REPRODUCTION
1. REPRODUCTION BY ASCOSPORES
A. HISTORICAL SURVEY
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_.
[Illustration: 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).
[Illustration: 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.
[Illustration: 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
[Illustration: 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.
[Illustration: 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.
[Illustration: 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).]
[Illustration: 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.
[Illustration: 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.
[Illustration: 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).
[Illustration: 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.
[Illustration: 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.
[Illustration: 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.