II. THE REPRODUCTIVE ORGANS
A. Theories of Descent in Ascolichens
It has been suggested that ascomycetous fungi, from which Ascolichens are directly derived, are allied to the Florideae, owing to the appearance of a trichogyne in the carpogonium of both groups. That organ in the red seaweeds is a long delicate cell in direct communication with the egg-cell of the carpogonium. It is a structure adapted to totally submerged conditions, and fitted to attach the floating spermatia.
In fungi there is also a structure considered as a trichogyne[981], which, in the Laboulbeniales, is a free, simple or branching organ. There is no other instance of any similar emergent cell or cells connected with the ascogonium of the Ascomycetes, though the term has been applied in these fungi to certain short hyphal branches from the ascogonium which remain embedded in the tissue. In the Ascomycetes examined all traces of emergent receptive organs, if they ever existed, have now disappeared; in some few there are possible internal survivals which never reach the surface.
In Ascolichens, on the contrary, the “trichogyne,” a septate hyphal branch extending upwards from the ascogonium, and generally reaching the open, has been demonstrated in all the different groups except, as yet, in the Coniocarpineae which have not been investigated. Its presence is a strong point in the argument of those who believe in the Floridean ancestry of the Ascomycetes. It should be clearly borne in mind that Ascolichens are evolved from the Ascomycetes: these latter stand between them and any more remote ancestry.
In the Ascomycetes, there is a recognized progression of development in the form of the sporophore from the closed perithecium of the Pyrenomycetes and possibly through the Hysteriaceae, which are partially closed, to the open ascocarp of the Discomycetes. If the fungal and lichenoid “trichogyne” is homologous with the carpogonial organ in the Florideae, then it must have been retained in all the groups of Ascomycetes as an emergent structure, and as such passed on from them to their lichen derivatives. Has that organ then disappeared from fungi since symbiosis began? There is no trace of it now, except as already stated in Laboulbeniales with which lichens are unconnected.
Were Ascolichens monophyletic in origin, one could more easily suppose that both the fungal and lichen series might have started at some early stage from a common fungal ancestor possessing a well-developed trichogyne which has persisted in lichens, but has been reduced to insignificance in fungi, while fruit development proceeded on parallel lines in both. There is no evidence that such progression has taken place among lichens; the theory of a polyphyletic origin for the different series seems to be unassailable. At the same time, there is no evidence to show in which series symbiosis started first.
It is more reasonable to accept the polyphyletic origin, as outlined above, from forms that had already lost the trichogyne, if they ever really possessed it, and to regard the lichen trichogyne as a new organ developing in lichens in response to some requirement of the deep-seated ascogonium. Its sexual function still awaits satisfactory proof, and it is wiser to withhold judgment as to the service it renders to the developing fruit.
B. Relation of Lichens to Fungi
a. Pyrenocarpineae. In Phycolichens (containing blue-green gonidia) and especially in the gelatinous forms, fructification is nearly always a more or less open apothecium. The general absence of the perithecial type is doubtless due to the gelatinous consistency of the vegetative structure; it is by the aid of moisture that the hymenial elements become turgid enough to secure the ejection of the spores through the narrow ostiole of the perithecium, and this process would be frustrated were the surrounding and enveloping thallus also gelatinous. There is only one minutely foliose or fruticose gelatinous family, the Pyrenidiaceae, in which Pyrenomycetes are established, and the gonidia, even though blue-green, have lost the gelatinous sheath and do not swell up.
In Archilichens (with bright-green gonidia), perithecial fruits occur frequently; they are nearly always simple and solitary; in only a few families with a few representatives, is there any approach to the stroma formation so marked among fungi. The single perithecium is generally semi-immersed in the thallus. It may be completely surrounded by a hyphal “entire” wall, either soft and waxy or dark coloured and somewhat carbonaceous. In numerous species the outer protective wall covers only the upper portion that projects beyond the thallus, and such a perithecium is described as “dimidiate,” a type of fruit occurring in several genera, though rare among fungi.
As to internal structure, there is a dissolution and disappearance of the paraphyses in some genera, their protective function not being so necessary in closed fruits, a character paralleled in fungi. There is a great variety of spore changes, from being minute, simple and colourless, to varied septation, general increase in size, and brown colouration. The different types may be traced to fungal ancestors with somewhat similar spores, but more generally they have developed within the lichen series. From the life of the individual it is possible to follow the course of evolution, and the spores of all species begin as simple, colourless bodies; in some genera they remain so, in others they undergo more or less change before reaching the final stage of colour or septation that marks the mature condition.
As regards direct fungal ancestors, the Pyrenocarpineae, with solitary perithecia, are nearest in fruit structure to the Mycosphaerellaceae, in which family are included several fungus genera that are parasitic on lichens such as Ticothecium, Müllerella, etc. In that family occurs also the genus Stigmatea, in which the perithecia in form and structure are very similar to dimidiate Verrucariae.
Zahlbruckner[982] has suggested as the starting point for the Verrucariaceae the fungus genus Verrucula. It was established by Steiner[983] to include two species, V. cahirensis and V. aegyptica, their perithecia being exactly similar to those of Verrucaria[984] in which genus they were originally placed. Both are parasitic on species of Caloplaca (Placodium). The former, on C. gilvella, transforms the host thallus to the appearance of a minutely lobed Placodium; the latter occupies an island-like area in the centre of the thallus of Caloplaca interveniens, and gives it, with its accompanying parasite, the character of an Endopyrenium (Dermatocarpon), while the rest of the thallus is normal and fertile.
Zahlbruckner may have argued rightly, but it is also possible to regard these rare desert species as reversions from an originally symbiotic to a purely parasitic condition. Reinke came to the conclusion that if a parasitic species were derived directly from a lichen type, then it must still rank as a lichen, a view that has a direct bearing on the question. The parallel family of Pyrenulaceae which have Trentepohlia gonidia is considered by Zahlbruckner to have originated from the fungus genus Didymella.
Compound or stromatoid fructifications occur once and again in lichen families; but, according to Wainio[985], there is no true stroma formation, only a pseudostroma resulting from adhesions and agglomerations of the thalline envelopes or from cohesions of the margins of developing fruit bodies. These pseudostromata are present in the genera Chiodecton and Glyphis (Graphidineae) and in Trypethelium, Mycoporium, etc. (Pyrenocarpineae). This view of the nature of the compound fruits is strengthened, as Wainio points out, by the presence in certain species of single apothecia or perithecia on the same specimen as the stromatoid fruits.
b. Coniocarpineae. This subseries is entirely isolated. Its peculiarity lies in the character of the mature fruit in which the spores, owing to the early breaking down of the asci, lie as a loose mass in the hymenium, while dispersal is delayed for an indefinite time. This type of fruit, termed a mazaedium by Acharius, is in the form of a stalked or sessile roundish head—the capitulum—closed at first and only half-open at maturity rarely, as in Cyphelium, an exposed disc. There is a suggestion, but only a suggestion, of a similar fructification in the tropical fungus Camillea in which there is sometimes a stalk with one or more perithecia at the tip, and in some species early disintegration of the asci, leaving spore masses[986]. But neither in fungi nor in other lichens is there any obvious connection with Coniocarpineae. In some of the genera the fungus alone forms the stalk and the wall of the capitulum; in others the thallus shares in the fruit-formation growing around it as an amphithecium.
The semi-closed fruits point to their affinity with Pyrenolichens, though they are more advanced than these judging from the thalline wall that is present in some genera and also from the half-open disc at maturity. The latter feature has influenced some systematists to classify the whole subseries among Cyclocarpineae. The thallus, as in Sphaerophorus, reaches a high degree of fruticose development; in other genera it is crustaceous without any formation of cortex, while in several genera or species it is non-existent, the fruits being parasites on the thalli of other lichens or saprophytes on dead wood, humus, etc. These latter—both parasites and saprophytes—are included by Rehm[987] and others among fungi, which has involved the breaking up of this very distinctive series. Rehm has thus published as Discomycetes the lichen genera Sphinctrina, Cyphelium, Coniocybe, Acolium, Calicium and Stenocybe, since some or all of their species are regarded by him as fungi.
Reinke[988] in his lichen studies states that it might not be impossible for a saprophytic fungus to be derived from a crustaceous lichen—a case of reversion—but that no such instance was then known. More exact studies[989] of parasymbiosis and antagonistic symbiosis have shown the wide range of possible life-conditions, and such a reversion does not seem improbable. We must also bear in mind that in suitable cultures, lichen hyphae can be grown without gonidia: they develop in that case as saprophytes.
On Reinke’s[988] view, however, that these saprophytic species, belonging to different genera in the Coniocarpineae, are true fungi, they would represent the direct and closely related ancestors of the corresponding lichen genera, giving a polyphyletic origin within this group. As fungus genera he has united them in Protocaliciaceae, and the representatives among fungi he distinguishes, as does Wainio[990], under such names as Mycocalicium and Mycoconiocybe.
If we might consider the saprophytic forms as also retrogressive lichens, a monophyletic origin from some remote fungal ancestor would prove a more satisfactory solution of the inheritance problem. This view is even supported by a comparison Reinke himself has drawn between the development of the fructification in Mycocalicium parietinum, a saprophyte, and in his view a fungus, and Chaenotheca chrysocephala, a closely allied lichen. Both grow on old timber. In the former (the fungus), the mycelium pervades the outer weathered wood-cells, and the fruit stalk rises from a clump of brownish hyphae; there is no trace of gonidia. Chaenotheca chrysocephala differs in the presence of gonidia which are associated with the mycelium in scattered granular warts; but the fruit stalk here also rises directly from the mycelium between the granules. The presence of a lichen thallus chiefly differentiates between the two plants, and this thallus is not a casual or recent association; it is constant and of great antiquity as it is richly provided with lichen-acids.
Reinke has indicated the course of evolution within the series but that is on the lines of thalline development and will be considered later.
c. Graphidineae. This series contains a considerable variety of lichen forms, but all possess to a more or less marked degree the linear form of fructification termed a “lirella” which has only a slit-like opening. There is a tendency to round discoid fruits in the Roccellae and also in the Arthoniae; the apothecia of the latter, called by early lichenologists “ardellae,” are without margins. In nearly all there is a formation of carbonaceous black tissue either in the hypothecium or in the proper margins. In some of them the paraphyses are branched and dark at the tips, the branches interlocking to form a strong protective epithecium. There are, however, constant exceptions, in some particular, to any generalization in genera and in species. Müller-Argau’s[991] pronouncement might be held to have special reference to Graphidineae: “that in any genus, species or groups of species are to be found which outwardly shew something that is peculiar, though of slight importance.” The most constant type of gonidium is Trentepohlia, but Palmella and Phycopeltis occasionally occur. The spores are various in colour and form; they are rarely simple.
The genus Arthonia is derived from a member of the Patellariaceae, from which family many of the Discomycetes have arisen. The course of development does not follow from a closed to an open fruit; the apothecium is open from the first, and growth proceeds from the centre outwards, the fertile cells gradually pushing aside the sterile tissue of the exterior. The affinity of Xylographa (with Palmella gonidia) is to be found in Stictis in the fungal family Stictidaceae, the apothecia of Stictis being at first closed, then open, and with a thick margin; Xylographa has a more elongate lirella fruit, though otherwise very similar, and has a very reduced thallus. Rehm[992] has classified Xylographa as a fungus.
The genera with linear apothecia are closely connected with Hysteriaceae, and evidently inherit their fruit form severally from that family. There is thus ample evidence of polyphyletic descent in the series. Stromatoid fruits occur in Chiodectonaceae, with deeply sunk, almost closed disc, but they have evidently evolved within the series, possibly from a dividing up of the lirellae.
In Graphidineae there are also forms, more especially in Arthoniaceae, on the border line between lichens and fungi: those with gonidia being classified as lichens, those without gonidia having been placed in corresponding genera of fungi. These latter athalline species live as parasites or saprophytes.
The larger number of genera have a poorly developed thallus; in many of them it is embedded within the outer periderm-cells of trees, and is known as “hypophloeodal.” But in some families, such as Roccellaceae, the thallus attains a very advanced form and a very high production of acids.
The conception of Graphidineae as a whole is puzzling, but one or other characteristic has brought the various members within the series. It is in this respect an epitome of the lichen class of which the different groups, with all their various origins and affinities, yet form a distinct and well-defined section of the vegetable kingdom.
d. Cyclocarpineae. This is by far the largest series of lichens. The genera are associated with algae belonging both to the Myxophyceae and the Chlorophyceae, and from the many different combinations are produced great variations in the form of the vegetative body. The fruit is an emergent, round or roundish disc or open apothecium in all the members of the series except Pertusariaceae, where it is partially immersed in thalline “warts.” In its most primitive form, described as “biatorine” or “lecideine,” it may be soft and waxy (Biatora) or hard and carbonaceous (Lecidea), in the latter the paraphyses being mostly coloured at the tips; these are either simple or but sparingly branched, so that the epithecium is a comparatively slight structure. The outer sterile tissue forms a protective wall or “proper margin” which may be entirely pushed aside, but generally persists as a distinct rim round the disc.
A great advance within the series arose when the gonidial elements of the thallus took part in fruit-formation. In that case not only is the hymenium generally subtended by a layer of algae, but thalline tissue containing algae grows up around the fruit, and forms a second wall or thalline margin. This type of apothecium, termed “lecanorine,” is thus intimately associated with the assimilating tissue and food supply, and it gains in capacity of ascus renewal and of long duration. This development from non-marginate to marginate ascomata is necessarily an accompaniment of symbiosis.
There is no doubt that the Cyclocarpineae derive from some simple form or forms of Discomycete in the Patellariaceae. The relationship between that family and the lower Lecideae is very close. Rehm[993] finds the direct ancestors of Lecidea itself in the fungus genus, Patinella, in which the apothecia are truly lecideine in character—open, flat and slightly margined, the hypothecium nearly always dark-coloured and the paraphyses branched, septate, clavate and coloured at the tips, forming a dark epithecium. More definitely still he describes Patinella atroviridis, a new species he discovered, as in all respects a Lecidea, but without gonidia.
In the crustaceous Lecideaceae, a number of genera have been delimited on spore characters—colourless or brown, and simple or variously septate. In Patellariaceae as described by Rehm are included a number of fungus genera which correspond to these lichen genera. Only two of them—Patinella and Patellaria—are saprophytic; in all the other genera of the family, the species with very few exceptions are parasitic on lichens: they are parasymbionts sharing the algal food supply; in any case, they thrive on a symbiotic thallus.
Rehm unhesitatingly derives the corresponding lichen genera from these fungi. He takes no account of the difficulty that if these parasitic (or saprophytic) fungi are primitive, they have yet appeared either later in time than the lichens on which they exist, or else in the course of ages they have entirely changed their substratum.
He has traced, for instance, the lichen, Buellia, to a saprophytic fungus species, Karschia lignyota, to a genus therefore in which most of the species are parasitic on lichens and have generally been classified as parasitic lichens. There is no advance in apothecial characters from the fungus, Karschia, to Buellia, merely the change to symbiosis. It therefore seems more in accordance with facts to regard Buellia as a genus evolved within the lichen series from Patinella through Lecidea, and to accept these species of Karschia on the border line as parasitic, or even as saprophytic, reversions from the lichen status. We may add that while these brown-spored lichens are fairly abundant, the corresponding athalline or fungus forms are comparatively few in number, which is exactly what might be expected from plants with a reversionary history.
Occasionally in biatorine or lecideine species with a slight thalline development all traces of the thallus disappear after the fructification has reached maturity. The apothecia, if on wood or humus, appear to be saprophytic and would at first sight be classified as fungi. They have undoubtedly retained the capacity to live at certain stages, or in certain conditions, as saprophytes.
The thallus disappears also in some species of the crustaceous genera that possess apothecia with a thalline margin, and the fruits may be left stranded and solitary on the normal substratum, or on some neighbouring lichen thallus where they are more or less parasitic; but as the thalline margin persists, there has been no question as to their nature and affinity.
Rehm suggests that many species now included among lichens may be ultimately proved to be fungi; but it is equally possible that the reverse may be the case, as for instance Bacidia flavovirescens, held by Rehm and others to be a parasitic fungus species, but since proved by Tobler[994] to be a true lichen.
A note by Lightfoot[995], one of our old-time botanists who gave lichens a considerable place in his Flora, foreshadows the theory of evolution by gradual advance, and his views offer a suggestive commentary on the subject under discussion. He was debating the systematic position of the maritime lichen genus Lichina, considered then a kind of Fucus, and had observed its similarity with true lichens. “The cavity,” he writes, “at the top of the fructification (in Lichina) is a proof how nearly this species of Fucus is related to the scutellated lichens. Nature disdains to be limited to the systematic rules of human invention. She never makes any sudden starts from one class or genus to another, but is regularly progressive in all her works, uniting the various links in the chain of beings by insensible connexions.”