Biological flora of Central Europe: Ranunculus reptans L.

Flora (2000) 195, 135-145 http://www. urbanfischer.de/joumals!flora

©by Urban & Fischer Verlag

Biological flora of Central Europe : Ranunculus replans L. D. PRATI 1 and M. PEINTINGER Institut fiir Umweltwissenschaften, Universitat Ziirich, Winterthurerstr. 190, CH-8057 Ziirich, Switzerland e-mail: [email protected], peinti @uwinst.unizh.ch 1 Corresponding author Present Address: Eidgenossische Forschungsanstalt fiir Wald, Schnee und Landschaft WSL, Gruppe Bioindikationen, Ziircherstr. 111, CH-8903 Birmendorf, Switzerland

Accepted: June 14, 1999

Summary Ranunculus reptans is a stoloniferous perennial herb of inundated lake shores. It is native to Central Europe, where it has become a rare and endangered species. This article reviews the morphology and taxonomic status, the distribution, ecology, population biology and genetics of this taxon.

Key words: Ranunculus rep tans, ecology, species biology, Central Europe

1. Taxonomy and morphology 1.1. Taxonomy Ranunculus reptans L. (Ranunculaceae) - Ufer-Hahnenfuss, Wurzelnder Sumpf-Hahnenfuss - Creeping Spearwort Section Flammula (WEBB) ROUY et FOUCAUD Synonyms:

R . .filiformis MICHX. R. flammula subsp. reptans (L.) SYME R. flammula L. var. reptans (L.) E. MEYER R. flammula L. var. intermedia HooK, R. flammula L. var. ovalis (BIGEL.) L. D. BENSON =R. reptans L. var. ovalis (BIGEL) TORR. et GRAY R. reptans has been regarded as a subspecies or variety of R. flammula, especially in the American literature (see e.g. BENSON 1955; COOK & JOHNSON 1968; MoRIN 1997), but in Central Europe R. rep tans is generally considered to be a separate species (HEm 1967; HEss et al. 1980; TunN et al. 1993). R. reptans can produce viable hybrids with R. flammula (GIBBS & GoRNALL 1976), but further biosystematic studies are needed to assess the taxonomic status of the species (MoRIN 1997; see also 3.12. Hybrids). 0367-2530/001195/02-135

$ 12.00/0

1.2. Morphology Ranunculus reptans is a perennial herb with creeping-filiform-branched stems which root at the nodes. Stems are thin (0.5-2 mm in diameter) and can reach a length of 10-20 (50) em within one growing season. Internodes of the creeping stem are 3-5 em long but in some individuals the first internode is much shorter (see Fig. 1). The leaf blades are linear, lanceolate or spatulate, 10-50mm long and 1-5mm wide and gradually narrowed into the petiole. The species shows a low degree of leaf dimorphism (CooK & JoHNSON 1968): under submerged conditions the leaves are small and filiform, 5-15 mm long and 1-2 mm wide (Fig. 2), whereas GLUCK (1911, p. 120ff.) noted that the filiform leaves under submerged conditions can attain a similar length than the leaves produced under terrestrial conditions. The flowers are bright yellow and small (diameter 5-20 mm). They have 5-7 oblong-elliptical petals 4-10mm long which exceed the calyx. Each petal has one nectariferous gland. The flower has numerous stamens and between 10-20 carpels. The polycarpic fruiting head is globose, c. 2-10 mm in diameter with obovate, slightly laterally compressed nutlets (achenes) which are glabrous and 1.5-2 mm long. Nutlets have a curved beak of about 1/4 of the length of the nutlet (0.4-0.6 mm). FLORA (2000) 195

135

Fig. 1. Schematic representation of the growth form and branching pattern of Ranunculus reptans. The primary shoot (pSh) with the first stolon (St 1) is shown at the top, the first stolon at a later stage with a second stolon generation (St2) is shown at the bottom. Co= Cotyledons, pR = primary roots, aR = adventitious roots, Tc T3 = terminal flowers 1-3 (modified after BARYKINA & PuSTOVOJTOVA 1973).

Terresttial

Aquatic

R A

B

c

D

Fig. 2. Leaf silhouettes of Ranunculus reptans grown under terrestrial (top) and aquatic (bottom) conditions. Two leaves from four genotypes (A-D) are drawn to show genotypic variation in leaf shape under terrestrial conditions.

The juvenile plant produces a rosette with 5-10 (- 20) leaves and adventitious roots quickly replace the primary root (BARYKINA & PUSTOVOJTOVA 1973). The primary shoot usually remains as a rosette and flowers only rarely (JENSEN 1912). The axillary buds of rosette leaves pro136

FLORA (2000) 195

duce 1-3 (-6) above-ground stolons that are typically bent and rooted at the nodes (Fig. 1). After 3-5 (-10) internodes the stolon becomes ascending and produces one terminal flower or a monochasial inflorescence with 2-4 flowers (TROLL 1964, p. 21lf, SEREBRJAKOVA 1981).

WW] •

Ranunculus reptans L.

+ extinct

? doubtful record

Fig. 3. The distribution of Ranunculus reptans on the northern hemisphere (after M. H. HoFFMANN, Halle).

The growth of the stolon is usually continued from the axillary bud of the last node (but see SEREBRJAKOVA 1981 ). The rooting nodes of the stolons can develop into secondary rosettes with 2-10 (-20) leaves from which new stolons can be produced. Observation on plants from Russia (cf. BARYKINA & PUSTOVOJTOVA 1973; SEREBRJAKOVA 1981) that the central meristem of rosettes grows out to a flower or inflorescence could not be affirmed with Central European plants. After the internodes between the rosettes decayed the rosettes become independent ramets which overwinter and eventually produce stolons in the following season. After the anthesis the flowering stems lies down and each node of the formerly ascending stolon can subsequently develop into a rosette with adventitious roots (Fig. 1). However, these rosettes have a considerably lower probability to produce further stolons than the ones from the plagiotropic part of the stolon. Thus, there

is a certain degree of functional specialisation among ramets in flowering rosettes for sexual reproduction and branching rosettes for vegetative growth (PRATI 1998). The closely related Ranunculus flammula is generally much larger than R. reptans. It is ascending and only the first nodes of the stem produce adventitious roots. In addition, the beak of the achenes is not curved and much smaller (only about 1/10 of the achene length) than in R. reptans.

2. Distribution and habitat requirements 2.1. Geographical distribution Ranunculus reptans has a circumpolar distribution and occurs mainly in the temperate to boreal-subarctic zones of Europe, Asia and North America (JALAS & SuoMIFLORA (2000) 195

137

NEN 1988; HEGI 1967; see Fig. 3). In Europe its range includes Central and Northern Europe with Iceland, Scandinavia and the Baltic countries as main centres of distribution. In the north the species grows beyond the polar circle, while the southernmost populations are found in Bulgaria. The species record from Central Italy is doubtfull (PIGNATTI 1982). British records probably refer to hybrids with R. flammula (see PADMORE 1957). The Central European populations around the Alps are probably relicts from the last ice age. Here, the species has become restricted to a few mainly pre-Alpine lakes although populations at 2 200 m elevation are known from Switzerland. Most of the Central European populations of R. rep tans are concentrated at Lake Constance and in the Southern Alps at Lake Como. Only few and partly very small populations are reported from Lac de Joux, Lac Neuchatel, Lago Maggiore, Brienzersee, Thunersee and in the upper Engadin in Switzerland, Alt-Aussee in Austria and Chiemsee, Hintersee and LOdensee in Southern Germany (HEGI 1980; HEss et al. 1980). Several reports in the literature (e.g. from the Black Forest) as well as many voucher specimens in herbaries (e.g. from Bavaria) refer to small specimens of Ranunculus flammula (SEBALD et al. 1990). In Northern Germany the occurrence of the species declined drastically and only few populations are left in Schleswig-Holstein and Mecklenburg (HAEUPLER & ScHONFELDER 1989). In North America the species is found from the south-west of Greenland through the arctic Canada and Newfoundland, south to New Jersey, Pennsylvania and Michigan, in the Rocky Mountains south to New Mexico and Arizona and at the west coast south to California (MoRIN 1997). In Asia the species occurs in the boreal-arctic zone of Russia, and goes south beyond 50° N in Mongolia, Manchuria and Japan (see Fig. 3).

2.2. Habitat The typical habitat of R. reptans is the eulittoral zone of periodically inundated lake shores with low vegetation cover (LANG 1967, 1973). Annual fluctuations of the water-level keep the vegetation open and are apparently necessary to prevent competitive exclusion of R. rep tans by taller species, especially grasses. Occasionally the species is found along silty or sandy river banks and in damp meadows and pastures that are strongly influenced by ground water. In contrast to R. flammula, R. reptans does not occur in bogs or fens. At higher altitudes R. reptans also grows along the banks of clear, oligotrophic and mineral-poor lakes of the alpine and subalpine zone. The soils are wet, usually nutrient-poor and often consist primarily of gravel and sand. Occasional138

FLORA (2000) 195

ly the species is found on soils that are silty and rich in humus. According to ELLENBERG et al. (1992) R. reptans is indifferent to soil pH.

2.3. Communities Ranunculus reptans is a characteristic species of the phytosociological class Littorelletea uniflorae (OBERDORFER & DIERSSEN 1977). At Lake Constance R. reptans typically occurs in the Deschampsietum rhenanae and Littorello-Eleocharitetum acicularis (LANG 1967, 1973; THOMAS et al. 1987; PEINTINGER 1995). Species that typically co-occur with R. reptans are listed in Table 1. At oligotrophic lakes at higher altitudes the species is found in association with species of the Callitricho-Sparganietum, e.g. Sparganium angustifolium, Callitriche palustris, Eleocharis quinqueflora, E. acicularis and Ranunculus trichophyllus (ELLENBERG 1996). In a pasture at Lake Como R. reptans was found to be associated with Agrostis stolonifera, Alopecurus aequalis, Gratiola officina/is and Myosotis nemorosa. From Bavaria only one vegetation record of R. reptans is known (Lodensee, Chiemgau) where the species cooccurs with Eleocharis acicularis, Plantago major, ]uncus articulatus, Molinia caerula and Potentilla reptans Table 1 . Frequency of different species in 26 vegetation records of Deschampsietum rhenanae communities from 7 locations at the western end of Lake Constance. Indicated is the percentage of records in which the species occurred in 1993 (modified after PEINTINGER 1995). Characteristic species Littorella uniflora (L.) AscH. Ranunculus reptans L. Carex viridula MICHAUX Myosotis rehsteineri WART. Deschampsia rhenana GREMLI Eleocharis acicularis (L.) R. et ScH. Carex panicea L. Species indicating disturbance of the community Agrostis stolonifera L. Phalaris arundinacea L. Poa annua L. Ranunculus sceleratus L. Accompanying species ]uncus alpino-articulatus L. Carex elata L. and C. acuta ALL. Allium schoenoprasum L. Cardamine pratensis L. Ranunculus ficaria L. Galium palustre L. Ranunculus repens L. Leontodon autumnalis L.

(%)

85 69 46 42 31 8 8

100 88 31 12 65 62 35 31 15 12 12 8

(SPRINGER 1996). Communities with R. reptans from oligotrophic lake shores in Norway and Iceland are described in DIERSSEN (1975).

2.4. Response to abiotic factors Annual water-level fluctuations appear to be essential for the preservation of the typical habitat that supports R. rep tans. At Lake Constance the rise of the water level begins in spring and results in the flooding of whole populations during 4-20 weeks between May and September. However, other lakes (e.g. Lake Como or lakes a higher elevation) may have different patterns of water-level fluctuations. The rise of the water level has direct and indirect effects on the growth of R. reptans. A direct response is a strong reduction in growth when the plants become submerged. According to our observatio~s the connections between rosettes decay quite rapidly and the larger leaves that have been produced in unsubmerged conditions are replaced by small filiform leaves. However, GLi.JcK (1911, p. 120ff.) observed that submerged plants produce longer internodes which could be interpreted as a mechanism to escape from the submerged condition. Only well-rooted rosettes can survive flooding and only unsubmerged plants flower. . An indirect_ effect of flooding is the strong suppresswn of supenor competitors, especially grasses like Agrostis stolonifera. Fluctuations of the water-level essentially prevent succession and keep the vegetation of the shore open. Populations of R. reptans eventually become extinct if inundation ceases due to regulations of lakes and rivers. For example, at Lake Zurich R. reptans became extinct during the first decades of this century, after water level fluctuations ceased because of the regulation of the river Linth (E. LANDOLT, pers. communication). Another important abiotic factor is the mechanical disturbance caused by the surf. Depending on the prevailing direction of the wind, parts of a lake shore may be more or less influenced by the wash of the waves which can prevent the successful establishment of seedlings of R. reptans. Established ramets can be washed away and thus serve as dispersal units (see 3.4. Reproduction).

2.5. Abundance Ra_nuncu!us rep tans often is one of the dominant species at mtact mundated gravel lake shores. There it can produce (together with Littorella uniflora) dense patches tightly packed with dozens of rosettes per 10 x 10 em. These patches can be monospecific or they can originate from the intermingled growth of R. reptans and L. uniflora.

3. Life cycle and biology 3 .1. Life cycle Ranunculus reptans is a polycarpic perennial hemicryptophyte. Although ELLENBERG et al. ( 1992) classified the species also as a hydrophyte, plants only rarely overwinter under submerged conditions. The species has a comp~ex life cycle with vegetative and sexual propagation. A high de~ree of vegetative propagation is attained by the productwn of rosettes with adventitious roots. During the submergence the stems die off and only well-rooted nodes eventually survive the flooding. Experimental studies on the effect of flooding suggest that survival and subsequent re-growth are positively correlated with the intensity of rooting and that therefore rooting intensity can be regarded as a measure of clone persistence. Seedling recruitment has been observed frequently in open patches, but whether seedling recruitment is successful also within dense patches is not known because detailed demographic investigations are difficult due to the inundated habitat. Nevertheless, as there are many open patches for population regeneration, the species probably can be considered as a clonal plant in which seedling recruitment occurs repeatedly in contrast to species in which seedling recruitment is restricted to the founding of a population (see ERIKSSON 1989). Because of the problems of individual-based demographic studies in the inundated habitat it is only possible to draw speculative conclusions on the relative contribution of sexual and vegetative propagation to population dynamics and the maintenance of genetic variation. Long-term vegetation studies suggest that density and abundance of R. reptans is mainly determined by clonal gro~th (PEINTINGER 1994). In addition, experimental studies under controlled conditions showed that the amount of resources invested in clonal growth exceeds by f~r the resources allocated to flower and seed productwn (PRATI 1998). However, even if the population dynamics in established stands is mainly driven by vegetative propagation, the role of sexual reproduction and successful seedling recruitment for the maintenance of genetic variation must not be underestimated. Even a very low rate of successful seedling recruitment can maintain high levels of genetic variation in clonal plants (ERIKSSON 1989, McLELLAN et al. 1997). This has in fact been found for larger populations of R. reptans at Lake Constance (see 3 .11. Genetic data).

3.2. Spatial distribution of plants within populations In the initial phase of colonisation clonal growth leads to a patchy distribution of genetic individuals within a population (PEINTINGER 1994). However, because the FLORA (2000) 195

139

vegetative mobility is rather large (up to 50 em in years with favourable conditions), genets soon intermingle with each other. Molecular studies using RAPD-PCR indicate that patches can consist of several genotypes of R. reptans (M. FISCHER, pers. communication). Especially established populations contain probably many different clones that are highly intermixed. No informations are available on the maximal age and size that individual clones can reach.

3.3. Phenology Ranunculus reptans flowers from April to September, but only if plants are not flooded. Therefore, the dynamics of water-level fluctuations largely determines flowering phenology (BAUMANN 1911). At Lake Constance high water levels occur in summer and last between 4-20 weeks (LANG 1967). Flowering normally starts in autumn once water levels are lower. However, in years in which the water level rises lateR. rep tans can also reproduce sexually in spring and thus has two reproductive periods per year. Sexual reproduction can fail completely in years with unusual long flooding periods. In lakes at higher altitude and in the southern Alps high water levels occur mainly in spring and plants flower during summer. After the water level sunk, new stolons grow out of a axillary buds of the rosette and start flowering within 4 weeks. Seed ripening lasts between 3 and 4 weeks. Seedlings have been observed both in spring and in autumn.

3.4. Reproduction Ranunculus reptans is a hermaphroditic but slightly proterandrous plant. Stamens open about 2 days before the carpels can be pollinated. The plants can reach maturity within their first year and normally reproduce once every year (but see above). R. reptans is mostly selfincompatible, but out of 40 genotypes tested in a crossing experiment, two genotypes proved to be self-compatible. Pollinators are flies of the family Syrphidae based on observation from Lake Constance, but further investigations need to show whether plants that flower in summer have other pollinators. BacHER ( 1938) reported that plants from Greenland showed a disturbed pollen meiosis that led to partly sterile pollen. Pollen sterility was also found in some plants from Lake Constance. There was a large genetic component in the proportion of sterile pollen: in some genotypes more than 50% of the pollen was aborted, whereas in the majority of plants less than 10% of the pollen was aborted. It remains to be investigated whether the reduced pollen 140

FLORA (2000) 195

40

10

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

Number of ripe seeds per ovule in a flower Fig. 4. Bimodal frequency distribution of the fertility of individual flowers of Ranunculus reptans suggesting pollination limitation. Based on 85 plants from two populations studied in autumn 1996.

quality is the result of inbreeding and whether small and/or isolated populations show a higher degree of pollen sterility. Because flowering is sometimes delayed because high water levels occur until late autumn, it is likely that pollination limitation occurs. Two populations at Lake Constance visited in 1996 showed a bimodal distribution for the seed set of individual flowers (seed/ovule ratio; Fig. 4 ). This suggests that some flowers were not visited by insects, while on the other hand even a few visits by pollinators appear to be sufficient to pollinate a large proportion of the ovules of a flower. This was supported by the observation that hand-pollination under controlled conditions generally resulted in a high seed set (65%). lt has been reported that all but 2-3 of the nutlets per flower may be abortive (KoMAROV 1937). However, our observations in the field suggest that in these cases the carpels may simply not have been pollinated. On average, a flower is produced after 4-5 internodes. Numbers of carpels (and ovules) per flower vary between 10-20. This variation has a considerable genetic component. Fertilised nutlets weigh on average 620 Jlg (standard deviation 165 Jlg; n = 30). The mass of nutlets also varies among genotypes, and there exists a negative phenotypic and genetic correlation between the number and the mass of nutlets per flower (PRATI 1998). Moreover, in a study with 32 genotypes of four different populations from Lake Constance, a genetic tradeoff was found between the degree of sexual and clonal growth. In addition, in a greenhouse experiment it was shown that these genetic differences could be attributed to differences between the sites of origin: plants from vegetation-free zones near the lake shore allocated proportionally more to clonal growth, whereas plants sampled further inland where interspecific com-

petition is higher allocated more to sexual reproduction (PRATI 1998). The dispersal over small distances appears to be effective and is probably promoted by water-level fluctuations. Permanent monitoring in two populations of R. replans at Lake Constance revealed successful colonisation of vegetation free zones by several individuals (PEINTINGER 1994). However, dispersal over longer distances along the lake shore is rather limited. Circumstantial evidence for limited dispersal is provided by one population of R. replans that is restricted to one end of the lake shore only, although the adjacent parts of the shore appear to be suitable for the species, judged by the presence of other associated species. JENSEN (1912) reported for plants from Greenland and Denmark that ripe fruits, if they are not wetted, can float for 1-2 weeks, but that majority of them sink within 48 hours if the surface gets wet. Long distance dispersal of the seeds by water birds, that has been found in Ranunculus repens and R. aqualilis (GILLHAM 1970, cited in ELLENBERG 1996) seems also unlikely in R. replans because, in contrast to the shallow water areas of the lakes, hardly any water birds are found at the lake shores. Molecular studies using RAPD-PCR revealed a gene flow of 0.75 individuals per generation between 14 analysed populations from Lake Constance (M. FISCHER, pers. communication). Whole rosettes are frequently washed away by the movement of the water (SCHROTER & KIRCHNER 1902). Transport of vegetative fragments has often been reported for other aquatic plants (see e.g. BARRETT et al. 1993). JOHANSSON & NILSSON (1993) reported for the related species Ranunculus lingua that dispersal by vegetative fragments occurs frequently and sometimes leads to successful establishment of new populations. However, for R. replans it is not known whether the vegetative fragments survive and can successfully root after transportation.

Seeds of Ranunculus flammula can produce a persistent seed bank (GRIME et al. 1988), but studies with R. replans are lacking. Several stages of seedling development are shown in Fig. 5.

3.6. Response to competition and management Ranunculus replans is a weak competitor (GAUDET & KEDDY 1995). It is quickly outcompeted by grasses, in particular Agroslis slolonifera, which is a commonly co-occurring species at the more inland parts of the lake shores (PEINTINGER 1994). Experimental studies in the greenhouse showed that competition by Agroslis slolonifera resulted in a 70% reduction of total plant biomass after 10 weeks of growth (PRATI 1998). Moreover, the species changed its allocation pattern when grown under interspecific competition. Plants allocated relatively more to sexual reproduction when growing in competition with Agroslis slolonifera, whereas they allocated relatively more to clonal growth in a competition-free environment (PRATI 1998). Other competitive interactions may occur under submerged conditions, when photosynthesis may be reduced because of shading by epiphytic algae. Such effects have been demonstrated for the co-occurring species Lillorella uniflora (SAND-JENSEN & SoNDERGAARD 1981). Growth and reproduction of R. replans can be negatively affected by alluvial deposits of algae which cover the plants after water levels have sunk. Thick algal deposits can result in the death of the whole vegetation. This has frequently happened in eutrophic lakes due to the stimulated algal growth and was probably the main reason (apart from habitat destruction) for the decline of the species during the last decades (THOMAS et al. 1987; PEINTINGER et al. 1997).

3.5. Germination 3.7. Herbivores and pathogens The seeds of R. replans germinate rather slowly. When seeds are kept moist they will germinate sporadically for up to 6 months, both in light and in darkness (CooK & JOHNSON 1968). We found that 50% of the seeds germinated within 15 weeks at 20 oc after stratification in cold water for 4 weeks. GRIME et al. (1988) reported at 50 of less than two weeks for the closely related species R. flammula. CooK & JoHNSON (1968) reported that germination can be boosted if seed are subjected to alternate freezing and thawing (four cycles of 1 h freeze, 4 h thaw) and that a high proportion of seeds germinates within six days.

The impact of herbivores appears to be negligible. There is hardly any damage to leaves, flowers or whole rosettes in natural populations that could be attributed to herbivores. Similarly, it has never been observed that parasites or diseases affect the plants in the field. Only on plants cultivated in the greenhouse mildew infections do sometimes occur. This apparent lack of interactions with herbivores and pathogens may be attributable to the inundated nature of the habitat, but the protective role of secondary metabolites in R. replans might be an alternative explanation (see 3. 9. Biochemical data). FLORA(2000) 195

141

Fig. 5. Stages in the development of Ranunculus reptans during the first 4 weeks after germination. (a) seed, (b) germinating seed, (c) 4-day-old seedling, (d) 4-week-old plant.

3.8. Mycorrhiza

3.10. Biochemical data

Twelve plants from three populations at Lake Constance were tested for their association with mycorrhizal fungi by hot staining the roots with trypan blue (after CLAPP et al. 1996). None of the plants showed any mycorrhiza and seedlings that were raised without mycorrhiza in sterilised soil grew vigorously.

Evidence for the proposed protection by secondary compounds is only circumstantial and based on findings in other species of Ranunculus. In R. lingua the secondary compound ranunculin, an unsaturated lactone common in several genera of the Ranunculaceae, has been found (AICHELE & SCHWEGLER 1994). When tissue is damaged, ranunculin is transformed into the toxic protoanemonin, a substance which also occurs in R. flammula (SCHONBECK & SCHLOSSER 1976). Ranunculus reptans has not been investigated for its content of secondary metabolites, but one can assume that it is similar to that of the closely related R. flammula.

3.9. Physiological data No information available. 142

FLORA (2000) 195

1000

~

!

.i

100

r:Q

10~-------.----------------.--------

Competition by Agrostis stolonifera

No competition

Fig. 6. Reaction norms of 32 genotypes of Ranunculus reptans cultivated with and withoutAgrostis stolonifera as a competitor. Dotted lines and squares denote genotypes and the mean of genotypes sampled from competition-poor parts of a lake shore. Solid lines and circles denote genotypes and the mean of genotypes sampled from competition-rich parts of a lake shore (data from PRATI 1998).

Protoanemonin inhibits the growth of microorganisms (SCHONBECK & SCHLOSSER 1976) and probably also deters herbivores. Ranunculus bulbosus which contains up to 1% ranunculin is avoided by herbivores, whereas R. repens which contains scarcely any of the compound is readily eaten (HARPER 1977).

3.11. Genetic data Chromosome number of R. reptans from various regions was 2n =32 [plants from Greenland (BocHER 1938), Schleswig-Holstein (SCHEERER 1939), Finnland (SORSA 1962) and Holland (GADELLA & KLIPHUIS 1966)]. Material from Northern Russia was found to have 2n =48 (JALAS & SUOMINEN 1988). The amount of nuclear DNA in R. flammula with the chromosome number 2n =32 is 12.7 pg (BENNENTT & SMITH 1976). The population genetic structure of four populations at Lake Constance was investigated using RAPD-PCR (PRATI 1998). This study revealed considerable genetic variation within populations which supports the observation that seedling recruitment does repeatedly occur in this species. In addition, some degree of population

divergence was found, but the number of populations studied was to small to allow general conclusions about the pattern of genetic variation at the population level. Quantitative genetic analyses were performed on the same plant material (PRATI 1998). This experiment revealed genetic differentiation within populations that could be attributed to the competition gradient at the lake shore (see also above: 3. 4. Reproduction). Vegetative offspring of genotypes that were sampled from two distinct sites within the gradient behaved differently when cultivated with and withoutAgrostis stolonifera as a competitor under controlled conditions (see Fig. 6). Genotypes sampled from competition-poor environments outperformed genotypes sampled from the competitive environment when they were cultivated without interspecific competition, and vice versa when cultivated with competition (PRATI 1998). Thus, at least for large populations at Lake Constance the environmental gradient at a lake shore can maintain genetic variation in life-history traits and despite pronounced vegetative propagation of this species, populations are not genetically impoverished.

3.12. Hybrids Ranunculus reptans can hybridise with its closest relative R. flammula (PADMORe 1957; GIBBS & GORNALL 1976). Experimentally performed crosses between eight plants from each species confirmed that the two species can produce viable F1-hybrids. The viability of F2hybrids, however, is not yet tested. The Fl-hybrids were morphologically more similar to R. flammula than to R. reptans. The leaves of the hybrids were generally larger and much more spatulate than in pureR. reptans, and hybrids tended to produce an ascending stem with a low degree of adventitious rooting at the nodes, similar toR. flammula. This suggests that the morphology of the more common and widely distributed species R. flammula is genetically dominant over the morphology of the rare specialist species R. rep tans. Natural hybridisation has been reported from the British Isles (STACE 1975, p. 124). PADMORE (1957) even argued that there are no pureR. reptans left in the British Isles and the creeping forms found at northern lakes are either R. flammula 'forma tenuifolius' or hybrids. Ranunculus flammula is a morphologically variable species and especially R. flammula 'forma tenuifolius' appears to be very similar to R. reptans (PADMORE 1957). However, in Central Europe it still remains to be investigated how often and to what degree natural hybridisation between the two species occurs. The typical habitats of the two species are well separated because R. rep tans does not occur in fens and bogs and R. flammula has never been observed growing at a lake shore FLORA (2000) 195

143

together with R. reptans. We only know from one population on a wet pasture at Lake Como where the two species occur close to each other and natural hybridisation seems likely.

founding of new populations at sites that were formerly colonised may be an important part of the management strategy for this species.

Acknowledgements

3.13. Status of the species Ranunculus reptans is indigenous in Central Europe at least since the last ice age. In Niedersachsen and Thtiringen R. reptans is extinct. In Schleswig-Holstein, MecklenburgVorpommem, Baden-Wtirttemberg, Bayem and .in Germany as a whole the species is on the Red List as a critically endangered plant (KORNECK et al. 1996). In Switzerland R. reptans is endangered (LANDOLT 1991). The number of populations in Central Europe declined drastically during the last decades mainly because of habitat destruction. The regulation of the water level of most pre-Alpine rivers and lakes has prevented yearly inundation of lake shores which appears to be essential not only for R. reptans, but for the whole community of Littorelletea. Human activities such as the construction of yacht harbours, public baths and camping grounds have destroyed further habitats (DIENST & WEBER 1993). In addition, eutrophication has led to the decline of the species in lakes in which fluctuations of the water level still occurs. Several mechanisms have been proposed for the negative impact of eutrophication on R. reptans (PEINTINGER et al. 1997). Increased nutrient availability could have promoted the growth of competitively superior species and nutrient increase may have stimulated algal growth which can destroy the community as alluvial deposits. In recent years clean water acts have reduced the negative impact of eutrophication and this might be one reason for the increase in the size of some populations at Lake Constance in the last ten years (PEINTINGER et al. 1997). However, other species may also profit from decreased eutrophication and this may lead to an increased competitive pressure on populations of R. reptans. Thus, the long-term effect of the change in water quality remains to be investigated. Nevertheless, since one can not assume that water level regulations which are the main cause for the decline of the species will be reversed, R. reptans must still be regarded as an endangered species in Central Europe. Further suitable habitats for R. reptans and other species of the Littorelletea-community should be created but only in one restoration project at Lake Constance a spontaneous colonisation by R. reptans has been reported (KRUMSCHEIDPLANKERT & SCHIJLLHORN 1993). The conservation strategy for this species should therefore be based on a strict protection of the remaining sites. Because dispersal appears to be rather limited and the establishment of new populations appears to be a rare event, artificial 144

FLORA (2000) 195

We are grateful to B. SCHMID and D. MATTHIES for encouraging to write this paper and to E. J. JAGER and an anonymous reviewer for many helpful informations. M. H. HOFFMANN kindly provided the map of distribution. Financial support was provided by the Swiss National Science Foundation, grant No. 31-39294.93 to Bernhard Schmid .

References AicHELE, D. & ScHWEGLER, H.-W. (1994): Die Bliitenpflanzen Mitteleuropas, Vol. 2. Franckh-Kosmos, Stuttgart. BARRETT, S.C. H., EcKERT, C. G. & HUSBAND, B. C. (1993): Evolutionary processes in aquatic plant populations. Aquat. Bot. 44: 105-145. BARYKINA, R. P. & PusTOVOYTOVA, V. I. (1973) Anatomomorphological study of Ranunculus repens L. and R. reptans L. in the ontogenesis (in Russian). Vestnik Moskovsk. Univ. Biol., 6: 28-39. BAUMANN, E. (1911): Die Vegetation des Untersees (Badensee). Schweizerbart, Stuttgart. BENNETT, M. D. & SMITH, J. P. (1976): Nuclear DNA amounts in angiosperms. Phil. Trans. Roy. Soc. Lond. B 274: 227-274. BENSON, L. (1955): The Ranunculi of the Alaskan arctic coastal plains and the Brooks Range. Amer. Midl. Natur. 53: 242-255. BocHER, T. W. (1938): Cytological studies in the genus Ranunculus. Dansk Bot. Ark. 9: 1-33. CLAPP, J.P., FITTER, A. H. & MERRYWEATHER, J. W. (1996): Arbuscular mycorrhizas. In: HALL, G. S. (ed.) : Methods for the examination of organismal diversity in soils and sediments. CAB International, Wallingford, 145-161. CooK, S. A. & JOHNSON, M.P. (1968): Adaptation to heterogenous environments. I. Variation in heterophylly in Ranunculusflammula L. Evolution 22:496-516. DIENST, M. & WEBER, P. (1993): Die Strandschmielen-Gesellschaft (Deschampsietum rhenanae 0BERD. 57) im westlichen Bodenseegebiet (Baden-Wiirttemberg, Thurgau). Limnol. aktuell5: 229-240. DIERSSEN, K. (1975): Zur Litoralvegetation oligotropher und mesotropher Gewiisser in Island und Nord-Norwegen. Beitr. naturk. Forsch. Stidw.-Dtl. 34: 57-77. ELLENBERG, H. (1996): Vegetation Mitteleuropas mit den Alpen, 5th edition. Ulmer, Stuttgart. ELLENBERG, H., WEBER, H. E., DULL, R., WIRTH, v. WERNER, W. & PAULISSEN, D. (1992): Zeigerwerte der Pflanzen in Mitteleuropa, 2nd edition. Erich Goltze KG, Gottingen. ERIKSSON, 0. (1989): Seedling dynamics and life histories in clonal plants. Oikos 55: 231-238. GADELLA, T. W. J. & KLIPHUIS, E. (1966): Chromosome number of flowering plants in the Netherlands. Verh. Koninkl. Nederl. Akad. Wetensch. C 69: 541-556.

GAUDET, C. L. & KEDDY, P. A. (1995) Competitive performance and species distribution in shoreline plant communities: a comparative approach. Ecology, 76: '280-291. GIBBS, P. E. & GoRNALL, R. J. (1976): A biosystematic study of the creeping spearworts at Loch Leven, Kinross. New Phytol. 77: 777-785. GLUCK, H. (1911): Biologische und morphologische Untersuchungen tiber Wasser- und Sumpfgewlichse. 3. Teil: Die Uferflora. G. Fischer, Jena. GRIME, P., HoDGSON, J. G. & HuNT, R. (1988): Comparative plant ecology : a functional approach to common British species. Unwin Hyman, London. HAEUPLER, H. & ScHONFELDER, P. (1989): Atlas der Farnund Bliitenpflanzen der Bundesrepublik Deutschland. Ulmer, Stuttgart. HARPER, J. L. ( 1977) : Population biology of plants. Academic Press, London. HEm, G. (1967): Illustrierte Flora von Mitteleuropa, Vol. 3. 3rd edition. Parey, Berlin. HESS, H. E., LANDOLT, E. & HIRZEL, R. (1980): Flora der Schweiz, Vol. 2. Birkhliuser, Basel. JALAS, J. & SuoMINEN, J. (1988): Atlas florae Europaeae: distribution of vascular plants in Europe. Cambridge University Press, Cambridge. JENSEN, K. (1912): Ranunculaceae. In: CoMMISIONEN FoR LEDELSEN AF DE GEOLOGISKE 0G GEOGRAPHISKE UNDERS0GELSER I GR0NLAND (ed.): Meddelelser om Gr!21nland. Seks og tredivte Hefte, 333-440. JoHANSSON, M. E. & NILSSON, C. (1993): Hydrochory, population dynamics and distribution of the clonal aquatic plantRanunculus lingua. J. Ecol. 81: 81-91. KoMAROV, V. L. (1937): Flora of the USSR, Vol. 7.lzdatel'stvo Akademii Nauk SSSR, Moskau, Leningrad. Translated from Russian ( 1970) : Israel Program fot·Scientific Translations, Jerusalem. KORNECK, D., SCHNITTLER, M. & VOLLMER, I. (1996): Rote Liste der Farn- und Bliitenpflanzen (Pteridophyta et Spermatophyta) Deutschlands. Schr.reihe Veg.kd 28: 21-187. KRUMSCHEID-PLANKERT, P. & SCHOLLHORN, W. (1993): Uferrenaturierung und Rohrichtschutz - Das E+E-Vorhaben ,Wiederansiedelung von Schilfbestlinden am Bodensee". Nat. Landschaft 68:403-411. LANDOLT, E. (1991): Gefahrdung der Farn- und Bliitenpflanzen in der Schweiz. Bundesamt fiir Umwelt, Wald und Landschaft BUWAL, Bern. LANG, G. (1967): Die Ufervegetation des westlichen Bodensees. Arch. Hydrobiol., Suppl. 32: 437-574. LANG, G. (1973): Die Vegetation des westlichen Bodenseegebietes. Pflanzensoziologie 17: 452 S. McLELLAN, A. J., PRATI, D., KALTZ, 0. & ScHMID, B. (1997): Structure and analysis of phenotypic and genetic variation in clonal plants. In: DE KRooN, H. & VAN GROENENDAEL, J. (eds) : The ecology and evolution of clonal plants, Backhuys Publishers, Leiden, 185-210. MoRIN, N. R. (ed.) (1997): Flora of North America (North of Mexico), Vol. 3. Oxford University Press, New York, Oxford. 0BERDORFER, E. & DIERSSEN, K. ( 1977) : Klasse Littorelletea

BR.-BL. ex Tx. 1947. In: OBERDOkFER, E. (ed.): Siiddeutsche Pflanzengesellschaften, Teil 1, 2nd edition. Fischer, Stuttgart, 182-192. P ADMORE, P. A. (1957) : The varieties of Ranunculus flammula L. and the status of R. scoticus E. S. MARSHALL and of R. reptans L. Watsonia 4: 19-27. PEINTINGER, M. (1994) : Untersuchungen zur Vegetationsdynarnik der Strandschrnielen-Gesellschaft im westlichen Bodenseegebiet. Diploma thesis, University ofWiirzburg, Wiirzburg, Germany. PEINTINGER, M. (1995): Die Strandschmielengesellschaft · (Deschampsietum rhenanae OBERDORFER 1957) im westlichen Bodenseegebiet - ein Vergleich von Vegetationsaufnahmen 1959 und 1993. Carolinea 53: 67-74. PEINTINGER, M., STRANG, 1., DIENST, M~ & MEYER, C. (1997): Verlinderungen der gefahrdeten Strandschmielengesellschaft am Bodensee zwischen 1989 und 1994. Z. Okol. Nat.sc. 6: 75-81. PIGNATTI, S. (1982): Flora d'Italia, Vol. 1. Edagricole, Bologna. PRATI, D. (1998): The genetics and life-history evolution of the clonal plantRanunculus reptans. Ph.D. thesis, University of Zurich, Zurich, Switzerland. SAND-JENSEN, K. & SoNDERGAARD, M. (1981): Phytoplankton and epiphyte development and their shading effect on submerged macrophytes in lakes of different nutrient status. Int. Revue Ges. Hydrobiol. 66: 529-552. ScHEERER, H. (1939): Chromosomenzahlen aus der Schleswig-Holsteinischen Flora 1. Planta 29: 636-642. ScHoNBECK, F. & SCijJ..OSSER, E. (1976): Preformed substances as potential'~rotectants. In: HEITEFuss, R. & WILLIAMS, P. H. (eds.): Physiological plant pathology. Springer, Berlin, 653-678. ScHROTER, C. & KIRCHNER, 0. (1902): Die Vegetation des Bodensees. 2. Teil. StettnerVerlag, Lindau. SEBALD, 0., SEYBOLD, S. & PHILIPPI, G. (1990): Die Farnund Bliitenpflanzen Baden-Wiirttembergs, Band 1. Ulmer, Stuttgart. SEREBRJAKOVA, T. J. (19Sl) Trudy M~skovsk. Obsc. lspyt. Prir. 56, 161-174. SoRSA, V. ( 1962): Chrorriosomenzahlen finnischer Kormophyten 1. Ann. Acad. Sci. Fenn. Ser. A IV, Biol. 58: 1-14. SPRINGER, S. (1996): Bemerkenswerte Pflanzengesellschaften in Siidbayem. Ber. Bayer. Bot. Ges. 66/67: 289-299. STACE, C. A. ( 1975): Hybridization and the flora of the British Isles. Academic Press, London. THOMAS, P., DIENST, M., PEINTINGER, M. & BUCHWALD, R. (1987): Die Strandrasen des Bodensees (Deschampsietum rhenanae und Littorello-Eleocharitetum acicularis): Verbreitung, Okologie, Gefahrdung und SchutzmaBnahmen. Veroff. Naturschutz Landschaftspflege Bad.-Wiirtt. 62: 325-346. TROLL, W. (1964): Die Infloreszenzen: Typologie und Stellung im Aufbau des Vegetationskorpers. G. Fischer, Jena. TUTIN, T. G., BURGES, N. A., CHATER, A. 0., EDMONDSON, J. R., HEYWOOD, V. H., MooRE, D. M., VALENTINE, D. H., WALTERS, S.M. & WEBB, D. A. (1993): Flora Europaea, 2nd edition. Cambridge University Press, Cambridge.

FLORA (ZOOO) 195

145