Ecological Significance of Seed Germination Characteristics in Flood-Meadow Species

Flora 199, 12–24 (2004) http://www.elsevier-deutschland.de/flora

Ecological significance of seed germination characteristics in flood-meadow species

Norbert Hölzel* & Annette Otte

Department of Landscape Ecology and Resources Management, Justus Liebig University Giessen, Heinrich-Buff-Ring 26–32, D-35392 Giessen, Germany

Submitted: May 27, 2003 · Accepted: Oct 2, 2003

Summary

In climate chamber and outdoor experiments we analysed germination traits of 42 vascular plant species typical of flood- meadows of the alliance Cnidion. In Central Europe such flood-meadows and their highly endangered character species are confined to large lowland river corridors with a dry and warm climate. Due to the prevailing ecological conditions, particularly the extremely high variability in soil moisture potential, it was hypothesised that flood-meadow species exhibit specific strategies in terms of germination phenology, temperature requirements and primary dormancy to avoid constraints on seedling recruitment imposed by flooding, drought and competition from established vegetation. Furthermore, we expected that germination characteristics could be a key for the causal understanding of range size, confinement to large river corridors, recent rarification processes, seed bank persistence and establishment success in restoration projects. PCA ordination of germination traits reflected a continuous gradient of increasing primary dormancy levels ranging from species with a high capacity for fast and almost complete germination over a wide range of temperatures to those with high and narrow temperature requirements and/or a delayed and asynchronous emergence. Many of the studied species germinated only at relatively high temperature in the year of shedding, but the primary conditional dormancy disappeared in most cases after a period of cold wet stratification. Requirements for chilling and/or high germination temperature were revealed to be the most common strategies for avoidance of harmful autumn and winter germination. The majority of the studied species tends to exploit particularly favourable regeneration niches in early spring. Surprisingly, many species with large long-term persistent soil seed banks exhibited relatively low dormancy levels in light; this was correlated with small seed size and a consequent higher probability of burial. We found no relationship between germination characteristics and river corridor confinement or Central Euro- pean range size. However, there was a significant trend in endangered species towards higher temperature requirements and delayed, asynchronous germination. This is presumably disadvantageous under the environmental conditions of subcontinental flood-meadows.

Key words: Dormancy, germination temperature requirements, grassland restoration, principal component analysis, seed bank, stratification

Introduction Zeiter 1999). Recruitment from seeds is often strongly hampered or even condemned to failure through compe- The temporal and spatial limitation of the “regeneration tition by established vegetation (Rusch & Fernández- niche” (Grubb 1977) has been increasingly identified as Palacios 1995; Kotorová & Lepsˇ 1999; Touzard one of the most critical constraints in the life-cycle of et al. 2002) as well as unfavourable environmental con- plant populations, and is a factor that may severely re- ditions such as frost and drought (Silvertown & duce diversity in plant communities (e. g. Stampfli & Dickie 1980; Ryser 1993). Consequently, successful

* Corresponding author: Department of Landscape Ecology and Resources Management, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany; e-mail: [email protected]

12 FLORA (2004) 199 0367-2530/04/199/01-012 $ 30.00/0 germination and seedling establishment in a given spe- cialised eastern species that are uncommon in Central cies will often depend on its ability to avoid or mini- Europe and close to the western limit of their range, such mize such constraints. Numerous previous studies have as Allium angulosum, Cnidium dubium, Scutellaria shown that seeds of many species boast the aptitude to hastifolia and Viola pumila (Hultén & Fries 1988). identify suitable conditions for seedling recruitment Ecologically these flood-meadows are characterized by (Grime 2001). Narrow temperature requirements, dor- an extremely high variability in soil water potential mancy cycles induced or broken by temperature fluc- (Burkart 1998; Leyer 2002). Whereas winter, spring tuations, warm or cold stratification, as well as other and early summer may often bring floods summers are environmental factors, such as fire or nitrate concentra- markedly dry and rapidly hardening clay soils are com- tions, are all mechanisms that regulate the onset of ger- mon (Dister 1980; Hölzel 1999). Thus, successful mination and help in detection of favourable micro-sites seedling recruitment may be hampered by flooding as with low competition (Thompson et al. 1977; Grime et well as by drought (Hölzel & Otte 2003a) and there al. 1981; Baskin & Baskin 2001; Hroudová & is only a relatively narrow time window with favourable Zákravsky 2003). Such dormancy breaking mecha- germination conditions. nisms were revealed to be of particular importance in In the present study, we investigated if there is a spe- species typical of temperate wet grasslands (e.g. Mil- cific response in germination characteristics of the typi- berg 1994; Schütz 1997; Knödler 2001; Jensen cal flora of flood-meadows to these particular ecologi- 2001). cal conditions. Furthermore, we attempted to assess Germination characteristics may play an equally whether germination characteristics can provide an important role in the formation of persistent soil seed explanation for the strict confinement of many charac- banks. Seeds exhibiting conditional or strict dormancy ter species to large river corridors with subcontinental (Baskin & Baskin 2001) are more likely to be buried climatic conditions. According to their Central Euro- and to establish large persistent reservoirs in the soil pean distribution pattern, it is postulated that characteri- (Thompson et al. 1993; Grime 2001). Seed regenera- stic flood-meadow species tend to have high tempera- tion strategies are now considered as a key for the cau- ture requirements for germination. sal understanding of the decline, persistence or spread of The study was carried out in the framework of a lar- species in changing landscapes (e. g. Schütz 2000b). ge-scale restoration project aimed at the re-establish- Information on germination characteristics is also ment of species-rich flood-meadows on ex-arable land particularly relevant for habitat restoration, in which by the transfer of diaspores with plant material from species-enrichment largely depends on re-establishment remnant stands (Hölzel & Harnisch 2002; Hölzel & by artificially introduced or naturally dispersed seeds Otte 2003). It is often claimed (e.g. Patzelt 1998; (e. g. Bakker & Berendse 1999; Patzelt et al. 2001). Schütz 2000b) that declining, rare and endangered By the creation of suitable regeneration niches at the species tend to have detrimental germination require- right time of the year, management schemes may posi- ments. Thus, we expected that germination traits could tively influence germination and the subsequent fate of be a key to detect the underlying mechanisms of suc- seedlings (Olff et al. 1994; Kotorová & Lepsˇ 1999; cessful or failing re-establishment of target species as Schütz 2000b). If seeds of target species are intro- well as for the optimisation of restoration measures. duced artificially, information on germination phenology, dormancy, response to storage and pre-treatments are essential to increase the likelihood of seeding success (Keller & Kollmann 1999; Budelsky & Gala- 2Material and Methods towitsch 1999). However, knowledge on germination characteristics is still extremely scarce particularly in 2.1 Study species rare and endangered species targeted for conservation and there are a great variety of possible response types Seeds of 42 species were collected in bulk from autochthonous (e.g. Baskin & Baskin 2001). This also applies to de- populations in flood-meadows along the northern Upper Rhi- clining and endangered species-rich flood-meadows of ne River, Germany, between the tributaries Neckar to the south the alliance Cnidion that include a large number of rare and Main to the north. Seed sampling took place between May plant species of Central European conservation concern and October depending on the time of ripening and included at (Schnittler & Günther 1999; Hölzel et al. 2002). least 50 different plant individuals. The species studied com- prise typical constituents of subcontinental flood-meadows, In their Central European distribution these alluvial representing a broad variety of families, life forms and strategy grasslands are strictly confined to large river corridors types (Table 1). Besides character species, which are more or with dry and warm subcontinental climatic conditions less confined to large lowland river corridors such as Allium (Korsch 1999; Burkart 2001). This distribution pat- angulosum, Arabis nemorensis, Cnidium dubium, Iris spuria, tern is reflected by the occurrence of many highly spe- Scutellaria hastifolia and Viola pumila (Burkart 2001) we

FLORA (2004) 199 13 Table 1. Traits of the studied species according to the following authors: Life form (Ellenberg et al. 1992), seed mass (Hölzel & Otte 2003/4a), river corridor area (Korsch 1999 and Burkart 2001), German Red List status (Korneck et al. 1996). Letters in bold indicate abbreviations for species names used in following tables and figures. Life forms: T = Therophyte, G = Geophyte, H = Hemicryptophyte. Confinement to river corridors: ++ strong, + weak, - none. Red List status: 1 = critically endangered, 2 = endangered, 3 = vulnerable, - = not threatened. Species Family Life Seed mass River Red form (mg) corridor List

Allium angulosum Liliaceae G 1.74 ++ 3 Alopecurus pratensis Poaceae H 0.71 – – Althaea officinalis Malvaceae H 3.41 + 3 Arabis nemorensis Brassicaceae H 0.06 ++ 2 Barbarea stricta Brassicaceae H 0.41 ++ – Cardamine parviflora Brassicaceae T 0.07 ++ 3 Carex praecox Cyperaceae H 0.16 + 3 Carex spicata Cyperaceae H 3.34 – – Carex tomentosa Cyperaceae H 1.44 – 3 Cerastium dubium Caryophyllaceae T 0.11 ++ 3 Cirsium tuberosum Asteraceae H 2.27 – 3 Cnidium dubium Apiaceae H 0.39 ++ 2 Elymus repens Poaceae H 4.50 – – Euphorbia palustris Euphorbiaceae H 10.47 ++ 3 Festuca arundinacea Poaceae H 3.16 – – Galium boreale Rubiaceae H 0.68 – – Galium wirtgenii Rubiaceae H 0.40 + – Inula britannica Asteraceae H 0.09 ++ – Inula salicina Asteraceae H 0.16 – – Iris spuria Liliaceae G 14.62 ++ 2 Lathyrus palustris Fabaceae H 12.85 + 3 Lythrum salicaria Lythraceae H 0.06 – – Peucedanum officinale Apiaceae H 12.32 + 3 Poa angustifolia Poaceae H 0.21 – – Potentilla reptans Rosaceae H 0.31 – – Pseudolysimachion longifolium Scrophulariaceae H 0.05 ++ 3 Pulicaria dysenterica Asteraceae H 0.04 – – Rumex thyrsiflorus Polygonaceae H 0.54 + – Sanguisorba officinalis Rosaceae H 1.95 – – Scutellaria hastifolia Lamiaceae H 0.68 ++ 2 Selinum carvifolia Apiaceae H 1.06 – – Senecio paludosus Asteraceae H 0.62 ++ 3 Serratula tinctoria Asteraceae H 1.26 – 3 Silaum silaus Apiaceae H 2.43 – – Symphytum officinale Boraginaceae H 3.65 – – Thalictrum flavum Ranunculaceae H 0.80 ++ – Valeriana pratensis Valerianaceae H 0.62 ++ – Veronica peregrina Scrophulariaceae T 0.06 + – Veronica serpyllifolia Scrophulariaceae H 0.05 – – Viola elatior Violaceae H 1.80 ++ 2 Viola persicifolia Violaceae H 0.68 ++ 2 Viola pumila Violaceae H 1.08 ++ 2 also studied more common and widespread components like 2.2 Experiment 1 Festuca arundinacea, Potentilla reptans, Rumex thyrsiflorus, Symphytum officinale and Veronica serpyllifolia. The study covers almost the entire spectrum of regionally rare and After field collection seeds of the 40 species used in this expe- endangered target species of flood-meadows (Korneck et al. riment were stored dry in darkness at room temperature (ca. 1996). Plant nomenclature follows Wisskirchen & Haeup- 20°C) until further use during the following winter season. ler (1998). The germination experiments were performed by spreading 50

14 FLORA (2004) 199 seeds of each species on a double layer of filter paper in steri- To describe germination characteristics for each species the le Petri dishes. In case of very large seeds only 25 seeds per following values were calculated: dish were used. Five dishes per treatment were incubated in LOPT, the optimal temperature for germination, was calcula- climate chambers at constant temperatures of 3, 7, 10, 15, 20, ted as weighted average of germination rates over all constant 25, 30, and 35°C and in a further chamber with diurnally fluc- temperatures in the climate chamber experiment, according to tuating temperatures 5/15 °C (8/16 hours). The latter tempe- the mode described by Olff et al. (1994): [(3 P3 + 7 P7 + rature regime was also applied to seeds that received cold wet 10 P10 + 15 P15 + 20 P20 + 25 P25 + 30 P30 + 35 P35)/(P3 + P7 + stratification at 3°C for 8 weeks prior the incubation, which P10 + P15 + P20 + P25 + P30 + P35)] in which P3 was percen- should mimic early spring germination conditions. The light tage germination at 3°C, P7 percentage germination at 7°C, regime in the climate chambers simulated long day conditions and so on. with 16 hours of light and 8 hours of darkness. The dishes were LMAX, the maximum germination rate, was defined as the regularly watered with distilled water to optimise moisture highest percentage of germination in one of the climate cham- conditions. The experiment lasted 6 weeks. Germinated seeds ber treatments after six weeks. were counted and removed once every week. Germination was GFAS was the maximum germination rate at constant tempe- defined as the emergence of the radicule. rature after 7 days in the climate chamber. TFAS was the temperature at which GFAS was reached. LOW was the lowest constant temperature with at least 5% 2.3 Experiment 2 germination. HIGH was the highest constant temperature with at least 5% Results obtained in climate chambers are often strongly diver- germination. gent from those set up in outdoor germination experiments, AMP was the range in degrees Kelvin between HIGH and and certain species may even completely fail to germinate LOW. under laboratory treatments (e. g. Grime et al. 1981; Patzelt ALT was the difference in germination rate at fluctuating tem- 1998). Thus, we combined both approaches in order to investi- peratures of 5/15°C in comparison to the constant tempera- gate germination phenology under more natural conditions. ture of 15°C. A total of 800 seeds of each species were sown in February STRAT, the effect of cold wet stratification, was the differen- into two Styrofoam basins (18 cm × 28 cm) filled with sterile ce in germination rate in comparison with ALT. garden soil and exposed at an experimental field near Giessen, FMAX was the maximum germination rate under outdoor con- Germany. During dry periods the basins were watered daily. ditions. Emerging seedlings were counted and removed at least every ONSET was the date of outdoor germination begin in days two weeks. The outdoor study was continued for 24 months. with daily averages above 5°C counted from the last day with a daily average below 1°C. FOPT was the date of the first germination peak under outdoor conditions (measured as for ONSET). 2.4 Experiment 3 PEAK1 was the maximum germination during one single To investigate primary dormancy levels (Baskin & Baskin count as a percentage of total final outdoor germination. 2001) and the timing of germination under near natural condi- PEAK4 was the maximum germination during the four fol- tions, seeds from a subset of 20 species were collected at the lowing weeks, measured as for PEAK1. time of shedding in the field and exposed about 2 weeks later SPAN was the period in days between the first and last count, under outdoor conditions. The mode of exposure and counting in which at least 5% of total final outdoor germination occur- was principally the same as in experiment 2. In contrast to red. natural field conditions the 800 sown seeds were watered regularly during dry periods. 2.6 Data analysis The correlation structure of germination traits was investi- 2.5 Characterisation of germination gated by principal component analysis (PCA) on a data matrix with z-transformed standardised variable values (Legendre For each laboratory and outdoor treatment, the percentage of & Legendre 1998). The traits LOPT, TFAS, HIGH and LOW seeds that had germinated after the end of the observation peri- were not included in the analysis because their calculation od was determined. To correlate temporal patterns of outdoor requires germination under constant temperatures in the cli- germination with thermal conditions we used meteorological mate chamber, which did not occur in a number of species. As data from the nearby (ca. 500 m) climate research station Lin- PCA does not accept missing values, the inclusion of these den. Starting on the last day with a daily average temperature traits would have lowered the number of analysed species. below 1°C we calculated the number of days with daily aver- Correlations between single germination traits and PCA-axis ages above 5°C as well as total temperature sums of daily scores, on the one hand, and species attributes such as seed averages until the onset and the first pronounced peak in out- mass (Hölzel & Otte 2003/4a), seed longevity, threat status, door germination, respectively. Both temperature traits revea- range size and type on the other hand were examined by non- led to be highly correlated (r2 = 0.98), thus we used only the parametric Spearman rank correlation coefficients. As a meas- number of days with averages above 5°C for further numeri- ure of seed longevity we applied the seed accumulation index cal analyses. (SAI) given in Hölzel & Otte (2003/4 a) for 36 of the stu-

FLORA (2004) 199 15 PEAK4 SPAN = as temperature sum, (d) in days, n.m. OPT LMAX TFAS GFAS AMP LOW HIGH ALT STRAT FMAX ONSET(s) ONSET(d) FOPT(s) FOPT(d) PEAK1 pumi – 2 – 0 0 – – 0 2 66 295 33 342 37 25 92 35 iol persiol elat – – 5 2 – – 0 0 0 0 – – – – 0 0 0 2 18 59 337 295 36 33 337 342 36 37 46 21 63 59 388 77 ero serp 15.1 100ero perealer prat 20 18.3 18.8 98 92 69 20 22 25 73 3 53 18 25 27 7 3 0 25 30 –1 –21 93 14 60 –16 200 59 64 181 17 197 19 21 200 194 17 197 19 78 21 28 99 46 95 16 95 38 21 yth sali 26.6 100 25 93 15 20 35 10 88 54 234 21 234 21 34 86 35 Care praeCare tome –Iris spuria –Pote rept –Scut hast 0 –Elym repe 0 –Poa angu – – 1 –Lath palu – 6 – n.m 0 0 3 – 0 n.m – 2 0 – 0 n.m 0 0 – n.m – 0 0 0 – n.m 0 – 0 – n.m 0 0 – – n.m – – 0 – n.m – 0 – – 0 n.m – 1 0 – 35 0 0 –2 24 0 2 54 101 6 76 2 0 280 0 490 68 –1 157 11 62 67 28 280 32 56 466 16 181 181 235 28 49 466 19 828 2156 24 19 49 164 80 466 28 882 181 38 48 235 49 29 80 30 19 24 82 28 84 724 38 19 51 42 21 381 35 75 53 91 86 42 88 24 45 Cera dubiAlop prat 10.6Card parv 11.2 100Gali wirt 13.8V 16 15 14.4 98Rume thyr 25 75Fest arun 15.3 82 10V 16.3 95 15 17V 2 65 97Gali bore 10 28 3Pseu long 27 8 20.1 20 90Arab nemo 21.9 27 20 22.6Care spic 38 3 7 88 27 91Cirs tube 84 22.9 7 20Sang offi 30 15 27 25 23.0 3Alli angu 30 3 28 25.4 30Serr tinc 1 66 46 25.8 3 – 46 82 30 10L 0 93 26.5 25Puli dys 20 30 –2 28 30 –1 –6 30 20Inul brit 78 36 –40 0 51 10 25 28.3Inul sali 2 96 7 10 36 36 28.8Barb stri 35 –2 –16 88 52 30 16 23 81 29.1 5Alth offi –20 35 30 58 20 29.9Thal flav 142 30 81 3 81 75 10 20 30.5 –19 7Cnid dubi 25 81 15 95 99 27.6 17 12Sila sila 35 20 20 15 8 – 25 8 21 107 30 30 47 15 35Peuc offi 15 142 32 32 8 30 15 73 30Euph palu – 71 – 9 98 – 5 15Symp offi –2 12 – 35 65 87 10 35 15 9Sene palu 3 – 25 81 20 15 10 197 – 16 42 14 4 142V – 38 0 20 10 74 23 81 197 197V 30 25 35 –2 – 84 22 46 137 31 –Viol 25 35 0 – 15 21 63 0 8 21 28 35 187 – 94 181 21 21 329 12 35 0 157 15 8 2 30 – 0 0 35 194 55 0 0 96 17 25 157 33 19 0 30 0 – 0 313 41 35 75 0 16 0 197 0 66 0 0 48 21 197 197 100 – 31 99 0 0 – – 70 16 35 – 0 0 17 0 252 91 98 75 21 181 – – 21 21 28 – 14 0 533 39 197 66 – – 316 98 47 286 2 18 14 200 – 28 70 197 35 93 19 56 828 – 21 28 11 5 14 197 0 32 34 78 0 414 17 21 37 5 39 38 61 99 8 34 80 22 21 269 0 34 181 48 25 26 48 50 39 197 76 48 48 21 501 88 30 81 77 200 38 19 197 84 157 828 74 157 94 49 21 28 32 181 17 39 520 53 97 28 21 80 200 16 18 16 33 93 47 19 18 88 90 313 31 17 197 74 100 13 197 35 38 181 35 62 181 21 22 21 234 9 19 48 37 90 19 84 111 21 65 16 51 25 97 45 95 39 84 61 18 18 149 71 45 44 Species Seli carv n.m n.m n.m n.m n.m n.m n.m n.m n.m 55 295 33 383 43 56 92 33 able 2. 1):Table Germination traits (for abbreviations see chapter 2.5) of 42 flood-meadow species (s) A B C D T = not measured.

16 FLORA (2004) 199 died species. To describe range size on a Central European sca- However, there were also some species with expli- le we used grid frequency data from the German flora mapping citly deviating behaviour indicating significantly lower project provided by the electronic resource Floraweb (BfN or higher temperature requirements. In Cerastium dubi- 2003). Threat status was assessed by a simple ordinal scale um and Cardamine parviflora outdoor germination star- ranging from 0 (unthreatened) to 2 (strongly threatened) based ted considerably earlier (< 10 days with averages > 5°C, on the list of Korneck et al. (1996). In the same way river corridor confinement was allocated from the specifications temperature sum < 100°C). In contrast, Althaea offi- of Korsch (1999) and Burkart (2001). Differences between cinalis, all Carex species, Inula britannica, I. salicina, groups were tested using a non-parametric Mann-Whitney Potentilla reptans, Scutellaria hastifolia and Thalictrum U-test. All calculations were carried out with STATISTICA flavum showed a much higher temperature requirement 6.0. with a first germination peak occurring only after 50 days with averages > 5°C and a temperature sum >500°C. In both response groups these results largely 3 Results coincided with the germination temperature requirements found in the laboratory experiment. 3.1 Patterns of single germination traits In 60% of the studied species more than 80% of the Under laboratory conditions only a limited proportion final outdoor germination took place within four weeks. of the studied species (Group A, Table 2) germinated In some, such as Arabis nemorensis, Cerastium dubium, with high rates over a wide range of constant tempera- Serratula tinctoria, Silaum silaus and Veronica serpylli- tures (AMP) or showed a clear preference for low ger- folia such rates were even reached during a single count. mination temperatures (OPT, LOW). In contrast, many This particularly synchronous germination behaviour is species reached maximum germination rates only at contrasted by other species that emerged over a long relatively high constant temperatures (OPT) above period with low but constant rates. This was most 20°C (Group B, Table 2). However, in all of these spe- obvious in Carex tomentosa, Euphorbia palustris, Scu- cies except Althaea officinalis and Barbarea stricta ger- tellaria hastifolia and Thalictrum flavum. mination rates increased considerably after 8 weeks of cold wet stratification (STRAT) and following low fluctuating temperatures (5/15°C), most strikingly in Lythrum salicaria and Sanguisorba officinalis. Positive 3.2 Multivariate analysis of germination traits effects of fluctuating temperatures (ALT) alone without The principal-component analysis (PCA) revealed the stratification were less pronounced and restricted to a correlation structure of the germination traits (Table 3, few species such as Cardamine parviflora and Cirsium Fig. 1). The first factor axis, which explained the bulk of tuberosum. In some other species they even caused a the variance (40.99%), reflected a continuous gradient decline in germination rate. In Apiaceae and some other from species with high, rapid and strongly synchronised species (Group C, Table 2) germination under labora- germination over a wide range of temperatures (left side tory conditions was confined to the stratification treat- of Fig. 2) to those with high temperature requirements ment (STRAT). and a delayed germination over a relatively long period A surprisingly high number of species (Group D, (right side of Fig. 2). Factor axis 2 largely coincided Table 2) almost completely failed to germinate under all with the variation of AMP, SPAN on the one hand and laboratory treatments, showing maximum germination PEAK4 on the other hand. Factor axes 3 and 4 predomi- rates below 5%. Under outdoor conditions in all of the- nantly represented the variance in STRAT and ALT, res- se species (except Cnidium dubium) the germination pectively (Table 3, Fig. 1 and 2). rates (FMAX) increased considerably and were usually well above 20%. In the outdoor treatment about half of the species had an initial pronounced germination peak (FOPT) after 3.3 Timing of germination after natural seed around 20 days with daily averages above 5°C, which is shedding equal to a temperature sum of ca. 200°C. Most species with a highly positive response to the cold wet stratifi- In experiment 3, in which the timing of germination cation treatment under laboratory conditions (STRAT) after natural seed release was investigated the following were found within this group. Galium boreale, Cnidium major response types appeared (Fig. 3): dubium, Sanguisorba officinalis, Selinum carvifolia and I) Potential for complete germination within the sea- all Viola species showed slightly higher temperature son of shedding: Among the species used in this experi- requirements (FOPT) with peak germination about two ment only the therophytes Cardamine parviflora and weeks later (around 30 days with averages > 5°C, tem- Cerastium dubium belong to this response type. Seeds perature sum > 300°C). of these species reached 100% of the final germination

FLORA (2004) 199 17 Table 3. Correlation between factor axes of PCA ordination and germination traits. High correlations are given in bold (for abbreviations of germination traits see chapter 2.5). Factor 1 Factor 2 Factor 3 Factor 4

Eigenvalue 4.51 1.34 1.19 0.96 Variance (%) 40.99 12.16 10.81 8.71 LMAX Ð0.89 –0.26 0.26 –0.15 GFAS Ð0.81 –0.38 0.14 –0.16 AMP Ð0.76 Ð0.50 0.06 –0.05 PEAK1 Ð0.64 0,26 –0.25 0.04 PEAK4 Ð0.73 0.47 –0.22 –0.06 ALT –0.35 –0.24 0.05 Ð0.78 STRAT –0.08 0,29 0.81 –0.25 FMAX Ð0.51 –0.28 –0.42 –0.29 ONSET 0.65 –0.36 0.08 –0.18 FOPT 0.59 –0.20 –0.34 –0.30 SPAN 0.62 Ð0.43 0.14 0.12

rate within two months after shedding in late May. Whe- reas germination started directly after sowing in Carda- Fig. 1. Biplot displaying correlation structure of germination mine parviflora the onset of germination in Cerastium traits along factor axis 1 and 3 in PCA-ordination (for abbre- dubium was about 4 weeks later. viations of germination traits see chapter 2.5). II) Potential for partial germination directly after shedding in late summer with a second peak in March/April of the following year: All species belon- ging to this response group germinated to a certain 3.4 Correlation between germination degree directly after shedding. However, germination stopped abruptly by the end of September at the latest, characteristics and other species traits when daily averages were usually still well above 10°C. Spring germination, in contrast, started at the earliest in According to Spearman rank correlation species with late February, with a significant peak in March at tem- small seed mass tended to germinate faster (GFAS) peratures considerably lower than those in early autumn (r = –0.51, p < 0.001) and had a higher temperature when germination stopped. Only in Inula salicina did amplitude (AMP) (r = –0.38, p < 0.05) and maximum germination start as late as April, indicating significant- germination rate (LMAX) (r = –0.44, p <0.01) under ly higher temperature requirements. laboratory conditions. No further correlations between seed weight and germination characteristics were III) No germination in the year of shedding, but found. almost complete and rapid germination in March/April Surprisingly, the tendency in species to build up long- of the following year: Most species of this group com- term persistent soil seed banks was positively correlated prise Apiaceae with relatively late seed release (Sep- with fast germination under laboratory conditions tember), but species with a much earlier shedding are (GFAS) (r = 0.40 p = 0.02) and a high outdoor germina- also represented, such as Galium boreale. Early spring tion rate (FMAX) (r = 0.35 p = 0.04). germination occurred very abruptly and was highly syn- Spearman rank correlation also revealed a significant chronised. Only Cnidium dubium showed a slightly but relatively weak correlation (r = 0.36 p = 0.02) bet- extended germination period towards summer. ween the first factor axis in PCA ordination and Red List IV) Delayed, slow germination over an extended status. A similar relationship was found between Red period, starting in the first summer after shedding: In List status and single germination traits such as LMAX most species of this response type significant germina- (r = –0.43 p = 0.006), GFAS (r = –0.32 p = 0.04), FOPT tion started no earlier than late April or May and conti- (0.43 p = 0.03) and SPAN (r = 0.37 p = 0.02), indicating nued over the whole summer season. In Carex tomen- a trend towards higher dormancy levels, increased tem- tosa peak germination occurred only in the second, and perature requirements and asynchronous germination in in Lathyrus palustris even in the third and fourth year endangered species. In contrast, there was no relation- (data not shown) after shedding. ship at all between germination traits and river corridor

18 FLORA (2004) 199 Fig. 2. Distribution of species in PCA ordination space along factor axes 1 and 3 (for abbreviations of species names see Table 1).

confinement or Central European range size. Identical gradient in germination traits was found by Olff et al. results (not shown) were obtained in group comparisons (1994) in the flora of Dutch wet meadows. by the Mann-Whitney U-test. A high capacity for spontaneous germination directly after shedding is typical of many dominant Poaceae in temperate grasslands (Thompson & Grime 1979), which could be confirmed in our study for Festuca arun- 4 Discussion dinacea. The relatively low total germination rates com- pared to other studies (Grime et al. 1981) achieved in 4.1 Germination strategies in flood-meadows some dominant grasses of flood-meadows, such as Alopecurus pratensis, Elymus repens and Poa angusti- In flood-meadows of the studied type the survival of folia, are probably partly due to heavy mildew infesta- insufficiently developed seedlings will often be severely tion within the climate chamber treatments and/or low hampered by frost damage and prolonged flooding quality of the seeds used. during the winter season (e. g. Voesenek & Blom According to Grime (2001) two major strategies can 1992). Equally, open patches with poor competition are be distinguished that enable seeds to delay germination more likely to occur in spring after the retreat of flood until the following spring and summer season: i) high water, which often creates gaps in established vegeta- temperature requirements for germination, which are tion. Consequently, it makes ecological sense that many usually not fulfilled during the autumn season, ii) a of the flood-meadow species studied exhibited various requirement for chilling to break dormancy. In accor- levels of conditional or even strict dormancy in the year dance with Washitani & Masuda (1990), who studied of shedding, while there were fewer species that germi- germination characteristics in a moist tall grassland nated spontaneously at high rates over a wide tempera- community in Japan, both strategy types could be found. ture range including lower temperatures. However, our study clearly established that some spe- The existing diversity of germination response types cies may combine both principal strategies for the avoi- in flood-meadow species was clearly visible in PCA- dance of harmful late autumn and winter germination. ordination, which reflected a continuous gradient of Within the year of shedding many of the studied species increasing dormancy levels along the first factor axis such as Allium angulosum, Arabis nemorenis, Cirsium (Fig. 1) with Cardamine parvifolia (non dormant) and tuberosum, Pseudolysimachion longifolium and others Carex tomentosa (highly dormant) as the most extreme showed relatively high temperature requirements to points of the spectrum (Fig. 2). An almost identical main reach significant germination rates, but came out of pri-

FLORA (2004) 199 19 Fig. 3. Timing in germination of freshly shed seeds under outdoor conditions.

mary conditional dormancy (Baskin & Baskin 2001) through established vegetation. Additionally, in some after a period of cold wet stratification. This phenome- species with high temperature requirements such as non could be observed in the climate chamber treat- Arabis nemorensis, Inula britannica and Sanguisorba ments as well as under outdoor conditions. Ecologically officinalis autumn germination is simply avoided by a this means that germination will stop well before the strongly delayed seed release. onset of the cool season while the same species are able Besides conditional dormancy enforced by high tem- to exploit gaps at relatively low temperatures in early perature requirements prior to chilling, hardening of spring. seed shells due to dry and warm weather conditions (or Under natural habitat conditions in flood-meadows dry storage prior to laboratory experiments) may also be dormancy after shedding will often also be enforced by responsible for poor germination in the year of shedding environmental constraints such as drought or shading (e. g. Otte 1996, Jensen 2001). This applies in parti-

20 FLORA (2004) 199 cular to species that lack a response to the stratification conditions. Consequently, in our study high tempera- treatment in the climate chamber but have high early ture requirements and/or delayed and asynchronous ger- spring germination rates such as Barbarea stricta, Viola mination were most common in perennial species with elatior and V. pumila or those with strongly increased a clear preference for the dampest parts of flood-mea- outdoor germination rates such as Allium angulosum, dows such as Euphorbia palustris, Lathyrus palustris, Euphorbia palustris and Galium boreale. All these spe- Scutellaria hastifolia, Thalictrum flavum and Viola per- cies exhibit relatively hard and compact seed shells that sicifolia. According to Grime et al. (1981) and Baskin obviously require softening in the course of prolonged & Baskin (2001) high temperature requirements and outdoor stratification. In particular, Euphorbia palustris dormancy levels are a common feature in temperate showed a high initial germination rate only in seeds wetland species. sown directly after shedding. When seeds were dry stored and sown in winter germination extended over a much longer period. This phenomenon may be referred 4.2 Germination characteristics and to as secondary induced physical dormancy (Baskin & seed bank persistence Baskin 2001). As in other studies (Grime et al. 1981; Patzelt In previous studies (Hölzel & Otte 2001; 2003/4a) 1998) Apiaceae proved to exhibit a strict chilling requi- species, such as Arabis nemorensis, Cardamine parvi- rement due to morphophysiological dormancy caused flora, Cerastium dubium, Lythrum salicaria, Pseudo- by an underdeveloped embryo (Stokes 1952; Baskin lysimachium longifolium, Potentilla reptans, Veronica & Baskin 2001), which necessarily delays germination peregrina, V. serpyllifolia were revealed to build up lar- until the spring season. ge long-term persistent seed banks. Surprisingly, with In accordance with Milberg & Andersson (1998) the exception of Potentilla reptans, all these species we found that differences in conditional dormancy were exhibited relatively low dormancy levels and a high largely compensated by cold stratification under out- potential for fast germination in light. Thus, the forma- door conditions resulting in a highly synchronised ger- tion of a long-term persistent soil seed bank is obvi- mination peak in March and early April. However, ously completely due to dark dormancy. Typically, all there was also a group of species in which high tempe- these species have very small seeds, which according to rature requirements did not disappear after chilling. Al- Grime (2001) almost generally show an obligatory light thaea officinalis, Potentilla reptans, Thalictrum flavum requirement for germination. There seems to be an in- and Scutellaria hastifolia and the Carex-species teresting link between the higher probability of burial in obviously require an obligatory extended period of small seeds (Thompson et al. 1993; Bekker et al. 1998) warm moist incubation under outdoor conditions to and their capacity for fast and almost complete germi- come out of dormancy. This confers with results repor- nation in light. Species with regeneration strategies ted by other authors (Baskin & Baskin 2001; Patzelt involving a large persistent soil seed bank typically 1998; Schütz 1997, 2000a; Ziron 2002). In most of exploit gaps in established vegetation caused by stocha- these species, high temperature requirements go hand in stic, largely unpredictable disturbances (Thompson & hand with a strongly delayed and asynchronous germi- Grime 1979; Grime 2001). Thus, the ability of sponta- nation over the whole summer period. Conspicuously, neous and rapid germination after exposure to light is an species with the most delayed and asynchronous germi- essential prerequisite for the successful exploitation of nation have relatively large and compact seeds with fea- such temporary gaps. This strategy is of particular tures of physical dormancy such as water-impermeable importance in ephemeral annuals of flood-meadows like testa (Lathyrus palustris) or particularly thick and hard Cardamine parviflora, Cerastium dubium and Veronica seed coats (Carex tomentosa, Iris spuria). After the peregrina. However, even among these annuals signifi- breaking of physical dormancy, at least Lathyrus palust- cant differences could be found in the main period of ris and Iris spuria exhibited no particular temperature germination. Cerastium dubium exhibited a delayed requirements for germination, as has been found in other germination directly after shedding obviously due to a studies for species of the same genera (Baskin & Bas- requirement for warm stratification to come out of dor- kin 2001; Grime et al. 1981). mancy at high temperatures, which is typical of facul- Asynchronous germination can be seen as a strategy tative winter annuals (e. g. Baskin & Baskin 1983a). In to minimise the risk of total failure of seed regeneration seed bank experiments (Hölzel & Otte 2001) this spe- due to regularly occurring disruptive environmental cies showed a pronounced germination peak in late sum- constraints such as drought, which is particularly rele- mer and early autumn. Equally, mass occurrence of vant in species with a delayed germination during sum- Cerastium dubium in the field coincides with years of mer. Equally, this strategy seems to be a benefit in low winter flooding intensity (Hölzel 1999). In con- amphibious habitats with strongly fluctuating moisture trast, Veronica peregrina is preferably a summer annual

FLORA (2004) 199 21 due to its strong response to cold wet stratification, not usually diminish the viability of existing popula- which was also found by Baskin & Baskin (1983b). tions, since most of the relevant species are long-lived Some species exhibiting particularly high dormancy and exhibit extensive clonal growth. In contrast, this levels such as Carex tomentosa and Viola persicifolia could become a serious problem in habitat restoration, were also found to create long-term persistent soil seed in which species re-establishment crucially depends on banks (Hölzel & Otte 2003/4a). However, their den- regeneration by introduced seeds (e. g. Patzelt 1998). sities were usually much lower than in small seeded spe- In a plant material transfer experiment aimed at recrea- cies, which may be caused by a lower probability of tion of a species-rich flood-meadow (Hölzel & Otte burial as well as a higher potential for germination in 2003), we found poor establishment success after four darkness (Grime 2001). Our results suggest that only years in a number of species with delayed and asyn- in relatively large seeded species dormancy levels est- chronous germination behaviour, such as Lathyrus ablished in germination experiments are a good predic- palustris, Scutellaria hastifolia, Thalictrum flavum and tor for the capacity of a certain species to build up per- almost all Carex species. Especially in Carex species the sistent seed banks. very specific and narrow germination requirements are obviously a major constraint and may explain their noto- riously low colonisation capacity (Grime et al. 1988; 4.3 Germination characteristics and Budelsky & Galatowitsch 1999; Schütz 2000a). rarification In most species with high germination temperature requirements, successful regeneration by seeds is prob- We did not find any single germination trait or a multi- ably confined to certain years with particularly favour- variate response type that corresponded with the con- able moisture conditions and low competition by finement of species to large river corridors. There established vegetation, as may occur in the course of appears to be nothing really particular in the germina- prolonged early summer flooding and following draw- tion behaviour of river corridor plants that could explain down (Jutila 2001; Hölzel & Otte 2003, 2003/4b). their conspicuous habitat and range restriction in Cen- As demonstrated in this study the majority of flood- tral Europe. A comparable set with similar variability in meadow species are able to exploit the particular favour- germination traits has been found in other temperate wet able recruitment conditions (constant moisture supply, grassland communities (Washitani & Masuda 1990; open vegetation structure) prevailing in early spring Olff et al. 1994; Patzelt 1998; Jensen 2001). (March/early April). Management schemes that support Equally, there were no significant differences in ger- the creation of open vegetation structures and patches of mination characteristics between species with small or bare soil at this time of the year – such as mowing and large Central European range. Comparable results were removal of plant litter, aftermath pasture or scarring of obtained by Thompson et al. (1999) who found no rela- the sward – may actively enhance regeneration by seeds tionship between germination traits and range size of (e.g. Kotorová & Lepsˇ 1999). vascular plants in the British flora. Although there was a significant albeit weak trend for higher dormancy levels in endangered species, we found little evidence Acknowledgements for the assumption made by Schütz (2000b) that germination traits may play a prominent role in the causal We are grateful to Martina Dehn, Christiane Lenz-Kuhl understanding of rarity and decline. Regeneration cha- and Josef Scholz-vom Hofe for their help with in collecting racteristics are obviously outweighed by other species seeds and performing germination experiments. Tobias traits such as habitat specialism and the respective life Donath and Lutz Eckstein provided helpful comments to Rod Snowdon strategy in the established phase, which have proved to a former version of this manuscript and po- lished our English. The comments of two anonymous referees be much better predictors of rarification processes in the greatly improved the quality of this paper. Our work was part- Western and Central European flora (Korneck et al. ly supported by grants from the Federal German Agency for 1998; Thompson et al. 1999; Grime 2001). Nature Conservation (BfN).

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