Annie Lorrain Smith

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

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

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

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

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

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

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

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

B. Forms of Reproductive Organs

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

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

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

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

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

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

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

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

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

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

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

C. Development of Reproductive Organs

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

1. DISCOLICHENS

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

2. PYRENOLICHENS

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

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

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

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

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

D. Apogamous Reproduction

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

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

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

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

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

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

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

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

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

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

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

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

E. Discussion of Lichen Reproduction

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

F. Final Stages of Apothecial Development

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

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

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

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

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

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

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

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

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

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

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

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

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

G. Lichen Asci and Spores

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

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

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

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

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

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

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

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

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

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

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

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

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

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

The polarilocular colourless spore is found in a connected series of lichens—crustaceous, foliose and fruticose (Placodium, Xanthoria, Teloschistes). In another series with a darker thallus (Rinodina and Physcia) the spore is brown-coloured, and the median septum cuts across the plasma-connection. In other respects the brown spore is similar to the colourless one and possesses a thickened wall with reduced cell-cavities.

The method of cell-division in these spores resembles that known as “cleavage by constriction,” in which the cross wall arises by an ingrowth from all sides of the cell; in time the centre is reached and the wall is complete, or an open pore is left between the divided cells. Cell “cleavage” occurs frequently among Thallophytes, though it is unknown among the higher plants. Among Algae it is the normal form of cell-division in Cladophora and also in Spirogyra, though in the latter the wall passes right across and cuts through the connecting plasma threads. Harper[684] found “cleavage by constriction” in two instances among fungi: the conidia of Erysiphe and the gametes of Sporodinia are cut off by a septum which originates as a circular ingrowth of the outer wall, comparable, he considers, with the cell-division of Cladophora.

The development of the thickened wall of polarilocular spores has been studied by Hue[685], who contends however that there is no true septation in the colourless spores so long as the central canal remains open. According to his observations the wall of the young spore is formed of a thin tegument, everywhere equal in thickness, and consisting of concentric layers. This tegument becomes continually thicker at the equator of the spore by the addition of new layers from the interior, and the protoplasmic contents are compressed into a gradually diminishing space. In the end the wall almost touches at the centre, and the spore consists of two polar cell-cavities with a narrow open passage between. A median line pierced by the canal is frequently seen. In a few species there is a second constriction cleavage and the spore becomes quadrilocular.

Hue insists that this spore should be regarded as only one-celled; for though the walls may touch at the centre, he says they never coalesce. He has unfortunately given no cytological observations as to whether the spore is uni- or binucleate.

In Xanthoria parietina, one of the species with characteristic polaribilocular spores, germination, it would seem, takes place mostly at one end only of the spore, though a germinating tube issues at both ends frequently enough to suggest that the spore is binucleate and two-celled. The absence of germination from one or other of the cells only may probably be due to the drain on their small resources. Hue has cited the rarity of such instances of double germination in support of his view of the one-celled nature of the spore. He instances that out of fifteen spores, Tulasne[686] has figured only three that have germinated at each end; Bornet[687] figures one in seven with the double germination and Bonnier[688] one in sixteen spores.

Further evidence is wanted as to the nuclear history of these hyaline spores. In the case of the brown spores, which show the same thickening of the wall and restricted cell-cavity, though with a distinct median septum, nuclear division was observed by RenÉ Maire[689] before septation in one such species, Anaptychia ciliaris.

II. SECONDARY SPORES

A. Reproduction by Oidia

In certain conditions of nutrition, fungal hyphae break up into separate cells, each of which functions as a reproductive conidium or oidium, which on germination forms new hyphae. Neubner[690] has demonstrated a similar process in the hyphae of the Caliciaceae and compares it with the oidial formation described by Brefeld[691] in the Basidiomycetes.

The thallus of this family of lichens is granular or furfuraceous; it never goes beyond the Lepra stage of development[692]. In some species it is scanty, in others it is abundant and spreads over large areas of the trunks of old trees. It is only when growth is especially luxuriant that oidia are formed. Neubner was able to recognize the oidial condition by the more opaque appearance of the granules, and under the microscope he observed the hyphae surrounding the gonidia gradually fall away and break up into minute cylindrical cells somewhat like spermatia in size and form. There was no question of abnormal or unhealthy conditions, as the oidia were formed in a freely fruiting thallus.

The gonidia associated with the oidial hyphae also showed unusual vitality and active division took place as they were set free by the breaking up of the encircling hyphae. The germination of the oidia provides an abundance of hyphal filaments for the rapidly increasing algal cells, and there follows a wide-spread development of the lichen thallus.

Oidial formation has not been observed in any other family of lichens.

B. Reproduction by Conidia

a. Instances of Conidial Formation. It is remarkable that the type of asexual reproduction so abundantly represented in fungi by the large and varied group of the Hyphomycetes is practically absent in lichens. An exception is to be found in a minute gelatinous lichen that grows on soil. It was discovered by Bornet[693] and called by him Arnoldia (Physma) minutula. From the thallus rise up simple or sparingly branched colourless conidiophores which bear at the tips globose brown conidia (Fig. 108). Bornet[694] obtained these conidia by keeping very thin sections of the thallus in a drop of water[693].

Yet another instance of conidial growth is given by Steiner[695]. He had observed that the apothecia on plants of Caloplaca aurantia var. callopisma Stein. differed from those of normal appearance in the warted unevenness of the disc and also in being more swollen and convex, the thalline margin being almost obliterated. He found, on microscopical examination, that the hymenium was occupied by paraphyses and by occasional asci, the latter seldom containing spores, and being usually more or less collapsed. The component parts of the apothecium were entirely normal and healthy, but the paraphyses and the few asci were crushed aside by the intrusion of numerous slender unbranched septate conidiophores. Several of these might spring from one base and the hypha from which they originated could be traced some distance into the ascogenous layer, though a connection with that cell-system could not be demonstrated. While still embedded in the hymenium, an ellipsoid or obovate swelling began to form at the apex of the conidiophore; it became separated from the stalk by a septum and later divided into a two-celled conidium. The conidiophore increased in length by intercalary growth and finally emerged above the disc; the mature conidium was pyriform and measured 15-20 µ × 9-11 µ.

Steiner regarded these conidia as entirely abnormal; pycnidia with stylospores are unknown in the genus and they were not, he alleges, the product of any parasitic growth.

b. Comparison With Hyphomycetes. The conidial form of fructification in fungi, known as a Hyphomycete, is generally a stage in the life-cycle of some Ascomycete; it represents the rapid summer form of asexual reproduction. The ascospore of the resting fruit-form in many species germinates on any suitable matrix and may at once produce conidiophores and conidia, which in turn germinate, and either continue the conidial generation or proceed to the formation of the perfect fruiting form with asci and ascospores.

Such a form of transient reproduction is almost impossible in lichens, as the hypha produced by the germinating lichen ascospore has little vitality without the algal symbiont. In natural conditions development practically ceases in the absence of symbiosis. When union between the symbionts takes place, and growth becomes active, thallus construction at once commences. But in certain conditions of shade and moisture, only the rudiments of a lichen thallus are formed, known as a leprose or sorediose condition. Soredia also arise in the normal life of many lichens. As the individual granules or soredia may each give rise to a complete lichen plant, they may well be considered as replacing the lost conidial fructification.

C. Campylidium and Orthidium

MÜller[696] has described under the name Campylidium a supposed new type of asexual fructification which he found on the thallus of tropical species of Gyalecta, Lopadium, etc., and which he considered analogous to pycnidia and spermogonia. Wainio[697] has however recognized the cup-like structure as a fungus, Cyphella aeruginascens Karst., which grows on the bark of trees and occasionally is parasitic on the crustaceous thallus of lichens. Wainio has also identified the plant, Lecidea irregularis, first described by FÉe[698], as also synonymous with the fungus.

Another name Orthidium was proposed by MÜller[699] for a type of fructification he found in Brazil which he contrasts or associates with Campylidium. It has an open marginate disc with sporophores bearing acrogenous spores. He found it growing in connection with a thin lichen thallus on leaves and considered it to be a form of lichen reproduction. Possibly Orthidium is also a Cyphella.

III. SPERMOGONIA OR PYCNIDIA

A. Historical Account of Spermogonia

The name spermogonium was given by Tulasne[700] to the “punctiform conceptacles” that are so plentifully produced on many lichen thalli, on the assumption that they were the male organs of the plant, and that the spore-like bodies borne in them were non-motile male cells or spermatia.

The first record of their association with lichens was made by Dillenius[701], who indicates the presence of black tubercles on the thallus of Physcia ciliaris. He figures them also on several species of Cladonia, on Ramalina and on Dermatocarpon, but without any suggestion as to their function. Hedwig’s[702] study of the reproductive organs of the Linnaean Cryptogams included lichens. He examined Physcia ciliaris, a species that not only is quite common but is generally found in a fruiting condition and with very prominent spermogonia, and has been therefore a favourite lichen for purposes of examination and study. Hedwig describes and figures not only the apothecia but also those other bodies which he designates as “punctula mascula,” or again as “puncta floris masculi.” In his later work he gives a drawing of Lichen (Gyrophora) proboscideus, with two of the spermogonia in section.

Acharius[703] included them among the lichen structures which he called “cephalodia”: he described them as very minute tubercles rising up from the substance of the thallus and projecting somewhat above it. He also figures a section through two “cephalodia” of Physcia ciliaris. Fries[704] looked on them as being mostly “anamorphoses of apothecia, the presence of abortive fruits transforming the angiocarpous lichen to the appearance of a gymnocarpous form.” Wallroth[705] assigned the small black fruits to the comprehensive fungus genus Sphaeria or classified lichens bearing spermogonia only as distinct genera and species (Pyrenothea and Thrombium). Later students of lichens—Schaerer[706], Flotow[707], and others—accepted Wallroth’s interpretation of their relation to the thallus, or they ignored them altogether in their descriptions of species.

B. Spermogonia as Male Organs

Interest in these minute “tubercles” and their enclosed “corpuscles” was revived by Itzigsohn[708] who examined them with an improved microscope. He macerated in water during a few days that part of the thallus on which they were developed, and, at the end of the time, discovered that the solution contained large numbers of motile bodies which he naturally took to be the corpuscles from the broken down tubercles. He claimed to have established their function as male motile cells or spermatozoa. The discovery seemed not only to prove their sexual nature, but to link up the reproduction of lichens with that of the higher cryptogams. The tubercles in which the “spermatozoa” were produced he designated as antheridia. More prolonged maceration of the tissue to the very verge of decay yielded still larger numbers of the “spermatozoa” which we now recognize to have been motile bacilli.

Tulasne[709] next took up the subject, and failing to find the motile cells, he wrongly insisted that Itzigsohn had been misled by mere Brownian movement, but at the same time he accepted the theory that the minute conceptacles were spermogonia or male organs of lichens. He also pointed out that their constant occurrence on the thallus of practically every species of lichen, and their definite form, though with considerable variation, rendered it impossible to regard them as accidental or of no importance to the life of the plant. He compared them with fungal pycnidia such as Phyllosticta or Septoria which outwardly they resembled, but whereas the pycnidial spores germinated freely, the spermatia of the spermogonia, as far as his experience went, were incapable of germination.

C. Occurrence and Distribution

a. Relation to Thallus and Apothecia. We owe to Tulasne[710] the first comparative study of lichen spermogonia. He described not only their outward form, but their minute structure, in a considerable number of representative species. A few years later Lindsay[711] published a memoir dealing with the spermogonia of the larger foliose and fruticose lichens, and, in a second paper, he embodied the results of his study of an equally extensive selection of crustaceous species. Lindsay’s work is unfortunately somewhat damaged by faulty determination of the lichens he examined, and by lack of the necessary discrimination between one thallus and another of associated and intermingled species. Both memoirs contain, however, much valuable information as to the forms of spermogonia, with their spermatiophores and spermatia, and as to their distribution over the lichen thallus.

Though spermogonia are mostly found associated with apothecia, yet in some lichens, such as Cerania (Thamnolia) vermicularis, they are the only sporiferous organs known. Not unfrequently crustaceous thalli bear spermogonia only, and in some Cladoniae, more especially in ascyphous species, spermogonia are produced abundantly at the tips of the podetial branches (Fig. 109), while apothecia are exceedingly rare. Usually they occur in scattered or crowded groups, more rarely they are solitary. Very often they are developed and the contents dispersed before the apothecia reach the surface of the thallus; hence the difficulty in relating these organisms, since the mature apothecium is mostly of extreme importance in determining the species.

In a very large number of lichens, both crustaceous and foliose, the spermogonia are scattered over the entire thallus (Fig. 110), covering it more or less thickly with minute black dots, as in Parmelia conspersa. In other instances, they are to some extent confined to the peripheral areas as in Parmelia physodes; or they occur on the extreme edge of the thallus as in the crustaceous species Lecanora glaucoma (sordida). In Pyrenula nitida they grow on the marginal hypothallus, usually on the dark line of demarcation between two thalli.

They tend to congregate on, and indeed are practically restricted to the better lighted portions of the thallus. On the fronds of foliose forms, they appear, for instance, on the swollen pustules of Umbilicaria pustulata, while in Lobaria pulmonaria, they are mostly lodged in the ridges that surround the depressions in the thallus. In Parmelia conspersa, Urceolaria (Diploschistes) scruposa and some others, they occasionally invade the margins of the apothecium or even the apothecial disc as in Lichina. Forssell[712] found that a spermogonium had developed among cells of Gloeocapsa that covered the disc of a spent apothecium of Pyrenopsis haematopis.

In fruticose lichens such as Usnea, Ramalina, etc. they occur near the apex of the fronds, and in Cladonia they occupy the tips of the ascyphous podetia or the margins of the scyphi. In some Cladoniae, however, spermogonia are produced on the basal squamules, more rarely on the squamules that clothe the podetia.

b. Form and Size. Spermogonia are specifically constant in form, the same type being found on the same lichen species all over the globe. The larger number are entirely immersed and are ovoid or roundish (Fig. 111 A) or occasionally somewhat flattened bodies (Nephromium laevigatum), or again, but more rarely, they are irregular in outline with an infolding of the walls that gives the interior a chambered form (Fig. 111 B) (Lichina pygmaea); but all of these are only visible as minute points on the thallus.

A second series, also immersed, are borne in small protuberances of the thallus. These very prominent forms are rarely found in crustaceous lichens, but they are characteristic of such well-known species as Ramalina fraxinea, Xanthoria parietina, Ricasolia amplissima, Baeomyces roseus, etc. Other spermogonia project slightly above the level of the thallus, as in Cladonia papillaria and Lecidea lurida; while in a few instances they are practically free, these last strikingly exemplified in Cetraria islandica where they occupy the small projections or cilia (Fig. 112) that fringe the margins of the lobes; they are free also in most species of Cladonia.

In size they vary from such minute bodies as those in Parmelia exasperata which measure 25-35 µ in diam., up to nearly 1 mm. in Lobaria laetevirens. As a rule, they range from about 150 µ to 400 µ across the widest part, and are generally rather longer than broad. They open above by a small slit or pore called the ostiole about 20 µ to 100 µ wide which is frequently dark in colour. In one instance, in Icmadophila aeruginosa, Nienburg[713] has described a spermogonium with a wide opening, the spermatiophores being massed in palisade formation along the bottom of a cup-like structure.

c. Colour of Spermogonia. Though usually the ostiole is visible as a darker point than the surrounding tissue, spermogonia are often difficult to locate unless the thallus is first wetted, when they become visible to slight magnification. They appear as black points in many Parmeliae, Physciae, Roccellae, etc., though even in these cases they are often brown when moistened. They are distinctly brown in some Cladoniae, in Nephromium, and in some Physciae; orange-red or yellow in Placodium and concolorous with the thallus in Usnea, Ramalina, Stereocaulon, etc.

D. Structure

a. Origin and Growth. The spermogonia (or pycnidia) of lichens when mature are more or less hollow structures provided with a distinct wall or “perithecium,” sometimes only one cell thick and then not easily demonstrable, as in Physcia speciosa, Opegrapha vulgata, Pyrenula nitida, etc. More generally the “perithecium” is composed of a layer of several cells with stoutish walls which are sometimes colourless, but usually some shade of yellow to dark-brown, with a darker ostiole. The latter, a small slit or pore, arises by the breaking down of some of the cells at the apex. After the expulsion of the spermatia, a new tissue is formed which completely blocks up the empty spermogonium. In filamentous lichens such as Usnea a dangerous local weakening of the thallus is thus avoided.

Spermogonia originate from hyphae in or near the gonidial zone. The earliest stages have not been seen, but MÖller[714] noted as the first recognizable appearance or primordium of the “pycnidia” in cultures of Calicium trachelinum a ball or coil of delicate yellowish-coloured hyphae. At a more advanced stage the sporophores (or spermatiophores) could be traced as outgrowths from the peripheral hyphae, directed in palisade formation towards the centre of the hyphal coil about 20-30 µ long and very slender and colourless. They begin to bud off spermatia almost immediately, as it has been found that these are present in abundance while the developing spermogonium is still wholly immersed in the thallus. Meanwhile there is gradually formed on the outside a layer of plectenchyma which forms the wall. Additional spermatiophores arise from the wall tissue and push their way inwards between the ranks of the first formed series. The spermogonium slowly enlarges and stretches and as the spermatiophores do not grow any longer a central hollow arises which becomes packed with spermatia (or spores) before the ostiole is open.

A somewhat similar process of development is described by Sturgis[715] in the spermogonia of Ricasolia amplissima, in which species the primordium arises by a profuse branching of the medullary hyphae in certain areas close to the gonidial zone. The cells of these branching hyphae are filled with oily matter and gradually they build up a dense, somewhat cylindrical body which narrows above to a neck-like form. The growth is upwards through the gonidial layer, and the structure widens to a more spherical outline. It finally reaches the outer cortex when some of the apical cell membranes are absorbed and a minute pore is formed. The central part becomes hollow, also by absorption, and the space thus left is lined and almost filled with multicellular branches of the hyphae forming the wall; from the cells of this new tissue the spermatia are abstricted.

b. Forms and types of Spermatiophores. The variations in form of the fertile hyphae in the spermogonium were first pointed out by Nylander[716] who described them as sterigmata[717]. He considered the differences in branching, etc. as of high diagnostic value, dividing them into two groups: simple “sterigmata” (or spermatiophores), with non-septate hyphae, and arthrosterigmata, with jointed or septate hyphae.

Simple “sterigmata” comprise those in which the spore or spermatium is borne at the end of a secondary branch or sterigma, the latter having arisen from a cell of the upright spermatiophore or from a simple basal cell. The arthrosterigmata consist of “short cells almost as broad as they are long, much pressed together, and appearing almost agglutinate especially toward the base; they fill almost the whole cavity of the spermogonium.” The arthrosterigmata may grow out into the centre of the cavity as a single cell-row, as a loose branching network, or, as in Endocarpon, they may form a tissue filling the whole interior. Each cell of this tissue that borders on a cavity may bud off a spermatium either directly or from the end of a short process.

The most important contributions on the subject of spermogonia in recent years are those of GlÜck[718] and Steiner[719]. GlÜck, who insisted on the “pycnidial” non-sexual character of the organs, recognized eight types of “sporophores” differing in the complexity of their branching or in the form of the “spores” (Fig. 113 A):

1. The Peltigera type: the sporophores consist of a basal cell bearing one or more long sterigmata and rather stoutish ellipsoid spores. (These are true pycnidia.)

2. The Psora type: a more elongate simple sporophore with sterigmata and oblong spores.

3. The Cladonia type: a branching sporophore, each branch with sterigmata and oblong spores.

4. The Squamaria type (called by GlÜck Placodium): also a branching sporophore but with long sickle-like bent spores.

5. The Parmelia type: a more complicated system of branching and anastomosing of the sporophores, with oblong spores.

6, and 7. The Sticta and Physcia types: in both of these the sporophores are multi-septate; they consist of a series of radiately arranged hyphae rising from a basal tissue all round the pycnidium. They anastomose to form a network and bud off “spermatia” from the free cells or rather from minute sterigmata. In the Physcia type there is more general anastomosis of the sporophores and frequently masses of sterile cells along with the fertile members occupy the centre of the pycnidium. The spermatia of these and the following Endocarpon type are short cylindrical bodies (Fig. 113 B).

8. Endocarpon type: the pycnidium is filled by a tissue of short broad cells, with irregular hollow spaces lined by fertile cells similar to those of the Sticta and Physcia types.

The three last named types of sporophores represent Nylander’s section of arthrosterigmata. Steiner has followed Nylander in also arranging the various forms into two leading groups. The first, characterized by the secondary branch or “sterigma,” he designates “exobasidial”; the second, comprising the three last types in which the spores are borne directly on the cells of the sporophore or on very short processes, he describes as “endobasidial.” Steiner also introduces a new term, fulcrum, for the sporophore.

The pycnidia in which these different sporophores occur are not, as a rule, characteristic of one family. Peltigera type is found only in one family and the Cladonia type is fairly constant in Cladoniae, but “Psora” pycnidia are found on very varying lichens among the Lecideaceae, Verrucariaceae and others. The Squamaria type with long bent spores is found not only in Squamaria (GlÜck’s Placodium) but also in Lecidea, Roccella, Pyrenula, etc. Parmelia type is characteristic of many Parmeliae and also of species of Evernia, Alectoria, Platysma and Cetraria. The Sticta type occurs in Gyrophora, Umbilicaria, Nephromium and Lecanora as well as in Sticta and in one species at least of Collema. To the Physcia type belong the pycnidia of most Physciaceae and of various Parmeliae, and to the closely related Endocarpon type the pycnidia of Endocarpon and of Xanthoria parietina.

c. Periphyses and Sterile Filaments. In a few species, Roccella tinctoria, Pertusaria globulifera, etc., short one-celled sterile hyphae are formed within the spermogonium near the ostiole, towards which they converge. They correspond to the periphyses in the perithecia of some Pyrenolichens, Verrucaria, etc. (described by Gibelli[720] as spermatiophores); they are also present in some of the Pyrenomycetes (Sordaria, etc.), and in many cases replace the paraphyses in function when these have broken down. Sterile hyphae also occur, towards the base, mingled with the fertile spermatiophores (Fig. 114). These latter were first described and figured by Tulasne[721] in the spermogonia of Ramalina fraxinea as stoutish branching filaments, rising from the same base as the spermatiophores but much longer, and frequently anastomosing with each other. They have been noted also in Usnea barbata and in several species of Parmelia, and have been compared by Nylander[722] to paraphyses. They are usually colourless, but, in the Parmeliae, are often brownish and thus easily distinguished from the spermatiophores. It has been stated that these filaments are sometimes fertile. Similar sterile hyphae have been recorded in the pycnidia of fungi, in Sporocladus (Hendersonia) lichenicola (Sphaeropsideae) by Corda[723] who described them as paraphyses, and also in Steganosporium cellulosum (Melanconieae). These observations have been confirmed by Allescher[724] in his recent work on Fungi Imperfecti. Keiszler[725] has described a Phoma-like, pycnidium parasitic on the leprose thallus of Haematomma elatinum. It contains short slender sporophores and, mixed with these, long branched sterile hyphae which reach to the ostiole and evidently function as paraphyses, though Keiszler suggests that they may be a second form of sporophore that has become sterile. On account of their presence he placed the fungus in a new genus Lichenophoma.

E. Spermatia or Pycnidiospores

a. Origin and Form of Spermatia. Lichen spermatia arise at the tips of the sterigmata either through simple abstriction or by budding. In the former case—as in the Squamaria type—a delicate cross-wall is formed by which the spermatium is separated off. When they arise by budding, there is first a small clavate sac-like swelling of the end of the short process or sterigma which gradually grows out into a spermatium on a very narrow base. This latter formation occurs in the Sticta, Physcia and Endocarpon types.

Nylander[726] has distinguished the following forms of spermatia:

1. Ob-clavate, the broad end attached to the sterigma as in Usneae, Cetraria glauca and C. juniperina.

2. Acicular and minute but slightly swollen at each end, somewhat dumb-bell like, in Cetraria nivalis, C. cucullata, Alectoria, Evernia and some Parmeliae, frequently borne on “arthrosterigmata.”

3. Acicular, cylindrical and straight, the most common form; these occur in most of the Lecanorae, Cladoniae, Lecideae, Graphideae, Pyrenocarpeae and occasionally they are budded off from arthrosterigmata.

4. Acicular, cylindrical, bent; sometimes these are very long, measuring up to 40 µ; they are found in various Lecideae, Lecanorae, Graphideae, Pyrenocarpeae, and also in Roccella, Pilophorus and species of Stereocaulon.

5. Ellipsoid or oblong and generally very minute; they are borne on simple sterigmata and are characteristic of the genera Calicium, Chaenotheca, Lichina, Ephebe, of the small genus Glypholecia and of a few species of Lecanora and Lecidea.

In many instances there is more or less variation of form and of size in the species or even in the individual. There are no spherical spermatia.

b. Size and Structure. The shortest spermatia in any of our British lichens are those of Lichina pygmaea which are about 1·4 µ in length and the longest are those of Lecanora crassa which measure up to 39 µ. In width they vary from about 0·5 µ to 2 µ. The mature spermogonium is filled with spermatia and, generally, with a mass of mucilage that swells with moisture and secures their expulsion.

The spermatia of lichens are colourless and are provided with a cell-wall and a nucleus. The presence of a nucleus was demonstrated by MÖller[727] in the spermatia of Calicium parietinum, Opegrapha atra, Collema microphyllum, C. pulposum and C. Hildenbrandii, and by Istvanffi[728] in those of Buellia punctiformis (B. myriocarpa), Opegrapha subsiderella, Collema Hildenbrandii, Calicium trachelinum, Pertusaria communis and Arthonia communis (A. astroidea). Istvanffi made use of fresh material, fixing the spermatia with osmic acid, and in all of these very minute bodies he demonstrated the presence of a nucleus which stained readily with haematoxylin and which he has figured in the spermatia of Buellia punctiformis as an extremely small dot-like structure in the centre of the cell. On germination, as in the cell-multiplication of other plants, the nucleus leads the way. Germination is preceded by nuclear division, and each new hyphal cell of the growing mycelium receives a nucleus.

c. Germination of Spermatia (pycnidiospores). The strongest argument in favour of regarding the spermatia of lichens as male cells had always been the impossibility of inducing their germination. That difficulty had at length been overcome by MÖller[727] who cultivated them in artificial solutions, and by that means obtained germination in nine different lichen species. He therefore rejected the commonly employed terms spermatia and spermogonia and substituted pycnoconidium and pycnidia. Pycnidiospore has been however preferred as more in accordance with modern fungal terminology. His first experiment was with the “spermatia” of Buellia punctiformis (B. myriocarpa) which measure about 8-10 µ in length and about 3 µ in width, and are borne directly on the septate spermatiophores (arthrosterigmata). In a culture drop, the spore had swelled to about double its size by the second or third day, and germination had taken place at both ends, the membrane of the spore being continuous with that of the germinating tube. In a short time cross septa were formed in the hyphae which at first were very close to each other. While apical growth advanced these first formed cells increased in width to twice the original size and, in consequence, became slightly constricted at the septa. In fourteen days a circular patch of mycelium had been formed about 280 µ in diameter. The development exactly resembled that obtained from the ascospores of the same species grown in the absence of gonidia. The largest thallus obtained in either case was about 2 mm. in diameter after three months’ growth. The older hyphae had a tendency to become brownish in colour; those at the periphery remained colourless. In Opegrapha subsiderella the development, though equally successful, was very much slower. The pycnidiospores (or spermatia) have the form of minute bent rods measuring 5·7 µ × 1·5 µ. Each end of the spore produced slender hyphae about the fifth or sixth day after sowing. In four weeks, the whole length of the filament with the spore in the middle was 300 µ. In four months a patch of mycelium was formed 2 mm. in diameter. Growth was even more sluggish with the pycnidiospores of Opegrapha atra. In that species they are rod-shaped and 5-6 µ long. Germination took place on the fifth or sixth day and in fourteen days a germination tube was produced about five times the length of the spore. In four weeks the first branching was noticed and was followed by a second branching in the seventh week. In three months the mycelial growth measured 200-300 µ across.

Germination was also observed in a species of Arthonia, the spores of which had begun to grow while still in the pycnidium. The most complete results were obtained in species of Calicium: in C. parietinum the spores, which are ovoid, slightly bent, and brownish in colour, swelled to an almost globose shape and then germinated by a minute point at the junction of spore and sterigma, and also at the opposite end; very rarely a third germinating tube was formed. Growth was fairly rapid, so that in four weeks there was a loose felt of mycelium measuring about 2 cm. × 1 cm. and 1 mm. in depth. Parallel cultures were carried out with the ascospores and the results in both cases were the same; in five or six weeks small black points appeared, which gradually developed to pycnidia with mature pycnidiospores from which further cultures were obtained.

On C. trachelinum, which has a thin greyish-white thallus spreading over old trunks of trees, the pycnidia are usually abundant. Lindsay had noted two different kinds and his observation was confirmed by MÖller. The spores in one pycnidium are ovoid, measuring 2·5-3 µ × 1·5-2 µ; in the other rarer form, they are rod-shaped and 5-7 µ long. In the artificial cultures they both swelled, the rod-like spores to double their width before germination, and sometimes several tubes were put forth. Growth was slow, but of exactly the same kind from these two types of spores as from the ascospores. At the end of the second month pycnidia appeared on all the cultures, in each case producing the ovoid type of spore.

In a second paper MÖller[729] recorded the partially successful germination of the “spermatia” of Collema (Leptogium) microphyllum, the species in which Stahl had demonstrated sexual reproduction. Growth was extraordinarily slow: after a month in the culture solution the first swelling of the spermatium prior to germination took place, and some time later small processes were formed in two or three directions. In the fourth month a branched filament was formed.

MÖller’s experiments with ascospores and pycnidiospores were primarily undertaken to prove that the lichen hyphae were purely fungal and parasitic on the algae. A series of cultures were made by Hedlund[730] in order to demonstrate that the pycnidiospores were asexual reproductive bodies; they were grown in association with the lichen alga and their germination was followed up to the subsequent formation of a lichen thallus.

d. Variation in Pycnidia. On the thallus of Catillaria denigrata (Biatorina synothea) Hedlund found that there were constantly present two types of pycnidia: the one with short slightly bent spores 4-8 µ × 1·5 µ, the other with much longer bent spores 10-20 µ × 1·5 µ; there were numerous transition forms between the two kinds of spores. Germination took place by the prolongation of the spore; the hypha produced became septate and branches were soon formed. Hedlund found that frequently germination had already begun in the spores expelled from the spermogonium. In newly formed thalline areolae it was possible to trace back the mycelium to innumerable germinating spores of both types, long and short.

Lindsay had recorded more than one form of spermogonium on the same lichen thallus, the spermatia varying considerably in size; but he was most probably dealing with the mixed growth of more than one species. The observations of MÖller and Hedlund on this point are more exact, but the limits of variation would very well include the two forms found by MÖller in Calicium trachelinum; and in the different pycnidia of Catillaria denigrata Hedlund not only observed transition stages between the two kinds of spores, but the longer pycnidiospores, as he himself allows, indicated the elongation prior to germination: there is no good evidence of more than one form in any species.

F. Pycnidia with Macrospores

Tulasne[731] records the presence on the lichen thallus of “pycnidia” as well as of “spermogonia”; the former producing stylospores, larger bodies than spermatia, occasionally septate and containing oil-drops or guttulae. These spores are pyriform or ovoid in shape and are always borne at the tips of simple sporophores. He compared the pycnidia with the fungus genera Cytospora, Septoria, etc. As a rule they occur on lichens with a poorly developed thallus, on some species of Lecanora, Lecanactis, Calicium, Porina, in the family Strigulaceae and in Peltigera.

There is no morphological difference between pycnidia and spermogonia except that the spermatia of the latter are narrower; but the difference is so slight that, as Steiner has pointed out, these organs found on Lecanora piniperda, L. Sambuci and L. effusa have been described at one time as containing microconidia (spermatia), at another macroconidia (stylospores). He also regards as macrospores those of the pycnidia of Calicium trachelinum which MÖller was able to germinate so successfully, and all the more so as they were brownish in colour, true microspores or spermatia being colourless.

MÜller[732] has recorded some observations on the pycnidia and stylospores of the Strigulaceae, a family of tropical lichens inhabiting the leaves of the higher plants. On the thallus of Strigula elegans var. tremula from Madagascar and from India, he found pycnidia with stylospores of abnormal dimensions measuring 18-26 µ in length and 3 µ in width, and with 1 to 7 cross septa. In Strigula complanata var. genuina the stylospores were 2-8-septate and varied from 7-65 µ, in length, some of the spores being thus ten times longer than others, while the width remained the same. MÜller considers that in these cases the stylospore has already grown to a septate hypha while in the pycnidium. As in the pycnidiospores, described later by Hedlund, the spores had germinated by increase in length followed by septation.

The spermogonia of Strigula, which are exactly similar to the pycnidia in size and structure, produce spermatia, measuring about 3 µ × 2 µ, and it is suggested by MÜller that the stylospores may represent merely an advanced stage of development of these spermatia. Both organs were constantly associated on the same thallus; but whereas the spermogonia were abundant on the younger part of the thallus at the periphery, they were almost entirely replaced by pycnidia on the older portions near the centre, only a very few spermogonia (presumably younger pycnidial stages) being found in that region.

Lindsay[733] has described a great many different lichen pycnidia, but in many instances he must have been dealing with species of the “Fungi imperfecti” that were growing in association with the scattered granules of crustaceous lichens. There are many fungi—Discomycetes and Pyrenomycetes—parasitic on lichen thalli, and he has, in some cases, undoubtedly been describing their secondary pycnidial form of fruit, which indeed may appear far more frequently than the more perfect ascigerous form, and might easily be mistaken for the pycnidial fructification of the lichen.

G. General Survey

a. Sexual or Asexual. It has been necessary to give the preceding detailed account of these various structures—pycnidia or spermogonia—in view of the extreme importance attached to them as the possible male organs of the lichen plant, and, in giving the results obtained by different workers, the terminology employed by each one has been adopted as far as possible: those who consider them to be sexual structures call them spermogonia; those who refuse to accept that view write of them as pycnidia.

Tulasne, Nylander and others unhesitatingly accepted them as male organs without any knowledge of the female cell or of any method of fertilization. Stahl’s discovery of the trichogyne seemed to settle the whole question; but though he had evidence of copulation between the spermatium and the receptive cell or trichogyne he had no real record of any sexual process.

Many modern lichenologists reject the view that they are sexual; they regard them as secondary organs of fructification analogous to the pycnidia so abundant in the related groups of fungi. One would naturally expect these pycnidia to reappear in lichens, and it might be considered somewhat arbitrary to classify pycnidia in Sphaeropsideae as asexual reproductive organs, and then to regard the very similar structures in lichens as sexual spermogonia. It has also been pointed out that when undoubted pycnidia do occur on the lichen thallus, as in Calicium, Strigula, Peltigera, etc., they in no way differ from structures regarded as spermogonia except in the size of the pycnidiospores—and, even among these, there are transition forms. The different types of spermatia can be paralleled among the fungal pycnidiospores and the same is also true as regards the sporophores generally. Those described as arthrosterigmata by Nylander—as endosporous by Steiner—were supposed to be peculiar to lichens; but recently Laubert[734] has described a fungal pycnidium which grew on the trunk of an apple tree and in which the spores are not borne on upright sporophores but are budded off from the cells of the plectenchyma lining the pycnidium. It may be that future research will discover other such instances, though that type of sporophore is evidently of very rare occurrence among fungi.

b. Comparison with Fungi. The most obvious spermogonia among fungi with which to compare those of lichens occur in the Uredineae where they are associated with the life-cycle of a large number of rust species. They are small flask-shaped structures very much like the simpler forms of pycnidia and they produce innumerable spermatia which are budded off from the tips of simple spermatiophores. The mature spermatium has a delicate cell-wall and contains a thin layer of cytoplasm with a dense nucleus which occupies almost the whole cavity, cytological characters which, as Blackman[735] has pointed out, are characteristic of male cells and are not found in any asexual reproductive spores. If we accept Istvanffi’s[736] description and figures of the lichen spermatia as correct, their structure is wholly different: there being a very small nucleus in the centre of the cell comparable in size with those of the vegetative hyphae (Fig. 115).

Fig. 115. a, spermatia; b, hypha produced from spermatium of Buellia punctiformis Th. Fr. × 950 (after Istvanffi).

Lichen “spermatia” also differ very strikingly from the male cells of any given group of plants in their very great diversity of form and size; but the chief argument adduced by the opponents of the sexual theory is the capacity of germination that has been proved to exist in a fair number of species. It is true that germination has been induced in the spermatia of the Uredines by several research workers—by Plowright[737], Sappin-Trouffy[738] and by Brefeld[739]—who employed artificial nutritive solutions (sugar or honey), but the results obtained were not much more than the budding process of yeast cells. Brefeld also succeeded in germinating the “spermatia” of a pyrenomycetous fungus, Polystigma rubrum, one of the germinating tubes reaching a length four times that of the spore; but it is now known that all of these fungal spermatia are non-functional, either sexually or asexually, and degenerate soon after their expulsion, or even while still in the spermogonium.

c. Influence of Symbiosis. In any consideration of lichens it is constantly necessary to hark back to their origin as symbiotic organisms, and to bear in mind the influence of the composite life on their development. After germination from the spore, the lichen hypha is so dependant on its association with the alga, that, in natural conditions, though it persists without the gonidia for a time, it attains to only a rather feeble growth of mycelial filaments. In nutritive cultures, as MÖller has proved, the absence of the alga is partly compensated by the artificial food supply, and a scanty thalline growth is formed up to the stage of pycnidial fruits. Not only in pycnidia but in all the fruiting bodies of lichens, symbiosis has entailed a distinct retrogression in the reproductive importance of the spores, as compared with fungi.

In Ascomycetes, the asci constitute the overwhelming bulk of the hymenium; in most lichens, there are serried ranks of paraphyses with comparatively few asci, and the spores are often imperfectly developed. It would not therefore be surprising if the bodies claimed by MÖller and others as pycnidiospores had also lost even to a considerable extent their reproductive capacity.

d. Value in Diagnosis. Lichen spermogonia have once and again been found of value in deciding the affinity of related plants, and though there are a number of lichens in which we have no record of their occurrence, they are so constant in others, that they cannot be ignored in any true estimation of species. Nylander laid undue stress on spermogonial characters, considering them of almost higher diagnostic value than the much more important ascosporous fruit. They are, after all, subsidiary organs, and often—especially in crustaceous species—they are absent, or their relation to the species under examination is doubtful.