7
E3
S^^^^^^^^^^^^^3S
Marine Biological Laboratory Library
Woods Hole, Mass.
Presented by
Hillary House
Publishers Ltd,
Jan. 8, 1962
s^^^^^^^^^^^^^s
n
The Morpholog)' of
Pteridophytes
BIOLOGICAL SCIENCES
PROFESSOR H. MUNRO FOX
M.A., F.R.S.
Emeritus Professor of Zoology in the University
of London
THE MORPHOLOGY
OF PTERIDOPHYTES
The structure of ferns and allied plants
K. R. SPORNE
M.A., PH.D., F.L.S.
Fellow of Downing College, Cambridge
and University Lecturer in Botany
(^i\
HUT HILLARY HOUSE RARY
New York
HUTCHINSON & CO. (Publishers) LTD
178-202 Great Portland Street, London, W.i
London Melbourne Sydney
Auckland Bombay Toronto
Johannesburg New York
•
First published 1962
© K. R. Sporne 1962
This book has been set in Times New Roman type
face. It has been printed in Great Britain by The
Anchor Press, Ltd., in Tiptree, Essex, on Antique
Wove paper.
To
H. H. T.
in grateful memory
Contents
3
4
5
6
7
Preface
Introduction
Psilophytopsida
Psilotopsida
Lycopsida
Sphenopsida
Pteropsida
General Conclusions
Bibliography
Index
9
II
28
38
50
94
114
175
183
189
807^18
Preface
For many years morphology was regarded as a basic discip-
line in the study of botany and, consequently, there have
been many textbooks dealing with the subject. The pterido-
phytes occupied varying proportions of these, and there
were even some textbooks devoted to a single group, such as
the ferns, within the pteridophytes. However, to the best of
my knowledge, no book dealing solely with the pteridophytes
has been pubHshed in the western hemisphere since 1936.
Some of the old classics have recently been reprinted, but
there is a need for a reappraisal of the old theories in the
Ught of recent knowledge. Contrary to general behef, the
study of morphology is a very live one, and many important
advances have been made, on both sides of the Atlantic, in
the last decade. Exciting new fossils have been discovered
and new techniques have been developed for studying living
organisms, to say nothing of the discovery of an entirely new
genus of lycopods in the High Andes of Peru.
Naturally, a book of this kind owes much to those that
have gone before, and the most important of these are Hsted
in the bibhography. The majority of the illustrations have
been redrawn from pubHshed accounts, either in these text-
books or in research literature, and this fact has been
acknowledged in every case by reference to the author's
name.
I should Hke, also, to acknowledge the help given un-
consciously by my colleagues in the Botany School, Cam-
bridge, discussions with whom over the years have crystal-
9
10 PREFACE
lized many of the ideas incorporated in this book. Most of
all, I owe a debt of gratitude to my teacher and friend, the
late Hugh Hamshaw Thomas, sc.d., f.r.s., who guided my
first thoughts on the evolution of plants and who was a
constant source of inspiration for more than twenty-five
years. It was he who first demonstrated to me that the study
of Hving plants is inseparable from that of fossils, a fact
which forms the basis for the arrangement of this book, in
which hving and fossil plants are given equal importance.
Finally, my grateful thanks are due to my wife for her
helpful criticisms during the preparation of the manuscript.
Jv. rv. S.
Cambridge
Introduction
The study of the morphology of Uving organisms is one of
the oldest branches of science, for it has occupied the
thoughts of man for at least 2,500 years. Indeed, the very
word 'morphology' comes from the ancient Greeks, while
the names of Aristotle and Theophrastus occupy places of
importance among the most famous plant morphologists.
Strictly translated, morphology means no more than the
study of form, or structure. One may well ask, therefore,
wherein lies the intense fascination that has captured the
thoughts and imagination of so many generations of
botanists from Aristotle's time to the present day; for the
study of structure alone would be dull indeed. The answer is
that, over the centuries, morphology has come to have wider
imphcations, as Arber- has explained in her Natural Philo-
sophy of Plant Form. In this book she points out that the
purpose of the morphologists is to 'connect into one
coherent whole all that may be held to belong to the intrinsic
nature of a living being'. This involves the study, not only of
structures as such, but also of their relations to one another
and their co-ordination throughout the hfe of the organism.
Thus, morphology impinges on all other aspects of hving
organisms (physiology, biochemistry, genetics, ecology, etc.).
Furthermore, the morphologist must see each hving organ-
ism in its relationship to other living organisms (taxonomy)
and to extinct plants (paleobotany) whose remains are
known from the fossil record of past ages extending back in
II
12 THE MORPHOLOGY OF PTERIDOPHYTES
time certainly 500 million years and probably as far back as
1,000 million (some even say 2,000 million) years. Clearly,
the morphologist cannot afford to be a narrow specialist.
He must be a biologist in the widest possible sense.
From taxonomy and paleobotany, the plant morpholo-
gist is led naturally to the consideration of the course of
evolution of plants (phylogeny), which to many botanists
has the greatest fascination of all. However, it must be
emphasized that here the morphologist is in the greatest
danger of bringing discredit on his subject. His theories are
not capable of verification by planned experiments and
cannot, therefore, be proved right or wrong. At the best,
they can be judged probable or improbable. Theories
accepted fifty years ago may have to be abandoned as im-
probable today, now that more is known of the fossil record,
and, hkewise, theories that are acceptable today may have
to be modified or abandoned tomorrow. It is essential, there-
fore, that the morphologist should avoid becoming dog-
matic if he is ever to arrive at a true understanding of the
course of evolution of hving organisms.
Within the plant kingdom the range of size is enormous,
for, on the one hand, there are unicellular algae and bacteria
so small that individuals are visible only under the micro-
scope, while, on the other hand, there are seed-bearing
plants, such as the giant Redwoods of California and the
Gums of AustraUa, some of which are probably the largest
living organisms that the world has ever known. Accompany-
ing this range of size, there is a corresponding range of
complexity of internal anatomy and of life-history. Some-
where between the two extremes, both in structure and in
Hfe-cycle, come the group of plants known as Pteridophytes,
for they share with seed plants the possession of well-
developed conducting tissues, xylem and phloem, but differ
from them in lacking the seed habit. Internally, they are
more complex than mosses and Uverworts, yet in life-cycle
they differ from them only in matters of degree.
INTRODUCTION
13
The basic life-cycle, common to bryophytes and pterido-
phytes, is represented diagrammatically in Fig. i. Under
normal circumstances there is a regular alternation between
a gametophyte (sexual) phase and a sporophyte (asexual)
phase. The male gametes, produced in numbers from an-
theridia, are known as antherozoids, since they are flagel-
lated and are able to swim in water, while the female gametes
(Qgg cells) are non-motile and are borne singly in flask-
shaped archegonia. Fusion between an egg cell and an
Gametophyte-
Egg ("V (E) Spermatozoid
II
2n
Zygote Sporophyte
++^ ® ^ Spores
-ri • ^(n)
Meiosis
Fig. 1
Life cycle of a homosporous pteridophyte
antherozoid results in the formation of a zygote, which
contains the combined nuclear material of the two gametes.
Its nucleus contains twice as many chromosomes as either
of the gamete nuclei and it is therefore described as diploid.
The zygote develops directly by mitotic divisions into the
sporophyte which is, Ukewise, diploid. Uhimately, there are
released from the sporophyte a number of non-motile spores,
in the formation of which meiosis brings about a reduction of
the nuclear content to the haploid number of chromosomes.
The life-cycle is then completed when these spores germinate
and grow, by mitotic divisions, into haploid gametophytes.
In mosses and liverworts, the dominant phase in the life-
cycle is the gametophyte, for the sporophyte is retained upon
it throughout its Hfe and is either partially or completely
14 THE MORPHOLOGY OF PTERIDOPHYTES
dependent on it for nutrition. By contrast, among pterido-
phytes the sporophyte is the dominant generation, for it very
soon becomes independent of the gametophyte (prothallus)
and grows to a much greater size. Along with greater size
is found a much greater degree of morphological and
anatomical complexity, for the sporophyte is organized into
stems, leaves and (except in the most ancient fossil pterido-
phytes and the most primitive Uving members of the group)
roots. Only the sporophyte shows any appreciable develop-
ment of conducting tissues (xylem and phloem), for although
there are recorded instances of such tissues in gametophytes,
they are rare and the amounts of xylem and phloem are
scanty. Furthermore, the aerial parts of the sporophyte are
enveloped in a cuticle in which there are stomata, giving
access to complex aerating passages that penetrate between
the photosynthetic pahsade and mesophyll cells of the leaf.
All these anatomical complexities confer on the sporo-
phyte the potentiaUty to exist under a much wider range of
environmental conditions than the gametophyte. However,
in many pteridophytes these potentialities cannot be realized,
for the sporophyte is limited to those habitats in which the
gametophyte can survive long enough for fertilization to
take place. This is a severe hmitation on those species whose
gametophytes are thin plates of cells that lack a cuticle and
are, therefore, susceptible to dehydration. Not all gameto-
phytes, however, are Umited in this way, for in some pterido-
phytes they are subterranean and in others they are retained
within the resistant wall of the spore and are thus able to
survive in a much wider range of habitats. It is notable that
wherever the gametophyte is retained within the spore the
spores are of different sizes (heterosporous), the larger
megaspores giving rise to female prothalH which bear only
archegonia, and the smaller microspores giving rise to male
prothaUi bearing only antheridia. Why this should be is not
known with certainty, but two possible reasons come to
mind, both of which probably operate together.
INTRODUCTION 15
The first concerns the nutrition of the prothallus and the
subsequent embryonic sporophyte. The retention of the
gametophyte within a resistant spore wall severely Hmits its
powers of photosynthesis and may even prevent it alto-
gether. Hence, it is necessary for such a prothallus to be
provided with abundant food reserves; the larger the spore,
the more that can be stored within it. This may well account
for the lage size of the spores which are destined to contain
an embryo sporophyte, but it does not explain why the pro-
thalli should be unisexual (dioecious). This is most probably
concerned with out-breeding. It is widely accepted that any
plant which habitually undergoes inbreeding is less likely to
produce new varieties than one which has developed some
device favouring out-breeding, and that such a plant is at a
disadvantage in a changing environment. It will tend to lag
behind in evolution. Now, monoecious gametophytes (bear-
ing both archegonia and antheridia) are much more hkely to
be self-fertihzed than cross-fertilized, unless they are actually
submerged in water. Yet, dioecious prothalli in a terrestrial
environment would be at an even greater disadvantage, for
they might never achieve fertilization at all, so long as the
antherozoid has to bear the whole responsibility of finding
the archegonium. This is where heterospory may operate to
the advantage of plants with dioecious prothalli. Those
spores which are destined to produce male prothaUi need
not carry large food reserves and can, therefore, afford to be
reduced in size to the barest minimum. From the same initial
resources, vast numbers of microspores can be produced and
this will allow some of the responsibility for reaching an
archegonium to be transferred to them. Blown by the wind,
they can travel great distances and some, at least, will fall on
a female prothallus in close proximity to an archegonium.
Thus, when the male prothallus develops, the antherozoids
Uberated from the antheridia have only a short distance to
swim and, in order to do so, need only a thin film of
moisture. Under ordinary circumstances, the chances may
l6 THE MORPHOLOGY OF PTERIDOPHYTES
be quite small that the particular microspore will have come
from the same parent sporophyte as the megaspore and thus
a fair degree of out-breeding will have been achieved. The
relative emancipation from the aquatic environment pro-
vided by the heterosporous habit will confer on the sporo-
phyte the freedom to grow almost anywhere that its own
potentiahties allow and the possibiUty of out-breeding will
favour more rapid evolution of those potentiahties. Most
morphologists agree that the evolution of heterospory was a
necessary step in the evolution of the seed habit and that,
therefore, it is one of the most important advances in the
whole story of land plant evolution.
The Ufe-cycle of a typical heterosporous pteridophyte may
be represented diagrammatically as in Fig. 2.
The distinction between heterospory and homospory is
one of the criteria used in the classification of pteridophytes,
in accordance with the general behef that reproductive
organs are a better guide to phylogenetic relationships than
are vegetative organs. They are held to be more *con-
servative', in being less susceptible to the immediate influence
of the environment. Likewise, therefore, the manner in
which the sporangia develop and the way in which they
are borne on the sporophyte constitute important taxo-
nomic characters.
The sporangium, in all pteridophytes, is initiated by the
laying down of a cross-wall in a superficial cell, or group of
cells. Since this wall is pericUnal (i.e. parallel to the surface)
each initial cell is divided into an outer and an inner daughter
cell. If the sporogenous tissue is derived from the inner
daughter cell, the sporangium is described as *eusporangiate'
and, if from the outer, as *leptosporangiate'. This definition
of the two types of sporangium is usually expanded to in-
clude a number of other differences. Thus, in leptosporangi-
ate forms, the sporangium wall and the stalk, as well as the
spores, are derived from the outer daughter cell, but, in
eusporangiate forms, adjacent cells may become involved
INTRODUCTION
17
in the formation of part of the sporangium wall and the stalk
(if any). Furthermore, the sporangium is large and massive
in eusporangiate forms, the wall is several cells thick and the
spore content is high, whereas, in leptosporangiate forms, the
sporangium is small, the wall is only one cell thick and the
spore content is low. Of these two types, the eusporangiate
is primitive and the leptosporangiate advanced.
Eggf " ) (^ Spermatozoid
Zygote
5 Gametophyte
cf Gametophyte
Meiosis
2n
I^^@ Microspores
-H — ► — —(^
0
*~~vIL//'~^ Megaspores
B
©
Sporophyte Meiosis
Fig. 2
Life cycle of a heterosporous pteridophyte
Until the early years of this century, it was widely beheved
that sporangia could be borne only on leaves and that such
fertile leaves, known as 'sporophylls', were an essential part
of all sporophytes. However, the discovery of Devonian
pteridophytes that were completely without leaves of any
kind, fertile or sterile, has led most morphologists to
abandon this 'sporophyll theory'. It is now accepted that in
some groups sporangia may be borne on stems, either
associated or not with leaves, and in others actually on the
leaves.
Important as reproductive organs are in classification,
l8 THE MORPHOLOGY OF PTERIDOPHYTES
vegetative organs are nevertheless of considerable import-
ance in classifying pteridophytes, for the shape, size, arrange-
ment and venation of leaves (and even presence or absence
of leaves) are fundamental criteria. It so happens that it is
difficult, if not impossible, to devise a definition of the term
'leaf that is entirely satisfying, but, for practical purposes,
it may be said that among pteridophytes there are two very
different types of leaf, known respectively as megaphylls and
microphylls. The famiUar fern frond is an example of the
former; it is large, branches many times and has branching
veins. By contrast, microphylls are relatively small, rarely
branch and possess either a limited vascular supply or none
at all ; the leaf trace, if present, is single and either remains
unbranched within the microphyll or, if it branches at all, it
does so to a limited degree and in a dichotomous manner.
As might be expected, the leaf traces supplying micro-
phylls cause little disturbance when they depart from the
vascular system (stele) of the parent axis, whereas those
supplying megaphylls are usually (though not invariably)
associated with leaf gaps. A stele without leaf gaps is termed
a protostele, the simplest type of all being the soUd proto-
stele. Fig. 3A illustrates its appearance diagrammatically as
seen in transverse section. In the centre is a solid rod of
xylem which is surrounded by phloem and then by pericycle,
the whole stele being bounded on the outside by a con-
tinuous endodermis. Another variety of protostele is the
medullated protostele, illustrated in Fig. 3B. In this the
central region of the xylem is replaced by parenchyma. Yet
other varieties of protostele will be described as they are
encountered in subsequent chapters. Steles in which there
are leaf gaps are known as dictyosteles, if the gaps occur
frequently enough to overlap, and as solenosteles if they are
more distantly spaced. Fig. 3C is a diagrammatic represen-
tation of a solenostele as seen in transverse section passing
through a leaf gap. The most remarkable feature is the way
in which the inside of the xylem cyhnder is lined with
___!.....
I'i'i'i
.III
1 1 1 1
i'i'i'i
* ^
K^''
Phloem
Metaxylem
Medu
Ila or pith
• Protoxylem
„._.-.— Endodermis
Fig. 3
Fem steles: a, solid protostele; b, meduUated protostele;
c, D, solenostele; e, f, dictyostele; g, dicyclic stele
20 THE MORPHOLOGY OF PTERIDOPHYTES
phloem, pericycle and endodermis, as if these tissues had
'invaded' the central parenchymatous region (though, need-
less to say, the developmental processes do not involve any
such invasion). Fig. 3E illustrates the structure of a dictyo-
stele in which three leaf gaps are visible in the one transverse
section. Frequently it happens that each leaf gap is associ-
ated with the departure of several leaf traces to the leaf, but
in this example, for clarity, only one trace is shown supply-
ing each leaf. The remaining portions of the stele are
referred to as meristeles and, although in transverse section
they appear to be unconnected, when dissected out and viewed
as three-dimensional objects they are seen to form a network.
Figs. 3D and 3F are perspective sketches of a solenostele
and a dictyostele, respectively, from which the surrounding
cortex and ground tissue have been removed in this way.
It must be pointed out at this stage that some morpholo-
gists use a different system of terminology and group to-
gether the medullated protostele and the solenostele as
varieties of so-called siphonosteles, on the grounds that
each has a hollow cylinder of xylem. The former they des-
cribe as an ectophloic siphonostele, because the phloem is
restricted to the outside of the xylem, and the latter they
describe as an amphiphloic siphonostele, because the phloem
lies both outside and inside the xylem. This practice, how-
ever, has disadvantages. First, it tends to exaggerate the
difference between the solenostele and the dictyostele — a
difference that reflects little more than a difference in the
direction of growth, for where leaves arise at distant inter-
vals on a horizontal axis their leaf gaps are unUkely to over-
lap, whereas leaves on a vertical axis are often so crowded
that their leaf gaps must overlap. Secondly, it overlooks the
fundamental distinction between the solenostele and the
medullated protostele — a physiological distinction depend-
ing on the position of the endodermis.
When gaps occur in a stele without any associated leaf
traces, they are described as perforations and the stele is said
INTRODUCTION 21
to be perforated. Thus, there may be perforated solenosteles
which, at a first glance, might be confused with dictyosteles ;
however, as soon as attention is paid to the relationship
between leaf traces and perforations, the distinction becomes
clear. When more than one stele is visible in any one trans-
verse section the plant is described as polystelic. Yet another
variant is the polycyclic stele, in which there are two or more
co-axial cyUnders of conducting tissue (Fig. 3G).
All the vascular systems mentioned so far are composed
entirely of primary tissues, i.e. tissues formed by the matura-
tion of cells laid down by the main growing point (apical
meristem). It is customary to draw a rough distinction
between tissues that differentiate before cell elongation has
finished and those that differentiate only after such growth
has ceased. In the former case, the xylem and phloem are
described as protoxylem and protophloem. They are so con-
structed that they can still alter their shape and can, thereby,
accommodate to the continuing elongation of the adjacent
cells. Accordingly, it is usual for the Ugnification of proto-
xylem elements to be laid down in the form of a spiral, or
else in rings. Metaxylem and metaphloem elements, by
contrast, do not alter their size or shape after differentiation.
The order in which successive metaxylem elements mature
may be centripetal or centrifugal. When the first xylem to
differentiate is on the outside and differentiation proceeds
progressively towards the centre, the xylem is described as
exarch and all the metaxylem is centripetal. When the proto-
xylem is on the inner side of the metaxylem and differentia-
tion occurs successively away from the centre, the xylem is
described as endarch and all the metaxylem is centrifugal.
A third arrangement is known as mesarch, where the proto-
xylem is neither external nor central and differentiation pro-
ceeds both centripetally and centrifugally. In Figs. 3A-3C
the xylem is mesarch, while in Fig. 3G it is endarch.
In addition to primary vascular tissues, some pterido-
phytes possess a vascular cambium from which secondary
22 THE MORPHOLOGY OF PTERIDOPHYTES
xylem and secondary phloem are formed. Cambial cells
possess the power of cell division even though the surround-
ing tissues may have lost it; they may either have retained
this power throughout the lapse of time since they were laid
down in the apical meristem, or they may have regained it
after a period of temporary differentiation. While relatively
uncommon in living pteridophytes, a vascular cambium was
widely present in coal-age times, when many members of the
group grew to the dimensions of trees. Just as, at the present
day, all trees develop bark on the outside of the trunk and
branches by the activity of a cork cambium, so also did these
fossil pteridophytes. In some, the activity of this meristem
was such that the main bulk of the trunk was made up of the
periderm which it produced.
Any attempt to interpret modern pteridophytes must
clearly take into account their forerunners, now extinct, in
the fossil record. This involves some understanding of the
ways in which fossils came to be formed and of the extent
to which they may be expected to provide information useful
to the morphologist. A fossil may be defined as ^anything
which gives evidence that an organism once hved'. Such a
wide definition is necessary to allow the inclusion of casts,
which are no more than impressions left in the sand by some
organism. Yet, despite the fact that casts exhibit nothing of
the original tissues of the organisms, they are nevertheless
valuable in showing their shape. At the other extreme are
petrifactions, in which the tissues are so well preserved by
mineral substances that almost every detail of the cell walls
is visible under the microscope. Between these two extremes
are fossils in which decay had proceeded, to a greater or
lesser degree, before their structure became permanent in
the rocks.
Under certain anaerobic conditions (e.g. in bog peat and
marine muds), and in the absence of any petrifying mineral,
plant tissues slowly turn to coal, in which little structure can
be discerned, apart from the cuticles of leaves and spores.
INTRODUCTION 23
Portions of plants that are well separated from each other
by sand or mud during deposition give rise to fossils known
as mummifications or compressions. From these, it is often
possible to make preparations of the cuticle, by oxidizing
away the coally substance with perchloric acid. Examina-
tion under a microscope may then reveal the outlines of the
epidermal cells, stomata, hairs, papillae, etc. In this way,
a great deal can be discovered from mummified leaves.
Mummified stems and other plant organs, however, yield
less useful results. Even their shape needs careful interpreta-
tion, because of distortion during compression under the
weight of overlying rocks.
By far the most useful fossils to the palaeobotanist are
those in which decay was prevented from starting, by the
infiltration of some toxic substance, followed by petrifaction
before any distortion of shape could occur. Such are, un-
fortunately, rare indeed. The most beautiful petrifactions
are those in silica, but carbonates of calcium and magnesium
are also important petrifying substances. Iron pyrites, while
common, is less satisfactory because the fine structure of the
plant is more difiicult to observe. While it has often been
said that during petrifaction the tissues are replaced molecule
by molecule, this cannot be correct, for the 'cell walls' in
such a fossil dissolve less rapidly in etching fluids than does
the surrounding matrix. This fact forms the basis of a rapid
technique for making thin sections of the plant material.*^
A poUshed surface is etched for a brief period in the appro-
priate acid and the cell walls that remain projecting above
the surface are then embedded in a film of cellulose acetate.
This is stripped off and examined under the microscope
without further treatment, the whole process having taken
no longer than ten minutes.
While it is frequently possible to discern the type of
thickening on the walls of xylem elements, it is, however,
rarely possible to make out much detail in the phloem of
fossil plants, for this is the region which decays most rapidly.
24 THE MORPHOLOGY OF PTERIDOPHYTES
Furthermore, most fossils consist only of fragments of
plants. It is then the task of the palaeobotanist to recon-
struct, as best he can, from such partly decayed bits, the
form, structure and mode of Ufe of the whole plant from
which they came. There is small wonder, then, that this has
been achieved for very few fossil plants. Many years may
elapse before it can be said with any certainty that a particu-
lar kind of leaf belonged to a particular kind of stem and, in
the meantime, each must be described under a separate
generic and specific name. In this way, the palaeobotanist
becomes unavoidably encumbered by a multiplicity of such
names.
For convenience of reference, the history of the Earth is
divided into four great eras. The first of these, the pre-
Cambrian era, ended about 500 milUon years ago and is
characterized by the scarcity of fossils, either of animals or of
plants. Then came the Palaeozoic era, characterized by
marine invertebrates, fishes and amphibians, the Mesozoic
by reptiles and ammonites and, finally, the Cainozoic, ex-
tending to the present day, characterized by land mammals.
These major eras are again divided into periods (systems)
and then subdivided again, chiefly on the basis of the fossil
animals contained in their strata. While such a scheme is
clearly satisfactory to the zoologist, it is less so to the
botanist, for the plants at the beginning of one period (e.g.
the Lower Carboniferous) are less like those of the end of
the period (the Upper Carboniferous) than Hke those of the
end of the previous period (the Upper Devonian). Thus, it
is more usual for the palaeobotanist to speak of the plants of
the Upper Devonian/Lower Carboniferous than of the
plants of the Carboniferous period.
The sequence of the various geological periods is summar-
ized as a table (p. 25), in which the time scale is based on in-
formation from R. N. C. Bowen^. Brief notes are included
to indicate the kind of vegetation that is beheved to have
existed during each period, but a word of caution is necessary
GEOLOGICAL PERIODS IN IHE NORTHERN HEMISPHERE
Era
Period
Age
in
years
Type of vegetation
u
Quaternary
I
Modern
o
N
O
z
Upper Tertiary, Pliocene
Miocene
10
20
Modern
<
Lower Tertiary, Oligocene
Eocene
Upper Cretaceous
35
50
75
Modern, with tropical
plants in Europe
u
o
N
Lower Cretaceous
Upper Jurassic
100
130
Gymnosperms dominant
(Conifers and
Bennettitales)
o
Lower Jurassic (Liassic)
Upper Triassic (Rhaetic)
140
160
Luxuriant forests of
Gymnosperms and
Ferns
Lower Triassic (Bunter)
Upper Permian
180
190
Sparse desert flora with
Gymnosperms
(Conifers and Bennetti-
tales)
Lower Permian
Upper Carboniferous
(Coal Measures)
200
Tall swamp forests with
early Gymnosperms,
Tree-Lycopods, Cala-
mites and Ferns
u
Lower Carboniferous
Upper Devonian
250
260
Early Gymnosperms,
large Tree-Lycopods
and Ferns
o
N
2
Middle Devonian
275
Rhynia vegetation in
marshy localities
<
Qu
Lower Devonian
Upper Silurian
300
Herbaceous marsh plants,
{Psilophyton and
Zosterophylhim) and
some small shrubs
Silurian
350
Marine algae
Ordovician
425
Marine algae
Cambrian
500
Marine algae, but some
evidence of land plants,
too
PRE-
CAMBRIAN
4500?
Fungi and Bacteria re-
ported to have occur-
red 2,000 million years
ago
26 THE MORPHOLOGY OF PTERIDOPHYTES
on this matter. It must always be remembered that our
knowledge of past vegetation is based on those fragments
of plants that happened to become fossilized and which,
furthermore, happen to have been unearthed. It follows,
therefore, that a species list will certainly be biassed in favour
of plants growing near a particular site of sedimentation and
will not give a true picture of the world's vegetation at that
time. Thus, until recently, it was thought that the only plants
alive in Cambrian times were marine algae and that the land
had not yet been colonized. This view would still be held
today if macroscopic remains provided the only evidence,
but recent discoveries of a wide range of cuticularized spores
have shown that there were also numerous land plants in
existence. Presumably, they were growing in some habitat
where fossilization of their macroscopic remains could not
occur. These discoveries of wind-borne spores alter the
whole picture of Cambrian vegetation and push further back
into antiquity the date of the first colonization of the land by
plants. Similar considerations no doubt apply throughout
the fossil record to a greater or lesser extent.
We turn now to the classification of pteridophytes. The
first object of any classification must be to group together
similar organisms and to separate dissimilar ones. In the
process the group is subdivided into smaller groups, each
defined so as to encompass the organisms within it. In the
early days of taxonomy, when few fossils were known, these
definitions were based on living plants. Then, as more and
more fossils were discovered, modifications became neces-
sary in order to accommodate them, and a number of
problems arose. The first arises from the fact that a fossil
plant, even when properly reconstructed, is known only at
the stage in its life-cycle at which it died. Other stages in its
life-cycle, or in its development, may never be discovered.
Yet, the classification of living organisms may (and indeed
should) be based on all stages of the life-cycle. The second
problem concerns the difficulty, when new fossils are dis-
INTRODUCTION
27
covered, of deciding whether to modify the existing defini-
tions of groups or whether to create new groups. Too many
groups would be liable to obscure the underlying scheme of
the classification and too few might result in each group being
so wide in definition as to be useless. The scheme on v/hich
this book is based is substantially the same as that proposed
by Reimers in the 1954 edition of Engler's Syllabus der
Pflauzenfamilien^^ and has been chosen because it seems to
strike a balance in the number and the size of the groups
that it contains. (An asterisk is used throughout to indicate
fossil groups.)
PTERIDOPHYTES
A PSILOPHYTOPSIDA*
Psilophy tales*
B PSILOTOPSIDA
Psilotales
C LYCOPSIDA
1 Protolepidodendrales*
2 Lycopodiales
3 Lepidodendrales*
4 Isoetales
5 Selaginellales
D SPHENOPSIDA
1 Hyeniales*
2 Sphenophyllales*
3 Calamitales*
4 Equisetales
E PTEROPSIDA
a Primofilices*
1 Cladoxylales*
2 Coenopteridales*
b Eusporangiatae
1 Marattiales
2 Ophioglossales
c Osmundidae
Osmundales
d Leptosporangiatae
1 Filicales
2 Marsileales
3 Salviniales
Psilophytopsida
Extinct plants. Only the sporophyte is known.
Rootless, with rhizomes and aerial branches that
are more or less dichotomous, either naked or
with small appendages spirally arranged. Proto-
stelic. Sporangia thick-walled, homosporous, borne
at the tips of branches.
Psilophytales*
Rhyniaceae* Rhynia* Horneophyton* {=Hornea),
Cooksonia,* Yarravia*
Zosterophyllaceae * Zosterophyllum *
Psilophytaceae* Psilophyton*
Asteroxylaceae* Aster oxylon*
The first member of this group ever to be described was
Psilophyton princeps in 1859^^, but for many years httle
notice was taken of this discovery. Indeed, many botanists
regarded it almost as a figment of the imagination, so differ-
ent was it from their preconceived ideas of land plants.
However, by 19 17 Kidston and Lang^° had started to des-
cribe a number of similar plants from Middle Devonian
rocks at Rhynie in Scotland, and it became accepted that
plants with such a simple organization had really existed.
Only then was the group Psilophytales created to include
them.
The chert deposits at Rhynie, some eight feet thick, are
28
PSILOPHYTOPSIDA 29
thought to represent a peat bog which became infiltrated
with siUca. In this way the plant remains became preserved,
some of them with great perfection. The chief plants to have
been described from these deposits are Rhynia major, Rhynia
Gwynne-Vaughani, Horneophyton Lignieri and Asteroxylon
Mackiei. Of these, the first three lacked leaves as well as
roots and are now grouped together in the Rhyniaceae along
with Cooksonia^^ and Yarravia^^ from Upper Silurian/Lower
Devonian rocks of Great Britain and Austraha respectively.
The general appearance of Rhynia major is illustrated in
Fig. 4E. It had a horizontal rhizome which branched in
a dichotomous manner and bore groups of unicellular
rhizoids at intervals. The tips of some rhizomes turned up-
wards and grew into aerial stems as much as 50 cm high and
up to 6 mm in diameter. These also branched dichotomously
and some of them terminated in pear-shaped sporangia up
to 12 mm long. The aerial parts were smooth and covered
with a cuticle in which stomata were sparingly present, their
presence indicating that the stems were green and photo-
synthetic. In transverse section (Fig. 4F) the stems are seen
to have had a cortex differentiated into two regions, often
separated by a narrow zone of cells with dark contents.
Whereas the outer cortex was of densely packed cells, the
inner cortex had abundant inter-cellular spaces with direct
access to the stomata; for this reason the inner cortex is
presumed to have been the main photosynthetic region. The
sporangium (Fig. 4H) had a massive wall, about five
cells thick, apparently without any specialized dehiscence
mechanism, and within it were large numbers of spores
about 65 ju. in diameter. The fact that these spores were
arranged in tetrads is taken to prove that they were formed
by meiosis and that the plant bearing them represented the
sporophyte generation. What the gametophyte might have
looked like no one knows, though the discovery of living
gametophytes of Psilotum containing vascular tissue has led
to a suggestions^ that some of the bits of Rhynia, identified
30 THE MORPHOLOGY OF PTERIDOPHYTES
as rhizomes, could have been gametophytes. Against this
view, however, is the fact that no archegonia or antheridia
have yet been convincingly demonstrated.
Rhynia Gwynne-Vaughani (Fig. 4G) was a smaller plant
than R. major, attaining a height of only 20 cm. It was
similar in having a creeping dichotomous rhizome with
groups of rhizoids, but the aerial parts of the plant differed
in several respects ; small hemispherical lumps were scattered
over the surface and, besides branching dichotomously, the
plant was able to branch adventitiously. An interesting
feature of the adventitious branches was that the stele was
not continuous with that of the main axis. It is possible that
they were capable of growing into new plants if detached
from the parent axis, thereby providing a means of vegeta-
tive propagation. The sporangia were only 3 mm long and
the spores, too, were smaller than those of i?. major. In other
respects (internal anatomy, cuticle, stomata, etc.) the two
species were very similar indeed.
Horneophyton Lignieri (Fig. 4I) was smaller still, its aerial
axes being only some 13 cm high and only 2 mm in maximum
diameter. It was first described under the generic name
Hornea, but in 1938 it was pointed out that this name had
already been used for another plant and a new name was
proposed, Horneophyton. The aerial axes were like those of
Rhynia major, in being quite smooth and in branching
dichotomously without any adventitious branches. In its
underground organs, Horneophyton was very different, for
it had short lobed tuberous corm-hke structures. From their
upper side aerial axes grew vertically upwards and on their
lower side were unicellular rhizoids. The stele of the aerial
axis did not continue into the tuber, which was parenchy-
matous throughout. Most of the tubers contained abundant
non-septate fungal hyphae, whose mode of life has been
the subject of some speculation. By analogy with other
groups of pteridophytes, it is commonly supposed that there
was a mycorrhizal association but, as Kidston and Lang^*^
%TTTT~TlTnf
TTnTTTiii^
Fig. 4
Zosterophyllum rhenanum: A, reconstruction; b, sporangial
region. Yarravia oblonga: c, sporangia. Cooksonia pertoni:
D, sporangia. Rhynia major: e, reconstruction; f, t.s. stem;
H, sporangium. Rhynia Gwynne-Vaughani : G, reconstruction.
Horneophyton Lignieri: i, reconstruction; J, k, sporangia
(a, b after Krausel and Weyland; c, Lang and Cookson; d,
Lang; e, g, h, i, j, k, Kidson and Lang)
32 THE MORPHOLOGY OF PTERIDOPHYTES
pointed out, some well-preserved tubers showed no trace
whatever of fungus. This fact suggests that, instead of being
mycorrhizal, the fungus was a saprophyte which invaded the
tissues of the tuber after death.
Another feature of interest, peculiar to Horneophyton, was
the presence of a sterile columella in the sporangium (Fig.
4J), a feature reminiscent of the mosses. One sporangium is
illustrated (Fig. 4K) which was bifid and it is interesting
that the columella was also bifid. This leads one to suppose
that the stem apex could be transformed into a sporangium
at any stage, even during the process of dichotomizing, and
rules out any idea of the sporangium being borne by a special
organ to which the name 'sporangiophore' might be given.
The generic names Yarravia and Cooksonia are given to
certain reproductive bodies detached from the plants which
bore them ; indeed, we have no idea at all what such plants
might have looked like. Yarravia (Fig. 4C) has been interpre-
ted as a slender unbranched axis, terminating in a radially
symmetrical group of five or six sporangia, partly fused
into a synangium, about i cm long. Although Lang and
Cookson,^^ who first described this genus, were unable to
demonstrate the presence of spores within the sporangia this
interpretation is widely accepted and has been used as the
starting point for phylogenetic speculations as to the nature
of the pollen-bearing organs of fossil seed-plants, and even
of their seeds. Cooksonia (Fig. 4D) was much more Hke the
other members of the Rhyniaceae, in that the sporangia
were borne singly at the tips of tiny forking branches. Each
sporangium was broader than it was long (one species
being 2 mm x i mm) and contained large numbers of spores
in tetrads.
The chief point of difference between the Zosterophyl-
laceae and the Rhyniaceae, described above, concerns the
manner in which the sporangia were borne, for instead of
terminating the main axes, they were in short terminal
spikes, each sporangium having a short stalk. The best
PSILOPHYTOPSIDA 33
known genus is Zosterophyllum itself, of which three species
have been described, one of them (Z. myretonianum) in
considerable detail."^ ^^ Its fossil remains occur in the Old
Red Sandstone of Scotland, and show that it grew in dense
tufts anchored to the ground by a tangle of branching
rhizomes. From these arose numerous erect dichotomous
branches, 15 cm or more in height and 2 mm in diameter,
cyhndrical and cuticularized, with a central vascular bundle
whose xylem tracheids bore annular thickenings. An Austra-
lian Upper Silurian species, Z. australianum, was similar,^®
but Z. Rhenanum, described from the Lower Devonian of
Germany,^* is said to have differed in having flattened stems.
For this reason, it is suggested that the German species must
have been partially submerged, as shown in the reconstruc-
tion (Fig. 4A). The way in which the sporangia were borne
is shown in Fig. 4B. The spikes varied in length from i cm
to 5 cm, with the sporangia arranged spirally upon them,
each sporangium being up to 4 mm broad. Dehiscence took
place by means of a transverse split in the sporangium wall.
Psilophyton, the genus which lends its name to the groups
Psilophytopsida and Psilophytales, besides occurring in
Canada and the United States, has also been found in
Devonian rocks of Scandinavia, France and Belgium.
Psilophyton princeps^^ is the best known species. Fig. 5F is a
reconstruction of the plant. It grew to a height of about i m
in dense clumps, arising from a tangle of creeping rhizomes
covered with rhizoidal hairs. The aerial branches seldom
exceeded i cm in diameter and branched profusely in a
manner that was rather different from that of the Rhynia-
ceae, for many of the dichotomies were unequal. In this way,
some parts of the plant give the appearance of a sympodial
arrangement, with a main stem and lateral branches.
The lower parts of the aerial shoots were clothed with
abundant outgrowths which have been variously described
as leaves, spines and thorns (Fig. 5G). Their tips appear to
have been glandular, they lacked stomata and vascular
B
34 THE MORPHOLOGY OF PTERIDOPHYTES
supply; so none of the descriptions seems to be really
appropriate. Since stomata were present in the cuticle
covering the stem, it is presumed that the principal site of
photosynthesis was in the cortex of the stem itself. However,
only mummified specimens have been found, with the result
that little is known about the internal anatomy of the stem,
except that the xylem tracheids had annular or scalariform
thickenings.
During their growth, the aerial axes were circinately
coiled in a manner similar to that seen in the young fronds
of a modern fern — a method of growth which, no doubt,
gives some protection to the dehcate stem apex, from
mechanical damage and from desiccation. Some of the
ultimate branches bifurcated and each fork terminated in a
sporangium up to 6 mm long and 2 mm wide (Fig. 5H),
within which were numerous spores in tetrads.
Two species of Aster oxylon are known, A. Mackiei^^,
which occurred along with Rhynia and Horneophyton in the
Rhynie chert, and A. elberfeldense^^ from Middle Devonian
rocks near Elberfeld, in Germany. While the German species
is known to have attained a height of about i m, the
Scottish species is believed to have been somewhat smaller,
but one can only guess at its height, for only portions of the
whole plant have been found. A. Mackiei had dichotomous
rhizomes whose internal structure was so hke that of Rhynia
that the two were, at first, confused. However, they were re-
markable in being completely without rhizoidal hairs.
Instead, small lateral branches of the rhizome grew down-
wards into the underlying peat, branching dichotomously as
they went, and it is assumed that they acted as the absorbing
organs of the plant (Fig. 5A).
The erect aerial axes were about i cm across at the base
and they branched monopodially, dichotomies being res-
tricted mainly to the lateral branches. Except right at the
base, and in the presumed reproductive regions of the shoot,
all the aerial axes were clothed with leaves arranged in a
,i I;, y h'
Fig. 5
Asteroxylon Mackiei: a, reconstruction of vegetative regions;
B, t.s. stem; c, reproductive regions; d, sporangium. Asteroxylon
elberfeldense : e, upper portions of plant (note circinate vernation).
Psilophyton princeps: F, reconstruction; G, enlarged portion of
stem, showing enations; H, sporangia
(a, c, d, after Kidson and Lang; e, Krausel and Weyland; f,
G, H, Dawson)
36 THE MORPHOLOGY OF PTERIDOPHYTES
rather irregular spiral. Whatever the appendages of Psilo-
phyton should be called, it is reasonable to call these leaves,
for they were up to 5 mm long, were dorsiventrally flattened
and were provided with stomata.
Compared with Rhynia, Asteroxylon Mackiei was much
more complex in its stem anatomy (Fig. 5B). In the centre
was a fluted rod of tracheids which, in transverse section,
had a stellate outhne. Some morphologists apply the term
*actinostele' to such a structure. It was, nevertheless, a solid
protostele, fundamentally, and its xylem consisted solely of
tracheids, either with spiral or with annular thickenings.
The smallest elements (protoxylem?) were near, but not
quite at, the extremities of the ridges, with the result that the
stele is described as mesarch. Surrounding the xylem, was a
zone of thin-walled elongated phloem cells. The cortex was
composed of three distinct layers, the middle one of which
was trabecular (i.e. it consisted of a wide space, crossed by
numerous radial plates of tissue), while the innermost and
the outermost were of compact parenchyma. Within any
transverse section through a leafy axis are to be seen
numerous small vascular bundles which, although called
*leaf traces', nevertheless stopped short without entering the
leaves. (These are omitted from Fig. 5B, for the sake of
clarity.) If traced inwards and downwards, they are seen to
have had their origin in one or other of the protoxylems.
No reproductive organs have been found actually in
organic connection with the leafy shoots of Asteroxylon
Mackiei, but, occurring along with them, were some
sporangial branches which are believed to represent the
fertile regions. These branches (Fig. 5C) were without leaves
and terminated in small-pear shaped sporangia about i mm
long (Fig. 5D). These contained spores in tetrads which were
shed by means of an apical dehiscence mechanism. Whether
these fertile branches were borne laterally or whether they
were the apical regions of the main axis is not known.
The appearance of Asteroxylon elberfeldense is known
PSILOPHYTOPSIDA 37
with more certainty and it lends support to the supposed
reconstruction of the Scottish species. A portion of the plant
is illustrated in Fig. 5E. The lower portions of the aerial axes
were clothed with leaves like those of ^. Mackiei, then came
a transition region with spine-Hke outgrowths like those of
Psilophytoji, while the distal regions were quite smooth.
Young developing branches were circinately coiled and the
tips of the ultimate branchlets were frequently recurved,
some of them bearing terminal sporangia. An interesting
feature of its internal anatomy was the presence of a central
pith region in the xylem of the larger axes — constituting a
medullated protostele.
It is impossible to overestimate the importance of the
Psilophytopsida to botanical thought. Their discovery not
only caused many botanists to abandon the classical theory
that there are three fundamental categories of plant organs
(stems, leaves and roots), but also led some of them to
develop new and far-reaching theories of land plant evolu-
tion. Thus, the simple Rhynia was adopted as the ideal
starting point for the 'telome theory' of Zimmermann—,
while Psilophyton and Asteroxylon were taken by others to
illustrate the 'enation theory' of the evolution of leaves.
These various theories will be discussed in greater detail in
the final chapter; in the meantime, one should bear in mind
the remarks of Leclercq^^ that these simple plants were by
no means the earhest land plants, that more complex plants
preceded them in the fossil record and that several other
types of land plant existed alongside them in Upper Silurian/
Lower Devonian times. These will be described in succeed-
ing chapters, along with the groups to which they are
beheved to be related.
3
Psilotopsida
Sporophyte rootless, with dichotomous rhizomes
and aerial branches. Lateral appendages spirally
arranged, scale-like or leaf-like. Protostelic (either
solid or meduUated). Sporangia thick walled,
homosporous, terminating very short lateral
branches. Antherozoids flagellate.
Psilotales
Psilotaceae Psilotum
Tmesipteridaceae Tmesipteris
This small group of plants is one of great interest to mor-
phologists because its representatives are at a stage of
organization scarcely higher than that of some of the earUest
land plants, despite the fact that they are living today. Their
great simphcity has been the subject of controversy for many
years, some morphologists interpreting it as the result of
extensive reduction from more complex ancestors. Others
accept it as a sign of great primitiveness.
Two species of Psilotum are known, P. nudum {=P.
triquetrum) and P.flaccidum {=P. complanatum), of which
the first is widespread throughout the tropics and subtropics
extending as far north as Florida and Hawaii and as far
south as New Zealand. Most commonly, it is to be found
growing erect on the ground or in crevices among rocks, but
it may also grow as an epiphyte on tree-ferns or among
other epiphytes on the branches of trees. P. flaccidum is a
38
PSILOTOPSIDA 39
much rarer plant, occurring in Jamaica, Mexico and a few
Pacific Islands, and is epiphytic with pendulous branches.
The organs of attachment in both species are colourless
rhizomes which bear numerous rhizoidal hairs and which,
in the absence of true roots, function in their place as organs
of absorption. In this, they are probably aided by a mycor-
rhizal association with fungal hyphae, that gain access to the
cortex through the rhizoids. Apical growth takes place by
divisions of a single tetrahedral cell which is prominent
throughout the hfe of the rhizome, except when dichotomy
is occurring. It is said^^ that this follows upon injury to the
apical cell as the rhizome pushes its way through the soil
and that two new apical cells become organized in the
adjacent regions. In any case, there is no evidence of a
median division of the original apical cell into two equal
halves ; to this extent, therefore, the rhizome cannot be said
to show true dichotomy.
In Psilotum nudum, some branches of the rhizome turn
upwards and develop into aerial shoots, commonly about
20 cm high, but as much as i m high in favourable habitats.
Except right at the base, these aerial axes are green and bear
minute appendages, usually described as 'leaves', despite the
fact that they are without a vascular bundle (cf. Psilophyton).
The axes branch in a regular dichotomous manner and the
distal regions are triangular in cross-section (Fig. 6A). In
the upper regions of the more vigorous shoots, the leaves
are replaced by fertile appendages (Fig. 6B) whose morpho-
logical nature has been the subject of much controversy.
Some have regarded them as bifid sporophylls, each bearing
a trilocular sporangium, but the interpretation favoured
here is that they are very short lateral branches, each bearing
two leaves and terminating in three fused sporangia.
Psilotum flaccidum differs from P. nudum in two import-
ant respects : its aerial branches are flattened and there are
minute leaf-traces which, however, die out in the cortex
without entering the leaves (cf. Asteroxylon).
40 THE MORPHOLOGY OF PTERIDOPHYTES
The internal anatomy of the rhizomes varies considerably,
according to their size, for those with a diameter of less
than I mm are composed of almost pure parenchyma, while
large ones possess a well-developed stele. Fig. 6C is a
diagrammatic representation of a large rhizome, as seen in
transverse section. In the centre is a solid rod of tracheids
with scalariform thickenings. As there is no clear distinction
between metaxylem and protoxylem, it is impossible to
decide whether the stele is exarch, mesarch or endarch.
Around this is a region which is usually designated as
phloem, although it is decidedly unlike the phloem of more
advanced plants, for its elongated angular cells are often
lignified in the corners. Surrounding this is a region of
'pericycle', composed of elongated parenchymatous cells,
and then comes an endodermis with conspicuous Casparian
strips in the radial walls. Three zones may often be dis-
tinguished in the cortex, the innermost of which is fre-
quently dark brown in colour because of abundant deposits
of phlobaphene (a substance formed from tannins by oxida-
tion and condensation). The middle cortex consists of
parenchymatous cells with abundant starch grains, while
the outer cortex contains, in addition, the hyphae of the
mycorrhizal fungus. In some cells the mycelium is actively
growing while in others it forms amorphous partially
digested masses.
In the colourless, or brown, transitional region at the base
of the aerial axes, the xylem increases in amount, becomes
medullated and spHts up into a variable number of separate
strands. This process of medullation continues higher up
the stem, as shown in Fig. 6D, and the central pith region
becomes replaced by thick-walled fibres. There is here a
transition from the protoxylem, with its helical or annular
helical thickenings, to scalariform metaxylem tracheids, the
protoxylem being exarch. The xylem is surrounded by a
region of thin-walled cells, not clearly separable as phloem
and pericycle, and the whole stele is enclosed in a well
Fig. 6
Psilotimi nudum: a, portion of plant, showing erect habit; b,
fertile region; c, t.s. rhizome; d, t.s. aerial shoot. Tmesipteris
tannensis: E, portion of plant, showing pendulous habit; f, g,
H, fertile appendages, viewed from different directions; i, t.s.
aerial shoot; J, t.s. distal region of shoot; k, theoretical inter-
pretation of sporangial apparatus of Psilotales ; l, m, abnormal
types of sporangial apparatus
(a, after Bold; b, e, f, g, h, Pritzel; J, Sykes)
42 THE MORPHOLOGY OF PTERIDOPHYTES
marked endodermis. The cortex is again divisible into three
regions, the innermost containing phlobaphene, the middle
region being heavily lignified and the outermost being
photosynthetic. The chlorophyllous cells in this outermost
region are elongated and irregularly 'sausage shaped', with
abundant air spaces between them, which connect with the
stomata in the epidermis. The leaves are arranged in a
roughly spiral manner in which the angle of divergence is
represented by the fraction i, but although internally they
are composed of chlorophyllous cells like those of the outer
cortex of the stem, they can contribute little to the nutrition
of the plant, for they are without stomata as well as having
no vascular supply.
In this last respect, the leaves are in marked contrast to
the fertile appendages, for these each receive a vascular
bundle, which extends to the base of the fused sporangia, or
even between them. In their ontogeny, too, they are markedly
different from the leaves, for they grow by means of an
apical cell, whereas the young leaf grows by means of
meristematic activity at its base.^^ Shortly after the two
leaves have been produced on its abaxial side, the apex of
the fertile appendage ceases to grow and three sporangial
primordia appear. Each arises as a result of perichnal
divisions in a group of superficial cells, the outermost
daughter cells giving rise, by further divisions, to the wall of
the sporangium, which may be as much as five cells thick at
maturity. The inner daughter cells provide the primary
archesporial areas, whose further divisions result in a mass of
small cells with dense contents. Some of these disintegrate
to form a semi-fluid tapetum, in which are scattered groups
of spore-mother cells, whose further division by meiosis
gives rise to tetrads of cutinized spores.
The genus Tmesipteris is much more restricted in its
distribution than Psilotum, for T. tannensis is known only
from New Zealand, Australia, Tasmania and the Polynesian
PSILOTOPSIDA 43
Islands, while another species, T. Vieillardi, is probably con-
fined to New Caledonia. (Some workers recognize a further
four species, of restricted distribution, although it is possible
that they warrant no more than subspecific status.) T.
tannensis most commonly grows as an epiphyte on the
trunks of tree-ferns or, along with other epiphytes, on the
trunks and branches of forest trees, in which case its aerial
axes are pendulous, but occasionally it grows erect on the
ground. By contrast, T. Vieillardi is more often terrestrial
than epiphytic. It may further be distinguished by its
narrower leaves and by certain details of its stelar
anatomy.
Like PsUotum, Tmesipteris is anchored by a dichotomous
rhizome with rhizoidal hairs and mycorrhizal fungus hyphae.
The aerial axes, however, seldom exceed a length of 25 cm
and seldom branch or, if they do so, then there is but a
single equal dichotomy. Near the base, the aerial axes bear
minute scale-hke leaves very similar to the leaves o^ PsUotum,
but elsewhere the branches bear much larger leaves, up to 2 cm
long, broadly lanceolate and with a prominent mucronate
tip (Fig. 6E). Their plane of attachment is almost unique
in the plant kingdom, for they are bilaterally symmetrical,
instead of being dorsiventral. They are strongly decurrent,
with the result that the stem is angular in transverse section
and they each receive a single vascular bundle which extends
unbranched to the base of the mucronate tip, but does not
enter it. In the distal regions of some shoots, the leaves are
replaced by fertile appendages which, like those oi PsUotum,
may be regarded as very short lateral branches, each bearing
two leaves and terminating in fused sporangia (normally
two) (Figs. 6F-6H).
The internal anatomy of the rhizome is so similar to that
of PsUotum that the same diagram (Fig. 6C) will suffice to
represent it. In the transition region of Tmesipteris tannensis
(Fig. 61), the central rod of tracheids becomes medullated and
sphts up into a variable number of strands which are mesarch
44 THE MORPHOLOGY OF PTERIDOPHYTES
(in contrast to the exarch arrangement in P silo turn), (T. Vieil-
lardi differs in having a strand of tracheids that continues up
into the aerial axis in the centre of the pith region.) Whereas
in the rhizome there is a well marked endodermis, in the
aerial axes no such region can be discerned. Instead, be-
tween the pericycle and the lignified cortex, all that can be
seen is a region of cells packed with brown phlobaphene.
The outer cortex contains chloroplasts, but the epidermis is
heavily cutinized and is without stomata. These are res-
tricted to the leaves (and their decurrent bases) which, like
the stem, are also covered with a very thick cuticle, but in
which are abundant stomata. The leaf-trace has its origin as
a branch from one of the xylem strands in the stem and
consists of a slender strand of protoxylem and metaxylem
tracheids surrounded by phloem. As the stem apex is
approached, the number of groups of xylem tracheids is
gradually reduced (Fig. 6J), all the tracheids being scalari-
form, even to the last single tracheid.
The vascular strand supplying the fertile appendages
branches into three, one to each of the abaxial leaves and
one to the sporangial region. The latter branches into three
again in the septum between the two sporangia. The early
stages of development closely parallel those in Psilotum,^^
giving rise to thick-walled sporangia containing large num-
bers of cutinized spores. Both sporangia dehisce simul-
taneously, by means of a longitudinal split along the top of
each.
When discussing the morphological nature of the fertile
appendages of the Psilotales, morphologists have made
frequent reference to abnormahties^* (the study of which is
referred to as 'teratology'). In both genera, the same types
of variation occur, some of which are represented diagram-
matically in Figs. 6L and 6M. The normal arrangement is
indicated in Fig. 6K — a lateral axis (shaded) terminating in
a sporangial region (black) and bearing two leaves (un-
shaded). In Fig. 6L one of the leaves is replaced by a com-
PSILOTOPSIDA 45
plete accessory fertile appendage, while in Fig. 6M both
leaves are so replaced and instead of the sporangial region
there is a single leaf. There has for a long time been a widely
held belief that freaks are 'atavistic', i.e. they are a reversion
to an ancestral condition. However, it must be stressed that
this beUef rests on very insecure foundations. As apphed
here, the conclusion has been that the reproductive organs
of the Psilotales are reduced from something more complex,
at one time assumed to have been a fertile frond. It may well
be, however, that the only justifiable conclusion is that, at
this level of evolution, leaf and stem are not clearly distinct
as morphological categories, and that they are freely inter-
changeable— interchangeable on the fertile appendages of
abnormal plants, just as, on any normal shoot, fertile
appendages replace leaves in the phyllotaxy.
Few botanists have had the good fortune to see living
specimens of the gametophyte (prothallus) stage of either
Psilotum or Tmesipteris, but all who have testify, not only to
their similarity to each other, but also to their remarkable
resemblance to portions of sporophytic rhizomes. So similar
are the prothalU and sex organs of Psilotum to those of
Tmesipteris that the same diagrams and descriptions will
suffice for both. Like the rhizomes the prothalli are irregu-
larly dichotomizing colourless cylindrical structures, covered
with rhizoids (Fig. 7A), and the similarity is further en-
hanced by the fact that they are also packed with mycor-
rhizal fungus hyphae. Both archegonia and antheridia are
borne together on the same prothallus (i.e. they are mon-
oecious), but because of their small size they cannot be used
in the field to distinguish prothaUi from bits of rhizomes.
Stages in their development are illustrated in Figs. 7B — H
(archegonia) and 7I — M (antheridia). ^^
The archegonium is initiated by a pericHnal division in a
superficial cell (Figs. 7B and 7C) which cuts off an outer
'cover cell' and an inner 'central cell'. The cover cell then
undergoes two anticUnal divisions, followed by a series of
46 THE MORPHOLOGY OF PTERIDOPHYTES
periclinal divisions to give a long protruding neck, composed
of as many as six tiers of four cells. The central cell, mean-
time, divides to produce a 'primary ventral cell' and a
'primary neck canal cell' (Fig. 7F). Beyond this stage
there are several possible variants, only one of which is
illustrated in Fig. 7G, where the primary ventral cell has
divided to give an egg cell and a ventral canal cell, while
the nucleus of the primary neck canal cell has divided
without any cross wall being laid down. In the mature
archegonium, however, most of the cells break down so as
to provide access to the egg cell from the exterior, through a
narrow channel between the few remaining basal cells of the
neck, whose walls, in the meantime, have become cutinized
(Fig. 7H).
The antheridium, likewise, starts with a perichnal division
in an epidermal cell (Fig. 7I). The outer cell is the 'jacket
initial' whose further divisions in an anticlinal direction give
rise to the single-layered antheridial wall, while the inner
'primary spermatogenous cell' gives rise to the spermato-
genous tissue, by means of divisions in many planes (Fig.
7L). At maturity (Fig. 7M) the antheridium is spherical,
projects from the surface of the prothallus and contains
numerous spirally coiled multiflagellate antherozoids (Fig.
7S). These escape into the surrounding film of moisture and,
attracted presumably by some chemical substance, find their
way by swimming to the archegonia, where fertilization
occurs.
Stages in the development of the young sporophyte from
the fertihzed egg are illustrated in Figs. 7N-R. The first
division of the zygote is in a plane at right angles to the axis
of the archegonium (Fig. 7O) giving rise to an outer 'epibasal
cell' and an inner 'hypobasal cell'. The latter divides re-
peatedly to give a lobed attachment organ called a 'foot'
(Fig. 7Q), while the epibasal cell, by repeated divisions,
gives rise to the first rhizome, from which other rhizomes
and aerial shoots are produced. Fig. 7R shows a young
PSILOTOPSIDA 47
sporophyte with three rhizomatous portions and a young
aerial shoot, the whole plant being still attached to the
gametophyte. This kind of embryology, where the shoot-
forming apical cell is directed outwards through the neck of
Fig. 7
Psilotum nudum: a, gametophyte; b-h, stages in development of
archegonium. Tmesipteris tannensis: i-m, stages in developing
antheridium; n-q, stages in developing sporophyte; r, young
sporophyte attached to prothallus ; s, spermatozoids
(a, q, s, after Lawson; b-h, Bierhorst; i-p, r, HoUoway)
the archegonium, is described as *exoscopic'. While relatively
unusual in pteridophytes, it is nevertheless universal in
mosses and hverworts. Indeed, the young sporophyte of the
liverwort Anthoceros is very similar indeed to that of
Tmesipteris, at least up to the stage illustrated in Fig. 7Q,
even in such details as the lobed haustorial foot, and some
morphologists have gone so far as to suggest some sort of
48 THE MORPHOLOGY OF PTERIDOPHYTES
phylogenetic relationship. However, until more is known of
the factors which determine the polarity of developing
embryos, such suggestions should be received with consider-
able caution.
For many years there has been speculation among
botanists as to the kind of life-cycle that might have been
exhibited by the earhest land plants. Some held the belief
that there was a regular alternation of sporophytes and
gametophytes that resembled each other in their vegetative
structure and that even their reproductive organs (sporangia
and gametangia, respectively) could be reconciled as having
a similar basic organization: on this basis, the generations
were regarded as 'homologous'. Others believed that the
sporophyte generation evolved after the colonization of the
land by gametophytic plants. From being initially very
simple, the sporophyte then evolved into something much
more complex, by reason of its possessing far greater poten-
tialities than the gametophyte. On this basis, the generations
were regarded as 'antithetic'. Until bona fide gametophytes
are described from the Devonian, or earlier, rocks, there is
little hope that this controversy will be resolved satis-
factorily. All that can be done is to examine the most
primitive living land plants and see whether, at this level
of evolution, the sporophyte appears to have fundamentally
different capabilities.
The extremely close similarity in external appearance
between the gametophytes of the Psilotales and their rhi-
zomes is, therefore, of more than passing interest. Until
1939, however, it was believed that there was one important
anatomical distinction between them, in that gametophytes
were without vascular tissue. In that year, Holloway^* des-
cribed some abnormally large prothalli of Psilotum from
the volcanic island of Rangitoto, in Auckland harbour. New
Zealand. These were remarkable in having well-developed
xylem strands, of annular and scalariform tracheids, sur-
rounded by a region of phloem which, in turn, was enclosed
PSILOTOPSIDA 49
by a clearly recognizable endodermis. There was, therefore,
almost no morphological feature distinguishing them from
the sporophytic rhizomes, except their archegonia and
antheridia. It was subsequently found^^ that the cells of these
prothalli contained twice as many chromosomes as those
from Ceylon (i.e. they were diploid), while the sporophytes
from this locality were tetraploid. To some botanists, this
appeared to be sufficient to explain the presence of vascular
tissue, and tended to diminish the importance of the similar-
ity of these gametophytes to the rhizomes. But it must be
emphasized that diploid prothalh are known elsewhere
among pteridophytes and that no morphological aberration
need necessarily accompany a simple doubling of the
chromosome number. This being so, then, whatever their
chromosome content, these abnormal vascularized prothalli
still provide strong support for the Homologous Theory of
Alternation of Generations. This topic is discussed further
in the final chapter.
Concerning chromosome numbers generally in the group,
it now appears that all plants of Psilotum nudum from Aus-
traha and New Zealand have the same chromosome number
n= 100-105, while plants from Ceylon are like Psilotum
flaccidum in having about half this number (n=52-54).
Tmesipteris tannensis has a chromosome number n=200+,
while of the six new species (or subspecies) recognized by
Barber^^ five have n=204-2io and one has n= 102-105. It is
suggested that both Psilotum and Tmesipteris occur in poly-
ploid series, but that both have the same basic number.
Lycopsida
Sporophyte with roots, stems and spirally arranged
leaves (microphylls). Protostelic (solid or medul-
lated) sometimes polystelic (rarely polycyclic). Some
with secondary thickening. Sporangium thick-
walled, homosporous or heterosporous, borne
either on a sporophyll or associated with one.
Antherozoids biflagellate or multiflagellate.
1 Protolepidodendrales*
Drepanophycaceae* Aldanophyton,"^ Baragwanathia*
Drepanophycus *
Protolepidodendraceae * Protolepidodendron *
2 Lycopodiales
Lycopodiaceae Lycopodites,^ Lycopodium,
Phylloglossum
3 Lepidodendrales*
Lepidodendraceae * Lepidodendron, * Lepidophloios, *
Bothrodendraceae* Bothrodendron"^
Sigillariaceae* Sigillaria*
Pleuromeiaceae* Pleuromeia*
4 Isoetales
Isoetaceae Nathorstiana* Isoetes, Stylites
5 Selaginellales
Selaginellaceae Selaginellites* Selaginella
50
LYCOPSIDA
51
Protolepidodendrales
Until 1953, when Aldanophyton was described from
Cambrian deposits in Eastern Siberia, ^^ Baragwanathia^^
was believed to be the earhest representative of the Lycop-
sida, for it occurs along with Yarravia in Silurian rocks of
Australia. It had fleshy dichotomizing aerial axes, thickly
clothed with leaves, and must have had a most remarkable
appearance, for the diameter of the axes ranged upwards
from I cm to 6*5 cm (Fig. 8A). In the centre was a slender
fluted rod of annular tracheids from which leaf traces passed
Fig. 8
Baragwanathia : A, fertile shoot. Drepanophyciis : b, reconstruc-
tion; c, sporophyll. Protolepidodendron: d, reconstruction;
E, leaf scars on large axis ; F. sporophyll
(a, after Lang and Cookson; b-f, Krausel and Weyland)
52 THE MORPHOLOGY OF PTERIDOPHYTES
out through the cortex into the leaves. The leaves were
about I mm broad and up to 4 cm long and, in fertile shoots,
they were associated with reniform sporangia arranged in
zones. The preservation of the specimens is not good enough
to show whether the sporangia were borne on the leaves or
merely among them, but that they were indeed sporangia is
estabhshed by the extraction of cutinized spores from them.
Not much is known of the growth habit of the plant, but
there are suggestions that the aerial branches arose from a
creeping rhizome. Drepanophycus (=Arthrostigma) and
Protolepidodendron both occurred in Lower and Middle
Devonian times: the former in Germany, Canada and
Norway; the latter in Scotland and Germany. Of the two,
Drepanophycus (Fig. 8B) was the more robust. Its aerial
axes were up to 5 cm thick and forked occasionally in a
dichotomous manner. It is beheved that they arose from
horizontal branching rhizomes. The aerial axes were covered
with spine-like outgrowths (up to 2 cm long) in a manner
reminiscent of Psilophyton, but with the difference that these
outgrowths had a vascular strand and could therefore
properly be called leaves. Some of them bore a single
sporangium either on the adaxial surface (Fig. 8C) or in
their axils, but these 'sporophylls' were scattered at random
over the axes instead of being gathered together into a
fertile zone.
Protolepidodendron (Fig. 8D) had dichotomous creeping
axes from which arose aerial axes up to 30 cm high and less
than I cm in diameter. All parts of the plant were clothed
(sometimes densely) with leaves having cushion-hke bases
and, in most species, bifurcated apices. Stems from which
the leaves had fallen showed a characteristic pattern of leaf-
bases (Fig. BE) arranged in a spiral manner. All the leaves
were provided with a single vascular strand and some of
them bore oval sporangia on their adaxial surfaces (Fig. 8F)
but, as in Drepanophycus, such sporophylls were not aggre-
gated into special fertile regions. Details of the stem ana-
LYCOPSIDA 53
tomy of Protolepidodendron are difficult to make out, but
there appears to have been a sohd three-angled protostele
in the centre, with some suggestion of a mesarch proto-
xylem.
Whether Aldanophyton was really a member of the Lycop-
sida cannot be determined with certainty, for no fertile
portions of the plant have been described. It had stems up to
13 mm in diameter, clothed with narrow leaves up to 9 mm
long and, although the preservation of the specimens leaves
much to be desired, one published photograph looks not
unlike Fig. 8E. Whatever its true affinities, this plant is an
important discovery, for it seems fairly certain that it was
a land plant and it therefore pushes further back into
antiquity the origin of land plants by some 200 million
years.
Lycopodiales
This group contains two genera of living plants, Lycopodium
('Club-mosses') and Phylloglossum, and one fossil genus,
Lycopodites. Of the 200 species of Lycopodium, the majority
are tropical in distribution, but some occur in arctic and
alpine regions. Phylloglossum, by contrast, is monotypic and
the single species, P. Drummondii, is restricted to New
Zealand, Tasmania and the south-eastern corner of
Australia. Not only do the various species of Lycopodium
occur in widely different cHmatic regions ; they also occupy
widely different habitats, for some are erect bog-plants,
others are creeping or scrambling, while yet others are
pendulous epiphytes, and this wide range of growth form is
paralleled by an extremely wide range of anatomical
structure. Indeed, some taxonomists have suggested that the
genus should be split into at least four new genera, so differ-
ent are the various species from one another. Whatever their
status, the following sections and subsections of the genus
are recognized by most botanists. ^^
54 THE MORPHOLOGY OF PTERIDOPHYTES
A Urostachya
1 Selago
2 Phlegmaria
B Rhopalostachya
1 Inundata
2 Clavata
3 Cernua
Members of the Urostachya never have creeping axes, but
have erect or pendulous dichotomous aerial axes, according
to whether they are terrestrial or epiphytic. Their roots
emerge only at the base of the axes, for although they have
their origin in more distal regions, they remain within the
cortex (many being visible in any one transverse section of
the stem). Perhaps the most important character, phylo-
genetically, is the lack of specialization of the sporophylls
which, as a result, resemble the sterile leaves more or
less closely. Another characteristic is that vegetative repro-
duction may frequently take place by means of bulbils.
These are small lateral leafy stem-structures which occur in
place of a leaf and which, on becoming detached, may
develop into complete new plants. The members of the
Rhopalostachya, by contrast, never reproduce by means of
bulbils. They are all terrestrial and, although the first formed
horizontal axes may be dichotomous, those formed later
have the appearance of being monopodial, by reason of their
unequal dichotomy, as also do the erect branch-systems.
Roots may emerge from the leafy branches, particularly in
the creeping parts of the plant.
Of the two sections, the Urostachya (and in particular
those belonging to the Selago subsection) are usually re-
garded as the more primitive. The British species Lycopodium
selago is illustrated in Fig. 9A. Its sporophylls (Fig. 9B) are
very similar indeed to the sterile leaves (Fig. 9C) and occur
at intervals up the stem, fertile zones alternating with sterile.
L. squarrosum shows a sUght advance on this, in that the
Fig. 9
Lycopodium selago : A, plant ; b, sporophyll ; c, leaf. L. inundatum:
D, plant; e, sporophyll; f, leaf. L. annotiniim: G, plant. L.
clavatum: H, plant; i, sporophyll; J, leaf. L. phlegmaria: k,
plant. L. volubile: l, plant; m, sterile branch; n, fertile branch
(b-j, after Hooker; k-n, Pritzel)
56 THE MORPHOLOGY OF PTERIDOPHYTES
sporophylls are aggregated in the terminal regions of the
axes, yet they can hardly be said to constitute a strobilus,
for the sporophylls do not differ from the sterile leaves to
any marked extent. All the species of the Phlegmaria sub-
section are epiphytic. L. phlegmaria itself is illustrated in
Fig. 9K. The pendulous dichotomous branches terminate
in branched strobih in which the sporophylls are smaller
and more closely packed than the sterile leaves but,
nevertheless, afford relatively little protection for the
sporangia.
The Inundata subsection of the Rhopalostachya is repre-
sented by the British species Lycopodium imindatum (Fig.
9D). Here, the strobilus is only slightly different in appear-
ance from the vegetative shoot, for the sporophylls (Fig.
9E) are only sUghtly modified for protecting the sporangia
(cf. sterile leaf. Fig. 9F). Within the Clavata subsection are
three more British species, L. annotimim, L. clavatiim and
L. alpinum, of which the first two are illustrated (Figs. 9G
and 9H). In this group, the sporophylls are aggregated into
very distinct strobili and are very different from the sterile
leaves, for they are provided with an abaxial flange (Fig. 9I)
which extends between and around the adjacent sporangia
belonging to the sporophylls below (cf. sterile leaf. Fig. 9J).
Whereas the strobih of L. annotinum terminate normal leafy
branches, those of L. claxatum are borne on specially
modified erect branches, whose leaves are much smaller and
more closely appressed. There are, thus, two different kinds
of sterile leaf in this species. The Cernua subsection includes
a number of species with very different growth habits.
L. cernuum has a creeping axis, from which arise at intervals
erect branch-systems resembhng tiny fir trees in being appar-
ently monopodial (for this reason sometimes called 'ground
pines'). In this species, all the sterile leaves are alike, but in
L. volubile (Fig. 9L) there are three or four kinds of sterile
leaves. It is a plant with a scrambhng habit and its main
axes are clothed with long needle-shaped leaves arranged
LYCOPSIDA 57
spirally, while the lateral branches are dorsiventral and
superficially frond-Hke. On these branches there are four
rows of leaves, two lateral rows of broad falcate leaves (Fig.
9M), an upper row of medium sized needle-hke leaves and a
row of minute hair-hke leaves along the under side. This
species, therefore, like several others in this section is highly
*heterophyllous'. The lateral branches in the more distal
regions of the plant are fertile and terminate in long narrow
strobih, which are frequently branched. As in the Clavata
subsection, the closely appressed sporophylls have, on their
dorsal (abaxial) side, either a bulge or a flange which pro-
vides some protection for the sporangia below.
The apical region of the stem in Lycopodhim differs
markedly from species to species, for it is almost flat in
L. selago, yet extremely convex in L. complanatum. In the
past, opinions have diff'ered as to whether growth takes
place from an apical cell, but it now appears that this is not
the case^^ and that any semblance of an apical cell is an
illusion caused by studying an apex just at the critical
moment when one of the surface cells is undergoing an
obhque division. All species are now held to grow by means
of an 'apical meristem', i.e. a group of cells undergoing
periclinal and antichnal divisions.
The sporehngs of all species are alike in their stelar
anatomy, for the xylem is in the form of a single rod with
radiating flanges. In transverse section these flanges appear
as radiating arms, commonly four in number. As the plant
grows, the later-formed axes of most species become more
complex, the xylem sphtting up into separate plates or into
irregular strands. However, some species retain a simple
stellate arrangement throughout their life, as in L. serration
(Fig. iiF) where there are commonly five or six radiating
arms of xylem. It is interesting that this species belongs to
the Selago subsection which on other grounds is regarded as
the most primitive, for some botanists, applying the doctrine
of recapitulation, have held that the embr>'onic structure of a
58 THE MORPHOLOGY OF PTERIDOPHYTES
plant indicates what the ancestral adult condition was like.
The stele of L. selago is similar to that of L. serratum, and
the number of radiating arms of xylem may be as low as
four. This is supposed to represent the ancestral condition
and the Selago subsection is regarded as primitive in its
stelar anatomy, as well as in its lack of a well defined strobilus.
Alternating with the xylem arms are regions of phloem,
separated from them by parenchyma, and the whole is sur-
rounded by parenchymatous 'pericycle', outside which is an
endodermis. The xylem strand of L. selago sometimes shows
a slight advance on this arrangement, in that it may be
separated into several areas with a variable number of
radiating arms. L. clavatumhsis a number of horizontal plates
of xylem, alternating with plates of phloem. An even greater
number of such plates is found in L. volubile (Fig. iiC).
To some extent this trend appears to be bound up with an
increasing dorsiventraUty of the shoot, which reaches its
culmination in the heterophyllous L. volubile. L. annotinum
lends some support to this idea, for its horizontal axes are
like those of L. clavatum, whereas its vertical axes are more
like those of L. selago. However, exceptions are numerous
and it may well be that no valid generalization of this kind
can be made.*^
Quite a different kind of complexity is illustrated by Ly co-
podium squarrosum (Fig. iiE), also placed in the Selago
subsection. A transverse section of the stem of this species
shows not only radiating arms of xylem, but also islands,
within the xylem, lined with parenchyma and containing
apparently isolated strands of phloem. Actually, however,
the whole structure is an anastomosing one, so that no
regions of phloem, or of xylem, are really isolated. This
process of elaboration has gone even further in L. cernuum,
where the appearance is of a sponge of xylem with phloem
and parenchyma filHng the holes (Fig. iiD).
Throughout the genus, the stele is exarch, the proto-
xylem elements being clearly recognizable by their 'indirectly
LYCOPSIDA 59
attached annular thickenings'^^ (i.e. occasional intercon-
nections occur between adjacent rings), while the meta-
xylem tracheids are either scalariform or have circular
bordered pits. The phloem consists of sieve cells which are
elongated and pointed, with sieve areas scattered over the
side walls. The endodermis is clearly recognizable, in young
stems only, when casparian strips may be seen. In older axes,
however, the walls become heavily hgnified along with the
cells of the inner cortex and their identity becomes obscured.
This lignified region extends through most of the cortex in
some species, whose stems are consequently hard and wiry,
while in other species, e.g. L. squarrosum, the stem may be
thick and fleshy. Stomata are present in the epidermis of the
stem and in the leaves where, in some species, they are on both
surfaces (*amphistomatic') and, in others, only on the under
side ('hypostomatic'). The leaves of some species are arranged
in a whorled or a decussate manner, but in most are spirally
arranged. However, in these, the phyllotactic fractions are
said to be unlike those of other vascular plants in forming
part of the series f, |, xt etc.^ (whereas the normal
phyllotactic fractions, J, J, f, f, y\ etc., are dervied
from the Fibonacci series). Each leaf receives a single trace,
which has its origin in one of the protoxylems of the stem
stele and continues into the leaf as a single unbranched vein
composed entirely of spirally thickened tracheids. It is of
interest that, in L. selago, the bulbils also receive this kind of
vascular bundle, for this supports the view that, at this level
of evolution, there is no clear morphological distinction
between the categories 'leaf and 'stem'. This is further sup-
ported by the fact that leaf primordia may be transformed
by suitable surgical treatment into regenerative buds.^^
The so-called 'roots', too, show varying degrees of simi-
larity to stems. All, except the first root of the sporehng, are
adventitious and endogenous in origin, arising in the peri-
cycle, and they are peculiar in not bearing endogenous
laterals. Instead, they branch dichotomously (very regularly
60 THE MORPHOLOGY OF PTERIDOPHYTES
in some species). They are provided with a root cap and
their root-hairs are paired (a most pecuHar arrangement).
The majority are diarch with a crescent-shaped xylem area,
but in some species the stele is very similar to that of the
stem, as in Lycopodium clavatum, where the xylem takes the
form of parallel plates.
Variations from species to species in the shape of the
sporophylls have already been described. In addition, there
is considerable variation in the manner in which the
sporangium is borne in relation to the sporophyll. In some,
e.g. Lycopodium selago and L. inundatum, the sporangium
is in the angle between the sporophyll and the cone axis, i.e.
it is axillary. In others, e.g. L. cernuum and L. clavatum (Fig.
loC), the sporangium is borne on the adaxial surface of the
sporophyll and may be described as *epiphyllous'. The
sporangial initials arise at a very early stage in the ontogeny
of the strobilus, normally on the ventral side of the sporo-
phyll, but in some species actually on the axis, whence they
are carried by subsequent growth changes into the axil. The
first sign of sporangial initials is the occurrence of perichnal
divisions in a transverse row of cells (three to twelve in
number) (Fig. loA). The innermost daughter cells provide
the archesporial cells by further division and also contribute
to the stalk of the sporangium, while the outermost cells (the
jacket initials) give rise to the wall of the sporangium (Fig.
loB). This is three cells thick just before maturity, but then
the innermost of the layers breaks down to form a tapetal
fluid. Like the sterile leaves, the sporophyll has a single vein,
which passes straight out into the lamina, leaving the
sporangium without any direct vascular supply. The mature
sporangium is kidney-shaped and dehisces along a trans-
verse line of thin-walled cells, so liberating the very numerous
and minute spores into the air.
In some species, the spores germinate without delay, while
still on the surface of the ground, but in others there may be
a delay of many years, by which time they may have become
Fig. 10
Lycopodium clavatum: A, b, c, stages in sporophyll development;
H, prothallus; J-o, stages in archegonial development; u-z,
embryology of young sporophyte. L. cermium: G, prothallus;
I, archegonium; q-t, embryology. L. Selago: e, surface-livmg
prothallus; f, subterranean prothallus; p, young sporophyte.
Phylloglossum Drummondii: D, complete plant
(f, foot; 1, leaf; r, root; s, suspensor; t, tuber; x, stem apex)
(e, f, j-o, u-z, after Bruchmann; g, i, q-t, Treub)
62 THE MORPHOLOGY OF PTERIDOPHYTES
deeply buried. Surface living prothalli are green and photo-
synthetic, but subterranean ones are, of necessity, colourless
and are dependent on a mycorrhizal association for their
successful development. Indeed, a mycorrhizal association
appears to occur in all species growing under natural con-
ditions, whatever their habit. As a generaUzation, it may be
said that those species inhabiting damp tropical regions
germinate rapidly and have green prothalli, whereas those of
cooler regions tend to germinate slowly and produce sub-
terranean prothalli. Lycopodium selago is interesting in this
respect, for it shows variabihty. Fig. loE illustrates a surface
living prothallus with photosynthetic upper regions, in
addition to the fungal hyphae in the lower parts (and
rhizoids). Fig. loF, on the other hand, is of a subterranean
prothallus, with fungal hyphae in the lower regions but
covered all over with rhizoids. Archegonia and antheridia are
restricted to the upper parts in both cases. L. cernuum pro-
vides an example of a surface-living prothallus (Fig. loG).
It is roughly cyUndrical and the upper regions bear numer-
ous green photosynthetic lobes, among which are borne the
gametangia. In L. clavatum (Fig. loH) and L. annotinum the
prothallus is colourless and subterranean; it is an inverted
cone with an irregular fluted margin, growing by means of a
marginal meristem which remains active for many years, and
the gametangia are developed over the central part of the
upper surface. Epiphytic species, e.g. L. phlegmaria, also
have colourless prothalli, but they are very slender, they
branch and they exhibit pronounced apical growth.
Archegonia and antheridia each arise from a single super-
ficial cell in which a periclinal division occurs. The subse-
quent cell divisions in the antheridial initials are similar to
those described for Tmesipteris (Fig. 7), but the mature
antheridium differs in being sunken into the tissues of the
prothallus. The archegonium diff'ers from that of Tmesipteris
in having several neck canal cells, which vary in number
according to whether the prothallus is subterranean or
LYCOPSIDA 63
surface living. In the latter species, the neck is very short
e.g. Lycopodium cernuum (Fig. lol), and there may be just
a single canal cell, apart from the ventral canal cell. At the
other extreme, the number of canal cells may be as high as
fourteen in L. complanatum (in the Clavata subsection),
while L. selago is intermediate, with about seven. Various
stages in the development of L. clavatum are illustrated in
Figs. loJ-N. At maturity all the canal cells break down and
part of the neck may also wither (Fig. loO). The anthero-
zoids are pear-shaped and swim by means of two flagella
at the anterior end, attracted chemotactically by citric acid
diffusing from the archegonium.^*
The orientation of the embryo in Lycopodium is endo-
scopic and this is determined at the first division of the
zygote, with the laying down of a cross wall in a plane at
right angles to the axis of the archegonium (Fig. loU). The
outermost cell, called the 'suspensor', undergoes no further
divisions, but the innermost cell gives rise to two tiers of four
cells, called the 'hypobasal' and 'epibasal' regions respectively
(Fig. loW). It is from the epibasal (innermost) tier that the
young plant is ultimately derived, by further divisions. The
hypobasal region remains small in some species, and in
others it swells up into a structure commonly called a *foot'.
L. clavatum is an example of the latter and various stages are
illustrated in Figs. loU-Z. In Fig. loX, the three regions of
the embryo are clearly demarcated (the suspensor cell, *s' ;
the middle hypobasal region, already beginning to swell
into a foot, 'f; the epibasal region with a stem apex, *x',
becoming organized), and the axis of the embryo has bent
through a right angle. This bending of the axis proceeds
further in Fig. loY and is completed in Fig. loZ, where, by
turning through two right angles, the stem apex is pointing
vertically upwards. The first root, 'r', is seen to be a lateral
organ, not forming part of the axis of the embryo, as indeed
is the case in all pteridophytes : not until the level of the seed
plants does the root (radicle) form part of the embryonic
64 THE MORPHOLOGY OF PTERIDOPHYTES
Spindle. L. selago (Fig. loP) is similar, except that the
hypobasal region does not swell up into a large foot.
Lycopodium cernuum (Figs. loQ-T) is an example of a very
different kind of embryology. As in L. selago, the hypobasal
region remains relatively small, but the organizing of a stem
apex is considerably delayed. The epibasal portion breaks
through the prothalhal tissue and swells out into a tuberous
'protocorm', 't'. Roughly spherical at the start, it is provided
with rhizoidal hairs and mycorrhizal fungus. On its upper
surface a cyhndrical green leaf ('protophyll'), '1', appears and
then, as the protocorm slowly grows, further protophylls
appear in an irregular manner. This stage may persist for a
long time and secondary protocorms \' may be formed as
shown in Fig. loT. Finally, however, a stem apex V
becomes organized and a normal shoot grows out. This type
of development has led, in the past, to much speculation as
to its phylogenetic significance, for the protocorm was held
by some to represent an atavistic survival of an ancestral
condition. However, Wardlaw^^ has offered an alternative
explanation, based on the metaboUsm of the prothallus and
young sporophyte in the various species of Lycopodium. He
suggests that an abnormally high carbon /nitrogen ratio may
delay the organization of a stem apex and may lead, also, to
a swelhng of the tissues, such being expected where mycor-
rhizal nutrition is supplemented by photosynthesis. On this
basis, the protocorm might well be regarded as a derivative
and retrograde development, rather than as a sign of
primitiveness.
When all facts are considered, it is Lycopodium selago
which is usually regarded as the most primitive species, in
lacking an organized strobilus, in having a relatively simple
vascular structure and in showing variabihty in behaviour in
its prothallus, but such conclusions can only be speculative
in the absence of clear fossil evidence. While there are fossil
remains, known as Lycopodites, they contribute Uttle to
these discussions. No petrified specimens have been found
LYCOPSIDA 65
and some of the mummified remains are now known to be
those of conifers. Some had well organized strobih ; others
did not. Lycopodites stockii, from the Lower Carboniferous
of Scotland, appears to have been heterophyllous, with its
leaves in whorls, and to have had a terminal cone as well as
scattered sporophylls among the sterile leaves. Clearly, there-
fore, this species was very different from the modern L.
selago and, in some respects, was nearer to some members
of the Phlegmaria subsection.
The sporophyte of Phylloglossum Drummondii, illustrated
in Fig. loD, is never more than about 4 cm high and appears
above ground only during the winter months, when it
develops a few cylindrical leaves like the protophylls of
Lycopodium cernuum. The most robust specimens develop,
in addition, a single erect stem terminating in a tiny strobilus.
During the hot summer months, when the ground is baked
hard, all the aerial parts wither and the plant survives this
unfavourable season as a tuber. Each year a new tuber is
formed (sometimes two or even three) from the apex of a
lateral stem-like structure, which grows out and downwards.
This parallel with the behaviour of the protocorm of L.
cernuum (Fig. loT) has led to the suggestion that Phyllo-
glossum exhibits *neoteny', in being able to produce spor-
angia while still in an embryonic stage of development.
Whatever the truth of this, it would certainly seem that some
of its pecuharities are adaptations which enable it to survive
adverse environmental conditions as a geophyte. From the
morphogenetic point of view, it is possible to see the
tuberization as a response to a high carbon /nitrogen ratio,
since the prothallus is both photosynthetic and mycorrhizal.
Perhaps all three 'causes' may apply, for they are not in-
compatible with each other and merely represent different
'grades of causality'.
Chromosome counts for Phylloglossum show a haploid
number n = about 255, with many unpaired chromosomes
at meiosis, suggesting a high degree of hybridization in its
c
66 THE MORPHOLOGY OF PTERIDOPHYTES
ancestry. Such a high number is beheved by some to be
characteristic of primitive plants, and in this connection it
is interesting to find that Lycopodium selago has a haploid
number n=i30, whereas species in other sections of the
genus have lower numbers (L. clavatum and L. annotinum
n = 34). But such a belief is justified only as a generalization.
High chromosome numbers may well point to ancient
origins in the majority of cases, but not in all, for polyploidy
could have occurred at any stage in the evolution of an
organism. Whenever it did occur, further evolution would
be retarded because of the masking of subsequent mutations.
Thus, if it occurred long ago, the ancient condition would
have become 'fixed', as may have happened in L. selago;
whereas, if it had happened recently, it would be possible for
an advanced morphological condition to be associated with
a high chromosome number, as in Phylloglossum perhaps.
By contrast with the Protolepidodendrales and the
Lycopodiales, which are homosporous, the three remaining
orders of the Lycopsida (Lepidodendrales, Selaginellales
and Isoetales) are heterosporous. Another feature that they
share is the possession of a ligule, on the basis of which they
are sometimes grouped together as the Ligulatae. The hgule
is a minute tongue-like membranous process, attached by a
sunken 'glossopodium' to the adaxial surface of the leaves
and the sporophylls. A study of hving heterosporous lyco-
pods shows that it reaches its maximum development while
the associated primordium of the leaf or the sporophyll is
still quite small. The mucilaginous nature of the cells and
the lack of a cuticle have led to the suggestion that the hgule
may keep the growing point of young leaves and young
sporangia moist, but the fact is that no-one knows its true
function. It may even be a vestigial organ whose function
has been lost.
'\ ■S€£%?---;.'- ^
;60
200
i
Primary Wood
Mixed Pith
10O
Pith
0 Protoxylem
— • — • — .— Endodermis
Fig. 11
Various Lycopod steles: a, Lepidophloios Wuenschianus. b,
Lepidodendron selaginoides. c, Lycopodium volubile. d, L.
cernuum. E, L. squarrosum. f, L. serratum
N.B. Leaf-traces have been omitted for the sake of clarity
(a, b, after Hirmer; c. d, Pritzel; e, Jones)
68 THE MORPHOLOGY OF PTERIDOPHYTES
Lepidodendrales
The Lepidodendrales, over 200 species of which are known,
first appeared in Lower Carboniferous times and reached
their greatest development in the Upper Carboniferous
swamp forests, in which members of the Lepidodendraceae,
Bothrodendraceae and Sigillariaceae were co-dominant with
the Calamitales and formed forests of trees 40 m or more in
height. The fourth family, Pleuromeiaceae, is represented
by a much smaller plant, Pleuromeia, from Triassic rocks,
and approached more nearly to the modern Isoetales. The
Carboniferous genera had stout trunks, some with a crown
of branches, others hardly branching at all, but all possessed
the same type of underground organs, known collectively as
Stigmarian axes. Some species of Lepidodendron, (e.g. L.
obovatum. Fig. 12A) showed very regular dichotomies in its
crown of branches, but others approximated to a mono-
podial arrangement because of successive unequal dicho-
tomies. While the trunks and branches of all species of
Lepidodendron and Lepidophloios were protosteHc and
exarch, there was nevertheless considerable variation in
stelar anatomy, from species to species, and from place to
place within one individual. Some species had soHd proto-
steles, others meduUated protosteles; some had abundant
secondary wood produced by a vascular cambium, some had
little and others had none at all; in some, the stele of the
trunk had secondary wood, while that of the branches
lacked it altogether. Thus, Lepidodendron pettycurense and
L. Rhodumnense (both Lower Carboniferous species) had
soUd protosteles, the former having secondary wood in
addition, but the latter being without it. Lepidodendron
selaginoides ( = L, vasculare), from the Coal Measures, pro-
vides an interesting case of partial meduUation, for the
central region of the axis consisted of a mixture of parenchy-
ma and tracheids, round which was a solid ring of tracheids.
The secondary wood of this species was often excentric in
its development, as illustrated in Fig. iiB.
LYCOPSIDA 69
Lepidophloios Wuenschianus, from the Lower Carbonifer-
ous of Arran, is known in considerable detail, for examples
have been found in which portions of the stele from various
levels had fallen into the rotted base of the trunk before
petrifaction occurred. This has made it possible to discover
something about the growth processes taking place in the
young aerial stem. The primary wood near the base was
soUd and only 5-5 mm across, halfway up the trunk it was
medullated, while near the top (Fig. 11 A) it was 15 mm
across and had a hollow space in the centre of the medulla.
It is concluded that, as the stem grew, its apical meristem
grew more massive and laid down a much broader pro-
cambial cylinder. Meantime, the cambium in the lower
regions had laid down more secondary wood than higher up,
with the result that the total diameter of the wood (primary
and secondary together) was about the same throughout the
length of the trunk (about 7 cm). In proportion to the over-
all diameter of the trunk (40 cm), however, this quantity of
wood is surprisingly small, when compared with that of a
dicotyledonous tree, where most of the bulk is made up of
wood. The difference probably Ues in the fact that the wood
of modern trees is concerned with two functions, conduc-
tion and mechanical support, whereas the wood of Lepido-
dendrales was concerned only with conduction. Mechanical
support was provided mainly by the thick woody periderm
which was laid down round the periphery of the trunk.
The metaxylem was composed of large tracheids with
scalariform thickenings, while the protoxylem elements
were much smaller and frequently had spiral thickenings.
The secondary wood consisted of radial rows of scalariform
tracheids and small wood-rays, through which leaf-traces
passed on their way out from the protoxylem areas. In most
specimens the phloem and even some of the cortex had
decayed before petrifaction occurred, but what is known of
the phloem suggests that it was small in amount and very
similar to that of modern lycopods.
70 THE MORPHOLOGY OF PTERIDOPHYTES
The primary cortex was relatively thin-walled and, within
it, a number of different regions are recognizable. Of these,
the most interesting is the so-called 'secretory tissue', made
up of wide thin-walled cells, whose horizontal walls became
absorbed in the formation of longitudinal ducts. Each leaf-
trace, as it passed through this region, acquired a strand of
similar tissue which ran parallel with it before splitting
into two 'parichnos strands' on entering the base of the leaf.
It is beheved that the secretory tissue was in some way
connected with the aeration of the underground organs, pro-
viding an air path from the stomata of the leaves, through
the mesophyll to the parichnos strand and so to the secretory
zone, which was continuous with a similar region in the
cortex of the Stigmarian axes.
The leaves, known as Lepidophyllum, were borne in a spiral
with an angle of divergence corresponding to some very
high Fibonacci fraction such as -fir^, -Us, etc. They
were Hnear, up to 20 cm long, triangular in cross-section
and with stomata in two longitudinal grooves on the
adaxial side. The vascular strand remained unbranched as
it ran the length of the leaf. The leaves were shed from the
trunk and larger branches by means of an absciss layer, and
the shape of the remaining leaf base and scar provides im-
portant details for distinguishing the various genera and
species. Fig. 12B shows the appearance of the trunk of a
Lepidodendron where, characteristically, the leaf bases were
elongated vertically. In some species, the leaf bases became
separated shghtly as the trunk increased in diameter, but in
others they remained contiguous, even on the largest axes.
No doubt this was brought about to some extent by an
increase in the size of the leaf base, much as a leaf scar
becomes enlarged on the bark of many angiospermous trees,
but such increase must have been relatively slight, for other-
wise the leaf bases would have become much broader in
proportion to their height. Evidently, therefore, the largest
leaf bases must have been large from the start, from which
Fig. 12
Lepidodendron : a, reconstruction; b, c, leaf bases. Lepidostrobus :
D, l.s. of an idealised cone; e, t.s. sporophyll. Lepidocarpon:
F, t.s.; G, l.s. Sigillaria: h, reconstruction; i, leaf bases. Stig-
marian appendages: J, t.s. (1, ligule pit; 2, area of leaf base; 3,
vascular bundle; 4, parichnos scars; 5, sporangium wall; 6,
flange of sporophyll; 7, ligule)
(a, b, c, h, I, after Hirmer; f, Scott; g, Hoskins and Cross)
72 THE MORPHOLOGY OF PTERIDOPHYTES
it follows that the axes bearing them must also have been
large, even when young.^eb Details of Sitypical Lepidodendron
leaf base are illustrated in Fig. 12C. Within the area of the
leaf scar (2) are to be seen three smaller scars, representing
the leaf-trace (3) and the two parichnos strands (4). Above
this hes the Hgule pit (i) and, in some species, below it are
two depressions that were once thought to be associated
with the parichnos system, but are now known to be caused
by shrinkage of thin-walled cells within the leaf cushion.
Lepidophloios is distinguished by its leaf bases being
extended horizontally, instead of vertically. Otherwise, the
anatomy of the trunks is indistinguishable from that of
Lepidodendron. Indeed, it has been suggested that the differ-
ences do not warrant a separation into two genera. However,
there were differences ; in the way the cones were borne. In
Lepidodendron, they were nearly always terminal, whereas
in Lepidophloios, they were borne some distance behind the
branch tip in a cauliflorous manner.
The cones of both genera are known as Lepidostrobus and
they consisted of a central axis around which sporophylls
were arranged in a compact spiral, their apices overlapping
so as to protect the sporangia. Further protection was
afforded by a dorsal projection, or 'heel', as illustrated in
the ideaHzed longitudinal section. Fig. 12D. The cones
varied in length from 5 cm to over 40 cm and must have
looked Hke those of modern conifers. Some cones contained
only megasporangia, others only microsporangia, while
others were hermaphrodite. In the latter, the megasporo-
phylls were at the base and the microsporophylls towards
the apex, as illustrated in Fig. 12D. This is the reverse of
the arrangement in gymnosperms and angiosperms, where
the microsporangial organs lie below the megasporangial
whenever they happen to be associated in a hermaphrodite
*flower'. The sporangia of Lepidostrobus were elongated and
attached throughout their length to the *stalk' of the sporo-
phyll, which was relatively narrow, compared with the
LYCOPSIDA 73
expanded apex of the sporophyll (Fig. 12E). The sporangium
wall was only one cell thick at maturity and dehisced along
its upper margin. Megaspores and microspores must have
been produced in enormous numbers, for they are extremely
abundant in all coal-measure deposits. Some megaspores
have been found with cellular contents, representing the
female prothallus, retained within the megaspore wall
('endosporic') as in Selaginella today, and occasionally
archegonia can be recognized.
The number of megaspores produced within each mega-
sporangium- varied considerably from species to species, and
in some was restricted to one. In Lepidocarpon (Figs. 12F
and 12G) the megaspore was retained in the sporangium,
which, in turn, was enveloped by two flanges from the stalk
of the sporophyll. The whole structure was shed Hke a seed
from the parent plant and has been regarded by some
botanists as actually being a stage in the evolution of a
seed. It would be much safer, however, to regard Lepido-
carpon as merely analogous to a seed, for the sporophyll
flanges are quite unlike the integuments of true seeds, except
perhaps in function. It is not known whether the micro-
spores germinated within the sht-hke 'micropyle' while the
megasporophyll was still on the tree, or whether it did so
after it had fallen to the ground.
Sigillaria (Fig. 12H) is characterized by the arrangement
of its leaf bases in vertical rows (Fig. 12I). It branched
much less than Lepidodendron or Lepidophloios and it bore
its cones in a cauliflorous manner. Furthermore, the leaves
were much longer, up to i m, grass-Hke and, in some species,
had two veins, possibly formed by the forking of a single
leaf-trace. Species from the Upper Carboniferous were
similar to Lepidodendron and Lepidophloios in their internal
anatomy, having a medullated protostele with a continuous
zone of primary wood. Some of the Permian species, e.g. S.
Brardi, however, showed a further reduction of the primary
wood, which was in the form of separate circummedullary
74 THE MORPHOLOGY OF PTERIDOPHYTES
Strands. This is most interesting, for it represents the
culmination of a trend which was also taking place, at
the same time, among several groups of early gymnosperms,
from the sohd protostele, through medullated protosteles
(first with mixed pith and then with pure pith) to a pith
surrounded by separate strands of primary wood.
From a distance, Bothrodendron must have looked very
similar to Lepidophloios, for it had a stout trunk with a
crown of branches covered with small lanceolate leaves and
its cones {Bothrodendrostrobus) were borne in a cauhflorous
manner. It differed, however, in the external appearance of
the trunk, for it had circular leaf scars that were almost
flush with the surface.
The underground organs of all the genera of Lepido-
dendrales so far described were so similar that they are all
placed in the form genus Stigmaria, and many are placed in
a single artificial species, S. ficoides. The base of the trunk
bifurcated once and then immediately again, to produce
four horizontal axes, each of which continued to branch
dichotomously many times in a horizontal plane. These
Stigmarian axes were most remarkable structures in many
respects. Thus, even at their growing points, perhaps lo m
from the parent trunk, they were frequently as thick as
4 cm. They bore lateral appendages, commonly called 'root-
lets', in a spiral arrangement. These were up to i cm in
diameter and were completely without root hairs. Internally
they show a remarkable resemblance to the rootlets of the
modern Isoetes in having had a tiny stele separated from the
outer cortex by a large space, except for a narrow flange of
tissue (Fig. 12J). In origin, they were endogenous, although
only just so. The axes on which they were borne were
pecuhar in being completely without metaxylem. In the
centre was either pith or a pith-cavity, round which were
protoxylem regions directly in contact with a zone of
secondary wood. This consisted of scalariform tracheids
interspersed with small wood-rays, but there were also very
LYCOPSIDA 75
broad rays (through which the rootlet traces passed) which
divided the wood into very characteristic wedge-shaped
blocks.
The true nature of Stigmarian axes has long been a
problem to morphologists, for although doubtless they per-
formed the functions attributed to roots in higher plants
(absorption and anchorage), yet they were different in so
many respects from true roots and, at the same time, were
so different from the aerial axes that they appear to have
belonged to a category of plant organization that was quite
unique. Even the nature of the 'rootlets' is open to question,
for specimens of Stigmarian axes are known which bore
leaf-like appendages instead of rootlets. Once more one is
forced to the conclusion that the categories root, stem and
leaf have no clear distinction at the lower levels of evolution.
Pleuromeia (Fig. 13 A) was a much smaller plant than the
other members of the Lepidodendrales, for its erect un-
branched stems were Httle more than i m high and 10 cm in
diameter. The lower parts of the stem were covered with
spirally arranged leaf scars, while the upper parts bore
narrow pointed ligulate leaves about 10 cm long, attached
by a broad base. The plant was heterosporous and dioecious,
and the sporangia were borne in a terminal cone made up of
numerous spirally arranged circular or reniform sporophylls.
Although early descriptions described the sporangia as on
the abaxial side of the sporophyll, most morphologists
believe this to be an error and it is usually accepted that, as
in all other lycopods, they were on the adaxial side. Verifica-
tion of this must await the discovery of better preserved
specimens, for no petrified material has yet been found. For
this reason, also, httle is known of the internal anatomy of
the plant.
Below the ground, Pleuromeia was strikingly different
from the other members of the Lepidodendrales, for, in-
stead of having spreading rhizomorphs of the Stigmaria
type, it terminated in four (or sometimes more) blunt lobes.
76 THE MORPHOLOGY OF PTERIDOPHYTES
From these were produced numerous slender forking root-
lets, very similar anatomically to those of Stigmaria and also
to those of Isoetes. Indeed, P/^wrome/a is commonly regarded
as a Hnk connecting the Isoetales with the Carboniferous
members of the Lepidodendrales.
Isoetales
Apart from the fossil genus Nathorstiana, the Isoetales con-
tain only the two living genera Isoetes and Stylites.
The genus Isoetes is world-wide in distribution, some
seventy species being known, of which three occur in the
British flora and are commonly called 'Quillworts'. /. lacus-
tris and /. echinospora grow submerged in lakes or tarns,
while /. hystrix favours somewhat drier habitats. Most of
the plant is below the level of the soil, with only the distal
parts of the sporophylls visible. These are linear structures
from 8 to 20 cm long in /. lacustris, but up to 70 cm in some
species growing in N. America and in Brazil. They constitute
the only photosynthetic parts of the plant and, as in many
aquatic plants, they contain abundant air spaces (lacunae).
The expanded bases of the sporophylls are without chloro-
phyll and overlap one another to form a bulb-hke structure
which surmounts a pecuUar organ, usually referred to as a
'corm'. The true morphology of the corm has long been the
subject of controversy, for it is obscured by a remarkable
process of secondary growth, involving an anomalous
cambium. This produces small quantities of vascular tissue
from its inner surface and large quantities of secondary
cortex towards the outside. This secondary cortex dies each
year, along with the sporophylls and roots attached to it, and
it becomes sloughed off" when the new year's growth of
secondary cortex is produced. Vertical growth of the corm
is extremely slow, with the result that the body of the plant
is usually wider than it is high.
Fig. 13F is a diagrammatic representation of a vertical
LYCOPSIDA 77
section through an old plant of Isoetes. To the right and left
are the shrivelled remains of the previous year's growth, the
several sporophyll-traces and root-traces being visible
within it. All the rest represents the present year's growth
surrounding the perennial central regions. Occupying the
centre is a solid protostele, the lower part of which is
extended into two upwardly curving arms, so that the over-
all shape resembles an anchor (Fig. 13G). This is made up of
mixed parenchyma and pecuUar iso-diametric tracheids
with hehcal thickenings. Towards the outside the tracheids
are arranged in radial rows but, nevertheless, they are of
primary origin (indeed, some workers hold that the whole
of the primary wood is protoxylem). Surrounding this
primary wood is a narrow zone of phloem (not shown in
Fig. 13F), and outside this is the tissue produced centri-
petally by the anomalous cambium. This commonly consists
of a mixture of xylem, phloem and parenchyma and is des-
cribed by the non-committal term 'prismatic tissue'. The
cambium, represented in Fig. 13F as a broken line, cuts
through the sporophyll-traces and root-traces of previous
years, leaving their truncated stumps still in contact with
the primary wood.
What little vertical growth there is takes place by means
of apical meristems at the top and bottom of the corm. The
lower of these is extended as a line beneath the anchor-
shaped primary xylem and is buried deeply in a groove.
Roots arise endogenously along the sides of this groove in a
very regular sequence and are carried round on to the under-
sides of the newly formed cortex. The stem apex is also
deeply sunken between the 'shoulders' of the corm and is
said to contain a group of apical initial cells. Sporophylls
arise in spiral sequence (with a phyllotaxy of |, t\ or
2®i in mature plants) and, as new secondary cortex is
formed, they are carried up on to the shoulders.
Stages in the development of the young sporophylls are
illustrated in Figs. 13J-L. At a very early stage, when the
Fig. 13
Pleuromeia: a, reconstruction. Nathorstiana : b, reconstruction.
Stylites: c, l.s. young plant; d. l.s. older plant; e, l.s. stele.
Isoetes: f, l.s. old plant (semi-diagrammatic); g, l.s. stele (at
LYCOPSIDA 79
primordium is only a few cells high, one conspicuous cell
on its adaxial surface undergoes a periclinal division to
produce a Hgule primordium (i). This soon gives rise to a
membranous ligule a few mm long which, for a time, is
much larger than the young sporophyll. Next, a velum initial
appears, from which is developed the velum (2) — a flange of
tissue which partly hides the sporangium in the mature
sporophyll, except for an oval opening called the 'foramen'.
The sporangium (3) arises as the result of pericHnal divisions
in a group of superficial cells near the base of the sporophyll,
on its adaxial side. The inner daughter cells are potentially
sporogenous, while the outer (peripheral) cells give rise to
the sporangium wall, three or four cells thick. Isoetes is
peculiar among living plants in that some of the potentially
sporogenous cells become organized into trabeculae of
sterile tissue which cross the sporangium in an irregular
manner. They subsequently become surrounded by a tapetal
layer which is continuous with the one derived from the
innermost layer of the sporangium wall.
The general appearance of the base of a mature sporo-
phyll is indicated in Figs. 13I and 13H, representing a longi-
tudinal section and an adaxial surface view respectively. The
sporangia of the Isoetales are larger than those of any other
living plant and have a very high spore content indeed. The
sporophylls formed earHest in the year and which, therefore,
lie outermost on the apex of the corm are megasporangial
and contain several hundred megaspores. Those formed
right angles to f); h, leaf base (adaxial view); i, l.s. leaf base;
J-L, development of leaf; m-o, development of male prothallus ;
p, antherozoid ; q, r, s, development of archegonium; t-x, develop-
ment of young sporophyte; y, megaspore with female prothallus
and young sporophyte
(1, ligule; 2, velum; 3, sporangium)
(a, after Hirmer; b, Magdefrau; c, d, Rauh and Falk; f, based
on Eames; J. k, Bower; m, n, o, Liebig; p, Dracinschi; q, r, s,
Campbell; t-y, La Motte)
80 THE MORPHOLOGY OF PTERIDOPHYTES
later are microsporangial and are estimated to contain up
to a million microspores each. Finally, a few sporophylls
with abortive sporangia are produced late in the season.
There is no special dehiscence mechanism and the spores
are released only when the sporophylls die and decay, as
they become sloughed off at the end of the season. The first
cell division within the microspore is an unequal one which
cuts off a small 'prothallial cell'. The other cell is called the
'antheridial cell' since, by successive divisions (Figs. 13M
and 13N), it gives rise to a jacket of four cells surrounding a
central cell from which four antherozoids are formed (Fig.
13O). These are spiral and multiflagellate (Fig. 13P) and are
released by the cracking of the microspore wall. As already
mentioned, this mode of development, where the prothallus
is retained within the spore wall, is described as 'endosporic'.
The female prothallus hkewise is endosporic. Within the
megaspore, free nuclear divisions take place for some time,
i.e. nuclei continue to divide without any cross-walls being
laid down between them. Then, when about fifty such nuclei
have become distributed round the periphery of the cyto-
plasm, cross-walls are slowly formed, starting in the region
immediately beneath the tri-radiate scar, but gradually
spreading throughout. Meanwhile, the megaspore wall
ruptures at the tri-radiate scar and an archegonium is
formed in the cap of cellular tissue which is thereby exposed.
Stages in the development of the archegonium are illustrated
in Figs. 13Q-S. If fertiUzation does not occur immediately,
further archegonia may develop among the rhizoids that
cover the apex of the gametophyte.
Stages in the development of the young sporophyte are
illustrated in Figs. 13 T-Y, in which the megaspore is sup-
posed to be lying on its side, as is commonly the case. The
first division of the zygote is in a plane at right angles to the
axis of the archegonium, or sUghtly oblique to it. That part
of the embryo formed from the outermost half, designated
'the foot', is indicated in the figures by obhque shading. As
LYCOPSIDA 8l
growth proceeds, the orientation of the embryo changes so
that the first leaf and the stem apex are directed upwards,
while the first root is directed obliquely downwards. It is of
interest that there is no quadrant specifically destined to
produce a stem apex, and that it appears relatively late in a
position somewhere between the first leaf and the first root.
In some species, there are no clearly defined quadrants at all.
Despite the absence of a suspensor, the embryology of
Isoetes may be described as endoscopic, since it is from the
inner half of the dividing zygote that the shoot is ultimately
formed.
For some time, the young embryo continues to be en-
closed within a sheath of prothaUial tissue which grows out
round it, but ultimately the various organs break through
and the first root penetrates the soil.
A chromosome count of n= lo has been obtained in one
species of Isoetes, and of n = 54-56 in several others.
Isoetes is clearly a remarkable genus, not only in its
pecuhar method of secondary thickening, but also in the
fact that all its leaves are, at least potentially, sporophylls.
For this reason, some morphologists regard the upper half
of the corm as representing a cone axis. The lower half they
regard as a highly reduced rhizomorph, homologous with
Stigmarian axes, and this is supported, not only by the
regular arrangement of the roots on the corm, but also by
the extraordinary similarity of the roots to Stigmarian root-
lets internally. If this view is correct, then the stem, as such,
must have become completely suppressed, along with its
leaves.
Stylites was unknown until 1954, when it was first dis-
covered, forming large tussocks round the margins of a lake
at an altitude of 4,750 m in the Peruvian Andes. Since then,
it has been examined in great detail by Rauh and Falk^^,
who claim that there are two species. Stylites is no less re-
markable than Isoetes, for it likewise exhibits a kind of
anomalous secondary thickening, though less active, and all
82 THE MORPHOLOGY OF PTERIDOPHYTES
its leaves are potential sporophylls. It differs from Isoetes,
however, in having hmited powers of vertical growth and in
being able to branch, both dichotomously and adventitiously,
so as to form the characteristic tussocks. Two plants are
illustrated in longitudinal section, one young and un-
branched (Fig. 13C), the other older and branching (Fig.
1 3D). Perhaps the most remarkable feature is the way in
which the roots are borne up one side only and receive their
vascular supply from a rod of primary wood which is quite
distinct from that supplying the sporophylls; the two run
side by side within the axis (Fig. 13E). The nature of the
axis is, therefore, even harder to interpret than in Isoetes.
Rauh and Falk draw a comparison with the Cretaceous
Nathorstiana (Fig. 13B) in which the roots arise from a
number of vertical ridges round the base of the stem. This
in turn may be compared with Pleuromeia and ultimately,
therefore, with the Lepidodendrales.
Selaginellales
This group contains two genera, one living (Selaginella) and
one fossiUzed {Selaginellites). More than 700 species of
Selaginella are known, of which some occur in temperate
regions, but the vast majority are confined to the tropics and
subtropics, where they grow in humid and poorly illuminated
habitats, such as the floor of rain-forests. Some, however,
are markedly xerophytic, inhabiting desert regions, and are
sometimes called 'resurrection plants' because of their
extraordinary powers of recovery after prolonged drought.
Relatively few are epiphytes, unlike Lycopodium. Some
form delicate green mossy cushions, others are vine-Uke,
with stems growing to a height of several metres, while
many have creeping axes, from which arise leafy branch
systems that bear a striking superficial resemblance to a
frond.
Hieronymus^2 divided the genus into the following
sections and subsections :
LYCOPSIDA 83
A Homoeophyllum
1 Cylindrostachya
2 Tetragonostachya
B Heterophyllum
1 Pleiomacrosporangiatae
2 Oligomacrosporangiatae
The Homoeophyllum section is a small one, consisting of
fewer than fifty species, all of which are isophyllous and have
spirally arranged leaves. The only native British species,
Selaginella selaginoides { = S. spinosa, = S. spinulosa) (Fig.
14A), is a typical example of this kind of organization and is
placed in the subsection CyUndrostachya because the spiral
arrangement extends also to the fertile regions. Species
belonging to the Tetragonostachya subsection differ in that
the sporophylls are arranged in four vertical rows, giving the
cone a four-angled appearance. All the members of the
Homoeophyllum section are monostelic, but S. selaginoides is
pecuhar in that the stele of the creeping region is endarch
(Fig. 14I), whereas that of the later-formed axes is exarch
(Fig. 14H), as in all other species. According to Bruchmann^
there is a Umited amount of secondary thickening in the so-
called hypocotyl region of this species; this is the only
record of cambial activity in the whole genus.
The Heterophyllum section is characterized by a markedly
dorsiventral symmetry and by anisophylly, for the leaves are
arranged in four rows along the axis, two rows of small leaves
attached to the upper side and two of larger ones attached
laterally. The fertile regions, however, are isophyllous and
the cones are four-angled, which makes them very clearly
distinguishable from the vegetative regions (Fig. 14F). The
section is divided, somewhat arbitrarily, on the number of
megasporophylls in the cone and is further subdivided on the
number of steles in the axis.
Most commonly the axis is monostelic and contains a
ribbon-shaped stele, e.g. Selaginella flabellata (Fig. 14K), but
> /
* .^'.'■■'^IVS
K
I'liifiTfTtillff'fif^'
1 ; ^
L (^J
Fig. 14
Selaginella selaginoides : a, whole plant; b, microsporophyll;
c, megasporophyll. S. Braunii: e, portion of plant; f, branch
tip + cone. S. Willdenowii : G, attachment of rhizophore.
LYCOPSIDA 85
some species have more complicated stelar arrangements.
S. Kraussiana, now naturalized in parts of the British Isles,
has a creeping habit and has two steles which run side by
side (Fig. 14 J), except at the nodes where they interconnect.
S. Braunii (Fig. 14E) is one of the many species which have a
creeping stem with erect frond-like branch systems: the
creeping axis is bi-stelic, with one stele lying vertically above
the other, while the erect axes are monostelic. S. Willdenowii
is a climbing, or vine-like, species and may have three
ribbon shaped steles (Fig. 14L) or even four. The most
complex of all is S. Lyallii, where the creeping axis is di-
cycHc and the aerial axes are polystelic. The central stele of
the creeping axis is a simple ribbon of metaxylem, without
any protoxylem, surrounded by phloem, pericycle and endo-
dermis. This is surrounded by a cylindrical stele which is
amphiphloic (i.e. has phloem to the inside as well as to the
outside of the xylem) and is bounded, both externally and
internally, by endodermis. Both steles play a part in the
origin of the many steles in the aerial axis, which number
twelve or thirteen, four of them being main ones to which the
leaf traces are connected, while the rest are accessory steles.
It is important to realize that, however complex the stem
of a mature plant may be, the young sporeUng Selaginella is
invariably monostehc, there being a gradual transition along
the axis until the adult condition is achieved. This observa-
tion has naturally, in the past, led to the supposition that
Steles : S. selaginoides, h (aerial axis), i (creeping axis) ;
S. Kraussiana, j; S. flabellata, k; S. Willdenowii, L.
Embryology: S. Martensii, m-p; S. selaginoides, q;
S. Poulteri, R, s, t; S. Kraussiana, u, v;
S. Galleottii, w ; S. denticulata, x.
Biflagellate sperm, y
(1, ligule; 2, rhizophore; 3, diaphragm; a, archegonial tube;
f, foot; r, root; s, suspensor; x, stem apex)
(a, b, c, f, after Hieronymus; h-l, Gibson; m-x, Bruchmann; v,
Dracinschi)
86 THE MORPHOLOGY OF PTERIDOPHYTES
Species which are monosteUc throughout are more primitive
than the more complex species. However, much caution is
necessary before accepting this view. In the first place, not
all monosteles are directly comparable (e.g. S. selaginoides
and S. Braunii). In the second place, it would seem that
some members of the monostelic Homoeophyllum group
are highly advanced in other respects. Thus, S. rupestris and
S. oregana (in the Tetragonostachya subsection) are re-
markable for the possession of vessels in their xylem.
Among the tracheids are Hgnified elements whose transverse
end-walls have dissolved, leaving a single large perforation
plate so that, hke drain pipes placed end to end, they provide
long continuous tubes. While it is true that vessels are known
in some other pteridophytes, they are not of this advanced
type which occurs, elsewhere, only among the flowering
plants. The metaxylem tracheids have scalariform thicken-
ings, while the protoxylem elements are helically thickened
and exhibit a feature which is found elsewhere only in
Isoetes — viz. the helix may be wound in different directions
in different parts of the cell.^^
The phloem, composed of parenchyma and sieve cells, is
very similar to that of Lycopodium and is separated from
the xylem by a region of parenchyma one or two cells
thick. To the outside of it is a region of pericycle, and then
comes a trabecular zone which is characteristic of Selaginella.
This zone differs markedly in detail from species to species,
but is usually a space, crossed in an irregular fashion by
tubular cells or by chains of parenchyma cells. Endodermal
cells are recognizable also in this region because of their
Casparian bands, but it sometimes happens that a single
Casparian band may encircle a bunch of several tubular
cells. Whatever the exact constitution of the zone, however,
it is very deUcate, with the result that the stele usually drops
out of sections cut by hand. The outer regions of the stem
are frequently made up of thick-walled cells and the epi-
dermis is said to be completely without stomata.
LYCOPSIDA 87
In Selaginella selaginoides, roots arise in regular sequence
from a swollen knot of tissue in the hypocotyl region, but
in most creeping species they arise at intervals along the
under side of the stem. They are simple monarch structures,
which branch dichotomously in planes successively at right
angles to each other, as they grow downwards into the soil.
Root-caps and root-hairs are present, just as in the roots of
other plants. A mycorrhizal association has been demon-
strated in S. selaginoides. In species with aerial branches, the
roots are associated with pecuhar organs, usually referred
to as *rhizophores', and some morphologists describe the
roots as borne on them, while others describe the rhizo-
phores as changing into roots on reaching the soil. Of these,
the second interpretation is probably the more accurate.
Rhizophores are particularly well developed in cHmbing
species, such as S. Willdenowii (Fig. 14G), where they grow
out from 'angle meristems' which occur in pairs, one above
and one below, at the junction of two branches. In some
species, only one of these is active while the other remains
dormant, as a small papilla. The active one grows into a
smooth shiny forking structure without leaves. Its branches
are without root-caps until they reach the soil, but then root-
caps appear and all subsequent branches take on the appear-
ance of typical roots. This is the normal behaviour, but the
fate of the angle meristems appears to be under the influence
of auxin concentrations, for damage to the adjacent branches
may result in their giving rise to leafy shoots, instead of
rhizophores. It is clear that the rhizophore fits neither into
the category 'stem' nor into the category 'root', but exhibits
some of the characters of each. It is not surprising, therefore,
that in the days when botanists believed in the reality of
these morphological categories, the rhizophores of Selagin-
ella were the subject of much argument.
The stem apex shows an interesting range of organiza-
tion, from species to species, for those with spirally arranged
leaves tend to have a group of initial cells, while dorsiventral
88 THE MORPHOLOGY OF PTERIDOPHYTES
Species usually have a single tetrahedral apical cell.^* Leaf
primordia are formed very close to the stem apex and, in
some species, appear to arise from a single cell. They give
rise to typical microphylls, receiving a single vascular bundle
which continues into the lamina as an unbranched vein. The
ligule, which is present on every leaf and sporophyll, appears
early in their ontogeny and develops from a row of cells
arranged transversely across the adaxial surface near the base
of the primordium. When fully grown it may be fan-shaped
or lanceolate and has a swollen *glossopodium' sunken into
the tissue of the leaf. There is much variation, according to
species, in the structure of the lamina of the leaf, for some
species possess only spongy mesophyll, while others have a
clearly defined palisade layer also. In some, the cells of the
upper epidermis and, in others, some of the mesophyll cells
contain only a single large chloroplast, a feature which is
reminiscent of the liverwort Anthoceros. In other species, all
the cells of the leaf contain several chloroplasts. There is
much variation, also, in the occurrence of stomata, some
species being amphistomatic and others hypostomatic.
Early stages in the development of the sporangia in
Selaginella are very similar to those in Lycopodium, and there
is a similar range of variation in the location of the primor-
dium. Thus, in some species, it arises on the axis, while in
others it arises on the adaxial surface of the leaf, between the
ligule and the axis. However, at maturity the sporangium
comes to lie in the axil of the sporophyll. The first division
is periclinal and gives rise to outer jacket initials and inner
archesporial cells. The jacket initials divide further to pro-
duce a two-layered sporangium wall and the archesporial
cells produce a mass of potentially sporogenous tissue, sur-
rounded by a tapetum. In microsporangia many cells of the
sporogenous tissue undergo meiosis to form tetrads of
microspores but, in the megasporangia of most species, all
the sporogenous tissue disintegrates, except for one spore
mother cell, from which four megaspores are formed. Some
LYCOPSIDA 89
Species, however, retain more than the one functional mega-
spore mother cell, so that up to twelve or even more mega-
spores may result. Yet other species are pecuhar in that, out
of the single tetrad of megaspores, one, two or three may be
abortive, so that in the extreme condition the megasporan-
gium may contain only one functional megaspore. S. rupestris
usually has two megaspores in each sporangium and some-
times only one, while S. sulcata regularly has only one.
S. rupestris is further remarkable in that the megaspores are
not shed, but are retained within the dehisced megasporan-
gium and fertilization takes place while it is still in situ.
Thus, it happens that young sporophytes may be seen grow-
ing from the cone of the parent sporophyte. Few seed-plants
have achieved this degree of vivipary, yet in Selaginella it
occurs in a species belonging to the allegedly primitive
Homoeophyllum group.
In those species whose cones contain both megasporo-
phylls and microsporophylls, it is usual for the former to be
near the base of the cone and the latter near the apex. This
further emphasizes the point, already made, that the arrange-
ment in lycopods is the inverse of that observed both in the
gymnospermous Bennettitales and in hermaphrodite flowers
of angiosperms.
Fig. 14D illustrates the appearance of a megasporophyll
in longitudinal section, with the hgule (i) and the differential
thickening in the sporangium wall, while Figs. 14B and 14C
illustrate a dehiscing microsporangium and megasporangium
respectively. Contractions of the thick-walled cells of the
megasporangium cause the megaspores to be ejected for a
distance of several centimetres, but dispersal of the micro-
spores is mainly by wind currents.
Long before the spores are shed, nuclear divisions have
started to take place, so that the prothallus is well advanced
when dehiscence occurs. The stages in the formation of the
male prothallus are very similar to those figured for Isoetes
and, at the moment of Uberation, the male prothallus
90 THE MORPHOLOGY OF PTERIDOPHYTES
commonly consists of thirteen cells (one small prothallial
cell, eight jacket cells and four primary spermatogenous
cells, of which the latter undergo further divisions to produce
128 or 256 biflagellate antherozoids— Fig. 14Y). Within the
megaspore, a large vacuole appears, around which free
nuclear divisions occur and then, subsequently, a cap of
cellular tissue becomes organized beneath the tri-radiate
scar. In some species, this cap is continuous with the rest of
the prothallus, which later becomes cellular too, but in
others a diaphragm of thickened cell walls is laid down, as
illustrated in Figs. 14R and 14U (3). Rupturing of the mega-
spore allows the cap to become exposed and it frequently
develops prominent lobes of tissue, covered with rhizoids,
between which are numerous archegonia. It has been
suggested that the rhizoids, as well as anchoring the mega-
spore, may serve to entangle microspores in close proximity
to the archegonia.
The archegonia are similar to those of Isoetes, except that
the neck is shorter and consists of two tiers of cells only.
The embryology of Selaginella is remarkable for the very
great differences that occur between species. These are
illustrated in Figs. 14M-X, all of which, for ease of com-
parison, are drawn as if the megaspore were lying on its
side. The first cross wall is in a plane at right angles to the
axis of the archegonium (Fig. 14M) and the fate of the
outermost half in the different species is indicated by
obUque shading. In S. Martensii (Figs. 14M-P) the outer half
gives rise to a suspensor (s), while the inner half gives rise to
all the rest of the embryo, with a shoot apex, (x), a root (r)
and a swollen foot (f). The axis of the embryo, in this species,
becomes bent through one right angle so as to bring the shoot
apex into a vertical position. S. selaginoides (Fig. 14Q)
is similar, except for the absence of a foot. S. Poulteri (Figs.
14R-T) is a species with a well developed diaphragm, through
which the embryo is pushed by the elongating suspensor. A
curvature through three right angles then brings the shoot into
LYCOPSIDA 91
a vertical position. S. Kraussiana (Figs. 14U and 14V) likewise
has a diaphragm, but in this species the venter of the arche-
gonium gradually extends through it (a), so carrying the
embryo with it into the centre of the prothallus. The outerhalf
of the dividing zygote provides, not only the vestigial suspensor,
but also the foot. The archegonium of S. Galeottii behaves in a
similar way, but the embryo is different (Fig. 14W) in that
the outer half provides the suspensor, the foot and also the
root. S. denticulata (Fig. 14X) has the various parts of the
embryo disposed as in S. Martensii (i.e. the root lies between
the suspensor and the foot) but they are derived in a com-
pletely different way, for they all come from the outermost
half of the dividing zygote.
Such extraordinary variations as these are very puzzHng
and have occupied the thoughts of many morphologists.
Some have held that the presence of a well developed sus-
pensor is a primitive character and that the reduction of this
organ in some species is a sign of relative advancement.
Its reduction seems to be correlated with the transference
of its function to the venter of the archegonium, and
this would certainly seem to be an advanced condition. As
to the *foot', all that can be said is that it has Httle reality
as a separate organ, since it can apparently be formed from
various regions of the embryo and may even be dispensed
with altogether.
Selaginella is pecuUar among pteridophytes for its low
chromosome numbers, n = 9 being the commonest number,
and its chrom.osomes are minute.
Selaginellites is the genus to which are assigned all fossil
remains of herbaceous lycopods that are known to have been
heterosporous. The recent examination of Selaginellites crassi-
cinctus'^^ is of particular interest, for within its cones were
found the megaspores Triletes triangularis, which have long
been known as one of the commonest spores in coal measure
deposits, but whose origin was hitherto unknown. This dis-
covery suggests that Selaginellites v^sls probably an important
92 THE MORPHOLOGY OF PTERIDOPHYTES
component of the flora of those times, contemporaneous
with the tree-Hke Lepidodendrales. Whereas this species was
similar to most Selaginella species in having four megaspores
in each sporangium, others had sixteen or even thirty-two,
which suggests that they had not progressed so far in the
direction of heterospory. While there is no general agree-
ment among botanists as to how the various groups of the
Lycopsida are related to each other, it is generally supposed
that the heterosporous forms must have evolved from some
homosporous ancestor.
In this connection, it is perhaps significant that, among
Selaginella species, the type regarded as the most primitive
(S. selaginoides) approaches most nearly to the Lycopodium
species which is regarded as the most primitive (L. selago).
Both are erect and isophyllous, with spirally arranged leaves
showing the least difference between fertile and sterile
regions and both having simple protostehc vascular systems.
The similarities extend even to the young embryo, as a com-
parison of Figs. loP and 14Q will show. The lack of a well
developed foot in each is interesting, and makes one wonder
whether it might have been absent from their ancestors also.
The most important differences between these two plants,
therefore, seem to be the heterospory of Selaginella and its
possession of a hgule. If it be accepted that heterospory is
derived from homospory, there remains only the ligule to be
explained. This is, indeed, difficult. There is no obvious
reason why, in lycopods, this structure should invariably be
associated with heterospory. Selaginella is usually grouped
with Isoetes and the Lepidodendrales on the basis of the
possession of these two characters, yet on other grounds
Selaginella stands apart from Isoetes. The multiflagellate
antherozoids of the latter suggest very fundamental differ-
ences. On the basis of the number of flagella, Lycopodium
and Selaginella should be grouped together. Unfortunately,
of course, we have no knowledge of the antherozoids of the
Lepidodendrales, but one's guess would be that they were
LYCOPSIDA 93
multiflagellate, like those of Isoetes and Stylites. One thing
is fairly certain — that Selaginella is not a direct descendant
of the Lepidodendrales. Apart from this, one's views on the
relationships of the Lycopsida must depend upon a decision
as to whether the ligule is more significant phylogenetically
than the number of flagella.
Sphenopsida
Sporophyte with roots, stems and whorled leaves.
Protostelic (solid or medullated). Some with secon-
dary thickening. Sporangia thick-walled, homo-
sporous (or heterosporous), usually borne in a re-
flexed position on sporangiophores arranged in
whorls. Antherozoids multiflagellate.
Hyeniales*
Protohyeniaceae* Protohyenia*
Hyeniaceae* Hyenia* Calamophyton
*
2 Sphenophyllales*
Sphenophyllaceae* Sphenophyllum* Sphenophyllos-
tachys* Bowmanites,* Eviostachya*
Cheirostrobaceae* Cheirostrobus*
3 Calamitales*
Asterocalamitaceae* Asterocalamites* Archaeocala-
mites*
Calamitaceae* Protocalamites* Calamites,*
Annularia,'^ Asterophyllites,*
Pro tocalamostachys, * Calamo-
stachys* Palaeostachya*
4 Equisetales
Equisetaceae Equisetites,* Equisetum
94
SPHENOPSIDA 95
Hyeniales
Until 1957 the earliest known representatives of the Sphen-
opsida were Hyenia and Calamophyton, both of which are of
Middle Devonian age, but in that year Ananiev discovered
the remains of a most interesting plant in Lower Devonian
rocks of western Siberia. This he named Protohyenia (Fig.
1 5 A). Although lacking some of the features which are
characteristic of the Sphenopsida, yet, as the generic name
suggests, it might well represent an early ancestor of the
group. From a creeping axis, erect branches arose at inter-
vals, bearing either sterile or fertile appendages in rather
indefinite whorls. The sterile appendages forked several
times and, although having the appearance of tiny lateral
branches, they probably functioned as leaves. The fertile
appendages were very similar, but terminated in sporangia.
These were unUke those of almost all other members of the
Sphenopsida, in that they were not reflexed.
Hyenia elegans (Fig. 15E) had a similar growth habit, as
we now reahze from the work of Leclercq,^^ for it had a stout
horizontal rhizome bearing roots and erect aerial stems up to
30 cm high, some sterile and others fertile. The sterile axes
bore whorls of forking appendages, alternating at successive
nodes and, as in the case of Protohyenia, it is difficult to
decide whether they should be regarded as leaves or as stems
performing the functions of leaves. The fertile axes bore
whorls of sporangiophores (Fig. 15F), which were similar to
the 'leaves', except that two segments were reflexed and
usually terminated in two sporangia each.
Other species of Hyenia are known, in which the aerial
axes were branched and which, therefore, resembled quite
closely the other Middle Devonian genus Calamophyton.
The illustration of C. primaevum (Fig. 15B) is taken from an
early description^^ which emphasizes the articulate nature of
the aerial axes, a feature which used to be regarded as
essential in defining the genus. However, other species, e.g.
C. bicephalum, are not so clearly articulated and it has been
Fig. 15
Protohyeniajanovii: A, reconstruction. Calamophyton: b, recon-
struction of C. primaevum; c, leaf, and d, sporangiophore of
C. bicephalum. Hyenia elegans: E, reconstruction; f, sporan-
giophore. Eviostachya Hoegi: G, sporangiophore; h, mode of
SPHENOPSIDA 97
suggested that the two genera merge into one another.®^
Certainly the sterile and fertile appendages of C. bicephalum
(Figs. 15C and 15D) were very similar to those of Hyenia,
the chief difference being that the fertile appendages of the
former forked more profusely and bore twelve sporangia,
instead of three or four, as in the latter. The lateral appen-
dages of C. primaevum are said to have been much simpler,
forking only once, and the sporangiophores are said to have
borne only two sporangia; the way in which they were
restricted to special fertile branches may represent early
stages in the evolution of the strobilus, which is so character-
istic of later sphenopsids.
Little is known of the internal anatomy of the Hyeniales,
but in Calamophyton there are indications of a triangle of
pith surrounded by tracheids with reticulate or scalariform
thickenings; it is also suggested that there may have been
some degree of secondary thickening.
Sphenophyllales
This group first appeared in the Upper Devonian and per-
sisted until the Lower Triassic, remains of stems as well as of
leaves being referred to the genus Sphenophyllum. Many
species are known, all of which are characterized by the
whorled arrangement of the leaves, usually in multiples of
three at each node (Fig. 15K). The stems were usually very
delicate, in spite of secondary thickening, for they seldom
exceeded i cm in diameter. Presumably, therefore, they
branching of sporangiophore. Cheirostrobus pettycurensis : i,
sporangiophore and bract. Sphenophyllostachys (= Bowmanites)
fertilis: J, reconstruction of part of cone. Sphenophyllum cunei-
folium: k, reconstruction; l, stele; m-o, leaves. Sphenophyllo-
stachys Dawsoni: p, part of cone in l.s.; Q, part of cone in t.s.
Sphenophyllostachys Roemeri: r, part of cone in t.s.
(a, after Ananiev; b, Krausel and Weyland; c, d, Leclercq and
Andrews; e-h, j, Leclercq; i, Scott; k, Smith; m-o, Jongmans;
p-R, Hirmer)
D
98 THE MORPHOLOGY OF PTERIDOPHYTES
were unable to support their own weight and must have been
prostrate on the ground, or must have depended on other
plants for support. In general appearance, they probably
looked rather hke a Galium ('Bedstraw'). The anatomy of
the stem was most peculiar in its resemblance to that of a
root, for in the centre was a triangular region of solid prim-
ary wood, with the protoxylems at the three corners in an
exarch position. In the Lower Carboniferous species, S,
insigne, the protoxylem tended to break down to form a
'carinal' canal, but in the Upper Carboniferous species this
rarely happened. Outside the primary wood, a vascular
cambium gave rise to secondary wood, first between the
protoxylems, and then later extending all round. However,
the wood opposite the protoxylems was composed of smaller
cells than on the intermediate radii, resulting in a pattern
which is quite characteristic and which is recognizable at a
glance in transverse sections (Fig. 15L). The primary wood
consisted entirely of tracheids (i.e. without any admixture of
parenchyma) and they bore multiseriate bordered pits on
their lateral walls. The tracheids of the secondary wood also
bore multiseriate pits, but they were restricted to the radial
walls. Between the tracheids, there were wood rays. These
were continuous in S. insigne, but were interrupted in S.
plurifoliatum where they were represented only by a group
of parenchyma cells in the angles between adjacent tracheids.
Large stems had a considerable thickness of cork on the
outside, formed from a deep-seated phellogen.
The leaves of Sphenophyllum showed a wide range of
structure, some being deeply cleft, while others were entire
and deltoid (Figs. 15M-O); yet all received a single vascular
bundle, which dichotomized very regularly within the
lamina. Some species were markedly heterophyllous, as
illustrated in Fig. 15K, and in these the deeply cleft leaves
were usually near the base, while the entire ones were higher
up on lateral branches, an arrangement that suggests that
the former might represent juvenile fohage.
SPHENOPSIDA 99
A number of cones, referred to the genera Sphenophyllo-
stachys or Bowmanites, have been found attached to the
parent plant; others, found detached, are placed in these
genera on the basis of their general similarity. A number of
other genera of cones are also referred to the Sphenophy Hales,
but on less secure grounds. Some of them represent the most
complex cones in the whole plant kingdom. One of the
earUest to appear in the fossil record is Eviostachya, des-
cribed by Leclercq^*, from the Upper Devonian of Belgium.
Less than 6 cm long and less than i cm in diameter, each cone
had at its base a whorl of six bracts. Above this were whorls
of sporangiophores, six in each whorl. Each sporangiophore
was itself highly compUcated (Fig. 1 5G) and branched in a very
characteristic way (Fig. 15H), bearing a total of twenty-seven
sporangia in a reflexed position. Sporangiophores in successive
whorls stood vertically above each other, as is characteristic of
the Sphenophyllales, but there were no bracts between them.
Cheirostrobus, from the Lower Carboniferous of Scotland,
was a large cone, 3-5 cm across, and had thirty-six sporangi-
phores in each whorl, subtended by the same number of
bracts, each with bifurcated tips (Fig. 15I). The arrangement
of the vascular supply to these appendages is interesting in
that a common 'trunk-bundle' supplied three sporangio-
phores and the three bracts subtending them. This has led
some morphologists to suggest a more comphcated inter-
pretation of the cone structure than is really necessary, based
on the supposition that each trunk-bundle represented the
vascular supply to one compound organ made up of three
fertile leaflets and three sterile leaflets.
Sphenophyllostachys fertilis { = Sphenophyllum fertile,
= Bowmanites fertilis) from the Upper Carboniferous (Fig.
15J) was also a complex cone. Up to 6 cm long and 2-5 cm
in diameter, it was made up of whorls of superimposed
sporangiophores, six in a whorl, each subtended by a pair
of sterile appendages (possibly homologous with one bifid
bract). Each sporangiophore terminated in a *mop' of
100 THE MORPHOLOGY OF PTERIDOPHYTES
branches, about sixteen in number, each bearing two re-
flexed sporangia. Only detached cones have, so far, been
found, but they are presumed to have belonged to some
member of the Sphenophyllales, because of the triarch or
hexarch arrangement of the primary wood in the axis.
Sphenophyllostachys { = Bowmanites) Dawsoni, on the
other hand, is known to have been borne on stems like those
of Sphenophyllum plurifoliatum. The cone was up to 12 cm
long and i cm in diameter and bore whorls of bracts, fused
into a cup near the base, but with free distal portions. In the
axils of these bracts, and fused with them to a certain extent
(Fig. 15P), were branched sporangiophores. In one form
(forma a) each sporangiophore had three branches arranged
in a very characteristic way (Fig. 15Q), each terminating in
a single reflexed sporangium. In another form (forma y),
there were six branches.
Sphenophyllostachys { = Bowmanites) Roemeri was similar
in its organization to S. Dawsoni, forma a, except that each
branch of the sporangiophores bore two reflexed sporangia
(Fig. 15R).
In recent years, a number of relatively simple cones have
been described, which are nevertheless beheved to belong to
the Sphenophyllales. Thus, in Bowmanites bifurcatus, each
sporangiophore forked only once, while in Litostrobus
iowensis the sporangia were borne singly on a short un-
branched stalk. In the latter species, the sporangia were not
reflexed but, despite this very simple organization, an
affinity with Bowmanites is presumed, because of the
number of bracts and the number of sporangia in a whorl
(twelve and six respectively).^ The discovery of these simple
cones has led to the suggestion that, within the Spheno-
phyllales, evolution has involved progressive simplification.
While the vast majority of the Sphenophyllales were
homosporous, at least one, Bowmanites delectus, was hetero-
sporous^ with megaspores about ten times the size of the
microspores.
SPHENOPSIDA lOI
Calamitales
This group reached the peak of its development in the Upper
Carboniferous, when a large number of arborescent species
was co-dominant with the Lepidodendrales in coal-measure
swamp forests ; yet by the end of the Permian the group had
become extinct. The first representatives to appear, in the
Upper Devonian, were the Asterocalamitaceae, a group
which differed from the later Calamitaceae in a number of
interesting details. Asterocalamites { = Archaeocalamites)
(Fig. i6A) had woody stems up to i6 cm in diameter,
strongly grooved on the outside, with the grooves con-
tinuing through successive nodes (i.e. not alternating). The
leaves, up to lo cm long, were in whorls at the nodes and
forked many times dichotomously, in a manner strongly
reminiscent of Calamophyton leaves. At intervals along the
more slender branches, there were fertile regions, in which
there were superimposed whorls of peltate sporangio-
phores, each bearing four reflexed sporangia (Fig. i6B).
Sometimes the fertile regions were interrupted by a whorl
of leaves, but these were apparently normal leaves and could
not be regarded as bracts. The absence of any regular
association between bracts and sporangiophores makes an
interesting comparison with the cones of the later Calami-
taceae.
Protocalamites was one of the earhest representatives of
the Calamitaceae, being present in the Lower Carboniferous
rocks of Pettycur, Scotland. Its stems were ridged, with the
ridges alternating in successive internodes, like those of
most members of the family, but they differed in one im-
portant respect. Examination of a transverse section of a
petrified stem (Fig. i6C) reveals a marked development of
centripetal wood, as well as centrifugal (i.e. the primary
wood was mesarch). As in Catamites and in Equisetum, the
protoxylem tended to break down to form a carinal canal.
Secondary wood was laid down to the outside of the meta-
xylem, but the primary wood-rays were so wide that it gives
Fig. 16
Asterocalamites {= Archaeocalamites) : A, stem and leaves;
B, fertile region. Protocalamites : c, part of internodal vascular
system. Protocalamostachys : d, sporangiophore. Calamites:
SPHENOPSIDA 103
the appearance of having been formed in separate strands,
although in fact it was formed from a continuous vascular
cambium.
Protocalamostachys is the name given to a peculiar cone
described by Walton^^^ from Lower Carboniferous rocks in
the Island of Arran. Two small pieces of the cone had
dropped into the hollow stump of a Lepidophloios before it
became petrified. Unhke the cones of other members of the
Calamitales, its sporangiophores branched twice (Fig. 16D),
instead of being peltate. In this respect, it showed some
affinities with the Sphenophyllales and also with the
Hyeniales. However, Walton compares it most closely with
Pothocites, a cone associated with leaves of the Astero-
calamites type. Furthermore, within the axis of the cone
there is centripetal primary wood as in the stem of Proto-
calamites.
The height to which Calamites grew is difficult to deter-
mine, because of the fragmentary nature of the remains, but
it is almost certain that some specimens must have attained
a height of 30 m with hollow trunks whose internal diameter
was up to 30 cm. Strictly speaking, the generic name
Calamites should be applied only to pith casts of stems and
branches, while petrified wood should be described under
E, reconstruction of Eiicalamites type. Annularia: F. Astero-
phyllites: G. Calamites {= Arthropitys): H, part of internodal
vascular system. Palaeostachya: i, sporangiophore and bract.
Calamostachys : J, part of cone in l.s. Eqiiisetum pratense: K,
plant with young sterile shoot; l, young fertile shoot with cone;
M, sporangiophore; n, spore with elaters; o, nodal vascular
arrangement (1, internodal bundles; 2, leaf trace; 3, branch
traces); p, antherozoid. Eqiiisetum sylvaticiim: Q, internodal
vascular bundle (4, carinal canal with remains of protoxylem).
Archegonium: r (E. hyemale). Embryo: s (E. arvense) (f, foot;
1, leaf primordia; r, root primordium; x, stem apex)
(a, after Stur; b, Renault; d, Walton; e, Hirmer; f, g, Abbott;
I, Baxter; J, Scott; k, l, Duval-Jouve; n, Foster and Gifford;
o, Fames; p, Sharp; r, Jeff'rey; s, Sadebeck)
104 THE MORPHOLOGY OF PTERIDOPHYTES
the form genus Arthropitys, but common usage has extended
the apphcation of the name Calamites to include all methods
of preservation. The pith casts exhibit ridges and grooves,
corresponding in number to the protoxylem strands, run-
ning up the inside of the secondary wood and alternating at
successive nodes. In this respect they differ from Meso-
calamites, in which there was some variabiUty from node to
node, the ridges sometimes alternating and sometimes con-
tinuing straight across the nodes. A number of subgenera
are recognized which differed in their mode of branching
and, hence, in their general form. The subgenus Eucalamites
branched at every node. Fig. i6E is oi Eucalamites carinatus,
in which there were only two branches at each node, but
other species branched more profusely. By contrast, the sub-
genus Stylocalamites branched only near the top of the erect
organpipe-Hke trunk.
Transverse sections of Calamites (Arthropitys) show very
little primary wood indeed, for secondary thickening pro-
vided most of the wood (Fig. i6H). The protoxylem was
represented by carinal canals and the small amount of
metaxylem present was entirely centrifugal. The wood rays
varied, according to species, dividing the secondary wood
into segments in some species, or losing their identity in a
continuous cylinder of wood in others. In all cases the wood
contained small wood-rays in addition, but otherwise was
composed entirely of tracheids with scalariform pitting or
with circular bordered pits on the radial walls.
The leaves of Calamites were unbranched, with a single
mid-vein, and occurred in whorls of four to sixty. In most
species, they were free to the base, but in a few they showed
some degree of fusion into a sheath. They are placed in one
or other of two form genera, according to their overall
shape, Annularia being spathulate or deltoid (Fig. i6F), while
Asterophyllites were linear (Fig. i6G). The latter were
pecuHar in being heavily cutinized, with the stomata res-
tricted to the adaxial surface, suggesting that the branches
SPHENOPSIDA 105
bearing them may have been pendulous. It is probable,
therefore, that the cones were pendulous, too.
The cones of Calamites were borne in a variety of ways,
in some species singly at the nodes, in others in terminal
groups or infructescences or on specialized branches. ^ Many
species are known, but most of them are placed in one or
other of the two genera Calamostachys and Palaeostachya.
As originally defined, these two genera were clearly distinct,
but, in the light of many newly discovered species, Andrews^
has questioned whether the distinction is now justified. In
both genera there were whorls of peltate sporangiophores
bearing four reflexed sporangia (Figs. 1 61 and 1 6 J), alternating
with whorls of bracts fused into a disc near their point of
attachment. Whereas the sporangiophores were in vertical
rows, the bracts in successive whorls alternated with one
another. While the number of bracts in a whorl bore a
definite relationship to the number of sporangiophores, the
actual numbers varied from species to species and, some-
times, from individual to individual. Calamostachys Binne-
yana, a cone about 3-5 cm long and 7-5 mm wide, had six
sporangiophores in each whorl and twelve bracts. C.
magnae-crucis was more complicated, in having alternating
vascular bundles in successive internodes within the cone
and in having sporangiophores and bracts so numbered that,
if 'n' were the number of vascular bundles, then the number
of sporangiophores was in in each whorl and the number of
bracts 3n; the number 'n' could be either seven or eight.
Most species were homosporous, but some were definitely
heterosporous. Thus, in C. casheana the megaspores were
three or four times the size of the microspores, while in
C americana they were about twice the size.
Whereas the sporangiophores of Calamostachys stood out
at right angles to the cone axis, those oi Palaeostachya stood
out at an angle of about 45°, and in some species they appear
to have been in the axil of the bract whorl below. P. vera had
eight to ten sporangiophores in each whorl and twice as
I06 THE MORPHOLOGY OF PTERIDOPHYTES
many bracts (according to an early description by Williamson
and Scott^^, but according to Hickling,*^ the same number).
Perhaps the most interesting feature shown by this species is
the course taken by the vascular bundle supplying the
sporangiophore. As illustrated in Fig. i6I, it travelled up in
the cortex of the cone axis to a point about midway between
the bracts, and then turned downwards, before entering the
stalk of the sporangiophore. To those morphologists who
regard vascular systems as highly conservative, this impUes
that Palaeostachya must have evolved from some ancestral
form in which the sporangiophore stood midway between
the bract whorls, as in Calamostachys, and that during the
'phyletic sUde' the vascular supply had lagged behind.
Palaeostachya Andrewsii showed the same feature, but in
P. decacnema the sporangiophore bundle took a direct
course. One concludes, therefore, that this last species is
more advanced than the others in this respect. In P.
Andrewsii, the numbers of sporangiophores and bracts in a
whorl were twelve and twenty-four respectively, while in
P. decacnema they were usually ten and twenty.
The above brief review of the Calamitales brings out some
interesting evolutionary trends, which are paralleled very
closely in the Lepidodendrales. Thus, the production of
increasing amounts of secondary wood was accompanied,
in both groups, by a reduction of the primary wood, of
which the centripetal metaxylem was the first to go, being
replaced either by pith or by a central hollow. At the same
time, there was a trend in the fertile regions from a 'Selago
condition' to a compact cone, in which the sporangia were
protected by overlapping sporophylls in one group and by
bracts in the other. Then, having reached their zenith to-
gether, both groups became extinct at about the same time.
Equisetales
The only representatives of the Sphenopsida that are alive
today belong to the single genus Equisetum and, of this, only
SPHENOPSIDA 107
some twenty-five species are known. Eleven of them occur
in the British Isles, where they are known as 'horse-tails'.
The genus is distributed throughout the world with the
exception of Australia and New Zealand, from which
countries it is completely absent. All the species are her-
baceous perennials, but there is an interesting range of
growth habits, for some are evergreen, while others die back
to the ground each year. Early statements that a Hmited
amount of secondary thickening occurs are now discredited,
for there is no evidence that a cambium is present in any
species. Most species are, therefore, very hmited in size; the
largest species, E. giganteum, has stems up to 13 m long, but
since they are only 2 cm thick the plant depends on the sur-
rounding vegetation for its support. The largest British
species, E. telmateia, sometimes attains a height of 2m and is
free-standing in sheltered locahties, but most species are
much smaller than this and are between 10 and 60 cm tall.
In all species there is a horizontal rhizome from which
arise aerial stems that branch profusely in some species
(e.g. Equisetum telmateia, E. arvense) or remain quite un-
branched in others (e.g. E. hiemale). The leaves, in all species,
are very small and are fused into a sheath, except for their
extreme tips which form teeth round the margin of the
sheath. They are usually without chlorophyll, photosyn-
thesis being carried out entirely by the green stems. In the
past, there have been discussions as to whether the small
leaves of Equisetum represent a primitive or a derived con-
dition, but, in the hght of the fossil record, it is now clear
that they have been reduced from larger dichotomous struc-
tures (i.e. that they are derived). The stems are ridged, each
ridge corresponding to a leaf in the node above, and the
ridges in successive internodes alternate with one another
(as, of course, do the leaves in successive leaf-sheaths).
There are, however, some departures from this regular
alternation, as the number of leaves in a whorl diminishes
from the base to the apex of the stem.^^
I08 THE MORPHOLOGY OF PTERIDOPHYTES
The sporangia are borne in a cone, which in some species
{Equisetum arvense) terminates a special aerial axis that
lacks chlorophyll, is unbranched and appears before the
photosynthetic axes. In other species the fertile shoot is
green and may subsequently give rise to vegetative branches
lower down (e.g. E. limosum and E. pratense), after the cone
has withered. In yet other species, most of the lateral
branches may terminate in a cone (e.g. the Mexican species
E. myriochaetum). This last arrangement is commonly re-
garded as the primitive condition, on the basis that it in-
volves the least speciahzation, but it must be reahzed that
real evidence for this view is lacking.
The internal anatomy of the stem of Equisetum presents
an interesting association of xeromorphic and hydromorphic
characters, together with a vascular system which is without
parallel in the plant kingdom today, and whose correct
morphological interpretation has long been the subject of
controversy. The ridges in the stem are composed of
sclerenchymatous cells, whose thick walls are so heavily
sihcified as to blunt the edge of the razor when cutting
sections. Stomata are restricted to the 'valleys' between the
ridges and are deeply sunken into pits whose openings may
be partly covered by a flange of cuticle. The walls separating
the guard cells from their accessory cells bear pecuHar comb-
like thickenings which are known elsewhere only in the
leaves of Calamites. Beneath each of the valleys is a 'vallecu-
lar canal' and the central region of the internodes of aerial
stems consists of a large space (but, in subterranean stems,
the centre may be occupied by pith). At the nodes, there is a
transverse diaphragm. Such an arrangement of air channels,
together with a very reduced vascular tissue, are features
normally found in water plants and contrast strikingly with
the heavy cuticle, sunken stomata and reduced leaves.
The internodal vascular bundles lie beneath the ridges of
the stem and are quite characteristic (Fig. i6Q). As in
Calamites, the protoxylem is endarch and is replaced by a
SPHENOPSIDA 109
carinal canal (4), in which may be seen lignified rings which
are all that remain after the dissolution of annular tracheids.
To the outside of each carinal canal, and on the same radius,
lies an area of phloem, flanked on either side by a lateral
xylem area. This lateral xylem may contain further proto-
xylem tracheids with annular thickenings, but otherwise
consists of metaxylem elements which may be tracheids
with helical thickening, or with pits, or may even be true
vessels. Two types of vessel element occur, one with simple
perforation plates and the other with reticulate, but it must
be emphasized that they are restricted to the internodes and
that they seldom occur more than three in a row. They do
not, therefore, form conducting channels of great length as
do the vessels of flowering plants. ^^ In some species (e.g.
Equisetum Utorale) each internodal bundle is surrounded by
its own separate endodermis, in others (e.g. E. palustre)
there is a single endodermis running round the stem outside
all the bundles, while in yet other species (e.g. E. sylvaticum.
Fig. 16Q) there are two endodermes, one outside and the
other inside all the bundles.
At the nodes (Fig. 16O) the vascular bundles (i) are
connected by a continuous cylinder of xylem, from which the
leaf traces (2) and branch traces (3) have their origin.
Neither vallecular canals nor carinal canals are present in
this region and there have been disagreements as to whether
there is any protoxylem here either, but the most recent
investigations confirm its presence as a constant feature. ^^
This disposes of the view, held by some, that the internodal
bundles represent leaf traces extending down through the
internode to the node below. An alternative view used to be
held— that the vascular network represents a kind of dictyo-
stele, in which the spaces between the internodal bundles
represent leaf-gaps. However, this is unhkely, in view of the
arrangement known to have existed in the earhest relatives
of the genus, such as Asterocalamites, where there was no
alternation at the nodes. Furthermore, this view overlooks
no THE MORPHOLOGY OF PTERIDOPHYTES
the peculiar way in which the internodes of Equisetum are
formed from an intercalary meristem. If analogies are to be
sought with other pteridophytes, then it is not the internode,
but the node, which should be compared. The vascular
structure of the node can best be looked upon as a meduUated
protostele. The internodal spaces then appear as perfora-
tions, albeit of a pecuhar (intercalary) origin.
Growth at the stem apex takes place as a result of the
activity of a single tetrahedral apical cell, daughter cells
being cut off in turn from each of its three cutting faces.
Despite the spiral sequence of such daughter cells, subse-
quent growth results in a whorled arrangement and three
daughter cells together give rise to all the tissues which make
up a node and an internode. It is interesting that, in the
first-formed stem of the young sporeUng, there are three
leaves in each whorl, but, nevertheless, it is stated that their
initiation is in no way determined by the position of the
cutting faces of the apical cell. Each leaf primordium grows
from a single tetrahedral apical cell, and in the angle be-
tween the leaf sheath and the axis, but on radii between the
leaves, lateral bud primordia arise, also with a single apical
cell. The lateral bud primordia subsequently become buried
by a fusion of the base of the leaf sheath with the axis, with
the result that, when it grows, it has to burst through the
leaf sheath, so giving the appearance of an endogenous
origin. However, not all branch primordia do grow, for in
species such as Equisetum hiemale, although present, they
are inhibited from growing beyond the primordial stage,
unless the main stem apex should be destroyed or damaged.
Each branch primordium, besides bearing leaf primordia,
also bears a root primordium which in aerial axes is also
inhibited from growing further. In underground axes, how-
ever, they are not inhibited in this way. It is interesting to
note that the roots which are apparently borne on a horizon-
tal rhizome are, in fact, borne by the axillary buds hidden
with its leaf sheaths, and not directly upon it.
SPHENOPSIDA III
The root grows from an apical cell with four cutting faces,
the outermost of which gives the root cap. It may be triarch,
tetrarch or diarch in its vascular structure and there is
usually just a single central metaxylem element. The stele is
surrounded by a pericycle, whose cells correspond exactly in
number and radial position with those of the endodermis,
since they are formed by a perichnal division in a ring of
common mother cells. This has led to the statement that the
root has a double endodermis, but this is incorrect, since the
cells of the inner ring are without Casparian strips, and must
be regarded as pericycle.
The cone (Fig. i6L) invariably terminates an axis, whether
it be the main axis or a lateral one, and bears whorls of
sporangiophores, without any bracts or other leaf-Hke
appendages interposed, although there is a flange of tissue
at the base of the cone called the 'collar'. Each sporangio-
phore is a stalked peltate structure, bearing five to ten
sporangia which, although having their origin on the outer
surface, become carried round during growth into a reflexed
position on the underside of the peltate head (Fig. i6M).
Within the cone axis, the vascular system forms a very
irregular anastomosing system, without discernible nodes
and internodes, from which the sporangiophore traces
depart without any regular association with the gaps. The
sporangiophore trace branches within the peltate head and
each branch terminates near a sporangium.
The sporangium has its origin in a single epidermal cell,
which divides perichnally into an inner and an outer cell.
The inner cell gives rise to sporogenous tissue. The outer cell
gives rise to further blocks of sporogenous tissue and also to
the wall of the sporangium. Adjacent cells may also add to the
sporogenous tissue. The sporangium may therefore be des-
cribed as eusporangiate in the widest sense and at maturity
the sporangium is several cells thick. The innermost wall
cells break down to form a tapetum, as also do some of the
spore mother cells, and the ripe sporangium is two cells
112 THE MORPHOLOGY OF PTERIDOPHYTES
thick, of which the outer layer shows a characteristic spiral
thickening.
Each spore, as it matures, has deposited round it four
spathulate bands, which are free from the spore wall except
at a common point of attachment (Fig. i6N). These are
hygroscopic, coiling and uncoihng with changes in humidity,
and are referred to as 'elaters', although what function they
perform during dehiscence of the sporangium is not clear.
McClean and Ivimey-Cook^^ have shown that a distribution
curve of the size of spores in Equisetum arvense is a bi-modal
one, suggesting that a shght degree of heterospory exists, the
large spores being some 25 per cent larger than the small
ones. Furthermore, the smaller spores give rise to small male
prothalli, whereas the large spores produce hermaphrodite
ones. Whether this represents the early stage of the evolution
of heterospory, or the last stages of a reversion to homo-
spory, cannot be determined but, in any case, Uttle out-
breeding advantage is likely to accrue, because the elaters
become so entangled as the spores are being released that
they are usually distributed in groups. Reports of com-
pletely dioecious prothalh have been pubHshed, but these are
probably based on observations made at a single moment in
time. The prothalh o^ Equisetum are long lived, and extended
observations would probably show that any one prothallus
has archegonia alone for a time and then antheridia alone,
as has indeed been demonstrated in some species. Differences
in nutrition can also influence the behaviour of the prothalh
for, under favourable conditions, only male prothahi result.
Further work on this fascinating subject is clearly necessary.
The prothallus consists of a flat cushion of tissue, varying
in size from i mm across to 3 cm in some tropical species.
From the underside are produced abundant rhizoids, and
from the upper side numerous irregular upright plates, or
lobes, which are dark green and photosynthetic. Archegonia
are formed in the tissue of the cushion between the aerial
plates and ji&ve projecting necks of two or three tiers of
,.^^
SPHENOPSIDA 113
cells in four rows. There may be a single neck canal cell or
there may be two boot-shaped cells, lying side by side, as
illustrated in Fig. 16R. There is also a ventral canal cell.
The antheridia are sunken in the tissue of the basal cushion,
but may also occur on the aerial lobes. They are massive and
give rise to large numbers of antherozoids, which are spirally
coiled and multiflagellate (Fig. 16P).
The first division of the zygote is in a plane more or less
at right angles to the axis of the archegonium. No suspensor
is formed and the embryo is exoscopic. Fig. 16S shows the
spatial relationships of the stem apex (x), the first leaves (1),
the root (r) and the foot (f), as described as long ago as 1878,
but it is now becoming clear that the various parts of the
embryo are not so constant in position and origin as was
formerly thought.
There can be little doubt that the Equisetales are related
to the Calamitales, but it is most unhkely that they represent
their direct descendants. Remains of herbaceous plants
resembHng Equisetum are placed in the genus Equisetites,
They are traceable right back through the Mesozoic to the
Palaeozoic, where several species have been described from
the Upper Carboniferous. The situation is thus closely
comparable with Selaginella, whose herbaceous ancestors
were living alongside the related arborescent Lepidoden-
drales in Carboniferous times.
Pteropsida
Sporophyte with roots, stems and spirally arranged
leaves (megaphylls) often markedly compound and
described as 'fronds' (although some early mem-
bers showed Uttle distinction between stem and
frond). Protostehc, solenostehc or dictyostehc,
sometimes polycyclic (rarely polysteUc). Some
with limited secondary thickening. Sporangia
thick- or thin-walled, homosporous or hetero-
sporous, borne terminally on an axis or on the
frond, where they may be marginal or superficial on
the abaxial surface. Antherozoids multiflagellate.
Some botanists widen the definition of the Pteropsida to
include, not only the megaphyllous pteridophytes, but also
the gymnosperms and angiosperms, on the supposition that
all three groups are related. While this may well be so, it
seems preferable to retain the distinction between pterido-
phytes and seed-plants and to restrict the definition of the
Pteropsida so as to exclude all but the ferns. Even so, the
group is an enormous one, with over 9,000 species, and
shows such a wide range of form and structure that it is
almost impossible to name one character which is diagnostic
of the group. The reader will have noticed that almost all of
the characters Usted at the head of this chapter are qualified
in some way.
It will readily be appreciated that, in such a large group,
the correct status of the various subdivisions is very largely
114
PTEROPSIDA 115
a matter of personal preference. Accordingly, there are
almost as many different ways of classifying the group as
there are textbooks dealing with it, and this is particularly
true of the fossil members of the group.
At this point, only the major subdivisions are presented,
the details being deferred until each subgroup is dealt with.
A Primofilices*
1 Cladoxylales*
2 Coenopteridales*
B Eusporangiatae
1 Marattiales
2 Ophioglossales
C Osmundidae
Osmundales
D Leptosporangiatae
1 Filicales
2 Marsileales
3 Salviniales
Primofilices
This is a remarkable group of plants that first appeared in
the Middle Devonian and survived until the end of the
Palaeozoic. As the name suggests, they were probably the
ancestors of modern ferns. They may be classified as follows :
1 Cladoxylales*
Cladoxylaceae* Cladoxylon* (Hierogramma,
Syncardia, Clepsydropsis)
Pseudosporochnaceae * Pseudosporochnus*
2 Coenopteridales*
Zygopteridaceae* Austroclepis'^ , Metaclepsydropsis*,
Diplolabis* Dineuron*
Rhacophyton* Ankyropteris,*
Etapteris* { = Zygopteris,
= Botrychioxylon) Tubicaulis*
tl6 THE MORPHOLOGY OF PTERIDOPHYTES
Stauropteridaceae* Stauropteris*
Botryopteridaceae * Bo try op teris *
The Cladoxylales are a particularly interesting group,
whose correct phylogeny has long been a matter of con-
troversy. On the one hand, they show a number of features
in common with the Psilophytales and, indeed, Pseudo-
sporochnus has only recently^® been transferred from that
group. On the other hand, they show features in common
with the Coenopteridales, whose later representatives had
already begun to look fern-hke before they became extinct.
The group thus stands in an intermediate position which
strongly suggests a genuine phylogenetic connection be-
tween the two groups.
Several species of Cladoxylon are known, of which the
earhest is C. scoparium, and our knowledge of this is based
on one specimen about 20 cm long from Middle Devonian
rocks of Germany. According to the reconstruction of the
plant by Kraiisel and Weyland^^ (Fig. 17 A), there was a
main stem, about 1-5 cm in diameter, which branched rather
irregularly. Some of the branches bore fan-shaped leaves
(Fig. 17B) ranging in size from 5 mm to 18 mm long. Some
leaves were much more deeply divided than others, but all
showed a series of dichotomies. On some of the branches,
the leaves were replaced by fertile appendages which were
also fan-shaped, each segment terminating in a single
sporangium (Fig. 17C).
The vascular system was highly complex and was poly-
stelic; each of the separate steles was deeply flanged; both
scalariform and pitted tracheids were present in the xylem.
Such complex vascular structure is characteristic of all the
species of Cladoxylon and some had the additional comph-
cation of secondary thickening. C. radiatum was similar to
C scoparium in that all the xylem was primary, and Fig.
17D illustrates the way in which several xylem flanges were
involved in the origin of a branch trace system. It also
PTEROPSIDA 117
illustrates the 'islands of parenchyma', as seen in transverse
section, which are a common feature of the Zygopteridaceae
too. Another feature, shared with the Coenopteridales, is the
presence of 'aphlebiae' at the base of the lateral branch (or
petiole?). These were similar in position to the stipules of
many flowering plants and received separate vascular
bundles (i).
Fig. 17E illustrates another type of stem structure, found
in Cladoxylon taeniatum and several other species, in which
each of the xylem strands has an outer region of radially
arranged tracheids which are thought to have been formed
from a cambium. The arrows in the figure indicate that three
of the stem steles were involved in the origin of branch
traces. Successive branches, petioles and pinnae of descend-
ing order had progressively simpler vascular structures,
without secondary wood, and are described under separate
form-generic names. Thus, Fig. 17F shows the Hierogramma
type of stelar arrangement, in which there were six xylem
regions, each with islands of parenchyma. Lateral branches
from this had four xylem areas and are known as Syncardia
(Fig. 17G). Clepsydropsis (Fig. 17H) was probably the next
type of branch, or petiole, although there has been some dis-
agreement among palaeobotanists about this. Its stele, as
seen in transverse section, had the shape of an hour-glass
(hence the generic name) and from it lateral pinna traces
were given off" alternately, along with a pair of aphlebia traces
(i). It should be noted that similar clepsydroid steles are
known from a number of plants belonging to the Coenop-
teridales.
Pseudosporochnus is represented in Middle Devonian
rocks of Germany, Scotland, Scandinavia and North
America, but our knowledge of its morphology is based
chiefly on the German species P. Krejcii (Fig. 17 1). It had an
erect stem with a swollen base and a bushy crown of branches
which forked dichotomously and terminated in small
sporangia. According to Kraiisel and Weyland^^ there were
Fig. 17
Cladoxylon: a, reconstruction of S. scoparium; b, leaf; c, fertile
appendages; d, origin of branch traces in C. radiatiim; e, C.
taeniatum, portion of stem near origin of branch trace; f,
PTEROPSIDA 119
no organs that could be called leaves and, for this reason,
the plant was placed in the Psilophytales. However, Leclercq
has recently discovered abundant remains of the plant and
investigations by her and Banks show that there are, in
fact, spirally arranged leaves with ^several successive pairs
of opposite divisions ; each of the numerous divisions then
divides by several successive dichotomies ; the whole appen-
dage is arranged in three dimensions'. Some of the leaves
were fertile and their ultimate divisions terminated in a pair
of sporangia. These workers were, furthermore, able to
observe the vascular system of the plant and found that it
had a very complex stellate form, as seen in transverse
section. Their conclusion, published in a preliminary note,^®
is that the genus has more in common with the Cladoxylaceae
than with any other group of plants and that it should cer-
tainly be removed from the Psilophytales.
Coenopteridales
This early group of ferns is a large one, consisting of many
genera and species. It showed a wide range of growth habit,
for some had creeping stems, others had erect trunks and
yet others were epiphytes. As with members of the Cladoxy-
lales, here too there is the problem of distinguishing leaf
Hierogramma type of stele; G, Syncardia type of stele; h, Clep-
sydropsis XyxiQ of siQlQ. Pseudosporochnus : i, reconstruction of
P. Krejcii. Metaclepsydropsis duplex: J, stem stele; k, petiolar
bundle near base ; l, petiolar bundle showing origin of laterals ;
M, model showing petiolar bundle giving off laterals. Ankyrop-
teris: N, A. Grayii, stem stele and origin of petiolar bundle; o,
A. westfaliensis, petiolar bundle. Etapteris: p, E. Scottii, petiolar
bundle and origin of laterals ; Q, E. Lacattei, reconstruction of
sterile frond; r, E. Lacattei, reconstruction of fertile frond;
s, E. Lacattei, sporangia
(1, aphlebia traces; 2, peripheral loop; 3, branch trace)
(a-c, I, after Krausel and Weyland; d-h, p, Bertrand; j-l,
Gordon; n, Scott; q, r, Hirmer; s, Renault)
120 THE MORPHOLOGY OF PTERIDOPHYTES
from stem and the term 'Phyllophore' is sometimes used
for intermediate orders of branching.
Austroclepsis, occurring in Lower Carboniferous rocks of
AustraUa, was first described^® as a species of Clepsydropsis,
on account of its clepsydroid petioles. However, the mode of
growth of the plant and the internal anatomy of the stem
show that it was not a member of the Cladoxylales. It had a
stout trunk, at least 30 cm in diameter and 3 m high, that
must have looked superficially like modern tree ferns, but it
differed fundamentally from these in that, within the mass of
roots constituting the main bulk of the trunk, there were
several stems instead of just one. These branched within the
trunk and gave off numerous petioles in a 2/5 phyllotactic
sequence and these, too, continued to run up within the
trunk. Each of the many stems had a single stele, usually
pentarch, in which there was a central stellate region of
mixed pith surrounded by a zone of tracheids. The petioles
had a rather narrow clepsydroid stele with two islands of
parenchyma bounded by ^peripheral loops' of xylem, and it
was from these peripheral loops that pinna traces were given
off from alternate sides at distant intervals, each associated
with aphlebiae.
Metaclepsydropsis duplex, from Lower Carboniferous
rocks of Pettycur, Scotland, ^^ had a creeping dichotomous
stem, from which erect *fronds' arose at intervals. Its stele
was circular in cross section or (just before a dichotomy) oval
(Fig. 17J), with an inner region of mixed pith and an outer
zone of large tracheids. The only protoxylem present was
that associated with the origin of a leaf trace, there being no
cauHne protoxylem at all. The leaf trace was at first oval in
cross section (Fig. 17K) but soon became clepsydroid (Fig.
17L). Pinnae were borne in alternate pairs, along with
aphlebiae (i). In giving rise to a pair of pinna traces, the
peripheral loop (2) became detached and then split into
two (3). A new peripheral loop then quickly re-formed.
Diplolahis Roemeri occurs in the same rocks and was very
PTEROPSIDA 121
similar to Metaclepsydropsis. Its stem anatomy differed,
however, in that the inner region of xylem consisted entirely
of tracheids. The tracheids of the outer region were arranged
in radial rows, but are nevertheless beheved by some to have
been primary in origin. The petiolar trace had a very narrow
'waist', with the result that it appeared X-shaped in cross
section.
Dineuron ellipticum, also from Pettycur, on the other hand
had no *waist' at all in the petiolar trace, which was elhptical
in cross section.
In all three of these Lower Carboniferous genera, the
origin of pinna traces was the same, suggesting that pairs of
lateral pinnae were arranged alternately along the petiole,
or phyllophore. The frond was thus a highly compound one
whose components formed a three-dimensional structure.
However, it had not been realized just how complex they
were until the important discovery, in 195 1, of a mummified
specimen of Rhacophyton zygopteroides.^^ That this plant
belonged to the Zygopteridaceae was established by examin-
ing its internal anatomy. It had a fairly stout stem bearing
roots and spirally arranged fronds. The lowermost fronds
were sterile and were bipinnate, the pinnules consisting of
dichotomous branchlets, apparently without any flattening
to form a lamina. The fertile fronds were much larger and
more complex, and had pairs of pinnae arranged alternately,
just as had been deduced for Metaclepsydropsis from a study
of petrified material. Each of the paired pinnae was similar
in its branching to a sterile frond. Whereas the lower pinna
pairs had branched aphlebiae, these were replaced in the
higher pinna pairs by profusely branched structures bearing
numerous terminal sporangia. These were about 2 mm long
and were without any specially thickened annulus.
At least eight species are known of the Upper Carbonifer-
ous genus Ankyropteris, which derives its name from the
fact that the petiolar trace in some species, e.g. A. westfali-
ensis, was shaped hke a double anchor (Fig. 17O). In some
122 THE MORPHOLOGY OF PTERIDOPHYTES
Other species the petiolar trace was much less extreme,
having less 'waist', but all were ahke in that the islands of
parenchyma were much extended tangentially and in that
the peripheral loop remained closed throughout the origin
of a pinna trace. Another pecuhar feature was that the pinna
trace was undivided, suggesting that the pinnae were single,
instead of paired as in most other members of the group. A.
Grayi, from British coal measures, had a stem of considerable
length which was over 2 cm in diameter. It was probably a
climbing plant. The petioles were borne in a 2/5 phyllotactic
spiral, corresponding with the five rays of the stellate stele
(Fig. 17N). As in other members of the group, there were
two distinct regions in the stele, but the inner region showed
a clear distinction between a zone of tracheids and a
central pith, while the outer region showed no evidence of
radial arrangement at all and was clearly primary in origin.
The petiolar traces of Etapteris were pecuhar in that the
'peripheral loops' remained open throughout (i.e. there were
no loops at all). Two pinna traces became detached, fused
and then separated again, before passing out into the paired
pinnae (Fig. 17P). The Permian species, E. Lacattei, is inter-
esting in having progressed further than other members of
the group in the evolution of a photosynthetic lamina, for
the ultimate pinnules were flattened (Fig. 17Q). In the fertile
regions of the frond (Fig. 17R) the pinnules were replaced
by groups of sporangia. These were club-shaped, slightly
curved, and had a distinct broad annulus of thickened cells
(Fig. 17S). Some Etapteris fronds were attached to trailing
stems, while others belonged to tree-ferns with stout trunks.
The nomenclature of the latter is, however, rather trouble-
some. The names Zygopteris and Botrychioxylon which have
been used are probably synonymous. Z. primaria had a
trunk about 20 cm in diameter, most of which consisted of a
tangle of rootlets and leaf bases. In the centre was a single
stem 1-5 cm across, with a five-rayed stele showing the usual
two regions, but in this case the outer region looks very much
PTEROPSIDA 123
as if it had been formed from a cambium, and many mor-
phologists describe it as secondary wood. Botrychioxylon
paradoxum had a very similar appearance, but in this stem
the cells of the inner cortex were also regularly arranged in
radial rows. It would seem, therefore, that the whole of the
growing point of the stem must have been organized in a
pecuharly regular manner and that great caution should be
used in describing even the outer xylem as secondary.
Some species of Tubicaulis were tree ferns, while others
were epiphytes. They are characterized by a frond form
which approached closely to that of a present-day fern, for
the fronds coming off in spiral sequence from the stem were
pinnate and the pinnae were arranged in one plane.
Stauropteris is represented by two species, S. burntislan-
dica from the Lower Carboniferous and S. oldhamia from
the Upper Carboniferous. Although the method of branching
of the frond was similar to that of many of the Zygopteri-
dales, differences in the vascular system are sufficient to
warrant the creation of a separate family. The most import-
ant of these is the absence of islands of parenchyma in the
xylem of the petiolar traces. It is beheved that, so far, only
portions of fronds have been found and that the stems have
yet to be discovered. Fig. 18A shows how the frond of S.
burntislandica was constructed, pairs of pinnae arising alter-
nately along the petiole, each associated with aphlebiae.
Then each pinna gave rise to secondary pinnae in the same
way and this pattern was repeated at all levels of branching
within the frond. The vascular system of the petiole of S.
oldhamia (Fig. 18B) consisted of four regions of xylem either
contiguous or separate from each other, each with a mesarch
protoxylem. The smaller branches, however, tended to have
a single tetrarch strand.
Perhaps the most interesting feature of all about Stauro-
pteris burntislandica is the fact that it was heterosporous.
Its megasporangia (Fig. 18C), when found isolated, are
called Bensonites fusiformis. They were strangely fleshy at
124 THE MORPHOLOGY OF PTERIDOPHYTES
the base and most commonly contained two functional
megaspores along with two very small and, presumably,
abortive ones, although examples have been found with
four, six or eight megaspores. It is believed that the whole
structure was shed from the parent plant without prior
dehiscence. The microsporangia of S. oldhamia (Fig. i8D)
were spherical, were typically eusporangiate in having a
thick wall and had a terminal stomium where dehiscence
took place, but there was no annulus of thick-walled
cells.
In the past, the Botryopteridaceae were often described as
much simpler in their organization than the rest of the
Coenopteridales, but recent investigations on both sides of
the Atlantic have demonstrated that this is far from the case.
Botryopteris antiqua, from the Lower Carboniferous of
Scotland, is the earliest known species and was also the
simplest in its internal anatomy. It had traihng dorsiventral
axes up to 2 mm in diameter, which gave rise to erect, or
semi-erect, radial stems bearing petioles, in spiral succession,
and roots. The petioles then underwent branching, of up to
five successive orders, to produce a multipinnate branch
system. There was no flattening of the pinnules to form a
lamina anywhere in the frond of this species and the distinc-
tion between stem and petiole is purely arbitrary. The three
types of stele are illustrated in Fig. i8E, where '2' indicates
the one belonging to the trailing dorsiventral axis. It was a
soUd rod of tracheids with multiseriate pits or with scalariform
or reticulate pits. The single protoxylem group was lateral
and almost, but not quite, exarch. The radial stems were
about the same diameter, but the stele was circular in cross
section with the smallest tracheids (protoxylem?) in the centre
(3). The petioles were somewhat smaller, up to 1-4 mm in
diameter, and had an oval stele with a lateral protoxylem (4).
As the branches of the frond divided and sub-divided, the
stele became smaller and smaller until the ultimate pinnules
had only a few tracheids or even only one. The sporangia
Fig. 18
Stauropteris burntislandica : a, reconstruction of part of frond;
c, megasporangium {=Bensonites fiisiformis). Stauropteris
oldhamia: b, vascular system; d,. microsporangium. Botryopteris :
E, vascular strands of B. antiqua; f, petiolar strand of B. ramosa;
G, petiolar strand of B.forensis; h, vascular system of ^. trisecta;
I, reconstruction of part of the frond of an advanced species;
J, sporangium of B. globosa.
(1, aphlebia traces; 2, dorsi ventral stele; 3, radial stele; 4,
dorsiventral petiole trace)
(a, c, e, after Surange; b, g, Bertrand; d, f, Scott; h, Andrews;
I, Delevoryas and Morgan; J, Murdy and Andrews)
were globose, up to 0-25 mm across, and had a multicellular
annulus that occupied almost half the surface area.
A comparison of this early species with those of the Upper
Carboniferous and the Permian shows that there was a
trend in the evolution of the petiole trace towards a greater
degree of dorsiventrahty, together with an increase in the
number of protoxylems. Thus, Botryopteris ramosa (Upper
125
126 THE MORPHOLOGY OF PTERIDOPHYTES
Carboniferous) had a shallow gutter-shaped stele with three
protoxylems (Fig. i8F), whereas B.forensis (Permian) had a
stele shaped like the Greek letter oj in transverse section, with
up to fifteen protoxylems (Fig. i8G). Some of these later
species, furthermore, are known to have had laminate
pinnules (Fig. i8I).
The complexity of the branching of the later species of
Botryopteris is illustrated by the reconstruction of the stelar
system ofB. trisecta (Fig. i8H). Its erect stem had a cyhndri-
cal protostele and bore leaves in a spiral sequence. The
petioles had an oval vascular strand and branched into three.
The two lateral branches then trisected again but, whereas
the median traces in each case were co shaped, the lateral
ones were cylindrical, Uke the stem stele. The whole frond
was arranged in three dimensions, except for the ultimate
pinnules which were disposed in one plane.
Associated with this plant were found some remarkable
spherical masses, containing thousands of sporangia, which
are believed to represent the fertile parts of the frond, al-
though in the meantime they are described under a separate
specific name, Botryopteris globosa. The whole mass was up
to 5 cm across and had, running through it, a system of
branches with w shaped steles, but how it was connected to
the parent plant is not known. Each sporangium was pear-
shaped (Fig. 1 8 J) and the distal half consisted entirely of
thick- walled cells, except for a stomium of thin-walled cells
over the apex. In most species of Botryopteris, the sporan-
gium wall is described as only one cell thick, suggesting that,
in this respect at least, they were leptosporangiate. It is
apparently true of some of the sporangia of B. globosa, but
not of all, for some clearly had a second layer of thin-walled
cells on the inside. This may well have shrivelled after the
spores had been shed, so becoming invisible when petrified.
Thus, although approaching the leptosporangiate condition,
B. globosa had certainly not yet achieved it, and the same is
probably true of all the species.
PTEROPSIDA 127
Eusporangiatae
Marattiales
Asterothecaceae* Psaronius* Asterotheca,^
Scolecopteris,* Acitheca,"^
Eoangiopteris*
Angiopteridaceae Angiopteris
Marattiaceae Marattia
Danaeaceae Danaea
Christenseniaceae Christensenia
Ophioglossales
Ophioglossaceae Ophiglossum Botrychium,
Helmin thostachys
Marattiales
It was customary in the past to describe the Carboniferous
as the Age of Ferns. This was because of the abundance of
large fern-like fronds in the coal-measures, but it is now
known that many of them really belonged to gymnosperms,
for they have been found in association with seeds. Indeed,
it is now suspected that most of them were gymnospermous.
However, there can be no certainty about sterile fronds and
these must, therefore, be placed in a number of form genera
defined on the basis of the overall shape of the frond and on
the shape and venation of the pinnules. Pecopteris is one of
these and a large number of species are known. Some of
them were certainly gymnosperms, but others were equally
certainly ferns, for they bore sori of thick-walled sporangia.
The frond, sometimes as much as 3 m long, was many times
pinnate and the pinnules were attached along their entire
base, each with a single midrib. The lateral veins were some-
what sparse and branched dichotomously once or twice
(Figs. 19D and 19E) or remained unbranched.
Asterotheca is the name given to pecopterid fronds bearing
sessile sori made up of four or five sporangia fused at the
base into a synangium, but with the distal part free (Fig.
Fig. 19
of E. Andrewsii. Acitheca: c, sorus of A. ^^^>''"^/^^^',,^' 'f 5 ^
pinnae. Asterotheca: e, fertile pinnae of A. Candolleam, f.
PTEROPSIDA 129
19F). The sori were commonly arranged in two series along
the pinna, as illustrated in Fig. 19E, each associated with a
veinlet in the lamina. Scolecopteris was similar, except that
the sorus was elevated on a short pedicel, or receptacle
(Fig. 1 9 A). In Acitheca, the sporangia were elongated and
pointed and were arranged round a central plug-hke recep-
tacle (Fig. 19C). Eoangiopteris is regarded as a more advanced
type of sorus^^ since it was Hnear instead of radial. Each had
a cushion-like receptacle, on which were five to eight
sporangia (Fig. 19B). In all these genera, the sporangium
wall was very massive, many cells thick, and the number of
spores Hberated from each was very high, e.g. up to 2,000
in Aster otheca parallela.
Fronds of these various types are often found in associa-
tion with stout trunks that bore a superficial resemblance to
those of modern tree-ferns, some of them as much as 15 m
high, but organic connection between fertile frond and
trunk has not yet been demonstrated conclusively. The
evidence, nevertheless, suggests that Asterotheca fronds were
borne in a crown at the summit of trunks known as
Psaronius. Many species, belonging to a number of sub-
genera of Psaronius, are known and most of them had
remarkably complex stelar anatomy. Some of them were as
much as 75 cm across, but most of this width was occupied
by a thick mantle of roots, for the single stem in the centre was
sorus. Angiopteris : G, h, sorus of A. crassipes; o, s, vascular
system oiA. evecta ; w, young embryo ; x, older embryo. Marat tia :
I, J, sorus ofM.fraxinea; Q, pinna; t, prothallus of M. Douglasii;
u, archegonium. Danaea: k, l, sorus of D. elliptica; r, pinna;
Y, embryo. Christensenia: m, n, sorus of C. aesculifolia ; p,
pinna ; v, rhizome with leaf base
(1, stipule; 2, stipular flange ; 3, flange of lamina; f, foot; 1, leaf;
r, root; s, suspensor; x, stem apex)
(a, b, f, after Mamay; c, Scott; d, Brogniart; e, Hirmer; g-n,
p-R, Bower; o, s, Shove; t, u, y, Campbell; v, Gwynne-Vaughan ;
X, Farmer)
£
130 THE MORPHOLOGY OF PTERIDOPHYTES
only a few cm in diameter. The stele of most species was a
polycyclic dictyostele which, in the more complex types,
contained as many as eleven interconnecting coaxial
cylinders (or, rather, inverted cones fitting inside one
another). Each was dissected into a number of mesarch
meristeles completely surrounded by phloem, and the leaf
traces at any particular level arose from the outermost
system, while the inner systems were concerned with the
origin of leaf traces at higher levels. The earhest examples,
however, were simpler than this in their internal anatomy,
e.g. P. Renaultii from the Lower Coal Measures had an
endarch solenostele; and there is evidence that even the
complex Permian species had a relatively simple structure
near the base of the trunk, as would be expected by analogy
with present-day ferns. Although the trunks were widest at
the base, this was not because the stem within was wider
but because there were a greater number of rootlets in the
mantle; the stem v/as actually smaller towards the base.
Some species had the leaves arranged distichously, some in
three or four vertical rows, while others had them arranged
spirally, as in most modern representatives of the group.
The Marattiales are represented at the present day by
about 200 species, placed in six (or seven) genera, most of
which are confined to the tropics. Angiopteris (lOO species)
is a genus of the Old World, extending from Polynesia to
Madagascar, while Danaea (thirty-two species) is confined
to the New World. Marattia (sixty species) is pan-tropical
and extends as far south as New Zealand. Christensenia
{ = Kaulfussia) is monotypic and is confined to the Indo-
Malayan region. Most species have massive erect axes, but
they never attain the dimensions of the fossil Psaronius. The
largest, although reaching a diameter of i m, seldom exceed
this in height. Christensenia and some species of Danaea,
however, have creeping horizontal axes. The fronds of some
species are larger than in any other living ferns and may be
as much as 6 m long, with petioles 6 cm in diameter. They
PTEROPSIDA 131
may be as much as five times pinnately compound or, in
some species, only once pinnate, like a Cycad leaf, while
a few species have a simple broad lamina. Christensenia is
pecuhar in having a palmately compound frond, as the
specific name, C. aesculifolia, imphes. It is also pecuhar in
having reticulate venation, for all the other genera have
open dichotomous venation. All show circinate vernation,
i.e. the young frond is coiled Hke a crozier and gradually
uncoils as it grows. This is a feature which they share with
Leptosporangiate ferns but which is absent from the
Ophioglossales. With the exception of Danaea trichoman-
oides, all the Uving members of the group have very leathery
pinnules in whose ontogeny several rows of marginal initials
are active (instead of a single row of marginal initial cells,
as is more usual in leaves of other plants). In many
species there are swelhngs, or pulvini, at the base of the
pinnae and pinnules, which play a part in the geotrophic
responses of the leaf, and in all species there are thick fleshy
stipular flanges at the base of the petiole. Fig. 19V illustrates
the appearance of the growing point of Christensenia, show-
ing how the stipules (i) are joined by a commissure (2),
and how they are folded over the primordium. After the
frond has died and has been shed, the stipules and the leaf
base remain attached to the axis and contribute much to its
overall diameter.
The young parts of Marattia and Angiopteris are covered
with short simple hairs, while those of Christensenia 2ind
Danaea bear peltate scales. Bower^ suggested that the nature
of the dermal appendages in ferns can be a useful indicator
of primitiveness or advancement, hairs being more primitive
than scales; on this basis, therefore, Christensenia is rela-
tively advanced and this conclusion is supported by its
possessing reticulate venation. A comparison of fossil and
recent members of the group suggests that there has been
progressive reduction in height, from the tree-hke Carbon-
iferous forms, through an intermediate stumpy erect axis, to
132 THE MORPHOLOGY OF PTERIDOPHYTES
an oblique or horizontal creeping rhizome; and on this basis,
too, Christensenia along with Danaea is to be regarded as
relatively advanced.
The stem grows by means of a bulky type of meristem, not
referable to a single initial celP and is characterized by the
absence of sclerenchyma. Mucilage canals and tannin cells
are abundant throughout and give the tissues a very sappy
texture. The vascular anatomy of the stem is the most
complex of all living pteridophytes and is surpassed in
complexity only by fossil members of the group, such as
Psaronius. A transverse section of the stem of Angiopteris
(Fig. 19O) reveals a number of concentric rings of meristeles
which, in a dissection (Fig. 19S), are seen to be part of a
series of complex and irregular meshworks lying one within
the other, yet interconnected by 'reparatory strands'. The
whole system may be described as a highly dissected poly-
cyclic dictyostele, but can best be visuahzed as a series of
inverted cones of lace stacked inside each other. Although
each meristele in the sporeUng is surrounded by an endo-
dermis, in the adult state the endodermis is completely
lacking.
The earliest protoxylem elements to Hgnify are 'annular-
reticulate', i.e. adjacent rings of lignin are interconnected by
a network of strands, whereas later ones are reticulate. The
metaxylem elements are scalariform and, in Angiopteris, the
orientation of the elongated bordered pits is sometimes
longitudinal, instead of transverse. This pecuhar arrange-
ment has been called 'ob-scalariform'^^ and occurs else-
where in the Ophioglossaceae and a few leptosporangiate
ferns {Dennstaedtia and Blechnum).
Each leaf, in a mature plant, receives a number of traces
which arise from the outermost system of meristeles (the cut
ends of the leaf traces are represented in black in Fig. 19S),
but the root traces may arise from the innermost regions of
the stele, threading their way through successive cones on
their way to the cortex (cross-hatched in Fig. 19O). In those
PTEROPSIDA 133
Species with erect axes, the roots may emerge from the
cortex some distance above the ground, so forming prop-
roots. They are polyarch, with as many as nineteen exarch
protoxylems and, while the aerial portions are medullated,
as soon as the roots penetrate the soil the xylem extends
right to the centre. Those of young plants usually contain
a mycorrhizal fungus within the cortex (an oomycete known
as Stigeosporium marattiacearun).
In all genera, the sori are borne in a *superficiar manner,
i.e. on the dorsal surface of the lamina, and beneath a vein
or a veinlet. Christensenia has circular sori irregularly dis-
tributed between the main veins (Fig. i9P)but, in all other
genera, the sorus is more or less elongated beneath a lateral
vein (Figs. 19Q and 19R). In Angiopteris the sporangia are
free from each other (Figs. 19G and 19H), but in Marattia,
Danaea and Christensenia they are fused into a synangium
(Figs. 19I-N). Danaea is peculiar in having fleshy flanges
of tissue (3) projecting between the adjacent synangia (or,
according to some, in having the synangia sunken into a
very fleshy pinnule).
The first stage in the development of a sporangium is a
perichnal division of a single epidermal cell, of which the
inner half gives rise ultimately to the archesporial tissue,
while the outer half gives rise to part of the sporangium wall,
the rest of the wall being produced by the activity of
adjacent cells. At maturity, the sporangium wall is many
cells thick and there is a tapetum formed from the innermost
wall cells. The occurrence of numerous stomata in the
sporangium wall is an interesting feature rarely found else-
where and presumably associated with its massive structure.
Very large numbers of spores are produced from each
sporangium (e.g. 1,440 in Angiopteris, 2,500 in Marattia and
over 7,000 in Christensenia) and, since all the sporangia
within a sorus mature and dehisce simultaneously, prodigious
numbers of spores are shed.
In those species with free sporangia, e.g. Angiopteris, there
134 THE MORPHOLOGY OF PTERIDOPHYTES
is a crude kind of annulus of thickened cells, whose contrac-
tions pull the sides of the sporangium apart along a line of
dehiscence on the inner face (Fig. 19H). Those with synangia
have no such device ; instead, a thin part of the sporangium
wall dries and shrinks to form a pore through which the
spores can fall (Figs. 19K-N). The whole sorus in Marattia
is very woody and, when ripe, splits into two halves which
are slowly pulled apart, so as to expose the pores in each
sporangium (Fig. 19J).
Germination of the spores is rapid, occurring within a few
days of being shed, and they develop directly into a massive
dark green thalloid prothallus, which is mycorrhizal and is
capable of living for several years. An old prothallus may
be several centimetres long and may resemble closely a
large thalloid liverwort (Fig. 19T). The prothallus is mon-
oecious but, while the antheridia occur on both the upper and
lower surface, the archegonia are confined to the lower
surface, where they occur on the central cushion along with
rhizoids. Both types of gametangia are sunken beneath the
surface of the prothallus and the antheridium is large and
massive. The archegonium (Fig. 19U) has a large ventral
canal cell (except in Danaea) and a neck canal cell with two
nuclei. The antherozoids are coiled and multiflagellate, as
in other ferns.
The first division of the zygote is at right angles to the
axis of the archegonium, and the embryo is endoscopic.
Thus, since the archegonial neck is directed downwards, the
embryo is orientated with its shoot uppermost and, as it
grows upwards, it bursts its way through the tissues of the
prothallus. A minute suspensor is present in Danaea (Fig.
19Y) and in some species of Angiopteris, but Marattia,
Christensenia and most species of Angiopteris are com-
pletely without a suspensor. This lack of constancy is
paralleled in the Ophioglossales and has led to speculation
as to its phylogenetic implications. A suspensor is generally
held to be a primitive character and its presence even if not
PTEROPSIDA 135
universal in the Eusporangiatae, places them at a lower
level of evolution than the remaining ferns, from which it is
completely absent.
The epibasal hemisphere gives rise to the shoot apex (x)
and the first leaf (1) (Fig. 19W), but there is no regular
pattern of cell divisions and the hypobasal region gives rise
to a poorly developed foot (f) and, somewhat later, to the
first root (r) (Fig. 19X).
Chromosome counts give a haploid number n = 40 in
Angiopteris.
Ophioglossales
This group of plants, completely without any early fossil
record, is represented by about eighty living species, belonging
to three genera. Botrychhim (thirty-five species) is cosmo-
politan in distribution and Ophioglossum (forty-five species)
is nearly so, but Helminthostachys (monotypic) is restricted
to Indo-Malaysia and Polynesia. Two species are fairly
common in the British Isles, Botrychium Iwiaria, 'Moon-
wort' (Fig. 20A) which grows in dry grassland and on rocky
ledges, and Ophioglossum vulgatum, 'Adder's Tongue' (Fig.
20G) in damp grassland, fens and dune-slacks, while a third
species, O. lusitanicum, is restricted to grassy cUff tops in
the Channel Islands and the Scilly Isles.
The stem, in most species, is very short and is erect,
except in a few epiphytic species of Ophioglossum and in
Helminthostachys, where it becomes a horizontal rhizome
as the plant grows larger. Where the stem is erect, the leaves
arise in a spiral sequence, but in temperate regions it is
normal for only one leaf to be produced each year. In
Helminthostachys, the leaves are borne in two ranks along
the rhizome ; they are large and ternately compound, but in
the other two genera they are usually much smaller. Those of
Botrychium are pinnately compound ; those of Ophioglossum
are simple or lobed and, unhke those of the other two
genera, have a reticulate venation. At the base of the petiole
136 THE MORPHOLOGY OF PTERIDOPHYTES
there is a pair of thin stipules which enclose the apical bud;
and the next leaf, when it begins to grow, has to break its
way through the thin sheath covering it. UnUke all other
living ferns their leaves are not circinately coiled when young.
In all three genera, the fertile fronds have two distinct
parts, the fertile part being in the form of a spike which
arises at the junction of the petiole with the sterile lamina, on
its adaxial side. The fertile spike is pinnately compound in
those genera with a compound lamina and simple in
Ophioglossum, where the lamina is simple. Its morpho-
logical nature has been the subject of some considerable
discussion in the past but is now generally thought to repre-
sent two basal pinnae which have become ontogenetically
fused, face to face (i.e. it is believed that some early ancestor
of the group had two fertile basal pinnae, whose primordia
became fused during subsequent evolution). Today, the only
evidence for the double nature of the spike lies in its vascular
supply.
The roots are peculiar in being completely without root
hairs, a feature which is possibly connected with their
mycorrhizal habit.
Growth of the stem apex is from a single apical cell, and
its products are characteristically soft and fleshy, for they
are without sclerenchyma. The stem of the young sporehng
is protostelic, but soon becomes medullated. Later on, the
stem of Botrychium becomes solenoxyUc, i.e. there are leaf
gaps in the xylem, but not in the single external endodermis.
Ultimately, the appearance of a sporadic internal endo-
dermis may give rise to a rudimentary solenostele. Botrychium
is the only genus of living ferns to show secondary cambial
activity, and in some species it may give rise to a consider-
able thickness of secondary wood, composed of tracheids
and wood-rays. Rhizomes of Helminthostachys pass through
much the same stages of stelar organization, but the largest
specimens go one stage further and achieve true soleno-
stely, with an internal as well as an external endodermis.
Fig. 20
Botrychium: a, B. lunaria; b, fertile pinnule; c, vascular supply
to sporangia; d, prothallus of B. virginianum; e, archegonium;
F, embryo of B. obliquum. Ophioglossum: g, O. vulgatum; h,
portion of fertile spike; i, vascular supply to sporangia; J,
prothallus of O. vulgatum; k, archegonium of O. pendulum;
L, embryo of O. vulgatum
(f, foot; 1, leaf; r, root; s, suspensor; x, stem apex)
(a, g, after Luerssen; b, h, Bitter; c, Goebel; d, k, Campbell;
E, Jeffrey; F, Lyon; J, l, Bruchmann)
Ophioglossum varies considerably in its internal anatomy,
according to species. Some possess an outer endodermis,
but in most species it is absent, even in the young stages. The
leaf gaps in the xylem overlap one another, giving rise to a
network of meristeles, which form a rudimentary kind of
dictyostele.
The xylem is endarch in Botrychium and Ophioglossum,
but mesarch in Helminthostachys. The earliest formed proto-
xylem tracheids are very similar to those of the Marattiales ;
137
138 THE MORPHOLOGY OF PTERIDOPHYTES
later ones are reticulate (some being ob-reticulate) but
scalariform tracheids are absent. ^^ A pronounced feature of
all three genera is the distinctly bordered circular pits in the
metaxylem tracheids, but early accounts of the universal
presence of a torus in the pit closing membrane appear to be
incorrect. Bierhorst^^ records them only in Botrychium
dissectum and states that even in this species they are not a
constant feature.
The sporangia in all three genera are 'marginal' in origin.
In Botrychium, they are borne in two rows along the
ultimate pinnules of the fertile spike (Fig. 20B) and each
receives its own separate vascular supply from a vein running
into the pinnule (Fig. 20C). In Helminthostachys, the axis of
the fertile spike bears numerous 'sporangiophores' in several
rows, each bearing several sporangia and a few tiny green
lobes at the tip. The spike of Ophioglossum bears two rows
of sporangia fused together, beyond which the axis projects
as a sterile process (Fig. 20G). A number of vascular bundles
run longitudinally up the middle, anastomosing occasionally
and giving off lateral branches to the sporangia (Fig. 20I).
Early stages of development of the sporangium are similar
to those in the Marattiales ; a single initial cell undergoes a
perichnal division, the inner half giving rise ultimately to
the archesporial tissue, while the outer half goes to form
part of the sporangium wall. Adjacent cells contribute
further to the wall, which is very massive and several cells
thick at maturity. A tapetum of several layers of cells is
formed from the inner regions of the sporangium wall,
which break down to form a continuous Plasmodium in
which the spores develop. As in Marattiales, there are
stomata in the sporangium wall.
Dehiscence of the sporangium is transverse in Botrychium
and Ophioglossum (Figs. 20B and 20H), but longitudinal in
Helmifithostachys, and large numbers of spores are released
(more than 2,000 in Botrychium and as many as 15,000 in
Ophioglossum).
PTEROPSIDA 139
The prothallus in all three genera is mycorrhizal. Indeed,
the presence of the appropriate fungus is essential for the
growth of the prothallus beyond the first few cell divisions.
In most cases the prothallus is deeply buried in the soil and
lacks chlorophyll, but cases have been reported of super-
ficial prothalli, in which some chlorophyll was present.
Some have abundant rhizoids, but others are completely
without them.
The prothallus of Botrychium virginianum (Fig. 20D) is a
flattened tuberous body, up to 2 cm long. Antheridia appear
first and are deeply sunken. Large numbers of antherozoids
are liberated from each and escape by the rupturing of a
single opercular cell. The archegonium has a projecting neck
several cells long, a neck canal cell with two nuclei, and a
ventral canal cell (Fig. 20E).
The prothallus of Ophioglossum vulgatum differs in being
cyhndrical, and may be as much as 6 cm long (Fig. 20J).
Frequently, there is an enlarged bulbous base, in which the
bulk of the mycorrhizal fungus is located. (In both Figs.
20D and 20 J, the extent of the fungus is indicated by a broken
line.) As in Botrychium, the antheridia are sunken and pro-
duce very large numbers of antherozoids. Unlike Botrychium,
however, its archegonia are sunken too. In Fig. 20K, the
archegonium is illustrated at a stage just before maturity,
when there are visible two nuclei in the neck canal cell, but
just before the basal cell has divided. Indeed, a ventral canal
cell has rarely been seen, presumably because it disintegrates
almost as soon as it is formed.
As in the Marattiales, the first division of the zygote is in a
plane at right angles to the archegonial axis. In Helmintho-
stachys, the outer (epibasal) hemisphere undergoes a second
division, so as to produce a suspensor of two cells, while
the hypobasal hemisphere gives rise to a foot, a root and,
later, the stem apex. The embryo is thus endoscopic, but
during its further development its axis becomes bent round
through two right angles, so as to allow the stem to grow
140 THE MORPHOLOGY OF PTERIDOPHYTES
vertically Upwards. The embryo of some species ofBotrychium
is likewise endoscopic and has a small suspensor (Fig. 20F),
but in others including B. lunaria, there is no suspensor and
the embryo is exoscopic; and this is true of all species of
Ophioglossum (Fig. 20L). In all cases there is considerable
delay in the formation of the stem apex, and in some species
it may be several years before the first leaf appears above
the ground, by which time many roots may have been
formed. These long delays suggest that the mycorrhizal
association is an important factor in relation to the nutrition,
not only of the prothallus, but also of the young sporophyte.
Chromosome counts show a surprising range within the
group, for Botrychium has a haploid number n = 45, Helmin-
thostachys n = 46 or 47, while in Ophioglossum vulgatum
n = 250-260 and in Ophioglossum reticulatum n = 63i + io
fragments.
Despite these divergent chromosome numbers, there can
be Httle doubt that the three genera of the Ophioglossales
are fairly closely related, nor that they represent an ancient
and primitive group of ferns despite the lack of fossil
representatives. The reticulate venation of Ophioglossum,
its consohdated fertile spike and its complete lack of a
suspensor together suggest that it has reached a more
advanced stage of evolution than either of the other two
genera. As in the Marattiales, it seems that the upright
stem is the basic condition, since even in Helminthostachys
the young plant has an erect axis.
Regarding the relationships between the Ophioglossales
and the Marattiales, it is not easy to decide which characters
are significant. Of the many characters common to the two
groups, most indicate merely that they have reached roughly
the same stage of evolution, rather than that they are closely
related. These may be briefly listed as i. basically erect axis,
2. stipules at the base of the petiole, 3. absence of scleren-
chyma, 4. sporadic endodermis, 5. massive sporangium wall,
with stomata, the sporangia showing a tendency to fusion,
PTEROPSIDA 141
6. large spore output, 7. prothallus long lived, 8. massive
antheridium, 9. suspensor present in some, absent in others.
Characters which suggest that the two groups are only
distantly related are the circinate vernation of the Maratti-
ales and their superficial sori, contrasting with the absence
of circinate vernation from the Ophioglossales and their
marginal sporangia.
Osmundidae
Osmundales
Osmundaceae Zalesskya^ ^ Thamnopteris^ ^ Osmundites"^,
Osmunda, Todea, Leptopteris
The modern representatives of the Osmundales occupy an
isolated position among the ferns, intermediate in many
respects between the Eusporangiatae and the Leptosporan-
giatae but not necessarily, therefore, finking the two groups
phylogenetically, for they are an extremely ancient group
with an almost complete fossil history extending as far
back as the Permian. Those that have survived to the
present day can truly be described as 'living fossils'.
All have erect axes, bearing a crown of leaves ; and the
same is true of the fossil members, some of which had trunks
I m or more in height. Among the earliest representatives,
in the Permian, were several species of Zalesskya. These had
a sofid protostele in which there were two distinct regions of
xylem (an inner region of short tracheids and an outer one
of elongated tracheids forming an unbroken ring). The same
was true of Thamnopteris Schlechtendalii, but T. Kidstonii
had a sfightly more advanced stelar anatomy, in that the
central region was occupied by a mixed pith of tracheids
and parenchyma. Osmundites Dunlopii from the Jurassic
was similar to T. Kidstonii, but the contemporaneous O.
Gibbeana showed some dissection of the xylem ring into
about twenty separate strands.*^ Nevertheless, the stele was
still strictly a protostele, since there was a continuous zone
142 THE MORPHOLOGY OF PTERIDOPHYTES
of phloem (and, presumably, endodermis) round the out-
side. The term 'dictyoxyHc stele' can conveniently be used
to describe this arrangement. Poor preservation does not
allow any statement to be made about the central pith
regions of these two forms, but in the Lower Cretaceous
O. Kolbei there was definitely a mixed pith. The Cretaceous
species O. skidegatensis had a pith of pure parenchyma and
showed a further advance in having some internal phloem,
while O. Carnieri was the most advanced of all, in being
truly dictyostehc. This is most interesting, for it is a con-
dition not achieved by any modern representatives of the
group. Most of these are no further advanced in stelar
anatomy than the Jurassic Osmundites Gibbeana.
Of the living genera, Osmunda (fourteen species) is wide-
spread in both hemispheres, Leptopteris (six species) is con-
fined to Australasia and the South Sea Islands, while Todea
is represented by the single species T. barbara, found in
S. Africa and Australasia. (Some taxonomists include
Leptopteris in the genus Todea.) Only one species, Osmunda
regalis — the 'Royal fern' — is represented in the British flora.
Its stems are massive and branch dichotomously to form
large hummocks. Todea barbara may have a free-standing
trunk I m or more high, and so also may Leptopteris
hymenophylloides, while one species of Leptopteris from
New Caledonia attains a height of 3 m.
A transverse section of the stem of a mature Todea (Fig.
21K) exhibits a typical dictyoxylic condition. The central
medulla is surrounded by separate blocks of xylem, outside
which there is phloem and a continuous endodermis.
Occasionally, some internal phloem occurs, but no internal
endodermis. Most species of Osmunda are similar, but O.
cinnamomea sometimes has an internal, as well as an
external, endodermis (Fig. 21B). The types of xylem element
present are similar, in some respects, to those of the
Marattiaceae,^^ and the position of the protoxylem ranges
from endarch in Todea to nearly exarch in Osmunda.
PTEROPSIDA 143
The leaves, in most species, are leathery in texture, but
those of Leptopteris hymenophylloides are comparable with
those of the Hymenophyllaceae ('filmy ferns') and have a
thin pellucid lamina, only two or three cells thick, from
which stomata are completely lacking. During their develop-
ment the leaves of all species exhibit circinate vernation and
are covered with hairs. The base of the petiole is broad and
winged in a manner reminiscent of the Eusporangiatae and,
after the frond has been shed, the leaf base is persistent,
adding considerably to the diameter and the mechanical
strength of the stem.
The fronds of Osmunda regalis are twice pinnate, those
produced first in each season being sterile. These are followed
by partially fertile fronds (Fig. 21 A), while the last to be
produced are often completely fertile. The fertile pinnules
are very reduced tassel-Hke structures, representing just the
midrib. In the absence of a lamina, the sporangia cannot be
'superficial' and are usually described as 'marginal'. In
partially fertile fronds of O. regalis, the fertile pinnules
occupy the distal regions, but in those of O. Claytoniana
they occupy the middle regions. Todea bar bar a has once-
pinnate fronds in which the fertile pinnules show scarcely
any modification and the sporangia are superficial, being
densely scattered over the under-surface of the lamina.
They occupy the basal regions of partially fertile fronds
(Fig. 21H). The fronds of Leptopteris hymenophylloides are
large and many times pinnate, with the sporangia scattered
sparsely along the veinlets of unmodified pinnules (Fig.
2 1 F). In no case is there any tendency for the sporangia to
become aggregated into sori, nor is there any sign of an
indusium.
The sporangium is not strictly leptosporangiate, for
several cells play a part in its initiation and, at maturity, it
is relatively large and massive with a stout short stalk.
There is some variation in the shape of the archesporial cell,
as illustrated in Figs. 21I and 21 J, for it may be tetrahedral,
144 THE MORPHOLOGY OF PTERIDOPHYTES
as in leptosporangiate ferns, or it may be cubical, as in the
Eusporangiatae. The tapetum is formed from the outermost
layers of the sporogenous tissue, unlike that of the Euspo-
rangiatae, and there is also a layer of tabular cells, formed
from the same regions, which becomes appressed to the
inner side of the sporangium wall. For this reason, at
maturity, the wall appears to be two cells thick. There is a
primitive kind of annulus, formed by a group of thick-walled
cells, on one side of the sporangium and a thin-walled
stomium, along which dehiscence occurs, extends from it
over the apex of the sporangium (Fig. 21G). Relatively large
numbers of spores are released from each sporangium (e.g.
about 128 in Leptopteris and more than 256 in Osmunda and
Todea). The spores contain chlorophyll and must germinate
rapidly if they are to do so at all.
The prothallus (Fig. 2tC) is large, fleshy and dark green,
resembhng a thalloid liverwort, up to 4 cm long. The
antheridia (Fig. 21D) project from the surface, as in Lepto-
sporangiatae, but are larger, have more wall cells and pro-
duce a greater number of antherozoids than do most of
them. The archegonia (Fig. 21E) are borne along the sides
of the midrib; they have projecting necks and differ from
those of leptosporangiate ferns only in the number of neck
cells (six tiers, instead of the usual four).
The embryology of the young sporophyte, too, shows
some features which distinguish the Osmundales from the
Leptosporangiatae. Not only is the first division of the
zygote vertical, but so also is the second. It is the third
division which is at right angles to the axis of the arche-
gonium, instead of the second. Subsequent divisions are
somewhat irregular and the embryo remains spherical for a
relatively long time. Ultimately, however, a shoot apex,
cotyledon, root and a large foot appear, but there is some
irregularity in their derivation from the initial octants.
Despite the marginal position of the sporangia in
Osmunda, as compared with their superficial position in the
Fig. 21
Osmunda: a, partly fertile frond of O. regalis; b, stele of O.
cinnamomea; c, prothallus of O. Claytoniana; d, antheridium ;
E, archegonium; g, sporangium. Leptopteris: f, fertile pinnule
of L. hymenophylloides. Todea: h, fertile frond of T. barbara;
I, J, sporangial primordia (i with tetrahedral archesporial cell,
J with cubical archesporial cell) ; k, stele
(a, f, h, after Diels; c-e, Campbell; g, Luerssen; i, J, Bower;
K, Seward and Ford)
other two genera, the three genera are so similar in other
respects that they are, without doubt, closely related, and
this conclusion is supported by chromosome counts. The
haploid number is n = 22 throughout.
Filicales
In the past, the name FiHcales was applied in the broadest
possible sense, so as to include all the ferns but, recently, its
use has been restricted, and it is applied just to the homo-
sporous leptosporangiate ferns (as in Engler's Syllabus der
145
146 THE MORPHOLOGY OF PTERIDOPHYTES
Pflanzenfamilien^^). However, even when thus restricted, it
is still by far the largest group of the pteridophytes, for it
contains almost 300 genera and about 9,000 species. Details
of their form and anatomy would occupy many volumes
and can only briefly be summarized here, the following
famihes, subfamiUes and genera having been selected to
illustrate the salient points (the classification is based on that
of Holttum^^).
Schizaeaceae Sehftenbergia* , Klukia*, Schizaea, Lygodium,
Mohria, Anemia
Gleicheniaceae Oligocarpia* , Gleichenites*, Gleichenia
Hymenophyllaceae Hymenophyllum, Trichomanes
Dicksoniaceae Coniopteris*, Dicksonia, Cibotium
Matoniaceae Matonidium*, Matonia
Dipteridaceae Clathropteris* , Dictyophyllum*,
Camptopteris* , Matonia, Phanerosorus
Cyatheaceae Alsophilites*, Alsophila, Hemitelia, Cyathea
Dennstaedtiaceae
Dennstaedtioideae Dennstaedtia, Microplegia
Pteridoideae Pteridium, Pteris, Acrostichum (?)
DavalUoideae Davallia
Oleandroideae Nephrolepis
Onocleoideae (?) Onoclea, Matteuccia
Blechnoideae Blechnum, Woodwardia
Asplenioideae Asplenium, Phyllitis
Athyrioideae Athyrium
Dryopteridoideae Dryopteris, Polystichufn
Lomariopsidoideae Elaphoglossum
Adiantaceae Adiantum, Cheilanthes, Pellaea,
Ceratopteris, Anogramma
Polypodiaceae Platy cerium, Polypodium, Stenochlaena(J)
As might be expected in such a large group, there is a
considerable range of form and growth habit, from tiny
annuals to tall tree-ferns and from protosteUc forms to those
PTEROPSIDA
147
with highly dissected polycycUc dictyosteles, yet all are aUke
in the early stages of development of the sporangium. This,
together with its stalk, arises from a single cell. The first
division of the initial cell (Fig. 22O) is into an apical cell (i)
Fig. 22
Development of gametangia and sporangia as found in lepto-
sporangiate ferns, a, typical gametophyte. b-h, stages in develop-
ment of antheridium (diagrammatic), i, dehiscing antheridium.
J, antherozoid of Pteridium. k-n, stages in development of
archegonium. o-s, stages in development of sporangium of
Polypodium
(1, apical cell; 2, basal cell; 3, jacket cell)
(a, k-n, o-s, after Foster and Gifford; b-h, Davie; J, Sadebeck)
and a basal cell (2). Further divisions take place in each
(Fig. 22P) and give rise to a primary sporogenous cell
(shaded in Fig. 22Q) and a jacket cell (3). The former gives
rise to a two-layered tapetum and to a number of spore
mother cells, surrounded by a sporangium wall one cell
thick. Further details of sporangium development differ
according to species, for some have a long slender stalk,
only one cell thick, while others have a short and relatively
148 THE MORPHOLOGY OF PTERIDOPHYTES
thick stalk; the majority have a vertical row of thick-walled
cells, constituting the annulus, while some have an obhque
row and others merely a group of thick-walled cells ; some
have a high spore output, while in most species it is thirty-
two or sixty-four.
Most commonly the prothallus is either cordate or
butterfly-shaped ranging in size from a few mm to i cm or
more across. There is a midrib several cells thick, but the
wings of the prothallus are only one cell thick. It is surface-
living, green and photosynthetic, and there are rhizoids on the
underside, among which antheridia and archegonia are borne ;
the archegonia are usually concentrated near the growing
point, or 'apical notch'. Departures from this typical form
occur in certain famihes, e.g. some have filamentous pro-
thalli, resembhng an algal filament, while even subterranean
prothalli are known, but this habit is extremely rare.
Stages in the development of the archegonium are illus-
trated in Figs. 22K-N, the only variations being in the
number of tiers of neck cells at maturity. The structure of the
antheridium is also fairly constant throughout the Filicales.
Figs. 22B-H represent the various stages in the development
of the commonest type. The way in which successive cross
walls bulge upwards or downwards is peculiar and is res-
ponsible for the formation of the characteristic ring-shaped
cells of which the mature antheridium wall is constructed.^^
At maturity, the cap cell is pushed off (Fig. 22I) to release
the antherozoids (usually thirty-two in number) (Fig. 22J).
Some famihes have a slightly more massive antheridium,
composed of a greater number of wall cells and containing
more antherozoids ; these are beheved to be more primitive
than the rest.
The embryology of the leptosporangiate ferns is Hkewise
very constant throughout. The first cross-wall is almost
invariably longitudinal and the second transverse. Thus, the
zygote is divided at a very early stage into four quadrants,
two directed towards the apical notch of the gametophyte
PTEROPSIDA 149
(called the inner and outer anterior quadrants) and two
away from the notch (called the inner and outer posterior
quadrants). The outer anterior quadrant ultimately gives
rise to the first leaf, the inner anterior to the shoot apex, the
outer posterior to the first root, and the inner posterior to
the foot. This, at least, is the procedure described in
classical studies, but more recently it has been stated that
the fate of the four quadrants is not always so clearly
defined. ^^
Statements that certain characters are primitive and others
advanced can be made with more certainty for the Filicales
than for any other group in the plant kingdom, because of
the large number of fossil representatives that are known.
Some of the famiUes had already become widespread by the
Mesozoic, while others appeared as long ago as the Car-
boniferous. A comparison of these with the rest of the living
Fihcales makes it possible to draw up an extensive list of
primitive characters for the group as a whole. The following
list is based on that of Bower^ (as modified by Holttum^^)
with additions by Stokey.^^
Rhizome — slender, creeping, dichotomous, with fronds in
two ranks on its upper side, protosteUc, covered with
hairs.
Fronds — large, amply branched, dichotomous and of un-
limited growth, the stipe (petiole) receiving a single leaf
trace, the ultimate pinnules narrow and with a single
vein; venation without anatomoses (i.e. *open').
Sort — containing few sporangia, terminating a vein.
Sporangia — relatively large, with stout stalk, without a
specialized annulus, developing and dehiscing simul-
taneously to liberate a large number of spores.
Spore germination — giving a plate rather than a filament
of cells.
Gametophyte — relatively large, thalloid, with a thick mid-
rib, slow to develop.
150 THE MORPHOLOGY OF PTERIDOPHYTES
Antheridium — large, containing several hundred anthero-
zoids ; wall cells more than four in number.
Archegonium — with a relatively long neck.
In the more advanced ferns, the dermal appendages are
usually scales instead of hairs and, as the stem assumes an
erect position, the leaves tend to form a crown at the apex.
With increasing size, the stelar anatomy becomes more
complex, the leaf-gaps overlap, and a dictyostele results.
True vessels are known to occur in at least two genera. ^^
The fronds become reduced in size and may have a simple
broad lamina with an entire margin and with anastomosing
veins, while the stipe receives a number of leaf traces. In
the most advanced ferns, the fronds are frequently 'jointed'
at the base, i.e. they are shed by means of an absciss layer, a
habit which may well be associated with Ufe outside the
tropics, in regions where seasonal changes in chmate may
be severe. Evolution of the sorus appears to have taken place
in stages, the first of which involved a regular gradate
sequence of development of the sporangia. The next resulted
in a mixed arrangement of old and young sporangia within
the sorus. Still more highly advanced is the condition des-
scribed as 'acrostichoid,' where the individuahty of the sorus
is lost and the sporangia form a 'felt' that covers the dorsal
surface of the lamina, irrespective of the position of vein
endings.
The various stages in soral evolution are often held to be
the most important indicators of relative advancement and,
on this basis, many pteridologists subdivide the Filicales into
SimpHces, Gradatae and Mixtae. It is important to reahze,
of course, that these subdivisions represent levels of evolu-
tion and not taxonomic groups. However, it is debatable
whether one character should be weighted to this extent, for
it is almost universally agreed among taxonomists that the
maximum possible number of characters should be used in
the assessment of phylogenetic status. If all the primitive
100
Fig. 23
Circular phylogenetic classification of the Filicales. Families and
subfamilies are arranged so that their radial position corres-
ponds to their relative advancement (primitive near the centre;
advanced near the outside). Broken lines enclose 'areas of
affinity', indicating close relationship. The numbers represent
successive grades of relative advancement, expressed as a per-
centage ('the advancement index'), ranging from the most
primitive (0%) to the most advanced (100%)
characters listed above are taken into account, it is possible
to calculate roughly an average 'advancement index' for
each family or subfamily, ranging from o per cent (the most
primitive) to lOO per cent (the most advanced). "^^ This has
151
152 THE MORPHOLOGY OF PTERIDOPHYTES
been done for the families and subfamilies selected for
detailed treatment, and they have been arranged (Fig. 23) on
a circular scheme, according to their advancement index.
The most primitive families are near the centre and the most
advanced are near the outside. The broken hnes, enclosing
'areas of affinity', indicate which groups are most closely
related to each other (in the main, the views expressed here
accord most closely with those of Holttum*^' ^^). Such a
scheme may be thought of as a view, looking down from
above, of the 'tree of evolution' of the Filicales, and while
it may not be acceptable to all taxonomists, it does avoid the
error, which is common to most phylogenetic classifications,
of suggesting that one modern family has evolved from
another modern family. ^^
The two most primitive famihes are the Schizaeaceae and
the Gleicheniaceae, and they are also the oldest, being repre-
sented in Carboniferous deposits by Senftenbergia and
Oligocarpia respectively. Both are represented in the Meso-
zoic, too (viz. Klukia and Gleichenites).
Schizaeaceae
The Schizaeaceae are represented today by four genera and
about 160 species, most of which are tropical or subtropical
in distribution. In all of them, the sporangia are borne
singly instead of in sori ('monosporangial sori') and they
show the most primitive type of dehiscence mechanism
known in the FiUcales. In all, the annulus consists merely of
a terminal group of thick-walled cells (Figs. 24A-D) and
dehiscence is longitudinal. The stalk of the sporangium is
short and thick and the spore output from each is 128 or 256.
The sporangia arise simultaneously, on the margin of the
frond, and are unprotected, except by the inrolUng of the
margin, or marginal flaps, of the pinnule. Lygodium is one of
the few modern genera of ferns to have fronds of unlimited
growth, forming twining structures 30 m or more in length.
Unlimited growth is a feature which, in most plants, is taken
PTEROPSIDA
153
to distinguish stems from leaves. When it occurs in fronds,
as in this case, it is, therefore, taken as evidence that they
have evolved from stem structures (or are still in the process
of doing so). Further evidence that the frond of Lygodium
Fig. 24
Sporangia of Filicales: a, Anemia; b, Schizaea; c, Lygodium;
D, Mohria; E, F, G, Gleichenia; H, i, Matonia; J, k, l, Hymeno-
phyllum; M, N, Cibotium; o, p, Hemitelia; Q, R, s, Dipteris;
T, u, Adiantum
(a-d, after Prantl; e-s, Bower; t, u, Miiller)
is very primitive is provided by the structure of the leaf
trace, which shows only slight departures from radial
symmetry. The other three genera have leaf traces which are
clearly dorsiventral and 'gutter-shaped'. Their stem struc-
tures, too, are more advanced for, whereas Lygodium has a
creeping protostelic rhizome, Schizaea has an oblique
rhizome with a medullated protostele, Anemia has a creep-
ing or oblique rhizome which is either solenostelic or dictyo-
steHc, while Mohria is dictyosteHc. It is interesting to note,
154 THE MORPHOLOGY OF PTERIDOPHYTES
also, that Mohria is the most advanced in its dermal
appendages, for they are glandular scales, whereas those of
the other three genera are hairs. In Anemia, only the two
lowermost pinnae are fertile.
The prothalli are flat thalloid structures, except in Schizaea,
where they are filamentous, with occasional mycorrhizal
cells and with the gametangia at the tips of short lateral
filaments. Bower remarked that these filamentous prothalli
are 'the simplest prothalli known among the Pteridophyta.
They suggest a primitive state, and provoke comparison
with green Algae'. However, their simplicity is now regarded
as the result of evolutionary speciaHzation, instead of repre-
senting a primitive state.
Of the four genera, Lygodium has the most complex
antheridial wall and the highest output of antherozoids
(156).
Gleicheniaceae
This family is represented by about 130 species belonging,
mostly, to the one genus, Gleichenia (some taxonomists
prefer to split the genus into four). A number of rather
different types of leaf morphology occur, two of which are
illustrated in Figs. 25C and 25D, but in all of them the growth
of the main rachis is arrested, until a pair of primary laterals
has formed. In some species, these are of limited growth
(Fig. 25C), but in others they too may terminate in dormant
buds, so producing a variety of patterns, some looking
superficially like a series of regular dichotomies (although,
in fact, they are psuedo-dichotomies, because of the dormant
apical bud in each angle). In others, there is a zig-zag
arrangement of branches (Fig. 25D). As in the Schizaeaceae,
therefore, the fronds are of indefinite growth, and some
attain a length of 7 m or more. They arise from a creeping
dichotomous rhizome which in most species is protosteHc.
A few, however, achieve a solenostelic condition, e.g.
G. pectinata, a relatively advanced condition which is associ-
PTEROPSIDA 155
ated with a larger number of sporangia in the sorus than is
usual in the genus. Yet, in this species, the dermal append-
ages are hairs, whereas scales are commonly present in
others. Divergent facts such as these serve to emphasize the
point that the evolution of different characters does not
necessarily keep step, the result being that most organisms
show a combination of advanced and primitive characters.
This is why it is unwise to focus attention unduly on one
character, when attempting to assess the relative advance-
ment of taxonomic groups.
The sporangia, in strong contrast to those of the Schizae-
aceae, are borne superficially on the adaxial side of the
frond. They develop simultaneously and are arranged in
sori containing, often, only a single ring of sporangia, seated
either at a vein ending or, more usually, over the middle of a
vein. There is no indusium at all covering the sorus, whose
only protection is a covering of hairs or scales. Each
sporangium is pear-shaped (Figs. 24E-G), has a stout stalk,
and dehisces by means of an apical slit. Dehiscence is
brought about by the contraction of the thickened cells of
the annulus, which runs obliquely round the sporangium
wall. Large numbers of sporangia are liberated from each,
ranging from 128 to more than 1,000.
The gametophyte is primitive, in that it is large, massive
and slow growing. When old, it becomes much fluted and
develops an endophytic mycorrhizal association. The anther-
idia are larger than in any other leptosporangiate fern and
resemble those of the Osmundales. Those of G. laevigata are
as much as ioo/a in diameter and contain several hundred
antherozoids.
Hymenophyllaceae
This group is commonly referred to as 'the filmy ferns',
because of their delicate fronds, the lamina of which is
usually only one cell thick. There are some 300 species of
Hymenophyllum, of which two occur in the British Isles, and
Fig. 25
Leaf form: a, Phanerosorus sarmentosiis ; b, Matonia pectinata;
c, Gleichenia longissima; d, G. linearis, var alternans. Sori: E,
Matonia pectinata ; F, Trichomanes alatum; g, Cibotium Barometz;
PTEROPSIDA 157
350 of Trichomanes, of which there is one in the British Isles.
Because of their deUcate nature, almost all of them are
confined to moist habitats, and most of them are restricted
to the tropics, where they commonly grow as epiphytes.
The British species H. tunbrigense may be seen growing on
rocks constantly wetted by the spray from waterfalls.
Most filmy ferns have a thin wiry creeping, protostelic,
rhizome, from which the fronds arise in two rows. In one
species, the stele of the rhizome is reduced to a single
tracheid, while in another there is said to be no xylem at
all. Some species are completely without roots. The leaf
trace is a single strand, which at the base of the stipe
shows marked similarity to the stem stele but, higher up the
stipe, broadens out into a gutter-shaped strand. The frond
is usually much branched, each narrow segment having a
single vein, but various degrees of 'webbing' occur and, in
one species, Cardiomanes reniforme ( = Trichomanes reni-
forme), there is a single expanded lamina. Nevertheless, the
venation is open in all species.
The sori are marginal, and most species are strictly
gradate. The vein leading to the sorus continues into a
columnar receptacle which, in Trichomanes, can grow by
means of an intercalary basal meristem until it forms a
slender bristle. The receptacle of Hymenophyllum has more
limited powers of growth or may lack them altogether. In
H, Cyathea Dregii; i, Dennstaedtia cicutaria; J, Micro lepia
Speliincae; k, Matteuccia struthiopteris {=Struthiopteris germa-
nicd); l, Dryopteris filix-mas; m, Polystichum lobatum; N,
Nephrolepis davallioides ; o, Pteris tripartita; p, Pteris cretica;
Q, Pteridiiim aqidlinum; R, Athyrium filix-femina; s, Adiantum
Parishii; T, Lomaria spicant; u, Blechnum occidentale; v.
Phyllitis scolopendrium : w, Asplenium lanceolatum
(1, outer indusium; 2, inner indusium)
(a, b, j, u, V, after Diels; c, d, o, Holttum; f, Eames; g, h, s,
Hooker; i, Baker; k, l, m, w, Luerssen; n, r, Mettenius; p, q,
T, Bower)
158 THE MORPHOLOGY OF PTERIDOPHYTES
such species, the sporangia are produced simultaneously,
but, where the receptacle can grow, new sporangia arise in
basipetal sequence. Surrounding the sorus is a cup-shaped
indusium in Trichomanes (Fig. 25F, where the broken Hne
indicates where the indusium was cut away to show the base
of the receptacle) and a two-lipped indusium in Hymeno-
phyllum.
The sporangium has a relatively thin stalk and an oblique
annulus, which brings about dehiscence along a lateral line
(Figs. 24J-L), by a process of slow opening, followed by
rapid closure as a gas phase suddenly appears in the cells
of the annulus. This mechanism is found throughout the
more highly evolved members of the Fihcales, and results in
the forcible ejection of the spores. The spore output varies
from 128 or 256 in Hymenophyllum to as low as thirty-two
in some species of Trichomanes.
The prothallus of Hymenophyllum is a strap-shaped
thallus, often only one cell thick, but, by contrast, the few
species of Trichomanes whose prothalH have been studied
have a filamentous structure which, like that of Schizaea, is
mycorrhizal.
Dicksoniaceae
The first recorded occurrence of a fossil member of the
Dicksoniaceae is of Coniopteris, from Jurassic rocks of
Yorkshire. Like modern members of the group, it had highly
compound fronds with marginal sori, protected by two flaps
(the upper and lower indusia). In the modern genus
Cibotium, the fronds are borne on stout creeping stems or on
low massive trunks, while some species of Dicksonia are tall
tree-ferns (e.g. D. antarctica), with a crown of leaves at the
summit of a tall trunk. All are characterized by a profuse
hairy covering over the stem and the base of the stipe, the
hairs being as much as 2 cm long in Cibotium barometz.
The stems are solenosteUc or (in species with erect axes)
dictyostelic, and the stele is deeply convoluted around a
PTEROPSIDA 159
large central pith region. There is a single gutter-shaped
strand entering the base of the stipe, but this soon breaks up
into numerous small bundles.
The sporangia are truly marginal in origin and arise in
strictly gradate sequence within a purse-hke box, formed by
the two indusia (Fig. 25G). They are long-stalked and have
an obhque annulus (Figs. 24M and 24N) which, in some
species, is very nearly vertical. The typical spore output per
sporangium is sixty-four.
Matoniaceae
This is a most interesting family, containing the two genera
Phanerosorus, from Sarawak and New Guinea, and Matonia,
from Malaya, Borneo and New Guinea. In spite of its
rarity at the present day, the family had many fossil repre-
sentatives in the Triassic. So characteristic is the method of
branching of the frond (Fig. 25B) that there can be little
doubt that the fossil Matonidium is correctly placed in this
family. After an initial dichotomy, each half of the frond
undergoes a regular series of unequal catadromic dicho-
tomies (i.e. each takes the main growing point further from
the median plane). Each pinna is pinnatifid and there are
anastomoses in the veinlets, particularly in the neighbour-
hood of the sori. Phanerosorus (Fig. 25A) has a frond of
indefinite growth which is long and slender and bears
dormant buds at the tips of some of its branches.
The stem of Matonia is creeping and hairy, and has a very
characteristic polycycHc stelar structure, with two co-axial
cylinders surrounding a central sohd stele. From these, a
single gutter-shaped leaf trace is formed, both cyhnders
playing a part in its origin.
The sori are superficial and consist of a small number of
sporangia arranged in a ring round the receptacle, which
continues into the stalk of an umbrella-shaped indusium
(Fig. 25E represents a vertical section through a young
sorus). There is an oblique convoluted annulus round the
l60 THE MORPHOLOGY OF PTERIDOPHYTES
Sporangium, dehiscence being lateral, although there is no
special stomium of thin-walled cells (Figs. 24H and 24I).
The spore output is sixty-four.
Dipteridaceae
This family is represented at the present day by some
eight species of the single genus Dipteris, restricted to the
Indo-Malayan region, but in Triassic times there were at
least three genera, Clathropteris, Dictyophyllum and Camp-
topteris. Again, the architecture of the leaf is quite character-
istic, and there can be little doubt as to the correct taxonomic
placing of these fossil forms. After an initial dichotomy, the
frond shows successive unequal dichotomies in an anadromic
direction (i.e. towards the median plane). This pattern is
represented in present-day species, in the venation of the
two halves of the frond. However, while the primary veins
are dichotomous, the smaller ones form a reticulum of a
highly advanced type, with blind-ending veinlets, as in the
leaves of many flowering plants.
The fronds arise at distant intervals along a creeping hairy
rhizome, whose vascular structure is a simple solenostele.
While some species have only a single leaf trace, others have
two entering the base of the stipe.
The sorus is superficial, completely without an indusium,
and the sporangia are interspersed with glandular hairs. In
Dipteris Lobbiana the sporangia arise simultaneously, but in
D. conjugata they are mixed. Thus, the single genus cuts
right across the division of the ferns into Simplices,
Gradatae and Mixtae.
The sporangia have relatively thin stalks (only four cells
thick) the annulus is obUque (Fig. 24Q-S), and dehiscence
is lateral. The spore output is sixty-four.
Cyatheaceae
This is the family to which most of the tree-ferns of the world
belong. Indeed, at one time, all tree-ferns were placed in it,
PTEROPSIDA l6l
but Dicksonia must clearly be removed on account of its
marginal sori, for the Cyatheaceae, as now constituted, have
superficial sori. The earUest known fossil representative of
the group is ^/^o;?/;////^^ from the Jurassic. Bower^ recognized
three Uving genera within the family: Alsophila with about
300 species, Hemitelia with about 100, and Cyathea with
about 300.
Although the largest may attain a height of 25 m, some
species are comparatively low-growing. Much of the dia-
meter of the trunk is composed of matted adventitious roots
and persistent leaf bases, while the stem within is relatively
small. Nevertheless, its stelar anatomy is highly complex for,
in addition to a convoluted dictyostele, there are abundant
medullary strands, and sometimes cortical strands too.
Broad chaffy scales form a dense covering over the stem
apex and the base of the frond.
The stipe receives a number of separate leaf-traces from
the lower margin of the associated leaf gap. While the fronds
of most species are several times pinnate, those of Cyathea
sinuata are simple. The venation is open in the majority of
species, except for very occasional vein fusions.
The three genera recognized by Bower are distinguished
by the character of the indusium but, otherwise, the sori
are very similar in their gradate development. In Alsophila
there is no indusium at all, in Hemitelia there is a large
scale at one side of the receptacle, and in Cyathea (Fig. 25H)
it extends all round the receptacle to form a cup which com-
pletely covers the globose sorus when young, but which
becomes torn as the sporangia develop and push through it.
Holttum,^^ however, regards this distinction between the
three genera as artificial, and prefers to merge them into the
one genus Cyathea. Furthermore, he has recently changed
his opinion as to the affinities of the family, for he now
draws attention to the close similarity between the scale-
like indusium of some species and the lower indusium of
Dicksonia.'^^^ *
l62 THE MORPHOLOGY OF PTERIDOPHYTES
The sporangium is relatively small, with a four-rowed
stalk, an oblique annulus (Figs. 24O and 24P), and a fairly
well marked lateral stomium. The spore output ranges from
sixty-four to sixteen, and even eight in some species.
We now come to the large assemblage of ferns whose sori
show the mixed condition and which Bower grouped to-
gether in the one big artificial family, the Polypodiaceae.
Some, he believed, had affinities with the Dicksoniaceae,
some with the Cyatheaecae and some with the Osmundaceae,
yet all had achieved the same advanced type of sporangial
structure, with a thin stalk, a vertical incomplete annulus,
and lateral dehiscence. Figs. 24T and 24U are two views of
the sporangium of Adiantum, which demonstrate the small
number of cells constituting the capsule, and the way in
which the stalk is composed of just one row of cells, in the
most highly evolved types.
In 1949 Holttum^^ suggested a more nearly natural
classification of these ferns, by creating a new family, the
Dennstaedtiaceae, within which he grouped a number of
subfamihes which, he believes, have affinities with the
Dicksoniaceae. In this new scheme of classification, the
Polypodiaceae constitute a very restricted family, having
affinities with the Matoniaceae, the Dipteridaceae being
absorbed into it. Within the Dennstaedtiaceae, so many
evolutionary processes have taken place that the group is
hard to define; indeed, it would almost seem that the sub-
families warrant elevation to family status.
Dennstaedtioideae
This is the most primitive of the subfamihes of the
Dennstaedtiaceae, for some species still retain the gradate
arrangement of sporangia in the sorus. Most have creeping
rhizomes with solenosteles. The sorus of Dennstaedtia (Fig.
25I) is very similar indeed to that of Dicksonia in having two
indusia. In Microlepia, however, the upper indusium is
PTEROPSIDA 163
greatly expanded (Fig. 25J), so that, in spite of its marginal
origin, the sorus appears to be superficial at maturity. This
represents an early stage in the evolutionary process which
Bower called the *Phyletic Slide', whereby the sorus ulti-
mately has a superficial origin despite is marginal ancestry.
Davallioideae
Davallia, likewise, has a superficial sorus at maturity,
covered by a funnel-shaped indusium, but which, neverthe-
less, is marginal in origin. The stem is creeping, with a peculiar
type of dissected solenostele, and is clothed with scales.
Oleandroideae
Nephrolepis has upright, dictyostelic stems with long run-
ners, by means of which vegetative reproduction occurs, for
the tips of the runners are capable of rooting and turning
into normal erect stems. Within the genus, there is a wide
range of soral form. A'^. davallioides (Fig. 25N) is very
similar to Microlepia, in that the upper indusium is scarcely
larger than the lower. In A'^. acuta, the sorus is superficial,
not only at maturity, but also in origin. A'^. dicksonioides
shows a different evolutionary trend, in that adjacent sori
are sometimes fused, and this trend has proceeded so far in
A^. acutifolia that the margin of the pinna has a sorus run-
ning continuously along it, between two linear indusia.
Pteridoideae
It is generally accepted that the sorus of Pteridium evolved
in a similar way to that of Nephrolepis acutifolia, for it, too,
is continuous along the margin of the pinnule (Fig. 25Q)
and is protected by two indusia. The upper indusium (i) is
relatively thick, but the lower one (2) is thin and papery.
Pteridium is one of the most successful ferns in its ability to
compete with flowering plants and this may, to some extent,
be due to the great depth at which its rhizomes spread be-
neath the surface of the soil. Its stele is a dicycHc perforated
164 THE MORPHOLOGY OF PTERIDOPHYTES
solenostele. Pteris also has a continuous sorus near the
margin of the lamina (i.e. the sorus is superficial in origin)
and the margin becomes inrolled to protect it (Fig. 25O).
In some species, e.g. Pteris cretica (Fig. 25P), the soral
region is somewhat expanded and indicates the way in
which the acrostichoid condition might have evolved. Indeed,
Bower suggested a close relationship between Pteris and
Acrostichum. Chromosome counts support this view, but
they also suggest that Pteris is wrongly classed with
Pteridium. The haploid numbers are, for Pteridium fifty-
two, for diflferent species of Pteris twenty-nine and 120 and
for Acrostichum thirty. The fact that in most of the Adianta-
ceae n = 29 or 30 suggests a possible affinity between Pteris
(and Acrostichum) and this family. It should be noted that
Lygodium, too, has a haploid number n = 29 or 30. Holttum
believes that another acrostichoid genus Stenochlaena is
closely related to Acrostichum, but a chromosome number
lying somewhere between seventy and eighty casts some
doubt on this. Bower placed it near Blechnum but, for the
time being, Stenochlaena should perhaps remain unplaced.
Onocleoideae
Holttum leaves this subfamily unplaced in his classification,
while Bower thought that it shows some affinities with the
Cyatheaceae and with the Blechnoideae. It contains two
genera, Matteuccia (two species) and Onoclea (monotypic).
Both are markedly dimorphic, with specially modified
fertile fronds. The fertile pinnae are narrow and the margins
are tightly inrolled so that protection of the sorus is derived
more from them than from the indusium, which is thin and
papery (Fig. 25K). Both are dictyostelic and covered with
scales. Matteuccia has open venation and Onoclea reticulate.
Dryopteridoideae
The ferns in this subfamily have a short stout stem which is
more or less erect, covered with scales and dictyostelic.
PTEROPSIDA 165
The stipe receives numerous leaf traces, and the venation is
open. The sori are superficial on the veins, or at vein endings,
and are covered by an indusium which in Dryopteris is
reniform (Fig. 25L) and in Polystichum is peltate (Fig. 25M).
Of these the reniform type is probably the more primitive,
for it is not far removed from the condition figured for
Nephrolepis (Fig. 25N). From this type, it is easy to
imagine the evolution of the radially symmetrical indusium
of Polystichum, by the extension of the 'shoulders' round the
point of attachment, followed by a 'fusion' to form a disc,
with a central point of attachment.
Athyrioideae
Some species of Athyrium have indusia that are identical in
shape with those of Dryopteris, but most have two types on
the same frond, as does the British A.filix-femina (Fig. 25R).
Here, there are some sori with reniform indusia and some in
which the indusium is extended along the lateral veins. The
vascular supply to the stipe of the frond consists of two leaf
traces, which unite into a single gutter-shaped strand higher up.
Lomariopsidoideae
All the members of this subfamily are acrostichoid. There
has been much discussion as to their affinities, but they
probably fie with the Davallioideae, for the stele of Elapho-
glossum is very similar to that of Davallia, in having two
large meristeles connected into a cyfinder by a network of
smaller bundles.
Asplenioideae
This subfamily, too, is befieved by Holttum to have affinities
with the Davalfioideae. The sorus of Asplenium (Fig. 25W)
is extended along the lateral veins and is protected by an
indusium which is usually acroscopic (i.e. its free margin is
directed towards the apex of the pinna). In this, it resembles
most of the sori of Athyrium. However, the vascular supply
l66 THE MORPHOLOGY OF PTERIDOPHYTES
to the stipe is different from that in Athyrium, for the two
bundles which enter it fuse into a single four-armed strand,
instead of into a gutter-shaped strand. The same is true of
Phyllitis. That Asplenium and Athyrium are closely related
seems fairly certain, since they have the same basic chromo-
some number, n = 36, and hybrids between them are known
to occur. In Phyllitis the sori occur in pairs, facing each
other, along the lateral veins (Fig. 25V), one acroscopic
and the other basiscopic.
Blechnoideae
Blechnum punctulatum forms a possible intermediate be-
tween Phyllitis and the more typical species of Blechnum,
for on one and the same frond both types of sorus may
occur, some in pairs facing each other and some showing
various degrees of fusion along a commissural vein. Wood-
wardia has a series of box-Hke sori, on either side of the mid-
rib, whose indusia are Uke hinged Hds. The typical Blechnum
sorus is a continuous one, as if the adjacent sori of a Wood-
wardia had become fused together, with the indusium facing
the midrib of the pinna (Fig. 25U). Each has beneath it a
commissural vein, which is visible in Fig. 25T, where part of
the two sori have been removed to expose it. The British
species, here figured, shows a considerable reduction of the
fertile lamina, and this reduction process has gone much
further in other members of the subgenus Lomaria, where the
lamina is almost completely lacking. Such species are
markedly dimorphic, for the sterile fronds have a normal
unreduced lamina. The genus shows a wide range of habit,
for some species are creeping, some are cHmbing, while
several have erect trunks, like small tree ferns.
Adiantaceae
This is a very diverse family, some members of which show
marked similarities with Mohria (Schizaeaceae). Their sori
are without indusia and occur along the veins or else form
PTEROPSIDA 167
'fusion sori' near the margin, much as in Pteris. Adiantum
has the sporangia restricted to the under side of special
reflexed marginal flaps of the lamina (Fig. 25S). The
majority of the members of the family inhabit fairly dry
regions and some are markedly xeromorphic, e.g. Cheilanthes
and Pellaea. However, at the other extreme, Ceratopteris is
a floating, or rooted, aquatic plant, now widespread in
tropical countries, where it chokes up canals and slow moving
rivers. Anogramma leptophylla is interesting, in having a
subterranean perennial prothallus, from which arise deUcate
annual sporophytes.
Polypodiaceae
Within this family are placed a number of genera of ferns,
all of which completely lack any kind of indusium. There are
about 1,000 species in the family, almost all tropical in
distribution (but note that Polypodium vulgare occurs in the
British flora), and most are epiphytic. Many have highly
complex anastomosing venation and some are acrostichoid,
e.g. Platycerium. This genus is markedly dimorphic, with
'nest leaves' appressed to the tree trunk on which it is grow-
ing, while the fertile fronds are quite diff'erent in shape and
give rise to the name 'Stag's horn fern'.
It will be clear, from this brief survey of the Filicales, that
there is much scope for disagreement among pteridologists
as to the relationships and detailed phylogeny of the group,
and that much more research is necessary before final con-
clusions can be reached. The areas of affinity indicated in
Fig. 23 must, therefore, be regarded as only tentative. On
the evidence so far available, it would seem that the group
might well be diphyletic, with two evolutionary starting
points, one with marginal and the other with superficial
sori. Furthermore, it seems clear that even among those with
marginal origins there has been a trend towards the super-
ficial condition. Should the Filicales prove to have been
l68 THE MORPHOLOGY OF PTERIDOPHYTES
monophyletic, however, then it is most probable that the
ancestral type had marginal rather than superficial sori, and
that the early Superficiales underwent a 'phyletic sUde' early
in their evolution, while the Marginales are proceeding more
slowly in the same direction.
'Water Ferns'
There are two interesting groups of leptosporangiate ferns
which, at one time, were classified together as the Hydro-
pterideae. Features which they show in common are hetero-
spory and a hydrophilous habit, but in other respects they
are so different as to warrant a much wider separation,
from each other and from the rest of the ferns. Accordingly,
their taxonomic status has been elevated to the Marsileales
and the Salviniales respectively.
Marsileales
Pilulariaceae Pilularia
Marsileaceae Marsilea, RegneUidium
All the members of the Marsileales have creeping rhizomes,
bearing erect leaves at intervals, on alternate sides. The only
member of the group represented in the British flora is
Pilularia globuUf era ('Pillwort'). Like all species oi Pilularia,
its leaves are completely v/ithout any lamina (Fig. 26A). The
leaves of the monotypic Brazihan genus RegneUidium have
two reniform leaflets. Marsilea occurs in temperate and
tropical regions, many of its sixty-five species occurring in
Austraha. Its leaves have four leaflets and somewhat
resemble a 'four-leaved clover' (Fig. 26B). All have soleno-
stelic rhizomes but, in Pilularia, the vascular structure is
much reduced, and the internal endodermis may be missing.
The sporangia, in all three genera, are borne in hard bean-
hke sporocarps, attached either to the petiole, near its base,
or in its axil, either stalked or sessile. The morphological
nature of these sporocarps has been the subject of much dis-
Fig. 26
Piliilaria: A, habit of P. globidifera. Marsilea: b, habit of M.
quadrifolia; c, vertical section of sporocarp; d, horizontal
section of sporocarp; e, dehiscing sporocarp; f, male game-
tophyte; g, female gametophyte of M. vestita; h, embryo within
female gametophyte
(f, foot ; 1, leaf; r, root ; x, stem apex)
(b, after Meunier; c, d, Eames — much simplified; E, Eames; f.
Sharp; g, Campbell; h, Sachs)
cussion, but it can most conveniently be regarded as a
tightly folded pinna (Hke a clenched fist) enclosing a number
of elongated sori, each covered by a membranous indusium.
Figs. 26C and 26D represent, very diagrammatically, the
structure of the sporocarp of Marsilea as seen in vertical and
horizontal sections, respectively (for clarity, the number of
sori has been reduced to two rows of five). Each receptacle
bears microsporangia laterally and megasporangia termin-
ally, and receives vascular bundles from a number of strands
169
lyO THE MORPHOLOGY OF PTERIDOPHYTES
running down in the wall of the sporocarp. Arching over the
top, is a gelatinous structure sometimes called a 'sporo-
phore' (cross-hatched in the figures) which swells up at
maturity and drags the paired sori from the sporocarp, as it
dehisces (Fig. 26E).
The sporocarp of Pilularia is similar in construction,
except that there are only four sori.
The sporangia are typically leptosporangiate in origin,
the sporangium wall is very thin, and there is a tapetum of
two or three layers of cells. The microsporangia contain
thirty-two or sixty-four microspores but, in the mega-
sporangia, all but one of the potential spores degenerate.
On dehiscence of the sporocarp, the delicate sporangium
wall rapidly decays and the spores begin to germinate almost
at once.
The male gametophyte (Fig. 26F) is extremely simple, as
in most heterosporous plants, consisting of nine cells only.
There is a single small prothaUial cell, and six wall cells
surround two spermatogenous cells (cross-hatched in the
figure) that give rise to sixteen antherozoids each.
The first cross-wall in the germinating megaspore is ex-
centrically placed and cuts off a small apical cell, whose
further divisions give rise to a single archegonium (Fig. 26G)
with a short neck of two tiers of cells, one neck canal cell,
a ventral canal cell and a large egg cell.
The first division of the zygote is longitudinal, and the
second transverse, giving four quadrants (Fig. 26H) of which
the outer two develop into the first leaf (1) and the first
root (r), while the inner two develop into the stem apex (x)
and the foot (f ). Meanwhile, the venter of the archegonium
grows and keeps pace, for a time, with the enlarging embryo
so as to form a sheath round it, from the underside of
which a few rhizoids may be produced. The first few leaves
in Marsilea are without a lamina and, therefore, closely
resemble the leaves of Pilularia.
It is often claimed that this interesting group of ferns
PTEROPSIDA 171
represents an evolutionary offshoot from an ancient schizae-
aceous stock. Arguments for this are based on the leaf form,
the type of hairs, the form of the sorus and the vestigial
annulus round the apex of the sporangium in Pilularia,^^
but the evidence is not very convincing and, in the absence
of early fossil representatives, the group must be regarded in
the meantime as an isolated one.
Salviniales
Salviniaceae Salvinia
Azollaceae Azolla
Whereas most of the members of the Marsileales are rooted
in the soil, either in or near water, all the members of the
Salviniales are actually floating. Azolla has pendulous roots,
but Salvinia is completely without them. Like the Marsile-
ales, their sporangia are borne in sporocarps. However, the
morphological nature of the sporocarps is quite different,
for each sporocarp represents a single sorus whose indusium
forms the sporocarp wall.
The only member of the group to be represented in the
British flora is Azolla filiculoides, described as recently
naturahzed from N. America. However, it was a native British
plant in Interglacial times.^^ It has an abundantly branching
rhizome, with a minute medullated protostele, and with
crowded overlapping leaves about i mm long (Fig. 27A).
These have two lobes, within the upper of which is a cavity
containing the blue-green alga Anabaena azollae.
Sporocarps arise on the first leaf of a lateral branch and
are usually of two kinds— large ones containing many
microsporangia and small ones containing a single mega-
sporangium, although sporocarps with both types of spor-
angium are sometimes present. The early stages of develop-
ment are similar in both types of sporocarp, for there is an
elongated receptacle on which numerous sporangial initials
arise. However, during development, the microsporangial
172 THE MORPHOLOGY OF PTERIDOPHYTES
initials abort in the one case (Fig. 27B) and the mega-
sporangial initials abort in the other. In both types of
sporangium there is an abundance of mucilaginous 'peri-
plasmodium', which becomes organized into 'massulae'. In
the megasporangium there are four such massulae, in one
of which the single megaspore is buried. Fig. 27C illustrates
the dehiscence of a megasporangium, the apex of which is
cast adrift as a cap over the four massulae. The megaspore
then germinates to produce a cap of prothallial tissue,
within which several archegonia develop (Fig. 27D).
When the microsporangium dehisces a variable number of
spherical frothy massulae are liberated, each with several
microspores near the periphery. Each bears a large number
of peculiar anchor-hke 'glochidia' (Fig. 27E). These become
entangled with the massulae surrounding a megaspore and,
together, they sink to the bottom, where the microspores
germinate, without being released from the massulae. The
male gametophyte (Fig. 27F) has a single antheridium from
which eight antherozoids are liberated.
The cleavage of the zygote is typical of the leptosporangi-
ate ferns, and as soon as the first leaf appears the sporehng
rises, carrying the massulae etc. once more to the surface.
There are about twelve species of Salvinia, several of
which occur in Africa. Its horizontal floating stems, up to
10 cm long, have a much reduced vascular anatomy and
bear leaves in whorls of three (Fig. 27G), two floating and
one submerged. Whereas the floating leaves are entire and
covered with pecuHar unwettable hairs, the submerged
leaves are finely divided into linear segments that bear a
striking resemblance to roots (Fig. 27H). However, it is
doubtful whether they perform the functions of roots.
Growth is rapid and fragmentation occurs easily, with the
result that ponds and lakes in tropical regions may rapidly
become covered and canals choked.
The first few sporocarps to be formed in each cluster
contain megasporangia, up to twenty-five in each, and the
PTEROPSIDA
173
later ones microsporangia, in large numbers, on branched
stalks (Fig. 27I). All except one of the potential megaspores
in each megasporangium abort, and the functional mega-
spore becomes surrounded by a thick perispore (Fig. 27J),
which later becomes cellular and comes to look, super-
ficially, like the pollen chamber of a gymnosperm seed.
Fig. 27
Azolla: a, portion of plant of A. filiculoides; b, sporocarp with
young megasporangium; c, megasporangium with massulae;
D, the same with female prothallus; e, massula from micros-
porangium; f, male prothallus. Salvinia: g, portion of plant of
S. natans; h, node with sporocarps; i, sporocarps with mega-
sporangia and microsporangia; J, megasporangium; k, micro-
sporangium; L, male prothallus; m, archegonium; n, female
prothallus with young sporeling attached
(1, column; 2, leaf; 3, root)
(b, after Pfeififer; c, e, Bernard; d, Campbell; f, l, Belajeff;
G, H, Bischoff; i, Luerssen; J, Weymar; k, h, Yasui; n, Lasser)
174 THE MORPHOLOGY OF PTERIDOPHYTES
Within the microsporangium, the sixty-four microspores
come to He at the periphery of a single frothy massula (Fig.
27K). They remain within the sporangium throughout and,
as they germinate, the male prothalli project all round. Each
male prethallus contains two antheridia (Fig. 27L) pro-
ducing a total of eight antherozoids.
The megaspore, too, remains throughout within the
sporangium, after it has become detached. The female pro-
thallus protrudes, as a cap of tissue from which extend
backwards two narrow horizontal wings, or *stabiHzers\
Several archegonia develop, in a row, across the upper side
of the projecting cap, each with a short neck, a neck canal
cell with two nuclei, and a ventral canal nucleus (Fig. 27M).
Fig 27N illustrates a young sporeHng, still attached to the
female prothallus within the megasporium, and shows the
peculiar development of a 'column' (i), which separates the
first leaf (2) and the stem (3) from the foot, which remains
embedded in the prothallus. The early stages of segmenta-
tion of the zygote are pecuHar and their morphological
relationships are not fully estabUshed. At no stage is a root
primordium distinguishable.
If the relationships of the Marsileaceae are obscure, those
of the Salviniales are even more so. The gradate origin of the
sporangia within the sporocarp, the intercalary growth of
the receptacle in Azolla and the vestigial oblique annulus
have led to the suggestion that the group has affinities with
the Hymenophyllaceae. However, this hardly seems accept-
able, in view of the many extraordinary features that mark
them off from all other ferns.
General Conclusions
In a book of this limited size it is impossible to describe
in detail all the fossil plants that are known. Accordingly
several major groups of vascular plants, many minor groups
and a large number of genera have had to be omitted. Thus,
there has been no mention of the Noeggerathiales, nor of the
Pseudoborniales, on the grounds that they occupy isolated
positions in the classification and throw almost no Hght at
all on the evolution of modern plants. For details of these
strange plants the reader is referred to textbooks of paleo-
botany, i. s. i*. 22
There are, also, several fossil genera of fronds and trunks
of which no mention has been made, since they seem to
stand midway between pteridophytes and gymnosperms
(e.g. Aneurophyton, Eospermatopteris, Tetraxylopteris, Proto-
pitys, Pitys, Archaeopteris, Callixylon and Archaeopitys),
and might appropriately be described in a text-book of
gymnosperms. However, there has been a recent suggestion^®
that these plants, while indeed ancestral to the gymno-
sperms, were, nevertheless, still at the level of pteridophytes
in their mode of reproduction. Brief mention of them must,
therefore, be made here. This suggestion arose out of the
discovery, in Upper Devonian rocks near New York, of
large fern-Hke fronds, known as Archaeopteris, actually in
organic connection with Callixylon, a large tree whose mas-
sive woody trunks were at least 20 m tall and more than i -5 m
across. The fronds of one species oi Archaeopteris are known
175
176 THE MORPHOLOGY OF PTERIDOPHYTES
to have had spores of two different sizes and hence cannot
have borne seeds as well. The realization that trunks with
this particular type of wood belonged to pteridophytes has
come as a surprise to many morphologists, for it has been
customary to think of them as gymnosperms. A new taxo-
nomic group has been suggested (Progymnospermopsida) to
contain the various genera listed above, that have affinities
both with the Pteropsida and with the seed-bearing plants.
While this group may indicate the direction in which the
pteridophytes were evolving towards higher forms, there are
unfortunately as yet no fossils linking them, in the reverse
direction, with their possible ancestors. Discussions still take
place as to whether pteridophytes evolved directly from
Algae or from Bryophyta, and as to whether, in either case,
they had a monophyletic or a polyphyletic origin. Until
more fossils are known from the Ordovician, Cambrian and
even the Pre-Cambrian, there would seem to be little hope of
agreement on these matters. There are some, indeed, who
doubt whether 'missing links' will ever be found. In the
meantime, relying on what we know with certainty to have
existed, we must guess at what their ancestors might have
been like.
Subjective processes of this kind have led to a number of
theories of land-plant evolution, of which theTelome Theory
has had the greatest number of adherents since it was first
propounded by Zimmermann-^ in 1930. According to this
theory, all vascular plants evolved from a very simple leafless
ancestral type, Uke Rhynia, made up of sterile and fertile
axes ('telomes'). In order to explain the wide diversity of
organization found in later forms, a number of trends are
supposed to have occurred, in varying degrees in the differ-
ent taxonomic groups. These are represented diagrammati-
cally in Fig. 28 (1-5) and are called respectively (i) plana-
tion, (2) over-topping, (3) syngenesis, (4) reduction, (5) re-
curving.
Starting from a system of equal dichotomies in planes
GENERAL CONCLUSIONS
177
successively at right angles (A), planation leads to a system
of dichotomies in one plane (B). Overtopping is the result
of unequal dichotomies, and tends to produce a main axis
with lateral branches (C) ; the culmination of this process is
Fig. 28
The Telome Theory: 1, planation; 2, overtopping; 3, syngenesis;
4, reduction; 5, re-curving, h-k, evolution in Sphenopsida;
L-o, evolution in Pteropsida; p-s, evolution in Lycopsida. The
Enation Theory : t-v, evolution of microphylls in Lycopsida
(a-s, after Zimmermann; t-v, Bower)
a monopodial system. Syngenesis results from the coales-
cence of apical meristems. When they fuse to form a
marginal meristem ('foliar syngenesis'), a lamina with veins
develops (D) and the process is called 'webbing'. Zimmer-
mann also visuahzes a second type of syngenesis ('axial
syngenesis') in which several branches become absorbed
into a single stout axis with a complex stelar anatomy (not
178 THE MORPHOLOGY OF PTERIDOPHYTES
shown in Fig. 28). While these three trends are in the direc-
tion of progressive elaboration, the fourth is in the opposite
direction ; reduction is supposed to have brought about the
evolution of the simple unbranched microphyll of the
Lycopsida. The fifth trend, re-curving, is found in several
groups of plants, where the sporangiophore becomes re-
flexed and the sporangium inverted, as in anatropous ovules.
Figs. 28H-K illustrate the way in which the sporangio-
phore might have evolved in the Sphenopsida. Here, re-
curving and syngenesis are the chief trends, resulting in a
peltate structure with reflexed sporangia. In the evolution of
the leaf of the Sphenopsida, however, the chief trends have
been planation, followed by reduction. Examples of inter-
mediate types existed among fossil members of the group :
Calamophyton, Hyenia, Eviostachya and Protocalamostachys
represented stages in sporangiophore evolution, while
Calamophyton and Asterocalamites provide stages in the
evolution of leaves. The Telome Theory, therefore, gives a
satisfactory explanation of the evolution of leaves, and of
sporangiophores, in this group. However, the growth habit
of the earliest members (e.g. Calamophyton, Protohyenia and
Hyenia) was a long way from the theoretical ancestral type.
In the Pteropsida (Figs. 28L-O), planation, overtopping
and webbing have combined to produce the sterile and fertile
fronds of modern ferns. The fossil record provides abundant
examples of intermediate types of frond form (e.g. Pseudo-
sporochnus, Stauropteris, Botryopteris) but, again, the
growth habit of the earUest members was far removed from
the ancestral type postulated by the Telome Theory (in fact,
Cladoxylon was superficially very similar to Calamophyton).
In the Lycopsida (Figs. 28P-S), the chief trend is supposed
to have been reduction. The bifid tips of the sporophylls and
leaves of Protolepidodendron may be brought forward in
support of this suggestion, but otherwise the fossil record
lacks good examples of intermediate types. The microphyll
had almost completed its evolution by the time the group
GENERAL CONCLUSIONS I79
first appeared in the Cambrian {Aldanophyton) or the
Silurian (Baragwanathia).
The great appeal of the Telome Theory lies in its economy
of hypotheses and in the way it allows the whole range of
form of vascular plants to be seen in a single broad unified
vista. Yet, to some botanists, this unifying influence is
regarded as a dangerous over-simphfication, to be treated
with great suspicion. It is in its appHcation to the Lycopsida
that it is most open to criticism and, in our present state
of knowledge, rightly so. The American palaeobotanist
Andrews 2^ sums up his views in the following words:
*Zimmermann's scheme for the pteropsids, or at least some
pteropsids, has much supporting evidence; his concept for
the articulates may be valid, but we are only on the verge of
understanding the origins of this group ; his concept for the
lycopsids is, so far as I am aware, purely hypothetical.'
Figs. 28T-V illustrate the Enation Theory of Bower^
which suggests that microphylls are not homologous in any
way with megaphylls. According to this theory, microphylls
started as bulges from the surface of the stem, and then
evolved into longer and longer projections, at first without
any vascular supply, then with a leaf trace that stopped short
in the cortex of the stem and, finally, with a vascular bundle
running the whole length of the organ. The microphyll,
therefore, has evolved by a gradual process of enlargement,
rather than by progressive reduction, and for this theory the
fossil record does provide some support : Psilophyton repre-
sents the first stage in the process (Fig. 28T), Asteroxylon
provides an example of the intermediate stage, where the
leaf-trace stops short (Fig. 28U), while Drepanophycus
represents a later stage with the leaf-trace entering the
lateral appendage (Fig. 28V).
Whether the Lycopsida evolved in this way, or in the
manner suggested by Zimmermann, the starting point is,
nevertheless, the same in both cases — a plant with naked
forking axes — and it has been customary to quote Rhynia
l8o THE MORPHOLOGY OF PTERIDOPHYTES
and Horneophyton as examples of this type of plant. How-
ever, they were certainly not the ancestors of pteridophytes.
As Leclercq^^ emphasizes, they occurred much too late in
the fossil record for this to be possible, and represent the
last surviving examples of that particular growth form. As
Andrews^* suggests, the emphasis that has been placed on
Rhynia has drawn attention away from the great diversity
of form that is now known in Silurian and Middle Devonian
plants, and has led to an uncritical acceptance of the thesis
that vascular plants are a monophyletic group.
So far, these speculations as to the course of pteridophy te
evolution have centred around the sporophyte, since it is
this phase of the hfe cycle that is represented in the fossil
record. Even more speculative is the evolution of gameto-
phytes, concerning which there are the two diametrically
opposed schools of thought referred to, near the end of
Chapter 3, as 'Antithetic' and 'Homologous'. Mention was
there made of abnormal gametophytes of Psilotum, contain-
ing vascular tissues. The significance of this interesting dis-
covery was somewhat diminished for a time, however, when
it was shown that they were diploid ; but in relation to dis-
cussions of antithesis and homology chromosome counts
are, in a sense, *red-herrings'. This is made apparent by the
phenomena of apogamy and apospory, cases of which have
been recorded many times in pteridophytes since they were
first observed in 1874.
Apogamy is the development of a sporophyte directly
from the gametophyte without the intermediate formation
and fertihzation of gametes. The resulting sporophyte,
therefore, has the same haploid chromosome count as the
gametophyte. By 1939'^^ apogamy had been recorded among
ferns, in Pteris, Dryopteris, Pellaea, and Trichomanes, where
it is frequently preceded by the appearance of tracheids in
the gametophyte. More recently ^^ it has been recorded in
Thelypteris, Pteridium, Phyllitis and several species of Lyco-
podium. In the case of Phyllitis, the haploid apogamous
GENERAL CONCLUSIONS l8l
sporophyte was successfully reared until it produced
sporangia; however, as would be expected since it contained
only one set of chromosomes, meiosis failed and no spores
were produced. ^^
Apospory is, in a sense, the reverse process, being the
production of gametophytes directly from sporophytes with-
out the intermediate formation of spores. Thus, when
detached pieces of fern fronds are placed on an agar surface
they frequently develop directly into gametophytes of
normal shape and form. In such cases, the gametophyte has
the same diploid chromosome count as the sporophyte. So
numerous are the recorded instances of this phenomenon
that BelP^ suggests that it must be general among ferns;
yet the exact conditions under which it happens cannot yet
be specified.
As to the causes of apogamy, several theories have been
put forward, but the final word has certainly not been said
on this fascinating problem. In many cases, ageing of the
prothallus seems to be an important factor. Recent work in
America^^ on Osmunda, Adiantum and Pteridium has, how-
ever, demonstrated that apogamy can be induced by grow-
ing the prothaUi on an agar culture medium rich in glucose.
Clearly, therefore, under these highly artificial circum-
stances, the external environment can be an important
factor. That this might be so had been suspected for a long
time, since otherwise it was difficult to understand why a
diploid zygote developing inside a fertilized archegonium
should give rise to a sporophyte, while a diploid cell
developing by apospory should give rise to a gametophyte.
Confirmation of the view that the internal environment of
the archegonium exerts an important formative influence on
the nature of the embryo has recently come from experi-
ments in which young embryos of Todea were dissected
from the archegonium and grown on an artificial medium. ^^^
It was found that those removed before the first division of
the zygote developed into flat thalloid structures, whereas
l82 THE MORPHOLOGY OF PTERIDOPHYTES
those removed in later stages of development grew into
normal sporophytes. Whether the environment is entirely
responsible, however, for the normal regular alternation of
generations has been questioned. BelP'^ suggests that there
must be some internal factor at work and looks upon
gametophyte and sporophyte as two levels of complexity,
reflecting different states of the cytoplasm, which can be
accounted for in terms of cell chemistry. This interesting
hypothesis should stimulate further research into the causes
of alternation of generations in hving plants.
The present position, then, seems to be that there is no
fundamental distinction between gametophytes and sporo-
phytes, since they can be induced to change from one to the
other in either direction. They are 'homologous', as far as
can be judged from living plants, and one is led to speculate,
therefore, that they were probably ahke in form and structure
in the earliest ancestors of land plants. Merker's suggestion,^^
already mentioned in Chapter 2, that the horizontal axes of
the Rhyniaceae were gametophytes, instead of sporophytic
rhizomes, is of enhanced interest, therefore, because if con-
firmed it will provide the only kind of evidence which can
really settle the controversy. As with most problems of
macro-evolution, it is the palaeobotanist who has the key
within his reach.
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Index
Page numbers in italic refer to illustrations
Acitheca, 128, 129
acrostichoid condition, 150
AcrosHchum, 164
'Adder's tongue' fern, 135, 137
Adiantaceae, 166
Adiantum, 153, 156, 167, 181
advancement index, 151
Aldanophyton, 51, 53, 179
Alsophila, 161
Alsophilites, 161
alternation of generations, 13, 182
Anemia, 153, 154
Angiopteridaceae, 127
Angiopteris, 128, 130
angle meristem, 84, 87
Ankyropteris , 118, 121
Annular ia, 102, 104
annulus, 144, 149, 153
Anogtamma, 167
antheridium, 13
antherozoid, 13
antithetic theory, 48, 180
aphlebiae, 117, 118, 123
apical meristem, 21, 57, 87
apogamy, 180
apospory, 181
Archaeocalamites, loi, 102
Archaeopteris, 175
archegonium, 13, 45
archesporial cells, 60
Arthropitys, 104
Arthrostigma, 52
Articulatae (= Sphenopsida), 94
Asplenioideae, 165
Aspleniuni, 156, 165
Asterocalamitaceae, loi
Asterocalamites, loi, 102, 178
Asterophyllites, 102, 104
Asterotheca, 127, 128
Asterothecaceae, 127
Asteroxylaceae, 28
Asteroxylon, 34, 35, 179
Athyrioideae, 165
Athyrium, 156, 165
Austroclepis, 120
Azolla, 171, 173
Azollaceae, 171
Baragwanathia, 51, 179
Blechnoideae, 166
Blechnum, 156, 166
Bothrodendraceae, 68
Bothrodendron, 74
Botrychioxylon, 122
Botrychium, 135, 137
Botryopteridaceae, 124
Botryopteris, 124, 125, 178
Bowmanites, g6, 99
bulbils, 54
CALAMITACEAE, lOI
Calamitales, loi
Calamites, 102, 103
Calamophytaceae, 94
Calamophyton, 95, g6, 178
Calamostachys, 102, 105
Callixylon, 175
cambium, 22, 69, 76, 83, 95, 103,
117, 136
Camptopteris , 160
Cardiomanes, 157
carinal canals, 98, loi, 104, 109
casts, 22, 104
Ceratopteris, 167
Cheilanthes, 167
Cheirostrobaceae, 94
Cheirostrobus, 96, 99
Christens enia, 128, 130
Christenseniaceae, 127
Cibotium, 158
circinate vernation, 34, 35, 131, 143
circummeduUary strands, 73
Cladoxylaceae, 115
Cladoxylales, 116
Cladoxylon, 116, 118, 178
classification, 27
189
190 INDEX
Clathropteris, i6o
Clepsydropsis, 117, 118
club mosses, 53
Coenopteridales, 119
compressions, 23
Coniopteris, 158
Cooksonia, 31, 32
cork cambium, 22
cover cell, 45, 47
Cyathea, 156, 161
Cyatheaceae, 160
CyHndrostachya, 83
Danaea, 128, 133
Danaeaceae, 127
Davallia, 163
Davallioideae, 163
Dennstaedtia, 156, 162
Dennstaedtiaceae, 162
Dennstaedtioideae, 162
dermal appendages, 131, 150
diaphragm, 84, 90
Dicksonia, 156, 158
Dicksopiaceae, 158
Dictyophyllum, 160
dictyostele, 18, ig
dictyoxylic stele, 142
dimorphism, 164, 167
Dineuron, 121
dioecism, 15, 112
diploid, 13
Dtplolabis, 120
Dipteridaceae, 160
Dipteris, 153, 160
Drepanophycaceae, 50
Drepanophycus, 51, 52, 179
Dryopteridoideae, 164
Dryopteris, 156, 164, 180
Elaphoglossum, 165
elaters, 102, 112
enation theory, 177, 179
endarch xylem, 21
endoscopic embryology, 81
endosporic development, 14, 73, 80
Eoangiopteris, 128, 129
epibasal, 46, 63
Equisetaceae, 94
Equisetales, 106
Equisetites, 113
Equisetum, 102, 106
Etapteris, 118, 122
Eucalamites, 102, 104
Eusporangiatae, 127
eusporangiate development, 16
Eviostachya, 96, 99, 178
exarch xylem, 21
exoscopic embryology, 47, 113, 140
FIBONACCI SERIES, 59, 70
filamentous prothalli, 154, 158
Filicales, 145
filmy ferns, 155
foot, 46, 61, 63, 90, 113, 135, 139,
149
foramen, 79
form genera, 74
fossilization, 22
GAMETOPHYTE, 1 3
geological periods, 24, 25
Gleichenia, 153, 154, 136
Gleicheniaceae, 154
Gleichenites, 146
glochidia, 172, 173
glossopodium, 66, 88
Gradatae, 150
ground pines, 56
HAPLOiD, 13
Helminthostachys, 135
Hemitelia, 161
Heterophyllum, 83
heterospory, 14, 17, 73, 80, 89, 100,
105, 112, 123, 170, 172
Hierogramtna, 117, 118
Homoeophyllum, 83
homologous theory, 48, 180
homospory, 13
Hornea, see Horneophyton
Horneophyton, 30, 31, 180
horsetails, 106
Hydropterideae, 168
Hyenia, 95, g6, 178
Hyeniaceae, 94
Hyeniales, 95
Hymenophyllaceae, 155
Hymenophyllum, 153, 155
hypobasal, 46, 63
iNDusiUM, 156, 158
Isoetaceae, 50
Isoetales, 76
Isoetes, 76, 78
JACKET INITIAL, 46
Klukia, 146
LEAF GAPS, 18
Lepidocarpon, 71, 73
Lepidodendraceae, 68
Lepidodendrales, 68
INDEX
191
Lepidodendron, 67, 68, yi
Lepidophloios, 67, 69
Lepidophylluni, 70
Lepidostrobus, 71, 72
Leptopteris, 143, 145
Leptosporangiatae, 145, 147
leptosporangiate development, 16,
145, 147
Ligulatae, 66
ligule, 66, 71, 78
Litostrobus, 100
Lornaria, 166
Lomariopsidoideae, 165
Lycopodiaceae, 50
Lycopodiales, 53
Lycopodites, 64
Lycopodium, 53, 55, 61, 67
Lycopsida, 50, 177
Lygodiiim, 152, 153
Marattia, 12S, 130
Marattiaceae, 127
Marattiales, 127
Marsilea, 168, i6g
Marsileaceae, 168
Marsileales, 168
massnlae, 172, 173
Matonia, 153, 156, i59
Matoniaceae, 159
Matonidium, 159
Matteuccia, 156, 164
megaphylls, 18, 114
megaspores, 14, 73, 80, 90, 124, 170,
172
meiosis, 13
meristeles, 20
mesarch xylem, 21
M esocalamites , 104
Metaclepsydropsis, 118, 120
metaxylem, 21
Microlepia, 156, 163
microphylls, 18, 179
microspores, 14, 73, 80, 89, 170, 172
Mixtae, 150
Mohria, 153
monoecism, 15
moonwort, 135
morphology, 11
mummifications, 23
mycorrhiza, 32, 39, 43, 45, 62, 87,
133, 134, 136, 139, 155
NECK CANAL CELL, 46, 62
neck cell, 46
neoteny, 65
Nephrolepis, 156, 165
OLEANDROIDEAE, 163
Oligocarpia, 146
Oligomacrosporangiatae, 83
Onoclea, 164
Onocleoideae, 164
Ophioglossaceae, 127
Ophioglossales, 135
Ophioglossum, 135, 137
Osmunda, 142, 145, 181
Osmundaceae, 141
Osmundales, 141
Osmundidae, 141
Osmundites, 141
out-breeding, 16
overtopping, J77
Palaeostachya, 102, 105
parichnos strands, 70
Pecopteris, 127, 128
Pellaea, 167, 180
perforated steles, 20
periderm, 22, 69
peripheral loops, 118, 120
petrifactions, 23
Phanerosorus, 156, 159
phlobaphene, 40, 44
phyletic slide, in Palaeostachya, 106
in ferns, 163
Phyllitis, 156, 166, 180
Phylloglossum, 61, 65
phyllophore, 120
phyllotaxy, 59, 70, 77, 120
phylogeny, 12
Pilularia, 168, i6g
Pilulariaceae, 168
planation, 177
Platy cerium, 167
Pleiomacrosporangiatae, 83
Pleuromeia, 75, 78
Pleuromeiaceae, 68
polycyclic steles, 19, 21, 85, 159
polyploidy, 49, 66
Polypodiaceae, {sensu lato), 162
[sensu stricto), 167
Polypodium, 167
polystely, 21, 84, 85, 116, 118
Polystichum, 156, 165
Pothocites, 103
primary spermatogenous cell, 46
primitive characters in Filicales, 149
Primofilices, 115
prismatic tissue, 77
prothallial cell, 80, 90
prothallus, 14
Protocalamites, loi, 102
Protocalamostachys, 102, 103, 178
protocorm, 64
192 INDEX
Protohyenia, 95, g6, 178
Protohyeniaceae, 94
Protolepidodendraceae, 50
Protolepidodendrales, 51
Protolepidodendron, 51, 52, 178
protophyll, 64
protostele, 18, jp
protoxylem, 21
Psaronius, 129
Pseudosporochnaceae, 115
Pseudosporochnus, 117, 118, 178
Psilophytaceae, 28
Psilophy tales, 28
Psilophyton, 33, J5, i79
Psilophytopsida, 28
Psilotaceae, 38
Psilotales, 38
Psilotopsida, 38
Psilotum, 38, 41, 47, 180
Pteridium, 156, 163, 180
Pteridoideae, 163
Pteris, 156, 164, 180
Pteropsida, 114
QUiLLWORT, 76
RECAPITULATION, doctrine of, 57
recurving, 176, J77
reduction, J77, 178
Regnellidium, 168
resvirrection plants, 82
Rhacophyton, 121
rhizophores, 84, 87
Rhopalostachya, 54
Rhynia, 29, 31, 179
Rhyniaceae, 28, 182
royal fern, 142
Salvinia, 172, 173
Salviniaceae, 171
Salviniales, 171
Schizaea, 153
Schizaeaceae, 152
Scolecopteris, 128, 129
secretory tissue, 70
Selaginella, 82, 84
Selaginellaceae, 50
Selaginellales, 82
Selaginellites, 91
Senftenbergia, 146
Sigillaria, 71, 73
Sigillariaceae, 68
Simplices, 150
siphonostele, 20
solenostele, 18, jp
solenoxylic stele, 136
SphenophyUaceae, 94
Sphenophyllales, 97
Sphenophyllostachys, g6, 99
Sphenophyllum, g6, 97
Sphenopsida, 94
sporangia, 16
sporocarps, 168, i6g, 171, 173
sporophore, 170
sporophyll, 17, 52, 54, 73, 75, 81
sporophyll theory, 17
sporophyte, 13
'Stag's horn' fern, 167
Stauropteridaceae, 116
Stauropteris, 123, 123, 178
steles, 18, Jp
Stenochlaena, 164
Stigmaria, 71, 74
stomium, 124, 126, 144
strobilus, 56
Stylites, 78, 81
Stylocalamites, 104
suspensor, 61, 63, 134, 140
Syncardia, 117, 118
syngenesis, 177
TAPETUM, 42, 60, 133, 144, 147
telome theory, 176
teratology, 44
Thamnopteris, 141
Thelyptens, 180
Tmesipteridaceae, 38
Tmesipteris, 41, 42, 47
Todea, 142, 145, 181
tree ferns, 158, 160
Trichomanes, 156, 157, 180
Triletes, 91
Tuhicaulis, 123
UNLIMITED GROWTH IN FERN FRONDS,
152, 154, J56, 159
Urostachya, 54
VALLECULAR CANALS, Io8
velum, 78, 79
ventral canal cell, 46
vessels, 86, 109
WATER FERNS, l68
Woodwardia, 166
Yarravia, 31, 32
Zalesskya, 141
ZosterophyUaceae, 28
Zosterophyllum, 31, 33
Zygopteridaceae, 115
Zygopteris, 122
zygote, 13
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