cinia mesneriana, one of the crown rusts, whose telia are produced on Rhamnus, is the progenitor of Fiiccinia coronata, which re- quires Rhamnus as its aecial host and Avena as its uredinial and telial host. Autoecism is therefore primitive, according to this group of students, and heteroecism has arisen as an adaptation. Evidence that the long-cycled forms are ancestral and that they may give rise to forms with simpler cycles is derived from studies of Fuccinia podophylli. This species hibernates as telio- spores, and the sporidia may initiate infections that early give rise to teliospores on the bud scales and stems. Shortly thereafter aecia appear on the leaf blades, and they too arise from the same primary source [Whetzel, Jackson, and Mains (1925)]. Pycnia accompany these aecia but are usually absent from the early crop of teliospores. In late summer teliospores are produced on mycelium from infection by aeciospores. Fuccinia podophylli is therefore not fixed but plastic in its cycle of development. It would appear more than a coincidence that species of Ure- dinopsis, Milesia, and Hyalospora have their uredinial and telial stages on ferns and their other stages on firs, that nearly all species of Gymnosporangium bear their telia on Juniperus or closely 332 THE BASIDIOMYCETES related Cupressineae and their aecial stage on the Maleae, and that such a large proportion of the species of Puccinia and Uromyces, having teliospores on grasses and sedges, produce aecia on the Compositae or Ranunculaceae. Facts like these stimulate inter- est in the whole problem of heteroecism, and the conclusion seems inevitable that there is as yet no known reason why rusts are limited and grouped in their aecial and telial host relationships. Sexuality of the Uredinales jManv students of fungi have concerned themselves with the sexuality of rusts. Some of the results of their work have al- ready been given in this report, especially if they deal with the relationship of pycniospores to the origin of the dicaryotic con- dition in aeciospore mother cells [Craigie (1927, 1931)]. Presumably the pycniospores in many species of rusts function as male cells, fusing with trichogynes that project to the surface from basal cells in the developing aecia. It must be remembered, however, that some rusts are not known to possess pycnia and that the pairing of nuclei must therefore be accomplished by some other mechanism. This subject cannot be seen in proper perspective, however, unless a few of the other important re- ports on the sexuality of rusts are given attention. Apparently the work of Poirault and Raciborski (1895) in 1895 constitutes the first real cytological contribution to knowledge of rusts. They described conjugate nuclear division but were in error con- cerning the chromosome number. The next year the extensive study of Sappin-Trouffy (1896) appeared, describing and amply illustrating soral development in 10 genera and 36 species of rusts. He also determined that the paired nuclei fuse during matura- tion of the teliospore and that reduction-division occurs early in the course of promycelial formation. Interest in the sexuality of rusts was keenly stimulated soon thereafter by Blackman (1904). From examination of the aecia of Fhraginidhmt violaceinn he described the migration of a small nucleus from an ordinary vegetative cell into a larger special cell (female cell) containing a larger nucleus. This process was re- garded as the initiation of the sexual act, and it was held that ac- tual fusion was delayed until maturation of the teliospore. He viewed the buffer cells above the chains of aeciospores as degener- THE MYCOPLASM HYPOTHESIS 333 ate trichogynes and regarded the spermatia as functionally vestigial. Christman (1905) employed Gynniocoma interstitialis, Uro- myces caladii, and PJoragimdmm speciosiim to study their nuclear activities. He interpreted the basal cells in aecia that gave rise to binucleated aeciospores as isogametes and the aeciospore mother cells as non-resting zygotes. In the meantime Blackman and Fraser (1906) continued their studies, using Uromyces poae, U. ficariae, Fucciiiia poarwn, P. malvaceanim, P. adoxae, and Melampsora rostrnpii, and concluded that Blackman's earher interpretation was correct for certain rusts but that Christman's was for others. A second paper by Christ- man (1907), using Phragviidiinn potentillae-canadensis, found the author upholding the conclusions of his earlier report. In 1908 Olive (1908), from studies with Triphraginmm iihnariae and Puc- cinia deformans, sought to harmonize the conflicting interpreta- tions of Blackman and Christman. In this paper Olive indicated that, if one of the pair of cells was tardily pushed up\\ard be- tween larger cells, the fusion would appear to arise from a vege- tative cell, thus agreeing ^\■ith the interpretation of Blackman. If, on the other hand, the cells arose side by side, there was fusion of equal gametes, as stated by Christman. Results of studies of like nature on approximately 40 other species by nearly a score of workers are tabulated by Arthur et al. (1929, pp. 120-121). The My ooplasm Hypothesis Many investigations have centered about attempts to learn how the cereal rusts hibernate. Perhaps none has directly or indi- rectly stimulated more study of rust hibernation than the myco- plasm hypothesis announced by Eriksson in 1894. He main- tained that during the winter there is an intimate mixture of the protoplasm of the rust with that of the host, so that the two cannot be distinguished. In the spring, when conditions favorable for growth return, the fungus plasma becomes organized into definite elongated, curved bodies (Korperchen), which grow out into the intercellular spaces and become mycelial. Ward (1902, 1903) early pointed out that the Korperchen were in reality haus- toria, and violent discussion ensued. Other papers by Eriksson (1897, 1903, 1922), which indicate maintenance of his firm be- S34 THE BASIDIOMYCETES lief in the mycoplasm hypothesis, followed. When he grew cereals in the greenhouse, the plants became infected. It seems his^hlv probable, however, that Eriksson made use of diseased seed grain and that insufficient care was exercised to prevent in- fection in his greenhouse experiments. Specialization Specialization of parasitism among rusts constitutes one of the most interesting and important problems in uredinology. A basic concept in this field requires that a species be regarded as a col- lection of morphologically similar organisms or strains that differ in ability to produce infection in different hosts. Although this matter is more fully discussed in Chapter 11, Volume II, it should be indicated at this point that experiments by Eriksson, Klebahn, Stakman, and many others have amply demonstrated the existence of specialized strains, races, and forms among cereal rusts. For example, Fiiccinia graminis consists of: {a) P. gravtinis tritici on Triticiivi viilgare. (b) P. graminis secalis on Secale cereale and other hosts. (c) P. graminis avenae on Avena sativa and other hosts. (d) P. graminis airae on Air a caespitosa. (e) P. gravjinis poae on Poa compressa and other species. (f ) P. grajiiinis agrostidis on Agrostis caninis and other species. In experiments extending over a long period, Stakman et al. (1934) have shown that barberry is essential for the production and perpetuation of varieties and forms of Piiccinia graminis. Of 675 aecial collections 34.2^0 were of the tritici variety, 63.7% of the secalis variety, and 2.1% of the avenae variety. Their evi- dence led them to conclude that the origin and persistence of the secalis, poae, and agrostidis varieties are dependent upon the pres- ence of barberries. They found the physiologic forms of P. graminis tritici to belong within 26 distinct form groups. In 8000 collections of urediniospores a new form was encountered about once in 100 collections, whereas in 71 collections made near rusted barberries 19 belonged among the 26 recognized forms, and 1 had never before been encountered within the United States. IMPORTANT SPECIES OF RUSTS 33S Physiologic forms have been demonstrated to exist among other varieties of P. graminis and among other cereal rusts. Knowledge of these matters requires perusal of the reports of the extensive researches by Stakman and his associates. Classification of Uredinales There are two outstanding extensive monographic treatises dealing with classification of the rusts: that by Arthur (1907- 1931), published in The North Ajiierican Flora; and Monographia Uredinanmi, a four-volume series by the Svdows (1904-1924). The Sydows' first volume is devoted to Puccinia, the second to Uromyces, the third to all other genera, and the fourth to im- perfect, cycled species. Other less comprehensive but very use- ful taxonomic w^orks include those by Arthur (1934), Cunning- ham (1931), Eriksson and Hennings' (1896), Faull (1932, 1934, 1938), Grove (1913), Kamei (1940), Kern (1911), Klebahn (1904), Long (1903), and Ale Alpine (1906). The Sydows (1904-1924) separate the rusts into 3 families as follows: 1. Promycellum external 2 2. Teliospores free, loosely fascicled, fused into a compound head, or in chains, but never compacted laterally into crusts; usually pedicellate Pucciniaceae 2. Teliospores fused laterally to form a crust, or in columns, rarely occurring singly in the host tissue; not stalked Alelampsoraceae 1. Promycelium internal, teliospores fused laterally, forming waxy closely adherent crusts Coleosporiaceae Arthur (1907-1931) employed essentially the same charac- teristics in his familial separations, but in his Manual of the Rusts in the United States and Canada only 2 families, the Alelamp- soraceae and the Pucciniaceae, are recognized. The Alelamp- soraceae are divided into 4 tribes, Puccinastreae, Cronartieae, Alelampsoreae, and Phakosporeae; and the Pucciniaceae into 3 tribes, Ravenelieae, Phragmidieae, and Aecidieae. Important Species of Rusts The rusts are of great economic importance because of the losses that they cause from their attacks, especially on cereals but 336 THE BASIDIOMYCETES also on fruits and vegetables, on fiber and forage crops, on orna- mentals, and on forest and shade trees. Among all these, Ptic- cinia grainims, with its varieties tritici, avenae, and secalis, is un- doubtedlv the most destructive, and is world-wide in distribution. Fiiccin'hi ghmiannii causes stripe or vellow rust of wheat, rye, and barley throughout the pid World, and was introduced into the Western Hemisphere about 25 years ago. Fiiccmia triticifja, causing leaf rust and producing aecia on Thalictrum, is another important rust of \\'heat. Fiiccivia coronata, the crown rust, at- tacks oats and bears its aecia on Rhamnus. The common leaf rust of rye, P. nibigo-vera (P. dispersa), is coextensive in range with its host and bears aecia on Anchusa. Oxalis stricta serves as the aecial host for corn rust, P. sorghi. This rust is widely dis- tributed in North America but normally does not cause serious losses. Among fruit rusts no other produces losses comparable in magnitude to those caused by Gymnosporangium. The mono- graph of Kern (1911) lists 40 species, all heteroecious except G. ber?7mdianiim. None has a uredinial stage except G. nootkatense^ occurring on Chamaecy parts nootkatensis. Crataegus serves as aecial host for 11 species, Amelanchier for 12, Pyrus for 7, Malus for 6, Sorbus for 6, Aronia for 4, Cydonia for 5, Cotoneaster for 2, Pourthiaea 2, and Peraphyllum, Fendlera, Porteranthus, Phila- delphus, 1 each. Two species, G. juniperi-virgmianae and G. globosinn, commonly attack apples in North America, and one, G. yamadae, attacks this fruit in the Orient. In the United States, G. chwipes is the most serious of the pear and quince rusts; in Europe, G. sabinae. The foliage and also twigs of stone fruits, especially peaches, cherries, and plums, are subject to attack by Tranzschelia pnim-spinosae, whose aecial stage is produced on Anemone, Hepatica, and Thalictrum. Cronarthmj ribicola, the cause of blister rust in five-needle pines, is among the best known and most destructive of tree rusts. Its pycnial and aecial stages appear on the trunks and branches of white pines, and the uredinial and telial stages occur on the foliage of currant (Ribes) and gooseberry (Grossularia). The pycnial stage first appears several years after inoculation; the aecial stage (peridermium) may not appear until the following year. The mycelium within pines is perennial and forms annual IMPORTANT SPECIES OF RUSTS 337 crops of aeclospores throughout the hfe of the infected branch or tree. Throughout the southeastern United States Cronartiinn qiier- ciiim? and C. cerebnnn incite the production of stem galls on pines. This stage (peridermium) on young trees causes dwarf- ing and crippling. The uredinial and telial stages occur on the lower leaf surface of various oaks. Cronart'mm coleosporioides (C. havknessii) causes the forma- tion of stem galls on ponderosa pine and other pines of the west- ern United States. The uredinial and telial stages of this rust occur on certain Scrophulariaceae, especially species of Castilleja and Pedicularis. Nearly a score of rusts having aecial stages on the needles of various pines occur throughout North America. The aecial stages of all are pink tubular protrusions, and all appear quite alike. The uredinial and telial stages of each are restricted to certain genera of comiposites, such as goldenrod or sunflowers, or to species of Senecio, Parthenium, Coreopsis, Euthamia, Son- chus, or Elephantopus. A group of widely spread rusts belonging to Uredinopsis and Milesia attacks various species of firs. Ferns constitute their al- ternate hosts. Uredinopsis viacrosperma on Fteridiinn aqiiUinhnn can persist from year to year in the complete absence of firs. Several species of Melampsora attack larch foliage. One of them, M. viediisae, bears pvcnia and aecia on species of Populus, and another, M. bigelowii, on species of Salix. Melampsora lini is widely prevalent wherever flax is grow n. It is full-cycled but autoecious. Melampsora farlo-ivii, common on hemlock leaves, twigs, and cones, has telia only. Throughout all tropical countries Cerotelium fici is the com- mon fig rust. Hemileia vastatriXy \\ith peculiar urediniospores that are echinu- late only on the exposed upper surface, has long been known to cause a serious disease of coffee in the tropics of the Old \\'orld. Although it has greatly restricted coflFee production there, as yet it has not become established in the Western Hemisphere. The most important rusts on vegetable crops include Puccinia asparagi on asparagus, Uromyces appendicidatiis on beans, Uro- myces fabae on peas, and Puccinia siibnitens on beets. All are SSS THE BASIDIOMYCETES auroecious except P. s-nlviitejis, the telial host of which is salt marsh grass, Di.^ichlis spicatj. Florists and gardeners have widely encountered Uroviyces caryopkyUinus on carnations, Fuccima cbrysantheiJii on chn's- ant'hemums. P. vialvaceannn on hollyhocks, P. antirrbini on snap- dragons, and various species of Phragmidium on roses. LITERATURE CITED Attfv. R. F.. "A c\-Toloeical srudv of heterothallism in Fuccima trhic'ma^' J. Agr. Research, -H: 734^754, 1932. "A c\-toloeical studv of heterothallism in Pucchiia coronatar J. Agr. Research, 4S: SU-S-M, 19323. -A c\-toloeical studv of heterothallism in flax rust." /. Agr. Research, 49:765-~9l, 1934. ""A c\Toloeical studv of heterothallism in Fuccima sorghi," J. Agr. Re- search, 49: 104~-1068. 1934a. Andrus. C. F.. "The mechanism of sex in Uromyces appenJicuhtus and L'. vignae," J. Agr. Research. 42: 559-587, 1931. Arthl-r. J. C, '-Taxonomic importance of the spermogonium," Bull. Tor- rey Botan. Club, SI: 125-159. 1904. "Amphispores of the grass and sedge rusts." Bull. Torrey Botan. Club, 5:.- 35-^1, 1905. "Uredinales," North. A??!. Flora. -.-83-969, 1907-1931. Manual of the rusts in United States and Canada. 438 pp. Lafayette, Ind. 1954. Arthur- J. C et al.. The plant rusts {Uredinales). 446 pp. John Wiley and Sons. New York. 1929. AsHwoRTH, E>oROTH\-. "An experimental and c\-tological study of the life histor\- of Endophyllum se7?ipervivi,'' Trans. Brit. Mycol. Soc, 19: 240-258, 1934. Barclay. A.. "On the life history- of a remarkable uredine on Jasniinwn grajjJiflonwi L. (Uroviyces curminghaimamis, n. sp.)," Trans. Linn. Soc. London, 3: 141. 1891. Bary. Anton de, "Recherches sur le developpement de quelques cham- pignons parasites," Ann. sci. nat. Botan., ser. 4, 20:5-148, 1863. (Vide pp. 68-101.) '•Neue Untersuchungen iiber die L'redineen, insbesondere die Entwickel- ung der Puccinia graifiims und den Zusammenhang derselben mit Aecidiwn berberidis," Monatsber. K. Freuss. Acad. Wiss. Berlin, 1865: 15-49. 1865. Bl-^ckman. \'. H.. "On the fertilization, alternation of generations, and general c\-tolog>- of the Uredineae." ^7777. Botany, 18: 323-373, 1904. Bi_\cK-MAN, V. U..ASD Helen C. I. Fr.\ser, "Further studies on the sexual- ity of the Uredineae," .-I7777. Botany, 20: 35-48, 1906. LITERATURE CITED 339 Brown, A. M., "A study of coalescing haploid pustules in Fiiccinia kelian- thi;' Phytopathology, 25: 1085-1090, 1935. "The sexual behavior of several plant rusts," Can. J. Research^ 18: 18-25, 1939. BuLLER, A. H. R., 'Fusions between flexuous hyphae and pycnidiospores in Puccinia gra?7tims" Nature, 141: 33-34, 1938. Christmax, A. H., "Sexual reproduction in the rusts," Botan. Gaz.^ 39: 267- 275, 1905. 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"Die heuti^e Stand der Getreiderostfrage," Ber. dent, botan. Ges., IS: 183- 194, 189". "The researches of Professor H. Marshall Ward on the bro\\-n rust of the bromes and the mycoplasm h\-pothesis,"' Arch. Botan., 1: 139-146, 1903. "The mvcoplasm theory: Its scientific importance and practical signifi- cance.'' Bull. Agr. Intemat. Inst., Monthly Bull. Agr. Intel. Plant Dis., 13: 269-2S0, 1922. Eriksson, J., and E. Hen-nings. Die Getr eider oste, ihre Geschickte, itnd 'Natur, saii'ie Massregeln gegen dieselbev. 463 pp. Stockholm. 1896. Faull. J. H., "Taxonomv and geographical distribution of the genus Mi- lesia," Contrib. Arnold Arboretum, 2: 1-138, 1932. "The biolo^- of Milesian rusts." /. Arnold Arborenmi, iJ: 50-85, 1934. "The biolos\- of rusts of the genus Uredinopsis," /. Arnold Arboretum, ;;>.• 402^36, 1938. Fro.mme, F. D., "The morphologv- and c\-tolog\- of the aecidium cup," Botan. Gaz., 58: 1-35. 1914. Gro\t, W. 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O., "The production of a promycelium by the aecidiospores of Caeovia nitens Burrill," Bidl Torrey Botan. Club, 40: 361-366, 1913. "Nuclear behavior in the promyceha of Caeovm nitens Burrill and Vuc- cinia peckiana Howe," Am. J. Botany, 1: 37-46, 1914. Long, AA'. H., "The Ravenehas of the United States and Mexico," Botan. Gaz., 35: 111-133, 1903. AIcAlpine, D., The rusts of Australia, vii + 349 pp. Melbourne, 1906. MoREAU, F., AND Mme. F., "Les Uredinees du groupe Endophyllum," Bidl. soc. botan. France, 66: 14-44, 1919. Moss, E. H., "The uredo stage of the Pucciniaceae," Ann. Botany, -/0;813- 847, 1926. Oli\-e, E. W., "Sexual cell fusions and vegetative nuclear divisions in the rusts," Ann. Botany, 22: 331-360, 1908. "Origin of heteroecism in the rusts," Phytopathology, 1: 139-149, 1911. Orton, C. R., "A working hypothesis on the origin of rusts, with special reference to the phenomenon of heteroecism," Botan. Gaz., 84: 113-138, 1927. Pady, S. M., "The role of intracellular mycelium in systemic infections of Rubus with the orange rust," MycoL, 27; 618-637, 1935. PiERSON, R. K., "Fusion of pycniospores with filamentous hyphae in the pycnium of the white-pine blister rust," Nature, 131:728-729, 1933. PoiR-\ULT, G., AND M. Raciborski, "Sut Ics noyeaux des Uredinees," /. Bot., i?; 318-332, 381-388, 1895. Rice, Mabel A., "The relation of Uromyces caladii and other rusts to their hosts," Bull. Torrey Botan. Club, 61: 155-162, 1934. Sappin-Trouffy, p., "Recherches histologiques sur la famille des Uredinees," Botaniste, S: 59-244, 1896. Stakm-\n, E. C, M. X. Levine, R. U. Cotter, and Lee Hines, "Relation of barberry to the origin and persistence of physiologic forms of Fuccinia graviinis-' J. Agr. Research, 48: 953-969, 1934. Sydow, p. and H., Monographia Uredinarwn, sen specierwn omniimi ad hunc usque dievi descriptio et adumbratio systematica. Leipzig. 1: 972 pp., 1904; 2:396 pp., 1910; 5;728 pp., 1915; ^:670 pp., 1924. Ward, H. Marshall, "On the relations between host and parasite in the bromes and their brome rust, Fuccinia dispersa Erik.," Ann. Botany, id: 233-315, 1902. EXOBASIDIACEAE 341 ''On the histology of Uredo dispersa Erik., and the mvcoplasm hypothe- sis," Phil. Trans. Roy. Soc. London, B, 196: 29-^6, 1903. Whetzel, H. H., H. S. Jackson, and E. B. Mains, "The composite Hfe history of Fiiccinia podopbylli Schw.," /. Agr. Research, 30: 65-79, 1925. ' HO.MOBASIDIO.MYCETES Hymenomycetes (Agaricales) As considered in this book, the As^aricales include 6 families of funm. Some mycolos^ists regrard certain of these families as of ordinal rank and the tribal groupings as of familial rank. These 6 families are separated as follows: 1. Basidiocarps lacking; parasitic on yascular plants Exobasidiaceae 1. Basidiocarps present; saprobic or parasitic 2 2. Basidiocarps arachnoid, membranaceous, leathery or \yoody, effused, shelying or erect; hymenium plane Thelephoraceae 2. Basidiocarps fleshy to cartilaginous; clayate to coralloid; hy- menium amphigenous Clayariaceae 2. Basidiocarps fleshy gelatinous, cartilaginous, or leatherv% yariable in form; hymenium typically of spines or tubercules Hydnaceae 2. Basidiocarps fleshy, leathery, or \yoody, resupinate, shelying, or pileate; hymenium pitted, poroid, daedaloid, or lamellate Polyporaceae 2. Basidiocarps usually fleshy, mostly stipitate and pileate, a few shelying; hymenium lamellate Agaricaceae Exobasidiaceae The fungi included in the Exobasidiaceae, approximately 30 species, are parasitic on leayes, stems, flo^^"ers, and fruits. Exo- basidium typifies the family. Its species produce marked hy- pertrophy and hyperplasia, especially on Ericaceae. Exobasidiiivi 'vaccinii deforms the shoots and leayes of cranberry, Oxy coccus 77?acro carp 071, and related species of A'accinium. Exobasidnn7i rhododendri incites the formation of larsre yesicular stalls, especially on the leayes of Rhododendron catawbiense and R. 7/iaxi77m77i. Exobasidni77i sy77iploci causes galls to form on 5y7;/- plociis tinctoria. On Azalea E. discoideii77i may induce the for- mation of hypertrophies 3 to 5 cm tall, \yhich resemble some- what the basidiocarps of Cantharellus. LonCT afjo Woronin studied Exobasidium, and more recently it was subjected to detailed study by Eftimiu and Kharbush 542 THE BASIDIOMYCETES (1927). The mycelium is abundantly intercellular, branched haustoria occurring within the host cells. The clavate basidia extend above the surface between the epidermal cells, much as do the asci in Taphrina. Each basidium bears from 2 to 8 basidio- spores. In culture the basidiospores of most species of Exoba- Remnants of universal veil Pileus or cap Volva, part of universal veil Bulbous base of stipe Mycelium Fig. 128. Structural features of a mature fruit body of Amanita, in diagram. sidium germinate in the manner of yeasts; E. rhododendriy which forms germ tubes, is a notable exception. Host differences have been largely employed in distinguishing species of Exobasidium, but it appears that the validity of such specific distinctions can be established only by reciprocal infec- tion experiments. Such experiments remain to be performed. THELEPHORACEAE 343 Kordyana, causing necrotic spots on tropical species of Com- melinaceae, forms fascicles of basidia and sterile hyphae that emerge from the stomata. The basidia are variable in form and are 2-spored. From illustrations of K, polliae in the study by Gaumann (1922), this genus may well be judged to be related to /^\ /^ /^ /^^ Microstroma, which appears to be established among the Fungi Imperfect! [Wolf (1929)]. Thelephoraceae L L 4 t 0 Fig. 129. Stages in formation of a clamp connection. The dicaryotic cell is a hyphal tip, and nuclear division is conjugate. This family contains approx- imately 20 genera and 1000 spe- cies of membranaceous to leath- ery fungi in which the hymenial surface is smooth or only slightly contoured. Under the title "The Thelephoraceae of North Amer- ica" Burt (1914-1926) published a series of taxonomic papers, the most comprehensive treatise extant on the family. Many Thelephoraceae are important causes of decay in woody plants. The sporocarps vary in shape from crustose or resupinate to bracket-shaped or funnel-shaped structures with the hymenium on one surface only. Sterile elements occur interspersed with basidia in a few genera, such as Aleurodiscus; in Peniophora and Hymenochaete they are sharp-pointed, whereas in Asterostroma they are stellate. These sterile elements are given different names based on shape and consistency. If they are hair-like, they are cystidia; if thickened and awl-like, they are setae; and corneous or gelatinous gloeocystidia. The nature of the sterile elements is taken into consideration in the separation of genera and of species. Little consideration has been given the developmental mor- phology of Thelephoraceae except in a few species. Corticiinn vagUTfi, widely known as a stem and root parasite of many kinds of economic plants, forms its oval basidia sparsely on an arach- 344 THE BASIDIOMYCETES noid or loosely compacted subiculum. Its Rhizoctonia solaiii stage may form compact brown sclerotia capable of withstand- ino^ long periods of unfavorable weather. Cortichnn koleroga is equally widely distributed in tropical and subtropical regions and produces thread blight of leaves, fruits, and twigs of many species of trees and shrubs. Its mycelial stage also belongs to Rhizoc- tonia, and sclerotial formation is in part determined by whether W A B C D E F G H I Fig. 130. Diagrammatic representations of stages in transformation of a dicarvotic hvphal tip into a basidium. the host tissues have a roughened surface. iMost species of Corci- cium have a papery to leathery hymenophore and lack the Rhi- zoctonia stage. Peniophora is quite like these kinds of Corti- cium, but awl-shaped cystidia are interspersed among the basidia. In the southeastern United States P. gigantea is one of the im- portant fungi involved in the decay of pine pulpwood stacked in yards. Coniophora cerebella also causes dry rot of coniferous wood throughout North America. Thelephora fimbriata and T. terrestris grow up from the soil of nursery beds and smother or strangle tree seedlings. They seem unable to penetrate living host tissues but are able at times to cause serious losses in forest-tree nurseries. Stereum is among the larger genera. Burt (1920) lists 80 CLAVARIACEAE 34S species as occurring in North America. In the account of Over- holts (1939) 27 species are recognized in Pennsylvania. Certain of them, notably Stereiim gaiisapatiim, cause decay of oak-sprout growth, especially if the sprouts arise high on the stumps. On oaks and other hardwoods 5. piistulosiim produces a wide-spread white pocket rot. Clavariaceae The Clavariaceae, or coral fungi, comprise 8 or more genera and approximately 500 species. Nearly all are saprophilous, oc- FiG. 131. Oidial production by Coprimis lagopiis. A. Diagram showing 48-hour-old haploid mycelium on the surface of dung agar, with short lateral oidial fructifications. B. Single oidiophore with an excreted drop of liquid at its apex. C. Oidia held together at apex of oidiophore in a drop of Hquid. D. When oidiophore is immersed in film of water, the oidia are dispersed. (Adapted from Brodie.) curring on the leaf mold of the forest floor, some few are quite surely mvcorrhizal, and a few are pathogenic. Their fructifica- tions are fleshy, cartilaginous, gelatinous, or, rarely, leather)'; they range from clavate to much-branched and coralloid. Some 346 THE BASIDIOMYCETES are tiny, being about 1 cm tall, whereas others, such as Sparassis crispa, may attain a diameter of nearly 0.5 meter. Clavariaceae undoubtedly possess among the most beautiful of fungus fructi- fications. Many species are edible. The monograph by Coker (1923), dealing with species of Clavaria occurring in Canada and the United States, is most serviceable for identification of species in these countries. That by Cotton and Wakefield (1918) serves for identification of Brit- ish species. Of most importance, perhaps, is Sparassis radicata, reported by Weir (1917) to kill and decay the roots and the sapwood of basal portions of trunks of fir (Pseiidotsuga taxifolia), pine {Finns monticola), and spruce (Picea engelmamiii). The fructi- fications have a long, very compact, root-like base, into w^hich soil particles may be incorporated, and which extends down to the deeper lateral tree roots. This root-like base terminates in rhizomorphs that penetrate the host; eventually the host roots succumb. Hydnaceae The Hydnaceae are characterized by possession of spiny or toothed hymenial surfaces. The fructifications may be resupi- nate, pileate, or stalked, varying in consistency from fleshy to leathery or woody. The Hydnaceae comprise 10 to 15 genera and approximately 600 species. Nearly all are saprophytic on wood, but a few cause heartwood rots of trees. Others occur on the forest floor. Taxonomic studies of this family have been conducted by Banker (1906), Miller (1933, 1933a, 1934, 1934a), and Miller and Boyle (1943), and their reports are invaluable in the identifica- tion of species. Hydninn cor all aides (also given the generic names Manina and Hericium) may form large fructifications on decaying logs. Hydmn7i erinaceiis {Manina cordijorinis) forms white conchoid fructifications, 13 to 15 cm across, with long-pointed, pendant teeth. The fructifications extend from branch scars on Nyssa, Quercus, Liquidambar, Platanus, and other hardwoods. Echino- dontiiim tinctoriinn forms large corky to woody fructifications on Tsuga in the Pacific Northwest and is an important cause of POLYPORACEAE 341 decay of standing timber. Hydniim septentrionale induces heartwood rot of maples. Polyporaceae The Polyporaceae, or pore fungi, as treated in this book, com- prise about 20 genera and perhaps 2000 species. They are of enormous importance as the cause of disease of standing timber Lamellate Fig. 132. Structural characters employed in identification of polypores, including: A to H, types of fruiting bodies, / to M, pore surfaces, N to P, setae, Q, paraphyses, R, cystidium. and decay of logs and lumber. Many American students have devoted themselves to problems of the taxonomy and classifica- tion of the polypores; among them are Murrill (1907-1908, 1910), Ames (1913), Overholts (1914, 1915), Burt (1917), Baxter (1927, 1929, 1932, 1933, 1934), Shope (1931), Humphrey and Leus (1931), and Lowe (1934). Similarly many mycologists in other 348 THE BASIDIOMYCETES parts of the world have given these fungi critical study. Accord has not been reached on generic and specific limits, as is evident from the fact that Murrill (1907-1908) recognizes 78 genera of North American polvpores, whereas others reduce this number to less than 20. Among the structural features which appear to constitute rational bases for generic distinction are: (1) consist- ency of the fructification, whether fleshy, gelatinous, leathery, corky, or woody; (2) shape of the fructification, whether resupi- nate, effuse-reflexed, bracket-like, applanate, ungulate, or stipi- tate; (3) shape of the pores, whether circular, angular, labyrinthi- form, daedalioid, or lamelliform; (4) nature of the pore layer, whether the pores are separable from the context (tissue of the pileus), whether the tissue of the pileus extends between the pores, w^hether the pores are shallow corrugations or well-defined pores, whether the pores are separate peg-like tubes, or whether their contiguous walls are united. The Polyporaceae may rather conveniently be divided into the following 4 tribes, according to Hennings: a. Basidiocarp effuse, at first plane but having fold-like elevations which anastomose to make shallow and irregular pits Meruleae a. Basidiocarp having tubes, alveolar areas, labvrinthiform passages, or radiating lamellae b. Substance of the hymenium continuous with dissepiments of the tubes; tubes not readilv separable from the context (hy- menophore) c. Tubes closelv contiguous Polyporeae c. Tubes standing sins^lv Fistulineae b. Substance of hvmenium easily separable from the hvmenophore Boleteae Meruleae. Aienilhis lacrymans, \\'hich typifies the genus, causes dry rot of woodwork in buildings. Extension of the fungus is accomplished by fibrous rhizomorphs. It forms wide- spreading gelatinous to cartilaginous fructifications that are re- ticulately folded or corrugated. Burt (1917) found that the ba- sidia are mature while the hymenial surface is still plane and that, by subsequent growth, folds appear; thus the basidia clothe the edges of the folds as well as the sides and bottom. In other Polyporaceae the pores are formed in advance of the maturation of basidia; hence some workers would exclude Merulius from this family. POLYPOREAE 349 PoLYPOREAE. In PoHa are placed all fleshy, leathery, or woody strictly resupinate forms having true pores. In a sense it is a form genus, since normally shelving species may at times be resupinate. The hymenium continues to develop centrifugally, ne^^' pores being formed in the zone near the margin. Baxter (1927, 1929, 1932, 1933, 1934) has devoted himself to the diffi- cult problem of classification of this genus. All species may Fig. 133. Daedalea quercma, lower surface of fructification. cause decay of timber, some being especially destructive to beams, floors, mine* props, and lumber piled in yards. Notable among these fungi are P. vapor aria and P. incrassata [Humphrey (1923)]. Polyporus includes a large number of species of pore fungi having shelving or stalked fructifications that may be fleshy when young but become hardened, leathery, or corky at maturity. The pore layer is usually quite different in texture and color from the remainder of the pileus. As thus delimited, Polyporus may well include several generic types. Polyporus versicolor and P. pargamemis are perhaps the most commonly encountered members of this genus. They cause de- cay of many species of deciduous woody plants, just as P. abieti- niis does of coniferous species. Polyporus sidphtireus, occurring 3S0 THE BASIDIOMYCETES at the base of deciduous trees, especially oaks, produces large, fused, imbricated shelves that are conspicuous because of their bright sulphur-yellow to orange color. Poly poms cinnabariniis has bright, cinnabar-colored brackets, especially on decaying oak branches. Polyponis sclnveinitzii is a common cause of butt rot of overmature coniferous trees. Fig. 134. Daedalea confragosa on birch. • Considerable interest has always centered around the polypores that produce giant sclerotia. The best known among them are P. sapiirema from Brazil and P. mylittiae from Australia. The Australian species may attain a weight of 30 to 40 or more lb. On the roots of various trees, especially pines, in the southeastern United States occur sclerotia that may attain a weight of over 20 lb. The polypore responsible, according to Wolf (1922) and Weber (1929), is Poria eocos. The Genus Fomes includes perennial punky to woody poly- pores. A new layer of pores is formed each year over that of the preceding year. Among the smaller species is F. ohioejise, with ungulate conchs about 1 cm in diameter; F. applanatus may BOLETEAE 351 have brackets nearly 1 meter in their largest dimension. Fomes igniarius, F. pini, and F. robiistiis, causing heartrot of standing timber, have large hoof-shaped fructifications with as many as 40 to 80 layers of pores. Fomes annosus causes root rot and basal- stem rot of conifers in Europe. Its fructifications form near the surface of the soil and may have incorporated in them twigs, leaves, and stones. In culture this fungus bears conidia belong- f" •• ^'^^^^^^ » *^ * WriiLil ^ \ «!r ^^^ 6 _^<. ^■■* ■ ■*^»^3^'«'5P* * ^9 p*^ «* ■ ■ • ^w* ■ s* i" ^jm^i^^A WW'^^I^^M^^^SiSi^^^^^^ Ii Lffyf i y ^K>^^^^^ j ■i^^^i- 5 ■'M^mmmm^m^ ^ '^ft^^^todlg*^ HTJ ^ i^ ^^^l^'^f^^^n ^f^ 1 1 Fig. 135. Stereinn frustulosimi on oak. ins: to Oedocephalinn globidiferiim. Studies [Miller (1942)] show that the incidence of root rot and butt rot on Jiinipenis virgmiana caused by F. annosiis in the southeastern United States is correlated with the degree of competition between cedars and the hardwoods that overtop them. FisTULiNEAE. Fistidhia hepatica, called the beef-steak fungus, orrows widely on deciduous trees, especially oaks. Its large, fleshy, fan-shaped fructifications, brown-red on the outside and blood-red within, are attached by thick stipes. The hymenium is beset wdth closely crowded, but separate, tubes that are closed when young but open at maturity. BoLETEAE. The fructifications of this tribe are fleshy, pileate, and mostly centrally stipitate. The pileus is thick and convex. 352 THE BASIDIOMYCETES and the stipe is stout. Boleteae grow on the forest floor, and many of them are mycorrhizal and always associated with a cer- tain species of tree. The development of boletes has been studied by Zeller (1914), Yates (1916), and Kiihner (1926). Boletus {Ceriomyces) zelleri and B. parasiticus, the second of which grows on the pilei of other boletes, are gymnocarpous. In Bo- Fig. 136. Fructification of Manina cordijorviis {Hydmim erinaceiis) . letiniis cassipes and Strobiloinyces strobilaceiis, however, an en- dogenous annular furrow appears, and a partial veil covers the young pore surface. As the pileus expands, the remnants of the veil remain as a ring surrounding the stipe or as a cortina on the margin of the pileus. Volvoboletus appears to possess a universal veil. The members of the other tribes of Polvporaceae are all gymnocarpous except Cryptoponis volvatus. The course of de- velopment among the Boleteae inclines some mycologists [Yates (1916)] to regard them not as polypores but as agarics. The taxonomic studies by Murrill (1910), Snell (1936), and Coker and Beers (1943) should be used in identification of this tribe. AGARICACEAE 353 Agaricaceae The Agaricaceae constitute approximately 100 genera and 10,000 species. Nearly all are fleshy, centrally stipitate, pileate forms. A few, notably Pleurotus, Claudopus, and Crepidotus, Fig. 137. Conchs of Fomes applanattis, as seen from above and from the pore surface. are laterally attached and conch-shaped. The feature which characterizes the family is the hymenial surface of radiating gills or lamellae. This family is of importance mainly because its members ac- complish the decomposition of dead plant tissues in the soil and 3S4 THE BASIDIOMYCETES because they form mycorrhizae, mainly on forest trees. A few are pathogenic; Amiillaria mellea on orchard and forest trees [Thomas (1934)] and Marasmhis sacchari on the roots of sugar cane are the best-known parasitic species. Nyctalis asterophora and N. parasitica parasitize other agarics. Marasjnius saramentosiis causes "horse-hair blight" of cacao in the tropics, and other species of this genus also are known to cause thread blights of forest trees. Marasmius crinis-eqid is not uncommon on oaks in the Gulf Coast states. The fructifications vary greatly in size and durabilit\^ Those of some species of My- cena may have pilei a few millimeters in diameter that are very ephemeral. Schizo- phylliim cormnune, which is quite leathery, can be dried repeatedly but revives on be- ing- moistened. In fact, it is remarkably adapted to xero- phytism. Agariciis arvensis may have pilei 40 cm in di- ameter. The fructifications of AjJtanita solitaria attain a height of 30 cm with pilei 20 cm in diameter. The shagg\- mane mushroom, Coprimis comatiis, has been recorded to have fructifications 36 cm tall and pilei 25 cm in circumference. Development of basidiocarps among agarics. The develop- ment of basidiocarps among gill fungi is none too well under- stood, mainly for the reason that relatively few species have been studied. The status of this subject can best be appreciated from examination of reports by Atkinson (1906, 1914, 1914a, 1914b, 1916), Douglas (1916, 1918, 1920), Sawyer (1917, 1917a), Moss (1923), and Hein (1930). The fruit bodies of gill fungi are commonly called mushrooms Fig. 138. Diagrammatic sections ot developing basidiocarps of Mycena subalkali?ia, of gymnocarpous type. A. Undifferentiated "button." B. Ini- tiation of pileus at apex of stipe. C. Hymenial surface becoming ap- parent at lower edge of young pileus. D. Lamellar development has pro- gressed, and margins of pileus are rolled inward toward the stipe. E. Development of lamellae is well advanced. (Adapted from Douglas.) DEVELOPMENT OF BASIDIOCARPS AMONG AGARICS 35 S H Fig. 139. Diagrammatic sections of developing basidiocarp of Psalliota campestris. A. Undifferentiated egg. B. An annular cavity has formed, marking the site of developing lamellae. C. Pileus and stipe have developed to the extent of being evident. D. Expanding pileus with inner veil rup- tured to expose the lamellae. E. Detail of cavity, as in B, with downward- coursing hyphae at the ceiling. F. Detail of these same hyphae, as in C. G. Later stage in growth of gill that extends into the cavity. H. Bit of mature hymenium and subhymenium. 3S6 THE BASIDIOMYCETES or toadstools. The vegetative portion of a typical one, Amanita, exists in decaying leaf mold as white threads or strands. Small, compact white spherical bodies (buttons) that may be found alonof these strands constitute the initials of fruit bodies. If thev are properly cut in half, it mav be observed that a membrane, the universal veil, invests the entire button and that the central axis is occupied by the developing stipe with the pileus or cap at the top. The edges of the cap curve downward. A circular chamber soon appears, surrounding the stipe toward the upper end. This chamber enlarges as development proceeds, and lamellae or gills, radiately arranged, grow into it. The edges of the gills approach the stipe but are separated from it by a thin tissue, the veil, which connects the gill edges and surrounds the stipe. At the approach of maturity the stipe elongates, and the gills open in an umbrella- like fashion. As they do, the universal veil is ruptured but per- sists as a cup (volva) at the base of the stipe and as scales on the upper surface of the pileus. The veil covers the gills below and eventuallv ruptures to leave a ring (annulus) around the stipe. As the cap expands, the gills, arranged like spokes in a wheel, hang with their edges directed downward. The surface of the gills is the hymenium (fruiting laver), which consists of a pali- sade of club-shaped basidia. Each basidium bears four basidio- spores that are discharged forcibly into the space between gills. Air currents disseminate the basidiospores. The student soon learns to distinguish certain of the more com- mon genera of mushrooms. Amanita, Amanitopsis, and Lepiota are white-spored with gills free from the stipe and can be recog- nized because Amanita possesses a volva and an annulus, Amani- topsis a volva only, and Lepiota an annulus only. Russula and Lactarius, also white-spored, have firm, thick caps and short, thick stipes that are spongy-stuffed within. They differ in that Lac- tarius possesses "milk" that exudes when the pileus is injured and mav rather quickly become yellow, blue, orange, pink, greenish, or gray. Clitocybe and Tricholoma are white-spored, do not possess an annulus or a volva, and have fleshy, fibrous stipes with a cartilaginous rind. The gills of Clitocybe are decurrent or broadly adnate; of Tricholoma, sinuate. Cantharellus has thick, decurrent gills that are forked. Cortinarius is ochre-spored and possesses a cobweb-like veil. Pleurotus and Claudopus have DEVELOPMENT OF BASIDIOCARPS AMONG AGARICS 557 eccentric stipes, those of Pleurotus being white-spored and those of Claudopus pink-spored. Psalliota is purple-brown-spored and has an annulus, and its gills are free from the stipe. Coprinus is black-spored, and its gills deliquesce. Several developmental types exist among gill fungi. In Hygro- phorus, Cantharellus, and Clitocybe the gills are gymnocarpous, Equal Unequal Flexuous Dichotomous Fig. 140. Diagrams of gill characters, as shown by the lower surface of the pileus. arising around the lower edge of a dome-shaped portion that is to be the pileus. The lower margin of the pileus arches down- ward toward the stipe primordium, and the hyphae from each may intertwine beloM' the developing gills. In Armillaria, Co- prinus, Lepiota, Lactarius, Alarasmius, Russula, and other genera a schizogenously formed furrow encircles the stipe primordium, marking the beginning of the differentiation of pileus and stipe. This furrow arises endogenously, and hyphae from the ceiling of the furrow grow downward to form the gills. The thin layer of fundament tissue beneath the furrow and extending from the 358 THE BASIDIOMYCETES margin of the pileus to the stipe is the inner veil or partial veil. Since it mav not increase by the addition or formation of new hvphal elements, it may escape detection when the pileus ex- pands to the extent of exposing the gills to the exterior. On the other hand, the partial veil mav be reinforced to such an extent that, when the pileus expands, it will remain as an annulus, mov- able or not, surrounding the stipe, or as a frayed cortina hanging from the edge of the pileus, or both annulus and cortina may exist. The annulus becomes well developed in Amanita, Armil- laria, Coprinus, Lepiota and Psalliota, and in Cortinarius arach- noid cortinae exist at the lower edge of freshly expanded pilei. Quite a distinct additional structure occurs in Amanita and Amanitopsis. Surrounding the entire outer surface of the young button, like an eg^g- shell, is a membranaceous layer, the universal veil. As the pileus expands, this shell ruptures circumscissilely, and its remnants may then be seen as scales at the upper surface of the pileus and as a cup-like sheath or volva around the base of the bulbous stipe. The partial veil in Amanita is also strongly devel- oped and may grow as the pileus expands, eventually tearing at the rim of the pileus; it then hangs skirt-like around the stipe. The universal veil has been demonstrated as an external layer around the primordia of Agariciis arveneis, A. campestris, A. comtuluSy and Amanitopsis vaginata [Atkinson (1914)]. Classification. In classifying asrarics it is essential first of all to divide them into wholly artificial tribes, the groupings being based upon color of the spores, as follows: (1) Leucosporae, spores hyaline; (2) Rhodosporae, spores pink to red; (3) Ochro- sporae, spores yellow to ochre; (4) Alelanosporae, spores dark brown, purple, or black. Manifestly the use of spore color as a primary basis of division results in separating similar genera into different tribes. If spore color cannot be determined by direct examination, a spore print should be made. The characters next employed in distinguishing genera in- clude: (1) shape of the pileus; (2) consistency and character of the stipe and its attachment to the pileus; (3) shape, arrangement, and attachment of the gills; (4) presence or absence of annulus, cortina, and volva; (5) nature of the pilear surface and stipe and their markings. With experience genera soon come to be satis- factorily recognized, but specific distinctions are much more difficult. Size and color of the fructifications, size and markings CLASSIFICATION 359 of the spores, presence of cystidia, presence of latex and its change of color on exposure, and change of color of basidiocarps on being bruised and their taste are among the features that must be Plane Convex Infimdibuliform Umbilicate Reflexed Involute Campanulate Fig. 141. Characteristic shapes of pilei, in diagram, used in distinguishing genera of mushrooms. taken into account in distinguishing species. Experienced my- cologists admit that species are separated on minor differences and that among the larger genera the species are monotonously similar. The bibliography on the taxonomy of Agaricaceae is very ex- tensive, a fact which can be appreciated by consultation of the references in North Avierican Flora, \^olume 9. Many of the 360 THE BASIDIOMYCETES treatises are comprehensive, for example, those of Gibson (1895), Atkinson (1900), Kauffman (1918), xMurrill (1910-1916, 1914- 1932), Rea (1922), Giissow and Odell (1927), Lange (1934), and Krieger (1936). Many other very useful papers are mono- graphs of individual genera, such as those by Burlingham (1908) on Lactarius, by Coker (1917) on Amanita and Amanitopsis and Adnexed Fig. 142. Diagrams representing the manner in which gills of mushrooms ^ mav be attached to the stipe. (1922) on Laccaria and Clitocybe, by Beardslee (1918) on Rus- sula, by Coker and Beardslee (1921) on Collybia, and by Over- holts (1927) on Phohota. Amonor the agarics none has greater interest to mycolomsts than Coprinus, pilei of which deHquesce during discharge of spores. The pilei, especially of the larger species, are campanu- late. Buller (1910) demonstrated that the gills undergo auto- digestion upward from the lower rim of the pileus. The gills are propped apart by cystidia. The basidiospores mature pro- gressively upward from the lower pilear margin and are dis- charged, falling free in the interlamellar spaces. The gills and LITERATURE CITED 361 cystidia undergo digestion progressively in the zone immediately behind that from which spores have been discharged. Fairy rings. From time to time over a period of more than 100 years certain Basidiomycetes have been observed to produce fructifications in rings, called "fairy rings." Such rings arise by initiation of growth at some point, followed by centrifugal spread of mycelium through the soil. The diameter of the ring in- creases from year to year. As the mycelium advances, the or- oranic matter is decomposed and exhausted, so that recession is impossible. Shantz and Piemeisel (1917) made an extensive study of fairy-ring formation by Agariciis tabular is in grasslands of Colorado. They also noted from previous records that more than 50 species of agarics, boletes, and puffballs, which they list, are known to produce fairy rings. LITERATURE CITED Ames, Adeline, "A consideration of structure in relation to genera of the Polyporaceae," Ann. MycoL, ii; 211-253, 1913. Atkinson, G. F., Studies of Americaji jiingi. 275 pp. Andrus and Church, Ithaca, N. Y., 1900. "The development of Agariciis campestris,^'' Botan. Gaz., 42: 241-264, 1906. "Homology of the 'universal veil' in Agaricus," Mycolog. Centr., 5: 13- 19, 1914.' "The development of Lepiota clypeolaria,'" Ann. MycoL, 12: 346-356, 1914a. "The development of Amanitopsis vaginata,'' Ann. MycoL, 12: 369-392, 1914b. "Origin and development of the lamellae in Coprinus," Botan. Gaz., 61: 89-130, 1916. Banker, H. J., "A contribution to a revision of the North American Hydna- ceae," Mein. Torrey Botan. Club, 72:99-144, 1906. Baxter, D. V., "Some Porias from the region of the Lake States," Mich. Acad. Sci., 6:67-76, 1927; P; 39-46, 1929. "Some resupinate polypores from the region of the Great Lakes," Mich. Acad. Sci., IS: 191-228, 1932; 27:421^39, 1933; 19:305-332, 1934. Beardslee, H. C, "The Russulas of North Carolina," /. Elisha Mitchell Sci. Soc, 33: 147-199, 1918. Buller, a. H. R., "The function and fate of the cystidia of Coprinus atramentariiis, together with some general remarks upon Coprinus fruit bodies," Ann. Botany, 2-^:613-628, 1910. Burlingham, G. S., "A study of the Lactariae of the United States," Mem. Torrey Botan. Club, 14: 1-109, 1908. Burt, E. A., "The Thelephoraceae of North America. I. Thelephora," Ann. Mo. Botan. Garden, 1: 185-228, 1914. 362 THE BASIDIOMYCETES II. "Craterellus," 7:327-350, 1914a. III. '-Craterellus borealis and Cyphella," 1: 357-382, 1914b. IV. •Exobasidium;" 2: 627-658, 1915. V. "Tremellodendron, Eichleriella, and Sebacina,'' 2:731-770, 1914c. M. "H^-pochonus," S: 203-241, 1916. VII. "Septobasidiiim," 5:319-343, 1916a. MIL "Coniophora," -^: 237-269, 1917. IX. "Aleurodiscus," 5:301-372, 1918. XI. "Tulasnella, \'eluticepS5 Mycobonia, Epithele, and Lachnocladium," 5:253-380, 1919. XII. -Stereum," 7:81-248, 1920. XIII. '"Cladoderris, Hvpolvssus, C\Tnatella, Skepperia, C\'tidia, Solenia, .Matrouchotia, .Microstroma, Protocoronospora, and Asterostroma," 11: 1-36, 1924. XIV. "Peniophora," 72:213-257, 1925. XV. '"Corticium, and supplement to the whole series," 13: 173-354, 1926. '■.Memlius in North America,'' Arm. Mo. Botan. Garden, 4: 305-362, 1917a. G>KER. \A'. C, "Amanitas of the eastern United States,'' /. Elisha Mitchell Set. Soc, 33: 1-88, 1917. *"The Laccarias and Clitocybes of North Carolina," '/. Elisha Mitchell Sci. Soc, 38: 98-126, 1922. The Clavarias of the United States and Canada. 209 pp. Universirv^ of North Carolina Press, Chapel Hill. 1923. CoKER, \^'. C, AND H. C. Beardslee, "The Collybias of North Carolina," /. Elisha Mitchell Sci. Soc, 57:83-107, 1921. CoKER, W. C, AND Alaia H. Beers, The Boletaceae of Xorth Carolijia. vii -!- 95 pp. University- of North Carolina Press. 1943. CoLsox, Barbar.\, "The cytology of the mushroom Psalliota campestris Quel.," Ann. Botany, 49: 1-18, 1935. Cotton-, A. D., and E. M. AA\\kefield, "A review of the British Clavariae," Trans. Brit. Mycol. Soc, 6: 164^198, 1918. Douglas. G. E., "A study of development in the genus Cortinarius," A??i. J. Botany, 5:319-335, 1916. ''The development of some exogenous species of agarics," A7?i. J. Bot- any, S: 36-54, 1918. '•Early development of Inocybe," Botan. Gaz.y 70:211-220, 1920. EFTLNirL-, P., AND S. Kharbush, '"Recherches histologiques sur les Exoba- sidiees," Rev. path, vegetal e entoijiol. agr. France, 14: 62-88, 1927. Gaum-\nn, E., ''Uber die Gattung Kordyana," A7j?i. Mycol., 20:257-271, 1922. Gibson, W. H., Our edible toadstools and vmshromns and hen:; to dis- tijigiiish the??i. x + 337 pp. Harper and Bros., New York. 1895. Gussow, H. T., AND W. S. Odell, Mushrooms and toadstools. An account of the more conmion edible and poisonous fungi of Canada. 274 pp. F. A. Achland, Onawa. 1927. Hein, Illo, ''Studies on morphogenesis in Agaricus (Psalliota) campestris,^'' A??z. J. Botany, 11: 882-915, 1930. LITERATURE CITED 363 Humphrey, C. J., ''Decav of lumber and building materials due to Foria incrassata (B. and C.) Burt.," Mycol, ISilsClll, 1923. Humphrey, C. J., and S. Leus, ''A partial revision of the Ganodenfia ap- planatwn group with special reference to oriental variants," Philipp. J. Sci., -/J: 483-589. 1931. K.\UFFMAN', C. H., "The Agaricaceae of Michigan," Mich. Geol. Biol. Survey, Piibl 26, Biol. ser. 5, 1: 1-924, 1918; 2r 1-101, 1918. Krieger, L. C. C, The vnishroovi handbook. 538 pp. The Macmillan Co., New York. 1936. Ki'HNER, R., "Contribution a I'etude des Hymenomycetes et specialement des Agaricaces," Botaniste, 11: 1-224, 1926. Laxge, Jakob E., Flora Agaricina Danica. 5 vols. Copenhagen, Denmark. 1934. Lowe, J. L., "The Polyporaceae of New York State," N. Y. State Coll. Forestry Tech. Pu'bl., 41: 1-142, 1934. Miller, J. K., ''Fmnes annosus and red cedar," /. Forestry, 41: 37-40, 1943. Miller, L. W., "The genera of the Hydnaceae," Mycol., 25: 286-302, 1933. "The Hvdnaceae of Iowa. I. The genera Grandinia and Ox\-dontJa," Mycoi, 25: 336-368, 1933a. II. "The genus Odontia," 26: 13-32, 1934. III. "The genera Radulum, Mucronella, Caldesiella, and Gloiodon," 26: 212-219, "l934a. Miller, L. W., and J. S. Bo\'le, "The Hydnaceae of Iowa," Unh. lozi'a Studies Nat. Hist., 18. 92 pp. 1943. Moss, E. H., "'Developmental studies in the genus Collybia," Trans. Roy. Can. hist., 14:321-335. 1923. Ml-rrill, W. a., -Polyporaceae," North Am. Flora, P: 1-131, 1907-1908. "Boletaceae," North Am. Flora, 9: 133-161, 1910. "Agaricaceae," North Am. Flora, 9: 162-426, 1910-1916; 10: 1-328, 1914- 1932. 0\TRH0LTS, L. O., "The Polyporaceae of Ohio," Ann. Mo. Botan. Garden, i: 81-155, 1914. "Comparative studies in the Polvporaceae," Ann. Mo. Botan. Garden, 2: 667-730, 1915. "A monograph of the genus Pholiota in the United States," ^-^7777. Mo. Botaii. Garden, 14:87-210, 1927. "The genus Stereum in Pennsylvania," Bull. Torrey Botan. Club, 66: 515-537, 1939. Rea, C. British Basidiomycetae, a handbook to the larger British fungi. xi + 799 pp. Cambridge University Press. 1922. Saw\-er, "W. H.. "The development of Cortinarius pholideus,'^ Ani. J. Botany, 4:520-532. 1917. "Development of some species of Phohota," Botan. Ga^z., 64: 202-229, 1917a. 364 THE BASIDIOMYCETES Shantz, H. L., and R. L. Piemeisel, "Fungus fairy rings in eastern Colorado and their effect on vegetation," /. Agr. Research, 11: 191-245, 1917. Shope, p. F., "The Polyporaceae of Colorado," Ajjn. Mo. Botan. Garden, ;: 251-280, 1902. Chapter 8 THE DEUTEROMYCETES (FUNGI IMPERFECTI) The Deuteromvcetes are in reality the trash pile or the left- overs, containing the conidial- or imperfect-stage remnants of the classes already discussed. In many ways they are of the greatest interest among all the classes of fungi and certainly are of time- consuming concern to the mycologist in his taxonomic prob- lems. They are not given extended treatment in texts mainly for the reason that the groupings are wholly artificial and hence are completelv without phvlogenetic significance. To date between 15,000 and 20,000 Fungi Imperfecti have been described. According to Bender (1931), this vast miscel- laneous assemblage represents 1331 form genera. They com- prise (1) the mycelial, sclerotial, and conidial stages of species having perfect stages, that is, zygospores, oospores, asci, basidia, and teliospores, and therefore properly belong in the classes already discussed, and (2) those species of fungi whose perfect stages are not known. Even though the zygospores or oosporic stages of certain Phvcomycetes have never been observed, these species are commonly placed among the Phycomycetes rather than among the Deuteromycetes because of the coenocytic na- ture of their assimilatory structures. Furthermore, many rusts are known only in the aecial or uredinial stage but are properly placed in the Uredinales among the imperfect form genera Aecidium, Peridermium, Caeoma, Roestelia, and Uredo. Since the hyphae of many Basidiomycetes possess clamp connections, this criterion is of value, in the absence of a basidial stage, in relating so-called imperfect fungi to the Basidiomycetes. It seems probable therefore that the great majority of species treated as Fungi Imiperfecti really are Ascomycetes whose connection with an ascogenous stage has not been established. Some may never have possessed a perfect stage or, if they did, may have lost it. 383 584 THE DEUTEROMYCETES (FUNGI IMPERFECTI) Many imperfect fungi are pathogenic to plants and sporulate on the plant organs only while these organs are still alive. After the death of the tissues, conditions may be favorable for the pro- duction of the perfect stage, which such species may be found to require for hibernation. Other species, however, produce co- Fig. 148. Types of fructifications among Fungi Imperfect!. A. P\'cnidium. B. Acervulus. C Conidiophores protruding separatelv from stoma. D. Sporodochium. E. Synnema. F. Penicillate conidiophore. G. Capitate conidiophore. nidia as readily on decaying plant organs as on living ones. Such species may be able to survive from one season to the next with- out the presence of a perfect stage. It must be remembered, however, that survival of the conidial stage throughout the ^\'in- ter in no way determines, so far as is now known, the production of the perfect stage. Many imperfect species, although placed in the same form genus, are totally unrelated, as becomes evident when their per- fect stages are taken into consideration. On the other hand, a structural parallelism between the conidial stage and ascomyce- tous stage is known to exist [Orton (1915)]. Evidence in sup- THE DEUTEROMYCETES (FUNGI IMPERFECTI) 385 port of both these apparently contradictory statements is of- fered by the imperfect form Genus Gloeosporium. Some species of the pyrenomvcetous genera Glomerella and Gnomonia have conidial stages belonging to Gloeosporium. The conidial stage of certain species of the discomycetous Pseudopeziza has also been regarded as Gloeosporium. Again, Marssonia (Marssonina) jiigland'is is the conidial stage of Gnovionia leptostyla, a pyreno- mycete, A\'hereas Marssonia rosae and M. fragariae a*re conidial stages of Diplocarpon rosae and D. earliana, respectively, both of ^^•hich are discomycetous. But life-history studies have revealed that the correlated parallelism between form of conidia and form of ascospores is a very useful feature in classification. Species of Guicrnardia, for example, have Phyllostictina as their conidial stage, species of Rhytisma have Alelasmia, species of Cordvceps have Isaria, species of Gibberella have Fusarium, species of Pleo- spora have Alternaria or Macrosporium, species of Elsinoe have Sphaceloma, species of \^enturia have Fusicladium, species of Coccomyces (Higginsia) have Cylindrosporium, and species of Sclerotinia {sensji lato) have Alonilia and Botrytis. Parallelism in form of conidia and ascospores, however, may not exist, as is shown by species of Diaporthe that possess conidial stages belong- ino^ to Phomopsis and by species of Alycosphaerella that have co- nidial stages among a variety of genera, including Phyllosticta, Ascochyta, Ramularia, Cercospora, Cercosporella, and Septoria, and by species of Nectria whose- conidial stages are classified as Tubercularia, Fusarium, or Cyhndrocarpon. Some genera, such as Balansia, Epichloe, and Dothichloe, on the other hand, possess conidial stages belonging to one and the same form genus. In these genera the conidial stages are included in Ephelis. The conidial stage and the perfect or ascigerous stage are rarely found in nature at the same season. Many species, especially those attacking annual host plants or the foliage and fruit of deciduous trees and shrubs, produce their ascigerous stage in the spring. It is apparent, therefore, that the perfect stage is less conspicuous than the conidial stage and hence is less frequently collected. These facts may account for the widely prevalent but erroneous opinion that the ascigerous stage of such fungi is of infrequent or rare occurrence. By means of pure-culture techniques it has been possible to secure evidence of o-enetic connection between the conidial stajje 386 THE DEUTEROMYCETES (FUNGI IMPERFECTI) and the ascigerous stage of a goodly number of fungi. Quite commonly cultures isolated from conidia s^ive rise to conidia in culture, and cultures isolated from ascospores also give rise to conidia. The production of ascocarps in cultures originating either from conidia or from ascospores is of very much less com- mon occurrence. The reasons for this situation are still largely unknown. The structure of the conidial fructification in culture may be quite different from that which characterizes the species when it is grown on its natural substrate. Cultures of Septoria, a pyc- nidial fungus, for example, may be hyphomycetous in that the conidia are abstricted in succession from the apex of short, lateral hyphal branches standing singly. Similarly, Cercospora in cul- ture mav form conidia by successive acrogenous delimitation of conidia from hvphal branches that stand singly, whereas in nature the conidia are abstricted acropleurogenously from fasciculate conidiophores. Classification. Several systems of classification of the Fungi Imperfecti have been proposed. The oldest one, used by Sac- cardo in Sylloge Fiingonnji, is serviceable and does not appear to have been materially improved by the several modifications pro- posed. In Saccardo's classification there are 4 orders, which may be distinguished as follows: 1. Conidia present 2 2. Conidia in globoid, cupulate, or shield-sriaped pycnidia Phomales (Sphaeropsidales, Phyllostictales) 2. Conidia not in pycnidia 3 3. Conidiophores short and aggregated at the surface of a thin parenchvmoid stroma (an acer\'ulus) Melanconiales 3. Conidiophores varvdng in length but not on an acervulus, formed singly in fascicles or on sporodochia (cushion-shaped structures) Moniliales (Hyphomycetes) 1. Conidia lacking Mycelia Sterila The Phomales comprise 4 families, separated as follows: 1. Pycnidia globoid 2 2. Pycnidia brown or black, membranaceous or carbonaceous Phomaceae (Sphaeropsidaceae) 2. Pycnidia hyaline or bright-colored, soft, fleshy, or waxy Zvthiaceae (Nectrioidaceae) 1. Pycnidia shield-shaped, sometimes radiately constructed Leptostromataceae DEVELOPMENT OF PYCNIDIA AND ACERVULI 381 1. Pycnidia discoid, cupulate, or hysteroid, sometimes opening irregu- larly Discellaceae (Excipulaceae) The Aloniliales are constituted of 4 families, distinguished as follows: 1. Hyphae, conidiophores, and conidia hyaline or cottony Moniliaceae (iMucedinaceae) 1. Hyphae, conidiophores, and conidia typically brown or dark Dematiaceae 1. Conidiophores aggregated into a cyhndric fascicle or synnema Stilbaceae 1. Conidiophores compacted, forming a globose, cushion-shaped, or cylindric structure, a sporodochium, bearing conidia at the upper surface. Tuberculariaceae The single family Alelanconiaceae of the Order Alelanconiales includes all imperfect fungi having acervular fruiting bodies, and the Alvcelia Sterila are not subdivided. Within each family further groupings are made by employing color, shape, and septation of conidia as the bases for these groupings, as follows: Amerosporeae: conidia 1-celled, spherical, ovoid, elongated, "or allantoid. Hyalosporeae: conidia hyaline. Phaeosporeae: conidia colored. Didymosporeae: conidia 2-celled. Hyalodidvmae: conidia hyaline. Phaeodidymae: conidia colored. Phragmosporeae: conidia transversely 3- or more-celled. Hyalophragmiae: conidia hyaline. Phaeophragmiae: conidia colored. Dictyosporeae: conidia divided by transverse and longitudinal septa. Hyalodictyae: conidia hyaline. Phaeodictyae: conidia colored. ' Scolecosporeae: conidia filamentous, thread-like, 1- to several-celled. Helicosporaeae: conidia coiled, 1- to several-celled. Staurosporeae: conidia radiately lobed or star-shaped, non-septate or septate. Development of pycnidia and acervuli. Few studies have been devoted primarily to the origin and development of pyc- nidia and acervuli. Incidental observations by a number of workers, how^ever, in connection with a particular species have revealed that all species conform to one or the other of two essen- tial types. These t)^pes de Bary long ago designated "meristog- enous" and "symphogenous." If the primordium of the fruiting 38S THE DEUTEROMYCETES (FUNGI IMPERFECTI) body arises by proliferation of a single hyphal cell or of a group of adjacent cells of a single hypha, the species is regarded as Fig. 149, Simple meristogenous origin of pvcnidium, A to C, in Phovia herbarimi. (Adapted from Kempton.) Svmphogenous origin of pvcnid- ium, D to F, of Endotbia parasitica. (Adapted from Anderson and Rankin.) meristogenous in origin. If the primordium of the fruiting body, on the other hand, arises from the interlacing and anastomosing of hyphal branches from several mycelial threads, which then proliferate to form a stroma, the species is regarded as sym- phogenous. The study by Mercer (1913) of pycnidial morpho- genesis in Fhouia richardiae showed that its primordia are of both types. Similarly, the pycnidia of other species, such as Septoria i DEVELOPMENT OF PYCNIDIA AND ACERVULI 389 polygononmi and Macropboina citndii, and the acervuli of Volii- tella {Colletotrichmn) circinans and Colletotrichinjj lagenarhim arise accordingr to either of these methods. Kempton (1919) studied the development of approximately a score of imperfect fungi, most of which were found to be meris- togenous. He divided the meristos^enous type into two kinds, simple and compound. In the simple type the fruiting body develops from a single hvpha, as has been indicated, and in the compound type, from two or more contiguous hyphae. He con- cluded that simple meristogenous development occurs more often amons^ Sphaeropsidales, ^\'hereas compound meristogenous and symphogenous types are more usual among xMelanconiales. TABLE 4 Type of Development of Pvcnidia and Acervuli Simple Compound Organism Meristogenous Meristogenous Symphogenous Phoma herbarum + — — Phoma destructiva + + ~ Phoma pyrina + ~ ~ Phoma cichorial + + ~ Phoma richardiae + — + Diplodia manilliana — — + Sphaeropsis malorum — + ~ Sphaeropsis citricola + + ~ Coniothyriiim pyrina '+ + — Septoria polygonorum + + + Septoria scrophulariae + + ~ Septoria helianthi + ~ ~ Sphaerella nigerristigma — — + (Septoria stage) Cicinnobolus cesatii — — + Sphaeronemella fragariae Meliola camelliae (pycnidial stage) Macrophoma citrulli Hendersonia opuntiae Endothia parasitica (pycnidial stage) Gloeosporium rufomaculans Gloeosporium musarum Colletotrichum lagenarium Pestalozzia palmar um Pestalozzia guepini Patellina fragariae Volutella jructi Volutella circinans + — — + — — + + + — + — — — + — — + — — + + + + + + — — — + + + — + — + + — + 390 THE DEUTEROMYCETES (FUNGI IMPERFECTI) An appreciation of the origin and modes of development of fruiting bodies among imperfect fungi may be gained from the compilation in Table 4, taken largely from Kempton. SPHAEROPSIDALES According to Bender (1931), this large order of the Fungi Imperfecti contains 568 genera, 359 of which are in the Sphaerop- sidaceae, 62 in the Zythiaceae, 88 in the Leptostromataceae, and 59 in the Excipulaceae. Extensive monographs of this order are not available. The treatise on Phyllosticta by Seaver (1922) is helpful, as are others that deal with special genera, such as Phomopsis, Septoria, and Cytospora. Sphaeropsidaceae. Members of Phyllosticta and Phoma are commonly parasitic on seed plants. These two genera are sepa- rated largely upon the basis of the organ attacked, Phyllosticta causing infections on the leaves and Phoma, on the stems and fruits. Distinction of species has been based principally upon the host. Phyllostictina, Macrophoma, and Dendrophoma are struc- turally quite like Phyllosticta and Phoma; all produce discrete pycnidia that arise innately. Some species of Phyllostictina are genetically connected with Guignardia, whereas certain species of Phyllosticta and Phoma have Mycosphaerella as their perfect stage. Phyllosticta solitaria, pathogenic to foliage, twigs, and fruits of apple [Guba (1925)], and Phoma lijigam, attacking the stems of cabbage [Henderson (1918)], are not known to possess a perfect stage. Coniothyrium is similar in structure to Phyllosticta and Phoma but has colored conidia. The pycnidia of Cytospora and Ceutho- spora are immersed in a stroma, and their conidia are hyahne. Ascochyta has hyaline 2-celled conidia, whereas those of Diplodia are colored and 2-celled. Diplodia zeae, producing a stem and ear rot of corn [Durrell (1923)], is wide-spread and is not known to have an ascigerous stage. Darliica fihnn, with 2-celled hyaline conidia, is of unusual interest because it is a hyperparasite on rusts. Species with hyaline, filamentous, several-septate conidia are placed in Septoria, which contains over 1000 species. Among them are such economically important ones as Septoria ly coper- SPHAEROPSIDALES 391 sici on tomato, S. apii on celery, S. avenue on oats, S. tritici and 5. nodonmi on wheat, S. secalis on rye, and 5. nibi on brambles. Weber (1923) connected 5. avenae with Leptosphaeria avenaria, and Roark (1921), 5. nibi with Mycosphaerella nibu Fig. 150. Pycnidium of Avierosporhim oecoiwviiciim, in vertical section of leaf of Vigua sinensis. Wojnoivicia gravnnis is wide-spread in Australia, northwestern Europe, and the Great Plains area of North America as a weak parasite on fall-sown cereal crops and certain other grasses [Sprague (1935)]. In Europe, Japan, and parts of the United States where snow lies deeply over grain fields and melts late in the spring, the young plants may be covered with a moldy growth. The tissues of in- jured plants contain small dark sclerotia, identified as species of Sclerotium. In reality these sclerotia are stages of Typhula, S92 THE DEUTEROMYCETES (FUNGI IMPERFECTI) notably T. graminemn, T. ho ana, and T. idahoemis [Remberg (1940)]. Zythiaceae. The most noteworthy members of this family are entomogenous, especially certain species of Aschersonia as A. aleywdis, A. goldiam, A. coffeae, and A. marginata. They at- tack scale insects and some of them have Hypocrella (among the Hvpocreales) as the perfect stage. Leptostromataceae. Flattened fruiting bodies are possessed bv the members of this family. Many are conidial stages of Hvpodermataceae and Phacidiaceae. Among the most familiar ones are species of Melasmia, certain of which have been ge- netically connected with Rhytisma. Leptothyrhnn pomi, the '^flv-speck" fungus of apples, is another well-known representa- tive. Colby (1920) created the generic name Gloeodes for this organism. Discosia, containing both saprophytic and parasitic species and having a seta at each end of the septate conidium, is also commonly encountered. ExciPULACEAE. The pvcnidia of species assigned to this family open rather widely. Such genera as Amerosporium, Ephelis, and Lecanosticta contain pathogens of economic importance. Ainero- sporhnn oeconovncinn, w'wkv dark setae around the ostiole^ forms on the foliage of cowpeas lesions that are brown at first but be- come grayish with age. It appears to be coextensive in range with its host. Species of Ephelis which have filamentous conidia constitute the conidial stages of Balansia, Epichloe, and Dothi- chloe, all of which are parasitic on grasses and have thread-like ascospores. The best-known species of Lecanosticta is ge- netically connected with Systremma acicola, \\'hich causes brown- spot needle disease of pines, especially longleaf pine. This fungus seriously menaces the growth of longleaf -pine seedlings, includ- ino- nursery-grown trees, and natural reproduction. MELANCOMALES This order consists of the single family Melanconiaceae, having 92 genera and more than 600 North American species [Bender (1931)]. Included in it are such well-known genera as Colleto- trichum, Gloeosporium, Myxosporium, Vermicularia, Melan- conium, Protocoronospora (Kabatiella), Marssonia, Coryn^um, Pestalozzia, and Cylindrosporium. MELANCONIALES S93 Diseases of many kinds of crop plants of tlie type called an- thracnoses are produced by species of Gloeosporium and Colleto- trichiim. When these funm involve woodv stems, the acervuli produced correspond to those characteristic of Myxosporium. Fig. 151. Microstrovm jiiglmidis. A. Portion of pustule showing clavate conidiophore, conidia borne on sterigmata, nuclei remaining in conidio- phore, and immature multinucleate conidiophores. B. Vertical section of pustule of Microstrovia jitglandis, occurring on hickory. Duke (1928) regards \^ermicularia and Colletotrichum as of the same generic type. Melanconium, represented by M. jiiligemnn, which causes "bird's-eye rot" of grape berries, has dark conidia. Certain species of vetch, notably Vicia satha, are widely at- tacked by a fungus first described as Protocoronospora mgri- cans, which was placed near Corticium. It seems instead to be related to the anthracnose-producing fungi [Wolf (1920)], but attendant problems of nomenclature have never been satisfac- 394 THE DEUTEROMYCETES (FUNGI IMPERFECTl) torily solved. Sampson (1928) properly employed Kabatiella caulivora for the red-clover pathogen previously designated Gloeosporhnn caulivonim. Its conidiophores and conidia and their germination and type of growth in culture are entirely like those of the so-called Protocoro7Wspora nigricans on vetch. The vetch pathogen, therefore, appears properly to belong in Kaba- tiella. The conidial stages of the black-spot fungus on roses and the leaf-scorch fungus on strawberries belong in the form Genus Alarssonia. The closely related Marssonina panattojiiana, causing "shot hole" on lettuce grown under glass, is not known, however, to possess an ascigerous stage. The twigs of peach throughout Europe and North America may be parasitized by Coryneinn beijerinckii. Acquaintance with Pestalotia (Pestalozzia), characterized by septate conidia that bear three or more hyaline setae, may be gained from the monograph by Guba (1929, 1932). Three species of Higginsia (Coccomyces), a discomycetous genus occurring on Prunus, namely, H. hiemalis^ H. pnmophorae, and H. hitescenSj have hyaline, thread-like conidia that belong in Cylindrosporium. The ascigerous stage of all other species of Cylindrosporium remains unknown. MONILIALES The Moniliales comprise 651 genera and more than 10,000 species, according to Bender (1931), and are divided into 4 famiHes. In the Moniliaceae there are 204 genera, in the Demati- aceae 206, in the Stilbaceae 89, and in the Tuberculariaceae 152. Moniliaceae. Certain members of this family, notably Asper- gillus and Penicillium, are encountered by mycologists, bac- teriologists, and plant pathologists everywhere for the reason that they are ubiquitous in distribution and essentially omnivorous in food habits. A few species of both genera are known to de- velop a perfect stage of the plectomycetous type and were for- merly placed in the Genus Eurotium. Most of them, however, are detached conidial stages. The erect conidiophore in Asper- gillus is apically enlarged, and from the surface of this enlarge- ment short bottle-shaped branches (sterigmata) arise. From each branch a chain of conidia is produced; instead the branch may MONILIALES B9S give rise first to a secondary branch. In Penicillium the erect conidiophore becomes digitately branched, the branches tending to be parallel to the main axis and to attain equal heights. Chains of conidia are borne from the apices of these ultimate branches. Aspergillus and Penicillium are of enormous importance. Peni- cillhnn glaiicinn causes decay of apples and pears in storage; P. italicuni and P. digitatiim produce decay of citrus fruits. Asper- gillus niger is used industrially in the production of certain or- ganic acids, such as citric, gallic, and gluconic. Aspergillus oryzae is employed in the preparation of Taka-diastase. Asper- gillus -fumigatus causes otomycosis, pulmonary disorders, es- pecially among workers who poHsh metals or handle furs and feathers, and pneumonic symptoms in grouse, quail, canaries, and other kinds of birds. Fenicilliiim roqueforti and P. camem- berti impart desirable flavors and odors to cheese. Members of both genera are involved in the production of mold on shoes, gloves, and other leather products, the spoilage of bread, pre- serves, and jeUies, and the mildewing of clothing, awnings, tents, and other articles made of cloth. The monographic treatises on Aspergillus by Thom and Church (1926) and on Penicillium by Thom (1930) are in- valuable in any study involving these genera. Botrytis contains numerous species and is another of the fre- quently encountered genera. The genus is characterized by much-branched conidiophores that bear clusters of spherical or ellipsoidal conidia, the entire structure having the aspect of a bunch of grapes. Members of the B. cinerea group cause the de- cay of many kinds of bulbs, fruits, and vegetables. They also parasitize young plants and blight the buds and flowers of many cultivated ornamental species. Some species of Botrytis have been genetically connected A\'ith Sclerotinia. Some hibernate by means of sclerotia. Ramularia and Cercosporella, containing many leaf-spot-pro- ducing fungi, are quite alike, as is indicated by the fact that both generic names have been frequently used for one and the same species. As the genera are at present delimited, there are two distinct t\^pes of fructifications. In one the short conidiophores emerge in fascicles from the stomata and produce the septate conidia acrogenously. Mature conidiophores have several scars near their tips, the scars marking the sites of attachment of S96 THE DEUTEROMYCETES (FUNGI IMPERFECTl) c =5 • p-1 C3 5/5 c c « .2 w TJ CI, S r:- c u o o c o u D c ^ o ^ o u o c o u c rt W2 (— — rt .2 's Q tH o Ml (/) . C/5 c CJ -u ■M a V. C o bo £ C/5 . 3 -O U SQ DEMATIACEAE S91 conidia. In the other type the reproductive hyphae form an arachnoid weft at the surface of the lesion, and the conidia are abstricted from short laterally formed conidiophores that stand singly. In the first group is Alycosphaerella vwri {Cercosporella uiaciilans), occurring on mulberry. In the second group are Ravmlaria areola on cotton and Cercosporella persicae on peach, which produce diseases commonly called frosty milde\v. The perfect stage of each has been determined to be Alycosphaerella. In Piricularia are species having simple or branched conidiophores bearing ovoid to pear-shaped, septate conidia. Piricularia oryzae is wide-spread on the foliage of rice. Piricularia grisea is com- mon on pasture and hay grasses. Dematiaceae. Cladosporium is encountered by all ^\'orkers who attempt to isolate fungi in culture. Its branched conidio- phores bear chains of acrogenously produced conidia, single- celled or two- or three-septate. The genus contains many sapro- phytic species that aid in the decomposition of all sorts of plant tissues and also several that produce disease in plants and ani- mals. Perfect stage connections are unknown. Cladosporiinii jiihinn blights the foliage of greenhouse-grown tomatoes. Peach scab, caused by C. carpophihnn, involves both the fruit and twigs [Keitt (1917)] and is especially destructive to late-maturing va- rieties. It hibernates in twig lesions. Cladosporiinn ciicwuerimnn causes scab on the fruit of cucumber. Several other important plant pathogens have been placed in Cladosporium, for example, C. citri^ but they properly belong in Sphaceloma, which has been established to be genetically connected with Elsinoe, a hemi- sphaeriaceous fungus. Chromoblastomycosis in man is caused by an extremely pleo- morphic species, for which a number of generic names, including Hormodendrum, Phialophora, Acrotheca, and Fonsecaea, have been proposed, but it may well be eventually placed in Clado- sporium. Serious diseases of cereal crops and wild grasses, called stripe diseases because of the shape of the lesions, are induced by Hel- minthosporium. This genus includes fungi ^\•ith stout, un- branched, septate conidiophores, and with colored, septate, thick- walled, boat-shaped conidia. A few species, such as H. ravenelii, completely envelope the inflorescences and are of such wide- spread occurrence that the hosts are called smut grass. 398 THE DEUTEROMYCETES (FUNGI IMPERFECTI) The closely related Genus Heterosporium was recently studied by Jacques (1941). The well-known H. iridis on Iris is geneti- cally connected with DidyuieU'ma macrospora. Jacques secured the perithecial stage in culture on sterile iris leaves. He found that H. omithogali is the conidial stage of Didyntellina orni- thogali. The developmental cycle of other important pathogens, including H. phlei on Fhleinn pratense, H. echimdatum on Dian- thiis caryophylhis, and H. variable on Spinacea oleracea, should be ^iven consideration. The two genera Alternaria and Alacrosporium, which are re- garded as synonymous by some and which are at least closely related to each other, have bottle-shaped conidia that are both transversely and longitudinally septate. The basal end is the larger. The conidiophores are stout, short, lateral hyphal branches. In Alacrosporium the conidia are produced singly; in Alternaria they form chains, the basal conidium being the old- est. The features possessed by these genera that are of taxonomic value are given consideration by Elliott (1917). A few species of Alternaria have been demonstrated to have Pleospora as their perfect stage. Among the better-known species parasitic on plants are Alternaria solani, causing early blight of potatoes, A. tenuis and A. longipes, pathogenic to to- bacco, A. citri, occurring on citrus, A. paiwx, found on ginseng, and A. brassicae var. nigrescens, which seriously blights the fo- liage of cantaloupes. Cercospora is undoubtedly the largest genus of the Dema- tiaceae, and its species are very destructive to cultivated plants. One or more species of Cercospora have been recorded as para- sites on practically every crop species and on many kinds of wild plants as well. The studies by Lieneman (1929) and Solheim (1929) give especial attention to taxonomic problems involving this genus. Its conidiophores are typically fasciculate and emerge from the stomata. The upper portions are covered with numer- ous scars left after the falling of the slender, clavate, septate co- nidia. Several species of Cercospora, such as C personata on peanuts, C. bolleana on figs, C. viiisae on banana, and C. lythra- ceannn on pomegranates, have been demonstrated to be imper- fect stages of Mycosphaerella. Cercospora beticola, especially destructive to sugar beets, and C. nicotianae, producing frog-eye DEMATIACEAE 399 400 THE DEUTEROMYCETES (FUNGI IMPERFECTI) spot of tobacco, are among the species of economic importance not kno\\'n to possess a perfect stage. There are approximately 12 genera and 75 species of fungi having peciiHar hehcal conidia. Some are entirely or partly hya- line, and the others have yellow, brown, or dark fructifications. This group has been monographed by Linder (1929). Many of them occur on decaying wood and bark, imparting to it an effuse, dark coating. Helicoma, Helicosporium, and Xenosporella are among the most common representatives. Helicoma ciirtisli is related to Lasiosphaeria pezizida, but connection with perfect stages has not been definitely established in any others of this group. Stilbaceae. The fungi that comprise the Stilbaceae are little known even to the experienced mycologist. Possibly the most familiar genera are Isaria and Graphium. Isaria is entomogenous. It is constituted of species having hyaline synnemata with hya- line, one-celled conidia that form over most of the surface of the synnema. Some species have Cordyceps as their perfect stage, whereas the perfect stage of others has not been observed. Isaria jarinosa w^as long regarded as the conidial stage of Cordyceps militaris. Fetch (1936), however, found that the two are not connected, Cephalosporium being the conidial stage of C. mili- taris. Graphium has dark-colored synnemata with dark, one-celled conidia formed apically. This genus is best known through G. iilmi, the cause of Graphium disease of elms (so-called Dutch elm disease). This fungus has Ceratostomella idmi as its perfect stage. A number of other species are associated with other species of Ceratostemella, which cause "blue stain" of logs and lumber. TuBERCULARiACEAE. In this family the Genus Fusarium is of outstanding interest. Its members are known to mycologists and plant pathologists the world over, because they cause destructive blights, wilts, and root rots of cereals, fiber plants, truck crops, ornamentals, and woody plants. Its species are extremely diffi- cult to identify, and consequently taxonomic problems have been given a generous share of attention. These matters are ex- tensively considered in the treatise by Reinking and WoUenweber (1935). A somewhat different point of view is maintained by Snyder and Hansen (1940, 1941). They studied the progeny of MVCELIA STERILA 401 cultures isolated from single spores of manv so-called species of the Sections Elegans and Alartiella. As a result they place 10 species, 18 varieties, and 12 forms belonging, according to Rein- king and WoUenweber, to Elegans in one species, Fzisarhnn oxy- sponnn. From Alartiella 5 parasites were placed as forms in F. solani, and 2 species, 3 varieties, and 1 form \\ere placed in Hypo- myces solani, a perithecial fungus. Gibber elk saiibmettii consti- tutes the perithecial stage of F. gramiiieiim, which causes scab on heads of barley, wheat, and other grains. AIYCELIA STERILA A score of genera and approximately 400 species have at one time or another been included in this non-sporiferous group. Some of them were removed from the group as their fertile stages were discovered. Many of them form sclerotia, which are com- pact structures of definite form, usually light-colored internally but having a dark, hard rind. In Sclerotium is included S. roljsii, which is especially destruc- tive to a wide variety of wild and cultivated species in the south- eastern United States. It attacks stems near the soil level. Its basidial stage is Corticium (Hypochnus). Sclerotium oryzae on rice and 5. delphinii on larkspur produce similar types of disease. Sclerotiinn bataticola occurs in warm res^ions the \\-orld over, attacking^ the roots of a wide variety of cultivated and wild species. Its sclerotia, which are 15 to 30 1.1 in diameter, form in abundance within the woody tissues. This organism possesses a conidial stage, designated Macrophoviina phaseoU by Ashby (1927). The wide-spread Rhizoctonia solani causes damping-off of seedlings and stem rot of more mature plants. It has Corticiimi vagiim as its perfect stage but appears as an arachnoid ^^•eft on the basal portion of diseased stems or over the soil surface. This fungus has characteristic coarse, septate hyphae whose lateral branches are constricted at their point of origin; a septum occurs just beyond the constriction in each lateral. Its brown sclerotia form in abundance on potato tubers. The Rhizoctonia stage and the sclerotial stage of Corticiinn koleroga, causing thread blights of many species of trees. 402 THE DEUTEROMYCETES (FUNGI IMPERFECTI) especially in tropical and subtropical regions, are of equal interest. Wolf and Bach (1927) regard this species as identical with C. stevensii on the basis of similarities in morphologic and cultural characteristics and on ability to produce reciprocal in- fections. Others, including Matsumoto and Yamamoto (1935), maintain that there are two separate species, mainly because of differences in sclerotial production. It does not seem reasonable, however, in view of the fact that sclerotia form sparsely on smooth surfaces and abundantly on rough surfaces, as on the fruit of Stavman apples and russet apples, respectively, and that strain differences \\ithin many single species of fungi are known, to regard C. koleroga and C. stevensii as distinct. Ozonium possesses loose, bright yellowish masses of mycelium that may unite into strands. Its best-known species is O. omniv- onim, commonly called the Texas root-rot fungus; its known host range includes approximately 500 species of herbaceous and woody plants, the most important of which is cotton. Sclerotia form in abundance in the soil. Sometimes a conidial stage, known as Fhymatotrichimi ommvoriim, is produced in large buff-colored patches over the soil surface in areas where cotton has been killed by this root-rot fungus. Pachvma includes fungi having enormous subterranean scle- rotia that have been used for food. Several have been connected with polypores. F achy ma cocos, having sclerotia that may weigh more than 20 lb, but more commonly weis^h 1 to 8 lb, was shown bv Wolf (1922) and Weber (1929) to be the sclerotial stage of Foria cocos. Tai and Wei (1933) reported the occurrence of this species in China, where it is known as fuhling or Chinese root and is used medicinally. It is cultivated on buried pine poles, the annual crop being more^than 1000 tons. Related spe- cies include "black-fellow's bread," Folyporus my lift ae of Aus- tralia, F. sapiirejna of southern Brazil, whose sclerotia may attain a weight of 40 lb, P. tiiberaster of Italy, and the more recently described P. tiickahoe of Canada [Giissow (1919)]. In summary, the Fungi Imperfecti are of unusual interest to the student of problems involving pleomorphism and complicated developmental cycles. Even after several hundred more years of study by many mycologists it is probable that not all these prob- lems will have been solved. LITERATURE CITED 403 LITERATURE CITED AsHBY, S. F., Macrophoviina pbaseoli (Alaubl.) comb, nov., the pycnidial stage of Rhizoctonia bataticola (Taub.) Butler," Tram. Brit. Mycol. Soc, 12: 141-147, 1927. Bender, H. B., The genera of Fungi Imperfecti: North A?7ierican species and hosts, with particular reference to Connecticut. Thesis, Yale Uni- versity. 2000 pp. 1931. (Unpublished.) The Fungi Imperfecti: Order Sphaeropsidales. With keys and references for gejiera. SI pp. 1934. Colby, A. S., "Sooty blotch of pomaceous fruits," ///. St a. Acad. Sci. Trans., 13: 139-174, 1920. Duke, Maud M., "The genera Vermicularia Fr. and CoUetotrichium Cda.," Trajis. Brit. Mycol. Soc, 13: 156-184, 1928. DuRRELL, L. W., "Dry rot of corn," Iowa Agr. Expt. Sta. Research Bull., 77:346-376, 1923. Elliott, J. A., "Taxonomic characters of the genera Alternaria and Macro- sporium," A7n. J. Botany, 4: 439-476, 1917. Grove, W. B., British stem and leaf fujigi {Coeloviycetes). A contribution to our knowledge of the Fungi hnperfecti belonging to the Sphaerop- sidales and the Melanconiales, Vol. I. xx + 488 pp. Cambridge Uni- versity Press, 1934. Vol. II. ix + 406 pp. Cambridge University Press, 1937. GuBA, E. F., "Phyllosticta leaf spot, fruit blotch, and canker of the apple; its etiology and control." ///. Agr. Expt. Sta. Bull, 21(^:481-551, 1925. "Monograph of the genus Pestalotia de Notaris. Pt. I," Phytopathology, iP: 191-232, 1929; Pt. II, Mycol, 2^:355-397, 1932. Gussow, H. T., "The Canadian tuckahoe," Mycol, ii: 104^110, 1919. Henderson, M. P., "The black-leg disease of cabbage caused by Fhoma lingain (Tode) Desm.," Phytopathology, 5-: 379-431, 1918. Jacques, J. E., "Studies in the genus Heterosporium," Contrb. Inst. Botan. Univ. Montreal, 39:7^6, 1941. Keitt, G. W., "Peach scab and its control," U. S. Dept. Agr. Bidl, 395: 1- 66, 1917. Kempton, F. E., "Origin and development of the pycnidium," Botan. Gaz., <^.!?: 233-254, 1919. LiENEMAN, Catherine, "A host index to the North American species of the genus Cercospora," Ann. Mo. Botan. Garden, 16: 1-52, 1929. Linder, D. H., "A monograph of the hehcosporous Fungi Imperfecti," Ann. Mo. Botan. Garden, 16: 227-388, 1929. Matsumoto, T., and W. Yamamoto, ''Hypochnus sasakii Shirai in com- parison with Corticiuni stevensii Burt and Corticiimi koleroga (Cooke) von Hohn.," Trans. Nat. Hist. Soc. Formosa, 25: 161-175, 1935. Mercer, W. B., "On the morphology and development of Fhoma richardiae, n. sp.," Mycolog. Centr., 2:244-253, 1913. Orton, C. R., "Structural parallelism between spore forms in the Ascomy- cetes," Mycol, 7:21-27, 1915. 404 THE DEUTEROMYCETES (FUNGI IMPERFECTI) Fetch, T., ^^Cordyceps viilitaris and Isaria farinosa,''^ Trails. Brit. Mycol. Soc, 20; 216-224, 1936. Reinking, O. a., and H. W. Wollenweber, Die Fiisarien, ibre Beschreib- u?jg, Schadtvirhnig, imd Bekmnpfimg. viii + 355 pp. P. Parey, Ber- lin. 1935. Remberg, Ruth E., "The snow molds of grains and grasses caused by Typbula itoaua and Typbida idaboefisis,'' Pbytopatbology, 30: 178-180, 1940. RoARK, E. W., "The Septoria leaf spot of Rubus," Pbytopatbology, 11: 327-333, 1921. Sampson, Kathleen, "Comparative studies of Kabatiella caidivora (Kirchn.) Karak. and Colletotricbiim trifolii Bain and Essarv, two fungi which cause red-cl,over anthracnose," Trans. Brit. Mycol. Soc, 13: 103-142, 1928. Seaver, F. J., "Phyllostictales," Nortb Avi. Flora, 6: 1-84, 1922. Snyder, A\\ C, and H. N. Hansen, "The species concept in Fusarium," Avi. J. Botany, 21: 64-67, 1940. "The species concept in Fusarium, with reference to section Martiella," Am. J. Bota?jy, 28: 738-742, 1941. SoLHEiM, W. G., "Morphological studies of the genus Cercospora," ///. Biol. Monog., 12: 1-84, 1929. Sprague, R., '"''Wopioivicia graviinis as a very weak, secondary parasite of winter cereal crops," Pbytopatbology, 25:405-419, 1935. Tai, F. L., and C. T. Wei, "Notes on Chinese fungi. III." Sinejisia, CoTitr. Metrop. Mzis. Nat. Hist. Acad. Siiiica, 4:83-128, 1933. Thom, Charles, Tbe Penicillia. xiii + 644 pp. Williams and Wilkins Co., Baltimore. 1930. Thom, Charles, and AI. B. Church, Tbe Aspergilli. xi + 272 pp. Wil- liams and Wilkins Co., Baltimore. 1926. Weber, G. F., "Septoria diseases of cereals," Pbytopatbology, 72:448-470, 537-585, 1922; 13: 1-23, 1923. "The occurrence of tuckahoes and Poria cocos in Florida," Mycol., 21: 113-130, 1929. Wolf, F. A., "A little-known vetch disease," /. Elisba Mitcbell Sci. Soc, 55:72-85, 1920. "The fruiting stage of the tuckahoe, Pacbyvia cocos,'' J. Elisba Mitchell Sci. Soc, 38: 127-137, 1922. "The relationship of Microstroma jnglandis (Bereng.) Sacc," /. Elisba Mitcbell Sci. Soc, 45: 130-136, 1929. W^olf, F. a., and W. J. Bach, "The thread-bhght disease caused by Cor- ticiinn koleroga (Cooke) von Hohn., on citrus and pomaceous plants," Pbytopatbology, 77:689-710, 1927. AUTHOR INDEX Ahrens, W. E., 205, 230 Ainsworth, G. C, 32, 39 Allen, R. F., 318, 338 Ames, Adeline, 347, 361 Ames, L. AI., 11, 200, 230 Anderson, A. P., 307, 308 Anderson, P. J., 226, 230 Andrus, C F., 205, 230, 317, 318, 338 Arens, K., 109, 111, 112, 115 Arnaud, G., 237, 241 Arthur, J. C, 312, 314, 315, 327, 328, 330, 333, 335, 338 Ashby, S. F., 401, 403 Ashworth, Dorothy, 326, 338 Atanasoff, D., 191,^193, 195, 197 Atkinson, G. F., 6* 62, 139, 191, 197, 257, 266, 354, 358, 360, 361, 378, 379 Ayers, T. E., 259, 266 Ayers, T. T., 126, 127 Bach, W. J, 20, 27, 402, 404 Bache-Wiig, Sara, 259, 266 Backus, M. P., 202, 230, 253, 266 Badcock, E. C, 23, 27 Ballard, W. S., 173, 178 Bambeke, C van, 368, 369 Banker, H. J., 346, 361 Barber, M. A., 17, 18, 27 Barbour, W. J., 184, 186 Barclay, A., 321, 338 Barger, G., 191, 195, 196, 197 Barnes, B., 85, 87 Barnett, H. L., 288, 291 Barrett, J. T., 69, 72 Bary, Anton de, 8, 9, 10, 12, 40, 41, 47, 53, 97, 102, 107, 139, 154, 162, 169, 173, 301, 328, 329, 338, 387 Bauch, R., 279, 283, 303, 304, 308 Bauhin, Gaspard, 4, 12 Baxter, D. V., 347, 349, 361 Beardslee, H. C, 360, 361, 362 Beers, Alma H., 352, 362 Behrens, A., 91 Bender, H. B., 383, 390, 392, 394, 403 Bensaude, AL, 11, 281, 283 Berdan, Helen B., 19, 27, 74, 76 Berkeley, AI. J., 8, 12, 133 Berlese,' A. N., 114, 115 Bessey, C. E., 62 Bcrzelius, J. J., 2 Bisby, G. R., 32, 39, 52, 53, 243, 245 Bishop, H, 89, 91 Bitancourt, A. A., 167, 171 Blackman, V. H, 190, 197, 332, 333, 338 Blackwell, E., 78, 82 Blain, W. L., 184, 186 Blakeslee, A. F., 11, 121, 122, 124, 127, 128 Bliss, D. E., 109, 115 Blodgett, F. M., 176, 178 Blomfield, J. E., 45, 53 Bodman, M. C, 286 Boedijn, K. B., 292, 298, 377, 379 Boyce, J. S., 178, 179 Boyle, J. S., 346, 363 Breda de Haan, J. van, 104 Brefeld, Oscar, 8, 12, 140, 145, 149, 157, 162, 301, 302, 308 Bresadola, J., 7, 12 Brierley, W. B., 160, 162 Brodie,' H. J., 282, 283, 284 Brooks, F. T., 220, 221, 230 Brown, A. AL, 318, 339 Brown, H. B., 230, 288 Brown, AV., 17, 18, 28 Bucholtz, F., 133, 134, 274, 275 Buddin, AV., 292, 298 Buhr, H., 279, 284 Buisman, Christine, 205, 230 Buller, A. H. R., 11, 127, 282, 283, 284, 286, 294, 298, 302, 318, 339, 360, 361 Bulliard, P., 5, 9, 12 Burgeff, H., 122, 127 Burk, Alyrle, 45, 55 Burkholder, AA^ H., 167, 171 Burlingham, G. S., 360, 361 * An italic 7mmeral indicates that the page contains an illustration. 405 406 AUTHOR INDEX Burt, E. A., 343, 344, 347, 348, 361, 362, 377, 378, 379 Butier, E. J., 78, 82, 100, 104, 189, 197 Butler, J. B., 64, 72 Callen, E. O., 122, 127 Camp, W. G., 46, 50, 53 Candolle, A. de, 328 Cardiff, I. D., 307, 308 Cavley, Dorothy, 188, 197 Chambers, H. S., 154, 162 Child, Marion, 228, 230 Chivers, A. H., 200, 230 Christiansen, J. J., 303, 304, 309 Christman, A. H., 333, 339 Chrzaszcz, T., 11 Chupp, Charles, 44, 53 Church, M. B., 155, 162, 395, 404 Cienkowski, L., 41, 43, 53, 54 Claussen, P., 97, 270, 271 Clements, F. E., 34, 39 Clinton, G. P., 24, 28, 102, 104, 109, 115, 205, 230, 305, 308 Cohen, A. L., 42, 54 Coker, W. C, 87, 92, 94, 97, 290, 291, 293, 298, 346, 352, 360, 362, 366, 367, 368, 369, 377, 379 Colbv, A. S., 392, 403 Colley, R. H., 313, 339 Colson, Barbara, 175, 179, 202, 230, 279, 284, 362 Conard, H. S., 370, 372, 378, 379 Cook, H. T., 109, 115 Cook, W. R. I., 44, 45, 54, 75, 76, 92, 97 Cooke, M. C, 7, 12 Cooper, G. O., 97 Cooper, J. R., 228, 230 Corda, A. C. I., 6, 12, 328 Corner, E. J. H., 248, 250, 270, 271 Comu, M., 83, 87, 317 Cotter, R. U., 334, 340 Cotton, A. D., 346, 362 Couch, J. N., 19, 28, 61, 62, 64, 66, 69, 73, 75, 77, 95, 97, 295, 297, 298, 366, 367, 368, 369, 377, 379 Cox, H. T., 66, 73 Craigie, J. H., 11, 317, 318, 332, 339 Cunningham, G. H., 335, 339, 367, 370, 372, 376, 377, 379, 380, 381 Currie, AI. E., 50, 54 Curtis, K. M., 66, 68, 73 Cutter, V. AL, 123, 128 Dale, E., 153, 154, 162 Dangeard, P. A., 43, 54, 76, 77, 153, 154, 162, 270, 271, 274, 275, 285, 286, 287, 288, 291, 301 Darker, G. D., 243, 245 Darkis, F. R., 109, 115, 116 Davidson, R. W., 212, 232 Diehl, H., 69, 73 Diehl, W. W, 191, 197, 381 Dietel, P., 330, 331, 339 Dixon, L. F., 109, 112, 115 Dobbs, C. G., 116, 128 Dodge, B. O., 11, 52, 54, 139, 157, 162, 202, 230, 270, 272, 298, 299, 326, 339, 381, 382 Dodge, C. W., 139, 143, 145, 161, 162, 366, 367, 368, 369 Doidge, Ethel Al., 178, 179, 237, 241 Douglas, G. E., 354, 362 Dowding, E. S., 270, 272 Drayton, F. D., 11, 261, 262, 266 Drechsler, C, 72, 73, 94, 97, 171 Duboscq, O., 134, 136 Duke, Alaud Al., 393, 403 Dunegan, J. C, 261, 267 Dunn, AI. S., 17, 18, 28 Durand, E. J., 266, 268 Durrell, L. W., 390, 403 Edgerton, C. W., 17, 18, 28, 220, 222, 230, 231 Edson, H. A., 101, 104 Eftimiu, Panca, 175, 179, 280, 284, 341, 362 Ehrlich, John, 187, 188, 197, 212, 231 Eidam, E., 143 Elliott, J. A., 205, 231, 398, 403 Emerson, Ralph, 78, 81, 82 Emmons, C. W., 160, 162 Engler, A., 7, 12, 133, 198, 259 Eriksson, J., 11, 333, 334, 335, 339 Etter, Bessie E., 23, 28 Ezekiel, W. N., 17, 18, 28 Falck, K., 193, 197 Farlow, W. G., 8, 180, 182, 186 Faull, J. H., 235, 236, 335, 339 Fenner, E. Aline, 120, 128 Fischer, E., 330, 366, 367, 368, 369, 372, 373, 374, 377, 379 AUTHOR INDEX 401 Fitzpatrick, H. AL, 87, 88, 207, 231, 294, 298, 368, 369 Fitzpatrick, R. E., 149, 150 Fleming, Alexander, 11 Fontana, Felice, 7, 12 Fox, D. L., 78, 82 Frank, B., 10 Fraser, H. C I., 154, 162, 333, 338 Fraser, Lillian, 178, 179 Fries, Elias, 5, 12, 30, 31, 32, 39, 40, 46, 133, 328 Fries, R. E., 381, 382 Fromme, F. D., 228, 231, 319, 339 Gaiser, L. O., 326, 339 Gaumann. E., 114, 115, 294, 298, 343, 362, 372 Gibson, W. H., 360, 362 Giddings, N. J., 102, 105 Giesenhaoren, K., 149, 150 Gilbert, E. M., 285, 286, 287 Gilbert, F. A., 48, 50, 54 Gilbert, H. C, 48, 54 Gilbert, W. W., 160, 162 Gilkev, Helen AL, 274, 275 Godfrey, G. H., 262, 266 Goldstein, Bessie, 129, 130, 132 Graff, P. W., 177, 179 Greororv, C T., 112, 115 Griffiths, D., 203, 231 Griggs, R. F., 74 Gro^ss, P. AL, 115, 116 Grove, W. B., 330, 335, 339, 403 Groves, J. W., 261, 266 Guba, E. F., 390, 394, 403 Guilliermond, A., 141, 144, 146 Gussow, H. T., 360, 362, 402, 403 Gwynne-Vaughan, H. C. L, 270, 272 Haack, G., 244, 245 Hahn, G. G., 259, 266 Haltern, F. H. van, 109, 115 Hanna, W. F., 17, 18, 28, 281, 284, 303, 304, 308 Hansbrough, J. R., 257, 266 Hansen, E. K., 9, 144, 145 Hansen, H. N., 400, 404 Harder, R., 81, 82 Harper, R. A., 10, 11, 52, 54, 118, 128, 175, 179, 270, 272, 303, 308 Harsch, R. AL, 23, 28 Harter, L. L., 205, 225, 226, 230, 231 Hartig, Robert, 8, 12 Harvey, J. V., 92, 97, 98 Hftch, W. R., 78, 81, 82 Heald, F. D., 207, 231, 307, 308 Hedgcock, G. G., 321, 339, 340 Hein, lUo, 354, 362 Henderson, Al. P., 390, 403 Hennings, E., 335, 339, 348 Henrici, A. T., 144, 146 Hesler, L. R., 217, 219, 231 Higgins, B. B., 211, 212, 231, 253, 267 Hildebrand, E. AL, 17, 28 Hines, Lee, 334, 340 Hiura, M., 23, 24, 28, 112, 115 Hodgson, R. W., 155, 162 Hohnel, F. von, 243, 245 Hohnk, W., 95, 97, 98 Hollos, G., 366, 367 Holton, C. S., 303, 307, 308 Honey, E. E., 260, 261, 267 Hooke, Robert, 4, 12 Horl, S., 300, 308 Howard, F. L., 49, 50, 54 Humphrey, C. J., 347, 349, 363 Humphries, A., 64, 72 Indoh, H., 81, 82, 88, 91 Istvanffi, G., 286, 287 Ivanoff, S. S., 105, 108 Iwanoff, N. N., 11 Jackson, H. S., 294, 298, 330, 331, 340, 341 Jacques, J. E., 398, 403 Jaczewski, A. de, 186 Jahn, E., 47, 48, 53, 54 Janssen, Zacharias, 2 Jeffers, W. F., 207, 231 Jenkins, A. E., 167, 171 Jenkins, W. A., 191, 197, 211, 212, 231 Jolivette-Sax, H. D. AL, 201, 231 Jones, F. R., 72, 73, 251, 257, 267 Jones, L. R., 102, 105 Jones, S. G., 219, 231, 244, 245, 257, 267 Juel, H. O., 142, 143, 146, 148, 150, 286, 287, 288, 291, 297, 299 Kamei, S., 335, 340 Kanouse, B. B., 78, 82, 88, 89, 91 Karling, J. S., 44, 45, 54, 66, 69, 73 Karsten, G., 314 Kasanowsky, V., 97, 98 408 AUTHOR INDEX Kauffman, C. H., 360, 363 Keene, Mary L., 122, 128 Keitt, G. W., 17, 18, 28, 397, 403 Kempton, F. E., 389, 390, 403 Kendrick, J. B., 94, 98 Kern, F. D., 321, 335, 336, 340 Kevorkian, A. G., 89, 91, 131, 132 Kharbush, S., 280, 284, 341, 362 Killian, C, 182, 186, 192, 197, 215, 231, 237, 241, 305, 308 King, C, 91 Kirby, R. S., 219, 231 Kirchhoff, H., 192, 197 Klebahn, H., 149, 150, 209, 211, 220, 222, 231, 237, 241, 255, 267, 313, 314, 330, 331, 334, 335, 340 Kniep, H., 11, 78, 82, 281, 284, 303, 304, 308 Koch, L. W., 180, 182, 186 Krieger, L. C. C, 360, 363 Kriiger, F., Ill, 112, 115 Kiihn, Julius, 8, 12 Kiihner, R., 288, 291, 352, 363 Kunkel, L. O., 45, 55, 326, 340 Kusano, S., 66, 67, 73 Lafar, Franz, 9, 12 Lagerheim, G. de, 83, 88, 290, 291, 292, 299 Laibach, F., 85, 88 Lander, Caroline A., 374, 376 Lange, J. E., 360, 363 LaRue, C. D., 17, 18, 28 Latham, D. H., 212, 232 Ledingham, G. A., 44, 55, 76, 77 Leeuwenhoek, Anthony van, 2, 144 Leger, L., 134, 136 Lehman, S. G., 226, 232 Leidy, Joseph, 134, 136 Lendner, A., 124, 128 Leus, S., 347, 363 Levine, M., 280, 284 Levine, M. N., 334, 340 Lewis, C. E., 143, 146 Lewis, L M., 201, 232 Liebig, Justus von, 2 Lieneman, Catherine, 398, 403 Lindau, G., 161, 180, 198, 208, 243, 245 Lindegren, C, 11 Linder, D. H., 293, 299, 400, 403 Lindgren, R. M., 207, 232 Linnaeus, Carl, 5, 12, 30, 32, 39 Lister, A., 41, 53, 55 Lloyd, C. G., 367, 374, 376, 377, 379, 380, 382 Lohman, M. L., 245 Lohwag, H., 370, 372, 377, 379 Long, W. H., 23, 28, 335, 340, 380, 382 Lowe, J. L., 347, 363 Lutman, B. F., 44, 45, 55, 102, 105, 299, 300, 303, 308 Luttrell, E. S., 239, 241 Macbride, T. H., 41, 53, 55 MacMurran, S. M., 155, 162 Magnus, P., 331 Mains, E. B., 331, 341 Maire, R., 44, 45, 55, 286, 287 Martin, Ella M., 148, 149, 150 Martin, G. W., 33, 34, 39, 41, 53, 55, 198, 232, 290, 291, 380, 381, 382 Massee, George, 7, 12, 41, 55, 191, 197, 272, 275, 366, 367, 370, 372, 373, 374 Matsumoto, T., 402, 403 Matthews, Velma D., 81, 82, 87, 92, 94, 97, 100, 105 McAlpine, D., 305, 308, 324, 335, 340 McCormick, F. A., 24, 28, 160, 162, 205, 230 McCranie, James, 81, 82 McDonough, E. S., Ill, 115 McLarty, D. A., 66, 69, 73 McLean, Ruth M., 60, 62, 109, 112, 115, 116 Melhus, L E., 107, 108, 109, 115 Melville, R., 85, 87 Mercer, W. B., 388, 403 Micheli, P. A., 4, 12, 40 Middleton, J. T., 100, 105 Miles, L. E., 220, 221, 232 Millardet, P. A., 114, 115 Miller, J. H., 163, 165, 171 Miller, J. K., 346, 363 Miller, L. W., 351, 363 Minden, M. von, 64, 73, 75, 77 Mix, A. J., 148, 149, 150 Miyake, K., 100, 105 Moller, A., 289, 290, 291, 294, 298, 299 MoUiard, M., 380, 382 Moreau, F., 118, 119, 128, 326, 340 Moreau, Mme. F., 340 Morgan, Enid, 92, 97 AUTHOR INDEX 409 Moss, E. H., 323, 340, 354, 363 Alounce, Irene, 281, 284 Murrell, W. A., 347, 348, 352, 360, 363 Nannfeldt, J. A., 246, 250, 251, 253, 257, 259, 260, 267, 268 Nannizzi, A., 152, 162 Nawaschin, S., 262, 267, 307, 308 Neuhoff, W., 287, 288, 291, 293, 299 Newton, Dorothy E., 281, 282, 284 NienbursT, W., 190, 197 Nobles, Mildred K., 283, 284 Odell, W. S., 360, 362 Olive, E. W., 42, 5S, 129, 132, 330, 331, 333, 340 Orton, C. R., 138, 139, 182, 184, 186, 330, 340, 384, 403 Osborn, T. G. B., 45, 55 Oudemans, C. A. J. A., 7, 12 Overholts, L. O., 345, 347, 360, 363 Owens, C. E., 188, 198 Padv, S. M., 313, 340 Palm, B. T., 45, 55, 107, 108 Parks, H. E., 272, 275 Pasteur, Louis, 2, 7, 144 Patouillard, N., 7, 13, 290, 291, 370, 372 Patterson, P. M., 97, 98 Percival, J., 68, 73 Persoon, C. H, 5, 13, 30, 31, 32, 39, 272, 328 Petch, T., 377, 380, 400, 404 Petersen, H. E., 104, 105 Piemeisel, R. L., 361, 364 Pierce, N. B., 148, 149, 150 Pierson, R. K, 317, 318, 340 Pinckard, J. A., 115, 116 Pinov, Ernest, 42, 55 Poirault, G., 332, 340 Poisson, R., 134, 136 Pomerleau, R., 220, 221, 232 Prantl, K., 7, 12, 133, 198, 259 Prevost, B., 7, 13, 299, 300, 308 Quelet, Lucien, 7, 13 Rabenhorst, L., 7, 13 Rabinowitsch, L., 372, 374 Raciborski, M., 332, 340 Raistrick, H., 11 Rankin, W. H., 226, 230 Raper, J. R., 17, 28, 95, 98 Raper, K. B., 41, 42, 43, 55, 155, 162 Rawitscher, F., 303, 304, 305, 308 Rawlins, T. E., 22, 28 Rea, Carleton, 360, 363 Reddick, D., 215, 232 Redi, F., 2 Reed, G. M., 176, 179 Rees, Olive M., 129, 130, 133 Rehsteiner, H., 374, 377 Reinking, O. A., 400, 401, 404 Remsberg, Ruth E., 392, 404 Renn, C. E., 43, SS Rice, Mabel A., 313, 340 Riker, A. J., 22, 28 Riker, R. S., 22, 28 Roark, E. W., 391, 404 Roberts, J. W., 261, 267 Robin, C, 134 Rodenheiser, H. A., 303, 308 Rogers, D. P., 290, 291 Rolfs, F. M., 226, 232 Rostafinski, J. T., 41, 55 Ryan, Ruth W., 237, 241 Sabouraud, R., 11 Saccardo, P. A., 7, 13, 32, 34, 39, 134, 171, 237, 259, 386 Sachs, Julius, 139, 380, 382 Sadebeck, R., 148, 149, 150 Salmon, E. S., 171, 173, 175, 176, 179 Sampson, Kathleen, 394, 404 Sappin-Trouffv, P., 326, 332, 340 Sartoris, G. B.', 299, 308 Satina, Sophia, 124, 128 Sawyer, W. H., 129, 132, 133, 354, 363 Schade, A. L., 89, 91 Scheffer, T. C, 207, 232 Schenk, A., 75, 77 Scherffel, A., 64, 73, 76, 77 Schilberszky, K., 67, 73 Schneider, A., 145, 146 Schrader, E., 97, 98 Schrenck, H. von, 220, 222, 232 Schroeter, J., 64, 73, 75, 77, 133, 259, 260 Schwartz, E. J., 44, 45, 54, 55 Schwartz, E. T., 45, 53 Schwarze, C. A., 118, 128 410 AUTHOR INDEX Schweinitz, L. D. de, 5, 13 Schweitzer, G., 270, 271, 272 Seal, J. L., 104, 105 Seaver, F. J., 186, 197, 203, 232, 246, 250, 268, 272, 390, 404 Seeler, E. V., Jr., 188, 189, 197 Setchell, W. A., 305, 308 Seymour, A. B., 7, 13 Shanor, L., 85, 88, 97, 98, 191, 198 Shantz, H. L., 361, 364 Shear, C. L., 34, 39, 220, 222, 226, 232, 298, 299 Shope, P. F., 347, 364 Shunk, I. v., 22, 28 Sibasaki, Y., 105, 108 Singers, P. v., 182 Skupienski, F. X., 42, 48, 50, 55 Sleumer, H. O., 303, 308 Smart, R. F., 48, 55 Smith, A. H., 279, 280, 284 Smith, C. O., 212, 232 Smith, D. J., 212, 232 Smith, E. C, 48, 56 Smith, Elizabeth H., 104, 105 Smith, Grant, 173, 179 Smith, R. E., 104, 105 Smith, Worthington G., 102, 105 Snell, W. H., 352, 364 Snvder, W. C, 400, 404 Soiheim, W. G., 398, 404 Sommerstorff, H., 101, 105 Sorgel, Georg, 81, 82 Spallanzani, L., 2 Sparrow, F. K., Jr., 61, 62, 64, 69, 72, 73, 76, 77, 83, 85, 87, 88 Spaulding, P., 220, 222, 232 Speare, A. T., 130, 133 Spegazzini, Carlos, 3, 241 Sprague, R., 391, 404 Stager, R., 193, 196, 198 Stakman, E. C, 11, 303, 304, 309, 324, 334, 335, 340 Stanley, I. N., 294, 299 Steinmann, A., 292, 298 Stevens, F. L., 107, 108, 177, 178, 179 Stevens, N. E., 217, 218, 226, 232 Stevenson, J. A., 105, 108 Stoneman, Bertha M., 222, 232 Stiiben, H., 81, 82 Sugano, Y., 105, 108 Swartz, Delbert, 374, 377 Swingle, D. B., 118, 128 Svdow, H., 7, 13, 178, 179, 180, 186, '236, 237, 241, 335, 340 Sydow, P., 7, 13, 335, 340 Tai, F. L., 402, 404 Tehon, L. R., 243, 245 Thaxter, R., 83, 88, 132, 133, 134, 233, 236 Theissen, F., 167, 171, 178, 179, 180, 186, 236, 237, 241 Thimann, K. V., 89, 91 Thom, Charles, 42, 55, 155, 157, 162, 395, 404 Thomas, H. E., 354, 364 Tiffnev, W. N., 94, 98 Tiller,' Rubv J., 226, 232 Tisdale, W. H., 72, 73 Tison, A., 44, 45, 55 Togashi, K., 105, 108 Tokunaga, Y., 75, 77 Toumefort, J. P. de, 4, 13 Tucker, C. iVI., 102, 104, 105 Tulasne, C, 6, 9, 13, 133, 328 Tulasne, L. R., 6, 9, 13, 133, 192, 198, 328 Unger, Franz, 7, 13, 317 Vandendries, R., 281, 284 Vanterpool, T. C, 76, 77 Varitchak, B., 141, 146 Vittadini, C, 272 Wager, H., 107, 108, 111, 112, 116 Wakefield, E. M., 292, 298, 346, 362 Walker, Leva B., 133, 134, 140, 146, 367, 368, 369, 373, 374, 380, 382 Ward, H. M., 160, 162, 333, 340, 341 Ware, W. AL, 292, 299 Weber, G. F., 109, 112, 116, 127, 128, 350, 364, 391, 402, 404 Wehmer, C, 11 Wehmever, L. E., 226, 228, 232 Wei, C' T., 402, 404 Weir, J. R., 243, 245, 346, 364 Weiss, Freeman, 263, 267 Welsford, E. J., 190, 197 Wernham, C. C, 45, 56 Weston, W. H., 109, 112, 116 Whelden, R. AI., 288, 291 Whetzel, H. H., 9, 13, 262, 265, 267, 331, 341 AUTHOR INDEX 411 W^hiffen, Alma J., 64, 66, 74 White, V. S., 373, 374, 380, 382 \\'hitc, W. L., 265, 267 \\'ianr, J. S., 105, 108 \\'ieben, Magdalene, 149, 150 \\'ildiers, E., 10 A^'illiamson, H. S., 270, 272 W'ilson, G. W., 107, 108, 114, 116 Wilson, O. T., 72, 74 \\'inaard, S. A., 145, 146 Wolf, F. A., 20, 22, 27, 28, 60, 62, 109, 112, 115, 116, 127, 128, 169, 171, 184, 186, 207, 209, 211, 212, 225, 231, 232, 253, 255, 265, 267, 343, 350, 364, 393, 402, 404 Wolf, F. T., 78, 82, 97, 98, 169, 171 Wollenweber, H. W., 400, 40 1, 404 Wood, Anna K., 220, 222, 232 Woronin, AI. S., 8, 13, 44, 56, 83, 88, 262, 267, 341 Woroninchin, N. N., 165, 167, 171 Yamamoto, W., 402, 403 Yates, H. S., 352, 364 Young, E. L., 43, 56 Zeller, S. M., 188, 198, 352, 364, 366, 367, 368, 369 Zikes, H., 154, 162 Zimmerman, H., 192, 198 Zopf, W., 43 Zundel, G. L., 305, 306, 309 SUBJECT INDEX Absidia, 118 caendeci, 22 cornealis, 116 cory?}ibifera, 116 glaiica, 122 * spinas a, 121 Acacia, 312, 313 Acantborbynchiis vaccinii, 202 Acervulus, 384, 387-390 Acblya, 58, 65, 69, i>5, 95, 97 a??zbisexnalis, 95, 98 bisexiialis, 95, 98 colorata, 98 flagellata, 96, 98 racemosa, 60 Achlyogeton, 75, 76 Achlyogetonaceae, 64 Achorion gypseimi, 152, 162 Acrasiaceae, 42 Acrasiales, 35, 41^3 Acrotheca, 397 Actinonema rosae, 253, 267 Adelopiis gmmaimi, 178, 179 Aecia, 318-321 Aecidieae, 335 Aecidiolum exanthematitm, 317 Aecidiuvi, 318, 520, 383 berberidis, 338 Aesczdus hippocastamnn, 211 Aethalium, 40, -^P Agaricaceae, 4, 33, 50, 341, 352, 353- 364 Agaricales, 38, 50, 341-364, 372 Exobasidiaceae, 341-343 Thelephoraceae, 343-345 Clavariaceae, 345-346 Hydnaceae, 346-347 Polyporaceae, 347-352 " Agaricaceae, 353-364 Agariciis, 4, 32, 277 arvensis, 354, 358 campestris, 358, 361, 362 C077itidiis, 358 tabidaris, 361 Agave, 145 Agropyroii occidentale, 195 «/^a, 195 caninis, 334 ^/Vfl caespitosa, 334 Albuginaceae, 58, 105-108 Albuginales, 62, 105-108 Albugo, 59, 61, 105 bliti, 105, 107, 108 Candida, 105, iO(J, 107, 108, 115 ipomoeae-pandiiranae, 105 occidentalis, 105 portidacae, 105, 107 spinulosa, 107 tragopogonis, 105, 107 Aleuria aurantia, 269 Aleurieae, 268 Aleurodiscus, 343 Alfalfa, 71, 72, 251, 257 Algae, 62, 63, 64, 69, 71, 73, 75, 99 desmids, 69, 75 diatoms, 69, 75 red, 235 Allantosphaeriaceae, 199, 227-228 Alloviyces, SI, 69, 78 aiiontahis, 81 arbuscida, 60, 78, 80, 81, 82 cystogemis, 81, 82 javanicus, 60, 78, 81, 82, 85 7HOJ2ilifor?ms, 81 Alternaria, 170, 385, 398 brassicae var. nigrescens, 398 cim, 398 longipes, 398 panax, 398 solajii, 398 fe7zz«X 398, 5PP Amanita, 211, 342, 356, 358, 360 bisporigera, 279 nniscaria, 50 solitaria, 354 Amanitopsis, 356, 358, 360 vaginata, 358, 361 /472 /V«//V numeral indicates that the page contains an illustration. 412 SUBJECT INDEX 413 Amaranthus, 105 Aviaiiroascus verrucosus, 153 Amazonia, 239 Ai)ibros'h% artemisiijolia, 73 Amelanchier, 336 Amerosporeae, 387 Amerosporiinn oecoiioinicimi, 391, 392 Amoebidiales, 134 Auiorphoviyces africajms, 234, 235 fiilagriae, 234, 235 Amphisphaeriaceae, 199, 207-208 Anchusa, 315, 336 Ancvlistales, 74 Ancylistes closterii, 74 Andropogon, 305 Anemone, 336 Annulus, 356 Antboxanthiini odoratiim, 196 Anthracnoses, 167, 219, 220, 222, 393 Ambracobia maurilabra, 250, 270 melalovia, 248 Anthiinis, 379 bore alls, 318 Apbanomyces, 63, 93, 94, 95, 97 laevis, 98 Aplanes, 93, 94 Aplospora Jiyssae, 323 Apodachlya, 88, 89 bracbynevia, 91 Apodacblyella completa, 91 xVpostemidium, 268 Apothecium, 150, 151, 245, 241, 249 Apples, 143, 173, 176, 215, 217, 220, 228, 336, 390, 392, 395 Arabis, 105 Aracbis hypogaea, 212 Arachniaceae, 374, 376 Aracbnioji, 380 albimi, 376 Araispora, 88, 89, 91 pidcbra, 91 Arcangeliella, 369 Archimycetes, 35 Arcyria, 52 denudata, 48, 50 incarjiata, 50 Arviillaria, 283, 357, 358 77iellea, 282, 354, 363 iiiucida, 281 Aronia, 336 Arthropods, 134 crabs, 135 millipeds, 135 Ascbersonia aleyrodis, 392 coffeae, 392 goldiana, 392 marginata, 392 Asclepiadaceae, 331 Ascoboleae, 268 Ascobolus, 248, 270 citrimis, 248 magnificiis, 248, 272 ster cor arms, 248, 272 strobilimis, 271, 272 viridis, 269 Ascocbyta, 208, 385, 390 pisi, 399 Ascodesmis, 270 viicroscopica, 269 porcina, 270 Ascoidea riibescens, 140, 146 Ascoideaceae, 140-143 Ascomycetes, 32, 33, 35, 37, 38, 137- 275, 383, 384 asexual reproduction, 137-138 assimilatory phase, 137 phylogeny, 139 sexual reproduction, 138 Hemiascomvcetes, 139-150 Endomvcetales, 140-146 Taphrinales, 146-150 Euascomycetes, 150-275 Plectomycetes, 152-179 Eurotiales, 152-162 Alyriangiales, 163-171 Erysiphales, 171-179 Pyrenomycetes, 179-245 Dothid'eales, 180-186 Hypocreales, 186-198 Sphaeriales, 198-232 Laboulbeniales, 232-236 Hemisphaeriales, 236-241 Hysteriales, 243-245 Discomycetes, 245-275 Inoperculates, 251-268 Helotiales, 251-267 Ostropales, 267-268 Operculates, 268-275 Pezizales, 268-272 Tuberales, 272-275 414 SUBJECT INDEX Ascophamis, 248, 270 carneiis, 248 gramilijorviiSy 248 isabellimiSy 269 Ascospores, explosive discharge of, 19, 24, 193, 200, 262 Ascotricha, 200 chartarum, 200 Aseroe, 379 Ash, 323 Asparagus, 337 Aspergillaceae, 152, 154-160 Aspergillales, 37, 152, 165 Aspergilhis, 25, 50, 154, 160, 394 clavatiis, 155 fischeri, 154 flavipes, 155 flaviis, 154, 155, 157 fimiigams, 155, 157, 395 glaucus, 154, 155, 157, 162 herbarionnji, 154, 162 nididans, 154, 155, 156, 157 niger, llo, 155, 157, 395 ochraceiis, 155 oryzae, 154, 155, i57, 162 quadril'meatiis, 156 repens, 154, 155, 162, 169 riigidosiis, 156 variaecolor, 156 versicolor, 155 iventii, 155, 157 Aspidiotus, 295 Asterina, 239, 241 Asterinella, 239 Asterostroma, 343 Astraeaceae, 373 Aulosjraphum, 239 Aitricidaria, 4, 128, 279, 280, 287 aiiricida-jiidae, 293, 294, 295 viesenterica, 295 Auriculariaceae, 4, 292-295 Auriculariales, 38, 278, 284, 286, 290, 291-299 Avena, 331 sativa, 334 Avocado, 167, 222 Azalea, 263, 341 Bacterhnn vermiforme, 145 Badhcmiia, SI Ulacina, 48, 50 magna, 48, 50 utricularis, 50 Bagnisiella, 167 Bagnisiopsis, 167 Balansia, 188, 191, 385, 392 hypoxylon, 191 Balsamiaceae, 274 Banana, 398 Barberry, 309, 317, 324, 328, 329, 330, 334 Barclay ella, 329 dejorijians, 326 Barley, 195, 302, 303, 307, 336, 401 Basidiobohis, 51, 129 lacertae, 132 ranarwn, 128, 130, 131, 132 Basidiomycetes, 32, 33, 35, 38, 39, 276-382, 383 basidiospores, 280 conidia, 282-283 diploidization, 281-282 mycelium, 280-281 types of basidia, 278-280 Heterobasidiomycetes, 284-341 Dacryomvcetales, 284-287 Tremellales, 287-291 Auriculariales, 291-299 Ustilaginales, 299-309 Uredinales, 309-341 Homobasidiomycetes, 341-381 Agaricales, 341-364 Gastromycetes, 364-382 Basidiophora, 109, 110 Basidium, 344 Basswood, 187, 188 Battarea, 373 Beans, 145, 220, 222, 328, 329, 337 Lima, 225 Beech, 140, 178, 187, 188, 266, 272, 298 Beets, 71, 94, 101, 337 Benzol, 115 Beta vidgaris, 109 BifKsella striiformis, 242 Binomial system, 5, 30 "Bios," 10 ' Birch, 142, 188 Birds, 395 Bird's-nest fungi, 276, 380-382 Bitter rot, 222 "Black molds," 116 "Black-fellow's bread," 402 Blake slea, 59, 127 trispora, 118, 120, 122, 123, 125, 127, 128 i SUBJECT INDEX 41 5 Blastocladia, 11, 78 prmgshewiii, 11, 78, 79, 82 Blastocladiales, 36, 62, 77-82, 84, 85, 87, 88 Blastocladielia, 81 Blue stain, 400 Boletaceae, 4, 361 Boleteae, 348, 351-352 Boletimis cassipes, 352 Boletus, 4, 32, 188, 190, 277, 280 parasiticus, 352 zelleri, 352 Bommerella, 200 Bordeaux mixture, 114 Botryosphaeria, 180 in flat a, 167 mascarensis, 167 ribis, 167, 168, 169, 110, 171 Botrytis, 4, 260, 270, 385 ciiierea, 260, 261, 266, 395, S99 convoluta,'266 Bondieria areolata, 269 Boz'ista, 364, 366, 375 Candida, 311 nigrescens, 374 plwtibea, 374 Bovistella ecbiimlata. 371 Brachypodimn sihaticimi, 196 Brassica, 105 Brania, 109, 7iO lactucae, 109, 114 Brevilegnia, 95, 97 diclina, 97 Bunt, 302, 307 Cabbage, 44, 66, 101, 390 Cacao, 354 Caeovia, 318, 319, 320, 383 72/f^7Z^, 339, 340 Calocera, 285 Calostoina, 313 hitescens, 311 Calostomataceae, 374 Calotheca, 114 Cahatia, 375 craniijormis, 374, 377 cyathifor?ms, 311 saccata, 374 Calvculosphaeria, 207 Calyptospora goeppertiana, 313 Cainarophylhis virgineiis, 279 Camellia, 381 Canavalia, 167 Candida, 144 Cantaloupes, 398 Cantharelhis, 283, 300, 341, 356, 357 cormicopioides, 279, 280 Capillitium, 40, 51-53 Capnodiaceac, 178 Capnodiinn citri, 178 Capsella, 105 Carex, 302 Carnations, 338 Carotene, 78 Carya illinoensis, 163 Caryophyllaceae, 331 Caryospora piitaminwn, 207, 208, 231 Castellania, 144 Castilleja, 337 Castor bean, 261 Catenaria anguilhdae, 64, 72 sphaerocarpa, 66 C at ost 0771a circtmiiscissiim 376 Caulothyriopeltis, 239 Celery, '391 Cellulin, 88 Cellulose, 64, 77, 83, 88, 200 Celtis, 114 Ce7ia7Jgiu77i abietis, 265 Cephalanthus, 323 Cephalosporiimi roseimi, 399, 400 Cephalidaceae, 124 Ceracea, 285 Ceratio77iyxa, 48 fructiculosa, 41 Ceratomycetaceae, 233 Ceratostomataceae, 198, 199, 203-207 C er at o St 0771 ell a fi77ibriata, 204, 205, 206, 230, 231 ips, 205 7ni7ior, 205 7no7iilifor77iis, 206 piceaperda, 205 pluria7midata, 205 pseiidotsiigae, 205 uh7ii, 203, 230 Cercis ca7jade77sis, 212 Cercosphaerella, 209 Cercospora, 209, 211, 385, 386, 398 araclmoidea, 212 betae, 399 beticola. 398 bolleana, 209, 211, 398 cercidicola, 212 crue7ita, 212 416 SUBJECT INDEX Cercospora lythracearinn, 211, 398 rmisae, 398 nicotianae, 398 per sic a, 212 persofiata, 398 nibi, in, in viticola, 211 Cercosporella, 209, 385, 395 viacidans, 397, 399 persicae, 397, 55^^ Cereals, 109, 176, 188, 219, 299, 307, 335, 391, 397, 400 CerioTnyces zelleri, 352, 364 Cerotelhmi fici, 337 Ceuthospora, 390 Chaetocladiaceae, 124 Chaetocladiuvt brefeldii, 120 jonesii, 120 Chaetomiaceae, 198, 200 Chaetomium, 200 Chcnnaecyparis nootkatensis, 336 thyoides, 258 Cheese, camembert, 159 Roquefort, 159 Cheiymenia stercorea, 248 Cherries, 146, 176, 180, 190, 220, 253, 261, 336 Chestnut, 225 Cblorosplenium aeruginosum, 165 Choajjephora, 58, 127 cucurbitarimi, 116, 122, 126, 117, 128 manshurica, 118 Choanephoraceae, 124 Chokecherry, 253 Chromoblastomycosis, 397 Chrysanthemum, 338 Chrysomyxa, 326, 330 abietis, 313, 316, 323 arctostaphyli, 321 ledi, 314 rhododendri, 314 Chrysophlyctis endobiotica 67 Chrysopsora, 326 Chytridiaceae, 64 Chytridiales, 19, 36, 45, 62, 63-74, 85 occurrence and cultivation, 64, 66 reproduction, 66 Olpidiaceae, 66-67 Synchytriaceae, 67-68 Woroninaceae, 69 Chytridiales, Rhizidiaceae, 69 Cladochytriaceae, 71-72 Hyphochytriaceae, 72 doubtful chytrids, 73 Ciboria, 260, 261 canmculoides, 265, 267 ficariae, 260 trifolioru772, 260 Ciborioideae, 259, 262, 265 Cicada, 132 Cicer arietmimi, 189 Cicimiobolus cesatii, 389 Cilia, 61 Ciliaria asperior, 250 scutellata, 248 Cinnamon, 222 Cmtractia, 301, 306 car ids, 300 7Jioj2tag?2ei, 304 Circinella conic a, 118 minor, 118 imtbellata, 118 Citric acid, 157, 395 Citrus, 128, 159, 167, 178, 208, 217, 218, 225, 395, 398 Cladochytriaceae, 58, 64, 171-172 Cladochytriimi, 72 hyalimmi, 19, 27 noivakoivskii, 63 replicatiim, 66, 73 Cladophora, 43 Cladosporium, 167, 397 carpophilum, 397 citri, 167 cucmnerinum, 397 iulvimz, 397 Clamp connections, 281, 343 Classification of fungi, by Bauhin, 4 by Fries, 5 by Linnaeus, 5 by MicheH, 4 by Persoon, 5 by Saccardo, 7 by Tournefort, 4 Clathraceae, 377, 378 Clathriis, 4, 31 cancellatus, 318 Claudopus, 353, 356, 357 Clavaria, 4, 32, 277, 285, 287 cinerea, 203, 279 cristata, 279 SUBJECT INDEX 411 Clavariaceae, 4, 341, 345-346 Clavariopsis, 287 prolifera, 290 Claviceps, 186, 187, 191, 197 paspali, 195, 196 purpurea, 191, 195, 196, 197, 198 rolfsii, 195 sesleriae, 196 ivilsoni, 196 Clavochytriuvi stomophilum, 6S, 66 Cleistothecium, 150, 1)1 Clitocybe, 283, 356, 357, 360 ex pall ens, 282 Closterium, 74 Clover, 128, 176, 182, 257, 260, 292, 313, 394 Coccidioidaceae, 143 Coccidioides bimiitis, 143 Coccomyces, 138, 385 hieinalis, 252, 253, 266 lutescens, 253 prunopborae, 253 Cocoa, 222 Coffee, 222, 283, 323, 337 Coleoptera, 233 Coleosporiaceae, 335 Coleosporium, 315, 319, 321, 323, 326, 330 soUdaginis, 324, 325 sonchi-arvensis, 329 Colletotrichum, 219, 392 393 circinans, 389 gloeosporioides, 20 lagenarium, 389 trifolii, 404 Collybia, 360 conigena, 281 Colus, 379 Comatrichia, 52 typhoides, 50 Commelinaceae, 343 Covipletoria coviplens, 128, 132 Compositae, 332 CoJiidio bolus, 128 iitricidosus, 131 villosus, 131 Conifers, 313, 351 Coniophora cerebella, 281, 282, 344 Coiiiothyrhim, 182, 390 pyrina, 389 Convolvulaceae, 105 Coprimis, 211, 357, 358, 360 atramentarius, 23, 361 Copr/777/5 coviatus, 354 ephemerus, 280 firnetarius, 281 lagopus, 281, 283, 284, 5^J viicaceus, 23, 281 narcoticiis, 281, 282 niveus, 281 radians, 284 rostrupianus, 282, 284 stercorarius, 281 Coprobia gramdata, 250 Coprophilous fungi, 116, 118, 127, 128, 152, 153, 200, 270 Coral fungi, 276, 345-346 Cordyceps, 161, 186, 187, 385 agaricijormia, 191, 197 capitata, 191 clavidata, 189, 194 'militaris, 191, 198, 400, 404 sphingum, 191 Coreopsis, 337 Corn, 66, 70, 71, 72, 300, 303. ^07, 336, 390 Corticium, 50, 291, 393, 401 bombycinum, 281, 282 calceum, 283 effuscatimi, 283 koleroga, 344, 401, 402, 403, 404 polygonium, 281 roseo-pallens, 283 stevensii, 402, 403 ■vagum, 343, 401 varians, 281 Cortinarius, 356, 358 pholideus, 363 Cory his avellana, 115 Coryneum, 392 beijerinckii, 394 Cotoneaster, 336 Cotton, 127, 141, 189, 220, 397 Cowpea, 116, 127, 189, 392 Cranberry, 67, 202, 222, 341 Crataegus, 78, 336 Craterellus, 288 bore alls, 362 Crepidotus, 353 Cribraria, 53 Cronartieae, 335 Cronartium, 315, 319, 323, 326, 330 asclepiadhmi, 331 cerebrinn, 337 coleosporoides, 313, 337 i barknessii, 337 418 SUBJECT INDEX Cronartiwn quercimvi, 313, 329, 337 ribicola, 313, 316, 318, 322 Cnicibiiliim, 381 vulgar e, 311, 380, 382 Crucifers, 44, 105 Cryptococciis fagi, 188, 197 Cryptoinyc'wa, 257 pteridis, 259, 266 Crypto poms rolvatus, 352 Ctenoiuyces serratiis, 152 Cucumbers, 176, 261, 397 Cucurbitaria, 138 Cucurbitariaceae, 199, 207 Cucurbits, 109, 127 Ciidonia hitea, 266 Cudonieae, 266 Cultivation of fungi, 21-27 media, 21, 22 agar, 21 pU, 11 temperature, 25 Cwminghaiiiella bertholletiae, 119 echmiilata, 119 Cupressineae, 332 Currant, 169, 187 Cyatlms, 380, 381 fascicidaris, 382 stercorals, 311, 381 striatiis, 382 Cydonia, 336 Cvlindrocarpon, 187, 385 Cylmdrosporhim, 253, 259, 307, 385, 392, 394 juglandis, 399 Cyjncidothea trifolii, 182, 183, 184 Cystobasidium, 292 Cystopsora, 328 Cystopiis candidiis, 108 Cytospora, 225, 390 Dacryomyces, 280 deliquesceiis, 285, 286 Dacrvomvcetaceae, 285 Dacryomvcetales, 38, 279, 284-287 Dactylis, 'l91 Daedalea confragosa, 350 juniperina, 23 qiiercina, 349 iinicolor, 281 Daldinia, 228 Dandelion, 173 Darling's disease, 143 Darluca filin/i, 390 Dasyscypba, 1^1 ellisiana, 259, 266 pini, 259, 266 ivillkovmiii, 259 Dasyspora faveolata, 319, 320 Delacroixia coronata, 131 Dematiaceae, 387, 394, 397-400 Dematophora, 203 Dendrochium, 189 Dendrophoma, 390 Dermateaceae, 246, 251-257 Dermatophytes, 11, 152, 153 Deuteromycetes, 32, 33, 383-404 classification, 386-387 development of pycnidia and acervuli, 387-390 Sphaeropsidales, 390-392 Melanconiales, 392-394 Moniliales, 394-401 iMycelia Sterila, 401-402 Dewberry, 222 Diachaea, 46 Dianthiis caryophyllus, 398 Diaporthaceae, 199, 224-226, 228 Diaportbe, 385 citri, 20, 220, 225 parasitica, 226 phaseolonnii, 215, 231 sojae, 115, 116 Diatrypaceae, 227 Diatrype, 228 Diatrypella, 228 Dibotryon luorbosimi, 180, 181, 186 Dicranopbora jidva, 121 Dicty diaetbaliwji phnnbeuni, 48, 50, 54 Dictydiinii cane ell atimi, 48 Dictyophora, 377, 378 Dicrv^osporeae, 387 Dictvosteliaceae, 42 Dictyosteliinn discoideimi, 41, 42, 43, 55 vine oroides, 42 piipiireinn, 42 Dictyiicbiis, 58, 60, 93, 95 monosporus, 95 Dicyma ainpidlifera, 200 Didymella, 170 Didy77iellina macrospora, 398 or7iithogali, 398 SUBJECT INDEX 419 Didyvmmi difforuie, 50 iiigripes var. xanthopiis, 50 Didvniosporeae, 587 Diplocarpon, 138, 253 earlhvia, 253, 254, 255, 385 rosae, 253, 255, 385 soraueri, 253, 25<^ Diploclad'mm mimis, 188 Diplodht, 219, 390 gossypina, 218 viauilliana, 389 natal ensis, 218 ze^?^, 390 Dipodasciis, 139 j//?/cy//5-, 740, 142 Diptera, 233 Discedera pedicellata, 311 Disc el I a platajji, 225 Discellaceae, 387 Discomvcetes, 5, 19, 31, 37, 50, 150, 236, 243, 245-275 Inoperculates, 251-268 Helotiales, 251-267 Ostropales, 267-268 Operculates, 268-275 Pezizales, 268-272 Tuberales, 272-275 Disc OS la, 392 artocreas, 399 Dispira cormita, 116, 126, 127 Disticblis spicata, 338 Doassansia, 302 jnartiaijofpana, 306 sagittariae, 305 Dothichloe, 188, 191, 385, 392 Dothideaceae, 180, 182-186 Dothideales, 37, 179, 180-186, 237 Dotbidella idmi, 186 Dothiora, 167 Dothioraceae, 163, 167-169 Dothiorella, 169 Downy mildews, 114 Draba^ 105 Drepanapezizoideae, 253 Diirandiomyces phillipsii, 268 Dutch elm disease, 203, 205, 400 Earthstars, 376 "Earth tongues," 266 Ebony, 222 Eccrina, 134 Zccrinales, 62, 134-136 Eccrinella ganwiari, 135, 136 Eccrinoides he/i/iegiiyi, 135, 136 Eccrinopsis hydrophilorin/i, 135 Echidnodella, 239 Echidnodes, 239 Echinodoutinn ti/ictoriinu, 346 Ectrogellaccae, 69 EidaiJiella spinosa, 152 Elapbomyces cervimis, 161, 191 gramdatus, 161, 191 Elaphomycetaceae, 152, 161, 274 Elephantopus, 337 Elm, 140, 182, 187, 203, 205, 220, 400 Elsinoe, 385, 397 australis, 167, 171 canavaliae, 167 fawcetti, 167, 171 piri, 167 veneta, 166 Elsinoeaceae, 163, 165-167 Elvella, 32, 248, 268, 271 elastic a, 269 Elvellaceae, 246, 268 Ely lints canadensis, 192 Elytroderma deformans, 242, 243 Empnsa ftmiosa, 130 jnuscae, 132 Endoconidia, 160 Endogonaceae, 62, 133-134 Endogone malleola, 133, 134 pisijonnis, 133 Endomyces decipiens, 143 niali, 143 Endomvcetaceae, 140, 143-144 Endomycetales, 37, 139, 140-146 Endophyllum eiiphorbiae-sylvaticae, 313, 321, 326 sejnpervivi, 326, 321, 338 Endoptychtim agaric aides, 370 Endosporeae, 35, 48 Endothia, 138 parasitica, 221, 223, 224, 226, 232, 388, 389 Englerulaceae, 178 Englerulaster, 239 Enteridimn, 52 splendens, 50 Enterobriis attenitatiis, 134, 136 420 SUBJECT INDEX Enterobnis elegaiis, 134, 136 spiralis, 134, 136 Enterobryus, 134 E7ito?fiopeziza, 255 soraiieri, 253, 256 Entovwpbtbora, 57, 128, ISO jinnosa, 129, 133 imiscae, 128, 130 pseudococci, 132 sciarae, 129 sphaerosper?na, 129, 132, 133 Entomophthorales, 36, 61, 62, 74, 128-132 Entomosporiiim nmciilatiim, 2SS, 256 Entophlyctis, 73 Entylovia, 301 ellisii, 307 nymphaeae, 299, 505 Eocronartiinn imiscicola, 294, 298, 299 Ephelis, 188, 191, 385, 392 Epicbloe, 188, 385, 392 typhina, 191, 194 Eremascaceae, 143 Eremascaceae Imperfectae, 143 Eremasciis, 138, 139 albidm, 141, 143 Ergot, 191, 195, 196, 197 Ericaceae, 341 Ervsiphaceae, 171-176, 177 Ervsiphales, 37, 171-179, 237 Erysiphe, 138, 172, 174, 175 cichoracearum, 173, 176 galiopsidis, 173, 175 graminis, 171, 173, 174, 176 polygoni, 172, 176 tortilis, 175 Escherichia coli, 42 Euascomycetes, 37, 139, 140, 141, 150-275 Euglena, 70 Euphorbia, 313 Eurotiales, 37, 152-162 Eiirotiuni, 154, 394 herhariorwn, 154 Eusclerotinia, 259, 260 Euthamia, 337 Eutuberaceae, 274 Excipulaceae, 387, 390, 392 Exidia, 287, 288, 289 Exoascales, 37, 139 Exoascus, 149 de^orvians, 150 Exobasidiaceae, 341-343 Exobasidiwn discoideiiin, 341 rhododendri, 280, 341, 342 symploci, 341 vaccina, 341 Exosporeae, 35, 48 Fabric, mildew of, 395 Fairy rings, 361 Favus, 152 Feathers, 152, 160, 395 Fendlera, 336 Fermentation, Aspergillus oryzae^ 157 germ theory of, 2, 7 Mucorales, 118 yeasts, 144-145 Ferns, 99, 259, 294, 309, 323, 33.1, 337 prothallia, 128, 132 Festuca, 195 Ficiis carica, 211 Figs, 145, 222, 337, 398 Fimetariaceae, 198, 199, 200-203 Fir, 331, 337 Douglas, 178, 259 white, 266 Fish, 94 Fisndijja hepatica, 281, 351 FistuHneae, 348, 351 Flax, 337 Florideae, 139 Eomes amiosus, 283, 351, 363 applanatus, 23, 350, 5J5 igtiiarius, 351 ohioense, 350 pini, 351 pinicola, 23 robineae, 23 robiistus, 351 roseiis, 23, 281 siibroseiis, 281 texafius, 23 Fonsecaea, 397 Fracchiaea, 207 Fraxinus, 212 Frogs, 128, 132 Fzdigo septica, 40, 46, 48, 49, 50 Fungi Imperfecti, 32, 33, 35, 39, 50, 343, 383-404 SUBJECT INDEX 421 Fungi Imperfecti, classification, 386- 387 development of pycnidia and acervuli, 387-390 Sphaeropsidales, 390-392 Melanconiales, 392-394 Moniliales, 394-401 Mvcelia Sterila, 401-402 Fur, '3 95 Fiisarhnn, 187, 188, 194, 385, 396, 400 oxysporimij 401 Elegans, 401 Martiella, 401 solani, 401 vasinjectiim, 189 Fusicladhnn, 385 deyidriticiim, 215, 217 Fusidium, 307 Gal actinia proteana, 250 saiiiosa, 250 Galera silignea, 280 Gallic acid, 395 Galloxvaya pinicola, 315 Ga7w?ianis locusta, 135 Ganoderma, 280 applanatiim, 363 curtisii, 23 Gasterella lutophila, 367, 368 Gastromycetes, 30, 32, 38, 46, 133, 272, 276, 279, 280, 281, 298, 364-382 Hymenogastrales, 367-369 Podaxales, 369-372 Sclerodermatales, 372-374 Lvcoperdales, 374-377 Phallales, 377-380 Nidulariales, 380-382 Gautieria, 366, 369 grave olens, 368 Geaster, 4, 277, 555 ■fornicatus, 371 hygrometricus, 311 velntimiSy 376 Geastraceae, 374 Gene a, 274 verrucosa, 213 Geoglossaceae, 246, 251, 266, 268 Geoglosseae, 266 Geoglossinn, 248 difforvie, 250 Geolegnia, 95 Gcopvxis, 248 Geotrichum, 144 Geranium robertianum, 111 Gibberella, 138, 385 saiibinettii, 188, 194, 401 zeae, 188 Gill fungi, 276, 353-364 Gills, 351, 360 Ginseng, 398 Gleditsia japonic a, 189 triacanthos, 189 Gleotulasnella, 290 Gloeodes, 392 Gloeosporiimi, 219, 222, 307, 385, 392, 393 caidivorinn, 394 cingidatinn. 111 vmsarwn, 389 nerviseqiami. 111, 225 riijomacidans, 389 Venetian, 167, 171 Glomerella, 138, 219, 220, 385 cingidata, 220 glycijies, 220, 224 gassy pa, 220 lagenaria, 220 lindenmthiana, 220 Glonium, 245 Gluconic acid, 395 Glyceria fliictans, 196 GnoiJionia, 219, 385 dispora, 199 erythrosto77ia, -219, 220, 230 leptostyla, 220, 222, 385 z//7;;fj, 220, 221, 232 veneta, 220, 222, 225" Gnomoniaceae, 199, 219-224 Gnomoniopsis, 222 Goldenrod, 337 Gojjapodya, 87 poly??7orpha, 87 prolifera, 59 siliquaejonms, 86 Gooseberries, 176 Goplana, 295 mirabilis, 313, 328 Gossvpium, 212 Grapes, 109, 176, 214, 215, 222, 393 Graphiola phoenicis, 305, 308 Graphiolaceae, 305 Graphiuin, 400 ulmi, 203, 230, 400 422 SUBJECT INDEX Grasses, 170, 171, 182, 186, 191, 193, 195, 219, 299, 302, 332, 391, 392, 397 Grossularia, 336 Gitepinia, 285 spatbularia, 286 Guigimrdia, 208, 214-215, 385, 390 baccae, 215 bidwellji, 214 Guttulinaceae, 42 Gvmnoascaceae, 152-153 Gynmoascus, 152 candidiis, 153 gypseitm, 162 reesii, 153 setosits, 153 Gyjimoconia mterstitialis, 313, 316, 318, 333 Gvmnomyces, 369 Gy?7mospora7igm?7i, 4, 315, 317, 319, 321, 330, 331 benimdianwn, 336 clavariaejorme, 316 clavipes, 313, 327, 336 globosimt, 336 jwiiperi-virghijanae, 312, 336 mdiis-avis, 313 nootkatejise, 336 sabinae, 330, 336 ymnadae, 336 Gvpsum blocks, 145 Gyrocephalus, 288 Gyrostroma, 189 Hamcnnelis virgifimna, 176 Haplosporanghnn, 118, 120 bisporale, 120 Harpocbytrhim hedeni, 6S Hazel nuts, 145 Helicobasidium piirpureiim, 292, 298 Helicoma ciirtisii, 399, 400 Helicoon reticidatiim, 399 Helicosporeae, 387 Helicosporium, 400 H ehninthosporhnn, 171, 176 clavariorum, 203 ravenelii, 397, 5i'P Helotiaceae, 246, 251, 259-266, 268 Helotiales, 37, 246, 247, 251-267 Helotium, 247 Helvellaceae, 246 Helvellales, 38, 247, 274 Hemiascomycetes, 37, 133, 139-150 Heviileia vastatrix, 323, 337 Hemisphaeriaccae, 236, 237, 241 Hemisphaeriales, 37, 152, 180, 236- 241 Heinitrichia, SI clavata, 50 serpida, 46, 48, 49 vesparhnn, 40, 50 Hempseed, 92, 100 Hendersonia opimtiae, 389 Hepatica, 336 Herbalists, 4 Hericium, 346 Hermaphroditism, 200, 201, 202, 262 Herpobasidhnn filicininn, 294, 298 Heterobasidiomycetes, 276, 279, 284- 341 Dacrvomycetales, 284-287 Tremellales, 287-291 Auriciilariales, 291-299 Ustilaginales, 299-309 Uredinales, 309-341 Heteroecism, 262, 312, 314, 328-332 Heterosporiimi, 398 echinidatinn, 398 iridis, 398 onnthogali, 398 phlei, 398 var labile, 398 Heterothallism, 121, 281, 288, 318 Hierachnn boreale, 111 Hlgglnsla, 253, 385 blevialls, 253, 394 line sc ens, 394 prunophorae, 394 Hirneola, 294 Histoplamta capsidatum, 143 History of mycology, among Greeks, Romans, 2, 3 influence of "authority," 1 invention of microscope, 2 morphologic approach, 9 Hoehnellomyces delectans, 298 Holcus, 195 Hollyhocks, 338 Homobasidiomvcetes, 38, 276, 291, 341-381 Agaricales, 341-364 Gastromycetes, 364-382 Hymenogastrales, 367-369 Podaxales, 369-372 Sclerodermatales, 372-374 SUBJECT INDEX 423 Homobasidiomycetes, Lycoperdales, 374-377 Phallales, 377-380 Nidulariales, 380-382 Honiothallism, 121 "Honey dew," 193, 195, 196, 208 Hops, 109, 176 Hormodendrum, 181, 182, 397 Humaria, 247 Humarieae, 268 Hyalocyphaceae, 246 Hyalodictyae, 387 Hyalodidymae, 387 Hyalophragmiae, 387 Hyaloria, 290 pilacre, 289 Hyaloriaceae, 287, 289 Hyalospora, 323, 331 Hyalosporeae, 387 Hvdnaceae, 341, 346-347 Hydnanghim carneimi^ 280, 368, 369 Hydnobolites c alif ornicus . 213 Hydnotrya tiilasnei, 213 Hydmmt, 32, 288 coralloides, 346 erhiaceits, 346, 3S2 septentrionale, 347 Hydrophihis picens, 135 Hygrophorus, 357 Hvmeniales, 38 Hymenochaete, 343 Hy7ne720gaster, 369, 372 behrii, 368 hit ens, 368 Hymenogastraceae, 368 Hymenogastrales, 38, 366, 367-369 Hymenomycetes, 11, 18, 20, 32, 50, 186, '276, 279, 280, 282, 283, 295, 341-364 Hymenoptera, 233, 297 Hyphal bodies, 129, 130 Hvphochytriaceae, 72 Hypholo77ia perpleximi, 281 Hyphomycetes, 31, 32, 39, 386 Hypoch7ms, 128, 401 sasakii, 403 terrestris, 281 Hvpocreaceae, 187 Hypocreales, 37, 179, 186-198, 392 Hvpocrella, 392 Hypoder777a defor777ans, 243, 245 Hypodermataceae, 243, 392 Hyp0777yces, 186, 190, 194 chrysosper777iiSj 188 lateritius, 188 ochraceiis, 188 rosellus, 188 sola7ji, 401 Hypoxylon, 228 Hysterangiaceae, 368 Hystera7igiu77i, 369 stolo77ijern77i var. a?77ericami777, 368 Hysteriaceae, 243, 244 Hysteriales, 37, 208, 241, 243-245, 268 Hysteriimt pidicare, 244 Hysterographiu777, 245 fraxi7ii, 244 Hysterothecium, HI, 243, 244 Industrial uses of fungi, 11 Inoperculatae (chytrids), 64 Inoperculates (Discomycetes), 246, 251-268 Helotiales, 251-267 Ostropales, 267-268 Insects, 99, 186, 191, 233, 400 beetle, 233 beetle larvae, 128 butterfly larvae, 128, 191 flies, 128 plant lice, 128, 208 scale insects, 128, 163, 178, 188, 191, 292, 295, 296, 297, 392 termites, 131 International Congress, 30 lola hookeriaTitmt, 294 jave7jsis, 294, 298 Ipo777oea purpurea, 222 Iris, 398 Irpex lactezis, 23 Is aria, 385, 400 farijjosa, 400, 404 Isoachlya, 94 Isolation methods, 15-21 acidulated media, 17 contaminants, 17 dilution method, 16-17 monosporic isolations, 17-19 streak method, 16 surface disinfection, 15 Ithyphalhis, 377 i777piidic7iSy 318 Iidiis piisilhis, 134 424 SUBJECT INDEX Jasiminmi grandiflonmi, 321, 338 Jelly fungi, 276, 282, 283, 284-295 Jimipenis, 270, 313, 331 covnminis, 257 7nexicana, 207 virgmiajia, 258, 312, 351 Kabatiella, 392 cmdivora, 394, 404 Kalchbrennera, 379 Keitbia, ISl chainaecyparissi, 258 jimiperi, 257, 258 tetraspora, ISl^ 258 thiijina, 258 tsitgae, 258 Keys, 34-39 Ascomycetes, 37, 38 Basidiomycetes, 38, 39 classes of fungi, 34, 35 Fungi Imperfecti, 39 Alyxomycetes, 35 Phycomycetes, 35, 36 Kordyaiia polliae, 343 Kitehneola uredinis, 324 Kiinkelia nitens, 313, 324, 326 Laboidbenia chaetophora, 235, 236 gyrinidaruTn, 235, 236 Laboidbeniaceae, 233 Laboulbeniales, 37, 152, 179, 180, 233- 236 Labyrinthula macrocystis, 43 Labvrinthulales, 35, 43 Laccaria, 360 Lachnea, 248 Lachneeae, 268 Laclmella, 248 piiii, 259 Lactarms, 125, 280, 283, 356, 357, 360 deliciosus, 2 Lagena radicicola, 76 Lagenidiales, 36, 62, 69, 74-77 Lagenidium, 61, 75, 76 americajiiim, 15 ejjtophytum, 76 giganteimi, 75 rabenhorstii, 15 Lager stroemia indie a, 173 Lambertella, 263, 265 Lamproderma, 52 Lamprospora areolata, 269 Larch, 259, 337 Larkspur, 401 Lasiobolus, 292 Lasiobotrys, 176 Lasiosphaeria pezizula, 400 Late blight of potato, 102, 104 Leather, 152, 395 Lecanium, 189 Lecanosticta, 392 acicola, 184, 185 Ledimi palustre, 261, 262 Leersia, 307 Legumes, 302 Leiotheca, 114 Lembosia, 239 Leiitimus lepideus, 23 LeJizites abietinus, 281 saepiaria, 23, 281 trabea, 281 Leocarpiis fragilis, 48, 50 . Leotia, 289 Lepidoptera, 191 Lepiota, 356, 357, 358 clypeolaria, 361 Leptoleg?iia, 58, 93, 94, 95, 97 candata, 97 Leptomitales, 36, 62, 72, 87, 88-91, 98 Leptoinitiis, 87, 88 lacteus, 89, 90, 91 Leptosphaeria, 170 avenaria, 391 Leptostrovia camelliae, 381 Leptostromataceae, 251, 386, 390, 392 Leptothyritmi pomi, 392 Lettuce, 109, 114, 261, 394 Leucogaster, 369 Leucophlebs, 369 Leucosporae, 358 Leveillula, 172 taiirica, 173 Licea, 53 Liceales, 35, 45 Lichens, 251 Ligniera, 44, 45 Lime-sulphur sprays, 148 Liquidambar, 346 Liver fluke, 66 Liverworts, 99 Lizards, 128, 132 Logoglomeris rugifera, 135 Lophiostomataceae, 199, 208, 243 SUBJECT INDEX 425 Lophodenmimt laricinimi, 242 nitens, 242 pinastri, 243, 245 Loquat, 222 Lychnis dioica, 300 Ly CO gala, 51 epidendnmt, 40, 50 Lycoperdaceae, 4, 366, 374 Lycoperdales, 38, 366, 374-377, 380 Lycoperdon, 4, 32, 277, 364, 365, 373 geiwnatwn, 374, SI 5, 376 pulcherriinwn, 374 pyrifor7ne, 282, 371, 375 ivrightii, 375 Alacowanites, 369 Macrochytrhnn botrydioides, 68, 72 Macropbonia, 169, 390 citridli, 389 Macrophomina phase oli, 401, 403 Macrosporium, 170, 385, 398 Magicicada septemdecivi, 132 Magnusiella, 148 Maleae, 332 Mallows, 315 Malus, 336 Mango, 222 Manilla cordifor?ms, 346, 352 Maples, 176, 187, 188, 257, 347 Marasmius, 357 crinis-eqid, 354 sacchari, 354 saramentosus, 354 Marssonia, 209, 219, 253, 392, 394 fragariae, 385 fraxini, 111 jiiglandis, 111, 385 rosae, 385 jiiglandis, 385 panattoniana, 394 Massospora cicadina, 129, 130, 752, 132, 133 Megachvtriaceae, 64 Mela??ip'sora, 314, 319, 326, 330 abietis-canadensis, 324 bigelowii, 337 caryophyllaceanmr, 315 farloivii, 315, 337 /i7z/, 318, 323, 525, 337 medusae, 527, 337 pinitorqua, 313 Melavipsora rostnipii, 333 Melampsoraceae, 326, 335 Melanipsoreac, 335 Melai/ipsorella, 323, 330 caryophyllaceariim, 331 elatina, 325 Melampsoridium, 323, 330 Melanconiaceae, 387, 392 Melanconialcs, 39, 386, 387, 392-394 Melanconis, 226 Melanconiimi, 392 jidigenimi, 393 Melanosporae, 358 Melasmia, 257, 258, 385, 392 Melia azadarrach, 114 Meliola, 177, 241 cainelliae, 389 circijiajis, 177, 179 corallina, 177 Aleliolaceae, 171, 176-179 Melons, 220 Meristogenous origin, 387, 388 Meruleae, 348 Mendiiis, 288 lacry??ians, 281, 348 Michelia veliitina, 313, 328 Micro glossinn viride, 250 Micromanipulator, 18 Microsphaera, 171, 172 berberidis, 175 grossidariae, 176 Micro stroma, 343 jiiglandis, 364, 55^5, 404 Microthyriaceae, 236, 237-241, 253 Mi/eW^, 317, 323, 331, 337 marginalis, 316 polypodophila, 324, 327 Milium effiisinn, 196 Mites, 26-27 ciiciillata, 166 miiscicola, 266 piisilla, 250 Molinia coenilea, 192 Mollisia, 247 Mollisiaceae, 268 Mollisioideae, 251 Monilia, 144, 2, 280 Mycenastrum, 555 Mycetozoa, 40, 41 Mycochytridineae, 36, 64 Mycoderma, 144 pemiciosa, 188, 55>P rosea, 188 Mycoplasm hypothesis, 11, 333, 334 Mycorrhiza, 10, 99, 161, 272, 345, 352, 354 Mycosphaerella, 138, 208-214, 385, 390, 398 arachidicola, 212 araclmoidea, 212 areola, 111 berkeleyi, 111 bolleana, 138, 20i?, 2i0, 211 c eras ell a, 211, 231 cercidicola, 111, 214 confiisa, 111 cruefita, 111 efflgiirata. 111 jraxinicola, 209, 212, 225 hieracii, 211 hippocastaiii, 111 lythracearuni, 211 7;/cn, 2/5, 397 nigerristigina, 211 nyssaecola, 209, 212 per sic ae. 111 personata, 211 poly?7iorpha, 111 pwictiformis f. ;f/7/^e, 211 rz/Z?/, 391 Mycosphaerellaceae, 199, 208-219 Mycotypha microspora, 120, 128 Myriangiaceae, 163-165, 167 Myriangiales, 37, 152, 163-171, 180, 208, 237 SUBJECT INDEX 427 Myriangium ciirtisii, 163, 165 diiriaei, 163, 164 Mytilidion scolecosponmi, 244 Alyxamoebae, 40, 41, 47 Myxochytridineac, 36, 64 iMyxogastres, 35, 45-53 Mvxomycetes, 30, 32, 33, 34, 35, 40- 56 artificial culture, 50-51 capillitium, 51-53 classification, 53 feeding of plasmodia, 49-50 fusion of swarmers, 49 spore germination, 47-49 taxonomy, 41 Myxosporiimi, 392, 393 valsoide^mi, 222, 225 Myzocytijmi, 75, 76 vertnicohim, 16 Naucoria lenticeps, 280 Nectria, 188, 385 cinnabarijia, 187 coccinea, 187, 188 ditissivm, 188 galligena, 188, 197 ipomoeae, 187 Nectriaceae, 187 Nectrioidaceae, 386 Needle cast, 244 Nematospora coryli, 145 lycopersici, 145 phase oli, 144, 145, 146 Nematosporangium, 100 Neocosmospora, 188 vasiiTfecta, 188, 189, 197 Nephrochytrhtm aiirajithmi, 66, 74 Net plasmodia, 43 Neiirospora, 1 1 sitophila, 202, 230 tetraspe-nna, 199, 202, 230 Nidula, 380, 381 Nidularia, 380, 381 Nidulariales, 39, 366, 373, 380-382 Nitschkieae, 207 Nomenclature, 30, 31 generic and specific names, 31 Latin descriptions, 31 Gastromycetes, 30 Myxomycetes, 30 Nomenclature, Uredinales, 30 Ustilaginales, 30 Nmwmilaria discreta, 227 Nyctalis asteropbora, 283, 354 parasitica, 283, 354 Nyssa, 212, 346 sylvatica, 163 Nyssopsora echinata, 327 Oak, 146, 187, 203, 222, 239, 272, 337, 345, 351, 354 Oats, 114, 195, 300, 302, 307, 336, 391 Ochrospora, 326 Ochrosporae, 358 Octavinia ravenelii, 371 Oedocepbahmi, 283 globidifenmi, 351 Oedogonium, 69, 85 Oidiopsis t auric a, 173, 179 Oidimn, 173, 174 tuckeri, \16 Oleander, 208 Olive a capitidi^orviis, 323 Olpidiaceae, 58, 64, 66-67, 69 Olpidiopsidaceae, 69 Olpidiopsis, 61, 63, 69 achlyae, 66, 69, 73 hixiirians, 63, 69 saprolegjiieae, 69, 73 Olpidiimi, 58 brassicae, 66, 67 viciae, 60, 67 Ombrophiloideae, 265 Omphalia ftavida, 283 Onion, 66, 109 Onygena, 160 eqiuna, 162 Onvgenaceae, 152, 160 Oomycetes, 36, 60, 83-116 Operculatae (chytrids), 64 Operculates (Discomycetes), 245^ 246, 268-275 Pezizales, 268-272 Tuberales, 272-275 Ophiobohis, 208 cariceti, 229, 231 cariceti var. grajninis, 219 graminis, 231 Ophioceras albicedrae, 207 Orbiliaceae, 246 Orcbestia gaminarella, 135 Oryza sativa, 308 428 SUBJECT INDEX Ostropa, 268 Ostropaceae, 246, 267 Ostropales, 246, 267-268 Otideeae, 268 Otomycosis, 157, 395 Ovularia, 209 Ovulinia, 161^ 263 azaleae, 263 Oxalis striata, 336 Oxycocciis ?nacrocarpon, 341 Ozoniuvi oiimivorwn, 402 Fachyvia cocos, 364, 402, 404 Fanaeolus cavipamilatus, 281 Fanopeiis herbstii, 135 Paper, 152, 159, 200 Papulospora, 245 Paradichlorobenzene, 115 Parasitella simplex, 116 Parthenium, 337 Parthenogenesis, 97, 143, 145, 228, 280 Paspalum dilatatiim, 196 floridamnn, 196 laeve, 196 Fassalus cornutiis^ 134 Fatella abiindans, 270 scutellata, 269, 271 Fatellina fragariae, 389 Faxina fiisicarpa, 269 Peaches, 176, 207, 261, 336, 394, 397 Peach-leaf curl, 146 Peanuts, 189, 398 Pear, 187, 188, 253, 336, 395 Peas, 94, 337 Pedicularis, 337 Penicillin, 11, 160 Fenicillium, 25, 50, 154, 157, 158, 394, 395 avellaneiiTn, 158 brefeldianum, 158 ca7Jie77iberti, 159 cnistaceimi, 158, 158 digit atiim, 159, 395 expansiiTfi, 159 glabnmi, 116 glauciim, 158j 395 italicimi, 159, 395 javaniciim, 158 hiteimi, 158 notatum, 116, 160 F enicilliuTn pfefferiammi, 116 purpiirogejium, 1 59 roqiieforti, 116, 158, 159 spiculisporum, 158 Feniophora, 343 allescheri, 283, 284 gigantea, 281, 344 sambiici, 281 Peraphyllum, 336 Peridermium, 318, 319, 383 Periplasm, 89, 91, 92, 100, 107, 111 Perisporiaceae, 171 Perisporiales, 37, 150, 171 Perithecium, 150, 151 Feronea jniniita, 132 Feronoplasinopara, HI celtidis, 114 ciibe7isis, 109 huvtuli, 109 vieliae, 114 ^ Fero72ospora, 110, 111 alsineannn, 109 destriictior, 109, 115 efz^y^, 109 ficariae, 115 parasitica, 116 schachtii, 109 tabacina, 24, 5P, 60, 62, 109, 111, 112, iii, 114, 115 viciae, 109 Peronosporaceae, 58 Peronosporales, 36, 61, 62, 98, 108-116 Pestalotia, 394 Festalozzia, 392, 394 guepini, 389 pahnartim, 389 uvicola, 399 Peyritschiellaceae, 233 Pez/z^, 32, 248 aurantia, 248, 250 badia, 271 repanda, 270 venosa, 11 \ vesicidosa, 269, 270, 271 Pezizaceae, 4, 246, 268 Pezizales, 38, 246, 247, 257. 268-272, 274 Pezize?e, 268 Pezizella, 248 Phacidiaceae, 246, 251, 257-259, 392 Phacidiales, 37, 236, 243, 247 Phaeodictyae, 387 SUBJECT INDEX 429 Phaeodidymae, 387 Phaeophragniiae, 387 Phaeosporeae, 387 Phakosporeae, 335 Phalaris arimdinacea, 331 Phallaceae, 4, 377 Phallales, 38, 366, 377-380 P hallo gaster, 369 sac cams, 368, 311 Phalloids, 377-380 Phallus, 4, 32, 377, 378 Phase olus lunatus, 167 Phialophora, 397 Philadelphus, 336 Philocopra coeruleotecta, 201, 231 Phleogena, 279 fagmea, 298 Phleogenaceae, 290, 292, 297-298 Phleospora, 208 Phleinn, 191 pratejjse, 398 Phlyctidiaceae, 64 Phoenix dactylifera, 305 Pholiota, 360 praecox, 281 Pho?na, 208, 390 cichorii, 389 destructiva, 389 herbarimty 388, 389 liiigam, 390, 403 pyrina, 389 richardii, 388, 389, 403 siibcmcta, 225, 226 Phomaceae, 386 Phomales, 39, 386 Phomopsis, 225, 226, 385, 390 dm, 220, 225 jimiperovora, 399 Phragmidieae, 335 Phraginidiinn, 4, 326, 338 americanuni, 321 incrassatimi, 328 potentillae-canadensis, 333 specioswn, 333 siibcorticinufn, 313, 323 violacemn, 316, 332 Phragmosporeae, 387 Phycomyces, 124 77/7^72^, 118, 122, 123, 126, 127, 128 Phycomycetes, 31, 32, 33, 34, 35, 36, 57-136, 140, 383 classification, 61-62 Phycomycetes, origin, 62 repetitional development, 59-60 sexual spores, 60-61 sporangium, 58-59 thallus, 57-58 zoospores, 61 Chytridiales, 63-74 Lagenidiales, 74-77 Biastocladiales, 77-82 Monoblepharidales, 83-88 Leptomitales, 88-91 Saprolegniales, 92-98 Pythiales, 98-105 Albuginales, 105-108 Peronosporales, 108-116 Mucorales, 116-128 Entomophthorales, 128-132 Endogonaceae, 133-134 Eccrinales, 134-136 Phyllachora graminis, 182 Phyllachoraceae, 180, 182 Phyllactijiia, 172 corylea, 173, 114, 175, 176, 179 Phyllosticta, 208, 211, 251, 385, 390 nyssae, 209, 212 phaseolina, 226 solitaria, 390 viridis, 209, 212, 232 Phyllostictales, 39, 386 Phyllostictina, 215, 385, 390 Phy?natotrichii7n omnivonmt, 402 Physalospora, 208, 217, 219 cydoniae, 111, 218, 219 jusca, 111, 218 gossypina, 218 rhodma, 217, 218, 219 Physarales, 35, 45 Physarella niirabilis, 52, 53 Physarum, 52 compressimt, 48 connatitm, 48 leucopiis, 48, 49 polycephalum, 41, 49, 50, 53, 54 serpida, 49 virescens, 49 virjde, 50 Physoderma, 72 zeae-maydis, 10, 71 Physodermataceae, 64 Physopella fici, 324 Phytophthora, 51, 58, 98, 99, 102 c act on 1777, 60 citrophthora, 104 430 SUBJECT INDEX Pbytopbthora iiifestaiis, 8, 60, 102, 104, 105, 115 mcotianae, 104 palviivora, 59, 104 parasitica, 104 phaseoli, 60 Picea, 316 engeliiianni, 346 viorinda, 326 Pichia iJiaiidshuricus, 145 Piersonia alveolata, 273 Piggotia jraxiiii, 111, 111 Pilacre, 279 jaginea, 298, 299 Pileolaria toxicodendri, 324 Pileus, 359 Piline, 176 Pilobolaceae, 124 Pilobohis, 116, 127 crystallimis, 118 oedipiis, 118 Pines, 182, 243, 257, 259, 265, 313, 336, 337, 344, 392 Pimis vionticola, 346 ponderosa, 243 syhestris, 331 virginiana, 3 1 5 Piptocephalidaceae, 124 Piptocepbalis, 59, 139 freseniaua, 116, 222 tiegbemiana^ 116 Piricidaria grisea, 397 orjirae, 397 Pisolitbus, 364, 380 tinctoriiis, 311, 373 Pitbya cupressi, 269, 270 Plasmodiocarp, 46, -^i^ Plasmodiopbora brassicae, 9, 13, 44, 52, 54, 55, 56 Plasmodiophorales, 35, 43-45, 69 Plasmodium, 40, 41, 44, 45, 46 Plasmopara, 110 viticola, 109, 112, 115 Plat aims, 346 occidentalis, 212 Platygloea, 293 Plectania coccinea, 271 Plectascales, 152-162, 200 Plectodiscella piri, 167, 171 veiieta, 167 Plectodiscellaceae, 165, 167 Plectomycetes, 37, 150, 152-179 Plectospira, 95 Pleomorphism, 31 Pleospbaeria citri, 208 Pleospora, 138, 170, 385, 398 Pleosporaceae, 208 Pleurage, 11 anserina, 138, 199, 200, 201, 230 caendeotecta, 199 zygospora, 199, 201, 232 Pleurotus, 211, 353, 356, 357 corticatiis, 283 ostreatus, 23 pinsitiis, 283 Plowrigbtia rnorbosiim, 180, i^i Plum pockets, 146 Plums, 180, 253, 261, 336 Poa, 191, 195 compress a, 334 pratensis, 192 Podaxaceae, 370 Podaxales, 38, 366, 369-372 Podaxis, 370 Podaxon, 370 Podocrea ahitacea, 188 Podospbaera, 111 biiincinata, 176 leiicotricba, 173 oxyacaiitbae, 173, 176 Polygomnn cbinense, 300 viviparimi, 316 Polypbagiis, 61 eiiglenae, 70 Polyporaceae, 4, 22, 50, 341, 347- 352, 5^7 Polyporeae, 348, 349-351 Po/yporz/5 abietiniis, 349 miceps, 23 cinnabarimis, 23, 349 dryopbihis, 23 jarlouoii, 23 niylittiae, 350, 402 obtusiis, 23 pargamenus, 349 perennis, 23 sapiirema, 350, 402 sidpbiireiis, 23, 349 tiiberaster, 402 tiickaboe, 402 versicolor, 349 SUBJECT INDEX 431 Folysphondylmm purpiireiim, 42 Folysticms hirsiitJis, 23 versicolor, 23 Polystigina, 191 nibrinu, 190, 197 Polystomellaceae, 236, 241 Fol'ytbrmchnn trifolii, 183, 184 Pomegranate, 398 Poplar, yellow, 188 Popiihis, 337 deltoides, 222 Pore fungi, 276, 347-352 Porta, 349 cocos, 350, 364, 402, 404 incrassata, 349, 363 ■vapor aria, 349 Porteranthus, 336 Porudaca oleracea, 105 Potato, 45, 67, 261, 292, 398 Pourthiaea, 336 Powdery mildews, 171-176 Privet, 222 Prospodiinn badbavnense, 323 plagiopiis, 323 Prosthecium, 226 Protoachlya, 95 Protocoro770spora, 392 nigricans, 393, 394 Protodontia, 288 Protogaster rhizophihis, 368 Protogastraceae, 368 Protohvdnum, 287 Protomerulius, 288 Protozoa, 62 Prunes, 207 Primus, 394 americaiaa, 253 aviinn, 253 cerasus, 211, 253 dome Stic a, 253 pennsylvanica, 211, 253 per sic a, 111 serotijia, 253 virginiana, 253 Ps alii Ota, 357, 358 campestris, 279, 280, 284, 555, 362 Pseiidococciis calceolariae, 132 Pseudopeziza, 385 viedicaginis, 257, 267 mfo/fi, 257, 267 Pseudopezizoideae, 257 Pseudoplasmodium, 41, 43 Pseitdoplectania nigrella, 269 Pseudosphacriaceac, 163, 169-171, 208 Pseiidotsiiga taxi folia, 259, 346 Pseudovalsa, 226 Psvchotria, 295 Pteridiinn aqiiiliniinn, 337 latins cidinn, 259 Pteris biaiirita, 146 Puccinastreae, 335 Piiccinia, 4 adoxae, 333 antirrhini, 338 as para gi, 337 caricis, 313 chrysanthemi, 324, 338 claytoniata, 319 coronata, 317, 318, 324, 527, 331, 336, 338 dejorvians, 333 dispersa, 315, 336, 340 fraxinata, 323 glinnarmn, 336 ■ grajjiinella, 330 graminis, 309, 570, 314, 317, 318, 323, 52-/, 328, 334, 335, 336, 338, 339, 340 agrostidis, 334 air^e, 334 avenae, 334, 336 poae, 334 secalis, 334, 336 mt/Vz, 334, 336 gri?jdeliae, 318, 327 belianthi, 317, 318, 339 malvaceanmi, 315, 525^, 333, 338 7ji.esneriana, 331 monopora, 323 peckiana, 340 perplexans, 323 poanmi, 323, 333 podopbylli, 324, 321, 331, 341 pringsheimiana, 317, 318 nibigo-vera, 336 senecionis, 321 seymoiiriana, 323 5-orgW, 318, 336, 338 sitbnitens, 337, 338 triticina, 318, 324, 336, 338 verbenicola, 323 vexans, 312 432 SUBJECT INDEX Tuccinia vivipctri, 316 xanthi, 318 Pucciniaceae, 326, 335 Pucciniastrum, 314, 323, 330 Pulfballs, 4, 40, 276, 361, 364-369, 372-377 Fiilvimda coiistellatio, 250 Funic a granatiim, 211 Pure culture, disadvantages of, 14 hanging-drop cultures, 21 Pvcnia, 315-318 Pycnidium, 384, 387-390, 388, 391 Fyronema confiiiens, 138, 246, 248, 268, 270, 271, 272 Pvrenomycetes, 5, 19, 31, 37, 50, 150, 179-245, 257 Dothideales, 180-186 Hvpocreales, 186-198 Sphaeriales, 198-232 Laboulbeniales, 232-236 Hemisphaeriales, 236-241 Hysteriales, 243-245 Fyrenopeziza, 248, 251 medicaginis, 251, 267 Fyreiiophora, 170, 171 tritici-repentis, 165 Pyrus, 336 Fytbiacystis citrophthora, 104 Pythiales, 36, 62, 69, 98-105 Fythio7?iorpha gonapodioides, 59, 60, 104 Pvthiopsis, 58, 93, 94 Fythhmi, 58, 61, 98, 100, 103, 104 aphanidermatiim, 101 de baryamim, 100, 101, 103, 105 diacarpum, 60 echinulatinn, 103 prolijerum, 59, 60 iilt'mmin, 101 Queletia, 373 Querciis, 346 agrijoUa, 111 Questieria, 239 Quince, 336 Radish, 94, 101 Raisins, 145 Rmmdaria, 208, 209, 211, 385, 395 areola, 1\1, 397 Ramularisphaerella, 209 Ranunculaceae, 317, 331, 332 Ranunculus ficaria, 260 Raphanus, 105 Raspberry, 167 Raveneha, 326, 329 cassiaecola, 321 pygmea, 313 volkesjiii, 313 Ravenelia, 326, 329 Relative sexuality, 89, 95 Resistant sporangia, 77 Reticularia lycoperdon, 50 Rhamnus, 324, 331, 336 Rheosporangimn aphajiidermatum, 101, 104 Rhino sp or idhnn seeberi, 143 Rhinotrichum, 298 Rbipidiinn, 88, 89, 91 europaeum, 91 Rhizidiaceae, 58, 64, 69-70, 72 Rhizidiomyces apophysatus, 19, 61, 65, 66 Rhizina inftata, 250, 269 Rhizoclonium, 101 Rhizoctonia bataticola, 403 crocorum, 292, 298, 299 solani, IS, 344, 399, 401 Rhizophidium carpophilum, 19, 66 globosum, 65 vmltiponmi, 19, 66 ovatimi, 69 polli7iis-pini, 69 Rhizopogon, 133, 369 nigrescens, 311 Rhizopus, 4, 118, 124 72igricans, 61, 116, 111, 118, 122, 124, 128 oryzae, 116 sexualis, 121, 122, 127 RhodochytriuTn spilanthidis, 73 Rhododendroji, 263 catawbiense, 341 juaxijnuTn, 341 Rhodophyceae, 139, 235 Rhodosporae, 358 Rhopobata vacciniana, 132 Rhynchophorojnyces rostratus, 234, 235 Rhyparobius, 268, 270 Rhytisma, 257, 385, 392 acerijiuvt, 257, 258, 161 Ribes, 166, 336 grossularia, 116 SUBJECT INDEX 433 Rice, 114, 307, 397, 401 Ricimis covnmmis^ 261 Robergea, 268 Roestelia, 318, 319, 321, 383 caiicellata, 330 Rosaceae, 317 Rosellinia clavariae, 203 qiiercina. 203 Roses, 176, 253, 313, 328, 338, 394 Rotifers, 101 Rozella, 69 Rubus, 212, 313, 391 Russula, 125, 280, 283, 356, 357, 360 Rusts, 276, 279, 281, 283, 291, 295, 309-341, 390 Rutstroemia, 262, 263, 265 Rve, 192, 195, 196, 303, 307, 315, 328, 336, 391 Sabina sabinoides, 231 Saboiiraiidites gypsemn, 162 Saccardiaceae, 163 Saccharomyces cerevisiae, 144, 145 elUpsoideus, 144, 145 viellacei, 145 piriformis, 145 pombe, 145 sake, 145 Saccharomycetaceae, 140 Saccharomycetales, 37, 139, 144-145 Saccoblastia intermedia, 293, 299 Saccoboliis violascens, 248 Sake, 145 Salamanders, 132 Salix, 337 Salsify, 105 Saprolegnia, 57, 58, 61, 69, 93, 94, 97 ferax, 98 monoica, 59, 96 parasitica, 94, 98 Saprolegniales, 19, 22, 36, 60, 61, 62, 69, 89, 92-98, 134, 141 Sapromyces, 88, 89, 91 androgyims, 89, 90 reins chii, 89, 91 Sarcoscypha, 248 Sarcoscvpheae, 268 Scale insects, 128, 163, 178, 188, 191, 292, 295, 296, 297, 392 Schizomycetes, 32 Schizophylhnn commune, 281, 354 Schizosaccharomyces hidwigii, 145 octosporus, 144, 145 Schizoxylon, 268 sepi?7Cola, 268 Schnallenzellen, 281 Scirrhia acicola, 182 Scleroderis abieticola, 266 ribis, 266 Scleroderma, 364, 366 bovista, 372 geaster, 366, 371, 373 Sclerodermataceae, 373, 380 Sclerodermatales, 39, 366, 372-374, 380 Sclerospora, 110 grajninicola, 23, 28, 109, 112, 114, 115, 116 inacrospora, 114 Sclerotia, 191, 192, 193, 195, 260 Sclerotinia, 11, 248, 259-262, 265, 385, 395 cmiericana, 261 cinerea, 261 fnicticola, 261 jriictigena, 261 gladioli, 262, 263, 266 heteroica, 261, 267 ricini, 261 sclerotiorum, 261 trifolionim, 260 7ir7J7da, 260, 261 Sclerotiniaceae, 265 Sclerotium, 391 bataticola, 401 delphinii, 401 oryzae, 401 rolfsii, 25, 401 Scolecosporeae, 387 Scorias spongiosa, 178 Scropliulariaceae, 331, 337 Sebacina, 287, 288 prolifera, 290 Sec ale cereale, 334 Secotiaceae, 370 Secotiimi, 372 agaricoides, 370, 372 Sedges, 332 Senecio, 337 Sepedonium, 194 chrysospermimi, 188 •/i'-/ SUBJECT INDEX Septobasidiaceae, 292, 295-297 Septohasidmj/i, 279, 295 pseiidopedicellatinn, 296 Septonenia, 245 Septoria, 208, 385, 386 apii, 391 aveime, 391 glycines, 399 heliiWthi, 389 lycopersici, 390, 391 nodoriivi, 391 polygonoriim, 388, 389 n/Z^z, 391 scroplmlariae, 389 se calls, 391 tritici, 391 Septoriosphaerella, 209 Septotiniii, 262 podophyllina, 265 Serratia fuarcescens, 42 Sesleria coendea, 196 Set aria viridis, 115 Shot-hole diseases, 253 Shropshiria, 305 S/WtY spinosa, 127 Sivibhivi sphaerocephalimi, 378, 379 Sirobasidiaceae, 287, 290 Sirobasidium, 290 Sirolpidiaceae, 69 Slime flux, 140 Slime molds, 40-56 Smuts, 276, 283, 299-309 Snapdragons, 338 So7Jnnerstorffia, 95 spinosa, 101 Sonchus, 337 Sooty molds, 171, 176-178 Sorbus, 336 Sordariaceae, 198, 200-203 Sorghum, 307 Sorocarp, 41, 42 Sorodiscus, 44, 45 Sorosphaera, 44, 45 veronicae, 53 Sorosporiinn, 306 reiliamim, 308 Soybeans, 189, 220, 226 Sparassis crispa, 346 r ad i cat a, 346, 364 Spartina, 323 Spermogonia, 315-318 Spen7iophthora gossypii, 140, 141, 142 Sphacelia, 187 Spbaceloma, 167, 385, 397 perseae, 167, 171 Sphacelotheca, 301, 306 reiliana, 307 sorghi, 307 Sphaerella nigerristigma, 389 Sphaeria bidwellii, 215 cariceti, 219 Sphaeriaceae, 198, 203, 207 Sphaeriales, 37, 169, 179, 180, 182, 198-232, 243 Chaetomiaceae, 200 Fimetariaceae (Sordariaceae), 200- 203 Sphaeriaceae, 203 Ceratostomataceae, 203-207 Cucurbitariaceae, 207 Amphisphaeriaceae, 207-208 Lophiostomataceae, 208 Alycosphaerellaceae, 208-219 Gnomoniaceae, 219-224 Diaporthaceae, 224-226 Allantosphaeriaceae, 227-228 Xylariaceae, 228-230 Sphaerobolaceae, 373 Sphaeroboliis, 366, 380 ioiveiisis, 373, 374, 382 stellatiis, 373, 374, 382 Sphaerocladia, 81 Sphaeronejiia fimbriata, 205 Sphaeronemella fragariae, 389 Sphaeropsidaceae, 31, 386, 390-392 Sphaeropsidales, 39, 386, 390-392 Sphaeropsis, 219 citric ol a, 389 malorinn, 218, 389 Sphaerosporangium, 100 Sphaerosporeae, 268 Sphaerostilbe, 186 Sphaerotheca, 172, 175, 179 castag7jei, 173 himndi, 112, 176 mors-uvae, 176 paimosa, 176 Sphagnum, 307 Spinacea oleracea, 109, 398 Spinach, 105, 307 Spiraea, 323 Spirobolus ?7iarginatiis, 134 SUBJECT INDEX 435 Spirogyra, 65, 69 Spongospora mbterra?iea, 44, 45, 51, 55 Spontaneous generation, 1, 2, 300 Spores, types of, 32, 34 Sporobolus, 323 Sporodesmium, 245 Sporod'mia, 124 grandis, 118, 121, 122, 123, 125 Sporodochium, 384 Sporone77ia pbacidioides, 251 platani, 222 SpororTfiiii, 199 coendeotecta, 201 SporotricbinJi, 200 globidijerwn, 399 Sporozoa, 45 Squash, 116, 176 Staurosporeae, 387 Stellaria media, 109 Stemonitales, 35, 45 Steinonitis fermginea, 50 jiisca, 50, 52, 53 splendens var. flaccida, 50 Stempbyl'mm botryosimi, 399 Stereimi, 344 jnistidosinn, 345, 351 gmisapanmi, 345 birsiitinn, 282 Sterigmatocystis, 154 Stictidaceae, 268 Stictis, 268 Stigeoclonium, 69 Stiginatea, 255 potentillae. 111 robertiani. 111, 239, 241 Stigmateaceae, 236, 237 Stiginatomyces haeri, 234, 235 Stigmma polymorpba, 111 Stilbaceae, 387, 394, 400 Stilbella, 189 Stilbimi, 283 vidgare, 297, 299 Stinkhorns, 276, 377-380 Stipa, 330 Stomatogene, 176 Strawberries, 253, 255, 394 Streptotbeca, 268 croiiam, 269 Strobilomyces strohilaceus, 352 Stromatinia, 259, 260 Stylina, 305 "Substitute sexuality," 202 Sugar beets, 398 Sugar cane, 354 Sunflower, 317, 337 Swarm cells, 41 Sweet potato, 105, 116, 188, 205 Svcamore, 220, 222 Symphogenous origin, 387, 388 Syiuplociis tinctoria, 341 Syncephalastrum, 119 Syncephalis, 59, 119 Synchytriaceae, 58, 64, 67-68 Syvcbytrhnn, 61 endobiotician, 60, 66, 67, 68, 71, 73 jidgens, 66, 73 vaccina, 61 Synnema, 384 Systrevwia acicola, 182, 184, 185, 392 idjni, 182, 184 Taeniellopsis flexilis, 135 Taka diastase, 395 Tapbrina, 342 aiirea, 149 came a, 148 cerasi, 146 coendescens, 146 coryli, 148, 150 deformans, 26, 149, 141, 148, 149, 150 epipbylla, 149 jobansonii, 148 klebabni, 149 mirabilis, 146 primi, 146 sadebeckii, 149 tosqidnetii, 149, 150 Taphrinales, 37, 139, 140, 146-150 Tapbrinopsis laiirencia, 146, 148 Tar spot, 257 "Target spot," 188 Tea, 222 Telia, 325-328 Teosinte, 71 Terfeziaceae, 152, 161, 274 Testicularia, 302 Tetramyxa, 44 Texas root-rot fungus, 402 Thalictrum, 336 Thamnidiaceae, 124 436 SUBJECT INDEX Tbmnmd'mm, 58 elegans, 118 Thecophora, 301 deforjjhvis, 302, 304 Tbekopsora areolata, 329 Tbelephora fivibriata, 344 terrestris, 344 Thelephoraceae, 22, 291, 341, 343-345 Theotheca, 268 Tbiehi'ia basic ol a, 159, 160, 162 sepedoniinn, 160 terricola, 160 Tbnvistotbeca, 93, 95, 97 clavata, 98 Tbiija occidentalis, 258 Thvriothecia, 236 Tbyronectria, 188 austro-cniiericana, 189 T/7i^ cordata, 211 TiUetia, 301 corona, 307 borrida, 307 /eivV, 307 spbagni, 307 rm/Vi, 300, 302, 505, 305, 307 Tilletiaceae, 302, 305 Titania, 226 Tobacco, 66, 101, 104, 109, 155, 160, 398, 400 Tolvposporella, 306 Tolvposporium, 302 Tomato, 45, 101, 145, 391, 392 Tomentella fiava, 283 gramdata, 283 Trmiietes mnericana, 281 peckii, 23 serialis, 23 Tranzscbelia pnmi-sp'mosae, 323, 52^, 336 Treinella, 288, 290 jiiciforviis, 287 lutescens, 290 viesentertca, 289 inycetopbila, 287 Tremellaceae, 287 Tremellales, 38, 279, 284, 286, 287- 291 Tremellineae, 31 Tremellodendron, 287, 288 Tremellodon, 287 Tricbia florijorviis, 50 Trichiales, 35, 45 Trichocyphella, 259 Trichocyphelloideae, 259 Tricbodernia, IS viride, 399 Tricboglosszmz birsutimi, 250 Tricholoma, 356 Trichopeltaceae, 236, 237 Trichophytoneae, 152 Trichospora, 326 Tricbotbechmi candidinn, 188 Trichothyriaceae, 241 Tricbotbyrhnn sarcinijenim, 241 Tripbragiuhnn idmariae, 323, 333 Triticinn vidgare, 334 Truffles, 4, 133, 161, 272-275 Tsiiga, 346 canadensis, 258, 315 Tuber, 4 aestivimi, 11^ brinnale, 213, 274 dryopbihnn, 274 excavatimi, 274 inagnatinn, 11^ melanosporwn, 11^ nitidwn, 11 ^ Tuberales, 38, 152, 161, 272-275 Tiibercularia, 385 I'ldgaris, 181 Tuberculariaceae, 38, 394, 400-401 Tiibiircinia, 302 trientalis, 300 Tulasnella, 290, 291 Tulasnellaceae, 290 Tulostoma, 279, 373 Tulostomataceae, 373, 374 Tylostoma, 373 campestre, 311 mammoswn, 311 Tympanis pijiastri, 257 Typbida, 391 graviineinn, 392 idaboensis, 392, 404 itoa7ja, 392, 404 Uhniis crassifolia, 210 Unciinda, 111 circinata, 176 clandestina, 175 genicidata, 116 lager stroemiae, 173 SUBJECT INDEX 437 Uncimila necator, 176 salicis, 173 Uiiderivoodia colimi'maris, 269 Uredinales, 30, 38, 262, 278, 282, 292, 309-341, 383 classification, 335 heteroecism, 328-332 important species, 335-338 mycoplasm hypothesis, 333-334 sexuality, 332-333 sori and spore forms, 315-328 speciaUzation, 334-335 Uredinella coccidophaga, 295 spimdosa, 295 Uredinia, 321-324 Uredinopsis, 323, 331 macrosperjna, 337 mirabilis, 324 osimmdae, 111 Uredo, 383 dispersa, 341 linearis, 328 rosae, 328 Urjuda crater iimi, 111 geaster, 268, 269, 270 Urocystis, 302 occidta, 303, 306, 307 Urovzyces, 314, 330 [338 appendictdatiis, 318, 328, 329, 337, caladii, 313, 333, 340 caryophylli7ms, 321, 338 cunninghamiajms, 321, 338 dactylidis, 323 erythronii, 320 fabae, 318, 324, 337 ficariae, 333 levis, 327 poae, 333 scutellatiis, 327 trifolii, 313 trifolii-hybridi, 318 vignae, 318, 338 Uromy cladiimt inaritinmm, 315 notabile, 312, 315 robi?2soni, 315 tepperianwn, 312 Urophlyctis alfalfae, 72, 73 Uropyxis aiiiorphae, 321 Urtica parvi flora, 313 Ustilaginaceae, 278, 302, 305 Ustilaginales, 30, 38, 278, 282, 299- 309 Ustilago, 301, 306 ^i^e/z^e, 300, 302, 307, 308 broviivora, 302, 304, 308 escidenta, 300, 308 grandis, 308 heiifleri, 299 /:)orrfei, 299, 300, 304, 307 /^m, 300, 304, 307, 308 longissijna, 304 7zw^a, 302, 303, 304, 307 olivaceae, 302 panic i-fnmiejitacei, 304 scabiosae, 301, 303 treiibii, 300 mVici, 299, 300, 303, 304, 307 violacea, 300, 304, 50<^, 308 zeae, 26, 299, 300, 302, 303, 304, 505, 307, 308, 309 Vaccijiiiim, 313, 341 idiginosimi, 261, 262 vitis-idaea, 261 "Valley fever," 143 F^/^^, 225 leucosto?7ia, 225, 226 Valsaceae, 227 Van Tieghem cells, 20, 21 Vaucheria, 43 Venturia, 138, 208, 215-217, 385 inaequalis, 215, 2i7, 231 Verbena, 323 Verbenaceae, 331 Vermicularia, 392, 393 Veronica chainaedrys, 53 Verticillitmi, 188, 200 globidigenim, 188 Vetch, 394 Vibrissea, 268 Vicia faba, 50 sativa, 393 sepizim, 109 VigJia sinejisis, 111 Vitis, 211 vinifera, 109 Volatile fungicides, 114-115 Vohitella circi72ans, 389 frz/rf/, 389 Volva, 356 Volvoboletus, 352 438 SUBJECT INDEX Walnut, 188, 220 Watermelon, 222 Wheat, 114, 195, 300, 302, 303, 307, 309, 328, 329, 330, 336, 391, 401 "AMiite rusts," 105, 107 Ulllia anoviala, 144, 145 Witches' broom, 243, 313 Wojnoivicia graviinis, 391, 404 Woronina, 69 Woroninaceae, 64, 66^ 69 Wynnea ciinericana, 269 Xeiwdoclms carbonarius, 321 Xenosporella, 400 Xylaria bypoxylon, 228 mail, 228 Xylaria polymorpha, 228 tentaculata, 228 Xyiariaceae, 199, 228-230 Yeasts, 9, 10, 11, 50, 144-146, 283, 299, 342 2jea mays, 1 1 5 Tjizania latifolia, 300 Zoophagiis, 99 insidians, 101, 105 2.0 St era marina, 43, 55 Zygomycetes, 36, 60, 116-134 'Lygorhynchus, 121 dangeardi, 122 heterogavms, 60, 122 Zythiaceae, 386, 390, 392