Image ©: Fred Rumsey
This project is focused on spore-producing vascular plants, which are composed of two distantly related lineages called lycopods and ferns. Since they both produce spores and have a similar life cycle, in the past they were usually united under the name ‘pteridophytes’ or ‘ferns and fern allies’. However, these groups are not monophyletic (they do not descend from a common evolutionary ancestor or ancestral group) since ferns are more closely related to seed plants than to lycopods.
Unlike seed plants, the life cycle of ferns and lycopods has two free-living stages, the sporophyte and the gametophyte. Sporophytes are the larger, complex plants that produce spores in sporangia, often aggregated in sori. In most ferns these are formed on the lower side of the leaf blade and in lycopods mostly in leaf axils. When landed in a suitable spot, the spores germinate into a gametophyte, a simple structure that produces female and male gametes (reproductive cells), the latter with flagellae that allow them to swim to the female gametes, usually in a thin film of water. When fertilisation has been successful, a new sporophyte develops and the gametophyte withers away. This peculiar life cycle is called the ‘alternation of generations’. Many ferns and lycopods also reproduce vegatatively via proliferous buds or bulbils on leaves, stems, rhizomes or on gametophytes.
Lycopods (class Lycopodiopsida) date back to the Silurian period (c. 425 million years ago; Rickards 2000) and they were the first dominant vascular land plants on Earth. Together with algae, liverworts, mosses, hornworts, ferns and early lineages of plants that are now extinct, they were responsible for the fixation of carbon in coal, oil and natural gas, and as such fixed large amounts of carbon dioxide from the atmosphere, making the air breathable and tempering the climate. Lycopods had a much greater diversity in the past than today, but this does not make the modern species ‘living fossils’. These are as well adapted as their flowering plant counterparts and many are recently evolved taxa, which have arisen in the new habitats formed by seed plants. An exception may be Selaginellaceae, since Permian Selaginella harrisiana (aged ca. 273 million) has a full set of extant Selaginella characteristics.
Lycopods are subdivided into three families: Lycopodiaceae (clubmosses), Selaginellaceae (spikemosses) and Isoëtaceae (quillworts). Terrestrial Selaginellaceae and aquatic Isoëtaceae are unique in having two types of spores (large and small ones), where the gametophyte develops inside the spore wall, and is possibly an adaptation to adverse environmental conditions in order to better protect small gametophytes. Endosporic germination can also be found in families of aquatic ferns (Marsileaceae and Salviniaceae). Lycopodiaceae are composed of three genera: Huperzia, Lycopodiella and Lycopodium, which differ in characters of branching patterns, the presence or absence of modified leaves, spore morphology, gametophyte shape and chromosome number. Lycopods differ from other vascular plants in having microphylls, simple leaves with only one central vein. Many lycopods have subterranean gametophytes that make an obligatory association with fungi (Merckx et al. 2012). Spores of lycopods with these subterranean gametophytes need some disturbance of the ground cover to penetrate into the soil, which is why colonisation of abandoned gravel and sandpits or soil following forest fires is often successful.
Globally, ferns (class Polypodiopsida) are subdivided into 11 orders, with a total of 21 families and some 215 genera, but the concept of families and genera in ferns remains a matter of controversy, with some authors preferring a higher degree of splitting. Polypodiales is the largest order encompassing most ferns, in which Polypodiaceae (c. 4,080 species) is the most species-rich family.
In general, ferns are distinguished from lycopods by having megaphylls, leaves that are usually supported by more than a single vein, often called ‘fronds’ to distinguish them from leaves of seed plants. Most extant ferns have sporangia on the underside of the leaf, although separate structures presenting the spores are common in several lineages. The vascular system is also usually more complex than in lycopods.
Ferns first appeared in the fossil record some 360 million years ago (during the Devonian Period), but most modern lineages of ferns are considerably younger, appearing during the Cretaceous (c. 145 million years ago). They evolved after flowering plants became dominant, creating many new habitats allowing remaining fern lineages to diversify. Most ferns therefore should also not be described as ‘living fossils’, possibly with the exception of horsetails (Equisetaceae), which have morphologically changed little for at least 250 million years. Fossil specimens are easily recognisable as a member of the modern genus Equisetum, possibly the oldest extant plant genus on Earth.
Ferns and lycopods occur in many different habitats, from mangrove forests and peat swamps to rocky mountain peaks and open deserts, but are most diverse in misty, humid tropical and subtropical cloud forests at mid elevations. The adaptations of ferns and lycopods into extreme habitats are noteworthy and in some genera (e.g., Marsilea) the mechanisms of adaptation to submergence and desiccation are similar, with the spores being protected in a hardened structure formed by specially modified leaves. Others have leaves that can recover after desiccation and many species reproduce vegetatively by producing buds on the leaves, allowing them to rapidly colonise new areas.
Although most ferns have green gametophytes that photosynthesize, some species have gametophytes that live exclusively in a parasitic relationship with fungi (mycoheterotrophs) and only produce chlorophyll once a sporophyte is developed. These mycoheterotrophic gametophytes are mainly found in Psilotaceae and Ophioglossaceae, which can be problematic for ex situ conservation, particularly for threatened species of moonworts (Botrychium). Some species of filmy ferns (Hymenophyllaceae) have gametophytes that can reproduce vegetatively and some populations rarely or never produce sporophytes. These can be found as gametophyte colonies, well outside the range where sporophytes occur, which have been suggested to be remnants of warmer periods in geological time.
To date, about 10,560 fern species and 1,290 lycopod species have been described worldwide and several dozens of new species are discovered every year. The majority of species are found in the tropics, where they benefit from constant warmth and humidity, with the highest diversity at mid elevations. However, ferns and lycopods can be found across the world in any type of habitat, varying from the Arctic tundra to tropical rainforests, from dry deserts to floating or submerged in lakes and rivers. In general, the diversity decreases at higher latitudes and in areas with less precipitation.
In Europe, there is also a clear gradient from east to west, where the more humid Atlantic regions host a higher abundance and number of species. This need for humidity is directly linked to the life cycle of ferns and lycopods, where water is needed for the free-swimming male gametes to reach the sessile female cells. In addition, gametophytes and some sporophytes (particularly Hymenophyllaceae) have thin layers of tissue that are prone to drying out. Therefore, ferns are usually found in humid environments, such as damp banks and damp areas in forests, peat bogs, sides of ditches and streams, inside rocky crevices, edges of wells, on damp walls and other humid places. In the more humid Atlantic regions there are several species that grow epiphytically on mossy branches of trees. This phenomenon is common in the humid tropics, but much less so in temperate regions.
However, there are a number of species in Europe that have developed strategies to survive in harsher, dry conditions, such as vernal pools, steppes and Mediterranean scrub, although in all these areas there is at least a period of humidity during which they reproduce. In general, most fern species are resilient when their main area of distribution and populations are not under threat. However, some species are sensitive to certain threats.
Ferns play essential roles in providing ecosystem services, such as soil erosion prevention, stream bank stabilisation, removal of pollutants from the environment, soil creation on barren habitats, carbon fixation and the provision of shelters and habitat for small animals. They have also been significantly used for horticultural purposes. Many species, native and exotic, are commonly grown in gardens and specialist collections.
Fiber from the rhizomes of Royal Fern (Osmunda regalis) was commonly used as an orchid growing medium (Sheehan 1960) and leaves of Maidenhair Fern (Adiantum capillus-veneris) are locally popular for making syrup. Scouring-Rush (Equisetum hyemale) was previously used to scrub pans and other metal objects. Young unfurling leaves of some species can be eaten, particularly those of Ostrich Fern (Onoclea struthiopteris), but carefully and in moderation as some strains of this fern are mildly poisonous and less palatable. In addition, some ferns are known for their medicinal properties, such as Adiantum capillus-veneris, whose fronds show antimicrobial activity or Equisetum arvense, which is used as diuretic and remineralizant, among others.
However, many other ferns are highly carcinogenic, with species such as the Common Bracken (Pteridium aquilinum) having genotoxic, cytotoxic, carcinogenic and immunomodulatory effects on animals and humans and it has a long history of poisoning grazing livestock.
Lycopods are less commonly cultivated, although some Selaginella species, particularly S. kraussiana, can be found in the horticultural trade. The spores of Lycopodium are high in fatty acids and ignite easily. Lycopodium powder was formerly widely collected from the wild and used in photography flash lights. It was also used for powdered surgical gloves, although this may cause allergic reactions in some patients and this practice has now been abandoned. Some fern and lycopod species have also been used to a smaller extent in the chemical industry as they contain a vast array of interesting chemicals resulting from their long evolutionary history.
In Europe, 38 lycopods and 156 ferns were identified, amounting to a total of 194 species. For the purposes of this report, endemic species are those that are known only from the European Assessment Zone. Of the 194 species in Europe, 28.4% (55 species) are considered endemic to the assessment region based on known, suspected, or inferred occurrences. This represents almost a third of the European fern and lycopod flora, with most of these endemic species being found in the Macaronesian region. Most endemic species have relatively small geographical ranges and are restricted to specific habitats.
Ferns are often good colonisers of new habitats, such as rocky slopes, masonry, reclaimed land and lava flows, including newly formed oceanic, volcanic islands. Once these habitats are reached and become isolated, speciation may then take place. The most diverse areas are mid-elevation tropical mountains and oceanic islands. The higher fern diversity of the Macaronesian islands can be explained by this as the islands are oceanic and in part subtropical. Speciation of ferns frequently happens through allopolyploidy, where two species cross forming a stable hybrid with more sets of chromosomes and thus become genetically isolated, new species. While polypoidy is a common feature in various plant groups, this particular form of speciation resulting from hybridisation is far more common among ferns than in flowering plants.
Some ferns, often odd-ploids of hybrid origin, achieve fertility through a subsexual process, creating fewer spores of the same ploidy level as the leafy plant (which means that the spores have the same number of chromosomes as the sporophyte). This creates uniform, essentially clonal lineages, which may interbreed with normal sexual plants creating a multiplicity of forms (microspecies) that are taxonomically problematic. A prime example is the Dryopteris affinis complex, in which many microspecies are known. Recognition of these taxa may strongly affect species numbers, conservation assessments and other analyses based on this. Particularly, their ability to produce sporophytes in the absence of fertilization allows successful colonisation in drier environments and improves the chances of single spore and longer distance colonisation, giving them an advantage over sexually reproducing taxa. The majority of invasive fern species of urban environments, both native and exotic, show this type of breeding system.
Aspleniaceae, which has a high diversity worldwide, is the most diverse family in Europe with 58 species. This family includes the genus Asplenium, which is the most species-rich genus of ferns in Europe. Aspleniaceae is closely followed by Polypodiaceae (42 species), which is the most species-rich family across the temperate regions of the Northern Hemisphere. Both are highly derived fern families that were able to diversify in the new habitats created by the diversification of angiosperms (Schneider et al. 2004). Many also form allopolyploid species and some produce hybrid swarms, making it difficult to discern between species. Therefore, it is not surprising that the highest number of endemic species belongs to Aspleniaceae (16 species, 27.6%), Polypodiaceae (14 species, 33.3%) and Isoëtaceae (13 species, 65%), the latter due to recent studies in the Mediterranean species of Isoëtes, a genus that was previously poorly known (Troia et al. 2016). Families with only a single native representative species in Europe include Cyatheaceae, Osmundaceae, Psilotaceae and Salviniaceae.