E. Parasitism
a. General Statement. The parasitism of Strigula complanata, an exotic lichen found on the leaves of evergreen trees, has been already described[927]; Dufrenoy[928] records an instance of hyphae from a Parmelia thallus piercing pine-needles through the stomata and causing considerable injury. Lichen hyphae have attacked and destroyed the protonemata of mosses. Cases have also been recorded of Usnea and Ramalina penetrating to the living tissue of the tree on which they grew, and there may be other similar parasitisms; but these exceptions serve to emphasize the independent symbiotic growth of lichens.
There are however some lichens belonging to widely diverse genera that have retained, or reverted to, the saprophytic or parasitic habit of their fungal ancestors, though the cases that occur are generally of lichens preying on other lichens. The conditions have been described as those of “antagonistic symbiosis” when one lichen is hurtful or fatal in its action on the other, and as “parasymbiosis” when the association does little or no injury to the host. The parasitism of fungi on lichens, though falling under a different category, in many instances exhibits features akin to parasymbiosis.
The parasitism of fungus on fungus is not unusual; there are instances of its occurrence in all the different classes. In the Phycomycetes there are genera wholly parasitic on other fungi such as Woronina and other Chytridiaceae; Piptocephalus, one of the Mucorini, is another instance. Cicinnobolus, one of the Sphaeropsideae, preys on Perisporiae; a species of Cordyceps is found on Elaphomyces, and Orbilia coccinella on Polyporus; while among Basidiomycetes, Nyctalis, an agaric, grows always on Russula.
There are few instances of lichens finding a foothold on fungi, for the simple reason that the latter are too short lived. On the perennial Polyporeae a few have been recorded by Arnold[929], but these are not described as doing damage to the host. They are mostly species of Lecidea or of allied genera. Kupfer[930] has also listed some 15 different lichens that he found on Lenzites sp.
b. Antagonistic Symbiosis. In discussing the nutrition of lichens[931] note has been taken of the extent to which some species by means of enzymes destroy the thallus of other lichens in their vicinity and then prey on the dead tissues. A constantly cited[932] example is that of Lecanora atriseda which in its early stages lives on the thallus of Rhizocarpon geographicum inhabiting mountain rocks. A detailed examination of the relationship between these two plants was made by Malme and later by Bitter[933]. Both writers found that the Lecanora thallus as it advanced caused a blackening of the Rhizocarpon areolae, the tissues of which were killed by the burrowing slender filaments of the Lecanora, easily recognized by their longer cells. The invader thereafter gradually formed its own medulla, gonidial layer and cortex right over the surface of the destroyed thallus. Lecidea insularis (L. intumescens) similarly takes possession of and destroys the thallus of Lecanora glaucoma and Malme[932] strongly suspects that Buellia verruculosa and B. aethalea may be living on the thallus of Rhizocarpon distinctum with which they are constantly associated.
Other cases of facultative parasitism have been studied by Hofmann[934], more especially three different species, Lecanora dispersa, Lecanora sp. and Parmelia hyperopta, which were found growing on the thick foliose thallus of Dermatocarpon miniatum. These grew, at first independently, on a wall along with many examples of Endocarpon on to which they spread as opportunity offered. The thallus of the latter was in all cases distorted, the area occupied by the invaders being finally killed. The attacking lichens had benefited materially by the more nutritive substratum: their apothecia were more abundant and their thallus more luxuriant. The gonidia especially had profited; they were larger, more brightly coloured, and they increased more freely. Hoffmann offers the explanation that the strain on the algae of providing organic food for the hyphal symbiont was relaxed for the time, hence their more vigorous appearance.
Arthonia subvarians is always parasitic on the apothecia of Lecanora galactina, and Almquist[935] discovered that the hymenium of the host alone is injured, the hypothecium and excipulum being left intact.
The “parasitism” of Pertusaria globulifera on Parmelia perlata and P. physodes, as described by Bitter[936], may also be included under antagonistic symbiosis. The hyphae pierce the Parmelia thallus, break it up and gradually absorb it. Chemical as well as mechanical influences are concerned in the work of destruction as both the fungus and the alga of the victim are dissolved. Lecanora tartarea already dealt with as a marauding lichen[937] over decaying vegetation may spread also to living lichens. Fruticose soil species, such as Cetraria aculeata and others, die from the base and the Lecanora gains entrance to their tissues at the decaying end which is open.
Arnold[938] speaks of these facultative parasites that have merely changed their substratum as pseudo-parasites, and he gives a list of instances of such change. In many cases it is rather the older thalli that are taken possession of, and, in nearly every case, the invader is some crustaceous species. The plants attacked are generally ground lichens or more particularly those that inhabit damp localities, such as Peltigera or Cladonia or certain bark lichens. Drifting soredia or particles of a lichen would easily take hold of the host thallus and develop in suitable conditions. To give a few of the instances observed, there have been found, by Arnold, Crombie and others:
on Peltigera canina: Callopisma cerina, Rinodina turfacea var., Bilimbia obscurata and Lecanora aurella;
on Peltigera aphthosa: Lecidea decolorans;
on Cladoniae: Bilimbia microcarpa, Bacidia Beckhausii and Urceolaria scruposa, etc.
Urceolaria (Diploschistes) has a somewhat bulky crustaceous thallus which may be almost evanescent in its semi-parasitic condition, the only gonidia retained being in the margin of the apothecia. Nylander[939] found isolated apothecia growing vigorously on Cladonia squamules.
Hue[940] describes Lecanora aspidophora f. errabunda, an Antarctic lichen, as not only a wanderer but as a “shameless robber.” It is to be seen everywhere on and about other lichens, settling small glomeruli of apothecia here and there on the thallus of Umbilicariae or between the areolae of Buelliae, and always too vigorous to be ousted from its position.
Bacidia flavovirescens has been regarded by some lichenologists[941] as a parasite on Baeomyces, but recent work by Tobler[942] seems to have proved that the bright green thallus is that of the Bacidia.
c. Parasymbiosis. There are certain lichens that are obligative parasites and pass their whole existence on an alien thallus. They may possibly have degenerated from the condition of facultative parasitism as the universal history of parasitism is one of increased dependence on the host, and of growing atrophy of the parasite, but, in the case of lichens, there is always the peculiar symbiotic condition to be considered: the parasite produces its own vigorous hyphae and normal healthy fruits, it often claims only a share of the carbohydrates manufactured by the gonidia. The host lichen is not destroyed by this parasymbiosis though the tissues are very often excited to abnormal growth by the presence of the invading organism.
Lauder Lindsay[943] was one of the first to study these “microlichens” as he called them, and he published descriptions of those he had himself observed on various hosts. He failed however to discriminate between lichens and parasitic fungi. It is only by careful research in each case that the affinity to fungi or to lichens can be determined; very frequently the whole of them, as possessing no visible thallus, have been classified with fungi, but that view ignores the symbiosis that exists between the hyphae of the parasite and the gonidia of the host.
Parasitic lichens are rather rare on gelatinous thalli; but even among these, a few instances have been recorded. Winter[944] has described a species of Leptoraphis, the perithecia of which are immersed in the thallus of Physma franconicum. The host is wholly unaffected by the presence of the parasite except for a swelling where it is situated. The foreign hyphae are easily distinguishable; they wander through the thallus of the host with their free ends in the mucilage of the gonidial groups from which they evidently extract nourishment. Species of the lichen genus Obryzum are also parasitic on gelatinous lichens.
The parasitic genus Abrothallus[945] has been the subject of frequent study. There are a number of species which occur as little black discs on various thalli of the large foliose lichens. They were first of all described as parasitic fungi, later Tulasne[946] affirmed their lichenoid nature as proved by the structure, consistence and long duration of the apothecia. Lindsay[947] wrote a monograph of the genus dealing chiefly with Abrothallus Smithii (Buellia Parmeliarum) and A. oxysporus, with their varieties and forms that occur on several different hosts. In some instances the thallus is apparently quite unaffected by the presence of Abrothallus, in others, as in Cetraria glauca, there is considerable hypertrophy produced, the portion of the thallus on which the parasites are situated showing abnormal growth in the form of swellings or pustules which may be regarded as gall-formations. Crombie[948] points this out in a note on C. glauca var. ampullacea, figured first by Dillenius, which is merely a swollen condition due to the presence of Abrothallus.
The internal structure and behaviour of Abrothallus has more recently been followed in detail by Kotte[949]. He recognized a number of different species growing on various thalli of Parmelia and Cetraria, but Abrothallus Cetrariae was the only one that produced gall-formation. The mycelium of the parasite in this instance penetrates to the medulla of the host lichen as a loose weft of hyphae which are divided into more or less elongate cells. These send out side branches, which grow towards the algal cells, and by their short-celled filaments clasp them exactly in the same way as do the normal lichen hyphae. Thus in the neighbourhood of the parasite an algal cell may be surrounded by the hyphae not only of the host, but also by those of Abrothallus. The two different hyphae can generally be distinguished by their reaction to iodine: in some cases Abrothallus hyphae take the stain, in others the host hyphae. In addition to apothecia, spermogonia or pycnidia are produced, but in one of the species examined by Kotte, Abrothallus Peyritschii on Cetraria caperata, there was no spermogonial wall formed. The hyphae also penetrate the host soredia or isidia, so that on the dispersal of these vegetative bodies the perpetuation of both organisms is secured in the new growth.
Abrothallus draws its organic food from the gonidia in the same way as the host species, and possibly the parasitic hyphae obtain also water and inorganic food along with the host hyphae. They have been traced down to the rhizinae and may even reach the hypothallus, but no injury to the host has been detected. It is a case of joint symbiosis and not of parasitism. Microscopic research has therefore justified the inclusion of these and other forms among lichens.
d. Parasymbiosis of Fungi. There occur on lichens, certain parasites classed as fungi which at an early stage are more or less parasymbionts of the host; as growth advances they may become parasitic and cause serious damage, killing the tissues on which they have settled.
Zopf[950] found several instances of such parasymbiosis in his study of fungal parasites, such as Rhymbocarpus punctiformis, a minute Discomycete which inhabits the thallus of Rhizocarpon geographicum. By means of staining reagents he was able to trace the course of the parasitic hyphae, and found that they travelled towards the gonidia and clasped them lichen-wise without damaging them, since these remained green and capable of division. At no stage was any harm caused to the host by the alien organism. Another instance he observed was that of Conida rubescens on the thallus of Rhizocarpon epipolium. By means of fine sections through the apothecia of Conida and the thallus of the host, he proved the presence of numerous gonidia in the subhymenial tissue, these being closely surrounded by the hyphae of the parasite, and entirely undamaged: they retained their green colour, and in size and form were unchanged. Zopf[951] at first described these parasites as fungi though later[951] he allows that they may represent lower forms of lichens.
Tobler[952] has added two more of these parasymbiotic species on the border line between lichens and fungi, similar to those described by Zopf. One of these, Phacopsis vulpina, belonging to the fungus family Celidiaceae, is parasitic on Letharia vulpina. The fronds of the host plant are considerably altered in form by its presence, being more branched and curly. Where the parasite settles a swelling arises filled with its hyphae, and the host gonidia almost disappear from the immediate neighbourhood, only a few “nests” being found and these very mucilaginous. These nests as well as single gonidia are surrounded by Phacopsis hyphae which have gradually displaced those of the Letharia thallus. The gonidia are excited to division and increase in number on contact with either lichen or fungus hyphae, but in the latter case the increase is more abundant owing doubtless to a more powerful chemical irritant in the fungus. As development advances, the Phacopsis hyphae multiply to the exclusion of both lichen hyphae and gonidia from the area of invasion. Finally the host cortex is split, the fungus bursts through, and the tissue beneath the parasite becomes brown and dead. Phacopsis begins as a “parasymbiont,” then becomes parasitic, and is at last saprophytic on the dead cells. The hyphae travel down into the medulla of the host and also into the soredial outgrowths, and are dispersed along with the host. The effect of Verrucula on the host thallus may also be cited[953].
Tobler gives the results of his examination of still another fungus, Karschia destructans. It becomes established on the thallus of Chaenotheca chrysocephala and its hyphae gradually penetrate down to the underlying bark (larch). The lichen thallus beneath the fungus is killed, but gonidia in the vicinity are sometimes clasped: Karschia also is thus a parasymbiont, then a parasite, and finally a saprophyte.
Elenkin[954] describes certain fungi which to some extent are parasymbionts. One of these, Conidella urceolata n. sp., grew on forms of Lecanora esculenta. The other, a stroma-forming species, had invaded the thallus of Parmelia molliuscula, where it caused gall-formation. As the growth of the gall was due to the co-operation of the lichen gonidia, the fungus must at first have been a parasymbiont. Only dead gonidia were present in the stroma; probably they had been digested by the parasite. Because of the stroma Elenkin placed the fungus in a new genus, Trematosphaeriopsis.
e. Fungi Parasitic on Lichens. A solution or extract of lichen thallus is a very advantageous medium in which to grow fungi. It is therefore not surprising that lichens are a favourite habitat for parasitic fungi. Stahl[955] has noted that the lichens themselves flourish best where there is frequent moistening by rain or dew with equally frequent drying which effectively prevents the growth of fungi. Species of Peltigera are however able to live in damp conditions: without being injured, they have been observed to maintain their vigour when cultivated in a very moist hothouse while all the other forms experimented with were attacked and finally destroyed by various fungi.
Lindsay[956] devoted a great deal of attention to the microscopic study of the minute fruiting bodies so frequently present on lichen thalli and published descriptions of microlichens, microfungi and spermogonia. He and others naturally considered these parasitic organisms to be in many cases either the spermogonia or pycnidia of the lichen itself. It is often not easy to determine their relationship or their exact systematic position; many of them are still doubtful forms.
There exists however a very large number of fully recognized parasitic microfungi belonging to various genera. Lindsay discovered many of them. Zopf[957] has given exact descriptions of a series of forms, with special reference to their effect on the host thallus. In an early paper he described a species, Pleospora collematum, that he found on Physma compactum and other Collemaceae. The hyphae of the parasite differed from those of the host in being of a yellow colour; they did not penetrate or spread far, being restricted to rhizoid-like filaments at the base of their fruiting bodies (perithecia and pycnidia). Their presence caused a slight protuberance but otherwise did no harm to the host; the Nostoc cells in their immediate vicinity were even more brightly coloured than in other parts of the thallus. In another paper[958] he gives an instance of gall-formation in Collema pulposum induced by the presence of the fungus Didymosphaeria pulposi. Small protuberances were formed on the margins of the apothecia, more rarely on the lobes of the thallus, each one the seat of a perithecium of the fungus. No damage was done to either constituent of the thallus.
Agyrium flavescens grows parasitically on the under surface of Peltigera polydactyla. M. and Mme Moreau[959] found that the hyphae of the fungus spread between the medullary filaments of the lichen; no haustoria were observed. The mature fruiting body had no distinct excipulum, but was surrounded by a layer of dead lichen cells.
It is not easy to determine the difference between parasites that are of fungal nature and those that are lichenoid; but as a general rule the fungi may be recognized by their more transient character, very frequently by their effect on the host thallus, which is more harmful than that produced by lichens, and generally by their affinity to fungi rather than to lichens. Opinions differ and will continue to differ on this very difficult question.
The number of such fungi determined and classified has gradually increased, and now extends to a very long list. Even as far back as 1896 Zopf reckoned up 800 instances of parasitism of 400 species of fungi on about 350 different lichens and many more have been added. Abbé Vouaux[960] is the latest writer on the subject, but his work is mostly a compilation of species already known. He finds representatives of these parasites in nine families of Pyrenomycetes and six of Discomycetes. He leaves out of account the much debated Coniocarps, but he includes with fungi all those that have been proved to be parasymbiotic, such as Abrothallus.
A number of fungus genera, such as Conida, etc., are parasitic only on lichens. Most of them have one host only; others, such as Tichothecium pygmaeum, live on a number of different thalli. Crustaceous species are often selected by the parasites, and no great damage, if any, is caused to these hosts, except when the fungus is seated on the disc of the apothecium, so that the spore-bearing capacity is lessened or destroyed.
In some of the larger lichens, however, harmful effects are more visible. In Lobaria pulmonaria, the fruits of which are attacked by the Discomycete, Celidium Stictarum[961], there is at first induced an increased and unusual formation of lichen apothecia. These apothecia are normally seated for the most part on the margins of the lobes or pustules, but when they are invaded by the fungus, they appear also in the hollows between the pustules and even on the under surface of the thallus. In the large majority of cases the fungus is partly or entirely embedded in the thallus; the gonidia in the vicinity may remain green and healthy, or all the tissues in the immediate neighbourhood of the parasite may be killed.
f. Mycetozoa Parasitic on Lichens. Mycetozoa live mostly on decayed wood, leaves, humus, etc. One minute species, Listerella paradoxa, always inhabits the podetia of Cladonia rangiferina. Another species, Hymenobolina parasitica, was first detected and described by Zukal[962] as a true parasite on the thallus of Physciaceae; it has since been recorded in the British Islands on Parmeliae[963]. This peculiar organism differs from other mycetozoa in that the spores on germination produce amoebae. These unite to form a rose-red plasmodium which slowly burrows into the lichen thallus and feeds on the living hyphae. It is a minute species, but when abundant the plasmodia can just be detected with the naked eye as rosy specks scattered over the surface of the lichen. Later the grey sporangia are produced on the same areas.