The characteristics and significance of soil spore banks of ferns

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1 The characteristics and significance of soil spore banks of ferns ADRIAN F. DYER - ROYAL BOTANIC GARDEN EDINBURGH, UK adrian@dyer499.freeserve.co.uk It is now widely accepted that at least some ferns can form soil spore banks reservoirs of live but dormant spores buried in the soil. No description of the reproductive biology of a terrestrial fern species is now complete without a consideration of the existence and potential role of a soil spore bank. However, little new information has been acquired during the last 10 years. Perhaps this is now an appropriate time to review our current understanding of soil spore banks in order to identify where further research should be directed. To do this, it is first necessary to recall the characteristics of the spore. The fern spore The fern spore is a single cell that carries the genetic potential for the development of both the gametophyte and sporophyte generations. It is the dispersal phase responsible for the colonisation of new sites. In many climates, spores are released over a limited period at the end of the growing season. The spore release season may be less clearly defined in some tropical climates. Most spores are dispersed by moving air. Several investigations have shown that many spores fall close to the source, particularly in sheltered woodland conditions, with the density reducing rapidly with distance. However there is much circumstantial evidence to indicate that some spores travel much greater distances, though no-one has determined what proportion of spores do this. The potential range is probably affected by spore size, shape, surface sculpturing, and longevity. Many spores can retain their viability for several years. By contrast, a minority of species, including Osmunda, form green spores that die after only a few days or weeks in storage. Low temperature prolongs viability. Longevity of both types of spores is dramatically increased after they have imbibed water. It is also known that spores from soil banks are viable after passing through the gut of earthworms. The first requirement for germination is water. This is taken up by the spore which then becomes physiologically active within a few hours. The second requirement, in most species, is for red light, to initiate germination. Then, provided that a suitable temperature and, in some cases, minerals are available, cells emerge from the spore wall. Thus, in the absence of water, at temperatures below 5 C, and, for most species, in the absence of light, germination is prevented and the spore remains quiescent until it dies.

2 The red-light response is mediated by phytochrome. At 20 0 C in the laboratory, the imbibed spore is committed to germination after about hours of red light, and will germinate even if subsequently returned to the dark. Some simple field experiments indicate that in natural conditions this commitment might require about 1 week exposed to daylight. Thus, any spore that penetrates the surface layers of the soil before being committed to germination will remain quiescent in the darkness below, thereby becoming part of the spore bank. Characteristics of soil spore banks Our knowledge of soil spore banks is limited and little has been added to it in recent years. This is due to the lack of experimental investigations and to the limitations of the method. Whenever possible, soil samples are taken just before the seasonal spore release, so that any spore bank detected must have been present throughout the year. This is called a persistent spore bank to distinguish it from ephemeral spore banks that do not survive in the soil longer than a few weeks or months. Results to date indicate that soil spore banks are widespread taxonomically, ecologically and geographically. Over 90 species have been identified in soil samples from various parts of the world. Surprisingly, both Osmunda regalis and Onoclea sensibilis form persistent soil spore banks even though their green spores are said to be short-lived. Spore banks have been found in a wide range of temperate habitats; indeed it is more difficult to find sites which have no spore bank. In most soils, two or more species are present; we have identified up to 7 species in a single small soil sample. In each case, the spores present in a sample are dominated by those species that have fertile sporophytes within 5m of the sample site but spores of other species from sources up to several kilometres away are sometimes also present in small numbers. We regularly find spores banks up to a depth of 30cm and have found them down to 1.25m. Usually the density of the spore bank (measured as the number of gametophytes formed in culture per unit volume of soil) declines with depth. Fern spore banks are accompanied sometimes by seed banks and frequently by bryophyte diaspore banks but the three types of propagule often show a different vertical distribution within the soil. This may reflect differences in the longevity of the different propagules, and/or differences in their movement through the soil. Even when seeds are present, the fern spores are much more abundant. Although there is circumstantial evidence to suggest that spores of at least some species have the potential for remaining viable in the soil for several

3 decades, there is little experimental confirmation. We know that buried spores at many sites survive for at least a year and in one experiment we demonstrated that a substantial spore bank could survive for at least 3 years. Other evidence suggests that spores may have the potential to survive longer in damp soil than in dry storage, though whether they do so will probably be determined by other factors such as predation. This leaves us with the question of how spore banks form how do dormant spores enter the soil, reach a depth (perhaps 5mm) where there is no light within the few days before they are committed to germination, and then move further down through the soil, sometimes reaching depths of over a metre within the lifetime of the spore? The obvious possibilities are: 1. by being carried by water percolating down through the soil, 2. by being moved on, in or by animals, or 3. by being buried under deposited soil. The only one that appears capable of acting consistently over large areas within the required time-scale is water but this has still to be confirmed experimentally. We are now in a position to consider the role of the soil spore bank in the natural life cycle. The potential significance of soil spore banks in the natural life cycle of a fern. The existence of soil spore banks is observed fact, but regeneration from a spore bank in the wild has not been directly observed. Their natural role must therefore be a matter of conjecture. Buried quiescent spores will have the potential for development whenever soil disturbance brings them once again into the light on the surface. The significance then of a persistent spore bank is that gametophyte development would not be restricted to the period just after dispersal when the spore first alights on the surface, but could occur whenever exposure coincides with suitable growing conditions. Soil spore banks that persist for many years could confer additional advantages. They would reduce the risk of population extinction. In this way they would serve a function similar to that of seed banks in angiosperms. Regeneration from persistent spore banks could also: 1. modify the breeding system by accumulating rare spores from distant sources, thereby increasing the opportunities for inter-gametophytic mating of colonising species; 2. provide a buffer against the consequences of low spore production in years with adverse weather conditions; 3. provide a buffer against dramatic changes in composition of the gene pool during severe fluctuations in population size; genotypes lost from the living sporophytes could be retrieved from the spore bank. The potential significance of spore banks in conservation.

4 The formation of a soil spore bank not only provides a natural strategy for survival and regeneration but can also be exploited to provide new opportunities for ex situ and in situ conservation. Ex situ conservation Natural spore banks in soil samples can be used as a source of ex situ collections or gene banks. Persistent spore banks have some advantages over sporophytes or newly-released spores for this purpose. 1. They can be collected at any time of year, which is important for inaccessible species with a short spore-release season. 2. Removal of a small soil sample at up to 1-2 metres from the plants will have no adverse effect on the population. 3. The soil samples are relatively compact, contain many spores and thus incorporate a large proportion of the available genetic diversity, and may even contain genotypes no longer present in the living sporophyte population. 4. The samples are easily transported and stored for several years. Indeed, storage in moist soil might be the simplest way to prolong the life of green spores. 5. The samples are easily cultured and sporophytes can be reared from the spore bank whenever required. 6. The soil will often contain spores of several species and thus preserve a fern community rather than a single species. At the same time, there are some possible disadvantages: 1. There is no guarantee that viable spores of the required species are in the soil sample and there is no way that this can be checked in the field. 2. There are severe restrictions on the import of soil samples across some national boundaries. 3. Not all the spores in a sample yield sporophytes and some species might be at a particular disadvantage in artificial culture conditions, making retrieval difficult. However, using this approach, we have established conservation collections for several species that are rare in Britain. In situ conservation Soil spore banks offer the possibility of in situ restoration of endangered populations, especially where the decline has been recent and due to man s activities. By creating the circumstances for which soil spore banks are preadapted, it might be possible to induce spontaneous regeneration. Artificial disturbance of the soil and, perhaps, the creation of local micro-habitats to provide shade, moisture, substrate stability, and protection from competition, might allow the establishment of gametophytes and young sporophytes. In

5 this way, a seriously depleted population might be augmented by individuals with genotypes native to the site without the need to transplant sporophytes raised ex situ. There is even the possibility that plants regenerating in situ could include genotypes no longer present in the remaining sporophytes. Further, it might be possible in this way to retrieve a population, or indeed even a species, which has recently become totally extinct. This approach has not yet been tried to my knowledge but I hope someone will do so when a suitable site is available. Priorities for future research. As described above, the indications are that soil spore banks are an important feature of the reproductive strategy of many ferns. However, to properly understand the role of spore banks in the wild, and their potential for conservation, much more information is required. We need to know more about the geographic, ecological and taxonomic distribution of persistent spore banks in species with seasonal spore-release. To answer these questions fully requires an improved method for determining the species present in soil spore banks.to better understand how soil spore banks form and persist, we need more research into spore biology: the dispersal characteristics, the physiology of spore ageing, the control of dormancy, the processes resulting in germination, and the factors which affect survival in the soil. Perhaps the most intriguing question to be answered concerns the longevity of spores in the soil. How long do spores in a spore bank remain viable? Direct evidence would require long term field experiments where an area is covered to prevent spore recruitment and samples are taken at intervals to determine survival. Indirect evidence might come from investigations of the mechanism and rate of spore movement down through the soil. In all these investigations we must not assume that all species are the same; it is likely that ferns are diverse in their establishment strategies. Finally, we need to explore further the possibilities of exploiting spore banks as long-term spore traps to investigate spore dispersal, and as a source of new individuals for in situ restoration programmes.