[i]

Cambridge Botanical Handbooks

Edited by A. C. Seward and A. G. Tansley

LICHENS

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CAMBRIDGE UNIVERSITY PRESS
C. F. CLAY, Manager
LONDON: FETTER LANE, E.C.4

LONDON: H. K. LEWIS AND CO., Ltd.,
136, Gower Street, W.C.1

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NEW YORK: THE MACMILLAN CO.

TORONTO: THE MACMILLAN CO. OF CANADA, Ltd.

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ALL RIGHTS RESERVED

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LICHENS

BY
ANNIE LORRAIN SMITH, F.L.S.
ACTING ASSISTANT, BOTANICAL DEPARTMENT, BRITISH MUSEUM

CAMBRIDGE:
AT THE UNIVERSITY PRESS
1921

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PRINTED IN GREAT BRITAIN

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PREFACE

The publication of this volume has been delayed owing to war conditions, but the delay is the less to be regretted in that it has allowed the inclusion of recent work on the subject. Much of the subject-matter is of common knowledge to lichenologists, but in the co-ordination and arrangement of the facts the original papers are cited throughout. The method has somewhat burdened the pages with citations, but it is hoped that, as a book of reference, its value has been enhanced thereby. The Glossary includes terms used in lichenology, or those with a special lichenological meaning. The Bibliography refers only to works consulted in the preparation of this volume. To save space, etc., the titles of books and papers quoted in the text are generally translated and curtailed: full citations will be found in the Bibliography. Subject-matter has been omitted from the index: references of importance will be found in the Table of Contents or in the Glossary.

I would record my thanks to those who have generously helped me during the preparation of the volume: to Lady Muriel Percy for taking notes of spore production, and to Dr Cavers for the loan of reprints. Prof. Potter and Dr Somerville Hastings placed at my disposal their photographs of the living plants. Free use has been made of published text-figures which are duly acknowledged.

I have throughout had the inestimable advantage of being able to consult freely the library and herbarium of the British Museum, and have thus been able to verify references to plants as well as to literature. A special debt of gratitude is due to my colleagues Mr Gepp and Mr Ramsbottom for their unfailing assistance and advice.

A. L. S.

London, February, 1920

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CONTENTS

[xix]

GLOSSARY

ERRATA

Transcriber’s Note: The errata have been corrected.

[xxiii]

INTRODUCTION

Lichens are, with few exceptions, perennial aerial plants of somewhat lowly organization. In the form of spreading encrustations, horizontal leafy expansions, of upright strap-shaped fronds or of pendulous filaments, they take possession of the tree-trunks, palings, walls, rocks or even soil that afford them a suitable and stable foothold. The vegetative body, or thallus, which may be extremely long-lived, is of varying colour, white, yellow, brown, grey or black. The great majority of lichens are Ascolichens and reproduction is by ascospores produced in open or closed fruits (apothecia or perithecia) which often differ in colour from the thallus. There are a few Hymenolichens which form basidiospores. Vegetative reproduction by soredia is frequent.

Lichens abound everywhere, from the sea-shore to the tops of high mountains, where indeed the covering of perpetual snow is the only barrier to their advance; but owing to their slow growth and long duration, they are more seriously affected than are the higher plants by chemical or other atmospheric impurities and they are killed out by the smoke of large towns: only a few species are able to persist in somewhat depauperate form in or near the great centres of population or of industry.

The distinguishing feature of lichens is their composite nature: they consist of two distinct and dissimilar organisms, a fungus and an alga, which, in the lichen thallus, are associated in some kind of symbiotic union, each symbiont contributing in varying degree to the common support: it is a more or less unique and not unsuccessful venture in plant-life. The algae—Chlorophyceae or Myxophyceae—that become lichen symbionts or “gonidia” are of simple structure, and, in a free condition, are generally to be found in or near localities that are also the customary habitats of lichens. The fungus is the predominant partner in the alliance as it forms the fruiting bodies. It belongs to the Ascomycetes[1], except in a few tropical lichens (Hymenolichens), in which the fungus is a Basidiomycete. These two types of plants (algae and fungi) belonging severally to many different genera and species have developed in their associated life this new lichen organism, different from themselves as well as from all other plants, not only morphologically but physiologically. Thus there has arisen a distinct class, with families, genera and species, which through all their varying forms retain the characteristics peculiar to lichens.

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In the absence of any “visible” seed, there was much speculation in early days as to the genesis of all the lower plants and many opinions were hazarded as to their origin. Luyken[2], for instance, thought that lichens were compounded of air and moisture. Hornschuch[3] traced their origin to a vegetable infusorium, Monas Lens, which became transformed to green matter and was further developed by the continued action of light and air, not only to lichens, but to algae and mosses, the type of plant finally evolved being determined by the varying atmospheric influences along with the chemical nature of the substratum. An account[4] is published of Nees von Esenbeck, on a botanical excursion, pointing out to his students the green substance, Lepraria botryoides, which covered the lower reaches of walls and rocks, while higher up it assumed the grey lichen hue. This afforded him sufficient proof that the green matter in that dry situation changed to lichens, just as in water it changed to algae. An adverse criticism by Dillenius[5] on a description of a lichen fructification is not inappropriate to those early theorists: “Ex quo apparet, quantum videre possint homines, si imaginatione polleant.”

A constant subject of speculation and of controversy was the origin of the green cells, so dissimilar to the general texture of the thallus. It was thought finally to have been established beyond dispute that they were formed directly from the colourless hyphae and, as a corollary, Protococcus and other algal cells living in the open were considered to be escaped gonidia or, as Wallroth[6] termed them, “unfortunate brood-cells,” his view being that they were the reproductive organs of the lichen plant that had failed to develop.

It was a step forward in the right direction when lichens were regarded as transformed algae, among others by Agardh[7], who believed that he had followed the change from Nostoc lichenoides to the lichen Collema limosum. Thenceforward their double resemblance, on the one hand to algae, on the other to fungi, was acknowledged, and influenced strongly the trend of study and investigation.

The announcement[8] by Schwendener[9] of the dual hypothesis solved the problem for most students, though the relation between the two symbionts is still a subject of controversy. The explanation given by Schwendener, and still held by some[10], that lichens were merely fungi parasitic on algae, was indeed a very inadequate conception of the lichen plant, and it was hotly contested by various lichenologists. Lauder Lindsay[11] dismissed the theory as “merely the most recent instance of German transcendentalism applied[xxv] to the Lichens.” Earlier still, Nylander[12], in a paper dealing with cephalodia and their peculiar gonidia, had denounced it: “Locum sic suum dignum occupat algolichenomachia inter historias ridiculas, quae hodie haud paucae circa lichenes, majore imaginatione quam scientia, enarrantur.” He never changed his attitude and Crombie[13], wholly agreeing with his estimate of these “absurd tales,” translates a much later pronouncement by him[14]: “All these allegations belong to inept Schwendenerism and scarcely deserve even to be reviewed or castigated so puerile are they—the offspring of inexperience and of a light imagination. No true science there.” Crombie[15] himself in a first paper on this subject declared that “the new theory would necessitate their degradation from the position they have so long held as an independent class.” He scornfully rejected the whole subject as “a Romance of Lichenology, or the unnatural union between a captive Algal damsel and a tyrant Fungal master.” The nearest approach to any concession on the algal question occurs in a translation by Crombie[16] of one of Nylander’s papers. It is stated there that a saxicolous alga (Gongrosira Kütz.) had been found bearing the apothecia of Lecidea herbidula n. sp. Nylander adds: “This algological genus is one which readily passes into lichens.” At a later date, Crombie[17] was even more comprehensively contemptuous and wrote: “whether viewed anatomically or biologically, analytically or synthetically, it is instead of being true science, only the Romance of Lichenology.” These views were shared by many continental lichenologists and were indeed, as already stated, justified to a considerable extent: it was impossible to regard such a large and distinctive class of plants as merely fungi parasitic on the lower algae.

Controversy about lichens never dies down, and that view of their parasitic nature has been freshly promulgated among others by the American lichenologist Bruce Fink[18]. The genetic origin of the gonidia has also been restated by Elfving[19]: the various theories and views are discussed fully in the chapter on the lichen plant.

Much of the interest in lichens has centred round their symbiotic growth. No theory of simple parasitism can explain the association of the two plants: if one of the symbionts is withdrawn—either fungus or alga—the lichen as such ceases to exist. Together they form a healthy unit capable of development and change: a basis for progress along new lines. Permanent characters have been formed which are transmitted just as in other units of organic life.

A new view of the association has been advanced by F. and Mme Moreau[20]. They hold that the most characteristic lichen structures—more particularly[xxvi] the cortex—have been induced by the action of the alga on the fungus. The larger part of the thallus might therefore be regarded as equivalent to a gall: “it is a cecidium, an algal cecidium, a generalized biomorphogenesis.”

The morphological characters of lichens are of exceptional interest, conditioned as they are by the interaction of the two symbionts, and new structures have been evolved by the fungus which provides the general tissue system. Lichens are plants of physiological symbiotic origin, and that aspect of their life-history has been steadily kept in view in this work. There are many new requirements which have had to be met by the lichen hyphae, and the differences between them and the true fungal hyphae have been considered, as these are manifested in the internal economy of the compound plant, and in its reaction to external influences such as light, heat, moisture, etc.

The pioneers of botanical science were of necessity occupied almost exclusively with collecting and describing plants. As the number of known lichens gradually accumulated, affinities were recognized and more or less successful efforts were made to tabulate them in classes, orders, etc. It was a marvellous power of observation that enabled the early workers to arrange the first schemes of classification. Increasing knowledge aided by improved microscopes has necessitated changes, but the old fundamental “genus” Lichen is practically equivalent to the Class Lichenes.

The study of lichens has been a slow and gradual process, with a continual conflict of opinion as to the meaning of these puzzling plants—their structure, reproduction, manner of subsistence and classification as well as their relation to other plants. It has been found desirable to treat these different subjects from a historical aspect, as only thus can a true understanding be gained, or a true judgment formed as to the present condition of the science. It is the story of the evolution of lichenology as well as of lichens that has yielded so much of interest and importance.

The lichenologist may claim several advantages in the study of his subject: the abundant material almost everywhere to hand in country districts, the ease with which the plants are preserved, and, not least, the interest excited by the changes and variations induced by growth conditions; there are a whole series of problems and puzzles barely touched on as yet that are waiting to be solved.

In field work, it is important to note accurately and carefully the nature of the substratum as well as the locality. Crustaceous species should be gathered if possible along with part of the wood or rock to which they are attached; if they are scraped off, the pieces may be reassembled on gummed paper, but that is less satisfactory. The larger forms are more easily secured;[xxvii] they should be damped and then pressed before being laid away: the process flattens them, but it saves them from the risk of being crushed and broken, as when dry they are somewhat brittle. Moistening with water will largely restore their original form. All parts of the lichen, both thallus and fruit, can be examined with ease at any time as they do not sensibly alter in the herbarium, though they lose to some extent their colouring: the blue-grey forms, for instance, often become a uniform dingy brownish-grey.

Microscopic examination in the determination of species is necessary in many instances, but that disability—if it ranks as such—is shared by other cryptogams, and may possibly be considered an inducement rather than a deterrent to the study of lichens. For temporary examination of microscopic preparations, the normal condition is best observed by mounting them in water. If the plants are old and dry, the addition of a drop or two of potash—or ammonia—solution is often helpful in clearing the membranes of the cells and in restoring the shrivelled spores and paraphyses to their natural forms and dimensions.

If serial microtome sections are desired, more elaborate methods are required. For this purpose Peirce[21] has recommended that “when dealing with plants that are dry but still alive, the material should be thoroughly wetted and kept moist for two days, then killed and fixed in a saturated solution of corrosive sublimate in thirty-five per cent. alcohol.” The solution should be used hot: the usual methods of dehydrating and embedding in paraffin are then employed with extra precautions on account of the extremely brittle nature of lichens.

Another method that also gave good results has been proposed by French[22]: “first the lichen is put into 95 per cent. alcohol for 24 hours, then into thin celloidin and thick celloidin 24 hours each. After this the specimens are embedded in thick celloidin which is hardened in 70 per cent. alcohol for 24 hours and then cut.” French advises staining with borax carmine: it colours the fungal part pale carmine and the algal cells a greenish-red shade.

Modern research methods of work are generally described in full in the publications that are discussed in the following chapters. The student is referred to these original papers for information as to fixing, embedding, staining, etc.

Great use has been made of reagents in determining lichen species. They are extremely helpful and often give the clinching decision when morphological characters are obscure, especially if the plant has been much altered by the environment. It must be borne in mind, however, that a[xxviii] species is a morphological rather than a physiological unit, and it is not the structures but the cell-products that are affected by reagents. Those most commonly in use are saturated solutions of potash and of bleaching-powder (calcium hypochlorite). The former is cited in text-books as KOH or simply as K, the latter as CaCl or C. The C solution deteriorates quickly and must, therefore, be frequently renewed to produce the required reaction, i.e. some change of colour. These two reagents are used singly or, if conjointly, K followed by C. The significance of the colour changes has been considered in the discussion on lichen-acids.

Iodine is generally cited in connection with its staining effect on the hymenium of the fruit; the blue colour produced is, however, more general than was at one time supposed and is not peculiar to lichens; the asci of many fungi react similarly though to a less extent. The medullary hyphae in certain species also stain blue with iodine.

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CHAPTER I
HISTORY OF LICHENOLOGY

A. Introductory

The term “lichen” is a word of Greek origin used by Theophrastus in his History of Plants to signify a superficial growth on the bark of olive-trees. The name was given in the early days of botanical study not to lichens, as we understand them, but to hepatics of the Marchantia type. Lichens themselves were generally described along with various other somewhat similar plants as “Muscus” (Moss) by the older writers, and more definitely as “Musco-fungus” by Morison[23]. In a botanical work published in 1700 by Tournefort[24] all the members of the vegetable kingdom then known were for the first time classified in genera, and the genus Lichen was reserved for the plants that have been so designated since that time, though Dillenius[25] in his works preferred the adjectival name Lichenoides.

A painstaking historical account of lichens up to the beginning of modern lichenology has been written by Krempelhuber[26], a German lichenologist. He has grouped the data compiled by him into a series of Periods, each one marked by some great advance in knowledge of the subject, though, as we shall see, the advance from period to period has been continuous and gradual. While following generally on the lines laid down by Krempelhuber, it will be possible to cite only the more prominent writers and it will be of much interest to British readers to note especially the work of our own botanists.

Krempelhuber’s periods are as follows:

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A seventh period which includes modern lichenology, and which dates after the publication of Krempelhuber’s History, was ushered in by Schwendener’s announcement in 1867 of the hypothesis as to the dual nature of the lichen thallus. Schwendener’s theory gave a new impulse to the study of lichens and strongly influenced all succeeding investigations.

B. Period I. Previous to 1694

Our examination of lichen literature takes us back to Theophrastus, the disciple of Plato and Aristotle, who lived from 371 to 284 B.C., and who wrote a History of Plants, one of the earliest known treatises on Botany. Among the plants described by Theophrastus, there are evidently two lichens, one of which is either an Usnea or an Alectoria, and the other certainly Roccella tinctoria, the last-named an important economic plant likely to be well known for its valuable dyeing properties. The same or somewhat similar lichens are also probably alluded to by the Greek physician Dioscorides, in his work on Materia Medica, A.D. 68. About the same time Pliny the elder, who was a soldier and traveller as well as a voluminous writer, mentions them in his Natural History which was completed in 77 A.D.

During the centuries that followed, there was little study of Natural History, and, in any case, lichens were then and for a long time after considered to be of too little economic value to receive much attention.

In the sixteenth century there was a great awakening of scientific interest all over Europe, and, after the printing-press had come into general use, a number of books bearing on Botany were published. It will be necessary to chronicle only those that made distinct contributions to the knowledge of lichens.

The study of plants was at first entirely from a medical standpoint and one of the first works, and the first book on Natural History, printed in England, was the Grete Herball[27]. It was translated from a French work, Hortus sanitatis, and published by Peter Treveris in Southwark. One of the herbs recommended for various ailments is “Muscus arborum,” the tree-moss (Usnea). A somewhat crude figure accompanies the text.

Ruel[28] of Soissons in France, Dorstenius[29], Camerarius[30] and Tabernaemontanus[31] in Germany followed with works on medical or economic botany and they described, in addition to the tree-moss, several species of reputed value in the art of healing now known as Sticta (Lobaria) pulmonaria, Lobaria laetevirens, Cladonia pyxidata, Evernia prunastri and Cetraria islandica. Meanwhile L’Obel[32], a Fleming, who spent the latter part of his life in England and is said to have had charge of a physic garden at[3] Hackney, was appointed botanist to James I. He published at Antwerp a large series of engravings of plants, and added a species of Ramalina to the growing list of recognized lichens. Dodoens[33], also a Fleming, records not only the Usnea of trees, but a smaller and more slender black form which is easily identifiable as Alectoria jubata. He also figures Lichen pulmonaria and gives the recipe for its use.

The best-known botanical book published at that time, however, is the Herball of John Gerard[34] of London, Master in Chirurgerie, who had a garden in Holborn. He recommends as medicinally valuable not only Usnea, but also Cladonia pyxidata, for which he coined the name “cuppe- or chalice-moss.” About the same time Schwenckfeld[35] recorded, among plants discovered by him in Silesia, lichens now familiar as Alectoria jubata, Cladonia rangiferina and a species of Peltigera.

Among the more important botanical writers of the seventeenth century may be cited Colonna[36] and Bauhin[37]. The former, an Italian, contributes, in his Ecphrasis, descriptions and figures of three additional species easily recognized as Physcia ciliaris, Xanthoria parietina and Ramalina calicaris. Kaspar Bauhin, a professor in Basle, who was one of the most advanced of the older botanists, was the first to use a binomial nomenclature for some of his plants. He gives a list in his Pinax of the lichens with which he was acquainted, one of them, Cladonia fimbriata, being a new plant.

John Parkinson’s[38] Herball is well known to English students; he adds one new species for England, Lobaria pulmonaria, already recorded on the Continent. Parkinson was an apothecary in London and held the office of the King’s Herbarist; his garden was situated in Long Acre. How’s[39] Phytographia is notable as being the first account of British plants compiled without reference to their healing properties. Five of the plants described by him are lichen species: “Lichen arborum sive pulmonaria” (Lobaria pulmonaria), “Lichen petraeus tinctorius” (Roccella), “Muscus arboreus” (Usnea), “Corallina montana” (Cladonia rangiferina) and “Muscus pixoides” (Cladonia). Several other British species were added by Merrett[40], who records in his Pinax, “Muscus arboreus umbilicatus” (Physcia ciliaris), “Muscus aureus tenuissimus” (Teloschistes flavicans), “Muscus caule rigido” (Alectoria) and “Lichen petraeus purpureus” (Parmelia omphalodes), the last-named, a rock lichen, being used, he tells us, for dyeing in Lancashire.

Merret or Merrett was librarian to the Royal College of Physicians. His Pinax was undertaken to replace How’s Phytographia published sixteen years previously and then already out of print. Merrett’s work was issued in 1666, but the first impression was destroyed in the great fire of London and most of the copies now extant are dated 1667. He arranged[4] the species of plants in alphabetical order, but as the work was not critical it fell into disuse, being superseded by John Ray’s Catalogus and Synopsis. To Robert Plot[41] we owe the earliest record of Cladonia coccifera which had hitherto escaped notice; it was described and figured as a new and rare plant in the Natural History of Staffordshire[41]. Plot was the first Custos of Ashmole’s Museum in Oxford and he was also the first to prepare a County Natural History.

The greatest advance during this first period was made by Robert Morison[42], a Scotsman from Aberdeen. He studied medicine at Angers in France, superintended the Duke of Orleans’ garden at Blois, and finally, after his return to this country in 1669, became Keeper of the botanic garden at Oxford. In the third volume of his great work[42] on Oxford plants, which was not issued till after his death, the lichens are put in a separate group—“Musco-fungus”—and classified with some other plants under “Plantae Heteroclitae.” The publication of the volume projects into the next historical period.

Long before this date John Ray had begun to study and publish books on Botany. His Catalogue of English Plants[43] is considered to have commenced a new era in the study of the science. The Catalogue was followed by the History of Plants[44], and later by a Synopsis of British Plants[45], and in all of these books lichens find a place. Two editions of the Synopsis appeared during Ray’s lifetime, and to the second there is added an Appendix contributed by Samuel Doody which is entirely devoted to Cryptogamic plants, including not a few lichens—still called “Mosses”—discovered for the first time. Doody, himself an apothecary, took charge of the garden of the Apothecaries’ Society at Chelsea, but his chief interest was Cryptogamic Botany, a branch of the subject but little regarded before his day. Pulteney wrote of him as the “Dillenius of his time.”

Among Doody’s associates were the Rev. Adam Buddle, James Petiver and William Sherard. Buddle was primarily a collector and his herbarium is incorporated in the Sloane Herbarium at the British Museum. It contains lichens from all parts of the world, many of them contributed by Doody, Sherard and Petiver. Only a few of them bear British localities: several are from Hampstead where Buddle had a church.

The Society of Apothecaries had been founded in 1617 and the members acquired land on the river-front at Chelsea, which was extended later and made into a Physick Garden. James Petiver[46] was one of the first Demonstrators of Plants to the Society in connection with the garden, and one of his duties was to conduct the annual herborizing tours of the apprentices in search of plants. He thus collected a large herbarium on the annual excursions, as well as on shorter visits to the more immediate[5] neighbourhood of London. He wrote many tracts on Natural History subjects, and in these some lichens are included. He was one of the best known of Ray’s correspondents, and owing to his connection with the Physic Garden received plants from naturalists in foreign countries.

Sherard, another of Doody’s friends, had studied abroad under Tournefort and was full of enthusiasm for Natural Science. It was he who brought Dillenius to England and finally nominated him for the position of the first Sherardian Professor of Botany at Oxford. Another well-known contemporary botanist was Leonard Plukenet[47] who had a botanical garden at Old Palace Yard, Westminster. He wrote several botanical works in which lichens are included.

Morison is the only one of all the botanists of the time who recognized lichens as a group distinct from mosses, algae or liverworts, and even he had very vague ideas as to their development. Malpighi[48] had noted the presence of soredia on the thallus of some species, and regarded them as seeds. Porta[49], a Neapolitan, has been quoted by Krempelhuber as probably the first to discover and place on record the direct growth of lichen fronds from green matter on the trunks of trees.

C. Period II. 1694-1729

The second Period is ushered in with the publication of a French work, Les Élémens de Botanique by Tournefort[50], who was one of the greatest botanists of the time. His object was—“to facilitate the knowledge of plants and to disentangle a science which had been neglected because it was found to be full of confusion and obscurity.” Up to this date all plants were classified or listed as individual species. It was Tournefort who first arranged them in groups which he designated “genera” and he gave a careful diagnosis of each genus.

Les Élémens was successful enough to warrant the publication a few years later of a larger Latin edition entitled Institutiones[51] and thus fitted for a wider circulation. Under the genus Lichen, he included plants “lacking flowers but with a true cup-shaped shallow fruit, with very minute pollen or seed which appeared to be subrotund under the microscope.” Not only the description but the figures prove that he was dealing with ascospores and not merely soredia, though under Lichen along with true members of the “genus” he has placed a Marchantia, the moss Splachnum and a fern. A few lichens were placed by him in another genus Coralloides.

Tournefort’s system was of great service in promoting the study of Botany: his method of classification was at once adopted by the German writer Rupp[52] who published a Flora of plants from Jena. Among these[6] plants are included twenty-five species of lichens, several of which he considered new discoveries, no fewer than five being some form of Lichen gelatinosus (Collema). Buxbaum[53], in his enumeration of plants from Halle, finds place for forty-nine lichen species, with, in addition, eleven species of Coralloides; and Vaillant[54] in listing the plants that grew in the neighbourhood of Paris gives thirty-three species for the genus Lichen of which a large number are figured, among them species of Ramalina, Parmelia, Cladonia, etc.

In England, however, Dillenius[55], who at this time brought out a third edition of Ray’s Synopsis and some years later his own Historia Muscorum, still described most of his lichens as “Lichenoides” or “Coralloides”; and no other work of note was published in our country until after the Linnaean system of classification and of nomenclature was introduced.

D. Period III. 1729-1780

Lichens were henceforth regarded as a distinct genus or section of plants. Micheli[56], an Italian botanist, Keeper of the Grand Duke’s Gardens in Florence, realized the desirability of still further delimitation, and he broke up Tournefort’s large comprehensive genera into numerical Orders. In the genus Lichen, he found occasion for 38 of these Orders, determined mainly by the character of the thallus, and the position on it of apothecia and soredia. He enumerates the species, many of them new discoveries, though not all of them recognizable now. His great work on Plants is enriched by a series of beautiful figures. It was published in 1729 and marks the beginning of a new Period—a new outlook on botanical science. Micheli regarded the apothecia of lichens as “floral receptacles,” and the soredia as the seed, because he had himself followed the development of lichen fronds from soredia.

The next writer of distinction is the afore-mentioned Dillen or Dillenius. He was a native of Darmstadt and began his scientific career in the University of Giessen. His first published work[57] was an account of plants that were to be found near Giessen in the different months of the year. Mosses and lichens he has assigned to December and January. Sherard induced him to come to England in 1721, and at first engaged his services in arranging the large collections of plants which he, Sherard, had brought from Smyrna or acquired from other sources.

Three years after his arrival Dillenius had prepared the third edition of Ray’s Synopsis for the press, but without putting his name on the title-page[58]. Sherard explained, in a letter to Dr Richardson of Bierly in Yorkshire, that “our people can’t agree about an editor, they are unwilling a foreigner should[7] put his name to it.” Dillenius, who was quite aware of the prejudice against aliens, himself writes also to Dr Richardson: “there being some apprehension (me being a foreigner) of making natives uneasy if I should publicate it in my name.” Lichens were already engaging his attention, and descriptions of 91 species were added to Ray’s work. So well did this edition meet the requirements of the age, that the Synopsis remained the text-book of British Botany until the publication of Hudson’s Flora Anglica in 1762.

William Sherard died in 1728. He left his books and plates to the University of Oxford with a sum of money to endow a Professorship of Botany. In his will he had nominated Dr Dillenius for the post. The great German botanist was accordingly appointed and became the first Sherardian Professor of Botany, though he did not remove to Oxford till 1734. The following years were devoted by him to the preparation of Historia Muscorum, which was finally published in 1741. It includes an account of the then known liverworts, mosses and lichens. The latter—still considered by Dillenius as belonging to mosses—were grouped under three genera, Usnea, Coralloides and Lichenoides. The descriptions and figures are excellent, and his notes on occasional lichen characteristics and on localities are full of interest. His lichen herbarium, which still exists at Oxford, mounted with the utmost care and neatness, has been critically examined by Nylander and Crombie[59] and many of the species identified.

Dillenius was ignorant of, or rejected, Micheli’s method of classification, adopting instead the form of the thallus as a guide to relationship. He also differed from him in his views as to propagation, regarding the soredia as the pollen of the lichen, and the apothecia as the seed-vessels, or even in certain cases as young plants.

Shortly after the publication of Dillenius’ Historia, appeared Haller’s[60] Systematic and Descriptive list of plants indigenous to Switzerland. The lichens are described as without visible leaves or stamens but with “corpuscula” instead of flowers and leaves. He arranged his lichen species, 160 in all, under seven different Orders: 1. “Lichenes Corniculati and Pyxidati”; 2. “L. Coralloidei”; 3. “L. Fruticosi”; 4. “L. Pulmonarii”; 5. “L. Crustacei” (with flower-shields); 6. “L. Scutellis” (with shields but with little or no thallus); and 7. “L. Crustacei” (without shields).

This period extends till near the end of the eighteenth century, and thus includes within its scope the foundation of the binomial system of naming plants established by Linnaeus[61]. The renowned Swedish botanist rather scorned lichens as “rustici pauperrimi,” happily translated by Schneider[62] as the “poor trash of vegetation,” but he named and listed about 80 species. He divided his solitary genus Lichen into sections: 1. “Leprosi tuberculati”; 2. “Leprosi scutellati”; 3. “Imbricati”; 4. “Foliacei”;[8] 5. “Coriacei”; 6. “Scyphiferi”; 7. “Filamentosi.” By this ordered sequence Linnaeus showed his appreciation of development, beginning, as he does, with the leprose crustaceous thallus and continuing up to the most highly organized filamentous forms. He and his followers still included the genus Lichen among Algae.

A voluminous History of Plants had been published in 1751 by Sir John Hill[63], the first superintendent to be appointed to the Royal Gardens, Kew. In the History lichens are included under the Class “Mosses,” and are divided into several vaguely limited “genera”—Usnea, tree mosses, consisting of filaments only; Platysma, flat branched tree mosses, such as lung-wort; Cladonia, the orchil and coralline mosses, such as Cladonia furcata; Pyxidium, the cup-mosses; and Placodium, the crustaceous, friable or gelatinous forms. A number of plants are somewhat obscurely described under each genus. Not only were these new Lichen genera suggested by him, but among his plants are such binomials as Usnea compressa, Platysma corniculatum, Cladonia furcata and Cladonia tophacea; other lichens are trinomial or are indicated, in the way then customary, by a whole sentence. Hill’s studies embraced a wide variety of subjects; he had flashes of insight, but not enough concentration to make an effective application of his ideas. In his Flora Britannica[64], which was compiled after the publication of Linnaeus’s Species Plantarum, he abandoned his own arrangement in favour of the one introduced by Linnaeus and accepted again the single genus Lichen.

Sir William Watson[65], a London apothecary and physician of scientific repute at this period, proposed a rearrangement and some alteration of Linnaeus’s sections. He had failed to grasp the principle of development, but he gives a good general account of the various groups. Watson was the progenitor of those who decry the makers and multipliers of species. So in regard to Micheli, who had increased the number to “298,” he writes: “it is to be regretted, that so indefatigable an author, one whose genius particularly led him to scrutinize the minuter subjects of the science, should have been so solicitous to increase the number of species under all his genera: an error this, which tends to great confusion and embarrassment, and must retard the progress and real improvement of the botanic science.” Linnaeus however in redressing the balance earned his full approbation: “He has so far retrenched the genus (Lichen) that in his general enumeration of plants he recounts only 80 species belonging to it.”

Linnaeus’s binomial system was almost at once adopted by the whole botanical world and the discovery and tabulation of lichens as well as of other plants proceeded apace. Scopoli’s[66] Flora Carniolica, for instance, published in 1760, still adhered to the old descriptive method of nomenclature,[9] but a second edition, issued twelve years later, is based on the new system: it includes 54 lichen species.

About this time Adanson[67] proposed a new classification of plants, dividing them into families, and these again into sections and genera. He transferred the lichens to the Family “Fungi,” and one of his sections contains a number of lichen genera, the names of these being culled from previous workers, Dillenius, Hill, etc. A few new ones are added by himself, and one of them, Graphis, still ranks as a good genus.

In England, Hudson[68], who was an apothecary and became sub-librarian of the British Museum, followed Linnaeus both in the first and later editions of the Flora Anglica. He records 102 lichen species. Withering[69] was also engaged, about this time, in compiling his Arrangement of Plants. He translated Linnaeus’s term “Algae” into the English word “Thongs,” the lichens being designated as “Cupthongs.” In later editions, he simply classifies lichens as such. Lightfoot[70], whose descriptive and economic notes are full of interest, records 103 lichens in the Flora Scotica, and Dickson[71] shortly after published a number of species from Scotland, some of them hitherto undescribed. Dickson was a nurseryman who settled in London, and his avocations kept him in touch with plant-lovers and with travellers in many lands.

E. Period IV. 1780-1803

The inevitable next advance was made by Weber[72] who at the time was a Professor at Kiel. In a first work dealing with lichens he had followed Linnaeus; then he published a new method of classification in which the lichens are considered as an independent Order of Cryptogamia, and that Order, called “Aspidoferae,” he subdivided into genera. His ideas had been partly anticipated by Hill and by Adanson, but the work of Weber indicates a more correct view of the nature of lichens. He established eight fairly well-marked genera, viz. Verrucaria, Tubercularia, Sphaerocephalum and Placodium, which were based on fruit-characters, the thallus being crustaceous and rather insignificant, and a second group Lichen, Collema, Cladonia and Usnea, in which the thallus ranked first in importance. Though Weber’s scheme was published in 1780, it did not at first secure much attention. The great authority of Linnaeus dominated so strongly the botany of the period that for a long time no change was welcomed or even tolerated.

In our own country Relhan at Cambridge and Sibthorp[73] at Oxford were making extensive studies of plants. The latter was content to follow Linnaeus in his treatment of lichens. Relhan[74] also grouped his lichens under one genus though, in a second edition of his Flora, he broke away from the Linnaean tradition and adopted the classification of Acharius.

[10]

Extensive contributions to the knowledge of English plants generally were made by Sir James Edward Smith[75] who, in 1788, founded the Linnean Society of London of which he was President until his death in 1828. He began his great work, English Botany, in 1790 with James Sowerby as artist. Smith’s and Sowerby’s part of the work came to an end in 1814; but a supplement was begun in 1831 by Hooker who had the assistance of Sowerby’s sons in preparing the drawings. Nearly all the lichens recorded by Smith are published simply as Lichen, and his Botany thus belongs to the period under discussion, though in time it stretches far beyond.

Continental lichenologists had been more receptive to new ideas, and other genera were gradually added to Weber’s list, notably by Hoffmann[76] and Persoon[77].

For a long time little was known of the lichens of other than European countries. Buxbaum[78] in the East, Petiver[79] and Hans Sloane[80] in the West made the first exotic records. The latter notes how frequently lichens grew on the imported Jesuit’s bark, and he quaintly suggests in regard to some of these species that they may be identical with the “hyssop that springeth out of the wall.” It was not however till towards the end of the eighteenth century that much attention was given to foreign lichens, when Swartz[81] in the West Indies and Desfontaines[82] in N. Africa collected and recorded a fair number. Swartz describes about twenty species collected on his journey through the West Indian Islands (1783-87).

Interest was also growing in other aspects of lichenology. Georgi[83], a Russian Professor, was the first to make a chemical analysis of lichens. He experimented on some of the larger forms and extracted and examined the mucilaginous contents of Ramalina farinacea, Platysma glaucum, Lobaria pulmonaria, etc., which he collected from birch and pine trees. About this time also the French scientists Willomet[84], Amoreux and Hoffmann jointly published theses setting forth the economic value of such lichens as were used in the arts, as food, or as medicine.

F. Period V. 1803-1846

The fine constructive work of Acharius appropriately begins a new era in the history of lichenology. Previous writers had indeed included lichens in their survey of plants, but always as a somewhat side issue. Acharius made them a subject of special study, and by his scientific system of classification raised them to the rank of the other great classes of plants.

Acharius was a country doctor at Wadstena on Lake Mälar in Sweden, as he himself calls it, “the country of lichens.” He was attracted to the[11] study of them by their singular mode of growth and organization, both of thallus and reproductive organs, for which reason he finally judged that lichens should be considered as a distinct Order of Cryptogamia.

In his first tentative work[85] he had followed his great compatriot Linnaeus, classifying all the species known to him under the one genus Lichen, though he had progressed so far as to divide the unwieldy Genus into Families and these again into Tribes, these latter having each a tribal designation such as Verrucaria, Opegrapha, etc. He established in all twenty-eight tribes which, at a later stage, he transformed into genera after the example of Weber.

Acharius, from the beginning of his work, had allowed great importance to the structure of the apothecia as a diagnostic character though scarcely recognizing them as true fruits. He gave expression to his more mature views first in the Methodus Lichenum[86], then subsequently in the larger Lichenographia Universalia[87]. In the latter work there are forty-one genera arranged under different divisions; the species are given short and succinct descriptions, with habitat, locality and synonymy. No material alteration was made in the Synopsis Lichenum[88], a more condensed work which he published a few years later.

The Cryptogamia are divided by Acharius into six “Families,” one of which, “Lichenes,” is distinguished, he finds, by two methods of propagation: by propagula (soredia) and by spores produced in apothecia. He divides the family into classes characterized solely by fruit characters, and these again into orders, genera and species, of which diagnoses are given. With fuller knowledge many changes and rearrangements have been found necessary in the application and extension of the system, but that in no way detracts from the value of the work as a whole.

In addition to founding a scientific classification, Acharius invented a terminology for the structures peculiar to lichens. We owe to him the names and descriptions of “thallus,” “podetium,” “apothecium,” “perithecium,” “soredium,” “cyphella” and “cephalodium,” the last word however with a different meaning from the one now given to it. He proposed several others, some of which are redundant or have fallen into disuse, but many of his terms as we see have stood the test of time and have been found of service in allied branches of botany.

Lichens were studied with great zest by the men of that day. Hue[89] recalls a rather startling incident in this connection: Wahlberg, it is said, had informed Dufour that he had sent a large collection of lichens from Spain to Acharius who was so excited on receiving them, that he fell ill and died in a few days (Aug. 14th, 1819). Dufour, however, had added the comment that the illness and death might after all be merely a coincidence.

[12]

Among contemporary botanists, we find that De Candolle[90] in the volume he contributed to Lamarck’s French Flora, quotes only from the earlier work of Acharius. He had probably not then seen the Methodus, as he uses none of the new terms; the lichens of the volume are arranged under genera which are based more or less on the position of the apothecia on the thallus. Flörke[91], the next writer of consequence, frankly accepts the terminology and the new view of classification, though differing on some minor points.

Two lists of lichens, neither of particular note, were published at this time in our country: one by Hugh Davies[92] for Wales, which adheres to the Linnaean system, and the other by Forster[93] of lichens round Tonbridge. Though Forster adopts the genera of Acharius, he includes lichens among algae. A more important publication was S. F. Gray’s[94] Natural Arrangement of British Plants. Gray, who was a druggist in Walsall and afterwards a lecturer on botany in London, was only nominally[95] the author, as it was mainly the work of his son John Edward Gray[96], sometime Keeper of Zoology in the British Museum. Gray was the first to apply the principles of the Natural System of classification to British plants, but the work was opposed by British botanists of his day. The years following the French Revolution and the Napoleonic wars were full of bitter feeling and of prejudice, and anything emanating, as did the Natural System, from France was rejected as unworthy of consideration.

In the Natural Arrangement, Gray followed Acharius in his treatment of lichens; but whereas Acharius, though here and there confusing fungus species with lichens, had been clear-sighted enough to avoid all intermixture of fungus genera, with the exception of one only, the sterile genus Rhizomorpha, Gray had allowed the interpolation of several, such as Hysterium, Xylaria, Hypoxylon, etc. He had also raised many of Acharius’s subgenera and divisions to the rank of genera, thus largely increasing their number. This oversplitting of well-defined genera has somewhat weakened Gray’s work and he has not received from later writers the attention he deserves.

The lichens of Hooker’s[97] Flora Scotica, which is synchronous with Gray’s work, number 195 species, an increase of about 90 for Scotland since the publication of Lightfoot’s Flora more than 40 years before. Hooker also followed Acharius in his classification of lichens both in the Flora Scotica and in the Supplement to English Botany[98], which was undertaken by the younger Sowerbys and himself. To that work Borrer (1781-1862), a keen lichenologist, supplied many new and rare lichens collected mostly in Sussex.

It is a matter of regret that Greville should have so entirely ignored lichens in his great work on Scottish Cryptogams[99]. The two species of[13] Lichina are the only ones he figured, and these he took to be algae. He[100] was well acquainted with lichens, for in the Flora Edinensis he lists 128 species for the Edinburgh district, arranging the genera under “Lichenes” with the exception of Opegrapha and Verrucaria which are placed with the fungus genus Poronia in “Hypoxyla.” Though he cites the publications of Acharius, he does not employ his scientific terms, possibly because he was writing his diagnoses in English. Two other British works of this time still remain to be chronicled: Hooker’s[101] contributions to Smith’s English Flora and Taylor’s[102] work on lichens in Mackay’s Flora Hibernica. Through these the knowledge of the subject was very largely extended in our country.

The classification of lichens and their place in the vegetable kingdom were now firmly established on the lines laid down by Acharius. Fries[103] in his important work Lichenographia Europaea more or less followed his distinguished countryman. The uncertainty as to the position and relationship of lichens had rendered the task of systematic arrangement one of peculiar difficulty and had unduly absorbed attention; but now that a satisfactory order had been established in the chaos of forms, the way was clear for other aspects of the study. Several writers expressed their views by suggesting somewhat different methods of classification, others wrote monographs of separate groups, or genera. Fée[104] published an Essay on the Cryptogams (mostly lichens) that grew on officinal exotic barks; Flörke[105] took up the difficult genus Cladonia; Wallroth[106] also wrote on Cladonia; Delise[107] on Sticta, and Chevalier[108] published a long and elaborate account of Graphideae.

Wallroth and Meyer at this time published, simultaneously, important studies on the general morphology and physiology of lichens. Wallroth[109] had contemplated an even larger work on the Natural History of Lichens, but only two of the volumes reached publication. In the first of these he devoted much attention to the “gonidia” or “brood-cells” and established the distinction between the heteromerous and homoiomerous distribution of green cells within the thallus; he also describes with great detail the “morphosis” and “metamorphosis” of the vegetative body. In the second volume he discusses their physiology—the contents and products of the thallus, colouring, nutrition, season of development, etc.—and finally the pathology of these organisms. He made no great use of the compound microscope, and his studies were confined to phenomena that could be observed with a single lens.

Meyer’s[110] work contains a still more exact study of the anatomy and physiology of lichens; he also devotes many passages to an account of their metamorphoses, pointing out that species alter so much in varying conditions, that the same one at different stages may be placed even in different genera;[14] he however carries his theory of metamorphosis too far and unites together widely separated plants. Meyer was the first to describe the growth of the lichen from spores, though his description is somewhat confused. Possibly the honour of having first observed their germination should be given to a later botanist, Holle[111]. The works of both Wallroth and Meyer enjoyed a great and well-merited reputation: they were standard books of consultation for many years. Koerber[112], who devoted a long treatise to the study of gonidia, confirmed Wallroth’s theories: he considered at that time that the gonidia in the soredial condition were organs of propagation.

Mention should be made here of the many able and keen collectors who, in the latter half of the eighteenth century and the beginning of the nineteenth, did so much to further the knowledge of lichens in the British Isles. Among the earliest of these naturalists are Richard Pulteney (1730-1801), whose collection of plants, now in the herbarium of the British Museum, includes many lichens, and Hugh Davies (1739-1821), a clergyman whose Welsh plants also form part of the Museum collection. The Rev. John Harriman (1760-1831) sent many rare plants from Egglestone in Durham to the editors of English Botany and among them were not a few lichens. Edward Forster (1765-1849) lived in Essex and collected in that county, more especially in and near Epping Forest, and another East country botanist, Dawson Turner (1775-1858), though chiefly known as an algologist, gave considerable attention to lichens. In Scotland the two most active workers were Charles Lyell (1767-1849), of Kinnordy in Forfarshire, and George Don (1798-1856), also a Forfar man. Don was a gardener and became eventually a foreman at the Chelsea Physic Garden. Sir Thomas Gage of Hengrave Hall (1781-1823) botanized chiefly in his own county of Suffolk; but most of his lichens were collected in South Ireland and are incorporated in the herbarium of the British Museum. Miss Hutchins also collected in Ireland and sent her plants for inclusion in English Botany. But in later years, the principal lichenologist connected with that great undertaking was W. Borrer, who spent his life in Sussex: he not only supplied a large number of specimens to the authors, but he himself discovered and described many new lichens.

American lichenologists were also extremely active all through this period. The comparatively few lichens of Michaux’s[113] Flora grouped under “Lichenaceae” were collected in such widely separated regions as Carolina and Canada. A few years later Mühlenberg[114] included no fewer than 184 species in his Catalogue of North American Plants. Torrey[115] and Halsey[116] botanized over a limited area near New York, and the latter, who devoted himself more especially to lichens, succeeded in recording 176 different forms, old and new. These two botanists were both indebted for help in their work[15] to Schweinitz, a Moravian brother, who moved from one country to another, working and publishing, now in America and now in Europe. His name is however chiefly associated with fungi. Later American lichenology is nobly represented by Tuckerman[117] who issued his first work on lichens in 1839, and who continued for many years to devote himself to the subject. He followed at first the classification and nomenclature that had been adopted by Fée, but as time went on he associated himself with all that was best and most enlightened in the growing science.

Travellers and explorers in those days of high adventure were constantly sending their specimens to European botanists for examination and determination, and the knowledge of exotic lichens as of other classes of plants grew with opportunity. Among the principal home workers in foreign material, at this time, may be cited Fée[118] who described a very large series on officinal barks (Cinchona, etc.) so largely coming into use as medicines; he also took charge of the lichens in Martius’s[119] Flora of Brazil. Montagne[120] named large collections, notably those of Leprieur collected in Guiana, and Hooker[121] and Walker Arnott determined the plants collected during Captain Beechey’s voyage, which included lichens from many different regions.

G. Period VI. 1846-1867

The last work of importance, in which microscopic characters were ignored, was the Enumeratio critica Lichenum Europaeum by Schaerer[122], a veteran lichenologist, who rather sadly realized at the end the limitations of that work, as he asks the reader to accept it “such as it is.” Many years previously, Eschweiler[123] in his Systema and Fée[124] in his account of Cryptogams on Officinal Bark, had given particular attention to the internal structure as well as to the outward form of the lichen fructification. Fée, more especially, had described and figured a large number of spores; but neither writer had done more than suggest their value as a guide in the determination of genera and species.

It was an Italian botanist, Giuseppe de Notaris[125], a Professor in Florence, who took up the work where Fée had left it. His comparative studies of both vegetative and reproductive organs convinced him of the great importance of spore characters in classification, the spore being, as he rightly decided, the highest and ultimate product of the lichen plant. In his microscopic examination of the various recognized genera, he found that while, in some genera, the spores conformed to one distinct type, in others their diversities in form, septation or colour gave a decisive reason for the establishment of new genera, while minor differences in size, etc. of the spores proved to be of great value in distinguishing species. The spore standard thus marks a new[16] departure in lichenology. De Notaris published the results of his researches in a fragment of a projected larger work that was never completed. Though his views were overlooked for a time, they were at length fully recognized and further elaborated by Massalongo[126] in Italy, by Norman[127] in Norway, by Koerber[128] in Germany and by Mudd[129] in our own country. Massalongo had drawn up the scheme of a great Scolia Lichenographica, but like de Notaris, he was only able to publish a part. After twelve years of ill-health, in which he struggled to continue his work, he died at the early age of 36.

Lindsay[130], Mudd and Leighton[131] were at this time devoting great attention to British lichens. Lauder Lindsay’s Popular History of British Lichens, with its coloured plates and its descriptive and economic account of these plants has enabled many to acquire a wide knowledge of the group. Mudd’s Manual, a more complete and extremely valuable contribution to the subject, followed entirely on the lines of Massalongo’s work. From his large experience in the examination of lichens he came to the conclusion that: “Of all organs furnished by a given group of plants, none offer so many real, constant and physiological characters as the spores of lichens, for the formation of a simple and natural classification.”

Meanwhile, a contemporary writer, William Nylander, was rising into fame. He was born at Uleaborg in Finland[132] in 1822 and became interested in lichens very early in his career. His first post was the professorship of botany at Helsingfors; but in 1863 he gave up his chair and removed to Paris where he remained, except for short absences, until his death. One of his excursions brought him to London in 1857 to examine Hooker’s herbarium. He devoted his whole life to the study of lichens, and from 1852, the date of his first lichen publication, which is an account of the lichens of Helsingfors, to the end of his life he poured out a constant succession of books or papers, most of them in Latin. One of his earliest works was an Essay on Classification[133] which he elaborated later, but which in its main features he never altered. He relied, in his system, on the structure and form of thallus, gonidia and fructifications, more especially on those of the spermogonia (pycnidia), but he rejected ascospore characters except so far as they were of use in the diagnosis of species. He failed by being too isolated and by his unwillingness to recognize results obtained by other workers. In 1866 he had discovered the staining reactions of potash and hypochlorite of lime on certain thalli, and though these are at times unreliable owing to growth conditions, etc., they have generally been of real service. Nylander, however, never admitted any criticism of his methods; his opinions once stated were never revised. He rejected absolutely the theory of the dual nature of lichens propounded by Schwendener without seriously examining[17] the question, and regarded as personal enemies those who dared to differ from him. The last years of his life were passed in complete solitude. He died in March 1899.

Owing to the very inadequate powers of magnification at the service of scientific workers, the study of lichens as of other plants was for long restricted to the collecting, examining and classifying of specimens according to their macroscopic characters; the microscopic details observed were isolated and unreliable except to some extent for spore characters. Special interest is therefore attached to the various schemes of classification, as each new one proposed reflects to a large extent the condition of scientific knowledge of the time, and generally marks an advance. It was the improvement of the microscope from a scientific toy to an instrument of research that opened up new fields of observation and gave a new impetus to the study of a group of plants that had proved a puzzle from the earliest times.

Tulasne was one of the pioneers in microscopic botany. He made a methodical study of a large series of lichens[134] and traced their development, so far as he was able, from the spore onwards. He gave special attention to the form and function of spermogonia and spermatia, and his work is enriched by beautiful figures of microscopic detail. Lauder Lindsay[135] also published an elaborate treatise on spermogonia, on their occurrence in the lichen kingdom and on their form and structure. The paper embodies the results of wide microscopic research and is a mine of information regarding these bodies.

Much interesting work was contributed at this time by Itzigsohn[136], Speerschneider[137], Sachs[138], Thwaites[139], and others. They devoted their researches to some particular aspect of lichen development and their several contributions are discussed elsewhere in this work.

Schwendener[140] followed with a systematic study of the minute anatomy of many of the larger lichen genera. His work is extremely important in itself and still more so as it gradually revealed to him the composite character of the thallus.

Several important monographs date from this period: Leighton[141] reviewed all the British “Angiocarpous” lichens with special reference to their “sporidia” though without treating these as of generic value. He followed up this monograph by two others, on the Graphideae[142] and the Umbilicarieae[143], and Mudd[144] published a careful study of the British Cladoniae. On the Continent Th. Fries[145] issued a revision of Stereocaulon and Pilophoron and other writers contributed work on smaller groups.

[18]

H. Period VII. 1867 and after

Modern lichenology begins with the enunciation of Schwendener’s[146] theory of the composite nature of the lichen plant. The puzzling resemblance of certain forms to algae, of others to fungi, had excited the interest of botanists from a very early date, and the similarity between the green cells in the thallus, and certain lower forms of algae had been again and again pointed out. Increasing observation concerning the life-histories of these algae and of the gonidia had eventually piled up so great a number of proofs of their identity that Schwendener’s announcement must have seemed to many an inevitable conclusion, though no one before had hazarded the astounding statement that two organisms of independent origin were combined in the lichen.

The dual hypothesis, as it was termed, was not however universally accepted. It was indeed bitterly and scornfully rejected by some of the most prominent lichenologists of the time, including Nylander[147], J. Müller and Crombie[148]. Schwendener held that the lichen was a fungus parasitic on an alga, and his opponents judged, indeed quite rightly, that such a view was wholly inadequate to explain the biology of lichens. It was not till a later date that the truer conception of the “consortium” or “symbiosis” was proposed. The researches undertaken to prove or disprove the new theories come under review in Chapter II.

Stahl’s work on the development of the carpogonium in lichens gave a new direction to study, and notable work has been done during the last forty years in that as in other branches of lichenology.

Exploration of old and new fields furnished the lichen-flora of the world with many new plants which have been described by various systematists—by Nylander, Babington, Arnold, Müller, Th. Fries, Stizenberger, Leighton, Crombie and many others, and their contributions are scattered through contemporary scientific journals. The number of recorded species is now somewhere about 40,000, though, in all probability, many of these will be found to be growth forms. Still, at the lowest computation, the number of different species is very large.

Systematic literature has been enriched by a series of important monographs, too numerous to mention here. While treating definite groups, they have helped to elucidate some of the peculiar biological problems of the symbiotic growth.

Morphology, since Schwendener’s time, has been well represented by Zukal, Reinke, Lindau, Fünfstück, Darbishire, Hue, and by an increasing number of modern writers whose work is duly acknowledged under each[19] subject of study. Hesse and Zopf, and more recently Lettau, have been engaged in the examination of those unique products, the lichen acids, while other workers have investigated lichen derivatives such as fats. Ecology of lichens has also been receiving increased attention. Problems of physiology, symbiosis, etc., are not yet considered to be solved and are being attacked from various sides.

British lichenologists since 1867 have been mainly engaged on field work, with the exception of Lauder Lindsay who published after that date a second great paper on the spermogonia of crustaceous lichens. Leighton in his Lichen Flora and Crombie in numerous publications gave the lead in systematic work, and with them were associated a band of indefatigable collectors. Among these may be recalled Alexander Croall (1809-85), a parish schoolmaster in Scotland whose Plants of Braemar include many of the rarer mountain lichens. Henry Buchanan Holl (1820-86), a surgeon in London, collected in the Scottish Highlands as well as in England and Wales. William Joshua (1828-98) worked mostly in the Western counties of Somerset and Gloucestershire. Charles Du Bois Larbalestier, who died in 1911, was a keen observer and collector during many years; he discovered a number of new species in his native Jersey, in Cambridgeshire and also in Connemara; his plants were generally sent to Nylander to be determined and described. He issued two sets of lichens, one of Channel Island plants, the other of more general British distribution, and he had begun the issue of Cambridgeshire lichens. Isaac Carroll (1828-80), an Irish botanist, issued a first fascicle of Lichenes Hibernici containing 40 numbers. More recently Lett[149] has reported 80 species and varieties from the Mourne Mountains in Ireland. Other more extensive sets were issued by Mudd and by Leighton, and later by Crombie and by Johnson. All these have been of great service to the study of lichenology in our country. Other collectors of note are Curnow (Cornwall), Martindale (Westmoreland), and E. M. Holmes whose valuable herbarium has been secured by University College, Nottingham.

The publication of the volume dealing with Lichenes in Engler and Prantl’s Pflanzenfamilien has proved a boon to all who are interested in the study of lichens. Fünfstück[150] prepared the introduction, an admirable presentation of the morphological and physiological aspects of the subject, while Zahlbruckner[151], with equal success, took charge of the section dealing with classification.

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CHAPTER II
CONSTITUENTS OF THE LICHEN THALLUS

I. LICHEN GONIDIA

Fig. 1. Physcia aipolia Nyl. Vertical section of thallus. a, cortex; b, algal layer; c, medulla; d, lower cortex. × 100 (partly diagrammatic).

The thallus or vegetative body of lichens differs from that of other green plants in the sharp distinction both of form and colour between the assimilative cells and the colourless tissues, and in the relative positions these occupy within the thallus: in the greater number of lichen species the green chlorophyll cells are confined to a narrow zone or band some way beneath and parallel with the surface (Fig. 1); in a minority of genera they are distributed through the entire thallus (Fig. 2); but in all cases the tissues remain distinct. The green zone can be easily demonstrated in any of the larger lichens by scaling off the outer surface cells, or by making a vertical section through the thallus. The colourless cells penetrate to some extent among the green cells; they also form the whole of the cortical and medullary tissues.

Fig. 2. Collema nigrescens Ach. Vertical section of thallus. a, chains of the alga Nostoc; b, fungal filaments. × 600.

These two different elements we now know to consist of two distinct organisms, a fungus and an alga. The green algal cells were at one time considered to be reproductive bodies, and were called “gonidia,” a term still in use though its significance has changed.

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1. GONIDIA IN RELATION TO THE THALLUS

A. Historical account of Lichen Gonidia

There have been few subjects of botanical investigation that have roused so much speculation and such prolonged controversy as the question of these constituents of the lichen plant. The green cells and the colourless filaments which together form the vegetative structure are so markedly dissimilar, that constant attempts have been made to explain the problem of their origin and function, and thereby to establish satisfactorily the relationship of lichens to other members of the Plant Kingdom.

In gelatinous lichens, represented by Collema, of which several species are common in damp places and grow on trees or walls or on the ground, the chains of green cells interspersed through the thallus have long been recognized as comparable with the filaments of Nostoc, a blue-green gelatinous alga, conspicuous in wet weather in the same localities as those inhabited by Collema. So among early systematists, we find Ventenat[152] classifying the few lichens with which he was acquainted under algae and hazarding the statement that a gelatinous lichen such as Collema was only a Nostoc changed in form. Some years later Cassini[153] in an account of Nostoc expressed a somewhat similar view, though with a difference: he suggested that Nostoc was but a monstrous form of Collema, his argument being that, as the latter bore the fruit, it was the normal and perfect condition of the plant. A few years later Agardh[154] claimed to have observed the metamorphosis of Nostoc up to the fertile stage of a lichen, Collema limosum. But long before this date, Scopoli[155] had demonstrated a green colouring substance in non-gelatinous lichens by rubbing a crustaceous or leprose thallus between the fingers; and Persoon[156] made use of this green colour characteristic of lichen crusts to differentiate these plants from fungi. Sprengel[157] went a step further in exactly describing the green tissue as forming a definite layer below the upper cortex of foliaceous lichens.

The first clear description and delimitation of the different elements composing the lichen thallus was, however, given by Wallroth[158]. He drew attention to the great similarity between the colourless filaments of the lichen and the hyphae of fungi. The green globose cells in the chlorophyllaceous lichens he interpreted as brood-cells or gonidia, regarding them as organs of reproduction collected into a “stratum gonimon.” To the same author we owe the terms “homoiomerous” and “heteromerous,” which he coined to describe the arrangement of these green cells in the tissue of the thallus. In the former case the gonidia are distributed equally through the structure; in the latter they are confined to a distinct zone.

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Wallroth’s terminology and his views of the function of the gonidia were accepted as the true explanation for many years, the opinion that they were solely reproductive bodies being entirely in accordance with the well-known part played by soredia in the propagation of lichens—and soredia always include one or more green cells.

B. Gonidia contrasted with Algae

In describing the gonidia of the Graphideae Wallroth[159] had pointed out their affinity with the filaments of Chroolepus (Trentepohlia) umbrina. He considered these and other green algae when growing loose on the trunks of trees to be but “unfortunate brood-cells” which had become free and, though capable of growth and increase, were unable to form again a lichen plant.

Further observations on gonidia were made by E. Fries[160]: he found that the green cells escaped from the lichen matrix and produced new individuals; and also that the whole thallus in moist localities might become dissolved into the alga known as Protococcus viridis; but, he continues, “though these Protococcus cells multiplied exceedingly, they never could rise again to the perfect lichen.” Kützing[161], in a later account of Protococcus viridis, also recognized its affinity with lichens; he stated that he could testify from observation that, according to the amount of moisture present, it would develop, either in excessive moisture to a filamentous alga, or in drier conditions “to lichens such as Lecanora subfusca or Xanthoria parietina.”

Fig. 3. Coenogonium ebeneum A. L. Sm. Tip of lichen filament, the alga overgrown by dark fungal hyphae × 600.

A British botanist, G. H. K. Thwaites[162], at one time superintendent of the botanical garden at Peradeniya in Ceylon, published a notable paper on lichen gonidia in which he pointed out that as in Collema the green constituents of the thallus resembled the chains of Nostoc, so in the non-gelatinous lichens, the green globose cells were comparable or identical with Pleurococcus, and Thwaites further observed that they increased by division within the lichen thallus. He insisted too that in no instance were gonidia reproductive organs: they were essential component parts of the vegetative body and necessary to the life of the plant. In a further paper on Chroolepus ebeneus Ag., a plant consisting of slender dark-coloured felted filaments, he described these filaments as being composed of a central strand which closely resembled the alga Chroolepus, and of a surrounding sheath of dark-coloured[23] cells (Fig. 3): “occasionally,” he writes, “the internal filament protrudes beyond the investing sheath, and may then be seen to consist of oblong cells containing the peculiar reddish oily-looking endochrome of Chroolepus.” Thwaites placed this puzzling plant in a new genus, Cystocoleus, at the same time pointing out its affinity with the lichen genus Coenogonium. The plant is now known as Coenogonium ebeneum. Thwaites was on the threshold of the discovery as to the true nature of the relationship between the central filament and the investing sheath, but he failed to take the next forward step.

Very shortly after, Von Flotow[163] published his views on some other lichen gonidia. He had come to the conclusion that the various species of the alga, Gloeocapsa, so frequently found in damp places, among mosses and lichens, were merely growth stages of the gonidia of Ephebe pubescens, and bore the same relation to Ephebe as did Lepra viridis (Protococcus) to Parmelia. The gonidium of Ephebe is the gelatinous filamentous blue-green alga Stigonema (Fig. 4), and the separate cells are not unlike those of Gloeocapsa. Flotow had also demonstrated that the same type of gonidium was enclosed in the cephalodia of Stereocaulon. Sachs[164], too, gave evidence as to the close connection between Nostoc and Collema. He had observed numerous small clumps of the alga growing in proximity to equally abundant thalli of Collema, with every stage of development represented from one to the other. He found cases where the gelatinous coils of Nostoc chains were penetrated by fine colourless filaments “as if invaded by a parasitic fungus.” Later these threads were seen to be attached to some cell of the Nostoc trichome. Sachs concluded, however, from very careful examination at the time, that the colourless filaments were produced by the green cells. As growth proceeded, the coloured Nostoc chains became massed towards the upper surface, while the colourless filaments tended to occupy the lower part of the thallus. He calculated that during the summer season the metamorphosis from Nostoc to a fertile Collema thallus took from three to four months. He judged that in favourable conditions the change would inevitably take place, though if there should be too great moisture no Collema would be formed. His study of Cladonia was less successful as he mistook some colonies of Gloeocapsa for a growth condition of Cladonia gonidia, an error corrected later by Itzigsohn[165].

Fig. 4. Ephebe pubescens Nyl. Tip of lichen filament × 600.

But before this date Itzigsohn[166] had published a paper setting forth his views on thallus formation, which marked a distinct advance. He did not[24] hazard any theory as to the origin of gonidia, but he had observed spermatia growing, much as did the cells of Oscillaria: by increase in length, and, by subsequent branching, filaments were formed which surrounded the green cells; these latter had meanwhile multiplied by repeated division till finally a complete thallus was built up, the filamentous tissue being derived from the spermatia, while the green layer came from the original gonidium. In contrasting the development with that of Collema, he represents Nostoc as a sterile product of a lichen and, like the gonidia of other lichens, only able to form a lichen thallus when it encounters the fructifying spermatia.

Braxton Hicks[167], a London doctor, some time later, made experiments with Chroococcus algae which grew in plenty on the bark of trees, and followed their development into a lichen thallus. He further claimed to have observed a Chlorococcus, which was associated with a Cladonia, divide and form a Palmella stage.

C. Culture Experiments with the Lichen Thallus

It had been repeatedly stated that the gonidia might become independent of the thallus, but absolute proof was wanting until Speerschneider[168], who had turned his attention to the subject, made direct culture experiments and was able to follow the liberation of the green cells. He took a thinnish section of the thallus of Hagenia (Physcia) ciliaris, and, by keeping it moist, he was able to observe that the gonidial cells increased by division; the moist condition at the same time caused the colourless filaments to die away. This method of investigation was to lead to further results. It was resorted to by Famintzin and Baranetzky[169] who made cultures of gonidia extracted from three different lichens, Physcia (Xanthoria) parietina, Evernia furfuracea and Cladonia sp. They were able to observe the growth and division of the green cells and, in addition, the formation of zoospores. They recognized the development as entirely identical with that of the unicellular green alga, Cystococcus humicola Naeg. Baranetzky[170] continued the experiments and made cultures of the blue-green gonidia of Peltigera canina and of Collema pulposum. In both instances he succeeded in isolating them from the thallus and in growing them in moist air as separate organisms. He adds that “many forms reckoned as algae, may be considered as vegetating lichen gonidia such as Cystococcus, Polycoccus, Nostoc, etc.” Meanwhile Itzigsohn[171] had further demonstrated by similar culture experiments that the gonidia of Peltigera canina corresponded with the algae known as Gloeocapsa monococca Kütz., and as Polycoccus punctiformis Kütz.

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D. Theories as to the Origin of Gonidia

Though the relationship between the gonidia within the thallus and free-living algal organisms seemed to be proved beyond dispute, the manner in which gonidia first originated had not yet been discovered. Bayrhoffer[172] attacked this problem in a study of foliose and other lichens. According to his observations, certain colourless cells or filaments, belonging to the “gonimic” layer, grew in a downward direction and formed at their tips a faintly yellowish-green cell; it gradually enlarged and was at length thrown off as a free globose gonidium, which represented the female cell. Other filaments from the “lower fibrous layer” of the thallus at the same time grew upwards and from them were given off somewhat similar gonidia which functioned as male cells. His observations and deductions were fanciful, but it must be remembered that the attachment between hypha and alga in lichens is in many cases so close as to appear genetic, and also it often happens that as the gonidium multiplies it becomes free from the hypha.

In his Mémoire sur les Lichens, Tulasne[173] described the colourless filaments as being fungal in appearance. The green cells he recognized as organs of nutrition, and once and again in his paper he states that they arose directly by a sort of budding process from the medullary or cortical filaments, either laterally or at the apex. This apparently reasonable view of their origin was confirmed by other writers on the subject: by Speerschneider[174] in his account of the anatomy of Usnea barbata, by de Bary[175], and by Schwendener[176] in their earlier writings. But even while de Bary accepted the hyphal origin of the gonidia, he noted[177] that, accompanying Opegrapha atra and other Graphideae, on the bark were to be found free Chroolepus cells similar to the gonidia in the lichen thallus. He added that gonidia of certain other lichens in no way differed from Protococcus cells; and as for the gelatinous lichens he declared that “either they were the perfect fruiting form of Nostocaceae and Chroococcaceae—hitherto looked on as algae—or that these same Nostocaceae and Chroococcaceae are algae which take the form of Collema, Ephebe, etc., when attacked by an ascomycetous fungus.”

All these investigators, and other lichenologists such as Nylander[178], still regarded the free-living organisms identified by them as similar to the green cells of the thallus, as only lichen gonidia escaped from the matrix and vegetating in an independent condition.

The old controversy has in recent years been unexpectedly reopened by Elfving[179] who has sought again to prove the genetic origin of the green cells. His method has been to examine a large series of lichens by making sections of the growing areas, and he claims to have observed in every case[26] the hyphal origin of the gonidia: not only of Cystococcus but also of Trentepohlia, Stigonema and Nostoc. In the case of Cystococcus, the gonidium, he says, arises by the swelling of the terminal cell of the hypha to a globose form, and by the gradual transformation of the contents to a chlorophyll-green colour, with power of assimilation. In the case of filamentous gonidia such as Trentepohlia, the hyphal cells destined to become gonidia are intercalary. In Peltigera the cells of the meristematic plectenchyma become transformed to blue-green Nostoc cells.

A study was also made by him of the formation of cephalodia[180], the gonidia of which differ from those of the “host” thallus. In Peltigera aphthosa he claims to have traced the development of these bodies to the branching and mingling of the external hairs which, in the end, form a ball of interwoven hyphae. The central cells of the ball are then gradually differentiated into Nostoc cells, which increase to form the familiar chains. Elfving allows that the gonidia mainly increase by division within the thallus, and that they also may escape and live as free organisms. His views are unsupported by direct culture experiments which are the real proof of the composite nature of the thallus.

E. Microgonidia

Another attempt to establish a genetic origin for lichen gonidia was made by Minks[181]. He had found in his examination of Leptogium myochroum that the protoplasmic contents of the hyphae broke up into a regular series of globular corpuscles which had a greenish appearance. These minute bodies, called by him microgonidia, were, he states, at first few in number, but gradually they increased and were eventually set free by the mucilaginous degeneration of the cell wall. As free thalline gonidia, they increased in size and rapidly multiplied by division. Minks was at first enthusiastically supported by Müller[182] who had found from his own observations that microgonidia might be present in any of the lichen hyphae and in any part of the thallus, even in the germinating tube of the lichen spore, and was in that case most easily seen when the spores germinated within the ascus. He argued that as spores originated within the ascus, so microgonidia were developed within the hyphae. Minks’s theories were however not generally accepted and were at last wholly discredited by Zukal[183] who was able to prove that the greenish bodies were contracted portions of protoplasm in hyphae that suffered from a lowered supply of moisture, the green colour not being due to any colouring substance, but to light effect on the proteins—an outcome of special conditions in the vegetative life of the plant. Darbishire[184] criticized Minks’s whole work with great care and he has arrived at the conclusion that the microgonidium may be dismissed as a totally mistaken conception.

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F. Composite Nature of Thallus

Schwendener[185] meanwhile was engaged on his study of lichen anatomy. Though at first he adhered to the then accepted view of the genetic connection between hyphae and gonidia, his continued examination of the vegetative development led him to publish a short paper[186] in which he announced his opinion that the various blue-green and green gonidia were really algae and that the complete lichen in all cases represented a fungus living parasitically on an alga: in Ephebe, for example, the alga was a form of Stigonema, in the Collemaceae it was a species of Nostoc. In those lichens enclosing bright green cells, the gonidia were identical with Cystococcus humicola, while in Graphideae the brightly coloured filamentous cells were those of Chroolepus (Trentepohlia). This statement he repeated in an appendix to the larger work on lichens[187] and again in the following year[188] when he described more fully the different gonidial algae and the changes produced in their structure and habit by the action of the parasite: “though eventually the alga is destroyed,” he writes, “it is at first excited to more vigorous growth by contact with the fungus, and in the course of generations may become changed beyond recognition both in size and form.” In support of his theory of the composite constitution of the thallus, Schwendener pointed out the wide distribution and frequent occurrence in nature of the algae that become transformed to lichen gonidia. He claimed as further proof of the presence of two distinct organisms that, while the colourless filaments react in the same way as fungi on the application of iodine, the gonidia take the stain of algal membranes.

G. Synthetic Cultures

Schwendener’s “dual hypothesis,” as it was termed, excited great interest and no little controversy, the reasons for and against being debated with considerable heat. Rees[189] was the first who attempted to put the matter to the proof by making synthetic cultures. For this purpose he took spores from the apothecium of a Collema and sowed them on pure cultures of Nostoc, and as a result obtained the formation of a lichen thallus, though he did not succeed in producing any fructification. He observed further that the hyphal filaments from the germinating spore died off when no Nostoc was forthcoming.

Bornet[190] followed with his record of successful cultures. He selected for experiment the spores of Physcia (Xanthoria) parietina and was able to show that hyphae produced from the germinating spore adhered to the free-growing[28] cells of Protococcus[191] viridis and formed the early stages of a lichen thallus. Woronin[192] contributed his observations on the gonidia of Parmelia (Physcia) pulverulenta which he isolated from the thallus and cultivated in pure water. He confirmed the occurrence of cell division in the gonidia and also the formation of zoospores, these again forming new colonies of algae identical in all respects with the thalline gonidia. He was able to see the germinating tube from a lichen spore attach itself to a gonidium, though he failed in his attempts to induce further growth. In our own country Archer[193] welcomed the new views on lichens, and attempted cultures but with very little success. Further synthetic cultures were made by Bornet[194], Treub[195] and Borzi[196] with a series of lichen spores. They also were able to observe the first stages of the thallus. Borzi observed spores of Physcia (Xanthoria) parietina scattered among Protococcus cells on the branch of a tree. The spores had germinated and the first branching hyphae had already begun to encircle the algae.

Fig. 5. Endocarpon pusillum Hedw. Asci and spores, with hymenial gonidia × 320 (after Stahl).

Fig. 6. Endocarpon pusillum Hedw. Spore germinating in contact with hymenial gonidia × 320 (after Stahl).

Additional evidence in favour of the theory of the independent origin of the colourless filaments and the green cells was furnished by Stahl’s[197] research on hymenial gonidia in Endocarpon (Fig. 5). By making synthetic[29] cultures of the mature spores with these bodies, he was able to observe not only the germination of the spores and the attachment of the filaments to the gonidia (Fig. 6), but also the gradual building up of a complete lichen thallus to the formation of perithecia and spores.

Fig. 7. Germination of spore of Physcia parietina De Not. in contact with Protococcus viridis Ag. × 950 (after Bornet).

Fig. 8. Physcia parietina De Not. Vertical section of thallus obtained by synthetic culture × 130 (after Bonnier).

Some years later Bonnier[198] made an interesting series of synthetic cultures between the spores of lichens germinated in carefully sterilized conditions, and algae taken from the open (Figs. 7 and 8). Separate control cultures of spores and algae were carried on at the same time, with the result that in one case lichen hyphae alone, in the other algae were produced. The various lichen spores with which he experimented were sown in association with the following algae:

(1) Protococcus.

Pure synthetic cultures of Physcia (Xanthoria) parietina were begun in August 1884 on fragments of bark. In October 1886 the thallus was several centimetres in diameter, and some of the lobes were fruited.

Physcia stellaris was also grown on bark; in one case both thallus and apothecia were developed.

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Parmelia acetabulum, another corticolous species, formed only a minute thallus about 5 mm. in diameter, but entirely identical with normally growing specimens.

(2) Pleurococcus.

Lecanora (Rinodina) sophodes, sown on rock in 1883, reached in 1886 a diameter of 13 mm. with fully developed apothecia.

Lecanora ferruginea and L. subfusca after three years’ culture formed sterile thalli only.

Lecanora coilocarpa in four years, and L. caesio-rufa in three years formed very small thalli without fructification.

(3) Trentepohlia (Chroolepus).

Opegrapha vulgata in two years had developed thallus and apothecia. The control culture of the spores formed, as in nature, a considerable felt of mycelium in the interstices of the bark, but no pycnidia or apothecia.

Graphis elegans. Only the beginning of a differentiated thallus was obtained with this species.

Verrucaria muralis (?)[199] gave in less than a year a completely developed thallus.

Bonnier also attempted cultures with species of Collema and Ephebe, but was unsuccessful in inducing the formation of a lichen plant.

H. Hymenial Gonidia

Reference has already been made to the minute green cells which were originally described by Nylander[200] as occurring in the perithecia of a few Pyrenolichens as free gonidia, i.e. unentangled with lichen hyphae. Fuisting[201] found them in the perithecium of Polyblastia (Staurothele) catalepta at a very early stage of its development when the perithecial tissues were newly differentiated from those of the surrounding thallus. The gonidia enclosed in the perithecium differed in no wise from those of the thallus: they had become mechanically enclosed in the new tissue; and while those in the outer compact layers died off, those in the centre of the structure, where a hollow space arises, were subject to very active division, becoming smaller in the process and finally filling the cavity. Winter’s[202] researches on similar lichens confirmed Fuisting’s conclusions: he described them as similar to the thalline gonidia but lighter in colour and of smaller size, measuring frequently only 2·3 µ in diameter, though this size increased to about 7 µ when cultivated outside the perithecium.

Stahl[203] sufficiently demonstrated the importance of these gonidia in[31] supplying the germinating spores with the necessary algae. They come to lie in vertical rows between the asci and, owing to pressure, assume an elongate form[204] (Figs. 5 and 6). They have been seen in very few lichens, in Endocarpon and Staurothele, both rather small genera of Pyrenolichens, and, so far as is known, in two Discolichens, Lecidea phylliscocarpa and L. phyllocaris, the latter recorded from Brazil by Wainio[205], and, on account of the inclusion of gonidia in the hymenium, placed by him in a section, Gonothecium.

I. Nature of Association between Alga and Fungus

a. Consortium and Symbiosis. These cultures had established convincingly the composite nature of the lichen thallus, and Schwendener’s opinion, that the relationship between the two organisms was some varying degree of parasitism, was at first unhesitatingly accepted by most botanists. Reinke[206] was the first to point out the insufficiency of this view to explain the long continued healthy life of both constituents, a condition so different from all known instances of the disturbing or fatal parasitism of one individual on another. He recognized in the association a state of mutual growth and interdependence, that had resulted in the production of an entirely new type of plant, and he suggested Consortium as a truer description of the connection between the fungus and the alga. This term had originally been coined by his friend Grisebach in a paper[206] describing the presence of actively growing Nostoc algae in healthy Gunnera stems; and Reinke compared that apparently harmless association with the similar phenomenon in the lichen thallus. The comparison was emphasized by him in a later paper[207] on the same subject, in which he ascribes to each “consort” its function in the composite plant, and declares that if such a mutual life of Alga and Ascomycete is to be regarded as one of parasitism, it must be considered as reciprocal parasitism; and he insists that “much more appropriate for this form of organic life is the conception and title of Consortium.” In a special work on lichens, Reinke[208] further elaborated his theory of the physiological activity and mutual service of the two organisms forming the consortium.

Frank[209] suggested the term Homobium as appropriate, but it is faulty inasmuch as it expresses a relationship of complete interdependence, and it has been proved that the fungus partly, and the alga entirely, have the power of free growth.

A wider currency was given to this view of a mutually advantageous growth by de Bary[210]. He followed Reinke in refusing to accept as satisfactory the theory of simple parasitism, and adduced the evident healthy life of the algal cells—the alleged victims of the fungus—as incompatible with the[32] parasitic condition. He proposed the happily descriptive designation of a Symbiosis or conjoint life which was mostly though not always, nor in equal degree, beneficial to each of the partners or symbionts.

b. Different Forms of Association. The type of association between the two symbionts varies in different lichens. Bornet[211], in describing the development of the thallus in certain members of the Collemaceae, found that though as a rule the two elements of the thallus, as in some species of Collema itself, persisted intact side by side, there was in other members of the genus an occasional parasitism: short branches from the main hyphae applied themselves by their tips to some cell of the Nostoc chain (Fig. 9). The cell thus seized upon began to increase in size, and the plasma became granular and gathered at the side furthest away from the point of attachment. Finally the contents were used up, and nothing was left but an empty membrane adhering to the fungus hypha. In another species the hypha penetrated the cell. These instances of parasitism are most readily seen towards the edge of the thallus where growth is more active; towards the centre the attached cells have become absorbed, and only the shortened broken chains attest their disappearance. The other cells of the chains remain uninjured.

Fig. 9. Physma chalazanum Arn. Cells of Nostoc chains penetrated and enlarged by hyphae × 950 (after Bornet).

In Synalissa, a small shrubby gelatinous genus, the hypha, as described by Bornet and by Hedlund[212], pierces the outer wall of the gelatinous alga (Gloeocapsa) and swells inside to a somewhat globose haustorium which rests in a depression of the plasma (Fig. 10). The alga, though evidently[33] undamaged, is excited to a division which takes place on a plane that passes through the haustorium; the two daughter-cells then separate, and in so doing free themselves from the hypha.

Fig. 10. Synalissa symphorea Nyl. Algae (Gloeocapsa) with hyphae from the internal thallus × 480 (after Bornet).

Hedlund followed the process of association between the two organisms in the lichens Micarea (Biatorina) prasina and M. denigrata (Biatorina synothea), crustaceous species which inhabit trunks of trees or palings. In these the alga, one of the Chlorophyceae, has assumed the character of a Gloeocapsa but on cultivation it was found to belong to the genus Gloeocystis. The cells are globose and rather small; they increase by the division of the contents into two or at most four portions which become rounded off and covered with a membrane before they become free from the mother-cell. The lichen hypha, on contact with any one of the green cells, bores through the outer membrane and swells within to a haustorium, as in the gonidia of Synalissa.

Fig. 11. Gonidia from Ramalina reticulata Nyl. A, gonidium pierced and cell contents shrinking × 560; B, older stage, the contents of gonidium exhausted × 900 (after Peirce).

Fig. 12. Pertusaria globulifera Nyl. Fungus and gonidia from gonidial zone × 500 (after Darbishire).

Penetrating haustoria were demonstrated by Peirce[213] in his study of the gonidia of Ramalina reticulata. In the first stage the tip of a hypha had pierced the outer wall of the alga, causing the protoplasm to contract away from the point of contact (Fig. 11). More advanced stages showed the extension of the haustorium into the centre of the cell, and, finally, the complete disappearance of the contents. In many cases it was found that penetration equally with clasping of the alga by the filament sets up an irritation which induces cell-division, and the alga, as in Synalissa, thus becomes free from the fungus. Hue[214] has recorded instances of penetration in an Antarctic species, Physcia puncticulata. It is easy, he says, to see the tips of the hyphae pierce the sheath of the gonidium and penetrate to the nucleus.

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Lindau[215] has described the association between fungus and alga in Pertusaria and other crustaceous forms as one of contact only (Fig. 12). He found that the cell-membrane of the two adhering organisms was unbroken. Occasionally the algal cell showed a slight indentation, but was otherwise unchanged. The hyphal branch was somewhat swollen at the tip where it touched the alga, and the wall was slightly thinner. The attachment between the two cells was so close, however, that pressure on the cover-glass failed to separate them.

Generally the hypha simply surrounds the gonidium with clasping branches. Many algae also lie free in the gonidial zone, and Peirce[216] claims that these are larger, more deeply coloured and in every way healthier looking than those in the grasp of the fungus. He ignores, however, the case of the soredial algae which though very closely invested by the fungus are yet entirely healthy, since on their future increase depends in many cases the reproduction of new individual lichens.

In a recent study of a crustaceous sandstone lichen, “Caloplaca pyracea,” Claassen[217] has sought to prove a case of pure parasitism. The rock was at first covered with the green cells of Cystococcus sp. Later there appeared greyish-white patches on the green, representing the invasion of the lichen fungus. These patches increased centrifugally, leaving in time a bare patch in the centre of growth which was again colonized by the green alga. The lichen fruited abundantly, but wherever it encroached the green cells were more or less destroyed. The true explanation seems to be that the green cells were absorbed into the lichen thallus, though enough of them persisted to start new colonies on any bare piece of the stone. In the same way large patches of Trentepohlia aurea have been observed to be gradually invaded by the dark coloured hyphae of Coenogonium ebeneum. In time the whole of the alga is absorbed and nothing is to be seen but the dark felted lichen. The free alga as such disappears, but it is hardly correct to describe the process as one of destruction.

This algal genus Trentepohlia (Chroolepus) forms the gonidia of the Graphideae, Roccelleae, etc. It is a filamentous aerial alga which increases by apical growth. In the Graphideae, many of which grow on trees beneath the outer bark (hypophloeodal), the association between the two symbionts may be of the simplest character, but was considered by Frank[218] to be of an advanced type. According to his observations and to those of Lindau[219], the fungal hyphae penetrate first between the cells of the periderm. The alga, frequently Trentepohlia umbrina, tends to grow down into any cracks of the surface. It goes more deeply in when preceded by the hyphae. In some species both organisms maintain their independent growth, though each shows increased vigour when it comes into contact with the other. In some[35] instances the cells of the alga are clasped by the fungus which causes the disintegration of the filament. The cells lose their bright yellow or reddish colour and are changed in appearance to greenish lichen gonidia; but no penetration by haustoria has ever been observed in Trentepohlia.

Bachmann’s[220] study of a similar gonidium in a calcicolous species of Opegrapha confirms Frank’s results. The algae had pierced not only between the looser lime granules but also through a crystal of calcium carbonate, and occupied nests scooped out in the rock by means of acid formed and excreted by their filaments. When association took place with the fungus, the algal cells were more restricted to a gonidial zone; but some of the cells, having been pushed aside by the hyphae, had started new centres of gonidia. On contact with the hyphae there was a tendency to bud out in a yeast-like growth.

In the thallus of the Roccelleae, the algal filament, also a Trentepohlia, is broken up into separate cells, but in the Coenogoniaceae, whether the gonidium be a Cladophora as in Racodium, or a Trentepohlia as in Coenogonium, the filaments remain intact and are invested more or less closely by the hyphae.

Fig. 13. Outer edge of Phycopeltis expansa Jenn., the alga attacked by hyphae and passing into separate gonidia × 500 (after Vaughan Jennings).

A somewhat different type of association takes place between alga and fungus in Strigula complanata, an epiphyllous lichen more or less common in tropical regions. Cunningham[221], who found it near Calcutta, described the algal constituent and placed it in a new genus, Mycoidea (Cephaleuros). It forms small plate-like expansions on the surface of the leaf, and also penetrates below the cuticle, burrowing between that and the epidermal cells; occasionally, as observed by Cunningham, rhizoid-like growths pierce deeper into the tissue—into and below the epidermal layer. Very frequently, in the wet season, a fungus takes possession of the alga and slender colourless hyphae creep along its surface by the side of the cell rows, sending out branches which grow downwards. Marshall Ward[222] described the same lichen from Ceylon. He states that the alga may be attacked at any stage, and if it is in a very young condition it is killed by the fungus; at a more advanced period of growth it continues to develop as an integral part of the lichen thallus, but with more frequently divided and smaller cells. Vaughan Jennings[223] observed Strigula complanata in New Zealand associated with a closely allied chroolepoid alga Phycopeltis expansa. He also noted the growth of the fungus over the alga breaking up the plates of tissue and[36] separating the cells which, from yellow, change to a green colour and become rounded off (Fig. 13). The mature lichen, a white thallus dotted with black fruits, contrasts strikingly with the yellow membranous alga. Lichen formation usually begins near the edge of the leaf and the margin of the thallus itself is marked by a green zone showing where the fungus has recently come into contact with the alga.

More recently Hans Fitting[224] has described “Mycoidea parasitica” as it occurs on evergreen leaves in Java. The alga, a species of Cephaleuros, though at first an epiphyte, becomes partially parasitic at maturity. It penetrates below the cuticle to the outer epidermal cells and may even reach the tissue below. When it is joined by the lichen fungus, both constituents grow together to form the lichen. Fitting adds that the leaf is evidently but little injured. In this lichen the alga in the grip of the fungus loses its independence and may be killed off: it is an instance of something like intermittent parasitism.

J. Recent views on Symbiosis and Parasitism

No hyphal penetration of the bright-green algal cell by means of haustoria had been observed by the earlier workers, Bornet[225], Bonnier[226] and others, though they followed Schwendener[227] in regarding the relationship as one of host and parasite. Lindau, also, after long study accepted parasitism as the only adequate explanation of the associated growth, though he never found the fungus actually preying on the alga.

In recent years interest in the subject has been revived by the researches of Elenkin[228], a Russian botanist who claims to have established a case for parasitism or rather “endosaprophytism.” He has demonstrated by means of staining reagents the presence in the thallus of large numbers of dead algal cells. A few empty membranes are to be found in the cortex and in the gonidial zone, but the larger proportion occur below the gonidial zone and partly in the medulla. He describes the lower layer as a “necral” or “hyponecral” zone, and he considers that the hyphae draw their nourishment chiefly from dead algal material. The fungus must therefore be regarded in this case as a saprophyte rather than a parasite. The algae, he considers, may have perished from want of sufficient light and air or they may have been destroyed by an enzyme produced by the fungus. The latter he thinks is the more probable, as dead cells are frequently present among the living algae of the gonidial zone. To the action of the enzyme he also attributes the angular deformed appearance of many gonidia and the paler colour and gradual disintegration of their contents which are finally used up as endosaprophytic nourishment by the fungus. Dead algal cells were more easily[37] seen, he tells us, in crustaceous lichens associated with “Pleurococcus” or “Cystococcus”; they were much less frequent in the larger foliose or fruticose lichens. Dead cells of Trentepohlia were also difficult to find.

In a second paper Elenkin records one clear instance of a haustorium entering an algal cell, and says he found some evidence of hyphal branches penetrating otherwise uninjured gonidia, round holes being visible in their outer wall, but he holds that it is the cell-wall of the alga that is mainly dissolved by the ferment and then used as food by the hyphae.

No allowance has been made by Elenkin for the normal wasting common to all organic beings: the lichen fungus is continually being renewed, especially in the cortical structures, and the alga must also be subject to change. He[229] claims, nevertheless, that his observations have proved that the one symbiont is always preying on the other, either as a parasite or as a saprophyte. He has likened the conception of symbiosis to that of a balance between two organisms, “a moveable equilibrium of the symbionts.” If, he says, we could conceive a state where the conditions of life would be equally favourable for both partners there would be true mutualism, but in practice one only is favoured and gains the upper hand, using its advantage to prey on the other. Unless the balance is redressed, the complete destruction of the weaker is certain, and is followed in time by the death of the stronger. The fungus being the dominant partner, the balance, he considers, is tipped in its favour.

Elenkin’s conclusions are not borne out by the long continued and healthy life of the lichen. There is no record of either symbiont having succumbed to the other, and the alga, when set free, is unchanged and able to resume its normal development. Without the alga the fungus cannot form the ascigerous fruit. Is that because as a parasite within the lichen it has degenerated past recovery, or has it become so adapted to symbiosis that in saprophytic conditions it fails to develop?

Another Russian lichenologist, U. N. Danilov[230], records results which would seem to support the theory of parasitism. He found that from the clasping hyphae minute haustoria were produced, which penetrate the algal cell-wall, and branch when within the outer membrane, thus forming a delicate network over the plasma; secondary haustoria arising from this network protrude into the interior and rob the cell-contents. He observed gonidia filled with well-developed hyphae and these, after having exhausted one cell, travel onwards to others. Some gonidia under the influence of the fungus had become deformed and were finally killed. As a proof of this latter statement he adduces the presence in the thallus of some gonidia containing shrivelled protoplasm, of others entirely empty. He considers, as further evidence in favour of parasitism, the finding of empty membranes as[38] well as of colourless gonidia filled with the hyphal network. This description hardly tallies with the usual healthy appearance of the gonidial zone in the normal thallus, and it has been suggested that where the fungus filled the algal cell, it was as a saprophyte preying on dead material.

The gradual perishing of algal cells in time by natural decay and their subsequent absorption by the fungus is undisputed. It is open to question whether the varying results recorded by these workers have any further significance.

These observations of Elenkin and Danilov have been proved to be erroneous by Paulson and Somerville Hastings[231]. They examined the thalli of several lichens (Xanthoria parietina, Cladonia sp., etc.) collected in early spring when vegetative growth in these plants was found to be at its highest activity. They found an abundant increase of gonidia within the thallus, which they regarded as sporulation of the algae, and the most careful methods of staining failed to reveal any case of penetration of the gonidia by the hyphae.

Nienburg[232] has published some recent observations on the association of the symbionts. In the wide cortex of a Pertusaria he found not only the densely compact hyphae, but also isolated gonidia. In front of these latter there was a small hollow cavity and, behind, parallel hyphae rich in contents. These gonidia had originated from the normal gonidial zone. They were moved upward by special hyphae called by Nienburg “push-hyphae.” After their transportation, the algae at once divide and the products of division pass to a resting stage and become the centre of a new thalline growth. A somewhat similar process was noted towards the apex of Evernia furfuracea. Radial hyphae pushed up the cortex, leaving a hollow space over the gonidial zone. Into the space isolated algae were thrust by “push-hyphae.” In this lichen he also observed the penetration of the algal cell by haustoria of the fungus. He considers that the alga reaps advantage but also suffers harm, and he proposes the term helotism to express the relationship.

An instructive case of the true parasitism of a fungus on an alga has been described by Zukal[233] in the case of Endomyces scytonemata which he calls a “half-lichen.” The mature fungus formed small swellings on the filaments of the Scytonema and, when examined, the hyphae were seen to have attacked the alga, penetrating the outer gelatinous sheath and then using up the contents of the green cells. It is only after the alga has been destroyed and absorbed, that asci are formed by the fungus. Zukal contrasts the development of this fungus with the symbiotic growth of the two constituents in Ephebe where both grow together for an indefinite time.

Mere associated growth however even between a fungus and an alga does not constitute a lichen. An instance of such growth is described by[39] Sutherland[234] in an account of marine microfungi. One of these, a species of Mycosphaerella, was found on Pelvetia canaliculata, and Sutherland claims that as no apparent injury was done to the alga, it was a case of symbiosis and that there was formed a new type of lichen. The mycelium, always intercellular, pervaded the whole host-plant, and the fungal fruits were invariably formed on the algal receptacles close to the oogonia. Their position there is, of course, due to the greater food supply at that region. Both fungus and alga fruited freely. A closer analogy could have been found by the writer in the smut fungus which grows with the host-cereal until fruiting time; or with the mycorrhiza of Calluna which also pervades every part of the host-plant without causing any injury. In the true lichen, the alga, though constituting an important part of the vegetative body, takes no part in reproduction, except by division and increase of the vegetative cells within the thallus. The fruiting bodies are always of a modified fungal nature.

2. PHYSIOLOGY OF THE SYMBIONTS

The occurrence of isolated cases of parasitism—the fungus preying on the alga—in any case leaves the general problem unsolved. The whole question turns on the physiological activity and requirements of the two component elements of the thallus. From what sources do they each procure the materials essential to them as living organisms? It is chiefly a question of nutrition.

A. Nutrition of Algae

a. Character of Algal Cells. Gonidia are chlorophyll-containing bodies and assimilate carbon-dioxide from the atmosphere by photosynthesis as do the chlorophyll cells of other plants. They also require water and mineral salts which, in a free condition, they absorb from their immediate surroundings, but which, in the lichen thallus, they must obtain from the fungal hyphae. If the nutriment supplied to them in their inclosed position be greater or even equal to what the cells could procure as free-living algae, then they undoubtedly gain rather than lose by their association with the fungus, and are not to be considered merely as victims of parasitism.

b. Supply of Nitrogen. Important contributions on the subject of algal nutrition have been made by Beyerinck[235] and Artari[236]. The former conducted a series of culture experiments with green algae, including the gonidia of Physcia (Xanthoria) parietina. He successfully isolated the lichen gonidia and, at first, attempted to grow them on gelatine with an infusion of the Elm bark from which he had taken the lichen. Growth was[40] very slow and very feeble until he added to the culture-medium a solution of malt-extract which contains peptones and sugar. Very soon he obtained an active development of the gonidia, and they multiplied rapidly by division[237] as in the lichen thallus. This proved to him conclusively the great advantage to the algae of an abundant supply of nitrogen.

Artari in his work has demonstrated that there are two different physiological races of green algae: (1) those that absorb peptones—which he designates peptone-algae—and (2) those that do not so absorb peptones. He tested the cells of Cystococcus humicola taken from the thallus of Physcia parietina, and found that they belonged to the peptone group and were therefore dependent on a sufficiency of nitrogenous material to attain their normal vigorous growth. It was also discovered by Artari that the one race can be made by cultivation to pass over to the other: that ordinary algae can be educated to live on peptones, and peptone-algae to do without.

We learn further from Beyerinck’s researches that Ascomycetes, the group of fungi from which the hyphae of most lichens are derived, are what he terms ammonia-sugar fungi; that is to say, the hyphae can abstract nitrogen from ammonia salts and, with the addition of sugar, can form peptones. The lichen peptone-algae are thus evidently, by their contact with such fungi, in a favourable position for securing the nitrogenous food supply most suited to their requirements. In their deep-seated layers, they are to a large extent deprived of light, but it has been proved by Artari[238] in a series of culture experiments extending over a long period, that the gonidia of Xanthoria parietina remain green in the dark under very varied conditions of nutriment, though the colour is distinctly fainter.

Recently Treboux[239] has revised the work done by Artari and Beyerinck in reference to Cystococcus humicola. He denies that two physiological races are represented in this alga, the lichen gonidia, in regard to the nitrogen that they absorb, behaving exactly as do the free-living forms of the species. He finds that the gonidium is not a peptone-carbohydrate organism in the sense that it requires nitrogen in the form of peptones, inorganic ammonia salts being a more acceptable food supply. Treboux concludes that his results favour the view that the gonidia are in an unfavourable situation for receiving the kind of nitrogenous compound most advantageous to them, that they are therefore in a sense “victims” of parasitism, though he qualifies the condition as being a lichen-parasitism or helotism. This view does not accord with Chodat’s[240] results: in his cultures of gonidia he observed that with glycocoll or peptone, which are nearly equivalent, they developed four times better than with potassium nitrate as their nitrogenous food, and he concluded that they assimilated nitrogen better from bodies allied to peptides.

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c. Effect of Symbiosis on the Alga. Treboux’s observations however convinced him that the alga leads but a meagre existence within the thallus. Cell-division—the expression of active vitality—was, he held, of rare occurrence in the slowly growing lichen-plant, and zoospore formation in entire abeyance. He contrasts this sluggish increase[241] with the rapid multiplication of the free-living algal cells which cover whole tree-trunks with their descendants in a comparatively short time. These latter cells, he finds, are indeed rather smaller, being generally the products of recent division, but mixed with them are numbers of larger resting cells, comparable in size with the lichen gonidia. He states further, that the gonidia are less brightly green and, as he judges, less healthy, though in soredial formation or in the open they at once regain both colour and power of division. Treboux had entirely failed to observe the sporulation which is so abundant at certain seasons.

Their quick recovery seems also a strong argument in favour of the absolutely normal condition of metabolism within the gonidial cell; and the paler appearance of the chlorophyll is doubtless associated with the acquisition of carbohydrates from other sources than by photosynthesis. There is a wide difference between any degree of unfavourable life-conditions and parasitism however slight, even though the balance of gain is on the side of the fungus. It is not too fanciful to conclude that the demand for nitrogen on the part of the alga has influenced its peculiar association with the fungus. In the thallus of hypophloeodal lichens it has been proved indeed that the alga Trentepohlia with apical growth is an active agent in the symbiotic union. Cystococcus and other green algal cells are stationary, but they are doubtless equally ready for—as many of them are equally benefited by—the association. Keeble[242] has pointed out in the case of Convoluta roscoffensis that nitrogen-hunger induces the green algae to combine forces with an animal organism, though the benefit to them is only temporary and though they are finally sacrificed. The lichen gonidia, on the contrary, persist for a long time, probably far beyond their normal period of existence as free algae.

Examples of algal association with other plants might be cited here: of Nostoc in the roots of Cycas and in the cells of Anthoceros, and of Anabæna in the leaf-cells of Azolla, but in these instances it is generally held that the alga secures only shelter. It was by comparing the lichen-association with the harmless invasion of Gunnera cells by Nostoc that Reinke[243] arrived at his conception of “consortism.”

d. Supply of Carbon. Carbon, the essential constituent of all organic life, is partly drawn from the carbon-dioxide of the air, and assimilated by[42] the green cells; it is also partly contributed by the fungus as a product of its metabolism. A proof of this is afforded by Dufrenoy[244]: he found a Parmelia growing closely round pine needles and even sending suckers into the stomata. He covered the lichen with a black cloth and after seven weeks found that the gonidia had remained very green. That growth had not been checked was evidenced by an unusual development of soredia and of spermogonia. Dufrenoy describes the condition as a parasitism of the algae on the fungus which in turn was drawing nourishment from the pine needles.

Artari[245] has proved that lichen gonidia can obtain carbohydrates from the substratum as well as by photosynthesis. He cultivated the gonidia of Xanthoria parietina and Placodium murorum on media which contained organic substances as well as mineral salts, while depriving them of atmospheric carbon-dioxide and in some cases of light also. The gonidia not only grew well but, even in the dark, they remained normally green, a phenomenon coinciding with Etard and Bouilhac’s[246] experience in growing Nostoc in the dark: with suitable culture media the alga retained its colour. Nostoc also grows in the dark in the rhizome of Gunnera. Radais’[247] experiments with Chlorella vulgaris confirmed these results. On certain organic media growth and cell-division were as rapid in the dark as in the light, and chlorophyll was formed. The colour was at first yellowish and the full green arrived slowly, especially on sugar media, but in ten days it was uniform and normal.

When making further experiments with the alga, Stichococcus bacillaris, Artari[248] found that it also grew well on an organic medium and that grape sugar was the most valuable carbonaceous food supply. Chodat[249] also found that sugar or glucose was a desirable ingredient of culture media.

Treboux[250], in his work on organic acids, has also proved by experimental cultures with a large series of algae, including the gonidia of Peltigera, that these green plants in the absence of light and in pure cultures would grow and form carbohydrates if the culture medium contained a small percentage of organic acids. The acids he employed were combined with potassium and were thus rendered neutral or slightly alkaline; acetate of potash proved to be the most advantageous compound of any that was tested. Amino-acids and ammonia salts were added to provide the necessary nitrogen. Oxalic acid and other organic acids of varying composition are peculiarly abundant in lichen tissues and may be a source of carbon supply. Marshall Ward[251] has found calcium carbonate crystals in the lower air-containing tissues of Strigula complanata.

Treboux finally concluded from his researches that just as fungi can[43] extract carbohydrates from many sources, so algae can secure their carbon supply in a variety of ways. He affirms that the metabolic activity of the alga in these cultural conditions is entirely normal, and the various cell-contents are formed as in the light. Whether, in this case, starch is formed directly from the acids or through a series of combinations has not been determined. Uhlir[252], with electric lighting, made successful cultures of Nostoc isolated from Collemaceae on silicic acid, proving thereby that these gonidia do not require a rich nutriment. A certain definite humidity was however essential, and bacteria were never eliminated as they are associated with the gelatinous membranes of Nostocaceae.

e. Nutrition within the Symbiotic Plant. Culture experiments bearing more directly on the nutrition of lichens as a whole were carried out by F. Tobler[253]. He proved that the gonidia had undoubtedly drawn on the calcium oxalate secreted by the hyphae for their supply of carbon. In a culture medium of poplar-bark gelatine he grew hyphae of Xanthoria parietina, and noted an abundant deposit of oxalate crystals on their cell-walls. A piece of the lichen thallus including both symbionts and grown on a similar medium formed no crystals, and microscopic examination showed that crystals were likewise absent from the hyphae of the thallus that had grown normally on the tree, the inference being that the gonidia used them up as quickly as they were deposited. It must be remembered in this connection, however, that Zopf[254] has stated that where lichen acids are freely formed as, for instance, in Xanthoria parietina, there is always less formation and deposit of calcium oxalate crystals, which may partly account for their absence in the normal thallus so rich in parietin.

Tobler next introduced lichen gonidia into a culture medium in which the isolated hyphal constituent of a thallus had been previously cultivated, and placed the culture in the dark. In these circumstances he found that the gonidia were able to thrive but formed no colour: they were obtaining their carbohydrates, he decided, not from photosynthesis, but from the excretory products such as calcium oxalate that had been deposited in the culture medium by the lichen hyphae. We may conclude with more or less certainty that the loss of carbohydrates, due to the partial deprivation of light and air suffered by the alga owing to its position in the lichen thallus, is more than compensated by a physiological symbiosis with the fungus[255]. It has indeed been proved that in the absence of free carbon-dioxide, algae may utilize the half-bound CO₂ of carbonates, chiefly those of calcium and magnesium, dissolved in water.

f. Affinities of Lichen Gonidia. Chodat[256] has, in recent years, made cultures of lichen gonidia with a view to discovering their relation to[44] free-living algae and to testing at the same time their source of carbon supply. He has come to the conclusion that lichen gonidia are probably in no instance the normal Protococcus viridis: they differ from that alga in the possession of a pyrenoid and in their reproduction by zoospores when free.

Careful cultures were made of different Cladonia gonidia which were morphologically indistinguishable, and which varied in size from 10 to 16µ in diameter, though smaller ones were always present. He recognized them to be species of Cystococcus: they have a pyrenoid[257] in the centre and a disc-like chromatophore more or less starred at the edge. These gonidia grew well on agar, still better on agar-glucose, but best of all with an addition of peptone to the culture. There was invariably at first a slight difference in form and colour in the mass between the gonidia of one species and those of another, but as growth continued they became alike.

In testing for carbon supply, he found that gonidia grew slowly without sugar (glucose), and that, as sources of carbon, organic acids could not entirely replace glucose though, in the dark, the gonidia used them to some extent; the colony supplied with potassium nitrate, and grown in the dark, had reached a diameter of only 2 mm. in three months. With glucose, it measured 5 mm. in three weeks, while in three months it formed large culture patches.

A further experiment was made to test their absorption of peptones by artificial cultures carried out both in the light and the dark. The gonidia grew poorly in all combinations of organic nitrogen compounds. When combined with glucose, growth was at once more vigorous though only half as much in the dark as in the light, the difference in this respect being especially noticeable in the gonidia from Cladonia pyxidata. He concludes that as gonidia in these cultures are saprophytic, so in the lichen thallus also they are probably more or less saprophytic, obtaining not only their nitrogen in organic form but also, when possible, their carbon material as glucose or galactose from the hyphal symbiont which in turn is saprophytic on humus, etc.

B. Nutrition of Fungi

Fungi being without chlorophyll are always indebted to other organisms for their supply of carbohydrates. There has never therefore been any question as to the advantage accruing to the hyphal constituent in the composite thallus. The gonidia, as various workers have proved, have also a marked preference for organized nourishment, and, in addition, they obtain carbon by photosynthesis. Chodat[258] considers that probably they are thus able to assimilate carbon-dioxide in excess, a distinct advantage to the hyphae. In some instances the living gonidium is invaded and the contents[45] used up by the fungus and any dead gonidia are likewise utilized for food supply. It is also taken for granted that the fungus takes advantage of the presence of humus whether in the substratum or in aerial dust. In such slow growing organisms, there is not any large demand for nourishment on the part of the hyphae: for many lichens it seems to be mere subsistence with a minimum of growth from year to year.

C. Symbiosis of other Plants

The conception of an advantageous symbiosis of fungi with other plants has become familiar to us in Orchids and in the mycorhizal formation on the roots of trees, shrubs, etc. Fungal hyphae are also frequent inhabitants of the rhizoids of hepatics though, according to Gargeaune[259], the benefit to the hepatic host-plant is doubtful.

An association of fungus and green plant of great interest and bearing directly on the question of mutual advantage has been described by Servettaz[260]. In his study of mosses, he was able to confirm Bonnier’s[261] account of lichen hyphae growing over such plants as Vaucheria and the protonema of mosses, which is undoubtedly hurtful; but he also found an association of a moss with one of the lower fungi, Streptothrix or Oospora, which was distinctly advantageous. In separate cultivation the fungus developed compact masses and grew well in peptone agar broth.

Cultures of the moss, Phascum cuspidatum, were also made from the spores on a glucose medium. The specimens in association with the fungus were fully grown in two months, while the control cultures, without any admixture of the fungus, had not developed beyond the protonema stage. Servettaz draws attention to the proved fact that, in certain instances, plants benefit when provided with substances similar to their own decay products, and he considers that the fungus, in addition to its normal gaseous products, has elaborated such substances, as acid products, from the glucose medium to the great advantage of the moss plant.

A symbiotic association of Nostoc with another alga, described by Wettstein[262], is also of interest. The blue-green cells were lodged in the pyriform outgrowths of the siphoneous alga, Botrydium pyriforme Kütz., which the author of the paper places in a new genus, Geosiphon. The sheltering Nostoc symbioticum fills all of the host left vacant by the plasma, and when the season of decay sets in, it forms resting spores which migrate into the rhizoids of the host, so that both plants regenerate together.

Wettstein has compared this symbiotic association with that of lichens, and finds the analogy all the more striking in that the membrane of his new alga had become chitinous, which he thinks may be due to organic nutrition.

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II. LICHEN HYPHAE

A. Origin of Hyphae

Lichen hyphae form the ground tissue of the thallus apart from the gonidia or algal cells. They are septate branched filaments of single cell rows and are colourless or may be tinged by pigments or lichen acids to some shade of yellow, brown or black. They are of fungal nature, and are produced by the mature lichen spore.

The germination of the spore was probably first observed by Meyer[263]. His account of the actual process is somewhat vague, and he misinterpreted the subsequent development into thallus and fruit entirely for want of the necessary magnification; but that he did succeed in germinating the spores is unquestionable. He cultivated them on a smooth surface and they grew into a “dendritic formation”—a true hypothallus. Many years later the development of hyphae from lichen spores was observed by Holle[264] who saw and figured the process unmistakably in Borrera (Physcia) ciliaris.

A series of spore cultures was undertaken by Tulasne[265] with the twofold object of discovering the exact origin of hyphae and gonidia and of their relationship to each other. The results of his classical experiment with the spores of Verrucaria muralis—as interpreted by him—were accepted by the lichenologists of that time as conclusive evidence of the genetic origin of the gonidia within the thallus.

Fig. 14. Germinating spores of Verrucaria muralis Ach. after two months’ culture × ca. 500 (after Tulasne).

The spores of the lichen in large numbers had been sown by Tulasne in early spring on the smooth polished surface of a piece of limestone, and were covered with a watch-glass to protect them from dust, etc. At irregular intervals they were moistened with water, and from time to time[47] a few spores were abstracted from the culture and examined microscopically. Tulasne observed that the spore did not increase or change in volume in the process of germination, but that gradually the contents passed out into the growing hyphae, till finally a thin membrane only was left and still persisted after two months (Fig. 14). For a considerable time there was no septation; at length cross-divisions were formed, at first close to the spore, and then later in the branches. The hyphae meanwhile increased in dimension, the cells becoming rounder and somewhat wider, though always more slender than the spore which had given rise to them. In time a felted tissue was formed with here and there certain cells, filled with green colouring matter, similar to the gonidia of the lichen and thus the early stages at least of a new thallus were observed. The green cells, we now know, must have gained entrance to the culture from the air, or they may have been introduced with the water.

B. Development of lichenoid Hyphae

Lichen hyphae are usually thick-walled, thus differing from those of fungi generally, in which the membranes, as a rule, remain comparatively thin. This character was adduced by the so-called “autonomous” school as a proof of the fundamental distinction between the hyphal elements of the two groups of plants. It can, however, easily be observed that, in the early stages of germination, the lichen hyphae, as they issue from the spore, are thin-walled and exactly comparable with those of fungi. Growth is apical, and septation and branching arise exactly as in fungi, and, in certain circumstances, anastomosis takes place between converging filaments. But if algae are present in the culture the peculiar lichen characteristics very soon appear.

Bonnier[266], who made a large series of synthetic cultures, distinguishes three types of growth in lichenoid hyphae (Fig. 15):

1. Clasping filaments, repeatedly branched, which attach and surround the algae.

2. Filaments with rather short swollen cells which ultimately form the hyphal tissues of cortex and medulla.

3. Searching filaments which elongate towards the periphery and go to the encounter of new algae.

In five days after germination of the spores, the clasping hyphae had laid hold of the algae which meanwhile had increased by division; the swollen cells had begun to branch out and ten days later a differentiation of tissue was already apparent. The searching filaments had increased in number and length, and anastomosis between them had taken place when[48] no further algae were encountered. The cell-walls of the swollen hyphae and their branches had begun to thicken and to become united to form a kind of cellular tissue or “paraplectenchyma[267].” At a later date, about a month after the sowing of the spores, there was a definite cellular cortex formed over the thallus. The hyphal cells are uninucleate, though in the medulla they may be 1-2-nucleate.

Fig. 15. Synthetic culture of Physcia parietina spores and Protococcus viridis five days after germination. s, lichen-spore; a, septate filaments; b, clasping filaments; c, searching filaments. × 500 (after Bonnier).

The hyphae in close contact with the gonidia remain thin-walled, and have been termed by Wainio[268] “meristematic.” They furnish the growing elements of the lichen either apical or intercalary. In most genera the organs of fructification take rise from them, or in their immediate neighbourhood, and isidia and soredia also originate from these gonidial hyphae.

As the filaments pass from the gonidial zone to other layers, the cell-walls become thicker with a consequent reduction of the cell-lumen, very noticeable in the pith, but carried to its furthest extent in the “decomposed” cortex where the cells in the degenerate tissue often become reduced to disconnected streaks indicating the cell-lumen, and the outer cortical layer is merely a continuous mass of mucilage.

All lichen tissues arise from the branching and septation of the hyphae, the septa always forming at right angles to the long axis of the filaments. There is no instance of longitudinal cell-division except in the spores of certain genera (Collema, Urceolaria, Polyblastia, etc.). The branching of the hypha is dichotomous or lateral, and very irregular. Frequent septation and coherent growth result in the formation of plectenchyma.

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C. Culture of Hyphae without Gonidia

Artificial cultures had demonstrated the germination of lichen spores, with the formation of hyphae, and from synthetic cultures of fungus and alga complete lichen plants had been produced. To Möller[269] we owe the first cultures of a thalline body from the fungus alone, both from spermatia and from ascospores. The germination of the spermatia has a direct bearing on their function as spores or as sexual organs and is described in a later chapter.

The ascospores of Lecanora subfusca were caught in a drop of water on a slide as they were ejaculated from the ascus, and, on the following day, a very fine germinating tube was seen to have pierced the exospore. The hypha became slightly thicker, and branching began on the third day. If in water alone the culture soon died off, but in a nutrient solution growth slowly continued. The hyphae branched out in all directions from the spore as a centre and formed an orbicular expansion which in fourteen days had reached a size of ·1 mm. in diameter. After three weeks’ growth it was large enough to be visible without a lens; the mycelial threads were more crowded, and certain terminal hyphae had branched upwards in an aerial tuft, this development taking place from the centre outwards. Möller marked this stage as the transition from a mere protothallus to a thallus formation. In three months a diameter of 1·5-2 mm. was reached; a transverse section gave a thickness of ·86 mm. and from the under side loose hyphae branched downwards and attached the thallus, when it had been transferred to a solid substratum such as cork. Above these rhizoidal hyphae, a stratum of rather loose mycelium represented the medulla, and, surmounting that, a cortical layer in which the hyphae were very closely compacted. Delicate terminal branches rose into the air over the whole surface, very similar in character to hypothallic hyphae at the margin of the thallus.

Lecanora subfusca has a rather small simple spore; it emitted germinating tubes from each end, and a septum across the middle of the spore appeared after germination had taken place. Another experiment was with a much larger muriform spore measuring 80 µ in length and 20 µ in thickness. On germination about 20 tubes were formed, some of them rising into the air at once, the others encircling the spore, so that the thallus took form immediately; growth in this case also was centrifugal. In three months a diameter of 6 mm. was reached with a thickness of 1 to 2 mm. and showing a differentiation into medulla and cortex. The hyphae did not increase in width, but frequently globose or ovate swellings arose in or at the ends, a character which recurs in the natural growth of hyphae both of lichens and of Ascomycetes. These swellings depend on the nutrition.

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Pertusaria communis possesses a very large simple spore, but it is multinucleate and germinates with about 100 tubes which reach their ultimate width of 3 to 4 µ before they emerge from the exospore. The hyphae encircle the spore, and an opaque thalline growth is quickly formed from which rise terminal hyphal branches. In ten weeks the differentiation into medulla and cortex was reached, and in five months the hyphal thallus measured 4 mm. in diameter and 1 to 2 mm. in thickness.

Möller instituted a comparison between the thalli he obtained from the spores and those from the spermatia of another crustaceous lichen, Buellia punctiformis (B. myriocarpa). After germination had taken place the hyphae from the spermatia grew at first more quickly than those from the ascospores, but as soon as thallus formation began the latter caught up and, in eight weeks, both thalli were of equal size.

Another comparative culture with the spermatia and ascospores of Opegrapha subsiderella gave similar results: the spores of that species are elongate-fusiform and 6-to 8-septate; germination took place from the end cells in two to three days after sowing. The germinating hyphae corresponded exactly with those from the spermatia and growth was equally slow in both. The middle cells of the spores may also produce germinating tubes, but never more than about five were observed from any one spore. A browning of the cortical layer was especially apparent in the hyphal culture from another lichen, Graphis scripta: a clear brown colour gradually changing to black appeared about the same period in all the cultures.

The hyphae from the spores of Arthonia developed quickest of all: the hyphae were very slender, but in three to four months the growth had reached a diameter of 8 mm. In this plant there was the usual outgrowth of delicate hyphae from the surface; no definite cortical layer appeared, but only a very narrow line of more closely interwoven somewhat darker hyphae. Frequently, from the surface of the original thallus, excrescences arose which were the beginnings of further thalli.

Tobler[270] experimenting with Xanthoria parietina gained very similar results. The spores were grown in malt extract for ten days, then transferred to gelatine. In three to five weeks there was formed an orbicular mycelial felt about 3 mm. in diameter and 2 mm. thick. The mycelium was frequently brownish even in healthy cultures, but the aerial hyphae which, at first, rose above the surface were always colourless. After these latter disappeared a distinct brownish tinge of the thallus was visible. In seven months it had increased in size to 15 mm. in length, 7 mm. in width and 3 mm. thick with a differentiation into three layers: a lower rather dense tissue representing the pith, above that a layer of loose hyphae where the gonidial zone would[51] normally find place, and above that a second compact tissue, or outer cortex, from which arose the aerial hyphae. The culture could not be prolonged more than eight months.

D. Continuity of Protoplasm in Hyphal Cells

Wahrlich[271] demonstrated that continuity of protoplasm was as constant between the cells of fungi as it has been proved to be between the cells of the higher plants. His researches included the hyphae of the lichens, Cladonia fimbriata and Physcia (Xanthoria) parietina.

Baur[272] and Darbishire[273] found independently that an open connection existed between the cells of the carpogonial structures in the lichens they examined. The subject as regards the thalline hyphae was again taken up by Kienitz-Gerloff[274] who obtained his best results in the hypothecial tissue of Peltigera canina and P. polydactyla. Most of the cross septa showed one central protoplasmic strand traversing the wall from cell to cell, but in some instances there were as many as four to six pits in the walls. The thickening of the cell-walls is uneven and projects variously into the cavity of the cell. Meyer’s[275] work was equally conclusive: all the cells of an individual hypha, he found, are in protoplasmic connection; and in plectenchymatous tissue the side walls are frequently perforated. Cell-fusions due to anastomosis are frequent in lichen hyphae, and the wall at or near the point of fusion is also traversed by a thread of protoplasm, though such connections are regarded as adventitious. Fusions with plasma connections are numerous in the matted hairs on the upper surface of Peltigera canina and they also occur between the hyphae forming the rhizoids of that lichen. The work of Salter[276] may also be noted. He claimed that his researches tended to show complete anatomical union between all the tissues of the lichen plant, not only between the hyphae of the various tissues but also between hyphae and gonidia.

III. LICHEN ALGAE

A. Types of Algae

The algal constituents of the lichen thallus belong to the two classes, Myxophyceae, generally termed blue-green algae, and Chlorophyceae which are coloured bright-green or yellow-green. Most of them are land forms, and, in a free condition, they inhabit moist or shady situations, tree-trunks, walls, etc. They multiply by division or by sporulation within the thallus; zoospores are never formed except in open cultivation. The determination of the genera and species to which the lichen algae severally belong is often uncertain, but their distribution within the lichen kingdom is as follows:

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a. Myxophyceae associated with Phycolichens. The blue-green algae are characterized by the colour of their pigments which persists in the gonidial condition giving various tints to the component lichens, and by the gelatinous sheath in which most of them are enclosed. This sheath, both in the lichen gonidia[277] and in free-living forms, imbibes and retains moisture to a remarkable extent and the thallus containing blue-green algae profits by its power of storing moisture. Myxophyceae form the gonidia of the gelatinous lichens as well as of some other non-gelatinous genera. Several families are represented[278]:

Fam. Chroococcaceae. This family includes unicellular algae with thick gelatinous sheaths. They increase normally by division, and colonies arise by the cohesion of the cells. Several genera form gonidia:

1. Chroococcus Naeg. Solitary or forming small colonies of 2-4-8 cells (Fig. 16) generally surrounded by firm gelatinous colourless sheaths in definite layers (lamellate). Chroococcus is considered by some lichenologists to form the gonidium of Cora, a genus of Hymenolichens.

2. Microcystis Kütz. Globose or subglobose cells forming large colonies surrounded by a common gelatinous layer (gonidia of Coriscium).

Fig. 16. Examples of Chroococcus. A, Ch. giganteus West; B, Ch. turgidus Naeg.; C and D, Ch. schizodermaticus West × 450 (after West).

Fig. 17. Gloeocapsa magma Kütz. × 450 (after West).

3. Gloeocapsa Kütz. (including Xanthocapsa). Globose cells with a lamellate gelatinous wall, forming colonies enclosed in a common sheath (Fig. 17); the inner integument is often coloured red or orange. These[53] two genera form the gonidia in the family Pyrenopsidaceae. Gloeocapsa polydermatica Kütz. has been identified as a lichen gonidium.

Fam. nostocaceae. Filamentous algae unbranched and without base or apex.

Nostoc Vauch. Composed of flexuous trichomes, with intercalary heterocysts (colourless cells) (Fig. 18). Dense gelatinous colonies of definite form are built up by cohesion. In some lichens the trichomes retain their chain-like appearance, in others they are more or less broken up and massed together, with disappearance of the gelatinous sheath (as in Peltigera); colour mostly dark blue-green.

Fig. 18. Examples of Nostoc. N. Linckia Born. A, nat. size; B, small portion × 340; C, N. coerulescens Lyngbye, nat. size (after West).

Fig. 19. Example of Scytonema alga. S. mirabile Thur. C, apex of a branch; D, organ of attachment at base of filament. × 440 (after West).

Nostoc occurs in a few or all of the genera of Pyrenidiaceae, Collemaceae, Pannariaceae, Peltigeraceae and Stictaceae, and N. sphaericum Vauch.[54] (N. lichenoides Kütz.) has been determined as the lichen gonidium. When the chains are broken up it has been wrongly classified as another alga, Polycoccus punctiformis.

Fam. Scytonemaceae. Trichomes of single-cell rows, differentiated into base and apex. Pseudo-branching arises at right angles to the main filament.

Scytonema Ag. Pseudo-branches piercing the sheath and passing out as twin filaments (Fig. 19); colour, golden-brown. This alga occurs in genera of Pyrenidiaceae, Ephebaceae, Pannariaceae, Heppiaceae, in Petractis a genus of Gyalectaceae, and in Dictyonema one of the Hymenolichens.

Fam. Stigonemaceae. Trichomes of several-cell rows with base and apex; colour, golden-brown.

Stigonema Ag. Stouter than Scytonema, with transverse and vertical division of the cells, and generally copious branching (Fig. 20). This alga occurs only in a few genera of Ephebaceae. S. panniforme Kirchn. (Sirosiphon pulvinatus Bréb.) has been determined as forming the gonidium.

Fam. Rivulariaceae. Trichomes with a heterocyst at the base and tapering upwards, enclosed in mucilage (Fig. 21).

Fig. 20. Stigonema sp. × 200 (after Comère).

Fig. 21. Examples of Rivularia; A, B, C, R. Biasolettiana Menegh.; D and E, R. minutula Born. and Fl. A and D nat. size; B, C and E × 480 (after West).

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Rivularia Thuret. In tufts fixed at the base and forming roundish gelatinous colonies; colour, blue-green. The gonidium of Lichinaceae has been identified as R. nitida Ag.

Algae belonging to one or other of these genera of Myxophyceae also combine with the hyphae of Archilichens to form cephalodia[279] and Krempelhuber[280] has recorded and figured a blue-green alga, probably Gloeocapsa, in Baeomyces paeminosus from the South Sea Islands. They also form the gonidia in a few species and genera of such families as Stictaceae and Peltigeraceae.

b. Chlorophyceae associated With Archilichens. The lichens of this group are by far the most numerous both in genera and species, though fewer algal families are represented.

Fam. Protococcaceae. Consisting of globular single cells, aggregated in loose colonies, dividing variously.

Fig. 22. Pleurococcus vulgaris Menegh. (Protococcus viridis Ag.). chl. chloroplast; p. protoderma stage; pa, palmelloid stage; py, pyrenoid. × 520 (after West).

1. Protococcus viridis Ag. (Pleurococcus vulgaris Menegh., Cystococcushumicola Naeg.). Cells dividing into 2, 4 or 8 daughter-cells and not separating readily; in excessive moisture forming short filaments. The cells contain parietal chloroplasts, and, according to Chodat[281], are without a pyrenoid (Fig. 22). This alga, and allied species, forms the familiar green coating of tree-trunks, walls etc., and, in lichenological literature, are quoted as the gonidia of most of the crustaceous foliose and fruticose lichens. Chodat[281], who has recently made comparative artificial cultures of algae, throws doubt on the identity of many such gonidia. He lays great emphasis on the presence or absence of a pyrenoid in algal cells. West, on the contrary, considers the pyrenoid as an inconstant character. Chodat insists that the gonidia that contain pyrenoids belong to another genus, Cystococcus Chod. (non Naeg.), a pyrenoid-containing alga, which, in addition to multiplying by division of the cells, also forms spores and zoospores when cultivated. He further records the results of his cultures of gonidia, and finds that those taken from closely related lichens, such as different species of Cladonia, though they are alike morphologically, yet show constant variations in the culture colonies. These, he holds, are sufficient to indicate difference of race if not[56] of species and he designates the algae, according to the lichen in which they occur, as Cystococcus Cladoniae pyxidatae, C. Cladoniae fimbriatae, etc.

Fig. 23. Cystococcus Cladoniae pyxidatae Chod. from culture × 800 (after Chodat).

Fig. 23 A. A, C, Chlorella vulgaris Beyer. B and C, stages in division × about 800 (after Chodat); E, Chl. faginea Wille × 520 (after Gerneck); F-I Chl. miniata; F, vegetable cell; G-I, formation and escape of gonidia × 1000 (after Chodat).

Meanwhile Paulson and Somerville Hastings[282] by their careful research on the growing thallus have thrown considerable light on the identity of the Protococcaceous lichen gonidium. They selected such well-known lichens as Xanthoria parietina, Cladonia spp. and others, which they collected during the spring months, February to April, the period of most active growth. Many of the gonidia, they found, were in a stage of reproduction, that showed a simultaneous rounding off of the gonidium contents into globose bodies varying in number up to 32. Chodat had figured this method of “sporulation” in his cultures of the lichen gonidium both in Chlorella Beij. and in Cystococcus Chod. (Fig. 23). It has now been abundantly proved that this form of increase is of frequent occurrence in the thallus itself. Chlorella has been suggested as probably the alga forming these gonidia and recently West has signified his acquiescence in this view[283].

2. Chlorella Beij. Occurring frequently on damp ground, bark of trees, etc., dividing into numerous daughter-cells, probably reduced zoogonidia (Fig. 23).

Chodat distinguishes between Cystococcus and Chlorella in that Cystococcus may form zoospores (though rarely), Chlorella only aplanospores. He found three gonidial species, Chlorella lichina in Cladonia rangiferina, Ch. viscosa and Ch. Cladoniae in other Cladonia spp.

3. Coccobotrys Chod. The cells of this new algal genus are smaller than those of Cystococcus or Protococcus and have no pyrenoid. They were isolated by Chodat from the thallus of Verrucaria nigrescens (Fig. 24), and, as they have thick membranes, they adhere in a continuous layer or thallus. Chodat also claims to have isolated a species of Coccobotrys from Dermatocarpon miniatum, a foliose Pyrenolichen.

4. Coccomyxa Schmidle. Cells ellipsoid, also without a pyrenoid. Two species were obtained by Chodat from the thallus of Solorinae and are recorded as Coccomyxa Solorinae croceae and C. Solorinae saccatae.

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Coccomyxa subellipsoidea is given[284] as the gonidium of the primitive lichen Botrydina vulgaris (Fig. 25). The cells are surrounded by a common gelatinous sheath.

Fig. 24. Coccobotrys Verrucariae Chod. from culture × 800 (after Chodat).

Fig. 25. Coccomyxa subellipsoidea Acton. Actively dividing cells, the dark portions indicating the chloroplasts × 1000 (after Acton).

5. Diplosphaera Bial.[285] D. Chodati was taken from the thallus of Lecanora tartarea and successfully cultivated. It resembles Protococcus, but has smaller cells and grows more rapidly; it is evidently closely allied to that genus, if not merely a form of it.

6. Urococcus Kütz. Cells more or less globose, rather large, and coloured with a red-brown pigment, with the cell-wall thick and lamellate, forming elongate strands of cells (Fig. 26). Recorded by Hue[286] in the cephalodium of Lepolichen coccophorus, a Chilian lichen.

Fam. Tetrasporaceae. Cells in groups of 2 or 4 surrounded by a gelatinous sheath.

1. Palmella Lyngb. Cells globose, oblong or ellipsoid, grouped without order in a formless mucilage (Fig. 27). Among lichens associated with Palmella are the Epigloeaceae and Chrysothricaceae.

Fig. 26. Urococcus sp. Group of cells much magnified (after Hassall).

Fig. 27. Palmella sp. × 400 (after Comère).

Fig. 28. Gloeocystis sp. × 400 (after Comère).

2. Gloeocystis Naeg. Cells oblong or globose with a lamellate sheath forming small colonies; colour, red-brown (Fig. 28). This alga along with Urococcus was found by Hue in the cephalodia of Lepolichen coccophora, but whereas Gloeocystis frequently occupies the cephalodium alone, Urococcus is always accompanied by Scytonema, the normal gonidium of the cephalodium.

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Fig. 29. A, Trentepohlia umbrina Born.; B, T. aurea Mart. × 300 (after Kütz.).

Fig. 30. Example of Cladophora. Cl. glomerata Kütz. A, nat. size; B, × 85 (after West).

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Fam. Trentepohliaceae. Filamentous and branched, the filaments short and creeping or long and forming tufts and felts or cushions; colour, brownish-yellow or reddish-orange.

Trentepohlia Born. Branching alternate; cells filled with red or orange oil; no pyrenoids (Fig. 29). A large number of lichens are associated with this genus: Pyrenulaceae, Arthoniaceae, Graphidaceae, Roccellaceae, Thelotremaceae, Gyalectaceae and Coenogoniaceae, etc., in whole or in part. Two species have been determined, T. umbrina Born., the gonidium of the Graphidaceae, and T. aurea which is associated with the only European Coenogonium, C. ebeneum (Fig. 3). Deckenbach[287] claimed that he had proved by cultures that T. umbrina was a growth stage of T. aurea.

Fam. Cladophoraceae. Filamentous, variously and copiously branched, the cells rather large and multinucleate.

Cladophora Kütz. Filaments branching, of one-cell rows, attached at the base; colour, bright or dark green; mostly aquatic and marine (Fig. 30). Only one lichen, Racodium rupestre, a member of the Coenogoniaceae, is associated with Cladophora. It is a British lichen, and is always sterile.

Fam. Mycoideaceae. Epiphytic algae consisting of thin discs which are composed of radiating filaments.

1. Mycoidea Cunningh. (Cephaleuros Kunze). In Mycoidea parasitica the filaments of the disc are partly erect and partly decumbent, reddish to green (Fig. 31). It forms the gonidium of the parasitic lichen, Strigula complanata, which was studied by Marshall Ward in Ceylon[288]. Zahlbruckner gives Phyllactidium as an alternative gonidium of Strigulaceae.

2. Phycopeltis Millard. Disc a stratum one-cell thick, bearing seta, adnate to the lower surface of the leaf, yellow-green in colour. Phycopeltis (Fig. 32) has been identified as the gonidium of Strigula complanata in New Zealand and of Mazosia (Chiodectonaceae), a leaf lichen from tropical America.

Fig. 31. Mycoidea parasitica Cunningh. much magnified (after Marshall Ward).

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There is some confusion as to the genera of algae that form the gonidia of these epiphyllous lichens. Phyllactidium given by Zahlbruckner as the gonidium of all the Strigulaceae (except Strigula in part) is classified by de Toni[289] as probably synonymous with Phycopeltis Millard, and as differing from Mycoidea parasitica in the mode of growth.

Fam. Prasiolaceae. Thallus filamentous, often expanded into broad sheets by the fusion of the filaments in one plane.

Prasiola Ag. Thallus filamentous, of one-to many-cell rows, or widely expanded (Fig. 33). The gonidium of Mastoidiaceae (Pyrenocarpeae).

Fig. 32. Phycopeltis expansa Jenn. much magnified (after Vaughan Jennings).

Fig. 33. Prasiola parietina Wille × 500 (after West).

B. Changes induced in the Alga

a. Myxophyceae. Though, as a general rule, the alga is less affected by its altered life-conditions than the fungus, yet in many instances it becomes considerably modified in appearance. In species of the genus Pyrenopsis—small gelatinous lichens—the alga is a Gloeocapsa very similar to G. magma. In the open it forms small colonies of blue-green cells surrounded by a gelatinous sheath which is coloured red with gloeocapsin. As a gonidium lying towards or on the outside of the granules composing the thallus, the red sheath of the cells is practically unchanged, so that the resemblance to Gloeocapsa is unmistakable. In the inner parts of the thallus, the colonies are somewhat broken up by the hyphae and the sheaths are not[61] only less evident but much more faintly coloured. In Synalissa, a minute shrubby lichen which has the same algal constituent, the tissue of the thallus is more highly evolved, and in it the red colour can barely be seen and then only towards the outside; at the centre it disappears entirely. The long chaplets of Nostoc cells persist almost unchanged in the thallus of the Collemaceae, but in heteromerous genera such as Pannaria and Peltigera they are broken up, or they are coiled together and packed into restricted areas or zones. The altered alga has been frequently described as Polycoccus punctiformis. A similar modification occurs in many cephalodia, so that the true affinity of the alga, in most instances, can only be ascertained after free cultivation.

Bornet[290] has described in Coccocarpia molybdaea the change that the alga Scytonema undergoes as the thallus develops: in very young fronds the filaments of Scytonema are unchanged and are merely enclosed between layers of hyphae. At a later stage, with increase of the thallus in thickness, the algal filaments are broken up, their covering sheath disappears, and the cells become rounded and isolated. Petractis (Gyalecta) exanthematica has also a Scytonema as gonidium, and equally exact observations have been made by Fünfstück[291] on the way it is transformed by symbiosis: with the exception of a very thin superficial layer, the thallus is immersed in the rock and is permeated by the alga to its lowest limits, 3 to 4 mm. below the surface, Petractis being a homoiomerous lichen. The Scytonema trichomes embedded in the rock become narrower, and the sheath, which in the epilithic part of the thallus is 4µ wide, disappears almost entirely. The green colour of the cells fades and septation is less frequent and less regular. The filaments in that condition are very like oil-hyphae and can only be distinguished as algal by staining reagents such as alkanna. They never seem to be in contact with the fungal elements: there is no visible appearance of parasitism nor even of consortism.

b. Chlorophyceae. As a rule the green-celled gonidium such as Protococcus is not changed in form though the colour may be less vivid, but in certain lichens there do occur modifications in its appearance. In Micarea (Biatorina) prasina, Hedlund[292] noted that the gonidium was a minute alga possessing a gelatinous sheath similar to that of a Gloeocapsa. He isolated the alga, made artificial cultures and found that, in the altered conditions, it gradually increased in size, threw off the gelatinous sheath and developed into normal Protococcus cells, measuring 7 to 10µ in diameter. The gelatinous sheath was thus proved to be merely a biological variation, probably of value to the lichen owing to its capacity to imbibe and retain moisture. Zukal[293] also made cultures of this alga, but wrongly concluded it was a Gloeocystis.

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Moebius[294] has described the transformation from algae to lichen gonidia in a species epiphytic on Orchids in Porto Rico. He had observed that most of the leaves were inhabited by a membranaceous alga, Phyllactidium, and that constantly associated with it were small scraps of a lichen thallus containing isolated globose gonidia. The cells of the alga, under the influence of the invading fungus, were, in this case, formed into isolated round bodies which divided into four, each daughter-cell becoming surrounded by a membrane and being capable, in turn, of further division.

Frank[295] followed the change from a free alga to a gonidium in Chroolepus (Trentepohlia) umbrinum, as shown in the hypophloeodal thalli of the Graphideae. The alga itself is frequent on beech bark, where it forms wide-spreading brownish-red incrustations consisting of short chains occasionally branched. The individual cells have thick laminated membranes and vary in width from 20 µ to 37 µ. The free alga constantly tends to penetrate below the cortical layers of the tree on which it grows, and the immersed cells become not only longer and of a thinner texture, but the characteristic red colour so entirely disappears, that the growing penetrating apical cell may be light green or almost colourless. As a lichen gonidium the alga undergoes even more drastic changes: the red oily granules gradually vanish and the cells become chlorophyll-green or, if any retain a bright colour, they are orange or yellow. The branching of the chains is more regular, the cells more elongate and narrower; usually they are about 13 to 21 µ long and 8 µ wide, or even less. Deeper down in the periderm, the chains become disintegrated into separate units. Another notable alteration takes place in the cell-membrane which becomes thin and delicate. It has, however, been observed that if these algal cells reach the surface, owing to peeling of the bark, etc., they resume the appearance of a normal Trentepohlia.

In certain cases where two kinds of algae were supposed to be present in some lichens, it has been proved that one species only is represented, the difference in their form being caused by mechanical pressure of the surrounding hyphae, as in Endocarpon and Staurothele where the hymenial gonidia are cylindrical in form and much smaller than those of the thallus. They were on this account classified by Stahl[296] under a separate algal genus, Stichococcus, but they are now known to be growth forms of Protococcus, the alga that is normally present in the thallus. Similar variations were found by Neubner[297] in the gonidia of the Caliciaceae, but, by culture experiments with the gonidia apart from the hyphae, he succeeded in demonstrating transition forms in all stages between the “Pleurococcus” cells and those of “Stichococcus,” though the characters acquired by the latter are transmitted to following generations. The transformation from spherical to cylindrical[63] algal cells had been also noted by Krabbe[298] in the young podetia of some species of Cladonia, the change in form being due to the continued pressure in one direction of the parallel hyphae.

Isolated algal cells have been observed within the cortex of various lichens. They are carried thither by the hyphae from the gonidial zone in the process of cortical formation, but they soon die off as in that position they are deprived of a sufficiency of air and of moisture. Forssell[299] found Xanthocapsa cells embedded in the hymenium of Omphalaria Heppii. They were similar to those of the thallus, but they were not associated with hyphae and had undergone less change than the thalline algae.

C. Constancy of Algal Constituents

Lichen hyphae of one family or genus, as a rule, combine with the same species of alga, and the continuity of genera and species is maintained. There are, however, related lichens that differ chiefly or only in the characters of the gonidia. Among such closely allied genera or sections of genera may be cited Sticta with bright-green algae and the section Stictina with blue-green; Peltidea similarly related to Peltigera and Nephroma to Nephromium. In the genus Solorina, some of the species possess bright-green, others blue-green algae, while in one, S. crocea[300], there is an upper layer of small bright-green gonidia that project in irregular pyramids into the upper cortex; while below these there stretches a more or less interrupted band of blue-green Nostoc cells. The two layers are usually separated by strands of hyphae, but occasionally they come into close contact, and the hyphal filaments pass from one zone to the other. In this genus cephalodia containing blue-green Nostoc are characteristic of all the “bright-green” species. Harmand[301] has recorded the presence of two different types of gonidia in Lecanora atra f. subgrumosa; one of them, the normal Protococcus alga of the species, the other, pale-blue-green cells of Nostoc affinity.

Forssell[302] states that in Lecanora (Psoroma) hypnorum, the normal bright-green gonidia of some of the squamules may be replaced by Nostoc. In that case they are regarded as cephalodia, though in structure they exactly resemble the squamules of Pannaria pezizoides, and Forssell considers that there is sufficient evidence of the identity of the hyphal constituent in these two lichens, the alga alone being different.

It may be that in Archilichens with a marked capacity to form a second symbiotic union with blue-green algae, a tendency to revert to a primitive condition is evident—a condition which has persisted wholly in Peltigera with its Nostoc zone, but is manifested only by cephalodia formation in the[64] Peltidea section of the genus. In this connection, however, we must bear in mind Forssell’s view that it is the Archilichens that are the more primitive[303].

The alien blue-green algae with their gelatinous sheaths are adapted to the absorption and retention of moisture, and, in this way, they doubtless render important service to the lichens that harbour them in cephalodia.

D. Displacement of Algae within the Thallus

a. Normal displacement. Lindau[304] has contrasted the advancing apical growth of the creeping alga Trentepohlia with the stationary condition of the unicellular species that multiply by repeated division or by sporulation, and thus form more or less dense zones and groups of gonidia in most lichens. The fungus in the latter case pushes its way among the algae and breaks up the compact masses by a shoving movement, thus letting in light and air. The growing hypha usually applies itself closely round an algal cell, and secondary branches arise which in time encircle it in a network of short cells. In the thallus of Variolaria[305] the hyphae from the lower tissues, termed push-hyphae by Nienburg[306], push their way into the algal groups and filaments composed of short cells come to lie closely round the individual gonidia. Continued growth is centrifugal, and the algae are carried outward with the extension of the hyphae (Fig. 12). Cell-division is more active at the periphery, that being the area of vigorous growth, and the algal cells are, in consequence, generally smaller in that region than those further back, the latter having entered more or less into a resting condition, or, as is more probable, these smaller cells are aplanospores not fully mature.

b. Local displacement. Specimens of Parmelia physodes were found several times by Bitter, the grey-green surface of which was marbled with whitish lines, caused by the absence of gonidia under these lighter-coloured areas. The thallus was otherwise healthy as was manifested by the freely fruiting condition: no explanation of the phenomenon was forthcoming. Bitter compared the condition with the appearance of lighter areas on the thallus of Parmelia obscurata.

Something of the same nature was observed on the thallus of a Peltigera collected by F. T. Brooks near Cambridge. The marking took the form of a series of concentric circles, starting from several centres. The darker lines were found on examination to contain the normal blue-green algal zone, while the colour had faded from the lighter parts. The cause of the difference in colouration was not apparent.

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E. Non-gonidial Organisms associated with Lichen Hyphae

Bonnier[307] made a series of cultures with lichen spores and green cells other than those that form lichen gonidia. In one instance he substituted Protococcus botryoides for the normal gonidia of Parmelia (Xanthoria) parietina; in another of his cultures he replaced Protococcus viridis by the filamentous alga Trentepohlia abietina. In both cases the hyphae attached themselves to the green cells and a certain stage of thallus formation was reached, though growth ceased fairly early. Another experiment made with the large filaments of Vaucheria sessilis met with the same amount of success (Fig. 34). The germinating hyphae attached themselves to the alga and grew all round it, but there was no advance to tissue formation.

Cultures were also made with the protonema of mosses. Either spores of mosses and lichens were germinated together, or lichen spores were sown in close proximity to fully formed protonemata. The developing hyphae seized on the moss cells and formed a network of branching anastomosing filaments along the whole length of the protonema without, however, penetrating the cells. If suitable algae were encountered, proper thallus formation commenced, and Bonnier considers that the hyphae receive stimulus and nourishment from the protonema sufficient to tide them over a considerable period, perhaps until the algal symbiont is met. An interesting variation was noted in connection with the cultures of Mnium hornum[308]. If the protonema were of the usual vigorous type, the whole length was encased by the hyphal network; but if it were delicate and slender, the protoplasm collected in the cell that was touched by hyphae and formed a sort of swollen thick-walled bud (Fig. 35). This new body persisted when the rest of the filament and the hyphae had disappeared, and, in favourable conditions, grew again to form a moss plant.

Fig. 34. Germinating hyphae of Lecanora subfusca Ach., growing over the alga Vaucheria sessilis DC., much magnified (after Bonnier).

F. Parasitism of Algae on Lichens

A curious instance of undoubted parasitism by an alga, not as in Strigula on one of the higher plants, but on a lichen thallus, is recorded by Forssell[309]. A group of Protococcus-like cells established on the thallus[66] of Peltigera had found their way into the tissue, the underlying cortical cells having degenerated. The blue-green cells of the normal gonidial layer had died off before their advance but no zone was formed by the invading algae; they simply withdrew nourishment and gave seemingly no return. The phenomenon is somewhat isolated and accidental but illustrates the capacity of the alga to absorb food supply from lichen hyphae.

Fig. 35. Pure culture of protonema of Mnium hornum L. with spores and hyphae of Lecidea vernalis Ach. a,a,a, buds forming × 150 (after Bonnier).

An instance of epiphytic growth has also been recorded by Zahlbruckner[310]. He found an alga, Trentepohlia abietina, covering the thallus of a Brazilian lichen, Parmelia isidiophora, and growing so profusely as to obscure the isidiose character towards the centre of the thallus. There was no genetic connection of the alga with the lichen as the former was not that of the lichen gonidium. Lichen thalli are indeed very frequently the habitat of green algae, though their occurrence may be and probably is accidental.

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CHAPTER III
MORPHOLOGY

GENERAL ACCOUNT OF LICHEN STRUCTURE

I. ORIGIN OF LICHEN STRUCTURES

The two organisms, fungus and alga, that enter into the composition of the lichen plant are each characterized by the simplicity of their original structure in which there is little or no differentiation into tissues. The gonidia-forming algae are many of them unicellular, and increase mainly by division or by sporulation into daughter-cells which become rounded off and repeat the life of the mother-cell; others, belonging to different genera, are filaments, mostly of single cell-rows, with apical growth. The hyphal elements of the lichen are derived from fungi in which the vegetative body is composed of branching filaments, a character which persists in the lichen thallus.

The union of the two symbionts has stimulated both, but more especially the fungus, to new developments of vegetative form, in which the fungus, as the predominant partner, provides the framework of the lichen plant-body. Varied structures have been evolved in order to secure life conditions favourable to both constituents, though more especially to the alga; and as the close association of the assimilating and growing tissues is maintained, the thallus thus formed is capable of indefinite increase.

A. Forms of Cell-Structure

There is no true parenchyma or cellular structure in the lichen thallus such as forms the ground tissue of the higher plants. The fungal hyphae are persistently filamentous and either simple or branched. By frequent and regular cell-division—always at right angles to the long axis—and by coherent growth, a pseudoparenchyma may however be built up which functions either as a protective or strengthening tissue (Fig. 36).

Fig. 36. Vertical section of young stage of stratose thallus (Xanthoria parietina Th. Fr.). a, plectenchyma of cortex; b, medullary hyphae; c, gonidial zone. × 500 (after Schwendener).

Lindau[311] proposed the name “plectenchyma” for the tangled weft of hyphae that is the principal tissue system in fungi as well as lichens. The more elaborated pseudoparenchyma he designates as “paraplectenchyma,” while the term “prosoplectenchyma” he reserved for the fibrous[68] or chondroid strands of compact filaments that occur frequently in the thallus of the larger fruticose lichens, and are of service in strengthening the fronds. The term plectenchyma is now generally used for pseudoparenchyma.

B. Types of Thallus

Three factors, according to Reinke[312], have been of influence in determining the thalline development. The first, and most important, is the necessity to provide for the work of photosynthesis on the part of the alga. There is also the building up of a tissue that should serve as a storage of reserve material, essential in a plant the existence of which is prolonged far beyond the natural duration of either of the component organisms; and, finally, there is the need of protecting the long-lived plant as a whole though more particularly the alga.

Wallroth was the first to make a comparative study of the different lichen thalli. He distinguished those lichens in which the green cells and the colourless filaments are interspersed equally through the entire thallus as “homoiomerous” (Fig. 2), and those in which there are distinct layers of cortex, gonidia, and medulla, as “heteromerous” (Fig. 1), terms which, though now considered of less importance in classification, still persist and are of service in describing the position of the alga with regard to the general structure. A less evident definition of the different types of thallus has been proposed by Zukal[313] who divides them into “endogenous” and “exogenous.”

a. Endogenous Thallus. The term has been applied to a comparatively small number of homoiomerous lichens in which the alga predominates in the development, and determines the form of the thallus. These algae, members of the Myxophyceae, are extremely gelatinous, and the hyphae grow alongside or within the gelatinous sheath. In the simpler forms the vegetative structure is of the most primitive type: the alga retains its original character almost unchanged, and the ascomycetous fungus grows along with and beside it (Fig. 4). Such are the minutely tufted thalli of Thermutis and Spilonema and the longer strands of Ephebe, in which the associated Scytonema or Stigonema, filamentous blue-green algae, though excited to excessive growth, scarcely lose their normal appearance, making it difficult at times to recognize the lichenoid character unless the fruits also are present.

Equally primitive in most cases is the structure of the thallus associated with Gloeocapsa. The resulting lichens, Pyrenopsis, Psorotichia, etc. are simply gelatinous crusts of the alga with a more or less scanty intermingling of fungal hyphae.

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In the Collemaceae, the gonidial cells of which are species of Nostoc (Fig. 2), there appears a more developed thallus; but in general, symbiosis in Collema has wrought the minimum of change in the habit of the alga, hence the indecision of the earlier botanists as to the identification and classification of Nostoc and Collema. Though in many of the species of the genus Collema no definite tissue is formed, yet, under the influence of symbiosis, the plants become moulded into variously shaped lobes which are specifically constant. In some species there is an advance towards more elaboration of form in the protective tissues of the apothecia, a layer of thin-walled plectenchyma being occasionally formed beneath or around the fruit as in Collema granuliferum.

In all these lichens, it is only the thallus that can be considered as primitive: the fruit is a more or less open apothecium—more rarely a perithecium—with a fully developed hymenium. Frequently it is provided with a protective thalline margin.

b. Exogenous Thallus. In this group, composed almost exclusively of heteromerous lichens, Zukal includes all those in which the fungus takes the lead in thalline development. He counts as such Leptogium, a genus closely allied to Collema but with more membranous lobes, in which the short terminal cells of the hyphae have united to form a continuous cortex. A higher development, therefore, becomes at once apparent, though in some genera, as in Coenogonium, the alga still predominates, while the simplest forms may be merely a scanty weft of filaments associated with groups of algal cells. Such a thallus is characteristic of the Ectolechiaceae, and some Gyalectaceae, etc., which have, indeed, been described by Zahlbruckner[314] as homoiomerous though their gonidia belong to the non-gelatinous Chlorophyceae.

Heteromerous lichens have been arranged by Hue[315] according to their general structure in three great series:

1. Stratosae. Crustaceous, squamulose and foliose lichens with a dorsiventral thallus.

2. Radiatae. Fruticose, shrubby or filamentous lichens with a strap-shaped or cylindrical thallus of radiate structure.

3. Stratosae-Radiatae. Primary dorsiventral thallus, either crustaceous or squamulose, with a secondary upright thallus of radiate structure called the podetium (Cladoniaceae).

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II. STRATOSE THALLUS

1. CRUSTACEOUS LICHENS

A. General Structure

In the series “Stratosae,” the plant is dorsiventral, the tissues forming the thallus being arranged more or less regularly in strata one above the other (Fig. 37). On the upper surface there is a hyphal layer constituting a cortex, either rudimentary or highly elaborated; beneath the cortex is situated the gonidial zone composed of algae and hyphae in close association; and deeper down the medulla, generally a loose tissue of branching hyphae. The lower cortex which abuts on the medulla may be as fully developed as the upper or it may be absent.

Fig. 37. Vertical section of crustaceous lichen (Lecanora subfusca var. chlarona Hue) on bark. a, lichen cortex; b, gonidia; c, cells of the periderm. × 100.

The growing tissue is chiefly marginal; the hyphae on the outer edge remain “meristematic”[316] and provide for horizontal as well as vertical extension; and there is also continual increase of the algal cells. There is in addition a certain amount of intercalary growth due to the activity of the gonidial tissue, both algal and fungal, providing for the renewal of the cortex, and even interposing new tissue.

B. Saxicolous Lichens

a. Epilithic Lichens. The crustaceous lichens forming this group spread over the rock surfaces. The support must be stable to allow the necessary time for the slowly developing organism, and therefore rocks that are friable or subject to continual weathering are bare of lichens.

aa. Hypothallus or Prothallus. The first stage of growth in the lichen thallus can be most easily traced in epilithic crustaceous species, especially in those that inhabit a smooth rock surface. The spore, on germination, produces a delicate branching septate mycelium which radiates on all sides, as was so well observed and recorded by Tulasne[317] in Verrucaria muralis (Fig. 14). Zukal[318] has called this first beginning the prothallus. In time the[71] cell-walls of the filaments become much thicker and though, in some species, they remain colourless, in others they become dark-coloured, all except the extreme tips, owing to the presence of lichen pigments—a provision, Zukal[319] considers, to protect them against the ravages of insects, etc. The prothallic filaments adhere closely to the substratum and the branching becomes gradually more dendroid in form, though sometimes hyphae are united into strands, or even form a kind of plectenchymatous tissue. This purely hyphal stage may persist for long periods without much change. In time there may be a fortuitous encounter with the algae (Fig. 38 A) which become the gonidia of the plant. Either these have been already established on the substratum as free-growing organisms, or, as accidentally conveyed, they alight on the prothallus. The contact between alga and hypha excites both to active growth and to cell-division; and the rapidly multiplying gonidia are as speedily surrounded by the vigorously growing hyphal filaments.

Fig. 38 A. Hypothallus of Rhizocarpon confervoides DC., from the extreme edge, with loose gonidia × 600.

Fig. 38 B. Young thallus of Rhizocarpon confervoides DC., with various centres of gonidial growth on the hypothallus × 30.

Schwendener[320] has thus described the origin and further development of prothallus and gonidia: on the dark-coloured proto- or prothallus, he noted small nestling groups of green cells which he, at that time, regarded as direct outgrowths from the lichen hyphae. These gonidial cells, increasing by division, multiplied gradually and gathered into a connected zone. He also observed that the hyphae in contact with the gonidia became more thin-walled and produced many new branches. Some of these newly formed branches grow upwards and form the cortex, others grow downwards and build up the medulla or pith; the filaments at the circumference continue to advance and may start new centres of gonidial activity (Fig. 38 B). In many species, however, this prothallus or, as it is usually termed at this stage, the hypothallus, becomes very soon overgrown and obscured by the vigorous increase of the first formed symbiotic tissue and can barely be seen as a white or dark line bordering the thallus (Fig. 39). Schwendener[321] has stated that probably only lichens that develop from the spore are distinguished by a protothallus, and that those arising from soredia do not form these first creeping filaments.

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Fig. 39. Lecanora parella Ach. Determinate thallus with white bordering hypothallus, reduced (M. P., Photo.).

bb. Formation of crustaceous tissues. Some crustaceous lichens have a persistently scanty furfuraceous crust, the vegetative development never advancing much beyond the first rather loose association of gonidia and[73] hyphae; but in those in which a distinct crust or granules are formed, three different strata of tissue are discernible:

1st. An upper cortical tissue of interlaced hyphae with frequent septation and with swollen gelatinous walls, closely compacted and with the lumen of the cells almost obliterated, not unfrequently a layer of mucilage serving as an outer cuticle. This type of cortex has been called by Hue[322] “decomposed.” It is subject to constant surface weathering, thin layers being continually peeled off, but it is as continually being renewed endogenously by the upward growth of hyphae from the active gonidial zone. Exceptions to this type of cortex in crustaceous lichens are found in some Pertusariae where a secondary plectenchymatous cortex is formed, and in Dirina where it is fastigiate[323] as in Roccella.

2nd. The gonidial zone—a somewhat irregular layer of algae and hyphae below the cortex—which varies in thickness according to the species.

3rd. The medullary tissue of somewhat loosely intermingled branching hyphae, with generally rather swollen walls and narrow lumen. It rests directly on the substratum and follows every inequality and crack so closely, even where it does not penetrate, that the thallus cannot be detached without breaking it away.

In Verrucaria mucosa, a smooth brown maritime lichen found on rocks between tide-levels, the thallus is composed of tightly packed vertical rows of hyphae, slender, rather thin-walled, and divided into short cells. The gonidia are chiefly massed towards the upper surface, but they also occur in vertical rows in the medulla. One or two of the upper cells are brown and form an even cortex. The same formation occurs in some other sea-washed species; the arrangement of the tissue elements recalls that of crustaceous Florideae such as Hildenbrandtia, Cruoria, etc.

Fig. 40. Young thallus of Rhizocarpon geographicum DC., with primary and subsequent (dotted lines) areolation × 5.

cc. Formation of areolae. An “areolate” thallus is seamed and scored by cracks of varying width and depth which divide it into minute compartments. These cracks or fissures or chinks originate in two ways depending on the presence or absence of hypothallic hyphae. Where the hypothallus is active, new areolae arise when the filaments encounter new groups of algae. More vigorous growth starts at once and proceeds on all sides from these algal centres, until similarly formed areolae are met, a more or less pronounced fissure marking the limits of each. This primary areolation, termed rimose or rimulose, is well seen in the thin smooth thallus of Rhizocarpon geographicum (Fig. 40); but the first-formed areolae are also very frequently slightly[74] marked by subsequent cracks due to unequal growth. The areolation caused by primary growth conditions tends to become gradually less obvious or to disappear altogether.

Secondary areolation is due to unequal intercalary growth of the otherwise continuous thallus[324]. A more active increase of any minute portions provokes a tension or straining of the cortex between the swollen areas and the surrounding more sluggish tissues; the surface layers give way and chinks arise, a condition described by older lichenologists as “rimose-diffract” or sometimes as “rhagadiose.” The thallus is generally thicker, more broken and granular in the older central parts of the lichen. Towards the circumference, where the tissue is thinner and growth more equal, the chinks are less evident. Sometimes the more vigorously growing areolae may extend over those immediately adjoining, in which case the covered portions become brown and their gonidia gradually disappear.

Strongly marked intersecting lines, similar to those round the margin of the thallus, are formed when hypothalli that have themselves started from different centres touch each other. A large continuous patch of crustaceous thallus may thus be composed of many individuals (Fig. 41).

Fig. 41. Rhizocarpon geographicum DC. on boulder, reduced (M. P., Photo.).

b. Endolithic Lichens. In many species, only the lower hyphae penetrate the substratum either of rock or soil. In a few, more especially those growing on limestone, the greater part or even the whole of the vegetative thallus and sometimes also the fruits are, to some extent, immersed[75] in the rock. It has now been demonstrated that a number of lichens, formerly described as athalline, possess a considerable vegetative body which cannot be examined until the limestone in which they are embedded is dissolved by acids. One such species, Petractis (Gyalecta) exanthematica, studied by Steiner[325] and later by Fünfstück[326], is associated with the blue-green filamentous alga, Scytonema, and is homoiomerous in structure, the alga growing through and permeating the whole of the embedded thallus. A partly homoiomerous thallus, associated with Trentepohlia, has been described by Bachmann[327]. He found the bright-yellow filaments of the alga covering the surface of a calcareous rock. By reason of their apical growth, they pierced the rock and dissolved a way for themselves, not only among the loose particles, but right through a clear calcium crystal reaching generally to a depth of about 200µ, though isolated threads had gone 350µ below the surface. Near the outside the tendency was for the algae to become stouter and to increase by intercalary growth and by budded yeast-like outgrowths; lower down they were somewhat smaller. The hyphae that became united with the algae were unusually slender and were characterized by frequent anastomoses. They closely surrounded the gonidia and also filled the loose spaces of the limestone with their fine thread-like strands. Though oil was undoubtedly present in the lower hyphae there were no swollen nor sphaeroid cells[328]. Some interesting experiments with moisture proved that the part of the rock permeated with the lichen absorbed much more water and retained it longer than the part that was lichen-free.

Generally the embedded tissues follow the same order as in other crustaceous lichens: an upper layer of cortical hyphae, next a gonidial zone, and beneath that an interlaced tissue of medullary or rhizoidal hyphae which often form fat-cells[328]. Friedrich[329] has given measurements of the immersed thallus of Lecanora (Biatorella) simplex: under a cortical layer of hyphae there was a gonidial zone 600-700µ thick, while the lower hyphae reached a depth of 12 mm.; he has also recorded an instance of a thallus reaching a depth of 30 mm.

On siliceous rocks such as granite, rhizoidal hyphae penetrate the rock chiefly between the thin separable flakes of mica. Bachmann[330] has recognized in these conditions three distinct series of cell-formations: (1) slender long-celled sparsely branched hyphae which form a network by frequent anastomoses; (2) further down, though only occasionally, hyphae with short thick-walled bead-like cells; and (3) beneath these, but only in or near mica crystals, spherical cells containing oil or some albuminous substance.

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c. Chemical Nature of the Substratum. Lichens growing on calcareous rocks or soils are more or less endolithic, those on siliceous rocks are largely epilithic, but Bachmann[331] found that the mica crystals in granite were penetrated, much in the same way as limestone, by the lichen hyphae. These travel through the mica in all directions, though they tend to follow the line of cleavage, thus taking the direction of least cohesion. He found that oil-hyphae were formed, and also certain peculiar bristle-like terminal branches; in other cases there were thin layers of plectenchyma, and gonidia were also present. If however felspar or quartz crystals, no matter how thin, blocked the way, further growth was arrested, the hyphae being unable to pierce through or even to leave any trace on the quartz[332]. On granite containing no mica constituents the hyphae can only follow the cracks between the different impenetrable crystals.

Stahlecker[333] has confirmed Bachmann’s observations, but he considers that the difference in habit and structure between the endolithic and epilithic series of lichens is due rather to the chemical than to the physical nature of the substratum. Thus in a rock of mixed composition such as granite, the more basic constituents are preferred by the hyphae, and are the first to be surrounded: mica, when present, is at once penetrated; particles of hornblende, which contain 40 to 50 per cent. only of silicic acid, are laid hold of by the filaments of the lichen before the felspar, of which the acid content is about 60 per cent.; quartz grains which are pure silica are attacked last of all, though in the course of time they also become corroded.

The character of the substratum also affects to a great extent the comparative development of the different thalline layers: the hyphal tissues in silicicolous lichens are much thinner than in lichens on limestone, and the gonidial zone is correspondingly wider. In a species of Staurothele on granite, Stahlecker[333] estimated the gonidial zone to be about 600 µ thick, while the lower medullary hyphae, partly burrowing into the rock, measured about 6 mm. Other measurements at different parts of the thallus gave a rhizoidal depth of 3 mm., while on a more finely granular substratum, with a gonidial zone of 350 µ, the rhizoidal hyphae measured only 1-1/2 mm. On calcareous rocks, on the contrary, with a gonidial zone that is certainly no larger, the hyphal elements penetrate the rock to varying depths down to 15 mm. or even more.

Lang[334] has recorded equally interesting measurements for Sarcogyne (Biatorella) latericola: on slaty rock which contained no mixture of lime, the gonidial zone had a thickness of 80 µ, a considerable proportion of the very thin thallus. Fünfstück[335] has indeed suggested that this lichen on acid[77] rocks is only a starved condition of Sarcogyne (Biatorella) simplex, which on calcareous rocks, though with a broader gonidial zone, has, as noted above, a correspondingly much larger hyphal tissue.

Stahlecker’s theory is that the hyphae require more energy to grow in the acid conditions that prevail in siliceous rocks, and therefore they make larger demands on the algal symbionts. It follows that the latter must be stimulated to more abundant growth than in circumstances favourable to the fungus, such as are found in basic (calcareous) rocks; he concludes that on the acid (siliceous) rocks, the epilithic or superficial condition is not only a physical but a biological necessity, to enable the algae to grow and multiply in a zone well exposed to light with full opportunity for active photosynthesis and healthy increase.

C. Corticolous Lichens

The crustaceous lichens occurring on bark or on dead wood, like those on rocks, are either partly or wholly immersed in the substratum (hypophloeodal), or they grow on the surface (epiphloeodal); but even those with a superficial crust are anchored by the lower hyphae which enter any crack or crevice of wood or bark and so securely attach the thallus, that it can only be removed by cutting away the underlying substance.

a. Epiphloeodal Lichens. These lichens originate in the same way as the corresponding epilithic series from soredia or from germinating spores, and follow the same stages of growth; first a hypothallus with subsequent colonization of gonidia, the formation of granules, areolae, etc. The small compartments are formed as primary or secondary areolae; the larger spaces are marked out by the encounter of hypothalli starting from different centres.

The thickness of the thallus varies considerably according to the species. In some Pertusariae with a stoutish irregular crust there is a narrow amorphous cortical layer of almost obliterated cells, a thin gonidial zone about 35 µ in width and a massive rather dense medulla of colourless hyphae. Darbishire[336] has described and figured in Varicellaria microsticta, one of the Pertusariaceae, single hyphae that extend like beams across the wide medulla and connect the two cortices. In some Lecanorae and Lecideae there is, on the contrary, an extremely thin thallus consisting of groups of algae and loose fungal filaments, which grow over and between the dead cork cells of the outer bark. On palings, there is often a fairly substantial granular crust present, with a gonidial zone up to about 80 µ thick, while the underlying or medullary hyphae burrow among the dead wood fibres.

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b. Hypophloeodal Lichens. These immersed lichens are comparable with the endolithic species of the rock formations, as their thallus is almost entirely developed under the outer bark of the tree. They are recognizable, even in the absence of any fructification, by the somewhat shining brownish, white or olive-green patches that indicate the underlying lichen. This type of thallus occurs in widely separated families and genera, Lecidea, Lecanora, etc., but it is most constant in Graphideae and in those Pyrenolichens of which the algal symbiont belongs to the genus Trentepohlia. The development of these lichens is of peculiar interest as it has been proved that though both symbionts are embedded in the corky tissues, the hyphae arrive there first, and, at some later stage, are followed by the gonidia. There is therefore no question of the alga being a “captured slave” or “unwilling mate.”

Frank[337] made a thorough study of several subcortical forms. He found that in Arthonia radiata, the first outwardly visible indication of the presence of the lichen on ash bark was a greenish spot quite distinct from the normal dull-grey colour of the periderm. Usually the spots are round in outline, but they tend to become ellipsoid in a horizontal direction, being influenced by the growth in thickness of the tree. At this early stage only hyphae are present; Bornet[338] as well as Frank described the outer periderm cells as penetrated and crammed with the colourless slender filaments. Lindau[339], in a more recent work, disputes that statement: he found that the hyphae invariably grew between the dead cork cells, splitting them up and disintegrating the bark, but never piercing the membranes. The purely prothallic condition, as a weft of closely entangled hyphae, may last, Frank considers, for a long period in an almost quiescent condition—possibly for several years—before the gonidia arrive.

It is always difficult to observe the entrance of the gonidia but they seem to spread first under the second or third layers of the periderm. With care it is possible to trace a filament of Trentepohlia from the surface downwards, and to see that the foremost cell is really the growing and advancing apex of the creeping alga. Both symbionts show increased vigour when they encounter each other: the thallus at once develops in extent and in depth, and, ultimately, reproductive bodies are formed. In some species the apothecia or perithecia alone emerge above the bark, in others the outer peridermal cells are thrown off, and the thallus thus becomes superficial to some extent as a white scurfy or furfuraceous crust.

The change from a hypophloeodal to a partly epiphloeodal condition depends largely on the nature of the bark. Frank[337] found that Lecanora pallida remained for a long time immersed when growing on the thick rugged bark of oak trunks. When well lighted, or on trees with a thin[79] periderm, such as the ash, the lichen emerges much earlier and becomes superficial.

Black (or occasionally white) lines intersect the thallus and mark, as in saxicolous lichens (Fig. 41), the boundary lines between different individuals or different species. The pioneer hyphae of certain lichens very frequently become dark-coloured, and Bitter[340] has suggested as the reason for this that in damp weather the hypothallic growth is exceptionally vigorous. When dry weather supervenes, with high winds or strong sunshine, the outlying hyphae, unprotected by the thallus, become dark-coloured. On the return of more normal conditions the blackened tips are thrown off. Bitter further states that species of Graphideae do not form a permanent black limiting line when they grow in an isolated position: it is only when their advance is checked by some other thallus that the dark persistent edge appears, a characteristic also to be seen in the crust of other lichens. The dark boundary is always more marked in sunny exposed situations: in the shade, the line is reduced to a mere thread.

Bitter’s restriction of black boundary lines to cases of encountering thalli only, would exclude the comparison one is tempted to make between the advancing hyphae of lichens and those of many woody fungi where the extreme edge of the white invaded woody tissue is marked by a dark line. In the latter case however it is the cells of the host that are stained black by the fungus pigment.

2. SQUAMULOSE LICHENS

A. Development of the Squamule

The crustaceous thallus is more or less firmly adherent to, or confused with, the substratum. Further advance to a new type of thallus is made when certain hyphal cells of soredium or granule take the lead in an ascending direction both upwards and outwards. As growth becomes definitely apical or one-sided, the structure rises free from the substratum, and small lobules or leaflet-like squamules are formed. Each squamule in this type of thallus is distinct in origin and not merely the branch of a larger whole.

In a few lichens the advance from the crustaceous to the squamulose structure is very slight. The granules seem but to have been flattened out at one side, and raised into minute rounded projections such as those that compose the thallus of Lecanora badia generally described as “subsquamulose.” The squamulose formation is more pronounced in Lecidea ostreata, and in some species of Pannaria; and the whole thallus may finally consist of small separate lobes as in Lecidea lurida, Lecanora crassa, L. saxicola,[80] species of Dermatocarpon and the primary thallus of the Cladoniae. Most of these squamules are of a firm texture and more or less round in outline; in some species of Cladonia, etc., they are variously crenate, or cut into pinnate-like leaflets. Squamulose lichens grow mostly on rocks or soil, occasionally on dead wood, and are generally attached by single rhizoidal hyphae, either produced at all points of the under surface, or from the base only, growth in the latter case being one-sided. In a few instances, as in Heppia Guepini, there is a central hold-fast.

A frequent type of squamulose thallus is that termed “placodioid,” or “effigurate,” in which the squamulose character is chiefly apparent at the circumference. The thallus is more or less orbicular in outline; the centre may be squamulose or granular and cracked into areolae; the outer edge is composed of radiating lobules closely appressed to the substratum (Fig. 42).

Fig. 42. Placodium murorum DC. Part of placodioid thallus with apothecia × 2.

All lichens with this type of thallus were at one time included in the genus Placodium, now restricted by some lichenologists to squamulose or crustaceous species with polarilocular spores. Many of them rival Xanthoria parietina in their brilliant yellow colouring.

Fig. 43. Lecania candicans A. Zahlbr., with placodioid thallus, reduced (S. H., Photo.).

There are also greyish-white effigurate lichens such as Lecanora saxicola, Lecania candicans (Fig. 43) and Buellia canescens, well-known British species.

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B. Tissues of Squamulose Thallus

The anatomical structure of the squamules is in general somewhat similar to that of the crustaceous thallus: an upper cortex, a gonidial zone, and below that a medullary layer of loose hyphae with sometimes a lower cortex.

1. The upper cortex, as in crustaceous lichens, is generally of the “decomposed”[341] or amorphous type: interlaced hyphae with thick gelatinous walls. A more highly developed form is apparent in Parmeliella and Pannaria where the upper cortex is formed of plectenchyma, while in the squamules of Heppia the whole structure is built up of plectenchyma, with the exception of a narrow band of loose hyphae in the central pith.

2. The gonidia are Myxophyceae or Chlorophyceae; the squamules in some instances may be homoiomerous as in Lepidocollema, but generally they belong to the heteromerous series, with the gonidia in a circumscribed zone, and either continuous or in groups. Friedrich[342] held that, as in crustaceous lichens the development of the gonidial as compared with the other tissues depended on the substratum. The squamules of Pannaria microphylla on sandstone were 100 µ thick, and the gonidial layer occupied 80 or 90 µ of the whole[343]. With that may be compared Placodium Garovagli on lime-containing rock: the gonidial layer measured only 50 µ across, the pith hyphae 280 µ and the rhizoidal hyphae that penetrated the rock 500 µ.

3. The medullary layer, as a rule, is of closely compacted hyphae which give solidity to the squamules; in those of Heppia it is almost entirely formed of plectenchyma.

4. The lower cortex is frequently little developed or absent, especially when the squamules are closely applied to the support as in some species of Dermatocarpon. In some of the squamulose Lecanorae (L. crassa and L. saxicola) the lowest hyphae are somewhat more closely interwoven; they become brown in colour, and the lichen is attached to the substratum by rhizoid-like branches. In Lecanora lentigera there is a layer of parallel hyphae along the under surface. Further development is reached when a plectenchyma of thick-walled cells is formed both above and below, as in Psoroma hypnorum, though on the under surface the continuity is often broken. The squamules of Cladoniae are described under the radiate-stratose series.

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3. FOLIOSE LICHENS

A. Development of foliose Thallus

The larger leafy lichens are occasionally monophyllous and attached at a central point as in Umbilicaria, but mostly they are broken up into lobes which are either imbricate and crowded, or represent the dividing and branching of the expanding thallus at the circumference. They are horizontal spreading structures, with marginal and apical growth. The several tissues of the squamule are repeated in the foliose thallus, but further provision is made to meet the requirements of the larger organism. There is the greater development of cortical tissue, especially on the lower surface, and the more abundant formation of rhizoidal organs to attach the large flat fronds to the support. There are also various adaptations to secure the aeration of the internal tissues[344].

B. Cortical Tissues

Schwendener[345] was the first who, with the improved microscope, made a systematic study of the minute structure of lichens. He examined typical species in genera of widely different groups and described their anatomy in detail. The most variable and perhaps the most important of the tissues of lichens is the cortex, which is most fully developed in the larger thalli, and as the same type of cortical structures recurs in lichens widely different in affinity as well as in form, it seems well to group together here the ascertained facts about these covering layers.

a. Types of Cortical Structure. Zukal[346], and more recently Hue[347], have made independent studies in the comparative morphology of the thallus and have given particular attention to the different varieties of cortex. They each find that the variations come under a definite series of types. Zukal recognized five of these:

1. Pseudoparenchymatous (plectenchyma): by frequent septation of regularly arranged hyphae and by coalescence a kind of continuous cell-structure is formed.

2. Palisade cells: the outer elongate ends of the hyphae lie close together in a direction at right angles to the surface of the thallus and form a coherent row of parallel cells.

3. Fibrous: the cortical hyphae lie in strands of fine filaments parallel with the surface of the thallus.

4. Intricate: hyphae confusedly interwoven and becoming dark in colour form the lower cortex of some foliose lichens.

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These four types, Zukal finds, are practically without interstices in the tissue and form a perfect protection against excessive transpiration. He adds yet another form:

5. A cortex formed of hyphae with dark-coloured swollen cells, which is not a protection against transpiration. It occurs among lower crustaceous forms.

Hue has summed up the different varieties under four types, but as he has omitted the “fibrous” cortex, we arrive again at five different kinds of cortical formation, though they do not exactly correspond to those of Zukal. A definite name is given to each type:

1. Intricate: an intricate dense layer of gelatinous-walled hyphae, branching in all directions, but not coalescent (Fig. 44). This rather unusual type of cortex occurs in Sphaerophorus and Stereocaulon, both of which have an upright rigid thallus (fruticose).

Fig. 44. Sphaerophorus coralloides Pers. Transverse section of cortex and gonidial layer near the growing point of a frond × 600.

Fig. 45. Roccella fuciformis DC. Transverse section of cortex near the growing point of a frond × 600.

2. Fastigiate: the hyphae bend outwards or upwards to form the cortex. A primary filament can be distinguished with abundant branches, all tending in the same direction; anastomosis may take place between the hyphae. The end branches are densely packed, though there are occasional interstices (Fig. 45). Such a cortex occurs in Thamnolia; in several genera of Roccellaceae—Roccellographa, Roccellina, Reinkella, Pentagenella, Combea, Schizopelte and Roccella—and also in the crustaceous genus Dirina. The fastigiate cortex corresponds with Zukal’s palisade cells.

3. Decomposed: in this, the most frequent type of cortex, the hyphae that travel up from the gonidial layer become irregularly branched and frequently septate. The cell-walls of the terminal branches become swollen into a gelatinous mass, the transformation being brought about by a change[84] in the molecular constituents of the cell-walls which permits the imbibition and storage of water. The tissue, owing to the enormous increase of the wall, is so closely pressed together that the individual hyphae become indistinct; the cell-lumen finally disappears altogether, or, at most, is only to be detected in section as a narrow disconnected dark streak. The decomposed cortex is characteristic of many lichens, crustaceous (Fig. 46) and squamulose, as well as of such highly developed genera as Usnea, Letharia, Ramalina, Cetraria, Evernia and certain Parmeliae.

Fig. 46. Lecanora glaucoma var. corrugata Nyl. Vertical section of cortex × 500 (after Hue).

Zukal took no note of the decomposed cortex but the omission is intentional and is due to his regarding the structure of the youngest stages of the thallus near the growing point as the most typical and as giving the best indication as to the true arrangement of hyphae in the cortex. He thus describes palisade tissue as the characteristic cortex of Evernia, since the formation near the growing point of the fronds is somewhat palisade-like and he finds fibrous cortex at the tips of Usnea filaments. In both these instances Hue has described the cortex as decomposed because he takes account only of the fully formed thallus in which the tissues have reached a permanent condition.

Fig. 47. Peltigera canina DC. Vertical section of cortex and gonidial zone × 600.

4. Plectenchymatous: the last of Hue’s types corresponds with the first described by Zukal. It is the result of the lateral coherence and frequent septation of the hyphae into short almost square or rounded cells (Fig. 47). The simplest type of such a cortex can be studied in Leptogium, a genus of[85] gelatinous lichens in which the tips of the hyphae are cut off at the surface by one or more septa. The resulting cells are wider than the hyphae and they cohere together to form, in some species, disconnected patches of cells; in others, a continuous cortical covering one or more cells thick, while in the margin of the apothecium they form a deep cellular layer. The cellular type of cortex is found also, as already stated, in some crustaceous Pertusariae, and in a few squamulose genera or species. It forms the uppermost layer of the Peltigera thallus and both cortices of many of the larger foliose lichens such as Sticta, Parmelia, etc.

5. The “fibrous” cortex must be added to this series, as was pointed out by Heber Howe[348] who gave the less appropriate designation of “simple” to the type. It consists of long rather sparingly branched slender hyphae that grow in a direction parallel with the surface of the thallus (Fig. 48). It is characteristic of several fruticose and foliose lichens with more or less upright growth, such as we find in several of the Physciae, and in the allied genus Teloschistes, in Alectoria, several genera of Roccellaceae, in Usnea longissima and in Parmelia pubescens, etc. Zukal would have included all the Usneae as the tips are fibrous.

Fig. 48. Physcia ciliaris DC. Vertical section of thallus. a, cortex; b, gonidial zone; c, medulla. × 100.

More than one type of cortex, as already stated, may appear in a genus: a striking instance of variability occurs in Solorina where, as Hue[349] has pointed out, the cortex of S. octospora is fastigiate, that of all the other species being plectenchymatous. Cortical development is a specific rather than a generic characteristic.

b. Origin of Variation in Cortical Structure. The immediate causes making for differentiation in cortical development are: the prevailing direction of growth of the hyphae as they rise from the gonidial zone; the amount of branching and the crowding of the filaments; the frequency of septation; and the thickening or degeneration of the cell-walls which may[86] become almost or entirely mucilaginous. In the plectenchymatous cortex, the walls may remain quite thin and the cells small as in Xanthoria parietina, or the walls may be much thickened as in both cortices of Sticta. As a result of stretching the cell may increase enormously in size: in some instances where the internal hyphae are about 3 µ to 4 µ in width, the cortical cells formed from these hyphae may have a cell cavity 15 µ to 16 µ in diameter.

c. Loss and Renewal of Cortex. Very frequently the cortex is covered over by a layer of homogeneous mucilage which forms an outer cuticle. It arises from the continual degeneration of the outer cell-walls and it is liable to friction and removal by atmospheric agency as was first described by Schwendener[350] in the weather-beaten cortex of Umbilicaria pustulata. He had noted the irregular jagged outline of the cross section of the thallus, and he then suggested, as the probable reason, the decay of the outer rind with the constant renewal of it by the hyphae from the underlying gonidial zone, though he was unable definitely to prove his theory. The peeling of the dead outer layer (with its replacement by new tissue) has however been observed many times since his day. It has been described by Darbishire[351] in Pertusaria: in that genus there is at first a primary cortex formed of hyphae that grow in a radial direction, parallel to the surface of the thallus. The walls of these hyphae become gradually more and more mucilaginous till the cells are obliterated. Meanwhile short-celled filaments grow up in serried ranks from the gonidial layer and finally push off the dead “fibrous” cortex. The new tissue takes on a plectenchymatous character, and the outer cells in time become decomposed and provide a mucilaginous cuticle which in turn is also subject to wasting.

The same process of peeling was noted by Rosendahl[352] in some species of brown Parmeliae, where the dead tissues were thrown off in shreds, though only in isolated patches. But whether in patches or as a continuous sheath, there is constant degeneration, with continual renewal of the dead material from the internal tissues.

The cortex is the most highly developed of all the lichen structures and is of immense importance to the plant as may be judged from the various adaptations to different needs[353]. The cortical cell-walls are frequently impregnated with some dark-coloured substance which, in exposed situations, must counteract the influence of too direct sunlight and be of service in sheltering the gonidia. Lichen acids—sometimes very brightly coloured—and oxalic acid are deposited in the cortical tissues in great abundance and aid in retaining moisture; but the two chief functions to[87] which the cortex is specially adapted are the checking of transpiration and the strengthening of the thallus against external strains.

d. Cortical Hairs or Trichomes. Though somewhat rare, cortical hairs are present on the upper surface of several foliose lichens. They take rise, in all the instances noted, as a prolongation of one of the cell-rows forming a plectenchymatous cortex.

In Peltidea (Peltigera) aphthosa they are especially evident near the growing edges of the thallus; and they take part in the development of the superficial cephalodia[354] which are a constant feature of the lichen. They tend to disappear with age and leave the central older parts of the thallus smooth and shining. In several other species of Peltigera (P. canina, etc.) they are present and persist during the life of the cortex. In these lichens the cells of the cortical tissue are thin-walled, all except the outer layer, the membranes of which are much thicker. The hairs rising from them are also thick-walled and septate. Generally they branch in all directions and anastomose with neighbouring hairs so that a confused felted tangle is formed; they vary in size but are, as a rule, about double the width of the medullary hyphae as are the cortical cells from which they rise. They disappear from the thallus, frequently in patches, probably by weathering, but over large surfaces, and especially where any inequality affords a shelter, they persist as a soft down.

Hairs are also present on the upper surface of some Parmeliae. Rosendahl[355] has described and figured them in P. glabra and P. verruculifera—short pointed unbranched hyphae, two or more septate and with thickened walls. They are most easily seen near the edge of the thallus, though they persist more or less over the surface; they also grow on the margins of the apothecia. In P. verruculifera they arise from the soredia; in P. glabra a few isolated hairs are present on the under surface.

In Nephromium tomentosum there is a scanty formation of hairs on the upper surface. They are abundant on the lower surface, and function as attaching organs. A thick tomentum of hairs is similarly present on the lower surface of many of the Stictaceae either as an almost unbroken covering or in scattered patches. In several species of Leptogium they grow out from the lower cortical cells and attach the thin horizontal fronds; and very occasionally they are present in Collema.

C. Gonidial Tissues

With the exception of some species of Collema and Leptogium lichens included under the term foliose, are heteromerous in structure, and the algae that form the gonidial zone are situated below the upper cortex and, therefore,[88] in the most favourable position for photosynthesis. Whether belonging to the Myxophyceae or the Chlorophyceae, they form a green band, straight and continuous in some forms, in others somewhat broken up into groups. In certain species they push up at intervals among the cortical cells, as in Gyrophora and in Parmelia tristis. In Solorina crocea a regular series of gonidial pyramids rises towards the upper surface. The green cells are frequently more dense at some points than at others, and they may penetrate in groups well into the medulla.

The fungal tissue of the gonidial zone is composed of hyphae which have thinner walls, and are generally somewhat loosely interlacing. In Peltigera[356] the gonidial hyphae are so connected by frequent branching and by anastomosis that a net-like structure is formed, in the meshes of which the algae—a species of Nostoc—are massed more or less in groups. In lichens with a plectenchymatous cortex, the cellular tissue may extend downwards into the gonidial zone and the gonidia thus become enmeshed among the cells, a type of formation well seen in the squamulose species, Dermatocarpon lachneum and Heppia Guepini, where the massive plectenchyma of both the upper and lower cortices encroaches on the pith. In Endocarpon and in Psoroma the gonidia are also surrounded by short cells.

A similar type of structure occurs in Cora Pavonia, one of the Hymenolichenes: the gonidial hyphae in that species form a cellular tissue in which are embedded the blue-green Chroococcus cells[357].

D. Medulla and Lower Cortex

a. Medulla. The hyphal tissue of the dorsiventral thallus that lies between the gonidial zone and the lower cortex or base of the plant is always referred to as the medulla or pith. It is, as a rule, by far the most considerable portion of the thallus. In Parmelia caperata (Fig. 49), for instance, the lobes of which are about 300 µ thick, over 200 µ of the space is occupied by this layer. It varies however very largely in extent in different lichens according to species, and also according to the substratum. In another Parmelia with a very thin thallus, P. alpicola growing on quartzite, the medulla measures scarcely twice the width of the gonidial zone. It forms a fairly massive tissue in some of the crustaceous lichens—in some Pertusariae and Lecanorae—attaining a width of about 600 µ.

Nylander[358] distinguished three types of medullary tissue in lichens:

(1) felted, which includes all those of a purely filamentous structure;

(2) cretaceous or tartareous, more compact than the felted, and containing granular or crystalline substances as in some Pertusariae; and lastly

(3) the cellular medulla in which the closely packed hyphae are divided[89] into short cells and a kind of plectenchyma is formed, as in Lecanora (Psoroma) hypnorum, in Endocarpon, etc.

Fig. 49. Parmelia caperata Ach. (S. H., Photo.).

The felted medulla is characteristic of most lichens and is formed of loose slender branching septate hyphae with thickish walls. This interwoven hyphal texture provides abundant air-spaces.

Hue[359] has noted that the walls of the medullary hyphae in Parmeliae are smooth, unless they have been exposed to great extremes of heat or cold, when they become wrinkled or scaly. They are very thick-walled in Peltigera (Fig. 50).

Fig. 50. Hyphae from lower medulla of Peltigera canina DC. × 600.

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b. Lower Cortex. In some foliose lichens such as Peltigera there is no special tissue developed on the under surface. In Lobaria pulmonaria large patches of the under surface are bare, and the medulla is exposed to the outer atmosphere, sheltered only by its position. In some other lichens the lowermost hyphae lie closer together and a kind of felt of almost parallel filaments is formed, generally darker in colour, as in Lecanora lentigera, and in some species of Physcia.

Most frequently however the tissues of the upper cortex are repeated on the lower surface, though differing somewhat in detail. In all of the brown Parmeliae, according to Rosendahl[360], the structure is identical for both cortices, though the upper develops now hairs, now isidia, breathing pores, etc., while the lower produces rhizinae. The amorphous mucilaginous cuticle so often present on the upper surface is absent from the lower, the walls of the latter being often charged instead with dark-brown pigments.

c. Hypothallic Structures. An unusual development of hyphae from the lower cortex occurs in the genera Anzia and Pannoparmelia—both closely related to Parmelia—whereby a loose sponge-like hypothallus of anastomosing reticulate strands is formed. In one of the simpler types, Anzia colpodes, a North American species, the hyphae passing out from the lower medulla become abruptly dark-brown in colour, and are divided into short thick-walled cells. Frequent branching and anastomosis of these hyphae result in the formation of a cushion-like structure about twice the bulk of the thallus. In another species from Australia (A. Japonica) there is a lower cortex, distinct from the medulla, consisting of septate colourless hyphae with thick walls. From these branch out free filaments, similar in structure but dark in colour, which branch and anastomose as in the previous species.

Fig. 51. Pannoparmelia anzioides Darb. Vertical section of thallus and hypothallus. a, cortex; b, gonidial zone; c, medulla; d, lower cortex; e, hypothallus. × ca. 450 (after Darbishire).

In Pannoparmelia the lower cortex and the outgrowths from it are several cells thick; they may be thick-walled as in Anzia, or they may be thin-walled as described and figured by Darbishire[361] in[91] Pannoparmelia anzioides, a species from Tierra del Fuego (Fig. 51). A somewhat dense interwoven felt of hyphae occurs also in certain parts of the under surface of Parmelia physodes[362].

This peculiar structure, regarded as a hypothallus, is probably of service in the retention of moisture. The thick cell-walls in most of the forms suggest some such function.

E. Structures for Protection and Attachment

Such structures are almost wholly confined to the larger foliose and fruticose lichens and are all of the same simple type; they are fungal in origin and very rarely are gonidia associated with them.

Fig. 52. Usnea florida Web. Ciliate apothecia (S. H., Photo.).

a. Cilia. In a few widely separated lichens stoutish cilia are borne, mostly on the margins of the thallus lobes, or on the margins of the apothecia (Fig. 52). They arise from the cortical cells or hyphae, several of which grow out in a compact strand which tapers gradually to a point. Cilia vary in length up to about 1 cm. or even longer. In some lichens they[92] retain the colour of the cortex and are greyish or whitish-grey, as in Physcia ciliaris or in Physcia hispida (Fig. 110). They provide a yellow fringe to the apothecia of Physcia chrysophthalma and a green fringe to those of Usnea florida. They are dark-brown or almost black in Parmelia perlata var. ciliata and in P. cetrata, etc. as also in Gyrophora cylindrica. The fronds of Cetraria islandica and other species of the genus are bordered with short spinulose brown hairs whose main function seems to be the bearing of “pycnidia” though in many cases they are barren (Fig. 128).

Superficial cilia are more rarely formed than marginal ones, but they are characteristic of one not uncommon British species, Parmelia proboscidea (P. pilosella Hue). Scattered over the surface of that lichen are numerous crowded groups of isidia which, frequently, are prolonged upwards as dark-brown or blackish cilia. Nearly every isidium bears a small brown spot on the apex at an early stage of growth. Similar cilia are sparsely scattered over the thallus, but their base is always a rather stouter grey structure, which suggests an isidial origin. Cilia also occur on the margin of the lobes.

As lichens are a favourite food of snails, insects, etc., it is considered that these structures are protective in function, and that they impede, if they do not entirely prevent, the larger marauders in their work of destruction.

Fig. 53. Rhizoid of Parmelia exasperata Carroll (P. aspidota Rosend.). A, hyphae growing out from lower cortex × 450. B, tip of rhizoid with gelatinous sheath × 335 (after Rosendahl).

b. Rhizinae. Lichen rootlets are mainly for the purpose of attachment and have little significance as organs of absorption. They have been noted in only one crustaceous lichen, Varicellaria microsticta[363], an alpine species that spreads over bark or soil, and which is further distinguished by being provided with a lower cortex of plectenchyma. In foliose lichens they are frequently abundant, though by no means universal, and attach the spreading fronds to the support. They originate, as Schwendener[364] pointed out, from the outer cortical cells, exactly as do the cilia, and are scattered over the[93] under surface or are confined to special areas. Rosendahl[365] has described their development in the brown species of Parmeliae: the under cortex in these lichens is formed of a cellular plectenchyma with thickish walls; the rootlets arise by the outgrowth of several neighbouring cells from some slight elevation near the edge of the thallus. Branching and interlacing of these growing rhizinal hyphae follow, the outermost frequently spreading outwards at right angles to the axis, and forming a cellular cortex. The apex of the rhizoid is generally an enlarged tuft of loose hyphae involved in mucilage (Fig. 53), a provision for securing firmer cohesion to the support; or the tips spread out as a kind of sucker. Not unfrequently neighbouring “rootlets” are connected by mucilage at the tips, or by outgrowths of their hyphae, and a rather large hold-fast sheath is formed.

Fig. 54. Peltigera canina DC. (S. H., Photo.).

Fig. 55. Peltigera canina DC. Under surface with veins and rhizoids (after Reinke).

In species of Peltigera (Fig. 54) the rhizinae are confined to the veins or ridges (Fig. 55); they are thickish at the base, and are generally rather long and straggling. Meyer[366] states that the central hyphae are stoutish and much entangled owing to the branching and frequent anastomosis of one hypha with another; the peripheral terminal branches are thinner-walled and free. These rhizinae vary in colour from white in Peltigera canina to brown or black in other species. Most species of Peltigera spread over grass or mosses, to which they cling by these long loose “rootlets.”

Lichen rhizinae, distinguished by Reinke[367] as “aerial rhizinae,” are more[94] or less characteristic of all the species of Parmelia with the exception of those belonging to the subgenus Hypogymnia in which they are of very rare occurrence, arising, according to Bitter[368], only in response to some external friction. They are invariably dark-coloured, rather short, about one to a few millimetres in length, and are simple or branched. The branches may go off at any angle and are sometimes curved back at the ends in anchor-like fashion. The Parmeliae grow on firm substances, trees, rocks, etc., and the irregularities of their attaching structures are conditioned by the obstacles encountered on the substratum. Not unfrequently the lobes are attached by the rhizinae to underlying portions of the thallus.

In the genus Gyrophora, the rhizinae are simple strands of hyphae (G. polyrhiza) or they are corticate structures (G. murina, G. spodochroa and G. vellea). They are also present in species of Solorina, Ricasolia, Sticta and Physcia and very sparingly in Cetraria (Platysma).

c. Haptera. Sernander[369] has grouped all the more distinctively aerial organs of attachment, apart from rhizinae, under the term “hapteron” and he has described a number of instances in which cilia and even the growing points of the thallus may become transformed to haptera or sucker-like sheaths.

The long cilia of Physcia ciliaris occasionally form haptera at their tips where the hyphae are loose and in active growing condition. Contact with some substance induces branching by which a spreading sheath arises; a plug-like process may also be developed which pierces the substance encountered—not unfrequently another lobe of its own thallus. The long flaccid fronds of Evernia furfuracea are frequently connected together by bridge-like haptera which rise at any angle of the thallus or from any part of the surface.

The spinous hairs that border the thalline margins in Cetraria may also, in contact with some body—often another frond of the lichen—form a hapteron, either while the spermogonium, which occupies the tip of the spine, is still in a rudimentary stage, or after it has discharged its spermatia. The small sucker sheath may in that case arise either from the apex of the cilium, from the wall of the spermogonium or from its base. By means of these haptera, not only different individuals become united together, but instances are given by Sernander in which Cetraria islandica, normally a ground lichen, had become epiphytic by attaching itself in this way to the trunk of a tree (Pinus sylvestris).

In Alectoria, haptera are formed at the tip of the thallus filament as an apical cone-like growth from which hyphae may branch out and penetrate any convenient object. A species of this genus was thus found clinging to[95] stems of Betula nana. Apical haptera are very frequent in Cladonia rangiferina and Cl. sylvatica, induced here also by contact. These two plants, as well as several species of Cetraria, tend, indeed, to become entirely epiphytic on the heaths of the Calluna formations. Haptera similar to those of Alectoria occur in Usnea, Evernia, Ramalina and Cornicularia (Cetraria). In Evernia prunastri var. stictoceros, a heath form, the fronds become attached to the stems and branches of Erica tetralix by hapteroid strands of slender glutinous hyphae which persist on the frond of the lichen after it is detached as small very dark tubercles surmounted, as Parfitt[370] pointed out, by a dark-brown grumous mass of cells. Plug-like haptera may be formed at the base of Cladoniae which attach them to each other and to the substratum. The brightly coloured fronds of Letharia vulpina are attached to each other in somewhat tangled fashion by lateral bridges or by fascicles of hyphae dark-brown at the base but colourless at the apices, exactly like aerial adventitious rhizinae. They grow out from the fronds generally at or near the tips and lay hold of a neighbouring frond by means of mucilage. These haptera are evidently formed in response to friction. Haptera along with other lichen attachments have received considerable attention from Galløe[371]. He finds them arising on various positions of the lichen fronds and has classified them accordingly.

After the haptera have become attached, they increase in size and strength and supply a strong anchorage for the plant; the point of contact frequently forms a basis for renewed growth while the part beneath the hapteron may gradually die off. Haptera are more especially characteristic of fruticose lichens, but Sernander considers that the rhizinae of foliose species may function as haptera. They are important organs of tundra and heath formations as they enable the lichens to get a foothold in well-lighted positions, and by their aid the fronds are more able to resist the extreme tearing strains to which they are subjected in high and unsheltered moorlands.

F. Strengthening Tissues of Stratose Lichens

Squamulose and foliose lichens grow mostly in close relation with the support, and the flat expanding thallus, as in the Parmeliae, is attached at many points to the substance—tree, rock, etc.—over which the plants spread. Special provision for support is therefore not required, and the lobes remain thin and flaccid. Yet, in a number of widely different genera the attachment to the substratum is very slight, and in these we find an adaptation of existing tissues fitted to resist tearing strains, resistance being almost invariably secured by the strengthening of the cortical layers.

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a. By development of the Cortex. Such a transformation of tissue is well illustrated in Heppia Guepini. The thallus consists of rigid squamules which are attached at one point only; the cortex of both surfaces is plectenchymatous and very thick and even the medulla is largely cellular.

The much larger but equally rigid coriaceous thallus of Dermatocarpon miniatum (Fig. 56) has also a single central attachment or umbilicus, and both cortices consist of a compact many-layered plectenchyma. The same structure occurs in Umbilicaria pustulata and in some species of Gyrophora, which, having only a single central hold-fast, gain the necessary stiffening through the increase of the cortical layers.

Fig. 56. Dermatocarpon miniatum Th. Fr. (S. H., Photo.).

In the Stictaceae there are a large number of widely-expanded forms, and as the attachment depends mostly on a somewhat short tomentum, strength is obtained here also by the thick plectenchymatous cortex of both surfaces. When areas denuded of tomentum and cortex occur, as in Lobaria pulmonaria, the under surface is not sensibly weakened, since the cortical tissue remains connected in a stout and firm reticulation.

b. By development of Veins or Nerves. Certain ground lichens belonging to the Peltigeraceae have a wide spreading thallus often with very large lobes. The upper cortex is a many-layered plectenchyma, but the under surface is covered only by a loose felt of hyphae which branch out into a more or less dense tomentum. As the firm upper cortex continues to increase by intercalary growth from the branching upwards of hyphae from the meristematic gonidial zone, there occurs an extension of the upper[97] thallus with which the lower cannot keep pace[372]. A little way back from the edge, the result of the stretching is seen in the splitting asunder of the felted hyphae of the under surface, and in the consequent formation of a reticulate series of ridges known as the veins or nerves; they represent the original tomentose covering, and are white, black or brown, according to the colour of the tomentum itself. The naked ellipsoid interstices show the white medulla, and, if the veins are wide, the colourless areas are correspondingly small. Rhizinae are formed on the nerves in several of the species, and anchor the thallus to the support. In Peltigera canina, the under surface is almost wholly colourless, the veins are very prominent (Fig. 55), and are further strengthened by the growth and branching of the parallel hyphae of which they are composed. They serve to strengthen the large and flabby thallus and form a rigid base for the long rhizinae by which the lichen clings to the grass or moss over which it grows.

The most perfect development of strengthening nerves is to be found in Hydrothyria venosa[373], a rather rare water lichen that occurs in the streams of North America. It consists of fan-like lobes of thin structure, the cortex being only about one cell thick. The fronds are about 3 cm. wide and they are contracted below into a stalk which serves to attach the plant to the substratum. Several fronds may grow together in a dense tuft, the expanded upper portion floating freely in the water. Frequently the plants form a dense growth over the rocky beds of the stream.

At the point where the stalk expands into the free erect frond, there arise a series of stout veins which spread upwards and outwards. They are definitely formed structures and not adaptations of pre-existing tissues: certain hyphae arise from the medulla at the contracted base of the frond, take a radial direction and, by increase, become developed into firm strands. The individual hyphae also increase in size, and the swelling of the nerve gives rise to a ridge prominent on both surfaces. They seldom anastomose at first but towards the tips they become smaller and spread out in delicate ramifications which unite at various points. There is no doubt, as Bitter[372] points out, that the nerves function as strengthening tissues and preserve the frond from the strain of the water currents which would, otherwise, tear apart the delicate texture.

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III. RADIATE THALLUS

1. CHARACTERS OF RADIATE THALLUS

In the stratose dorsiventral thallus, there is a widely extended growing area situated round the free margins of the thallus. In the radiate thallus of the fruticose or filamentous lichens, growth is confined to an apical region. Attachment to the substratum is at one point only—the base of the plant—thus securing the exposure of all sides equally to light. The cortex surrounds the fronds, and the gonidia (mostly Protococcaceae) lie in a zone or in groups between the cortex and the medulla. It is the highest type of vegetative development in the lichen kingdom, since it secures the widest room for the gonidial layer, and the largest opportunity for photosynthesis.

Fig. 57. Roccella fuciformis DC.

Shrubby upright lichens consist mostly of strap-shaped fronds, either simple or branched, which may be broadened to thin bands (Fig. 57) or may be narrowed and thickened till they are almost cylindrical. The fronds vary in length according to the species from a few millimetres upwards:[99] those of Roccella have been found measuring 30 cm. in length; those of Ramalina reticulata, the largest of all the American lichens, extend to considerably more.

Lichens of filamentous growth are more or less cylindrical (Fig. 58). They are in some species upright and of moderate length, but in a few pendulous forms they grow to a great length: specimens of Usnea longissima have been recorded that measured 6 to 8 metres from base to tip.

Fig. 58. Usnea barbata Web. (S. H., Photo.).

The radiate type of thallus occurs in most of the lichen groups but most frequently in the Gymnocarpeae. In gelatinous Discolichens it is represented in the Lichinaceae. It is rare among Pyrenocarpeae: there is one very minute British lichen in that series, Pyrenidium actinellum, and one from N. America, Pyrenothamnia, that are of fruticose habit.

2. INTERMEDIATE TYPES OF THALLUS

Between the foliose and the fruticose types, there are intermediate forms that might be, and often are, classified now in one group and now in the other. These are chiefly: Physcia (Anaptychia) ciliaris, Ph. leucomelas and the species of Evernia.

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In the two former the habit is more or less fruticose as the plants are affixed to the substratum at a basal point, but the fronds are decumbent and the internal structure is of the dorsiventral type: there is an upper “fibrous” cortex of closely compacted parallel hyphae, a gonidial zone—the gonidia lying partly in the cortex and partly among the loose hyphae of the medulla—and a lower cortex formed of a weft of hyphae which also run somewhat parallel to the surface. Both species are distinguished by the numerous marginal cilia, either pale or dark in colour. These two lichens are greyish-coloured on the upper surface and greyish or whitish below.

Evernia furfuracea with a basal attachment[374], and with a partly horizontal and partly upright growth, has a dorsiventral thallus, dark greyish-green above and black beneath, with occasional rhizinae towards the base. The cortex of both surfaces belongs to the “decomposed” type; the gonidial zone lies below the upper surface, and the medullary tissue is of loose hyphae. In certain forms of the species isidia are abundant on the upper surface, a character of foliose rather than of fruticose lichens. E. furfuracea grows on trees and very frequently on palings.

Fig. 59. Evernia prunastri Ach. (M. P., Photo.).

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E. prunastri, the second species of the genus, is more distinctly upright in habit, with a penetrating basal hold-fast and upright strap-shaped branching fronds, light-greyish green on the “upper” surface and white on the other (Fig. 59). The internal structure is sub-radiate; both cortices are “decomposed”; the gonidial zone consists of somewhat loose groups of algae, very constant below the “upper” surface, with an occasional group in the pith near to the lower cortex in positions that are more exposed to light. There is also a tendency for the gonidial zone to pass round the margin and spread some way along the under side. The medulla is of loose arachnoid texture and the whole plant is very limp when moist. It grows on trees, often in dense clusters.

3. FRUTICOSE AND FILAMENTOUS

A. General Structure of Thallus

The conditions of strain and tension in the upright plant are entirely different from those in the decumbent thallus, and to meet the new requirements, new adaptations of structure are provided either in the cortex or in the medulla.

Cortical Structures. With the exception of the distinctly plectenchymatous cortex, all the other types already described recur in fruticose lichens; in various ways they have been modified to provide not only covering but support to the fronds.

a. The fastigiate cortex. This reaches its highest development in Roccella in which the branched hyphal tips, slightly clavate and thick-walled, lie closely packed in palisade formation at right angles to the main axis (Fig. 45). They afford not only bending power, but give great consistency to the fronds. The cortex is further strengthened in R. fuciformis[375] by the compact arrangement of the medullary hyphae that run parallel with the surface, and among which occur single thick-walled filaments. The plant grows on maritime rocks in very exposed situations; and the narrow strap-shaped fronds, as stated above, may attain a length of 30 cm., though usually they are from 10 to 18 cm. in height. The same type of cortex, but less highly differentiated, affords a certain amount of stiffness to the cylindrical much weaker fronds of Thamnolia.

b. The fibrous cortex. This type is found in a number of lichens with long filamentous hanging fronds. It consists of parallel hyphae, rarely septate and rarely branched, but frequently anastomosing and with strongly thickened “sclerotic” walls. Such a cortex is the only strengthening element in Alectoria, and it affords great toughness and flexibility to the thong-like[102] thallus. It is also present in Ramalina (Alectoria) thrausta, a species with slender fronds (Fig. 60).

Fig. 60. Alectoria thrausta Ach. A, transverse section of frond; a, cortex; b, gonidia; c, arachnoid medulla × 37. B, fibrous hyphae from longitudinal section of cortex. × 430 (after Brandt).

In Usnea longissima the cortex both of the fibrillose branchlets and of the main axis is fibrous, and is composed of narrow thick-walled hyphae which grow in a long spiral round the central strand. The hyphae become more frequently septate further back from the apex (Fig. 61). Such a type of cortex provides an exceedingly elastic and efficient protection for the long slender thallus.

Fig. 61. Usnea longissima Ach. Longitudinal sections of outer cortex. A, near the apex; B, the middle portion of a fibril. × 525 (after Schulte).

The same type of cortex forms the strengthening element in the fruticose or partly fruticose members of the family Physciaceae. One of these, Teloschistes flavicans, is a bright yellow filamentous lichen with a somewhat straggling habit. The fronds are very slender and are either cylindrical or slightly flattened. The[103] hyphae of the outer cortex are compactly fibrous; added toughness is given by the presence of some longitudinal strands of hyphae in the central pith.

Another still more familiar grey lichen, Physcia ciliaris, has long flat branching fronds which, though dorsiventral in structure, are partly upright in habit. Strength is secured as in Teloschistes by the fibrous upper cortex. Other species of Physciae are somewhat similar in habit and in structure.

In Dendrographa leucophaea, a slender strap-shaped rock lichen, Darbishire[376] has described the outer cortex as composed of closely compacted parallel hyphae resembling the strengthening cortex of Alectoria and very different from the fastigiate cortex of the Roccellae with which it is usually classified.

B. Special strengthening Structures

a. Sclerotic strands. This form of strengthening tissue is characteristic of Ramalina. With the exception of R. thrausta (more truly an Alectoria) all the species have a rather weak cortical layer of branching intricate thick-walled hyphae, regarded by Brandt[377] as plectenchymatous, but more correctly by Hue[378] as “decomposed” on account of the gelatinous walls and diminishing lumen of the irregularly arranged cells.

Fig. 62. Ramalina minuscula Nyl. A, transverse section of frond × 37; B, longitudinal strengthening hyphae of inner cortex × 430 (after Brandt).

In R. evernioides, a plant with very wide flat almost decumbent fronds of soft texture, in R. ceruchis and in R. homalea there is a somewhat compact medulla which gives a slight stiffness to the thallus. The other species of the genus are provided with strengthening mechanical tissue within the cortex formed of closely united sclerotic hyphae that run parallel to the surface (Fig. 62). In a transverse section of the thallus, this tissue appears[104] sometimes as a continuous ring which may project irregularly into the pith (R. calicaris); more frequently it is in the form of strands or bundles which alternate with the groups of gonidia (R. siliquosa, R. Curnowii, etc.). In R. fraxinea these strands may be scarcely discernible in young fronds, though sometimes already well developed near the tips. Occasionally isolated strands of fibres appear in the pith (R. Curnowii), or the sclerotic projections may even stretch across the pith to the other side (R. strepsilis) (Fig. 75 B).

In the Cladoniae support along with flexibility is secured to the upright podetium by the parallel closely packed hyphae that form round the hollow cylinder a band called the “chondroid” layer from its cartilage-like consistency.

b. Chondroid axis. The central medullary tissue in Ramalina is, with few exceptions, a loose arachnoid structure; often the fronds are almost hollow. In one species of Usnea, U. Taylori, found in polar regions, there is a similar loose though very circumscribed medullary and gonidial tissue in the centre of the somewhat cylindrical thallus, and a wide band of sclerotic fibres towards the cortex.

Fig. 63 A. A, Usnea barbata Web. Longitudinal section of filament with young adventitious branch. a, chondroid axis; b, gonidial tissue; c, cortex. × 100 (after Schwendener). B, U. longissima Ach. Hyphae from central axis × 525 (after Schulte).

In all other species of Usnea the medulla itself is transformed into a strong central strand of long-celled thick-walled hyphae closely knit together by frequent anastomoses (Fig. 63 A). This central strand of the Usneas is known as the “chondroid axis.” A narrow band of loose air-containing hyphae and a gonidial zone lie round the central axis between it and the outer cortex (Fig. 63 A, b). At the extreme apex, the external cortical hyphae grow in a direction parallel with the long axis of the plant, but further back, they branch out at right angles and become swollen and mostly “decomposed” as in the cortex of Ramalina.

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In Letharia (L. vulpina, etc.) the structure is midway between Ramalina and Usnea: the central axis is either a solid strand of chondroid hyphae or several separate strands.

Fig. 63 B. Usnea longissima Ach. A, transverse section of fibril × 85. B, a, chondroid axis; b, gonidial tissue; c, cortex × 525 (after Schulte).

In three other genera with upright fruticose thalli, Sphaerophorus, Argopsis and Stereocaulon, rigidity is maintained by a medulla approaching the chondroid type. In Sphaerophorus the species may have either flattened or cylindrical branching stalks, but in all of them, the centre is occupied by longitudinal strands of hyphae. Argopsis, a monotypic genus from Kerguelen, has a cylindrical branching thallus with a strong solid axis; it is closely allied to Stereocaulon, a genus of familiar moorland lichens. The central tissue of the stalks in Stereocaulon is also composed of elongate, thick-walled conglutinate hyphae, formed into a strand which is, however, not entirely solid.

C. Survey of Mechanical Tissues

Mechanical tissues scarcely appear among fungi, except perhaps as stoutish cartilaginous hyphae in the stalks of some Agarics (Collybiae, etc.), or as a ring of more compact consistency round the central hyphae of rhizomorphic strands. It is practically a new adaptation of hyphal structure confined to lichens of the fruticose group, where there is the same requirement as in the higher plants for rigidity, flexure and tenacity.

Rigidity is attained as in other plants by groups or strands of mechanical tissue situated close to the periphery, as they are so arranged in Ramalina and Cladonia; or the same end is achieved by a strongly developed[106] fastigiate cortex as in Roccella. Bending strains to which the same lichens are subjected, are equally well met by the peripheral disposition of the mechanical elements.

Tenacity and elasticity are provided for in the pendulous forms either by a fibrous cortex as in Alectoria, or by the chondroid axis in Usnea. Haberlandt[379] has recorded some interesting results of tests made by him as to the stretching capacity of a freshly gathered pendulous species in which the central strand was from ·5 to 1 mm. thick. He found he could draw it out 100 to 110 per cent. of its normal length before it gave way. In an upright species the frond broke when stretched 60 to 70 per cent. In both of the plants tested, the central strand retained its elasticity up to 20 per cent. of stretching. The outer cortical tissue was cracked and broken in the experiments. Schulte[380] calculated somewhat roughly the tenacity of Usnea longissima and found that a piece of the main axis 8 cm. long carried up to 300 grms. without breaking.

D. Reticulate Fronds

In the upright radiate thallus, more especially among the Ramalinae, though also among Cladoniae[381], there has appeared a reticulate thallus resulting from the elongate splitting of the tissues, and due to unequal growth tension and straining of the gelatinous cortex when swollen with moisture. In several species of Ramalina, the strap-shaped frond is hollow in the centre; and strands of strengthening fibres give rise to a series of cortical ridges. The thinner tissue between is frequently torn apart and ellipsoid openings appear which do not however pierce beyond the central hollow. Such breaks are irregular and accidental though occurring constantly in Ramalina fraxinea, R. dilacerata, etc.

A more complete type of reticulation is always present in a Californian lichen, Ramalina reticulata, in which the large flat frond is a delicate open network from tip to base (Fig. 64). It grows on the branches of deciduous trees and hangs in crowded tufts up to 30 cm. or more in length. Usually it is so torn, that the real size attainable can only be guessed at. It is attached at the base by a spreading discoid hold-fast, and, in mature plants, consists of a stoutish main axis from which side branches are irregularly given off. These latter are firm at the base like the parent stalk, but soon they broaden out into very wide fronds. Splitting begins at the tips of the branches while still young; they are then spathulate in form with a slightly narrower recurved tip, below which the first perforations are visible, small at first, but gradually enlarging with the growth of the frond.

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Fig. 64. Ramalina reticulata Krempelh. Portion of frond (after Cramer).

[108]

Ramalina reticulata is an extremely gelatinous lichen and the formation of the network was supposed by Lutz[382] to be entirely due to the swelling of the tissues, or the imbibition of water, causing tension and splitting. A more exact explanation of the phenomenon is given by Peirce[383]: he found that it was due to the thickened incurved tip, which, on the addition of moisture, swells in length, breadth and thickness, causing it to bend slightly upwards and then curve backwards over the thallus, thus straining the part immediately behind. These various movements result in the splitting of the frond while it is young and the cortices are thin and weak.

Peirce made a series of experiments to test the capacity of the tissues to support tensile strains. In a dry state, a piece of the lichen held a weight up to 150 grms.; when wet it broke with a weight of 30 grms. It was also observed that the thickness of the frond doubled on wetting.

E. Rooting Base in Fruticose Lichens

Fruticose and filamentous lichens are distinguished by their mode of attachment to the substratum: instead of a system of rhizinae or of hairs spread over a large area, there is usually one definite rooting base by which the plant maintains its hold on the support.

Intermediate between the foliose and fruticose types of thallus are several species which are decumbent in habit, but which are attached at one (or sometimes more) definite points, with but little penetration of the underlying substance. One such lichen, Evernia furfuracea, has been classified now as foliose, and again as fruticose. The earliest stage of the thallus is in the form of a rosette-like sheath which bears rhizinae on the under surface, very numerous at the centre of the sheath, but entirely wanting towards the periphery. A secondary thallus of strap-shaped rather narrow fronds rises from the sheath and increases by irregular dichotomous branching. These branches, which are considered by Zopf[384] as adventitious, may also come into contact with the substratum and produce a few rhizinae at that point; or if the frond is more closely applied, the irritation thus produced causes a still greater outgrowth of rhizinae and the formation of a new base from which other fronds originate. These renewed centres of growth are not of very frequent occurrence; they were first observed and described by Lindau[385] in another species, Evernia prunastri, and were aptly compared by him to the creeping stolons of flowering plants.

Evernia furfuracea grows frequently on dead wood, palings, etc., as well as on trees. E. prunastri grows invariably on trees, and has a more constantly upright fruticose habit; in this species also, a basal sheath is present, and the attachment is secured by means of rhizoidal hyphae which penetrate deeply into the periderm of the tree, taking advantage of the openings[109] afforded by the lenticels. The sheath hyphae are continuous with the medullary hyphae of the frond, and gonidia are frequently enclosed in the tissues; the sheath spreads to some extent over the surface of the bark, and round the base of the fronds, thus rendering the attachment of the lichen to the tree doubly secure.

Among Ramalinae, the development of the base was followed by Brandt[386] in one species, R. Landroensis, an arboreal lichen from S. Tyrol. A rosette-like sheath was formed consisting solely of strands of thick-walled hyphae which spread over the bark. There were no gonidia included in the tissue.

A different type of attachment was found by Lilian Porter[387] in corticolous Ramalinae—R. fraxinea, R. fastigiata, and R. pollinaria. The lichens were anchored to the tree by strands of closely compacted hyphae longitudinally arranged and continuous with the cortical hyphae. These enter the periderm of the tree by cracks or lenticels, and by wedge action cause extensive splitting. The strands may also spread horizontally and give rise to new plants. The living tissues of the tree were thus penetrated and injured, and there was evidence that hypertrophied tissue was formed and caused erosion of the wood.

Fig. 65. Ramalina siliquosa A. L. Sm., on rocks, reduced (M. P., Photo.).

Several Ramalinae—R. siliquosa, R. Curnowii, etc.—grow on rocks, often in extremely exposed situations, in isolated tufts or in crowded swards (Fig. 65). The separate tufts are not unfrequently connected at the base by[110] a crustaceous thallus. It is possible also to see on the rock, here and there, small areas of compact thalline granules that have scarcely begun to put out the upright fronds. These granules are corticate on the upper surface and contain gonidia; from the lower surface, slender branching hyphae in rhizoid-like strands penetrate down between the inequalities and separable particles of the rock, if the formation is granitic. They frequently have groups of gonidia associated with them, and they continue to ramify and spread, the pure white filaments often enough enclosing morsels of the rock. The upright fronds are continuous with the base and are thus securely anchored to the substratum.

On a smooth rock surface such as quartzite a continuous sward of Ramalina growth is impossible. The basal hyphae being unable to penetrate the even surface of the rock, the attachment is slight and the plants are easily dislodged. They do however succeed, sometimes, in taking hold, and small groups of fronds arise from a crustaceous base which varies in depth from ·5 to 1 mm. The tissues of this base are very irregularly arranged: towards the upper surface loose hyphae with scattered groups of algae are traversed by strands of gelatinized sclerotic hyphae similar to the strengthening tissues of the upright fronds, while down below there are to be found not only slender hyphae, but a layer of gonidia visible as a white and green film on the rock when the overlying particles are scaled off.

Darbishire[388] found that attachment to the substratum by means of a basal sheath was characteristic of all the genera of Roccellaceae. He looks on this sheath, which is the first stage in the development of the plant, as a primary or proto-thallus, analogous to the primary squamules of the Cladoniae, and he carries the analogy still further by treating the upright fronds as podetia. The sheath of the Roccellaceae varies in size but it is always of very limited extent; it is mainly composed of medullary hyphae, and gonidia may or may not be present. The whole structure is permanent and important, and is generally protected by a well-developed upper cortex similar in structure to that of the upright thallus, i.e. of a fastigiate type. There is no lower cortex.

The two British species of Roccella—R. fuciformis and R. phycopsis—grow on maritime rocks, the latter also occasionally on trees. In R. fuciformis, the attaching sheath is a flat structure which slopes up a little round the base of the upright frond. It is about 2 mm. thick, the cortex occupying about 40 µ of that space; a few scattered gonidia are present immediately below. The remaining tissue of the sheath is composed of firmly wefted slender filaments. Towards the lower surface, there is a more closely compacted dark brown layer from which pass out the hyphae that penetrate the rock.

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The sheath of R. phycopsis is a small structure about 3 to 4 mm. in width and 1·5 mm. thick. A few gonidia may be found below the dense cortical layer, but they tend to disappear as the upright fronds become larger and the shade, in consequence, more dense. Lower down the hyphae take an intensely yellow hue; mixed with them are also some brown filaments. A somewhat larger sheath 7 to 8 mm. wide forms the base of R. tinctoria. In structure it corresponds—as do those of the other species—with the ones already described.

In purely filamentous species such as Usnea there is also primary sheath formation: the medullary hyphae spread out in radiating strands which force their way wherever possible into the underlying substance; on trees they enter into any chink or crevice of the outer bark like wedges; or they ramify between the cork cells which are split up by the mere growth pressure. By the vertical increase of the base, the fronds may be hoisted up and an intercalary basal portion may arise lacking both gonidia and cortical layer. Very frequently several bases are united and the lichen appears to be of tufted habit.

A basal sheath provides a similar firm attachment for Alectoria jubata and allied species: these are slender mostly dark brown lichens which hang in tangled filaments from the branches of trees, rocks, etc.

These attaching sheaths differ in function as well as in structure from the horizontal thallus of the Cladoniaceae. They may be more truly compared with the primary thallus of the red algae Dumontia and Phyllophora which are similarly affixed to the substratum, while upright fronds of subsequent formation bear the fructifications.

IV. STRATOSE-RADIATE THALLUS

1. STRATOSE OR PRIMARY THALLUS

A. General Characteristics

Fig. 66. Cladonia pyxidata Hoffm. Basal squamule and podetium. a, apothecia; s, spermogonia (after Krabbe).

This series includes the lichens of one family only, the Cladoniaceae, the genera of which are characterized by the twofold thallus, one portion being primary, horizontal and stratose, the other secondary and radiate, the latter an upright simple or branching structure termed a “podetium” which narrows above, or widens to form a trumpet-shaped cup or “scyphus” (Fig. 66). The apothecia are terminal on the podetium or on the margins of the scyphi; in a few species they are developed on the primary thallus. Some degree of primary thallus-formation has been demonstrated in all the genera, if not in all the species of the family. The genus Cladina was established to include those species of Cladonia in which, it was believed, only a secondary[112] podetial thallus was present, but Wainio[389] found in Cladonia sylvatica a granular basal crust and, in Cladonia uncialis, minute round scales with crenate margins measuring from ·5 to 1 mm. in width. In some species (subgenus Cladina) the primary thallus is quickly evanescent, in others it is granular or squamulose and persistent. Where the basal thallus is so much reduced as to be practically non-existent, apothecia are rarely developed and soredia are absent. Renewal of growth in these lichens is secured by the dispersal of fragments of the podetial thallus; they are torn off and scattered by the wind or by animals, and, if suitable conditions are met, a new plant arises.

Cladonia squamules vary in size from very small scales as in Cl. uncialis to the fairly large foliose fronds of Cl. foliacea which extend to 5 cm. in length and about 1 cm. or more in width. It is interesting to note that when the primary thallus is well developed, the podetia are relatively unimportant and frequently are not formed. As a rule the squamules are rounded or somewhat elongate in form with entire or variously cut and crenate margins. They may be very insignificant and sparsely scattered over the substratum, or massed in crowded swards of leaflets which are frequently almost upright. In colour they are bluish-grey, yellowish or brownish above, and white beneath (red in Cl. miniata), frequently becoming very dark-coloured towards the rooting base. These several characteristics are specific and are often of considerable value in diagnosis. In certain conditions of shade or moisture, squamules are formed on the podetium; they repeat the characters of the basal squamules of the species.

B. Tissues of the Primary Thallus

The stratose layers of tissue in the squamules of Cladonia are arranged as in other horizontal thalli.

a. Cortical tissue. In nearly all these squamules the cortex is of the “decomposed” type. In a few species there is a plectenchymatous formation—in Cl. nana, a Brazilian ground species, and in two New Zealand species, Cl. enantia f. dilatata and Cl. Neo-Zelandica. The principal growing area is situated all round the margins though generally there is more activity at the apex. Frequently there is a gradual perishing of the squamule at the base which counterbalances the forward increase.

The upper surface in some species is cracked into minute areolae; the cracks, seen in section, penetrate almost to the base of the decomposed gelatinous cortex. They are largely due to alternate swelling and contraction of the gelatinous surface, or to extension caused, though rarely, by intercalary growth from the hyphae below. The surface is subject to weathering and peeling as in other lichens; but the loss is constantly repaired by the upward growth of the meristematic hyphae from the gonidial zone; they push up[113] between the older cortical filaments and so provide for the expansion as well as for the renewal of the cortical tissue.

b. Gonidial tissue. The gonidia consisting of Protococcaceous algae form a layer immediately below the cortex. Isolated green cells are not unfrequently carried up by the growing hyphae into the cortical region, but they do not long survive in this compact non-aerated tissue. Their empty membranes can however be picked out by the blue stain they take with iodine and sulphuric acid.

Krabbe[390] has described the phases of development in the growing region: he finds that differentiation into pith, gonidial zone and cortex takes place some little way back from the edge. At the extreme apex the hyphae lie fairly parallel to each other; further back, they branch upwards to form the cortex, and to separate the masses of multiplying gonidia, by pushing between them and so spreading them through the whole apical tissue. The gonidia immediately below the upper cortex, where they are well-lighted, continue to increase and gradually form into the gonidial zone; those that lie deeper among the medullary hyphae remain quiescent, and before long disappear altogether.

Where the squamules assume the upright position (as in Cladonia cervicornis), there is a tendency for the gonidia to pass round to the lower surface, and soredia are occasionally formed.

c. Medullary tissue. The hyphae of the medulla are described by Wainio as having long cells with narrow lumen, and as being encrusted with granulations that may coalesce into more or less detachable granules; in colour they are mostly white, but pale-yellow in Cl. foliacea and blood-red in Cl. miniata, a subtropical species. They are connected at the base of the squamules with a filamentous hypothallus which penetrates the substratum and attaches the plant. In a few species rhizinae are formed, while in others the hyphae of the podetium grow downwards, towards and into the substratum as a short stout rhizoid.

d. Soredia. Though frequent on the podetia, soredia are rare on the squamules, and, according to Wainio[391], always originate at the growing region, from which they spread over the under surface—rather sparsely in Cl. cariosa, Cl. squamosa, etc., but abundantly in Cl. digitata and a few others. In some instances, they develop further into small corticate areolae on the under surface (Cl. coccifera, Cl. pyxidata and Cl. squamosa).

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2. RADIATE OR SECONDARY THALLUS

A. Origin of the Podetium

The upright podetium, as described by Wainio[392] and by Krabbe[393], is a secondary product of the basal granule or squamule. It is developed from the hyphae of the gonidial zone, generally where a crack has occurred in the cortex and rather close to the base or more rarely on or near the edge of the squamule (Cl. verticillata, etc.). At these areas, certain meristematic gonidial hyphae increase and unite to form a strand of filaments below the upper cortex but above the gonidial layer, the latter remaining for a time undisturbed as to the arrangement of the algal cells.

This initial tissue—the primordium of the podetium—continues to grow not only in width but in length: the basal portion grows downwards and at length displaces the gonidial zone, while the upper part as a compact cylinder forces its way through the cortex above, the cortical tissue, however, taking no part in its formation; as it advances, the edges of the gonidial and cortical zones bend upwards and form a sheath distinguishable for some time round the base of the emerging podetium.

Even when the primary horizontal thallus is merely crustaceous, the podetia take origin similarly from a subcortical weft of hyphae in an areola or granule.

B. Structure of the Podetium

a. General structure. In the early stages of development the podetium is solid throughout, two layers of tissue being discernible—the hyphae forming the centre of the cylinder being thick-walled and closely compacted, and the hyphae on the exterior loosely branching with numerous air-spaces between the filaments.

In all species, with the exception of Cl. solida, which remains solid during the life of the plant, a central cavity arises while the podetium is still quite short (about 1 to 1·5 mm. in Cl. pyxidata and Cl. degenerans). The first indication of the opening is a narrow split in the internal cylinder, due to the difference in growth tension between the more free and rapid increase of the external medullary layer and the slower elongation of the chondroid tissue at the centre. The cavity gradually widens and becomes more completely tubular with the upward growth of the podetium; it is lined by the chondroid sclerotic band which supports the whole structure (Fig. 67).

b. Gonidial tissue. In most species of Cladoniaceae, a layer of gonidial tissue forms a more or less continuous outer covering of the podetium,[115] thus distinguishing it from the purely hyphal stalks of the apothecia in Caliciaceae. Even in the genus Baeomyces, while the podetia of some of the species are without gonidia, neighbouring species are provided with green cells on the upright stalks clearly showing their true affinity with the Cladoniae. In one British species of Cladonia (Cl. caespiticia) the short podetium consists only of the fibrous chondroid cylinder, and thus resembles the apothecial stalk of Baeomyces rufus, but in that species also there are occasional surface gonidia that may give rise to squamules.

Fig. 67. Cladonia squamosa Hoffm. Vertical section of podetium with early stage of central tube and of podetial squamules × 100 (after Krabbe).

Krabbe[394] concluded from his observations that the podetial gonidia of Cladonia arrived from the open, conveyed by wind, water or insects from the loose soredia that are generally so plentiful in any Cladonia colony. They alighted, he held, on the growing stalks and, being secured by the free-growing ends of the exterior hyphae, they increased and became an integral part of the podetium. In more recent times Baur[395] has recalled and supported Krabbe’s view, but Wainio[396], on the contrary, claims to have proved that in the earliest stages of the podetium the gonidia were already present, having been carried up from the gonidial zone of the primary thallus by the primordial hyphae. Increase of these green cells follows normally by cell-division or sporulation.

Algal cells have been found to be common to different lichens, but in Cladoniae Chodat[397] claims to have proved by cultures that each species tested has a special gonidium, determined by him as a species of Cystococcus, which would render colonization by algae from the open much less probable. In addition, the fungal hyphae are specific, and any soredia (with their combined symbionts) that alighted on the podetium could only be utilized if they originated from the same species; or, if they were incorporated, the hyphae belonging to any other species would of necessity die off and be replaced by those of the podetium.

c. Cortical tissue. In some species a cortex of the decomposed type of thick-walled conglutinate hyphae is present, either continuous over the whole surface of the podetium, as in Cl. gracilis (Fig. 68), or in interrupted areas or granules as in Cl. pyxidata (Fig. 69) and others. In Cl. degenerans, the spaces between the corticated areolae are filled in by loose filaments without any green cells. Cl. rangiferina, Cl. sylvatica, etc. are non-corticate, being covered all over with a loose felt of intricate hyphae.

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Fig. 68. Cladonia gracilis Hoffm. (S. H., Photo.).

Fig. 69. Cladonia pyxidata Hoffm. (S. H., Photo.).

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In the section Clathrinae (Cl. retepora, etc.) the cortex is formed of longitudinal hyphae with thick gelatinous walls.

d. Soredia. Frequently the podetium is coated in whole or in part by granules of a sorediate character—coarsely granular in Cl. pyxidata, finely pulverulent in Cl. fimbriata. Though fairly constant to type in the different species, they are subject to climatic influences, and, when there is abundant moisture, both soredia and areolae develop into squamules on the podetium. A considerable number of species have thus a more or less densely squamulose “form” or “variety.”

C. Development of the Scyphus

Two types of podetia occur in Cladonia: those that end abruptly and are crowned when fertile by the apothecia or spermogonia (pycnidia), or if sterile grow indefinitely tapering gradually to a point (Fig. 70); and those that widen out into the trumpet-shaped or cup-like expansion called the scyphus (Fig. 69). Species may be constantly scyphiferous or as constantly ascyphous; in a few species, and even in individual tufts, both types of podetium may be present.

Fig. 70. Cladonia furcata Schrad. Sterile thallus (S.H., Photo.).

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Wainio[398], who has studied every stage of development in the Cladoniae, has described the scyphus as originating in several different ways:

a. From abortive Apothecia. In certain species the apothecium appears at a very early stage in the development of the podetium of which it occupies the apical region. Owing to the subsequent formation of the tubular cavity in the centre of the stalk, the base of the apothecium may eventually lie directly over the hollow space and, therefore, out of touch with the growing assimilating tissues; or even before the appearance of the tube, the wide separation between the primordium of the apothecium and the gonidia, entailing deficient nutrition, may have produced a similar effect. In either case central degeneration of the apothecium sets in, and the hypothecial filaments, having begun to grow radially, continue to travel in the same direction both outwards and upwards so that gradually a cup-shaped structure is evolved—the amphithecium of the fruit without the thecium.

The whole or only a part of the apothecium may be abortive, and the scyphus may therefore be entirely sterile or the fruits may survive at the edges. The apothecia may even be entirely abortive after a fertile commencement, but in that case also the primordial hyphae retain the primitive impulse not only to radial direction, but also to the more copious branching, and a scyphus is formed as in the previous case. It must also be borne in mind that the tendency in many Cladonia species to scyphiform has become hereditary.

Baur[399], in his study of Cl. pyxidata, has taken the view that the origin of the scyphus was due to a stronger apical growth of the hyphae at the circumference than over the central tubular portion of the podetium, and that considerable intercalary growth added to the expanding sides of the cup.

Scyphi originating from an abortive apothecium are characteristic of species in which the base is closed (Wainio’s Section Clausae), the tissue in that case being continuous over the inside of the cup as in Cl. pyxidata, Cl. coccifera and many others.

b. From polytomous Branching. Another method of scyphus formation occurs in Cl. amaurocrea and a few other species in which the branching is polytomous (several members rising from about the same level). Concrescence of the tissues at the base of these branches produces a scyphus; it is normally closed by a diaphragm that has spread out from the different bases, but frequently there is a perforation due to stretching. These species belong to the Section Perviae.

c. From arrested Growth. In most cases however where the scyphus is open as in Cl. furcata, Cl. squamosa, etc., development of the cup[119] follows on cessation of growth, or on perforation at the summit of the podetium. Round this quiescent portion there rises a circle of minute prominences which carry on the apical development. As they increase in size, the spaces between them are bridged over by lateral growth, and the scyphus thus formed is large or small according to the number of these outgrowths. Apothecia or spermogonia may be produced at their tips, or the vegetative development may continue. Scyphi formed in this manner are also open or “pervious.”

d. Gonidia of the Scyphus. Gonidia are absent in the early stages of scyphus formation when it arises from degeneration of the apical tissues, either fertile or vegetative; but gradually they migrate from the podetium, from the base of young outgrowths, or by furrows at the edge, and so spread over the surface of the cup. Soredia may possibly alight, as Krabbe insists that they do, and may aid in colonizing the naked area. Their presence, however, would only be accidental; they are not essential, and scyphi are formed in many non-sorediate species such as Cl. verticillata. The cortex of the scyphus becomes in the end continuous with that of the podetium and is always similar in type.

e. Species without Scyphi. In species where the whole summit of the podetium is occupied by an apothecium, as in Cl. bellidiflora, no scyphus is formed. There is also an absence of scyphi in podetia that taper to a point. In those podetia the hyphae are parallel to the long axis and remain in connection with the external gonidial layer so that they are unaffected by the central cavity. Instances of tapering growth are also to be found in species that are normally scyphiferous such as Cl. fimbriata subsp. fibula, and Cl. cornuta, as well as in species like Cl. rangiferina that are constantly ascyphous.

The scyphus is considered by Wainio[400] to represent an advanced stage of development in the species or in the individual, and any conditions that act unfavourably on growth, such as excessive dryness, would also hinder the formation of this peculiar lichen structure.

D. Branching of the Podetium

Though branching is a constant feature in many species, regular dichotomy is rare: more often there is an irregular form of polytomy in which one of the members grows more vigorously than the others and branches again, so that a kind of sympodium arises, as in Cl. rangiferina, Cl. sylvatica, etc.

Adventitious branches may also arise from the podetium, owing to some disturbance of the normal growth, some undue exposure to wind or to too[120] great light, or owing to some external injury. They originate from the gonidial tissue in the same way as does the podetium from the primary thallus; the parallel hyphae of the main axis take no part in their development.

In a number of species secondary podetia arise from the centre of the scyphus—constantly in Cl. verticillata and Cl. cervicornis, etc., accidentally or rarely in Cl. foliacea, Cl. pyxidata, Cl. fimbriata, etc. Wainio[401] has stated that they arise when the scyphus is already at an advanced stage of growth and that they are to be regarded as adventitious branches.

The proliferations from the borders of the scyphus are in a different category. They represent the continuity of apical growth, as the edges of the scyphus are but an enlarged apex. These marginal proliferations thus correspond to polytomous branching. In many instances their advance is soon stopped by the formation of an apothecium and they figure more as fruit stalks than as podetial branches.

E. Perforations and Reticulation of the Podetium

Perforations in the podetial wall at the axils of the branches are constant in certain species such as Cl. rangiferina, Cl. uncialis, etc. They are caused by the tension of the branches as they emerge from the main stalk. A tearing of the tissue may also arise in the base of the scyphus, due to its increase in size, which causes the splitting of the diaphragm at the bottom of the cup.

Among the Cladoniae the reticulate condition recurs now and again. In our native Cladonia cariosa the splitting of the podetial wall is a constant character of the species, the carious condition being caused by unequal growth which tears apart the longitudinal fibres that surround the central hollow.

A more advanced type of reticulation arises in the group of the Clathrinae in which there is no inner chondroid cylinder. In Cladonia aggregata, in which the perforations are somewhat irregular, two types of podetia have been described by Lindsay[402] from Falkland Island specimens: those bearing apothecia are short and broad, fastigiately branched upwards and with reticulate perforations, while podetia bearing spermogonia are slender, elongate and branched, with fewer reticulations. An imperfect network is also characteristic of Cl. Sullivani, a Brazilian species. But the most marvellous and regular form of reticulation occurs in Cl. retepora, an Australian lichen (Fig. 71): towards the tips of the podetia the ellipsoid meshes are small, but they gradually become larger towards the base. In this species the outer tissue, though of parallel hyphae, is closely interwoven and forms[121] a continuous growth at the edges of the perforations, giving an unbroken smooth surface and checking any irregular tearing. The enlargement of the walls is solely due to intercalary growth. The origin of the reticulate structure in the Clathrinae is unknown, though it is doubtless associated with wide podetia and rendered possible by the absence of an internal chondroid layer. The reticulate structure is marvellously adapted for the absorption of water: Cl. retepora, more especially, imbibes and holds moisture like a sponge.

Fig. 71. Cladonia retepora Fr. From Tasmania.

F. Rooting Structures of Cladoniae

The squamules of the primary thallus are attached, as are most squamules, to the supporting substance by strands of hyphae which may be combined into simple or branching rhizinae and penetrate the soil or the wood on which the lichen grows. There is frequently but one of these rooting structures and it branches repeatedly until the ultimate branchlets end in delicate mycelium. Generally they are grey or brown and are not[122] easily traced, but when they are orange-coloured, as according to Wainio[403] they frequently are in Cladonia miniata and Cl. digitata, they are more readily observed, especially if the habitat be a mossy one.

In Cl. alpicola it has been found that the rooting structure is frequently as thick as the podetium itself. If the podetium originates from the basal portion of the squamule, the hyphae from the chondroid layer, surrounding the hollow centre, take a downward direction and become continuous with the rhizoid. Should the point of insertion be near the apex of the squamule, these hyphae form a nerve within the squamule or along the under surface, and finally also unite with the rhizoid at the base, a form of rooting characteristic of Cl. cartilaginea, Cl. digitata and several other species.

Mycelium may spread from the rhizinae along the surface of the substratum and give rise to new squamules and new tufts of podetia, a method of reproduction that is of considerable importance in species that are generally sterile and that form no soredia.

Many species, especially those of the section Cladina, soon lose all connection with the substratum, there being a continual decay of the lower part of the podetia. As apical growth may continue for centuries, the perishing of the base is not to be wondered at.

G. Haptera

The presence of haptera in Cladoniae has already been alluded to. They occur usually in the form of cilia or rhizinae[404], but differ from the latter in their more simple regular growth being composed of conglutinate parallel hyphae. They arise on the edges of the squamules or of the scyphus, but in Cl. foliacea and Cl. ceratophylla they are formed at the points of the podetial branches (more rarely in Cl. cervicornis and Cl. gracilis). By the aid of these rhizinose haptera the squamule or branch becomes attached to any substance within reach. They also aid in the production of new individuals by anchoring some fragment of the thallus to a support until it has grown to independent existence and has produced new rhizinae or hold-fasts. They are a very prominent feature of Cl. verticillaris f. penicillata in which they form a thick fringe on the edges of the squamules, or frequently grow out as branched cilia from the proliferations on the margins of the scyphus.

H. Morphology of the Podetium

In the above account, the podetia have been treated as part of the vegetative thallus, seeing that, partly or entirely, they are assimilative and absorptive organs. This view does not, however, take into account their origin and development, in consideration of which Wainio[405] and later Krabbe[406][123] considered them as part of the sporiferous organ. This view was also held by some of the earliest lichenologists: Necker[407], for instance, constantly referred to the upright structure as “stipes”; Persoon[408] included it, under the term “pedunculus,” as part of the “inflorescence” of the lichen, and Acharius[409] established the name “podetium” to describe the stalk of the apothecium in Baeomyces.

Later lichenologists, such as Wallroth[410], looked on the podetia as advanced stages of the thallus, or as forming a supplementary thallus. Tulasne[411] described them as branching upright processes from the horizontal form, and Koerber[412] considered them as the true thallus, the primary squamule being merely a protothallus. By them and by succeeding students of lichens the twofold character of the thallus was accepted until Wainio and Krabbe by their more exact researches discovered the endogenous origin of the podetium, which they considered was conclusive evidence of its apothecial character: they claimed that the primordium of the podetium was homologous with the primordium of the apothecium. Reinke[413] and Wainio are in accord with Krabbe as to the probable morphological significance of the podetium, but they both insist on its modified thalline character. Wainio sums up that: “the podetium is an apothecial stalk, that is to say an elongation of the conceptacle most frequently transformed by metamorphosis to a vertical thallus, though visibly retaining its stalk character.” Sättler[414], one of the most recent students of Cladonia, regards the podetium as evolved with reference to spore-dissemination, and therefore of apothecial character. His views are described and discussed in the chapter on phylogeny.

Reinke and others sought for a solution of the problem in Baeomyces, one of the more primitive genera of the Cladoniaceae. The thallus, except in a few mostly exotic species, scarcely advances beyond the crustaceous condition; the podetia are short and so varied in character that species have been assigned by systematists to several different genera. In one of them, Baeomyces roseus, the podetium or stalk originates according to Nienburg[415] deep down in the medulla of a fertile granule as a specialized weft of tissue; there is no carpogonium nor trichogyne formed; the hyphae that grow upward and form the podetium are generative filaments and give rise to asci and paraphyses. In a second species, B. rufus (Sphyridium), the gonidial zone and outer cortex of a thalline granule swell out to form a thalline protuberance; the carpogonium arises close to the apex, and from it branch the generative filaments. Nienburg regards the stalk of B. roseus as apothecial and as representing an extension of the proper margin[416] (excipulum proprium), that of B. rufus as a typical vegetative podetium.

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In the genus Cladonia, differentiation of the generative hyphae may take place at a very early stage. Wainio[417] observed, in Cl. caespiticia, a trichogyne in a still solid podetium only 90µ in height; usually they appear later, and, where scyphi are formed, the carpogonium often arises at the edge of the scyphus. Baur[418] and Wolff[419] have furnished conclusive evidence of the late appearance of the carpogonium in Cl. pyxidata, Cl. degenerans, Cl. furcata and Cl. gracilis: in all of these species carpogonia with trichogynes were observed on the edge of well-developed scyphi. Baur draws the conclusion that the podetium is merely a vertical thallus, citing as additional evidence that it also bears the spermogonia (or pycnidia), though at the same time he allows that the apothecium may have played an important part in its phylogenetic development. He agrees also with the account of the first appearance of the podetium as described by Krabbe, who found that it began with the hyphae of the gonidial zone branching upwards in a quite normal manner, only that there were more of them, and that they finally pierced the cortex. Krabbe also asserted that in the early stages the podetia were without gonidia and that these arrived later from the open as colonists, in this contradicting Wainio’s statement that gonidia were carried up from the primary thallus.

It seems probable that the podetium—as Wainio and Baur both have stated—is homologous with the apothecial stalk, though in most cases it is completely transformed into a vertical thallus. If the view of their formation from the gonidial zone is accepted, then they differ widely in origin from normal branches in which the tissues of the main axis are repeated in the secondary structures, whereas in this vertical thallus, hyphae from the gonidial zone alone take part in the development. It must be admitted that Baur’s view of the podetium as essentially thalline seems to be strengthened by the formation of podetia at the centre of the scyphus, as in Cl. verticillata, which are new structures and are not an elongation of the original conceptacular tissue. It can however equally be argued that the acquired thalline character is complete and, therefore, includes the possibility of giving rise to new podetia.

The relegation of the carpogonium to a position far removed from the base or primordium of the apothecium need not necessarily interfere with the conception of the primordial tissue as homologous with the conceptacle; but more research is needed, as Baur dealt only with one species, Cl. pyxidata, and Gertrude Wolff confined her attention to the carpogonial stages at the edge of the scyphus.

The Cladoniae require light, and inhabit by preference open moorlands, naked clay walls, borders of ditches, exposed sand-dunes, etc. Those with large and persistent squamules can live in arid situations, probably because[125] the primary thallus is able to retain moisture for a long time[420]. When the primary thallus is small and feeble the podetia are generally much branched and live in close colonies which retain moisture. Sterile podetia are long-lived and grow indefinitely at the apex though the base as continually perishes and changes into humus. Wainio[421] cites an instance in which the bases of a tuft of Cl. alpestris had formed a gelatinous mass more than a decimetre in thickness.

I. Pilophorus and Stereocaulon

These two genera are usually included in Cladoniaceae on account of their twofold thallus and their somewhat similar fruit formation. They differ from Cladonia in the development of the podetia which are not endogenous in origin as in that genus, but are formed by the growth upwards of a primary granule or squamule and correspond more nearly to Tulasne’s conception of the podetium as a process from the horizontal thallus. In Pilophorus the primary granular thallus persists during the life of the plants; the short podetium is unbranched, and consists of a somewhat compact medulla of parallel hyphae surrounded by a looser cortical tissue, such as that of the basal granule, in which are embedded the algal cells. The black colour of the apothecium is due to the thick dark hypothecium.

Stereocaulon is also a direct growth from a short-lived primary squamule[422]. The podetia, called “pseudopodetia” by Wainio, are usually very much branched. They possess a central strand of hyphae not entirely solid, and an outer layer of loose felted hyphae in which the gonidia find place. A coating of mucilage on the outside gives a glabrous shiny surface, or, if that is absent, the surface is tomentose as in St. tomentosum. In all the species the podetia are more or less thickly beset with small variously divided squamules similar in form to the primary evanescent thallus. Gall-like cephalodia are associated with most of the species and aid in the work of assimilation.

Stereocaulon cannot depend on the evanescent primary thallus for attachment to the soil. The podetia of the different species have developed various rooting bases: in St. ramulosum there is a basal sheath formed, in St. coralloides a well-developed system of rhizoids[423].

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V. STRUCTURES PECULIAR TO LICHENS

1. AERATION STRUCTURES

A. Cyphellae and Pseudocyphellae

The thallus of Stictaceae has been regarded by Nylander[424] and others as one of the most highly organized, not only on account of the size attained by the spreading lobes, but also because in that family are chiefly found those very definite cup-like structures which were named “cyphellae” by Acharius[425]. They are small hollow depressions about 1/2 mm. or more in width scattered irregularly over the under surface of the thallus.

a. Historical. Cyphellae were first pointed out by the Swiss botanist, Haller[426]. In his description of a lichen referable to Sticta fuliginosa he describes certain white circular depressions “to be found among the short brown hairs of the under surface.” At a later date Schreber[427] made these “white excavated points” the leading character of his lichen genus Sticta.

In urceolate or proper cyphellae, the base of the depression rests on the medulla; the margin is formed from the ruptured cortex and projects slightly inwards over the edge of the cup. Contrasted with these are the pseudocyphellae, somewhat roundish openings of a simpler structure which replace the others in many of the species. They have no definite margin; the internal hyphae have forced their way to the exterior and form a protruding tuft slightly above the surface. Meyer[428] reckoned them all among soredia; but he distinguished between those in which the medullary hyphae became conglutinated to form a margin (true cyphellae) and those in which there was a granular outburst of filaments (pseudocyphellae). He also included a third type, represented in Lobaria pulmonaria on the under surface of which there are numerous non-corticate, angular patches where the pith is laid bare (Fig. 72). Delise[429], writing about the same time on the Sticteae, gives due attention to their occurrence, classifying the various species of Sticta as cyphellate or non-cyphellate.

Acharius had limited the name “cyphella” to the hollow urceolate bodies that had a well-defined margin. Nylander[430] at first included under that term both types of structure, but later[431] he classified the pulverulent “soredia-like” forms in another group, the pseudocyphellae. As a rule they bear no relation to soredia, and algae are rarely associated with the protruding filaments. Schwendener[432], and later Wainio[433], in describing Sticta aurata from Brazil, state, as exceptional, that the citrine-yellow pseudocyphellae of that species are sparingly sorediate.

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Fig. 72. Lobaria pulmonaria Hoffm. Showing pitted surface. a, under surface. Reduced (S. H., Photo.).

Fig. 73. Sticta damaecornis Nyl. Transverse section of thallus with cyphella × 100.

b. Development of Cyphellae. The cortex of both surfaces in the thallus of Sticta is a several-layered plectenchyma of thick-walled closely packed cells, the outer layer growing out into hairs on the under surface of most of the species. Where either cyphellae or pseudocyphellae occur, a more or less open channel is formed between the exterior and the internal tissues of the lichen. In the case of the cyphellae, the medullary hyphae which line the cup are divided into short roundish cells with comparatively thin walls (Fig. 73). They form a tissue sharply differentiated from the loose hyphae that occupy the medulla. The rounded cells tend to lie in vertical rows, though the arrangement in fully formed cyphellae is generally[128] somewhat irregular. The terminal empty cells are loosely attached and as they are eventually abstricted and strewn over the inside of the cup they give to it the characteristic white powdery appearance.

According to Schwendener[434] development begins by an exuberant growth of the medulla which raises and finally bursts the cortex; prominent cyphellae have been thus formed in Sticta damaecornis (Fig. 73). In other species the swelling is less noticeable or entirely absent. The opening of the cup measures usually about 1/2 mm. across, but it may stretch to a greater width.

c. Pseudocyphellae. In these no margin is formed, the cortex is simply burst by the protruding filaments which are of the same colour—yellow or white—as the medullary hyphae. They vary in size, from a minute point up to 4 mm. in diameter.

d. Occurrence and Distribution. The genus Sticta is divided into two sections: (1) Eusticta in which the gonidia are bright-green algae, and (2) Stictina in which they are blue-green. Cyphellae and pseudocyphellae are fairly evenly distributed between the sections; they never occur together. Stizenberger[435] found that 36 species of the section Eusticta were cyphellate, while in 43 species pseudocyphellae were formed. In the section Stictina there were 38 of the former and only 31 of the latter type. Both sections of the genus are widely distributed in all countries, but they are most abundant south of the equator, reaching their highest development in Australia and New Zealand.

In the British Isles Sticta is rather poorly represented as follows:

Structures resembling cyphellae, with an overarching rim, are sprinkled over the brown under surface of the Australian lichen, Heterodea Mülleri; the thallus is without a lower cortex, the medulla being protected by thickly woven hyphae. Heterodea was at one time included among Stictaceae, though now it is classified under Parmeliaceae. Pseudocyphellae are also present on the non-corticate under surface of Nephromium tomentosum, where they occur as little white pustules among the brown hairs; and the white impressed spots on the under surface of Cetraria islandica and allied species, first determined as air pores by Zukal[436], have also been described by Wainio[437] as pseudocyphellae.

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There seems no doubt that the chief function of these various structures is, as Schwendener[438] suggested, to allow a free passage of air to the assimilating gonidial zone. Jatta[439] considers them to be analogous to the lenticels of higher plants and of service in the interchange of gases—expelling carbonic acid and receiving oxygen from the outer atmosphere. It is remarkable that such serviceable organs should have been evolved in so few lichens.

B. Breathing-Pores

Fig. 74. Parmelia exasperata Carroll. Vertical section of thallus. a, breathing-pores; b, rhizoid. × 60 (after Rosendahl).

a. Definite Breathing-Pores. The cyphellae and pseudocyphellae described above are confined to the under surface of the thallus in those lichens where they occur. Distinct breathing-pores of a totally different structure are present on the upper surface of the tree-lichen, Parmelia aspidota (P. exasperata), one of the brown-coloured species. They are somewhat thickly scattered as isidia- or cone-like warts over the lichen thallus (Fig. 74) and give it the characteristically rough or “exasperate” character. They are direct outgrowths from the thallus, and Zukal[440], who discovered their peculiar nature and function, describes them as being filled with a hyphal tissue, with abundant air-spaces, and in direct communication with the medulla; gonidia, if present, are confined to the basal part. The cortex covering these minute cones, he further states, is very thin on the top, or often wanting, so that a true pore is formed which, however, is only opened after the cortex elsewhere has become thick and horny. Rosendahl[441], who has re-examined these “breathing-pores,” finds that in the early stage of their growth, near the margin or younger portion of the thallus, they are entirely covered by the cortex. Later, the hyphae at the top become looser and more frequently septate, and a fine network of anastomosing and intricate filaments takes the place of the closely cohering cortical cells. These hyphae are divided into shorter cells, but do not otherwise differ from those of the medulla. Rosendahl was unable to detect an open pore at any stage, though he entirely agrees with Zukal as to the breathing function of these structures. The gonidia of the immediately underlying zone are sparsely arranged and a few of them are found in the lower half of the cone; the hyphae of the medulla can be traced up to the apex.[130] Zukal[442] claims to have found breathing-pores in Cornicularia (Parmelia) tristis and in several other Parmeliae, notably in Parmelia stygia. The thallus of the latter species has minute holes or openings in the upper cortex, but they are without any definite form and may be only fortuitous.

Fig. 75 A. Ramalina fraxinea Ach. A, surface view of frond. a, air-pores; b, young apothecia. × 12. B, transverse section of part of frond. a, breathing-pore; f, strengthening fibres. × 37 (after Brandt).

Fig. 75 B. Ramalina strepsilis Zahlbr. Transverse section of part of frond showing distribution of: a, air-pores, and f, strengthening fibres. × 37 (after Brandt).

Zukal[442] published drawings of channels of looser tissue between the exterior and the pith in Oropogon Loxensis and in Usnea barbata. He considered them to be of definite service in aeration. The fronds of Ramalina dilacerata by stretching develop a series of elongate holes. Reinke[443] found openings in Ramalina Eckloni which pierced to the centre of the thallus, and Darbishire[444] has figured a break in the frond of another species, R. fraxinea (Fig. 75 A), which he has designated as a breathing-pore. Finally Brandt[445], in his careful study of the anatomy of Ramalinae, has described as breathing-pores certain open areas usually of ellipsoid form in the compact cortex of several species: in R. strepsilis (Fig. 75 B) and R. Landroensis, and in the British species, R. siliquosa and R. fraxinea. These openings are however mostly rare and difficult to find or to distinguish from holes that may be due to any accident in the life of the lichen. It is noteworthy that Rosendahl found no further examples of breathing-pores in the brown Parmeliae that he examined in such detail. No other organs specially adapted for aeration of the thallus have been discovered.

b. Other openings in the Thallus. Lobaria is the only genus of Stictaceae in which neither cyphellae nor pseudocyphellae are formed; but in two species, L. scrobiculata and L. pulmonaria, the lower surface is marked[131] with oblong or angular bare convex patches, much larger than cyphellae. They are exposed portions of the medulla, which at these spots has been denuded of the covering cortex. Corresponding with these bare spots there is a pitting of the upper surface.

A somewhat similar but reversed structure characterizes Umbilicaria pustulata, which as the name implies is distinguished by the presence of pustules, ellipsoid swellings above, with a reticulation of cavities below. Bitter[446] in this instance has proved that they are due to disconnected centres of intercalary growth which are more vigorous on the upper surface and give rise to cracks in the less active tissue beneath. These cracks gradually become enlarged; they are, as it were, accidental in origin but are doubtless of considerable service in aeration.

In some Parmeliae there are constantly formed minute round holes, either right through the apothecia (P. cetrata, etc.), or through the thallus (P. pertusa). Minute holes are also present in the under cortex of Parmelia vittata and of P. enteromorpha, species of the subgenus Hypogymnia. Nylander[447], who first drew attention to these holes of the lower cortex, described them as arising at the forking of two lobes; but though they do occur in that position, they as frequently bear no relation to the branching. Bitter’s[448] opinion is that they arise by the decay of the cortical tissues in very limited areas, from some unknown cause, and that the holes that pierce right through the thallus in other species may be similarly explained.

Still other minute openings into the thallus occur in Parmelia vittata, P. obscurata and P. farinacea var. obscurascens. In the two latter the openings like pin-holes are terminal on the lobes and are situated exactly on the apex, between the pith and the gonidial zone; sometimes several holes can be detected on the end of one lobe. Further growth in length is checked by these holes. They appear more frequently on the darker, better illuminated plants. In Parmelia vittata the terminal holes are at the end of excessively minute adventitious branches which arise below the gonidial zone on the margin of the primary lobes. All these terminal holes are directed upwards and are visible from above.

Bitter does not attribute any physiological significance to these very definite openings in the thallus. It has been generally assumed that they aid in the aeration of the thallus; it is also possible that they may be of service in absorption, and they might even be regarded as open water conductors.

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C. General Aeration of the Thallus

Definite structures adapted to secure the aeration of the thallus in a limited number of lichens have been described above. These are the breathing-pores of Parmelia exasperata and the cyphellae and pseudocyphellae of the Stictaceae, with which also may be perhaps included the circumscribed breaks in the under cortex in some members of that family.

Though lichens are composed of two actively growing organisms, the symbiotic plant increases very slowly. The absorption of water and mineral salts must in many instances be of the scantiest and the formation of carbohydrates by the deep-seated chlorophyll cells of correspondingly small amount. Active aeration seems therefore uncalled for though by no means excluded, and there are many indirect channels by which air can penetrate to the deeper tissues.

In crustaceous forms, whether corticate or not, the thallus is often deeply seamed and cracked into areolae, and thus is easily pervious to water and air. The growing edges and growing points are also everywhere more or less loose and open to the atmosphere. In the larger foliose and fruticose lichens, the soredia that burst an opening in the thallus, and the cracks that are so frequent a feature of the upper cortex, all permit of gaseous interchange. The apical growing point of fruticose lichens is thin and porous, and in many of them the ribs and veins of their channelled surfaces entail a straining of the cortical tissue that results in the formation of thinner permeable areas. Zukal[449] devoted special attention to the question of aeration, and he finds evidence of air-passages through empty spermogonia and through the small round holes that are constant in the upper surface of certain foliose species. He claims also to have proved a system of air-canals right through the thallus of the gelatinous Collemaceae. Though his proof in this instance is somewhat unconvincing, he establishes the abundant presence of air in the massively developed hypothecium of Collema fruits. He found that the carpogonial complex of hyphae was always well supplied with air, and that caused him to view with favour the suggestion that the function of the trichogyne is to provide an air-passage. In foliose lichens, the under surface is frequently non-corticate, in whole or in part; or the cortex becomes seamed and scarred with increasing expansion, the growth in the lower layers failing to keep pace with that of the overlying tissues, as in Umbilicaria pustulata.

It is unquestionable that the interior of the thallus of most lichens contains abundant empty spaces between the loose-lying hyphae, and that these spaces are filled with air.

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2. CEPHALODIA

A. Historical and Descriptive

The term “cephalodium” was first used by Acharius[450] to designate certain globose apothecia (pycnidia). At a later date he applied it to the peculiar outgrowths that grow on the thallus of Peltigera aphthosa, already described by earlier writers, along with other similar structures, as “corpuscula,” “maculae,” etc. The term is now restricted to those purely vegetative gall-like growths which are in organic connection with the thallus of the lichen, but which contain one or more algae of a different type from the one present in the gonidial zone. They are mostly rather small structures, and they take various forms according to the lichen species on which they occur. They are only found on thalli in which the gonidia are bright-green algae (Chlorophyceae) and, with a few exceptions, they contain only blue-green (Myxophyceae). Cephalodia with bright-green algae were found by Hue[451] on two Parmeliae from Chili, in addition to the usual blue-green forms; the one contained Urococcus, the other Gloeocystis. Several with both types of algae were detected also by Hue[451] within the thallus of Aspicilia spp.

Flörke[452] in his account of German lichens described the cephalodia that grow on the podetia of Stereocaulon as fungoid bodies, “corpuscula fungosa.” Wallroth[453], who had made a special study of lichen gonidia, finally established that the distinguishing feature of the cephalodia was their gonidia which differed in colour from those of the normal gonidial zone. He considered that the outgrowths were a result of changes that had arisen in the epidermal tissues of the lichens, and, to avoid using a name of mixed import such as “cephalodia,” he proposed a new designation, calling them “phymata” or warts.

Further descriptions of cephalodia were given by Th. M. Fries[454] in his Monograph of Stereocaulon and Pilophorus; but the greatest advance in the exact knowledge of these bodies is due to Forssell[455] who made a comprehensive examination of the various types, examples of which occurred, he found, in connection with about 100 different lichens. Though fairly constant for the different species, they are not universally so, and are sometimes very rare even when present, and then difficult to find. A striking instance of variability in their occurrence is recorded for Ricasolia amplissima (Lobaria laciniata) (Fig. 76). The cephalodia of that species are prominent upright branching structures which grow in crowded tufts irregularly scattered over the surface. They are an unfailing and conspicuous specific character of the lichens in Europe, but are entirely wanting in North American specimens.

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Fig. 76. Ricasolia amplissima de Not. (Lobaria laciniata Wain.) on oak, reduced. The dark patches are tufts of branching cephalodia (A. Wilson, Photo.).

As cephalodia contain rather dark-coloured, blue-green algae, they are nearly always noticeably darker than the thalli on which they grow, varying from yellowish-red or brown in those of Lecanora gelida to pale-coloured in Lecidea consentiens[456], a darker red in Lecidea panaeola and various shades of green, grey or brown in Stereocaulon, Lobaria (Ricasolia), etc. They form either flat expansions of varying size on the upper surface of the thallus, rounded or wrinkled wart-like growths, or upright branching structures. On the lower surface, where they are not unfrequent, they take the form of small brown nodules or swellings. In a number of species packets of blue-green algae surrounded by hyphae are found embedded in the thallus, either in the pith or immediately under the cortex. They are of the same nature as the superficial excrescences and are also regarded as cephalodia.

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B. Classification

Forssell has drawn up a classification of these structures, as follows:

I. Cephalodia vera.

1. Cephalodia epigena (including perigena) developed on the upper outer surface of the thallus, which are tuberculose, lobulate, clavate or branched in form. These are generally corticate structures.

2. Cephalodia hypogena which are developed on the under surface of the thallus; they are termed “thalloid” if they are entirely superficial, and “immersed” when they are enclosed within the tissues. They are non-corticate though surrounded by a weft of hyphae. Forssell further includes here certain placodioid (lobate), granuliform and fruticose forms which develop on the hypothallus of the lichen, and gradually push their way up either through the host thallus, or, as in Lecidea panaeola, between the thalline granules.

Nylander[457] arranged the cephalodia known to him in three groups: (1) Ceph. epigena, (2) Ceph. hypogena and (3) Ceph. endogena. Schneider[458] still more simply and practically describes them as Ectotrophic (external), and Endotrophic (internal).

II. Pseudocephalodia.

These are a small and doubtful group of cephalodia which are apparently in very slight connection with the host thallus, and show a tendency to independent growth. They occur as small scales on Solorina bispora[459] and S. spongiosa and also on Lecidea pallida. Forssell has suggested that the cephalodia of Psoroma hypnorum and of Lecidea panaeola might also be included under this head.

Forssell and others have found and described cephalodia in the following families and genera:

Sphaerophoraceae.

Lecideaceae.

Cladoniaceae.

Pannariaceae.

Peltigeraceae.

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Stictaceae.

Lecanoraceae.

Physciaceae.

C. Algae that form Cephalodia

The algae of the cephalodia belong mostly to genera that form the normal gonidia of other lichens. They are:

Stigonema,—in Lecanora gelida, Stereocaulon, Pilophorus robustus, and Lecidea pelobotrya.

Scytonema,—a rare constituent of cephalodia.

Nostoc,—the most frequent gonidium of cephalodia. It occurs in those of the genera Sticta, Lobaria, Peltigera, Nephroma, Solorina and Psoroma; occasionally in Stereocaulon and in Lecidea pallida.

Lyngbya and Rivularia,—rarely present, the latter in Sticta oregana[462].

Chroococcus and Gloeocapsa,—also very rare.

Scytonema, Chroococcus, Gloeocapsa and Lyngbya are generally found in combination with some other cephalodia-building alga, though Nylander[463] found Scytonema alone in the lobulate cephalodia of Sphaerophorus stereocauloides, a New Zealand lichen, and the only species of that genus in which cephalodia are developed; and Hue[460] records Gloeocapsa as forming internal cephalodia in two species of Aspicilia. Bornet[464] found Lyngbya associated with Scytonema in the cephalodia of Stereocaulon ramulosum, and, in the same lichen, Forssell[465] found, in the several cephalodia of one specimen, Nostoc, Scytonema, and Lyngbya, while, in those of another, Scytonema and Stigonema were present. In the latter instance these algae were living free on the podetium. Forssell[465] also determined two different algae, Gloeocapsa magma and Chroococcus turgidus, present in a cephalodium on Lecidea panaeola var. elegans.

As a general rule only one kind of alga enters into the formation of the cephalodia of any species or genus. A form of Nostoc, for instance, is invariably the gonidial constituent of these bodies in the genera, Lobaria, Sticta, etc. In other lichens different blue-green algae, as noted above, may occupy the cephalodia even on the same specimen. Forssell finds alternative algae occurring in the cephalodia of:

Lecanora gelida and Lecidea illita contain either Stigonema or Nostoc;

Lecidea panaeola, with Gloeocapsa, Stigonema or Chroococcus;

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Lecidea pelobotrya, with Stigonema or Nostoc;

Pilophorus robustus, with Gloeocapsa, Stigonema, or Nostoc.

Fig. 77. Lecanora gelida Ach. a, lobate cephalodia × 12 (after Zopf).

Riddle[466] has employed cephalodia with their enclosed algae as diagnostic characters in the genus Stereocaulon. When the alga is Stigonema, as in S. paschale, etc., the cephalodia are generally very conspicuous, grey in colour, spherical, wrinkled or folded, though sometimes black and fibrillose (S. denudatum). Those containing Nostoc are, on the contrary, minute and are coloured verdigris-green (S. tomentosum and S. alpinum).

Instances are recorded of algal colonies adhering to, and even penetrating, the thallus of lichens, but as they never enter into relationship with the lichen hyphae, they are antagonistic rather than symbiotic and have no relation to cephalodia.

D. Development of Cephalodia

a. Ectotrophic. Among the most familiar examples of external cephalodia are the small rather dark-coloured warts or swellings that are scattered irregularly over the surface of Peltigera (Peltidea) aphthosa. This lichen has a grey foliose thallus of rather large sparingly divided lobes; it spreads about a hand-breadth or more over the surface of the ground in moist upland localities. The specific name “aphthosa” was given by Linnaeus to[138] the plant on account of the supposed resemblance of the dotted thallus to the infantile ailment of “thrush.” Babikoff[467] has published an account of the formation and development of these Peltidea cephalodia. He determined the algae contained in them to be Nostoc by isolating and growing them on moist sterilized soil. He observed that the smaller, and presumably younger, excrescences were near the edges of the lobes. The cortical cells in that position grow out into fine septate hairs that are really the ends of growing hyphae. Among the hairs were scattered minute colonies of Nostoc cells lying loose or so closely adhering to the hairs as to be undetachable (Fig. 78 A). In older stages the hairs, evidently stimulated by contact with the Nostoc, had increased in size and sent out branches, some of which penetrated the gelatinous algal colony; others, spreading over its surface, gradually formed a cortex continuous with that of the thallus. The alga also increased, and the structure assumed a rounded or lentiform shape. The thalline cortex immediately below broke down, and the underlying gonidial zone almost wholly died off and became absorbed. The hyphae of the cephalodium had meanwhile penetrated downwards as root-like filaments, those of the thallus growing upwards into the new overlying tissue (Fig. 78 B). The foreign alga has been described as parasitic, as it draws from the lichen hyphae the necessary inorganic food material; but it might equally well be considered as a captive pressed into the service of the lichen to aid in the work of assimilation or as a willing associate giving and receiving mutual benefit.

Fig. 78 A. Hairs of Peltigera aphthosa Willd. associated with Nostoc colony much magnified (after Babikoff).

Fig. 78 B. Peltigera aphthosa Willd. Vertical section of thallus and cephalodium × 480 (after Babikoff).

Th. M. Fries[468] had previously described the development of the cephalodia in Stereocaulon but failed to find the earliest stages. He concluded from his observations that parasitic algae were common in the cortical layer of the lichens, but only rarely formed the “monstrous growths” called cephalodia.

b. Endotrophic. Winter[469] examined the later stages of internal cephalodine formation in a species of Sticta. The alga, probably a species of Rivularia, which gives origin to the cephalodia, may be situated immediately below the upper cortex, in the medullary layer close to the gonidial zone, or between the pith and the under cortex. The protuberance caused by the increasing tissue, which also contains the invading alga, arises accordingly either on the upper or the lower surface. In some cases it was found that the normal gonidial layer had been pushed up by the protruding cephalodium[139] and lay like a cap over the top. The cephalodia described by Winter are endogenous in origin, though the mature body finally emerges from the interior and becomes either epigenous or hypogenous. Schneider[470] has followed the development of a somewhat similar endotrophic or endogenous type in Sticta oregana due also to the presence of a species of Rivularia. How the alga attained its position in the medulla of the thallus was not observed.

Fig. 79. Nephroma expallidum Nyl. Vertical section of thallus. a, endotrophic cephalodium × 100 (after Forssell).

Both the algal cells of internal cephalodia and the hyphae in contact with them increase vigorously, and the newly formed tissue curving upwards or downwards appears on the outside as a swelling or nodule varying in size from that of a pin-head to a pea. On the upper surface the gonidial zone partly encroaches on the nodule, but the foreign alga remains in the centre of the structure well separated from the thalline gonidia by a layer of hyphae. The group is internally divided into small nests of dark-green algae surrounded by strands of hyphae (Fig. 79). The swellings, when they[140] occur on the lower surface of the lichen, correspond to those of the upper in general structure, but there is no intermixture of thalline gonidia. That Nostoc cells can grow and retain the power to form chlorophyll in adverse conditions was proved by Etard and Bouilhac[471] who made a culture of the alga on artificial media in the dark, when there was formed a green pigment of chlorophyll nature.

Endotrophic cephalodia occur in many groups of lichens. Hue[472] states that he found them in twelve species of Aspicilia. As packets of blue-green algae they are a constant feature in the thallus of Solorinae. The species of that genus grow on mossy soil in damp places, and must come frequently in contact with Nostoc colonies. In Solorina crocea an interrupted band of blue-green algae lies below the normal gonidial zone and sometimes replaces it—a connecting structure between cephalodia and a true gonidial zone.

c. Pseudocephalodia. Under this section have been classified those cephalodia that are almost independent of the lichen thallus though to some extent organically connected with it, as for instance that of Lecidea panaeola which originate on the hypothallus of the lichen and maintain their position between the crustaceous granules.

The cephalodia of Lecanora gelida, as described by Sernander[473], might also be included here. He watched their development in their native habitat, an exposed rock-surface which was richly covered with the lichen in all stages of growth. Two kinds of thallus, the one containing blue-green algae (Chroococcus), the other bright-green, were observed on the rock in close proximity. At the point of contact, growth ceased, but the thallus with bright-green algae, being the more vigorous, was able to spread round and underneath the other and so gradually to transform it to a superficial flat cephalodium. All such thalli encountered by the dominant lichen were successively surrounded in the same way. The cephalodium, growing more slowly, sent root-like hyphae into the tissue of the underlying lichen, and the two organisms thus became organically connected. Sernander considers that the two algae are antagonistic to each other, but that the hyphae can combine with either.

The pseudocephalodia of Usnea species are abortive apothecia; they are surrounded at the base by the gonidial zone and cortex of the thallus, and they contain no foreign gonidia.

E. Autosymbiotic Cephalodia

Bitter[474] has thus designated small scales, like miniature thalli, that develop constantly on the upper cortex of Peltigera lepidophora, a small lichen not uncommon in Finland, and first recorded by Wainio as a variety of Peltigera[141] canina. The alga contained in the scales is a blue-green Nostoc similar to the gonidia of the thallus. Bitter[475] described the development as similar to that of the cephalodia of Peltigera aphthosa, but the outgrowths, being lobate in form, are less firmly attached and thus easily become separated and dispersed; as the gonidia are identical with those of the parent thallus they act as vegetative organs of reproduction.

Bitter’s work has been criticized by Linkola[476] who claims to have discovered by means of very thin microtome sections that there is a genetic connection between the scales and the underlying thallus, not only with the hyphae, as in true cephalodia, but with the algae as well, so that these outgrowths should be regarded as isidia.

In the earliest stages, according to Linkola, a small group of algae may be observed in the cortical tissue of the Peltigera apart from the gonidial zone and near the upper surface. Gradually a protruding head is formed which is at first covered over with a brown cortical layer one cell thick. The head increases and becomes more lobate in form, being attached to the thallus at the base by a very narrow neck and more loosely at other parts of the scale. In older scales, the gonidia are entirely separated from those of the thallus, and a dark-brown cortex several cells in thickness covers over the top and sides; there is a colourless layer of plectenchyma beneath. At this advanced stage the scales are almost completely superficial and correspond with the cephaloidal rather than with the isidial type of formation. The algae even in the very early stages are distinct from the gonidial zone and the whole development, if isidial, must be considered as somewhat abnormal.

3. SOREDIA

A. Structure and Origin of Soredia

Soredia are minute separable parts of the lichen thallus, and are composed of one or more gonidia which are clasped and surrounded by the lichen hyphae (Fig. 80). They occur on the surface or margins of the thallus of a fairly large number of lichens either in a powdery excrescence or in a pustule-like body comprehensively termed a “soralium” (Fig. 81). The soralia vary in form and dimensions according to the species. Each individual soredium is capable of developing into a new plant; it is a form of vegetative reproduction characteristic of lichens.

Fig. 80. Soredia. a, of Physcia pulverulenta Nyl.; b, of Ramalina farinacea Ach. × 600.

Acharius[477] gave the name “soredia” to the powdery bodies with reference to their propagating function; he also interpreted the soredium as an “apothecium of the second order.” But long before his time they had been[142] observed and commented on by succeeding botanists: first by Malpighi[478] who judged them to be seeds, he having seen them develop new plants; by Micheli[479] who however distinguished between the true fruit and those seeds; and by Linnaeus[480] who considered them to be the female organs of the plant, the apothecia being, as he then thought, the male organs. Hedwig[481], on the other hand, regarded the apothecia as the seed receptacles and the soredia as male bodies. Sprengel’s[482] statement that they were “a subtile germinating powder mixed with delicate hair-like threads which take the place of seeds” established finally their true function. Wallroth[483], who was the first really to investigate their structure and their relation to the parent plant, recognized them as of the same type as the “brood-cells” or gonidia; and as the latter, he found, could become free from the thallus and form a green layer on trees, walls, etc., in shady situations, so the soredia also could become free, though for a time they remained attached to the lichen and were covered by a veil, i.e. by the surrounding hyphal filaments. Koerber[484] also gave much careful study to soredia, their nature and function. As propagating organs he found they were of more importance than spores, especially in the larger lichens.

Fig. 81. Vertical section of young soralium of Evernia furfuracea var. soralifera Bitter × 60 (after Bitter).

According to Schwendener[485], the formation of soredia is due to increased and almost abnormal activity of division in the gonidial cell; the hyphal filament attached to it also becomes active and sends out branches from the cell immediately below the point of contact which force their way between the newly divided gonidia and finally surround them. A soredial “head”[143] of smaller or larger size is thus gradually built up on the stalk filament or filaments, and is ultimately detached by the breaking down of the slender support.

a. Scattered Soredia. The simplest example of soredial formation may be seen on the bark of trees or on palings when the green coating of algal cells is gradually assuming a greyish hue caused by the invasion of hyphal lichenoid growth. This condition is generally referred to as “leprose” and has even been classified as a distinct genus, Lepra or Lepraria. Somewhat similar soredial growth is also associated with many species of Cladonia, the turfy soil in the neighbourhood of the upright podetia being often powdered with white granules. Such soredia are especially abundant in that genus, so much so, that Meyer[486], Krabbe[487] and others have maintained that the spores take little part in the propagation of species. The under side of the primary thallus, but more frequently the upright podetia, are often covered with a coating of soredia, either finely furfuraceous, or of larger growth and coarsely granular, the size of the soredia depending on the number of gonidia enclosed in each “head.”

Soredia are only occasionally present on the apothecial margins: the rather swollen rims in Lobaria scrobiculata are sometimes powdery-grey, and Bitter[488] has observed soredia, or rather soralia, on the apothecial margins of Parmelia vittata; they are very rare, however, and are probably to be explained by excess of moisture in the surroundings.

b. Isidial Soredia. In a few lichens soredia arise by the breaking down of the cortex at the tips of the thalline outgrowths termed “isidia.” In Parmelia verruculifera, for instance, where the coralloid isidia grow in closely packed groups or warts, the upper part of the isidium frequently becomes soredial. In that lichen the younger parts of the upper cortex bear hairs or trichomes, and the individual soredia are also adorned with hairs. The somewhat short warted isidia of P. subaurifera may become entirely sorediose, and in P. farinacea the whole thallus is covered with isidia transformed into soralia. The transformation is constant and is a distinct specific character. Bitter[488] considers that it proves that no sharp distinction exists between isidia and soralia, at least in their initial stages.

Fig. 82. Usnea barbata Web. Longitudinal section of filament and base of “soredial” branch × 40 (after Schwendener).

c. Soredia as Buds. Schwendener[489] has described soredia in the[144] genus Usnea which give rise to new branches. Many of the species in that genus are plentifully sprinkled with the white powdery bodies. A short way back from the apex of the filament the separate soredia show a tendency to apical growth and might be regarded as groups of young plants still attached to the parent branch. One of these developing more quickly pushes the others aside and by continued growth fills up the soredial opening in the cortex with a plug of tissue; finally it forms a complete lateral branch. Schwendener calls them “soredial” branches (Fig. 82) to distinguish them from the others formed in the course of the normal development.

B. Soralia

In lichens of foliose and fruticose structure, and in a few crustaceous forms, the soredia are massed together into the compact bodies called soralia, and thus are confined to certain areas of the plant surface. The simpler soralia arise from the gonidial zone below the cortex by the active division of some of the algal cells. The hyphae, interlaced with the green cells, are thin-walled and are, as stated by Wainio[490], still in a meristematic condition; they are thus able readily to branch and to form new filaments which clasp the continually multiplying gonidia. This growth is in an upward or outward direction away from the medulla, and strong mechanical pressure is exerted by the increasing tissue on the overlying cortical layers. Finally the soredia force their way through to the surface at definite points. The cortex is thrown back and forms a margin round the soralium, though shreds of epidermal tissue remain for a time mixed with the powdery granules.

a. Form and Occurrence of Soralia. The term “soralium” was first applied only to the highly developed soredial structures considered by Acharius to be secondary apothecia; it is now employed for any circumscribed group of soredia.[491] The soralia vary in size and form and in position, according to the species on which they occur; these characters are constant enough to be of considerable diagnostic value. Within the single genus Parmelia, they are to be found as small round dots sprinkled over the surface of P. dubia; as elongate furrows irregularly placed on P. sulcata; as pearly excrescences at or near the margins of P. perlata, and as swollen tubercles at the tips of the lobes of P. physodes (Fig. 83). Their development is strongly influenced and furthered by shade and moisture, and, given such conditions in excess, they may coalesce and cover large patches of the thallus with a powdery coating, though only in those species that would have borne soredia in fairly normal conditions.

Soralia of definite form are of rather rare occurrence in crustaceous lichens,[145] with the exception of the Pertusariaceae, where they are frequent, and some species of Lecanora and Placodium. They are known in only two hypophloeodal (subcortical) lichens, Arthonia pruinosa and Xylographa spilomatica. Among squamulose thalli they are typical of some Cladoniae, and also of Lecidea (Psora) ostreata, where they are produced on the upper surface towards the apex of the squamule.

Fig. 83. Parmelia physodes Ach. Thallus growing horizontally; soredia on the ends of the lobes (S. H., Photo.).

b. Position of soraliferous Lobes. According to observations made by Bitter[492], the occurrence of soralia on one lobe or another may depend to a considerable extent on the orientation of the thallus. He cites the variability in habit of the familiar lichen, Parmelia physodes and its various forms, which grow on trees or on soil. In the horizontal thalli there is much less tendency to soredial formation, and the soredia that arise are generally confined to branching lobes on the older parts of the thallus.

That type of growth is in marked contrast with the thallus obliged to take a vertical direction as on a tree. In such a case the lobes, growing downward from the point of origin, form soralia at their tips at an early stage (Fig. 84). The lateral lobes, and especially those that lie close to the substratum, are the next to become soraliate. Similar observations have been made on the soraliferous lobes of Cetraria pinastri. The cause is probably due to the greater excess of moisture draining downwards to the lower parts of the thallus. The lobes that bear the soralia are generally[146] narrower than the others and are very frequently raised from contact with the substratum. They tend to grow out from the thallus in an upright direction and then to turn backwards at the tip, so that the opening of the soralium is directed downwards. Bitter says that the cause of this change in direction is not clear, though possibly on teleological reasoning it is of advantage that the opening of the soralium should be protected from direct rainfall. The opening lies midway between the upper and lower cortex, and the upper tissue in these capitate soralia continues to grow and to form an arched helmet or hood-covering which serves further to protect the soralium.

Fig. 84. Parmelia physodes Ach. Thallus growing vertically; soredia chiefly on the lobes directed downwards, reduced (M. P., Photo.).

Similar soralia are characteristic of Physcia hispida (Ph. stellaris subsp. tenella), the apical helmet being a specially pronounced feature of that species, though, as Lesdain[493] has pointed out, the hooded structures are primarily the work of insects. In vertical substrata they occur on the lower lobes of the plant.

Apical soralia are rare in fruticose lichens, but in an Alpine variety of[147] Ramalina minuscula they are formed at the tips of the fronds and are protected by an extension of the upper cortical tissues. Another instance occurs in a Ramalina from New Granada referred by Nylander to R. calicaris var. farinacea: it presents a striking example of the helmet tip.

c. Deep-seated Soralia. In the cases already described Schwendener[494] and Nilson[495] held that the algae gave the first impulse to the formation of the soredia; but in the Pertusariaceae[496], a family of crustaceous lichens, there has been evolved a type of endogenous soralium which originates with the medullary hyphae. In these, special hyphae rise from a weft of filaments situated just above the lowest layer of the thallus at the base of the medulla, the weft being distinguished from the surrounding tissue by staining blue with iodine. A loose strand of hyphae staining the usual yellow colour rises from the surface of the “blue” weft and, traversing the medullary tissue, surrounds the gonidia on the under side of the gonidial zone. The hyphae continue to grow upward, pushing aside both the upper gonidial zone and the cortex, and carrying with them the algal cells first encountered. When the summit is reached, there follows a very active growth of both gonidia and hyphae. Each separate soredium so produced consists finally of five to ten algal cells surrounded by hyphae and measures 8 µ to 13 µ in diameter. The cortex forms a well-defined wall or margin round the mass of soredia.

A slightly different development is found in Lecanora tartarea, one of the “crottle” lichens, which has been placed by Darbishire in Pertusariaceae. The hyphae destined to form soredia also start from the weft of tissue at the base of the thallus, but they simply grow through the gonidial zone instead of pushing it aside.

In his examination of Pertusariaceae Darbishire found that the apothecia also originated from a similar deeply seated blue-staining tissue, and he concluded that the soralia represented abortive apothecia and really corresponded to Acharius’s “apothecia of the second order.” His conclusion as to the homology of these two organs is disputed by Bitter[497], who considers that the common point of origin is explained by the equal demand of the hyphae in both cases for special nutrition, and by the need of mechanical support at the base to enable the hyphae to reach the surface and to thrust back the cortex without deviating from their upward course through the tissues.

C. Dispersal and Germination of Soredia

Soredia become free by the breaking down of the hyphal stalks at the septa or otherwise. They are widely dispersed by wind or water and soon make their appearance on any suitable exposed soil. Krabbe[498] has stated[148] that, in many cases, the loosely attached soredia coating some of the Cladonia podetia are of external origin, carried thither by the air-currents. Insects too aid in the work of dissemination: Darbishire[499] has told us how he watched small mites and other insects moving about over the soralia of Pertusaria amara and becoming completely powdered by the white granules.

Darbishire[499] also gives an account of his experiments in the culture of soredia. He sowed them on poplar wood about the beginning of February in suitable conditions of moisture, etc. Long hyphal threads were at once produced from the filaments surrounding the gonidia, and gonidia that had become free were seen to divide repeatedly. Towards the end of August of the same year a few soredia had increased in size to about 450µ in diameter, and were transferred to elm bark. By September they had further increased to a diameter of 520µ, and the gonidia showed a tendency towards aggregation. No further differentiation or growth was noted.

More success attended Tobler’s[500] attempt to cultivate the soredia of Cladonia sp. He sowed them on soil kept suitably moist in a pot and after about nine months he obtained fully formed squamules, at first only an isolated one or two, but later a plentiful crop all over the surface of the soil. Tobler also adds that soredia taken from a Cladonia, that had been kept for about half a year in a dry room, grew when sown on a damp substratum. The algae however had suffered more or less from the prolonged desiccation, and some of them failed to develop.

A suggestion has been made by Bitter[501] that a hybrid plant might result from the intermingling of soredia from the thallus of allied lichens. He proposed the theory to explain the great similarity between plants of Parmelia physodes and P. tubulosa growing in close proximity. There is no proof that such mingling of the fungal elements ever takes place.

D. Evolution of Soredia

Soredia have been compared to the gemmae of the Bryophytes and also to the slips and cuttings of the higher plants. There is a certain analogy between all forms of vegetative reproduction, but soredia are peculiar in that they include two dissimilar organisms. In the lichen kingdom there has been evolved this new form of propagation in order to secure the continuance of the composite life, and, in a number of species, it has almost entirely superseded the somewhat uncertain method of spore germination inherited from the fungal ancestor, but which leaves more or less to chance the encounter with the algal symbiont.

From a phylogenetic point of view we should regard the sorediate lichens as the more highly evolved, and those which have no soredia as phylogenetically[149] young, though, as Lindau[502] has pointed out, soredia are all comparatively recent. They probably did not appear until lichens had reached a more or less advanced stage of development, and, considering the polyphyletic origin of lichens, they must have arisen at more than one point, and probably at first in circumstances where the formation of apothecia was hindered by prolonged conditions of shade and moisture.

That soredia are ontogenetic in character, and not, as Nilson[503] has asserted, accidental products of excessively moist conditions is further proved by the non-sorediate character of those species of crustaceous lichens belonging to Lecanora, Verrucaria, etc. that are frequently immersed in water. Bitter[504] found that the soredia occurring on Peltigera spuria were not formed on the lobes which were more constantly moist, nor at the edges where the cortex was thinnest: they always emerged on young parts of the thallus a short way back from the edge.

Bitter[504] points out that in extremely unfavourable circumstances—in the polluted atmosphere near towns, or in persistent shade—lichens, that would otherwise form a normal thallus, remain in a backward sorediose state. He considers, however, that many of these formless crusts are autonomous growths with specific morphological and chemical peculiarities. They hold these outposts of lichen vegetation and are not found growing in any other localities. The proof would be to transport them to more favourable conditions, and watch development.

4. ISIDIA

A. Form and Structure of Isidia

Many lichens are rough and scabrous on the surface, with minute simple or divided coral-like outgrowths of the same texture as the underlying thallus, though sometimes they are darker in colour as in Evernia furfuracea. They always contain gonidia and are covered by a cortex continuous with that of the thallus.

This very marked condition was considered by Acharius[505] as of generic importance and the genus, Isidium, was established by him, with the diagnostic characters: “branchlets produced on the surface, or coralloid, simple and branched.” In the genus were included the more densely isidioid states of various crustaceous species such as Isidium corallinum and I. Westringii, both of which are varieties of Pertusariae. Fries[506], with his accustomed insight, recognized them as only growth forms. The genus was however still accepted in English Floras[507] as late as 1833, though we find it dropped by Taylor[508] in the Flora Hibernica a few years later.

[150]

The development of the isidial outgrowth has been described by Rosendahl[509] in several species of Parmelia. In one of them, P. papulosa, which has a cortical layer one cell thick, the isidium begins as a small swelling or wart on the upper surface of the thallus. At that stage the cells of the cortex have already lost their normal arrangement and show irregular division. They divide still further, as gonidia and hyphae push their way up. The full-grown isidia in this species are cylindrical or clavate, simple or branched. They are peculiar in that they bear laterally here and there minute rhizoids, a development not recorded in any other isidia. The inner tissue accords with that of the normal thallus and there is a clearly marked cortex, gonidial zone and pith. A somewhat analogous development takes place in the isidia of Parmelia proboscidea; in that lichen they are mostly prolonged into a dark-coloured cilium.

In Parmelia scortea the cortex is several cells thick, and the outermost rows are compressed and dead in the older parts of the thallus; but here also the first appearance of the isidium is in the form of a minute wart. The lower layers (4 to 6) of living cortical cells divide actively; the gonidia also share in the new growth, and the protuberance thus formed pushes off the outer dead cortex and emerges as an isidium (Fig. 85). They are always rather stouter in form than those of P. papulosa and may be simple or branched. The gonidia in this case do not form a definite zone, but are scattered through the pith of the isidium.

Here also should be included the coralloid branching isidia that adorn the upper surface and margins of the thallus of Umbilicaria pustulata. They begin as small tufts of somewhat cylindrical bodies, but they sometimes broaden out to almost leafy expansions with crisp edges. Most frequently they are situated on the bulging pustules where intercalary growth is active. Owing to their continued development on these areas, the tissue becomes slack, and the centre of the isidial tuft may fall out, leaving a hole in the thallus which becomes still more open by the tension of thalline expansion. New isidia sprout from the edges of the wound and the process may again be repeated. It has been asserted that these structures are only formed on injured parts of the thallus—something like gall-formations—but Bitter[510] has proved that the wound is first occasioned by the isidial growth weakening the thallus.

Fig. 85. Vertical section of isidia of Parmelia scortea Ach. A, early stage; B. later stage. × 60 (after Rosendahl).

[151]

B. Origin and Function of Isidia

Nilson[511] (later Kajanus[512]) insists that isidia and soredia are both products of excessive moisture. He argues that lichen species, in the course of their development, have become adapted to a certain degree of humidity, and, if the optimum is passed, the new conditions entail a change in the growth of the plant. The gonidia are stimulated to increased growth, and the mechanical pressure exerted by the multiplying cells either results in the emergence of isidial structures where the cortex is unbroken, or, if the cortex is weaker and easily bursts, in the formation of soralia.

This view can hardly be accepted; isidia as well as soredia are typical of certain species and are produced regularly and normally in ordinary conditions; both of them are often present on the same thallus. It is not denied, however, that their development in certain instances is furthered by increased shade or moisture. In Evernia furfuracea isidia are more freely produced on the older more shaded parts of the thallus. Zopf[513] has described such an instance in Evernia olivetorina (E. furfuracea), which grew in the high Alps on pine trees, and which was much more isidiose when it grew on the outer ends of the branches, where dew, rain or snow had more direct influence. He[514] quotes other examples occurring in forms of E. furfuracea which grew on the branches of pines, larches, etc. in a damp locality in S. Tyrol. The thalli hung in great abundance on each side of the branches, and were invariably more isidiose near the tips, because evidently the water or snow trickled down and was retained longer there than at the base.

Bitter[515] has given a striking instance of shade influence in Umbilicaria. He found that some boulders on which the lichen grew freely had become covered over with fallen pine needles. The result was at first an enormous increase of the coralline isidia, though finally the lichen was killed by the want of light.

Isidia are primarily of service to the plant in increasing the assimilating surface. Occasionally they grow out into new thallus lobes. The more slender are easily rubbed off, and, when scattered, become efficient organs of propagation. This view of their function is emphasized by Bitter who points out that both in Evernia furfuracea and in Umbilicaria pustulata other organs of reproduction are rare or absent. Zopf[513] found new plants of Evernia furfuracea beginning to grow on the trunk of a tree lower down than an old isidiose specimen. They had developed from isidia which had been detached and washed down by rain.

[152]

VI. HYMENOLICHENS

A. Supposed Affinity with other Plants

Lichens in which the fungal elements belong to the Hymenomycetes are confined to three tropical genera. They are associated with blue-green algae and are most nearly related to the Thelephoraceae among fungi. The spores are borne, as in that family, on basidia.

Fig. 86. Cora Pavonia Fr. (after Mattirolo).

The best known Hymenolichen, Cora Pavonia (Fig. 86), was discovered by Swartz[516] during his travels in the W. Indies (1785-87) growing on trees in the mountains of Jamaica, and the new plant was recorded by him as Ulva montana. Gmelin[517] also included it in Ulva in close association with Ulva (Padina) Pavonia, but that classification was shortly after disputed by Woodward[518] who thought its affinity was more nearly with the fungi and suggested that it should be made the type of a new genus near to Boletus (Polystictus) versicolor. Fries[519] in due time made the new genus Cora, though he included it among algae; finally Nylander[520] established the lichenoid character of the thallus and transferred it to the Lecanorei.

It was made the subject of more exact investigation by Mattirolo[521] who[153] recognized its affinity with Thelephora, a genus of Hymenomycetes. Later Johow[522] went to the West Indies and studied the Hymenolichens in their native home. The genera and species described by Johow have been reduced to Cora and Dictyonema; a new genus Corella has since been added by Wainio[523].

Johow found that Cora grew on the mountains usually from 1000 to 2000 ft. above sea-level. As it requires for its development a cool damp climate with strong though indirect illumination, it is found neither in sunny situations nor in the depths of dark woods. It grows most freely in diffuse light, on the lower trunks and branches of trees in open situations, but high up on the stem where the vegetation is more dense. It stands out from the tree like a small thin bracket fungus, one specimen placed above another, with a dimidiate growth similar to that of Polystictus versicolor. Both surfaces are marked by concentric zones which give it an appearance somewhat like Padina Pavonia. These zones indicate unequal intercalary growth both above and below. The whole plant is blue-green when wet, greyish-white when dry, and of a thin membranaceous consistency.

B. Structure of Thallus

There is no proper cortex in any of the genera, but in Cora there is a fastigiate branching of the hyphae in parallel lines towards the upper surface; just at the outside they turn and lie in a horizontal direction, and, as the branching becomes more profuse, a rather compact cover is formed. The gonidia, which consist of blue-green Chroococcus cells, lie at the base of the upward branches and they are surrounded with thin-walled short-celled hyphae closely interwoven into a kind of cellular tissue. The medulla of loose hyphae passes over to the lower cortex, also of more or less loose filaments. The outermost cells of the latter very frequently grow out into short jagged or crenate processes (Fig. 87).

Fig. 87. Cora Pavonia Fr. Vertical section of thallus. a, upper cortex; b, gonidial layer; c, medulla and lower cortex of crenate cells; d, tuft of fertile hyphae. × 160. e, basidia and spores × 1000 (after Johow).

[154]

In Corella, the mature lichen is squamulose or consists of small lobes; in Dictyonema there is a rather flat dimidiate expansion; in both the alga is Scytonema, the trichomes of which largely retain their form and are surrounded by parallel growths of branching hyphae. The whole tissue is loose and spongy.

Corella spreads over soil on a white hypothallus without rhizinae. In the other two genera which live on soil, or more frequently on trees, there is a rather extensive formation of hold-fast tissue. When the dimidiate thallus grows on a rough bark, rhizoidal strands of hyphae travel over it and penetrate between the cracks; if the bark is smooth, there is a more continuous weft of hyphae. In both cases a spongy cushion of filamentous tissue develops at the base of the lichen between the tree and the bracket thallus. There is also in both genera an encrusting form which Johow regarded as representing a distinct genus Laudatea, but which Möller found to be merely a growth stage. Möller[524] judged from that and from other characteristics that the same fungus enters into the composition of both Cora and Dictyonema and that only the algal constituents are different.

C. Sporiferous Tissues

As in Hymenomycetes, the spores of Hymenolichens are exogenous, and are borne at the tips of basidia which in these lichens are produced on the under surface of the thallus. In Cora the fertile filaments may form a continuous series of basidia over the surface, but generally they grow out in separate though crowded tufts. As these tufts broaden outwards, they tend to unite at the free edges, and may finally present a continuous hymenial layer. Each basidium bears four sterigmata and spores (Fig. 87 e); paraphyses exactly similar to the basidia are abundant in the hymenium. In Dictyonema the hymenium is less regular, but otherwise it resembles that of Cora. No hymenium has as yet been observed in Corella; it includes, so far as known, one species, C. brasiliensis, which spreads over soil or rocks.

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CHAPTER IV
REPRODUCTION

1. REPRODUCTION BY ASCOSPORES

A. Historical Survey

The earliest observations as to the propagation of lichens were made by Malpighi[525] who recorded the presence of soredia on the lichen plant and noted their function as reproductive bodies. He was followed after a considerable interval by Tournefort[526] who placed lichens in a class apart owing to the form of the fruit: “This fruit,” he writes, “is a species of bason or cup which seems to take the place of seeds in these kinds of plants.” He figures Ramalina fraxinea and Physcia ciliaris, both well fruited specimens, and he represents the “minute dust” contained in the fruits as subrotund in form. The spores of Physcia ciliaris are of a large size and dark in colour and were undoubtedly seen by Tournefort. Morison[527], in his History of Oxford Plants, published very shortly after, dismissed Tournefort’s “seeds” as being too minute to be of any practical interest.

Micheli[528], with truer scientific insight, made the fruiting organs the subject of special study. He decided that the apothecia were floral receptacles, receptacula florum, and that the spores were the “flowers” of the lichen. He has figured them in a vertical series in situ, in a section of the disc of Solorina saccata[529] and also in a species of Pertusaria[529], in both of which plants the ascospores are unusually large. He adds that he had not so far seen the “semina.”

Micheli’s views were not shared by his immediate successors. Dillenius[530] scarcely believed that the spores could be “flowers” and, in any case, he concluded that they were too minute to be of any real significance in the life of the plant.

Linnaeus[531], and after him Necker[532], Scopoli[533] and others describe the apothecia as the male, the soredia as the female organs of lichens. These old time botanists worked with very low powers of magnification, and easily went astray in the interpretation of imperfectly seen phenomena.

Koelreuter[534], a Professor of Natural History in Carlsruhe, who published a work on The discovered Secret of Cryptogams, next hazarded the opinion that the seeds of lichens originated from the substance of the pith, and that the overlying cortical layer supplied the fertilizing sap. Hoffmann[535][156] devoted a great deal of attention to lichen fructification and he also thought that fertilization must take place within the tissue of the lichens. He regarded the soredia as the true seeds, while allowing that a second series of seeds might be contained in the scutellae (apothecia).

A distinct advance was made by Hedwig[536], a Professor of Botany in Leipzig, towards the end of the eighteenth century. He followed Tournefort in selecting Physcia ciliaris for research, and in that plant he describes and figures not only the apothecia with the dark-coloured septate spores, but also the pycnidia or spermogonia which he regarded as male organs. The soredia, typically represented and figured by him on Parmelia physodes, he judged to be “male flowers of a different type.”

Acharius[537] did not add much to the knowledge of reproduction in lichens, though he takes ample note of the various fruiting structures for which he invented the terms apothecia, perithecia and soredia. Under still another term gongyli he included not only spores, but the spore guttulae as well as the gonidia or cells forming the soredia.

Hornschuch[538] of Greifswald described the propagation of the lower lichens as being solely by means of a germinating “powder”; the more highly organized forms were provided with receptacles or apothecia containing spores which he considered as analogous to flowers rather than to fruits. The important contributions to Lichenology of Wallroth[539] and Meyer[540] close this period of uncertainty: the former deals almost exclusively with the form and character of the vegetative thallus and the function of the “reproductive gonidia.” Meyer, a less prolix writer, very clearly states that the method of reproduction is twofold: by spores produced in fruits, or by the germinating granules of the soredia.

B. Forms of Reproductive Organs

From the time of Tournefort, considerable attention had been given to the various forms of scutellae, tuberculae, etc., as characters of diagnostic importance. Sprengel[541] grouped these bodies finally into nine different types with appropriate names which have now been mostly superseded by the comprehensive terms, apothecia and perithecia. A general classification on the lines of fruit development was established by Luyken[542], who, following Persoon’s[543] classification of fungi, and thus recognizing their affinity, summed up all known lichens as Gymnocarpeae with open fruits, and Angiocarpeae with closed fruits.

a. Apothecia. As in discomycetous fungi, the lichen apothecium is in the form of an open concave or convex disc, but generally of rather small[157] size, rarely more than 1 cm. in diameter (Fig. 88); there is no development in lichen fruits equal to the cup-like ascomata of the larger Pezizae. In most cases the lichen apothecium retains its vitality as a spore-bearing organ for a considerable period, sometimes for several years, and it is strengthened and protected by one or more external margins of sterile tissue. Immediately surrounding the fertile disc there is a compact wall of interwoven hyphae. In some of the shorter-lived soft fruits, as in Biatora, this hyphal margin may be thin, and may gradually be pushed aside as the disc develops and becomes convex, but generally it forms a prominent rim round the disc and may be tough or even horny, and often hard and carbonaceous. This wall, which is present, to some extent, in nearly all lichens, is described as the “proper margin.” A second “thalline margin” containing gonidia is present in many genera[544]: it is a structure peculiar to the lichen apothecium and forms the amphithecium.

Fig. 88. Lecanora subfusca Ach. A, thallus and apothecia × 3; B, vertical section of apothecium. a, hymenium; b, hypothecium; c, thalline margin or amphithecium; d, gonidia. × 60 (after Reinke).

At the base of the apothecium there is a weft of light- or dark-coloured hyphae called the hypothecium, which is continued up and round the sides as the parathecium merging into the “proper margin.” It forms the lining of a cup-shaped hollow which is filled by the paraphyses, which are upright closely packed thread-like hyphae, and by the spore-containing asci or thecae, these together constituting the thecium or hymenium. The paraphyses are very numerous as compared with the asci; they are simple or branched,[158] frequently septate, especially towards the apex, and mostly slender, varying in width from 1-4µ, though Hue describes paraphyses in Aspicilia atroviolacea as 8-12µ thick. They may be thread-like throughout their length, or they may widen towards the tips which are not infrequently coloured. Small apical cells are often abstricted and lie loose on the epithecium, giving at times a pruinose or powdered character to the disc. In some genera there is a profuse branching of the paraphyses to form a dense protective epithecium over the surface of the hymenium as in the genus Arthonia.

The apothecia may be sessile and closely adnate to or even sunk in the thallus, or they may be shortly stalked. The thalline margin shares generally the characters of the thallus; the disc is mostly of a firm consistency and is light or dark in colour according to genus or species; most frequently it is some shade of brown. Marginate apothecia, i.e. those with a thalline margin, are often referred to as “lecanorine,” that being a distinctive feature of the genus Lecanora. In the immarginate series, with a proper margin only, the texture may be soft and waxy, termed “biatorine” as in Biatora; or hard and carbonaceous as in the genus Lecidea, and is then described as “lecideine.”

In the subseries Graphidineae, the apothecium has the form of a very flat, roundish or irregular body entirely without a margin, called an “ardella” as in Arthonia; or more generally it is an elongate narrow “lirella,” in which the disc is a mere slit between two dark-coloured proper margins. The hypothecium of the lirellae is sometimes much reduced and in that case the hymenium rests directly on a thin layer above the thalline tissue as in Graphis elegans (Fig. 89).

Fig. 89. Graphis elegans Ach. A, thallus and lirellae; B, vertical section of furrowed lirella. × ca. 50.

Lichen fruits require abundant light, and plants growing in the shade are mostly sterile. Naturally, therefore, the reproductive bodies are to be found on the best illuminated parts of the thallus. In crustaceous and in most foliose forms, they are variously situated on the upper surface, wherever the light falls most directly. In the genera Nephromium and Nephromopsis, on the contrary, they arise on the under surface, though at the extreme margin, but as the fertile lobes eventually turn upwards the apothecia as they mature become fully exposed. In shrubby or fruticose lichens their position is lateral on the fronds, or more frequently at or near the tips.

b. Perithecia. The small closed perithecium is characteristic of the Pyrenocarpeae which correspond with the Pyrenomycetes among fungi. It[159] is partially or entirely immersed in the thallus or in the substratum on which the lichen grows, and is either a globose or conical body wholly surrounded by a hyphal wall, when it is described as “entire” (Fig. 90), or it is somewhat hemispherical in form and the outer wall is developed only on the upper exposed part: a type of perithecium usually designated by the term “dimidiate.” As the perithecial wall gives sufficient protection to the asci, the paraphyses are of less importance and are frequently very sparingly produced, or they may even be dissolved and used up at an early stage. The thallus of the Pyrenocarpeae is often extremely reduced, and the perithecia are then the only visible portion of the lichen.

A few lichens among Graphidineae and Pyrenocarpeae grow in a united body generally looked on as a stroma; but Wainio[545] has demonstrated that as the fruiting bodies give rise to this structure by agglomeration—by the cohesion of their margins—it can only be regarded as a pseudostroma. Two British genera of Pyrenolichens, Mycoporum and Mycoporellum, exhibit this pseudo-stromatoid formation.

Fig. 90. A, entire perithecium of Porina olivacea A. L. Sm. × ca. 40; B, dimidiate perithecium of Acrocordia gemmata Koerb. × ca. 20.

C. Development of Reproductive Organs

As most known lichens belong to the Ascolichens, the study of development has been concentrated on that group. Tulasne[546] was the first to make a microscopic study of lichen tissues and he described in considerable detail the general anatomical structure of apothecia and perithecia. Later, Fuisting[547] traced the development of a number of perithecia through their different stages of growth, but his most interesting discovery was made in Lecidea fumosa, a crustaceous Discolichen with an areolate thallus in which the apothecia are seated on the fungal hyphae between the areolae. In the very early stages represented by a complex of slender hyphae, he observed an unbranched septate filament with short cuboid cells, richer in contents than the surrounding filaments and somewhat similar to the structure known to mycologists as “Woronin’s hypha,” which is an ascogonial structure. These specialized cells disappeared as the hymenium began to form.

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1. DISCOLICHENS

Fig. 91. Collema microphyllum Ach. Vertical section of thallus. a, carpogonium; b, trichogyne. × 350 (after Stahl).

a. Carpogonia of Gelatinous Lichens. Stahl’s[548] work on various Collemaceae followed on the same lines as that of Fuisting. The first species selected by him for examination, Collema (Leptogium) microphyllum’ is a gelatinous lichen which grows on old trunks of poplars and willows. It has a small olive-green thallus which, in autumn, is crowded with apothecia; the spermogones or pycnidia appear as minute reddish points on the edge of the thallus. Within the thallus, and midway between the upper and lower surface, there arises, as a branch from a vegetative hypha, a many-septate filament coiled in spiral form at the base, with the free end growing upwards and projecting a short distance above the surface and occasionally forked (Fig. 91). The tip-cell is slightly swollen and covered with a mucilaginous coat continuous with the mucilage of the thallus. The whole structure, characterized by the larger size and by the richer contents of its cells, was regarded by Stahl as a carpogonium, the coiled base representing the ascogonium, the upright hypha functioning as the receptive organ or trichogyne, comparable to that of the Florideae. The spermatia, which mature at this early stage of carpogonial development, are expelled from a neighbouring spermogonium on the addition of moisture and easily reach the protruding trichogyne. They adhere to the mucilaginous wall of the end-cell, and, in two or three instances, Stahl found that copulation had taken place. As the affixed spermatium was empty, he concluded that the contents had passed over into the trichogyne, and that the nucleus had travelled down to the ascogonium. Certain degenerative changes that followed seemed to confirm[161] the view that there had been fertilization: the cells of the trichogyne had lost their turgidity and at the same time the cross-walls had swollen considerably and stood out like knots in the hypha (Fig. 92). The ascogonial cells had also increased not only in size but in number by intercalary division, so that the spiral arrangement became obscured. Ascogenous hyphae arose from the ascogonial cells, and asci cut off by a basal septum were finally formed from these hyphae. Lateral branches from below the septum also formed asci.

Fig. 92. Collema microphyllum Ach. Carpogonium and trichogyne after copulation × 500 (after Stahl).

Stahl’s observations were repeated and extended by Borzi[549] on another of the Collemaceae, Collema nigrescens. In that plant the foliaceous thallus is of thin texture and has a distinct cellular cortex. The carpogonia were found at varying depths near to the cortical region; the ascogonium, of two and a half to four spirals, consisted of ten to fifteen cells with very thin walls, the trichogyne of five to ten cells, the terminal cell projecting above the thallus. Borzi also found spermatia fused with the tip-cell.

A further important contribution was made by Baur[550] in his study of Collema crispum[551]. There occur in nature two forms of this lichen, one of them crowded with apothecia and spermogonia, the other with a more luxuriant thallus, but with few apothecia and no spermogonia. On the latter almost sterile form Baur found in spring and again in autumn immense numbers of carpogonia—about one thousand in a medium sized thallus—which nearly all gradually lost the characteristics of reproductive organs, and, anastomising with other hyphae, became part of the vegetative system. In a few cases in which, presumably, a spermatium had fused with a trichogyne, very large apothecia had developed.

As the first-mentioned form was always crowded with apothecia in every stage of development, as well as with carpogonia and spermogonia, it seemed natural to conclude that the difference was entirely due to the presence or absence of spermatia in sufficient numbers to ensure fertilization. The period during which copulation is possible passes very rapidly, though subsequent development is slow, occupying about half-a-year from the time of fertilization to the formation of the first ascus.

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Baur confirmed Stahl’s observations on the various developmental changes. In several instances he found a spermatium fused with the trichogyne, though he could not see continuity between the lumina of the fusing cells. After copulation with the spermatium the trichogyne nucleus, which occupied the lower third of the terminal cell, had disappeared, and the plasma contents had acquired a deeper tint; the other trichogyne cells, which had also lost their nuclei, were partly collapsed owing to the pressure of the surrounding tissue, and openings were plainly visible through some of the swollen septa, especially of the lower cells. In addition the ascogonial cells, all of which were uninucleate, had increased in number by intercalary division. Plasma connections were opened from cell to cell, but only in the primary septa, the later formed cell-membranes being continuous. Ascogenous hyphae had branched out from the ascogonium as a series of uninucleate cell rows from which the asci finally arose.

Baur’s interpretation was that the first cell of the ascogonium reached by the male nucleus after its passage down through the cells of the trichogyne represented the egg-cell, and that, after fusion, the resultant nucleus divided, and a daughter nucleus passed on to the other auxiliary-cells. No male nucleus nor fusion of nuclei was, however, observed by him, and his deductions rest on conjecture.

Krabbe[552] and after him Mäule[553] found in Collema pulposum reproductive organs similar to those described by Stahl, but in a recent paper on an American form of that species a peculiar condition has been described by Freda Bachmann[554]. She[555] found that the spermatia originated, not in spermogonia, but as groups of cells budded off from vegetative hyphae within the tissue of the lichen and occupying the same position as spermogonia, i.e. the region close below the upper surface. The trichogynes, therefore, never emerged into the open, but travelled towards these internal spermatia, and fusion with them was effected. The changes that afterwards took place in the carpogonial cells were similar to those that had been recognized by Stahl and Baur as consequent on fertilization.

Additional cytological details have been published in a subsequent paper[556]: after fusion with the spermatium the terminal cell of the trichogyne collapsed, its nucleus became disintegrated and the cross septa of the lower trichogyne cells became perforated, these perforations being closed again at a later stage by a gelatinous plug. The nuclear history is more doubtful: the disappearance of the nuclei from the spermatium and from the terminal cell of the trichogyne was noted; two nuclei were seen to be present in the penultimate cell, and these the author interpreted as division products of the[163] original cell nucleus. In the same cell, lying close against the lower septum and partly within the opening, there was a mass of chromatin material which might be the male nucleus migrating downwards. The next point of interest was observed in the twelfth cell from the tip in which there were two nuclei, a larger and a smaller, the latter judged to be the male cell, the small size being due to probable division of the spermatium nucleus either before or after leaving the spermatium. It is stated however that the spermatium was always uninucleate. Meanwhile the cells of the ascogonium had increased in size, the perforations of the septa between the cells became more evident, and their nuclei persisted. In one cell at this stage two nuclei were present, one of the two presumably a male nucleus; no fusion of nuclei was observed in the ascogonial cells. Later the cross walls between the cells were seen to have disappeared more completely and migration of nuclei had taken place, so that some of the cells appeared to be empty while others were multinucleate. Considerable multiplication of the nuclei occurred before the ascogenous hyphae were formed: twelve nuclei were observed in a part of the ascogonium which was just beginning to give off a branch. Several branches might arise from one cell, and their cells were either uni- or binucleate, the nuclei being larger than those of the vegetative hyphae. The formation of the asci was not distinctly seen, but young binucleate asci were not uncommon. The fusion of the two nuclei was followed by the enlargement of the ascus and the subsequent nuclear division for spore formation. In the first heterotypic division twelve chromosomes, double the number observed in the vegetative nucleus, were counted on the equatorial plate. In the third division they were reduced to the normal number of six, from which F. Bachmann concludes that a twofold fusion must have taken place—in the ascogonium and again in the ascus.

Spiral or coiled ascogonia were observed by Wainio[557] in the gelatinous crustaceous genus Pyrenopsis, but the trichogynes did not reach the surface. In Lichina[558], a maritime gelatinous lichen where the carpogonia occur in groups, trichogynes have not been demonstrated.

A peculiarity of some gelatinous lichens noted by Stahl[559] and others in species of Physma, and by Forssell[560] in Pyrenopsis and Psorotichia, is the development of carpogonia at the base of, and within the perithecial walls of old spermogonia. No special significance is however attached to this phenomenon, and it is interesting to note that a similar growth was observed by Zukal[561] in a pyrenomycetous fungus, Pleospora collematum, a harmless parasite on Physma compactum and other Collemaceae. The structures invaded were true pycnidia of the fungus as the minute spores were seen to germinate. A “Woronin’s hypha” at the base of several of these pycnidia developed asci which pushed up among the spent sporophores.

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b. Carpogonia of non-gelatinous Lichens. The soft loose tissue of the gelatinous lichens is more favourable for the minute study of apothecial development than the closely interwoven hyphae of non-gelatinous forms, but Borzi[562] had already extended the study to species of Parmelia, Anaptychia, Sticta, Ricasolia and Lecanora, and in all of them he succeeded in establishing the presence of ascogonia and trichogynes. After him a constant succession of students have worked at the problem of reproduction in lichens.

Lindau[563] published results of the examination of a considerable series of lichens. In Anaptychia (Physcia) ciliaris, Physcia stellaris, Ph. pulverulenta, Ramalina fraxinea, Placodium (Lecanora) saxicolum, Lecanora subfusca and Lecidea enteroleuca he demonstrated the presence of ascogonia with trichogynes. In Parmelia tiliacea and in Xanthoria parietina he found ascogonia but failed to see trichogynes. In none of the species examined by him did he observe any fusion between the trichogyne and a spermatium.

In Anaptychia ciliaris he was able to pick out extremely early stages by staining with a solution of chlor-zinc-iodine. Mäule[564] applied the same test to Physcia pulverulenta, but found that to be successful the reaction required some time. Certain cells of the hyphae—mostly terminal cells—in the lower area of the gonidial zone and even occasionally in the pith (according to Lindau) coloured a deep brown, while the ordinary thalline hyphae were tinted yellow. He assumed that these were initial ascogonial cells on account of the richer plasma contents, and also because of the somewhat larger size of the cells. In the same region of the thallus young carpogonia were observed as outgrowths from vegetative hyphae, though the trichogynes had not yet reached the surface.

Fig. 93. Physcia pulverulenta Nyl. Vertical section of thallus and carpogonium before fertilization. a, outer cortex; b, inner cortex; c, gonidial layer; d, medulla. × ca. 540 (after Darbishire).

Fig. 94. Physcia (Anaptychia) ciliaris DC. Vertical section of developing ascogonium. a, paraphyses; b, ascogonial hyphae; c, ascogonial cells. × 800 (after Baur).

At a more advanced stage the carpogonia were seen to be embedded in the gonidial zone and occurred in groups. The cells of the ascogonium, easily recognized by the darker stain, were short and stout, measuring about 6-8µ in length and 4·4µ in width. They were arranged in somewhat indistinct spirals; but the crowding of the groups resulted in a confused intermingling of the various generative filaments. The trichogynes composed of longer narrower cells rose above the hyphae of the cortex; they also stained a deep brown and the projecting cell was always thin-walled. Lindau frequently observed spermatia very[165] firmly attached to the trichogyne cell but without any plasma connection between the two. The changes in the trichogyne described by Stahl and Baur in Collemaceae were not seen in Anaptychia; the peculiar swelling of the septa seems to be a phenomenon confined to gelatinous lichens. During the trichogyne stage in this lichen the vegetative hyphae from the medulla grow up and surround the young carpogonia, and, at the same time, very slender hyphae begin to branch upwards to form the paraphyses. Darbishire’s[565] examination of Physcia pulverulenta demonstrated the presence of the coiled ascogonium and the trichogyne in that species (Fig. 93).

Baur[566] has also given the results of an examination of Anaptychia. He frequently observed copulation between the spermatium and the tip of the trichogyne, but not any passage of nucleus or contents. After copulation the ascogonial cells increased in size and became irregular in form, and open communication was established between them (Fig. 94). There was no increase in their number by intercalary division as in Collema. After producing ascogenous hyphae the cells were seen to have lost their contents and then to have gradually disappeared. The fertile hyphae, which now took a blue colouration with chlor-zinc-iodine, gradually spread out and[166] formed a wide-stretching hymenium. Several carpogonia took part in the formation of one apothecium.

The tissue below the ascogonium meanwhile developed vigorously, forming a weft of encircling hyphae, while the upper branches grew vertically towards the cortex. Gonidia in contact with the developing fruit also increased, and, with the hyphae, formed the exciple or thalline margin. The growth upward of the paraphyses raises the overlying cortex which in Anaptychia is “fibrous”; it gradually dies off and allows the exposure of the disc, though small shreds of dead tissue are frequently left. In species such as those of Xanthoria where the cortex is of vertical cell-rows, the apothecial hyphae simply push their way between the cell-rows and so through to the open.

Baur found the development of the apothecium somewhat similar in the crustaceous corticolous lichen, Lecanora subfusca. After a long period of sterile growth, spermogonia appeared in great abundance, and, a little later, carpogonia in groups of five to ten; the trichogynes emerged very slightly above the cortex; they were now branched. The ascogonia were frequently a confused clump of cells, though sometimes they showed distinct spirals. The surrounding hyphae had taken a vertical direction towards the cortex at a still earlier stage, and the brown tips were visible on the exterior before the trichogynes were formed. The whole growth was extremely slow.

In Physcia stellaris the carpogonia occurred in groups also, though Lindau[567] thinks that, unlike Anaptychia (Physcia) ciliaris, only one is left to form the fruit. Only one, according to Darbishire[568], entered into the apothecium in the allied species, Physcia pulverulenta. In the latter plasma connections were visible from cell to cell of the trichogyne, and, after copulation with the spermatium, the ascogonial cells increased in size—though not in number—and the plasma connections between them became so wide that the ascogonium had the appearance of an almost continuous multinucleate cell or coenogamete[569]. As in gelatinous lichens, each of these cells gave rise to ascogenous hyphae.

c. General Summary. The main features of development described above recur in most of the species that have been examined.

(1) The carpogonia arise in a complex of hyphae situated on the under side of, or immediately below the gonidial zone. Usually they vary in number from five to twenty for each apothecium, though as many as seventy-two have been computed for Icmadophila ericetorum[570], and Wainio[571] describes them as so numerous in Coccocarpia pellita var., that their trichogynes covered some of the young apothecia with a hairy pile perceptible with a hand lens, though at the same time other apothecia on the same specimens were absolutely smooth.

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(2) The trichogynes, when present, travel up through the gonidial and cortical regions of the thallus; Darbishire[572] observes that in Physcia pulverulenta, they may diverge to the side to secure an easier course between the groups of algae. They emerge above the surface to a distance of about 15µ or less; after an interval they collapse and disappear. Their cells, which are longer and narrower than those of the ascogonium, are uninucleate and vary in number according to species or to individual lichens. Baur[573] thought that possibly several trichogynes in succession might arise from one ascogonium.

(3) How many carpogonia share in the development of the apothecium is still a debated question. In Collema only one is functional. Baur[574] was unable to decide if one or more were fertilized in Parmelia acetabulum, and in Usnea Nienburg[575] found that, out of several, one alone survived (Fig. 95). But in Anaptychia ciliaris and in Lecanora subfusca Baur[574] considers it proved that several share in the formation of the apothecium. In this connection it is interesting to note that, according to Harper[576] and others, several ascogonia enter into one Pyronema fruit.

Fig. 95. Usnea barbata Web. Carpogonium with trichogyne × 1100 (after Nienburg).

(4) The ascogonial cells, before and after fertilization, are distinguished from the surrounding hyphae by a reaction to various stains, which is different from that of the vegetative hyphae, and also by the shortness and width of their cells. The whole of the apothecial primordium is generally recognizable by the clear shining appearance of the cells.

(5) The ascogonia do not always form a distinct spiral; frequently they lie in irregular groups. Each cell is uninucleate and may ultimately produce ascogenous hyphae, though in Anaptychia Baur[574] noted that some of the cells failed to develop.

(6) The hyphae from the ascogonial cells spread out in a complex layer at the base of the hymenium, and send up branches which form the asci, either, as in most Ascomycetes, from the penultimate cell of the fertile branch, or from the last cell, as in Sphyridium (Baeomyces rufus)[575] and in Baeomyces roseus. The same variation has been observed in fungi—in a species of Peziza[577], in which it is the end-cell of the branch that becomes the mother-cell of the ascus; but this deviation from the normal is evidently of rare occurrence either in lichens or fungi.

d. Hypothecium and Paraphyses. The hypothecium is the layer of hyphae that subtends the hymenium, and is formed from the complex of[168] hyphae that envelope the first stages of the carpogonia. It is vegetative in origin and distinct from the generative system.

In lichens belonging to the Collemaceae, the paraphyses rise from the branching of the carpogonial stalk-cell immediately below the ascogonium[578], but have no plasma connection with it. They are thus comparable in origin with the paraphyses of many Discomycetes.

In several genera in which the algal constituents are blue-green, such as Stictina, Pannaria, Nephroma, Ricasolia and Peltigera, Sturgis[579] found that reproduction was apogamous and also that asci and paraphyses originated from the same cell-system: a tuft of paraphyses arose from the basal cell of the ascus, or an ascus from the basal cell of a paraphysis. These results are at variance with those of most other workers, but the figures drawn by Sturgis seem to be clear and convincing.

Again in Usnea barbata, as described by Nienburg[580], the ascogonial cells, after the disappearance of the trichogyne, branch profusely not only upwards towards the cortex but also downwards and to each side. The upward branches give rise normally to the asci, the lower branches produce the subhymenium and later the paraphyses, and the two systems are thus genetically connected, though they remain distinct from each other, and asci are never formed from the lower cells.

In most heteromerous lichens, however, the origin of the paraphyses is exclusively vegetative: they arise as branches from the primordial complex that forms the covering hyphae of the ascogonium both above and below. Schwendener[581] had already pointed out the difference in origin between the two constituents of the hymenium in one of his earlier studies on the development of the apothecium, and this view has been repeatedly confirmed by recent workers, except by Wahlberg[582] who has insisted that they rise from the same cells as the asci, a statement disproved by Baur[583]. The paraphyses originate not only from the covering hyphae, but from vegetative cells in close connection with the primordium. In this mode of development, lichens diverge from fungi, but even in these a vegetative origin for the paraphyses has been pointed out in Lachnea scutellata[584] where they branch from the hyphae lying round the ascogonium.

There is no general rule for the order of development. In Lecanora subfusca Baur[583] found that vertical filaments had reached the surface by the time the trichogyne was formed, and their pointed brown tips gave a ready clue to the position of the carpogonia. In Lecidea enteroleuca[585] they show their characteristic form and arrangement before there is any trace of ascus formation. In Solorina[585] they are well formed before the ascogenous hyphae appear. In other lichens such as Placodium saxicolum[586], Peltigera[169] rufescens[587] and P. malacea[587] the two systems—paraphyses and ascogonium—grow simultaneously, though in P. horizontalis the ascogonium has disappeared by the time the paraphyses are formed. In the genus Nephroma, in Physcia stellaris and in Xanthorina parietina the paraphyses are also late in making their appearance.

In most instances, the paraphyses push their way up between the cortical cells which gradually become absorbed, or they may stop short of the surface as in Nephromium tomentosum[587]. The overlying layer of cortical cells in that case dies off gradually and in time disappears. Such an apothecium is said to be “at first veiled.” Later formed paraphyses at the circumference of the apothecium form the parathecium, which is thus continuous with the hypothecium.

e. Variations in apothecial Development. Lichens are among the least stereotyped of plants: instances of variation have been noted in several genera.

aa. Parmeliae. A somewhat complicated course of development has been traced by Baur[588] in Parmelia acetabulum. In that lichen the group of three to six carpogonia do not lie free in the gonidial tissue, but originate nearer the surface (Fig. 96) and are surrounded from the first by a tissue connected with, and resembling the tissue of the cortex. In the several ascogonia, there are more cells and more spirals than in Collema or in Physcia, and all of them are somewhat confusedly intertwined. The trichogynes are composed of three to five cells and project 10 to 15µ above the surface. When further development begins, the ascogonial cells branch out and form a primary darker layer or hypothecium above which extends the subhymenium, a light-coloured band of loosely woven hyphae. Branches from the ascogonial hyphae at a later stage push their way up through this tissue and form above it a second plexus of hyphae—the base of the hymenium. Baur considers this a very advanced type of apothecium; he found it also present in Parmelia saxatilis, though, in that species, the further growth of the first ascogonial layer was more rapid and the secondary plexus and hymenium were formed earlier in the life of the apothecium. He has also stated that a similar development occurs in other genera such as Usnea, though Nienburg’s[589] work scarcely confirms that view.

Fig. 96. Parmelia acetabulum Dub. Vertical section of thallus and carpogonial group × 550 (after Baur).

[170]

In the brown Parmeliae, Rosendahl[590] found the same series of apothecial tissues, but he interprets the course of development somewhat differently: the basal dark layer or hypothecium he found to be of purely vegetative origin; above it extended the lighter-coloured subhymenium; the ascogenous hyphae were present only in the second layer of dark tissue immediately under the hymenium.

In most lichens the primordium of the apothecium arises towards the lower side of the gonidial zone, the hyphae of which retain the meristematic character. In Parmeliae, as was noted by Lindau[591] in P. tiliacea, and by Baur[592] and Rosendahl[590] in other species, the carpogonial groups are formed above the gonidial zone, either immediately below the cortex as in P. glabratula, or in a swelling of the cortex itself as in P. aspidota, in which species the external enlargement is visible by the time the trichogynes reach the surface. In P. glabra, with a development entirely similar to that of P. aspidota, no trichogynes were seen at any stage. The position of the primordium close under the cortex is also a feature of Ramalina fraxinea as described by G. Wolff[593]. The trichogynes in that species are fairly numerous.

A further peculiarity in Parmelia acetabulum attracted Baur’s[592] attention. Carpogonia with trichogynes are extremely numerous in that species as are the spermogonia, the open pores of which are to be found everywhere between the trichogynes, and yet fertilization can occur but rarely, as disintegrating carpogonia are abundant and very few apothecia are formed. Baur makes the suggestion that possibly cross-fertilization may be necessary, or that the spermatia, in this instance, do not fertilize and that development must therefore be apogamous, in which case the small number of fruits formed is due to some unknown cause. Fünfstück[594] thought that degeneration of the carpogonia had not gone so far, but that a few had acquired the power to develop apogamously. In Parmelia saxatilis only a small percentage of carpogonia attain to apothecia, although spermogonia are abundant and in close proximity, but in that species, unlike P. acetabulum, a large number reach the earlier stages of fruit formation; the more vigorous apothecia seem to inhibit the growth of those that lag behind.

bb. Pertusariae. In Pertusaria, the apothecial primordium is situated immediately below the gonidial zone; the cells have a somewhat larger lumen and thinner walls than those of the vegetative hyphae. In the ascogonium there are more cells than in Parmelia acetabulum; the trichogynes are short-lived, and several carpogonia probably enter into the formation of each apothecium; the paraphyses arise from the covering hyphae. So far the course of development presents nothing unusual. The peculiar pertusarian feature as described by Krabbe[595], and after him by Baur[596], does not appear[171] till a later stage. By continual growth in thickness of the overlying thallus, the apothecia gradually become submerged and tend to degenerate; meanwhile, however, a branch from the ascogonial hyphae at the base of the hymenium pushes up along one side and forms a secondary ascogonial cell-plexus over the top of the first-formed disc. A new apothecium thus arises and remains sporiferous until it also comes to lie in too deep a position, when the process is repeated. Sometimes the regenerating hypha travels to the right or left away from the original apothecium, it may be to a distance of 2 mm. or according to Fünfstück even considerably farther. Fünfstück[597] has gathered indeed from his own investigations that such cases of regeneration are by no means rare: ascogenous hyphae, several centimetres long, destined to give rise to new apothecia are not unusual, and their activity can be recognized macroscopically by the linear arrangement of the apothecia in such lichens as Rhizocarpon (petraeum) concentricum (Fig. 97).

Fig. 97. Rhizocarpon petraeum Massal. Concentrically arranged apothecia, reduced (J. Adams, Photo.).

In Variolaria, a genus closely allied to or generally included in Pertusaria, Darbishire[598] has described the primordial tissue as taking rise almost at the base of the crustaceous thallus: strands of delicate hyphae, staining[172] blue with iodine, mount upwards from that region through the medulla and gonidial zone[599]. The ascogonium does not appear till the surface is almost reached.

cc. Graphideae. Several members of the Graphidaceae were studied by G. Wolff[600]: she demonstrated the presence of carpogonia with emerging trichogynes in Graphis elegans, a species which is distinguished by the deeply furrowed margins of the lirellae (Fig. 89). Before the carpogonia appeared it was possible to distinguish the cushion-like primordial tissue of the apothecium in the thallus which is almost wholly immersed in the periderm layers of the bark on which it grows. The trichogynes were very sparingly septate, and a rather large nucleus occupied a position near the tip of the terminal cell. The dark carbonaceous outer wall makes its appearance in this species at an early stage of development along the sides of the lirellae, but never below, as there is always a layer of living cells at the base. After the first-formed hymenium is exhausted, these basal cells develop a new apothecium with a new carbonaceous wall that pushes back the first-formed, leaving a cleft between the old and the new. This regenerating process, somewhat analogous to the formation of new apothecia in Pertusaria, may be repeated in Graphis elegans as many as five times, the traces of the older discs being clearly seen in the channelled margins of the lirellae.

Fig. 98. Cladonia decorticata Spreng. Vertical section of squamule and primordium of podetium. a, developing podetium; b, probably fertile hyphae; c, cortical tissue; d, gonidial cells. 1 × 600 (after Krabbe).

dd. Cladoniae. The chief points of interest in the Cladoniae are the position of the apothecial primordia and the function of the podetium, which are discussed later[601]. Krabbe[602] determined not only the endogenous origin of the podetium but also the appearance of fertile cells in the primordium (Fig. 98). Both frequently take rise where a crack occurs in the cortex of the primary squamule, the cells of the gonidial tissue being especially active at these somewhat exposed places. The fertile hyphae elongate and branch within the stalk of the developing podetium, sometimes very early, or not until there is a pause in growth, when carpogonia are formed. As a rule trichogynes emerge in great numbers[600], generally close to, or rather below, the spermogonia. In Cl. pyxidata[603] the carpogonia are characterized by the large diameter of the cells—three to five times that of the vegetative hyphae. Though most of the trichogynes disappear at an early stage, some of them may persist for a considerable period. As development proceeds, the vegetative hyphae interspersed among the ascogonial cells grow upwards, slender[173] branches push up between them and gradually a compact sheath of paraphyses is built up. The ascogenous hyphae meanwhile spread radially at the base of the paraphyses and the asci begin to form. The apothecia may be further enlarged by intercalary growth, and this vigorous development of vegetative tissue immediately underneath raises the whole fruit structure well above the surface level.

Sättler[604] in his paper on Cladoniae[605] cites as an argument in favour of fertilization the relative positions of carpogonia and spermogonia on the podetia. The carpogonia with their emerging trichogynes being situated rather below the spermogonia. Both organs, he states, have been demonstrated in eleven species; he himself observed them in the primordial podetia of Cladonia botrytes and of Cl. Floerkeana.

2. PYRENOLICHENS

a. Development of the Perithecium. It is to Fuisting[606] that we owe the first account of development in the lichen perithecium. Though he failed to see the earlier stages (in Verrucaria Dufourii), he recognized the primordial complex of hyphae in the gonidial zone of the thallus, from which originated a vertical strand of hyphae destined to form the tubular neck of the perithecium. Growth in the lower part is in abeyance for a time, and it is only after the neck is formed, and the fruiting body is widened by the ingrowth of external hyphae, that the asci begin to branch up from the tissue at the base.

Fig. 99. Dermatocarpon miniatum Th. Fr. Vertical section of thallus and carpogonial group × 600 (after Baur).

b. Formation of Carpogonia. Stahl[607] had indicated that not only in gymnocarpous but also in angiocarpous lichens, it would be found that carpogonia were formed as in Collema. Baur[608] justified this surmise, and demonstrated the presence of ascogonia in groups of three to eight, with trichogynes that reached the surface in Endocarpon (Dermatocarpon) miniatum (Fig. 99). It is one of the few foliaceous Pyrenolichens, and the leathery thallus is attached to the substratum by a central point, thus allowing in the thallus not only peripheral but also intercalary growth, the latter specially active round the point of basal attachment; carpogonia may be found in any region where the tissue is newly formed, and at any season. The upper cortex is composed of short-celled thick-walled[174] hyphae, with branching vertical to the surface, and so closely packed that there is an appearance of plectenchyma; the medullary hyphae are also thick-walled but with longer cells. The carpogonia of this species arise as a branch from the vegetative hyphae and are without special covering hyphae, so frequent a feature in other lichens. The trichogynes bore their way through the compact cortex and rise well above the surface. After they have disappeared—presumably after fertilization—the vegetative hyphae round and between the ascogonia become active and travel upwards slightly converging to a central point. The asci begin to grow out from the ascogenous hyphae of the base before the vertical filaments have quite pierced the cortex.

Pyrenula nitida has also been studied by Baur[609]. It is a very common species on smooth bark, with a thin crustaceous thallus immersed among the outer periderm cells. Unlike most other lichens, it forms carpogonia in spring only, from February to April. A primordial coil of hyphae lies at the base of the gonidial layer, and, before there is any appearance of carpogonia, a thick strand of hyphae is seen to be directed upwards, so that a definite form and direction is given to the perithecium at a very early stage. The ascogonial cells which are differentiated are extremely small, and, like those of all other species examined, are uninucleate. There are five to ten carpogonia in each primordium; the trichogynes grow up through the hyphal strand and emerge 5-10 µ above the surface. After their disappearance, a weft of ascogenous tissue is formed at the base, and, at the same time, the surrounding vegetative tissue takes part in the building up of a plectenchymatous wall of minute dark-coloured cells. Further development is rapid and occupies probably only a few weeks.

In many of the pyrenocarpous lichens—Verrucariae and others—the walls of the paraphyses dissolve in mucilage as the spores become mature, a character associated with spore ejection and dispersal. In some genera and species, as in Pyrenula, they remain intact.

D. Apogamous Reproduction

Though fertilization by an externally produced male nucleus has not been definitely proved there is probability that, in some instances, the fruit may be the product of sexual fusion. There are however a number of genera and species in which the development is apogamous so far as any external copulation is possible and the sporiferous tissue seems to be a purely vegetative product up to the stage of ascus formation.

In Phlyctis agelaea Krabbe[610] found abundant apothecia developing normally and not accompanied by spermogonia; in Phialopsis rubra studied[175] also by him the primordium arises among the cells of the periderm on which the lichen grows, and he failed to find any trace of a sexual act. In his elaborate study of Gloeolichens Forssell[611] established the presence of carpogonia with trichogynes in two species—Pyrenopsis phaeococca and P. impolita, but without any appearance of fertilization; in all the others examined, the origin of the fruit was vegetative. Wainio[612] records a similar observation in a species of Pyrenopsis in which there was formed a spiral ascogonium and a trichogyne, but the latter never reached the surface.

Neubner[613] claimed to have proved a vegetative origin for the asci in the Caliciaceae; but he overlooked the presence of spermogonia and his conclusions are doubtful.

Fünfstück[614] found apogamous development in Peltigera (including Peltidea) and his results have never been disputed. The ascogonial cells are surrounded at an early stage by a weft of vegetative hyphae. No trichogynes are formed and spermogonia are absent or very rare in the genus, though pycnidia with macrospores occur occasionally.

Some recent work by Darbishire[615] on the genus supplies additional details. The apothecial primordium always originated near the growing margin of the thallus, where certain medullary hyphae were seen to swell up and stain more deeply than others. These at first were uninucleate, but the nuclei increased by division as the cells became larger, and in time there was formed a mass of closely interwoven cells full of cytoplasm. “No coiled carpogonia can be made out, but these darkly stained cells form part of a connected system of branching hyphae coming from the medulla further back.” Long unbranched multi-septate hyphae—evidently functionless trichogynes—travelled towards the cortex but gradually died off. Certain of the larger cells—the “ascogonia”—grew out as ascogenous hyphae into which the nuclei passed in pairs and finally gave rise to the asci.

These results tally well with those obtained by M. and Mme Moreau[616], though they make no mention of any trichogyne. They found that the terminal cells of the ascogenous hyphae were transformed into asci, and the two nuclei in these cells fused—the only fusion that took place. In Nephromium, one of the same family, the case for apogamy is not so clear; but Fünfstück found no trichogynes, and though spermogonia were present on the thallus, they were always somewhat imperfectly developed.

Sturgis[617] supplemented these results in his study of other lichens containing blue-green algae. In species of Heppia, Pannaria, Hydrothyria, Stictina and Ricasolia, he failed to find any evidence of fertilization by spermatia.

Solorina, also a member of Peltigeraceae, was added to the list of[176] apogamous genera by Metzger[618] and his work was confirmed and amplified by Baur[619]: certain hyphae of the gonidial zone branch out into larger ascogonial cells which increase by active intercalary growth, by division and by branching, and so gradually give rise to the ascogenous hyphae and finally to the asci. Baur looked on this and other similar formations as instances of degeneration from the normal carpogonial type of development. Moreau[620] (Fernand and Mme) have also examined Solorina with much the same results: the paraphyses rise first from cells that have been produced by the gonidial hyphae; later, ascogenous hyphae are formed and spread horizontally at the base of the paraphyses, finally giving rise at their tips to the asci. Metzger[618] had further discovered that spermogonia were absent and trichogynes undeveloped in two very different crustaceous lichens, Acarospora (Lecanora) glaucocarpa and Verrucaria calciseda, the latter a pyrenocarpous species and, as the name implies, found only on limestone.

Krabbe[621] had noted the absence of any fertilization process in Gyrophora vellea. At a later date, Gyrophora cylindrica was made the subject of exact research by Lindau[622]. In that species the spermogonia (or pycnidia) are situated on the outer edge of the thallus lobes; a few millimetres nearer the centre appear the primordia of the apothecia, at first without any external indication of their presence. The initial coil which arises on the lower side of the gonidial zone consists of thickly wefted hyphae with short cells, slightly thicker than those of the thallus. It was difficult to establish their connection with the underlying medullary hyphae since these very soon change to a brown plectenchyma. From about the middle of the ascogonial coil there rises a bundle of parallel stoutish hyphae which traverse the gonidial zone and the cortex and slightly overtop the surface. They are genetically connected at the base with the more or less spirally coiled hyphae, and are similar to the trichogynes described in other lichens. Lindau did not find that they had any sexual significance, and ascribed to them the mechanical function of terebrators or borers. The correctness of his deductions has been disputed by various workers: Baur[619] looks on these “trichogynes” as the first paraphyses. The reproductive organs in Stereocaulon were examined by G. Wolff[623], and the absence of trichogynes was proved, though spermogonia were not wanting. She also failed to find any evidence of fertilization in Xanthoria parietina, in which lichen the ascogenous hyphae branch out from an ascogonium that does not form a trichogyne.

Rosendahl[624], as already stated, could find no trichogynes in Parmelia glabra. In Parmelia obscurata, on the contrary, Bitter[625] found that carpogonia with trichogynes were abundant and spermogonia very rare. In other species of the subgenus, Hypogymnia, he has pointed out that apothecia are either[177] absent or occur but seldom, while spermogonia are numerous, and he concludes that the spermatia must function as spores or conidia. Baur[626] however does not accept that conclusion; he suggests as probable that the male organs persist longer in a functionless condition than do the apothecia.

Still more recently Nienburg[627] has described the ascogonium of Baeomyces sp. and also of Sphyridium byssoides (Baeomyces rufus) as reduced and probably degenerate. His results do not disprove those obtained by Krabbe[628] on the same lichen (Sphyridium fungiforme). The apothecia are terminal on short stalks in that species. When the stalk is about ·5mm. in height, sections through the tip show numerous primordia (12 to 15) ranged below the outer cortex, though only one, or at most three, develop further. These ascogonial groups are connected with each other by delicate filaments, and Nienburg concluded that they were secondary products from a primary group lower down in the tissue. Spirals were occasionally seen in what he considered to be the secondary ascogonia, but usually the fertile cells lie in loose uncoiled masses; isolated hyphae were observed to travel upwards from these cells, but they never emerged above the surface.

Usnea macrocarpa—if Schulte’s[629] work may be accepted—is also apogamous, though in Usnea barbata Nienburg[627] found trichogynes (Fig. 95) and the various developments that are taken as evidence of fertilization. Wainio[630] had demonstrated emergent straight trichogynes in Usnea laevis but without any sign of fertilization.

E. Discussion of Lichen Reproduction

In Ascolichens fertilization by the fusion of nuclei in the ascogonium is still a debated question. The female organ or carpogonium, as outlined above, comprises a twisted or spirally coiled multi-septate hypha, with a terminal branch regarded as a trichogyne which is also multi-septate, and through which the nucleus of the spermatium must travel to reach the female cell. It is instructive to compare the lichen carpogonium with that of other plants.

a. The Trichogyne. In the Florideae, or red seaweeds, in which the trichogyne was first described, that organ is merely a hair-like prolongation of the egg-cell and acts as a receptive tube. It contains granular protoplasm but no nucleus and terminates in a shiny tip covered with mucilage. The spermatium, unlike that of lichens, is a naked cell, and being non-motile is conveyed by water to the tip of the trichogyne to which it adheres; the intervening wall then breaks down and the male nucleus passes over. After this process of fertilization a plug of mucilage cuts off the trichogyne, and it withers away.

[178]

In Coleochaete, a genus of small freshwater green algae, a trichogyne is also present in some of the species: it is again a prolongation of an oogonial cell.

In the Ascomycetes, certain cells or cell-processes associated with the ascogonium have been described as trichogynes or receptive cells. In one of the simpler types, Monascus[631], the “trichogyne” is a cell cut off from the ascogonial cell. When fertilization takes place, the wall between the two cells breaks down to allow the passage of the male nucleus, but closes up when the process is effected. In Pyronema confluens[632] it is represented by a process from the ascogonial cell which fuses directly with the male cell. A more elaborate “trichogyne” has been evolved in Lachnea stercorea[633], another Discomycete: in that fungus it takes the form of a 3-5-septate hypha with a longer terminal cell; it rises from some part of the ascogonial cell but has no connection with any process of fertilization, so that the greater elaboration of form is in this case concomitant with loss of function.

In the Laboulbeniaceae, a numerous and very peculiar series of Ascomycetes that live on insects, there are, in nearly all of the reproductive bodies, a carpogonial cell, a trichophoric cell and a trichogyne. The last-named organ is in some genera a simple continuous cell, in others it is septate and branched, occasionally it is absent[634]. The male cells are spermatia of two kinds, exogenous or endogenous, and the plants are monoecious or dioecious. Laboulbeniaceae have no connection with lichens. Faull[635], a recent worker on the group, states that though he observed spermatia attached to the trichogynes, he was not able to demonstrate copulation (possibly owing to over-staining), nor could he trace any migration of the nucleus through the trichophoric cell down to the carpogonial cell. In two species of Laboulbenia that he examined there were no antheridia, and the egg-cell acquired its second nucleus from the neighbouring trichophoric cell. These conjugate nuclei divided simultaneously and the two daughter nuclei passed on to the ascus and fused, as in other Ascomycetes, to form the definitive nucleus.

Convincing evidence as to the importance of the trichogyne in fungi was supposed, until lately, to be afforded by the presence and functional activity of that organ associated with spermogonia in a few Pyrenomycetes—in Poronia, Gnomonia and Polystigma. Poronia was examined by M. Dawson[636] who found that a trichogyne-like filament distinct from the vegetative hyphae rose from the neighbourhood of the ascogonial cells. It took an upward course towards the exterior, but there was no indication that it was ever receptive. In Gnomonia erythrostoma and in Polystigma rubrum spermogonia with spermatia—presumably male organs—are produced in abundance shortly before the ascosporous fruit is developed. The spermatia in both cases exhibit[179] the characters of male cells, i.e. very little cytoplasm and a comparatively large nucleus that occupies most of the cell cavity, along with complete incapacity to germinate. Brooks[637] found in Gnomonia that tufts of the so-called trichogynes originated near the ascogonial cells, but they were “mere continuations of ordinary vegetative hyphae belonging to the coil.” They are septate and reach the surface, and the tip-cell is longer than the others as in the lichen trichogyne.

A somewhat similar arrangement is present in Polystigma, in which Blackman and Welsford[638] have proved that the filaments, considered as trichogynes by previous workers, are merely vegetative hyphae. A trichogyne-like structure is also present in Capnodium, one of the more primitive Pyrenomycetes, but it has no sexual significance.

Lindau[639] in his paper on Gyrophora suggested that the trichogyne in lichens acted as a “terebrator” or boring apparatus, of service to the deeply immersed carpogonium in enabling it to reach the surface. Van Tieghem[640] explained its presence on physiological grounds as necessary for respiration, a view also favoured by Zukal[641], while Wainio[642] and Steiner[643] see in it only an “end-hypha,” the vigorous growth of which is due to its connection with the well-nourished cells of the ascogonium.

Lindau’s view has been rejected by succeeding writers: as has been already stated, it is the paraphyses that usually open the way outward for the apothecium. Van Tieghem’s theory has been considered more worthy of attention and both Dawson and Brooks incline to think that the projecting filaments described above may perform some service in respiration, even though primarily they may have functioned as sexual receptive organs.

There is very little support to be drawn from fungi for the theory that the presence of a trichogyne necessarily entails fertilization by spermatia. Lichens in this connection must be judged as a class apart.

It has perhaps been too lightly assumed that the trichogyne in lichens indicates some relationship with the Florideae[644]. Such a view might be possible if we could regard lichens and Florideae as derived from some common remote ancestor, though even then the difference in spore production—in one case exogenous, and in the other in asci and therefore endogenous—would be a strong argument against their affinity. But all the evidence goes to prove that lichens are late derivatives of fungi and have originated from them at different points. Fungi are interposed between lichens and any other ancestors, and inherited characters must have been transmitted through them. F. Bachmann’s suggestion[645] that Collema pulposum should be regarded “as a link between aquatic red algae and terrestrial ascomycetes such as Pyronema and the mildews” cannot therefore be accepted. It seems more[180] probable that the lichen trichogyne is a new structure evolved in response to some physiological requirement—either sexual or metabolic—of the deeply embedded fruit primordium.

b. The Ascogonium. In fungi there is usually one cell forming the ascogonium, a coenogamete, which after fertilization produces ascogenous hyphae. There are exceptions, such as Cutting[646] found in Ascophanus carneus, in which it is composed of several cells in open contact by the formation of wide secondary pores in the cell-walls. In lichens the ascogonium is divided into a varying number of uninucleate cells. Darbishire[647] (in Physcia) and Baur[648] (in Anaptychia) have described an opening between the different cells, after presumed fertilization, that might perhaps constitute a coenogamete. Ascogenous hyphae arise from all, or nearly all the cells, whether fertilized by spermatia or not, and asci continue to be formed over a long period of time. There may even be regeneration of the entire fruiting body as described in Graphis elegans and in Pertusaria, apparently without renewed fertilization.

Spermogonia (or pycnidia) and the ascosporous fruits generally grow on the same thallus, though not unfrequently only one of the two kinds is present. As the spermogonia appear first, while the apothecia or perithecia are still in the initial stages, that sequence of development seems to add support to the view that their function is primarily sexual; but it is equally valid as a proof of their pycnidial nature since the corresponding bodies in fungi precede the more perfect ascosporous fruits in the life-cycle.

The differences in fertility between the two kinds of thallus in Collema crispum may be recalled[649]. Baur considered that development of the carpogonia was dependant on the presence of spermatia: a strong argument for the necessity of fertilization by these. The conditions in Parmelia acetabulum, also recorded by Baur, lend themselves less easily to any conclusion. On the thallus of that species the spermogonia and carpogonia present are out of all proportion to the very few apothecia that are ultimately formed. Though Baur suggested that cross-fertilization might be necessary, he admits that the development may be vegetative and so uninfluenced by the presence or absence of spermatia.

It is the very frequent occurrence of the trichogyne as an integral part of the carpogonium that constitutes the strongest argument for fertilization by spermatia. There is a possibility that such an organ may have been universal at one time both in fungi and in lichens, and that it has mostly degenerated through loss of function in the former, as it has disappeared in many instances in lichens. Again, there is but a scanty and vestigial record of spermogonia in Ascomycetes. They may have died out, or they may have developed into the asexual pycnidia which are associated with so many species. If we take that view we may trace the same tendency in lichens, as[181] for instance in the capacity of various spermatia to germinate, though in lichen spermogonia there has been apparently less change from the more primitive condition. It is also possible that some process of nuclear fusion, or more probably of conjugation, takes place in the ascogonial cells, and that in the latter case the only fusion, as in some (or most) fungi, is between the two nuclei in the ascus.

If it be conceded that fully developed carpogonia with emergent trichogynes, accompanied by spermogonia and spermatia, represent fertilization, or the probability of fertilization, then the process may be assumed to take place in a fairly large and widely distributed series of lichens. Copulation between the spermatium and the trichogyne has been seen by Stahl[650], Baur[651] and by F. Bachmann[652] in Collema. In Physcia pulverulenta Darbishire[653] could not prove copulation in the earlier stages, but he found what he took to be the remains of emptied spermatia adhering to the tips of old trichogynes. Changes in the trichogyne following on presumed copulation have been demonstrated by several workers in the Collemaceae, and open communication as a result of fertilization between the cells of the ascogonium has been described in two species. This coenocytic condition of the ascogonium (or archicarp), considered by Darbishire and others as an evidence of fertilization, has been demonstrated by Fitzpatrick[654] in the fungus Rhizina undulata. The walls between the cells of the archicarp in that Ascomycete became more or less open, so that the ascogenous hyphae growing from the central cells were able easily to draw nutrition from the whole coenocyte, but no process of fertilization in Rhizina preceded the breaking down of the septa and no fusion of nuclei was observed until the stage of ascus formation.

The real distinction between fertile and vegetative hyphae lies, according to Harper[655], in the relative size of the nuclei. F. Bachmann speaks of one large nucleus in the spermatium of Collema pulposum which would indicate sexual function. There is however very little nuclear history of lichens known at any stage until the beginning of ascus formation, when fusion of two nuclei certainly take place as in fungi to form the definitive nucleus of the ascus.

The whole matter may be summed up in Fünfstück’s[656] statement that: “though research has proved as very probable that fertilization takes place, it is an undoubted fact that no one has observed any such process.”

F. Final Stages of Apothecial Development

The emergence of the lichen apothecium from the thallus, and the form it takes, are of special interest, as, though it is essentially fungal in structure, it is subject to various modifications entailed by symbiosis.

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a. Open or closed Apothecia. Schwendener[657] drew attention to two types of apothecia directly influenced by the thallus: those that are closed at first and only open gradually, and those which are, as he says, open from the first. The former occur in genera and species in which the thallus has a stoutish cortex, as, for instance, in Lobaria where the young fructification has all the appearance of an opening perithecium. The open apothecia (primitus aperta) are found in non-corticate lichens, in which case the pioneer paraphyses arrive at the surface easily and without any converging growth. Similar apothecia are borne directly on the hypothallus at the periphery, or between the thalline areolae, and they are also characteristic of thin or slender thalli as in Coenogonium.

In both types of apothecium, the paraphyses pierce the cortex (Fig. 100) and secure the emergence of the developing ascomata.

Fig. 100. Physcia ciliaris DC. Vertical section of apothecium still covered by the cortex. a, paraphyses; b, hypothecium; c, gonidia of thallus and amphithecium. × 150 (after Baur).

b. Emergence of the Ascocarp. Hue[658] has taken up this subject in recent years and has described the process by which the vegetative hyphae surrounding the fruit primordium, excited to active growth by contact with the generative system, take part in the later stages of fruit formation. The primordium generally occupies a position near to, or just within, the upper medulla, and the hyphae in contact with it soon begin to branch freely in a vertical direction, surrounding the developing fruit and carrying it upwards generally to a superficial position. The different methods of the final emergence give two very distinct types of mature apothecium: the lecideine in which the gonidial zone takes no part in the upward growth, and the lecanorine into which the gonidia enter as an integral part.

In the lecideine series (Fig. 101) the encircling hyphae from the upper medulla rise as a compact column through the gonidial zone to the surface of the thallus; they then spread radially before curving up to form the outer[183] wall or “proper margin” round the spore-bearing disc. The branching of the hyphae is fastigiate with compact shorter branches at the exterior. In such an apothecium gonidia are absent both below the hypothecium and in the margins.

Fig. 101. Lecidea parasema Ach. Vertical section of thallus and apothecium with proper margin only × ca. 50.

In lecanorine development the ascending hyphae from the medulla, in some cases, carry with them algal cells which multiply and spread as a second gonidial layer under the hypothecium (Fig. 102). These hyphae may also spread in a radial direction while still within the thallus and give rise to an “immersed” apothecium which is lecanorine as it encloses gonidia within its special tissues, for example, in Acarospora and Solorina. But in most cases the lecanorine fruit is superficial and not unfrequently it is raised on a short stalk (Usnea, etc.); both the primary gonidial zone of the thallus and the outer cortex are associated with the medullary column of hyphae from the first and grow up along with it, thus providing the outer part of the apothecium, an additional “thalline margin” continuous with the thallus itself. It is an advanced type of development peculiar to lichens, and it provides for fertility of long continuance which is in striking contrast with the fugitive ascocarps of the Discomycetes.

Fig. 102. Lecanora tartarea Ach. Vertical section of apothecium. a, hymenium; b, proper margin or parathecium; c, thalline margin or amphithecium. × 30 (after Reinke).

The distinction between lecideine and lecanorine apothecia is of great value in classification, but it is not always easily demonstrable; it is occasionally necessary to examine the early stages, as in the more advanced the thalline margin may be pushed aside by the turgid disc and become practically obliterated.

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The “proper margin” reaches its highest development in the lecideine and graphideine types. It is less prominent or often almost entirely replaced when the thalline margin is superadded, except in genera such as Thelotrema and Diploschistes which have distinct “double margins.”

There is an unusual type of apothecium in the genus Gyrophora. The fruit is lecideine, the thalline gonidia taking no part in the development. The growth of the initial ascogenous tissue, according to Lindau[659], is constantly towards the periphery of the disc so that a weak spot arises in the centre which is promptly filled by a vigorous sterile growth of paraphyses. This process is repeated from new centres again and again, resulting in the irregularly concentric lines of sterile and fertile areas of the “gyrose” fruit (Fig. 103). The paraphyses soon become black at the tips. Asci are not formed until the ascogenous layer has acquired a certain degree of stability, and spores are accordingly present only in advanced stages of growth.

Fig. 103. Apothecial gyrose discs of Gyrophora cylindrica Ach. × 12 (after Lindau).

G. Lichen Asci and Spores

a. Historical. The presence of spores, as such, in the lichen fruit was first established by Hedwig[660] in Anaptychia (Physcia) ciliaris. He rightly judged the minute bodies to be the “semina” of the plant. In that species they are fairly large, measuring about 50µ, long and 24µ thick, and as they are very dark in colour when mature, they stand out conspicuously from the surrounding colourless tissue of the hymenium. Acharius[661] also took note of these “semina” and happily replaced the term by that of “spores.” They may be produced, he states, in a compact nucleus (Sphaerophoron), in a naked disc (Calicium), or they may be embedded in the disc (Opegrapha and Lecidea). Sprengel[662] opined that the spores—which he figures—were true seeds, though he allows that there had been no record of their development into new plants. Luyken[663] made a further contribution to the subject by dividing lichens into gymnocarpous and angiocarpous forms, according as the spores, enclosed in cells or vesicles (thecae), were borne in an open disc or in a closed perithecium.

In his Systema of lichen genera Eschweiler[664], some years later, described and figured the spores as “thecae” enclosed in cylindrical asci. Fée[665] in contemporary works gave special prominence to the colour and form of the spores in all the lichens dealt with.

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b. Development of the Ascus. The first attempt to trace the origin and development of lichen asci and spores was made by Mohl[666]. He describes the mother-cell (the ascus) as filled at first with a clouded granular substance changing later into a definite number—usually eight—of simple or septate spores. Dangeard[667] included the lichens Borrera (Physcia) ciliaris and Endocarpon (Dermatocarpon) miniatam among the plants that he studied for ascus and spore development. He found that in lichens, as in fungi, the ascus arose usually from the penultimate cell of a crooked hypha (Fig. 104) and that it contained at first two nuclei derived from adjoining cells. These nuclei are similar in size to those of the vegetative hyphae, and in each there is a large nucleolus with chromatin material massed on one side. Fusion takes place, as in fungi, between the two nuclei, and the secondary or definitive nucleus thus formed divides successively to form the eight spore-nuclei. Baur[668] and Nienburg[669] have confirmed Dangeard’s results as regards lichens, and René Maire[670] has also contributed important cytological details on the development of the spores. In Anaptychia (Physcia) ciliaris he found that the fused nucleus became larger and that a synapsis stage supervened during which the long slender chromatin filaments became paired, and at the same time shorter and thicker. The nuclear membrane disappeared as the chromatin filaments were united in masses joined together by linin threads which also disappeared later. At the most advanced stage observed by Maire there was visible a nucleolus embedded in a condensed plasma and surrounded by eight medianly constricted filaments destined to form the equatorial plate. A few isolated observations were also made on the cytology of the ascus in Peltigera canina, in which lichen the preceding ascogonial development is wholly vegetative. The secondary nucleus was seen to contain a chromatin mass and a large nucleolus; in addition two angular bodies of uncertain signification were associated with the nucleolus, each with a central vacuole. The nucleolus disappeared in the prophase of the first division and four double chromosomes were then plainly visible. The succeeding phases of the first and the second nuclear division were not seen, but in the prophase of the third it was possible to distinguish four chromatin masses outside the nucleolus. The slow growth of the lichen plant renders continuous observation extremely difficult.

Fig. 104. Developing asci of Physcia ciliaris DC. × 800 (after Baur).

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F. Bachmann[671] was able to make important cytological observations in her study of Collema pulposum. As regards the vegetative and ascogonial nuclei, five or perhaps six chromosomes appeared on the spindle when the nucleus divided. In the asci, the usual paired nuclei were present in the early stages and did not fuse until the ascus had elongated considerably. After fusion the definitive nucleus enlarged with the growth of the ascus and did not divide until the ascus had attained full size. The nucleolus was large, and usually excentric, and there were at first a number of chromatin masses on an irregular spirem. In synapsis the spirem was drawn into a compact mass, but after synapsis, “the chromatin is again in the form of a knotty spirem.” In late prophases the chromosomes, small ovoid bodies, were scattered on the spindle; later they were aggregated in the centre, and, in the early metaphase, about twelve were counted now split longitudinally. There were thus twice as many chromosomes in the first division in the ascus as in nuclear divisions of the vegetative hyphae. F. Bachmann failed to see the second division; there were at least five chromosomes in the third division.

Considerable importance is given to the number of the chromosomes in the successive divisions in the ascus since they are considered to be proof of a previous double fusion—in the ascogonium and again in the ascus—necessitating, therefore, a double reduction division to arrive at the gametophytic or vegetative number of five or six chromosomes in the third division in the ascus. There have been too few observations to draw any general conclusions.

c. Development of Spores. The spore wall begins to form, as in Ascomycetes, at the apex of the nucleus with the curving over of the astral threads, the nucleus at that stage presenting the figure of a flask the neck of which is occupied by the centrosome. The final spore-nucleus, as observed by Maire, divides once again in Anaptychia and division is followed by the formation of a median septum, the mature spore being two-celled. In Peltigera the spore is at first ovoid, but both nucleus and spore gradually elongate. The fully formed spore is narrowly fusiform and by repeated nuclear division and subsequent cross-septation it becomes 4- or even 5-6-celled.

The spores of lichens are wholly fungoid, and, in many cases, form a parallel series with the spores of the Ascomycetes. Markings of the epispore, such as reticulations, spines, etc., are rarely present (Solorina spongiosa), though thickening of the wall occurs in many species (Pertusariae, etc.), a peculiarity which was first pointed out by Mohl[672] who contrasted the spore walls with the delicate membranes of other lichen cells. Some spores, described as “halonate,” have an outer gelatinous covering which probably prevents the spore from drying up and thus prolongs the period of possible germination. Both asci and spores are, as a rule, more sparingly produced[187] than in fungi; in many instances some or all of the spores in the ascus are imperfectly formed, and the full complement is frequently lacking, possibly owing to some occurrence of adverse conditions during the long slow development of the apothecium. In the larger number of genera and species the spores are small bodies, but in some, as for instance in the Pertusariae and in some Pyrenocarpeae, they exceed in size all known fungus spores. In Varicellaria microsticta, a rare crustaceous lichen of high mountains, the solitary 1-septate spore measures up to 350 µ, in length and 115 µ in width. Most spores contain reserve material in the form of fat, etc., many are dark-coloured; Zukal[673] has suggested that the colour may be protective.

Their ejection from the ascus at maturity is caused by the twofold pressure of the paraphyses and the marginal hyphae on the addition of moisture. The spores may be shot up at least 1 cm. from the disc[674].

d. Spore Germination. Meyer[675] was the first who cultivated lichen spores and the dendritic formation which he obtained by growing them on a smooth surface was undoubtedly the prothallus (or hypothallus) of the lichen. Actual germination was however not observed till Holle[676] in 1846 watched and figured the process as it occurs in Physcia ciliaris.

Spores divided by transverse septa into two or more cells, as well as those that have become “muriform” by transverse and longitudinal septation, may germinate from each cell.

Fig. 105. Multinucleate spore of Lecidea (Mycoblastus) sanguinaria Ach. × 540 (after Zopf).

Fig. 106. Germination of multinucleate spore of Ochrolechia pallescens Koerb. × 390 (after de Bary).

e. Multinucleate Spores. These spores, which are all very large, occur in several genera or subgenera: in Lecidea subg. Mycoblastus (Fig. 105), Lecanora subg. Ochrolechia and in Pertusariaceae. Tulasne[677] in his experiments with germinating spores found that in Lecanora parella (Ochrolechia pallescens?) germinating tubes were produced all over the surface of the spore (Fig. 106). De Bary[678] verified his observations in that and other species and added considerable detail: about twenty-four hours after sowing spores of Ochrolechia pallescens, numerous little warts arose on the surface of the[188] spore which gradually grew out into delicate hyphae. All these spores contain fat globules and finely granular protoplasm with a very large number of minute nuclei; the presence of the latter has been demonstrated by Haberlandt[679] and later by Zopf[680] who reckoned about 200 to 300 in the spore of Mycoblastus sanguinarius. These nuclei had continued to multiply during the ripening of the spore while it was still contained in the ascus[680]. Owing to the presence of the large fat globules the plasma is confined to an external layer close to the spore wall; the nuclei are embedded in the plasma and are connected by strands of protoplasm. The epispore in some of these large spores is extremely developed: in some Pertusariae it measures 4-5 µ in thickness.

f. Polaribilocular Spores. The most peculiar of all lichen spores are those termed polaribilocular—signifying a two-celled spore of which the median septum has become so thickened that the cell-cavities with their contents are relegated to the two poles of the spore, an open canal frequently connecting the two cell-spaces (Fig. 107). Other terms have been suggested and used by various writers to describe this unusual character such as blasteniospore[681], orculiform[682] and placodiomorph[683] or more simply polarilocular.

The polarilocular colourless spore is found in a connected series of lichens—crustaceous, foliose and fruticose (Placodium, Xanthoria, Teloschistes). In another series with a darker thallus (Rinodina and Physcia) the spore is brown-coloured, and the median septum cuts across the plasma-connection. In other respects the brown spore is similar to the colourless one and possesses a thickened wall with reduced cell-cavities.

Fig. 107. Polarilocular spores. a, Xanthoria parietina Th. Fr.; b, Rinodina roboris Th. Fr.; c, Physcia pulverulenta Nyl.; d, Physcia ciliaris DC. × 600.

The method of cell-division in these spores resembles that known as “cleavage by constriction,” in which the cross wall arises by an ingrowth from all sides of the cell; in time the centre is reached and the wall is complete, or an open pore is left between the divided cells. Cell “cleavage” occurs frequently among Thallophytes, though it is unknown among the higher plants. Among Algae it is the normal form of cell-division in Cladophora and also in Spirogyra, though in the latter the wall passes right across and cuts through the connecting plasma threads. Harper[684] found “cleavage by constriction” in two instances among fungi: the conidia of Erysiphe and the gametes of Sporodinia are cut off by a septum which originates as a circular ingrowth of the outer wall, comparable, he considers, with the cell-division of Cladophora.

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The development of the thickened wall of polarilocular spores has been studied by Hue[685], who contends however that there is no true septation in the colourless spores so long as the central canal remains open. According to his observations the wall of the young spore is formed of a thin tegument, everywhere equal in thickness, and consisting of concentric layers. This tegument becomes continually thicker at the equator of the spore by the addition of new layers from the interior, and the protoplasmic contents are compressed into a gradually diminishing space. In the end the wall almost touches at the centre, and the spore consists of two polar cell-cavities with a narrow open passage between. A median line pierced by the canal is frequently seen. In a few species there is a second constriction cleavage and the spore becomes quadrilocular.

Hue insists that this spore should be regarded as only one-celled; for though the walls may touch at the centre, he says they never coalesce. He has unfortunately given no cytological observations as to whether the spore is uni- or binucleate.

In Xanthoria parietina, one of the species with characteristic polaribilocular spores, germination, it would seem, takes place mostly at one end only of the spore, though a germinating tube issues at both ends frequently enough to suggest that the spore is binucleate and two-celled. The absence of germination from one or other of the cells only may probably be due to the drain on their small resources. Hue has cited the rarity of such instances of double germination in support of his view of the one-celled nature of the spore. He instances that out of fifteen spores, Tulasne[686] has figured only three that have germinated at each end; Bornet[687] figures one in seven with the double germination and Bonnier[688] one in sixteen spores.

Further evidence is wanted as to the nuclear history of these hyaline spores. In the case of the brown spores, which show the same thickening of the wall and restricted cell-cavity, though with a distinct median septum, nuclear division was observed by René Maire[689] before septation in one such species, Anaptychia ciliaris.

II. SECONDARY SPORES

A. Reproduction by Oidia

In certain conditions of nutrition, fungal hyphae break up into separate cells, each of which functions as a reproductive conidium or oidium, which on germination forms new hyphae. Neubner[690] has demonstrated a similar process in the hyphae of the Caliciaceae and compares it with the oidial formation described by Brefeld[691] in the Basidiomycetes.

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The thallus of this family of lichens is granular or furfuraceous; it never goes beyond the Lepra stage of development[692]. In some species it is scanty, in others it is abundant and spreads over large areas of the trunks of old trees. It is only when growth is especially luxuriant that oidia are formed. Neubner was able to recognize the oidial condition by the more opaque appearance of the granules, and under the microscope he observed the hyphae surrounding the gonidia gradually fall away and break up into minute cylindrical cells somewhat like spermatia in size and form. There was no question of abnormal or unhealthy conditions, as the oidia were formed in a freely fruiting thallus.

The gonidia associated with the oidial hyphae also showed unusual vitality and active division took place as they were set free by the breaking up of the encircling hyphae. The germination of the oidia provides an abundance of hyphal filaments for the rapidly increasing algal cells, and there follows a wide-spread development of the lichen thallus.

Oidial formation has not been observed in any other family of lichens.

B. Reproduction by Conidia

a. Instances of Conidial Formation. It is remarkable that the type of asexual reproduction so abundantly represented in fungi by the large and varied group of the Hyphomycetes is practically absent in lichens. An exception is to be found in a minute gelatinous lichen that grows on soil. It was discovered by Bornet[693] and called by him Arnoldia (Physma) minutula. From the thallus rise up simple or sparingly branched colourless conidiophores which bear at the tips globose brown conidia (Fig. 108). Bornet[694] obtained these conidia by keeping very thin sections of the thallus in a drop of water[693].

Fig. 108. Conidia developed from thallus of Arnoldia minutula Born. × 950 (after Bornet).

Yet another instance of conidial growth is given by Steiner[695]. He had observed that the apothecia on plants of Caloplaca aurantia var. callopisma Stein. differed from those of normal appearance in the warted unevenness of the disc and also in being more swollen and convex, the thalline margin being almost obliterated. He found, on microscopical examination, that the hymenium was occupied by paraphyses and by occasional asci, the latter seldom containing spores, and being[191] usually more or less collapsed. The component parts of the apothecium were entirely normal and healthy, but the paraphyses and the few asci were crushed aside by the intrusion of numerous slender unbranched septate conidiophores. Several of these might spring from one base and the hypha from which they originated could be traced some distance into the ascogenous layer, though a connection with that cell-system could not be demonstrated. While still embedded in the hymenium, an ellipsoid or obovate swelling began to form at the apex of the conidiophore; it became separated from the stalk by a septum and later divided into a two-celled conidium. The conidiophore increased in length by intercalary growth and finally emerged above the disc; the mature conidium was pyriform and measured 15-20 µ × 9-11 µ.

Steiner regarded these conidia as entirely abnormal; pycnidia with stylospores are unknown in the genus and they were not, he alleges, the product of any parasitic growth.

b. Comparison With Hyphomycetes. The conidial form of fructification in fungi, known as a Hyphomycete, is generally a stage in the life-cycle of some Ascomycete; it represents the rapid summer form of asexual reproduction. The ascospore of the resting fruit-form in many species germinates on any suitable matrix and may at once produce conidiophores and conidia, which in turn germinate, and either continue the conidial generation or proceed to the formation of the perfect fruiting form with asci and ascospores.

Such a form of transient reproduction is almost impossible in lichens, as the hypha produced by the germinating lichen ascospore has little vitality without the algal symbiont. In natural conditions development practically ceases in the absence of symbiosis. When union between the symbionts takes place, and growth becomes active, thallus construction at once commences. But in certain conditions of shade and moisture, only the rudiments of a lichen thallus are formed, known as a leprose or sorediose condition. Soredia also arise in the normal life of many lichens. As the individual granules or soredia may each give rise to a complete lichen plant, they may well be considered as replacing the lost conidial fructification.

C. Campylidium and Orthidium

Müller[696] has described under the name Campylidium a supposed new type of asexual fructification which he found on the thallus of tropical species of Gyalecta, Lopadium, etc., and which he considered analogous to pycnidia and spermogonia. Wainio[697] has however recognized the cup-like structure as a fungus, Cyphella aeruginascens Karst., which grows on the bark of trees and occasionally is parasitic on the crustaceous thallus of lichens. Wainio has[192] also identified the plant, Lecidea irregularis, first described by Fée[698], as also synonymous with the fungus.

Another name Orthidium was proposed by Müller[699] for a type of fructification he found in Brazil which he contrasts or associates with Campylidium. It has an open marginate disc with sporophores bearing acrogenous spores. He found it growing in connection with a thin lichen thallus on leaves and considered it to be a form of lichen reproduction. Possibly Orthidium is also a Cyphella.

III. SPERMOGONIA OR PYCNIDIA

A. Historical Account of Spermogonia

The name spermogonium was given by Tulasne[700] to the “punctiform conceptacles” that are so plentifully produced on many lichen thalli, on the assumption that they were the male organs of the plant, and that the spore-like bodies borne in them were non-motile male cells or spermatia.

The first record of their association with lichens was made by Dillenius[701], who indicates the presence of black tubercles on the thallus of Physcia ciliaris. He figures them also on several species of Cladonia, on Ramalina and on Dermatocarpon, but without any suggestion as to their function. Hedwig’s[702] study of the reproductive organs of the Linnaean Cryptogams included lichens. He examined Physcia ciliaris, a species that not only is quite common but is generally found in a fruiting condition and with very prominent spermogonia, and has been therefore a favourite lichen for purposes of examination and study. Hedwig describes and figures not only the apothecia but also those other bodies which he designates as “punctula mascula,” or again as “puncta floris masculi.” In his later work he gives a drawing of Lichen (Gyrophora) proboscideus, with two of the spermogonia in section.

Acharius[703] included them among the lichen structures which he called “cephalodia”: he described them as very minute tubercles rising up from the substance of the thallus and projecting somewhat above it. He also figures a section through two “cephalodia” of Physcia ciliaris. Fries[704] looked on them as being mostly “anamorphoses of apothecia, the presence of abortive fruits transforming the angiocarpous lichen to the appearance of a gymnocarpous form.” Wallroth[705] assigned the small black fruits to the comprehensive fungus genus Sphaeria or classified lichens bearing spermogonia only as distinct genera and species (Pyrenothea and Thrombium). Later students of lichens—Schaerer[706], Flotow[707], and others—accepted Wallroth’s interpretation of their relation to the thallus, or they ignored them altogether in their descriptions of species.

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B. Spermogonia as Male Organs

Interest in these minute “tubercles” and their enclosed “corpuscles” was revived by Itzigsohn[708] who examined them with an improved microscope. He macerated in water during a few days that part of the thallus on which they were developed, and, at the end of the time, discovered that the solution contained large numbers of motile bodies which he naturally took to be the corpuscles from the broken down tubercles. He claimed to have established their function as male motile cells or spermatozoa. The discovery seemed not only to prove their sexual nature, but to link up the reproduction of lichens with that of the higher cryptogams. The tubercles in which the “spermatozoa” were produced he designated as antheridia. More prolonged maceration of the tissue to the very verge of decay yielded still larger numbers of the “spermatozoa” which we now recognize to have been motile bacilli.

Tulasne[709] next took up the subject, and failing to find the motile cells, he wrongly insisted that Itzigsohn had been misled by mere Brownian movement, but at the same time he accepted the theory that the minute conceptacles were spermogonia or male organs of lichens. He also pointed out that their constant occurrence on the thallus of practically every species of lichen, and their definite form, though with considerable variation, rendered it impossible to regard them as accidental or of no importance to the life of the plant. He compared them with fungal pycnidia such as Phyllosticta or Septoria which outwardly they resembled, but whereas the pycnidial spores germinated freely, the spermatia of the spermogonia, as far as his experience went, were incapable of germination.

C. Occurrence and Distribution

a. Relation to Thallus and Apothecia. We owe to Tulasne[710] the first comparative study of lichen spermogonia. He described not only their outward form, but their minute structure, in a considerable number of representative species. A few years later Lindsay[711] published a memoir dealing with the spermogonia of the larger foliose and fruticose lichens, and, in a second paper, he embodied the results of his study of an equally extensive selection of crustaceous species. Lindsay’s work is unfortunately somewhat damaged by faulty determination of the lichens he examined, and by lack of the necessary discrimination between one thallus and another of associated and intermingled species. Both memoirs contain, however, much valuable information as to the forms of spermogonia, with their spermatiophores and spermatia, and as to their distribution over the lichen thallus.

Though spermogonia are mostly found associated with apothecia, yet [194]in some lichens, such as Cerania (Thamnolia) vermicularis, they are the only sporiferous organs known. Not unfrequently crustaceous thalli bear spermogonia only, and in some Cladoniae, more especially in ascyphous species, spermogonia are produced abundantly at the tips of the podetial branches (Fig. 109), while apothecia are exceedingly rare. Usually they occur in scattered or crowded groups, more rarely they are solitary. Very often they are developed and the contents dispersed before the apothecia reach the surface of the thallus; hence the difficulty in relating these organisms, since the mature apothecium is mostly of extreme importance in determining the species.

Fig. 109. Cladonia furcata Schrad. Branched podetium with spermogonia at the tips (after Krabbe).

Fig. 110. Physcia hispida Tuckerm. Ciliate frond. a, spermogonia; b, apothecia. × ca. 5 (after Lindsay).

In a very large number of lichens, both crustaceous and foliose, the spermogonia are scattered over the entire thallus (Fig. 110), covering it more or less thickly with minute black dots, as in Parmelia conspersa. In other instances, they are to some extent confined to the peripheral areas as in Parmelia physodes; or they occur on the extreme edge of the thallus as in the crustaceous species Lecanora glaucoma (sordida). In Pyrenula nitida they grow on the marginal hypothallus, usually on the dark line of demarcation between two thalli.

They tend to congregate on, and indeed are practically restricted to the[195] better lighted portions of the thallus. On the fronds of foliose forms, they appear, for instance, on the swollen pustules of Umbilicaria pustulata, while in Lobaria pulmonaria, they are mostly lodged in the ridges that surround the depressions in the thallus. In Parmelia conspersa, Urceolaria (Diploschistes) scruposa and some others, they occasionally invade the margins of the apothecium or even the apothecial disc as in Lichina. Forssell[712] found that a spermogonium had developed among cells of Gloeocapsa that covered the disc of a spent apothecium of Pyrenopsis haematopis.

In fruticose lichens such as Usnea, Ramalina, etc. they occur near the apex of the fronds, and in Cladonia they occupy the tips of the ascyphous podetia or the margins of the scyphi. In some Cladoniae, however, spermogonia are produced on the basal squamules, more rarely on the squamules that clothe the podetia.

b. Form and Size. Spermogonia are specifically constant in form, the same type being found on the same lichen species all over the globe. The larger number are entirely immersed and are ovoid or roundish (Fig. 111 A) or occasionally somewhat flattened bodies (Nephromium laevigatum), or again, but more rarely, they are irregular in outline with an infolding of the walls that gives the interior a chambered form (Fig. 111 B) (Lichina pygmaea); but all of these are only visible as minute points on the thallus.

Fig. 111. Immersed spermogonia. A, globose in Parmelia acetabulum Dub. × 600; B, with infolded walls in Lecidea (Psora) testacea Ach. × 144 (after Glück).

A second series, also immersed, are borne in small protuberances of the thallus. These very prominent forms are rarely found in crustaceous lichens, but they are characteristic of such well-known species as Ramalina fraxinea, Xanthoria parietina, Ricasolia amplissima, Baeomyces roseus, etc. Other spermogonia project slightly above the level of the thallus, as in Cladonia papillaria and Lecidea lurida; while in a few instances they are practically free, these last strikingly exemplified in Cetraria islandica where they occupy the small projections or cilia (Fig. 112) that fringe the margins of the lobes; they are free also in most species of Cladonia.

[196]

In size they vary from such minute bodies as those in Parmelia exasperata which measure 25-35 µ in diam., up to nearly 1 mm. in Lobaria laetevirens. As a rule, they range from about 150 µ to 400 µ across the widest part, and are generally rather longer than broad. They open above by a small slit or pore called the ostiole about 20 µ to 100 µ wide which is frequently dark in colour. In one instance, in Icmadophila aeruginosa, Nienburg[713] has described a spermogonium with a wide opening, the spermatiophores being massed in palisade formation along the bottom of a cup-like structure.

c. Colour of Spermogonia. Though usually the ostiole is visible as a darker point than the surrounding tissue, spermogonia are often difficult to locate unless the thallus is first wetted, when they become visible to slight magnification. They appear as black points in many Parmeliae, Physciae, Roccellae, etc., though even in these cases they are often brown when moistened. They are distinctly brown in some Cladoniae, in Nephromium, and in some Physciae; orange-red or yellow in Placodium and concolorous with the thallus in Usnea, Ramalina, Stereocaulon, etc.