UNIVERSITY OF CALIFORNIA

il

THE LIBRARY

OF

THE UNIVERSITY
OF CALIFORNIA

LOS ANGELES

Cambridge Botanical Handbooks

Edited by A. C. SEWARD and A. G. TANSLEY

FUNGI

ASCOMYCETES, USTILAGINALES, UREDINALES

6508 8

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PALEOMYCES ASTEROXYLI

from the Old Red Sandstone, Muir of Rhynie, Aberdeenshire, x 100; after
Kiclston and Lang

FUNGI

ASCOMYCETES, USTILAGINALES,
UREDINALES

BY
DAME HELEN GWYNNE-VAUGHAN,

(FORMERLY H. c. i. FRASER)
D.B.E., LL.D., D.Sc., F.L.S.

PROFESSOR OF BOTANY IN THE UNIVERSITY OF LONDON

AND
HEAD OF THE DEPARTMENT OF BOTANY, BIRKBECK COLLEGE

CAMBRIDGE

AT THE UNIVERSITY PRESS
1922

53860

PRINTED KJ GREAT BRITAIN

PREFACE

IT is impossible to study the Fungi without being impressed by the
undiminished value of much of the older work, and especially of that
of de Bary, or without recognizing the soundness of his general and very
many of his particular conclusions in the light of subsequent investigation.
While I have tried to give something approaching adequate references to
recent literature, I have thought it superfluous to name the more general
works of those earlier authors who are quoted in de Bary's Comparative
Morphology of the Fungi, Mycetozoa and Bacteria and elsewhere. By such
investigations the foundations of modern mycology have been laid and their
discoveries have passed into the groundwork of our knowledge.

The intention of the following pages is to present the fungus as a living
individual: the scope is mainly morphological, but, in dealing with objects
so minute, morphology passes insensibly into cytology. The introduction
deals with fungi in general ; the special part of this volume is limited to the
consideration of the Ascomycetes, Ustilaginales and Uredinales. The
manuscript was completed early in 1917, but an endeavour has been made
to bring it up to date.

The majority of the illustrations are drawn from published researches,
and I have to thank those authors who have given me permission to copy
their figures. Illustrations, the source of which is not stated, are original.
In the case of original figures the magnification and the authority for the
species are given ; this has also been done in other cases whenever the
information was available.

I am grateful to many past and present students for specimens and
information ; to Miss W. Page for figure 112; to Miss H. Tayler for reading
proofs; to Mr Charles Dobb for valuable help in the preparation of figures;
to Mr E. S. Salmon for advice on the section dealing with specialization of
parasitism ; and especially to my friends Miss E. J. Welsford and Mr J.
Ramsbottom for assistance in a number of ways.

The earlier written parts of the book, and consequently the whole, owe
much to the unfailing interest and wise criticism of my husband.

H. C. I. GWYNNE-VAUGHAN.

LONDON,

September, 1921

CONTENTS

INTRODUCTION

GENERAL . . ,

Vegetative Structure . .

Sexual Reproduction ......

Spores and Spore Mother-cells ....

Accessory Spores ......

Morphology of the Spore .....

Classification .......

SAPROPHYTISM, PARASITISM AND SYMBIOSIS

^SAPROPHYTISM

Saprophytes on Wood .....

Saprophytes on Soil

Coprophilous Fungi . . . .
Fungi on Fatty Substrata . . .
Fungi producing Alcoholic Fermentation .
Soot Fungi ........

PARASITISM

Facultative Parasites . . ...
Obligate Parasites

SYMBIOSIS .

Endotrophic Mycorhiza . . . ...

Exotrophic Mycorhiza .....

SPECIALIZATION OF SAPROPHYTISM AND PARASITISM
Heteroecism .......

Biological Species ......

REACTIONS TO STIMULI

Chemotropism .......

Hydrotropism .......

Aerotropism and Osmotropism ....

Phototropism .......

Phototaxis ........

Formative Influence of Light ....

Geotropism ........

ASCOMYCETES

GENERAL

The Ascospores .......

The Ascus . .

The Ascocarp .......

The Paraphyses .......

The Peridium .......

Alternation of Generations .....

Early Investigators . . . .

CONTENTS

Cytology ......... 4°

The Fusion in the Ascus . . . . . . 41

Fertilization ........ 41

Development of the Ascus ...... 42

Meiosis ......... 43

The Third Division in the Ascus .... 44

Chromosome Association ...... 45

The Theory of a Single Nuclear Fusion ... 45

The Significance of the Fusion in the Ascus . . 47

Pseudapogamy . . . . . . . . 48

Spore-Formation ....... 48

Phylogeny ......... 49

PLECTOMYCETES 55

PLECTASCALES 56

Endornycetaceae ........ 57

Saccharomycetaceae ....... 62

Gymnoascaceae ........ 66

Aspergillaceae ........ 68

Onygenaceae ........ 76

Elaphomycetaceae and Terfeziaceae .... 77

ERYSIPHALES 78

Erysiphaceae ........ 79

Perisporiaceae ........ 90

Microthyriaceae ........ 91

EXOASCALES 91

Exoascaceae ........ 93

DISCOMYCETES 95

PEZIZALES 100

Pyronemaceae ........ 101

Pezizaceae ......... 107

Ascobolaceae . . . . . . . .116

Helotiaceae and Mollisiaceae ..... 122

Celidiaceae, Patellariaceae and Cenangiaceae . . 124
Cyttariaceae . ... . . . . .125

HELVELLALES 127

Rhizinaceae . . . . . . . . .128

Helvellaceae . . . . . . . .129

Geoglossaceae . . . . . . . .131

PHACIDIALES 132

Stictaceae . . . . . . . ... 132

Phacidiaceae . . . . . . . -133

HYSTERIALES 133

TUBERALES 135

Tuberaceae . . . . . . . . 135

CONTENTS xi

PAGE

PYRENOMYCETES . 139

>HYPOCREALES . . - 143

Nectriaceae . . . . . . . . 143

Hypocreaceae . .... . . . .146

^DOTHIDEALES . . . . *. . . . .152

^SPHAERIALES . ... . . . . . 153

Chaetomiaceae . ' . . . . . . . 155

Sordariaceae . . . . . . . .156

Sphaeriaceae . . . . . . . .158

Ceratostomataceae . . . . . . 159

Amphisphaeriaceae . . . . . -159

Lophiostomataceae ....... 160

Mycosphaerellaceae ....... 160

Pleosporaceae . . . . . . . . 161

Gnomoniaceae . . . . . . . .163

Valsaceae ......... 164

Diatrypaceae ........ 165

Xylariaceae . . . . . . . . .165

*LABOULBENIALES 171

BASIDIOMYCETES ....-...'. 183

GENERAL 183

HEMIBASIDIOMYCETES 184

USTILAGINALES 184

Ustilaginaceae . . . . . f . . .188
Tilletiaceae . . . . . . . 193

PROTOBASIDIOMYCETES 196

UREDINALES 196

Spores and Sori ........ 196

Teleutospore . . . . . . .197

Basidiospore . . . . . . . .197

Spermogonium ....... 198

Aecidium 200

Uredosorus . . . . . . . . 204

Teleutosorus ....... 205

Omission of Spore Forms ...... 207

Heteroecism . . . . . . . .210

Specialization of Parasitism . . . . .211

Nuclear Division . . . . . . .211

Nuclear Association . . . . . .213

Phylogeny . . . . . . .210

Pucciniaceae . . . . . . .219

Cronartiaceae . . . . . . .219

Melampsoraceae . . . . ... . 219

Coleosporiaceae . . . . . . . . 220

GENERAL BIBLIOGRAPHY (Books dealing with several Groups)1 222

INDEX . . .... . . . . . . . . 223

1 Books and papers dealing with individual fungi or groups of fungi are cited in the Bibliography
at the end of the relevant section or in foot-notes in the text.

CHAPTER I
INTRODUCTION

The Fungi are parasitic or saprophytic Thallophyta entirely destitute of
chlorophyll, and possessing in the very large majority of cases a vegetative
portion, the mycelium, made up of filaments or hyphae. The group is a very
ancient one, the earliest known undoubted fungi occurring among the remains
of Rhynia and Hornia in the Old Red Sandstone of the Muir of Rhynie,
Aberdeenshire. This material consists of aseptate hyphae and vesicles which
doubtless served the purpose of reproduction (frontispiece)1.

Fungal hyphae may be non-septate and coenocytic, or they may under-
go transverse septation, in which case their constituent cells are either uni-
nucleate or multinucleate. Any division other than transverse is extremely
rare; it occurs, for example, in the development of certain multicellular
(muriform) spores (fig. I ), and in the initiation of the perithecium in Strickeria
and of the pycnidium in Pleospora and Phoma*.

As a rule the hyphae are richly branched ; they elongate by apical growth
and usually spread loosely through the substratum ; in certain cases, especially
in relation to the fructifications of the higher forms, they become woven
into a dense mass which gives in section the appearance of a tissue, and
is therefore described as pseudoparenchymatous; when fructifications are
embedded in such a mass it is termed a stroma; a similar weft of hyphae
sometimes give rise to root-like strands of which the best example is the so-
called rhizomorph of Armillaria mellea, or to a compact resting body or
sclerotium the outer cells of which are modified to form a thick-walled rind,
protecting the vegetative mycelium against desiccation.

Frequent anastomoses take place between hyphae, either by means of
short branches forming loops, bridges or H-pieces, or by means of so-called
clamp-connections which join adjacent cells; such arrangements facilitate
the passage of food and may, in certain cases, become sufficiently numerous
to form a net-work.

The mycelium begins its development as a germ-tube put out from one •
of the numerous types of fungal spore. Where the spore wall is very thin
the wall of the germ-tube may be continuous with it (zoospores), but in the
majority of cases the wall of the germ-tube is continuous only with the

1 Kidston, R. and Lang, W. H. On Old Red Sandstone Plants showing Structure from the Rhynie
Chert Bed, Aberdeenshire, Trans. Roy. Soc. Ed. 1921.

2 Kempton, F. E. Origin and Development of the Pycnidium, Bot. Gaz. 1919, Ixviii, p. 233.

2 INTRODUCTION [CH.

inner layer of the spore wall. In such cases one or more germ-tubes may
break through the wall of the spore at spots not previously recognizable, or
they may find an exit through special pits or germ-pores formed during
the development of the spore. The germ-tube elongates and receives the
contents of the spore.

In cases where a mycelium is not developed the plant body consists
entirely of reproductive structures (Yeast, Archimycetes).

The typical fungal protoplast consists of a mass of granular or reticulate
cytoplasm, which in the older regions leaves a vacuole in the centre of the
cell or filament; the nucleus, where its size has permitted of detailed in-
vestigation, has a structure quite similar to that of other plants and animals,
and usually divides by mitosis, showing a well-marked spindle with cen-
trosomes and asters. The development of the spindle is extranuclear in
certain Uredinales. One or more nucleoli are commonly present and are
thrown out into the cytoplasm during karyokinesis. The extrusion of chro-
matin bodies has been described in Helvetia crispa.

The cell wall consists of cellulose; often a special variety known as
fungus cellulose is present. The storage materials include amylo-dextrin
or soluble starch, amyloid, a reserve-cellulose, both of which turn blue with
iodine; oil, glycogen, and various protein substances. The protoplasm gives
rise also to a number of ferments which not only enable the plant to deal
with its food materials, but bring into solution the walls of the host cells,
and so make possible the penetration of parasitic hyphae.

Sexual reproduction among the fungi takes place by the union of two
uninucleate or multinucleate cells which may be similar in structure and
behaviour, or may be differentiated as an antheridium and an oogonium.
Each of these organs contains one or more distinct gametes, or else a number
of gametes which do not become rounded off from one another or separated
from the wall of the parent cell, but are indicated by separate nuclei lying
in an undifferentiated mass of cytoplasm. To organs of the latter type the
term coenogamete is sometimes applied in recognition of their multinucleate
character; it is, however, inappropriate, since they are not gametes, but
gametangia. In the vast majority of fungi free swimming gametes are not
developed ; the sole exceptions are found in the genus Monoblepharis, where
uniciliate or biciliate spermatozoids are set free and swim to the female
organ.

A state of affairs in which the antheridium as a whole must grow or be
carried to the oogonium involves a risk that normal fusion will fail to occur,
while at the same time the presence of multinucleate sexual organs and of
vegetative cells between which anastomoses readily occur offers considerable
opportunities for some form of "reduced" fertilization. The replacement of
normal fertilization by the fusion of two female or two vegetative nuclei, or

I] GENERAL CHARACTERS OF THE FUNGI 3

of a female and a vegetative nucleus, is very common among fungi, and a
complete disappearance of even this reminiscence of a sexual process is by
no means rare. It has been suggested that the variety of food material which
fungi as parasites and saprophytes obtain from their substratum may make
the stimulus of fertilization less important, and it is possible also that among
these plants competition is less severe than among holophyta or holozoa.
At any rate the group shows a progressive disappearance of normal
sexuality.

The sexual fusion or its equivalent is followed in all investigated cases
by a reducing division or meiotic phase, so that, as in other plants or
animals, the number of chromosomes is doubled in fertilization and sub-
sequently halved in meiosis, and diploid1 and haploid phases follow one
another.

The meiotic phase is usually associated with spore-formation which, in
many of the lower fungi, takes place on the germination of the zygote. In
a much greater number of cases a period of vegetative development inter-
venes between the association of the nuclei in fertilization or otherwise and
chromosome reduction, and we have a well-marked alternation of generations
in which a haploid gametophyte bears the sexual cells or their equivalent,
and a diploid sporophyte gives rise to spores which in turn constitute the first
stage of a new gametophytic generation. It is not at all uncommon to find
several sporophytes arisingfrom a single gametophyte, and the gametophytic
mycelium frequently sends out branches which grow around and protect the
sexual cells and their products. Where fertilization or any equivalent process
has wholly disappeared we may expect to find a similar morphological
alternation of generations, though without the corresponding cytological
changes; but in some cases, as in the large group of Fungi imperfecti, a
sporophyte is no longer developed, or at any rate has not been identified.

Spores and Spore mother-cells. In the higher fungi the characteristic
spores of the sporophyte, with the development of which meiosis is definitely
associated, may be produced either endogenously as ascopores in a mother-
cell of definitely restricted size termed an ascus, or exogenously as basidio-
spores on the exterior of a cell or row of cells known as a basidium. The
asci or basidia are frequently arranged in parallel series forming a fertile
layer or hymenium sometimes of considerable extent. They arise from a
sub-hymenial layer immediately below the hymenium, and among them
are interpolated elongated vegetative cells or paraphyses, which are probably
concerned in their nutrition and perhaps assist spore dispersal by keeping
the mother-cells separate. The ascus and basidium and their products have
long been recognized as essential features in classification.

1 The diploid unit may be defined as a protoplast the nuclear content of which includes the
double number of chromosomes.

4 INTRODUCTION [CH.

In the lower fungi, spore formation may be associated with the meiotic
phase, but the spores produced resemble those concerned in the accessory
methods of reproduction.

Accessory spores. The accessory or non-sexual methods of repro-
duction have no relation to any sexual process either normal or reduced,
and therefore no significance in the alternation of generations; they are
devices for rapid multiplication comparable with the gemmae in Marchantia
or the arrangements for vegetative propagation in higher plants. The spores
concerned may be borne either on the sporophyte (rusts, etc.) or, as in the
majority of cases, on the gametophyte.

In many of the lower fungi zoospores are developed in spherical, ovoid
or tubular zoosporangia ; this is the case especially in aquatic forms. In
relation to the change from aquatic to subaerial conditions the contents of
the sporangium may come to be shed as walled non-motile spores, or the
sporangium may itself be set free without division of its contents. Such a
structure, borne externally on its parent hypha, is termed a conidium, and
is the characteristic accessory reproductive unit of the fungi. In the large
majority of cases the conidium germinates by means of a germ-tube, but
where the fungus has not completely abandoned its aquatic habit the
conidium, if it falls in wet conditions, may give rise to zoospores either in-
ternally or in a vesicle borne on a short hypha. The conidia are developed
either singly or in groups on conidiophores; these may be free, they may
be gathered into a sheaf or coremium, or they may be formed inside a
special flask-shaped receptacle known as a pycnidium; they show an almost
endless variety in form and arrangement.

A less common reproductive cell is the chlamydospore; these are borne
either singly or in chains in the course of the ordinary vegetative hyphae or
at the ends of special branches ; they are characterized, as their name im-
plies, by an exceptionally thick wall.

In certain species and under certain conditions whole hyphae may break
up into series of separate cylindrical cells or spores. Such a spore is termed an
oidium. Oidium-formation appears to be a rapid and efficient method of
multiplication and is the only one found in the fungi of such diseases as
favus (Achorion Schoenleinii\ pityriasis versicolor (Microsporon furfur}
and thrush (Manilla albicans}.

In these cases attempts to cultivate any more characteristic fructification
have failed, and the fungus cannot therefore be assigned to any particular
group.

Morphology of the spore. The individual spore whether belonging to
the principal or accessory fructification is, when first formed a hyaline
colourless cell; in the course of development it may divide to produce
a row or a mass of cells and in the latter case is described as muriform •

i] GENERAL CHARACTERS OF THE FUNGI 5

it may also become variously coloured. In the large majority of cases the
spore is enclosed by a double wall consisting of a delicate endospore and
an epispore which may be smooth or variously sculptured; it may develop
small projections and is then said to be warted or verrucose, or it may be
reticulate, exhibiting a number of more or less regular polygonal depressions
between which anastomosing ridges are present.

Many conidia and other thin walled fungal spores possess the power,
in suitable media, of budding or sprouting; giving rise, that is to say,
to new cells as simple lateral outgrowths which are soon nipped off. This
method of propagation is shown in the conidia of the yeasts, in some of
which it has wholly superseded the development of a mycelium. Asco-
spores are found to bud in the Exoascaceae, and basidiospores in the
Ustilaginales.

Classification. The fungi are divided into three great groups according
to the septation of their mycelium, and the characters of their principal
spores.

FUNGI

/eo-etative mycelium vegetative mycelium
aseptate septate

I ~1

characteristic spores characteristic spores

endogenous, ascospores exogenous, basidiospores

PHYCOMYCETES ASCOMYCETES BASIDIOMYCETES

They may be further subdivided as follows:

PHYCOMYCETES

I

P

n

mycelium rudimentary mycelium well

or obsolete deve oped

sexual reproduction by sexual reproduction by

oospo.es ; asexual zygospores ; asexual

spores often motile spores non-

Archimycetes Oo^ycetes ,^^^

I'.

INTRODUCTION

[CH.

ascocarp, if present,

either with no definite

ostiole, or shield-shaped,

or with asci irregularly

arranged

Plectomyietes

1. Plectascales

2. Erysiphales

3. Exoascales

ASCOMYCETES

1

ascocarp wide open

when ripe ; asci in

parallel rows

Discomyeetes

1. Pezizales

2. Helvellales

3. Phacidiales

4. Hysteriales

5. Tuberales

ascocarp flask-shaped ;

opening by an ostiole

when ripe ; asci in

parallel rows

Pyrenovtycetes

1. Hypocreales

2. Dothideales

3. Sphaeriales

4. Laboulbeniales

number of basidiospores
indefinite

Hemibasidiomycetes

I. Ustilaginales

BASIDIOMYCETES

number of basidiospores
definite, usually four

r

basidium septate
Protobasidiomycetes
i. Uredinales
2. Auriculariales
3. Tremellales

1
basidium continuous
A utobasidiomycetes
i. Hymenomycetes
2. Gasteromycetes

SAPROPHYTISM, PARASITISM AND SYMBIOSIS

Since fungi under no circumstances possess chlorophyll, they are neces-
sarily dependent for their food supply upon some sort of relation with another
organism. As saprophytes they may utilize organic storage materials
(sugar, etc.) or waste products, or may break up dead tissues as a source of
supply; as parasites they may prey upon living cells with consequences to
the host that vary from trifling inconvenience to complete destruction, or as
symbionts they may establish a relationship with another organism in
which the advantages are not wholly on one side.

These various arrangements are connected by intermediate forms, and
by forms capable of parasitism or saprophytism according to circumstances.
A species which is strictly limited to one type of nutrition is an obligate
saprophyte, parasite, or symbiont, a species which is usually saprophytic
but capable of parasitic existence on occasion, is described as a hemi-
saprophyte or facultative parasite, and a form which is usually parasitic,
but sometimes saprophytic as a hemi-parasite, or facultative saprophyte.

I] SAPROPHYTISM

SAPROPHYTISM

According to our present knowledge the large majority of fungi are
saprophytic; a considerable proportion of forms in each of the great groups
and especially a very large number of the Basidiomycetes obtain their
nutrition in this way.

On Wood. Ascomycetes and Basidiomycetes are important agents in
the breaking up of wood; their hyphae absorb the starch and protoplasm
of the unaltered cells of the wood and medullary rays and penetrate into the
fibres, vessels and tracheids, either passing through the pits and especially
the bordered pits, or penetrating the walls. They act upon the walls so that
these become delignified and give characteristic cellulose reactions and the
middle lamella is dissolved. The enzyme responsible for this change was
first isolated by Czapek in the case of Meruliits lacrymans, the fungus of
dry rot. Its action seems to spread in a plane parallel to the surface of the
wall either from the pits, which thus become much enlarged, or from the
delicate passages left by the protoplasmic connections which originally
traversed the walls of the young wood elements. The whole mass of wood
loses weight and may reach the easily broken and almost powdery condition
known as touch-wood. In this way considerable damage may be done to
timbers (dry rot, Merulius lacrymans), paving blocks (Lentinus lepideus), etc.,
but also considerable advantage may ensue from the restoration to the soil
of the material of fallen tree trunks, twigs and branches.

The part played by the higher fungi is here specially important as almost
the only other agents of destruction of lignified tissues seem to be certain
molluscs and Crustacea which act by boring into the wood.

On Soil. Yeasts and filamentous fungi are abundant in woodland soils
and they are also of frequent occurrence in cultivated soil; the microscopic
forms show a remarkable similarity in different localities; even in Europe and
America the same genera and often the same species are obtained ; in culture
there is a regular succession of forms, first the Mucoraceae, then Penicillium
and Eurotium and later the black and brown Hyphomycetes. A large
number of Basidiomycetes also develop in the soil.

The fungi of the soil utilize the sugar, starch, pectose and hemi-cellulose^
which are returned to the ground in dead plants and plant organs, and, in_
common with certain bacteria, they act upon cellulose, breaking it up into_
soluble substances and humus. In several cases evidence has been brought
forward that some of these fungi are capable of assimilating free nitrogen
but negative results have also been very common.

The activity of these fungi is well exemplified by the "fairy-rings" ,»f
dark green grass often seen in poor pastures. The soil Just outside the rin£
is rich in the mycelium of one or two common fungi; few hyphae are foun<J

8 INTRODUCTION [CH.

under the ring itself and none in the area enclosed by it. The ring is depen-
dent upon the growth of the fungus which spreads outwards in all directions,
from the centre, the mycelium dying off as the food materials in the soil are,
exhausted; in the transition region, where the fungal hyphae themselves are
disintegrating, the soil is in high condition, it contains organic residues recently
formed" and capable of rapid change and the grass is especially luxuriant;,'
the ring accordingly is just inside the region of maximum fungal activity. '

A certain number of fungi belonging to theTuberales, Elaphomycetaceae,
Terfeziaceae and Hymenogasteraceae are completely subterranean or
hypogeal in their development. They produce closed fructifications. pro-
tected by a stout wall of interwoven hyphae. As the spores approach
maturity the fructifications develop a strong scent, varying much in character
and from the human standpoint either pleasant or disagreeable, which serves
to attract animals and especially rodents. The fructification is eaten and
the spores pass uninjured through the alimentary canal, and are thus dis-
tributed. The truffles (Tuber spp.) are the best known of these forms.

Coprophilous Fungi. Fungi feeding on organic remains in the soil often
benefit by the presence of natural manures and incidentally help to break
up these substances so that they become available for the higher plants.

From such fungi it is no great transition to the extensive coprophilous
flora of which the habitat is the dung of various animals and especially of
herbivorous species. In addition to the rich nitrogenous food supply which
these fungi obtain, the presence of cellulose in the straw and other vegetable
debris in the dung is an important factor in their nutrition^ This is well
shown by the fact that many coprophilous species fail to fruit in artificial
culture of dung decoction and agar, unless they are provided with cellulose.
Cotton wool or pieces of filter paper laid on the substratum admirably serve
this purpose; the latter are soon broken into small flocculent scraps. In
nature Zygomycetes, Ascomycetes and Basidiomycetes succeed each other
in fairly regular order and, speaking generally, show very similar adaptations
to their habitat. In many Ascomycetes (Ascobolaceae, Sordariaceae) the
spores are surrounded by mucilage and form together a projectile which
owing to its weight can be shot to a much greater distance than would be
possible for single spores. The sudden ejection of the spore mass seems to
depend on the absorption of water by the mucilaginous contents of the
ascus. After ejection the mass dries up and becomes firmly attached to the
substratum on which it has fallen. In the same way the spores in the
sporangium of Pilobolus are surrounded by a gelatinous envelope which
swells in the presence of water and bursts the sporangium wall, so that the
whole sporangium is shot off as a single mass and adheres by means of the
gelatinous layer to the body against which it strikes.

The grass surrounding the dung receives an ample supply of spores and

I] SAPROPHYTISM 9

spore masses; later, if it is eaten by some herbivorous animal, the spores
pass uninjured through the alimentary canal and germinate while still in the
intestine or on being ejected with the dung. In some cases the wall of the
spore seems to have become so effectually adapted to resist injury during
its passage through the animal that it is incapable of either stretching or
cracking as a preliminary to germination except after digestion or some
other special treatment.

Thus de Bary succeeded in germinating spores of species Pilobolus and
Mucor in water and those of Sordaria and Coprimes in nutrient solution, by
exposing them to a temperature between 35° and 40° C; Massee and Salmon
obtained germination in the spores of A scobolus perplexans, and A. glaber,
after about 20 hours in either tap water or dung decoction, at a temperature
of about 27° C. ; I found that spores otLachnea stercorea germinated in an alka-
line medium (preferably dung decoction) after incubation for several hours
at 38° C. (the temperature of the body of the cow), and Welsford succeeded
by the same means in germinating the spores of A scobolus furfuraceus, and
Cutting those of Ascophanus carneus. Ramlow, however, describes the ger-
mination of spores of the last named species at room temperature in twenty-
four hours. Further, Dodge was able to germinate the spores of several
Ascobolaceae on dung agar by exposing them for 5 or 10 minutes to a
temperature of 50° to 70° C., and Ramlow germinated those of Ascobolus
immersus by sowing them on agar which was still hot after sterilization. In
certain cases the action of direct sunlight was found by Dodge sufficient to
induce a moderate percentage of germinations and to raise the temperature
of the liquid containing the spores to about 50° C. in half an hour.

Finally, as I am informed by Mr Ramsbottom, germination may be in-
duced mechanically by cracking or breaking the epispore, for example by
rubbing the spores between two coverslips, so that all the above methods
are a mere variety of means towards this end.

In the case of Lachnea stercorea, spores incubated for 18 to 40 hours,
either in a succession of digestive fluids, or in dung extract, only germinated
approximately 50 hours after the beginning of the experiment. It is probable
that they do so in nature about two days after being swallowed. In Asco-
phanus carneus, also common on cow dung, germination is much more rapid,
taking place under similar circumstances in a single night, so that the spores
under natural conditions may be inferred to germinate while actually in the ,
intestine. Further development, however, is in all cases dependent upon the
fungus reaching the exterior of the mass of dung.

In Coprinus sterquilinus, Baden found that not only warmth and an alka- [
\ line medium (aqueous extract of horse dung), but the presence of certain
j bacteria also was necessary for germination. Appropriate bacteria may
Sometimes be a factor in the development of the ascocarp (Molliard) and

INTRODUCTION [CH-

there are many ideations that certain fungi gro* ^er in impure than^in

that spores of Ascobolus Winteri failed to germinate on the agar i,
^Tr r^^^anT^^Baaen found that the presence of
bacteria prevented the germination of the spores. It may be worth con-
sidering whether the progressive development of bacteria in the dung may
be a factor in the succession of fungi which appear on it.

Another factor of some importance in the development of coprophilous
and perhaps of other fungi is the action of direct sunlight. Cultures which
remain sterile in a darkened room can often be induced to fruit by placing
them in a sunny window; reference has already been made to the occasional
action of sunlight on spores. Many coprophilous fungi are moreover pos
tively heliotropic; this is well shown by the sporangiophores of Pilobolus
and the perithecia of Sordaria and its allies. The ejection of the spores into
an open space is in this way ensured.

Fungi on Fatty Substrata. It is probable that all or most fungi are
able to utilize fats and oils; such substances are a common form of food
reserve in the spores (zoospores, oospores, uredospores, etc.), in the mycelium,
and especially in the sclerotia where, in the case of Claviceps purpurea, the
proportion of fat reaches as much as 35 per cent.; in several cases the fat-
splitting enzyme, lipase, has been extracted.

It is therefore not surprising that many fungi grow readily on a fatty
substratum, some, such as Empusa and species of Cordyceps, on animal re-
mains, some on other fungi and some on oil-containing fruits and seeds
and on cotton, rape and other oil-cakes which are made from the waste re-
maining after such seeds have been crushed ; they may reduce the oil content
of the cake from over 10 per cent, to between I and 2 per cent, in two years.
Eurotium zn&Penirillium occur on the layer of sweet oil placed over bottled
fruits to prevent decomposition and together with other genera are concerned
in the " ripening " of cheese. The related Monascus heterosporus does con-
siderable damage in parts of Australia and New Zealand if it is allowed to
get a footing on stored tallow.

Fungi producing alcoholic Fermentation. A number of fungi obtain
nutriment from solutions consisting largely of soluble carbohydrates and
they may also obtain energy by directly breaking up certain of these sub-
stances without the intervention of oxygen and with the formation of ethyl
alcohol, carbon dioxide and small quantities of other substances. This reaction
is due to the presence of the enzyme zymase and is known as alcoholic
fermentation.

!] SAPROPHYTISM n

In its simplest possible form it may be represented by the equation:

Only certain monosaccharides with the formula C6Hi2O6 (glucose, fructose)
are capable of undergoing alcoholic fermentation; polysaccharides (cane-
sugar, lactose, maltose) must undergo a preliminary hydrolysis resulting in
the production of appropriate monosaccharides before alcoholic fermentation
can take place.

The majority of the fungi capable of inducing these changes are yeasts
(Saccharomycetaceae) acting either alone or in conjunction with appropriate
bacteria; they are very commonly present as epiphytes on the skin of ripe
fruits and feed on the drops of sugary solution that may be exuded or escape
where the skin is broken. At other times, even in the winter, they may be
found in the neighbouring soil, but they are very rarely present upon unripe
fruits, presumably because any cells that happen to be carried there soon die.

A number of yeasts are made use of economically in baking, where their
value depends on the formation of carbon dioxide, causing the dough to "rise,"
as well as in brewing and the other processes concerned with the production
of alcohol. The characteristic yeast of wine which ferments glucose (or grape-
sugar)is found in abundance at vintage time on the grapes and their stalks, and
the cider yeasts on apples ; the yeast of beer on the other hand, which acts
on the sugar formed in germinating barley, is not known in the wild state.

In the production of a number of alcoholic beverages the yeast acts sym-
biotically with one or more bacteria ; this is the case in the group of organisms
included in the "ginger-beer plant"1 which, added to commercial ginger,
sugar and water, causes the formation of ginger-beer. The "plant" has the
appearance of lumpy irregular masses rather like pieces of soaked tapioca
or sago; its essential constituents, as Marshall Ward demonstrated in 1892,
are the yeast Saccharomyces pyreformis and the bacterium B. vermiforme;
the bacterium is able to utilize the products of the metabolism of the yeast,
and can do so most successfully at their first formation, that is, in the
neighbourhood of the living yeast cell ; the yeast benefits by the removal of
these substances, the accumulation of which would inhibit its development,
and is able, in the presence of the bacterium (and of appropriate food
materials), to continue its activity for weeks as shown by the evolution of
carbon dioxide. The relation between the two organisms is thus a symbiosis
in which each constituent gains by its association with the other.

A similar combination appears to exist in the materials used for two
different fermentations of lactose or milksugar which underlie the productions
of the beverages known as kephir and koumiss. Kephir is prepared from

1 The ginger-beer plant is also known as Californian bees and by other popular names ; both
lately and after the Crimean War a tradition arose that it had been brought to this country by
soldiers from overseas. Cf. J. Ramsbottom, Trans. Brit. Myc. Soc. 1920, p. 86.

[2

INTRODUCTION tCH-

ws' milk in the Caucasus, and koumiss from mares' milk in South Western
Siber" In I both these cases the formation of alcohol depends on the yeast,
md that of lactic acid is due to bacterial activity.

^different type of association is found in the preparation of the Japanese
rice^vt! or sake! Here the starch of the rice is hydrolysed by Euro***
Oryzae and the resultant sugar is fermented by a yeast

In other cases zymase is secreted by filamentous fungi such as RJnzopus
nigricans, Penidllium glaucum, and Eurotium nigrum. Mucor racemosus^
certain other species when cultivated in sugar solution form ovoid cells which
multiply by budding and cause active fermentation.

Soot Fungi. The soot fungi (Meliola, Capnodium, etc.), like the wild
yeasts are epiphytic saprophytes; they occur on leaves frequented by green
fly and obtain their food from the "honey-dew" excreted by these insects
Their mycelium grows rapidly and forms a sooty coating on the leaves ol
the host, but does not become thick enough to injure them by excluding light.

SAPROPHYTISM: BIBLIOGRAPHY

1892 WARD, H. MARSHALL. The Ginger-Beer Plant and the Organisms composing it.
Phil. Trans, clxxxiii, p. 125.

1895 KLOCKER, A. and SCHIONNING, H. Experimented Untersuchungen uber die
vermeintliche Umbildung des Aspergillus oryzae in einem Saccharomyceten.
Centralbl. fur Bakt. Abt. ii; i, P- 777-

1896 KLOCKER, A. and SCHIONNING, H. Experimented Untersuchungen uber die
vermeintliche Umbildung verschiedenen Schimmelpilze in Saccharomyceten. Cen-
tralbl. fur Bakt. Abt. ii; ii, p. 185.

1897 WARD, H. MARSHALL. On the Biology of Stereum hirsutum. Phil. Trans, clxxxix,
p. 123.

1898 WARD, H. MARSHALL. Penicillium as a Wood-destroying Fungus. Ann. Bot. xii,
p. 565.

1899 BIFFEN, R. H. A Fat-destroying Fungus. Ann. Bot. xiii, p. 363.

1899 CZAPEK, F. Zur Biologic der holzbewohnenden Pilze. Ber. deut. bot. Ges. xvii,

p. 1 66.

1901 BIFFEN, R. H. On the Biology of Bulgaria polymorpha, Wett. Ann. Bot. xv, p. 119.
1901 GREEN, J. REYNOLDS. The Soluble Ferments and Fermentation. Cambridge

Univ. Press.

1901 MASSEE, G. and SALMON, E. S. Researches on Coprophilous Fungi. AnivBot. xv,

P- 3i3-

1902 VON SCHRENK, H. Decay of Timber and the Means of Preventing it. U.S. Dept.
of Agr. Bureau of Plant Industry. Bull. 14, New York.

1903 MOLLIARD, M. Sur une Condition qui favorise la Production des Pe'ritheces chez
les Ascobolus. Bull. Soc. Myc. Fr. xix, p. 150.

1905 BULLER, A. H. R. The Destruction of Wooden Paving Blocks by the Fungus
Lentinus lepideus, Fr. Journ. Econ. Biol. i, p. I.

1906 BULLER, A. H. R. Polyporus squamosus as a Timber destroying Fungus. Journ.
Econ. Biol. i, p. 101.

1907 FRASER, H. C. I. On the Sexuality and Development of the Ascocarp in Lachnea
stercorea, Pers. Ann. Bot. xxi, p. 349.

1907 \VELSFORD, E. J. Fertilization in Ascobolus furfuraceus. New Phyt. vi, p. 136.

J] PARASITISM ,3

1909 BULLER, A. H. R. Researches on Fungi. Longmans, Green & Co, London
1909 BULLER, A. H. R. The Destruction of Wood by Fungi. Sci Prog xi p i '
1909 CUTTING, E. M. On the Sexuality and Development of the Ascocarp in Ascothanus

carneus. Ann. Bot. xxiii, p. 399.
1912 DALE, E. On the Fungi of the Soil. Ann. Myc. x, p. 452.

1912 DODGE, B. O. Methods of Culture and the Morphology of the Archicarp in Certain
Species of the Ascobolaceae. Bull. Torrey Bot. Club, xxxix, p. 139.

1913 GODDARD, H. N. Can Fungi living in Agricultural Soil Assimilate free Nitrogen?
Bot. Gaz. Ivi, p. 249.

1913 MCBETH, I. G/and SCALES, F. M. Destruction of Cellulose by Bacteria and Fungi
U.S. Dept. of Agr. Bureau of Plant Industry. Bull. 266, New York.

1914 RAMLOW, G. Beitrage zur Entwicklungsgeschichte der Ascoboleen. Myc. Centralbl
v, P- 537-

1915 BADEN, M. L. Observations on the Germination of the Spores of Coprinus ster-
quilinus, Fr. Ann. Bot. xxix, p. 135.

1915 SCALES, F. M. Some Filamentous Fungi tested for Cellulose destroying Power.

Bot. Gaz. Ix, p. 149.
1920 HALL, A. D. The Soil. John Murray, London, 3rd ed. (Fairy Rings, p. 278).

PARASITISM

Facultative Parasites. Several fungi which are capable of passing
through their whole development as saprophytes are also occasionally found
on living plants as facultative parasites or hemi-saprophytes. It was first
shown by de Bary that such fungi possess the power of disintegrating and
killing the tissues in advance, so that they are not parasitic in any strict
sense, but first kill the cells of their host and then live saprophytically upon
the dead remains. This is well seen in Botrytis cinerea, the detailed knowledge
of which is due to Blackman and Welsford, and to Brown. When the spores
of Botrytis cinerea are placed in a drop of nutrient fluid on the leaves of
the broad bean ( Vicia faba), they show the first signs of a germ-tube in
2-3 hours ; the outer walls of the developing tube soon become modified to
form a mucilaginous sheath by means of which the hypha adheres to its
substratum. After growing for a while along the surface of the leaf the
germ-tube turns down and its tip, filled with dense protoplasm, becomes
pressed against the cuticle where it may or may not swell somewhat and
become spread out to form an enlargement or simple adpressorium; as
growth continues the germ-tube is held firmly in place by its mucilaginous
coat and the cuticle is ruptured mechanically by the pressure of its tip. The
fungus now penetrates directly into an epidermal cell, or grows more or less
horizontally in the subcuticular layers; in either case these layers become
swollen, and in doing so appear to stretch the cuticle and make its penetration
by other germ-tubes easier. As the hyphae make their way through the
epidermis the cells of the palisade parenchyma become affected ; their nuclei
begin to disintegrate, the chloroplasts swell, and the starch almost disappears.
In the bean a dark coloration is one of the characteristic signs of death, and

,4 INTRODUCTION [CH.

this colour change spreads through the mesophyll in advance of the fungal
hyphae. The hyphae, in fact, have been shown to secrete an enzyme which
both disintegrates the walls of the host cells and causes the death of the
protoplasts; it is however quite unable to affect the cuticle, the penetration
of the outer walls of the epidermis being mechanical; a corresponding
mechanism has been demonstrated in Colletotrichum Lindemuthianum and it
may be inferred that the same occurs in other less fully investigated cases.

Penetration of the cuticle is, however, by no means a necessary preliminary
to parasitism, whether obligate or/facultative, for the hyphae of many fungi
enter the host through the stomata, and in others, the so-called wound
parasites, infection only takes place where a previous injury has exposed
the internal tissues.

It is a curious point, and one deserving further investigation, that while
the germ-tubes from certain fungal spores always make use of the stomata
as a means of entrance, certain others completely ignore them, even though
the germinating spore happens to lie close to a stoma; it is possible that in
the former case a hydrotropic or negatively phototropic stimulus and in the
latter a contact stimulus alone or in addition is operative. In Botrytis cinerea
hyphae sometimes grow into an already seriously infected leaf by way of
the stomata; this may be related to the fact that the stomatal space becomes
charged with fluid due to the breaking down of the host cells.

A positively chemotropic reaction has often been suggested (Miyoshi)
as explaining the entrance of the germ-tube into the leaf, but recent in-
vestigation (Fulton, Robinson, Graves) show that positively chemotropic
sensitiveness is weak or absent in all the hyphae studied.

In Botrytis the mycelium commonly enters the cells of the host, but in
other fungi it may develop wholly in the intercellular spaces, killing those
cells with which it comes in contact and benefiting by the food materials
that diffuse out through the dead protoplast; such forms may be described
as saprophytic in the same sense as Botrytis.

As might be expected fungi whose attack is mainly directed to the
elements of the wood flourish equally well on living and on dead tissue; the
harm that they do to their host largely depends on the fact that they cut
off the water supply to the regions beyond the infected area. This is the case
with Nectria cinnabarina, and the fact that in this species the ascocarps are
produced on dead tissue emphasizes its saprophytic or hemi-saprophytic
character. We have here a case where the survival of the host is of no ad-
vantage to the attacking fungus.

Obligate Parasites. In the case of obligate parasitism, on the other
hand, it is evident that the death of the host involves the death of the fungus,
and it is to the interest of the parasite that death should be postponed^ at
least until the latter has itself made provision for reproduction.

J] PARASITISM ,5

The relations of the parasitic fungus to its host are extremely various;
some, especially certain unicellular parasites (<9///^V,w, Woronina)go through
their whole development inside the cells of the host, some live wholly in the
intercellular spaces (Gnomonia) or under the cuticle (Exoascus, Tapkrina)
and obtain nutriment by osmosis; others possess an intercellular mycelium
from which short branches are sent into the living cells of the host; these
branches may become specialized to form haustoria of limited growth and
more or less definite form (Cystopus, Ustilago, etc.). In all the above cases
the parasite is inside the host and may be described as endophytic.

In a certain number of forms the development of the parasite is external,
and may be described as epiphytic. This is the case in many mildews
(Erysiphaceae) which obtain their food supply by sending haustoria into
the epidermal cells of the host; it is also the case in the Laboulbeniales
where food is absorbed in many species through the unbroken membranes
of the host, and where the parasite probably causes a minimum of damage
and inconvenience.

The influence on the parasite of its method of life is already shown at a
very early stage in development. Thus the conidia or zoosporangia of
Cystopus candidus germinate better at low temperatures than high; their
minimum is near zero, their maximum about 25° C. and their most favourable
temperature, under ordinary circumstances, io°C. The spread of the fungus
by zoospores depends on the presence of water on the foliage of the host,
a fall of temperature leads to the deposition of dew, thus providing the con-
dition for the activity of the zoospores, and at the same time serves as a
stimulus to their development.

In contrast to the above the uredospores of Puccinia dispersa, which give
rise to a germ-tube directly, germinate between 10° and 27° C. but most
readily at about 20° C. ; the high temperatures appropriate to the germina-
tion of the spores of coprophilous fungi mayalso be recalled in this connection.
The relation between the parasite and its host may be strictly localized,
as in the Laboulbeniales and in those Archimycetes which enter a single
cell and complete their development within it; or the parasite may spread
far beyond the point of infection, extending through or over the existing
parts of the host and keeping pace with its growth when the new tissues are
developed; in this way the mycelium of certain of the Ustilaginales is found
year after year in the tissues of the herbaceous host, dying down when it
prepares for the winter, and growing with its growth; perennial mycelia are
not uncommon in Exoascaceae,Uredinales and other forms which infect trees.
The parasite may modify the host tissues by its invasion, chiefly in the
direction of abnormal growth or hypertrophy. The simplest instance of such
an effect is the enlargement of a single cell due to the entrance of the para-
site; this is found in the infection of various algae and fungi by Olpidium,

16 INTRODUCTION [CH.

and of the dandelion and other angiosperms by Synchytrium; in the latter
instance the cells surrounding the seat of infection are also enlarged.

In many cases fresh cell formation as well as enlargement of the host
cells takes place; this may be limited to the neighbourhood of the infected
spot so that the host organ becomes locally deformed; thus "peach leaf curl"
and many similar abnormalities are formed by Exoascus and its allies; and
irregular rose-coloured blisters are produced on the leaves of Ericaceae in-
fected by Exobasidium. More elaborate deformations are produced by some
of the Ustilaginales, and, in the case of "witches'-brooms," by the rusts and
Exoascaceae.

A witch's-broom is a bunch of modified twigs, caused usually by insects,
but sometimes by fungi. In the latter case it is the product of a lateral bud,
which, stimulated by the presence of the fungus, or by the food material
which the cells of the fungus deflect from its proper course, grows out to
form an abnormally dense bush of twigs; its leaves are produced earlier than
those of healthy branches and, even in the case of normally evergreen conifers,
are deciduous, falling off at the end of each season. Here the specialized
shoot, in spite of its contained parasite, appears to flourish, though to the
detriment of the rest of the tree; it may indeed be suggested that something
approaching symbiosis has been established, but in this relationship the
fungus is clearly the dominant partner1.

SYMBIOSIS

The physiological conditions under which the thallus of a lichen is built
up are somewhat similar; the algal cells appear healthy and are capable of
vegetative multiplication, but the fact that the fungus alone is concerned in
the development of the fructification sufficiently indicates its supremacy.
In the case of Thermutis orlutina the alga is devoured by the fungus in
preparation for the formation of the fruit.

In mycorhiza, that is in the structures formed by the association be-
tween the mycelium of a fungus and the roots (or other organs) of one of the
higher plants, the advantages of the symbiotic relation often belong less to
the fungus than to its partner so that the vascular plant may actually become
dependent on its fungal associate and unable to develop in its absence. The
mycelium may be either endotrophic, forming a skein of branched and
interwoven filaments in the cells of the host and sending comparatively few
hyphae to the exterior; or it may be exotrophic, that is to say mainly ex-
ternal in development.

Endotrophic Mycorhiza. An extreme case of obligate symbiosis has
been described by Rayner for the ling, Calluna vulgaris, which grows in
association with a fungus resembling the members of the genus Phoma in

1 For bibliography, see p. 19.

I] SYMBIOSIS i;

its morphological characters. The mycelium not only extends through the
roots and colourless parts, but grows into the subaerial tissues of the stem,
leaves, flowers and fruit. Moreover the seedling is regularly infected on
germination by the hyphae which have penetrated the seed coat. When
deprived of its fungus by sterilization of the seed, the seedling fails to develop,
its root system in particular being inhibited; when subsequently infected
from artificial culture it renews its growth. If, however, a weak seedling is
inoculated from a vigorous culture it is completely parasitized and destroyed ;
the fungus in such a case may be regarded as having escaped from the con-
trol of its partner.

The fungi. present in the orchids investigated by Bernard were referred
to the form genus Rhizoctonia1, certain species of which have been shown to
be conidial stages of the basidiomycete Hypochnus. It is significant that
conidia are never produced on a healthy host plant, though they can be
obtained when the mycelium is grown in culture; in the cells of the host a
tangled weft of hyphae develops and ultimately undergoes digestion, forming
an amorphous mass. In Odontoglossum the mycelium does not enter the
stem, and in Vanda and its allies it is confined to the perennial roots; in
the Cattleyeae the roots are deciduous and their disappearance is followed
by an autonomous phase; in Bletilla hyacintliiiia, also, the mycelium never
invades the green, superficial rhizome, but the young roots are regularly in-
fected as they reach the length of a few centimetres. In winter the orchid
is represented by its rhizome alone and its activity at the beginning of fresh
growth is consequently autonomous; the symbiotic phase follows on the
development of the new roots and lasts about six months, covering the period
of the maturation of the seeds. Duringthe autonomous phase the fungus vege-
tates in the soil and loses, to some extent, its "virulence" or power of infection.

Bletilla differs from the cases previously described in that its symbiosis is
facultative and development can take place without infection, but the seed-
lings grow slowly and are delicate; inoculation by a mycelium greatly reduced
in virulence has little effect, the hyphae enter a few cells and are at once
digested ; a mycelium, on the other hand, which has attained a high degree of
virulence, penetrates at once to the region of attachment of the suspensor and
instead of undergoing premature digestion spreads through the host cells
while the seedling grows rapidly and its lower part swells to form a protocorm.

The restriction of the mycelium to the non-chlorophyllous regions of
these orchids is not accidental, for the contents of certain of the stem cells
have a poisonouseffecton thefungus. It follows that here the mycelium cannot
penetrate into the ovary and the infection of the germinating seed is conse-
quently a matter of chance, hence the difficulty frequently experienced in
inducing the germination of orchids.

1 Burgeff, in 1909, proposed the new generic name Orcheomyces for these fungi.

2

I8 INTRODUCTION [CH-

Kusano has shown that the rootless, saprophytic orchid, Gastrodea elata
becomes dependent on the formation of mycorhiza only on the incidence o
its flowering period ; it is capable of vegetative growth without infection, and
the distribution of the fungus in its tissues is strictly limited; the fungus i
this case is Armillaria mellea, a well-known facultative parasite.

This may be regarded as a relatively early stage in the development of
endotrophic symbiosis in which the angiosperm succeeds in utilizing as a
factor in its own nutrition the mycelium of the attacking parasite. It suggests
that in this relationship we are dealing not with an association of two or-
ganisms for the benefit of both, but with a struggle between the would-be
parasite and the host which controls, makes use of, and finally becomes
dependent upon it. The balance of power is often very delicate, and any
weakening on the part of the angiosperm gives the fungus an opportunity
to assume the parasitic habit ; thus the endotrophic fungus regularly becomes
parasitic on the old stamens and corolla of Arbutus and on the dying leaves.
Endotrophic mycorhiza occurs in the Ericaceae and in their allies showing,
so far as investigation has gone, the same extreme conditions as in Calluna ;
in certain Gentianaceae, Solanaceae, Labiatae, Umbelliferae, Ranunculaceae
and Liliaceae, in most if not all orchids, in species of Viola and Arum, and,
according to the researches of von Tubeuf, in gymnospermous trees other
than the Abietineae.

Endotrophic mycorhiza is also found in certain liverworts and mosses,
and in many of the Pteridophyta. It is well developed in the prothallus
of Lycopodium and in the leafy plant of species of both Lycopodium and
Selaginella, in the roots of Cyathea and of several of the Marattiaceae, and
in both the prothallus and sporophyte of the Psilotaceae and Ophioglos-
saceae. In most of these cases it does not appear to be essential to the
nutrition of the sporophyte since the latter seldom shows a correlated reduc-
tion of the assimilatory apparatus, but it is often a principal factor in the
nutrition of the prothallus, which in the presence of mycorhiza may be
subterranean and lacking in chlorophyll. Mycorhiza has been recorded in a
number of fossil plants.

Bernard has suggested a relationship between tuberization and the
presence of an endotrophic mycelium. It is significant that very many sym-
biotic plants, including notably the orchids and the sporophyte and gameto-
phyte of the lycopods, tend to assume a tuberous habit or to develop bulbs
or protocorms. Bernard's researches have disclosed mycorhiza in tuber-
forming species of Solatium, indicating a similar origin for the potato.

Exotrophic Mycorhiza The majority of our forest trees, including
Abietineae, Salicaceae, Fagaceae and Betulaceae, as well as some other plants,
possess an exotrophic mycelium forming a dense felt over the apical parts
of the infected roots; under this influence the development of root hairs is

I] SYMBIOSIS I9

impeded and characteristic short, coral-like branches are formed. Sarcodes
sanguined and Monotropa Hypopitys are non-green holosaprophytes with
exotrophic mycorhiza; in the former the whole root system is covered by
the mycelium of the fungus, in the latter the apices alone are free.

In other cases infection seldom takes place in all roots; it is extensive
in soils rich in vegetable debris, and is absent in poor soils free from humus;
under these circumstances root hairs are formed and the roots function in
the normal way. When present it would appear that the mycorhiza not only
absorbs water and dissolved salts, but the vascular plant is further enabled
by its means to utilize directly the organic remains in the soil.

The relation between an exotrophic fungus and its host, at least when
the latter contains chlorophyll, would appear to be much more casual than
is the case with endotrophic forms; like the latter it may arise as an at-
tempted parasitism on the part of the fungus, controlled and utilized by the
vascular plant. The absence of exotrophic mycorhiza in poor soils may depend
at least as much on the absence of saprophytic mycelia capable of causing
infection, as on the fact that a fungal associate would, under the circumstances,
be of little value to the green plant. Exotrophism would seem to be more
to the advantage of the fungal partner than endotrophism, since fructifica-
tions are often found on mycelia in exotrophic association with the roots of
vascular plants; and some subterranean species, such as the truffles, fruit .
only in the neighbourhood of appropriate trees.

The fungi concerned in these curious relationships include representatives
of all the great groups; the endotrophic mycelium of the prothalli of Lyco-
podiuin has been referred to the genus Pythium, and that of the Marattiaceae
to Stigeosporium, a genus nearly related to Phytophthora, that of several
orchids to Rhizoctonia (== Hypochnusl) and of others to Nectria; the myce-
lium of species of Elaphomyces forms mycorhiza with the roots of Pinus and
other conifers; that of the Boleti with conifers and grasses and with willow,
poplar, hornbeam and birch, that of Tricholoma terreum with beeches and firs,
that of Lactarius piperatus and of species of Cortinarius with beeches and
oaks, that of species of Geaster with conifers. Reference has already been
made to the association of Armillaria mellea with the orchid Gastrodea
elata, and of P/ioma-\ike species with the Ericaceae.

Finally there is little doubt that several of the Tuberaceae and Hymeno-
gasteraceae are frequent constituents of mycorhiza.

PARASITISM AND SYMBIOSIS: BIBLIOGRAPHY
1863 DE BARY, A. Recherches sur le deVeloppement de quelques champignons parasites.

Ann. Sci. Nat. xx, p. 95.
1888 WARD, H. MARSHALL. Some Recent Publications bearing on the Sources of

Nitrogen in Plants. Ann. Bot. i, p. 325.
1890 OLIVER, F. W. On Sarcodes sanguinea, Torr. Ann. Bot. iv, p. 303.

2—2

20 INTRODUCTION [CH-

1891 FRANK B Ueber die auf Verdauung von Pilzen abzielende Symbiose der mit
endotrophen Mycorhizen begabten Pflanzen, so wie der Leguminosen uncl Erie
Ber. d. deutsch. Bot. Ges. ix, p. 244.

1894 MIYOSHI, M. Ueber Chemotropismus der Pilze. Bot. Zeit. lii, p. i.

1902 LANG, W. H. On the Prothalli of Ophioglossum pendulum and Helminlhostachys
zeylanica. Ann. Bot. xvi, pp. 28 and 36.

1904 CAVERS, F. On the Structure and Biology of Fegatella conica. Ann. Bot. xvm, p. 95

1904 MASSEE, G. On the Origin of Parasitism in Fungi. Phil. Trans. B. cxcvii, p. 7-

1904 WEISS, F. E. A Mycorhiza from the Lower Coal Measures. Ann. Bot. xvin, p. 255.

1905 GALLAUD, I. Etudes sur les mycorhizes endotrophes. Rev. Gen. Bot. xvii, p. i.

1906 FULTON, H. R. Chemotropism of Fungi. Bot. Gaz. xli, p. 81.

1908 BOWER, F. O. The Origin of a Land Flora. Macmillan & Co., London, pp. 240,
477 el sff.

1909 BERNARD, N. devolution dans la symbiose des Orchiddes et leurs champignons
commensaux. Ann Sci. Nat. 9me ser. ix, p. i.

1909 BURGEFF H. Die Wurzelpilze der Orchideen. Fischer, Jena.

jgii BKRNARD, N. Sur la fonction fungicide des bulbes d'Ophryddes. Ann. Sci. Nat.

9me ser. xiv, p. 221.

1911 BERNARD, N. Les mycorhizes des Solatium. Ann. Sci. Nat. 9rae se"r. xiv, p. 235.
191 1 KUSANO, S. Gastrodea elata and ks Symbiotic Association with Armillaria meliea.

Journ. Coll. Agric. Tokio, iv, p. i.
191 1 MF.LHUS, I. E. Experiments on Spore Germination and Infection in Certain Species

of Oomycetes. Univ. Wise. Agric. Expt. Sta. Research Bull, xv, p. 25.

1914 ROBINSON, W. Some Experiments on the Effect of External Stimuli on the Sporidia
of Puccinia malvacearum (Mont.). Ann. Bot. xxviii, p. 331.

1915 RAYNER, M. C. Obligate Symbiosis in Calluna. Ann. Bot. xxix, p. 97.

1915 BROWN, W. Studies in the Physiology of Parasitism. I. Ann. Bot. xxix, p. 313.

1916 BLACKMAN, V. H.and WELSFORD, E. J. Studies in the Physiology of Parasitism. II.
Ann. Bot. xxx, p. 389.

1916 BROWN, W. Studies in the Physiology of Parasitism. III. Ann. Bot. xxx, p. 399.
1916 GRAVES, A. H. Chemotropism in Rhizopus nigricans. Bot. Gaz. Ixii, p. 337.

1916 RAYNER, M. C. Recent Developments in the Study of Endotrophic Mycorhiza.
New Phyt. xv, p. 161.

1917 BROWN, W. On the Physiology of Parasitism. New Phyt. xvi, p. 109.

1917 DUFRENOY, J. The Endotrophic Mycorhiza of Ericaceae. New Phyt. xvi, p. 222.
1917 WEST, C. On Stigeosporium Marattiacearum and the Mycorrhiza of the Marattia*

ceae. Ann. Bot. xxxi, p. 77.
1919 DKY, P. K. Studies in the Physiology of Parasitism. V. Infection by Colletotrichum

Lindeimithianum. Ann. Bot. xxxiii, p. 305.
1921 RAMSBOTTOM, J. Orchid Mycorhiza. Catalogue of J. Charlesworth & Co., Haywards

Heath, p. i.

SPECIALIZATION OF SAPROPHYTISM AND PARASITISM
Fungi vary very much in the extent to which they are adapted or re-
stricted to a particular habitat. In some species the range is very wide, as in
the case of Eurotium herbariorum or Penicillium glaucum which may occur
under suitable conditions of temperature and moisture on almost any plant
remains, on plant products such as bread or jam, or on substances of animal
origin and, in the case of Penicillium, especially on cheese.

Eurotium herbariorum^^ some other species are even found in the human

SPECIALIZATION 2I

ear, where they produce the condition known as otomycosis aspergillana but
they develop on the secretions and not in the living cells, so that, although
they give rise to a disease, they are not true parasites.

Similarly Synchytrium aureum infects all sorts of dicotyledons and Phyk
lactima Corylea occurs on the leaves of many trees.

In other cases the range is somewhat narrowed ; many species of Hydnum
are found only in fir woods, Pyronema confluens and a number of other fun<n
occur in nature only on burnt ground, Onygena equina is restricted to the
hoofs and horns of various animals, and several species (Sordaria macrospora
Podospora coprophUa, Ascobolus immersus, Ascophanus equinus, etc.) develop
upon different kinds of dung but on no other substratum. ' Some of the
coprophilous fungi on the other hand may appear in addition on other sub-
stances, especially on those rich in cellulose— Ascophanus carnetis has been
recorded upon paper or rope, Gymnoascus Reesii on wasps' nests, Xylaria
Tulasnei on soil.

Parasites again may be limited to hosts of a particular family; Cystopus
candidus to the Cruciferae, Claviceps pitrpurea to grasses, Ustilago violacea
to the Caryophyllaceae.

Still greater restriction is observed in the case of such saprophytes as
Erinella apala on the dead stems of species of Juncus and Pilacre faginea
on rotten beech wood, and in the case of the parasites which attack the
species of a single genus, such as Rhytisma Acerinum on Acer, Poly stigma
rubrum on Prunus, Peronospora Euphorbiae on Euphorbia.

Even more definite is the specialization of fungi which are capable of
obtaining nutriment only from a single species; this occasionally happens
among saprophytes, such as Dasyscypha dandestina on dry stems of Rubus
idaeus ; it may be surmised that in many such cases new habitats will ulti-
mately be brought to light.

Among parasites restriction to a single species is very common ; Sclerotinia
tuberosa forms its sclerotium attached to the rhizome of Anemone nemorosa,
Exoascus Betulae develops on Betula alba, and Ustilago Maydis on Zea Mays.
De Bary gave to this state the name monoxeny, in contradistinction to
the term polyxeny, which he applied to cases where hosts of several different
species may be attacked. Every sort of intermediate grade may exist between
those outlined above ; parasites may attack only two or three closely related
members of a genus (Exobasidium Rhododendri on Rhododendron hirsutum
and R. ferrugineum\ they may attack a genus and one or two species
belonging to related genera, they may be capable of development on certain
genera of a family and not on the rest, or again, while commonly restricted
to a particular family, they may occur also on members of neighbouring
groups; thus Phytophthora infestans is found usually on the Solanaceae and
exceptionally on the scrophulariaceous species Anthocercis viscosa and
Schizanthus Grahami.

22

INTRODUCTION tCH-

all the cases of parasitism considered above, the fungus, whether

i«iy*^

to a ingle species'of host, or they may be capable of occurring on a
number of different forms. Heteroecism is known in Scleroma Led* but
in no other fungi except the Uredinales or rusts, and its full consignation
must be postponed till that group has been described. It may be considered
here as one of the possible alternatives confronting a parasite on a host
which dies down early in the year. Under such circumstances the parasite
mav continue its development on the dead tissue, it may await in the form
of resting spores the reappearance of its host, or its spores may prove capable
of germinating on a new host species, and it may carry on its development
as a parasite and reinfect its original host next spring, thus becoming
heteroecious. It must be noticed, however, that by no means all the
existing spring or summer hosts of heteroecious fungi die down early
in the year, so that other and possibly secondary factors will have to be
considered.

Biological species. There is no doubt that within wide or narrow limits
related host plants are apt to show common susceptibility to infection ; this
is well exemplified by Pucdnia Malvacearum which was first observed in this
country on cultivated hollyhocks in 1873 and has since established itself on
the indigenous species of Malva, Alt/tea and Lavatera as well as in green-
houses on Abntilon.

Common susceptibility may even be used as a criterion of relationship,
so that liability to the attacks of Piptocephalis Freseniana, the obligate
parasite of the Mucorales, has afforded a means of distinguishing new
members of that group.

These facts point to a definite adaptation on the part of the fungus to
its habitat; this adaptation may be very simple, a species, for example, would
not be likely to occur on dung unless its spores could pass uninjured through
the alimentary canal of an animal, or it may reach the complexity of a
delicately balanced reaction between host and fungus, as in some of the
mycorhiza described in the preceding pages.

Specialization has been most fully investigated and has possibly reached
its highest levels in the adaptation of various rusts and mildews to their
graminaceous hosts, but it is shown in varying degrees by other fungi1. Like

1 Wormald has shown that there are two biological species of Monilia (Sclerotinia) cinerea, one
of which produces a Blossom Wilt and Canker Disease on the apple tree while the other is unable

SPECIALIZATION 23

many fruitful mycological discoveries this was foreshadowed by de Bary
who in 1863, noticed that the structural differences between the aecidia of
Chrysomyxa Rhododendri and C. Ledi were so slight that he regarded these
as " rather biological than morphological species."

Thirty years later Eriksson recognized that the rust of wheat, Puccinia
Graminis, which infects wheat, barley, rye, oats and various wild grasses,
is a collective species, consisting of a number of biological forms which',
though they differ in no recognizable structural character, yet differ in the
powers of infection of their spores, since uredospores grown on wheat are
incapable of directly infecting rye, barley or oats, those on oats cannot
directly infect wheat, rye or barley, and those on barley and rye, though
they can infect both rye and barley, will not develop if sown on oats or
wheat. Now Puccinia Graminis is a heteroecious species producing two
kinds of spores (uredospores and teleutospores) on grasses, and aecidiospores
in cluster-cups on the barberry. But, though all the different biological forms
alike develop their cluster-cups on the barberrry, Eriksson found that they
remained constitutionally distinct, for aecidiospores derived from the form
upon oats proved capable of infecting among cereals only oats, aecidiospores
from the form upon rye or barley, only rye or barley and so on.

In other words each form of Puccinia Graminis is so closely adapted to
the particular cereal on which it occurs that its spores can only attack
successfully and directly that particular graminaceous host or a limited
number of its immediate allies.

Marshall Ward, working with the uredospores of Puccinia dispersa, made
clear that the susceptibility or immunity of the host does not depend on
structural characters, and suggested rather the existence of enzymes or
toxins or both in the cells of the fungus, and of antitoxins or similar sub-
stances in the cells of the host.

This hypothesis has been greatly strengthened by the work of Marchal
and of Salmon on the Erysiphaceae or mildews in which group both the
conidia and ascospores of biological species are similarly specialized in
their powers of infection. Not only are there no structural peculiarities in
the resistant hosts of these fungi, but Salmon was able, by suitable treatment,
to break down their resistance. This may be achieved in various ways:
(i) a minute piece of tissue, including the epidermis and the greater part of
the mesophyll, is cut with a razor from one side of the leaf and spores are
sown on the opposite side; (2) the leaf to be inoculated is touched for a few
seconds on the upper surface with a red-hot knife and the spores are sown
on the lower surface opposite the burnt spot.

The result of such treatment is the ready infection of host species

to cause infection except of a flower directly inoculated. Biological species have also been identified

among smuts, and by Diedicke in Pleospora.

24

INTRODUCTION

[CH.

normally immune from the attacks of the biological form used. Thus if
conidia oiErysiphe Graminis growing on wheat, are sown on uninjured leaves
of wheat and barley, the result is the infection of the wheat but never of the
barley; yet the conidia grown on wheat readily infect the uninjured surface
of a cut or burnt barley leaf; in the case of the burnt leaf, where the whole
thickness of the leaf in the burnt region becomes discoloured and apparently
dead, the mycelium is found on the living cells which border the altered
patch. Since the cuticle, hairs and other anatomical characters of the epi-
dermis on which the spores are sown are not affected by the treatment of
the cut leaf, it is clear that resistance does not depend on such factors; it
must be referred, as in the case of rusts, to the physiological condition of the
cells or of their contents. In nature injuries caused by insects are sufficient to
destroy in the same way the resistance of the potential host.

These facts have a practical bearing since diseases on the weed grasses
surrounding a field of corn, even if they are not able directly to affect the
uninjured leaves of the crop, may establish themselves on injured tissues.

The various hosts of a given morphological species of fungus differ very
much in their susceptibility to infection by the different biological forms of
the parasite; thus Bromns racemosus, though markedly susceptible to its
own form of Erysiphe Graminis, is completely immune against infection by
conidia of the same species grown on B. commutatus, B. interrnptus, B. velu-
tinus and others. This immunity is particularly remarkable in the case of

conidium on
commutatus

conidium on
secalinns

conidium on
interruptus

conidium on
hordeaceus

conidium on
velutinus

the conidia from B. commutatus, since B. racemosus is morphologically so close
:o B. commutatus that it is regarded by most systernatists as no more than
a variety of that species.

conidia on
arduennensis

conidia on
commutatus

conidia on
secalinus

conidia on
adoensis

i] SPECIALIZATION 25

Another remarkably resistant species is Bromus mollis, yet the so-called
B. "hordeaceus" the seed of which was sent to Cambridge from Petrograd, and
which is morphologically indistinguishable from B. mollis, is nevertheless
susceptible to infection by the biological species which B. mollis is able to
resist. In other words the morphological species B. mollis includes two
groups or races possessingdistinct physiological (or constitutional) characters
and respectively immune and susceptible to infection.

In the caseof certain parasitic fungi, and especially of Puccinia glumarum,
the yellow rust on wheat, Biffen has shown that resistance to the attacks of
the parasite is a recessive character in the Mendelian sense. When a variety
susceptible to rust was crossed by another practically immune from it, the
offspring was at least as much infected as the original rusty type. In the
next generation segregration took place in the ordinary way, three-quarters
of the plants being rusty and the remaining quarter standing green and un-
injured among them. In relation to this investigation Marryat showed that
the rust hyphae are checked after entering the stomata of the resistant plants
either by the death of the host tissue locally, accompanied by the starvation
and death of the parasite, or, after a more protracted struggle, by the gradual
degeneration of the invading hyphae. If, as has been suggested above,
resistance depends on the presence of an antitoxin, the dominance of sus-
ceptibility in this case must be taken to indicate that the development of
the antitoxin is inhibited by the presence of some additional factor in the
dominant forms. Cases may be expected where, in the absence of an
inhibitor, resistance is dominant and depends on the presence of the anti-
toxin or its progenitor. Such a case is suggested by the work of Biffen on the
inheritance of immunity to ergot, but here two factors appear to be involved.

The susceptible races have in some instances an importance beyond that
implied in their own liability to infection; it has been suggested that they
may serve as a bridge by which the fungus can pass from its original host
to a species resistant to direct attack.

This was indicated by the work of Marshall Ward on Puccinia dispersa,
and by Salmon using Bromus "hordeaceus" as a bridging host. Inoculation
experiments showed that the form of Erysiphe Graminis on Bromus racemosus
was incapable of developing on uninjured B. commutatus but that it never

failed to produce full infection on B. -hordeaceus." The mycelium on its new
host gave rise in due course to conidia and some of these, when transfers
to B. commutatus, succeeded in establishing themselves and produce.
infection in eight days.

26 INTRODUCTION [CH.

Freeman and Johnson, in 1911, described barley as a bridging host for
biological forms of Puccinia Graminis on other cereals and, in the same
year, Pole Evans found that the heterozygote between strains immune and
susceptible to infection by black rust was even more susceptible than the
susceptible parent and was capable of acting as a bridging species from
which the immune parent could be infected.

On the other hand an increasing number of investigators, working with
isolated strains under rigidly controlled conditions, have failed to confirm the
existence of bridging species and, according to Stakman and his assistants,
there is no evidence that biological species are changed by their sojourn on
a particular host. Such a change would imply a certain physiological
plasticity on the part of the fungus, since it would be capable of becoming
acclimatized, on the bridging host, to conditions similar to those awaiting it
on the form resistant to direct attack.

In the case of Puccinia Graminis the problem is further complicated by
the fact that a considerable number of biological forms are parasitic on the
varieties of wheat, so that the same variety may be susceptible in one
locality and immune in another according to the distribution of the parasite.

SPECIALIZATION OF PARASITISM ETC.: BIBLIOGRAPHY

1863 Dfc BARV, A. Recherches sur le developpement de quelques champignons parasites.

Ann. Sci. Nat. seV. 4, xx, p. 5.
1894 ERIKSSON, J. Ueber die Specialisirung des Parasitismus bei den Getreiderostpilzen.

Her. der dent. Bot. Ges. xii, p. 292.
1898 ERIKSSON, J. A General Review of the Principal Results of Swedish Research into

Grain Rust. Bot. Gaz. xxv, p. 26.
1902 DIKDICKE, H. Ueber den Zusammenhang zwischen Pleospora- und Helmintho-

jr/or/ww-Arten. Centralbl. f. Bakt. ix, Abt. ii, p. 317.
1902 WARD, H. MARSHALL. On the Relations between Host and Parasite in the Bromes

and their Brown Rust, Puccinia dispersa (Erikss.). Ann. Bot. xvi, p. 233.

1902 WARD, H. MARSHALL. Experiments on the Effect of Mineral Starvation on the
Parasitism of the Uredine Fungus, Puccinia dispersa, on Species of Bromus. Proc
Roy. Soc. Ixxi, p. 138.

1902-3 MARCHAL, E. De la Specialisation du parasitisme chez VErysiphe Graminis.
Comptes Rendus, cxxxv, p. 210, and cxxxvi, p. 1280.

1903 WARD, H. MARSHALL. Further Observations on the Brown Rust of the Bromes
Puccinia dispersa (Erikss.) and its adaptive Parasitism. Ann. Myc i p 1*2

1903 SALMON, ES. On the Specialization of Parasitism in the Erysiphace'ae. Bei'heftc 2,
Bot. Central, xiv, p. 261.

903 ™ *™ ^'^ °f ASC°Sp°reS in the Erysiphaceae. Journ. Bot.

1904 MASSEE, G. On the Origin of Parasitism in Fungi. Phil Trans B

1904

' and its

J] REACTIONS TO STIMULI 2?

1905 WARD, H. MARSHALL. Recent Researches on the Parasitism of Fungi. Ann. Bot.
xix, p. i.

1907 BIFFEN, R. H. Studies in the Inheritance of Disease Resistance. I. Journ Aer Sci

ii, p. 109.

1907 MARRYAT, D. C. E. Notes on the Infection and Histology of two Wheats immune
to the Attacks of Pucdnia glumarum, yellow Rust. Journ. Ag. Sci. ii, p i->9

1911 FREEMAN, E. M. and JOHNSON, E. C. The Rusts of Grains in the United States.
U.S. Dept. Ag. Bureau of Plant Industry. Bull. 216.

1911 POLE EVANS, I. B. South African Cereal Rusts, with Observations on the Problem
of Breeding Rust-resisting Wheats. Journ. Ag. Sci. iv, p. 95.

1912 BIFFEN, R. H. Studies in the Inheritance of Disease Resistance. II. Journ. Ag. Sci.
iv, p. 421.

1914 VARILOV, N. I. Immunity to Fungous Diseases as a Physiological Test in Genetics
and Systematics, exemplified in Cereals. Journ. Genetics, iv, p. 49.

1918 STAKMAN, E. C., PIEMEISEL, F. J., and LEVINE, M. N. Plasticity of Biologic Forms
of Pucdnia graminis. Journ. Ag. Research, xv, p. 221.

1919 WORMALD, H. The 'Brown Rot' Disease of Fruit Trees, with Special Reference
to two Biologic Forms of Monilia cinerea, Bon. I. Ann. Bot. xxxiii, p. 361.

REACTIONS TO STIMULI

Among the fungi, response takes place to a large number of external
stimuli, most of which are concerned with nutrition and the distribution of
the spores. A special series of reactions which demands further investigation
takes place in relation to the formation, approach and fusion of the sexual
organs. The stimulus in question may be effective very early in development
for de Bary found that the presence of the oogonium in Pythium de
Baryanum stimulates the formation of antheridia and Blakeslee observed
directive growth or " zygotaxis " in morphologically undififerentiated hyphae
of Mucor Mucedo. In Mucor and its allies the formation of the gametangia
follows on the contact of appropriate branches. The stimulus inducing
directive growth is presumably chemical, as in other and better known cases
of the approach of gametes or gametangia; but we have at present no
knowledge of the substances concerned or of much more than the fact that
the reaction occurs. In some of the higher fungi, where the antheridium is
liberated as a spermatium, it would appear to be carried passively to the
female structure, but in Zodiomyces among the Laboulbeniales and perhaps
in a few other Ascomycetes (Ascobolus carbonarius, Lachnea creted) the tri-
chogyne moves towards the male organ.

Chemotropism. The most marked chemotropic reaction of vegetative
hyphae and germ-tubes is a negative one; they tend to grow away from the
products of their own metabolism or so-called "staling" substances. Clark,
in 1902, concluded that Rhizopus nigricans1 is negatively chemotropic to
some secretion of its own mycelium and that the negative response is much

1 Rhizopus nigricans, Ehrenb. - Mucor stolonifer, Ehrenb.

,8 INTRODUCTION [CH-

natu and in artificial culture. In so far as a clear field is
tend to grow equally in all directions from the point where infection took
pace The same factor may account, as Stevens and Hall have suggested
for the alternate dense and sparse zones which characterize many fungal
colonies and are independent of changes in light and temperature. Energet,
.rowth results in the deposition of katabolic substances, and growth is corre-
spondingly reduced till a few scattered hyphae pass beyond the inhibiting
influence and give rise to a new ring of richly branched mycelium. In older
colonies the germination of fresh spores outside the zone of staling substanc
doubtless adds to this effect.

The very definite character of the reaction is demonstrated by the ex-
periments of Graves, who used the germ-tubes of Rhizopus nigricans on con-
trasted agar media separated by a perforated mica plate. Hyphae developing
in agar made up with turnip juice grew towards the perforations which led
to fresh but otherwise identical agar on the other side of the mica plate.

Hyphae under similar conditions turned from turnip juice, in which
growth had taken place, to plain agar, or indeed to any fresh substance
that was not in itself definitely repellant, even if, as in the case of plain agar,
its nutritive value was low.

On the other hand, the hyphae turned away from the perforations in the
mica plate if these led to nutritive agar on which mycelium had already
developed and if the substratum on which the germ-tubes were growing was
by comparison fresh. This was the case even after the mycelium on the
staled agar had been taken away, the products of its metabolism which re-
mained in the agar having themselves a repellant effect. This effect was
removed by exposure to a temperature of ioo°C., showing that the staling
substances are altered or destroyed by heat.

A somewhat different example of the inhibiting effect of these katabolic
staling substances was observed by Balls for the "sore-skin" fungus of cotton.
When the nutritive medium is limited in extent, growth comes to an end
more rapidly at high temperatures than at low. This is due not to the
earlier exhaustion of the available food supply, but to the more rapid ac-
cumulation of staling substances when growth is accelerated. Media in
which growth has come to an end prove capable of supporting further
growth if diluted with an equal quantity of water. By this means the staling
substances are sufficiently diluted to lose their inhibiting effect, while the
nutritive materials, even though diluted, are still sufficient to support growth.

J] REACTIONS TO STIMULI 2g

By the addition of staled media to his cultures Balls was able to show that
accumulation of staling substances was a limiting factor in the growth of
his fungus.

The products of past metabolism are not the only factors which exercise a
negatively chemotropic influence; Miyoshi showed that hyphae tend to grow
away from acids, alkalis, alcohol, toxic compounds and certain neutral salts.

He also brought forward evidence of the positively chemotropic effect of
a number of salts and of sugar and other nutritive materials; but his results
are vitiated by the fact that he was unaware of the importance of staling
substances and accepted, as due to the attraction of the new medium, curva*
tures which really depended on the repellant effect of the old. Neverthe-
less, positive chemotropism exists and may be observed when the staling
substances have been taken into account.

Thus Graves found that, while all the germ-tubes of Rhizopus nigricans
turned from the turnip juice agar on which they had been growing to fresh
turnip juice agar, only 60 to 90 % turned to fresh plain agar, and, when
growth had just begun in the turnip juice agar and staling was consequently
less, a smaller proportion of hyphae sought the plain substratum. Positively
chemotropic reactions towards cane-sugar and glucose were also demon-
strated but they were relatively weak. It may be inferred that the dominant
influence governing the distribution of a parasitic fungus in its host, like that
governing the distribution of saprophytic forms in culture, is negative chemo-
tropism excited by the products of metabolism.

This inference is borne out by the observation of- Robinson that the
germ-tubes from the basidiospores of Puccinia Malvacearum failed to show
any positively chemotropic curvature towards fragments of the host leaf.

Hydrotropism. Positive hydrotropism is probably effective in vegetative
hyphae under appropriate conditions; thus Fulton found that, when spores
of various species were grown on gelatine between two perforated mica
plates with a relatively moist medium on one side and a relatively dry one
on the other, they grew through the perforations towards the moist rather
than towards the dry medium; hyphae of Mucor Mucedo grew through per-
forations in a mica plate from firm gelatine into water, but hyphae of
Rhizopus nigricans, though they grew into the relatively moist gelatine near
the holes, turned away from the fluid water below.

Germ-tubes of Puccinia Malvacearum were found by Robinson to grow
from drops of water into the surrounding moist atmosphere, but on gelatine
in moist air they tended to penetrate the gelatine. It would seem that the
response varies, as is indeed to be expected, with the conditions of the fungus
in question, but in some of these and perhaps other tropic reactions, there is at
least a suspicion of the negatively chemotropic influence of staling substances.

Negative hydrotropism has been described for the sporangiophores of

INTRODUCTION [CH-

the Mucora.es and, together with transpiration, has been held responsible for

li.h and by means of this reaction are able to adjust themselves m a post-
lion favourable to the distribution of their spores, the direction of light
indicating the direction of open space.

Among the Mucorales the sporangiophores of various species of Pilobolus,
Mncor Phycomyces and no doubt of many other genera bend towards the
li<rht 'in the genus Pilobolus the hemispherical sporangium is borne on an
aseptate sporangiophore which develops a swelling or bulb just below the
sporangium and another at its base. A new set of sporangia matures daily
and is discharged in the morning or early afternoon. The young sporangio-
phores of the species studied by Jolivette1 showed a recognizable phototropic
curvature about 30 minutes after their exposure to light from a new direc-
tion; growth is apical and the tips, as they grow, bend towards the source
of light Curvature is arrested during the early stages of the formation of the
sporangium and is resumed again when the subsporangial bulb is beginning
to forrn; during the later stages of development curvature takes place just
below the bulb. In this way the bulb and the terminal sporangium are
pointed in the direction of the light and some accuracy of aim is secured.
In a series of experiments, involving some 20,000 specimens, in which light
reached the culture through apertures I cm. in diameter, nearly 90 °/0 of the
sporangia hit either the aperture itself or the walls within I cm. on each side
of it. When illuminated by two equal sources of light the sporangiophores
point to either one or the other; this is obviously a useful adaptation as an
intermediate aim would fail of its object. When the sources of light differed
the sporangia were found to be shot off in larger numbers towards the light
in which the proportion of blue rays was greater. The species1 studied by
Parr also responded more readily to blue or violet than to other rays, the
presentation time gradually decreasing from red to violet although the
sporangiophores were responsive to light from all regions of the spectrum.

Among Ascomycetes a positively phototropic response is found in the
necks of the perithecia in Sordaria and many other Pyrenomycetes, and is
sufficiently delicate to induce a zig-zag development of the neck if the
direction of light is repeatedly changed. The asci of Ascobolus immersus
and A . furfuracens are also positively phototropic so that an appropriate
direction is obtained for the ejection of their large spore mass.

As early as 1877 Brefeld recorded sensitiveness to light in the stipe of
various Coprini, and found that normal pilei failed to develop in its

1 Specific name not given.

J] REACTIONS TO STIMULI 3,

absence. In Coprinus niveus, and Coprinus curtus, both coprophilous species
Buller found a well-marked positively phototropic response in young fruit
bodies so that they push up from between or beneath the irregularities of
the substratum. The stipe ceases to be phototropic when the pileus begins
to expand and develops instead a negatively geotropic reaction; by these
means the apex of the stipe is brought out into the light and the horizontal
expansion of the pileus is ensured. A similar succession of reactions takes
place in the development of the sporophore of Lentinus lepideus; the young
stipe is positively phototropic and in the absence of light grows straight
onwards without giving rise to a pileus ; in a sufficiently strong illumination
the pileus soon appears and, as its development proceeds, the positively
phototropic response changes to a negatively geotropic one. Amanita phal-
loides and A. crenulata show, according to Streeter, a positively phototropic
reaction even after the appearance of the pileus.

Corresponding reactions are to be expected in other pileate species
growing on irregularly shaped substrata; on the other hand Agaricus cant-
pestris, growing on ground, is quite insensitive to light, negative geotroprsm
being, under normal conditions, sufficient to secure the satisfactory adjust-
ment of its parts.

A negatively phototropic reaction is very much less frequent than a
positive response; Robinson found, however, that germ-tubes from the
basidiospores of Puccinia Malvacearum and the conidia of Botrytis sp. turn
away from a unilateral source of light, while those from the aecidiospores of
Puccinia Poarum and from the conidia of Peronospora parasitica and Peni-
dllium glaucum are indifferent.

Phototaxis. A phototactic reaction has been observed by Strasburger
in the zoospores of Chytridium vorax, and by Wager in those of Polyphagtis
Euglenae. Both these species parasitize motile green organisms, Chytridium
infecting Chlamydococcus pluvialis, and Polyphagus, Euglena viridis. The
host organisms react to light since they obtain their carbon supplies by
photosynthesis, and the phototactic reaction of the parasite brings it into the
region where the hosts are to be found.

Formative Influence of Light. Irrespective of phototropic response the
formative influence of light is important. Buller found that the sporophores
of Polyporus squamosus, though quite irresponsive to the direction of light,
fail to give rise to pilei unless illuminated. The same is true of many other
Hymenomycetes, including those which, like Lentinus lepideus and the
species of Coprinus mentioned above, are positively phototropic. In many
cases only a brief period of illumination during the early stages of develop-
ment is essential. Similarly, light appears to stimulate the development of
ascocarps in certain Ascomycetes, and cultures may remain sterile in dark-
ness or very dim light.

32 INTRODUCTION [CH.

On the other hand Stevens and Hall found that the pycnidia of Phyllo-
sticta sp. were irregularly scattered in continuous darkness but developed in
regular concentric zones when exposed to the alternation of dayand night; the
rudiments of the pycnidia in this case are laid down mainly during the night.

Geotropism. The influence of gravity has been very inadequately studied
among the lower fungi, little having been done since Sachs, in his Lectures
on the Physiology of Plants in 1882, described the sporangiophores of Mucor
and Phycomyccs as bending up and the rooting hyphae down ; he worked
with filaments extending in all directions from a suspended piece of bread.
Kny in 1881 reported that the mycelia of Mucor Mncedo and RJiizopus nigri-
cans and also that of Eurotium repens are indifferent to gravity, and Miyoshi
denied any geotropic reaction in his fungi.

Davvson in 1900 found that the stromata of Poronia punctata, a copro-
philous pyrenomycete, show a well-marked negatively geotropic reaction
from the earliest stages of their development and the same will probably
prove true of other forms with upright stromata or with stalked fructifications
like the Helvellales and many Pezizales.

Among the Hymenomycetes negative geotropism was first recorded by
Sachs in 1860, and soon after by Hofmeister in 1863. In stipitate forms the
stalk is always negatively geotropic as soon as the pileus develops, though,
in some of the Coprini and in Lentinus lepidens, this may be preceded, as
already seen, by a phase in which light is the directive influence.

Buller in 1909, and Streeter in the same year, showed that the geotropic
response is of the nature of a gradual adjustment. The growing stalk swings
beyond the vertical line, changes its direction and swings across it again,
passing the vertical two or three times before it comes to rest. Curiously
enough this method is followed in Amanita crenulata, in which the stalk
reaches its full development in. twenty-four hours, although there is not time
for a complete adjustment, and the sporophore often comes to rest beyond
the vertical line. The young stipe in Amanita elongates throughout its
length until more than half grown ; the zone of most rapid elongation is just
below the pileus, it finally becomes narrower and narrower until growth
ceases. Streeter was able to locate the perceptive region in the stipe,
not in the pileus. Amanita showed a definite geotropic response when
placed in a horizontal position for only one minute before being rotated on a
klinostat. When stimulation lasted for a shorter period (15 or 30 seconds)
no upward curvature ensued but a spiral curve was formed in the direction
in which the klinostat moved. The latent period of young, vigorous
specimens is about 40 minutes.

In the stemless Hymenomycetes, as in the stipitate forms, the orientation
of the pileus takes place in response to gravity. This may be seen on any old
stump where the bracket-shaped species of Tlulephora, Stereum, Polyporus

i] REACTIONS TO STIMULI 33

or Polystictus grow out as horizontal plates. Hasselbring found that the fruit
bodies of Polystictus cinnabarinus , when rotated on a klinostat during their
development, were no longer differentiated into a dorsal sterile and a ventral
fertile region, but that hymenial tubes were formed over the whole surface.
Alike in the Hydnaceae, Agaricaceae and Polyporaceae the trama plates
of the fertile region are positively geotropic. In stemless forms this reaction
is responsible for the orientation of the hymenium ; it may be particularly well
seen in some of the Hydnaceae where the spines grow downward whatever
the orientation of the sporophore, and it could doubtless be demonstrated
also in Tremellodon among the Tremellaceae. In stipitate species it appears
as a supplementary reaction coming into play if further adjustment is needed
when the stipe is fully grown. The limitations of the method in the gill-
bearing fungi are obvious for, if the pileus is oblique and the gills undergo much
curvature, they become crowded together and interfere with spore dispersal.

REACTIONS TO STIMULI : BIBLIOGRAPHY

1869 HOFMEISTER, W. Ueber die durch die Schwerkraft bestimmten Richtungen von
Pflanzentheilen. Jahrb. wiss. Bot. iii, p. 92.

1877 BREFELD, O. Ueber die Bedeutung des Lichtes fur die Entwickelung der Pilze.
Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, p. 127.

1878 STRASBURGER, E. Wirkung des Lichtes und der Warme auf Schwarmsporen. Jena.

1879 VON SACHS, J. Ueber Ausschliessung der geotropischen und heliotropischen Kriim-
mungen wahrend des Wachsens. Arb. d. Bot. Inst. Wiirzburg, ii, p. 209. Or Lectures
on the Physiology of Plants. Eng. Trans., 1887. Clarendon Press, Oxford, p. 700.

1881 DE BARY, A. Untersuchungen iiber die Peronosporeen und Saprolegnieen und die

Grundlagen eines naturlichen Systems der Pilze. Beitr. zur Morph. und Phys. d.

Pilze, iv, p. 85 of separate.
1 88 1 KNY, L. Ueber den Einfluss ausserer Krafte auf Anlegung von Sprossungen

thallosser Gebilde. Sitz. Bot. Ver. Brandenburg, xxiii, p. 8.
1894 MIYOSHI, M. Uber Chemotropismus der Pilze. Bot. Zeit. Hi, p. i.
1900 DAWSON, M. On the Biology of Poronia punctata (L.). Ann. Bot. xiv, p. 245.
1902 CLARK, J. F. On the toxic properties of some copper compounds, with special

reference to Bordeaux Mixture. Bot. Gaz. xxxiii, p. 45.
1906 FULTON, H. R. Chemotropism of Fungi. Bot. Gaz. xli, p. 81.

1906 PFEFFER,W. The Physiology of Plants. Eng. Trans. Clar. Press, Oxford, iii, p. 183.

1907 HASSELBRING, H. Gravity as a Form-Stimulus in Fungi. Bot. Gaz. xliii, p. 251.

1908 BALLS, W. L. Temperature and Growth. Ann. Bot. xxii, p. 558.

1909 BULLER, A. H. R. Researches on Fungi. Longmans, Green & Co., London.
1909 STEVENS, F. L. and HALL, J. G. Variations of Fungi due to Enviro

Gaz. xlviii, p. I.
1909 STREETER, S. G. The Influence of Gravity on the Direction of Growth of

Bot. Gaz. xlviii, p. 414.
1914 JOLIVETTE, H. D. M. Studies in the Reactions of Pilobolus to Light S

1914 ROBINSON,' W.' Some Experiments on the Effect of External Stimuli on the Sporidia

of Puccinia malvacearum (Mont.). Ann. Bot. xxviii, p. 331.
1914 WAGER, H. Movements of Aquatic Micro-Organisms in Response

Forces. The Naturalist, No. 689, p. 171.

1916 GRAVES, A. H. Chemotropism in Rhizopus nigricans. Bot. Gaz. l.xn, p.
1918 PARR, R. The Response of Pilobolus to Light. Ann. Bot. xxxn, p. i

G.-v.

CHAPTER II

ASCOMYCETES

The Ascomycetes include over 15,000 species, all of which, excepting only
the yeasts, possess a well-developed mycelium of richly branched and septate
hyphae. The cells of the mycelium may be uninucleate, as in the Erysi-
phaceae and species of Chaetomium and Sordaria, or they may contain
a few or several nuclei; energetic growth and a rapid succession of nuclear
divisions often cause the nuclei of multinucleate elements to be arranged
in pairs.

Multiplication may take place by means of conidia, oidia, or chlamydo-
spores, but the characteristic method of reproduction is by ascospores or
spores produced in the interior of a mother-cell or ascus.

The Ascospores. In the large majority of species the ascospores are
elliptical in outline, but they may be spherical or globose, as in Ascodesmis
nigricans, long and narrow (filiform) as in species of Cordyceps or Claviceps,
or of intermediate form. They contain a densely granular or reticulate
cytoplasm in which one or more oil drops are usually present. The epispore
may be smooth or variously sculptured ; in several cases it is verrucose, in
others reticulate; the latter arrangement is particularly well seen in Asco-
bolus furfumceus.

All ascospores are colourless when first formed; they may remain so
when ripe, or may assume a variety of colours.

The young spore is unicellular and uninucleate1. Before it is set free the
nucleus may divide, and this division is frequently accompanied by wall-
formation so that, like the asexual spore of Pellia, the a'scospore may be
regarded as undergoing premature germination. Divisions may take place
in three dimensions, so that the spore is muriform (fig. i), or the septa may
be all in one plane so that it consists of a row of cells (fig. 2 a).

The multicellular spore thus produced may break up into its constituent
cells, which proceed with their development independently, or it may function
as a single structure.

In examining any of these characters or in measuring the size of the
spore it is essential to deal with fully mature examples since the distinctive
sculpturing, pigmentation, etc., may not appear till late in development.
Spores which have escaped naturally from the ascus may be used with safety.

* Lewton Brain (Ann, Bot. 1901) describes the spores of Cordyceps ofkioglossoides as multi-
nucleate from their first inception.

CH. II]

ASCOMYCETES

The Ascus. The ascus or mother-cell of the spores is a spherical oval
club-shaped, or almost cylindrical organ with a narrow, more or less elongated

Fig. i. Pleospora sp.; germinating spores, x 1000.

base. When moderately young it contains a single nucleus which undergoes
three karyokinetic divisions giving rise to
eight daughter nuclei (fig. 3). Asci of the a
short, stout type are full of dense cyto-
plasm ; in the relatively cylindrical forms
the ends are usually vacuolate, but a broad,
granular belt fills the middle region and
contains the nuclei. -The spores are cut
out by free cell-formation so that a certain
amountof cytoplasm remainsoutside them,
constituting the epiplasm. It becomes
charged with glycogen and other food
substances, and is a source of supply to
the developing spores.

In the vast majority of cases the mature
ascus contains eight spores, but in a certain
number of species, though eight nuclei are
produced, only one or a few are utilized as centres of spore-formation.
Thus a single spore is sometimes developed in Tuber, two is the regular
number in Phyllactinia, and four in many of the Laboulbeniales ; in
Bulgaria poly morpha eight spores are initiated but only four reach maturity.
In Endomyces it is probable that the ascus nucleus divides only twice,
and the four spores utilize all the available nuclei. On the other hand ad-
ditional nuclear divisions sometimes precede spore-formation so that the

3—2

Fig. 2. Spores of a. Geoglossttm diffortne
Fr.; b. Delitschia furfitracea Niessl;
c. Rhytisma aceritium (Pers.) Fr.; d.
Chaetomium Kuntzeanum Zopf ; f.
Podospora minuta (Fuck.) Wint. ;
x 500.

ASCOMYCETES

[CH.

number of spores is increased. There are sixteen or thirty-two in the species

of Rhyparobins, sixteen to
sixty-four in Podospora pleio-
spora, and in Podospora curvi-
colla one hundred and twenty-
eight.

The arrangement of the
spores in the ascus is usually
constant for a given species ;
they may be uniseriate, in a
single row; biseriate, in two
rows somewhat irregularly
placed, in which case they are
often uniseriate when young;
fasciculate if long narrow
spores are arranged in a pa-
rallel bundle; or inordinate if
they show no regular arrange-
ment. In the simplest forms
the spores are liberated by the
decay of the ascus walls, and,
where a definite fruit body is
present, they remain for a
time enclosed by its outer
layers. In other cases, in-
cluding the majority of Dis-
comycetes and Pyrenomy-
cetes, the ascus opens explosively either by an irregular tear or by dehiscence
along a definite line, and the spores are shot out in a jet of liquid while the
deflated ascus sinks back to about half its size (figs. 4, 5). In forms with an
explosive mechanism the ascus often elongates considerably during the latter
part of its development; the spores are arranged at the upper end and either
float suspended in the fluid contents of the ascus, or are attached to the
apex and to one another by cytoplasm ic strands (Sordaria, Podospora,
fig. 24

The explosive ejection of spores from different asci may be simultaneous
or successive ; in a certain number of forms with an exposed hymenium
of parallel asci (Pezizales, Helvellales, Exoascales) successive discharge
takes place under moist conditions, but any disturbance leading to rapid
loss of water causes the simultaneous liberation of a number of spore
masses, so that the cloud of spores is visible even to the naked eye. This
phenomenon, which is known as "puffing," may be brought about under

Fig. 3. Humaria rutilaits (Fr.) Sacc.; hymenial layer
showing asci and paraphyses in various stages of develop-
ment, x 400.

II]

ASCOMYCETES

37

conditions of moderate dryness, such as occur out of doors on a fine autumn
day by shaking the fructifications, or even by currents of air set up bv
walkmg past them. It can be initiated, as de Bary pointed out, when

Fig. 4. Mitrula laricina Mass. ;
development and ejection of
biseriate spores, x 600.

Fig. 5. Sepultaria coronaria Mass.; uni-
seriate spores ; ascus opening by a lid ;
branched, septate, clavate paraphyses;
x6oo.

isolated asci lying in water are suddenly exposed to the action of glycerine
or alcohol, and is clearly due to alterations of tension affecting a
number of asci at about the same stage of development. After the fructifi-
cation has puffed once or a few times a rest of some hours during which

533SO

8 ASCOMYCETES LCH-

resh asci reach maturity is necessary before the phenomenon can be

Ascocarp In a few genera, asci are developed singly on the
mycelium, but in the great majority of cases they arise in closely associated

groups, and are surrounded
by a protective wall or peri-
dium of sterile filaments so
that a definite fructifica-r
tion, the ascocarp or asco-
phore, is formed. This
structure is usually more or
less spherical and com-
pletely closed in the young
stages; it may retain this
form at maturity, opening
only by the decay or irregu-
lar splitting of its walls, it
may assume a flask-shaped
outline and open by a ter-
minal poreorostiole(fig.6),
or it may spread out to form
a cup in the concavity of
which the asci are fully ex-
posed(fig. 7). Totheclosed
or flask- shaped forms the
term perithecium is ap-
plied, the cup and its vari-
ants are known as apo-
thecia. Inthesimplerasco-
carps the asci are irregu-
larly scattered ; in the apo-
thecia and flask-shaped perithecia they are regularly arranged, forming a
more or less parallel series and intermingled with paraphyses. /-y

The Paraphyses. The paraphyses of the Ascomycetes are slender hairs,
of about the same length as the asci ; they usually develop earlier than the
latter, and have a protective and possibly a nutritive function ; in the
simpler ascocarps their place is taken by the inner layers of the sheath.
The paraphyses are often clavate or club-shaped in form with a rather
swollen tip (fig. 5), sometimes cylindrical (fig. 4) or pointed (lanceolate),
or sometimes with curled or twisted ends; they may be simple or branched,
septate or continuous, hyaline or provided with coloured contents ; orange
red granules are common and often give a brilliant tinge to the whole

Fig. 6. Sordaria sp.\ ascocarp in longitudinal section
showing asci, paraphyses and periphyses ; x 400.

II]

ASCOMYCETES

39

hymenium. In Desmotascus\ a pyrenomycetous fungus parasitic on Bromelia
the paraphyses are replaced by a thin-walled pseudoparenchyma recalling
the arrangement in the higher Plectomycetes.

The Peridium. The peridium or wall of the ascocarp is a weft of sterile
hyphae in which the individual
filamentsare sometimes clear-
ly distinguished, sometimes
closely interwoven to form a
pseudoparenchyma; the walls
of the outer cells are some-
times considerably thickened
and may be variously pig-
mented ; in many cases they
give rise to hairs (Lacknea,
Ckaetomium) or other ap-
pendages (Erysiphaceae).

Alternation of Genera-
tions. The Ascomycetes show /"^C^
a well-marked alternation of
generations modified by the
wide occurrence of apogamy
in the group.

In forms where fertiliza-
tion is still retained the myce-
lium arising from the germination of the ascospores gives rise to the sexual
organs. These show a considerable variety of form and in the vast majority
of cases are clearly differentiated as male and female structures. The male
branch consists of an antheridial hypha or stalk and a terminal antheridium
which, in some of the more complex forms, is detached and carried by the
wind or otherwise as a spermatium. The female branch or archicarp
possesses a stalk of one or more cells, bearing the oogonium ; sometimes
a terminal trichogyne is present by means of which connection is established
between the oogonium and antheridium. The term ascogonium has been
used at various times as the equivalent of archicarp or oogonium, or to
indicate the oogonium after fertilization, but it does not appear essential in
any of these senses. In certain cases where the walls are partly broken
down between several cells in the middle of the archicarp, the term oogonial
region is applied to them. An archicarp of this type is sometimes known
as a scolecite. The gametangia each contain one or several nuclei, but
the contents are in no case rounded off as independent gametes. The

Fig. 7. Lachnea stercorea (Pers.) Gill.; ascocarp in longi-
tudinal section showing young asci and paraphyses ; the
oogonium is still recognizable; x 160. a. sheath, />. para-
physes, c. ascus, d. ascogenous hyphae, e. oogonium,
/. stalk of archicarp.

1 1919, Stevens, F. L., " Perithecia
Ixvii, p. 422.

ith an Interfascicular Pseudoparenchyma," Bot. Gautte,

40 -A9COMYCETES tCH'

contents of the antheridium enter the oogonium which, as a result of this
association, gives rise in nearly every case, with or without preliminary
septation, to a number of filaments, the ascogenous hyphae, from the tips
of which asci grow out. The ascogenous hyphae thus constitute the spore
phyte while the vegetative mycelium, on which the sexual organs are borne,
is the gametophyte. The gametophyte gives rise to the peridium and the
paraphyses, and on it the various accessory spores are produced.

Early Investigators. The history of the minute study of the Asco-
mycetes may be said to have begun in \jg\ when Builliard, in his Histoire
des Champignons de France, described the asci as female organs, and sug-
gested that their fertilization was accomplished by some substance emanating
from the paraphyses.

In and after 1863 the classical researches of de Bary and his pupils
established the existence of male and female organs at the beginning of
ascocarp formation in a number of species. They brought forward evidence
of the occurrence of fertilization in some cases and in others of development
without an antheridium (parthenogenesis) or without either male or female
organs (apogamy), they showed that the paraphyses and sheath of the
ascocarp arise from the vegetative mycelium and the ascogenous hyphae
from the female branch. The conclusions reached by de Bary are summed
up in the fifth chapter of his book on the 'Comparative Morphology and
Biology of the Fungi, Mycetozoa and Bacteria, first published in 1 884, and
they have been largely confirmed by subsequent investigation.

In 1 88 1 Eidam observed the formation of the ascus in the very simple
genus Eremascus, where it arises from two separate filaments which become
intertwined and fuse at their tips.

De Bary's views were extensively criticized, especially by van Tieghem
and Brefeld, who both denied the occurrence of sexuality in the group.
These and other writers sought to explain the antheridial filament as part
of the sheath, and the archicarp as a precocious ascogenous hypha, or, in
certain lichens, as a boring or a respiratory organ. Brefeld was the author
of a scheme of classification, which, if too rigid to endure the test of sub-
sequent work, was at least exceedingly convenient. With it, and especially
in the text book of his disciple von Tavel (1892), his view that the higher
fungi lacked sexuality was widely disseminated.

Cytology. In the meantime considerable advances were being made in
the study of cytology and of the cytological methods necessary for the exami-
nation of minute forms. De Bary, in 1863, had recognized the presence of a
single or definitive nucleus in the immature ascus of Pyronema confluens and
some other species, and the successive appearance as development proceeded
of two, four, and eight nuclei. He found that the eight nuclei lay at more or
less equal distances apart, and that each became surrounded by a mass of

n]

ASCOMYCETES

Fig. 8. Humaria rutilans (Fr.) Sacc.; a. ascogenous
cell containing two nuclei cut off from the uninu-
cleate terminal cell and stalk ; b. fusion in the ascus,
the nuclei are just passing into synapsis; both
x 1875.

cytoplasm forming the primordium of a spore. In 1879 Schmitz observed
nuclei in the vegetative cells of several Ascomycetes, and in 1893 Gjurasin in
Pesiza vesiculosa recognized that the divisions in the ascus are karyokinetic.
The Fusion in the Ascus. In 1894, Dangeard showed in Pesiza vesi-
culosa and other forms with a well-developed fructification, that the ascus at
its first inception is binucleate and that the two nuclei subsequently unite
to form the definitive nucleus of de Bary. He at first believed that the ascus
was produced in these cases, as in
Eremascus, by the fusion of two
independent filaments, but he
was soon able to ascertain that
the young ascus arises, not by the
union of two separate hyphae, but
from the penultimate cell of a
single recurved filament. The
apex of this filament receives two
nuclei which undergo a simulta-
neous karyokinesis, so that four
are formed. One of these lies at
the tip of the hypha, and one
passes back into the lower part, while the other two lie in the curved
portion, and become separated from their sister nuclei by transverse walls
(fig. 8). The terminal cell of the hypha thus contains a single nucleus
and the penultimate cell is regularly binucleate ; it grows out laterally
to form the ascus, and its two nuclei fuse soon after they come together.

The fusion in the ascus was the first nuclear fusion observed among
Ascomycetes and its discoverer, Dangeard, accepting it as a sexual process,
regarded the ascus as an egg, and the sexual apparatus described by de
Bary and his pupils as at most vestigial. It is probable that this view was
influenced by his first opinion that the ascus arose from the fusion of two
separate filaments, but it was not modified by his subsequent discovery of
the true process.

Fertilization. In the following year (1895) both de Bary's observations
and those of Dangeard were confirmed by Harper, working on the common
mildew Sphaerotheca Humuli^. Harper saw the development of a uninucleate
oogonium and a uninucleate antheridium. He observed the passage of the
male nucleus into the oogonium and the fusion there of the sexual nuclei.
After fertilization the oogonium underwent septation, giving rise to a row
of cells of which the penultimate contained two nuclei, and, after these had
fused, developed into the ascus (fig. 9). He thus demonstrated that in this
fungus there is a normal fusion of male and female nuclei, followed by a

i Sphaerotheca Humuli (DC.) Burr.= Sphaerotheca Castagiiei Lev.

ASCOMYCETES

[CH.

42

second fusion in the ascus, and in the following year he recorded the same

process in Erysiphe Polygoni.

Fig. o Spkatrothtca. Hwnuli (DC.) Burr.; a. and b. antheridium and oogonmm ; c. entrance of male
nucleus- d fusion in oogonium, antheridium without nucleus; e. fusion nucleus in oogonmm;
/ and g. septation of oogonium ; h. two nuclei in ascus ; *. ascus after nuclear fusion ; after Harper.

In 1900, Harper observed fertilization in the oogonium of Pyronema
confluens; here, however, the gametangia are both multinucleate and fer-
tilization consists of the fusion in pairs of a large number of male and female
nuclei. Many asci are produced, each from a recurved filament in the pen-
ultimate cell of which a second nuclear fusion occurs.

Development of the Ascus. Though the young ascus, so far as obser-
vation goes, is almost invariably binucleate and the seat of a nuclear fusion,
the details of its formation are not always the same. In 1905 Maire showed
that in Galactinia snccosa and occasionally in other forms a series of three
or four binucleate cells is produced at the end of each ascogenous hypha.
The nuclei of the terminal cell undergo simultaneous division and two are cut
off at the apex by a transverse wall. These fuse and the cell containing them
becomes the ascus. Harper in Erysiphe, and other authors in various other
plectomycetous fungi have found that any cell of an ascogenous hypha, if it
contains two nuclei, may give rise to an ascus without preliminary nuclear
division.

In some of those species in which the ascus is derived from a binucleate
penultimate cell the curvature of the hypha is so great that the uninucleate
terminal cell lies in contact with the stalk cell of the ascus. When this
happens the terminal and stalk cells sometimes fuse, a nucleus wanders from
one to the other, and the cell thus provided with two nuclei grows out as a

IJ] ASCOMYCETES

continuation of the ascogenous hypha, and gives rise to fresh asci (fig IO)
This process was first recorded in 1908 for Humaria rutilans and has since
been observed by McCubbin in Helvetia elastica, by Carruthers in HelJL
m#« and by Claussen in Pyronema confluens. It suggests either that some
advantage is to be derived from an absence of relationship between the
nuclei which fuse in the ascus, or that a scheme of rigid nuclear economy
is in force. The former hypothesis is somewhat weakened by the fact that
no means of avoiding close relationship appear to exist in the Plectomycetes
Meiosis. Very soon after the ascus is cut off, preparations are made
for the fi^t nuclear division, which was shown in 1905 by Guilliermond,
Harper and Maire, working independently on various fungi, to be heterotype
and to be followed by a second which is homotype in character- their

Fig. 10. Humaria rutilans (Fr.)
Sacc. ; an ascus (a) the terminal cell
connected with which has continued
its growth and given rise to another
ascus (b) from the terminal cell of which
a third ascus (c) has arisen, x 1250.

7K6**

Fig. n. Humaria rutilans (Fr.) Sacc.; a. asco-
genous hypha showing sixteen chromosomes in
. each nucleus, x 1950; b. fusion nucleus of ascus
passing out of synapsis, x 1 300 ; c. fusion nucleus
of ascus showing sixteen gemini, x 1950.

observations have since been widely confirmed by a number of investi-
gators, and synapsis, the secofid contraction and the formation of typical
gemini have been seen, as well as the reduction of the chromosome number.
Thus in Humaria rutilans, which the exceptionally large nuclei render
a convenient subject of study, each of the fusing nuclei possesses sixteen
chromosomes (fig. 1 1 a), so that the definitive nucleus has thirty-two ; after
meiosis is complete sixteen can be counted in each daughter nucleus. This
fungus is somewhat exceptional in that synapsis begins separately in each
of the two nuclei of the young ascus before they fuse (fig. 8 b) indicating

44

ASCOMYCETES

[CH.

a"i<e ends of the nuclear area (fig. ,2)'. In other invest.gated spec.es
only one synaptic knot is formed.

Fie 12 Helvetia crispa Fr.; fusion nuclei in ascus showing
the contraction of the chromatin in two separate masses,
x 2000 ; after Carruthers.

The third Division in the Ascus. The meiotic phase is followed by a
third division in which a further change in the chromosome number has

been described. This was first re-
corded by Maire, in 1905, in the
case of Morchella esculenta, and,
with certain variations in detail,
in two other Discomycetes. In M.
esculenta there are eight chromo-
somes in the first telophase, and
four in the third, and also in the
subsequent nuclear division which
takes place in the spore. The next
case to be brought forward was
Humaria ruti/ans, in 1907, and
two more (Ascobolus furfuraceus
and Pyronema confluens) were re-
corded by Dangeard in the same
year (fig. 13). It was soon after
suggested (Eraser, 1908) that the
halving of the chromosome num-
ber which had been observed in these species constituted a second reduction
phase, bearing the same relation to the fusion in the ascus that meiosis bears
to the fusion of the sexual nuclei. For this reduction the term brachymeiosis

1 This arrangement may occasionally be found in Humaria rutilans, and occasionally also the
two nuclei of the young ascus proceed as far as the second contraction without undergoing fusion.

Fig. 13. Ascobolus fitrfitraceus Pers.; a. early ana-
phase of the first division in ascus showing 14 of
16 daughter chromosomes; b. metaphase of the
second division showing four chromosomes ; c. third
division showing four; after Dangeard.

II]

ASCOMYCETES

45

was proposed. The occurrence of a brachymeiotic reduction has since been
observed in several other fungi, and has also been in several cases denied.

Chromosome Association. There are a number of fungi, of which
Phyllactinia Corylea is perhaps the most fully studied, in which no change in
the chromosome number takes place
throughout the life-history. In Phyl-
lactinia, Harper showed in 1905 that
the chromosomes remain visible in
strands attached to the central body
throughout the resting stages. In
each of the nuclei of the developing
ascus eight such strands can be
clearly seen (fig. 14), and their asso-
ciation in pairs can be followed, so
that they appear as eight strands in
the spireme stage, and as eight
chromosomes on the spindle. In the
smaller sexual nuclei Harper found
a similar arrangement. It would
thus appear that in this fungus chro-
mosome association follows directly
on nuclear fusion, so that the fusion
of two nuclei with n univalentstrands
produces not a nucleus with 2n
strands, but one with n bivalent strands. If this is so in the oogonium the
nuclei which fuse in the ascus will each possess n bivalent chromosomes,
and the definitive nucleus will show not 4^ univalerrt chromosomes but «
which are quadrivalent. In the same way neither meiosis nor brachymeiosis
will affect the chromosome number, but will affect only the valency of the
chromosomes. This is the case in Phyllactinia, where in all stages of the
three divisions in the ascus, eight chromosomes are found. It must be
noted, however, that in cases where no fusion occurred in the life-history
except that which immediately precedes meiosis, the chromosome number
would similarly remain unchanged ; the latter interpretation has been
urged as evidence that forms in which the chromosome number is unaltered
throughout the life-history are therefore necessarily without a fusion in the
oogonium.

The Theory of a Single Nuclear Fusion. The possibility that the
fusion in the ascus is the only nuclear fusion in the life-history of the
Ascomycetes, and represents the postponed union of sexual nuclei which
had become associated in fertilization was first mooted by Raciborski in
1895, in a letter to Professor Harper, and was published in 1896. This view

Fig. 14. Phyllactinia Corylea (Pers.) Karst.;
fusion nuclei in ascus showing eight chromatin
strands attached at a common point; after
Harper.

46

ASCOMYCETES

[CH.

received a considerable impetus in 1907 and 1912, from the work of Claussen
on Pyronema confluent. According to the latter author the male nuclei enter
the oogonium and pair with the female nuclei, but do not fuse with them.
The sexual nuclei pass in pairs into the ascogenous hyphae (fig. 15), and

eventually they or their descendants
fuse in the ascus. For Claussen, there-
fore, there is a single fusion (that in
the ascus) and a single reduction (the
meiotic) in the life-history of Pyronema.
His interpretation has been followed
by Schikorra on Monascus, by Faull on
Laboulbenia, and by Ramlow on Asco-
bolusimmersusw&Ascophamiscarneus.
The last-named author figures certain
"fusions" in the oogonial region of his
fungi, but regards them as pathological.
Claussen's hypothesisdemandsthat
the attraction between the sexual
nuclei, though not sufficient to cause
fusion, yet holds them together in the
multinucleate ascogenous hyphae and
is transmitted to their descendants
when nuclear division has occurred1.
It is based on three chief grounds :

1 i ) the failure to observe fusions in
the oogonium or their interpretation,
if found, as pathological phenomena;

(2) the recognition of as many
chromosomes in the third division in
the ascus as in the first;

(3) the observation of paired nuclei
in the ascogenous hyphae.

The first of these grounds has a mainly negative value ; in regard to
the second, further investigation is very much to be desired ; the statement
of the chromosome number without figures is of little value, nor is any
figure of the third division significant except that of the late anaphase ; in the
earlier stages chromosomes are scattered about the spindle, so that there is
no criterion by which a metaphase showing eight undivided chromosomes
can be distinguished with surety from an early anaphase showing two sets of

1 A comparison is sometimes instituted between the sporophyte of the Ascomycetes and that of
the rusts. In the rusts, however, each pair of nuclei is enclosed in a separate cell and the hypothesis
of nuclear attraction throughout the vegetative phase is accordingly not required.

Pyronema cotiflttens', sexual apparatus
and paired nuclei in the ascogenous hyphae;
<7. antheridium ; b. trichogyne ; c . oogonium ;
d. ascogenous hyphae ; x 1040; after Claussen.

ASCOMYCETES

47

four. Further the adhesion of chromosomes already described for Phvllac-
tima must not be forgotten.

The occurrence of paired nuclei in the ascogenous hyphae was thus the
most important evidence in favour of Claussen's view until in 1916 Welsford
showed that the nuclei even of gametophytic, multinucleate hyphae are
habitually paired if rapid growth and division are taking place; this is due
to the fact that mitoses follow
one another so rapidly that the
daughter nuclei of any parti-
cular division have not time to
move apart, before they them-
selves divide. Such paired nu-
clei have often previously been
figured though without attract-
ing special attention ; excellent
examples are to be seen in
Nichols' paper on the Pyreno-
mycetes1 or in Ramlow's more
recent work on Ascophanuscar-
neus*. It seems hardly possible
to place a different interpreta-
tion on the nuclei which lie
close together in the ascoge-
nous hyphae.

According to our present
knowledge of the cytology of
the Ascomycetes there are two
nuclear fusions in the life-
history of these plants.

The Significance of the Fusion in the Ascus. If this be the case it
remains to consider the significance of the fusion in the ascus. The presence
of more than one nucleus in this cell, destined to be one of the largest in
the life-cycle of the fungus, is hardly surprising especially in coenocytic
forms. In uninucleate species it forms part, as Harper pointed out in 1905,
of the quantitative adjustment frequently observed between cytoplasm and
nuclear material. But this nucleo-cytoplasmic relation does not explain why
fusion should take place between the nuclei concerned or why they should
be regularly two in number3. It is possible that, crowded as they are in the
newly constituted ascus, the nuclei merely flow together as they make ready
for the prophases of division. Whatever may have been the determining

1 Sot. Gaz. 1896, xxii, pi. xv, fig. 32. 2 Myc. Centralbl. 1915, pi. i, fig. n.

3 In Humaria ruttlans, however, and doubtless in other forms, young trinucleate, and quadri-

nucleate asci are found.

16. Ascophanns carneus Pers.; germinating spores
with paired nuclei in the germ-tubes, x^o; after
Ram low.

48 ASCOMYCETES [CH.

cause of the second fusion in the ancestors of our present Ascomycetes, it
is clear that in the forms now extant the existence of a second reduction
must be an important factor; in this respect the organism may well be
moving in a vicious circle.

Pseudapogamy. The above, at any rate, seems to be the case in respect of
the much more important fusion of the sexual nuclei. In Humaria granulate
no antheridium is developed, and the female nuclei, as recorded by Blackman
and Fraser in 1906, fuse in pairs in the oogonium before passing into the
ascogenous hyphae. The same state of affairs was observed by Welsford in
Ascobolus furfuraceus in 1907, and by Cutting in Ascophanus carnens and
Dale in Enrotium repens in 1909; it is difficult to see how any important
physiological benefit can ensue from the union of closely related nuclei
developed in the same cell; the determining cause would seem to be the
need of preparation for the meiotic phase already established in the life-
history. In Lachnea stercorea an antheridium is present and fuses with the
terminal cell of the multicellular trichogyne, but the male nuclei never
reach the oogonium, and here also the female nuclei unite in pairs.

In Humaria rntilans matters have gone still further; not only is the
antheridium lacking but the archicarp also is not developed. Nuclear fusion,
sometimes preceded by the migration of one of the fusing nuclei, takes place
in the vegetative cells of the developing apothecium. The cells containing
fusion nuclei give rise to ascogenous hyphae, while those in which fusion has
not occurred produce the paraphyses and the sheath. A similar state of affairs
has been reported by Carruthers in Helvetia crispa, and evidence of its occur-
rence in Poly stigma rubruwhas been noted by Blackman and Welsford/

These reduced forms, belonging respectively to de Bary's categories of
parthenogenesis and apogamy, have thus proved to be pseudapogamous
in the sense of Farmer and Digby1, since in them normal fertilization is re-
placed by the union in pairs of female or vegetative nuclei. Meiosis takes
place as usual.

Spore-Formation. After the third division in the ascus, preparations
for spore-formation begin. This stage was first described in detail by Harper
in 1895, and was subsequently elucidated by him in other papers, and
especially in his very full study of the mildews in 1905. As the third mitosis
comes to an end the eight daughter nuclei, or those of them about which
spore-formation is to take place, become pear-shaped, a beak being pushed
or pulled out from each- the centrosome lies at the tip of the beak and from
t spread the astral rays, to the activity of which Harper is inclined to attri-
bute the formation of the beak. As development proceeds, these rays become
folded over so that they extend past the nucleus, and Harper describes them

:ombming side by side to form a continuous, broad, umbrella-like mem-

1 Ann. Bol. 1907, xxi, p. 191.

n]

ASCOMYCETES

49

brane which gradually closes in to produce, by further marginal growth, the
ellipsoidal plasma membrane of the spore. In this way the whole body of
the spore is cut out from the undifferentiated cytoplasm of the ascus by a
process of free cell formation, and its membrane is formed by the fusion of
the astral rays.

A different account of the development of the membrane was given by
Faull in 1905. According to his investigations the spore is cut out by the
gradual differentiation from the centrosome downwards of a limiting layer
of hyaline or finely granular cytoplasm, in the production of which the
astral radiations play no part.

. In many of the Discomycetes, however, the importance of the aster in
spore-formation is very marked, and the spore is outlined by radiations
passing out from the centrosome (fig. 17). These radiations, in Humaria

Fig. 1 7. Humaria rutilans (Fr.) Sacc. ; stages of spore formation,
xi875.

rutilans, Peziza vesiculosa, or Lachnea stercorea, doubtless indicate the paths
of altered substances emanating from the centrosome as a centre of activity,
and flowing back past the nucleus as the developing beak pushes into the
cytoplasm. As these substances increase a membrane is formed, and the
spore, or the part of it near the centrosome, is cut out. In the delimitation
of the region remote from the centrosome the vacuoles in the cytoplasm of
the ascus may take part. These vacuoles are especially plentiful in Ascobolns
furfuraceus, and in this fungus their share in spore-formation is important.
After the spore is delimited the differentiation of its wall is largely due to
the epiplasm, and is not complete till the ascus is almost ripe.

Phylogeny. The recognition of the specialized character of the ascus
has led to a general assumption of the monophyletic origin of the Ascomy-
cetes, and speculation as to their possible ancestry has run along two main
lines. They have been regarded as derived eitherfroma phycomycetous group,
or from the Red Algae or the ancestors of the latter. An independent origin
either among the flagellates or the Green Algae has also been proposed.

The suggestion of a floridean relationship was first made by Sachs, in
1874, and has recently been supported by Harper, Dodge1 and ,

1 Bull. Torrey Bot. Club, 1914, xli, P- '57-

4

5o ASCOMYCETES [CH.

comparison of the sporogenous filaments of a Red Alga with the ascogenous
hyphae, of the algal trichogyne with the unicellular trichogynes of some
Ascomycetes, and of the spermatia in the two groups is certainly suggestive,
but it assumes that the trichogyne in the two cases is homologous, a very
doubtful point, and it involves the corollary that all the simpler Ascomycetes
are derived by reduction from the more complex.

The derivation of the group from the Phycomycetes was upheld by
Winter in 1874, by de Bary in and after 1881, by Brefeld in 1889, and lately
by Atkinson1 in 1914.

Any conclusion however, as to either the origin or the inter-relationships
of the Ascomycetes, must await a detailed knowledge of the development
of the ascocarp and of the morphology of the sexual apparatus in a much
larger number of species.

So far the development of the ascocarp throws little light on the problems
of phylogeny ; in the great majority of cases the ascogenous hyphae are
enclosed when young by a weft of gametophytic filaments, and, in the
simplest of such cases, this arrangement persists till the asci are ripe and
the gametophytic hyphae decay. In other cases there is a considerable
variation in the time and extent of the opening of the fructification, though
its mature form is of two main types. In view of this fact it is clear
that the Pyrenomycetes, in which the perithecium is flask-shaped, opening
by an ostiole, and the Discomycetes, in which the apothecium is typically
cup-shaped and wide open at maturity, are justified as form groups and this
long established arrangement is not contradicted by what we know of the
development of the sexual organs.

The Discomycetes show three types of sexual apparatus :

(1) The oval antheridium and somewhat elongated, coiled archicarp of
Ascodesmis. Here the archicarp ends in a one-celled trichogyne and the
unicellular oogonium becomes septate after fertilization and gives rise to a
few short ascogenous hyphae2.

(2) An oval antheridium, unicellular trichogyne, and more or less spherical
oogonium which does not undergo septation. This type is found in Pyronema,
and may be traced in Humaria granulata, and presumably in other forms
where a large oval cell has been seen at the base of the developing ascocarp.
It is present also in Lachnea stercorea, if the septate trichogyne of this species
can be looked upon as a secondary development. It is the characteristic
type of the Pezizaceae.

(3) A scolecite or stout septate archicarp, the distal cells of which form a
trichogyne and the proximal a stalk, while the middle region is multicellular,

1 Ann. Mis. Bot. Card. 1914, ii, p. 3I5.

* Another simple form is TMeMus, which shows certain suggestive analogies to Sphaerotheca,
but demands further investigation.

H] ASCOMYCETES 5I

the cells communicating by means of large pits, and one (Ascobolus furfura-
ceus} or more (Ascophamts carneus, Lachnea cretea, Rhizina undulatd) of them
give rise to ascogenous hyphae. This is the characteristic archicarp of the
Ascobolaceae and is found also in Lachnea cretea and in Rhizina undulata
as well as in Collema pulposum and some other lichens. Unfortunately the
details of normal fertilization are not yet available in these forms so that it
cannot be said definitely whether the oogonial region is multi- or unicellular
at the fertilization stage. In many cases fertilization is known to be "reduced"
and in the majority an antheridium has not been recorded. In Ascobolus
carbonarius, a small, spermatium-like, attached cell (the male conidium of
Dodge) has been observed in association with the tip of the trichogyne;
somewhat similar attached cells have been seen in Collema pulposum ; in
other lichens typical, detached spermatia have been described. Here the
type of maximum septation is reached and shows a septate trichogyne, an
oogonial region sooner or later septate, and a spermatium-like antheridium.

The second or spherical type may be derived very readily from the first;
the genera Ascodesmis and Pyronema are alike in the development of their
sexual organs and the structure of their sheath; the significant difference
between them lies in the spherical shape of the oogonium in Pyronema
which may well be responsible for the absence of septation. The third or
scolecitic type could also be derived through an increase of septation and
reduction in the size of the antheridium from Ascodesmis; the coloured spores
and reticulate epispore characteristic of that genus and of many Ascobolaceae
may be, as Massee suggests, a further indication of relationship.

The sexual apparatus of the Pyrenomycetes culminates in a septate
trichogyne, septate oogonial region and detached antheridium (spermatium)
so closely comparable with those of the discomycetous type of maximum
septation as to suggest some cross relationship between the groups. The
very distinct type of ascocarp, however, in Gnomonia, Poly stigma and other
Pyrenomycetes on the one hand, and in the Ascobolaceae and their allies
on the other appears at present to negative this possibility and to indicate
rather a case of parallel development.

In the Laboulbeniales the trichogyne is septate, and the oogonium is
unicellular and undergoes septation after the fertilization stage, but, of the
row produced, only one cell gives rise to asci. The fertilizing agent may be
a walled spermatium budded off externally, or it may be a non-motile mass
of protoplasm ejected from an attached organ.

The detailed development of the lower Pyrenomycetes has as yet been
even less studied than that of the higher forms, and all that can be said is
that apparently the antheridium is of a simple attached type and that the
archicarp is somewhat elongated, often coiled and sooner or later septate. The
larger gametangia among these forms would well repay detailed investigation.

4—2

ASCOMYCETES

[CH.

trichogyne o,

oogonium i cell,
never septate,-

antheridium attached.

PLECTOMYCETES

SACCHAROMYCETACEAE
ENDOMYCETACEAE

trichogyne o,

oogonium i cell,
septate after fert.,

antheridium attached.

Sphaet

ERYSIPH

i i

I i

i j

i i

•otheca
ACEAE

GYM

VOASCACEAE |

trichogyne i cell,

oogonium i cell,
septate after fert.,

antheridium attached.

ASPERGILLACEAE

! LOWER PYRENO-
MYCETES

Ascodesmis

\

trichogyne i cell,

oogonium i cell,
never septate,

antheridium attached,
large.

cn

W

U 1 i

Pyronema

in

M
PEZIZACEAE t_

W

y

incomplete develop-
ment of septate
type with antheri-
dium set free.

p 1 • 1

§ LABO\JLBEN;IALES

CH

Lachnea stercorea
Lachnea cretea Rhizina (/}
ASCOBOLACE:AE Q

complete development
of septate type
with antheridium
set free.

HIGHER PYRENOM\

LICt
rCETES

E

C

si-

rtlema pulposum
S

The dotted lines indicate possible and the continuous lines rather

more probable relationships.

"I ASCOMYCETES 53

In the forms here grouped together as Plectomycetes, we have three or
four varieties of sexual apparatus, but the richly septate types are never
reached and detached spermatia are not known. The antheridium is a uni-
nucleate or coenocytic cell borne at the end of a stalk; the most elaborate
archicarp is that of Eurotium with a unicellular trichogyne and an oogonium
which becomes septate after the fertilization stage. In Gymnoascus there is
no trichogyne and the compact sheath of the Aspergillaceae is represented
by an open weft of hyphae.

In the Erysiphaceae a trichogyne is not developed and the oogonium
becomes septate after fertilization, but only one cell gives rise to ascogenous
hyphae or (in Sphaerotheca) becomes the single ascus.

In the Endomycetaceae two enlarged cells unite, and the single ascus is
the immediate product of their union. The fusing cells arise on the same
mycelium as the conidia, and in Endomyces they are of different size; each
is uninucleate and after the union of their nuclei the fusion nucleus divides
to form the nuclei of the ascospores which may be four or eight in number;
in view of what is known in other asci it may be inferred that in the course
of these divisions meiotic reduction takes place.

Should this inference prove correct, and there seems no other stage of
the life-history at which meiosis is likely to occur, we have here a diploid
phase of the briefest possible duration, meiosis immediately succeeding
fertilization. This condition may be either primitive or reduced ; ascogenous
hyphae have not yet been interpolated or have already disappeared. The
only indication in favour of the latter hypothesis is the occurrence in certain
species of three nuclear divisions in the ascus and eight ascospores; there
are, however, other cases, such as the oogonium of the Fucaceae, where a
third division regularly follows meiosis even when all the nuclei formed are
not to be utilized, and in consequence the significance of the third mitosis
cannot be pressed. If the Endomycetaceae be regarded as primitive, or
rather as a simple offshoot from a primitive common ancestor, the ascogenous
hyphae must be regarded as an interpolated phase in the life-history, and
this interpolation seems to have entailed (i) the septation of the cell in which
fertilization takes place, and (2) the formation of one or more asci from one
or more of its subdivisions.

These changes have been established in certain simple forms through
which the rest may have been derived :

( i ) Erysiphaceae ; the vegetative cells are generally uninucleate ; the oogo-
nium after fertilization divides to form a row of cells, and from one of these
ascogenous hyphae grow out. The single ascus of Sphaerotheca and Podosphacra
is presumably the result of reduction, since there seems no explanation of
the development of a sporophyte unless the number of spores resulting from
a single sexual act is thereby increased. As simple forms go, the sheath is

54 ASCOMYCETES [CH. II

here fairly elaborate; the asci are regularly arranged. The Erysiphaceae
may possibly have given rise to the Laboulbeniales, the only other group in
which a single daughter cell of the oogonium is responsible for the asci, and
perhaps to the lower Pyrenomycetes also ; these, like the Erysiphaceae, have
regularly arranged asci, and in Chaetomium fimete the perithecium is without
an ostiole.

(2) Gymnoascus and its allies ; the gametangia are not much differentiated ;
both, like the mycelial cells, are multinucleate (it is difficult to gauge the
significance of this character in Fungi) and the oogonium, or an outgrowth
from it, becomes septate after fertilization and gives rise to ascogenous
hyphae. Among the Endomycetaceae, Dipodascus suggests itself as .the
most probable representative of the ancestor of these forms. The asci in the
Gymnoascaceae are irregularly arranged and the sheath is rudimentary.
Clearly such a form may have given rise to the Aspergillaceae and to the
rest of the higher Plectascales but perhaps to no other group.

(3) Ascodesmis is a third type which might be derived either directly
or through the erysiphaceous type from an endomycetous ancestor ; the
antheridium and oogonium are but little differentiated, but the latter is
furnished with a trichogyne and becomes septate after fertilization; the
ascogenous hyphae are few and the sheath simple. Massee indeed places
this genus near Gymnoascus although the asci are regularly arranged. It
cannot be far removed from the ancestor of the other Discomycetes.

The table on page 52 may perhaps serve to elucidate some of these
hypotheses.

CHAPTER III

PLECTOMYCETES

THE group Plectomycetes is constituted to include those relatively simple
forms which possess neither the cup-shaped apothecium of the Discomycetes,
nor the flask-shaped perithecium opening by a definite ostiole which
characterizes the Pyrenomycetes. In the majority of the remaining Asco-
mycetes a rounded ascocarp is produced, but it opens either by the decay
of its walls, or by an irregular split or tear. The asci may arise from the
floor of this fructification, and stand parallel one to another, or they may be
irregularly disposed, the fertile hyphae forming a tangled weft. In other
families the asci are naked; they stand parallel in the Exoascaceae, but in
these parasitic forms their position is probably determined by the fact that
they grow up between the epidermal cells or under the cuticle of the host,
and may be without phylogenetic significance. In the Endomycetaceae
they are irregularly disposed on the mycelium, and in the Saccharomyceta-
ceae a mycelium is not developed.

In the majority of species the asci are club-shaped, pyriform or oval,
they arise indifferently from the terminal or intercalary cells of the fertile
hyphae, and the regular bending over of the tip of the ascogenous filament
characteristic of the Discomycetes and Pyrenomycetes is not found among
them1. The ascospores are usually continuous and hyaline; in the large
majority of cases the gametophytic mycelium gives rise to conidia.

In the Exoascales the asci arise on a mycelium of binucleate cells and
the origin of the binucleate arrangement is unknown; but in the other main
groups of Plectomycetes the form of the sexual organs has been recorded,
'and a number of species show functional sexuality.

In the Endomycetaceae and Saccharomycetaceae fusion takes place
between similar or nearly similar cells, a single fusion nucleus is formed in
the zygote and there gives rise to the nuclei of the ascospores.

In the Erysiphaceae the mycelial cells and gametangia are uninucleate
the antheridium and oogonium differ in size and after fertilization the zygote
(oogonium) undergoes septation and one of its cells either becomes the
single ascus or branches and gives rise to several asci.

In the Gymnoascaceae and Aspergillaceae the cells of the mycelium
and sexual branches are multinucleate, the oogonium is furnished with a

1 The group corresponds, therefore, to Dangeard's Rectascees with the addition of his Game-

tangiees and Choristogametees (Le Botaniste, 1907, p. 28).

56 PLECTOMYCETES [CH-

trichogyne and the zygote (oogonium) after septation gives rise to numerous
asci which arise from its several cells.

In none of the Plectomycetes are the more complicated forms of sexual
apparatus reached ; the trichogyne and oogonial region are never mult*
cellular and the antheridium never becomes a spermatium.

The structure of the reproductive branches thus bears out the inference
drawn from the characters of the ascigerous stage that the species included
under the Plectomycetes are simple and for the most part presumably
primitive. The group is a collection of forms at a somewhat similar level
of development, and may or may not prove to be a natural arrangement ;
in this it resembles the Discomycetes and Pyrenomycetes.

It is within this group that the vegetative sporophyte has been developed
and the fusion in the ascus established, and it is probably among these forms
that the explanation of the peculiarities of ascomycetous morphology is to
be sought.

The group Plectomycetes includes some 1200 species and may be sub-
divided as follows :

Asci irregularly arranged PLECTASCALES.

Asci parallel

Ascocarp developed ERYSIPHALES.

Ascocarp lacking EXOASCALES.

PLECTASCALES

The Plectascales include all those Ascomycetes in which the asci are
arranged irregularly, at different levels and diversely orientated. In the
better developed forms the ascogenous hyphae are enclosed in a definite
peridium made up of an inner nutritive and an outer protective sheath, or
they are surrounded, as in Gymnoascus, merely by an open weft of hyphae.
The latter arrangement suggests a connection with the Endomycetaceae,
a series of simple species in which the asci are quite unprotected ; it has
been shown, by the recent studies of Guilliermond and others, that these in
turn lead to species in which a mycelium is seldom developed, and finally
to the typical yeasts, where the endosporogenous cells are scarcely recogniz-
able as asci.

To these may be added a few other simple forms of uncertain relationship
so that the Plectascales include the Plectascineae, the Protascineae, and
some of the Hemiasci of the authors of Engler's Natilrlichen Pflanzen-
familien, and contain some of the simplest members of the Ascomycetes.

Among these the Saccharomycetaceae have presumably been derived
by reduction from such forms as the Endomycetaceae where a mycelium is
normally developed. In both groups a single fusion occurs in the life-history
and immediately precedes the formation of the ascospores. It might be

in] PLECTASCALES 57

possible to regard this fusion as representing the non-sexual fusion in the ascus
which characterizes the members of other groups of Ascomycetes, and to
look upon the gametophyte and sexual organs as having wholly disappeared.

On the other hand, the fact that fusion is between separate cells, and
not between nuclei located in the same cell, and the further fact that the
fusing cells sometimes differ in size and behaviour (and not infrequently
fail to fuse) recall characteristics of the sexual process in other fungi, and
indicate that we are dealing here with forms in which the vegetative hyphae
are gametophytic, the uniting cells are gametangia, the diplophase is repre-
sented only by the fusion nucleus, the ascospores are formed directly in the
oogonium, and the anomalous second fusion does not occur. In Guillier-
mondia, where the fusion cell buds out a daughter cell in which the asco-
spore is produced, we may conceivably have the rudiment — or the vestige —
of an ascogenoiis hypha, and in Dipodascus the outgrowth of the gametangium
after fertilization may have a similar significance. Should the Endomyce-
taceae prove to be primitive, the history of the higher Ascomycetes becomes
that of the interpolation of a vegetative sporophyte between fertilization
and meiosis.

The Plectascales, as defined above, include the following families:

Asci naked.

Vegetative cells forming a mycelium ; asci distinct

from vegetative cells ENDOMYCETACEAE.

Vegetative cells single or loosely attached ; asci not

differentiated from vegetative cells SACCHAROMYCETACEAE.

Asci surrounded by loosely interwoven hyphae GYMNOASCACEAE.

Asci surrounded by a definite peridium.
Ascocarp subaerial

Sessile ASPERGILLACEAE.

Stalked ONYGENACEAE.

Ascocarp subterranean

Peridium distinct from walls of ascocarp ;

spore mass powdery at maturity ELAPHOMYCETACEAE.

Peridium continuous with walls of asco-
carp ; spore mass never powdery TERFEZIACEAE.

Endomycetaceae

In the Endomycetaceae the mycelium is usually well developed and
bears numerous asci each of which is either the product of a separate and
presumably sexual fusion, or parthenogenetically produced. Oidia, chlamy-
dospores and yeast-like conidia may be formed. The majority of the
Endomycetaceae are saprophytic on sugary substances or on exudations
from plants. Endomyces Mali is described as an active parasite on apples
and various species are parasitic on other fungi. The principal genera are
Eremascus and Endomyces.

58 PLECTOMYCETES [CH-

Only two species of Eremascus are known. E. albus -as discovered by
Eidam in 1881 in a bottle of malt extract. The contents had gone bad and

their surface was covered with a
growth of various fungi, amongst
which was the new genus. It pro-
duced a fine, snowy white, septate
mycelium from which pairs of fer-
tile hyphae grew out, curled round
one another and fused at their tips
(fig. 1 8). The fused portion was
cut off from the fertile hypha below,
and eventually produced eight
spores. Unfortunately Eidam's
species was lost and has never
reappeared.

In 1907, however, Stoppel, on
opening some pots of apple and
gooseberry jelly, discovered a very
similar form which she named Ere-
mascus fertilis. This species, like
E. albus, possesses a branching,
septate mycelium. The cells at
first contain several nuclei; these,
according to Stoppel, are arranged
in pairs, but Guilliermond, in a
subsequent investigation, found
that such an arrangement, even
when present in the young mycelium, did not persist. It is no doubt
dependent upon rapidity of growth.

From this mycelium pairs of uninucleate branches grow up, usually from
the same, sometimes from different hyphae, and fuse at their apices (fig. 19).
Their nuclei also fuse and after three karyokinetic divisions eight spores are
formed. Sometimes, especially in old cultures, the fertile hyphae may
produce asci without fusion. These are usually small and generally contain
four spores or even a lesser number. As a rule three nuclear divisions take
place in the parthenogenetic asci, and eight nuclei are formed, though they
do not all function. According to Guilliermond it would seem that the
number of spores is conditioned not by any cytological peculiarity, but
rather by the supply of nutritive material.

The species of the genus Endomyces possess a branched, septate myce-
lium. It may break up into oidia, which sometimes become surrounded by
thick walls and form cysts, or it may produce yeast-like conidia which

Fig. 1 8. Eremascus albus Eidam; a. b. c. d. sexual
apparatus; e. f. f. h. fusion of gametangia; i. /.
k. development of asci ; /. parthenogenetic ascus ;
x 900-1000; after Eidam.

Ill]

PLECTASCALES

59

Fig. 19. Eremascus fertilis Stoppel; stages in the formation of the ascus, both by fusion of two
cells and parthenogenetically ; after Guilliermond.

Fig. 20. Endomyces Magnusii Ludw.; a. b. antheridium and oogonmm in contact; c. oogomum after
fusion of sexual nuclei; d. parthenogenetic ascus; Endomyces fibuhger L.ndner; e. coi ugatio
between two neighbouring cells, at the end of the hypha is a group of young asci, / no
parthenogenetic asci; after Guilliermond.

6o

PLECTOMYCETES

[CH.

themselves multiply by budding. Under appropriate conditions the mycelium
also bears naked, four-spored asci, the development of which has been
studied by Guilliermond.

In Endomyccs Magnnsii vegetative multiplication is by the separation
of oidia cut off by transverse walls. The ascus is the product of a definite
sexual process in which an elongated, swollen cell and a relatively narrow
one grow up, bend towards one another and unite. The single nucleus of
the smaller cell passes into the larger and fuses with its nucleus. Two karyo-
kinetic divisions take place, so that four nuclei and ultimately four spores
are produced (fig. 20). Fusion appears to take place indifferently between
unrelated or closely related filaments and parthenogenesis is not uncommon.

In E. fibuliger, about half the asci result from the union of two filaments
while the remainder are parthenogenetic. The fusing hyphae are in most
cases closely related, often appearing as protuberances on each side of a
septum. They are similar at the time of fusion, but afterwards the growth
of one ceases, while the other swells to form the ascus. Besides producing
asci E. fibuliger multiplies rapidly by means of yeast-like conidia, which
closely resemble the cells of species of Saccharomyces (fig. 21).

Fig. 21. Endotnyces fibuliger Lind-
ner; formation of conidia; after
Guilliermond.

\Z. 11. Dipodasats albidus Lagerh.; fusion of con-
jugating cells and nuclei ; after Dangeard.

Wotkta decolorans, the only known species of the genus Wolkia has a

ig mycelium, growing luxuriantly at a temperature of about 26° C ; in the

immature state the mycelium is light pink, later globular red bodies appear

e are the asci and are formed at the ends of single hyphae without

*m,nary fus,on. At first they contain dense cytoplasm and a large vacuole;

er they become filled with blackish ascospores from two to* fifteen in

umber; ,„ old cultures the spores are sometimes septate

Ill]

PLECTASCALES

W. decolorans has been identified by van der Wolk as the cause of "vellow
grams, a serious disease of stored rice which is endemic in the East 'indies
and elsewhere, but is prevented by attention to thoroughly dry conditions.

The only known species of Dipodascus, D. albidus, was discovered by de
Lagerheim in Quinto in 1892 on the gummy secretion of Puya one of the
Bromeliaceae. It was found again in IQOI by Juel, in Sweden, on the sap
of an injured birch, and has been described by both these investigators and
by Dangeard. The mycelium consists of multinucleate cells; it may break
up to form oidia and may produce many-spored asci.

In the initiation of the ascus two branches grow up from the same or
different hyphae and fuse at their apices (fig. 22). Both are multinucleate-
one is rather larger than the
other and continues its growth
after fertilization to form the
single ascus. Soon after the
fusion of the sexual cells one
of the nuclei in each is recog-
nizable as larger than its neigh-
bours. These two nuclei unite,
usually in the larger cell, while
the rest of the nuclei degenerate.
The fusion nucleus passes up
into the developing ascus,
undergoes several divisionsand
eventually gives rise to the nu-
clei of the spores (fig. 23).

Dipodascus differs from Eremascus and the other Endomycetaceae in the
presence of accessory nuclei in its gametangia, and from all except Wolkia,
in the formation of numerous spores in its ascus. In spite of these differences
the resemblance seems sufficiently close to permit its inclusion in the same
group.

ENDOMYCETACEAE: BIBLIOGRAPHY

1883 EIDAM, E. Zur Kenntniss der Entwickelung bei den Ascomyceten. Cohn's Beitrage

zur Biol. der Pflanzen, iii, p. 385.
1892 DE LAGERHEIM, G. Dipodascus albidus eine neue geschlechtliche Hemiascee.

Jahrb. fur. wiss. Bot. xxiv, p. 549
1902 JUEL, H. O. Ober Zellinhalt, Befruchtung und Sporenbildung bei Dipodiiscus.

Flora, xci, p. 47.
1907 DANGEARD, P. A. Recherches sur le developpement du peVithece chez les Ascomy-

cetes. Le Botaniste, x, p. 30.

1907 STOPPEL, R. Eremascus fertilis, nov. spec. Flora, xcvii, p. 332.
1909 GUILLIERMOND, A. Recherches cytologiques et taxonomiques sur les Endomyce-

tacees. Rev. Ge"n. de Bot. xxi, p. i.

Fig- 23.

Dipodascus albidus Lagerh.; development of
ascus and ascospores; after Juel.

6, PLECTOMYCETES [CH-

I909 KuiCKER, A. Endomyces Javanensis, n. sp. C. R. des trav. du lab. de Carlsberg,

,* ™/Dtt WOLK P. C. Protascus colorans a new genus and a new species of the
* P^otalcLae Gr'oup; the source of "Yellow-Grains" in Rice. Myc. Centralbl. ui,

,9,4 RAMSBOTTOM, J. The Generic Name Protascus. Trans. Brit. Myc. Soc. v, p. 143-

Saccharomycetaceae

The Saccharomycetaceae, or yeasts, are widely distributed on, or in, all
sorts of sugary media; they occur mainly as separate cells which are only
exceptionally united to form a short mycelium.

The individual cells are round or elliptical, bounded by a delicate
membrane and containing, in the cases studied in detail, a large nuclear
vacuole with a chromatin network and a well-marked, laterally placed
nucleolus. Division is amitotic. In the cytoplasm are refractive granules
of volutin, glycogen and oil.

Multiplication is by transverse division and separation of the daughter
cells (Schizosaccharomyces}, or more usually by budding, that is to say by the
formation of successive lateral outgrowths which ultimately assume the
form and size of the parent cell (Zygosaccharomyces, Saccharomyces, Saccharo-
mycopsis). Each bud receives a nucleus and cytoplasm and is cut off
by a wall. Before its separation it may itself bud again, and in this way
considerable colonies may be produced.

Under suitable conditions, and especially when growing on a moist, solid
substratum, the cell contents may round themselves up to form one to eight
(usually two or four) spores. These so-called endospores are the ascospores
of the yeast, the ordinary vegetative cell functioning as an ascus either
independently or after conjugation with another similar cell.

One of the most striking features of the yeasts and one which gives
them a considerable economic importance is the power possessed by many
species of producing alcoholic fermentation in certain sugars. This pro-
perty is due to the presence of the enzyme zymase which is secreted by
the yeast cells during fermentation, but which is not present in the resting
cells, being soon decomposed when the reaction comes to an end. The
activity of zymase is dependent on the presence of two co-enzymes ; the
first is a soluble phosphate which enters into temporary combination with
part of the carbohydrate, but it is ineffective in the absence of a second
factor of unknown constitution. The unknown co-enzyme is dialysable and
not destroyed by boiling; it may be separated from 'the yeast juice by
filtration under pressure, both filtrate and residue being inactive alone.

Even the yeasts which produce the largest proportion of alcohol utilize
five to six per cent, of the available sugar in the formation of glycerine,

Ill]

PLECTASCALES

succinic acid, acetic acid, and small quantities of other substances. The
amount of these by-products varies during the progress of fermentation
and according to external conditions. In particular, fermentation is affected
by the presence or absence of free oxygen. Under conditions of plentiful
aeration the yeast grows and multiplies rapidly and much of the sugar is
used as food; under anaerobic conditions, on the other hand, the main part
of the sugar is utilized in respiration, alcoholic fermentation is more complete
and the quantity of alcohol produced is greater in proportion to the number
of cells concerned.

On the ground that their daughter cells are produced by septation, and
not, as in other genera, by budding, Guilliermond postulates for the species
of Schizosaccharomyces a derivation from the neighbourhood of Endomyces
Magnusii in which the mycelium cuts off free cells by transverse septation.
He refers such genera as Saccharomyces, in which budding" occurs, to the
line which gave rise to Endomyces fibuliger where asexual multiplication
takes place in a similar way (fig. 24).

Erf.

Sc.M.a.

L.J.n

Fig. -24. Diagram of the phylogeny of the Yeasts; after Guilliermond. Er. f., Eremascus fertilis.
End. f., Endomyces fibuliger. Sa. c., Saccharomycopsis capsularis. Z., Zygosaccharomyces. *>*.,
charomyces. L. J. II, Johannesberg yeast II. End. M., Endomyces Magnusii. End. d., Endo-
es decipiens Sc. o., Schizosaccharomyces octosporus. Sc. M., Schizosaccharomyces mellacn.

Sacc

myces decipi

Sc. M. a. , Sch. mellacei, apogamous variety

Conjugation, as a preliminary to the formation of asci, was first described
by Schionning in 1895 in Schizosaccharomyces and was afterwards studied
in some cytological detail by Guilliermond (1901). In Sch. octosporus, two
neighbouring cells of similar size put out processes which fuse to form
a conjugation tube ; the nuclei pass into the tube and undergo fusion, after
which the two associated cells enlarge and form, as a rule, a single oval

PLECTOMYCETES

[CH.

Fig. 75. Sehitosaccharomyca octosponts Beyrinck ; conjuga-
tion and formation of ascospores ; after Guilliermond.

structure, the ascus. The fusion nucleus divides to form four or eight
daughter nuclei about which ascospores are organized (fig. 25). Sometimes

the limits of the conjugating
cells can be distinguished
after the ascospores are
formed, two or four lying
in each of the original cells.
In the closely related
Sch. Pombe and Sch. mel-
lacei copulation takes place
in a very similar way, but
the union of the conjugating
cells is less complete than is usually the case in Sch. octospoms, and the
number of ascospores is regularly four. The mature ascus is thus dumb-bell
shaped, with two spores in each enlargement.

Also in 1901 Barker discovered the yeast Zygosaccharomyces Barkeri
and observed in it a conjugation similar to that of Sch. Pombe.

Following on these observations a number of other cases of conjugation
among the yeasts have been recognized. Many species form two spores,
one at each end of a dumb-bell shaped ascus ; in others a single spore is
produced, the fusion nucleus passing from the conjugation tube into one of
the fusion cells, while the other remains empty.

Such cases lead up to the state of affairs in Zygosaccharomyces Chevalieri
where conjugation is between two cells of different sizes, the whole contents
of the smaller passing into the larger cell which is then cut off by a wall.
In the larger cell nuclear fusion takes place and one to four ascospores are
formed.

In Guilliermondia fulv escens conjugation is between a mature cell and
its bud. The whole contents of the bud pass back into the parent cell, nuclear
fusion takes place and a fresh bud is put out in which the single ascospore
develops. It has been suggested that this represents a rudimentary sporo-
phyte. The problems connected with meiosis hardly arise here if, as Wager
has shown for Saccharomyces, amitosis is the rule.

In Debaryomyces globosus, copulation takes place sometimes between two
similar cells, sometimes, as in Guilliermondia, between a mature cell and its
bud. In either case one or two spores are produced

In most species with sexually formed asci parthenogenesis is not un-
common. In Schwanniomyces occidentals and in Torulaspora Rosei it has
become the rule. The cells in which the ascospores are about to be formed
put out processes which are directed towards neighbouring cells at the same
stage of development. But they do not fuse, and ascospores are formed in each
cell independently. In T. Rosei more than one process is sometimes put out.

mJ PLECTASCALES 6$

Such cases lead up to the conditions found in the large majority of
yeasts where ascospore formation takes place not only without effective
conjugation but without any vestiges of that process.

Among forms with parthenogenetically produced asci Guilliermond
(1902) has observed a peculiar process in Saccharomy codes Ludwigii. Here
the rather elongated ascus gives rise to four ascospores; these on germination
swell up, put out beaks towards each other and fuse in pairs. Fusion is
usually between spores in the same ascus, but occasionally, when one of the
four ascospores has degenerated, between spores of different groups. Each
spore is uninucleate, the nuclei pass into the conjugating tube and there
fuse. A similar process takes place in Willia Satiirnns and in the so-called
Yeast of Johannesberg, II.

Afterwards an outgrowth from the middle of the conjugation tube is
developed ; it may give rise to a short hypha which soon breaks up into
separate cells, it may produce lateral buds in an ordinary yeast-like manner,
or it may give rise at once, especially on carrot and under conditions favour-
able to ascus formation, to four endospores. In the last case the life-history
differs from that of Zygosaccharomyces principally in the abbreviation of the
vegetative phase, in other cases a vegetative phase is inserted not as usual
before conjugation, but between conjugation and the development of the
spores. Guilliermond regards the pairing of the ascospores as a secondary
process following the establishment of parthenogenesis. In any case it
admirably illustrates the plasticity of the simpler fungi.

SACCHAROMYCETACEAE : BIBLIOGRAPHY

1895 SCHIONNING, H. Nouvelle et singuliere formation de 1'ascus dans une levure.

Meddelelser fra Carlsberg Laboratoriet. iv, p. 30.

1901 BARKER, T. P. A Conjugating "Yeast." Proc. Roy. Soc. Ixviii, p. 345.
1901 GUILLIERMOND, A. Recherches sur la sporulation des Schizosaccharomycetes.

Comptes Rendus Ac. Sci. cxxxiii, p. 242.
1901 HANSEN, E. C. Grundlinien zur Systematik der Saccharomyceten. Centralbl. fur

Bakt. Abt. ii; xii, p. 529.
1903 GUILLIERMOND, A. Recherches sur la germination des spores chez le Schizosac-

charomyces Ludwigii. Bull. Soc. Myc. de France, xix, p. 18.
1903 LEPESCHKIN, W. W. Zur Kenntniss der Erblichkeit bei den einzelligen Organismen.

Centr. f. Bakt. Abt. ii; x, p. 145.
1905 GUILLIERMOND, A. Recherches sur la germination des spores et la conjugaison

chez les levures. Rev. Gen. de Bot. xvii, p. 337.

1909 KLOCKER, A. Deux nouveaux Genres de la Famille des Saccharomycetes. C. R.
des trav. du lab. de Carlsberg, vii, p. 273.

1910 GUILLIERMOND, A. Sur un curieux exemple de parthe'noge'nese observe* dans une
levure. C. R. Soc. Biol. de Paris, Ixviii, p. 363.

1910 GUILLIERMOND, A. Quelques remarques sur la copulation des levures. Ann. Myc.
vii, p. 287.
G.-V. 5

gg PLECTOMYCETES [CH-

I9IO WAGER, H. and PENISTON, A. Cytological Observations on the Yeast Plant. Ann.
19,i GU.'LUERMO^A. Les Progres de la Cytologie des Champignons. Prog. Rei Bot.

v, pp. 433 and468' KofoKOTlNE A G. Guilliermondia, un nouveau genre de la
iromycetes a copulation hdterogamique. Bull, du Jard. Imp. de

VND^H. XLaPconj7ugaison des spores chez les levures. Rev. Gen. de Bot. xxv,

,4 BA^I'SS W M. The Nature of Enzyme Action. Monographs on Biochemistry.
Longmans, Green & Co., London (and see literature cited).

Gym noascaceae

The Gymnoascaceae differ from the Endomycetaceae in that their asci
are borne on a sporophytic mycelium which originates from the female

organ after the fertilization stage.
These ascogenous hyphae are sur-
rounded by a loose weft of protec-
tive filaments which bear spines or
variously coiled or hooked branches
(fig. 26). The asci are ovoid or pyri-
form, and each contains eight spores.
The species of Gymnoascus occur
in various habitats, on dung, bees'
nests, dead grass, etc.

In G. Reesii, according to Dale,
two branches grow up from the
same hypha, one on each side of
a septum, and become twisted
around one another. These are the
antheridium and oogonium ; their
x 265; free ends swell into club-shaped

Fig. 76. Gymnoascus sp.; a. ascocarp
b. ascus and free ascospores, x 1040.

heads which lie in close contact and

each becomes delimited by a transverse septum. The walls between them
break down, and the contents of the antheridium pass over into the
oogonium (fig. 27 a, b}. Both cells are at first uninucleate, but later coeno-
cytic, and, though the history of the nuclei has not been traced, it seems
almost certain that fusion must sooner or later occur.

Up to this point the sexual cells are usually quite similar in form, but
now the antheridium grows larger and more spherical, remaining almost
straight, while the oogonium puts out a prolongation which winds around
it, undergoes septation and soon branches to give rise to ascogenous
hyphae (fig. 27 c).

Ill]

PLECTASCALES

In G. candidus (fig. 27 d) the antheridium and oogonium already differ
in form at the time of their union, and, in the majority of cases, appear to

Fig. 27. Gymnoasciis Reesii Baran.; a. surface view of conjugating cells;
b. the same in longitudinal section ; c. a later stage, septate oogonium
giving rise to ascogenous hyphae ; Gymnoascus candidus Eidam ;
d. surface view of conjugating cells; e. same in longitudinal section;
all after Dale. Ctenomyces serratus Eidam; f. surface view of con-
jugating cells, x-400; after Eidam.

arise from different hyphae. As in G. Reesii the antheridium is straight,
but the oogonium elongates before fusion and grows spirally around it till
the apices meet and fuse (fig. 27 e). Afterwards the oogonium undergoes
septation and gives rise to ascogenous hyphae. The sheath of protective
hyphae is very scanty, represented by a few thin-walled filaments.

Amanroascus verrucosus forms sexual organs which, in their early stages,
closely resemble those of G. Reesii. Two similar multinucleate hyphae
grow up, and later one of them, the oogonium, enlarges considerably; it
branches without septation, and gives rise to ascogenous hyphae which are
cut off by transverse walls. Our knowledge of development in this species
is due to Dangeard, who has not observed fusion between the sexual
cells.

In Ctenomyces serratus (fig. 27 f\ which occurs saprophytically on
feathers, organs quite similar to those of G. candidus have been described
by Eidam, and more recently by Dangeard. They are multinucleate, and
the oogonium is long and elaborately coiled and ultimately becomes seg-
mented. In this species, as in the others he has studied, Dangeard regards
the central hypha not as an antheridium, but as a nutritive structure which
he terms a trophogone. He denies the passage of its contents into the
female organ.

5—2

68

PLECTOMYCETES

GYMNOASCACEAE: BIBLIOGRAPHY

,880 EIIUM, K. Beitras zur Kcnntniss der Gymnoasceen. Cohn's Beitrage, iii, p. 267.
1003 UM.K, E. Observations on the Gymnoascaceae. Ann. Bot xvn, p. 571-
W DANGEARD, P. Recherches sur le developpement du penthece chez les Ascomy-
cetes. Le Botaniste, x, pp. 86 and 97.

Aspergillaceae

The Aspergillaceae are distinguished from the earlier families of the
Plectascales by the fact that their ascogenous filaments are surrounded by
a closely interwoven sheath of sterile hyphae so that a closed fruit or peri-
thecium is formed. In many species, the development of an ascus-fruit is
rare, and reproduction depends on the abundant and very efficient conidia;
in others, which, judging by the form of their conidial fructification, should
belong to this family, ascocarps are unknown.

The species occur either saprophytically or parasitically upon a wide
variety of substrata. Many of the saprophytic forms, including species of
Eurotium and Pcnicillinm, grow with especial readiness on fatty substances,
Emericella erythrospora occurs on olives, and Monascus heterospoms on
glycerine or tallow.

Several species of Pcnicillium together with other fungi and bacteria
are concerned in the "ripening" of cheese, on the proteids of which they
act by means of a proteolytic enzyme.

The species of Microascus, ApJianoascus and some others are coprophilous,
and several members of the family occur on wood.

The parasitic forms are less numerous; various species of Penicillium
and Eurotium are pathogenic on man and animals, and some, if they obtain
entrance through a wound or other aperture, are the cause of ripe rot in fruit.
Thielavia basicola, the only member of the family which causes an
important plant disease, is sometimes separated from the Aspergillaceae
and classed with the Perisporiaceae. This species infects the roots of tobacco
and certain other plants, and in the early stages multiplies by means of
hyaline conidia (endospores) produced inside mycelial branches, from the
ends of which they are afterwards expelled, givingthe infected root a mildewed
appearance. Later, thick-walled brown chlamydospores are differentiated
in rows at the ends of hyaline filaments so that the root is covered with
a dark coating. Normal development of the root is prevented and the host
killed or stunted ; if recovery does not take place perithecia are developed
on the dead plant.

The formation of the perithecium in most investigated species is initiated
by the appearance of sexual organs, from the stalks of which the cells of the
sheath arise. In Microascus and in Emericella the sheath opens by a pore,
but in the majority of cases it remains closed, and the ascospores are finally

Ill]

PLECTASCALES

69

liberated by its decay. The asci are spherical or pyriform and contain two
to eight continuous spores, the walls of which may be variously ornamented.
In both Penicillium and Eurotium the perithecium may develop an excep-
tionally thick wall, and pass into a resting stage sometimes several weeks
in duration. Such a structure is described as a sclerotium.

In Eurotium herbariorum1 the development of perithecia is readily
induced by cultivation on prune agar2 made up with forty per cent, of cane-
sugar. Ripe perithecia appear after ten days or a fortnight at 15° C.
A similar method should probably prove successful with other species.

The only known species of Aphanoascus, A. cinnabarinus, was found by
Zukal on the dung of alligators. The character of its perithecium wall
(fig. 28) suggests a transition stage between the Gymnoascaccae, in which it is

Fig. 18. Aphanoascus cinnabarinus Zukal ; a. elongated, septate archicarp and swollen
antheridium ; b. ascogenous hyphae and sheath; after Dangeard.

placed by Dangeard, and the Aspergillaceae. Multinucleate conidia are borne
laterally or terminally on the mycelium. The sexual organs arise from the
same or different hyphae; the antheridium (Dangeard's trophogone) becomes
swollen, and the elongated archicarp, which appears at first to be without
septa, coils round it; their fusion has not been observed. Each at first
contains from three to ten nuclei; later the number rises to about twenty
in the antheridium and as many as forty in the archicarp. According to
Dangeard the contents of the antheridium degenerate, though the cell itself
persists for a considerable time. The archicarp undergoes septation, branches,
and gives rise to asci. In the meantime vegetative hyphae grow up and
invest the essential organs, forming a loose tangle around them The inner
part of the investment remains in this state and is eventually absorbed, but

1 Eurotium herbariorum (Wigg.) Link = ^~. Aspergillus glaucits de Bary, and Aspergillus
herbariorum Wigg.

- Ten prunes are placed in a small saucepan of water and allowed to simmer, being broken open
when soft; when the fluid is reduced to about looc.c. it is poured off, the sugar dissolved in it and
five per cent, agar agar stirred in. Material grown on this medium is excellent for class work ; it
should be examined under the microscope while still attached to a thin slice of agar.

PLECTOMYCETES

[CH-

Penicillium.

In the investigated species of the genus E«rotium(AsfergiUuS), the
ascospores and conidia are commonly multinucleate and g.ve nse on ger-
mination to a septate mycelium each cell of which contams severa, fe

Conidiophores appear early; they arise as a rule from densely tangled
knots of swollen mycelium, and appear as thick, multinucleate hyphae. The
tip of the conidiophore becomes swollen and rounded off and ,ts cytoplasm
shows a reticulate arrangement. A little later numerous stengmata bud
out (fig. 29), and the nuclei stream up the strands of cytoplasm towar

A

Fig. 20. Eurotinm herbariorum (Wigg.) Link ; development of conidiophores and conidia,

X625.

them. Several nuclei pass to each sterigma and thence to the conidia which
develop in acropetal succession. At maturity each conidium contains in
E. repens about twelve nuclei, in E. herbariorum four, and in E. fumigatus,
E. flavus and E. davatus, as described by Dangeard, only one.

The general features of the sexual organs of Eurotiwn herbariorum were
described by de Bary in his classical researches of 1870. He distinguished
a coiled, septate archicarp, and saw that its tip fused with a comparatively
straight antheridial hypha, the membranes between breaking down, and he
recognized that from it the asci are ultimately derived.

More recently it has been shown that the archicarp of Eurotiwn is
made up of three parts: a multicellular stalk, a unicellular oogonium, and
a unicellular trichogyne. In E. herbariorum these parts may be clearly
distinguished (fig. 30 a), but they are not always equally definite in E. repens.

Ill]

PLECTASCALES

In any case the archicarp becomes more or less twisted and near it another
septate hypha appears, from the end of which the unicellular antheridium is
cut off. Like the cells of the vegetative mycelium, all parts of the sexual
organs are coenocytic.

Fusion takes place between the antheridium and trichogyne, but the
contents of the male organ have not been seen to enter the oogonium.

Fig. 30. Eurotium herbariorum (Wigg.) Link; a. young archicarp; b, archicarp and
abortive antheridium ; c. ascocarp containing asci and spores; x 625.

Dale has observed the fusion of nuclei in pairs in the oogonium of E. repens,
and Domaradsky in that of E. Fischeri, but it seems probable that we are
dealing here with a union of female nuclei such as occurs in various Disco-
mycetes. Even if normal fertilization sometimes takes place it is certainly
not general, for the antheridium often fails to reach the trichogyne (fig. 30^),
and is sometimes entirely absent. This appears to be always the case in
E. flavus and it is common in other genera.

Nevertheless the oogonium becomes septate and from its several parts
branches develop, the nuclei pass into them, and at their ends eight-spored
asci develop. The ascus is formed from the terminal or the penultimate cell
of a hypha and in it a fusion of two nuclei takes place.

Shortly before the septation of the oogonium, vegetative hyphae begin
to grow up about the sexual organs, from the stalks of which they mostly
arise as branches, and themselves branch freely. Some of the branches grow
inwards forming a nutritive layer, the cells of others, as shown by de Bary,
become tabular and more or less empty, they secrete a golden yellow

PLECTOMYCETES

[CH.

substance, readily soluble in alcohol, in the form of a thick, brittle pellicle.
These constitute the protective sheath (fig. 30*:), by the decay of which,
after the disappearance of the nutritive hyphae and later of the ascus walls,
the spores are finally set free. The ascospores are spherical or lenticular
often with a sculptured epispore.

In most species of Penicillinm reproduction takes place almost entirely
by means of the abundant conidia borne in chains on the branched, brush-
like conidiophores (fig. 3 1 ). Ascocarps are rare, and a detailed study of their
development has yet to be made.

o o

Fig. 32. Penicillium glaticum Link;

conjugating cells, x6^o; after
Brefeld.

Fig. 3i. Penicillium giaucum Link; conidiophon
and conidia, x ,00.

Brefeld, in 1871, succeeded in obtaining perithecia of P. glaucum- by

.vatmg his material under reduced oxygen pressure. He cautiously

tened shces of bread with distilled water, and after six or seven days

development of the mycelium was proceeding energetically,

1 Penidllium glaucum Link = P. crustaceiun L.

Ill]

PLECTASCALES

enclosed them between glass plates so as to reduce the entrance of air, and
the development of conidia. Similarly Zukal a few years later obtained
sclerotia by excluding air. The formation of the perithecia in Brefeld's
material was initiated by the appearance of pairs of simple, stout hyphae
which twisted round one another (fig. 32), and from one or both of which
branches later arose. Brefeld regarded them as possibly oogonial and
antheridial.

A further study of these organs, the simple form of which suggests
a comparison with Gymnoascus, is much to be desired. Penicilliiini glaiicum
includes several biological species or strains, and it is quite possible that
Brefeld's success depended not only on
• the methods employed, but also on the
use of a fortunate variety.

Klocker, in 1903, obtained asci in his
new species P. Wortmanni, and another
new and very curious ascigerous species,
PenicUlium venniculatum, was described
by Dangeard in 1907. The vegetative
cells, unlike those of related forms, are
uninucleate and bear a very scanty supply
of conidia. Perithecia are abundant; in
their initiation two branches take part.
The oogonium is at first uninucleate but
as it elongates the nucleus undergoes
several divisions. In the meantime a
second branch appears, usually borne on
a narrower filament ; it cuts off a uninu-
cleate or occasionally binucleate terminal
cell which applies itself to the middle of
the oogonium, and the intervening walls
disappear (fig. 33). Apparently, however,
fertilization does not take place; the nu-
cleus of the terminal cell is described as
degenerating in situ while the oogonium
undergoes septation and is transformed
into a row of usually binucleate cells.
Narrow vegetative hyphae grow up around
this structure, and the perithecium is
formed in the usual way.

The archicarp of this species shows
no importantpeculiarities but the terminal
uninucleate cell of the other branch is

74

PLECTOMYCETES

[CH.

difficult to place; it seems almost inevitable to homologize it with an
antheridium, but the relation of a uninucleate antheridium to a multinucleate
female organ is by no means clear. Degeneration of the superfluous nuclei
as in Dipodasais might be postulated. For Dangeard, the structure is a
trophogone concerned only in nutrition and without sexual significance.

The genus Monascus contains some five or six species, of which the most
fully investigated are M. purpureus and the form studied by Barker and
since named M. Barkeri by Dangeard. This species is used by the Chinese
for the manufacture of an alcoholic liquor known as Samsu. ,

In both species there is an abundant mycelium bearing chains of
ovoid conidia; later it assumes a reddish tinge and fruits are formed; their
development may be traced with some readiness in hanging drop cultures.
Certain branches of the mycelium cut off each a small, terminal cell which
elongates and bends sideways to form the antheridium (fig. 34). A pro-
longation of the penultimate cell grows up alongside it and a trichogyne

Fig. 34. Monascus Barkeri Dang.; development of oogonium,
trichogyne and antheridium, x9oo; after Barker.

and oogonium are cut off by transverse walls. The oogonium contains four

>ix, and the antheridium three or four nuclei. According to Dangeard

ie antheridial (trophogone) nuclei degenerate in situ but other authors find

ion takes place between the antheridium and trichogyne and that the

male nuclei travel through the trichogyne to the oogonium (fig. 35) where

they pair Wlth th female nudei Accord.ng ^ Sch.k ^fusion

ot occur at this stage in M. purpureus but is postponed till the sexual

Ill]

PLECTASCALES

75

nuclei have travelled in pairs to the asci, where they unite; but Kuyper, in
M. Barken, reports fertilization in the female organ.

After the fertilization stage the oogonium enlarges and gives rise to asco-
genous hyphae while the an-
theridium and trichogyne de-
generate. Investing filaments
grow up to form a sheath, the
inner layers of which consist of
delicate, nutritive cells. These
degenerate early, producing a
mass of protoplasm amongst
which the ascogenous hyphae
ramify. From the penultimate
cells of the latter binucleate
asci are developed, and after the
nuclei have fused eight spores
are formed. The ascus wall
breaks down and the spores are
finally set free after the decay
of the outer layer of the sheath.

This sheath, with the en-
closed mass of free ascospores,
was long regarded as a single
organ containing an indefinite
number of spores ; for this
reason the fungus was placed
in the Hemiasci and given the
generic name of Monascus.
The later stages of develop-
ment are in fact difficult to
follow and have been variously interpreted by different authors. Thus
Dangeard describes the oogonium as undergoing septation before it branches,
while Barker interprets the mass of protoplasm in which the young asci are
found as the remains of the oogonium invaginated by the growth into it of
the ascogenous hyphae. Kuyper and Ikeno, on similar grounds, believed
the asci to be produced by free cell formation within the oogonium, no
ascogenous hyphae being developed.

Fig. 35. Monascus purptireus Went. ; a. b, stages in
the development of the oogonium; after Dangeard.
Monascus X. Schikorra ; c. entrance of male nuclei
into trichogyne; d. pairing of nuclei in the oogonium ;
after Schikorra.

ASPERGILLACEAE : BIBLIOGRAPHY

1870 DE BARY, A. Eurotium, Erysiphe, Cincinnobolus nebst Bemerkungen iiber die

Geschlechtsorgane der Ascomyceten. Beitr. z. Morph. und Phys. der Pilze, iii, p. i.

1874 BREFELD, O. Botanische Untersuchungen iiber Schimmelpilze, ii, Penicillium, p. I.

7fi PLECTOMYCETES [CH-

,887ZUKA, H. OberK».,urd=rAskenfruch,von/'OT^OT««^- K. K. zoo.

IS

I907 SS^CL^^^H.S. TheMorphology

,908^^^

,909*:^^^

,909 SCH.KORRA, W. Ueber die Entwickelungsgeschichte von JJfi»Hw««. Zeits

,9,0 ?HOM,PC37 Cultural Studies of Species of Penicillin. U.S. Dept. Agr.
Animal Industry Bull. 118.

Bureau

Onygenaceae

The Onygenaceae include only the remarkable genus Onygena, There
are some six" species, all limited in habitat to such animal substances as
horns, hoofs, feathers, fur and skin. This peculiarity, together with the
absence of conidia, the thin wall of the perithecium, and the fact of its
dehiscence by lobes or by a circular split, distinguishes the members
of the group from the other Plectascales, which they resemble in the
irregular arrangement of their asci. Two of the six species have sculptured
spores and sessile fructifications which thus approach those of the Aspergill-
aceae, while in the other four the spores are smooth and the fructification
stalked. To the latter group belongs Onygena eqidna, described by Marshall
Ward in 1899. The ascospores germinate only after a prolonged resting
period or after treatment with gastric juice ; thus treated they produce a
vigorous mycelium on which the ascocarp first appears as a dome-shaped
mass of white hyphae ; a little later it becomes covered with loose cells
among which air is entangled, rendering the fruit very difficult to wet. As
development proceeds a number of hyphae grow outwards and divide into
short segments, certain of which swell up and are liberated as chlamydo-
spores, covering the whole of the stroma with a dense powder.

Meantime the hyphae which gave rise to these become crowded together
to form the pseudoparenchymatous sheath. Internally asci are produced
and give rise each to eight spores, but the ascus walls soon disappear and

in] PLECTASCALES 77

the spores lie free amongst the vegetative hyphae. This mature stage, in
which there is no trace of asci, caused Onygena to be variously classified
with the Myxomycetes and with the Lycoperdaceae before its true position
was discovered. There is no evidence of the existence of sexual organs.

ONYGENACEAE: BIBLIOGRAPHY

1899 WARD, H. MARSHALL. Onygena equina Willd. A Horn-destroying Fungus. Phil.

Trans. B. cxci, p. 269.
1917 BRIERLEY, W. B. Spore Germination in Onygena equina^ Willd. Ann. Bot. xxxi,

P- 17-

Elaphomycetaceae and Terfeziaceae

In the next two families, Elaphomycetaceae and Terfeziaceae, the fruit
is subterranean. The species differ from the other hypogeal Ascomycetes,
the Tuberales, with which they are still sometimes classified, and resemble
the subaerial Plectascales in the irrtgular arrangement of their asci, which
are scattered or grouped in nests surrounded by sterile branches (fig. 37). The
gleba or central complex of hyphae is not at any stage of development in
communication with the exterior.

In the Elaphomycetaceae the ascocarp is surrounded by a thick yellow
or brown peridium, the asci are subglobose and the gleba breaks up at
maturity into a powdery mass of spores. The only genus is' Elaphomyces.
The mycelium of certain species develops in relation to the roots of Pinus
and other conifers, and the ascocarp is often parasitized by species of the
pyrenomycetous fungus Cordyceps. E. granulatus, the commonest British
species, is the host of C. capitata, and E. variegatus of C. ophioglossoides
(fig. 1 10).

In the Terfeziaceae (figs. 36, 37) the peridium is much less distinct, and

Fig. 36. Terfezia olbiensis Tul. ; section of fructification ; after Tulasne.

in some cases is represented merely by an ascus-free region around the
periphery of the fruit. Moreover the spores do not, as in the Elaphomy-
cetaceae, form a powdery mass at maturity.

PLECTOMYCETES

[CH.

ERYSIPHALES

The Erysiphales are characterized by an abundant superficial mycelium,
which may be white (colourless) or dark-coloured. The perithecia are
spherical, ovoid or flattened, and are usually without an ostiole; the peridium
is thin and membranous; the asci are arranged in a regular layer at the
base of the perithecium.

The group includes some 600 species, the majority of which are external

parasites or epiphytes upon the
leaves of higher plants. They are
grouped into three families, of
which the Microthyriaceae are
but little known, and of doubtful
position, and the Erysiphaceae
and Perisporiaceae show several
points in common both with the
Plectascales, from which they
differ in the regular arrangement
of their asci, and with the Pyre-
nomycetes, from which they are
for the most part distinguished
by the absence of an ostiole.

Their taxonomic position is
probably somewhere between
these two groups, and they have,
under various systems of classifi-
cation, been placed in closer proxi-
mity sometimes to the one and
sometimes to the other. Their in-
clusion here in the Plectomycetes
is due to the fact that they, or
rather their best-known family,
the Erysiphaceae, show indica-
tions of being a primitive group.
The simple type of male and
female organs, the latter without
a trichogyne, and the simple
e of the perithecium are evidence in this direction.
The families of the Erysiphales may be distinguished as follows :
Aerial mycelium colourless (or white). Perithecia more
or less globose without an ostiole, furnished with
conspicuous appendages.

Conidia of oidium type. ERYSIPHACEAE.

Fig- 37- Terfezia olbiensis Tul. ; section through
hymenium, showing asci irregularly arranged •
after Tulasne.

in] ERYSIPHALES 79

Aerial mycelium dark-coloured or rarely absent. Peri- •

thecia globose or ovoid, without appendages.

Conidia not of oidium type. PERISPORIACEAE.

Aerial mycelium dark-coloured or absent. Perithecia
flattened or shield-shaped, with an ostiole at the
apex, without appendages.

Conidia absent. MICROTHYRIACEAE.

A further and probably important distinction which separates the
Erysiphaceae from the other two families is the character of the ascus and
ascospores. In Erysiphe and its allies the ascus is more or less globose, the
spores are always continuous and colourless, and the number of spores in
the ascus is frequently reduced. In the Perisporiaceae, on the other hand,
the ascus is relatively elongated and sometimes cylindrical, and the spores
are commonly two or more celled and often dark-coloured. Most species
agree, however, with the Erysiphaceae in the absence of paraphyses. The
Microthyriaceae approach the Perisporiaceae rather than the Erysiphaceae
in the characters of the ascus and spore, but, as already stated, they are
clearly distinguished by the curious flattened perithecium.

It remains for future research to determine whether these families should
be grouped together, or whether the Perisporiaceae and Microthyriaceae are
true Pyrenomycetes and should be placed in that alliance. In our present
extensive ignorance of the initiation and development of their perithecia, it
seems unwise to remove them from their traditional position in the neigh-
bourhood of the Erysiphaceae.

Erysiphaceae

The members of the Erysiphaceae are popularly known as white or
powdery mildew or blight. They have a practically worldwide distribution,
but have been recorded especially in Europe and the United States.

They are obligate parasites on the leaves or young shoots and inflores-
cences of flowering plants. The germinating conidium or ascospore gives
rise to an abundant, superficial, septate mycelium of uninucleate cells, which
ramifies over the leaf in every direction, forming a white web-like coating,
and sends haustoria into the epidermal cells of the host. In the simplest
cases the haustorium is a slender tube which swells up inside the host cell;
in other species it is branched, sometimes forming finger-like processes, and
frequently there is an external disc or swelling (adpressorium), from which,
or from the mycelium in the neighbourhood of which, the haustorium proper
arises and pushes into the epidermal cell. As a rule the fungus does not
penetrate further, but in Erysiphe Graminis Salmon was able to induce
endophytic growth and nutrition by allowing the conidia to germinate on
wounded leaves ; in Phyllactinia Corylea the branches of the aerial mycelium

So

PLECTOMYCETES

[CH.

enter the stomata, extend through the intercellular spaces and send haustoria
into the neighbouring cells, and in Erysiphe (or Oidiopsis} taurica the whole
mycelium during the conidial stage is located in the^ tissues of the host.
We have thus, within the limits of the family, a transition between ecto- and
endoparasitism through hemiendophytic forms, and forms which are endo-
phytic under abnormal conditions. When perithecia are about to be produced
and the mycelium emerges and spreads over the surface of the host leaf, the
hyphae both o>i Pliyllactinia and of E. taurica showhaustorial branches (ad-
pressoria), though no haustoria are produced. It may be inferred that the
ectophytic condition with haustoria penetrating the epidermal cells is primi-
tive in the group.

Indian and Persian specimens of E. taurica have been found under
practically desert conditions, others have been collected on plants of the
steppes of Turkestan at a height of 6000 feet, and in localities exposed to
very dry winds. The suggestion has consequently been made that the
endophytic habit in this family is an adaptation to xerophytic conditions,
since it both provides shelter for the developing mycelium and obviates the
necessity of piercing through the cuticle, which in desert plants is of
considerable thickness.

The Erysiphaceae are propagated during the summer by rather large
oval uninucleate conidia (fig. 38). These are ordinarily produced in rows

on simple conidiophores with one or
more basal cells. In the endophytic
E. taurica, however, the conidia are
borne singly on branched conidio-
phores which emerge through the
stomata of the host.

In the case of Phyllactinia Cory-
lea, which is met with on a large
number of deciduous trees, variations
occur in the shape of the conidia
borne on different hosts, and indicate
the existence of morphological dis-
tinctions between the biological
forms of the species.

Before the connection between the
conidia and the perithecia of the
Erysiphaceae was understood, the
nenc name, Oidium, was applied to the former. The name is still used
> indicate the characteristic form of the conidial stage and to describe
dia when the perithecia are unknown. This was the case with the
powdery vine mildew. The conidial form, known as Oidium Tuckeri became

Fig. 38. Sphaerotheca pannosa Wallr. ; conidio-
phores and conidia, x 240.

in] ERYSIPHALES 8l

prevalent in Europe in 1845-6, but perithecia were not observed till 47 years
later, when they appeared during two successive seasons in various localities
in France, and the fungus was identified with the American vine mildew,
Uncinula necator, in which perithecia are common. The unusual production
of the perithecial stage was attributed to the sudden alternation of high and
low temperatures which characterized the seasons in question. The survival
of the fungus in the absence of ascospores has been attributed to the persist-
ence of the mycelium, and also to the development of conidia capable of
passing the winter in the resting state. Fortunately the disease is readily
kept in check by the application of appropriate sprays.

A very similar case is that of the oak mildew. In or about 1904, oak
scrub in England and many parts of Europe became infected with the
conidial form O. Quercinum; in 1911 perithecia were found in France, and
the parasite was identified with the common American form Microsphaera
Aim which frequently occurs on oaks in the United States. Here again
exceptional seasonal conditions appear to have been necessary for the
formation of the perithecial stage.

In a different manner climate has affected the development of the goose-
berry mildew, Sphaerotheca mors-uvae, which was introduced into Europe
from America about 1900. Very numerous perithecia are developed but a
considerable proportion either fail to mature or fail to survive the winter.
Infection of the young shoots in the spring appears to depend on the earliest
formed perithecia, which alone have had time to mature and lodge in the
bark or between the bud scales of the host. For this reason prevention is
here much more difficult than in the case of the vine mildew, since the
mature perithecia are very difficult to kill and the spread of the disease
must be combated by the removal of infected shoots in the autumn, or by
appropriate methods of cultivation.

The perithecia of the Erysiphaceae appear in the late summer or autumn ;
they are spherical or subglobose, 50— 300/4(0-05 to^O'smm.) in diameter
and furnished with simple or branched appendages; they are fixed in
position by means of a secondary mycelium. When quite young the peri-
thecia appear white and glistening like the vegetative mycelium ; later they
become clear yellow and finally brown in colour. Their development is by
no means simultaneous, so that a considerable range of stages can often be
seen within the field of an ordinary hand lens.

During development the wall of the perithecium is differentiated into
inner and outer layers (fig. 39). The inner layer is several cells thick ; its
cells are rich in cytoplasm with thin, apparently unmodified walls; it is in
contact with the developing asci, about which it forms a packing, and to
which it supplies food material. Outside this layer is a strengthening and
protective zone of several series of cells with scanty contents, the walls of

6

PLECTOMYCETES

[CH.

Fig. 39. Erysiphe Polygoni; young perithecium containing
uninucleate asci ; after Harper.

82

which undergo a change apparently analogous to lignification. In Phyllactinia
the outermost layer, from which the secondary mycelium and the character-
istic appendages are derived,
consists of thin-walled cells,
but in other genera it is not
differentiated from the pro-
tective zone.

A single ascus or several
may be formed in the peri-
thecium ; the ascospores,
numbering two to eight in
each ascus, begin to develop
during the summer or au-
tumn, but they remain in
the perithecium under nor-
mal conditions and do not
germinate till the beginning
of the following year, when
they are set free by the rupture of the perithecium wall, and produce the
first infections of the season. In Erysiphe Graminis and Sphaerotheca mors-
uvae some of the.perithecia separate readily from the mycelium in August,
and, if supplied with moisture, will eject their spores after a few hours. They
may in this way prove a source of infection in the season in which they
were produced, and this is probably true of other species also, and should
be borne in mind if ripe ascospores are being searched for.

The family includes six genera, all of which are British, and are readily
distinguished (fig. 40).

In Sphaerotheca (one ascus), and in Erysiphe (several asci), the perithecial
appendages are filamentous, unbranched or branched irregularly, and very
like the ordinary hyphae of the mycelium; in Podcsphaera (one ascus), and
in Microsghaera (several asci), they are usually dichotomously branched ; in
Uncinnla the apices of the appendages are spirally coiled, and in PJfyllactinia
the perithecium bears stiff, pointed hairs with swollen bases. In this genus
also the apex of the perithecium is furnished with a ring of richly branched
penicillate cells. At about the time of spore-formation these break down,
forming a sticky gelatinous cap, by means of which the perithecium, after
it is first set free, adheres upside down to its original host plant or to other
objects. In view of this peculiarity the ascription of Phyllactinia to any
host in contact with which its perithecia may be found demands careful veri-
fication.

The function of the true appendages in the Erysiphaceae is somewhat
variable. In Phyllactinia the bulb at the base of the appendage is thick-

Ill]

ERYSIPHALES

walled over its upper surface, but an oval region remains thin on the lower
side. As the ripening perithecium loses water so do the appendage*; the
thin area below the bulb is pushed in by atmospheric pressure, the under
surface becomes consequently shorter than the upper and the end of the
spine is pulled down till subsequent moistening straightens it again (Harper).

Fig. 40. Perithecia of a. Erysiphe tortilis (Wallr.) Fr.; b. Microsphaeria sp.; c, Uncinula
Aceris (DC.) Sacc.; d. Phyllactinia Corylea (Pers.) Karst.; x 120.

These hygroscopic movements may be repeated many times- according to
weather conditions, even after the living protoplast has disappeared from
the appendage (Neger); and at last the perithecium is loosened from its
attachment.

In other cases, such as Erysiphe and Sphaerotheca, the appendages
may help to anchor the perithecium to its host during development; in
Uncinula necator their apices become mucilaginous (Salmon), and they serve,
much as do the penicillate cells of Phyllactinia, to attach the free perithecium
upside down to the substratum.

The development of the perithecium was first described in 1863 by

6—2

PLECTOMYCETES

[CH.

de Bary, who was able to recognize an antheridium and oogonium and the
formation of an ascus or asci from the latter. These and several subsequent
investigations have rendered the reproductive processes in the Erysiphaceae
better known than perhaps in any other group of fungi.

Sphaerotheca Huniuli1 occurs on a variety of common plants, on the
cultivated strawberry, where it is responsible for strawberry mildew,
and especially on the hop. On the latter it is widely distributed in
autumn, and, if the female inflorescences are infected, may do considerable
damage.

The male and female organs arise as lateral branches from the mycelium,
and project at right angles to the infected surface; they are borne on dif-
ferent hyphae, but there is no evidence that these are derived from distinct
mycelia. The oogonium, when fully grown, is an oval, uninucleate structure
two or three times the size of an ordinary vegetative cell; it is cut off from
the parent hyphae and a stalk cell may be differentiated below it (fig. 41 a).

r,, 1 f f"U m ?°S°nium; <*• fertilization; ,. fusion nucleus; /. nuclei

' * young perithecium with binucleate s^enous

1 S. Hiimuli (DC.)

Castagtiei Lev.

Ill]

ERYSIPHALES

The antheridial branch is much narrower; it applies itself to the side of
the oogonium and when first cut off contains a single nucleus (fig. 41 a).
It is clearly differentiated from the hyphae of the sheath not only by its
form and behaviour but by its much earlier appearance and definite relation
to the oogonium. Its nucleus soon divides ; one of the daughter nuclei
passes to the apex of the branch and a wall is formed cutting off the uni-
nucleate antheridium. The oogonial nucleus is rather larger than those of
the vegetative cells, the antheridial nucleus decidedly smaller.

The investigations of Harper, and subsequently of Blackman and Eraser,
show that the wall between the oogonium and antheridium now breaks down
(fig. 41 b}, the male nucleus passes into the oogonium, travels to the female
nucleus and fuses with it (fig. 41 c, d}. The pore between the sexual cells
soon closes and the cytoplasm left behind in the antheridium degenerates,
sometimes forming a densely staining cap on the oogonium. The fertilized
oogonium elongates, the fusion nucleus divides (fig. 41 f) and a wall separates
the daughter nuclei so that two uninucleate cells are formed. The upper
divides again and eventually a row of cells is produced, the penultimate con-
taining two nuclei while the others are uninucleate (fig. 41 £•). The formation
of the first wall is sometimes delayed, so that the undivided oogonium may
for a time show two or three nuclei.

At about the time when the sexual organs reach maturity the develop-
ment of the sheath begins, branches grow out from the stalk of the oogonium
and enclose the sexual organs in a
single layer of cells. These give off
branches towards the interior, and
thus a second zone is formed whose
cells become rich in cytoplasm and
contain two or three nuclei each. The
nutritive and protective envelopes are
thus laid down and their further de-
velopment produces the typical sheath
already described.

Meantime the penultimate cell of
the septate oogonium enlarges to form
the single ascus characteristic of
Spliaerotheca, the terminal cell and
the cells below the ascus are pushed
aside and disappear, the two nuclei

fuse, the USUal three successive nuclear Fig. 42. Sphaerotheca //«*«/* (DC.) Burr.; de-
velopment of archicarp ; in c. two nuclei, re-

di visions take place, and asCOSpores garded as the product of division, are shown in
i j the oogonium, while a cell at the top of the

are produced. oogonium, regarded as the antheridium, still

The only record of the number of contains a nucleus; after Winge.

86

PLECTOMYCETES

[CH.

chromosomes is that of Winge who describes eight in the first and second
mitoses, and four in the third, and suggests that a brachymeiotic reduction
takes place.

According to the interpretations of Dangeard and Winge fertilization
does not take place in the oogonium of SpJiaerotJieca Humuli. For them
the degenerating mass in the antheridium includes the male nucleus which
thus degenerates in situ and the two nuclei seen lying side by side in the
female organ represent the product of a premature division (fig. 42).

Again Bezssonoff working on Sphaerotheca mors-uvae, the economically
important gooseberry mildew, records the entrance of the male nucleus into
the oogonium, but does not observe its fusion with the female nucleus. He
finds four chromosomes throughout the divisions in the ascus.

Erysipfte Polygoni1 occurs on the leaves and stems of a considerablevariety
of hosts belonging to a number of different families. The development of the
sexual organs takes place much as in Sphaerotheca Humuli, and, here also,
Harper has observed the entrance of the male nucleus into the oogonium,
and its fusion with the female nucleus (fig. 43^). After fertilization the

Fig. 43. ErysiphePolygoni; a. fertilization; b. young perithecium
with ascogenous hyphae ; after Harper.

protective hyphae begin to grow up, the oogonium elongates, the fusion
nucleus divides till a row of from five to eight nuclei is produced, transverse
walls appear, and a row of cells is formed of which the penultimate contains
two or more nuclei.

From the surface of the penultimate cell, and perhaps sometimes from
that of ,.., neighbours filaments bud out (fig. 43*), branch rapidly to form

In the' T' " T ^*™' These ™ the ascogenous hyphae.

hem some six or eight intercalary cells, which will give rise to asci

:come distinguished by the fact that each contains two n^ The rest

.ifk, P,,Kmi

„„„„„„,.,

Ill]

ERYSIPHALES

lose their contents and are displaced by the developing asci. Later the
fusion of the two nuclei in each ascus takes place, and in each eight spores
are formed.

Dangeard, investigating the development of E. Polygoni and E. Cicho-
racearum, notes that in his material the oogonium underwent septation
before a row of nuclei was formed, and that cells other than the penultimate
contained two or more nuclei. Usually in E. Cichoracearum and sometimes
in E. Polygoni the oogonial branch consisted of two cells; this corresponds
with the arrangement in the antheridial branch, which is regularly bicellular.
In both cases the lower cell is to be regarded as a stalk. In regard to the
occurrence of fertilization Dangeard's conclusions correspond with those
which he reached in relation to Sphaerotheca.

Phyllactinia Corylea infects the leaves of deciduous trees and shrubs in-
cluding ash, oak, beech, hazel and hornbeam.

The sexual organs arise (Harper 1905), as in other mildews, where two
hyphae intersect. They become closely applied to each other, and, as the
oogonium grows more quickly than the antheridial branch, it becomes some-
what twisted around the latter. The subsequent history is very like that of
Sphaerotheca or Erysiphe. A uninucleate antheridium is cut off, the male
nucleus enters the female organ (fig. 44^), nuclear fusion takes place, the

Fig. 44. Phyllactinia Corylea (Pers.) Karst.; a. fertilization;
b. fusion nucleus in oogonium ; c. d. young perithecia ; alter
Harper.

oogonium elongates and enlarges in diameter and the fusion nucleus divides.
The first nuclear division is apparently never accompanied by cell wall
formation, so that a binucleate stage persists for some time. Finally, however,

PLECTOMYCETES

[CH.

the usual row of three to five cells is formed. The penultimate cell regularly
contains more than one nucleus ; the rest, as a rule, are uninucleate.

Just after fertilization the sheath begins to grow up (fig. 44 b), springing
in this case from the stalk cell of the antheridium, as well as from that of
the oogonium, and developing into the three layers described above.

The ascogenous hyphae arise as lateral branches from the septate
oogonium (fig. 44*:), all or most being derived from the penultimate cell
about which they are crowded and intertwined. They are at first multi-
nucleate, and, as development proceeds, push up vertically within the peri-
thecium (fig. 45); septation then takes place. The asci, of which there are
several in each perithecium, arise as lateral outgrowths from the intercalary
cells, or are formed directly from the terminal cells of the ascogenous hyphae.
Each young ascus contains two nuclei, but the remaining cells are almost
without exception uninucleate. Fusion takes place in the ascus (fig. 46) and
is followed by three nuclear divisions ; as a rule only two spores are formed.

F'g-45- Phyllactinia Cory lea (Pers.) Karst.; peri-
lecmm containing uninucleate asci; after Harper.

Fig. 46. Phyllactinia Corylea
(Pers.) Karst.; a. b. fusion in
ascus; after Harper.

Chr°mOSOmeS (fiS' 47) have been observed throughout the life-

In Plyllactinia CoryUa and also in Microspkaera Aim (Sands, ,907) and
vanous spec.es of Erysip,* (Harper, ,905), the organization of he re tin-
nucleus „ very characteristic. A deeply staining central body lies against
the nuclear membrane and to this the chromatin threads L attached
From ,t they extend into the central cavity of the nucleus forming a sheaf
of d,vergent rays connected laterally by delicate fibrillae (fig 46)

Ill]

ERYSIPHALES

89

In Phyllactinia there is evidence that the number of main strands
corresponds to the number of chromosomes, and that, in fact, these persist

Flg- 47- Phyllactinia Corylea (Pers.) Karst.; a. metaphase of first division in ascus; b, ana-
phase of first division ; c. anaphase of second division in ascus ; d. anaphase of third
division; after Harper.

throughout the resting stages that intervene between successive divisions,
and fuse in pairs after nuclear fusion.

ERYSIPHACEAE: BIBLIOGRAPHY

1895 HARPER, R. A. Die Entwickelung des Peritheciums bei Sphaerotheca Castagnei.
Ber. d. deutsch. Bot. Gesell. xiii, p. 475.

1896 HARPER, R. A. Uber das Verhalten der Kerne bei der Fruchtentwickelung einiger
Ascomyceten. Jahrb. fur wiss. Bot. xxix, p. 655.

1897 DANGEARD, P. A. Second memoire sur la production sexuelle des Ascomycetes.
Le Botaniste, v, p. 245.

1897 HARPER, R. A. Kernteilung und freie Zellbildung im Ascus. Jahrb. fiir wiss. Bot.

xxx, p. 249.

1900 SALMON, E. S. A Monograph of the Erysiphaceae. Mem. Torrey Bot. Club, ix, p. I.
1903 NEGER, F. W. Neue Beobachtungen iiber das spontane Freiwerden der Erysipheen-

fruchtkorper. Centr. f. Bakt. Parasit. u. Infekt. ii, Abt. x, p. 570.
1905 BLACKMAN, V. H. and FRASER, H. C. I. Fertilization in Sphaerotheca. Ann. Bot.

xix, p. 567.
1905 HARPER, R. A. Sexual Reproduction and the Organisation of the Nucleus in Certain

Mildews. Publ. Carn. hist. Washington.

1905 SALMON, E. S. On Endophytic Adaptation shown by Erysiphe graminis D.C.
under cultural conditions. Phil. Trans, cxcviii, p. 87.

1906 SALMON, E. S. On Oidiopsis taurica an Endophytic member of the Erysiphaceae.
Ann. Bot. xx, p. 187.

1907 DANGEARD, P. A. L'origine du perithece chez les Ascomycetes. Le Botaniste, x,
p. 216.

1907 SALMON, E. S. Notes on the Hop Mildew. Journ. Agr. Sci. ii, p. 327.

1907 SANDS, M. C. Nuclear Structure and Spore Formation in Microsphaera Aim. Trans.

Wisconsin Acad. Sci., Arts and Letters xv, pt. 2, p. 733.
1911 WINGE, O. Encore le Sphaerotheca Castagnei. Bull. Soc. Myc. de France, xxvu,

p. 211.

90 PLECTOMYCETES [CH.

1912 FOEX, M. Les conidiophores des Erysiphace"es. Rev. Ge"n. Bot. xxiv, p. 200.

1913 SALMON, E. S. Spraying Experiments against the American Gooseberry Mildew,
Journ. S. E. Ag. Col. xxii, p. 404-

1913 SALMON, E. S. Observations on the Life-History of the American Gooseberry
Mildew, Journ. S. E. Ag. Col. xxii, p. 433.

1913 SALMON, E. S. Observations on the Perithecial Stage of the American Gooseberry
Mildew, Journ. S. E. Ag. Col. xxii, p. 440.

1914 BKZSSONOFF, M. N. Sur quelques faits relatifs a la formation du pe"rithece et la
delimitation des ascospores chez les Erysiphaceae. Comptes Rendus Ac. Sci. clviii,
p. 1123.

Perisporiaceae

The Perisporiaceae include about three hundred species, many of which
are but little known, while none have been cytologically investigated. They
develop as epiphytes on the leaves or young parts of plants, or occur on
decaying plant substances. They usually possess a dark-coloured filamentous
mycelium, but this sometimes forms a firm stroma, or again may be altogether
lacking. The perithecia are superficial, dark in colour, and usually more or
less spherical ; they are typically without appendages, but mycelial out-
growths from their base may simulate these structures as in Meliola. The
wall of the perithecium is generally membranous, more rarely carbonaceous
and brittle; as a rule there is no definite opening but sometimes an irregular
rent is formed at the apex (Antennarid), and sometimes the perithecium
opens by valves (Capnodiwri). The asci are elongated and more or less
cylindrical and the spores have one or more septa and are sometimes
muriforrn; paraphyses are not generally developed.

Dimerosporium, the largest genus with some sixty species, is epiphytic on
the leaves of angiosperms.and one species (D. Collinsii} forms witches'-brooms
on the service-berry. The mycelium is dark-brown, the spores two-celled.

The species of Capnodium, Apiosporium and Meliola, are among the soot
fungi, which form a black coating on leaves. They are purely epiphytic and
saprophytic, subsisting on the honey dew secreted by insects, and doing little
damage, as they are seldom thick enough to interfere with the supply of light.

In several species a considerable variety of accessory fructifications are
produced. Thus Meliola Penzigi, the "sooty-mould" of the orange, has
conidia which differ little from the vegetative cells, multi-cellular conidia,
conidia borne in small spherical pycnidia, and conidia abstricted from
conidiophores in pustules or conceptacles, which may be flask-shaped or
variously branched ; some of these accessory spores are developed in great
abundance and perithecia are relatively rare.

PERISPORIACEAE: BIBLIOGRAPHY

1897 WEBBER, H.J. Sooty Mould of the Orange and its Treatment. U.S. D*pt Ag. Veg.

Phys. and Path. Bull. 13.
1892 ELLIS, J. B. and EVERHART, B. M. North American Pyrenomycetes. Ellis and

Everhart, New Jersey.

in] EXOASCALES gi

Microthyriaceae

The aerial mycelium of the Microthyriaceae is dark-coloured and super-
ficial ; the flattened perithecia are shield-shaped and only the upper part of
the sheath is fully developed ; it consists of a disc of radiating hyphae,
which increase by branching as they grow towards the periphery, and are
firmly attached one to another along their lateral walls. In this way a
continuous layer of pseudoparenchyma is formed, below which the asci
develop more or less at right angles to the surface of the leaf. The asci are
cylindrical or pyriform, and the spores frequently bicellular. A definite
ostiole may be formed, as in Microthyrium, or the perithecium may tear
open at the apex as in Asterina. These two, with about forty and ninety
species respectively, and Asterella with sixty are the largest genera in the
family. The species are mainly tropical with a few representatives in Europe
and North America.

MICROTHYRIACEAE: BIBLIOGRAPHY

1913 THIESSEN, F. Uber einige Mikrothyriaceen. Ann. Myc. xi, p. 493.-

1914 THIESSEN, F. Uber Membranstructuren bei die Microthyriaceen. Myc. Centr. iii,
P- 273-

EXOASCALES

The Exoascales form a group of obligate parasites on vascular plants ;
they cause hypertrophy of the infected parts, producing yellow, red or purple
discolorations, blisters, curling of the leaves, malformation of the fruit, and
sometimes abnormal branching with the formation of tufts of fasciated twigs
known as witches'-brooms. The latter peculiarity is by no means always
attributable to the Exoascales but is induced also by certain rusts and by
the attacks of insect parasites. The Exoascales are responsible for several
diseases of economic importance including peach leaf curl induced by
Exoascus deformans, a witches' broom on cherries due to E. Cerasi, and the
distortion known as pocket plums caused by the presence of E. Pruni, which
infects the flesh of the fruit and inhibits the development of the stone.

Infection apparently takes place at about the time of the opening of the
buds of the host, probably by means of spores deposited on the bud-scales ;
in cold, moist weather, when the young leaves are in a state of lowered
vitality, the fungus readily gains entrance; it can be checked by the use of
appropriate sprays. Once in the leaf the hyphae in most cases ramify
between the cells of the host, but in Taphrinopsis Latirencia on Pteris
biaurita they are intracellular. No haustoria are developed.

The mycelium may be annual or it may be perennial, hibernating mainly
in the cortex and medulla of the young twigs and causing hypertrophy,
especially of the hypodermal tissue, so that infected branches appear abnor-

PLECTOMYCETES

[CIL

92

mally thick. In such cases the destruction of the infected parts is necessary

in order to combat the disease.

The fertile mycelium is richly branched and consists of relatively short
cells; it is developed mainly on the leaves or carpels of the host, and in

Fig. 48. Exoascits deformans (Berk.) Fuck., x 1000.

these regions asci are produced. Sometimes the mycelium permeates the
whole tissue and the asci arise from hyphae below the epidermal cells and
push up among them (Taphrina anrea\ sometimes the fertile hyphae lie
between the epidermal cells (Magnusiella Potentillae), but in the majority
of cases the asci are developed above the epidermal cells and just below the
cuticle (Exoascus deformans). In the species of Taphrinopsis occurring on
Pteris the asci are produced within the epidermal cells.

The asci either arise directly from the mycelium (figs. 49, 50) or each is
borne on a small, cubical stalk cell (fig. 48) which is cut off from the ascus

Fig. 49. Taphrina aurea (Pers.) Fr.; young asci, x 500.

Ill]

EXOASCALES

93

mother-cell during development. Two nuclei can frequently be recognized
in the cells of the fertile mycelium, and the young ascus, in all investigated
cases, is binucleate. The two nuclei fuse, the fusion nucleus undergoes three
successive divisions and eight spores are formed (fig. 48). In many species
budding of the ascospore takes place, so that the mature ascus contains
numerous minute conidia (fig. 50) by means of which the fungus is distributed.
The Exoascales include the single family Exoascaceae ; with this is
sometimes associated the Ascocorticiaceae containing the saprophytic

Fig. 50. Taphrina aurea (Pers.) Fr. ; mature asci, x 500.

genus Ascocorticium with five known species. The asci of Ascocorticiitm,
like those of the Exoascaceae, are cylindrical in form, parallel in arrange-
ment and quite unprotected. It is open to question whether the parallel
arrangement of the asci in the Exoascaceae has any phylogenetic significance
or is not rather the result of their development on the surface of the carpel
or leaf. The cylindrical form of the ascus, however, does not suggest a
primitive group. It may perhaps be inferred that the Exoascaceae are
reduced forms derived from one of the phyla with protected asci ; there
does not appear at present to be any clue to their probable ancestry. The
same is true of the Ascocorticiaceae, of the development of which even less
is known.

Exoascaceae

The classification of the Exoascaceae, and especially the separation of
the two principal genera, Exoascus and Taphrina, has been based on a
variety of different characters including the form of the ascus, the develop-
ment or not of conidia from the ascospores, the annual or perennial character
of the mycelium and the presence or absence of a stalk cell. Boudier
defines Exoascus as having asci usually octosporous and usually provided
with a basal cell; Taphrina as having asci usually polysporous, sometimes
provided with a basal cell.

94 PLECTOMYCETES [CH. in

The mycelium on which the asci are borne consists wholly or mainly of
binucleate cells. The young ascus, as shown by Dangeard in 1894, is at
first binucleate; the nuclei soon fuse and the fusion nucleus divides in
preparation for spore-formation.

In Taphrina Cerasi Ikeno in 1903 described the presence, after nuclear
fusion, of a densely staining nucleolus or chromatin body as the only nuclear
structure in the ascus. A spindle was formed, apparently from the substance
of the nucleolus, the remainder of which became the single chromosome.
The latter divided by a simple karyokinesis, the spindle was reabsorbed
and the process twice repeated to give rise to eight chromatin bodies about
which the spores were delimited. In Taphrina Kusanoi and other species
Ikeno found no sign of karyokinetic division but the chromatin body under-
went successive direct divisions to give rise to eight spore nuclei.

The nuclei of the Exoascaceae are small and difficult to stain so it is
possible that future investigation may modify Ikeno's account ; should it
be confirmed it may perhaps be regarded as indicating stages in the dis-
appearance of karyokinesis and a useful comparison may be instituted with
the similar processes in the Uredinales.

EXOASCACEAE: BIBLIOGRAPHY

1887 KNOWLES, E. L. The Curl of Peach Leaves; a Study of the Abnormal Structure

produced by Exoascus deformans. Bot. Gaz. xii, p. 216.

1894 DANGEARD, P. A. La reproduction sexuelle desAscomycetes. Le Botaniste, iv, p. 30.
1903 IKENO, S. Die Sporenbildung von Taphrina-krtva. Flora, xcii, p. i.

CHAPTER IV

DISCOMYCETES

THE term Discomycetes is applied to those groups in which the fruit is
more or less cup-shaped (fig. 51), with the hymenium fully exposed at
maturity, and to their immediate allies. The ascocarp is surrounded by a
peridium or sheath of closely interwoven hyphae which is closed at first and
later is pushed apart by the paraphyses, so that at last it forms the outer

Fig.

Otidea aurantia Mass.;
nat. size.

ipotheci, Fig. 52. Lachnea stercorea (Pers.) Gill.; ascocarp in
longitudinal section showing young asci and para-
physes, x 160. a. sheath; b. paraphyses; c. ascus;
a. ascogenous hyphae ; e. oogonium ;/. stalk of archicarp.

wall of the cup (fig. 52). The lower part of the cup is filled by the hypo-
thecium, a tangle of hyphae, some vegetative, some ascogenous. These
give rise to the sub-hymenial layer where the paraphyses have their origin
and where the young asci are developed. The asci and paraphyses grow up
together and rise to the surface of the ascocarp forming the hymenium or
fertile disc which is spread over the interior of the cup. The asci are more
or less cylindrical and parallel one to another and to the paraphyses (fig. 53).
They open either by a lid (fig. 55) or by the ejection of a plug (fig. 54).
They arise in succession so that large numbers may be produced in a single
ascocarp. If the hypothecium is well developed the apothecial cup is full
and the hymenium lies across the brim like the skin on a bowl of custard ;
if the development of the hypothecium is slight the hymenium spreads over

96

DISCOMYCETES

[CH.

the sides and bottom of the cup. In many cases, as in Peziza vesiculosa and
Otidca aurantia, the cup is small and comparatively full when it first opens,
and grows larger and deeper as development proceeds.

Fig. 53. Hiimaria rutilans (FY.) Sacc. ; hymenial layer
showing asci and paraphyses in various stages of develop-
ment, x 400.

Fig. 54. Mitrula laricina Mass.;
development and ejection of
biseriate spores , x 600.

This typically discomycetous ascocarp or^apothecium, which is well seen
in the Pezizales, may be connected in one direction, through the Patel-
lariaceae and their allies, with the fructifications of the Phacidiales, which are
partly closed with a more or less stellate aperture, and with the characteristic-
ally elongated fructifications of the Hysteriales, which open by a narrow
slit. The apothecia of this last series show a close resemblance to the
perithecia of certain Pyrenomycetes, and, as far as their mature structure
is concerned, they may be placed as logically in one group as the other.
Nor have we at present any information with regard to development which
can decide the question. It remains even possible that the Hysteriales are
a transition series and that some of the forms grouped among Discomycetes
may have arisen from the Pyrenomycetes or vice versa.

In another direction the typical apothecium, when very widely open
suggests the reflexed ascocarp of Rhizina or Sphaerosoma and such a type

IV]

DISCOMYCETES

97

may, by invagination of the fertile surface, have produced the closed fruit
of the truffles. The simpler Tuberales may have had a similar origin, or
may have arisen direct from a pezizaceous
form, such as Sepultaria, with which Genea
has several points in common.

It is not impossible that \h&Rhizina group,
by the development of a sterile stalk, has also
produced the Helvellaceae and it may be the
Geoglossaceae as well. But the latter family,
because of the characteristic method of dehis-
cence of its ascus (by the ejection of a plug
of wall material), has sometimes been looked
upon as related to the Helotiaceae and their
allies which show a similar dehiscence.

Massee has developed a theory that forms
with large, coloured, and elaborately sculp-
tured spores, tend to be primitive. He thus
regards the Tuberaceae and Geoglossaceae
as ancient groups from both of which pezi-
zaceous forms have sprung.

Bucholtz's work on the development of
Tuber diminishes the probability that this is
a primitive type, or one that has given rise
to cup-shaped forms, and it seems easier to
think of Genea and its allies as derived from
the Pezizales by the diminution in size of
the external aperture, the shortening and
broadening of the ascus and the increased
convolution of the hymenium, than to regard
them as giving rise to that group by the
contrary changes. It is, however, not impro-
bable that the Pezizales are polyphyletic in
origin, and that some of them may have been
derived from the higher Geoglossaceae.

So far we have considered mainly the
external characters of the fruit and the struc-
ture of the ascus, but when we turn to the
Pezizales we find a further, and possibly a more valuable, criterion in the
structure of the sexual organs.

The antheridium is known in very few cases. A large, oblong coenocytic
cell has been described in Ascodesmis, and a similar, though larger, organ
in Pyronema and in Lachnea stercorea, and we have also, if its position

G.-V. 7

Fig. 55. Sepultaria coronaria Mass.;
uniseriate spores ; ascus opening by
a lid ; branched, septate, clavate
paraphyses ; x 600.

98

DISCOMYCETES

[CH.

should be ultimately established, the curious stalked conidium of Ascobolus

carbonarius. ... .

The archicarp is of much commoner occurrence, and seems more likely
to be useful as a gauge of relationship. Among Discomycetes the simplest
type is undoubtedly that of Ascodesmis or Thelebolus; the significant details
in Tkelebolus are not fully known, but in Ascodesmis we have a stout, twisted
hvpha divided into three parts, the unicellular trichogyne, the unicellular
coenocvtic oogonium and the multicellular stalk (fig. 56). After fertilization

Fig. 56. Ascodesmis nigricans Van Tiegh.; sexual
apparatus; a. trichogyne; b. antheridium ; c.
oogonium; d. stalk; e. gametophytic hypha;
after Claussen.

Fig- 57- Pyronema confluens; spherical oogo-
nium giving rise to ascogenous hyphae; a. an-
theridium ; b. trichogyne; c. oogonium ; d. as-
cogenous hyphae; x 1040; after Claussen.

the oogonium becomes septate, so that the fertile part is multicellular and
the ascogenous hyphae arise from several cells. This type closely approxi-
mates to that in Eurotium and1 some other Plectascales, and there seems
reason to regard it as a primitive female organ among Discomycetes.

From it may be derived the spherical oogonium of Pyronema (fig. 57)
which differs mainly in the fact, no doubt connected with its shape, that it
does not become septate after fertilization, so that the ascogenous hyphae
arise from one cell only. The same is true of Lachnea stercorea, which

iv] DISCOMYCETES 99

differs in its multicellular trichogyne, and of Humaria gramdata, and perhaps
some other forms in which the trichogyne, like the antheridium, has dis-
appeared.

Another group is distinguished by the multicellular oogonial region of
the archicarp, which has also a stalk and a terminal region (or trichogyne)
of several cells each (fig. 58). This type of female
organ is sometimes termed a scolecite. It occurs
in Lachnea cretea and in several species of Asco-
bolus and Ascophanus.

In A scobolus furfur aceus several of the central
cells communicate one with another by means of
pores, but only one of them gives rise to asco-

Fig 58. Ascobolus furfuraeeus

genous hyphae ; in some other species of Asco- pers.; archicarp, x74o; after
bolus and in the genus AscopJianus ascogenous Dodge.
hyphae arise from several communicating cells; the same is true of Lachnea
cretea, where three or four cells become practically continuous owing to the
disappearance of the transverse septa between them.

In the trichogyne also, or terminal region of the archicarp, pores are
formed in the transverse walls, so that this multicellular organ offers no bar
to the passage of male nuclei.

Such structures may well have been derived from the Ascodesmis type
by the elongation and transverse septation of the parts of the archicarp.
Our knowledge of the sexual organs of the Pezizales thus suggests that they
may have been derived, along two principal lines of development, from
a common ancestor within the group.

In only two other families of Discomycetes, the Rhizinaceae (R/iisina
and Sphaerosomd) and the Geoglossaceae (Leotia} has an oogonium been
recognized. In each of these a large fertile cell is present, but its develop-
ment is not known and no suggestions as to phylogeny can therefore be
based upon it.

Our knowledge of the development and especially of the reproductive
organs of the Discomycetes is still very incomplete and further research is
very necessary. As has been shown in Leotia, Humaria and other cases, it
by no means follows that because one member of a genus has lost its sexual
apparatus the same will be true of others. Every available species should
be investigated.

The Discomycetes include over 4000 species and may be subdivided as
follows :

Hymenium fully exposed at maturity

mature ascophore cup-shaped PEZIZALES.

mature ascophore reflexed or stalked with the fertile
region often convoluted

7—2

I00 DISCOMYCETES [CH,

Hymenium incompletely exposed at maturity

ascophore round, aperture usually stellate PHACIDIALES.

ascophore elongated, opening by a slit HYST

Hymenium enclosed at maturity TUBERALES.

PEZIZALES

The Pezizales are characterized by the fleshy or sometimes leathery
ascocarp, bounded, except in the Pyronemaceae, by a more or less definite
peridium which is closed at first and opens later, giving the mature fruit a
cup or saucer shape.

This dehiscence is due to the growth of a conical mass of paraphyses
which push out at the apex of the ascocarp. Fresh paraphyses and, a little
later, asci grow up amongst those first formed and the peridium is pushed
wide open and the hymenium exposed.

The asci contain usually eight, but sometimes four, sixteen, thirty-two,
or numerous spores, which germinate typically by means of germ-tubes, but
which, in a few cases, give rise by budding to conidia. Various accessory
spores, including conidia, chlamydospores and oidia, are also produced.

The mycelium is well developed and filamentous, rarely forming a scle-
rotium. The species are parasitic or saprophytic on the ground or on dead
parts of plants ; in many cases they are coprophilous.

Considering the very large size of the group the number of species
investigated is small. In a few of these, normally functional male and
female organs have been found, in some the antheridium has disappeared,
and in many the oogonium is also lacking. Where an oogonium is present
it gives rise to the ascogenous hyphae, while the paraphyses originate from
the stalk or from the surrounding cells (fig. 52).

The grou-p may be divided into the following families :

Peridium continuous with hypothecium

Peridium incomplete ; ascocarps usually compound PYRONEMACEAE.

Peridium well-developed
asci not rising above the surface when ripe ; asco-

spores usually uniseriate PEZIZACEAE.

asci rising above the surface when ripe ; ascospores

often coloured and biseriate ASCOBOLACEAE.

Peridium distinct from hypothecium

Peridium of elongated hyphae (pseudoprosenchymatous) HELOTIACEAE.
Peridium pseudoparenchymatous MOLLISIACEAE.

Peridium absent or ill-defined ; epithecium formed CELIDIACEAE.

Peridium tough ; epithecium formed

ascocarp free PATELLARIACEAE.

ascocarp embedded when young CENANGIACEAE.

Apothecia numerous, sunk in a stroma CYTTARIACEAE.

IV]

PEZIZALES

101

Pyronemaceae

The Pyronemaceae are a small group distinguished from the other

Pezizales by the fact that the peridium, or lateral boundary of protective

hyphae around the fruit, is not well developed.

This is not always regarded as a sufficiently important character to

warrant their separation from the Pezizaceae and many authors include

them in that group.

The only important genera are Ascodesmis and Pyronema, species of

both of which have been somewhat fully investigated.

Ascodesmis nigricans^ (fig. 59) is a small coprophilous form.

The sexual organs appear in artificial culture about forty-eight hours

after the germination of the spore.

Stout, multinucleate hyphae grow

up from the mycelium and dicho-
tomize (fig. 6oa) to give rise to some

six or eight archicarps. Near these,

and usually from the same filament,

one or two antheridial hyphae arise.

They grow towards the archicarps

(fig. 60 b) and dichotomize (fig. 60 c),

while around each of their terminal

cells or antheridia, an archicarp

becomes wrapped (fig. 60 d).

In the meantime walls are laid
down, so that the various archicarps
and antheridia become cut off from
their neighbours, and each archicarp
divides transversely to form a tri-
chogyne and an oogonium. The trichogyne usually contains two nuclei,
the oogonium five or six and the antheridium about the same number. The
nuclei of the trichogyne soon degenerate, and, as observed by Claussen, the
wall between this cell and the antheridium is broken down (fig. 60 e\ so
that open communication is established. The male nuclei pass into the
oogonium, where for a time ten or twelve nuclei may be counted, then fusion
of these in pairs takes place (fig. 6o/). Subsequently the oogonium enlarges
somewhat and undergoes septation ; large ascogenous hyphae, usually about
three in number, bud out from it (fig. 60^-), and quickly give rise to asci
(fig. 60 h). Ascus formation is apparently quite typical, the spores are
spherical and have a characteristically sculptured epispore (fig. 6o/). At

1 Claussen described the cytology of this species under the name of Boudiera hypoborea Karst. ;
see Cavara, Ann. Myc. iii, 1905, p. 363, and Dangeard, Botaniste, x, 1907, p. 247, for nomenclature.

59- Ascodesmis nigricans Van Tiegh. ; apo-
thecium, X34o; after Claussen.

102

DISCOMYCETES [CH-

about the time of fertilization vegetative filaments begin to grow up (fig. 60 d\
and at last form a loose investment around and among the developing asc,
(fig. 59)-

Fig. 60. Ascodesmis nigricans Van Tiegh. ; a. b. c. d. development of the sexual apparatus'; a. and
b. x 1000, c. xnoo, d. x 800 ; e. communication between antheridium and trichogyne, xi3<x>;
f .fusion in oogonium, x 1600; g. septate oogonium and ascogenous hypha; antheridium and
trichogyne shrivelled, x 1000; h. uninucleate ascus, x noo; /'. sculptured spores in ascus, x 750;
after Claussen.

Pyronema confluens^ occurs on burnt ground or on charred and decayed
leaves in woods. Its fruits are pink or salmon-coloured, its mycelium to a
great extent superficial, and its sexual apparatus of unusually large size.
The latter fact led to an early study of its development.

It was described by de Bary in 1863, by the brothers Tulasne in 1865
and 1866, by van Tieghem in 1884, and by Kihlman in 1885, and a very
clear understanding of the morphology of the sexual organs was reached.
A swollen, elongated antheridium was recognized and a more or less globular

1 Pyronema confluem Tul. = P. omphaloides (Bull.) Fuckel.

IV]

PEZIZALES

103

oogonium, from which a trichogyne protruded (fig. 61 b). The union of the

trichogyne and antheridium was observed and it was shown that from the

oogonium ascogenous hyphae subsequently

arose. Van Tieghem recorded that the species

is very susceptible to external conditions, the

antheridium sometimes being reduced in size

or absent, though the oogonium nevertheless

developed normally and produced ascogenous

hyphae.

In 1900 appeared the classical researches
of Harper, followed in 1903 and 1907 by
Dangeard's, and in 1912 by Claussen's investi-
gations.

The mycelium is made up of cells of varying
length, regularly multinucleate, containing six
to twelve nuclei, and filled with cytoplasm of
a loose, spongy structure. The mycelium is
sparse and loose, but the reproductive organs
are very abundant so that the ascocarps, when
mature, are often crowded together,

The first indication of sexual reproduction
consists in the appearance of thick hyphae,
very similar to the corresponding filaments in
Ascodesmis, and tending, like them, to stand
at right angles to the substratum. They dicho-
tomize (fig. 6 1 a), the terminal cells become swollen, and two types, the more
spherical oogonium and the more elongated antheridium, are distinguished ;
these arise on separate branches, but from the same mycelium. Both are
multinucleate from their initiation.

Very soon a slight elevation appears on the oogonium; it elongates
rapidly to form the multinucleate trichogyne and, before its growth is
complete, is separated from the oogonium by a wall; the trichogyne and
antheridium grow towards one another, the tip of the trichogyne meeting
sometimes the apex, but more commonly the flank of the male organ.

The mature oogonium is a spherical or flask-shaped cell filled with
dense cytoplasm and containing many nuclei which are very much larger
than those of the ordinary vegetative cells. Its stalk consists of two or
three broad cells, its apex is continued into the trichogyne. The nuclei of
the latter increase but little in size and are thus much smaller than those of
the essential organs at maturity. The nuclei of the antheridium are almost
as large as those of the female cell, but its protoplasm is less dense owing
perhaps to the absence of accumulated reserve materials. It would appear

Fig. 6 1 . Pyronema confltiens Tul. ; a.
development of sexual apparatus ;
b. mature oogonia and antheridia ;
x 390 ; after de Bary.

DISCOMYCETES

[CH.

104

that in both oogonium and antheridium some nuclei degenerate

Hvphae from the ascogonial and antheridial branches and also from the

surrounding cells, begin to grow up even before ferfhzahon, and later

envelop the sexual organs. .

When fertilization is about to take place an area of cytoplasm in the
region of the antheridium, against the wall of which the tip of the trichogyne
is pressed is differentiated as a very finely granular disc from which the
nuclei are withdrawn. Although located in the antheridium this area
resembles the receptive spot seen in the oosphere of many algae. The tip
of the trichogyne has by this time developed as a beak-like projection, and
this also is empty of nuclei and contains dense and finely granular cytoplasm.

The walls of the antheridium and trichogyne now break down at the
point of contact and a pore is formed. The process is gradual, consisting
probably of a softening and solution of the wall material, which seems to

Fig. 62. Pyronema conjluens ; a. antheridium, trichogyne and oogonium,
male and female nuclei collected in the middle of the latter ; b. c. fusion
of male and female nuclei ; after Harper.

spread out into the cytoplasm of the beak, suggesting that the solvent
action is mainly exerted from the interior of the trichogyne. The open
pore now becomes thickened around its margin so that an exceedingly
strong ring unites the antheridium and trichogyne, and they can be bent
or turned upon each other without being pulled apart. This arrangement
is no doubt necessary to withstand the strain set up by the flow of nuclei
from the relatively wide cavity of the antheridium through the narrow pore
and beak.

IV]

PEZIZALES

105

While the formation of the pore is in progress the nuclei of the tricho-
gyne degenerate, and, by the time that they are completely disorganized a
migration of the male nuclei through the pore begins. Ultimately the
contents of the trichogyne degenerate still further, till the cytoplasm and
nuclei together form a densely staining mass which may be recognized even
in the mature fruit. The male nuclei continue to pass into the tube until it
is densely filled, and sometimes a trifle swollen. According to most observers
the wall at the base of the trichogyne now breaks down so that an open
passage is formed and the male nuclei travel through (fig. 63 a), and mingle

Fig. 63. Pyronema confluens; a. entrance of male nuclei into oogonium, x 1435; b. association of
male and female nuclei, x 1160; c. ascogenous hyphae with nuclei in pairs, x82o; after
Claussen.

with the female nuclei. After their migration is complete a fresh wall is
laid down across the base of the trichogyne, cutting off the oogonium once
more as a single spherical cell.

The female nuclei meantime become aggregated together (fig. 620) and
form a hollow sphere or dome or a sickle-shaped group. This is no doubt
a provision for insuring their association with the male nuclei with the
greatest certainty and dispatch.

According to both Harper and Claussen, the sexual nuclei now pair;
Harper has recorded complete fusion at this stage (fig. 62 b}, while Claussen
(fig. 63 b} regards the nuclei as merely associated in preparation for their
ultimate union in the ascus. Dangeard. on the other hand, denies the dis-
appearance of the wall between the oogonium and trichogyne or the passage
of the male nuclei beyond the latter organ, and Brown has described a
variety in which the trichogyne and antheridium fail to unite.

io6

DISCOMYCETES

[CH.

In any case the greater part of the male cytoplasm does not enter the
oogonium but is left behind in the antheridium and trichogyne ; con-
sequently these organs, after their function is complete, remain, to the
superficial view, unchanged for a long period, till they are crushed at last
by the growth of the investing hyphae, or perhaps destroyed by bacteria
(Harper, p. 354).

Before the stages described above, the oogonium has begun to bud out
(fig. 6~2a) at various points, giving rise to the ascogenous hyphae. Into
these the nuclei pass, a few, no doubt unpaired, being left behind in the
oogonium. The hyphae elongate, branch freely and undergo septation, and,
as the vegetative filaments grow up, they ramify among them and at last
bend over and give rise to asci from their penultimate cells. Claussen has
described a paired arrangement of the nuclei in the ascogenous hyphae
(fig. 63*:), and believes the members of each pair to be respectively male
and female.

After the ascogenous and vegetative hyphae are thoroughly interwoven,
a rapid stretching upward of the whole mass ensues. In this growth the
vegetative hyphae outstrip the reproductive ones, and form at first a cone-
shaped mass, made up of their elongated, slender, densely aggregated tips.
These upper extremities of the vegetative hyphae are the young paraphyses.
Their number is constantly increased by the pushing in of new branches
from below, and thus the conical outline of the mass is maintained. The
ascogenous hyphae grow for a certain distance in company with the
vegetative filaments, then their upward growth ceases, and they spread out

horizontally, forming a rather dense layer
below the cone of paraphyses. This is the
base of the hymenium.

Usually in Pyronema, as in Ascodesmis,
several oogonia are invested by a common
sheath, and their ascogenous hyphae mingle
to form the hymenium of a single ascocarp
(fig. 64), but ascocarps developed in relation
to a single pair of sexual organs are not
unknown.

The formation of the asci in Pyronema
is quite typical. The number of chromo-
somes is probably ten (Harper), or twelve
(Claussen), at any rate in the first divisions
in the ascus. Dangeard records a smaller
number in the third division, and in the
variety inigneum Brown describes five
throughout.

Fig. 64. Pyronema conjliiens; diagram-
matic section through ascocarp ; after
Harper.

iv] PEZIZALES 107

As development proceeds the sexual organs become completely crushed
an'd are at last no longer recognizable. At an early stage it becomes
impossible to trace the connection between the ascogenous hyphae and the
oogonium, and, during a great part of their development, these depend for
their nutrition upon the paraphyses and other vegetative cells.

A secondary mycelium grows downwards to the substratum, obtaining
food material from it and serving for the attachment of the mature ascocarp.
Special storage cells appear in the hypothecium.

PYRONEMACEAE: BIBLIOGRAPHY

1863 DE BARY, A. Entwickelungsgeschichte der Ascomyceten. Leipzig.

1865 TULASNE, L. R. and C. Selecta fungorum Carpologia, iii. Imperial, typograph.,
Paris.

1866 TULASNE, L. R. and C. Note sur les phenomenes de copulation que pre"sentent
quelques Champignons. Ann. Sci. Nat. vi, p. 217.

1884 VAN TIEGHEM, Ph. Culture et developpement du Pyronema confluens. Bull. Soc.
Bot. de France, xxxi, p. 355.

1885 KIHLMAN, O. Zur Entwickelungsgeschichte der Ascomyceten. Pyronema confluens.
Acta Soc. Sci. Fennicae, xiv, p. 337.

1900 HARPER, R. A. Sexual Reproduction in Pyronema confluens, and The Morphology

of the Ascocarp. Ann. Bot. xiv, p. 321.
1905 CLAUSSEN, P. Zur Entwickelungsgeschichte der Ascomyceten. Bondiera. Bot. Zeit.

Ixiii, p. i.
1907 DANGEARD, P. A. Recherches sur le developpement du perithece chez les Ascomy-

cetes. Le Botaniste, x, pp. 247 and 259.
1909 BROWN, W. H. Nuclear Phenomena in Pyronema confluens. Johns Hopkins Univ.

Circ. vi, p. 42.
1912 CLAUSSEN, P. Zur Entwickelungsgeschichte der Ascomyceten. Pyronema confluens.

Zeitschr. f. Botanik, iv, p. I.
1915 BROWN, W. H. The Development of Pyronema confluens, van inigneum. Am.

Journ. Bot. ii, p. 289.

Pezizaceae

The Pezizaceae form a rather large group. The ascocarp is superficial,
sessile or stalked, usually with a well-marked peridium fleshy or waxy in
consistency, and soon decaying after maturity. The spores are usually
hyaline and continuous (though septate in some small species) and are
typically uniseriate. The asci do not project above the level of the disc at
maturity, as they do in the Ascobolaceae. The species are mostly sapro-
phytic, many occurring on the ground, and a few, especially the smaller
forms, on dung. The subdivisions depend on the shape of the spores, the
size and consistency of the ascocarp, and the presence or absence of hairs.

In the majority of forms the fruit is fleshy and without hairs;
species are often grouped together in the single genus Pezisa, but i
probably more convenient to separate them. The name Peziza is retain
for large species with a sessile or subsessile cup, regular in form and

loS

DISCOMYCETES

[CH.

centimetres or more across as in P. vesiculosa. The genus Humaria includes
similar but smaller species, often less than one centimetre in diameter. In
Otidca the sides of the ascophore are laterally split, or vertically incurved
and wavy. In Acetabula and Gcopyxis the ascophore is stalked. In Lacknea,
as well as in some other genera, the fruit is beset with hairs and in Sepultaria
it is hairy and more or less sunk in the soil.

Lachnca stercorea is a small orange species occurring during the winter
and spring on the dung of various animals, especially of cows. With
Humaria granulata and Ascobolus furfuraceus, it is among the very common
coprophilous forms, appearing in many parts of Britain with great regularity
when the Piloboli have died down, and the cow pad is beginning to dry.
It is about 4mm. in diameter and is furnished with numerous stout, septate
hairs.

The archicarp arises as a side branch from the vegetative mycelium, and
divides to form four or more cells. The terminal cell or oogonium is oval
in shape and larger than the others. It contains between two and three
hundred nuclei and is filled with finely granular cytoplasm. In the cell next
below the oogonium, the cytoplasm is also more dense and the nuclei more
numerous than in the other cells of the fertile branch.

Hyphae grow up from the lower cells of the archicarp, and from the
branch which bears it, and form a dense weft above which the oogonium rises.

Fig. 6?. Lachnea stercorea (Pers.) Gill.;
and antheridium, XS

. young archicarp, x8oo; £. archicarp
; P. Highley del.

The oogonium sends out either laterally, or from its apex, a stout branch
or trichogyne. It is cut off by a wall and divides into four to six cells, the
terminal of which is much larger than the others (fig. 65 a). The tip of the
trichogyne protrudes for a time beyond the developing sheath, but later,
with the whole fertile branch, it is enclosed by vegetative hyphae.

iv] PEZIZALES I09

At this stage a large, more or less oval sac is often found to be continuous
with the terminal, or receptive, cell of the trichogyne into which a proportion
of its contents pass (fig. 65^). There seems no doubt that this sac is the
antheridium, but its development is not known, and there is no evidence
that its contents ever pass beyond the receptive cell of the trichogyne.
Indeed all the available evidence shows that both antheridium and trichogyne
are now merely vestigial structures.

Nevertheless the development of the oogonium continues, its nuclei
increase to something over 500 in number, and ascogenous hyphae bud out.
Before passing into these the oogonial nuclei fuse in pairs, so that normal
fertilization is here replaced by the union of female nuclei. The ascogenous
hyphae branch and give rise to asci, in each of which eight spores are
produced in the usual way. The karyokinetic figures are small but very
clear, there are four chromosomes in the first and second divisions, but in
the third telophase only two have been recorded. There is some evidence
that the chromosomes show regular and characteristic differences of form,
which reappear in successive divisions.

The peridium, though much better developed than in the Pyronema-
ceae, is never completely closed, as in Humaria or Ascobolus, across the
top of the ascocarp. The paraphyses are numerous and contain orange
granules.

Lachnea scutellata occurs on decaying wood, forming bright red apothecia.
The archicarp consists of seven to nine cells, the subterminal of which
enlarges to form the oogonium. The nuclei in this cell divide, and, according
to Brown, show five short, stout chromosomes. He did not observe nuclear
fusion or association in the oogonium, but regards the nuclei lying in contact
as the two daughter nuclei of a single mitosis. Large ascogenous hyphae
develop, undergo septation, and branch freely. Their tips bend over and
asci are formed in the usual way from the penultimate cells. The terminal
cells may undergo further growth and give rise, as in several other Disco-
mycetes, to new asci. Nuclear fusion takes place in the young ascus, and is
followed by a meiotic reduction. Five gemini are recorded, but, in the
anaphase of the first division, ten chromosomes travel towards each pole.
This Brown takes to indicate an early fission of the daughter chromosomes.
In the second and third divisions five chromosomes are seen throughout.
Brown infers the occurrence of a single fusion in this species, that in the
ascus, and a single reducing division1.

Laclmea cretea has a pale buff apothecium, beset with hairs (fig. 66#).
It has been found on plaster ceilings, and, like many other saprophytic
species, grows readily in artificial culture.

1 The magnification of Brown's figures of the divisions in the oogonium is enormous (x 11,100),
and their details should therefore probably be received with some caution.

no

DISCOMYCETES

[CH.

The archicarp (figs. 66b-e) consists of a long, branched, muticellular
trichogyne, an oogonial region of three or four coenocytic cells and a
multicellular stalk. No antheridium has been observed. In the trichogyne
(fie, 66 e) pores are formed between the adjacent cells, and are closed after
a Time by "callus" pads. In the central part of the archicarp the transverse
septa are completely broken down, so that a very wide passage is formed,
and nuclei pass readily from cell to cell (fig. 66/). All the cells give rise

Fig. 66. Lachnea cretea Phil.; a. mature ascocarp, x 90; b. c. development of archicarp,
X3oo; d. older archicarp showing crowded nuclei, x 40x5 ; e mature archicarp with
elaborately branched trichogyne, x 400 ; /. three ascogonial cells united by very large
pores, X400.

to ascogenous hyphae. Thus the oogonial region, though developmentally
multicellular, is for all practical purposes unicellular at maturity, and offers
no greater difficulties in the way of fertilization than the oogonium of
Pyronema itself.

The branched character of the trichogyne is exceptional among Disco-
mycetes ; it might, no doubt, facilitate the establishment of contact with an

IV]

PEZIZALES

in

attached antheridium if the latter developed at a distance. But branching
might also be regarded as a secondary or vegetative development, appearing
after normal fertilization had ceased to occur.

The presence of pores in the transverse septa of the trichogyne suggests
that the function of that organ in relation to an antheridium has only
recently been lost.

Fig. 67. Humaria gramilata Quel.; young archicarp, x32o; after Blackman
and Fraser.

The ascogenous hyphae contain many nuclei irregularly arranged. Asci
are formed in° the usu'al way, their nuclei show about J*—™
in the first division. Owing to the small size of the nucle, further

details have not been studied in this species.

[[2 DISCOMYCETES [CH-

Hnmariagmnulata is a common red or orange coprophilous form. The
archicarp develops as a side branch from an ordmary hypha The apical
c I of this branch increases in size and becomes sphencal, formmg the
ooeonium (fi- 67) • it contains large numbers of well-marked nucle,. When
it Ts Jgrown the oogonia! nuclei fuse in pairs (fig. 68 a), and the fusion
nuclei pass into the ascogenous hyphae (fig. 68 /,). There ,s no s,gn of e.ther
trichogyne or antheridium.

Fig. 68. Hmnaria gramdata Quel.; a. fusion of nuclei in oogonium, xjsoo; b. oogonium
giving rise to ascogenous hyphae, x 1250; after Blackman and Fraser.

Vegetative cells grow up and invest the archicarp, forming a close
pseudoparenchymatous sheath in which the ascogenous hyphae ramify.
They give rise at last to asci in the usual way.

Four chromosomes have been recorded in the ascogenous hyphae,
eight in the first division in the ascus and four in the two subsequent

PEZIZALES

mitoses. This implies that the gametophytic number is four, and that the
gemim are formed immediately after the fusion in the oogonium, so that in
the ascogenous hyphae there are four bivalent instead of eight univalent
chromosomes. In the meiotic prophase which follows the fusion in the

is a d°uble number of gemini' since two sp°r°phytic nuclei

In Humaria granulate, the antheridium has disappeared and normal
fertilization is replaced by fusion of female nuclei in pairs in the oogonium.

Fig. 69. Humaria rutilans (Fr.) Sacc.; very young ascocarp,
x 500.

In another species of this genus, Humaria rutilans1, reduction has gone yet
further and not even an archicarp is produced. The apothecium arises as
a dense weft of tangled filaments, which for a time differ from one another
only in the relatively thick walls of the outer hyphae, and the richer proto-
plasmic content of the inner (fig. 69). Each cell of the weft contains one
or a few nuclei. After a while the nuclei in the central part of the mass
may be seen to be of two sizes, and the smaller have been found to fuse in

1 Humaria rutilans (Fr.) Sacc. = Pe ziza rutilans Fr. in Boudier, hones, PI. 315.
G.-V. 8

DISCOMYCETES

[CH.

pairs (fig. 700), giving rise to the larger. Sometimes in connection with
this process a nucleus migrates through the wall from one cell to another
(fig. 70 b\ as in prothallia of ferns. Thus in H. rutilans, where the sexual
organs are completely lacking, normal fertilization is replaced by the union
of vegetative nuclei in pairs.

Fig. 70. Htimaria rutilans (Fr.) Sacc.; a. fusion in a vegetative hypha; b. migration
of nucleus from one vegetative cell to another; both x noo.

The cells which contain fusion nuclei now give rise to ascogenous
hyphae, while, from the rest, the paraphyses and cells of the outer sheath
arise.

^ The asci are very large, and their nuclei particularly clear. The number
of chromosomes in the nuclei of the ascogenous hyphae, and in the first
and second divisions in the ascus and in the prophase of the third is sixteen
(figs. 71, 72). In the third telophase eight have been recorded by Maire and
by Eraser (fig. 73), and sixteen by Guilliermond (fig. 74).

*ig. 71- Humaria rutilans (Fr.) Sacc.; a. asco-
genous hypha showing sixteen chromosomes in
each nucleus x 195o; b. fusion nucleus of ascus
passmgoutofsynapsis, x 1300;, .fusion nucleus
of ascus showing sixteen gemini, x 1950

IV]

PEZIZALES

In several other members of the Pezizaceae, for example in Peziza
vesiculosa (Eraser and Welsford) and Peziza tectoria, development appa-
rently takes place, as in Humaria rutilans, without the formation of sexual
organs.

In Otidea aurantia (Eraser and Welsford), a large cell, no doubt part of
an archicarp, has been recorded in the early stages, and in Peziza thele-
boloides, Humaria Roumegueri, and H. carbonigena, there is a well-marked
oogonial region of one or more cells.

Fig. 72. Humaria rutilans (Fr.) Sacc.; a. telophase of second division in ascus,
x 3370 ; b. prophase of third division in ascus, showing sixteen curved chromo-
somes, x 2808.

Fig. 73. Humaria rutilans (Fr.) Sacc.; a. meta-
phase of third division in ascus, x 2080 ; b. polar
view of telophase of third division in ascus,
showing eight curved chromosomes, x 3100.

Fig. y4. Humaria rutilans; telo-
phase of third division in ascus;
after Guilliermond.

8—2

Il6 DISCOMYCETES [CH.

PEZIZACEAE: BIBLIOGRAPHY
1905 GUILLIERMOND, A. Remarques sur le Karyokinese des Ascomycetes. Ann. Myc.

1905 MAIRE, R. Recherches cytologiques sur quelques Ascomycetes. Ann. Myc. in,

1906 BLACKMAN, V. H. and FRASER, H. C. I. On the Sexuality and Development of
the Ascocarp in Humaria granulata. Proc. Roy. Soc. B. 77, p. 354-

1907 FRASER, H. C. I. On the Sexuality and Development of the Ascocarp in Lachnea
stercorea. Ann. Bot. xxi, p. 349.

1908 FRASER, H. C. I. Contributions to the Cytology of Humaria rutilans. Ann. Bot.
xxii, p. 35

1908 FRASER, H. C. I. and WELSFORD, E. J. Further Contributions to the Cytology of
the Ascomycetes. Ann. Bot. xxii, p. 465.

1909 FRASER, H. C. I. and BROOKS, W. E. St J. Further Studies on the Cytology of
the Ascus. Ann. Bot. xxiii, p. 537.

1911 BROWN, W. H. The Development of the Ascocarp in Lachnea scutellata. Bot. Gaz.

lii, p. 275.
1911 GUILLIERMOND, A. Les Progres de la cytologie des Champignons. Prog. Rei

Bot. vi, p. 389.
1913 FRASER (GWYNNE-VAUGHAN), H. C. I. The Development of the Ascocarp in

Lachnea cretea. Ann. Bot. xxvii, p. 554.

Ascobolaceae

The large majority of the Ascobolaceae are coprophilous ; their ascocarp
is soft and fleshy or somewhat gelatinous, and they possess a well-marked
sheath which is closed during the early stages of development. They are
distinguished from the Pezizaceae by the usually multiseriate arrangement
of their spores, and by the fact that, when ripe, the asci stand well up above
the hymenium before the spores are discharged. Often the asci are large
and few in number ; the spores are brown or violet in Ascobolus, Saccobolus
and Boudiera, hyaline in the other genera ; they are usually ellipsoid, but
round in Boudiera and Cubonia ; in Saccobolus they are enclosed in a special
membrane within the ascus and are ejected together ; and in Thelebolus
and Rhyparobus they are sixteen or more in number.

In most of the species investigated there is a conspicuous multicellular
coiled archicarp, the central part of which gives rise
to ascogenous hyphae. Some of the species also
produce conidia {Ascobolus carbonarius), or chlamy-
dospores (Ascobolus furfur aceus (Welsford), Asco-
pJianus carneus}.

Ascobolus furfuraceus is one of the commonest
dung species, the ascocarp is green or brown in

b. /r. Ascobolus furfura- , . ,

fens Fers ; archicarp, x 74o; colour with a characteristic scurfy margin. The
after Dodge. archicarp (fig. 75) consists of sometimes as many

.IV]

PEZIZALES

117

as twenty (Dodge), sometimes a much smaller number of cells. These are
at first uninucleate (Harper, Welsford), or multinucleate (Dangeard); later
they always contain numerous nuclei (fig. 76a). One of them, usually the

Fig. 76. Ascobolus furfur aceus Pers.; a. young archicarp, x 750; b. rather older
specimen showing pores between the cells, x 625 ; after Welsford.

fourth from the apex (Welsford), enlarges, buds out ascogenous hyphae and
functions as the oogonium. Those near the base form a stalk, and those
towards the apex may be regarded as constituting a now functionless
trichogyne.

The cells on each side of the oogonium communicate with it by means
of pores (fig. 76 b). Additional nuclei pass into it from both the stalk and
terminal cells, and Welsford has observed their fusion in pairs in the
oogonium. The fusion nuclei pass into the ascogenous hyphae. The asci
are large and produce each eight spores which are violet or brownish in
colour ; the epispore is characteristically sculptured at maturity. There are
eight chromosomes in the first division in the ascus, and four in the second
and third (Dangeard (fig. 13), Fraser and Brooks).

In Ascobolus glaber the archicarp is larger and more twisted than in
A. furfur aceus, and consists of some
twenty or thirty cells from one or more
of which the ascogenous hyphae develop
(Dangeard).

In Ascobolus Winteri, a form occur-
ring on goose dung, and apparently
limited to this habitat, the archicarp
(fig. 77), as described by Dodge, con-
sists of three parts, a stalk of two or
three cells, a series of larger, central
cells, which give rise to the ascogenous
hyphae, and a terminal row of three

Fig. 77. Ascobolus Winteri Rehm.; archi-
carp, x 1080 ; after Dodge.

DISCOMYCETES

[CH.

n8

or four cells, which diminish gradually in diameter and which he terms

a trichogyne.

In Ascobolus immersus the mycelium consists of multmucleate cells, the
archicarp is larger than that of A. Winteri and contains some twenty
divisions, it is otherwise very similar. The cells contain numerous large
nuclei and pores develop between them ; the ascogenous hyphae arise from
a single cell. Ramlow observed nuclear fusions in the central cell of the
archicarp, but referred them to bad fixation. His explanation may be

adequate here, but it does not
invalidate the observations of
authors who have recorded
fusions in properly fixed ma-
terial. In archicarps which he
held to be satisfactorily fixed
Ramlow saw pairing of nuclei
in the ascogenous cell, and
records that they wandered in
pairs into the ascogenous hy-
phae (fig. 78), not fusing till
the asci were about to develop.
In the divisions of the ascus
the number of chromosomes is stated by Ramlow to be sixteen through-
out, but he does not figure the essential third anaphase.

Ascobolus carbonarius occurs on burnt ground among charcoal. The
ascocarp is scurfy (furfuraceous), and greenish, 'or later brownish in colour.
Numerous conidia are formed on the mycelium, and, according to Dodge,
it is from a conidium, germinating while still attached to its stalk, that the
archicarp is produced. It consists of a multicellular stalk, a fertile portion
which contains twenty to forty cells arranged in a loose irregular spiral, and

a terminal trichogyne more or
less coiled, tapering towards
the end, and including some
ten to twenty cells. The apex
of this trichogyne is found to
wrap itself tightly round a
second conidium, attached,
like the first, to its stalk (fig.
79). This conidium is re-
garded by Dodge as the an-
theridium, but no cytological
details have as yet been published.

Ascophanus carneus is a somewhat variable species. Its red, pink, or

Fig. 78. Ascobolus immersus Pers. ; archicarps showing
paired nuclei, x 1000; after Ramlow.

Fig. 79. Ascobolus carbonarius Karst. ; archicarp, x 280 ;
after Dodge.

IV]

PEZIZALES

119

orange apothecia occur on the dung of cows and rabbits, on old leather,
rope and similar habitats. Chlamydospores are sometimes produced.

As in Ascobolus, the archicarp is a coiled, multicellular filament; it varies
considerably both in the size and number of its cells and in the amount of
twisting which it undergoes.

The central oogonial region includes three to seven large cells with
granular contents. Between this and the parent hypha is a stalk of variable
length and beyond it is a terminal portion (or trichogyne) of not more than
seven cells which are narrower than the rest and appear to degenerate early
(Cutting).

The cells come into communication with one another by large pores (fig.
Si a), and Cutting has shown that
nuclear fusions (fig. 81 b} take place
in all the cells of the oogonial
region, and that all of them give
rise to ascogenous hyphae.

Ramlow also saw nuclear fusions
in these cells, but heexplained them,
as in Ascobohis immersus, as due to
bad fixation. He also saw and
figured exceptionally large nuclei,
which had apparently become
swollen, and were about to degene-
rate. For him the normal process
is the association of nuclei in pairs
(fig. 80) without fusion, and their
passage, still associated, into the
ascogenous hyphae; here walls are

F'ig. 80. A scophanus carneiisfers.; old archicarp,
showing associated nuclei, x 800; after Ramlow.

formed so that the hypha consists of a series of binucleate cells. These

Fie 8 1 Ascofihanus carneus Pers.; a. section through young ascocarp, showing
nuclear fusion in two cells of the archicarp, x 580 ; b. two cells of an archicarp,
showing nuclear fusions, x 1240; after Cutting.

nuclei, when satisfactorily fixed, showed a well-marked centrosome.
Ramlow was unable to see whether one or several cells of the archicarp

120

DISCOMYCETES

[CH.

gave rise to ascogenous hyphae ; an investigation sufficiently searching to
determine this point might have led to the recognition of nuclear fusions
in normal material.

The ascospore has a single large nucleus, and gives rise to multi-
nucleate germ-tubes in which Ramlow's figures show numerous nuclei in
pairs (fig. 1 6).

In Ascophanus ochraceus Dangeard describes eight to fifteen oogonia as
taking part in the formation of a single fruit. These, it would appear, are
all borne upon the same hypha ; they may arise from adjacent cells, and
indeed sometimes open into one another, so that the whole series seems
equivalent to the oogonial region of A. carneus. Each cell, however, is
described as bearing a twisted, multicellular trichogyne, which would indicate
that each is an independent organ. Large ascogenous hyphae arise from the
several " oogonia," and the view suggests itself that the so-called trichogyne
may be in fact a premature ascogenous hypha. It is, at least, difficult to
distinguish the one from the other in Dangeard's figures, and the species
certainly requires further investigation.

Saccobolus violascens is a violet or greyish violet species about I mm. in
diameter. The archicarp is a coiled structure and is divided into only three
or four cells (Dangeard), the central of which gives rise to ascogenous
hyphae, while vegetative filaments grow up from the stalk and neighbouring
mycelium (fig. 82).

Fig. 82. Saccobolus violascens Boud.;
archicarp ; after Dangeard.

F'g- 83. Thelebohis stercoreus Td
ascocarp with single ascus, x 2<
after Brefeld.

The species of Rhyparobius and Thelebolus, the two genera with many

IV]

PEZIZALES

121

multicellular archicarps, each rather like the single scolecite of Ascobolus.
The cells are not connected by pores, and ascogenous hyphae arise from
several in each archicarp.

In R. brunneus Dangeard reports a single archicarp, consisting of a short,
somewhat twisted branch. Ramlow has also recorded a single archicarp in
R. polysporus and Barker in an unnamed species. Overton has made some
study of the development of the numerous spores in R. Pelletieri. The
ascus nucleus divides as usual to form eight free nuclei, these undergo a
period of rest and growth and then divide further till thirty-two free nuclei
are formed. Around these the spores are delimited in the usual way.

Thelebolus stercoreus has a mycelium of uninucleate cells, from one of
which the archicarp arises as a thick branch containing a single nucleus.
Later two, four, and finally eight, are seen (fig. 85), and then septation takes

Fig.

^— - -_'

B4. Thelebolus stercoreus Tde. ; a. young ascocarp with binucleate asci ; b. ascus
containing fusion nucleus, both x 810 ; after Ramlow.

place, so that a row of cells is formed. Most of these are uninucleate, but
one contains two nuclei (fig. 84^); it enlarges and becomes the single ascus ;
in it the two nuclei fuse (fig. 84^). The definitive nucleus divides karyo-
kinetically, sometimes as many as ten times, so that 1042 nuclei are formed.

Fig. 85. Thelebolus stercoreus, Tde.; development of archicarp, x 1750; after Ramlow.

Spore-formation takes place apparently in the usual way. The wall of the
ripe ascus is about 2/* thick, but a thinner region is present at the apex, sc
that a concave papilla is differentiated, which is concerned in the dehiscence
of the ascus. A sheath of vegetative hyphae grows up from the surrounding

cells.

122

DISCOMYCETES [CH.

In Thelcbolns Znkalii the origin of the ascocarp has been observed from a
pair of intertwined hyphae (Ramlovv, 1914), but the cytology and further
development have not yet been described.

The closest analogy to the development of the ascocarp in Thelebolus is
perhaps to be found in SphaerotJieca among the Erysiphales. I n both we have
a hypha which is at first uninucleate, later multinucleate. In both it divides
to form a row of cells most of which enclose one nucleus. In both a single
binucleate cell, typically penultimate, gives rise to the single ascus in which
nuclear fusion takes place. But in SpliaerotJieca the original uninucleate
structure is the fertilized oogonium, while in Thelebolus stercoreus an anthe-
ridium has not been demonstrated. It remains to be seen what light the
investigation of Tli. Zukalii will throw on these homologies. In view of
the direct transformation of one cell of the row into an ascus, it becomes
unjustifiable to correlate the septate structure here with the young archicarp
of the Ascoboli or AscopJiani.

ASCOBOLACEAE: BIBLIOGRAPHY

1896 HARPER, R. A. Ueber das Verhalten der Kerne bei der Fruchtentwickelung einiger

Ascomyceten. Jahr. fiir wiss. Bot. xxix, p. 655
1903, 4 BARKER, P. T. B. The Development of the Ascocarp in Rhyparobius. Kept.

Brit. Assoc. Southport and Cambridge.
1906 OVERTOX, J. B. The Morphology of the Ascocarp and Spore-formation in the many

spored Ascus of Thecotheus Pelletieri. Bot. Gaz. Ixii, p. 450.

1906 RAM LOW, G. Zur Entwickelungsgeschichte von Thelebolus stercoreus. Bot. Zeit.
Ixiv, p. 85.

1907 DANGEAKD, P. Recherches sur le developpement du perithece chez les Ascomy-
cetes. Le Botaniste, x, p. 304.

1907 WELSKORD, E. J. Fertilization in A scobolus frtrfuraceus. New Phyt. vi, p. 156.
1909 CUTTING, E. M. On the Sexuality and Development of the Ascocarp in Ascophanus

carneus. Ann. Bot. xxiii, p. 399.
1909 FRASER, H. C. I. and BROOKS, W. E. St J. Furthur Studies on the Cytology of

the Ascus. Ann Bot. xxiii, p. 537.
1912 DODGE, B. O. Methods of Culture and the Morphology of the Archicarp in certain

Species of the Ascobolaceae. Bull. Torrey Bot. Club, xxx, p. 139.
1914 RAM LOW, G. Beitrage zur Entwickelungsgeschichte der Ascoboleen Myc Cen-

tralbl. v, p. 177.

Helotiaceae and Mollisiaceae

The Helotiaceae and Mollisiaceae are distinguished from the Pezizaceae

by the fact that their peridium differs more or less definitely in structure

from the hypothecium. In Helotiaceae the peridium is prosenchvrhatous

>mposed of elongated parallel hyphae, usually light in colour and thin-

ed. In the Molhs.aceae it is parenchymatous, of round or polygonal

cells usually thick-walled and dark-coloured. In both families the ascus

! ejection of a plug, and not, as in most Discomycetes, by a lid.

iv] PEZIZALES I23

The apothecia of the majority of forms included in these two families
are small, often stalked, sometimes attached to a sclerotium ; they are waxy
in consistency and may be glabrous or hairy. Most are saprophytes, often
occurring on dead plants, some are parasitic. In Helotiaceae they are
almost always sunk in the substratum (immersed), and in Mollisiaceae
frequently superficial.

Among the Mollisiaceae Pseudopeziza Trifolii is parasitic and causes the
leaf-spot disease of clover. The leaves become increasingly spotted and
die, so that the crop is often seriously injured. In this case the ascocarps
are sessile and distinctly erumpent, developing within the tissue of the leaf,
and breaking through the epidermis at maturity. There are several other
species of Pseudopeziza, most on dead stems and leaves, a few on the living
tissues of wild plants. The species of Tapesia occur on wood, branches,
and dead leaves. The ascocarps are stipitate and pilose or downy, they are
found in groups seated on a spreading weft of branched interwoven hyphae,
by means of which the genus is readily distinguished. T. fusca is to be
found on fallen twigs of larch and other plants.

Among the Heliotiaceae the genus Helotium includes a number of species
found on dead leaves, stems, beechmast, and similar habitats; these fungi
are light-coloured, waxy and frequently stipitate.

Another large genus, Dasyscypha, has a sessile or short-stalked ascocarp,
thin and delicate in texture, and externally pilose; the species are sapro-
phytic or parasitic. Dasyscypha Willkommii is the cause of a serious
disease, the well-known Larch Canker. The apothecia are externally yellow
with an orange disc. The ascospores give rise to germ-tubes which are
unable to penetrate the bark, but obtain entrance through wounds caused
by hail, ice or snow, or by the destruction of the needles by insects. The
Larch moth (Coleophora laxicelld), for instance, is known to cause less injury
in mountainous than in lower regions, and the fungal disease is propor-
tionately less prevalent in the mountains. The mycelium ramifies chiefly
through the soft bast, but may penetrate the wood as far as the pith. It
spreads only in the autumn and winter, never in summer when the growth
of the host is active. Where it spreads into the bark the tissues turn
brown and shrivel, causing depressed canker spots in which yellowish white
stromata are produced. These give rise to minute unicellular conidia, and
later, if the atmosphere is sufficiently moist, to ascocarps.

In the genus Sclerotinia the stalked ascocarps arise from sclerotia (fig. 86).
A number of species are parasitic : 5. tuberosa on Anemone nodosa ; 5. sclero-
tiorum on the potato, cabbage and other hosts in the stems of which the
sclerotia are formed; S.fructigena and 5. cinerea on species of Prunus and
Pyrus where they give rise to brown rot, blossom wilt and other pathological
conditions ; S. bulborum on hyacinth and other bulbs, and various species on

124

DISCOMYCETES

[CH.

rs of the Vaccinieae, where the sclerotia are formed on the fruits
i" the conidia are produced in chains and are separated by small
cellulose disjunctors. They have a characteristic smell of almonds and
are tried o the flower by insects, and probably also by wmd ; they
"rmTnate to form septate hyphae which enter and fill the ovary. The

Fig. 86. Sderotinia tuberosa (Hedw.) Fuck.; sclerotia and apothecia, nat. size.

mummified berries fall prematurely, lie during winter on the earth, and in
spring give rise to the goblet shaped apothecia. In other species the conidia
are borne on a conidiophore and belong to the form-genus Botrytis ; the
conidial phase on Primus and Pyrus is known as Monilia. The ascospores
are unicellular and hyaline and often of unequal size.

Celidiaceae, Patellariaceae, and Cenangiaceae

In the previously described families the consistency of the ascocarp is
either fleshy or waxy. In the following three, Celidiaceae, Patellariaceae,
and Cenangiaceae, it is leathery, horny, or cartilaginous, and the ends of the
paraphyses are interwoven to form a layer above the asci known as the
epithecium. The hypothecium is well developed, the ascospores are some-
times more than eight in number and are one to many-celled; in some
species pycnidia are present. The three families are sometimes grouped
together as Dermateaceae.

iv] PEZIZALES 125

Some of the Celidiaceae occur on wood or bark, but the majority are
parasitic on the thalli or apothecia of lichens, their hyphae ramify among
the living tissues of the host, and they were at first believed to be themselves
lichen species. They are, however, without a thallus, and so without an
algal constituent, and the host plant is clearly distinguished by its own
fructification developed in the absence of the parasite. The fruits of Celidium
variant, for example, form black points on the apothecia, or rarely on the
thallus of the lichen Lecanora glaucoma. In this family the peridium is
absent or but little developed.

The Patellariaceae are for the most part saprophytic, but include also
a number of lichen parasites. These are erumpent, but the saprophytic
forms are superficial, and are thus differentiated from the Cenangiaceae.
They are distinguished from the Celidiaceae by the well-marked peridium
of small, dark-coloured cells. The fruits are closed at first and either become
flattened out as they develop, or open by a narrow or a star-shaped slit.

In the Cenangiaceae the ascocarps are erumpent, sometimes developed
on a stroma. They are dark-coloured, with a tough or somewhat gelatinous
sheath, and, when mature, are cup or pitcher shaped ; pycnidia or spermo-
gonia are present in some genera.

Bulgaria polymorpha, one of the best known species, occurs on dead
trunks of trees, particularly beech. The cup is i to 4 cm. across, and is
externally umber brown. The hymenium is black and shining and level or
almost level with the top of the cup. The ascocarps burst through the bark
as small, rusty brown, scurfy knobs, which gradually expand at the apex.
The substance is soft and tough, resembling india-rubber in consistency and
appearance. The species is readily distinguished by its four, slightly curved,
brown ascospores. It is stated to be a dangerous enemy of the oak, but
details of its parasitism are not known.

The genus Coryne is placed by many systematists in the neighbour-
hood of Bulgaria. C. sarcoides is a common species on rotten trunks and
stumps. The apothecia are crowded and dull red or purple in colour.
Amongst them, or often occurring alone, are the conidial fructifications,
rather paler in colour. Minute conidia are abstricted froin the ends of the
fertile hyphae. The ascospores are septate.

Cyttariaceae

The very curious family Cyttariaceae contains only one genus, Cyttaria.
Six species are known, occurring in New Zealand, Tasmania, and South
America ; all are parasitic upon species of Notkojagns.

C. Darwinii occurs very commonly in Tierra del Fuego, where it was
collected by Darwin in 1833.

126

DISCOMYCETES

[CH.

"In the beech forests," he says, "the trees are much diseased; on the
rough excrescences grow vast numbers of yellow balls. They are of the
colour of the yolk of an egg, and vary in size from that of a bullet to that
of a small apple ; in shape they are globular, but a little produced towards
the point of attachment. They grow both on the branches and stems in
groups. When young they contain much fluid and are quite tasteless, but
in their older and altered state they form a very essential article of food for
the Fuegian. The boys collect them and they are eaten uncooked with
fish." He observed that they were smooth when young, "the external
surface marked with white spaces as of a membrane covering a cell"; later
the whole surface is "honeycombed by regular cells." These are the separate
apothecia, considerable numbers of which occur on the same stroma. Bertero,
at about the same time, recorded that the Chilian species (C. Berteroi} threw

tWig °f N°h °fagUS

™Sx- f; ° °agUS ™™<»>» with knobs beari

gus, x s, b. group of stromata; c. single stroma cut across; all after Berkeley.

with knobs bearing the

iv] HELVELLALES 127

"out of these cavities an impalpable powder when it was touched, exactly
as is observed in the Peziza vesiculosa"

In all species the stromata seem to grow from a distinct disc (fig. 87),
formed from the bark or the bark and wood of the host, and traversed in
all directions by the mycelium, which doubtless gives rise to a fresh crop
each season. The asci are rather short and cylindrical and contain eight
ovoid spores.

In C. Dai"winii Berkeley observed that the lower part of the stroma was
granulated as if beset with a small, black, parasitic Sphaeria; Fischer inter-
preted these structures as spermogonia or pycnidia, and was able to observe
them on different parts of the stroma of C. Hookeri-*x\& C. Harioti. He also
noted, below the developing apothecia of C. Darwinii, certain stout, coiled,
branching hyphae, which were at this stage almost without contents. Their
appearance suggests that they are ascogenous hyphae, but Fischer made the
alternative suggestion that they might be archicarps. In view of the presence
of putative spermatia he made some search for trichogynes reaching to the
surface of the stroma,but could find none, nor any evidence of a sexual process.

The Cyttariaceae have been compared to those members of the Cenan-
giaceae in which the apothecia arise from a common stroma, and in which
pycnidia or spermogonia are also present.

In many directions they require further investigation.

CYTTARIACEAE: BIBLIOGRAPHY

1842 BERKELEY, M. J. On an edible Fungus from Tierra del Fuego and an allied Chilian
Species. Trans. Linn. Soc. Lond. xix, p. 37.

1847 BERKELEY, M. J. Fungi. Hooker's Flora Antarctica, ii, p. 453.

1848 BERKELEY, M. J. Decades of Fungi. Lond. Journ. Bot. 2nd series, vii, p. 576.

1885 BUCHANAN, J. On Cyttaria Pnrdiei. Trans. New Zealand Inst. xviii, p. 317.

1886 FISCHER, E. Zur Kenntniss der Pilzgattung Cyttaria. Bot. Zeit. xlvi, p. 812.

HELVELLALES

The members of the Helvellales are saprophytes, growing chiefly on the
ground, sometimes on decayed wood and branches. Most are large, fleshy
and stipitate. The hymenium is spread over the upper surface, and, in the
few forms studied, is covered at first by a veil or membrane through which
the paraphyses break, much as in the Pezizas, and which may be homologized
with their peridium. There are three families :

Ascophore flattened, not stalked RHIZINACEAE.

Ascophore stalked

fertile region of head distinct from stalk, ascus opening

by a lid HELVELLACEAE.

fertile region not always distinct from stalk, ascus opening
by a plug GEOGLOSSACEAE.

DISCOMYCETES

Rhizinaceae

[CH.

The Rhizinaceae are characterized by their unstalked fructification, and
include the genera Rhizina and Sphaerosoma.

Rhizina has a flattened, crust-like ascophore, more or less concave below,
and attached to the soil by root-like strands of mycelium. The asci cover
the upper surface.

Rhisina inflata occurs in this country only as a saprophyte, growing
on soil, but in both France and Germany it has been found to attack
conifers. The disease, known as ring disease, or root fungus, extends from
a centre, infecting one plant after another and causing them to lose their
needles and die. The mycelium ramifies in the intercellular spaces of
the cortex, and within as well as between the cells of the bast, so that the
sieve-tubes are completely filled. It forms also masses of pseudoparenchyma
between the dead and diseased tissues of the host.

The development of the ascocarp has been studied in R. undulata where
Fitzpatrick found a long, multicellular archicarp recalling that of some of
the Ascobolaceae. He regards the terminal cell or cells as a trichogyne
but there is no evidence that normal fertilization ever takes place or that
male organs are ever developed. In due course, the central cells become
continuous through large pores, and give rise to ascogenous hyphae into
which the nuclei pass. Fitzpatrick observed paired nuclei in the oogonial
region and in the ascogenous hyphae, and infers that nuclear association
occurs in the archicarp, but that there is only one fusion, that in the ascus.

Sphatrosomajanczeivskianum Roup. ; apothecium showing
oogonial cell, x 70 ; after Rouppert.

iv] HELVELLALES

129

In Sphaerosoma the ascophore is more or less sunk in the substratum,
and is attached by rooting hyphae which
are sometimes grouped on a short pedicel.
It is concave when young, but later forms
an irregularly globose mass over the upper
surface of which the hymenium is spread
• (fig. 89). It resembles, in fact, a Pesiza
which becomes very much reflexed at
maturity.

In Sph. Janczewskianum (fig. 88), a large Fig. 89. Sphaerosoma fu^ts (Klotz.)
oogonial cell has been recognized from RQ"p-; apothecium, x6; after Roup-
which the ascogenous hyphae originate,

but no details of its development are known. This genus has been variously
placed in the Tuberaceae and Pezizaceae as well as in its present position.
It shows resemblances to some of the former in its habitat under fallen
leaves, and to the latter group in many points of general structure.

RHIZINACEAE : BIBLIOGRAPHY

1909 ROUPPERT, C. Revision du genre Sphaerosoma. Bull. Acad. Sci. de Cracovie, p. 75.
1918 FITZPATRICK, H. M. Sexuality in Rhizina undulata Fries. Bot. Gaz. Ixv, p. 201.

Helvellaceae

The Helvellaceae are represented by five genera, Helvetia (fig. 900),
Morchella (fig. 90 &), Verpa, Gyromitra, and Cidaris ; of these the first four
are British. In all a definite fertile head is distinguished from the sterile
stalk, and over the more or less convoluted surface of the head the hymenium
extends.

Development has been studied only in species of Helvetia where the
fruit arises as a tuft of branching, septate hyphae, and no archicarp has
been observed.

In H. elasttca, young ascophores, about o-5 mm. in diameter, show no
signs of fertile hyphae. A membrane of interwoven filaments encloses the
whole fruit body, and below this a palisade of club-shaped hyphae is differ-
entiated. As growth proceeds the membrane becomes broken, and the
palisade increases in regularity, forming the boundary of the fructification
except where, at the apex, the paraphyses are growing up. Later, as these
increase in number, the ascogenous hyphae appear among them, and
numerous asci are formed.

In H. crispa the later stages of development are very similar to those
in H. elastica. Here nuclear fusions have been observed in the young

DISCOMYCETES

[CH.

130

ascogenous hyphae, replacing, as in Humaria rutilans, the obsolete sexual

fusions, and preceding the fusions in the asci. Carruthers has studied the

Fig. 90. a. Hdvella crispa (Scop.) Fr. ; b. and c. Morchella vulgaris Pers.; after Boudier.

nuclear divisions, and finds two chromosomes in the vegetative and four in
the fertile hyphae. Four again appear in the first and second (meiotic)
divisions in the ascus, after the second fusion has taken place, and two are
recorded in the telophase of the third division, and in the mitosis in the
spore. The ripe spore normally contains eight nuclei.

In both species, after an ascus has arisen from the penultimate cell of
a hypha, the terminal cell may grow on, giving rise to others, and may fuse
before doing so with the third cell of the hypha, which is the stalk-cell of
the previously formed ascus.

In Morchella esculenta the nuclear divisions of the ascus have been
studied by Maire. After observing eight chromatin bodies in the prophase
of the first division in the ascus, he found four in the prophase and anaphase
of the third, and in the divisions of the spore nuclei ; this corresponds closely
with Carruthers' results in Helvetia crispa.

HELVELLACEAE : BIBLIOGRAPHY
1905 MAIRE, R. Recherches cytologiques sur quelques Ascomycetes. Ann. Myc.iii,p. 123.

1910 McCUBBlN, W. A. Development of the Helvellinaceae. I. Helvetia elastica. Bot.
Gaz. xlix, p. 195.

191 1 CARRUTHERS, D. Contributions to the Cytology of Helvella crispa. Ann. Bot. xxv,
p. 243.

IV]

HELVELLALES

Geoglossaceae

The Geoglossaceae grow usually in damp or moist situations such as
low, wet woods and shady slopes. They occur on soil or on dead branches
or leaves, and two species of Mitrula are parasitic on living moss. The
family includes some eight genera of which five are British.

Fig. 91. a. Geoglossnm hirsnluin Pers., nat. size; b. Spathularia clavata Sacc.,
nat. size; c. Leotia lubrica Pers., form stipitata, xf ; after Massee.

The ascophore is erect and stipitate with the fertile portion terminal,
and either club-shaped (fig. 91 a, b\ laterally compressed, or forming a cup
or a pileus (fig. 91 c.}. In some of the simpler forms, as in Geoglossum
hirsutum, there is no clear line
of demarcation between the fertile
and sterile regions. The ascus con-
tains eight spores and opens by the
ejection of a plug.

The young ascocarp consists of a
dense tangle of vegetative filaments ;
in the early stages a more or less
conspicuous veil has been identified
in several genera (though not as yet
in Geoglossum}. It is composed, as
in the Helvellaceae, of interwoven
hyphae, derived from and continuous
with the outer layer of the fruit body.
There are indications that it opens
at first by a pore at the apex, but it

soon breaks up into scales and dis-

Fig.
appears. st

i. Geoglossum hirsutum Pers., x 230; b.

02.
Spathularia davata Sacc., x 400; after Massee.

9—2

I32 DISCOMYCETES [CH.

In Z<Y>/W lubrica a large branching cell, presumably an oogonium,
occurs at the base of the very young ascocarp and appears to give rise to
the ascogenous hyphae.

As far as the characters of the mature fruit are concerned, two lines of
development can be traced, both starting from Geoglossum and passing, the
one through Spathularia to Vibrissea, the other through Mitrula and Leotia
to the Helvellaceae.

In the species of Spathularia and Vibrissea, as in Geoglossum, the spores
are very long, narrow and septate, lying side by side in the ascus. Geo-
glossum is distinguished by its coloured spores (fig. 92 a), the other two genera,
in both of which the spores are hyaline (fig. 92 £), by the form of the
fructification.

In the rest of the Geoglossaceae, as in the Helvellaceae, the spores are
elliptical and hyaline, and are arranged one above the other in the ascus.
They may be continuous or septate. In Mitrula the fertile region is
irregularly club-shaped, and in Leotia pileate.

A relationship to the Pezizales suggests itself at various points, and
perhaps especially through Leotia, to the Helotiaceae and Mollisiaceae where,
as in the Geoglossaceae, the ascus opens by a slit or pore from which a plug
of wall substance is ejected, not as in the majority of the Helvellales and
Pezizales by a definite lid.

GEOGLOSSACEAE : BIBLIOGRAPHY

1897 MASSEK, C. A Monograph of the Geoglossaceae. Ann. Eot. xi, p. 225.

1908 DURAND, E. J. The Geoglossaceae of North America. Ann. Myc. vi, p. 387.

1910 BROWN, W. H. The Development of the Ascocarp of Leotia. Bot. Gaz. 1, p. 443.

PHACIDIALES

In the Phacidiales the ascocarp is immersed in the matrix. It is usually
small in size and leathery, waxy, or coriaceous in consistency; an epithecium
is often developed. Certain members of the group resemble the Hysteriales
in many points and differ from them chiefly in the greater exposure of the
fertile disc at maturity.

There are two chief families.

Stictaceae

The Stictaceae constitute a considerable group of small forms, occurring
saprophytically on wood or other plant remains. Their development and
minute anatomy, apart from systematic characters, is practically uninvesti-
gated. They have a fleshy or waxy disc, pale and clear coloured, usually
white, yellow, or tinged with pink. The sheath is not always developed, when
present it is thin and white and is mealy owing to the presence of particles

IVJ PHACIDIALES I33

of calcium oxalate; when the fruit opens it forms a white border around the
hymemum. The pale colour, and the ragged or toothed dehiscence of the
sheath are very characteristic.

Phacidiaceae

The Phacidiaceae are distinguished by their black, thick-walled apothecia,
usually scattered, sometimes, as in Rhytisma, grouped on a black stroma.
Where the fertile disc is circular the sheath splits in a stellate manner, but
where it is elongated, dehiscence takes place by means of a slit running
along its entire length. The species occur chiefly on dead herbaceous stems
or leaves, but a few are parasitic.

Rhytisma Acerinum (fig. 93) infects the leaves of various species of Acer
(maple and sycamore). The mycelium ramifies in the living tissues of the

Fig. 93. Rhytisma Acerinum (Pers.) Fr.; apothecium, x 160.

host and causes yellow spots on the leaves about three weeks after infection.
Some five weeks later pycnidia develop under the cuticle and produce small
unicellular conidia. The epidermis and underlying tissues of the host become
filled with hyphae and a dense, black sclerotium is completed. In this state
the leaf falls and next spring the sclerotia thicken and become wrinkled;
finally they burst by elongated fissures and expose the discs of the apothecia.
The ascospores are filiform and septate; they are ejected with some force
and reach the living leaves to which they are probably carried by the wind.

HYSTERIALES

The Hysteriales are characterized by the black, elongated ascocarp,
dehiscing by a longitudinal slit, so narrow that the disc.is almost permanently
concealed.

The species are all minute; in some the disc is narrowly elliptical, in

,34 DISCOMYCETES [CH.

some it branches in a stellate manner, in others the ascocarp is raised and
laterally compressed so as to resemble a miniature mussel or oyster shell
standing on its hinge and with the opening uppermost. In this case, or
when the ascocarp is superficial, it is rigid and carbonaceous in consistency,
when developed beneath the epidermis of the host it is membranous.

The ascospores are coloured or hyaline and are frequently septate ; they
may be very long and narrow and may be surrounded by a gelatinous
membrane.

In a few cases pycnidia are known, producing oblong, unicellular, hyaline

conidia.

The majority of species are saprophytic on old wood, bark, or dry leaves.
The mycelium is intercellular, and is sometimes parasitic on living plants
though the apothecia reach maturity only on parts that have been killed.

The details of cytology and development are not known, nor do these
minute species, growing often on a hard substratum, seem very promising
objects of study.

The subdivisions of the Hysteriales, of which Hysteriaceae and Hypo-
dermataceae are the chief, depend upon the consistency of the sheath, on
the form of the ascocarp, and on whether it is superficial or immersed.

Lophodermium Pinastri (Hypodermataceae) produces pine-blight or
needle-cast in the seedling of Finns sylvestris and other conifers, causing
them to drop their leaves. The mycelium ramifies in the leaf and gives rise
first to pycnidia and later, usually after the leaf has fallen, to ascocarps.
These are black and oblong, opening by a narrow slit. The spores are filiform
and continuous. The disease does very considerable damage to young plants,
often causing death. It attacks mature trees also and, though these are not
themselves seriously injured, they act as centres of infection, particularly in
the neighbourhood of seedbeds and nurseries.

In the form of their fructification the Hysteriales are intermediate between
the Discomycetes on the one hand, and the Pyrenomycetes on the other,
and have been variously included under either of these headings. Their
black, coriaceous ascocarps, opening by a narrow slit, differ from those of
certain Phacidiales chiefly in the less exposure of the disc.

They approach the Sphaeriales in the frequent occurrence of coloured,
septate spores, as well as in the consistency and often in the form of the
ascocarp, which is distinguished from a true perithecium chiefly by its
elongated opening, and by the absence of periphyses1. Possibly a study of
their minute anatomy may lead to more definite knowledge of their
relationships.

1 For definition, see p. 140.

IV]

TUBERALES

TUBERALES

135

The Tuberales are typically subterranean though some species are only
imperfectly buried, or grow among decaying leaves. When mature the
fruits emit a powerful odour by which rodents are apprised of their where-
abouts. The ascocarp is eaten and the spores dispersed after passing through
the alimentary canal of the animal.

The ascocarp is more or less globose, sometimes completely closed,
sometimes with a small opening. The hymenium may form a smooth lining
to the fruit or may be thrown into elaborate folds so that the fertile region
is divided into chambers. The asci contain one to eight spores, but, as far
as is known, eight nuclei are always produced. The epispore is often
elaborately ornamented at maturity.

Early investigators classed the Tuberaceae with the hypogeal Gastero-
mycetes, and a consequence of this survives in the use of the term gleba to
describe the contents of the ascocarp, including both vegetative hyphae and
hymenium.

The Tuberales include a single family, the Tuberaceae; their relationship
is probably to the Pezizaceae and Rhizinaceae. One or more series can be
traced between these families and the truffles, the principal modifications
being in the direction of adaptation to subterranean conditions by increased
protection of the hymenium. This appears to have been achieved either by
retaining the closed form of the young pezizaceous apothecium (Genea ,
PacJiyphloeus) or by invagination of the fertile layer (Tuber) over a widely
exposed surface such as is found in Rhizina or Sphaerosoma. In either
case room has been made for
additional asci by throwing the
hymenium into elaborate folds.
Massee, however, regards the
globose asci and dark-coloured
sculptured spores of Tuber as
primitive, and derives from it
Genea, and thence the Pezi-
zales.

Tuberaceae

In Hydnocystis and Genea
the ascocarp is fleshy or warted;
it has a single aperture often
more or less closed by project-
ing hyphae. Internally the
hymenium may form a smooth Fig. 94-. a. Genea KlotzschU* and Br.; ascus and para-
J J physis ; b. Genea htspidula Vitt. ; apothecium ; c.

lining, or, in Genea, is more Genea sphaerica Vitt.; apothecium; after Massee.

136

DISCOMYCETES

[CH.

often divided into chambers, all of which communicate with the apical
opening. The asci are cylindrical and contain eight uniseriate spores (fig.
94 a}. The simplest species in fact resemble a nearly closed Peziza (fig.

94 ^, 4

In Stephensia and PacJiypJiloeus the hymenium is more elaborately con-
voluted ; the asci in Pachyphloeus are stouter, and the spores irregularly
biseriate.

In Balsamia (figs. 95, 96) the asci are broadly oblong or subglobose; the
mature ascocarp is completely closed and surrounded by a pseudoparen-
chymatous sheath. The youngest ascocarps of B. platyspora which

Fig. 95. Balsamia vulgaris Vitt.; after Tulasne.

Fig 96. Balsamia vulgans MM.; section
through hymenium ; after Tulasne.

v*

Fig. 97. Tuber rufum Pico ; general view
of fertile region ; after Tulasne.

IV]

TUBERALES

137

Bucholtz was able to examine, showed a system of internal chambers lined
by the hymenium and communi-
cating at one or more points with
the exterior. As development pro-
ceeds these cavities increase in size
and the hymenium becomes further
convoluted, so that additional cham-
bers are formed.

In Tuber the ascocarp is ir-
regularly globose, fleshy or some-
times almost woody; internally the
walls which divide the gleba are
extensively branched, and the free
space between them is diminished,
so that the layers of the hymenium
are brought close together and
constitute the fertile "veins." Other
"veins," white and sterile, run be-
tween the hymenial layers and serve
as air chambers (fig. 97). The asci
are often globose, and the spores
usually four in number, but the
number varies, and is sometimes
reduced to two or one (fig. 98).

The development of the fruit
has been studied by Bucholtz in Tuber puberulum (fig. 99). The very
young ascocarp consists of a mass of hyphae, the outer rather more loosely
interwoven than the inner.. Around the lower part a dense basal sheath is
differentiated. Soon the first signs of the fertile veins appear as invagina-
tions of the upper surface, and internally the loose tissue of the sterile veins
becomes recognizable.

Owing to the rapid growth of the upper portion of the young fruit, the
basal sheath is bent backwards, while at various points along the fertile veins
the first signs of asci appear. Later the peripheral tissues become thickened,
together with the remains of the basal sheath, and form the peridium. This
ultimately closes over the points where the fertile veins are in communication
with the exterior. Thus the young 'fruit is open at first, the hymenium
becomes internal by invagination and the peridium which covers the mature
ascocarp is a secondary formation.

The development of the fructification in Choiromyces macaudriformis
approaches that of T. puberulum, but the basal sheath and peridium are
less conspicuous.

Tuber rufutn Pico; section through
hymenium ; after Tulasne.

,38 DISCOMYCETES [CH. iv

The ascocarps of many species of Tuber are edible, the most esteemed
being T. melanosporum which does not occur in Britain. They grow chiefly

Fig. 99. Tuber pubertilum (B. and Br.) Ed. Fisch. ; a. — e. development of ascocarp ; a. x 52;
b. and c. x 28 ; d. and e.xii;/. section through mature ascocarp, x 6 ; all after Bucholtz.

in soils consisting of sand mixed with clay and containing, iron, or in mixed
alluvium; the soil must be porous to secure sufficient aeration.

Truffles occur in chestnut, oak, and especially beech woods and there is
evidence that they form mycorhiza with the roots of these trees. The relation
would appear to be of advantage to the fungus since the success of the culti-
vation of edible truffles under oaks in France depends on keeping the roots
near the surface.

TUBERACEAE : BIBLIOGRAPHY

1903 BUCHOLTZ, F. Zur Morphologie und Systematik der Fungi hypogaei. Ann. Myc. i,
p. 152.

1905 FAULL, J. H. Development of Ascus and Spore Formation in Ascomycetes. Proc.
Boston Soc. Nat. Hist, xxxii, p. 77.

1906 BOULANGER, E. Notes sur la Truffe. Soc. Myc. xx-xxii, pp. 77 etc.

1908 BUCHOLTZ, F. Zur Entwickelung der Choiromyces Fruchtkorper. Ann. Myc. vi,
P- 539-

1909 MASSKE, G. The Structure and Affinities of British Tuberaceae. Ann. Bot. xxiii,
P- 243-

1910 BUCHOLTZ, F. Zur EntvvickelungsgeschichtedesBalsamiaceen-Fruchtkorpersnebst
Bemerkungen zur Verwandtschaft der Tuberineen. Ann. Myc. viii, p. 121.

CHAPTER V

PYRENOMYCETES

THE Pyrenomycetes include some 10,000 species; they are characterized by
the fact that their ascocarp or perithecium is a more or less flask-shaped
organ opening by a narrow pore, the ostiole, and containing a hymenium
spread in a regular manner
over the floor and lower part
of the sides (fig. 100). It thus
differs from the perithecium of
the higher Plectascales where
the asci are irregularly scat-
tered, and from that of the
Erysiphales where, except in
the flattened perithecium of
the Microthyriaceae, an ostiole
is not developed. By some au-
thors the term Pyrenomycetes
is used to include all these
groups and even certain other
forms, such as the Tuberales.
A study of the development of
the truffles, however, has made
clear their affinity with the
Pezizales ; the mildews consti-
tute a well defined and isolated
group, distinguished, so far as
they are known, by the form
of their sexual organs ; and
the higher Plectascales differ
from the present series and re-
semble the simpler forms with which they have here been classified in the
important character of the arrangement of their asci.

There remain four groups, the Hypocreales, the Dothideales, the
Sphaeriales, and the Laboulbeniales.

The last are true Pyrenomycetes in the sense that they possess regularly
arranged asci and a perithecium opening by an ostiole, but they are dis-
tinguished by so many special characters that, though included under this
heading, they can best be dealt with apart.

Fig. loo. Sordaria sp.; ascocarp in longitudinal section
showing asci, paraphyses and periphyses, x 400.

140

PYRENOMYCETES [CH.

The Hypocreales, Dothideales and Sphaeriales, have in common more
or less pyriform or flask-shaped perithecia ; these are sometimes isolated and
free, sometimes sunk in the tissue of the host, and sometimes embedded in
a stroma or cushion of fungal tissue. The perithecium is lined by delicate
filaments, some of which, the periphyses, grow along and partially close
the neck, and may protrude through the ostiole, while others (paraphyses)
are mingled with the asci in the venter of the fruit. The neck of the peri-
thecium varies very much in length, and is often markedly phototropic, the
ostiole being directed towards the light, and thus incidentally towards a clear
space so that, when the spores are shed, as wide a distribution as possible
is ensured. So definite is this reaction in, for example, species of Sordaria,
that if the direction of light be changed every four or five days during
development, a series of corresponding bends in the neck are produced. In
Sordaria and its allies the asci elongate, reaching up to the ostiole and in
turn discharging their spores; in species of Spumatoria and Ckaetomium the
asci deliquesce to form a mucilaginous mass which readily absorbs water
and expands, being squeezed up the neck and exuded at the ostiole where
it persists until dissolved by rain or dew.

Accessory fructifications include chlamydospores and various types of
conidia which may be borne separately on free conidiophores, or grouped
together in pycnidia. In some cases there is evidence that the so-called
pycnidia are spermogonia, and the spores they produce spermatia, but no
case has been brought to light in which these still fulfil their function as
fertilizing agents.

A consideration of our rather scanty knowledge of the initiation of the
perithecium in this group brings to light three main types of development,
(i) In Chaetomium, in Sordaria (fig. 101) and its allies and in species of
Hypomyces and Melanospora there is a coiled archicarp of four or five cells;
these are uninucleate in Hypomyces lateritus,
Chaetomium spirale and Podospora hirsuta,
multinucleate in Sordaria and Hypocopra and
in other species of Chaetomium.

In Sordaria macrospora the archicarp is
straight instead of coiled and in 5. fimiseda
a swollen terminal cell has been reported.
A pair of initial hyphae has been described
in Rosellina quercina, but in no case has a
sufficiently detailed study been made either
to reveal nuclear fusions in the archicarp or
to justify the inference that they do not occur.
F"der these circumstances it is possible to
judge of the function of these initial filaments

v]

PYRENOMYCETES

141

only on the somewhat incomplete evidence that they give rise to ascogenous
hyphae and on the basis of their resemblance to the sexual branches of other
Ascomycetes. There is a very similar coiled hypha in certain species of
Eurotium which is certainly a functional archicarp. Comparison may also
be made with the female branch of Ascodesmis nigricans and with that of
the Erysiphaceae.

(ii) The second type of pyrenomycetous initial organ (fig. 102) may

Fig. 102. Polystigma rubrumJ^C'', mature
archicarp, x 800 ; after Blackmail and
Welsforcl.

Fig. 103. Xylaria polymorfha (Pers.) Grev.;
archicarp embedded in stroma, x 1000.

readily be derived from the first. It occurs in forms where the perithecium is
immersed either in the substratum or in a stroma, and its essential character
is the prolongation of the tip of the archicarp to form a trichogyne-like
organ. The appearance of this structure is associated with the development
of spermatia in spermogonia. Archicarps of the type in question are found
in Polystigma among the Hypocreales and in Gnomonia, Poronia and
Mycosphaerella among the Sphaeriales. In all these genera, however, the
trichogyne appears to be merely vestigial ; in Polystigma it never reaches
the exterior of the host-leaf, in Gnomonia its connection with the coiled
oogonial region is doubtful and in Mycosphaerella and Poronia it degenerates
early. In Polystigma the ascogenous hyphae arise from vegetative cells and
not from the archicarp and it is at least possible that the same is the case
in the other genera named. A comparison is obvious between the archicarps
of these forms and those of several Lichens and of such Discomycetes as

PYRENOMYCETES

[CH.

142

Lachnea cretea and the Ascoboli, where the coiled and septate archicarp is

often still functional.

A very common initial organ in forms with embedded perithecia is the
short filament of cells sometimes known as Woronin's hypha (fig. 103). The
cells are large and contain well-marked nuclei and lie in a nest of small-
celled vegetative mycelium. Woronin's hypha has been found among the
Hypocreales mNectria and among the Sphaeriales in Xylaria zn&Hypoxylon ;

it remains to be shown whether
it still functions. It may have
originated from the simple archi-
carps of the Lower Pyrenomy-
cetes or by reduction from forms
with a multicellular trichogyne.
With its final disappearance we
reach such completely apogamous
species as those of Cordyceps and
Claviceps.

(iii) A quite distinct type of
primordium has been described
in Strickeria, Sporormia and Pleo-
spora; in these cases the asco-
genous and vegetative filaments
arise from a common initial cell
which divides not only transverse-
ly, but longitudinally, forming a
compact tissue (fig. 104). Other hyphae may anastomose with this mass,
or it may give rise alone to the whole fructification. Possibly some sugges-
tion of its origin may be found in the peculiar, but apparently normally
fertilized oogonium of Leptosphaeria.

The Pyrenomycetes do not appear to have given rise to any higher
forms, and have themselves a greater vegetative development than any other
Ascomycetes.

They may be subdivided as follows :

Wall of perithecium differentiated from stroma;

perithecium wall and stroma, if present, soft in
texture, either colourless or light coloured

Fig. 104. Strickeria sp.; initial cells of ascocarps ;
after Nichols.

perithecium wall and stroma, if present, firm, leathery

or brittle, dark in colour
Perithecium always sunk in a stroma from the tissue of

which its wall is not differentiated ; colour of stroma

black or dark brown
Minute, external parasites on insects, perithecium borne

on a receptacle which also bears appendages; spores

two-celled

HYPOCREALES.

SPHAERIALES.

DOTHIDEALES.

LABOULBENIALES

v] HYPOCREALES 143

HYPOCREALES

The Hypocreales are readily distinguished by the clear colour and more
or less fleshy consistency of the perithecium or stroma. In the majority of
Pyrenomycetes the colour is black or dark brown, but here bright red,
yellow, blue, and various paler shades are found, and it is only quite
occasionally that so dark a tint as brown or dirty violet appears.

The asci contain usually eight, sometimes four, and sometimes many
spores. The spores are in most cases hyaline, but are dark-coloured in
Melanospora and its allies ; they are elliptical or filiform, and may be one
or more celled.

In a number of species conidia as well as ascospores are produced.

The group includes both saprophytic and parasitic forms.

There are some sixty genera of Hypocreales, and the group is subdivided
primarily according to the development of the stroma. In the simplest forms
the stroma is absent, and the separate perithecia may or may not be partly
sunk in the substratum, in others a filamentous or a fleshy stroma appears,
and the perithecia are more or less embedded. In the highest members the
perithecia originate deep in the stroma, and remain immersed in it throughout
their development.

Upon these characters the subdivision of the group is based :

Stroma absent, or, when present, with perithecia entirely

superficial NECTRIACEAE.

Stroma forming a conspicuous matrix in which the peri-
thecia are partially or entirely immersed HYPOCREACEAE.

Nectriaceae

The species of the genus Hypomyces are for the most part parasitic upon
the pilei of various Hymenomycetes. H. aurantius occurs on old Polypori
and on species of Stereum.

Here the free perithecia are roughly oval in form, orange yellow in
colour, and seated on a delicate filamentous stroma. The perithecium wall
consists of an outer coat of narrow, closely woven hyphae, and an inner
layer of larger, thinner-walled cells with scanty contents. The cavity becomes
filled with paraphyses and developing asci, and is prolonged into the neck
lined with short periphyses. The spores are two-celled and the wall at each
end is usually prolonged into a point.

Development has been studied by Moreau in Hypomyces lateritus, a form
parasitic on species of Lacterius, and placed by Maire in the genus Peckiella
by reason of its unicellular spores. The cells of the vegetative mycelium are
uninucleate, and the archicarp appears among them as a coil of uninucleate

I44 PYRENOMYCETES [CH.

cells; there is no sign of an antheridium. Nuclear division without wall-
formation takes place in the archicarp so that each cell contains two or
occasionally three nuclei. At a later stage, after abundant branching, the
young perithecium contains a number of binucleate cells; from these the
asci arise, the hypha bending over and cutting off a binucleate subterminal
cell in the usual way. No fusion but that in the ascus was observed by
Moreau. The chief interest of this life history lies in the origin of the bi-
nucleate condition, as in some Basidiomycetes, by nuclear division.

In Melanospora the stroma may be absent, but when present is charac-
teristically fleshy; the perithecium neck is elongated; the species occur on
the fructifications of the Fyrenomycetes, on those of Pezizaceae and
Tuberaceae, on various plant remains and in one or two cases on living
plants; thus M. damnosa may be a serious disease on wheat and rye.

The development of M. parasitica was studied by Kihlman; this species
is a parasite on certain fungi parasitic on insects, including Cordyceps militaris,
which is itself a member of the Hypocreaceae.

The first sign of the development of perithecia is the yellow coloration
of the mycelium, which has hitherto been white.

The archicarp is a stout, twisted, multicellular hypha forming two or
more coils and ending in a somewhat pointed cell; its growth is renewed
after the development of the sheath has begun and it divides into some
fifteen cells; one of these, which may be termed the ascogenous cell, divides
in three directions, forming a true tissue from which the asci arise.

Melanospora Zobelii^ is parasitic on various fungi and especially on the
disc of certain Pezizaceae; Nichols found that the spores germinate to give
rise to a mycelium in the cells of which the nuclei are arranged more or less
in pairs2. The archicarp is a coiled or curved branch which becomes septate;
near it a more slender antheridial hypha may develop, and, in some cases,
may fuse with the female organ.

Vegetative hyphae give rise to a sheath of the usual type with an outer
layer, two or three cells thick, of thick-walled, isodiametric cells, and an inner
layer of laterally compressed tubular cells; within this is a loose spongy
parenchyma of cells rich in contents from which the asci arise. A connection
between the archicarp and the asci has not been traced, but it seems probable
that the whole central tissue of the perithecium may be derived from the
divisions or branches of the archicarp perhaps, as in M '. parasitica, by means
of an ascogenous cell.

A further study of the development of the perithecium and especially of
the origin of the asci in this genus is much needed. The facts, -especially in
M. parasitica, suggest that the divisions of the archicarp after the develop-

1 Melanospora Zobelii (Corda) Fuckel = Ceratostoma brevirostre Fuckel.

2 Presumably owing to rapid division ; cf. p. 47, ante.

v] HYPOCREALES 145

ment of the sheath has begun, may correspond to the septation of the
fertilized oogonium in other forms. Further, the origin of the asci from a
single cell points to the Erysiphales and Laboulbeniales, and in view of the
longitudinal divisions, perhaps especially to the latter.

In Nectria the usually red or yellow perithecia are produced in groups on
stromata of the same colour; the asci contain eight ascospores which are two-
celled, and often produce conidia by budding while still in the ascus. The
genus is large, including some 250 species among which N. cinnabarina, the
commonest in this country, is of very frequent occurrence on the living and
dead branches of deciduous trees. The mycelium from the germinating
spores is unable to penetrate the bark of the host, and infection takes place
only through open wounds. Once established, however, the mycelium spreads
rapidly especially in the xylem. The cambium and other tissues are not
attacked but die as a result of the destruction of the wood, so that as develop-
ment proceeds branch after branch is killed. Meanwhile the stromata appear
(fig. 105); in the conidial stage they are bright pink and occur at all seasons

Fie 10 =,. Nectria cinnabarina (Tde.) Fr. on a fallen twig; a. conidial stroma; b. young
perithecia; x6; E. J. Welsford del.

on the dead and living branches; perithecia are produced only in the autumn
and winter and only after the tissues have been killed ; they are deep red
in colour and are partly immersed in the deep red stromata. When a peri-
thecium is about to be formed a coil of hyphae larger than the ordinary
filaments of the stroma appears a little below the surface, and probably
represents the remains of whatever sexual apparatus originally gave rise to
the ascogenous hyphae.

Nectria cinnabarina is thus one of the rather numerous fungi which pro-
duce conidia during their parasitic phase, and ascospores only when the
death of the host has rendered them saprophytic. In view of the life-history
of this species it is obvious that there are two methods of checking the damage
which it does; the burning of infected branches on which the development
of the spores takes place, and the painting over of open wounds through
which alone the entrance of the mycelium is effected.

I46

PYRENOMYCETES [CH.

NECTRIACEAE : BIBLIOGRAPHY

1882 MAYR, H. Ueber den Parasitismus von Nectria cinnabarina. Untersuchungen aus

der forstbot. Institut zu Miinchen, iii, p. i.
1885 KIHLMAN, O. Zur Entwickelungsoeschichte der Ascomyceten Melanospora para-

sitica. Acta Soc. Sci. Fennicae, xiv, p. 313.
1896 NICHOLS, M. A. The Morphology and Development of certain Pyrenomycetous

Fungi. Hot. Gaz. xxii, p. 301.

1909 MASSEE, G. On a New Genus of Ascomycetes (Gibsonia). Ann. Bert, xxni, p. 335.
1909 SHAVER, F. J. Notes on North American Hypocreales. Mycologia, i, p. 41.
1914 MOKEAU, F. Sur le developpement du perithece chez une Hypocreale le Peckiella

laterita, (Fries) Maire, R. Bull. Soc. Bot. de France, Ixi, p. 160.

Hypocreaceae

Polystigina is a small genus, the best-known member of which, P. rubrum,
develops on the leaves oiPrunns spinosa, of P. insititia and of the cultivated
plum, where it produces conspicuous orange, yellow or scarlet stromata.
Each of these is the result of a separate infection, and spreads over only a
small part of the leaf, so that in autumn, when the leaves are shed, the host
is freed from the disease. The fungus, however, hibernates in the fallen leaves,
and next spring the ascospores mature, reach the young leaves and there
germinate.

Its development was first studied by Fisch in 1882, and by Frank in
1883, and these authors described trichogynes and the union of the latter
with spermatia. More recent investigations, however, have shown that these
organs, though present, are now no longer functional.

The germinating ascospore gives rise to a mycelium which ramifies
among the cells of the host and forces them apart; the hyphae become
massed especially in the intercellular spaces below the stomata, and often
push their way to the exterior between the guard cells. Finally the stroma
may extend from the upper to the lower epidermis, and only a few isolated
cells of the mesophyll remain in the infected region. The hyphae are multi-
nucleate, they contain orange pigment and their originally thin walls are
modified to form thick gelatinous membranes perforated by fine pits. The
gelatinous walls are probably utilized as reserve material, for they are partly
absorbed during the later stages of development after the fall of the leaf.

During the summer, large flask-shaped spermogonia appear and open
on the underside of the leaf, usually in the position of a stoma. The wall of
the spermogonium consists of densely interwoven filaments and it is lined
by thin, uninucleate spermatial hyphae (fig. 106). The mature spermatium
is a filiform curved structure, narrowed at its free end; it contains a single,
much elongated nucleus, staining homogeneously, and occupying the lower
half or two-thirds of the cell. All attempts to bring about the germination

y] HYPOCREALES H7

of these spermatia have failed, and no relation of any kind has been de-
monstrated between them and the female organ, consequently they must be
regarded as no longer functional, and their original use can be inferred only
from their structure. Their small size, scanty contents, and large nucleus
suggest that they are more appropriately constituted to act as fertilizing
agents than as a means of vegetative propagation.

The archicarp first appears as a multinucleate hypha, which becomes
septate and somewhat elaborately coiled. The base can usually be traced
to a vegetative filament; the apex ends freely in the mass of uninucleate
mycehal cells (fig. 102); most of the cells of the archicarp contain several
nuclei, but a few are uninucleate. The archicarps usually develop singly,
generally below or near a stoma, through which vegetative filaments project
(fig. 107). These projecting hyphae were regarded by Fisch and Frank as

Fig. 107. Poly stigma rubrum DC.; vege-
Fig. 1 06. PoIj>sttg-warul>ruMDC.;sper- tative hyphae projecting through stoma

mogonium, x 250; after Blackman and above archicarp, xo,oo; after Black man

Welsford. and Welsford.

trichogynes, but Blackman and Welsford, and later Nienburg, failed to
trace any connection between them and the coiled archicarps. On the
contrary, the latter end blindly within the stroma with or without branching,
and it is only quite occasionally that they can even be traced upwards
towards the stomata.

Nienburg observed the formation of a pore between a multinucleate
cell at the base of the archicarp and the large uninucleate cell next in
order to it. At a later stage he found that the uninucleate cell had become
binucleate, the nuclei being at first somewhat different in structure, and
that certain large cells, which apparently developed from it, also contained

I48

PYRENOMYCETES

[CH.

two nuclei each. In his opinion, the second nucleus in the originally uni-
nucleate cell, is derived from its multinucleate neighbour, which he terms
the antheridium ; the other binucleate cells receive their nuclei from it by
conjugate division, and are the beginnings of ascogenous hyphae. Though
he was unable to see either the entrance of the second nucleus, or the
process of conjugate division, his facts are decidedly suggestive, but they
point less to normal fertilization than to the pseudapogamous association
of a vegetative and a female nucleus.

The binucleate character of the later formed large cells may, .as he
suggests, be due to conjugate division, but, since he finds that the numerous
binucleate cells in the sheath1 are the result of rapid growth, this character
in the large cells is evidently susceptible of the same explanation. In any
case the rest of the archicarp degenerates and owing to the refractory
character of the material the ascogenous hyphae could not be further traced.

According to Blackman and Welsford, all the cells of the archicarp
degenerate without giving rise to ascogenous hyphae, and being functionless,
retain their contents so that they can be recognized during the later stages
of development as densely staining masses (fig. 108). The perithecia (fig.
109) arise in their neighbourhood, one in association with each archicarp,
and the vegetative cells produce ascogenous hyphae, which become dis-
tinguished by their large size, dense contents and well-marked nuclei. These

Fig. 1 08. Poly stigma rubrum DC.; young 'perithe-
cium; the ascogenous hyphae are not yet clearly
distinguished, many of the nuclei are in pairs, the
darkly stained remains of the archicaip are visible
near the periphery; x68o; after Blackman and
Welsford.

Fig. 109. Polystigma rubrum DC.; mature peri-
thecium, x 270; after Blackman and Welsford.

1 Nienburg, p. 390, end of first paragraph.

vl HYPOCREALES 149

authors found some evidence that a first nuclear fusion takes place in the
ascogenous hypha before the differentiation of the asci.

The ascus is formed in the usual way from the penultimate cell of the
hypha; the usual nuclear fusion and successive nuclear divisions take place
during its development.

In the genus Podocrea, the stroma is erect, and sometimes branched; in
Hypocrea it is usually hemispherical or bolster-shaped and is colourless, or
yellow or brown in colour. The majority of species occur saprophytically
on wood, or as parasites on the larger fungi. In both genera and in
their immediate allies, the spores are two or more celled. The systematic
position of Podocrea alutacea^ has undergone curious vicissitudes; in con-
sideration of its form it was at first placed among the Basidiomycetes as
Clavaria simplex, later it was regarded as a compound structure, the pyreno-
mycetous fungus being held to be parasitic, according to different authors,
on Clavaria ligula and on species of Spathularia. The stalk being thus
attributed to another fungus, the ovoid perithecial portion was referred to
the genus Hypocrea. The question was set at rest by Atkinson, who succeeded
in growing the normal upright stromata in pure culture from ascospores
alone, and thus demonstrated that only one fungus was concerned.

The species of Epichloe occur parasitically on grasses the stems of which
become coated by the stromata. The stroma is at first white, then yellow; in
the early stages of its development oval conidia are produced, later the peri-
thecia, which are completely embedded in the stroma, reach maturity; the
ascospores, like those of the remaining genera of the Hypocreaceae, are fili-
form; Dangeard has shown that they are at first elliptical and uninucleate;
later they elongate, the nucleus divides and the spore undergoes septation.

The genus Cordyceps (fig. no) includes about sixty species ; these are
mainly tropical forms parasitic on insects, the bodies of which they transform
into sclerotia from which the stromata grow out. The peculiar appearance
of these structures has given rise to curious views as to their significance
and medicinal value; thus Berkeley reports that Cordyceps sinensis is a
"celebrated drug in the Chinese pharmacopoeia, but from its rarity only used
by the Emperor's physician." The striking belief that it is "a herb in
summer and a worm in winter," may perhaps sufficiently account for the
esteem in which it was held.

The ascospores are multicellular and filiform and when shed break up
into their separate cells. Germ-tubes from these, or from the conidia, infect
the insect either as a caterpillar or chrysalis, and penetrating into its interior
give rise to cylindrical conidia which enter the blood-stream and increase
by yeast-like budding till the insect dies. A mycelium then appears and

i Podocrea alutacea Lindau = /W<w//w«<* aliitacettin (Pers.) Atkinson.

150

PYRENOMYCETES

[CH.

the formation of the sclerotium begins; chains of subaenal cpmdia may be
produced on conidiophores arranged in a coremium or fascic e of paralle
hvphae. This is the haria condition, and though there is little doubt that
it is a stage in the development of the Cordyceps, the ultimate proof by
culture has yet to be given.

Fig. no. a. Cordyceps militaris (L.) Link; b. Cordyceps ophioglossoides (Ehrh.) Link;
after Tulasne.

The mature sclerotium is a compact mass of interwoven hyphae whose
cells are rich in glycogen and oily matter. During its development the in-
ternal organs of the host are completely destroyed and replaced by the
mycelium, the skin alone remaining intact. From this mummified structure
one or more stromata arise, emerging between two segments of the skin,
usually near the head. The stroma is differentiated into an erect, sterile
stem, which may be simple or branched, and a globose or elongated, fleshy,
fertile portion, usually terminal on the stem and bearing the perithecia (fig.
ill). It is pale or bright coloured; red in the best known British species,
C. militaris ; and in other forms, purple, flesh-coloured, lemon-yellow or of
various shades of brown.

v]

HYPOCREALES

Fig. in. Cordyceps Barnesii Thwaites ;
perithecia, x 1 70 ; after Massee.

As development proceeds the ovate or flask-shaped perithecia are dif-
ferentiated ; they always arise deep in the stroma and may remain completely
or partially immersed or may become superficial as they approach maturity.
Where they are more or less free the surface
of the head is usually rough, whereas when
they are entirely immersed it is smooth,
but in some cases the free perithecia stand
so close together as to produce a smooth
appearance. The cytological details of
development have not been studied ; the
perithecia arise from the vegetative cells
of the stroma and in no case have any signs
of sexual organs been seen; it would thus
appear that Cordyceps is completely apoga-
moiis. The first sign of the perithecium
is the differentiation of a knot of deeply
staining vegetative hyphae.

The asci are long and slender with
slightly swollen apices into which the spores
do not penetrate; at maturity the contents
of the apex swell and the wall is ruptured. The spores are arranged in a
parallel manner, in a fascicle slightly twisted on its axis, and are nearly as long
as the ascus; they are hyaline, very slender and almost always multicellular;
they break up readily into their constituent cells which, as already stated,
germinate separately to infect a new host. According to the investigations
of Lewton-Brain several nuclear divisions take place in the ascus before
spore-formation and the spores are multinucleate from their first inception.

Two species, C. ophioglossoides (fig. iio£) and C. capitata, are parasitic
on underground fungi of the genus Elaphomyces and do not produce true
sclerotia; for these reasons they are sometimes separated as another genus
Cordylia.

The species of Claviceps, like those of Cordyceps, possess filiform asco-
spores, and form sclerotia from which the stromata arise. The genus is,
however, much smaller, including only six species parasitic on various
Gramineae. Of these the best known is the almost cosmopolitan species
C.purpurea, the ergot, on rye and other cultivated grasses.

The ascospores germinate on the flowers of the host, and give rise to
a mycelium which ramifies at first in the outer coats of the ovary and
ultimately fills its whole cavity, forming a sclerotium. Outside the ovary,
conidia are budded off, and at the same time a sweet fluid, the so-called
honey-dew, is excreted ; it attracts insects which carry the conidia with

i52 PYRENOMYCETES [CH.

them to other flowers, where they at once germinate, and further infections
are produced. On the completion of the conidial stage the sclerotia assume
a firmer texture, and become dark purple or bluish black in colour. If they
fall to the ground or are sown with the seed they give rise next spring to
numerous stromata with violet stalks and reddish yellow heads. According
to Fisch, the perithecia originate from two or three hyphal cells, which
become filled with strongly refractive protoplasm and divide in all directions
to form a roundish mass of cells distinguished from those of the rest of the
stroma by their size and contents. As in Cordyceps, there is no trace of
sexual organs. The perithecia are immersed in the stroma, and the asci
produce filiform but continuous spores.

The sclerotium is well supplied with reserve materials and contains certain
poisonous substances including ergotic acid, a narcotic which diminishes
reflex excitability ; sphacelic acid, the main cause of ergot poisoning, it
gives rise to gangrene, and large doses produce tetanus of the uterus and
cramp ; cornutin, an alkaloid causing contraction of the uterus.

Thus the ergot sclerotia, if eaten with the grass by cattle, or included in the
grain used for bread-making, are responsible for serious disease. When grain
was less carefully purified than at present the inhabitants of whole districts
sometimes became afflicted with gangrene, and the occurrence of the sclerotia
in pastures is liable, owing to the presence of cornutin, to cause abortion in
sheep or cows, so that many local traditions as to the prevalence of abortion
in certain farms, or in certain byres, are probably traceable to this cause.

Cornutin is of medicinal value, and the sclerotia are collected for this
purpose.

HYPOCREACEAE : BIBLIOGRAPHY

1843 BERKELEY, M. J. On some Entomogenous Sphaeriae. London Journal of Botany,
ii, p. 205.

1882 FISCH, C. Beitrage zur Entwickelungsgeschichte einiger Ascomyceten. Bot. Zeit.
xl, p. 850. •

1883 FRANK, E. Ueber einige neue oder wenige bekannte Pflanzen Krankheiten. Ber.
der deutsch. hot. Ges. i, p. 761.

1895 MASSEE, G. A Revision of the Genus Cordyceps. Ann. Bot. ii, p. 207.

iooi LEWTON-BRAIN, L. Cordyceps ophioglossoides. Ann. Bot. xv, p. 522.

1905 ATKINSON, G. F. Life-history of Hypocrea alutacea. Bot. Gazette, xl, p. 401.

1907 DANGEARD, P. A. Recherches sur le development du perithece chez les Ascomy-

cetes. Le Botaniste, x, p. 352.
1912 BLACKMAN, V. H. and WELSFORD, E. J. The Development of the Perithecium of

Polystigma rubrum. Ann. Bot. xxvi, p. 761.

1914 NlENBERG,W. Zur Entwickelungsgeschichte von Polystigma rubra. Zeitschr. fur
Bot. vi, p. 369.

DOTHIDEALES

The Dothideales constitute a small group of some four hundred species
included in twenty-four genera, forming a single family, the Dothideaceae'
They are parasites or saprophytes on the leaves and stems of higher plants

v] SPHAERIALES I53

on which they produce stromata usually below the epidermis and finally
exposed by its rupture.

The stroma is externally black and hard, built up of hyphae closely
interwoven to form a pseudoparenchyma ; internally it is of much looser
consistency, and is often white or brownish in colour. The perithecia are
without definite walls, so that the asci develop in mere cavities in the stroma,
which however have the globose form of ordinary perithecia, and are
bordered by cells rather smaller and narrower than those of the surrounding
mycelium. In some cases, where the inner tissue of the stroma is very
loosely interwoven, the perithecium is, however, definitely delimited.

In Dothidea the stromata form black projecting cushions, which in
D. virgiiltorum occur on the living, as well as the dead stems and branches
of the birch.

In Plowrightia the very similar stromata run together in masses.
P. morbosa is a serious disease attacking species of Primus, especially the
cherry and plum. The mycelium penetrates the living branches which
become swollen and deformed and on which stromata and finally perithecia
are produced.

SPHAERIALES

The Sphaeriales are distinguished by the dark colour and membranous,
corky or carbonaceous texture of their perithecia, and of their stromata when
present. They number already considerably over six thousand species, and
new species are constantly being brought to light, so that there is no doubt
that a study of the tropical forms, at present very incompletely known,
will greatly increase their number. Not only the number of species,
but the number also of -individuals is very considerable; the majority are
saprophytes, and serve a useful purpose in bringing about the first stages of
decay in such resistant materials as wood and straw. They greatly outnumber
the Hypocreales and Dothideales, and it is from their black or brown colour
and often charred appearance that the name Pyrenomycetes is derived.

The origin of the group has been proposed through Chaetoniium, which
is sometimes without an ostiole, from the Erysiphales, or, in view of the
structure of the sexual organs, from an Eurotium-\\\n& form among the
Plectascales.

Unfortunately their small size and resistant texture as well as the nature
of their habitat make many of the simpler species unfavourable subjects of
study, and our knowledge of their development is at present very fragmentary.
Sordaria and some others can be grown on artificial media and satisfactory
results may be anticipated from a further application of this method. Some
of the larger forms with a well-developed stroma can readily be handled but
in none of these has normal sexuality yet been observed.

The perithecia in the simplest forms are borne singly, free or partially

154

PYRENOMYCETES

[CH.

embedded in the substratum; from these may be traced a series of inter-
mediate forms culminating in the elaborate stromata and sunken perithecia
of the highest species. There is, in fact, a marked parallelism between the
Sphaeriales and Hypocreales, and it is by no means clear that the colour
and texture of the stroma and perithecium walls are of sufficient im-
portance as criteria of relationship to justify their separation, nor is it
indicated that the members of the families Nectriaceae or Hypocreaceae
resemble one another more closely than the numerous Sphaeriales, though
these are dispersed among a series of eighteen or nineteen families. The
method of classification is however convenient, and considerably more
knowledge will be required before a natural system of classification can -be
elaborated. In the meantime, the subdivisions of the Sphaeriales rest on
the structure and development of the stroma, the form of the ostiole, and
the colour and septation of the spores. As in the Hypocreales, various
sorts of accessory fructifications are present.

In the first eight families of the Sphaeriales the perithecia are more or
less free, though they may be partly sunk in the substratum, or in a weft
of hyphae, or may be seated on a definite stroma.

In the remaining ten families the perithecia are immersed either in the
substratum, or in a stroma which may reach considerable elaboration.
The most important of the eighteen families of the Sphaeriales are:
Perithecia free

Peridium membranous
ostiole beset with long hairs often elaborately

coiled or branched

ostiole without long hairs; mainly coprophilous
Peridium leathery or carbonaceous
short neck

long, sometimes filiform neck
Perithecia embedded in substratum
Perithecia immersed, upper part free
ostiole round
ostiole elliptical

Perithecia completely immersed, ostiole only pro-
jecting

peridium membranous or leathery, neck short
paraphyses absent
paraphyses present

peridium leathery or carbonaceous, neck long
Perithecia embedded in stroma

Stroma developed within substratum, differen-
tiated from it
Stroma free
ascospores very small, sausage-shaped and

hyaline or light brown, unicellular
ascospores unicellular, rarely bicellular, dark
brown

CHAETOMIACEAE.
SORDARIACEAE.

SPHAERIACEAE.
CKRATOSTOMATACEAE.

AMPHISPHAERIACEAE.
LOPHIOSTOMATACEAE.

MYCOSPHAERELLACEAE.

PLEOSPORACEAE.

GNOMONIACEAE.

VALSACEAE.

DlATRYPACEAE.

XYLARIACEAE.

v]

SPHAERIALES

155

Chaetomiaceae

The Chaetomiaceae occur on straw, paper, dung and other waste
materials; they possess free, thin-walled perithecia beset with numerous
characteristic, long hairs (fig. 112), which are often elaborately branched
or coiled. On these, or on the ordinary vegetative mycelium, conidia are
produced. An ostiole is lacking in Ch.fimete, presumably the most primitive
member of the genus; in the remaining species it is present and the peri-
thecium is of the typical sphaeriaceous form.

In Chaetomium spirale the cells of the mycelium contain each a single
nucleus, the archicarp arises as a coiled branch and divides into four or
more uninucleate cells. There is no sign of an antheridium. Vegetative
hyphae grow up from the stalk of the archicarp, and from the filament on
which' it is borne, and form a sheath, the outer cells of which are prolonged
as hairs. Small pyriform conidia are abundant.

Ch. Kunzeanum shows a very similar archicarp (fig. 1 1 3), but here the
cells, as described by Vallory for the variety chlorimim, each contain several
nuclei which are often found approximated in pairs. This arrangement is
reported to be as common in the vegetative mycelium as in the cells of the
archicarp, and is doubtless a result of rapid division.

Fie. 112. Chaetomium pannositm Wallr.; xjo:
W. Page del.

113. Chaetomium Kunuanum
; archicarps ; after Oltmanns.

1 56

PYRENOMYCETES

[CH.

In due course the archicarp becomes surrounded by a sheath of vegetative
hyphae within which its growth is continued so that a mass of cells is pro-
duced from which asci at last arise. In the meantime the sheath becomes
differentiated into an outer coat of relatively large, brown-walled hyphae,
and an inner layer of smaller cells which become narrow and elongated. As
development proceeds a cavity appears within the perithecium, usually just
above the ascogenous cells, and branches from the lining mycelium grow

out to form the periphyses; paraphyses
are not produced (fig. 114).

The ripe spores are shed into the
cavity of the perithecium, and do not
reach the exterior immediately on leav-
ing the ascus.

In addition to the above, two or
three otherspecieshave been examined,
and show the same type of archicarp
and of perithecium, but in no case has
any further cytological detail been
worked out.

The uninucleate species in particu-
lar would probably repay investigation
and special attention ought to be given
to the septation of the archicarp and
to the number of cells from which ascogenous hyphae originate.

Fig. 114. Chaetomium Knnzeanum Zopf;
perithecium, x 200 ; after Zopf.

CHAETOMIACEAE : BIBLIOGRAPHY

1881 ZOPF, W. Zur Entwickelungsgeschichte der Ascomyceten. Chaetomium. NovaActa

Acad. C. Leop.-Carol. G. Nat. Cur. xlii, p. 199.
1887 OLTMANNS, F. Ueber die Entwickelung der Perithecien in der Gattung Chaetomium.

Bot. Zeit. xlv, p. 193.
1907 DANGEARD, P. A. Recherches sur le deVeloppement du perithece chez les Ascomy-

cetes. Le Botaniste, x, p. 329.
1911 VALLORY, J. Sur la formation du pdrithece dans le Chaetomium Kunzeanum Zopf.

var. chlormum Mich. Comptes Rendus, cliii, p. 1012.

Sordariaceae

The Sordariaceae are mainly coprophilous ; their perithecia are typically

ree, sometimes superficial, sometimes so deeply embedded in the substratum

ittle more than the neck protrudes from it. The genus Hypocopra is

:ceptional in possessing a small stroma in which the perithecium is

immersed, but it resembles Sordaria in all other points. The present family

ffers from the Chaetomiaceae in bearing only short filaments instead of

SPHAERIALES

157

long hairs around the ostiole, and from the Sphaeriaceae in the habitat and
type of spore. The mycelium is in most cases composed of multinucleate
cells, but in Podospora hirsuta the .cells are uninucleate (fig. 115), recalling
the condition in several species of Chaetomium.

The commonest type of archicarp is a stout, coiled, septate hypha which
soon becomes surrounded by vegetative filaments; it is usually terminal, but
is occasionally intercalary, for instance in Sordaria fimicola. Dangeard has
found a straight archicarp (fig. 1 16) in Sordaria macrospora, and in 1868, for
S. fimiseda, Woronin described an archicarp with a swollen terminal cell
recalling the oogonium of Humaria grannlata.

Fig. if 5. Podospora hirsnta
Dang., archicarp; alter Dan- Fig. 116. Sordaria macrosforaAuersw.; a. straight archicarp; after
geard. Dangeard.

In Sporormia intermedia the perithecium is initiated by the enlargement
of a multinucleate mycelial cell which is often intercalary. It undergoes
not only transverse but also longitudinal divisions, forming a pseudoparen-
chymatous massof uninucleate cells(fig. 1 17), with which various neighbouring
cells anastomose. The mass thus formed is responsible for the whole contents
of the perithecium, though the outer walls may be formed by ordinary
vegetative hyphae. In view of this fact it seems doubtful whether the initial
cell should here be regarded as an
oogonium, that is to say as having at
one time had a sexual significance,
and not rather as a preliminary stage
in the development of such a mass of
hyphae as initiates the apogamous
perithecium of Claviceps and its allies.

\L

In some of the Sordariaceae each
spore is surrounded by a layer of

Fig.

117. Sporormia intermedia Auersw. ; initial
cells of perithecium ; after Dangeard.

I58 PYRENOMYCETES [CH.

mucilage (Sordaria macrospora, S. fimicola, etc.), in others (fig. 2 e) one or
two appendages are produced (S.fimiseda, S. coprophila, Podospora anserina,
etc.). These may be gelatinous and derived wholly or partly from the epi-
plasm apparently much as the ordinary thickening of the spore wall is
derived, or they may form part of the young spore. In the latter case they
are at first rich in protoplasm, but later most of their contents pass into the
middle portion of the spore, which becomes ovoid, and the appendage is cut
off by a wall (S. globosa). Both types of appendage may occur on the same
spore. They are sometimes hooked and they become twisted together and
serve to attach the spores one to another. The uppermost appendage appears,
in some cases at any rate, to become fastened to the tip of the ascus (S.
Brefeldii.

SORDARIACEAE : BIBLIOGRAPHY

1883 ZOPF, \V. Zur Kenntniss der anatomischen Anpassung der Pilzefruchte an die

Funktion der Sporentleerung. Zeitschr. fur Naturwiss. iv ; ii, p. 540.
1886 WORONIN, M. Sphaeria Lemaneae, Sordaria Jimiseda, Sordaria coprophila und

Arthrobotrys oligospora. Beit, zur Morph. und Phys. der Pilze, iii, p. 325.
1901 MASSEE, G., and SALMON, E. Researches on Coprophilous Fungi. Ann. Bot. xv,

P- 3i5-
1907 DANGEARD, P. A. Recherches sur le de'veloppement du perithece chez les Ascbmy-

cetes. Le Botaniste, x, p. 333.
1912 WOLF, F. A. Spore Formation in Podospora anserina, (Rabh.) Wint. Ann. Myc.

x, p. 60.

Sphaeriaceae

The perithecia of the Sphaeriaceae are superficial, and are borne singly

or in groups; the peridium may be smooth or beset with hairs or spines.

The papillate ostiole distinguishes this family from the succeeding forms

with free perithecia.

The majority are saprophytic on plant remains, frequently on wood;

some are parasites, such as the species
of Coleroa (fig. 1 18), which occur on the
leaves of Potentilla, Rubus, and other
flowering plants.

Rosellina quercina, the oak root fun-
gus, attacks the roots of oak seedlings;
the hyphae enter the living cells of the
cortex and pith ; they are at first hyaline,
later dark in colour, and become twisted
together into strands, the so-called rhi-
zoctonia; these attack the roots of neigh-
bouring oak plants, wrap a weft of hyphae

Fig. us. Coleroa Potentiliae (Fr.) Wint.; about them and enter their cells. The

fungus may form black, chambered scle-

SPHAERIALES

159

rotia which originate in the cortex of the host root ; reproduction is by
means of conidia formed in summer on the surface of the soil, and further
by ascospores produced in perithecia. Hartig has found that the perithecium
is initiated by the development of a pair of thick hyphae rich in contents.
These become enclosed within a mass of vegetative tissue, but their subse-
quent behaviour has not been determined, and no details of development
are known either here or in other members of the family.

SPHAERIACEAE : BIBLIOGRAPHY

1880 HARTIG, R. Der Eichenwurzeltodter Rosellina quercina. Untersuch. aus der forst-
botanische Inst. zd Miinchen iii, p. i.

Ceratostomataceae

The Ceratostomataceae resemble the Sphaeriaceae in most of their
characters; they are distinguished by the elongated neck of the perithecium,
which is often drawn out to form a delicate hair-like process. The method
of liberation of the spores in this family presents an interesting problem,
but neither that question nor the development of the perithecium has yet
been elucidated.

A mphisphaeriaceae

In the Amphisphaeriaceae the young perithecium is sunk in the substra-
tum ; as it matures it becomes more or less free, though in contrast to the con-
dition in the Sphaeriaceae and Ceratostomataceae, its base isalvvays immersed.

Development has been studied in a species of Teichospora and a species of
Teichosporella, now both included
under the genus Strickeria, charac-
terized by its muriform spores.
The spore produces numerous
germ-tubes which give rise to a
mycelium of multinucleate cells ;
certain cells increase in size and be-
come both transversely and longi-
tudinally divided till a parenchy-

matous mass is produced (fig. 1 19).
Other vegetative hyphae may form
a scanty investment, but often the
perithecium develops without this
addition.

Asci appear as large uninu-
cleate cells, and the tissue around
them disorganizes. The outer hy-
phae become hard and dark only
when the perithecium approaches maturity.

19. Strickeria sp. ; initial cells of ascocarps;
after Nichols.

i6o

PYRENOMYCETES [CH.

The type of development here is very similar to that already described
for Sporormia ; it seems very doubtful whether the initial cell of the peri-
thecium should be regarded as an oogonium, or whether the development
is purely vegetative. The peculiarity in either case is the formation of the
bulk of the perithecium from a single cell instead of, as in the majority of
forms, from a complex of interwoven hyphae differentiated into sexual and
vegetative components.

AMPHISPHAERIACEAE: BIBLIOGRAPHY

1896 NICHOLS, M. A. The Morphology and Development of certain Pyrenomycetous
Fungi. Bot. Gaz. xxii, p. 301.

LopJiiostomataceae

The perithecia of the Lophiostomataceae are borne singly; during de-
velopment they are embedded in the substratum, and they may so remain
or may become partially free at maturity. There is no stroma, and the
peridium is black and brittle. So far there is a close resemblance to the
Amphisphaeriaceae, but the Lophiostomataceae are distinguished by the
form of the ostiole, which is very large and laterally compressed, so that in
external appearance they approach certain of the Hysteriales which in many
cases they further resemble in their habitat on vegetable remains such as
wood and bark. None of the species has been investigated in detail.

Mycosphaerellaceae

The Mycosphaerellaceae are parasitic forms occurring usually on leaves
and giving rise to various kinds of leaf-spot. The perithecia are sunk in the
substratum and develop either under the cuticle or beneath the epidermis,
breaking through at maturity. The ascospores are usually septate, frequently
bicellular and sometimes dark-coloured; except in the transitional genus
Stigmatea, paraphyses are not developed. In several cases the formation
of the perithecia is preceded by a conidial stage.

Mycosphaerella nigerristigma forms pycnidia on the living leaves of
Primus pennsylvanica and perithecia after the leaves have fallen. A tri-
chogyne like that of Polystigma has been recorded ; it degenerates, leaving a
basal cell, but whether this functions is not known.

MYCOSPHAERELLACEAE : BIBLIOGRAPHY
19.4 HIGGINS, B. B. Life-History of a new species of Sphaerella. Myc. Centralbl. iv,

v]

SPHAERIALES

161

Pleosporaceae

The Pleosporaceae are saprophytes or in a few cases parasites, for the
most part on seed plants but in some cases on Pteridophyta, Bryophyta or
Lichens. The penthecia are immersed in the substratum, the ostiole only
projecting, but they may become more or less exposed by the rupture of the
covering tissues. The peridium is leathery or membranous.

The genus Pleospora includes some 225 species, several of which occur
on grams and other grasses where they show biological specialization
Pleospora herbarum is a facultative parasite on the leaves of angiosperms •
the penthecium is initiated by the division of a hypha into numerous short
cells from which branches grow out. The central cells, and later the basal
parts of the branches, divide in various directions till an irregular paren-
chymatous mass is formed. By further growth and division the mass
assumes a globular shape and the central cells become elongated and differ-
entiated as paraphyses. Later, asci appear, developing from the same cells
as the paraphyses and each produces eight muriform spores (fig. 120).

Fig. 120. Pleospora sp.; germinating spores, x 1000.

Multicellular conidia also develop on branched hyphae, the terminal cells
of which form the sterigmata. After the spore is shed the hypha may continue
to grow, a new sterigma being formed above the old one. The name Macrospo-
rimn parasiticum was formerly applied to the conidial stage of this species.

The genus Venturia includes over fifty species, several of which are para-
sitic on living leaves; the perithecium is immersed and the large ostiole beset
with stiff hairs or bristles. The species grouped under Fusidadium among
the Hyphomycetes are in some cases conidial forms of this genus. The
conidia are two-celled, borne on short conidiophores arranged in groups;
F. dendriticum is the cause of scab or black-spot on apples, and F. Pyrinum
of a similar disease on pears.

G.-V. i 1

PYRKNOMYCETES

[CH.

LeptospJuuria includes some 500 species characterized by the papillate
or conical ostiole, usually free from hairs. The majority are saprophytes on
plant remains, some are parasites on land plants, and some on the Red
Algae.

L. Leinaneae occurs on the thallus of various species of Lemanea (fig. 121).
The mycelium consists of uninucleate cells and ramifies in the intercellular
spaces of the host, sending branched haustoria into the cells. Here and there
the hyphae are dilated (fig. 122 a, b\ and in these regions show denser and
more refractive contents than usual. Fusion takes place between the dilated
portions (fig. \22c,d} which may be terminal or intercalary, and there is

\ «

Fig. 121. Leplosphacria Lemaneae (Cohn)
Brierley ; transverse section through thal-
lus of Lemanea, showing perithecium,
x 125; after Brierley.

Fig. 122. Leptosphaeria Le-
maneae (Cohn) Brierley ;
a. b. c. d. stages of fusion
between dilated hyphae ;
after Brierley.

evidence that the nucleus of one of the swollen cells passes across into the

other, which may therefore be termed the oogonium, and fuses with its

The oogonium then divides to form a number of multinucleate

s from which ascogenous hyphae arise. The nuclei in these hyphae are

paired and the usual fusion takes place in the ascus. From the cells adjoining

e oogonium the delicate hyphae of the sheath grow up. The morphology

the sexual organs in this genus is quite unusual, but they may perhaps

best be compared with the dilated cell observed by Dangeard in the initiation

the perithecium in Sporormia intermedia- in that case, however there

does not appear to be a functional antheridium, and vegetative cells as

well as ascogenous hyphae are stated to develop from the initial cell ; the

semblance demands further investigation.

VJ SPHAERIALES r63

The family is rich in conidial forms, and it is probable that several species
Fungi Imperfecti, including the pycnidial genera Phoma and Hendersonia
and also Cercospora, a form with long septate conidia on free conidiophores
are stages in the development of members of the Pleosporaceae.

PLEOSPORACEAE: BIBLIOGRAPHY

1886 WORONIN, M. Sphaeria Lemaneae, Sordaria fimiseda, Sordaria coprophila, und
Arthrobotrys oligospora. Beit, zur Morph. und Phys. der Pilze iii p 3-^5

1889 MIYABE KlNGO. On the Life History of Macrosporium parasiticum, Thum. Ann.
Bot. 111, p. i.

1913 BRIERLEY, W. B. The Structure and Life History of Leptosphaeria Z>;*<r««w(Cohn).
Mem. and Proc. Manchester Lit. and Phil. Soc. Ivii, 2, p. i.

Gnomoniaceae

The Gnomoniaceae are for the most part saprophytic on the leaves or
other parts of plants. The perithecia are embedded in the substratum from
which their long necks project. The ascus is characterized by a thickened
apex through which a canal allows the exit of the spores. The spores are
hyaline and paraphyses are usually not developed. The family differs from
the Pleosporaceae in the long neck of the perithecium and the thickened
apex of the ascus. There is no stroma, and this fact, as well as the dark
colour, distinguishes Gnomonia from the similar genus Polystigma among
the Hypocreales.

Gnomonia erythrostoma is the cause of an epidemic disease known
as cherry-leaf-scorch, which attacks the foliage of Primus avium and of
several varieties of the cultivated sweet cherry. The mycelium ramifies on
the leaf and runs back to the base of the petiole, where it prevents the
formation of the absciss layer. In consequence the infected leaves do not
fall, but remain hanging on the branches ; they are the only source of
infection in the following summer, and their destruction is therefore a sure
method of checking the disease.

Infection usually takes place in June; towards the end of August spermo-
gonia appear; they are shallower than those of Polystigma, but otherwise
very like them, with a wall of closely compacted hyphae and a small circular
ostiole opening on the under surface of the leaf. The spermatial hyphae are
narrow and tapering, and their extremities are abstricted to form the sper-
matia, each of which contains a long threadlike nucleus and a relatively small
amount of cytoplasm.

Soon after the spermogonia have begun to develop certain hyphae near
the lower epidermis of the leaf become entwined to form more or less
spherical coils, the primordia of the ascocarps. Their apices project in
groups of four or five through the stomata, and the terminal cells become

164 PYRENOMYCETES [CH.

swollen and apparently mucilaginous; these projecting filaments were re-
garded by Frank as trichogynes, but more recently Brooks has found evi-
dence that they arise from the outer cells of the perithecium and that, what-
ever their origin, they now no longer function as receptive structures. Sper-
matia are often found attached to their terminal cells, but, in view of the
enormous number of spermatia liberated on the under surface of the leaf,
they could hardly fail to be found in relation to any projecting filament.

In the lower part of the coils certain cells become differentiated by their
denser cytoplasm and larger nuclei, and no doubt represent the oogonial
regions of the archicarps. No union of nuclei has however been observed
in them and it is at least doubtful whether they give rise to the ascogenous
hyphae. The latter do not become clearly differentiated till the oogonial
cells have disappeared ; asci are formed either from the terminal or sub-
terminal cells; in the young ascus two nuclei fuse.

Throughout the divisions in the ascus and in the division of the spore
nucleus Brooks has reported four chromosomes. Those in the first division
in the ascus are short and thick, resembling heterotype chromosomes in
appearance, and there seems reason to believe that reduction occurs at this
stage.

The life-history of Gnomonia shows many points in common with that
of Polystigma\ both are at first leaf parasites, and complete their develop-
ment saprophytically on the dead leaf. Both produce spermogonia with
filiform spermatia and perithecia developed in relation to coiled archicarps.

An important point of difference is that in Polystigma a stroma is formed
and the fungus hibernates on the fallen leaves below the tree without being
injured by their decay; in Gnomonia no stroma is present and the fungus
inhibits the formation of the absciss layer so that the withered leaves
remain on the branches and provide a matrix in which the perithecia can
be formed.

GNOMONIACEAE: BIBLIOGRAPHY
1886 FRANK, B. Ueber Gnomonia erythrostoma, die Ursache einer jetzt herrschenden

Bhittkrankheit der Siisskirschen im Altenlande, nebst Bemerkungen iiber Infection

bei blattbewohnenden Ascomyceten der Baume iiberhaupt, etc. Ber. der deutsch.

Bot. Gesell. iv, p. 200
1910 BROOKS, F. T. The Development of Gnomonia erythrostoma, the Cherry- Leaf-Scorch

Disease. Ann. Bot. xxiv, p. 585.

Valsaccae

The perithecia of the Valsaceae are produced frequently in compact

groups on a black stmma from which their long necks alone project. The

stroma ,s very variable in form ; it is developed within the substratum and

: or less d.fferentiated from it, sometimes indicated only by a black

on the wood or bark of the host and by a black margin, sometimes

vl SPHAERIALES l6s

extended as a thin black layer over a considerable area and ending irregularly ;
sometimes, as in species of Valsa, forming black cushions erumpent through
the bark of the host. In a few cases the stroma surrounds only the upper
part and not the base of the perithecium, and we have thus a transition from
the rudimentary stromata of some of the earlier families.

The peridium is black and leathery, the asci usually long stalked, the
spores uni- or multicellular, and hyaline or dark-coloured.

Conidia are frequently present, borne on free conidiophores or produced
within pycnidia.

The genus Valsa includes some four hundred species and Diaporthe a
rather larger number. The majority are saprophytic on wood and other re-
sistant parts of plants.

Diatrypaceae

In the Diatrypaceae the stroma is developed under the bark of the host,
and forms either a cushion or a thin, flat layer which later becomes exposed.
Conidia of various kinds are produced, but the conidial and perithecial
stromata are often distinct and whereas the latter are of the usual dark
colour and carbonaceous consistency the former are frequently light-coloured
and fleshy. This separation and the usually unicellular, small, hyaline,
curved ascospores are the principal characters of the family.

The genus Calosphaeria is exceptional in lacking a perithecial stroma;
its perithecia are free and it could appropriately be placed in one of the
groups near the Pleosporaceae but that a conidial stroma is present and
closely resembles that of the Diatrypaceae; the ascospores, moreover, are of
the characteristic curved form, so that Calosphaeria may, it appears, more
fitly be regarded as a reduced member of the group. The species of Calo-
sphaeria, like the other Diatrypaceae, occur chiefly on dead wood but
C. princeps infects the living branches of cherry, plum and peach.

In Diatrype the "most characteristic stroma is a black corky tissue of
indefinite extent in which the perithecia are completely immersed ; the ascus
contains eight spores in contrast to the numerous spores of certain species of
Calosphaeria and of Diatrypella, a genus further distinguished by the cushion-
shaped stroma.

Xylariaceae

The Xylariaceae occur chiefly on wood; they represent the highest
development of the Sphaeriales and are characterized by the free superficial
stroma which is only very rarely, as in Hypoxylon, partly sunk in the sub-
stratum, and shows every variety of form from a spreading crust on the
surface of the host, as in the genus Nummularia, some species of which

1 66

PYRENOMYCETES

[CH

approximate Diatrype, to the almost spherical cushions of "£^ <<£ 2
and the erect, simple, or branched stromata of Xyhna (fig. 124) and
allies The perithecia are arranged just below and at right angles to the
surface of the stroma; their development may be preceded by the formation
of conidia which often cover the young stroma with a whitish powder.

Fig. 123. Hypoxylon coccineum Bull.; the smallest stroma bears conidia, the others perithecia;
after Tulasne.

Poronia punctata occurs on old horse dung; the stromata are about
i cm. in height, stalked and expanded above into a cup or disc (fig. 125),
which, in the earlier stages of development, is covered by a greyish-white
film of conidia; later the ostioles of the numerous perithecia appear as black
dots scattered over the surface of the disc (fig. 126). The asci, when ripe,
protrude through the ostiole so that the dark brown spores are shed outside
the perithecium.

Dawson was able readily to obtain pure cultures, both from the asco-
spores and from the conidia, on 10 per cent, gelatine made up with decoction
of horse dung.

The ascospore forms a single lateral germ-tube, which develops septa
and branches freely. The conidia produce germ-tubes from either end or
from both and sometimes also laterally ; the mycelium is at first much more
delicate than that derived frorh the ascospores but soon becomes indistin-
guishable from it. Branches arise from points just below the cross walls ;

SPHAERIALES

167

frequent lateral anastomoses occur and crystals of calcium oxalate, which

have become separated from the substratum, are found among the filaments.

Hyphae become massed together to form the stroma which in the

very young stages consists entirely of vegetative filaments densely inter-

Fig. 124. Xyiaria Hypoxyhn Grev., after Tulasne.

woven and rising vertically from the surface of the substratum. As they
grow the stromata assume their characteristic shape, conid.a appear -and
drops of pinkish or yellowish fluid are exuded. When these dry up, black
dots indicating the position of the ripening perithecia are s

1 68

PYRENOMYCETES

[CH.

Fig. 125. Poronia pimctata (L.) Fr.; a. surface, b. lateral view
after Tulasne.

Fig. .26. Poronia pnnctata (L.) Fr.; stroma cu

t across ; after Tulasne.

v]

SPHAERIALES

169

The perithecium is initiated by the development of a coil of large,
deeply-staining cells forming the archicarp. It arises amongst the vegetative
filaments of the stroma, forms a couple of loops and is continued towards
the surface of the stroma as a slender multicellular trichogyne (fig. 127 a).
At an early stage the coiled portion becomes surrounded by a knot of small,
densely-staining hyphae ; later the trichogyne disappears, degeneration
progressing from the base to the apex ; the investing filaments grow more
actively on the side of the archicarp towards the surface of the stroma, so
that the young perithecium becomes pear-shaped (fig. 127^, c)\ further
growth renders it hollow, and the upper part becomes lined with delicate
periphyses (fig. 127 d). At the base of the developing perithecium is a group

Fig. 127. Poronia punctat

: (L.) Fr. ; a. archicarp, x 275 ; b. c. and d. young peri
after Dawson.

205;

of stout, deeply-staining hyphae, from which the asci arise and which occupy
the position of the coiled archicarp in earlier stages. Later the base and
sides of the perithecium are covered by numbers of filiform, septate para-
physes, and amongst these the asci develop.

It seems pretty clear that the trichogyne now no longer functions; tl
is borne out by the fact that degeneration proceeds from its base upwar
and not from its apex, as might have been expected if a male nucleus wet
travelling down. It is probable, though it has not actually been dei
strated, that the ascogenous hyphae are derived from the archicarp, b
view of the complete degeneration of this organ in Gnomon*,*
to conclude without further evidence that it is still functional ™P°™
punctate. The species deserves further investigation, especially

and Hypoxylon the young stroma is covered by a tangle

PYRENOMYCETES

[CH.

of cbnidiophores, from which small oval conidia are abstricted. In Xylaria
these form a white coating, in marked contrast to the older black portions
of the stroma, where the perithecia are maturing, and justify the name
candle-snuff fungus, applied to some of the commoner species. If, in either
genus, the stroma be sectioned during the conidial stage, nests of small
hyphae, similar to those in Poronia, will be found, and are the first indica-
tions of the perithecia.

Sometimes a stouter hypha with larger nuclei, presumably an archicarp,
is recognizable (fig. 128), but it has not been shown to function, and there
is no evidence of normal sexuality. It is however not unlikely that some
of these species, which are conveniently easy to microtome, will repay
further investigation. At a later stage ascogenous hyphae are readily recog-
nizable (fig. 129).

Fig. 128. Xylaria polymorpha (Pers.)
Orev. ; archicarp embedded in
stroma, x 1000.

Fig. 129. Xylaria polymorpha (Pers.) Grev.; septat
archicarp, x 1000.

XYLARIACEAE : BIBLIOGRAPHY

v]

LABOULBENIALES

LABOULBENIALES

The group Laboulbeniales includes some six hundred species arranged
in over fifty genera. All are minute external parasites on insects, chiefly on
members of the Coleoptera. They appear to do but little injury to the host,
inducing at most a slight irritation but never causing death, indeed their own
existence depends on that of the insect to which they are attached since,
unlike many other fungi, their life ends with that of their host.

The Laboulbeniales are all of fairly simple structure (fig. 130) and show
an underlying similarity of type. In all cases the vegetative part consists of
a receptacle, usually two-celled, attached to the integument of the host by
a blackened base or foot. From the receptacle grow out filamentous appen-
dages on or among which the male organs are produced and, with a few
exceptions, the receptacle of the same individual also gives rise to a female
organ from which a perithecium liberating ascospores is eventually developed.

The plant is covered by a thin, homogeneous membrane which is ex-
ceedingly tough and impervious and is developed from the gelatinous coat
of the spore; it efficiently protects the cells from desiccation.

Within this envelope the cell walls (except those of the receptive parts
of the trichogyne and of the internal cells of the perithecium) are very thick
and laminated. In certain cases, and especially in the genus Laboulbenia,
they are traversed by fibrillae which arise from the innermost wall layer
and are attached to the inner surface of the envelope. The cells are uni-
nucleate (fig. 131) with rather dense, granular or reticulate cytoplasm and

Fig. 130. Laboulbenia triordinata Thaxterjx 135;
after Thaxter.

Fig. 131. Laboulbenia (haftophora
young perithecium and tricho-
gyne, x36o; after Faull.

172

PYRENOMYCETES

[CH.

contain oil globules. Between adjacent cells that have the same origin the
protoplasm is continuous through broad pits. The cytoplasm on each side
dips into the pit, forming a thick strand which, in Laboulbenia at least, appears
to be intersected by the middle lamella (Faull). The latter in favourable
cases is seen to be perforated by one or more fine pores through which com-
plete continuity is established1. There is evidence that a stout strand of
cytoplasm unites contiguous cells in the appendages.

The spores are remarkably uniform throughout the group, being in-
variably hyaline and fusiform or acicular in shape and almost invariably
two-celled (fig. 132). The cells are commonly of unequal size, that nearest
the apex of the ascus being the larger, and both
are uninucleate. The spore is clothed in a gelati-
nous sheath especially well developed about the
upper end which, when the spore is discharged
from the perithecium, is destined to come in con-
tact with the integument of the host. Here the
gelatinous mass enables the spore to take up the
oblique position in which germination occurs.

The lower extremity of the spore (its apex
while in the ascus) forms the foot. As a rule the
gelatinous envelope in this region becomes hard,
opaque, black and more or less elastic and thus,
while adhering firmly to the substratum, it may
give the plant a certain freedom of movement.
This elasticity is found especially in forms on sub-
merged and rapidly swimming hosts where it
allows the parasite to lie back along the body
of the insect. Sometimes the foot is cut off from
the rest of the plant by a wall, more often it is continuous with and forms
part of the basal cell of the receptacle. In the great majority of cases it
does not penetrate into the substance of the host but is in contact with
the surface by a thin membrane through which materials are absorbed into
its cavity.

here are a certain number of forms, however, especially those occurring

on soft-bodied insects or on the soft parts of others, in which a definite

izoidal apparatus is developed and penetrates the body of the host. These

s show no greater vegetative luxuriance than other members of the

group and apparently do not benefit by their more elaborate absorptive orga.n

The receptacle, like the foot, develops from the lower segment of the

isists, m the simplest cases, of two superposed cells and (in

off for the Red Algae <"Neue

Fig. 132. Laboulbenia elon-
gata Thaxter ; bicellular
spore; after Thaxter.

v]

LABOULBENIALES

173

monoecious forms) bears the appendages in a terminal position and the
perithecium laterally (fig. 1 36).

More rarely the receptacle consists of a larger number of cells variously
arranged and reaching a considerable complexity in such forms as Zodio-
myces vorticellarius (fig. 133).

One or more appendages are borne on the receptacle. These are more
or less filamentous and often elaborately branched. They bear the male
organs and serve also for the protection of the delicate trichogyne and perhaps
facilitate fertilization by holding a drop of water around the organs con-
cerned. The primary appendage is developed from the upper segment of
the germinating spore and is terminal ; the later formed secondary append-
ages, when present, are outgrowths from the cells of the receptacle.

The male element is a non-motile cell which as early as 1896 was
homologized by Thaxter with the spermatium of the Red Algae. The
latter organ has now been shown to be an antheridium1 in which the
nuclear divisions are reduced to one, or have altogether disappeared ; it is
liberated entire from the male plant and carried passively to the female
organ. It seems very probable that in the simplest cases, where they are
produced externally at the tips of more or less specialized branches (fig. 1 34),

Fig. 133. Zodiomyces vorticellarius Thaxter; after
Thaxter.

Fig. 134. Ceratomyces rostra'
tus Thaxter; exogenous
spermatia ; alter Thaxter.

Wolfe, Ann. Bot. xviii, 1904- Yamanouchi, Bet. Gaz. Ixii, 1906.

174

PYRENOMYCETES

[CH

the " antherozoids " or spermatia of the Laboulbeniales have the same signi-
ficance as those of other fungi. They fall off when mature and the cells from
which they were formed may give rise to others in the same position.

In Coreomyces instead of a segment of the branch being detached to form
the spermatium, a portion of its contents is extruded. This arrangement
leads to the more specialized endogenous organ which is found in Stigma-
tomyces (fig. 1 36) and in many other forms. Here the naked mass of proto-
plasm cut off from the parent cell may be regarded as the homologue of
the spermatium, or the parent cell may be recognized as an antheridium
and the detached segments as non-motile spermatozoids. They function, in
any case, as sperms or male elements. They are detached from the contents
of a flask-shaped cell and are extruded through an elongated neck opening
at maturity to the exterior. Between the neck and the venter a diaphragm
of cellulose is deposited and is perforated by a narrow opening so that the
sperms are nipped off as they pass into the neck. They are uninucleate, the
nucleus of the parent cell undergoing successive divisions so that a series of
sperms are produced. The parent cell has been termed an antheridium but
if the spermatium is antheridial in character the name cannot appropriately
be used for the cell in which it is borne, though the term spermogonium is
applicable.

These sperm-forming organs may be produced singly or in groups, each
with its neck opening independently to the exterior, or they may form com-
pound structures (fig. 135), the necks of several cells
penetrating a single adjacent cell into the cavity of
which the sperms are discharged and from which they
escape by a common duct, the so-called secondary
neck, which may be a mere extension of the cell
forming the common cavity or, in a few cases, may
involve other cells also. The individual sperms are
formed in much the same way in the compound as
in the simple organs, but instead of being cut off
from the parent mass of protoplasm by a diaphragm
at the base of the primary neck they remain attached
till the neck widens abruptly at its end, and they
are extruded into the common chamber. Hundreds,
or even thousands, may be formed during the period
of activity of a single compound organ. The exo-
genously produced sperms are always walled where-
as those formed endogenously are naked when first
set free ; later a thin wall may be secreted.

The female organs are formed from the basal
cell of the spore and are thus necessarily lateral. This condition is often
obscured in the mature plant where the developing perithecium may push

after

v]

LABOULBENIALES

'75

Fig. 136. Stiginatomyces Baeri Peyritsch ; development of the perithecium ; a. shows the two-celled
receptacle, a single appendage bearing five simple, endogenous spermatial organs, and the beginning
of the perithecium; /;. — /'. indicate successive stages in the development cf the perithecium; the
trichogyne first appears in d. ; in e. spermatia are being shot out and some are attached to the
trichogyne; in i. two of the four ascogenous cells are shown, with the superior sterile cell above
them, and the primary and secondary inferior sterile cells below; after Thaxter.

the perithecium. It divides transversely ; the upper of its daughter cells gives
rise to the female organ, the lower divides several times (fig. 136^), and
ultimately forms the double wall of the perithecium, a function fulfilled by
a complex of neighbouring hyphae in Ascomycetes with a richer vegetative
development.

The upper cell, the initial of the female organ, divides, separating the
female cell below (fig. 136^) and a cell above, which divides once more to
form the terminal trichogyne and the subjacent trichophoric cell (fig. 136^).

1 76

PYRENOMYCETES

[CH.

All the cells are uninucleate. The female cell is called by Thaxter a
carpogonium or carpogonic cell in conformity with the term used for the
Red Algae, but it obviously corresponds to the cell in which fertilization is
now known to occur in other Ascomycetes and will therefore here be termed
the oogonium.

In Stigmalomyces Baeri the trichogyne is simple (fig. 136^, e) but in
many other members of the group it undergoes frequent septation and
branches freely. The apices of the branches are alone receptive and may-
straight or spirally coiled (fig. 1 37). However elaborate, the trichogyne quickly
disappears, collapsing and breaking off as soon as its function is fulfilled.

In endogenous species the sperms are shot direct on to the trichogyne or
carried to it by the water which ordinarily surrounds these filaments when
the hosts are hiding in moist places. In Zodiomyces on the other hand,
where the spermatia are formed externally, they fall off the parent branches
on to the cup-shaped receptacle, and there appear to be sought by the
trichogyne which is at first bent over (fig. 1380) and later lifts itself after a
spermatium has become attached (fig. 138$).

F'g- 137- Compsomyces verticillatus Thaxter; after Thaxter.

Fig. 138. Zodiomyces •vorticdlarius
Thaxter; trichogyne a. before and
b. after attachment of spermatium ;
after Thaxter.

In any case numerous male cells reach the trichogyne and, though the
actual process of fertilization has not yet been seen, it appears likefv that
it is accomplished.

Afterwards the oogonium divides into three superposed cells, the sterile
nor cell the sterile superior cell and a fertile cell lying between the two

fi *(' u middle CeU CUtS off a secondary sterile cell below

& 1360 which like the other sterile cells is eventually destroyed. It then

divides longltudinally into four "ascogenic" cells, two of which are shown in

VJ LABOULBENIALES l??

fig. 136*, and from these asci bud out, arising in a more or less distinctly
double row (fig. 1 39 a). Some variation occurs in different species in the later
divisions and in the number of ascogenic cells. In Pofyascomyces (fig. 140)
more than thirty are present, covering a basal area from which numerous asci
bud upwards, so that the condition approximates that in other Ascomy-
cetes. Faull describes the ascogenic cells as binucleate, each containing two

Fig- 139- Stigmatomyces Bacri Peyritsch; a. young
asci ; b. ascus containing four spores ; c. mass of
spores in perithecium ; after Thaxter.

Fig. 140. Polyascomyces Tricho-
phyae Thaxter; after Thaxter.

nuclei which undergo conjugate division whenever an ascus is formed. As
a result the young ascus is binucleate and nuclear fusion followed by three
divisions takes place in the usual way. As a rule four only of the eight
nuclei function; the spores are produced in a manner quite characteristic
of the Ascomycetes generally. In the ascus they are usually disposed more
or less definitely in pairs and the members of a pair are discharged together
from the perithecium and germinate side by side.

In monoecious species one member of a spore pair may frequently
produce a smaller and weaker individual than the other, while in Laboulbenia
inflata the atrophy of one at an early stage of development is a regular
phenomenon. In Stigmatomyces Sarcophagae the smaller individual is uni-
sexual, producing only male cells, while the larger is hermaphrodite (fig. 141 ).

In dioecious species the paired spores are of rather different sizes. The
smaller spore gives rise to a male plant, the larger to a female, so that by
their association at a point of contact with the host a condition essential
for the perpetuation of such species is secured. The cytological changes by
which this segregation of sex is brought about between the members of a
pair should be of great interest and demand investigation.

PYRENOMYCETES

[CH.

There is an obvious suggestion in these phenomena of a transition
between the monoecious and dioecious condition but it is not clear in which
direction the series should be read. It might be
inferred that the male plant had become atro-
phied after the female had acquired spermatial
organs, or on the other hand that, as in many
other groups of plants, a hermaphrodite con-
dition was primitive and segregation a later
development.

Ainorp)winyces Falagriae may be taken as
an example of a dioecious form which shows
also several other peculiarities. The spores are
unique amongst those of Laboulbenialesin being
aseptate (fig. 142). The difference between the
spores producing male and female plants is slight
at first but becomes very apparent on germi-
nation. In each case the spore divides into
three superposed cells (fig. 143 a), in the male the
terminal cell elongates and forms a single male
organ liberatingendogenous sperms. The second
cell maybe regarded as the basal cell of this struc-
ture and the lowest as a unicellular receptacle,
or they may be held to constitute together a
two-celled receptacle. There are no appendages.
In the female the lowest cell, which may
become partly divided, forms the receptacle, the
next above gives rise to the perithecial wall
and the terminal cell to the female organ proper.
The perithecium and its contents are therefore
here terminal, a state of affairs not met with
elsewhere in the group. The terminal cell divides
in the usual way to form an oogonium, a tricho-
phoric cell and a trichogyne ; the latter is short
and branching (fig. 143^). The development
of the perithecium (fig. 144) seems fairly typical
and the asci apparently contain four spores.

!• ig. 141. Stigmatomyces Sarco-
/>hagne Thaxter ; male and her-
maphrodite individuals, x 260;
after Thaxter.

In 1912, Faull published an account of the
cytology of two species of Laboulbenia, L. chaeto-
phora, and L. Gyrinidarum. Both occur on the

same host, and could not be distinguished in the young stages. Both are

parthenogenetic, no male cells being formed.

vl LABOULBENIALES I/9

A trichogyne, trichophoric cell and oogonium are formed in the usual way
(fig. 131). According to Faull nuclear division takes place both in the oogo-
nium, and in the trichophoric cell, and the partition between these two breaks
down so that a long cell containing a row of four nuclei is formed (fig. 145 a).

Fig. 143. Amorphomyces Falagriae Thaxter; male and
fe

Fig. 142. Amorphomyces Fala-
griae Thaxter ; paired spores ;
after Thaxter. female individuals; a. young, b. mature; after Thaxter.

Walls cut off the upper and the lower nucleus, and a
central binucleate cell is left, the lower nucleus of which
is presumably a daughter of the oogonial and the upper
of the trichophoric- nucleus. These divide simultaneously
and a binucleate inferior sterile cell is separated from the
binucleate fertile cell. This in turn divides to form the
ascogenic cells, from which the asci are to develop, and
these and the asci which they produce are therefore
binucleate. The two nuclei in the ascus fuse and their
union is regarded by Faull as the only nuclear fusion
which occurs in this very curious life history. Meiosis
then takes place, followed by the third division. The
upper daughter nuclei of this division degenerate and
around the lower nuclei spores are organized. In each
spore the nucleus divides once and a transverse septum
is formed. Faull describes four chromosomes (fig. 145^)
at every stage but figures an apparently larger number in
the first division in the ascus where the structures repre-
sented are evidently gemini (fig. 145 b}.

tnytes Falagrias
Thaxter ; male and

The Laboulbeniales are subdivided by Thaxter ac-
cording to the method of formation of the male cells,

female individuals,
the latter with peri-
thecium containing
spores ; after Thax-
ter.

12 — 2

PYRENOMYCETES

[CH.

1 80

whether exogenous or endogenous, and in the latter case whether produced
in simple or compound organs. In this way three families, Peyntschiel-
laceae (compound endogenous), Laboulbeniaceae (simple endogenous) and
Ceratomycetaceae (exogenous) are distinguished.

Fig. 14^. Laboulbenia chaetophora (?). a. cell formed by hinucleate
oogonial and trichophoric cells, x 430 ; b. first division in ascus
described by Fauil as the anaphase, xisio; c. nuclear division in
spore, showing four chromosomes, x 2800; after Faull.

Since almost all our knowledge of the group is due to the brilliant work
of Professor Thaxter of Harvard it follows that the North American species
are far better known than those of other localities. Such material as he was
able to obtain from warmer regions proved, however, exceedingly rich in
representatives of the group, and it is probable that further study will show
them to be widely distributed. The known European species are few, and
only two have been identified in Great Britain.

The systematic relations of the Laboulbeniales are not easy to deter-
mine. They are pretty evidently monophyletic, and are highly specialized
along lines dependent on their peculiar habitat. The form and develop-
ment of the ascus is typical of the Ascomycetes, and the Laboulbeniales
clearly belong to that group, though it is difficult to indicate their affinities
within it.

In the Laboulbeniales the young female branch consists of four parts,
the initial cell of the perithecium wall, the oogonium (carpogenic cell of
Thaxter), the trichophoric cell and the trichogyne. These correspond pretty
clearly with the archicarp of other groups. The initial cell of the perithecium
wall constitutes a stalk-cell from which the enveloping hyphae develop.
The trichophoric cell should probably be included as part of the trichogyne,
which in this sense always consists of at least two cells. After fertilization
the oogonium divides to form a row of cells, which are, from below upwards,

v] LABOULBENIALES ,8r

the inferior sterile cell, the secondary inferior sterile cell, the mother-cell1
of the ascogenic cells and the superior sterile cell. The subterminal of these
alone gives rise to asci ; this it does by dividing longitudinally into a definite
number of ascogenic cells from which the asci are budded out.

A multicellular trichogyne is not uncommon among Ascomycetes, and
the division of the oogonium after fertilization into a row of cells is a
well-known phenomenon occurring among Plectascales, Erysiphales, and
Discomycetes. In most cases several cells of the septate oogonium give
rise to ascogenous hyphae, but in the Erysiphales only the subterminal
cell of the row does so. In Erysiphe this cell, which always contains at
least two nuclei, gives rise to several asci and differs from the sub-
terminal cell of the Laboulbeniales chiefly in the fact that the asci are
produced from short outgrowths instead of, as in Stigmatomyces and its
allies, from daughter cells formed by longitudinal division. In this character
then, the Laboulbeniales would appear most nearly to approach the Erysi-
phaceae, which they also resemble in the formation of the sheath from the
stalk cell of the oogonium, but they differ from them in possessing a tricho-
gyne, an organ not known in that group, where the antheridium comes into
direct contact with the oogonium.

The Laboulbeniales and Erysiphaceae have also in common the uni-
nucleate character of their vegetative cells.

In the structure of their ascocarp, opening as it does by a narrow aperture,
the Laboulbeniales approach most closely to the other Pyrenomycetes.

The male element in the Laboulbeniales is a non-motile, uninucleate
structure which may be budded off externally from the parent cell, or
extruded from it as a naked mass of protoplasm.

Amongst the Fungi spermatia occur in the Pyrenomycetes and Lichens
and also characterize the Uredinales, but in all these cases they are budded
off externally as walled structures. The spermatium both in the Red Algae
and in the Fungi has been homologized with a reduced antheridium, and,
as has already been pointed out, the exogenous male element no doubt
bears the same significance among the Laboulbeniales. We have no satis-
factory indication as to the relative primitiveness of the endogenous and
the exogenous condition, but it may be noted that exogenous forms only
are known among Fungi other than Laboulbeniales. The endogenous organ
may be derived from the branch which cuts off exogenous, walled spermatia,
or it may represent quite a different response to the need for non-motile
male elements, the parent cell being the homologue of the antheridium and
the fertilizing element that of a spermatozoid.

These various characters, approximating to those of sometimes one,

1 This cell is described by Thaxter as the ascogonium. The word has acquired a somewhat
different sense in other Ascomycetes.

i82 PYRENOMYCETES [CH. y

sometimes another group of Ascomycetes, seem on the whole to indicate no
very close relationship, but suggest rather that the Laboulbeniales were
derived from an ancestral form, already definitely ascomycetous but not
otherwise highly specialized, and that they have undergone elaborate and
characteristic modifications after branching off from the main line. Their
nearest affinities are with the Erysiphales and Pyrenomycetes.

The resemblances between the Laboulbeniales and the Red Algae have
been regarded as significant in connection with the hypothetical relationship
of the higher Fungi to that group.

LABOULBENIALES: BIBLIOGRAPHY

1896 THAXTER, R. Contribution towards a Monograph of the Laboulbeniaceae, Pt. I.

Mem. Am. Acad. Arts and Sciences, xii, p. 195.
1908 BIFFEN, R. H. First Record of Two Species of Laboulbeniaceae for Britain. Trans.

Brit. Myc. Soc. iii, p. 83.
1908 THAXTER, R. Contribution towards a Monograph of the Laboulbeniaceae, Pt. II.

Mem. Am. Acad. Arts and Sciences, xiii, p. 219.

1911 FAULL, J. H. The Cytology of the Laboulbeniales. Ann. Bot. xxv, p. 649.

1912 FAULL, J. H. The Cytology of Laboulbenia chaetophora and L. Gyrinidarufn.
Ann. Bot. xxvi, p. 325.

CHAPTER VI
BASIDIOMYCETES

THE Basidiomycetes include over 13,000 species possessing a well-developed
mycelium, which, among the higher forms, builds up an elaborate fruit-body
such as may be observed in the toadstools, bracket fungi and puff balls.

They are characterized by the fact that their principal spores, the basidio-
spores, are borne externally on the mother-cell or basidium. The young
basidium contains two nuclei ; these fuse, and the fusion nucleus divides twice,
providing the nuclei of the four spores ; each spore is formed at the end of
a stalk or sterigma through which the nucleus passes to enter the developing
spore. The two divisions in the basidium constitute a meiotic phase. In the
Autobasidiomycetes the basidium is without septa, and the spores, except
where some fail to develop, are regularly four in number for each basidium.
In the Protobasidiomycetes the basidium is divided into four cells, each of
which gives rise to a single spore ; the walls are transverse in the Uredinales
and Auriculariales, longitudinal or oblique in the Tremellales. In the Hemi-
basidiomycetes (Ustilaginales) septa may or may not be present in the
basidium, but the fusion nucleus divides more than twice, and more than
four spores are produced.

In Puccinia, Phragmidium and other Uredinales, and in Sirobasidinvt
and its allies, the basidia are developed in chains, in other cases they are
borne singly. In the Ustilaginales and in the majority of the Uredinales the
nucleus and cytoplasm of the basidium are at first enclosed in a thick wall
formingthebrand-sporeorteleutospore cell, which becomes detached, form-
ing an additional means for the distribution of the plant; later the contents
are extruded as a thin-walled promycelium on which the basidiospores are
produced. In other Basidiomycetes the basidia are thin- walled throughout
their development and produce spores while still attached to the mycelium.

The basidiospore is unicellular, round or oval in shape, usually with
a smooth, rather thin wall. Echinulate or warted spores occur in a few
species, and in many families, especially among gill-bearing fungi, dark or
bright-coloured spores are common.

In a considerable number of genera accessory spores are also produced.

Except for the production of their characteristic spores externally on
basidia, the Ustilaginales and Uredinales differ in almost every particular
from the majority of the Basidiomycetes; they are obligate parasites with
a delicate mycelium ramifying in the tissues of the host and they lack the
elaborate stroma characteristic of the Autobasidiomycetes. It has therefore
seemed advisable to deal with them as distinct groups, separating them for
purposes of description from the Basidiomycetes proper.

CHAPTER VII

HEMIBASIDIOMYCETES

USTILAGINALES

THE Ustilaginales, Brand fungi, Smuts or Bunts, constitute a group of some
4O£> obligate parasites on the higher plants, giving rise in the tissues of the
host to characteristic, usually dark-coloured resting-spores, the brand-spores,
teleutospores or chlamydospores. These are developed in considerable
quantities, either singly, in pairs, or in clusters known as spore-balls, and
when ripe break through the host tissue, forming a pustule or sorus. No
distortion of the host is caused during the period of vegetative growth, but
in preparation for the formation of spores very considerable hypertrophy
may be induced.

Ustilago Treubii on the stem of Polygonum chinense in Java causes the

formation of elaborate galls (fig. 146)
provided with vascular tissue and
growing by means of a cambium;
Ustilago Maydis produces whitish
swellings and blisters, often as large
as a fist, on the stem, leaves, roots, and
especially the flowers of Zea Mays;
and Urocystis Vzolae deforms the stems
and leaves of various species of Viola.
Several other smuts develop their
spores in the ovary of the host plant, or
infect the stamens, filling the anthers
with spores and benefiting by the
means of distribution provided for the
pollen. Ustilago antheraruml even
induces development in the staminal
rudiments of the normally pistillate
flowers of Lychnis dioica. The stamens
formed undergo dehiscence as usual
and differ from those of the male
flowers only in the presence of fungal
spores instead of pollen in their anthers.
In all these cases and in most of the Ustilaginales spore- formation is
strictly localized, but in the genus Entyloma and its allies spores may be
formed at almost any point.

1 Ustilago antherarum (DC.) Fr.= Ustilago violacea (Pers.) Fuck.

Fig. 146. Ustilago Treubii Solms ; stem of
Polygonum with " fruit gall," nat. size ; after
Solms Laubach.

CH. VII]

USTILAGINALES

185

The mature brand-spore is uninucleate, and is surrounded by a delicate
endospore and by an epispore which may be smooth or variously sculptured
and usually contains pigment, giving the spore a black, brown, or violet
colour.

On germination the spore gives rise to a short tube, the promycelium or
basidium (fig. 147), into which its contents pass, the nucleus undergoing at

Fig. 147. Ustilago Scabiosae Sow. ; development of basidium ; after Harper.

least two divisions; the basidium in turn produces a number of uninucleate
sporidia or basidiospores. The basidium may be unicellular, giving rise to
a bunch of basidiospores at its apex (Tilletia (fig. 148(7)), or multicellular,
usually four-celled, producing one or
more basidiospores from each cell (Us-
tilago (fig. 147*?)). The nucleus of the
parent cell does not travel into the
basidiospore but divides, sending one
daughter nucleus into the spore, while
the other, remaining in the basidial cell,
may undergo further divisions so that
nuclei are provided for a number of
spores.

Under suitable conditions the basi-
diospores are cut off in considerable
numbers. They may further multiply
by budding, giving rise to conidia, or
a delicate mycelium may be formed
from which conidia are abstricted ( 7V'/-
letid). A supply of conidia is produced by these means in dung decoction
and other nutrient solutions, and no doubt in the damp, manured soil of the

g. 148. Tilletia Tritici (Bjerk) Wint. ; a.
basidium thirty hours after germination of
brand-spore; Rafter conjugation of basidio-
spores ; x 300 ; after Plowright.

1 86

HEMIBASIDIOMYCETES

[CH.

Fig. 149. Ustilago antherarum Fr.; a. and b. conju-
gating basidiospores; c. conjugation between a cell
of the basidium and a basidiospore ; after Harper.

fields. As a rule the conidia are of the same oblong form as the basidio-
spores, but, in the genus Tilletia and some of its allies, they may be stout or
sickle-shaped, whereas the basidiospores are long and narrow.

In Entyloma the brand-spores are capable of germination on the tissues
of the host leaf, where they give rise to hyphae which penetrate through
the stomata and form basidia from which basidiospores are produced.

During their development the cells of the basidium, the basidiospores,

or the conidia budded out from
them, may become united in
pairs (figs. 148 £, 149), by means
of a tube of variable length put
out by one or both participants
and recalling somewhat the con-
jugation tube of the Zygnema-
ceae. The growth of these tubes
is very accurately directed and
appears to depend on a chemo-
tropic stimulus.

In the majority of cases the
nucleus of one of the associated
cells passes down the tube into
the other, but does not fuse with its nucleus (fig. 150). Later both nuclei
divide, and a mycelium of binucleate cells is produced. It is on this
mycelium that the infection of the host depends ; it penetrates the tissues
usually of the seedling, but sometimes of the developing parts of the mature
plant, being in most cases derived from spores which adhered to the seed
coat. These may be destroyed by dipping the seed into hot water or formalin
solution before sowing.

Once in the tissues of the host the binucleate mycelium penetrates in all

directions, ramifying between
the cells of the host and send-
ing haustoria into them. The
internodes of the stem are tra-
versed by long, unbranched
hyphae, but in the nodes branch-
ing is frequent, and here also
the majority of the haustoria are to be found. Where the host is perennial
the mycelium perennates in it, and, if the host dies down during the winter,
remains alive but quiescent in the upper part of the root stock till the growth
of new shoots in spring gives it a fresh opportunity of development.

Conidia have been recorded on the parasitic mycelium of Tuburcinia
and Entyloma but are not of common occurrence at this stage.

Fig. 150. Ustilago Hordei; conjugation; after
Lutman.

vn]

USTILAGINALES

187

In the regions where the formation of brand-spores is to take place, the
mycelium becomes richly branched and often swollen and gelatinous. In
Ustilago and -Sphacelotheca the sporogenous hyphae are divided into a
number of short segments in each of which the contents form a spore
surrounded by an independent membrane. The spores are enclosed at first
within the gelatinous parent walls, but later these disappear so that the
whole mycelium is transformed into a pulverulent mass of spores. In
Tilletia and Entyloma the sporogenous cells are budded off laterally from
the mycelium.

In Tuburcinia a number of richly septate hyphal branches become inter-
woven, forming a knot or spore-ball in which spores to the number of 50
or 100 are developed from within outwards. In Urocystis the spore-ball is
small and the outer cells remain pale or colourless and do not function as
spores though they resemble them in form (fig. 151). In Doassansia the
outer sterile cells are wedge-shaped, and in Sorosporium they form a
gelatinous investment in which their individual boundaries are no longer
recognizable.

after Plowright.

Raw.tscher.

The young spore, like the cells of the mycelium from which it is derived,
contains two nuclei (fig. 1520). These undergo fusion, so that the mature
spore is uninucleate (fig. 152*). The pairing of the nuclei, wh.ch begin
with the association of the basidiospores (or their conidia), is
in the brand-spore.

The minute investigation of the group may be said to have begun m
1807 when Prevost recorded the germination of the spore
Tritid. His work was continued by Berkeley, Tulasne, de Bary, the 1
pupil Fischer von Waldheim, and Brefeld.

Many of these early investigators observed the union of the sporuha m

I88 HEMIBASIDIOMYCETES [CH.

pairs, and, the nuclei not being identified, there was some question as to
whether the process was to be regarded as sexual (de Bary), or as a merely
vegetative phenomenon (Brefeld), like the formation of H-pieces and clamp-
connections.

In 1894 Dangeard described the fusion of nuclei in the young brand-
spore, but it was not till several years later that this was correlated with
the union of the sporidia and the nuclear life-history made clear. The
salient points of this history are (l) nuclear association, (2) nuclear fusion,
(3) germination of the brand-spore, and formation of the basidium. At this
stage the fusion nucleus divides twice or oftener, and uninucleate cells are
formed. This sequence of events indicates that the basidium and its spores
are the starting point of a brief haploid phase, which gives way to the diploid
generation when conjugation takes place.

The life-history of the Ustilaginales would appear to be reduced rather
than primitive, the conjugation of the spores replacing some ordinary
sexual process; but the present state of our knowledge scarcely permits
speculation as to what the earlier alternation of generations may have been.
Tuburcinia primnlicola, which has two parasitic phases, respectively uni-
nucleate and binucleate, suggests closer comparison with the Uredinales
than with any other investigated form.

The Ustilaginales are divided into two groups, distinguished by the
character of the basidium, which is septate in the Ustilaginaceae and con-
tinuous in the Tilletiaceae. The two families are of about equal size, in-
cluding together over 400 species.

The difficulty .at first experienced in classifying these fungi is indicated
by the occurrence of such names as Uredo, Caeoma, Erysiphe, Ascomyces
(= Exoascus), and Lycoperdon among the older synonymy of the species.

Ustilaginaceae

Ustilago, with nearly 200 species, is the most important genus of the
Ustilaginaceae. It is cosmopolitan, occurring on all sorts of host plants, and
is characterized by the fact that its brand-spores are produced singly.

Ustilago Carbo infects species ofAvena, Triticum and Hordeum, the forms
on the different hosts being biologically distinct. Rawitscher observed that
the spores germinate readily in dilute nutritive solutions, forming a three
or four celled basidium from which basidiospores may be abstricted in the
usual way. More commonly, however, the basidia develop without spore-
formation into branched mycelia, between the cells of which conjugation
may take place. Union is accomplished between neighbouring cells of the
same filament by means of short outgrowths, which meet and fuse as in the

VIIJ USTILAGINALES l89

formation of clamp-connections (fig. ,53,), or between um}
through a conjugation tube (fig. ,53^ Where basidiospores are formed
they c0njugate in a similar manner. In every case the nucleus of one
of the paired cells passes over into the other, and the two nuclei lie close
Aether though without fusion. The mycelium throughout the develop,
ment of the host plant consists of binucleate cells and breaks up in spore-
formation into binucleate segments (fig. 152 *). Each spore has

thus two nuclei which fuse during development so that the mature brand-
spore is uninucleate.

In Ustilago Avenae, U. Homeland U. Tritici, sub-species of U. Carbo
Lutman observed that on conjugation some of the cytoplasm of one of the
cells passed over with the nucleus, the empty cell becoming shrivelled
(fig. 154)- In U. A-venae a long fusion tube is frequently formed and both

Fig- 153. Ustilago Carbo: a. formation of basidium; Fig. 154. Ustilago Uordei;

b. conjugation; c. binucleate mycelium; after conjugation; after Lut-

Rawitscher. man.

nuclei, as well as the greater part of the cytoplasm, pass into it, leaving the
conjugating cells comparatively empty. In these varieties of U. Carbo Lutman
found that, after conjugation, the two nuclei lie closely pressed together so
that it was sometimes impossible to differentiate them.

Ustilago Tragopogonis pratensis is parasitic on Tragopogon pratensis, in
the flower heads of which it produces a mass of dark violet spores. In the
young flower buds hyphae are abundant only in the anthers and ovary.
Later they spread to the surface of these organs and form a dense mycelium
of delicate filaments. According to Dangeard and to Rawitscher they divide,
with the onset of spore-formation, into small binucleate cells; nuclear fusion
takes place and the spore acquires a thick reticulate wall. In germination
a three or four celled basidium is produced, each cell containing a single
nucleus, and gives rise to uninucleate basidiospores, which increase by
budding.

190

HEMIBASIDIOMYCETES

[CH.

Federley.in 1903, described specimens of this fungus in which conjugation
is followed not only by the migration of the nucleus of one of the cells

concerned, but also by nuclear
fusion (fig. 155). In view of
the fusion in the young spore
recorded by Dangeard and by
Ravvitscher the details of de-
velopment in this species de-
mand further investigation.

Ustilago Maydis, the smut
of Zea Mays, induces con-

F'g- '5r- Ustilago Tragopogonis pratensis (Pers.) Wint. ; siderable hypertrophy. The
conjugation and nuclear fusion ; after Federley. , r . .

deformations contain a mass

of gelatinous mycelium from which brand-spores are produced. When
mature, the spore mass causes the rupture of the enclosing tissues, and the
spores escape. They germinate to produce basidia from which uninucleatc
basidiospores are abstricted. These in turn multiply by budding, but, accord-
ing to Rawitscher, they never conjugate, nor do they form a definite mycelium
(fig. 156*7). In the infection of the host plant, hyphae are for the first time
developed, and, unlike those of most investigated smuts, consist of uninu-
cleate cells (fig. 156^). This is the case even when the hyphae begin to
break up in preparation for spore-formation. At this stage, however, the ends
of adjacent cells are seen to become swollen where they are in contact, the wall
separating their protoplasm breaks down, the two nuclei come together in

Fig. 156. UMagoMaydis\ a. basidiospores, x54o; b. uninucleate mycelium x42O;
after Ravvitscher.

VII]

USTILAGINALES

191

the swollen region and ultimately fuse (fig. 157). Thus the mature brand-
spore in Ustilago Mayfts, as in other species, contains a single fusion nucleus.
Here, however, the nuclear association which usually takes place in the basidio-
spore is postponed till just before spore-formation. The parasitic mycelium
is therefore haploid instead of diploid as in the majority of cases.

A very similar state of affairs has been described by I. Massee in
Ustilago Vaillantii which attacks various liliaceous plants, hibernating in
the bulb and forming spores in the anthers and ovary. In these organs
the hyphae produce numerous short branches divided by transverse septa
into cuboid cells which, like the cells of the vegetative mycelium, contain
each a single nucleus. Alternate septa disappear by deliquescence so that
binucleate segments are formed in each of which the two nuclei approach one
another and fuse to form the single nucleus of the spore.

Germination in water takes place in the usual way; four-celled basidia
are produced and give rise to basidiospores. Among these there is no evidence
of conjugation.

Ustilago antherarum forms its spores in the stamens of members of the
Caryophyllaceae ; pollen-formation is inhibited, and the anthers become filled
with fungal spores, which are distributed by the mechanism prepared for the
dispersal of the pollen. Germination takes place in dung decoction with
great readiness, the tubes being put out in three or four hours. Harper has
observed that when the spore nucleus undergoes mitosis one of the daughter
nuclei remains in the spore while the other passes into the basidium (fig. 1 580).
Here it divides, the two resultant daughter nuclei are separated by a wall, the
nucleus remote from the spore divides again and a second wall is formed.
Thus the three-celled basidium characteristic of this species is constituted.

Fig. 157. Ustilago Maydis; a. uninucleate cells
before spore-f< .rmation ; b. conjugation; c. young,
uninucleate brand-spores ; after Rawitscher.

Fig. 158. Ustilago antherarum
Fr ; a. germinati"n of brand-
spore; b. conjugation; after
Harper.

I92 HEMIBASIDIOMYCETES [CH.

Basidiospores are budded off in abundance from all three cells, and in turn
give rise to conidia. In the meantime the basidium has separated from its
parent brand-spore, and the spore, after nuclear division, may produce another
basidium, and others in- succession at the same spot, so that free basidia
accumulate in the culture. If cultures in nutrient solution are allowed to
starve, association now takes place between basidial cells, basidiospores or
conidia by means of conjugating tubes (fig. 1 58 £). The paired cells increase
markedly in volume, but no interchange of cytoplasm takes place and the
nuclei remain in their respective cells without visible change. Harper observed
that when fresh beerwort was supplied to his cultures at this stage the produc-
tion of conidia began again. They are produced from one or both of the con-
jugating cells, but only a single nucleus is concerned in the development of
each conidium, the other remains quiescent and the conidia are uninucleate.
In a host plant, the name of which is not recorded, Werth and Ludwig
failed to find binucleate elements, the youngest cells in which they could iden-
tify the nuclei being uninucleate (fig. I59«). They infer that in this species

nuclear association fails to take

place> and "° binucleate stage
exists. This hypothesis accords

we^ witn Harper's observations,
on the saprophytic phase which

•r 'g- ' 59 Ustilago antherantm P r. ; a. young brand-
spores b older brand-spores; c. basidia ; d. basidio- he Studied ill material grown On
spores ; after Werth and Ludwig T i • IL r\ i LI f. j

Lychnis alba. On the other hand,

a binucleate stage was identified by him in the sporogenous cells of U. an-
therarum on Saponaria, and by Dangeard on Lychnis dioica. These facts
suggest the possibility of two or more varieties of U. antherarum on different
hosts and differing in their cytological behaviour; the forms studied by
Dangeard and Harper point to a condition comparable to that of U. Maydis,
while Werth and Ludwig's observations indicate the possibility of a truly
apogamous strain. A complete life-history of this fungus, in material obtained
from a single host, would probably prove of interest.

Another possibly apogamous form is Ustilago levis, a common 'smut
on oats. According to Lutman the basidio-
spores give rise to considerable numbers of
conidia. These are multinucleate if formed in
crowded masses, uninucleate when comparatively
isolated. Germinated conidia found on the epi-

dermis of infected seedlings usually contain two

or three nuclei. The parasitic hyphae are multi-
Fig. .160. Ustilago levis (K. and nucleate and their swollen ends, when Spore-
Is.) Magn.; mycelium with r ,

mu'tii uc'eate and binucleate lormation is about to take place, contain ten to
:Us; after Lutman fifteen nuclei. The final segments however are

VII]

USTILAGINALES

193

uninucleate or binucleate (fig. 160), but it is not known whether fusion takes
place in them. The multinucleate character of the mycelial cells strongly
suggests that no preliminary pairing of the nuclei occurs.

In Ustilago Zeae Lutman also observed a mycelium of multinucleate
cells ; at the time of spore-formation binucleate and uninucleate cells and
finally uninucleate spores 'appear.

Tilletiaceae

The principal genera of the Tilletiaceae are Tilletia, Entyloma, Ttiburcinia,
Urocystis and Doassansia. They have in common the continuous basidium
with a terminal group of spores.

Tilletia Tritici and T.foetens are the stink brands of wheat, so called by
reason of the strong odour of trimethylamin or herring brine given out by the
brand-spores. The two species differ in the character of the epispore which
is smooth in T. foetens, reticulate in T. Tritici. In both cases spores are
produced in the ovaries of the host, all tissues of which, except the outer
coat, are destroyed. The spore masses are garnered with the crop, and
damage all grains with which they are threshed or ground. The infected
flour and contaminated chaff and straw are causes of disease in man and
animals.

On the germination of the brand-spore of T. Tritici the nucleus passes
into the basidium and divides three times so that eight nuclei are formed.
Eight basidiospores are budded off in a
bunch at the apex of the basidium, and
each receives a single nucleus. Frequently
additional nuclear divisions take place
and ten, twelve, or sixteen uninucleate
spores may be produced. When the spores
are fully formed short conjugating tubes
grow out and connect neighbouring
spores, often while these are still attached
to the basidium (fig. 161).

According to Rawitscher the nucleus
of one cell of the pair passes over into
the other and the nuclei lie near one
another but without fusion. After con-
jugation the spores may become septate;
from those which contain two nuclei fila-
ments of binucleate cells grow out, and
may give rise to conidia which are also binucleate. Under suitable conditions
the binucleate hyphae bring about infection by pushing between the cells
of the host seedling. In the cells of the sporogenous mycelium fusion of the

13

Fig

61. Tilletia Tritici (Bjerk) Wint.;
a. basidium thirty hours after germination
of brand-spore; b. conjugation of basidio-
spores ; X3oo; after Plowright.

HEMIBASIDIOMYCETES

[CH.

194

pairs of associated nuclei takes place. Rawitscher observed a quite similar

life-history in T. laevis.

In the parasitic mycelium of Doassansia Alismatis and Entyloma Glancn
(fig. 162) Dangeard observed binucleate cells and the fusion of their nuclei

Fi". 162. Development of brand-spores ; a. Doassansia Alismatis
(Nees) Corn.; b. Entyloma Glaucii Dang.; after Dangeard.

in pairs in preparation for the formation of the brand-spores. The same
stages were recorded by Lutman \nDoassansiadeformans, Entyloma Nympheae
and Urocystis A nemones (fig. 163).

Fig. 163. Urocystis Anemones (Pers.) Wint. ; mycelium and young spore
ball ; afiei Lutman.

Tuburcinia primulicola infects various species of Primula and gives rise
to conidia as well as to brand-spores during its parasitic stage. Wilson
has shown that the conidia develop in the young flower on a mycelium
of uninucleate cells which apparently persists in the host plant throughout
the winter. When the flower opens the conidia conjugate in pairs, and a
nucleus passes through the connecting tube so that one conidium is empty
and the other binucleate. Germ-tubes with paired nuclei are later produced
and doubtless give rise to the mycelium of binucleate cells which bears the
brand-spores. This mycelium ramifies in the superficial tissue of the placenta
and between the ovules, giving rise to brand-spores in the same flowers in
which the conidia were previously developed. On the germination of the

v"] USTILAGINALES 195

brand-spores, basidia and basidiospores appear, but no conjugation could be
observed. T. primulicola thus resembles the Uredinales in having two
parasitic generations, the one with uninucleate, the other with binucleate
cells. Its hibernating, uninucleate mycelium also recalls the parasitic
mycelium of Ustilago Maydis, or of U. Vaillantii, which consists of uni-
nucleate cells.

USTILAGINALES : BIBLIOGRAPHY

1807 PREVOST, B. Memoire sur la cause immediate de la Carie. Fontanel, Montauban.
1847 BERKELEY, M. J. Propagation of Bunt. Trans. Hort. Soc. London, ii, p. 113.
1847 TULASNE, L. R. and C. Me"moire sur les Ustilaginees comparers aux Uredine'es.
Ann. Sci. Nat. 3 ser. vii, p. 12.

1853 DE BARY, A. Untersuchungen iiber die Brandpilze und die durch sie verursachten
Krankheiten der Pflanzen. Miiller, Berlin.

1854 TULASNE, L. R. and C. Second Mernoire sur les Ure"dinees et Ustilagine'es. Ann.
Sci. Nat. 4 ser. ii, p. 113.

1867 FISCHER von WALDHEIM, A. Sur la structure des spores des Ustilagine'es. Bull.

de la Soc. Imp. des Nat. de Moscou, xl, p. 242.
1883 BREFELD, O. Botanische Untersuchungen iiber Hefenpilze. V, die Brandpilze.

Felix, Leipzig.

1887 ZU SOLMS LAUBACH, H. Ustilago Treu&ii Solms. Ann. dujard. bot.de Buitenzorg, vi,
p. 79.

1888 WARD, H. MARSHALL. The Structure and Life History of Entyloma Ranunculi
(Bonorden). Phil. Trans, clxxviii, p. 173.

1889 PLOWRIGHT, C. B. A Monograph of the British Uredineae and Ustilagineae.
Kegan Paul, Trench & Co., London.

1894 DANGEARD, P. A. Recherches histologiques sur la famille des Ustilagine'es.

Le Botaniste, iii, p. 240.
1899 HARPER, R. A. Nuclear Phenomena in certain stages in the development of the

Smuts. Trans. Wisconsin Acad. Sci. Arts and Letters, xii, p. 475.
1904 FEDERLEY, H. Die Copulation der Conidien bei Ustilago Tragopogi pratensis

Pers. Ofversigt af Finska Vetensk. Soc. Forhandlingar, Ixvi, No. 2, p. i.

1910 MCALPINE, D. The Smuts of Australia. J. Kemp, Melbourne.

1911 LUTMAN, B. S. Some Contributions to the Life-history and Cytology of the Smuts.
Trans. Wisconsin Acad. Sci. Arts and Letters, xvi, pt. ill, p. 1911.

1912 RAWITSCHER, F. Beitrage zur Kenntniss der Ustilagineen. Zeitschr. f. Bot. iv,
P- 673.

1912 WERTH, E. and LUDWIG, K. Zur Sporenbildung bei Rost und Brandpilzen. Ber. d.

deutsch. Bot. Ges. xxx, p. 522.
1914 MASSEE, I. Observations on the Life-history of Ustilago Vaillantii, Tul. Journ.

Econ. Biol. ix, p. 7.

1914 RAWITSCHER, F. Zur Sexualitat der Brandpilze Tilletia tritici. Ber. d. deutsch.
Bot. Ges. xxxii, p. 310.

1915 WILSON, M. The Life-History and Cytology of Tubiirrinia primulicola Rostrup.
B. A. Report, Sect. K. 1915.

13—2

CHAPTER VIII

PROTOBASIDIOMYCETES

UREDINALES

THE rust-fungi, members of the group Uredineae, Uredinales or Aecidio-
mycetes, including over 1700 species, are without exception obligate parasites
on the stems, on the sporophylls and especially on the leaves of vascular
plants, usually on those of angiosperms or gymnosperms but in one or two
cases of ferns.

The mycelium ramifies in the tissues of the host, sends haustoria into
the cells, and may act as a local stimulant causing more or less marked
hypertrophy and consequent curling or malformation of the infected part.
Starch may be stored by the host, and this is so abundant in the hyper-
trophies caused by the aecidial mycelium of Puccinia Cartels on the nettle,
Urtic a parvifolia, that they are eaten by the Himalayans; one or two other
species are similarly employed. Where the mycelium penetrates into the
perennial tissues of the host it is itself perennial.

Spores and Sori. On the mycelium several kinds of spore are produced,
minute spermatia in spermogonia, aecidiospores in aecidia, uredospores and
teleutospores, sometimes mixed, sometimes separate, in more or less definite
sori. One or more of these types of spore may be lacking, but the teleuto-
spores are almost invariably present, and it is on them that the classification
of the group depends.

Naturally enough it was some time before the various types of spore
were recognized as belonging to the same fungus and the old generic names

Fig. ,64. Germinating telentos^res; a. Phra^nidium bulbosum Schm.; b. Triphragmidium Ulmariae
Lk., c. Coleosponum Soncht Lev.; d. Uromy:es appendiculatus (Fabae) Lev.; after Tulasne.

CH" VIIIJ

UREDINALES

197

i 11 me IClCUlOSpt

and Uredo, still survive in our nomenclature

The teleutospores (figs. ,64, ,65, ,66) may be unicellular or they may
be made up of two or more cells forming a compound structure, each ceH of

/^>

Fig 165. Cronartium
asclepiadeum Fr. ; te-
leutospore mass with

basidia and spores; af- Fig. 166. Melampsora betulina Desmaz.; germinating teleutospores:
ter Tulasne. after Tulasne.

which germinates independently. The teleutospore is simple in Uromyces,
Coleosporium, and Melampsora, it is two-celled in Gymnosporangium and
Puccinia, it is built up of three to ten superposed cells in Phragmidium, and
of a larger number in Xenodochus. In Triphragmidium it consists of three
cells laterally placed and in Chrysomyxa and Cronartium the simple teleuto-
spores are so massed together as to simulate compound forms; their real
nature is revealed by their early separation one from another. One-celled
teleutospores occur exceptionally in the two-celled species and are known
as mesospores.

The teleutospores may be massed together and incrusted in the tissues
of the host, or they may be detached readily from their stalks and carried
by the, wind or by other agencies. Further development may take place as
soon as conditions are favourable, or may be delayed till after a resting
period, usually till the spring following development.

In either case the nucleus in each cell ultimately undergoes two successive
divisions, which constitute a meiotic phase> and the daughter nuclei are
separated by transverse walls, so that four uninucleate cells are produced.
The teleutospore-cell thus functions as a tetrasporangium and divides into
four portions, constituting the transversely septate basidium. From each cell
a short, pointed branch or sterigma arises, its end dilates, a basidiospore

198

PROTOBASIDIOMYCETES

[CH.

(sporidium) is formed and receives the nucleus and cytoplasm of the cell
from which it arose.

In Coleosporitun, Ocliropsora, and Chrysospora, nuclear division and
septation take place within the teleutospore wall, and the basidiospores are
budded out from it, so that the teleutospore cell becomes the basidium
directly; in the majority of cases, however, the structure of the teleutospore
is not such as readily to allow further growth, and development takes place
after the extrusion of the contents as a tubular outgrowth, the so-called
promycelium, surrounded only by a delicate membrane (fig. 167). The
nucleus migrates into this structure and here nuclear division takes place,
transverse septa are formed and the basidiospores are produced. But it
must be noted that the nucleus and cytoplasm of the young basidium are
those of the teleutospore cell, whether development takes place within the
original wall or by means of a promycelium.

When the basidiospore germinates its germ-tube penetrates through the
cuticle of the host and forms a mycelium of uninucleate cells bearing
spermogonia and aecidia.

The spermogonium is usually found on the adaxial side of the leaf; it
consists of a group of more or less parallel, unbranched, upwardly directed
hyphae, arising from a small-celled tangle below the epidermis or cuticle of
the host.

In the majority of cases the outer hyphae of each group elongate to form
paraphyses, so that the spermogonium is restricted in extent, and acquires
a flask-shaped or pyriform outline; the paraphyses push up through the
ruptured epidermis of the host to project at a narrow ostiole (fig. 168 b}. In

JR- 167. Gymtwsporangium davariaeforme
ees; germinating teleutosporcs ; x 666.

ig- i68. a. Phragnndium violaceum
Wint., Xj30; b. Gymnosporangium
davanaeforme Rees, x 260 • sper-
mogonia; after Blackman.

VIII]

UREDINALES

199

simpler forms, such as Phragmidium, the spermogonium is indefinite in
extent, and consists of spermatial hyphae arranged beneath the cuticle, which
is perforated in the centre of the mass to form an ostiole. No regular para-
physes are produced but a few spermatial hyphae may elongate and project
as sterile threads (fig. 168 a).

The spermatial hypha is a long, narrow cell with a central elongated
nucleus. It is furnished at its free end with a ring of thickening which may
be concerned with the disjunction of the
spermatium. The development of the
latter begins by the pushing out of a
finger-like projection at the apex of the
parent hypha. When it has attained its
full size the nucleus of the hypha divides
and one of the daughter nuclei enters the
spermatium, which is cut off by a wall
formed just above the thickened ring
(fig. 169).

The mature spermatium is a small
more or less oval cell, enclosed in a very .-..

» rig. 109. Gymnosporangittm davariaeformc
thin wall. The Cytoplasm is finely Kees ; development of spermatia, xu8s;

granular with apparently no reserve afte

material, and the nucleus is of relatively large size. When cultivated in
solution of sugar or honey, spermatia have been induced to undergo a form
of yeast-like budding, and this has been observed under natural conditions
by Robinson in Puccinia Poarum. But, though many attempts have been
made, it has so far proved impossible to bring about the formation of a
mycelium. It seems, therefore, pretty clear that the spermatia are useless
as agents of infection, and they differ also in structure from ordinary asexual
spores. On the other hand the suggestion was long ago made that they
may be male reproductive elements, and this is borne out by their large
nuclei and lack of reserve material, and is by no means invalidated by the
fact that they possess some slight power of germination. Recent investigation
has shown that they are now no longer functional.

As a rule considerable numbers of spermatia are to be found in various
stages of degeneration scattered around the ostioles of the spermogonia.
In some cases the spermatia are aggregated in sticky masses and appear
to attract insects. The presence of sugars in the spermogonial contents has
been demonstrated for species of Uromyces, Puccinia, Endophyllum, and
Gymnosporangium ; in some cases the spermogonia also possess a strong
odour as in Puccinia suaveolens, or occur on bright spots which contrast
with the green of the surrounding tissue. Such spots are usually yellow or
orange, but are white in Uromyces Fabae and reddish-purple in Puccinia

200

PROTOBASIDIOMYCETES

[CH.

rmitis A corresponding discoloration takes place around the young
and there is thus some suggestion that the spermatia, when functional,
vere carried to their destination by insects.

The aecidia occur in groups, usually on the abaxial side of the leaf ; m

them the aecidiospores are
produced in basipetal rows
(fig. 170) alternating with
small, abortive, intercalary
cells, by the disintegration of
which they are set free. They
may be carried to consider-
able distances by the wind,
and there is evidence that
they are sometimes distri-
buted by means of insects or
of snails. The mature aecidio-
spore is usually subglobose
or polygonal in form, it is
enclosed in a thick wall per-
forated by several germ-pores,
and contains red, yellow or
orange pigment, and always
two nuclei. In germination
a hypha is put out which
enters the host plant through
one of the stomata and so
penetrates into the inter-
cellular spaces.

The development of the
aecidium begins by the mass-
ing of hyphae either deep in
the tissues of the host (Gym-
nosporangium clavariaeforme,
Puccinia Poarum (Blackman and Fraser '06), Puccinia Falcariae (Ditt-
schlag ' 10)), or directly below the epidermis (Phragmidium violaceum (Black-

Fig. 170. Uromyces /totf Raben.; aecidium just before
_ the epidermis is broken through, x 310; after Black-
man and Fraser.

Fig. 171

Uromyces Poae Raben. ; young aecidium,
< 370; after Blackman and Fraser.

man '04), Uromyces Poae (Blackman and Fraser '06) (fig. 171),
Claytoniata (Fromme '14)) ; these hyphae give rise to a more or less regular
series of uninucleate cells. These are the fertile cells, but, before developing
further, each, at any rate in the relatively primitive forms (caeomata), may
cut off one or occasionally more terminal sterile cells which ultimately
degenerate. The fertile cells may unite laterally in pairs (fig. 172), so that
binucleate compound cells are formed ; they may similarly pair with the

VIII]

UREDINALES

20 1

cells below them (Fromme '14), or each may receive a second nucleus by
migration from a neighbouring vegetative cell (fig. 173). In each case they
now constitute the basal
cells of the rows of spores
and they proceed at once to
cutoffaecidiospore mother-
cells, each of which in turn
divides to separate a small
intercalary cell below from
the aecidiospore above.

Exceptionally binucle-
ate cells may be observed
before the fertile layer is
d i fferen t iated . In Puccinia
Poarnm nuclear migrations
sometimes take place be-
tween the vegetative cells
at the base of the very
young aecidium. These
cells may grow up, either
at once or after division, to
form fertile cells.

The aecidiospores, then,
are the products of a sexual
process by means of which
two nuclei become associated within the
limits of a single protoplasmic mass, form-
ing the dikaryon or synkaryon of Maire.
The nuclei thus brought together do not
fuse, but undergo simultaneous division
(fig. 174), so that a daughter nucleus from
each passes into every new cell. Conjugate
division is continued when the aecidiospore
germinates and a mycelium of binucleate
cells is produced. The sporophyte of the
rusts is thus normally inaugurated in the
fertile cells of the aecidium.

It is not unusual to find spores and
vegetative cells which contain three or
more nuclei ; in these, as in the binucleate
cells, and, indeed, in multinucleate cells of
many different groups of plants, conjugate

Fig. 172. Phragmidium speaosum Fr. ;

cells; b. fusion of two fertile cells; after Christman.

Fig. 173. Phragmidium violaceum Wint.; migration of
second nucleus into fertile cell of caeoma, x 950 ; after
Blackman.

Fig. 1 74. Melampsora Rostrupi Wagn. ;
paired fertile cells, x uoo; after
Blackman and Fraser.

202

PROTOBASIDIOMYCETES [CH.

division takes place (fig. 175)- The origin of the trinudeate cel1 b^ the
fusion of three fertile cells has been observed, and no doubt it may arise by
the migration of a second vegetative nucleus.

Fig- J75- Pttccinia Poarum Niels.; conjugate division, x 2280;
after Blackman and Fraser.

At the periphery of the aecidium the cells cut off from the basal cells
divide in the usual way, so that two cells corresponding respectively to the
aecidiospore and the intercalary cell are formed from each. The upper
(aecidiospore) cells acquire very thick striated walls, lose their contents
and form a sheath or pseudoperidium about the sporogenous part. The
behaviour of the lower cells varies considerably ; Kurassanow has shown
that in some cases they are quite small, like typical intercalary cells, while
in others they are relatively well developed and form part of the pseudo-
peridium. This is especially the case where the tissue to be broken through
by the developing aecidium is dense or extensive. Centrally the pseudo-
peridium arches over the contents of the aecidium.' In this region it is
derived from the cells first cut off by the central basal cells. These, like the
others, divide transversely, and one of the daughter cells, usually the outer
one, corresponding to the aecidiospore, becomes one of the elements of the
pseudoperidium (Dittschlag, Kurassinovv). When the aecidium reaches
maturity the pseudoperidium pushes through the epidermis of the host and
is then itself ruptured and exposes the ripe spores. It becomes torn and
recurved so that the characteristic cluster-cup is produced (fig. 176). The
pseudoperidium is sometimes much elongated and cylindrical or inflated,
producing the forms known as roestelia (Gymnosporanginni)^ and peri-
dermium (Coleosporium, Cronartium and allied genera), so-called from their
old generic names, or it may be represented only by a few paraphyses or
altogether absent (Phragmidium, Melampsord). The latter forms, to which
the term caeoma is applied, are probably primitive.

In the majority of cases, after the fertile and sterile cells have been
formed and nuclear association has taken place, the basal cells each give
rise to a single chain of spores, but occasionally (Puccinia Falcariae (fig.
177), Endophylltim Semperuivi) they may branch and thus produce two or
more spore-rows. In certain other species the basal cells regularly form
a number of lateral buds or branches and each of these is cut off as a spore

VIII]

UREDINALES

203

Fig. 1 76. Puccinia Graminis Pers. ; a. infected leaf of Berberis vulgaris,
nat. size ; b. group of aecidia, x 5. Uromyces Poae Rabenh. ; c.
infected leaf of Ranunculus jicaria, nat. size ; d. group of aecidia,
X2o; E. J. Welsford del.

mother-cell (fig. 178). The spore mother-cell divides in the usual way,
separating the aecidiospore above from its sister-cell below, but the latter
here forms an elongated stalk instead of an intercalary cell. Each outgrowth
of the basal cell thus produces only a single spore, the mode of formation
of which is exactly similar to that of a uredospore. The fructification has
generally been regarded as a uredosorus and is known as the primary
uredosorus, in reference to its appearance relatively early in the season.

Fig. 177. Puccinia Falcariae; branched
fertile cell of aecidium or primary
uredosorus, x 1200; after Dittschlag.

Fig. 178. Phragmidium Potcnlillae-Canadensts
Diet.; a. conjugation; b. branched fertile
cell ; after Christman.

PROTOBASIDIOMYCETES

FCH
rK.^> i vDrLjiisi^m j- *->*- * ~~

But the fact that these sori are developed on the same mycelium as the
spermooonia, the fact that in their fertile cells nuclear association takes
place and the fact that in the formation of the fertile cell a sterile cell is cut
off, all suggest that the true homology is with the aecidium.

' The mycelium formed by the germination of the aecidiospore grows with
renewed energy. It consists of binucleate cells giving rise to uredospores.
These are borne in groups or uredosori (fig. 179) which may be surrounded

Fig. i-y. a. Phragmidium Ruin Pers.; uredosorus, x 600 ; after Sappin-Trouffy; b. Phragmidium
violaceum Wint.; uredosorus, X48o; after Blackman.

by paraphyses, or in certain genera (Pucciniastrum, Uredinopsis) by a pseudo-
peridium. In the young sorus a regular layer of somewhat rectangular basal
cells is formed, from which the uredospore mother-cells arise. In Coleo-
sporinm, in Chrysomyxa, and in the secondary caeomata of Phragmidium
subcorticium, they are produced in vertical rows like the typical aecidiospore
mother-cells and divide to form uredospores and intercalary cells, but,
in the large majority of cases, they appear as a succession of buds from
different parts of the basal cell. Each bud elongates, its nuclei undergo
conjugate division, a stalk is cut off which grows in length but remains
narrow, while the uredospore enlarges considerably, its contents acquire an
orange or yellow colour, and its wall is variously roughened in most species
by minute projections on the surface. Two or more germ-pores are usually
present and the uredospore, like the cells which give rise to it, is invariably
binucleate ; it produces a binucleate mycelium on which teleutospores or
further crops of uredospores are formed.

Certain species (Puccinia z^;ra;z.y,etc.),occurring under very dry conditions,

VIII]

UREDINALES

205

produce a second type of uredospore with thick walls which are adapted to
survive unfavourable conditions; these are known as amphispores.

Both aecidio- and uredospores germinate readily and without a rest if
fully ripe, but many are shaken off by wind and rain before they reach
maturity and remain incapable of germination. Moreover it is stated that
spores will not ripen properly on leaves that have been removed from the
plant.

Sooner or later the mycelium of binucleate cells gives rise to teleuto-
spores ; these are characteristically grouped together in teleutosori (fig. 1 80),

Fig. 180. a. Phraginidiuin Rzibi Pers. ; teleutosorus, X2.fo; after Sappin-Trouffy; b. Phragmidium
violaceum Wint.; teleutosorus, X24o; after Blackman.

except in the genus Uredinopsis, on ferns, where they are scattered. Like the
uredospores the teleutospores are with or without paraphyses and like them
arise from rectangular basal cells. They appear as narrow binucleate
outgrowths in which one or more divisions take place so that, in the
majority of cases, a stalk is formed below and the simple or compound
teleutospore is produced above (fig. 181). The stalk may increase consider-
ably in length (^Gymnosporangiiun^ Uromyces, Puccinid) or may be very
short or absent (Coleosporium, Melampsora}.

As already stated the young teleutospore cell is binucleate (fig. 182);
when the wall is fully thickened the two nuclei fuse and the spore passes
into the resting state. On the renewal of its development two nuclear
divisions occur and the gametophytic phase is initiated with the production
of the uninucleate basidiospore.

In the Uredinales the fertilization process thus takes place in two stages,
nuclear association being separated by a longer or shorter series of vegetative
cells from nuclear fusion. We have here a difference in degree though not

206

PROTOBASIDIOMYCETES

[CH.

in kind from the normal process. In Pinus sylvestris* the male and female
nuclei lie side by side but do not fuse till their chromosomes become mingled
on the first spindle of the embryo ; in many of the protozoa and in some
other animals a series of conjugate divisions may precede the combination
of the paternal and maternal chromosomes in a single membrane.

Fig. 181. Piifdnia Podophylli S.;
fertile cell of teleutosorus giving
rise to teleutospores ; after Christ-

Fig. 182. Phrasfinidium violaceum Went.; a. teleuto-
spores, x 1080; b. fusion of nuclei in teleutospore,
xis-zo; after Blackman.

It may be hazarded that in the Uredinales the similarity of the physio-
logical history of the nuclei before they become associated is responsible
for a minimum of attraction between them, so that there is no sufficiently
strong impulse towards fusion till meiosis is about to take place ; being,
however, in the same cell, they have no opportunity of dissolving partnership
and the influences which bring about meiosis affect both alike.

A considerable similarity exists in the arrangement of the different
groups of sporogenous cells. The uredo- and teleutosori are clearly com-
parable, both are of indefinite extent, with or without a border of paraphyses,
and both consist of groups of rectangular basal cells from which the spore
mother-cells arise in horizontal series and divide to produce the simple or
compound spore and the stalk-cell. Sometimes, however, the uredospores
are borne in vertical series, one below the other, and the sister-cells of the
spore form short, intercalary cells instead of stalk cells (fig. 183).

This arrangement and that of the so-called primary uredospores link the
uredosorus to the aecidium, suggesting the homology of the stalk and inter-
calary cells. In the simplest aecidia, those of the caeoma type, we have a

1 Blackman, V. H., 1898, Phil. Trans. B. cxc, p. 395

VIII]

UREDINALES

207

Fig. 183. Coleosporium Son-
chi ; uredosorus, x 54.5 ;
alter Holden and Harper.

group of basal cells of indefinite extent, from which the aecidiospore mother-
cells are cut off. The aecidium is, in fact, no more a definite organ than the
uredo- or teleutosorus, and only appears so in the
more elaborate forms because of the modification of
its peripheral cells to form a pseudoperidium. The
important distinction lies not in the general morpho-
logy of the sorus, but in the fact that an association
of two nuclei from different cells takes place in the
basal cell of the aecidium and in the specialization
indicated by the separation of the sterile cells.

In its general structure the spermogonium, con-
sisting as it does of a series of spermatial hyphae
with or without circumjacent paraphyses, is not very
different from the other sori, and, in the simplest
cases, it also is of indefinite extent.

Omission of Spore Forms. In many rusts one
or more spore forms are omitted ; the case where the
so-called primary uredospore is substituted for the typical aecidiospore has
been already described ; these and others in which the characteristic aecidium
or caeoma alone is lacking are distinguished by the prefix brachy.

Hemi- indicates the presence of uredo- and teleutospores without aecidia
or spermogonia.

The suffix opsis is used for forms with aecidia and teleutosori. They
lack uredosori but a few uredospores are sometimes found in the teleutosorus.

Micro- and lepto- forms -have teleutospores with a few occasional
uredospores and sometimes spermogonia. The teleutospores germinate in
the former group only after a period of rest, in the latter upon the same
host plant as soon as they reach maturity.

Species with the full complement of spores are distinguished by the
prefix eu.

As already pointed out, the sporophyte in some of the brachy- species
starts from the fertile cells at the base of the so-called uredosorus, and this
may very probably prove to be true in all cases where the ordinary aecidium
is absent and spores developed like uredospores accompany the spermogonia.

The alternation of generations in the -opsis forms is also normal, for
these are characterized by the omission of typical uredosori the development
of which is related to no significant change in the nuclear life-history.

In micro- and lepto- forms the basidiospore germinates to produce, as in
eu- species, a mycelium of uninucleate cells on which spermogonia may
occasionally be borne. The mycelium becomes binucleate either during
vegetative development (Uromyces Scillarum, Puccinia Adoxae) or below
the young teleutosorus, and the fusion in the teleutospore takes place in

208

PROTOBASIDIOMYCETES

[CH.

the usual way. In the micro- form Puccinia transformans Olive observed
that the binucleate condition was brought about by the fusion in pairs of
cells to form the basal cells from which the teleutospores arose and the
same has been reported by Moreau for Puccinia Buxi and Uromyces Ficariae.
In Puccinia Malvacearum Moreau occasionally found a difference in size
between the fusing cells, and Werth and Ludwig observed the migration
of the nucleus of the smaller cell into the 'larger (fig. 184^).

Below the teleutosorus of Puccinia Podopliylli also, Christman found
nuclear migrations in progress (fig. 184^). Such cases clearly suggest that
here, as in the mycelium below the aecidium of P. Poanim and in the
prothallus of pseudapogamous ferns, the sporophyte is initiated by the
association of two vegetative nuclei. Christman, however, observed that in
certain cases migration took place between cells already binucleate, and he
hence regards migrations in this case, and is inclined to regard all other
migrations in rusts, as due to pathological causes.

^s&-x

S.; migrations at base of teleutosorus; after Christman.

A sporophytic stage of exceptionally brief duration is also found in the
species of Endophyllum and in the form on Rnbns frondosus known as
Kunkelia mtens\ In both cases the characteristic spores are developed in
basipetal chains (fig. 185), and in both the fertile cells which give rise to
them fuse in pairs (Olive '08; Hoffmann 'it), so that the spore mother-cells,
intercalary cells and spores receive two nuclei each. In Endophyllum the
spores are enclosed in a pseudoperidium of barren cells so that the sorus
appears as a typical aecidium, in Kunkelia nitens it is of simpler, indefinite

1 Kunkelia nitens (Schwein.) Arthur = Caeoma nitens Burr.

VIII]

UREDINALES

209

form ; in both cases it is borne in association with spermogonia on a
mycelium of uninucleate cells. But the spore germinates like a teleutospore

Fig. 1 86. Endophyllum Sempervivi Lev.; spores giving rise to
basidia; both after Hoffmann.

(fig. 1 86); its two nuclei fuse (fig. 187), its contents are extruded as a pro-
mycelium, two successive nuclear divisions occur, cross walls appear and four
basidiospores are produced, which, in due course, give rise to a uninucleate
mycelium. The'sporophytic stage thus endures only from the fusion of the
fertile cells until the germination of the spores which they produce.

Incidentally these observations in the case of Kunkelia nitens have
demonstrated that the caeoma of this fungus is not a stage in the life-history
of the teleutospore-producing Puccinia Peckiana on the same host, for the
mycelial cells of P. Peckiana are binucleate and the teleutospores germinate
in the usual way.

The development of an apo-
gamous aecidium has been ob-
served by Moreau in a variety
of Endophyllum Euphorbiae on
Euphorbia sylvatica ; here the
basal cells, aecidiospores and
cells of the pseudoperidium are
uninucleate throughout their
development, the aecidiospore
germinates to form a promy-

.. ,. , r 11 Fur 18? Endofiliyllitm Setnptrvivi Lev.; a. nuclear

cehum Of three or four cells \^\^ tpore% synapsis in fusion nucleus; after

and neither nuclear association Hoffmann.

G:-V.

2io PROTOBASIDIOMYCETES [CH.

nor nuclear fusion takes place at any stage, the diplophase being wholly
omitted.

Heteroecism. In many rusts the gametophytic and sporophytic mycelia
occur on different host plants. Such forms are termed heteroecious in
contrast to the autoecious species where the whole life-history is passed
on a single host. It is not surprising that the different spore forms on such
species were recognized and described some time before it was understood
that they are stages in the life-history of a single fungus. The final proof
of the relationship of the aecidia and spermogonia on the one hand and the
uredo- and teleutosori on the other, was given by de Bary in 1865 for
Puccinia Gmminis, the wheat rust or, as the teleutospore stage was called
by early investigators, the wheat mildew. In this plant the haplophase occurs
on the leaves of the Barberry (Berberis vulgaris) and the diplophase on
wheat, oats, rye and other grasses.

Long, however, before this relationship was demonstrated, and even
before the fungal nature of the disease was known, farmers had begun to
suspect some malign connection between barberry bushes and their wheat
crop, and had observed that dark areas of blackened and injured wheat
were apt to occur in the neighbourhood of such plants. In the State of
Massachusetts an act was passed requiring the inhabitants to extirpate all
barberry bushes before a given date in 1760 and Marshall, of Norfolk,
writing in 1781, says that "it has long been considered as one of the first
of vulgar errors among husbandmen that the barberry plant has a pernicious
quality (or rather a mysterious power) of blighting wheat which grows near
it1." It is hardly to be wondered at that learned persons of the time
repudiated this belief, or, as Marshall says of himself, "very fashionably
laughed at it." It was not till 1797 that Persoon identified the wheat disease
as a fungus and gave it the name it still bears. In 1805 Sir Joseph Banks
called attention to its resemblance to the rust on the barberry, suggesting
that it might be one and the same species, "and the seed transferred from
the barberry to the corn."

In 1816 Schoeler, a Danish schoolmaster, set himself to deal with the
matter experimentally, and applied rusted barberry leaves to some marked
plants of rye ; after a few days these were badly affected while not one
rusty plant could be found elsewhere in the field. His discovery was con-
firmed by the investigations of de Bary, who performed the infection in both
directions and under more critical conditions, and it has since been shown
that a large proportion of the rusts are in fact heteroecious.

It seems pretty evident that the autoecious condition must have been
primitive and it would be of interest to know what factors determined the
adoption of different hosts for the different phases of the life-history.

1 Rural Economy of Norfolk, 2nd ed. vol. ii, p. 19, London, 1795.

vm] UREDINALES 211

Christman and Olive have inferred that the ancestral type of the heteroecious
species was a form with teleutospores only, a lepto- or a micro- form occurring
on the host of the present gametophyte. Other investigators (Tranzschel
'04, Grove '13) who regard the aecidium as an essential constituent of the
primitive rust, have suggested that heteroecism may have arisen in relation
to host plants with a short vegetative period. In such a case there would
hardly be time for the production of the full complement of spores and the
fungus might either shorten its elaborate life-history.giving the micro- or simi-
lar forms ( Uromyces Scillarum on wild hyacinth, Pucciniafusca on anemone),
or some of the spores might become adapted to life on a new host. This
might be the case in particular with the aecidiospores, the development of
which, owing perhaps to the recent fertilization stage, is especially vigorous.
Aecidiospores must fall on hundreds of leaves besides those of the host,
and the germ-tubes in their case enter through the stomata. If then an
aecidiospore germinated and penetrated a satisfactory host it is suggested
that a mycelium might develop and further adaptations might fix the
heteroecious habit. Again it is readily understandable that the Gramineae
and other hosts with similarly refractory cuticles are easily infected by the
germ tubes from the aecidio- and uredospores which pass through the
stomata but not by those of the basidiospores which, in a large majority of
cases, penetrate the walls of the epidermal cells. This fact may be significant
in relation to the return of the parasite to its gametophytic host each spring.

There is reason to believe that some species have an autoecious and a
heteroecious variety and the study of such forms is likely to prove of great
assistance.

Specialization of Parasitism. The parasitism of the rusts shows very
marked specialization so that biological species have arisen, which, though
they may be morphologically indistinguishable, differ from one another in
their power to infect different hosts. Injury to the host may break down
its resistance to attack and may render it liable to infection by a species to
which it is normally immune.

Under favourable conditions rust appears suddenly, and spreads with
great rapidity. Eriksson believed such epidemics to depend on the presence
in the seeds or buds of the host plant of the protoplasm of the rust,
indistinguishably mingled with that of the host, a mixture to which the term
mycoplasm was applied. He considered that the protoplasm of the fungus
remained unaltered till the leaves were formed ; under appropriate conditions
it then separated itself rapidly from that of the host and developed into the
ordinary spore-bearing mycelium. The investigations of Marshall Ward
and others have not substantiated this hypothesis.

Nuclear Division. It would appear, from the work of various observers,
that nuclear division in the Uredinales has undergone a process of simpli-

14—2

212

PROTOBASIDIOMYCETES

[CH.

fication and in some cases it shows but few of the characters of normal
mitosis. In the spermatial hyphae of Gymnosporangium davariaeforme^ for
example, Blackmail has described a condensation of the nucleus to form
a deeply staining body out of which the nucleolus is squeezed. The chromatin
is drawn apart into two apparently homogeneous masses between which
a kinoplasmic thread represents the spindle. A similar process takes place
in the division of the conjugate nuclei in this and other forms, but the spindle
is generally recognizable somewhat earlier, at a time when the chromatin
of each nucleus still forms a single mass. As a rule the spindles of the
conjugate nuclei lie parallel one to another (fig. 188).

Moreau, following Sappin-Trouffy, has recorded two chromosomes or

./...,. chromatin masses formed from
each nucleus in various 'Uredi-
neae. Olive on the other hand
in Triphragmidium Ulmariae
and Uromyces Stirpi has found
a clearly defined spindle and
centrosomes and has succeeded
in recognizing several separate
chromosomes ; a similar state
of affairs has been recorded by
Christman for Phragmidium
spedosum so that it would ap-
pear that the different species
of rusts are at dissimilar levels
in this matter, though a further
study of carefully fixed material
might be undertaken with ad-
vantage.

In all cases, however, the
divisions of the fusion nucleus

Fig. 1 88. Uromyces Poae Raben.; conjugate divisions
in aecidium, x 1330; a'ter Blackmail and Eraser.

Coleosporium Senecionis; mitosis in teleuto-
spores ; after Arnaud.

of the teleutospore are much
more elaborate than those in the
vegetative cells and show some
of the characteristics of a meiotic
In Coleosporium (fig. 189) the fusion nucleus at first possesses a
-marked reticulum of interlacing threads. This undergoes a stage of
^ration in one part of the nuclear area, which no doubt corresponds
> synapsis, and afterwards loosens out, increases in thickness and forms a
The spireme breaks up and its segments are seen to be double
.ghout their length. In the meantime centrosomes and spindle fibres
d and characteristic gemini are recognizable on the- spindle.

VIII]

UREDINALES

213

Moreau describes only two, but Harper and Holden found a larger number,
which became crowded together and more or less fused during the later
stages of the first and also during the second division.

In Gymnosporangium clavariaeforme (fig. 190) the first division is initiated,
as in Coleosporium, by a synaptic phase, after which a spireme is formed and
breaks up into chromosomes.
These pass on to the spindle
but soon lose their individuality
and travel in irregular masses
to the poles.

The development of the
spindle has also been traced in
this species ; its formation is
extra-nuclear and it lies free in
the cytoplasm before coming
into relation with the dividing
nucleus. This type is fairly
common among animals but is
of exceptional occurrence in
plants.

Nuclear Association. The
cytology of the aecidium was
first described in detail in 1904
by Blackman, for Phragmidium
violaceum, a species occurring orf
the bramble. The aecidium here is of the caeoma type, consisting of a group
of fertile cells of indefinite extent and usually bounded at the periphery by
a number of thin-walled paraphyses.

Its formation begins by the massing of hyphae below the epidermis of
the leaf where they form a series of uninucleate cells two or three layers
thick. The cells next the epidermis increase in size and each divides by a
transverse wall parallel to the surface of the leaf, separating an upper sterile
cell from the fertile cell below.
The sterile cells remain cubical
and ultimately disintegrate ; the
fertile cells elongate to form a
more or less regular layer and
paired nuclei appear in them,
first at the centre and later
towards the periphery of the

group (fig. 191). Fig I9f phragmidi,tm molaceum Went.;

The second nucleus in the x 140 ; after Blackman.

clavariaeforme Rees ;
ivision in basidium, x 1460; after Blackman.

PROTOBASIDIOMYCETES

[CH.

fertile cells of Pkragmidium violaceum was shown by Blackman and subse-
quently by Welsford to be derived from one of the smaller cells at the base
of the fertile layer. It is thus a vegetative nucleus; it enters the fertile cell
by migrating through the wall, becoming much drawn out and laterally com-
pressed. It leaves a pore which may be identified after its passage (fig. 192).

i

g. 192. Phragwidium violaceum Went.; caeoma; a. migration of nucleus
from vegetative cell of one hypha to fertile cell of another, x 1040; b. and
r. binucleate cells showing the pore through which the second nucleus has
passed, x 1010; after Welsford.

After entering the fertile cell the second nucleus is at first smaller and
denser than that originally present, but soon becomes
similar to it in size and consistency. The fertile cell
now elongates and in doing so pushes through and
destroys the sterile cell above. The associated nuclei
divide simultaneously, a transverse wall is formed
between the pairs of daughter nuclei cutting off the
aecidiospore mother-cell, and the process is several
times repeated so that a r&w of cells is formed. Each
of these divides again to separate a small, binucleate
intercalary cell below from the binucleate aecidiospore
above.

A similar type of development initiated by the
migration of a vegetative nucleus into the fertile cell,
was observed by Blackman and Eraser in the aecidia
of Pucdnia Poarum and Uromyces Poae (fig. 193). But
in neither of these was the sterile cell satisfactorily
identified.

In such cases it seems reasonably clear that the
entrance of the second nucleus is not a primitive
process but a form of reduced fertilization where a

Fig. 193. Uro'iiyces Poae
Kaben.; nuclear migra-
tionsin young aecidium .
XQSO; after Blackman
and Fraser.

vin] UREDINALES

215

vegetative nucleus has replaced that of the no longer functional male
element. As already shown there is a strong presumption that this male
element was the spermatium and the fertile cell may then be regarded
as an oogonium and the young aecidium as a group or sorus of female
reproductive organs.

In this connection Blackman has suggested a possible origin of the
sterile cell; in Phragmidium violaceum he found it to be occasionally
elongated and pushed up between the cells of the epidermis so that it was
covered only by the cuticle (fig. 194); if in the past it broke through this
also, it would have formed an efficient trichogyne and may well have func-
tioned as such.

In the related species Phragmidium speciosum, Christman, in 1905,
described a similar development of sterile and reproductive cells, but in
this case the fertile cells become inclined one towards another in pairs and,
at the point of contact, the walls dissolve so that the protoplasts come into
relation, at first through a small pore, but later along the greater part of
their length. Binucleate cells are thus formed (fig. 195), conjugate division

Fig 104. Phragmidium violaceum Went. ; Fig. 195. Phragmidium speciosum Kr. ;

caeoma; sterile cell pushing up between fertile cells after conjugation ; aecicho-

epidermal cells of host, x 1300; after spore mother-cell above ; after Chnst-

Blackman. man-

takes place and aecidiospore mother-cells are cut off so that a single row
of aecidiospores is developed from each pair of gametes. Christman regards
the fertile cells as isogametes between which conjugation takes place, and
the sterile cells merely as buffers, of which the function is to assist in the
rupture of the epidermis.

His observations on Phragmidium speciosum were confirmed in 1906 by
Blackman and Eraser for Melampsora Rostrupi on Mercurialis (fig. 174);
these authors pointed out that the fusion of the fertile cells is a reduced
fertilization, strictly comparable to that in Ph. violaceum but achieved by the
union of female cells in pairs instead of by the entrance of a vegetative
nucleus into the female cell. This interpretation is confirmed by the fact

PROTOBASIDIOMYCETES

[CH.

216

that Moreau found both processes (cell-fusion being considerably more
common than migration) in the same caeoma in Phragmidium subcor^uvn.
Since 1905 nuclear association by the fusion of fertile cells in pairs has
been observed in a number of species, and seems, according to our present
knowledge, to be the usual method.

In the primary uredosorus of Triphragmidium Ulmartae and in certain
other species, Olive, in 1908, found arrangements of an intermediate type.
„ Here the cells of the young fructification

form a more or less regular layer and cut
off sterile cells in the usual way. Other
hyphae then push up among them, and
cell fusion and nuclear association take
place (fig. 196). Fusion begins through
a narrow pore which afterwards broadens,
and in many cases the nucleus of the
younger cell migrates into the older one.
The process is thus intermediate between
those first observed by Blackman and
Christman respectively, and the younger
hypha, which does not cut off a sterile cell,
may be regarded as either a vegetative
structure or a gametangium. Olive suggests that the migrations, recorded
by Blackman and by Blackman and Eraser, may be merely early stages of
a completer cell-fusion ; the recent critical work of Welsford, however, nega-
tives this hypothesis, nor would the occurrence of cell-fusion be of much
importance once nuclear association had taken place.

Phylogeny. The interpretation given to the processes which take place
in the aecidium affects the conception of other spore-forms in the Uredinales
and indeed of the phylogeny of the group.

For Christman, the sporophyte arises by the conjugation of undifferen-
tiated or scarcely differentiated isogametes which fuse to form the basal
cells of the aecidium. The spermatia cannot on this interpretation be male
organs, and he regards them as the once-functional asexual spores of the
gametophyte. .The basal cells of the aecidium are homologized with those
of the uredo- and teleutosori, and the fact is emphasized that the basal
cells of the primary uredosorus and sometimes of the teleutosorus also may
arise by cell-fusions similar to those in the aecidium. Christman is inclined
therefore to regard the micro- species, in which the only spore-forms are
teleutospores, or teleutospores and spermatia, as the primitive rusts, and to
see in them a gametophytic mycelium bearing asexual spores (spermatia)
and undifferentiated gametes by the union of which the basal cells of the
teleutosorus are produced. Outgrowths of these cells bear the teleutospores

Fig. 196. Triphragmidium Ulmariae
(Schum.) Link; primary uredosorus;
condition intermediate between migra-
tion and conjugation of fertile cell;
after Olive.

vm] UREDINALES 217

in the germination of which the sporophyte comes to an end and the new
gametophyte is initiated.

Into this simple life-history the uredospore and aecidiospore are held to
be afterwards successively inserted as extensions of the sporophytic phase.

From such a point of view the rust might be related directly to the
Phycomycetes or other simple forms.

Blackman's work, on the other hand, indicates that the spermatium is
an abortive male element, the fertile cells of the aecidium are female organs
which, in the absence of normal fertilization, either fuse in pairs or receive
a vegetative nucleus by migration. In micro- forms the female organs have
disappeared and the abbreviated life-cycle, like that of the pseudapogamous
ferns, shows the sporophyte initiated by an association of two vegetative
nuclei. The eu- forms (or the -opsis forms with teleutospores, aecidiospores
and spermatia), are therefore primitive and the forms with a shorter life-
history are of secondary origin and reduced. The female organ consists of
two cells, the upper of which may have functioned as a trichogyne.

Comparing the two hypotheses it may be noted that Blackman's has
the advantage of correlating all the known facts, since the association of
female nuclei in pairs and of female and vegetative nuclei are both observed
methods of replacing normal fertilization. Christman, on the other hand, is
obliged to ignore the migrations of vegetative nuclei, or to regard them as
pathological. Even for this reason alone it would appear, in the present state
of our knowledge, more probable that the Uredinales are a group in which
the normal sexual process has disappeared, and is replaced by various forms
of pseudapogamy. The young aecidia must then be regarded as groups of
female organs, each consisting of a fertile and a sterile cell, and the sper-
mogonia would appear to be corresponding groups of male organs, the
spermatia or antheridia, with the filaments which bear them.

A third suggestion proposes Endophyllum as a primitive form. The
mycelium of uninucleate cells bears spermatia and cluster-cups. At the
base of the cup fusion of fertile cells in pairs occurs, and spores and inter-
calary cells are produced in chains. The spore germinates by the formation
of a septate basidium on which four basidiospores are produced in E.
EupJwrbiae, but an irregular number, sometimes as many as eight from one
cell, in E. Sempervivi.

In Uromyces Cunninghamianus (on Jasminuiii) Barclay, in 1 89 1 , observed
that the aecidiospore germinates by a tube in which one transverse wall is
formed and the cells give rise to secondary hyphae which produce infection.
On the resultant mycelium, spores similar in arrangement to aecidiospores
are formed; so that here, as in Coleosporium, we have the accessory spores
of the diplophase produced in chains. In the same sorus teleutospores,
which are in this genus unicellular, may also arise. The cytology of this

2iS PROTOBASIDIOMYCETES [CH.

species has not been investigated, but there is an indication of a transition
between Endophyllwn and the eu- forms It is postulated that the cells of
the promycelium of an Endophyllum-Vkz ancestor might have produced
infection directly instead of by means of basidiospores. Nuclear fusion and
meiosis would be postponed till the formation of teleutospores, which would
arise as the typical spores of this new vegetative sporophyte. Later the
teleutospore would become specialized as a resting spore and uredospores
would take on the function of rapid propagation of the plant.

But Endophyllum has a definite cluster-cup, and well-marked peridium,
and is therefore not likely to be primitive, though it may point to an
hypothetical primitive ancestor; a species must rather be sought with a
caeoma from the aecidiospores of which promycelia are produced. Such
a form has been recognized in Kunkelia nitens.

There remain to be considered the various forms of teleutospore.
Presumably the unicellular type is more primitive than the multicellular.
Simple teleutospores occur in Melampsora (where also the aecidiospores
are developed in a caeoma), in Uromyces and in the Coleosporiaceae. In
the last-named family meiosis and septation take place inside the teleuto-
spore wall, but the elaboration of the other spore-forms forbids this group
being regarded as primitive, though the internal basidium may be.

It may be hazarded that the ancestral rust bore spermogonia or groups
of male organs and groups of female organs of the caeoma type, that the
individual male organ was an antheridium or spermatium set free from its
parent hypha, that the female organ consisted of a fertile cell or oogonium
and a sterile cell which was perhaps elongated to form a trichogyne reaching
up to the surface of the host, and that the product of fertilization was
a series of aecidiospores. It may further be suggested that either the
aecidiospore germinated by giving rise at once to a promycelium or that
an alternation of vegetative generations occurred and that the sporophyte
bore simple teleutospores or tetrasporangia inside which septation took
place.

The members of the Uredinales may be arranged in four families :
Germination by a promycelium (except in Chrysopsora]

Teleutospores stalked PUCCINIACEAE.

Teleutospores sessile

arranged in series but separating later CRONARTIACEAE,

one or many celled, loose in tissue of host or

united in a flat layer under the epidermis MELAMPSORACEAE.

Germination without a promyceliHm, formation of basi-
dium internal; teleutospores sessile or with a lateral
Pedlcel COLEOSPORIACEAE.

VIII1 UREDINALES 219

Pucciniaceae*.

The teleutospores of the Pucciniaceae are provided with a stalk which
is often well developed, but is in some cases short or becomes detached at
an early stage (deciduous). The teleutospores are one-celled in Uromyces
and Hemileia, two-celled in Pucdnia and Gymnosporangium ; they are made
up of three cells in Triphragmidium, and in Phragmidium of three or more
cells. Gymnosporangium is further characterized by the long pedicels of the
teleutospores and the fact that they are imbedded in a gelatinous mass.
The uredospores are solitary and the aecidiospores produced either in
caeomata (Triphragmidium, Phragmidium), or in aecidia, which in Gymno-
sporangium are commonly elongated to form flask-shaped or cylindrical
roestelia.

This family probably includes some of the most highly developed
members of the Uredinales, but it includes also several species with caeo-
mata, and one, Chrysopsora Gynoxidis, belonging to a monotypic genus in
Ecuador, in which the two cells of the stalked teleutospore germinate by
internal septation and the protrusion of sterigmata bearing basidiospores
as in Coleosporium.

Cronartiaceae

In the Cronartiaceae the teleutospores are unicellular and sessile, so that
they simulate multicellular spores. In Chrysomyxa they form waxy crusts,
and in Cronartium a cylindrical body. A pseudoperidium is developed
around the aecidiospores.

The genus Endophyllum is sometimes placed here, sometimes a separate
family, the Endophyllaceae, is constituted for it ; it differs from the rest of
the Cronartiaceae and from the majority of the rusts in the fact that its
basidia are developed from spores resembling aecidiospores which arise in
an aecidium-like sorus protected by a pseudoperidium.

Melampsoraceae

The teleutospores are sessile, loose in the tissue of the host in Uredi-
nopsis, in the other members of the family grouped in a flat layer under the
epidermis. In Melampsora and its immediate allies they are unicellular ;
in other genera they are divided either vertically into two cells or by
cruciately arranged septa into four.

The aecidiospores may be surrounded by a pseudoperidium or arranged
in a caeoma ; sometimes a pseudoperidium is present around the uredosorus
also.

1 For Bibliography of this and other families, see the end of the group.

220 PROTOBASIDIOMYCETES [CH.

Coleosporiaceae

The outstanding character of the Coleosporiaceae is the method of
germination of the unicellular teleutospore which undergoes septation directly
and, in Coleosporium and Ochropsora, without the protrusion of a pro-
mycelium ; in Zaghouania the contents of the teleutospore divide within
the teleutospore-wall to form four cells, but emerge before the basidiospores
appear.

The aecidia are cup-shaped in Ochropsora, but in Coleosporium and
Zaghouania they are of the peridermium type with a cylindrical, more
or less inflated peridium ; this elaborate type of aecidial sorus makes it
impossible to regard the family as primitive though' it may perhaps have
branched off early from the line leading to the commoner type of rust.

UREDINALES : BIBLIOGRAPHY

1889 PLOWRIGHT, C. B. A Monograph of the British Uredineae and Ustilagineae.

Kegan Paul, Trench & Co., London.

1891 BARCLAY, A. On the Life history of a remarkable Uredine on Jasmi num grandi-
florum. Trans. Linn. Soc. Bot. ii, p. 141.

1895 POIRAULT, G. and RACIBORSKI, M. Sur les noyaux des Uredinees. Journ. de Bot.
ix, pp. 318 and 381.

1896 SAPPIN-TROUFFY, P. Recherches histologiques sur la famille des Uredine'es.
Le Botaniste, v, p. 59.

1902 DUMEE, P. and MAIRE, R. Remarques sur le Zaghouania Phyllyreae, Pat. Bull.
Soc. Myc. France, xviii, p. 17.

1903 HOLDEN, R. J, and HARPER, R. A. Nuclear Divisions and Nuclear Fusion in
Coleosporium Sonchi-arvensis, Lev. Trans. Wisconsin Acad. Sci., Arts and Letters,
xiv, pt. i, p. 63.

1904 BLACKMAN, V. H. On the Fertilization, Alternation of Generations and general
Cytology of the Uredineae. Ann. Bot. xviii, p. 323.

1904 TRANZSCHEL, W. Ueber die Moglichkeit die Biologic wertwechselnder Rostpilze
auf Grund morphologischer Merkmale vorauszusehen. Arb. Kais. Petersburg
Naturf. Gesell. xxxv, p. i.

1905 CHRISTMAN, A. H. Sexual Reproduction in the Rusts. Bot. Gaz. xxxix, p. 267.
1905 ERIKSSON, J. On the Vegetative Life of some Uredineae. Ann. Bot. xix, p. 53.

1905 WARD, H. MARSHALL. Recent Researches on the Parasitism of Fungi. Ann. Bot.
xix, p. i.

1906 BLACKMAN, V. H. and FRASER, H. C. I. Further Studies on the Sexuality of the
Uredineae. Ann. Bot. xx, p. 35.

1906 MCALPINE, D. The Rusts of Australia. J. Kemp, Melbourne. •

1907 CHRISTMAN, A. H. The Nature and Development of the Primary Uredospore.
Irans. Wisconsin Acad. Sci. xv, p. 517.

190? CHRISTMAN, A. H. Alternation of Generations and the Morphology of the Spore-
forms in Rusts. Bot. Gaz. xliv, p. 81.

1908 OLIVF E. W Sexual Cell-Fusions and Vegetative Nuclear Divisions in the Rusts.
Ann. Bot. xxu, p. 331.

1910 DITTSCHLAG E. Zur Kenntnis der Kernverhaltnisse von Puccinia Falcariae.
Centralbl. f. Bakt. Abt. ii, B. 28.

vm] UREDINALES 221

igi I HOFFMANN, A. W. H. Zur Entwickelungsgeschichte von Endophyllum Setnpervivi.

Centralbl. fiir Bakt. Parasit. Infect, xxxii, p. 137.

1911 MAIRE, R. La Biologic des Ure*dinales. Prog. Rei Bot. iv, p. 109.
1911 OLIVE, E. W. Origin of Heteroecism in Rusts. Phytopathology i, p. 139.

191 1 SHARP, L. W. Nuclear Phenomena in Puccinia Podophylli. Bot. Gaz. li, p. 463.

1912 FROMME, F. D. Sexual Fusions and Spore Development of the Flax Rust. Bull.
Torrey Bot. Club, xxxix, p. 113.

1912 RAMSBOTTOM, J. Some Notes on the History of the Classification of the Uredinales
with full list of British Uredinales. Brit. Myc. Soc. IV, p. 77.

1912 WERTH, E. and LUDWIG, K. Zur Sporenbildung bei Rost- und Brandpilzen. Ber.
deutsch. Bot. Ges. xxx, p. 522.

1913 ARNAUD, G. La Mitose chez Capnodium meridionale et chez Coleosporium Sene-
cionis. Bull. Soc. Myc. de France, xxix, p. 345.

1913 GROVE, W. B. The British Rust Fungi. Camb. Univ. Press.

1913 GROVE, W. B. The Evolution of the Higher Uredineae. New Phyt. xii, p. 89.

1914 FROMME, F. D. The Morphology and Cytology of the Aecidium Cup. Bot. Gaz.
Iviii, p. I.

1914 KUNKEL, L. O. Nuclear Behaviour in the promycelia of Caeoma nitens, Burrill,

and Puccinia Peckiana Howe. Am. Journ. Bot. i, p. 37.
1914 KURASSANOW, L. Uber die Peridienentwicklung im Aecidium. Ber. deutsch. Bot.

Ges. xxxii, p. 317.

1914 MOREAU, Mme F. Les phenomenes de la sexualite chez les Uredinees. Le Botaniste,
xiii, p. 145.

1915 WELSFORD, E. J. Nuclear Migrations in Phragmidium viohiceum. Ann. Bot. xxix,

P- 293-

1916 KUNKEL, L. O. Further Studies on the orange rusts of Rubus in the United States.
Bull. Torrey Bot. Club, xliii, p. 559.

1917 ARTHUR, J. C. Orange Rusts of Rubus. Bot. Gaz. Ixiii, p. 501.

GENERAL BIBLIOGRAPHY

1861 TULASNE, R. C. and L. Fungi Hypogaei. Klincksieck, Paris.

1861-5 TULASNE, R. C. and L. Selecta Fungorum Carpologia. Imperial. Typograph.,

Paris.

1882-1913 SACCARDO, P. A. Sylloge Fungorum. Published by the author. Padua.
1884 DE BARY, A. Comparative Morphology and Biology of the Fungi, Mycetozoa and

Bacteria. Eng. Trans. 1887. Clarendon Press, Oxford.
1884-97 RABENHORST, L. Kryptogamen Flora. Pilze, by G. WINTER and E. FISCHER.

Ed. Krummer, Leipzig.
1887 PHILLIPS, W. A Manual of British Discomycetes. Kegan Paul, Trench & Co.,

London.

1892 VON TAVEL, F. Vergleichende Morphologic der Pilze. Fischer, Jena.
1892-5 MASSEE, G. British Fungus Flora. Bell & Sons, London.
1895 VON TUBEUF, K. F. Diseases of Plants. Eng. Trans., 1897. Longmans, Green

& Co., London.
1897-1900 ENGLER, A. and PRANTL, K. Die natiirlichen Pflanzenfamilien. Fungi, by

J. SCHROTER, G. LINDAU, E. FISCHER and P. DIETEL. Engelmann, Leipzig.
1904-11 BOUDIER, E. Icones Mycologicae. Klincksieck, Paris.
1906 MASSEE, G. A Text Book of Fungi. Duckworth & Co., London.
1909 BULLER, A. H. R. Researches on Fungi. Longmans, Green & Co., London.

1909 SWANTON, E. W. Fungi and How to Know Them. Methuen, London.

1910 DUGGAR, B. M. Fungous Diseases of Plants. Ginn & Co., New York.
1913 MASSEE, G. Mildews, Rusts and Smuts. Dulau & Co., London.

1913 STEVENS, F. L. The Fungi which cause Plant Disease. Macmillan Co., New York.
1918 BUTLER, E. J. Fungi and the Diseases of Plants. Thacker, Spink & Co., Calcutta.

1918 HARSHBKRGER, J. W. A Textbook of Mycology and Plant Pathology. J. & A.
Churchill, London.

1919 HILEY, W. E. The Fungal Diseases of the Common Larch. Clarendon Press,
Oxford.

INDEX

A glossary has not been prepared for this, volume, but the page on which the definition of a technical
term will be found is shown in the index in clarendon type, and the same method is used for indicating
the principal reference to a family or genus.

Abietineae, 18

Abutilon, 11

Accessory spore, 4 ; and see Conidium

Achorion Schoenleinii, 4

Adpressorium, 13, 79

Aecidiomycetes, see Uredinales

Aecidiospore, 23, 200, 201, 217, 219

Aecidium, 200, 206, 214, 220

Aerotropism, 30

Agaricaceae, 33

Agaricus catnpestris, 3 1

Alcoholic fermentation, 10 et sqq., 62

Alternation of generations, 39, 188, 218

Althea, 22

Amanita crenulata, 31, 32

A . phalloides, 31
Amauroascus verrucosus, 67
American vine mildew, 81
Amorphomyces Falagriae, 178, 179 (Figs. 142-

H4)

Amphisphaeriaceae, 154, 159
Amphispores, 205
Anemone nemorosa, 21

A. nodosa, 123

Antheridium, 2, 39, 50, 52, 53, 54, 66, 67, 69,
7X> 73' 74> 85, 97, 108, 174, 181, 217, 218
" Antherozoid," 174
Anthocercis viscosa, 21
Aphanoascus cinnabarinus, 69 (Fig. 28)
Apogamy, 151, 152, 209; and see Pseudapogamy
Apothecium, 38, 95, 96, 101, 123, 124, 128. 129,

133

Appendages, 158, 171, 175
Arbutus, 1 8
Archicarp, 39, 40, 48, 50, 51, 69, 73, 98, 99,

108, in, 116, 117, 118, 119, 120, 140, 141,

144, 155, 157, 169, 170
Archimycetes, 2, 5, 15
Armillaria mellea, i, 18, 19
Arnaud, G., 212, 221
Arthur, J. C., 221
Ascobolaceae, 8, 9, 51, 52, 100, 116 et sqq.',

bibliography, 122

Ascobolus carbonarius, 27, 51, 118 (Fig. 79)
A. furfuraceus, 9, 30, 34, 44 (Fig. 13), 48, 49,

51, 99 (Fig. 58), 116 (Fig. 75), 117 (Fig.

76)

A.glaber, 9, 117

A. immersus, 9, 21, 30, 46, 118 (Fig. 78)
A. perplexans, 9
A. Winteri, 10, 117 (Fig. 77)
Ascocarp, 38, 39, 50, 55, 66, 71, 77, 95, no,

113, 119, 120, 121, 123, 131, 135, 138, 139,

142, 159

Ascocorticiaceae, 93
Ascocorticium, 93

Ascodesmis, 50, 51, 52, 54, 98, 101

A. ttigricans, 34, 98 (Fig. 56), 101 (Fig. 59),

102 (Fig. 60)
Ascogenic cells, 176
Ascogenous hyphae, 39, 40, 43, 46, 47, 53, 56,

66, 69, 75, 86, 88, 98, 106, 113, n4, 117
Ascogonium, 39; and see oogonium
Ascomycetes, 5, 6, 7, 8, 30, 34 et sqq.
Ascophanus carneus, 9, 21, 46, 47 (Fig. 16), 48,

51, 1x8, 1 19 (Figs. 80, 81)
A. equinus, 21

A. ochraceus, \ 20
Ascophore, 38, 129
Ascospore, 3, 34, 61, 64, 79, 149

Ascus, 3, 34, 35 et seq., \\ et seq., 58 et seq., 89,
92,93, 95, 115, 177

Aspergillaceae, 52, 54, 55, 57, 68 et sqq. ; biblio-
graphy, 75

Aspergillus herbariorum (see Eurotium herba-
rforum)

Association, chromosome, 45, 113; nuclear, 46,
205, 206, 213, 214, 216

Atkinson, G. F., 50, 152

Auriculariales, 6, 183

Autobasidiomycetes, 6, 183

Autoecism, 22, 210

Bacterium vermiforme, 1 1
Baden, M. L., 9, 10, 13
Balls, W. L., 28, 29, 33
Balsamia platyspora, \ 36

B. vulgaris, 136 (Figs. 95, 96)
Banks, Sir Joseph, 210

Barberry, 210; and see Berberis vulgaris
Barclay, A., 217, 220
Barker, B. T. P., 64, 65, 76, 121, 122
Bary, A. de, 9, 13, 19, 21, 23, 26, 27, 33, 37,
40, 50, 70, 75, 84, 102, 103, 107, 187, 188,

195, 210, 222

Basidiomycetes, 5, 6, 7, 8, 183

Basidiospore, 3, 183, 186, 190, 192, 193, 197. «°7'

209

Basidium, 3, 183, 185, 189, 193, 213
Bayliss, VV. M., 66
Berberis vulgaris, 203 (Fig. 176), 210
Berkeley, M. J., 126, 127, 149, 152, 187, 195
Bernard, N., 17, 18, 20
Bertero, 126
Betulaalba, 21
Betulaceae, 18
Bezssonoff, M. N., 86, 90
Biffen, R. II., n, 25, 27, i8a
Biological species, 22 et syq., 161
Biseriate spores, 36, 37 (frig. 4)
Blackman, V. H., 198. 199, 201, 204, 206, an,

213, 214, 215. ll6- "7i "°

224

INDEX

Blackman and Fraser, H. C. I., 48,84, 85, 89, 1 1 1 ,

II2,Il6, 200, 201. 202, 1 1 2, 2 1 4, 215,210,220

and Welsford, E. J., 13, 20, 48, 141, 147, '

148, 152

Blakeslee, A. F., 27
Bletilla, 17

B. hyacinthina, 17
Blight, see Erysiphaceae
Boleti, 19
Bolrytis, 14, 31

B. cinerea, 13, 14
Boudier, E., 113, 130, 222
Boudiera hypoborea -(see Ascodesmis nigricans)
Boulanger, E., 138
Bower, F. O., 20
Brachymeiosis, 44
Brand fungi ; see Ustilaginales
Brand-spore, 183, 184, 187, 191, 192, 194
Brefeld, O., 30, 33, 40, 50, 72, 75, 120, 187,

188, 195

Brierley, W. B., 77, 162, 163
Bromelia^ 39
Bromus adoensis, 24

B. arduennensis, 24

B. commutatus, 24, 25

B, " hordeaceus" 24, 25

/>. inlerntpliis, 24

B. mollis, 24, 25

B. racemosus, 24, 25

B. secalinus, 24

B. vehttinus, 24
Brooks, F. T., 164

Brooks, W. E. St J., see Fraser and Brooks

Brown, W., 13, 20

Brown, W. H., 105, 107, 116 132

Bryophyta, 161

Buchanan, J., 127

Bucholtz, F., 97, 137, 138

Budding, 5, 60, 62, 93, 185, 199

Builliard, P., 40

Bulgaria poly morpha, 35, 125

Buller, A. H. R., 12, 13, 31, 32, 33, 222

Bunts, see Ustilaginales

Burgeff, H., 17, 20

Butler, E. J., 222

Caeoma, 201, 202, 213, 214, 215
Caeoma nit ens (see Kunkelia nitens)
" Californian bees," 1 1
Calluna vulgarh, 16
Calosphaeria, 165

C. princefs, 165
Capnodium, 12

Carruthers, D., 43, 44, 48, 130
Caryophyllaceae, 21, 191
Cattleyeae, 17

Cavara, F., 101

Cavers, F., 20

Celidiaceae, 100, 124

Celidiutn varians, 125

Cell-fusion, 215, 216

Cenangiaceae, loo, 124

Central body, 88

Ceratomyces rostratus, 173 (Fig. 134)

Ceratomycetaceae, 180

Ceratostoma brevirostre (see Mclanospora Zobelii]

Ceratostomataceae, 154., 159

Cercospora, 163

Chaetomiaceae, 154, 155 et set}.
Chaetomium chlortmtrn, 155

C.fimele, 54, 155

C. Kuntzeamtm 35 (Fig. 2), J-55 (Fig. 113),
1 56 (Fig. 114)

C. pannosuin Wallr., 155 (Fig. 112)

C. spirale, 140, 155

Chambers, H. S., see Fraser and Chambers
Chemotropism, I4, 27, 186
Cherry-leaf-scorch, 163
Chlamydococctis pluvialis, 3 1
Chlamydospore, 4, 57
Choironiyces maeandriformis, 137
Christnian, A. H., 201, 203, 206, 208, 210, 212,

215, 2l6, 217, 220

Chromatin, 44, 4.5, 94
Chromosome association, 45, 113
Chromosomes, 4.3, 44 (Fig. 13), 89, 106, 109,
112, 113, 114 (Fig. 71), 115 (Figs. 72-4),
117, 130, 164, 179, 180, 212
Chrysomyxa, 204, 219

C. Ledi, 23

C. Rhododendri, 23
Chrysopsora, 198, 218

C. Gynoxidis, 219
Chytridium vorax, 31
Cidaris, 129
Clannp-connections, i
Clark, J. F., 27, 33
Classification of Fungi, 5

Claussen, P., 43, 46,98, 101, 102, 104, 105, 107
Clavate paraphyses, 38
Claviceps purpiirea, 10, 21, 151
Coenogamete, 2
Coleophora laxicella, 123
Coleoptera, 171
Coleosporiaceae, 218, 220
Coleosporium, 198, 204, 212, 220

C. Senecionis, 212 (Fig. 189)

C. Sonchi, 196 (Fig. 164), 207 (Fig. 183)

C. Sonchi-arvensis (see C. Sonchi)
Coleroa Potenlillae, 158 (Fig. 118)
Collema pulposum, 51, 52
Colletotrichum Lindeniuthianum, 14
Compsomyces verticillatus, 176 (Fig. 137)
Conidiophores, 4, 70, 72, 80
Conidium, 4, 15, 24, 57, 58, 60 (Fig. 21), 70, 72
(F'g- 3J)> 74, 79> 80, 90, 98, 118, 125, 133,
145, 14.9, 151, 161, 166, 170, 185, 186, 194
Conjugate division, 46, 177, 186, 201, 202, 204,

206

Conjugation, 59, 63, 186, 189, 190, 194, 208
is, 9

C. curtus, 31

C. niveus, 31

C. stertjuilimts, 9

Coprophilous Fungi, 8, 108, 112, 116, 156
Cordyceps, 10, 149

C. Barnesii, 151 (Fig. 111)

C. capitata, 151

C. militaris^ 150 (Fig. no)

C. ophio^lossoides, 34, 150 (Fig. no), 151

C. stnensis, 149
Coremium, 4
Coreomyces, 1 74
Cortinarius, 19

INDEX

225

Coryne, 125

C. sarcoides, 125
Cronartiaceae, 218, 219
Cronartium, 219

C. asclepiadeuin, 197 (Fig. 165)
Cruciferae, 21

Ctenomyces serratus, 67 (Fig. 27)
Cutting, E. M., 9, 13, 48, 119, 122
Cyathea, 18
Cystopus, 15

C. candidns, 15, 21
Cytology of the Ascomycetes, 40 et sqq.

of the Ustilaginales, 187 et sqq.

of the Uredinales, 201 et sqq.. 211 et sag.

Cyttaria, 125

C. Berteroi, 126
C Darwinii, 125, 127
C. Gunnti, 126 (Fig. 87)
C. Harioti, 127

C. Hookeri, 127

Cyttariaceae, 100, 125 et sqq. ; bibliography, 127
Czapek, F., 7, 12

Dale, E., 13,48,66,67,68, 71, 76

Dangeard, P. A., 41, 44, 55, 60, 61, 67, 68, 69,
73. 74' 75. 76> 86, 87, 89, 94, 101, 105,
107, 117, 120, 121, 122, 140, 152, 156, 157,
I5-S, 188, 189, 192, 194, 195

Dasyscypha, 123

D. clandestina, 2 1

D. Willkotumii, 123 '
Davvson, M., 32, 33, 166, 169, 170
Debaryoinyces globosus, 64
Dehiscence of ascus, 36 et sqq.
Delitschia furjuracea, 35 (Fig. 2)
Dermataceae, 124
Desmotascus, 39
Dey, P. K., 20
Diatrypaceae, 154, 165
Diedicke, H., 23, 26
Dietel, P., 222

Digby, L., see Farmer and Digby
Dikaryon, 46, 201

Dimeromyces Africamts, 174 (Fig. 135)
Diplophase or diploid phase, 3
Dipodascus, 54, 57, 61

D. albiaus, 60 (Fig. 22), 6r (Fig. 23)
Discomycetes, 6, 49, 50, 52, 95 et sqq., 181
Dittschlag, E., 200, 202, 203, 220
Division, conjugate, 202
Doassansia, 187

D. Alismatis, 194 (Fig. 162)

D. deformans, 194
Dodge. B. O., 9, 10, 13, 49, 99, 116, 117, 118,

122

Domaradsky, M., 71, 76
Dothinea vir^nltorum, 153
Dothjdeaceae, 152
Dothideales, 6, 140, 142, 152
Dufrenoy, J. , 20
Duygar, B. M., 222
Dumee, P., and Maire, R., 220
Durand, E. J., 132

Early investigators (Ascomycetes), 40

Ectoparasite, 80

Eidam, E., 40, 58, 61, 67, 68

G.-V.

'Elaphomyces, 19

E. granttlatus, 77

E. variega'us, 77
Elaphomycetaceae, 8, 57, 77
Emericeila erythrospora, 68
Empitsa, 10
Endogenous spore, 3
Endomyces, 35, 53, 58 et sqq.

E. decipitns, 63 (Fig. 24)

E. fibuliger, 59 (Fig. 20), 60 (Fig. 21), 63
(*''g 24)

E. Magmtsii, 59 (Fig. 20), 60, 63 (Fig. 24)

£. Mali, 57

Endomycetaceae, 52, 53, 55, yj et sqq.; biblio-
graphy, Oi
Endophyllnm, 199, 208, 217, 218, 219

E. Enphorbiae, 209, 2 1 7

jE. bempervivi, 202, 208 (Fig. 185), 209 (Figs.

186, 187), 2,7

Endophytic parasite, 15, 79, 80
Endospore, 62
Endotrophic mycorhiza, 16
Engler, A., and Prantl, K., 222
Entomophthorales, 5
Entyloma, 186, 187

E. Glaucii, 194 (Fig. 162)

E. Nyinpheae, 194
Epic hi oe, 149
Epiphytic parasite, 15
Epiplasm, 35, 49
Eremascus, 40

E. albus, 58 (Fig. 1 8)

E.fertilis, 58, 59 (Fig. 19), 63 (Fig. 24)
Ericaceae, 18

Eriksson, J., 23, 26, 211, 220
Ennella apala, 21
Erysiphaceae, 15, 23, 52, 53, 55, 78, wet sqq.,

181 ; bibliography, 89
Erysiphales, 6, 56, 78 et sqq., 181
Erysiphe Cichoracearuw, 87

E. communh (see E. 1'olygoni)

E. Graminis, 24, 25, 79, 82

E. Alartii (see E. Polygoni)

E. Polygoni, 42, 82 (Fig. 39), 86 (Fig. 43), 87

E. taurica, 80

E. tortilis, 83 (Fig. 40)
Eitglena viridis, 31
Euphorbia sylvattca, 209
Eurolinm, 7, 10, 53, 70

E. Aspergillus glauctts (see E* herbariorum)

E. herbanonim, 20, 69, 70 (Fig. 29), 71 (Fig.

30)

E. nigrum, 12

£. Oryzae, 12

E. repftts, 32, 48

Exoascaceae, e, 15, 16, 54, 55, 93 et seq.
Exoascales, 6, 36, 55, 56, 91 et sqq.
Exoascus, 15, 1 6, 93

E. Betttlae, 21

E. dffonnans, 91, 92 (Fig. 48)
Exobasidium, 16

£. Rhododendri, i \
Exogenous spore 3
Exotrophic mycorhiza, 16, 1 8

Facultative parasites, 6, 13
Facultative saprophyte, 6

15

226

INDEX

Fagaceae, 18

Fairy-rings, 7

Farmer J. B., and Digby, L., 48

Fasciculate spores, 36

Fatty substratum, fungi on, 10

Faull, J. H., 46, 49, 138, 172, 178, 179, 180, 182

Federley, H., 190, 195

Fermentation, alcoholic, 10 et sqq. , 62

Fertile cell (Uredinales), 200

Fertilization, 2, 3

in Ascomycetes, 41, 57, 85, 87, 101, 104,
176

in Uredinales, 205
Fisch, C., 146, 152
Fischer, E., 127, 222
Fischer von Waldheim, A., 187, 195
Fitzpatrick, 11. M., 128, 129
Foex, M., 90

Frank, B., 20, 146, 152, 164
Fraser, H. C. I., 12, 44, 114, 116

— and Blackman, V. H., see Blackman and
Fraser

and Brooks, W. E. St J., 117, 122

— and Chambers, H. S., 76

— and Welsford, E. J., 115
Freeman, E. M., and Johnson, E. C., 26, 27
Fromme, F. D., 200, 201, 221

Fruit gall, 184

Fulton, H. R., 14, 20, 28, 33
Fungi, the, I

Fungi imperfecti, 3, 7, 163
Fusicladium , 1 6 1
/". dendriticuHi, 161

F. Pyrinum, 161

Fusion, cell, i, 57 et sqq., 64, 186, 215, 216;
in the ascus, 41 et sqq., 47, 130; nuclear,
45 et sijq., 48, 59, 60, 86, 87, 101, 105, 109,
112, 114, 117, 119, 121, 129, 149, 177,
1 88 et sqq., 206 et sqq.

Galactinia succosa, 42
Gallaud, 1., 20
Gametophyte, 40
Gasteromycetes, 6
Gastrodca data, 18
Geasler, 19
Gemini, 43 (Fig. H)
Geiiea, 97

G. /iispidnla, 135 (Fig. 94)
G. Klotzschii, 135 (Fig. 94)
G. sphaerica, [35 (Fig. 94)

Gentianaceae, 18

Geoglossaceae, 97, 99, 127, 131 et seq.

Geoglossum diffortne, 35 (Fig 2)

G. hirsutum, 131 (Figs. 91, 92)
Geotropism, 32
Germ-pore, 2, 200

Germ-tube, I, 13, 14, 28, 29, 47, 149
Ginger-beer plant, 1 1
Gjurasin, S., 41
Gleba, 135
Gnowonia, 15, 51, 163

G. erythrostotna, 163
Gnomoniaceae, 1 54, 163 et sea.
Goddard, H. N., 13 '
Gooseberry mildew, 8[
Graves, A. H., 14, 20, 28, 29, 33

Green, J. Reynolds, 12

Green Algae, 49

Grove, \V. B., 211, 221

Guilliermond, A., 43, 56, 58, 59, 60, 61, 63, 64,

65, 66, 114, 115, ir6
Gmlliennondia, 57

G. fulvescens, 64

Gwynne-Vaughan, H. C. I. ; see Fraser
Gymnoascaceae, 52, 54, 55, '57, 66ets<?y.; biblio-
graphy, 68
Gymnoascus, 53, 54, 66 (Fig. 26)

G. Candidas, 67 (Fig. 27)

G. Reesii, 21, 66, 67 (Fig. 27)
Gymnoconia interstitialis, 208
Gymnosporangium, 219

G. clavariaeforme Rees, 198 (Figs. 167, 168),

199 (Fig. 169), 200, 212, 213 (Fig. 190)
Gyromitra, 129

Hall, A. D., 13

Hall, J. G., see Stevens and Hall
Hansen, E. C., 65
Haplophase or haploid phase, 3
Harper, R. A., 41, 42, 43, 45, 47, 48, 49, 82,
85, 86, 87, 88, 89, 104, 105, 106, 107, 117,
122, 18-;, 186, 191, 192, 195

and Holden, R. J. ; see Holden and Harper

Harshberger, J. W., 222
Hartig, R., 159
Hasselbring, H., 33
Haustorium, 15, 79, 80
Heliotropism, see phototropism
Helotiaceae, 97, 100, 122 et seq.
Helotium, 123
Helvetia, 129

H. crispa, 2, 43, 44 (Fig. 12), 48, 129, 130
(Fig. 90)

//. elastica, 43, 129
Helvellaceae, 97, 127, 129 et seq.
Helvellales, 6, 32, 36, 99, 127
Hemibasidiomycetes, 6, 183, 184^ sqq.
HemLeia, 219
Hemi-parasite, 6
Hemi-saprophyte, 6, 13
Bender sonia, 163
Heteroecism, 22, 210
Higgins, B. B., 160
Highley, P., 108
Hiley, W. E., 222
Hoffmann, A. W. H., 208, 209, 220
Hofmeister, W., 32, 33

Holden, R.J., and Harper, R. A., 207, 213, 220
Hop mildew, 84
H or ma, i
H-piece, I
Hitmaria carbonigena, 115

H. granulala, 48, 50, in (Fig. 67), 112 (Fig.
68), 113

If. Roitmegueri, 115

H. ritttlans, 36 (Fig. 3), 4i (Fig. 8), 43 (Figs.
10, n), 44, 47, 48, 49 (Fig. 17), 96 (Fig.
53). "3 (Fig. 69), 114 (Figs. 70, 71), 115
(Figs. 72-74)
Hyaline cell, 4
Hydnaceae, 33
Hydnum, 21
Hydrotropism, 14, 29

INDEX

227

Hymenial layer, 36, 96

Hymenium, 3, 78, 95, 136, 137, 139

Hymenogasteraceae, 8, 19

Hymenomycetes, 6, 32

Hypertrophy, 15, 16, 91, 184, 196

Hypha, i, ^.r, 56, 58, 60, 91, 95, 101, 103, 106,

129, 146, 162, 167, 199
Hyphomycetes, 7 ; and see Fungi imperfecti
Hypochnus, 17
Hypocopra, 140, 156
Hypocrea, 149

Hypocreaceae, 143, 146^^.; bibliography, 152
Hypocreales, 6, 140, 142, 143
Hypodermataceae, 134
Hypogeal fungi, 8, 77, 135
Hypomyces aurantius, 143

H. lateritus, 140, 143
Hypothecium, 95

Hy poxy Ion coccineum, 166 (Fig. 123)
Hysteriaceae, 134
Hysteriales, 6, 96, roo, 133

Ikenc, S., 75, 76, 94

Inordinate spores, 36

Intercalary cells (Uredinales), 86, 200, 202

Isaria, 150

Johannesberg yeast II, 63 (Fig. 24), 65
Johnson, E. C., see Freeman and Johnson
Jolivette, H. D. M., 30, 33
Juel, H. O., 61

Kempton, F. E., i

Kephir, n

Kidston, R., and Lang, W. H., i

Kienitz-Gerloff, F., 172

Kihlman, O., 102, 107, 144, 146

Kldcker, A., 62, 65, 73, 76

r and Schionning, H., 12

Knowles, E. L., 94

Kny, L., 32, 33

Konokotine, A. G., see Nadson and Konokotine

Koumiss, 12

Kunkel, L. O., 221

Knnkelia miens, 208, 209, 218

Kurassanow, L., 202, 221

Kusano, S., 18, 20

Kuyper, H. P., 75, 76

Labiatae, 18
Laboulbenia, 46, 171

L. chaetophora, 171 (Fig. 131), 178, 180 (Fig.

H5)

L. elongata, 172 (Fig. 132)

L. Gyrinidarum, 178

L. inflata, 177

L. triordinata, 171 (Fig. 130)
Laboulbeniaceae, 180
Laboulbeniales, 6, 15, 35, 51, 52, 54, 142, 171

et sqq. ; bibliography, 182
Lachnea cretea, 27, 51, 52, 109, no (Fig. 66)

L. scutellata, 109

L. stercorea, 9, 39 (Fig. 7), 48, 49, 50, 52,

95. (F'g- 52), 108 (Fig. 65)
Lactarius piperatus, 19
Lagerheim, G. de, 6r
Lanceolate paraphyses, 38

Lang, W. H., 20

and Kidston, R. ; see Kidston and Lang

Larch canker, 123

Larch moth, 123

Lavatera, 21

Lentinus Upideus, 7, 31

Leotia lubrica, 131 (Fig. 91), 132

Lepeschkin, W. W., 65

Leptosphaeria, 162

L. Leinaneae, 162 (Figs. 121, 121)
Levine, M. N., see Stakman, Piemeisel, and

Levine

Lewton-Brain, L., 34, 151, 152
Lichens, 52, 161, 181
Light, formative influence of, 31
Liliaceae, 18
Lindau, G., 222
Lophiostomataceae, 154, 160
Lophodermium Pinastri, 134
Ludwig, K., see Werth and Ludwig
Lutman, B. S., 186, 189, 192, 193, 194, 195
Lychnis alba, 192

L. dioica, 192
Lycopodiutn, 18, 19

McAlpine, D., 195

McBeth, I. G., and Scales, F. M., 13

McCubbin, W. A., 43, 130

Maire, R., 42, 43, 44, 114, 116, 130, 143, 201,

220

Malva, 22
Marattiaceae, 18, 19
Marchal, E., 23, 26
Marchand, H., 66
Marchantia, 4
Marryat, D. C. E., 25, 27
Marshall, W., 210
Massee, G., 20, 26, 51, 54, 97, 131, 132, 135,

138, 146, 151, 152, 222

and Salmon, E. S., 9, 12, 158

Massee, I., 191, 195
Mayr, H., 146
Meiosis, 3, 43, 53, 209, 212
Melampsora, 218, 219

M. belutina, 197 (Fig. 166)

M. Rostrupi, 201 (Fig. 174), 215
Melampsoraceae, 218, 219
Melanospora, 144

M. damnosa, 144

M. parasitica, 144

M. Zobelii, 144
Melhus, I. E., 20
Me I tola, 12

M. Penzigi, 90
Merulius lacrymans, 7
Mesospore, 197
Microsphaera, 82, 83 (Fig. 40)

M. Alni, 8 1, 88
Micros poron furfur, 4
Microthyriaceae, 78, 79, 91
Migration, nuclear, 48, 114, 186, 201, 208, 214
Mildew, white, see Erysiphaceae
Mitrula laridna, 37 (Fig. 4), 96 (Fig. 54)
Miyabe Kingo, 163
Miyoshi, M., 14, 20, 29, 32, 33
Molliard, M., 9, 12
Mollisiaceae, 100, 122 et seq.

228

INDEX

Jfonasftis, 46, 74

M. Barken, 74 (Fig. 34)

M. heterosponis, 10, 68

.47. pnrpur,-us, 75 (Fig. 35)

M. X., 75 (F«g- 35)
Manilla, 124

J7. albicans, 4

V17. (Selerotitria) tittered, 22
Monoblfpharis, 2
Monotropa Hypopitys, 19
Monoxeny, 21
Morchella. 129

J7 esfttlenta, 44, 130

J7. vulgans, 130 (Fig. 90)
Moreau, F., 146
Moreau, Mme F., 208, 209, 212, 213, 216,

221

Mttfor, 9. 10, 27, 32

J7. MuceJo, 27, 29, 32

.17. racemosits, 12

/J7. stohnifer (see Rhizopus nigricans)
Mucoraceae, 7
Mucorales, 5, 22, 30
M uniform spore, 4, 34
Mycelium, i, 15, 17, 18, 34, 58, 79, 91, 103, 189,

i <io, 192, 194, 196, 197
Mycoplasm, 211
Mycorhiza, 16 et sqq.
Mycosphasrella nigfrristigma, 160
Mycosphaerellaceae, 154, 160

Nadson. C. A., and Konokotine, A. G., 66
Nectria, 19, 145

N. cinnaharina, 14, 145 (Fig. 105)
Nectriaceae, 143 el sec/.', bibliography, 146
Neger, F. W., 89

Nichols, M. A., 47, 142, 144, 146, 159, 160
Nienbutg. W., 147, 148, 152
Non-motile spore, 4

Nuclear association, 46, 205, 206, 213, 214
Nuclear division (Uredinales), 211
Nuclear fusion, 45 rf sqq., 48, 59, 60, 86, 87, 101,
105, 109, 121, 129, 149, 177, 188 et sqq.,
206 et sqq.

Nuclear migration, 48, 114, 186, 201, 208, 214
Nuclei, paired, 42, 46, 47, 60, 75, 177, 186, 201

Oak mildew, 8(
Obligate parasite, 6, 14
Of/tropsora, 19*, 220
Odontoglossum , 1 7
Oidiopsts taurica, 80
Oiflium, 4, 57, 58, 80
Oiditim, 80

0. Qtiercinum, 81

O. Tuckeri, 80

Olive, F. W., 76, 208, 210, 212, 216, 220
Oliver, F. W., 19
Olpidium, 15
Oltmanns, K., 155, 156
Ony^ena equina, 2 1 , 76
Onygenaceae, 57, 76 et sqq,
Oogonial region, 39, 119

Oogonium, 2, 39, 4I, 51, 52, 54, 67, 71, 74, 75,
84. 85,87,98, 101, 103, 112, 176, 180,215,

Oomycetes, 5

Ophioglossaceae, 18

Orcheomyces, 17

Osmotropism, 30

Ostiole, 38

Otidea aiirantia, 95 (Fig. 51). ^5

Otomycosis aspergillana, 20

Overton, J. B., 120, 121, 122

Page, W., 155
Paraphyses, 3, 36, 37, 38
Parasite, 6
facultative, 13
obligate, 14

Parasitism, 6, 13 et sqq.; bibliography, 19 ;
specialization of, 20 et sqq. (bibliography,
26), 2ir

Parr, R., 30, 33
Patellariaceae, 96, 100, 124
Penicillin m, 7. 10, 72

P. crustaceutn (see P. glaucuni]
P. glancum, 12, 20, 31, 72 (Figs. 31, 32)
P. venniculatnm, 73 (Fig. 33)
P. Wortmanni, 73

Peniston, A., see Wagner and Peniston
Peridermium, 202
Peridium, 38, 39
Periphyses, 38, 140
Perisporiaceae, 79, 90

Perithecium, 38, 68, 8r, 82, 83, 86, 87, 88, 90,
9'. 137. '45- 148, 151. I54> *56> J57. 158,
162, 169, 171, 175
Peronospora Euphorbiae, 21

P. parasitica, 31
Peronosporales, 5
Persoon, C. H., 210
Peyritschiellaceae, 180
Peziza rutilans (see Humaria rutilans)
P tectoria, 1 1 5
P. theleboloideS, 115
P. vesiculosa, 41, 49, 115

Pezizaceae, 50, 52, 100, 107 et sqq., 144; biblio-
graphy, 1 16

Pezi/ales, 6, 36, 96, 97, 99, 100 et sqq.
Pfeffer, W., 33
Phacidiaceae, 133
Phacidiales, 6, 96, 100, 132 et seq.
Phillips, W., 222
Phoma, i, 1 6, 163
Phototaxis, 31
Phototropism, 14, 30
Phragmidium, 197, 199, 202, 219
P. bitlbosuHi, 196 (Fig. 164)
P. Polentillae-Canadensis, 203 (Fig. 178)
P. Ritbi, 204 (Fig 179), 205 (Fig. 180)
P. speciosum, 201 (Fig. 172), 212, 215 (Fig.

195)

P. subcorticiiim, 204, 216
P. violaceum, 198 (Fig. 168), 200, 201 (Fig.
173), 204 (Fig. 179), 205 (Fig. 180), 206
(Fig. 182), 213 (Fig. 191), 214 (Fig. 192),

2'5 (Fig- 194)
Phycomvces, 32
Phycomycete's, 5
Phyllattinia, 35, 45, 8%, 83, 87

P. Cory/ea, 21, 45 (Fig. 14), 79, 80, 83 (Fig.

40), 87 (Fig. 44), 88 (Figs. 45, 46), 89

(Fig. 47)

INDEX

229

Phyllosticta, 32

Phylogeny, 49 et sqq., 63, 96 et sqq., 140, 180,

188, 2 16

Phytophthora infestans, 2 1
Piemeisel, F. J., tttf Stakman, Piemeisel, and

Levine

Pilacrefaginea, 21
Pilobolus, 8, 9, 10, 30
Pimts sylvestris, 134, 206
Piplocephalis Freseniana, 22
Plectascales, 6, 56 et sqq., 181
Plectomycetes, 6, 52, 53. 55 ^ sqq.
Pleospora, i, 23, 35 (Fig. i), 161 (Fig. 120)

P. hetbarum, 161

Pleosporaceae, 154, 161 ; bibliography, 163
Plowright, C. B., 185, 187, 193, 195, 220, 222
Plowright ia morbosa, 153
Podocrea, 149

P. alutacea, 149
Podosphaera, 53
Podospora, 157

P. anserina, 158

P. coprophila, 21

/*. curvicolla, 36

/*. A r«//a, 140, 157 (Fig. 115)

P. minuta, 35 (Fig. 2)

P. p/eiospora, 36

Podostroma alutaceum (see Podocrea alutacea)
Poirault, G-, and Raciborski, M., 220
Pole Evans, I. B , 26, 27
Polyascomyces, 177

P. Trichophyae, 177 (Fig. 140)
Polyphagus Euglenae, 31
Polyporaceae, 33
Polyporus squamosus, 31
Polystictus cinnabarinus, 33
Polystignia, 51, 146

P. ritbrum, 21, 48, 141 (Fig. 102), 146, 147

(Figs. 1 06, 107), 148 (Figs. 108, 109)
Polyxeny, 21
Poronia punctata, 32, 166, 1 68 (Figs. 125, 126),

169 (Fig. 127)

Prantl. K., see Engler and Prantl
Prevost, B., 187, 195
Primary uredosorus, 203, 216
Promycelium, 183, 198
Protascns colorans (see Wolkia decolorant)
Protubasidiomycetes, 6, 183, 196 et sqq.
Prtinus pennsylvanica, 160
Pseudapogamy, 2, 3, 48, 71, 109, 113, 114, 117,

119, 130. 149, 187, 205
Pseudoparenchyma, I
Pseudoperidium, 202, 219
Pseudopeziza Trifolii, 123
Psilotaceae, 18

Pteridophyta, 18, 91, 161, 196
Puccinia, 219

P. Adoxae, 207

P. Btixi, 208

P. Carets, 196

P. Claytoniata, 200

P. dispersa, 15, 23

P. Falcariae, 200, 202, 203 (Fig. 177)

P. fust a, 211

P. glum arum, 25

P. Graminis, 23, 26, 203 (Fig. 176), 210

P. Malvacearum, 22, 29, 31, 208 (Fig. 184)

Puccinia (cont.)

P. Peckiana, 209

P. Phragmitis, 200

P. Poarum, 31, 199, 2OO, 201, 202 (Fig. 17*),
208, 214

P. Podophylli, 206 (Fig. 181), 208 (Fig. 184)

P. suaveolens, 199

P. transformans, 208

P. vexans, 204
Pucciniaceae, 218, 219
Pucciniastrum, 204
Puffing, 36, 127
Puya, 6 1
Pycnidium, i, 4

Pyrenomycetes, 6, 47, 50, 51, 52, 139 et sqq., 181
Pyrotuma, 50, 51, 52, 102

P. confiuens 21, 40, 42, 43, 44, 46 (Fig.
15). 98 (Fig. 57). 102, 103 (Fig. 61), 104
(Fig. 62), 105 (Fig. 63), 106 (Fig. 64)

P. omphaloides (see P. conjluens)
Pyronemaceae, 100, 101 et sqq. ; bibliography,

107
Pylkium, 19

P. de Baryanum, 27

Rabenhorst, L., 222
Raciborski, M., 45

and Poirault, G.; see Poirault and Raci-
borski

Ramlow, G., 9, 13, 46, 47, 118, 119, 121, 122
Ramsbottom, J., 9, 20, 62, 221
Ranunculaceae, 18
Ranunculus fie aria, 203 (Fig. 176)
Rawitscher, F., 187, 188, 189, 190, igf, 193,

i94» 195

Rayner, M. C, 16, 20

Reactions to stimuli, 27 et sqq.; bibliography, 33
Receptacle, 171, 175
Red Algae, 49, 50, 162, 172, 173, 181
Reproduction, sexual, 2; and set conjugation,
fertilization, pseudapogamy ; non-sexual, 4 ;
and see ascospore, basidiospore, conidium
Reticulate spore. 5
Rhiztna, 52, 128

R. itiflata, 128

R. undulata, 51, 128

Rhizinaceae, 99, 127 et sqq.; bibliography, iig
Rhizoctonia, 158
Rhizoclonia, 17, 1 8
Rhizomorph, i
Rhizopus, 10

R. nigricans, 12, 27 et sqq., 31
Rhododendron ferrugineum , 2 1

R. hirsutum, 1 1
Rhynia, \
Rhyparobius. 36

R. bruntieus, 121

R. (Thfcotheus) PeUetieri, 120

R. po/ysporus, 121
Rhytisma Acennum, 21, 35 (Fig. 2), 133 (Fig.

93)

Robinson, W., 14, 20, 29, 31, 33, 199
Roestelia, 202
Rosellina quercina, 140, 158
Rouppert. C, 128, 129
Rubus idaeus, 1 1
Rust-fungi, see Uredinales

230

INDEX

Saccardo, P. A., 222
Saccharomyces, 62, 63 (Fig. 24)

5. pyreformis, i r
Saccharomycetaceae, 7, i r, 52, 55, 56, 57, 62 et

sijq.; bibliography, 65
Saccharomycodes Lttdioigii, 65
Saccharomycopsis capsnlaris, 63 (Fig. 24)
Saccobolus violascens, 120 (Fig. 82)
Sachs, J. von, 32, 33, 49
Sake, 12
Salicaceae, 18
Salmon, E. S., 23, 25, 26, 79, 89, 90; J^ also

Massee and Salmon
Samsu, 74

Sands, M. C., 88, 89
Sappin-Trouffy, I'., 204, 205, 212, 220
Saprolegniales. 5
Saprophytes, 6
Saprophytism, 6, 7 et sqq.; bibliography, 12;

specialization of, 20 et sqq.
Barcodes satt guinea, 19

Scales, F. M., 13; see also McBeth and Scales
Schikorra, W.,46, 74, 75, 76
Schionning, H., 63, 65 ; see also Klocker and

Schionning

Schizanthns Grahami, i \
Sthizosccharomyces mellacei, 63 (Fig. 24), 64

S. octosponts, 63 (Fig. 24), 64 (Fig. 25)

.£ Pombe, 64
Schmitz, F., 41
Schoeler, N. P., 210
Schrenk, H. von, 12
Schroter, J., 222
Schwanniomyces occidentalism 64
Sclerotinia, 123

S. bulbonim, 123

S. cinerea, 123

S.fntctigena, 123

S. Let/i, 22

S. sclerotiorum, 123

6". tiiberosa, 21, 123, 124 (Fig. 86)

S. Vaccinii, \i\
Sclerotium, i, 124, 150, 152
Scolecite, 39, 50, 99, 1 16
Seaver, F. J., 146
Selaginella, 18
Sepultaria, 97

S. coronaria, 37 (Fig. 5), 97 (Fig. 55)
Sexual reproduction, 2, 103; and see conjugation,

fertilization, pseudapogamy
Sharp, L. W., 221
Sheath, 69, 85, 148
Smuts, see Ustilaginales
Soil, fungi on, 7
Solanaceae, 18, 21
Solatium, 18

Solms Laubach, H. zu, 184, IQS
Soot fungi, 12
Sooty-mould, 90

S. coprophila, 158
S.fimicola, i4o (Fig. 101)
S.fimiseda, 140, I57
S.globosa, 158

S macnspora,ii, 140, 157 (Fig. 116)
Sordanaceae.8, 154, 156; etsqq. bibliography, 158

Sore-skin fungus, 28

Sorosporium, 187

Sorus, 184, 196

Spathularia clavata, 131 (Figs. 91,92)

Specialization, 20 et sqq., 211

Spermatial hypha, 146, 163, 199, 207

Spermatium, 39, 146, 164, 173, 174, 199

Spermogonium, 147 (Fig. 106), 163, 198

Sphacelotheca, 187

Sphaeria, ill

Sphaeriaceae, 154, 158

Sphaeriales, 6, 140, 142, 153 et seq.

Sphacrosoma, 128, 129

S. fuscescens, 129 (Fig. 89)

S.Janczewskiamtm, 128 (Fig. 88), 129
Sphaerotheca, 52, 53, 83

S. Castagnei (see S. fftimuli)

S. ffumu/i, 41, 42 (Fig. 9), 84 (Fig. 41), 85
(Fig. 42)

S. mors-nvae, 8r, 82, 86

S. pannosa, 80 (Fig. 38)
Spore, i, 3, 4, 35, 48, i6r, 172, 196
Spore-ball, 184, 187, 194
Spore-formation, 48, 49
Spore forms, omission of, in Uredinales, 207
Spore mother-cell, 3, 35
Sporidium, 198

Spor or mia intermedia, 157 (Fig. 117)
Sprouting, 5
Stakman, E. C., Piemeisel, F. J., and Levine,

M. N., 26, 27
Staling substances, 27
Stalk, of antheridial branch, 39, 87, 88; of

archicarp, 85, 87, 88
Sterigma, 183

Sterile cell (Uredinales), 200, 207
Stevens, F. L., 39, 222

and Hall.'j. G., 28, 32, 33

Stictaceae, 132
Stigeosporium, 19

Stigmatomyces Baeri, 174, 175 (Fig. 136), 176,
«77 (Fig. 139)

S. Sarcophagae, 177, 178 (Fig. 141)
Stimuli, reactions to, 27 et sqq.', bibliography,

33

Stoppel, R., 58, 61
Strasburger, E., 31, 33
Strawberry mildew, 84
Streeter, S. G., 31, 32, 33
Strickeria, i, 142 (Fig. 104), 159 (Fig. 119)
Stroma, i, 32, 140, 145, 149, 150, 166, 168
Sub-hymenial layer, 3, 95
Substrata, fatty/io
Swanton, E. W., 222
Symbionts, 6

Symbiosis, 6, \6etsijq.; bibliography, 19
Synchytriuni, 16

S. aureum, i \
Synkaryon, 201

Tapesia fusca, 123
Taphrina, 15, 93

T. aurea, 92 (Fig. 49), 93 (Fig. 50)

/. Cerast, 94

T. Kusanoi, 94
Tavel, F. von, 40, 222
Teleutosorus, 205, 206

INDEX

231

Teleutospore, 23, 196, 197, 205, 206, 212, 218,

219, 220

Teleutospore cell, 183, 197, 205
Tcrfezia olbiensis, 77 (Fig. 36), 78 (Fig. 37)
Terfeziaceae, 8, 57, 77
Thaxter, R., 171, 172,

178, 179, 180, 181,
Thelebolus, 50

173, 174,
182

'75, 176, 177,

Uromyces (cont.)

U. Poae, 200 (Figs. 170, 171), 203 (Fig. 176),
2,2 Fig. 188), 2,4 (Fig. ,93)

U. bdllartiHi, 207, 211

U. Scirpi, 212
Urtica parvi folia, 196
Ustilaginaceae, 188 et sqq.

„>

Thermutis orlutina, 16

Thielavia basicola, 68

Thiessen, F , 91

Thorn, C., 76

Tieghem, Ph. van, 40, 102, 107

Tilletia, 187, 193

T.foetens, 193

T. laevis, 194

T. Tritici, 185 (Fig. 148), 187, 193 (Fig.

161)

Tilletiaceae, 193; bibliography, 195
Torulaspora Rosei, 64
Tragopogon pratensis, 189
Tranzschel, W., 211, 220
Tremellales, 6, 183
Tremellodon, 33
Trichogyne, 39. 51, 52, 53

^ 103, 171, 176, 215
Tncholoma terrettm, 19
Trichophoric cell, 180
Tripliragmidium, 219

T. Ulniariae, 196 (Fig. 164), 212, 216 (Fig.

196)

Truffles, 8, 138
Tuber, 8, 35, 137

T. puberuhtm, 137, 138 (Fig.
(Fie.

U. antherarum, 184, 186 (Fig. 149), 191 (Fig.

158), 192 (Fig. 159)
U. Avenae, ,89
U. Carbo, 187 (Fig. 152), 188, 189 (Fig.

U. Hordei, 186 (Fig. 150), 189 (Fig. 154)

U. levis, 192 (Fig. 160)

U. Maydis, 21, 184, 190 (Fig. 156), 191 (Fig.

157), 195

U. Scabiosae, 185 (Fig. ,47)
U. Tragoponis pratensis, 189, 190 (Fie. i«)
U. Treubii, ,84 (Fig. ,46)
U. Tritici, 189
U. Vaillantii, 191, 195
U. violacea, 21, 184
U. Zeae, 193

T. rufum, 136 (Fig. 97), 137

54, 71, 74, 98, 99, Vaccinieae, ,24

Vallory, J., 155, 156
Valsa, 165
Valsaceae, 154, 164
Vanda, 17
Varilov, 1., 27
Venturia, 161
Verpa. 129
Verrucose spore, 5
Vicia faba, 13

)

ig- 98)

Tuberaceae, 19, 97, 135 et seq., 144; biblio-
graphy, 138

Tuberales, 6, 8, 97, 100, 135
Tubeuf, K. F. von, 18, 222
Tuburcmia, 186, 187

T. primulicola, 188, 194, 195
Tulasne, L. R. and C., 77, 78, 102, 107, 136, 137,
150, 166, 167, 168, 170, 187, 195, 196, 197,

222

Umbelliferae, 18
Uncinula, 82

U. Ac>ris, 83 (Fig. 40)

U. nee at or, 81, 83
Uniseriate spores, 36, 37 (Fig. 5)
Uredineae, see Uredinales
Uredinales, 2. 6, 15, 22, 181, 183, 196 et sqq.;

bibliography, 220
Uredinopsis, 204, 219
Uredosorus, 204, 206, 207, 216
Uredospore, 23, 204
Urocystis, 187

U. Anemones, 194 (Fig. 163)

U. Fischer i, 187 (Fig. 151)

U. Violae, 184
Uromyces, 199, 205, 218, 219

U. appendiculattis , 196 (Fig. 164)

U. Cunninghamianus, 217

U. Fabae, 199

U. Ficariae, 208

Wager, H., 31, 33, 64

and Peniston, A., 66

Walled non-motile spore, 4

Ward, H. Marshall, 11, 12, ,9, 23, 25, 26, 27,

76, 77, 195, 211, 220
Weiss, F. E , 20
Welsford, E. J., 9, u, 47, 48, 117, 122, 145, 203.

2,4, 216, 221

and Blackman, V. H., see Blackman and

Welsford

and Fraser, H. C. I., see Fraser and

Welsford

Werth, E., and Ludwig, K., 192, 195, 208, 22,

West, C., 20

Wheat mildew, 23, 79, 210

Wtllia Saturnus, 65

Wilson, M., ,94, 195

Winge, O., 85, 86, 89

Winter, G., 50, 222

Witch 's-broom, 16, 90, 91

Wolf, F. A., 158

Wolfe, J. J., 173

Wolk, J. P. van der, 6,, 62

Wolkia decolorans, 60, 61

Wood, fungi on, 7

Wormald, H , 22, 27

Woronin, M-, 157, 158, 163

Woronin'> hypha, 142

Uoronina, 15

Wound parasites, 14

INDEX

Xylaria Hypoxylon, 167 (Fig. 124)

A", polymorpha, 141 (Fig. 103), 170 (Figs. 128,

12Q)

A'. Tulasnei, 21
Xylariaceae, 154, 165 ct sqq. ; bibliography, 170

Vamanouchi, S., 173

Yeasts, 2, 7, u ; and see Saccharomycetaceae

Zaghoitania, 220
Zea Mays, 21, 190

Zodioviyces, 27

Z. v'orticellaritis, 173 (Fig. 133), 176 (Fig. 138)
Zoosporangium, 4, 15
Zoospore, 1,4. 15
Zopf, W., 156, 158
Zukal, H., 73, 76
Zygomycetes, 5, 8
Zygosacchnromyces, 63 (Fig. 24)

Z. fiarkeri, 64

Z. Chevalieri, 64
Zygotaxis ,27
Zymase, 10, 12, 62

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