PROSEA, Introduction to Ferns and allies
Definition and diversity
Within the vascular plants, the pteridophytes constitute the third major group besides the angiosperms (flowering plants) and the gymnosperms (which includes the conifers and the cycads). The pteridophytes are apparently characterized by a negative character, namely the lack of flowers and seeds of even the simplest kind. Instead, they reproduce by means of spores, single, unfertilized cells designed to be dispersed and give rise to an alternating generation of completely different and much simpler plants, the prothalli. In section 1.4.3 this will be described by some detail. Four classes of pteridophytes are distinguished, which are briefly introduced below (see also Figure 1).
Ferns are the best known and dominant class, both in number of species and in number of individuals. They are characterized within the pteridophytes by their large leaves. Their often delicately divided leaves frequently shun direct sunlight and dominate the aspect of many forests. One family excepted (Ophioglossaceae), they all can be easily determined as ferns by the young leaves that burgeon curled up spirally, not without reason often compared with the top end of a violin (fiddle head), or a bishop's staff (crozier).
The clubmosses and related families constitute a second class. They have small leaves (cylindrical and rush like in one family) with the sporangia borne in the leaf axils. The clubmosses and the spikemosses are the better known members of this class. The unsuspecting observer will often take them for mosses, though they are generally coarser and sturdier. Some scrambling species may attain a length of several metres with solid, cord like main axes. The clubmosses as a rule do not compete well with modern plants and they are mostly found in niche habitats as epiphytic, epilithic and terrestrially growing species in mountain heaths. The spikemosses on the other hand are, at least in the Asian tropics, predominantly found in the shade of the forest floor or as low epiphytes. The third member family of this class, the grass like aquatic quillworts, has few species in tropical South East Asia, and all are very rare. Most representatives are found in clear mountain lakes and rivers.
Horsetails are characterized by the stems, consisting of distinct nodes, with more or less conspicuous vertical ridges. The stems may bear whorls of branches, each a little below a sheath of much reduced leaves. The sporangia are borne on sporangiophores, which are arranged in strobili (spikes). Usually there is a single strobilus at the top of the stem, but additional ones may develop at the top of the branches. In some species (not in South East Asia) the spike bearing stems are pale without chlorophyll, thicker and of softer texture than the sterile stems. Generally they are found on rather moist soils. They vary in size from 10 cm up to 12 m tall and to 2.5 cm in diameter, and in growing habit from insignificant to aggressively invasive.
Whisk ferns (Psilopsida)
Of the vascular plants, the members of the whisk ferns have the least complex organization. The plants consist of (sparsely or profusely) dichotomously branched axes, arising from a subterranean rhizome. The rhizome is rootless, and this is a unique feature of whisk ferns among all vascular plants. Two genera have representatives in South East Asia, which grow as epiphytes, or terrestrially in humus rich soil or mounds of humus.
Choice of species
Contrary to most Prosea volumes, the present volume does not focus on a specific commodity, but rather on a taxonomically specified group of plants. The criteria for including species therefore had to be reformulated as not every one of the thousands of pteridophyte species has been recognized as a valuable resource to humans. Hence, the criterion for selection for this volume is whether any mention is made in the literature of the use of a species occurring in South East Asia. One exception was made, however, for the use as an ornamental. Although their popularity has fluctuated, for the last centuries ferns have appealed to many gardeners and indoor plant lovers for their delicate shapes and exotic allure. Virtually any kind of fern that can be found, transplanted or reproduced and kept alive has found a use as an ornamental somewhere, though not often on a large scale. To avoid a pointless enumeration of species for which only incidental interest has been shown, only those ornamental species that have become commercially important are included in Chapter 2.
Mosses are not vascular plants and they do not belong to the pteridophytes. However, the very few moss species covered by Prosea do not justify a separate subvolume and therefore they have been included in this subvolume in Chapter 3.
Origin and geographic distribution
The species diversity of a region, expressed as the number of species, varies from almost none in polar and arid regions and isolated islands to as many as 2000 in New Guinea. The highest diversity of pteridophyte species is found at lower latitudes, but even in the tropics, highly diverse regions are paralleled by very poor areas. By far the most diverse areas are the tropical mountains. At a rough estimate, 65% of the pteridophyte species are found in the wet tropics in areas without a marked dry period. The taxonomic diversity of the tropics is furthermore expressed by large numbers of genera and families, many of which do not occur in more temperate regions. Some 4400 pteridophyte species are known from South East Asia. At present, worldwide 10 500-11 300 species have been described, a number that is expected to increase to about 12 000-15 000 (Roos, 1996). The region therefore ranks amongst the world's richest fern floras. Other regions with high pteridophyte diversity include the western American mountain ranges from southern Mexico to Bolivia, south eastern Brazil and Madagascar. Remarkably, intermittent regions such as Amazonia, continental Africa and the Indian subcontinent are much less diverse (Tryon, 1986).
Some 30% of the fern species have relatively small ranges and some of them even are limited to a single mountain. Less than 10% of the species have very wide to cosmopolitan ranges, while the bracken (Pteridium aquilinum (L.) Kuhn) is ranked among the top ten most abundant vascular plants of the world.
Homosporous ferns all have a nearly equivalent capacity for dispersal and migration. Estimates of the annual spore production of an individual fern range, depending on the species and size, from 100 000 to 3 billion. A single spore can, by self fertilization, give rise to an adult sporophyte. Evidence from floras of oceanic islands shows that 800 km distance is not a significant barrier to the migration of a fern flora (Tryon, 1986). Still geographic barriers do exist. Several fern species have naturalized after deliberate or inadvertent introduction by humans, sometimes with detrimental effects to the indigenous vegetation. Large intermittent areas without suitable habitats, such as deserts and oceans, can effectively block the expansion of a species' distribution. High mountain ranges also seem difficult to pass. Nevertheless, the differences in species ranges must be based on the ecology of the environment rather than dispersal. The ecological flexibility of the various life stages of a fern (spore germination, gametophyte, sporophyte) may vary considerably. Thus long living sporophytes may persist in areas where they can no longer reproduce sexually. This makes it hard to explain the observed species ranges.
Most fern families have wide distributions and only a few of the smaller ones are confined to South East Asia and northern Australia, for example Cheiropleuriaceae, Dipteridaceae and Matoniaceae. While several genera have representatives in a limited region only, many others have a circumglobal distribution. This is explained partly by their great age. During the tens to hundreds of millions of years of their existence they have had opportunities to cross the barriers raised by the oceans which, in past eras, were narrower than they are nowadays. The oldest genera even preceded the disintegration of the Triassic Pangea into the predecessors of the present continents.
Importance of ferns and fern allies
Pteridophytes are not normally thought of as useful plants. Good (1933) puts it straight from the shoulder: "the pteridophytes (ferns and their allies) are also relatively useless". The best he could make of them are their dead remains amassed as coal to be used as fuel. The world's coal deposits originate from vast pteridophyte forests that lived during the carboniferous era, before the onset of seed plants. No vast fortunes are to be made from the cultivation of any of the species and the only occasion the general population is likely to take notice is when a fern becomes an aggressive and successful weed. Nevertheless, agricultural societies dependent on what the land can offer them have appreciated the value of ferns more keenly. May (1978) published a review of the uses of pteridophytes throughout the world, listing over 100 applications of various fern species. Ferns are found to provide food, medicine, fibre, craft and building material, abrasives and of course decoration (Croft, 1985). Table 1 shows a survey of primary and secondary uses of the described species and genera in this volume. Uncertainty exists as to what extent reported uses still continue. Throughout this subvolume the information compiled is often based on literature sources that are over 50 years old (e.g. Burkill, 1935; Heyne, 1927; Ochse, 1931; Quisumbing, 1951). Often no indications were available that the cited uses still continue to be practised into present times. In these cases it has been decided to use the past tense, although recent applications could not be ruled out and, as incidental experiences suggest, present day applications might still be very much the same.
Several fern species store starch as a reserve, especially in the rhizome. In the past these ferns served as an supplementary food source or to produce alcohol. However, due to the low quantity and quality of the starch, this habit has nowadays been largely abandoned. Species treated within this volume that have served as source of starch include Angiopteris evecta (G. Forst.) Hoffm., Cibotium barometz (L.) J. Smith, Cyathea spp. and Pteridium aquilinum (L.) Kuhn.
Many fern species have been recognized as having leaves that can be eaten as a vegetable. Some of them have an exquisite taste and are sold as a delicacy. Especially the young leaves that are still curled (croziers) or partly curled are consumed. When the leaves mature, the increasing concentrations of certain chemical constituents such as alkaloids, damage the taste and in some species may eventually impose adverse health effects upon the consumer. The older leaves also become unpalatable as a result of the build up of structural material.
The ferns most commonly used as a vegetable in South East Asia are the "green fern" Diplazium esculentum (Retz.) Swartz and the "red fern" Stenochlaena palustris (Burm.f.) Bedd. The way in which they are prepared varies in accordance with the cook's preference from salad to steamed, boiled, or fried. In an experiment in the Philippines cooked fiddleheads of the following ferns have been tried as a vegetable or as a component of a stew: Acrostichum aureum L., Angiopteris evecta (G. Forst.) Hoffm., Blechnum orientale L., Cyathea contaminans (Wall. ex Hook.) Copel., Diplazium esculentum, Nephrolepis hirsutula (G. Forst.) C. Presl, Pleocnemia irregularis (C. Presl) Holttum, Pteris ensiformis Burm.f. and Stenochlaena palustris (Burm.f.) Bedd.). Diplazium esculentum was found to be the most palatable. Other factors determining the suitability of fern fronds as vegetables include the production rate of new leaves, and the availability of young fronds throughout the year. There have been some experiments to bring Diplazium into cultivation, but up till now most if not all of the supply to the markets is harvested from the wild.
Remarkably many fern species accumulate metal salts from the soil in which they root. For a few species, in areas with difficult access to other sources of salt, this has led to a use that involved burning the fern down to their ash, which is rich in salt. The ash is strewn on cooked food before consumption, or mixed with water and drunk. The salt, like most other vegetable salts, is higher in potassium content than common salt.
The most common use, in terms of the number of species involved, is medicinal. Most records are based on uses in traditional medicine. A number of species were described in pharmacopoeias many centuries ago and have been continuously used in herbal medicine ever since. No pteridophytes are used at present as a source of (western) pharmaceutical compounds, though of some the constituents are being synthesized. In the past doubt has been expressed as to whether the supposed medicinal value of ferns is due to their properties and that they should be attributed to the psychological and placebo effect (Croft, 1999). It is noteworthy, however, that the same or related fern species have found similar medicinal applications even on different continents. Furthermore, in several cases laboratory research has revealed biological activities of fern extracts that could account for the medicinal uses in traditional and herbal medicine. Traditional medicines are often prescribed for internal use as decoctions of infusions. Both preparation processes are water based, but lipophylic solvents such as ethanol often extract other pharmacologically active compounds, such as antibiotics, that are not or hardly present in the aqueous solutions (Kelmanson et al., 2000). Extraction with wine, as is practised in old European herbals, is not commonly done in tropical South East Asia. Currently, most research efforts on the efficacy of pteridophytes as medicines, or as a constituent of formulations, are concentrated around Chinese herbal medicine (CHM, also known as TCM or traditional Chinese medicine). CHM has always been used by the Chinese communities in South East Asia, and nowadays also by an increasing number of others, as an alternative or in addition to pharmaceutical medicine. Integration of CHM and pharmaceutical medicine has only recently started to come to fruition, due to differences in philosophies, research standards and the inaccessibility of the Chinese literature. Claims by CHM about remedies for diseases that still present unanswered challenges to pharmaceutical medicine (e.g. see Selaginella Pal. Beauv. uses for cancer and Huperzia serrata (Thunb. ex Murray) Trevis. for Alzheimer) have led to increased interest in ethnobotany and research into herbal medicine.
1.2.3 Structural materials
The trunk of tree ferns is sometimes used as instant construction material for bridges and fences. The fibrous material is resistant to decay and long lasting. In some areas it is used for the construction of houses too, but possibly only where tree ferns are plentiful and other suitable timber is scarce. The stem can be cut into sections of the desired dimensions, polished and then made into vases, pencil holders and umbrella holders, or split and the harder portion used for inlaying or making fancy boxes and frames. Fibrous splints can be obtained from the petioles and rachises of various species, and these are used for making ropes and wickerwork. Especially Lygodium Swartz is still a popular material and apart from products for personal use such as cases, belts and baskets, items are produced for the handicraft and tourist industry.
Most ferns can be kept as ornamentals as long as adequate care is provided. Before introducing a species as an ornamental some key factors must be considered that may influence its commercial success. These factors comprise a combination of characters that make a fern attractive to the customers and properties that are important to the commercial growers. Currently successful ornamental fern species have the following common characteristics: closely placed fronds which give them a full foliage look, symmetry in overall outline, small to medium size, an evergreen habit and at least one unusual characteristic that makes them special, e.g. colour, texture, or shape. Moreover, they should be able to stand adverse cultural conditions and not too sensitive to relative humidity or temperature when marketed for indoor use, or they need to be inexpensive enough to be disposable.
Commercial nurseries demand species that are inexpensive to produce and deliver to the market. Fast growing species are preferred, such as those that can be reproduced by spores or mass vegetative cloning (tissue culture). The ferns should be resistant to measures to control diseases and pests. Finally they should not easily be damaged during transport from the grower to the market (Hoshizaki, 1992). When evaluating a fern species for ornamental use one should bear in mind the great variation in climate between the various international markets. Outdoor horticultural markets range from cool temperate to tropical with various regimes of precipitation and relative humidity. Ferns for indoor use may not be expected to experience so much variation in temperature, but relative humidity will be different in e.g. centrally heated buildings in northern temperate areas and air conditioned or open constructions in warmer zones. South East Asia has been the origin of several commercially interesting ornamental fern species. Platycerium bifurcatum (Cav.) C. Chr. and Asplenium nidus L. have become rather important products. Without doubt, other species could also be developed, although it is questionable whether growers within the South East Asian region are able to compete on the international markets due to transport costs and plant hygiene import restrictions. For local markets ferns are often gathered from the forest. Most of these are common and can be collected in quantity without endangering the species, but locally there may be adverse impacts on the forest diversity.
1.2.5 Other uses
Ferns have traditionally been used for various other purposes. The decorative values of ferns and their allies have invited their use for personal decoration, either casually or for ceremonial occasions. Especially fibrous species (Dicranopteris Bernh., Lygodium Swartz) or those that form long, flexible strings that can be interwoven without breaking (Selaginella Pal. Beauv., Lycopodium L.) are suitable for this purpose. Houses and ceremonial places were also decorated with ferns, either by adorning them on purpose, or by just allowing ferns to remain where they appeared spontaneously. Ferns have also found a place in rituals and magic. Leaves of Nephrolepis Schott were placed among the bones of deceased close relatives at death ceremonies in New Guinea. Magical properties were attributed to Blechnum orientale L., Drynaria (Bory) J. Smith and Hemionitis arifolia (Burm.f.) T. Moore. The rough surface of horsetails, caused by fine crystals of silica on their stem surface, found a special use as a scouring and smoothing aid. The sandpaper like qualities of Equisetum ramosissimum Desf. have led to its use in shaping and smoothing tools, ornaments and weapons, but is also acknowledged to be useful for cleaning pans and other cooking utensils. Although many of the traditional uses have been abandoned and replaced by modern materials, nevertheless new applications still arise. Ferns frequently are the subject of various fields of scientific research. Modern uses include widely differing applications such as sewage water treatment, hydrogen production, gold prospecting, composting and the development of new pharmaceutical products.
1.2.6 Economic aspects
The annual trade value of ornamental and cut foliage ferns is estimated at 150-300 million US$. Despite this considerable amount, statistics on the global fern production and trade are not easily obtained as auction sales are monitored by regional offices and rarely published in national censuses. Consequently, the economic facts and figures presented here do not offer a coherent view of the economic role of the fern trade. In the Netherlands the most traded ferns are Nephrolepis, Asplenium and Adiantum. In 1997, 12 million Nephrolepis plants were produced by tissue culture. Still, a substantial part of the propagation is achieved by means of spores, or by taking cuttings (especially of Selaginella). Originally, the tissue-culture laboratories were mainly found in western Europe, but at present the sector is expanding to eastern Europe (Poland) and Asia (Sri Lanka, Indonesia) (Vidalie, 2000). In Florida (United States) fern production in 1996 amounted to a wholesale value of 97 million US$. The total production of leatherleaf fern (Ruhmora) in the United States in 1997 was 60 million US$, with a production area of 1750 ha. In 1999 Japan imported cut stems worth 4 billion yen, which for a substantial part were ferns from China, the United States and Costa Rica. Cut flowers and ferns are the third ranking agricultural export commodity in Costa Rica, following bananas and coffee. The main obstacle to Costa Rican flower and fern exporters is the infrastructure, which is inadequate for rapid transport abroad. The primary market for Costa Rican ferns is the European Union (mostly The Netherlands and Germany). In 1995 the total export value for ferns was about 50 million US$, with a yearly growth of 10-20%. Ferns may also play a role in the local economy. Little is known about the impact of diffuse markets, such as represented by the roadside booths selling ornamentals, either collected from the wild or propagated in artisanal gardens. The use of traditional medicine may involve both economic and logistic factors. Occasionally, local economies specialize in ferns. In the State of Rio Grande do Sul (Brazil) Rumohra adiantiformis (G. Forst.) Ching is abundant in early stages of degraded forest areas. In meeting the demand from flower shops, this species has been heavily exploited since 1970s, and has become the major source of income for an estimated 3000 families in the Brazilian Mata Atlântica Biosphere Reserve (Elisabetsky & Coelho de Souza, 2001). Pteridophytes used in herbal medicine must constitute a considerable trade volume, as they are supplied to a consumer market worth billions of dollars. However, as far as is known neither the production nor the trade flows are being monitored.
Many pteridophytes exhibit relatively slow growth while preferring conditions that would normally be considered unhealthy from a phytopathological point of view. Nevertheless, indications of damage caused by fungi or invertebrate herbivores are rare. A diverse phytochemical armament of widely differing degrees and types, including antibiotics, which is taxonomically widespread among the pteridophytes, is probably the most effective and widespread strategy in promoting direct vegetative survival. However, little is yet understood about which substances are employed to achieve effective defence and exactly what they are targeted against (Page, 2002). Not only the sporophytes are armed with a load of repellents, but also the gametophytes and even the spores. In ferns occur chemically unusual intra cellular cements that bind cells together, different from those of spermatophytes (Manton, 1950). They may be indigestible to those animals with an HCl mediated digestive tract. The wide molecular diversity of secondary metabolites throughout the plant kingdom represents an extremely rich biogenic resource for the discovery of novel drugs and for developing innovative drugs. Not only do plant species yield raw material for useful compounds, the molecular biology and biochemistry provide pointers for rational drug development. Many of the compounds found in pteridophytes fall into two groups, the alkaloids and the phenols. Some important groups with their most important classes are briefly summarized below (abridged from from de Padua et al., 1999).
The term "alkaloid" is used here for plant derived compounds containing one or more nitrogen atoms (usually in a heterocyclic ring) and usually having a marked physiological action on humans or animals. Alkaloids in plants are believed to be waste products and a nitrogen source. They are thought to play a role in plant protection and germination and to be plant growth stimulants. Alkaloids are especially common in lycopods. Many alkaloids are pharmaceutically significant, e.g. huperzine A, a reversible inhibitor of the enzyme acetylcholinesterase, that is involved in the breakdown of the neurotransmitter acetylcholine.
1.3.2 Phenols and phenolic glycosides
Phenols probably constitute the largest group of secondary plant metabolites. They range from simple structures with one aromatic ring to complex polymers such as tannins and lignins. Examples of phenolic classes include tannins, coumarins and their glycosides, quinones, flavonoids, lignans and related compounds.
The chemistry of tannins is complex. Tannins are able to react with proteins. On being treated with a tannin, a hide absorbs the stain and is protected against putrefaction, thereby being converted into leather (for more information, see Lemmens & Wulijarni Soetjipto, 1992). Though tannins are widespread in plants, their role in plants is still unclear. They may be an effective defence against herbivores, but it is likely that their major role in evolution has been to protect plants against fungal and bacterial attack. The high concentrations of tannins in the non living cells of many trees (heartwood, bark), which would otherwise readily succumb to saprophytes, have been cited in support of this hypothesis. Some authorities consider tannins to be waste products and it has also been suggested that leaf tannins are active metabolites used in the growing tissues. However, tannins in different plant species probably have different functions. Tannins are used against diarrhoea and as antidotes in poisoning by heavy metals. Their use declined after the discovery of the hepatotoxic effect of absorbed tannic acid. Recent studies have reported that tannins have anticancer and anti HIV activities.
Coumarins and their glycosides
Coumarins are benzo α pyrone derivatives that are common in plants both in a free state and as glycosides. They give a characteristic odour of new mown hay and occur, for instance, in the hay scented fern Dryopteris aemula (Aiton) O. Kuntze. They are biosynthetically derived via the shikimic acid pathway. The biological activities reported are spasmolytic, cytostatic, molluscicidal, antihistaminic and antifertility.
Quinones are oxygen containing compounds that are oxidized homologues of aromatic derivatives and are characterized by a 1,4 diketo cyclohexa 2,5 diene pattern (paraquinones) or by a 1,2 diketo cyclohexa 3,5 diene pattern (orthoquinones). Some quinones have some medicinal value in the form of antibacterial and cytotoxic activities, others are powerful fungicides, laxatives or hair colourants.
Flavonoids are the compounds responsible for the colour of flowers, fruits and sometimes leaves, or contribute to the colour by acting as co pigment. Flavonoids protect the plant from UV damaging effects. The basic structure of flavonoids is 2 phenyl chromane or an Ar C3 Ar skeleton. Recently, flavonoids have attracted interest due to the discovery of their pharmacological activities as anti inflammatory, analgesic, antitumour, anti HIV, antidiarrhoeal, antihepatotoxic, antifungal, antilipolytic, anti oxidant, vasodilator, immunostimulant and anti ulcerogenic. Examples of biologically active flavonoids are rutin for decreasing capillary fragility and quercetin as antidiarrhoeal.
Lignans and related compounds
Lignans and related compounds are derived from condensation of phenylpropane units. Neolignans are also condensation products of phenylpropanoid units, but the actual bond varies and involves no more than one β carbon (8 3', 8 1', 3 3', 8 0 4' for example). Designated lignans or neolignans result from the condensation of 2-5 phenylpropanoid units (e.g. sesquilignans and dilignans, lithospermic acid). Lignans are substances deposited at the end of the formation of the primary and secondary cell walls. Lignans display antitumour pharmacological activity.
1.3.3 Terpenoids and steroids
Terpenoids and steroids are derived from isoprene (a 5 carbon unit), which is biosynthesized from acetate via mevalonic acid. Monoterpenes are the most simple constituents in the terpene series and are C10 compounds. They arise from the head to tail coupling of two isoprene units. Sesquiterpenoid lactones are well known as bitter principles. Sesquiterpenes possess a broad range of biological activities due to the α methylene-γ lactone moiety and epoxides. Their pharmacological activities are antibacterial, antifungal, anthelmintic, antimalarial and molluscicidal.
Diterpenes constitute a vast group of C20 compounds arising from the metabolism of 2E,6E,10E geranylgeranyl pyrophosphate. They are present in some animals and plants. Diterpenes have some therapeutic applications. For instance, taxol and its derivatives from Taxus L. are anticancer drugs. Other examples are forskolin, with antihypertensive activity, zoapatanol, an abortifacient and stevioside, a sweetening agent.
Triterpenes are C30 compounds arising from the cyclization of 3S 2,3 epoxy,2,3 squalene. Tetracyclic triterpenes and steroids have similar structures, but their biosynthetic pathway is different. Steroids contain a ring system of three 6 membered and one 5 membered ring; because of the profound biological activities encountered, many natural steroids together with a considerable number of synthetic and semi synthetic steroidal compounds are employed in medicine (e.g. steroidal saponins, cardioactive glycosides, corticosteroid hormones, mammalian sex hormones). The pharmaceutical applications of triterpenes and steroids are considerable. Cardiac glycosides have been used in medicine without replacement by synthetic drugs.
Saponins constitute a vast group of glycosides which occur in many plants. They are characterized by their surfactant properties; they dissolve in water and, when shaken, form a foamy solution. Saponins are classified by their aglycone structure into triterpenoid and steroid saponins. Most saponins have haemolytic properties and are toxic to cold-blooded animals, especially fish. The steroidal saponins are important precursors for steroid drugs, including anti inflammatory agents, androgens, oestrogens and progestins. Triterpene saponins exhibit various pharmacological activities: anti inflammatory, molluscicidal, antitussive, expectorant, analgesic and cytotoxic. Examples include the ginsenosides, which are responsible for some of the pharmacological activity of ginseng and the active triterpenoid saponins from liquorice.
Among the extant land plants, the ferns are only surpassed in diversity by the angiosperms. Worldwide their number is estimated at about 12 000 species in about 225 genera. Until the early 20th Century the extant pteridophytes were subdivided into three classes: - the Pteropsida (also Filicopsida, Polypodiopsida), or ferns; - the Sphenopsida, or horsetails; - the Lycopsida, or clubmosses, spikemosses and quillworts. During the last century consensus arose that the whisk ferns, being a very primitive group, justify a fourth class on its own, the Psilotopsida. To these four classes the term "ferns and fern allies" is applied in colloquial speech. Although united in the Pteridophyta division, it should be noted that this grouping is based on similarities of the life cycles rather than common ancestry. Their origins go back in geologic time to the Devonian and Carboniferous eras and their inclusion in the Pteridophyta is a matter of convenience, although a few recent authors have chosen to raise the four classes to the level of division (e.g. McCarthy, 1998). It is often suggested that the Pteropsida in this sense are polyphyletic still and that the Ophioglossales (represented in this subvolume by Ophioglossum L. and Helminthostachys Kaulf.) and Marattiales (represented in this volume by Angiopteris Hoffm.) may be not correctly placed here. Cladistic methods, using a great number of morphological and biochemical characters, are currently being deployed to resolve these relationships (e.g. Pryer et al., 2001), but have not yet resulted in a definitive classification scheme.
The ferns are a diverse group, but they are easily distinguished from the other classes by their large leaves with a more or less complex pattern of venation. The sporangia grow on the leaves, but these may be modified into highly specialized organs. Six orders constitute this class, of which five have circinate leaves.
These are plants with solid, herbaceous stems and numerous small, moss like leaves (or rush like, in Isoëtes L.). The sporangia reside solitarily in the axils of the fertile leaves, which can be very different from the sterile leaves and form a terminal strobilus. The quillwort family (Isoëtaceae) is essentially aquatic and very rare in South East Asia. The clubmosses (Lycopodiaceae) are firm herbaceous plants, either dichotomously branched or with a creeping main axis. All species of spikemosses (Selaginellaceae) within the area of this book have dorsi ventral flattened branches with the lateral leaves the largest. Like the quillworts but unlike the clubmosses they are heterosporous, so some of the sporangia contain megaspores that are large enough to be discerned by the naked eye. The plants are generally soft herbaceous.
The horsetails have hollow, articulated stems built of clearly distinct joints. The leaves have been reduced to scales that stand in whorls around the joints, forming a sheath that encloses the next internode. The stems can be branched; the branches are built like the stem but much smaller and stand in whorls around the sheaths. The sporangia grow under peltate sporangiophores, forming a terminal strobilus (spike). The spores are green with four hygroscopic ribbon like appendages called elaters. The elaters quickly coil up when moistened, thus reducing the wind resistance near suitable habitats for germination. Although the spores come in one size, the gametophytes are unisexual, the male ones remaining smaller than the female ones.
The whisk ferns are the only free living vascular land plants without true roots. The stems are dichotomously branched and bear few leaves or only green scales. The sporangia are fused in groups of three that stand solitary on the branches. There is one family represented by two living genera, Psilotum Sw. and Tmesipteris Bernh. The aerial shoot of Psilotum is a very simple green structure consisting of a dichotomously branching axis without leaves but with exceedingly small scale like appendages called prophylls, which are mere flaps of tissue. Trilobed synangia are borne on short lateral branches. The underground rhizome is irregularly branched and is covered with fine, long, brown rhizoids. Tmesipteris differs morphologically from Psilotum by its well-developed foliage leaves supported by a single vein, and the bilobed synangium.
Fossil Pteropsida have been found from the Lower Carboniferous. All six families known from the end of the Carboniferous became extinct by the Lower Permian. In a second major filicalean evolutionary radiation during the Permian, Triassic and Jurassic several families arose which still have extant representatives (Cyatheaceae, Dicksoniaceae, Dipteridaceae, Matoniaceae, Osmundaceae and Schizaeaceae). A subsequent radiation among the polypodiaceous ferns began in the Upper Cretaceous while flowering plants already had gained dominance over much of the land surface. In the 19th Century most pteridologists classified the ferns into families based on a few characters only. Especially, analogous to the importance of reproductive organs in flowering plants, the position, the shape and morphology of the sori determined the family to which a genus should belong. The resulting families were often very large and, as understood today, not in accordance with the presumed lines of evolution, or on the other hand segregated on the base of characters that vary between related genera. In the course of the 20th Century new classifications were accepted that take more characters into account, such as the venation pattern, the anatomy of the petioles, and, in the second half of the century, the number of chromosomes. Especially the Polypodiaceae, or the "modern" ferns, have long persisted as an extremely large and heterogeneous family. Various authors though, have proposed regrouping the ferns into families in varying combinations. One of the most comprehensive classifications published (Kramer & Green, 1990) reflects best the present state of general consensus. This synthesis was based on similarities between genera rather than differences, thus reflecting their relationships more explicitly. As several relationships still need to be revealed this classification will also be worked over in time, alternative views even coexist at present. For the time being, however, this is a good standard to go by, if one has to be chosen. In this Prosea subvolume the nomenclature of families and genera is in accordance with this classification, even when it diverges from prevailing literature of the region.
The most commonly used descriptive terminology is illustrated in the Figures 2a and 2b.
The leaves (fronds) of a fern are formed at or near the apex of its main axis or stem, the rhizome. The rhizome can, depending on the species, attain different growth forms. In many ferns the stem is erect and radially symmetric. It is then called a "caudex", which may also be prostrate or ascending. The fronds grow in a crown like bundle on top of the caudex, radiating in all directions and roots grow downwards from all sides. The majority of species with a caudex gain little height and the leaves are based at or somewhat below soil level, but some of the most conspicuous species exhibit a potent heigth growth resulting in an appreciable stem of sometimes more then 20 m tall. The creeping rhizomes produce their leaves at regular distances though they still may be crowded when the intervals are short. This kind of rhizome can be dorsiventrally differentiated with leaves arising in two or more rows from the upper surface and roots growing from the side that is appressed against the substratum. Most epiphytic ferns have creeping rhizomes, but they are not uncommon in terrestrial species either.
Creeping rhizomes often branch either in an irregular fashion or dichotomously; the caudices as a rule do not branch though ramifications may be induced by damage to the growing apex. The vast majority of ferns with a caudex are terrestrial; most epiphytes have a creeping rhizome though frequently a short one. In few cases, the rhizome is green and photosynthetically active but generally it is well protected and covered with scales. Very rarely the rhizome is naked. Usually there is at least some form of indumentum, at least on the growing tips, to protect these vulnerable parts from physical damage, herbivory, or desiccation. The same indumentum is formed around the young unrolling fronds and usually the remains on the petiole base of full grown leaves constitute a helpful character in identifying the species, but with time they may fall off. The indumentum is often of considerable diagnostic importance and may comprise scales, wax excretions, hairs, bristles and remainders of leaves, in any combination. The shape, colour, types of apex and base and the presence of marginal hairs and glands are important characters. Many advanced families of ferns have flat scales with a darker central area on a broad base. Sometimes four of the walls of the cells are very prominent whereas the two remaining ones are thin and translucent or clear. Seen with a hand lens this looks like lace or lattice work; this kind of scales is called clathrate and their presence is a helpful character. The rhizomes normally do not increase in diameter, but in some cases the structure is reinforced by hairs, fibres, or mats of adventitious roots and remains of leaves. The anatomical structure of the stem is of considerable taxonomic importance. The stele or central vascular cylinder of the axis may be - solid, the primitive protostele (as in most Gleicheniaceae); - a central vascular cylinder with a core of non vascular tissue, the medullated protostele or siphonostele (e.g. Dipterus and most members of the Ophioglossaceae); - slightly more complex and feature a hollow cylinder with leaf gaps from which the vascular strands to the fronds develop; the most simple form is a solenostele, e.g. as in Davallia where the leaf gaps are widely separated and do not overlap; more complex is a dictyostele, e.g. as in the Thelypteridaceae, where the leaf gaps overlap and form an elaborate network.
Only adventitious roots occur in ferns. In tree ferns such as Cyathea J.E. Smith and Dicksonia L'Hér., numerous roots are found near the base of the caudices, providing stability. Primitive fern allies of the genera Psilotum and Tmesipteris are entirely rootless. In the floating aquatic fern Salvinia molesta D.S. Mitch., the submerged leaf is modified to form root like structures, but true roots are absent.
The stipe of the fern frond is also known as the petiole. Well developed petioles are only found in the true ferns and are absent or extremely short in the fern allies. Normally, the petiole is continuous from the rhizome to the lamina, but in some species it is articulated. This means that the precise location where the old leaf will be severed from the plant is predetermined. Fallen leaves leave behind a neat scar (abscission mark), either directly on the rhizome, or at a small distance above the petiole base. In some groups the rhizomes form modified outgrowths (phyllopodia), usually densely clothed with scales, onto which the petiole articulates. Phyllopodia are found in the families Davalliaceae, Polypodiaceae, and the genera Arthropteris J. Sm., Elaphoglossum J. Sm. and Oleandra Cav. Leaves with non articulated petioles leave behind remaining petiole bases of varying length and with roughly cut off upper ends. In most families the petiole is not articulated to the rhizome. The colour of the petioles is not a constant character of a family or a genus since it varies and overlaps between species of a genus, or between genera in a family. The colour varies from green, stramineous to brown or purple. Green petioles are observed in nearly all families but such petioles usually turn brownish or stramineous as they mature. The colour character may be useful in distinguishing species. The petiole may be winged (alate) and grooved (sulcate), whereas those that are circular in transverse section are called terete. The shape, number and arrangement of the vascular bundles and the configuration of the xylem strand are characteristics of several families, but these characters are rarely used in the descriptions.
The (primary) rachis is the continuation of the petiole into the lamina or blade. However, when the lamina is not completely divided up to its central axis, but embedded within leaf tissue for its entire length beyond the stalk, the central axis is called the costa rather than rachis. Likewise the pinnae can have pinnae rachises when the leaf is at least 2 pinnate. The main vein of the pinna is also called the costa when the leaf is 1 pinnate only. It should be noted though, that in some literature these terms are used with a different meaning: there the rachis is the main axis of the lamina, whereas the costa is the main axis of the pinna, or lower order segments. Details of the rachis, such as indumentum and grooves, are frequently used as distinguishing characters in the identification of ferns. Typically the rachis is pinnately branched, that is, the primary rachis continues more or less in a straight line to the basis, branching off at regular intervals, alternating on the left side and the right side like a fish bone. In some cases, the rachis is dichotomously branched: at each node the rachis splits into two equal branches. When the apical branch of a pinnately divided leaf does not develop, only the two pinnae grow sideways, which apparently also results in a dichotomous branching. This is referred to as pseudodichotomous, although the apical bud remains visible in the fork, thus giving away the underlying pinnate nature of this pattern.
The flattened, leaf like blade of the fern frond is called the lamina and it varies from simple to highly dissected. Most ferns have a number of leaves that are more or less uniform. In a considerable number of species, however, the fertile leaves are different from the sterile ones. Generally, the fertile leaves are more erect than the sterile leaves and also narrower, longer, or more constricted. Some large epiphytes, such as Platycerium Desv. and Drynaria (Bory) J. Smith, form specialized sterile leaves, closely appressed to the substratum, which protect the rhizome, conserve moisture and collect litter and humus. The venation patterns of ferns are of great taxonomic significance. Basically the venation can be free or areolate. When the venation is free, the veinlets, once they have branched off, run towards the margin without ever connecting again to another vein. When the venation is areolate (also "reticulate" or "anastomosing"), the veins do meet again with other veins, and by doing so they form closed cells, the areoles. Combinations of the two patterns can be found. Quite often there are a few rows of areoles along the costa whereas the outer veins run free towards the margin. Also areoles may contain free veinlets, often short and little branched. When the lamina is very thick and coriaceous the veins may be concealed. In these cases it can be helpful to view the lamina against a powerful light source. The vein endings may be enlarged and club shaped, often of a somewhat different colour or translucency than the surrounding leaf tissue. These are called hydathodes, organs which have an excretory function.
In most ferns the sporangia are produced on the back side of the lamina. Usually the sporangia are clustered together into heaps or pouches with a characteristic shape, position and protection. These clusters are called sori. Sometimes the sori become confluent and can no longer be separated by eye. In several species the sporangia cover considerable parts of the leaf surface, so no sori can be distinguished. This condition is called "acrostichoid". In many genera the sori are protected by a special flap like membranous structure termed the indusium. This structure is essentially an outgrowth from the leaf epidermis and may be attached laterally or centrally. The indusium may be linear, rounded or reniform, oblong, or double and borne back to back. In most cases it roughly follows the shape of the sorus. Some ferns have a false indusium, a soral protection formed by the reflexed margin of the lamina. The sporangia are sometimes additionally protected, especially when immature, by modified hairs or scales known as paraphyses.
The spores are formed within specialized organs, the sporangia. At the higher taxonomic subdivisions (above family level) the shape and construction of the sporangia are characteristic. In its simplest form, the sporangium is a solid walled hollow sphere containing thousands of spores. This kind of sporangium may be found in spikes (e.g. Helminthostachys, Ophioglossum), branch ends, or, as in clubmosses, in the axils of specialized leaves. In most ferns the sporangium is thin walled, stalked and small. Running completely or partially around the sporangium body is a ring or group of specialized cells, called the annulus. The cells of the annulus have their inner cell walls thickened in such a way, that when the cells become dehydrated, the whole annulus bends outward, acting as a spring that forcibly ruptures the sporangial wall and releases the spores. In most families the annulus runs vertically, but in others it runs horizontally or forms a closed circle at top of the sporangium (e.g. Lygodium) Inside the sporangium there are 16 cells that act as spore mother cells by undergoing meiosis and forming tetrads of haploid spores. The sporangia of the Marattiaceae (Angiopteris) are borne on the abaxial surface, either free or aggregated in synangia. They are large, sessile and either lack or have a rudimentary annulus.
Spores are single celled structures that are tiny and light enough to be dispersed by wind. The haploid spores in a tetrad have an exceedingly resistant outer protective coat which is generally composed of a thin inner layer called the intine, and an outer layer, the exine. Some spores have a covering outside the exine, called the perispore, derived from the periplasm around the spores. The perispore may be ornamented with ridges, spines, warts or balloon like wings. The ornamentation and the ultrastructure of the spore wall are taxonomically important and are best observed using electron microscopic visualization. For a comprehensive study with superb photographs, see Tryon and Lugardon (1991). Commonly, a spore has a proximal surface, which faces the centre of the tetrad, and a distal surface that faces the periphery of the tetrad. On the proximal surface is a mark called the laesura which is an "aperture" in the exine. Spores may be trilete, radially symmetric, tetrahedral to globose, with a triradiate aperture, or monolete, i.e. of bilateral symmetry, more or less bean shaped, with a linear aperture. Monolete spores are the most common since they predominate in some large groups (e.g. Asplenium L., Cyclosorus Link and the Polypodiaceae). Trilete spores are considered to be the less advanced type as they are found earlier in the fossil record and are dominant in more primitive families. It is assumed that monolete spores have been derived from a trilete ancestor. This appears to have occurred on several occasions, since both types of spore occur in 12 distantly related genera. Most pteridophytes produce one kind of spore only, thus they are homosporous. Four families (Azollaceae, Marsiliaceae, Salviniaceae and Selaginellaceae) are heterosporous and produce two kinds: small (10-60 μm) microspores and large (up to more than 1 mm) megaspores. Consequently, the gametophytes of the heterosporous families are either male or female, as opposed to the monoecious gametophytes of the homosporous ferns.
Gametophytes have been little used to identify species. They exhibit relatively few macromorphological characters, that in addition do not show much variation on the species level. Consequently, they have not received much attention by taxonomists, although micromorphology (e.g. of the gametangia) and isozyme patterns may include more information than hitherto exploited (Raine et al., 1996). At a higher taxonomic level the type of gametophyte can be very characteristic. The prothallus of leptopsporangiate ferns is often typically membranaceous, heart shaped and commonly less than 1 cm in size (Fig. 3(1). It has chlorophyll and is dark green, and near the sinus of the heart it is attached to the substrate by root like hairs arising from the lower surface, the rhizoids. It is amongst these rhizoids that the passive or female sex cells develop. The egg cells are hidden within flask like female organs, the archegonia. At some distance other organs are formed (the antheridia) that will produce the active or male sex cells. Gametophytes of homosporous ferns normally produce both male and female sex cells and are capable of self fertilization. However, mechanisms exist, such as asynchronous maturation, that enhance the probability of outbreeding. Heterosporous ferns produce either male (from the microspores) or female prothalli (from the megaspores - Fig. 3(6, 7). Different shapes are found in other groups. Several kinds of marginal outgrowths occur (Fig. 3(3), while others are basically filamentous (Fig. 3(2). Ophioglossaceae (Fig. 3(4), Lycopodiaceae (Fig. 3(5) and Psilotaceae have pale, lumpy, subterranean gametophytes that spend a long time living saprophytically in association with a mycorrhizal fungus, before giving rise to the green sporophyte.
The dominant stage in the life history of the pteridophytes is the generation that produces the spores and therefore is called the sporophyte. The ferns, horsetails and clubmosses as commonly known are in the sporophyte generation and the descriptions in the following chapter apply to this generation. The sporophyte forms spores by meiosis, the type of cell division that reduces the number of chromosomes to half the number that are in the nuclei of the sporophyte cells. The spores commonly have very hard outer walls, often with intricate decorations of points and ridges. They grow in specialized organs called sporangia. Different groups within the Pteridophyta have their own types of sporangia. Many of those have mechanisms to assist the mature spores to leave the thin layer of slack air immediately around the sporophyte so they can be taken away by the wind and effectively dispersed. Many pteridophytes grow erect spikes or specialized upright fertile leaves to promote effective dispersion of the spores. The large megaspores of the heterosporous ferns impose an extra challenge to the dispersion process. The megaspores are frequently transported by water, but launching of the spores by hydrostatic pressure may also occur. The hard outer shell of the spores helps them to survive the unfavourable conditions as they are blown through the air and after they have been deposited and are awaiting a chance to germinate. Some spores remain dormant in soil spore banks for several years. A few groups though, have green, non resting spores that will stay viable only for a few days or weeks and perish if no suitable conditions for germination are met within that time. Upon germination the spore shell breaks along a predetermined opening and the alternate generation starts to grow out. At first, this is a simple uniseriate thread of cells; soon afterwards it develops into a more specific shape. Note that since the spore was formed by meiosis, this plantlet has a haploid chromosome count. Later in its development it will produce sex cells or gametes and therefore this generation is called the gametophyte, as opposed to sporophyte. Another name often used for the gametophyte is prothallus. The motile male gametes need a film of water to swim actively to the female gametes. This need for a period of free water poses a severe constraint on whether a habitat can be colonized by ferns. The tender construction of most gametophytes also limits the possible environments to sites that are suitable for both the sporophyte and the gametophyte. However, despite their fragility, gametophytes may be surprisingly resilient to desiccation, reviving multiple centres of growth even after months of dehydration. A striking difference in the cytology of ferns compared to other plants is the high chromosome numbers. The sporophyte (diploid) counts range from less than 20 to over 1200. Many fern genera have existed for several hundreds of million years and these high numbers have resulted from repeated polyploidization during their history. There is, however, no unequivocal relation between the age of a genus and its chromosome count. Although the driving forces are not yet understood, at present the process can be observed and induced. Polyploidization follows from fertilization and nuclear fusion of a diploid gametophyte (apospory). Diploid gametophytes can originate from somatic sporophyte tissue that anomalously develops into a prothallus, or from an aberrant sporogenesis in which the meiotic process is rendered ineffectual (Manton, 1950). A special case of polyploidy is alloploidy, where part of the genome descends from a different species. Alloploidy originates from hybridization, followed by a chromosome doubling. Hybridization between related pteridophyte species is rather frequent. This type of hybrid has, instead of a double set of analogous chromosomes, two single sets of chromosomes, one from each of the parents. While hybrid sporophytes can develop well, indeed often grow more vigorously than either of the parent species, they are sterile, as the two different chromosome sets do not allow a regular pairing of the analogues during the meiosis. However, when the number of chromosomes are doubled by apospory, normal meiosis can proceed and fertile spores can be formed. From cytological analyses it appears that alloploidy is a common phenomenon. In some fern floras a high percentage is of alloploid origin. It is assumed that alloploidy is especially common in unstable environments (on a geological time scale), where new genetic combinations can rapidly take advantage of the newly created niches. Various causes, such as hybridization, can impose a sterility barrier by preventing regular meiosis during spore development. One strategy described above, is to double the chromosome number to enable meiosis with a doubled genome. Another strategy is to skip the reduction phase altogether and to produce spores with the somatic chromosome count. To prevent inadvertent genome doubling at each transition from gametophyte to sporophyte, the omission of the meiosis must be counterbalanced by not fusing the nuclei of sex cells on the gametophyte. The sporophyte develops directly from the tissue of the gametophyte and both phases therefore have the same chromosome count. This process is called apogamy, and it enables even triploid species to disperse by spores. The consequence is that outbreeding has become impossible.
Whereas reproduction by spores offers great advantages such as long distance dispersion and the exchange of genetic variation, it is not always the most effective strategy to rapidly spread over the suitable habitat of an established parent plant. The gametophyte phase is easily influenced by less than optimal environmental conditions, and it may take a long time before the young sporophyte is strong enough to stand up to the competition of other plants. Therefore, many fern species have evolved ways to reproduce asexually. The most common approach is by long creeping rhizomes, that may conquer a large area with considerable speed. Given time, a single clone may cover many hectares. Some aquatic ferns improve this process by fragmenting the rhizome, thus realizing an almost exponential growth. Also young plantlets in a more or less reduced state (bulbils) may be formed on the leaves, which, after disconnection or even before that, give rise to new sporophytes. When these young plants grow at the drooping apices of the leaves, a series of clonal individuals may "walk" a path through the forest.
During millions of years of evolution pteridophyte species have adapted to a wide range of environments, from the poles to the equatorial forests, from deserts to lake bottoms, from the seashore to high mountains. Only a submerged existence in salt water seems to be beyond their adaptive possibilities. Consequently, they exhibit a range of habits and life forms to cope successfully with this variety of habitats. The sporophytes vary in size from moss like and a few mm long to tree like and 20 m tall, including terrestrial, scrambling, climbing, epiphytic, epilithic, xerophytic, amphibious, aquatic, halophytic, floating and sub arboreal forms. The environment and substrate in which they grow are reflected in their habit and often their appearance. Frequently they are classified on the basis of their substrate into classes as epiphytes, terrestrial and aquatic plants. However, as they vary in their degree of specialization, many species do not keep to their class. Lower epiphytes are also found on the forest floor, aquatic species survive extended periods of complete emersion (or reverse) and terrestrial ones may extend into the trunks of trees. Especially fallen logs form a transient environment where both remaining and newly settling species mix with invading terrestrial ferns and deadwood specialists. In spite of these transgressions, major families of pteridophytes are predominantly terrestrial, epiphytic or aquatic respectively, several morphological characters being correlated with the growing habit defined in this manner. A better understanding is obtained by taking the (micro )climate into account together with their growing habit. Several classifications of the tropical environment from a pteridological point of view have been used (Holttum, 1938; Page, 1979; Tindale, 1998). Here a simplified classification is presented to give some insight into the morphological adaptations commonly seen in ferns.
1.5.1 Rain forests
The rain forests are characterized by a per-humid climate. They are found at lower altitudes, generally below 1000 m. The temperature is fairly constant and neither water supply nor water loss are problematic, though leaching of nutrients from the leaves by excess rainfall may be a factor that needs to be taken into account. The forest floor offers a sheltered habitat, usually with good drainage although marsh forests with permanently or seasonally waterlogged soils are not rare. The most important limiting abiotic factor is light. As it is intercepted by many layers of leaves, only a tiny fraction of the radiant tropical sunlight reaches the lowest strata. As an adaptation to this, ferns of the forest floor mostly have thin textured leaves and seem capable to maintain photosynthesis at remarkably low levels of light. The individual plants are typically well spaced, avoiding competition for light, nutrients, or other resources. There is little air movement in the rain forest, and so that the spores are better dispersed the fertile leaves are frequently narrower and more elevated than the barren trophic leaves. Another strategy to reach higher is to climb the trees. Quite a number of ferns start on the forest floor, but send their long creeping rhizomes up along the trunks of trees. Some of them climb as high as the canopy and thus effectively escape the sheltered, moist environment near the forest floor into the dry epyphytic habitat of section 1.5.3. The low climbers adhere to the bark with many fine roots from the tightly appressed rhizome. When the roots penetrate the superficial layers of the bark, they are able to extract water and nutrients. In these cases the terrestrial origin of a plant may perish and the plant will become truly epiphytic. True epiphytes depend on the rain and water draining off for their water supply. Often there is no strict division between epiphytes and ferns of epilithic habit (i.e. growing on rocks). Especially small ferns may effectively root in the moss layer, regardless of whether the moss grows on living or dead trunks or on stone. Many have membranaceous leaves with only two layers of cells (e.g. Trichomanes L.) and the adult sizes may be as little as 2 cm or less. Nevertheless, rocks and cliffs in the forest provide a range of habitats that specialized species can take advantage of. Since they are always sloping and often steeply so, waterlogged substrates requiring special adaptations for the oxygen supply of the roots hardly occur. On the other hand, the water supply varies from very constant in the crevices of larger cliffs to complete dependence on airborne moisture on exposed surfaces. Often the canopy is open to some extent, allowing more light to penetrate. The weathering of the stone could provide the epilithic ferns with a much richer nutrient supply than elsewhere in the rain forest, but the mineral sediment can also be biologically inert. Generally though, it is a favourable habitat for many fern species. In fact, ferns are better adapted to exploit this habitat than many seed plants, as they lack a thick taproot but have filamentous rhizomes capable of creeping into the smallest fissures. Due to the nature of the cracks and fissures in rock, a few deep clefts offer an extremely strong anchorage, but the surfaces in between may be smooth, or hard and inhospitable. Under these circumstances small ferns with erect (non creeping) rhizomes are favoured. However, other species follow crevices with their creeping rhizomes for a considerable distance. Where streams break open the canopy, the aspect of the vegetation changes as the terrestrial plants grow larger and more vigorous. There is heavy competition for light as there is at the forest edge and in temporary clearings. Ferns seen here often grow to large sizes with finely divided leaves, often developing a scrambling habit or a tall, trunk like stem. Smaller ferns growing where they could be washed over by the variable water levels, adopt a habit of surviving extended periods of submersion undamaged by the current (e.g. Microsorum pteropus (Blume) Copel.).
1.5.2 Montane habitat
In montane forests at around 2000 m mist and condensate may become the prime source of water. As the presence of the clouds is so constant, reaching from the forest floor to well above the canopy, the high epiphytes do not need any special adaptation to prevent too much water loss and to protect them from intense radiation. The trees are shorter than in the lowland forests and the canopies less dense, so the forest floor receives more light. It is hardly surprising that this is where the richest fern floras are found. At higher altitudes the trees become really dwarfed and finally are replaced by shrubs. Mosses become a dominant factor in the vegetation. The soil may also be partly unprotected by vegetation. When the welkin breaks open the sunlight is rich in ultraviolet radiation. Like the angiosperms, ferns living here therefore have leathery leaves covered by scales or a dense hairy indumentum, unless growing in well protected sites. Often the leaf margins curl inward to further reduce the exposed surface. Reddish pigments may also be present. At even higher altitudes of over 3500 m the shrubs also disappear, leaving nothing but the protection of boulders and rock to shelter the remaining plants from radiation and wind. During the frequent showers and at night temperatures may drop to around freezing point.
1.5.3 Dry epiphytic habitat
The lower strata of the rain forest are well insulated from many direct climatic influences by several layers of vegetation. Many epiphytes, however, escape these lower reaches in search of light or nutrients and settle for less protected positions higher up in the trees. The more abundant light and earlier access to the nutrient chain come at a price, as the epiphyte has no access to water reservoirs. It is directly dependent on precipitation while at the same time being more vulnerable to desiccation due to sun and wind. The bright sunlight may also cause damage to the living tissues of the leaves. Similar conditions are found out of the rain forest reaches, in savannas and solitary trees in cultured land. Common adaptations to withstand the low relative humidity and high insolation include leathery leaves and protection of the leaves by hairs or scales. Especially in areas with a marked dry season, these environmental effects are aggravated as relative scarcity of water is accompanied by the hosting trees shedding their leaves. Under these conditions the ferns may bide their time in dormancy, with or without becoming deciduous. Another remarkable adaptation, especially seen in some polypodiaceous ferns (e.g. Drynaria, Platycerium), is the formation of special fronds that are closely appressed to the substrate. In this way they protect the roots and centres of growth, but their shelter also provides a milder microclimate which favours the decomposition and recycling of nutrients. These shield fronds are frequently shaped in a way that facilitates the funnelling of falling litter towards the roots of the plant.
1.5.4 Exposed habitats
The habitats where ferns are exposed without protection to the elements of the tropical climate are varied and deserve a further classification. However, this is beyond the scope of this introduction. They include open rock faces, temporarily exposed soils, such as road cuttings, plantations and disaster sites, fresh- and salt-water marshlands, deserts and open water. The ample (or even excess) availability of light is here the common factor, whereas precipitation, desiccation and water stress vary to a great degree. As a general rule, ferns are not very competitive and under favourable conditions the struggle for resources is often lost against angiosperms. However, in more extreme conditions they still do well as is proved by their large species diversity and virtually ubiquitous distribution. Time is sometimes also on their side, as under disturbed circumstances such as clearings and plantations where a rapid clonal growth enables some species to establish and maintain a dense, competitive stand for many years, until they are finally outcompeted by specialists of the more stable conditions. However, when the environment continues to be disturbed, as often occurs in plantations, they may behave like a weed that is hard to eradicate. Their easily dispersed spores also enable the pteridophytes to rapidly colonize barren areas, such as after forest fires or volcanic eruptions. In arid habitats pteridophytes can grow as well as any xerophyte, but at least once during their lifetime they need free water as the male gametes need a film of water on the surface of the gametophyte to swim to the egg cells. A little dew, though, will do for this.
Most pteridophytes with creeping rhizomes are easily propagated vegetatively by divisions of rhizome branches. The divisions should have an active growing tip, which can be recognized by the fresh colour and the young leaves arising at short distances behind the tip. The development of growing tips from side buds on thick rhizomes may be stimulated by partly cutting through the buds. All cuts should be made with a sharp, clean knife. Care must be taken not to injure the growing tips and to keep as much soil to the roots as possible, but damaged leaves and old roots should be removed. The cutting should be planted as deep in the soil as it was before, or slightly deeper if the roots remain uncovered. If the cutting does not bear roots, it may be placed half of its diameter within the soil and secured with bent wire, or, length allowing, diagonally with the growing tip emerging from the soil. The divisions should be kept moist, but not wet, and in light but not exposed to the sun. To keep the relative humidity high, thin leaved species may require glass or plastic sheet covering, which can gradually be removed when the plants grow up. Inorganic fertilizer is applied after 15-20 days, but organic fertilizer should be avoided at this early stage as the bacteria and fungi it contains may turn against the vulnerable explants.
Some species produce vegetative reproduction organs such as runners, bulbils, or even buds developing into young plantlets whilst still attached to the parent leaves. When available these organs are better suited for vegetative reproduction than rhizome divisions. To reduce the risks during their early life stages, the organs are left to root and to grow well before detaching them, allowing them to profit from nutrients and water supplied by the parent plant.
1.6.2 Tissue culture
A technically more advanced means of vegetative propagation is tissue culture (also: meristem culture) which allows for mass multiplication under well controlled conditions, though starting with tiny bits of parent material. For commercial use, this technique offers significant advantages: the product is free of diseases, the quality is high and constant, the application is not dependent on parent plants to form spores and it is much faster. To start, apical meristems are taken from parent plants. The meristems consist of actively dividing cells that are not yet infected by germs. They are cleaned and externally sterilized and then transferred to a sterile, often fluid growing medium where they are kept under controlled conditions for several weeks to let them start multiplying by dividing. Part of the produced cell clumps is explanted to a solid artificial growing medium to grow young plantlets, while the rest is kept in stock for a new production cycle. Many variations in medium composition and treatments (e.g. with plant hormones) exist to stimulate the growth of the meristems and the development into plantlets.
1.6.3 Spore propagation
Spores are the natural means of reproduction of all pteridophytes and growing ferns from spores can be as simple as shedding the spores over a container with moist soil and waiting. However, various techniques have been developed to obtain a more reliable production. The following just provides some examples, for details see Hoshizaki (2000). Leaves should be selected that have light brown sori. A 10× hand lens should be used to check whether the sporangia are not still green or are empty pockets that have shed the spores already. The leaf could also be placed with the sori down on a sheet of white paper and gently tapped with the fingernail. Mature sporangia will then shed the spores as a fine greyish-brown dust. To harvest the spores the leaf can also be left on a paper sheet for a day or two. The spores will precipitate on the paper when the sporangia dry and dehisce. Tapping the leaf speeds up the process, but also increases the amount of contamination. Non sporal debris should be removed as much as possible as it promotes the growth of algae, fungi and mosses. Various minute mesh devices have been applied to sieve the fluff from the spores. The spores are normally stored dry in paper envelopes, but good results have also been obtained with wet storage in the fridge. For commercial use, the spores are normally not sterilized. However, it is strongly advised that the growing media and containers be sterilized. A semi natural growing medium, a mixture of fine sand and one to two parts of finely screened peat moss is most often used commercially. Alternatively, a fluid nutrient solution (e.g. Knop's, Hoagland's, or Turtox) can be used. The medium should cover the bottom of the container permanently, which means a layer of about 7.5 mm depth. Agar media offer few advantages over fluid media unless the plants have to remain sterilized. After dusting the media surface with spores, the containers are entirely or partly closed to prevent water loss and contamination with fungi. The containers should receive low to medium intensity light. In about two weeks germination becomes visible by a thin green mat of threads on the medium surface. Gradually these threads develop into recognizable prothalli about 1 cm in diameter. When the prothalli are large enough they may be manipulated to ensure or avoid cross fertilization. Fertilization will not occur when the prothalli are not covered with a thin film of water. It may be necessary to apply misting to obtain this condition. Other overhead watering should not be applied and likewise dripping from overhead condensation on the container lid should be avoided, as this promotes fungal growth. Moulds that develop nonetheless should be killed as soon as they become visible, by isolating the patch and applying a fungicide. After fertilization, the young sporophytes soon emerge. Once they are large enough to handle, they may be carefully transplanted.
1.7 Genetic resources and breeding
Many pteridophytes are fastidious habitat discriminators and thus vulnerable to loss of genetic diversity. At least 700 species are globally endangered (Dyer & Lindsay, 1996). Extinction or drastic reduction in genetic variation is a negative development because of the intrinsic value of the disappearing taxa, the impoverishment of the ecosystem, but also because of the decline of the chemical potential of bioactive substances, most of which have yet to be discovered. One example is the clubmosses of the genus Huperzia Bernh., from which valuable alkaloids and terpenoids have been extracted that are raw materials for the development of new medicines against serious diseases such as dementia (e.g. see the treatment of Huperzia serrata (Thunb. ex Murray) Trevis.). Some of the constituents occur in a wide range of related species, but others are specific to a single species or even to a taxon of lower rank. Many of these have a restricted distribution and logging, collecting and exploitation for personal or commercial purposes lead to a rapid decline of populations. It is feared that a number of species will become extinct in the future.
Ex-situ conservation can be achieved by maintaining living plants, but also by collections of viable spores. The viability of spores decreases over time, with rates varying from weeks to tens of years until none of the spores of a batch will germinate when sown. The common practice of storing dry, either at room temperature or cold, may be inferior to wet storage in retaining the germination capacity of the spores (Lindsay et al., 1992). In-situ conservation of pteridophytes and their ecosystems must always be the ideal. No environment is better suited to allow the subsistence of a species than its own. At present, however, ex-situ approaches must accompany in-situ measures to maintain the integrity of the gene pool for threatened species until in-situ conservation is practised (Page et al., 1992). Botanic gardens play an important role in ex-situ conservation and worldwide coordination of activities is being initiated. However, the conservation of tropical pteridophytes is lagging behind the temperate species due to lack of funding and organization and the number of species involved. The task of conservation of plant diversity has up to now mainly been shouldered by governmental and non governmental organizations, but seen in the light of the vast research budgets of pharmacological companies, these companies should also be urged to shoulder responsibility in safeguarding future plant resources both for the general interest and for themselves. As ferns are not horticultural crops, breeding is not normally done. Two exceptions exist, being Azolla Lamk and ornamentals. During the last decades, races of the mosquito fern Azolla have been selected towards a maximized nitrogen output under various cropping conditions. Azolla species have been hybridized and various genotypes of the symbiotic cyanobacterium were tried. The various selections and cultivars are still available from the International Rice Research Institute (IRRI). Breeding ferns for ornamental purposes has a long tradition. As long as ferns have been kept as ornamentals, plants with aberrant leaves or variegated colours have received special attention and their offspring or clones were distributed amongst other fern lovers. Especially 19th Century England, during the Victorian "fern craze" or "pteridomania", saw the origin of many cultivars and hybrids. Nowadays a large part of the market for ornamentals is still occupied by cultivars with misshapen leaves and breeders are continuously trying to create new cultivars that appeal to fashion sensitive customers.
With the ever-growing importance of the urban lifestyle at the expense of rural life, the distance between man and nature tends to increase. Younger generations achieve valuable skills for making their living in the city rather than to survive in remote areas where one has to depend on what nature can provide. It is therefore to be expected that botanical knowledge for daily use will disappear in the South East Asian countries, as it has virtually disappeared in industrialized countries. Yet today, in rural areas, there is still a living tradition of using plants found in the wild for food, medicine, construction and other purposes. It is a living tradition in the sense that, with modern transport and communication, new ideas about plant use in other areas reach the erstwhile isolated communities. These are tried and, when found to be valuable, find a place in the tradition, or lead to experiments to explore new possibilities. Scientific research thus can play a two way role, both as recorder of remaining ethnobotanical knowledge and as mediator of ideas between remote areas. Ferns as food do have a future. The young leaves of most ferns can be eaten as a vegetable, but not all are of equal quality. From the ferns treated in the next chapter, it may become clear that several of them have been selected for food by availability rather than palatability. However, as qualitatively adequate nutrition is not yet secured in all parts of the world, they may remain important as an additional food source. Other species though, have a good taste and feel by absolute standards and these could be developed into more important products. In New England (United States) and Japan small high value markets already exist with young fern croziers as delicacies and opportunities exist for the export of other species. To guarantee a steady supply of constant quality, cultivation of these ferns might be taken up. Ferns as fibres only play a role in artisanal production. Some of these products, such as fishing gear, are expected to disappear once they cannot compete with industrial products. For others a small market will remain in the tourist industry and traditional production. Nowadays in most areas, tree ferns are only used incidentally or casually as construction material. They are very well suited for the construction of makeshift bridges as they hardly rot or get slippery, but further development is not foreseen. A better opportunity lies in the production of high quality horticultural materials. In deforested middle elevation areas tree ferns grow and reproduce very well. Tree-fern farming for pots and fibres could generate access to a capital market. Care must be taken not to deplete the spontaneously grown stands of tree ferns, to comply with international regulations (required for export), to prevent erosion and to save future resources. The future of ferns as medicine could proceed in several ways, and which one it will be, if not a combination, is hard to predict. Most medicinal uses of ferns in South East Asia refer to traditional applications. In western Europe traditional knowledge about medicinal herbs disappeared as pharmacological medicines became widely available. In China, on the other hand, herbal medicine persists and is solidly rooted in society and the medical community. Other Asian countries occupy an intermediate position. Many people in South East Asia do not yet have access to pharmacological medicines, either for logistic or economic reasons. When this situation changes, their traditional medicine will be relatively well documented and partly backed up by scientific research. Marketing by representatives of pharmacological medicine or herbal medicine also will exert influence. Scientific knowledge about the pharmacological properties of medicinal ferns is by no means complete, although an increasing number of publications is filling in this gap. Ferns that have a recorded medicinal use are always more or less common species. It is rather worrying to think of the potential of the less accessible species that remain undiscovered by traditional medicine. With the ongoing threat to the tropical environment and its species diversity, this potential may be lost forever.
1.9 Recommended literature
The identification of South East Asian pteridophytes is often hampered by the lack of accessible literature. The Flora Malesiana project caters for this need by publishing a separate series on the Pteridophyta (van Steenis & Holttum, 1959-1981; Holttum, 1991; Kalkman & Nooteboom, 1998). The parts that have been published offer up-to-date revisions of the treated genera found in Malaysia, Singapore, Brunei, Indonesia, the Philippines and Papua New Guinea. Regrettably, the series, that was initiated in 1959, progresses slowly and a number of families have still not been covered yet. Therefore, other identification works dedicated to smaller areas are still necessary. For Peninsular Malaysia the Flora of Malaya (Holttum, 1968) provides an excellent entry, although it only treats the ferns, leaving lycopods and selaginellas to pose a problem. Piggott (1996) gives a colour photograph for most of the species described in Holttum. The Philippine pteridophyte flora has been described completely but the publication is hard to obtain and taxonomically outdated (Copeland, 1960). For Indonesia, fern floras are old and not all in English (Backer & Posthumus, 1939). For Indo-China the fern flora is old and in French (Tardieu-Blot, et al., 1939-1951). The Thai fern flora is well covered by the Flora of Thailand (Tagawa & Iwatsuki, 1979-1989). Finally, from neighbouring regions, the Flora of Taiwan (Huang, 1994) and Flora of Australia (McCarthy, 1998) prove very useful additional sources. The morphology and biology of ferns and fern allies is usually poorly covered in general text books, which concentrate on spermatophytes. A good introduction in a palaeobotanical context is found in Sporne (1975); exhaustive descriptions of the anatomy, morphology and development are given by Parihar (1989). In relation to the spore morphology, the atlas of Tryon & Lugardon (1991) provides thousands of detailed scanning electron microscope micrographs of spores of all pteridophyte genera, revealing intricate details. Accounts of the ecology of ferns are more commonly found. However, most of them are limited to not very profound habitat descriptions. A more systematic approach to the classification of tropical fern habitats is given by Holttum (1938) and Page (1979). Page (2002) presents a thorough reflection on the ecology of ferns, including their intrinsic biological possibilities and limitations.
3 Bryophytes (mosses)
The bryophytes (Bryophyta) consist of about 20 000 species, and are divided into 3 groups: Anthocerotopsida, Marchantiopsida (Hepaticae) and Bryopsida (Musci). The last 2 groups contain the majority of species and are usually called liverworts and mosses, respectively. They are distinguished by their vegetative structure and mode of development of the reproductive organs (gametangia and sporogonia).
Bryophytes play important ecological roles in natural ecosystems. In South-East Asia, montane forests, above 1200 m altitude, are richest in bryophytes, most of them being epiphytic. The bryophyte-rich forest reaches an optimum at about 2500 m altitude. Trees in the high mountain forest always have epiphytic bryophytes, which are sometimes very conspicuous, e.g. the hanging garlands of Aerobryum. The so-called "moss forest" is a sure indicator of an everwet (humid) climate, and is often found in depressions on the high mountains, where damp conditions prevail. It is an ecological type of the "elfin forest", which is the primary forest formation above 2000 m. In the cloud belt of mountains, also the soil, rocks and fallen logs may be carpeted with bryophytes, mostly liverworts. Extensive carpets of hydrophilic terrestrial mosses such as Sphagnum are limited to wet localities in the mountains. Lowland forest may be rich in bryophyte species, but the proportion in the total vegetation is usually small.
A comprehensive review of the worldwide uses of bryophytes is available, including decorative, household and medicinal uses, as soil additives, for horticultural practices and as bio-indicators for environmental degradation (Glime & Saxena, 1991). Species are included that are commonly found in the Old World tropics, e.g. Herbertus, Leucobryum, Marchantia, Rhodobryum and Sphagnum species. Compared to the ferns and especially seed plants, bryophytes are little used in South-East Asia. One of the reasons for this is that they are not abundant in lowland rain forest, where human settlements are often located. However, limited use of bryophytes has been documented for a few useful mosses for Peninsular Malaysia: Calymperes, Campylopus and Sphagnum are used for medicinal purposes, stuffing mattresses and decoration (Burkill, 1966). Field observations in remote mountainous areas in South-East Asia have confirmed the tribal usage of large and showy moss plants, such as Dawsonia, Pogonatum and Spiridens species, together with fern allies such as Huperzia, Lycopodiella, Lycopodium and Selaginella, as body decoration and to ward off evil spirits. Sphagnum (peat moss) is sometimes used as nesting material for artificial incubation of eggs in crocodile farms in the Philippines. The use of dried moss material (e.g. Sphagnum, Hypnum and Trachypodopsis) for fuel and house construction, as reported for temperate regions (Pant & Tewari, 1989), has not been observed in South-East Asia. It appears that the largest market for moss products is in the cities due to the demand of horticulture. Large and small packages of moss mixtures, labeled as "peat moss", are sold in department stores and supermarkets. They are used in potting mixtures for greenhouses and nurseries and are also employed for soil improvement in gardens. Surveys made in Singapore, Malaysia, Thailand and the Philippines have shown that the moss mixtures sold in markets usually contain large amounts of Ectropothecium, Homaliodendron, Neckeropsis, Thuidium and Vesicularia, but also liverworts, including Bazzania, Heteroscyphus and Pallavicinia. However, the mosses which are most in demand by orchid growers are Leucobryum and Sphagnum, both of which can store a large amount of water. In the Cameron Highlands, a major centre of horticulture in Peninsular Malaysia, large bags of Sphagnum moss imported from Canada can be purchased. A newly-developed market for mosses is the trade in aquarium plants. Javan moss (Taxiphyllum barbieri (Cardot & Copp.) Z. Iwats.), which is indigenous in South-East Asia, has become a popular aquarium plant for fish hobbyists around the world. Mosses commonly used by bonsai enthusiasts (e.g. in Singapore) to decorate the potted landscape are species of Bryum and Philonotis and, to a lesser extent, Isopterygium, Vesicularia and the thalloid liverwort Riccia. These bryophytes are often widespread in the region. Recently the introduction of Ochrobryum kurzianum Hampe from Thailand has been reported to be used as an ornamental moss in bonsai potting in Singapore (Tan & Tan, 2000). The custom of building a moss garden, which has been practised for centuries in Japan, has not yet caught on in South-East Asia. Bryophytes are used on a small scale in local handicraft industries manufacturing souvenirs and memorabilia, e.g. postcards, bookmarks and paperweights, using the bryophytes as a motif. Other incidental uses of bryophytes are in packaging, as well as in window-dressing and showcasing gift displays at department stores during the Christmas season. Although several studies have yielded convincing experimental data for anti-tumour and anti-microbial properties of bryophytes (Spjut et al., 1986, 1988; Raymundo et al., 1991; Lorimer et al, 1996; Soh and Chan 2001), bryophytes are not prescribed in traditional medicine in South-East Asia. This contrasts with the situation in China, where many folk medicinal uses of bryophytes have been described (Ding, 1982). Several of the species used in China are also found in South-East Asia.
Because of the unique chemistry of liverworts, many species have been examined for the presence of bioactive compounds (Asakawa 1999). There is an on-going programme at the Department of Chemistry of the National University of Singapore, where liverwort chemistry is under investigation. Part of this programme is aimed at finding compounds with promising pharmaceutical applications.
Trade figures of bryophytes in South-East Asia are not available, but are probably insignificant. All moss products originate directly from the wild. Because of the slow growth of many bryophytes, the quantity harvested needs to be monitored and regulated by the government in regions where collection is common, in order to assure the continued survival of vegetations dominated by bryophytes. Bryophytes play important ecological roles in natural ecosystems. To realize their commercial potential, more utilization studies are needed. But first of all there is a need to document fully the diversity and species distribution of this poorly known group of plants and understand well its biology and ecology.
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