Chapter III: Morphology (3)

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.

_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

_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.

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.

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

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

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

2. CEPHALODIA

A. HISTORICAL AND DESCRIPTIVE

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

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

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

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

B. CLASSIFICATION

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

I. CEPHALODIA VERA.

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

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

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

II. PSEUDOCEPHALODIA.

These are a small and doubtful group of cephalodia which are apparently in very slight connection with the host thallus, and show a tendency to independent growth. They occur as small scales on _Solorina bispora_[459] and _S. spongiosa_ and also on _Lecidea pallida_. Forssell has suggested that the cephalodia of _Psoroma hypnorum_ and of _Lecidea panaeola_ might also be included under this head.

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

Sphaerophoraceae.

_Sphaerophorus_ (_S. stereocauloides_).

Lecideaceae.

_Lecidea_ (_L. panaeola_, _L. consentiens_, _L. pelobotrya_,
etc.).

Cladoniaceae.

_Stereocaulon_, _Pilophorus_ and _Argopsis_.

Pannariaceae.

_Psoroma_ (_P. hypnorum_).

Peltigeraceae.

_Peltigera_ (_Peltidea_), _Nephroma_ and _Solorina_.

Stictaceae.

_Lobaria_, _Sticta_.

Lecanoraceae.

_Lecania_ (_L. lecanorina_), _Aspicilia_[460].

Physciaceae.

_Placodium bicolor_[461].

C. ALGAE THAT FORM CEPHALODIA

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

_Stigonema_,—in _Lecanora gelida_, _Stereocaulon_, _Pilophorus robustus_, and _Lecidea pelobotrya_.

_Scytonema_,—a rare constituent of cephalodia.

_Nostoc_,—the most frequent gonidium of cephalodia. It occurs in those of the genera _Sticta_, _Lobaria_, _Peltigera_, _Nephroma_, _Solorina_ and _Psoroma_; occasionally in _Stereocaulon_ and in _Lecidea pallida_.

_Lyngbya_ and _Rivularia_,—rarely present, the latter in _Sticta oregana_[462].

_Chroococcus_ and _Gloeocapsa_,—also very rare.

_Scytonema_, _Chroococcus_, _Gloeocapsa_ and _Lyngbya_ are generally found in combination with some other cephalodia-building alga, though Nylander[463] found _Scytonema_ alone in the lobulate cephalodia of _Sphaerophorus stereocauloides_, a New Zealand lichen, and the only species of that genus in which cephalodia are developed; and Hue[460] records _Gloeocapsa_ as forming internal cephalodia in two species of _Aspicilia_. Bornet[464] found _Lyngbya_ associated with _Scytonema_ in the cephalodia of _Stereocaulon ramulosum_, and, in the same lichen, Forssell[465] found, in the several cephalodia of one specimen, _Nostoc_, _Scytonema_, and _Lyngbya_, while, in those of another, _Scytonema_ and _Stigonema_ were present. In the latter instance these algae were living free on the podetium. Forssell[465] also determined two different algae, _Gloeocapsa magma_ and _Chroococcus turgidus_, present in a cephalodium on _Lecidea panaeola_ var. _elegans_.

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

_Lecanora gelida_ and _Lecidea illita_ contain either _Stigonema_ or _Nostoc_;

_Lecidea panaeola_, with _Gloeocapsa_, _Stigonema_ or _Chroococcus_;

_Lecidea pelobotrya_, with _Stigonema_ or _Nostoc_;

_Pilophorus robustus_, with _Gloeocapsa_, _Stigonema_, or _Nostoc_.

Riddle[466] has employed cephalodia with their enclosed algae as diagnostic characters in the genus _Stereocaulon_. When the alga is _Stigonema_, as in _S. paschale_, etc., the cephalodia are generally very conspicuous, grey in colour, spherical, wrinkled or folded, though sometimes black and fibrillose (_S. denudatum_). Those containing _Nostoc_ are, on the contrary, minute and are coloured verdigris-green (_S. tomentosum_ and _S. alpinum_).

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

D. DEVELOPMENT OF CEPHALODIA

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

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

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

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

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

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

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

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

E. AUTOSYMBIOTIC CEPHALODIA

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

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

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

3. SOREDIA

A. STRUCTURE AND ORIGIN OF SOREDIA

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

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

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

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

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

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

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

B. SORALIA

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

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

Soralia of definite form are of rather rare occurrence in crustaceous lichens, with the exception of the Pertusariaceae, where they are frequent, and some species of _Lecanora_ and _Placodium_. They are known in only two hypophloeodal (subcortical) lichens, _Arthonia pruinosa_ and _Xylographa spilomatica_. Among squamulose thalli they are typical of some _Cladoniae_, and also of _Lecidea_ (_Psora_) _ostreata_, where they are produced on the upper surface towards the apex of the squamule.

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

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

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

Apical soralia are rare in fruticose lichens, but in an Alpine variety of _Ramalina minuscula_ they are formed at the tips of the fronds and are protected by an extension of the upper cortical tissues. Another instance occurs in a _Ramalina_ from New Granada referred by Nylander to _R. calicaris_ var. _farinacea_: it presents a striking example of the helmet tip.

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

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

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

C. DISPERSAL AND GERMINATION OF SOREDIA

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

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

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

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

D. EVOLUTION OF SOREDIA