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- Materials and methods
1 The relationship between size and floristic composition of the seed bank and vegetation dynamics was studied between 1976 and 1996 in 0.75 ha of an abandoned Cirsietum rivularis meadow. The plot was divided into 100-m2 (10 × 10 m) quadrats and sampled 5-yearly to map the vegetation and determine the soil seed bank.
2 Densities of seeds in the soil fluctuated as succession proceeded. The initially small seed bank trebled by 15 years after abandonment, before falling, after 20 years, to approximately the same as in the initial stage.
3 The floristic richness of the seed bank decreased during succession, with the number of species falling from 38 to 25. The diversity of life forms, however, increased in later periods, with tall herbs, shrubs and trees appearing after 10 years.
4 Seed bank floristic composition is apparently both a product of the species composition of the current vegetation and a record of the long-term substitution of species. Other factors, including the structure of the vegetation, also influence the accumulation of seeds in the soil.
5 Although changes in number of species show a directional pattern, the seed bank size fluctuated in the course of succession on these fertile wet meadows.
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- Materials and methods
Mechanisms of secondary succession are assumed to involve the bank of seeds in the soil, and thus to depend on the different patterns observed for seed banks. For example, succession on fallow land (a habitat markedly transformed by humankind) has been described in terms of directional change, in which the floristic richness of the seed bank declines between the initial and terminal stages, in parallel with the density of seeds (Pickett & McDonnell 1989; Roberts & Vankat 1991). However, succession in semi-natural grassy or meadow communities tends to show other types of change (Donelan & Thompson 1980; Patridge 1989; Milberg 1995) in which the greatest density of seeds in the soil occurs during the temporary (herb-dominant) stage (Oosting & Humphreys 1940).
Many of the patterns described for seed banks fail to reflect the species composition of the above-ground vegetation (Leck et al. 1989). This is often linked with a failure of the seeds of many species to persist in the seed bank (Thompson 1992) but may also be due to some species present in a seed bank failing to be detected by the particular method used (Gross 1990; Bakker et al. 1996; Ter Heerdt et al. 1996; Thompson et al. 1997). Long-term simultaneous and multi-faceted research on the dynamics of both the vegetation and the seed bank are therefore needed to understand the relationships between the species compositions. The influence of the seed bank on the course of succession is also dependent on the relative importance of the bank of seeds present in the soil as the process is initiated, compared with the subsequent influx of seeds from the exterior.
The aim of the present research was thus to determine the pattern of the seed bank during secondary succession from meadow to forest, as part of a series of studies on vegetational change in abandoned meadows carried out in Polanłowieża Primeval Forest between 1972 and 1996. Correlation with data on the dynamics of the vegetation and the demography of species participating in succession (Falińska 1989, 1991) should allow for a fuller recognition of the role of the seed bank in secondary succession, by determining the degree to which changes in floristic composition are reflected in the species composition of the seed bank. In particular, we considered whether seed banks differ in particular successional stages or include the same species throughout development from meadow to willow scrub.
We also determined whether species that play a significant role in vegetational development can be absent from or only weakly represented in the seed bank, and if species occurring only sporadically in the vegetation, or altogether absent from it, can account for a significant proportion of the seed bank.
In essence, we investigated whether the composition of the seed bank is wholly or partially determined by the floristic composition of the vegetation or is dependent on random events.
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- Materials and methods
The results indicate that, in the course of meadow to forest succession, seed bank size fluctuates: a low density was found initially but rose over threefold after 15 years before falling back to a level similar to that recorded at the initial stage. However, according to earlier studies (Falińska 1981, 1996) the density of seeds in a stable (climax) floodplain forest community adjacent to the abandoned meadow was twice as high as in a willow scrub similar to the end-point community here.
Other studies conducted in semi-natural communities and on arable land (Graham & Hutchings 1988; Cavers & Benoit 1989; Rice 1989; Levassor et al. 1990; Hester et al. 1991; Milberg 1992; Bakker et al. 1996; Mitchell et al. 1997, 1998) show different patterns from those observed here. For instance, although the highest density of seeds was found at the temporary (macroforb) stage (Oosting & Humphreys 1940) it came as late as in the forest community in another (Patridge 1989). Directional changes in the density and species richness of the seed bank during succession have very rarely been described (Pickett & McDonnell 1989; Roberts & Vankat 1991), perhaps because the numerous vegetation changes that occur during succession may not be linear in nature. The floristic composition of the seed bank is partly determined by the current species composition of communities but depends also upon the vegetation history (Grandin & Rydin 1998) and on the biological properties of plants (Harper 1977; Silvertown 1980, 1981). Factors such as fecundity, seed germination ability (Cook 1980; Fenner 1985; Baskin & Baskin 1989), longevity (Baker 1989; Rice 1989; Milberg 1990; McDonald 1993; Thompson et al. 1997), migration, mode of seed dispersal (Rabinowitz 1981), life history (Grime et al. 1988) and size and shape of seed (Thompson et al. 1993; Hutchings & Booth 1996a, 1996b), may be important and can sometimes be regarded as random events. The low number of seeds at the beginning of this succession, in spite of the richness of species, probably results from the fact that the meadows had been mowed during the flowering period (Falińska 1991) so that few plants would have set fruit. Five years after the last mowing of the meadow the number of seeds had doubled. The cessation of mowing would allow the majority of plants to set seed, thus increasing the supply to the soil, and clonal plants to multiply the number of generative ramets, as documented in studies on the demography of species during succession carried out in the same area (Falińska 1986, 1991). The highest seed density in the soil 15 years after the cessation of mowing may have resulted from seed accumulation in the soil because of abundant production combined with limited germination due to the increasing density of clonal plants (Falińska 1995, 1997). Soil from under the canopy of willows contained seeds of meadow species, e.g. Cirsium palustre, Ranunculus acris and Lychnis flos-cuculi (Table 3), that were no longer present in the vegetation, which confirms earlier reports that seeds of certain species are long-lived (Cook 1980; Roberts 1981; Fenner 1985; Milberg 1990; McDonald 1993; Thompson et al. 1997). It is not clear why the seeds of forest species did not begin to appear in the soil until several years after meadow abandonment, as the meadow was adjacent to a forest. The rich meadow vegetation may have limited the inflow of migrating seeds because penetration into the soil may occur only when gaps appear in the vegetation as a result of the death of clones of the dominant species (see data for Filipendula ulmaria;Falińska 1995). Vegetative reproduction may significantly affect the role of the seed bank in succession as it leads to formation of a compact vegetation cover. The appearance of gaps may be needed to facilitate the emergence of seedlings and vegetation regeneration (Pakeman & Hay 1996). Such limitation may also be responsible for the decreasing density of seeds as willow scrub formed. Similar results have been obtained by other authors, for example Davies & Waite (1998), who found a negative correlation between the age of the scrub and the size of the seed bank.
Table 3. Presence of species in the seed bank at the initial (meadow) and early terminal (willow brushwood) succession stages. The assessment was carried out for the total number of seeds in the soil (SB), seedling emergence in the in greenhouse (GSB) and seedling emergence under field conditions (F)
| ||Meadow (0–5 years)||Willow brushwood (15–20 years) |
|Cirsium palustre|| * || * || * || * || * || * |
|Cirsium rivulare|| * || * || * || * || * || * |
|Lychnis flos-cuculi|| * || * || * || * || * || * |
|Ranunculus sp.|| * || * || * || * || * || * |
|Myosotis scorpioides|| * || * || * || * || * || * |
|Galium palustre|| * || * || * || * || * || * |
|Viola epipsila|| * || * || * || * || * || * |
|Viola palustris|| * || * || * || * || * || * |
|Filipendula ulmaria|| * || * || * || * || * || * |
|Lythrum salicaria|| * || * || * || * || * || * |
|Lysimachia vulgaris|| * || * || * || * || * || * |
|Urtica dioica|| * || * || * || * || * || * |
|Scutellaria galericulata|| * || * || * || * || * || * |
|Peucedanum palustre|| * || * || * || * || * || * |
|Caltha palustris|| * || * || * || || * || * |
|Crepis paludosa|| * || * || * || || * || * |
|Juncus effusus|| * || * || * || || * || * |
|Rumex acetosa|| * || * || * || || * || * |
|Lotus corniculatus|| * || * || * || || || * |
|Cerastium holosteoides|| * || * || * || || * || |
|Epilobium palustre|| * || * || * || * || || |
|Potentilla anserina|| * || * || * || || * || |
|Polygonum bistorta|| * || * || * || * || || * |
|Geum rivale|| * || * || * || || || * |
|Aegopodium podagraria|| * || * || || || || * |
|Plantago lanceolata|| * || * || || || || * |
|Betula pendula|| * || || || * || || * |
|Scirpus sylvaticus|| * || || || || || * |
|Lathyrus pratensis|| * || * || * || || || |
|Vicia cracca|| * || * || * || || || |
|Trifolium repens|| * || * || * || || || |
|Cardamine pratensis|| * || * || * || || || |
|Campanula patula|| * || * || * || || || |
|Potentilla palustris|| * || * || * || || || |
|Geranium palustre|| * || * || * || || || |
|Mentha arvensis|| * || * || * || || || |
|Polemonium caeruleum|| * || * || || || || |
|Galeopsis tetrahit|| * || * || || || || |
|Symphytum officinale|| * || || || || || |
|Taraxacum officinale|| * || || || || || |
|Senecio jacobaea|| * || || || || || |
|Anemone nemorosa|| || || || || || * |
|Populus tremula|| || || || || || * |
|Solanum dulcamara|| || || || * || * || * |
|Lycopus europaeus|| || || || * || * || * |
|Rubus sp.|| || || || * || * || |
|Geum urbanum|| || || || * || * || |
|Geranium robertianum|| || || || * || * || |
|Cardamine amara|| || || || * || * || |
|Impatiens noli-tangere|| || || || * || * || |
|Salix sp.|| || || || * || || * |
|Alnus glutinosa|| || || || || || * |
|Frangula alnus|| || || || || || * |
Data from all three methods indicate that the density of forest plant seeds in the soil increased as succession progressed, as observed for seed banks in other forest communities (Falińska 1981; Pirożnikow 1983; Patridge 1989; Pickett & McDonnell 1989; Nakagoshi 1996). However, complete return of the abandoned meadows to forest is expected to take about 150–200 years (Faliński 1986) and the total seed bank size will probably increase and decline several times during this period.
The number of species in the seed bank decreased over the course of succession from 38 to 25. While there might be increasing difficulties in identifying seeds as groups such as grasses, sedges and willows become dominant, this is unlikely to explain the reduction in species as only two species of sedge (Carex acutiformis and Carex cespitosa) and one of willow (Salix cinerea) were common in the vegetation.
It is also worth emphasizing that as well as supplying the recruits needed for the development of new species compositions during succession, the seed bank will, if seeds of meadow species persist, allow regeneration of the meadow if succession is arrested. Emergence in the field after mowing shows that although their proportion decreased gradually in successive years in favour of the forest species, meadow species constituted a considerable part of the pool of seedlings for at least 20 years (Fig. 3c). Juncus effusus, Urtica dioica and Scirpus sylvaticus seedlings were very rare in these plots, and thus it can be assumed that moderate disturbance during succession (by removing vegetation) preserves the floristic richness, although environmental screening leads to the continued absence of some species. The seed reservoir in the soil is therefore of great significance for the regeneration of the vegetation following disturbance, as has often been proposed (Grubb 1988; Hutchings & Russell 1989; Silvertown & Tremlett 1989; Thompson 1992; McDonald 1993; McDonald et al. 1996; Pakeman & Hay 1996; Mitchell et al. 1997, 1998).
Estimates of seed bank size made according to three different methods gave different results (Fig. 2). The total number of seeds picked out of the soil was 2–3 times higher than the size of the seed bank assessed by seedling emergence under laboratory conditions, and 10–20 times higher than suggested by seedling emergence in experimental plots in the meadow. These differences were to some extent expected, if only due to the varying types of seed dormancy and different temperature and humidity requirements (Thompson & Grime 1979; Cook 1980; Fenner 1987; Thompson 1987). No single method can determine the full species composition of a seed bank, because a researcher picking out the seeds of the soil may overlook very small seeds, while counting deeply dormant and non-viable seeds, and the period of observation of seedling emergence in the laboratory may be too short to allow full germination of many species. Our results are consistent with those of Jensen (1969), who showed that seedling emergence distinguished only 40% of the pool of seeds while for the pick-out method the proportion ranged from 70% to 80%.
The role of the seed bank depends on the period over which seeds remain viable in the soil, although this is very difficult to determine. Observation of long-term changes in species composition of seed bank and vegetation in permanent plots (Table 1) allowed the longevity of the seeds of some species to be assessed. Comparison of the species in the seed bank and vegetation of meadows unmown for 20 years showed that seeds of some meadow species may persist in the soil until early phase forest has developed. However, some of these species become infrequent as succession proceeds (Falińska 1991) and continued production cannot explain the presence of their seeds, often in large numbers, after 20 years, suggesting that seeds must remain viable for at least 5 or 10 years. All three methods for determining the seed bank suggest that Ranunculus acris, Lychnis flos-cuculi and Myosotis scorpioides show such behaviour, as seeds were present in the soil after 15 or 20 years, in spite of an almost complete disappearance from the vegetation 10 years after mowing ceased. The longevity of seeds of these species has previously been noted (Thompson et al. 1997). The viability of Juncus effusus seeds has been estimated at several hundred years (Milberg 1990; Milberg & Hansson 1993), and many studies draw attention to the frequent appearance of this species after disturbance, even in natural communities where its presence or proximity had not been noted previously (Pirożnikow 1983). Several other species, e.g. Taraxacum officinale, Trifolium repens and Campanula patula, which have been reported to have long-term seed bank (tens of years) (Thompson et al. 1997), did not persist in the seed bank in this study (Table 3). The hypothesis that durable seed banks may be a survival strategy typical of light-demanding species assumes that the germination of seeds in the soil is obstructed by a lack of incident light (Pickett & McDonnell 1989), and that it is only when plant cover is disturbed and microhabitat conditions change that exposure and germination take place (Thompson & Grime 1979; Thompson 1992). The ecological consequence of this hypothesis is disturbance-dependent emergence of seedlings from the seed bank. While virtually all the species of genera such as Epilobium and Trifolium are capable of forming durable seed banks in some circumstances (Thompson et al. 1997), their seeds were not present here 20 years after the cessation of mowing, and as the species had disappeared from the vegetation within the first 10 years the viability of their seeds would seem not to have exceeded 10 years in this case.
Thus, the floristic composition of the seed bank at a particular time is not a mirror reflection of the vegetation at that stage of succession, but rather a record of the history of changes in the vegetation. Succession, however, depends on the varying proportions of particular groups of species in the seed bank, which play different roles at different stages in the sequence, leading to the formation of necromass, herb canopy or tree canopy.
Descriptions of seed banks in various studies show that there are at least three patterns during succession (Fig. 4). Unidirectional changes are observed in both density and species richness, corresponding with Clement’s succession model of unidirectional changes in vegetation. This pattern was described for seed banks where succession started in a weed community (Roberts & Vankat 1991). On the other hand, data from semi-natural meadows indicate that during succession the seed bank fluctuates either regularly or with variable peaks (a fluctuation–lottery pattern) as a result of both the long-term turnover of species and of various other processes that significantly affect the seed bank size as well as random events (Lavorel & Lebreton 1992). Just as there is more than one succession model (Glenn-Lewin et al. 1992) various seed bank models may be possible (Leck et al. 1989).
Many studies have indicated that a given succession may follow several different paths (Prentice 1986; Van der Maarel 1988). For instance, in various parts of a 15-ha abandoned meadow (Falińska 1991) (i) trees appeared directly without a long-term species turnover; (ii) patches of two to three herb dominants developed and after 15 years were colonized by willow and alder trees; and (iii) the floristic compositions changed according to the classical Clement’s model. The data on the seed bank described in the present paper are representative of the second path of forest regeneration in meadows. Both the course of succession and the seed bank pattern often depend on the initial situation, i.e. on the type of vegetation in which succession begins. Directional changes in species richness and density of seeds in the soil are most likely to occur in disturbed environments. On the other hand, if, as here, succession starts in semi-natural vegetation, the seed bank will probably follow a fluctuation–lottery pattern.