(Brassicaceae): Evidence from the soil seed bank and ...

Bot. Jahrb. Syst.

125

4

405–429

Stuttgart, 8. September 2004

Population dynamics of Cardamine amara L. (Brassicaceae): Evidence from the soil seed bank and aboveground populations By

Marcus Koch, Marion Huthmann and Karl-Georg Bernhardt With 5 tables

Abstract KOCH, M., HUTHMANN, M. & BERNHARDT, K.-G.: Population dynamics of Cardamine amara L. (Brassicaceae): Evidence from the soil seed bank and aboveground populations. — Bot. Jahrb. Syst. 125: 405–429. 2004. — ISSN 0006-8152. In a recently presented paper we investigated the spatial distribution of genetic diversity in a strictly outcrossing cruciferous plant species, Cardamine amara, comparing surface population with subpopulations stored as seeds in the soil seed bank using isozyme analysis. Genetically, thirty-six populations from an area of approximately 900 square kilometres were investigated in a geographically well-defined region in Northwestern Germany. For ten out of these 36 populations, detailed soil seed bank analyses have been performed. Comparisons of soil seed bank composition and aboveground vegetation have been tested to serve as indicator of the environmental dynamics influencing floristic composition of the total habitat. Herein we are presenting the original and complete soil seed bank data of the different Cardamine amara habitats and comparing them to the actual vegetation cover. In total, we recovered 142 plant species (including 3 Equisetum species and Athyrium filix-femina from the pteridophytes), of which 78 were found also in the soil seed bank (including Athyrium filix-femina). These plant species have been characterized within seven groups depending on their occurrence in the soil seed bank and/or actual vegetation. Because particular attention has been paid on environmental dynamics, we fractionated the soil samples according to their depth (0–10 and 10–20 cm) and provided the according information about seed distribution. However, in four species only seeds occurred with a significantly higher frequency in the lower soil fraction than in the upper soil layer. Keywords: aboveground vegetation, Brassicaceae, Cardamine amara, soil seed bank.

DOI: 10.1127/0006-8152/2004/0125-0405

0006-8152/04/0125-0405 $ 06.25

© 2004 E. Schweizerbart’sche Verlagsbuchhandlung, D-70176 Stuttgart

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M. Koch et al., Population dynamics of Cardamine amara L.

Introduction Phenotypic plasticity of a plant species is assumed to play a dominant role in adaptation processes in natural populations. An organism exhibits phenotypic plasticity if its morphology or anatomy or physiology depends on changes in the external environment (SCHMALHAUSEN 1949). Phenotypic plasticity is an important part of a plant’s ability to survive in a heterogeneous environment that changes spatially and temporally (BRADSHAW 1965, JAIN 1979, LLOYD 1984, WATSON & CASPER 1984). The cruciferous plant Cardamine amara is such an example of a widely distributed Central European plant species found in wet and disturbed habitats mostly influenced by water movements and regular flooding. Soil seed bank characteristics such as longevity, seed density or vertical distribution of seeds might reflect or be the consequence of such variable phenotypic characters or life traits. We initially characterized this species genetically in the context of differing and changing environments (KOCH et al. 2003) and considering individuals also stored as seeds in the soil seed bank. The most comprehensive and “up-to-date” summary on phenotypic plasticity is given in PIGLIUCCI (2001) and it is outlined that if plasticity has any ecological consequence, it has to impact organismal fitness. Here, plasticity of a particular trait influencing and increasing fitness in a particular environment can be regarded as “adaptive”. However, in a different environment this phenotypic plasticity may become “passive”. Accordingly, adaptive phenotypic plasticity is always connected with measurements and estimations of plant fitness (for details see PIGLIUCCI 2001). Changes in morphological, physiological, reproductive and life-history traits have been reported for many plant species (SCHLICHTING 1986, SULTAN 1987, 1995, PIGLIUCCI 2001), and numerous studies have compared phenotypic plasticity among wild populations of a single species (e.g. COOK & JOHNSON 1968, WILKEN 1977, KUIPER 1983, SCHEINER & GOODNIGHT 1984, WOOD & DEGABRIELE 1985, LOTZ & BLOM 1986, MACDONALD & CHINAPPA 1988, BLAIS & LECHOWICZ 1989, SCHLICHTING & LEWIN 1990, RENDON & NUNUZ-FARFAN 2001, WAHL et al. 2001, QUINN & WERTHERINGTON 2002, CALLAHAN & PIGLIUCCI 2002, PIGLIUCCI & KOLODYNSKA 2002). But there is also increasing work on the model plant of molecular biologist, Arabidopsis thaliana, taking advantage of modern molecular techniques and other resources such as availability of e.g. genetically defined strains, inbred lines, or crosses (ZHANG & LECHOWICZ 1994, PIGLIUCCI & BYRD 1998, SCHEINER & CALLAHAN 1999, CALLAHAN et al. 1999, CAMARA et al. 2000, PIGLIUCCI & SCHMITT 1999, PIGLIUCCI et al. 1999, PIGLIUCCI & MARLOW 2001, POLLARD et al. 2001). However, more recently also comparative approaches using a phylogenetic context have been introduced (PIGLIUCCI & BYRD 1998, PIGLIUCCI et al. 1999) and also molecular genetics have been considered more frequently (PIGLIUCCI & BYRD 1998, FISCHER et al. 2000). Phenotypic variation has been also analyzed in a few cruciferous plants such as the weed Raphanus raphanistrum (WILLIAMS & CONNER 2001 and references


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herein), Arabis serrata (OYAMA 1994) or Capsella bursa-pastoris (HURKA & NEUFFER 1997 and references therein). However, there is only limited knowledge about the importance of the soil seed bank and its function as resource of well-adapted individuals to changing environmental conditions compared to its actual aboveground subpopulations (e.g. KOCH et al. 2003). Analysis of phenotypic plasticity of the soil seed bank is mostly restricted to dormancy and germination phenomena (BASKIN & BASKIN 1995), or seed bank populations have been analyzed without comparisons with its actual aboveground population. The soil seed bank and its genetic diversity are of great importance. Seed banks are widely recognized as reservoirs of potentially large amounts of genetic variability in plant populations (TEMPLETON & LEVIN 1979, BROWN & VENABLE 1986, MCGRAW 1987, BAKER 1989, MCGRAW & VAVREK 1989, SIMPSON et at. 1989). This variability, while hidden at any one time, could have profound consequences for the persistence and evolutionary response of populations over long periods (MCGRAW et al. 1991). The soil seed bank consists of diaspores and represents a multidimensional genetical reservoir (in space and time). Therefore the soil seed bank should contribute to a greater extent to the overall genetic variation of a particular species depending on the amount of diaspores which are present. In investigations of the soil seed bank from habitats such as cultivated land it has been demonstrated that the total phenotypic variation of single species and its populations is “stored” within the soil seed bank (BERNHARDT & HURKA 1989, BERNHARDT 1995, GÜNTER 1997, HURKA & HAASE 1982), and this is especially true for weeds and pioneer species, which tend to have a long-term persistent diaspore bank (THOMPSON et al. 1997). Knowledge about the population genetics and population dynamics also contributed to a better understanding of adaptive strategies of plant populations. Great efforts have been undertaken to understand the genetics and dynamics of populations of numerous plant species. As outlined above, the majority of these investigations did not consider the genetic diversity stored in the soil seed bank. But depending on the type of the soil seed bank and the reproductive biology of the selected species, the seed bank of a particular population is an essential resource for the recruitment and establishment of a new generation. Depending on the spatial genetic structure of the subpopulations (aboveground population and belowground population stored as seeds or other diaspores) major changes in the genetic constitution of plant populations may occur during their history, either by random environmental changes and disturbances, by selection or through processes such as changes in the breeding system with temporary variations in outcrossing rates. Such changes in the genetic constitution of a particular population might have a significant impact on the survival potential of the total population in a long-term perspective (COHEN 1966, KALISZ & MCPEEK 1992). A seed bank could serve as a genetic buffer that increases effective population size. It has been shown for some species that the processes of population size

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decrease, genetic erosion and process of extinction are highly correlated (VAN TREUREN et al. 1991, OSTERMEIJER et al. 1994, FISCHER & MATTHIES 1998). The seed bank also functions as a “genetic memory”, as viable seeds stored in the soil seed bank represent offspring from former established and adapted plants. Depending on seed longevitiy these seed reservoirs may store the genetic information necessary to follow environmental changes to maintain genetic homogeneity and population viability (FRANKEL & SOULÉ 1981, VRIJENHOEK 1994). Via seed dispersal over larger distances, the soil seed bank can also serve as reservoir for genotypes not present in the aboveground population, and therefore might serve as a source of genetic novelty (OUBORG et al. 1999). In summary, the soil seed bank not only reduces the rate of genetic erosion (e.g. via genetic drift), but also may compensate environmental changes in space and time. It can be expected that genetic structure in aboveground plant populations is nonrandomly distributed, the result of mating system, diaspore propogation, clonal growth, migration and selection. And, moreover, it has been shown that within a population, changing mixed-mating system, varying from year to year, are possible (e.g. HURKA & NEUFFER 1997). These assumptions demonstrate the necessity to include the subpopulation from the soil seed bank into population studies. However, despite the potentially significant genetic impacts of seed banks, only a few investigations directly examined the genetic diversity of aboveground populations versus the genetic diversity stored in the soil seed bank (HURKA & HAASE 1982, TONSOR et al. 1993, ALVAREZ-BUYLLA & GARAY 1994, CABIN 1996, MCCUE & HOLTSFORD 1998, MAHY et al. 1999, KOCH et al. 2003). These investigations should have greater impact on our current view of plant populations. MCCUE & HOLTSFORD (1998) have shown that the enlarged effective population size (Ne) has great influence on expected inbreeding coefficients. Analysis of Calluna vulgaris indicated that the seed bank preserves genetic diversity at a very local scale (MAHY et al. 1999), and CABIN (1996) discussed microselective forces to explain local-scale differentiation in Lesquerella fendleri. These studies suggest that the aboveground population system represents a nonrandom genetic subset of the underlying seed bank. The results from our previous work on Cardamine amara (KOCH et al. 2003) can be summarized as follow: (1) Desite the possibility of clonal growth and vegetative propagation, the outcrossing mating system maintain high level of genetic variation within a population. (2) Accordingly, dispersal of vegetative plant units seems to play a minor role during colonization and population establishment. (3) Data from JANIESCH et al. [1991, recalculated and cited in THOMPSON et al. (1997)] favouring the establishment of a long-term persistent seed bank type, with seeds persisting in the soil for at least five years [for definition see THOMPSON et al. (1997)], have been substaintiated. (4) Genetic variation of seed bank populations from different depths differs significantly from each other, depending on continuous seed rain and soil movement caused by water dynamics. (5) All subpopulations were rather unbiased in expected versus observed mean het-


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erozygosity — however, in wet woodland populations FIS decreased from seedling to surface populations thus indicating a trend of increasing heterozygosity. (6) In conclusion, it has been demonstrated that established C. amara populations do not represent simple genetic subsets of the underlying seed banks. In this study we present the primary soil seed bank data of diploid, permanent outcrossing, perennial Cardamine amara and all plant species co-occurring at the habitats under study. Cardamine amara is propagating vegetatively via rhizomes and migration of clonal units is possible. Extreme variation in population size is possible, and thus there is a high chance for complete extinction of the surface population through catastrophic events. However, a permanent soil seed bank (THOMPSON et al. 1997, KOCH et al. 2003) is built up, and is influenced by the relative movement of the top soil layers. Our objectives in this study were to present and discuss the soil seed bank data of the total vegetation from the previously analysed study sites (KOCH et al. 2003) and compare both datasets. Initially, the study had been initiated to test if C. amara could serve as a key species to monitor restoration efforts in the upper Hase river system (Lower Saxony, Germany) and its headwater. This species is a typical element of several vegetation types associated with springs, creek and river bank, and wet meadows, and therefore might mirror inreasing environmental dynamics (mostly flooding), one of the central aims of restoration efforts (BERNHARDT 1996). The Hase river system has been greatly influenced by human activities. Major parts of the river itself and also adjacent creeks have been regulated and canalised. Several springs in the area of the headwaters have been enclosed, with water from upper parts of the creeks used for fishery, to result in the degradation of wet woodland alder forests. Wet meadows along the river system have been drained and transformed into intensively used meadows and arable fields. However, in the last few years major efforts have been undertaken to “restore” the Hase river system and to establish a more natural situation.

Material and methods Investigation sites We investigated ten sites with C. amara populations differing in habitat dynamics, floristic composition and total population size. All sites have been selected for total soil seed bank analysis because of high abundance of C. amara. Characterization and enumeration of study sites follow KOCH et al. (2003) and is indicated in Table 1. The investigation area is located between two hill ranges in Northwest Germany, the Teutoburger Wald in the South and the Wiehengebirge in the North with Osnabrück in its centre (refer to Fig. 1 in KOCH et al. 2003). The lowland between the two hill ranges is fed by the Hase river in SE-NW direction, with most creeks and small streams draining directly or indirectly into the Hase river. The populations investigated are a subset of populations from a large scale genetic analysis covering an area of approximately 900 km² (KOCH et al. 2003).

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Table 1. Characterization of the sampling sites. The enumeration of populations investigated follows KOCH et al. (2003). All accessions were collected by KOCH & HUTHMANN. origin of population

height above population area [m²] habitat type sea level [m] of Cardamine amara

1 Sudenfeld-Holperdorp, 135 Hagen a.T.W. 2 Retention bassin, 80 Hagen a.T.W. 3 Im Grund, Hagen a.T.W. 105 4 Tecklenburg 175 5 Hasbergen-Gaste, Goldbach 68 6 Westerbeck, Westerkappeln 60 7 Gut Sandfort, Osnabrück 95 8 Nemden, Hase 75 9 Ostercappeln 65 10 Hitzhausen 65

1500 200 1000 100 20 20 10 20 5000 20

wet woodland retention bassin, pioneer vegetation wet woodland wet woodland creek bank wet woodland creek bank river bank wet woodland wet meadow

Soil seed bank analysis The Cardamine amara stands selected for soil seed bank investigations showed different floristic characteristics (Table 1). However, at all sites C. amara contributed more than 5%, and in eight out of ten cases between 25 and 100% to the actual vegetation cover. These stands are characterized by different habitat dynamics as influenced by flooding or agricultural activities (decreasing dynamic environmental influence: retention bassin > river and creek banks > wet meadow > wet woodland, refer to KOCH et al. 2003). From each site two study plots (4 m² in size) were established with a minimum distance of 5 m from each other, and 20 soil samples from each plot were collected using a 5 cm diameter core to 20 cm depth during January and February 2000. The soil samples were divided into two fractions (0–10 cm, 10–20 cm) representing a total soil volume of 4000 cm³ per fraction and plot. The samples were processed by hand to remove all vegetative parts which might resprout, and thoroughly mixed to form a bulk sample prior to the subsequent semi-automatic concentration procedure. The concentration procedure was performed with a sieving machine (RETSCH AS200 digit) using sieves of different mesh width (4 mm, 2 mm, 1 mm, 0.8 mm, 0.5 mm, 0.2 mm, 0.1 mm) and continuous cold water rinsing during the sieving procedure. The concentrated soil samples were laid out over sterilised soil in plastic trays and exposed to natural temperature conditions from February 2000 until December 2000. Emerging seedlings of all species were counted and removed on a weekly basis. Unidentifiable seedlings were transplanted into separate pots and grown until identification was possible. The seed bank results are presented as total number of seedlings characterized or as seedling densities (seedling/m²) for each study site (Tables 2 and 3).


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Analysis of the actual vegetation The total actual vegetation was classified using the method according to BRAUN-BLAN(1964) using data collected in May and August 2000. The botanical nomenclature of taxa follows WISSKIRCHEN & HAEUPLER (1998). QUET

Vegetation data analysis The relation between seed bank and aboveground vegetation of the ten selected study sites was determined using the Sörensen index (SÖRENSEN 1948): S = 2c/(a + b + 2c) where: a is the number of species present only in the aboveground vegetation, b is the number of species present only in the seed bank and c is the number of species present both in the aboveground vegetation and the seed bank. Because soil samples were taken during the winter season, we computed an additional SÖRENSEN index to exclude those species from the analysis which have been shown to build up no soil seed bank at all (data compilation in THOMPSON et al. 1997).

Results and discussion Soil seed bank and actual vegetation The ten study sites were grouped into four categories: a) wet meadow (site 10), b) river and creek banks (sites 5, 7, 8), c) retention bassin (site 2), and d) wet woodland (sites 1, 3, 4, 6, 9). The soil seed bank data are summarized in Table 2 under consideration of the species composition of the actual vegetation, with distinction between seedling origin from the two soil depths (0–10 cm and 10–20 cm). A total of 78 species germinating from the soil samples during the investigation period have been characterized in detail. The frequency of occurrence of a particular species in the soil seed bank varied greatly (Table 3). Soil seed bank density varied from 19900 seedling/m² (site 3) to 89 000 seedlings/m² (site 9) (Table 3), and four species, Urtica dioica, Cardamine amara, Juncus effusus and Veronica beccabunga dominated the soil seed bank and contributed to more than 50% of all seedlings. Seedlings of 27 species were present only in the seed bank (group 1, Table 4). Another 33 species were present at least at some study sites only in the seed bank, while they were also present in the aboveground vegetation on other permanent plots (groups 2, 3 und 4 in Table 4). All 60 species built up (at least short-term) persistent seed banks. Seedlings of 17 species occurred only in the seed bank, when they were also present in the aboveground vegetation (groups 5 and 6 in Table 4). Both these species and another 64 species occurred only in the aboveground vegetation (group 7 in Table 4), built up a transient seed bank. Only a few species (group 5 in Table 4) are found both in the soil seed bank and always in the actual vegetation. From these seven species, only C. amara and Urtica dioica occurred at all ten study sites. In contrast to the remaining

Table 2. Distribution of the total numbers of seeds isolated from soil samples from two different depths (A: 0–10 cm; B: 10–20 cm). The enumeration of sample sites follows Table 1 and has been consistently used within the manuscript and is in congruence with the enumeration used in KOCH et al. (2003). # species that showed an at least two-times higher number of seeds from soil fraction B than from fraction A.

412 M. Koch et al., Population dynamics of Cardamine amara L.


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Table 2. (cont.)

414



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species of group 5 and 6, both species are thought to have built up a persistent seed bank through the vertical distribution of seeds (Tables 2 and 3). In our case these two species also differentiate the four different selected vegetation types. Highest seedling numbers (C. amara plus U.dioica) were found at wet woodland sites (mean 28480 seedling/m², SD 13600), whereas the wet meadow (6800 seedling/m²), retention bassin (200 seedlings/m²) and the river and creek banks (9700 seedlings/m², SD 2300) show lower numbers. Considering different soil depth (Table 3), C. amara seeds are not present in the top 10 cm soil layer at population sample sites from the retention bassin and from two out of the three sites located at river or creek banks. Habitat dynamics are slightly reflected when total soil seed bank and actual vegetation were compared using the SÖRENSEN index (Table 5a and 5b) with highest values found for the wet meadow (0.513) and the retention bassin (0.456). Lower similarities between aboveground vegetation and soil seed bank have been found for river banks (mean 0.358) and wet woodland (mean 0.396). These results correlate with our initial assumptions on different degrees of environmental dynamics primarily caused by water flooding (depending on intensity and frequency): river and creek banks > wet woodland > retention bassin > wet meadow. For comparison, the SÖRENSEN indices in our study are lower than in studies from other wet meadows not highly influenced by regular flooding. For example, JENSEN (1998) estimated a mean SÖRENSEN index of 0.72 (SD 0.05) for wet meadow habitats. Our soil seed bank data (Table 4) are consistent with other comparisons of plant species seed bank types (compiled in THOMPSON et al. 1997). In all groups in which seeds occur only in the seedbank (either permanent or at particular sites) these groups consist of a high amount of species building up a permanent soil seed bank. This is true for group 1 (for 73% of the species are known that they can build up a permanent soil seed bank), group 2 (75%), group 3 (86%) and group 4 (80%). In group 5 and group 6 seeds are only present in the seed bank if they are occurring simultaneously in the actual vegetation, consequently only 67% and 60% of the species, respectively, are known for a permanent seed bank. Species which we have listed in group 7 occurred only in the actual vegetation, and, compared to the compiled data of THOMPSON et al. (1997) only 40% of them have been reported to build up a permanent seed bank. If we calculate the same numbers of species building up permanent seed banks and differentiate the different habitats, the seed bank from wet woodland sites contains 70% (SD 10.4%) plant species potentially building up a permanent soil seed bank, whereas the remaining habitats contain 81.6% (SD 2.2%) species in the soil seed bank building up a permanent soil seed bank. The difference is not significant. Similar results are obtained when total soil seed bank densities were compared: wet woodland sites with 51540 seedlings/m² (SD 22824) versus remaining sites with 44980 seedlings/m² (SD 19454). However, results obtained from a neighbour-joining tree calculated from pairwise distances demonstrate close grouping of wet woodland data samples

Table 3. Total number of seeds isolated from the different sample sites. Seed numbers have been re-calculated as [number of seeds/m²]. Species are grouped according to their frequency of occurrence among the 10 study sides considering both fractions of the soil seed bank (0–10 cm; 10–20 cm) and total number of seeds.



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Table 3. (cont.)

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419

(soil seed bank and actual vegetation, respectively), indicating a significant similarity within each of these groups (refer to Fig. 3 in KOCH et al. 2003). Little is known about the population dynamics of Cardamine amara. Some evidence came from a phylogenetic-systematic study at Urner Boden in Switzerland (URBANSKA et al. 1997). Here C. amara consistently occurred in wet to partly flooded sites characterized by flowing water. Wood clearings and the installation of new man-made habitats have enforced hybrid speciation between other Cardamine species (URBANSKA et al. 1997), and this might be regarded as a first indicator of dynamic population structure in terms of range and genetic fluctuation (within and even between species). There is only one report for the soil seed bank type (JANIESCH et al. 1991), describing a permanent soil seed bank with a density of 570 seeds/m² (reviewed in THOMPSON et al. 1997). This study was performed in vegetation types similar to our wet woodland sites (alder forests) sampled in our study. At our wet woodland study sites with minor environmental disturbances there are no major fluctuations in population size, and in spring C. amara often covers more than 75% of the total area. In these habitats one could assume more extensive clonal propagation on a local scale relative to highly disturbed habitats such as river banks. This is indeed the case when one considers the trend of heterozygosity excess in surface populations (KOCH et al. 2003, Tables 5 and 6), which might be best explained by vegetative propagation biasing the HARDY-WEINBERG equilibrium of a permanent outcrossing population. More regularly occurring species with permanent seed banks are often annual, early successional taxa. These characteristics do not match C. amara, although it builds up an extensive seed bank at the wet woodland sites under study, which are likely of long- to short-term persistence. BAKKER et al. (1996) provided a dichotomous key to evaluate seed bank types. Considering the seed bank types as defined by BAKKER et al. (1996), it is apparent that soil layers are subdivided by depth for several populations which frequently have higher seed frequencies in the upper layer (Tab. 2). In other cases (highly disturbed habitats) seeds are missing in the first layer, but are present with low numbers (compared to wet woodland sites) in lower soil layers. While nothing is known regarding the “clonal part” of the population, the total diaspore bank (seeds plus vegetative propagules) should be regarded as genetic resource for the surface population. We totally removed vegetative parts of the population from the soil samples prior to analysis to avoid biases in the seed bank data. Our analysis is thus biased by sampling.

Seed bank demography Some authors assume that dispersal via water is an important determinant of plant distribution and abundance on flood plains (NILSSON et al. 1994, JOHANNSSON et al. 1996, BERNHARDT 1996). Most studies also indicate that

Table 4. Aboveground vegetation (AV: abundance according to BRAUN-BLANQUET 1964) and seed bank density (SB: seedlings/m²) of the ten study sites (refer to Table 1). Species were grouped according to their presence/absence in the aboveground vegetation and in the seed bank. Vegetation types are as follows: wet meadow (pop. no. 10), creek or river banks (pop. nos. 7, 5, 8). wet woodland (pop. nos. 4, 6, 9, 3, 1), retention bassin (pop. no. 2).



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Table 4. (cont.)

422



423

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Table 5a. Sörensen index [Si = 2c/(a + b + 2c); with a: number of species in the aboveground vegetation, b: number of species in the soil seed bank, c: number of species occurring in the aboveground vegetation and in the soil seed bank]. For these calculations only those species have been considered, which have been described to build up at least a transient soil seed bank (data compilation according to THOMPSON et al. 1997). Sampling site SB 10 SB 7

SB 5

SB 8

SB 4

SB 6

SB 9

SB 3

SB 1

SB 2

AV AV AV AV AV AV AV AV AV AV

0.410 0.339 0.383 0.366 0.204 0.321 0.262 0.140 0.214 0.269

0.254 0.182 0.178 0.414 0.118 0.146 0.130 0.095 0.195 0.108

0.295 0.333 0.233 0.333 0.363 0.205 0.227 0.300 0.256 0.286

0.494 0.364 0.328 0.410 0.214 0.443 0.235 0.188 0.254 0.305

0.344 0.311 0.261 0.316 0.229 0.286 0.491 0.326 0.381 0.263

0.262 0.381 0.233 0.259 0.250 0.205 0.182 0.390 0.308 0.229

0.424 0.383 0.333 0.475 0.324 0.409 0.408 0.311 0.394 0.350

0.466 0.407 0.400 0.303 0.227 0.353 0.321 0.269 0.353 0.470

10 7 5 8 4 6 9 3 1 2

0.526 0.386 0.276 0.261 0.170 0.370 0.271 0.182 0.148 0.280

0.480 0.339 0.351 0.441 0.217 0.302 0.172 0.185 0.189 0.245

Table 5b. Sörensen index [Si = 2c/(a + b + 2c); with a: number of species in the aboveground vegetation, b: number of species in the soil seed bank, c: number of species occurring in the aboveground vegetation and in the soil seed bank]. For these calculations all species have been considered. Sampling site 10

7

5

8

4

6

9

3

1

2

Sörensen index 0.513 0.325 0.363 0.394 0.350 0.425 0.472 0.378 0.373 0.456

aquatic dispersal is just one among many other properties which enable survival in the different semiaquatic environments of flood plains, including: high regenerative potentials, plasticity of life cycles, suitability for wind dispersal, production of a high number of viable seeds (Cardamine amara), high germination rate and rapid formation of seed banks (BILL et al. 1999). Some species are able to change their ability to form a short- or long-term persistent seed bank. This is the case for Juncus bufonius (BERNHARDT 1993) demonstrating phenotypic plasticity even on the level of seed bank type establishment. This is furthermore obvious from compiled literature data, as many taxa have been reported with different seed bank types (Table 4, seed bank type definition according to the compiled data of THOMPSON et al. 1997). It is not surprising that at least some species which we have found have been reported with different seed bank types: Epilobium roseum occurred regularly in our investigated seed banks but is nearly completely missing in the actual vegetation. This species may therefore constitute at least a short-term persistent seed bank, although


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only transient seed banks have been described so far. Similar results were also obtained for Lycopus europaeus. One could argue that habitats exposed to high levels of environmental variability caused by flooding, e. g. gravel banks in flood plains, exhibit significantly lower seed densities in the soil seed bank (SKOGLUND 1990, BILL et al. 1999) relative to those exposed to less dynamically influenced habitats. The influence of seed dispersal via water is reduced (BRUGBAUER & BERNHARDT 1991, NILSSON 1997, PARKER & LECK 1985). Moreover, one could speculate that genetic variation provided on the population level enables plants to switch between different soil seed bank strategies depending on environmental conditions, similar to phenotypic plasticity in life history traits (HURKA & NEUFFER 1991, WALKER et al. 1986). Interestingly, our data do not support this idea on a broad scale. We did not find significantly more seeds in the total soil seed bank from wet woodland sites compared to the remaining sites, and even the percentage of species which potentially build up permanent soil seed banks do not increase. In addition, despite high environmental dynamics we also found only four species (Carex acutiformis, Poa palustre, Ranunculus sceleratus, Veronica beccabunga) with a highly significant increased number of seeds in the lower soil seed layer (10–20 cm). The reason for this is unknown. The most likely explanantion for this might be that the plasticity of seed banks and seed bank types is too great to be significantly reflected in the number of sample sites investigated herein. This is supported by soil seed bank analysis of wet meadows (JENSEN 1998). The mean total seedling density of 65396 seedlings/m², SD 35367, (recalculated from Table 2 in JENSEN 1998) is comparable to the value for investigation site 10 (wet medow) with 69000 seedlings/m². However, the variance of 35367 seedlings is remarkable and demonstrates the plasticity of the system. In the case of C. amara the observed patterns of seed number distribution (Table 2) follow the expectations, and we therefore conclude that population biology of this species is greatly affected by differing environmental changes caused by water dynamics. Acknowledgments Thanks go to DANIEL LAUBHANN for experimental support in the greenhouse.

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