Cambridge Botanical Handbooks

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

LICHENS

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LICHENS

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

CAMBRIDGE:
AT THE UNIVERSITY PRESS
1921

PRINTED IN GREAT BRITAIN

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

CONTENTS

GLOSSARY

Acrogenous, borne at the tips of hyphae; [see spermatium], [312].

Allelositismus, Norman’s term to describe the thallus of Moriolaceae (mutualism), [313].

Amorphous cortex, formed of indistinct hyphae with thickened walls; [cf. decomposed cortex].

Amphithecium, thalline margin of the apothecium, [157].

Antagonistic symbiosis, hurtful parasitism of one lichen on another, [261 et seq.]

Apothecium, open or disc-shaped fructification, [11], [156] et passim. Veiled apothecium, [169]. Closed or open at first, [182].

Archilichens, lichens in which the gonidia are bright green (Chlorophyceae), [52], [55] et passim.

Ardella, the small spot-like apothecium of Arthoniaceae, [158].

Areola (areolate), small space marked out by lines or chinks on the surface of the thallus, [73] et passim.

Arthrosterigma, septate tissue-like sterigma (spermatiophore), [197].

Ascogonium, the cell or cells that produce ascogenous hyphae, [180 et seq.]

Ascolichens, lichens in which the fungus is an Ascomycete, [159], [173] et passim.

Ascus, enlarged cell in which a definite number of spores (usually 8) are developed; [cf. theca], [157], [184].

Ascyphous, podetia without scyphi, [119] et passim.

Biatorine, apothecia that are soft or waxy, and often brightly coloured, as in Biatora, [158].

Blasteniospore, [see polarilocular spore].

Byssoid, slender, thread-like, as in the old genus Byssus.

Campylidium, supposed new type of fructification in lichens, [191].

Capitulum, the globose apical apothecium of Coniocarpineae; [cf. mazaedium], [319].

Carpogonium, primordial stage of fructification, [160], [164] et passim.

Cephalodium, irregular outgrowth from the thallus enclosing mostly blue-green algae; or intruded packet of algae within the thallus, [11], [133] et passim.

Chrondroid, hard and tough like cartilage, a term applied to strengthening strands of hyphae, [104], [114].

Chroolepoid, like the genus Chroolepis (Trentepohlia).

Chrysogonidia, yellow algal cells (Trentepohlia).

Cilium, hair-like outgrowth from surface or margin of thallus, or margin of apothecium, [91].

Consortium (consortism), mutual association of fungus and alga (Reinke); also termed “mutualism,” [31], [313].

Corticolous, living on the bark of trees, [363].

Crustaceous, crust-like closely adhering thallus, [70-79].

Cyphella, minute cup-like depression on the under surface of the thallus (Sticta, etc.), [11], [126].

Decomposed, term applied to cortex formed of gelatinous indistinct hyphae (amorphous), [73-81] et passim, [357].

Determinate, thallus with a definite outline, [72].

Dimidiate, term applied to the perithecium, when the outer wall covers only the upper portion, [159].

Discoid, disc-like, an open rounded apothecium, [156].

Discolichens, in which the fructification is an apothecium, [160 et seq.]

Dual hypothesis, the theory of two organisms present in the lichen thallus, [27 et seq.]

Effigurate, having a distinct form or figure; [cf. placodioid], [80], [201].

Endobasidial, Steiner’s term for sporophore with a secondary sporiferous branch, [200].

Endogenous, produced internally, as spores in an ascus, [179]; [see also under thallus].

Endolithic, embedded in the rock, [75].

Endosaprophytism, term used by Elenkin for destruction of the algal contents by enzymes of the fungus, [36].

Entire, term applied to the perithecium when completely surrounded by an outer wall, [159].

Epilithic, growing on the rock surface, [70].

Epiphloeodal, thallus growing on the surface of the bark, [77].

Epiphyllous, growing on leaves, [363].

Epithecium, upper layer of thecium (hymenium), [158].

Erratic lichens, unattached and drifting, [259].

Exobasidial, Steiner’s term for sporophore without a secondary sporiferous branch, [200].

Exogenous, produced externally, as spores on tips of hyphae; [see also under thallus].

Fastigiate cortex, formed of clustered parallel hyphal branches vertical to long axis of thallus, [82].

Fat-cells, specialized hyphal cells containing fat or oil, [75], [215] et passim.

Fibrous cortex, formed of hyphae parallel with long axis of thallus, [82].

Filamentous, slender thallus with radiate structure, [101 et seq.]

Foliose, lichens with a leafy form and stratose in structure, [82-97].

Foveolae, Foveolate, pitted, [373].

Fruticose, upright or pendulous thallus, with radiate structure, [101 et seq.]

Fulcrum, term used by Steiner for sporophore, [200].

Gloeolichens, lichens in which the gonidia are Gloeocapsa or Chroococcus, [284], [373], [389].

Gonidium, the algal constituent of the lichen thallus, [20-45] et passim.

Gonimium, blue-green algal cell (Myxophyceae), constituent of the lichen thallus, [52].

Goniocysts, nests of gonidia in Moriolaceae, [313].

Gyrose, curved backward and forward, furrowed fruit of Gyrophora, [184].

Hapteron, aerial organ of attachment, [94], [122].

Haustorium, outgrowth or branch of a hypha serving as an organ of suction, [32].

Helotism, state of servitude, term used to denote the relation of alga to fungus in lichen organization, [38], [40].

Heteromerous, fungal and algal constituents of the thallus in definite strata, [13], [68], [305] et passim.

Hold-fast, rooting organ of thallus, [109], [122] et passim.

Homobium, interdependent association of fungus and alga, [31].

Homoiomerous, fungal and algal constituents more or less mixed in the thallus, [13], [68], [305] et passim.

Hymenial gonidia, algal cells in the hymenium, [30], [314], [315], [327].

Hymenium, apothecial tissue consisting of asci and paraphyses; [cf. thecium], [157].

Hymenolichens, lichens of which the fungal constituent is a Hymenomycete, [152-154], [342].

Hypophloeodal, thallus growing within the bark, [78], [364].

Hypothallus, first growth of hyphae (proto- or pro-thallus) persisting as hyphal growth at base or margin of the thallus, [70], [257] et passim.

Hypothecium, layer below the thecium (hymenium), [157].

Intricate cortex, composed of hyphae densely interwoven but not coalescent, [83].

Isidium, coral-like outgrowth on the lichen thallus, [149-151].

Lecanorine, apothecium with a thalline margin as in Lecanora, [158].

Lecideine, apothecium usually dark-coloured or carbonaceous and without a thalline margin, [158].

Leprose, mealy or scurfy, like the old form genera, Lepra, Lepraria, [191].

Lichen-acids, organic acids peculiar to lichens, [221 et seq.]

Lignicolous, living on wood or trees, [366].

Lirella, long narrow apothecium of Graphideae, [158].

Mazaedium, fructification of Coniocarpineae, the spores lying as a powdery mass in the capitulum, [176].

Medulla, the loose hyphal layer in the interior of the thallus, [88] et passim.

Meristematic, term applied by Wainio to growing hyphae, [48].

Microgonidia, term applied by Minks to minute greenish bodies in lichen hyphae, [26].

Multi-septate, term applied to spores with numerous transverse septa, [316 et seq.]

Murali-divided, Muriform, term applied to spores divided like the masonry of a wall, [187].

Oidium, reproductive cell formed by the breaking up of the hyphae, [189].

Oil-cell, hyphal cell containing fat globules, [215].

Orculiform, [see polarilocular].

Orthidium, supposed new type of fructification in lichens, [192].

Palisade-cells, the terminal cells of the hyphae forming the fastigiate cortex, [82], [83].

Panniform, having a felted or matted appearance, [260].

Paraphysis, sterile filament in the hymenium, [157].

Parasymbiosis, associated harmless but not mutually useful growth of two organisms, [263].

Parathecium, hyphal layer round the apothecium, [157].

Peltate, term applied to orbicular and horizontal apothecia in the form of a shield, [336].

Perithecium, roundish fructification usually with an apical opening (ostiole) containing ascospores, [158] et passim.

Pervious, referring to scyphi with an opening at the base (Perviae), [118].

Phycolichens, lichens in which the gonidia are blue-green (Myxophyceae), [52] et passim.

Placodioid, thallus with a squamulose determinate outline, generally orbicular; [cf. effigurate], [80].

Placodiomorph, [see polarilocular].

Plectenchyma (Plectenchymatous), pseudoparenchyma of fungi and lichens, [66] et passim.

Pleurogenous, borne laterally on hyphal cells; [see spermatium], [312].

Pluri-septate, term applied to spores with several transverse septa, [321 et seq.]

Podetium, stalk-like secondary thallus of Cladoniaceae, [114], [293 et seq.]

Polarilocular, Polaribilocular, two-celled spores with thick median wall traversed by a connecting tube, [188], [340-341].

Polytomous, arising of several branches of the podetium from one level, [118].

Proper margin, the hyphal margin surrounding the apothecium, [157].

Prothallus, Protothallus, first stages of hyphal growth; [cf. hypothallus], [71].

Pycnidiospores, stylospores borne in pycnidia, [198] et passim.

Pycnidium, roundish fructification, usually with an opening at the apex, containing sporophores and stylospores; [cf. spermogonium], [192 et seq.]

Pyrenolichens, in which the fructification is a closed perithecium, [173] et passim.

Radiate thallus, the tissues radiate from a centre, [98 et seq.]

Rhagadiose, deeply chinked, [74]; [cf. rimose].

Rhizina, attaching “rootlet,” [92-94].

Rimose, Rimulose, cleft or chinked into areolae, [73].

Rimose-diffract, widely cracked or chinked, [74].

Scutellate, shaped like a platter, [156].

Scyphus, cup-like dilatation of the podetium, [111], [117].

Signature, a term in ancient medicine to signify the resemblance of a plant to any part of the human body, [406], [409].

Soralium, group of soredia surrounded by a definite margin, [144].

Soredium, minute separable particle arising from the gonidial tissue of the thallus, and consisting of algae and hyphae, [141].

Spermatium, spore-like body borne in the spermogonium, regarded as a non-motile male cell or as a pycnidiospore, [201].

Spermogonium, roundish closed receptacle containing spermatia, [192].

Sphaeroid-cell, swollen hyphal cell, containing fat globules, [215].

Squamule, a small thalline lobe or scale, [74] et passim.

Sterigma, Nylander’s term for the spermatiophore, [197].

Stratose thallus, where the tissues are in horizontal layers, [70].

Stratum, a layer of tissue in the thallus, [70].

Symbiont, one of two dissimilar organisms living together, [32].

Symbiosis, a living together of dissimilar organisms, also termed commensalism, [31, 32 et seq.]

Tegulicolous, living on tiles, [369].

Terebrator, boring apparatus, term used by Lindau for the lichen “trichogyne,” [179].

Thalline margin, an apothecial margin formed of and usually coloured like the thallus; [cf. amphithecium].

Thallus, vegetative body or soma of the lichen plant, [11], [421]. Endogenous thallus in which the alga predominates, [68]. Exogenous thallus in which the fungus predominates, [69].

Theca, enlarged cell containing spores; [cf. ascus].

Thecium, layer of tissue in the apothecium consisting of asci and paraphyses; [cf. hymenium], [157].

Trichogyne, prolongation of the egg-cell in Florideae which acts as a receptive tube; septate hypha in lichens arising from the ascogonium, [160], [177-181], [273].

Woronin’s hypha, a coiled hypha occurring in the centre of the fruit primordium, [159], [163].

ERRATA

Transcriber’s Note: The errata have been corrected.

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.

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 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 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; 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 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.

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:

I. From the earliest times to the end of the seventeenth century.

II. Dating from the arrangement of plants into classes called genera by Tournefort in 1694 to 1729.

III. From Micheli’s division of lichens into different orders in 1729 to 1780.

IV. The definite and reasoned establishment of lichen genera based on the structure of thallus and fruit by Weber in 1780 to 1803.

V. The arrangement of all known lichens under their respective genera by Acharius in 1803 to 1846.

VI. The recognition of spore characters in classification by De Notaris in 1846 to 1867.

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 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 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 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 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 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”; 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, 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.

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 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.

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 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; 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 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 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 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.

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 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.

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.

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.

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 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 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.

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 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.

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 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 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.

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 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 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 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.

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 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 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 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 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 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 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.

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 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 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 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 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.

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 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 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.

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.

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 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:

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 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. (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).

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 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.

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.

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).

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).

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 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.

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 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 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.

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 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.

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 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.

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).

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 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.

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 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 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 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.

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 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.

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 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, 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.

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.

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.

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 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 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 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 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, 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 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.

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 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 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 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 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 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.

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 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.

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: 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.

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.).

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 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 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 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.

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 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.

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

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 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 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.

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 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 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).

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, 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.

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

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

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.).

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 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 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 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 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] 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.

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 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].

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.

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 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:

§ Eusticta (with bright-green gonidia).

Cyphellate: S. damaecornis.

Pseudocyphellate: S. aurata.

§ Stictina (with blue-green gonidia).

Cyphellate: S. fuliginosa, S. limbata, S. sylvatica, S. Dufourei.

Pseudocyphellate: S. intricata var. Thouarsii, S. crocata.

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.

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. 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 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.

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.