Part 37

The recent observations and exceedingly ingenious experiments of Falck have shown that the sporophores of the Basidiomycetes--especially the large sporophores of such forms as _Boletus_, _Polyporus_--contain quantities of reserve combustible material which are burnt up by the

## active metabolism occurring when the fruit-body is ripe. By this means

the temperature of the sporophore is raised and the difference between it and the surrounding air may be one of several degrees. As a result convection currents are produced in the air which are sufficient to catch the basidiospores in their fall and carry them, away from the regions of comparative atmospheric stillness near the ground, to the upper air where more powerful air-currents can bring about their wide distribution.

_Classification._--It has been accepted for some time now that the majority of the fungi proper fall into three main groups, the Phycomycetes, Ascomycetes and Basidiomycetes, the Schizomycetes and Myxomycetes (Mycetozoa) being considered as independent groups not coming under the true fungi.

The chief schemes of classification put forward in detail have been those of P.A. Saccardo (1882-1892), of Oskar Brefeld and Von Tavel (1892), of P.E.L. Van Tieghem (1893) and of J. Schroeter (1892). The scheme of Brefeld, which was based on the view that the Ascomycetes and Basidiomycetes were completely asexual and that these two groups had been derived from one division (Zygomycetes) of the Phycomycetes, has been very widely accepted. The recent work of the last twelve years has shown, however, that the two higher groups of fungi exhibit distinct sexuality, of either a normal or reduced type, and has also rendered very doubtful the view of the origin of these two groups from the Phycomycetes. The real difficulty of classification of the fungi lies in the polyphyletic nature of the group. There is very little doubt that the primitive fungi have been derived by degradation from the lower algae. It appears, however, that such a degradation has occurred not only once in evolution but on several occasions, so that we have in the Phycomycetes not a series of naturally related forms, but groups which have arisen perfectly independently of one another from various groups of the algae. It is also possible in the absence of satisfactory intermediate forms that the Ascomycetes and Basidiomycetes have also been derived from the algae independently of the Phycomycetes, and perhaps of one another.

A natural classification on these lines would obviously be very complicated, so that in the present state of our knowledge it will be best to retain the three main groups mentioned above, bearing in mind that the Phycomycetes especially are far from being a natural group. The following gives a tabular survey of the scheme adopted in the present article:

A. PHYCOMYCETES. Alga-like fungi with unicellular thallus and well-marked sexual organs.

CLASS I.--Oomycetes. Mycelium usually well developed, but sometimes poor or absent. Sexual reproduction by oogonia and antheridia; asexual reproduction by zoospores or conidia.

1. Monoblepharidineae. Mycelium present, antheridia with antherozoids, oogonium with single oosphere: Monoblepharidaceae.

2. Peronosporineae. Mycelium present; antheridia but no antherozoids; oogonia with one or more oospheres: Peronosporaceae, Saprolegniaceae.

3. Chytridineae. Mycelium poorly developed or absent; oogonia and antheridia (without antherozoids) known in some cases; zoospores common: Chytridiaceae. Ancylistaceae.

CLASS II.--Zygomycetes. Mycelium well developed; sexual reproduction by zygospores; asexual reproduction by sporangia and conidia.

1. Mucorineae. Sexual reproduction as above, asexual by sporangia or conidia or both: Mucoraceae. Mortierellaceae, Chaetocladiaceae, Piptocephalidaceae.

2. Entomophthorineae. Sexual reproduction typical but with sometimes inequality of the fusing gametes (gametangia ?): Entomophthoraceae.

B. HIGHER FUNGI. Fungi with segmental thallus; sexual reproduction sometimes with typical antheridia and oogonia (ascogonia) but usually much reduced.

CLASS I.--Ustilaginales. Forms with septate thallus, and reproduction by chlamydospores which on germination produce sporidia; sexuality doubtful.

CLASS II.--Ascomycetes. Thallus septate; spores developed in special type of sporangium, the ascus, the number of spores being usually eight. Sexual reproduction sometimes typical, usually reduced.

Exoascineae, Saccharomycetineae, Perisporinea, Discomycetes, Pyrenomycetes, Tuberineae, Laboulbeniineae.

CLASS III.--Basidiales. Thallus septate. Conidia (basidiospores) borne in fours on a special conidiophore, the basidium. Sexual reproduction always much reduced.

1. Uredineae. Life-history in some cases very complex and with well-marked sexual process and alternation of generations, in others much reduced; basidium (promycelium) derived usually from a thick-walled spore (teleutospore).

2. Basidiomycetes. Life-history always very simple, no well-marked alternation of generations; basidium borne directly on the mycelium.

(A) Protobasidiomycetes. Basidia septate. Auriculariaceae, Pilacreaceae, Tremellinaceae.

(B) Autobasidiomycetes. Basidia non-septate. Hymenomycetes, Gasteromycetes.

A. PHYCOMYCETES.--Most of the recent work of importance in this group deals with the cytology of sexual reproduction and of spore-formation, and the effect of external conditions on the production of reproductive organs.

_Monoblepharidaceae_ consists of a very small group of aquatic forms living on fallen twigs in ponds and ditches. Only one genus, _Monoblepharis_, can certainly be placed here, though a somewhat similar genus, _Myrioblepharis_, with a peculiar multiciliate zoospore like that of Vaucheria, is provisionally placed in the same group. _Monoblepharis_ was first described by Cornu in 1871, but from that time until 1895 when Roland Thaxter described several species from America the genus was completely lost sight of. _Monoblepharis_ has oogonia with single oospheres and antheridia developing a few amoeboid uniciliate antherozoids; these creep to the opening of the oogonium and then swim in. The resemblance between this genus and _Oedogonium_ among the algae is very striking, as is also that of _Myrioblepharis_ and _Vaucheria_.

_Peronosporaceae_ are a group of endophytic parasites--about 100 species--of great importance as comprising the agents of "damping off" disease (_Pythium_), vine-mildew (_Plasmopara_), potato disease (Phytophthora), onion-mildew (_Peronospora_). _Pythium_ is a semi-aquatic form attacking seedlings which are too plentifully supplied with water; its hyphae penetrate the cell-walls and rapidly destroy the watery tissues of the living plant; then the fungus lives in the dead remains. When the free ends of the hyphae emerge again into the air they swell up into spherical bodies which may either fall off and behave as conidia, each putting out a germ-tube and infecting the host; or the germ-tube itself swells up into a zoosporangium which develops a number of zoospores. In the rotting tissues branches of the older mycelium similarly swell up and form antheridia and oogonia (fig. 4). The contents of the antheridium are not set free, but that organ penetrates the oogonium by means of a narrow outgrowth, the fertilizing tube, and a male nucleus then passes over into the single oosphere, which at first multinucleate becomes uninucleate before fertilization. _Pythium_ is of interest as illustrating the dependence of zoospore-formation on conditions and the indeterminate nature of conidia. The other genera are more purely parasitic; the mycelium usually sends haustoria into the cells of the host and puts out branched, aerial conidiophores through the stomata, the branches of which abstrict numerous "conidia"; these either germinate directly or their contents break up into zoospores (fig. 5). The development of the "conidia" as true conidial spores or as zoosporangia may occur in one and the same species (_Cystopus candidus_, _Phytophthora infestans_) as in _Pythium_ described above; in other cases the direct conidial germination is characteristic of genera--e.g. _Peronospora_; while others emit zoospores--e.g. _Plasmopara_, &c. In _Cystopus_ (_Albugo_) the "conidia" are abstricted in basipetal chain-like series from the ends of hyphae which come to the surface in tufts and break through the epidermis as white pustules. Each "conidium" contains numerous nuclei and is really a zoosporangium, as after dispersal it breaks up into a number of zoospores. The Peronosporaceae reproduce themselves sexually by means of antheridia and oogonia as described in _Pythium_. In _Cystopus Bliti_ the oosphere contains numerous nuclei, and all the male nuclei from the antheridium pass into it, the male and female nuclei then fusing in pairs. We thus have a process of "multiple fertilization"; the oosphere really represents a large number of undifferentiated gametes and has been termed a coenogamete. Between _Cystopus Bliti_ on the one hand and _Pythium de Baryanum_ on the other a number of cytologically intermediate forms are known. The oospore on germination usually gives origin to a zoosporangium, but may form directly a germ tube which infects the host.

[Illustration: From Strasburger's _Lehrbuch der Botanik_, by permission of Gustav Fischer.

FIG. 4.--Fertilization of the Peronosporeae. After Wager.

1, _Peronospora parasitica_. Young multinucleate oogonium (og) and antheridium (an).

2, _Albugo candida_. Oogonium with the central uninucleate oosphere and the fertilizing tube (a) of the antheridium which introduces the male nucleus.

3, The same. Fertilized egg-cell (o) surrounded by the periplasm (p).]

[Illustration: FIG. 5.--_Phytophthora infestans_. Fungus of Potato Disease.

A, B, Section of Leaf of Potato with sporangiophores of _Phytophthora infestans_ passing through the stomata D, on the under surface of the leaf.

E, Sporangia.

F, G, H, J, Further development of the sporangia.

K, Germination of the zoospores formed in the sporangia.

L, M, N, Fertilization of the oogonium and development of the oospore in _Peronospora_.]

_Saprolegniaceae_ are aquatic forms found growing usually on dead insects lying in water but occasionally on living fish (e.g. the salmon disease associated with _Saprolegnia ferax_). The chief genera are _Saprolegnia, Achlya, Pythiopsis, Dictyuchus, Aplanes._ Motile zoospores which escape from the zoosporangium are present except in Aplanes. The sexual reproduction shows all transitions between forms which are normally sexual, like the Peronosporaceae, to forms in which no antheridium is developed and the oospheres develop parthenogenetically. The oogonia, unlike the Peronosporaceae, contain more than one oosphere. Klebs has shown that the development of zoosporangia or of oogonia and pollinodia respectively in _Saprolegnia_ is dependent on the external conditions; so long as a continued stream of suitable food-material is ensured the mycelium grows on without forming reproductive organs, but directly the supplies of nitrogenous and carbonaceous food fall below a certain degree of concentration sporangia are developed. Further reduction of the supplies of food effects the formation of oogonia. This explains the sequence of events in the case of a _Saprolegnia_-mycelium radiating from a dead fly in water. Those parts nearest the fly and best supplied develop barren hyphae only; in a zone at the periphery, where the products of putrefaction dissolved in the water form a dilute but easily accessible supply, the zoosporangia are developed in abundance; oogonia, however, are only formed in the depths of this radiating mycelium, where the supplies of available food materials are least abundant.

_Chytridineae._--These parasitic and minute, chiefly aquatic, forms may be looked upon as degenerate Oomycetes, since a sexual process and feeble unicellular mycelium occur in some; or they may be regarded as series of primitive forms leading up to higher members. There is no means of deciding the question. They are usually included in Oomycetes, but their simple structure, minute size, usually uniciliate zoospores, and their negative characters would justify their retention as a separate group. It contains less than 200 species, chiefly parasitic on or in algae and other water-plants or animals, of various kinds, or in other fungi, seedlings, pollen and higher plants. They are often devoid of hyphae, or put forth fine protoplasmic filaments into the cells of their hosts. After absorbing the cell-contents of the latter, which it does in a few hours or days, the fungus puts out a sporangium, the contents of which break up into numerous minute swarm-spores, usually one-ciliate, rarely two-ciliate. Any one of these soon comes to rest on a host-cell, and either pierces it and empties its contents into its cavity, where the further development occurs (_Olpidium_), or merely sends in delicate protoplasmic filaments (_Rhizophydium_) or a short hyphal tube of, at most, two or three cells, which acts as a haustorium, the further development taking place outside the cell-wall of the host (_Chytridium_). In some cases resting spores are formed inside the host (_Chytridium_), and give rise to zoosporangia on germination. In a few species a sexual process is described, consisting in the conjugation of similar cells (_Zygochytrium_) or the union of two dissimilar ones (_Polyphagus_). In the development of distinct antheridial and oogonial cells the allied Ancylistineae show close alliances to _Pythium_ and the Oomycetes. On the other hand, the uniciliate zoospores of _Polyphagus_ have slightly amoeboid movements, and in this and the pseudopodium-like nature of the protoplasmic processes, such forms suggest resemblances to the Myxomycetes. Opinions differ as to whether the Chytridineae are degraded or primitive forms, and the group still needs critical revision. Many new forms will doubtless be discovered, as they are rarely collected on account of their minuteness. Some forms cause damping off of seedlings--e.g. _Olpidium Brassicae_; others discoloured spots and even tumour-like swellings--e.g. _Synchytium Scabiosae_, _S. Succisae_, _Urophlyctis_, &c., on higher plants. Analogies have been pointed out between Chytridiaceae and unicellular algae, such as Chlorosphaeraceae, Protococcaceae, "Palmellaceae," &c., some of which are parasitic, and suggestions may be entertained as to possible origin from such algae.

The _Zygomycetes_, of which about 200 species are described, are especially important from a theoretical standpoint, since they furnished the series whence Brefeld derived the vast majority of the fungi. They are characterized especially by the zygospores, but the asexual organs (sporangia) exhibit interesting series of changes, beginning with the typical sporangium of _Mucor_ containing numerous endospores, passing to cases where, as in _Thamnidium_, these are accompanied with more numerous small sporangia (sporangioles) containing few spores, and thence to _Chaetocladium_ and _Piptocephalis_, where the sporangioles form but one spore and fall and germinate as a whole; that is to say, the monosporous sporangium has become a conidium, and Brefeld regarded these and similar series of changes as explaining the relation of ascus to conidium in higher fungi. According to his view, the ascus is in effect the sporangium with several spores, the conidium the sporangiole with but one spore, and that not loose but fused with the sporangiole wall. On this basis, with other interesting morphological comparisons, Brefeld erected his hypothesis, now untenable, that the Ascomycetes and Basidiomycetes diverge from the Zygomycetes, the former having particularly specialized the ascus (sporangial) mode of reproduction, the latter having specialized the conidial (indehiscent one-spored sporangiole) mode. In addition to sporangia and the conidial spores referred to, some Mucorini show a peculiar mode of vegetative reproduction by means of gemmae or chlamydospores--i.e. short segments of the hyphae become stored with fatty reserves and act as spores. The gemmae formed on submerged Mucors may bud like a yeast, and even bring about alcoholic fermentation in a saccharine solution.

[Illustration: From Strasburger's _Lehrbuch der Botanik_, by permission of Gustav Fischer.

FIG. 6.--_Mucor Mucedo._ Different stages in the formation and germination of the zygospore. (After Brefeld, 1-4. 5 from v. Tavel, _Pilze_.)

1, Two conjugating branches in contact.

2, Septation of the conjugating cells (a) from the suspensors (b).

3, More advanced stage, the conjugating cells (a) are still distinct from one another; the warty thickenings of their walls have commenced to form.

4, Ripe zygospore (b) between the suspensors (a).

5, Germinating zygospore with a germ-tube bearing a sporangium.]

The segments of the hyphae in this group usually contain several nuclei. At the time of sporangial formation the protoplasm with numerous nuclei streams into the swollen end of the sporangiophore and there becomes cut off by a cell-wall to form the sporangium. The protoplasm then becomes cut up by a series of clefts into a number of smaller and smaller pieces which are unicellular in _Pilobolus_, multicellular in _Sporodinia_. These then become surrounded by a cell-wall and form the spores. This mode of spore-formation is totally different from that in the ascus; hence one of the difficulties of the acceptance of Brefeld's view of the homology of ascus and sporangium. The cytology of zygospore-formation is not known in detail; the so-called gametes which fuse are multinucleate and are no doubt of the nature of gametangia. The fate of these nuclei is doubtful, probably they fuse in pairs (fig. 6).

Blakeslee has lately made some very important observations of the Zygomycetes. It is well known that while in some forms, e.g. _Spordinia_, zygospores are easily obtained, in others, e.g. most species of _Mucor_, they are very erratic in their appearance. This has now been explained by Blakeslee, who finds that the Mucorinae can be divided into two groups, termed homothallic and heterothallic respectively. In the first group zygospores can arise by the union of branches from the _same_ mycelium and so can be produced by the growth from a single spore; this group includes _Spordinia grandis_, _Spinellus fusiger_, some species of _Mucor_, &c. The majority of forms, however, fall into the heterothallic group, in which the association of branches from two mycelia _different in nature_ is necessary for the formation of zygospores. These structures cannot then be produced from the product of a single spore nor even from the thalli derived from _any_ two spores. The two kinds of thalli Blakeslee considers to have a differentiation of the nature of sex and he distinguishes them as ( + ) and (-) forms; the former being usually distinguished by a somewhat greater luxuriance of growth.

The classification of the Mucorini depends on the prevalence and characters of the conidia, and of the sporangia and zygospores--e.g. the presence or absence of a columella in the former, the formation of an investment round the latter. Most genera are saprophytes, but some--_Chaetocladium_, _Piptocephalis_--are parasites on other Mucorini, and one or two are associated casually with the rotting of tomatoes and other fruits, bulbs, &c., the fleshy parts of which are rapidly destroyed if once the hyphae gain entrance. Even more important is the question of mycosis in man and other animals, referred to species of _Mucor_, and investigated by Lucet and Costantin. Klebs has concluded that transpiration is the important factor in determining the formation of sporangia, while zygote-development depends on totally different conditions; these results have been called in question by Falck.

The _Entomophthoraceae_ contain three genera, _Empusa_, _Entomophthora_ and _Basidiobolus_. The two first genera consist of forms which are parasitic on insects. _Empusa Muscae_ causes the well-known epidemic in house-flies during the autumn; the dead, affected flies are often found attached to the window surrounded by a white halo of conidia. _B. ranarum_ is found in the alimentary canal of the frog and growing on its excrement. In these three genera the conidia are cast off with a jerk somewhat in the same way as the sporangium of _Pilobolus_.

B. HIGHER FUNGI.--Now that Brefeld's view of the origin of these forms from the Zygomycetes has been overthrown, the relationship of the higher and lower forms of fungi is left in obscurity. The term _Eumycetes_ is sometimes applied to this group to distinguish them from the Phycomycetes, but as the same name is also applied to the fungi as a whole to differentiate them from the Mycetozoa and Bacteria, the term had best be dropped. The Higher Fungi fall into three groups: the _Ustilaginales_, of doubtful position, and the two very sharply marked groups _Basidiales_ and _Ascomycetes_.

[Illustration: From Vine's _Students' Text Book of Botany_, by permission of Swan Sonnenschein & Co.

FIG. 7.--Germinating resting-gonidia. A, of _Ustilago receptaculorum_; B, of _Tilletia Caries_.

sp, The gonidium.

pm, The promycelium.

d, The sporidia: in B the sporidia have coalesced in pairs at v.]

I. _Ustilaginales._--This includes two families Ustilaginaceae (smuts) and Tilletiaceae (bunts). The bunts and smuts which damage our grain and fodder plants comprise about 400 species of internal parasites, found in all countries on herbaceous plants, and especially on Monocotyledons. They are remarkable for their dark spores developed in gall-like excrescences on the leaves, stems, &c., or in the fruits of the host. The discovery of the yeast-conidia of these fungi, and their thorough investigation by Brefeld, have thrown new lights on the group, as also have the results elucidating the nature of the ordinary dark spores--smuts, bunt, &c.--which by their mode of origin and development are chlamydospores. When the latter germinate a slender "promycelium" is put out; in _Ustilago_ and its allies this is transversely septate, and bears lateral conidia (sporidia); in _Tilletia_ and its allies non-septate, and bears a terminal tuft of conidia (sporidia) (fig. 7). Brefeld regarded the promycelium as a kind of _basidium_, bearing lateral or terminal conidia (comparable to _basidiospores_), but since the number of basidiospores is not fixed, and the basidium has not yet assumed very definite morphological characters, Brefeld termed the group _Hemibasidii_, and regarded them as a half-way stage in the evolution of the true Basidiomycetes from Phycomycetes, the _Tilletia_ type leading to the true basidium (Autobasidium), the _Ustilago_ type to the protobasidium, with lateral spores; but this view is based on very poor evidence, so that it is best to place these forms as a separate group, the _Ustilaginales_. The yeast-conidia, which bud off from the conidia or their resulting mycelium when sown in nutrient solutions, are developed in successive crops by budding exactly as in the yeast plant, but they cannot ferment sugar solutions. It is the rapid spread of these yeast-conidia in manure and soil waters which makes it so difficult to get rid of smuts, &c., in the fields, and they, like the ordinary conidia, readily infect the seedling wheat, oats, barley or other cereals. Infection in these cases occurs in the seedling at the place where root and shoot meet, and the infecting hypha having entered the plant goes on living in it and growing up with it as if it had no parasitic

## action at all. When the flowers form, however, the mycelium sends

hyphae into the young ovaries and rapidly replaces the stores of sugar and starch, &c., which would have gone to make the grain, by the soot-like mass of spores so well known as smut, &c. These spores adhere to the grain, and unless destroyed, by "steeping" or other treatment, are sown with it, and again produce sporidia and yeast-conidia which infect the seedlings. In other species the infection occurs through the style of the flower, but the fungus after reaching the ovule develops no further during that year but remains dormant in the embryo of the seed. On germination, however, the fungus behaves in the same way as one which has entered in the seedling stage. The cytology of these forms is very little known; Dangeard states that there is a fusion of two nuclei in the chlamydospore, but this requires confirmation. Apart from this observation there is no other trace of sexuality in the group.

II. _Ascomycetes._--This, except in the case of a few of the simpler forms, is a very sharply marked group characterized by a special type of sporangium, the ascus. In the development of the ascus we find two nuclei at the base which fuse together to form the single nucleus of the young _ascus_. The single nucleus divides by three successive divisions to form eight nuclei lying free in the protoplasm of the ascus. Then by a special method, described first by Harper, a mass of protoplasm is cut out round each nucleus; thus eight uninucleate ascospores are formed by free-cell formation. The protoplasm remaining over is termed _epiplasm_ and often contains glycogen (fig. 8). In some cases nuclear division is carried further before spore-formation occurs, and the number of spores is then 16, 32 and 64, &c.; in a few cases the number of spores is less than eight by abortion of some of the eight nuclei. The ascus is thus one of the most sharply characterized structures among the fungi.