Introduction

The study of the morphology of living 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 implications, as Arber has explained in her Natural Philosophy 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 coordination throughout the life of the organism. Thus, morphology impinges on all other aspects of living organisms (physiology, biochemistry, genetics, ecology, etc.). Furthermore, the morphologist must see each living organism in its relationship to other living organisms (taxonomy) and to extinct plants (palaeobotany) whose remains are known from the fossil record of past ages extending back in 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 palaeobotany, the plant morphologist 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 improbable today, now that more is known of the fossil record, and, likewise, theories that are acceptable today may have to be modified or abandoned tomorrow. It is essential, therefore, that the morphologist should avoid becoming dogmatic if he is ever to arrive at a true understanding of the course of evolution of living 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 microscope, while, on the other hand, there are seed-bearing plants, such as the giant Redwoods of California and the Gums of Australia, some of which are probably the largest living organisms that the world has ever known. Accompanying this range of size, there is a corresponding range of complexity of internal anatomy and of life-history. Somewhere between the two extremes, both in structure and in life-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 liverworts, yet in life-cycle they differ from them only in matters of degree.

The basic life-cycle, common to bryophytes and pteridophytes, is represented diagrammatically in Fig. 1. 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 antheridia. are known as antherozoids, since they are flagellated and are able to swim in water, while the female gametes (egg cells) are non-motile and are borne singly in flaskshaped archegonia. Fusion between an egg cell and an 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, likewise, diploid. Ultimately, 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.

Life cycle of a homosporous pteridophyte

In mosses and liverworts, the dominant phase in the lifecycle is the gametophyte, for the sporophyte is retained upon it throughout its life and is either partially or completely dependent on it for nutrition. By contrast, among pteridophytes 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 pteridophytes and the most primitive living members of the group) roots. Only the sporophyte shows any appreciable development 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 photo synthetic palisade and mesophyll cells of the leaf.

All these anatomical complexities confer on the sporophyte the potentiality 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 limitation on those species whose gametophytes are thin plates of cells that lack a cuticle and are, therefore, susceptible to dehydration. Not all gametophytes, however, are limited in this way, for in some pteridophytes 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 prothalli which bear only archegonia, and the smaller microspores giving rise to male prothalli 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.

The first concerns the nutrition of the prothallus and the subsequent embryonic sporophyte. The retention of the gametophyte within a resistant spore wall severely limits its powers of photosynthesis and may even prevent it altogether. 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 large size of the spores which are destined to contain an embryo sporophyte, but it does not explain why the prothalli 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 (bearing both archegonia and antheridia) are much more likely to be self-fertilized 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 prothalli 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 liberated 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 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 provided by the heterosporous habit will confer on the sporophyte the freedom to grow almost anywhere that its own potentialities allow and the possibility of out-breeding will favour more rapid evolution of those potentialities. 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 life-cycle of a typical heterosporous pteridophyte may be represented diagrammatically as in Fig. 2.

Life cycle of a heterosporous pteridophyte

The distinction between heterospory and homospory is one of the criteria used in the classification of pteridophytes, in accordance with the general belief that reproductive organs are a better guide to phylogenetic relationships than are vegetative organs. They are held to be more ‘conservative’, 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 taxonomic 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 periclinal (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 include a number of other differences. Thus, in leptosporangiate 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 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.

Until the early years of this century, it was widely believed 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, vegetative organs are nevertheless of considerable importance in classifying pteridophytes, for the shape, size, arrangement 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 familiar 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.

Fern steles

As might be expected, the leaf traces supplying microphylls 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 solid protostele. 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 continuous 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 representation 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 cylinder is lined with phloem, pericycle and endodermis, as if these tissues had ‘invaded’ the central parenchymatous region (though, needless to say, the developmental processes do not involve any such invasion). Fig. 3E illustrates the structure of a dictyostele in which three leaf gaps are visible in the one transverse section. Frequently it happens that each leaf gap is associated with the departure of several leaf traces to the leaf, but in this example, for clarity, only one trace is shown supplying 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 morphologists use a different system of terminology and group together 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 describe 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, however, 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 intervals on a horizontal axis their leaf gaps are unlikely to overlap, 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 depending 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 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 transverse section the plant is described as polystelic. Yet another variant is the polycyclic stele, in which there are two or more coaxial cylinders of conducting tissue (Fig. 3G).

All the vascular systems mentioned so far are composed entirely of primary tissues, i.e. tissues formed by the maturation 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 constructed 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 lignification of protoxylem 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 protoxylem is on the inner side of the metaxylem and differentiation 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 protoxylem is neither external nor central and differentiation proceeds 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 pteridophytes possess a vascular cambium from which secondary xylem and secondary phloem are formed. Cambial cells possess the power of cell division even though the surrounding 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 lived’. 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. 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. Examination 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 interpretation, 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, unfortunately, 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 difficult 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 polished surface is etched for a brief period in the appropriate 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. Furthermore, most fossils consist only of fragments of plants. It is then the task of the palaeobotanist to reconstruct, as best he can, from such partly decayed bits, the form, structure and mode of life 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 particular 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 million 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, extending 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 like 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.

Geological periods in the northern hemisphere

The sequence of the various geological periods is summarized as a table (p. 25), in which the time scale is based on information from R. N. C. Bowen. Brief notes are included to indicate the kind of vegetation that is believed to have existed during each period, but a word of caution is necessary 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 necessary 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 discovered, of deciding whether to modify the existing definitions 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 which this book is based is substantially the same as that proposed by Reimers in the 1954 edition of Engler’s Syllabus der Pflanzenfamilien 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.)

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