Recent distribution and phytosociological affiliation of Ludwigia palustris in Slovakia

Ludwigia palustris has always been a very rare species in Central Europe. In Slovakia, its occurrence remained unconfirmed for over 60 years and it was therefore considered extinct. The paper reports its rediscovery on two sites in SE Slovakia. Both localities were found in the Latorica River catchment area in 2015 when persistent summer droughts enabled the development of natural mudflat vegetation in the dried oxbows. Confirmation of this historic site indicates the long-term survival ability of the species. We assigned L. palustris dominated vegetation in the class Isoëto-Nanojuncetea, association Ludwigio palustris-Lindernietum procumbentis. This association is new to Slovakia as well as for Central Europe. The stands of this association developed on the exposed muddy shores of disconnected oxbow lake.

Ludwigia palustris is regarded as subatlantic-submediterranean-circumpolar species [8] with a large distribution range.It occurs in North America, central and northern part of South America, Africa (mainly in north and south parts of the continent), Asia (the temperate zone in the western part of the continent), and Europe.The European distribution range includes almost the entire continent except the N and NE parts.It is also known from the Caucasus (Georgia).Naturalized occurrence has been reported from Hawaii, Australia, and New Zealand [1,9,10].
In Central Europe, L. palustris is very rare.Most localities are situated in the western and southwestern parts of Hungary [11].In the Hungarian red list, it is evaluated as vulnerable [12].In Austria, the species is classified as critically endangered: although it is still present in southeastern part of the country, in western and southern regions it became already extinct [13][14][15][16].In the Czech Republic, the plant is listed as an extinct species with unresolved historic distribution [17,18].There are undated collections of Zahlbruckner from the vicinity of Nové Hrady (deposited in herbarium PRC), evidently from the first half of the nineteenth century.There is no further collection or published data from the Czech Republic after that time (Grulich, personal communication, 2016).In Poland, it was found only in three locations in the western part of the country, in the Nysa Łużycka River basin.The last report of the species is from 1928.Recently, L. palustris has been declared extinct in Poland [19].In Ukraine, L. palustris was found in a single location in the NE edge of the Pannonian lowland north of the town of Berehovo in the Čierny močiar marshland [20].The species disappeared recently as a consequence of the marshland's drainage [21].
In Slovakia, there were known four historic sites of the species until the first half of the twentieth century, later it was considered as a missing species [8,22,23], recently as probably extinct [24].
Regarding its life form, L. palustris is perennial [1] but sometimes reported also as therophyte or hydrotherophyte [8,22].Plants of the terrestrial form have more robust growth and shorter internodes, with smaller leaves than plants living in the water.The species habitat is restricted to lowland areas where it grows on shallow water bodies, e.g., in water reservoirs, ditches, and marshy banks of standing and slowly flowing waters.It requires wet, muddy, and sometimes flooded sandy soils poor in calcium and rich in nutrients and humus [8,19].
From the phytosociological point of view, in the study area, L. palustris is placed in the class Isoëto-Nanojuncetea, alliances Nanocyperion flavescentis and Elatini-Eleocharition ovatae [25,26], however, current data are lacking for Central Europe.Therefore, this study is aimed to (i) inform about both historical and recent localities of L. palustris in Slovakia, (ii) provide phytosociological data of stands with its presence in Slovakia, and (iii) compare the vegetation composition with other available published phytosociological data in the surrounding countries of Europe.

Study area
The field work was conducted in SE Slovakia in the Tisza River catchment area.Orographically it belongs to the Východoslovenská Lowland (SE Slovakia), which is the NE edge of the Pannonian Basin.The landscape is flat with minimal elevation difference (max.10 m), and is formed by a dense network of the rivers Ondava, Laborec, Latorica, and Bodrog.The longest section is that of the Latorica River, which was very rich in meanders in the past.After the redirection of the riverbed between 1953 and 1965, the meanders have been preserved as oxbows and cut backwaters [27].These places represent important areas for numerous wetland habitats rich in rare plant species within the intensively used landscape.

Collection and processing of data
The data concerning the distribution of the species were collected from herbaria BRA, BRNM, BRNU, SLO, PR, PRC, and SAV.Herbarium abbreviations are according to Vozárová and Sutorý [28].The result of this study is presented on the grid map.The map was designed by the program ArcGis, version 9.2.Coordinates of historical localities were taken from Google Earth.Coordinates of recent localities were obtained during field research using GPS equipment (Garmin CS 60); the numbers of grid squares follow Niklfeld [29].
The phytosociological relevés were sampled according to the Zürich-Montpellier approach using the adapted 9-grade Braun-Blanquet's scale [30].The species nomenclature for vascular plants follows Flora Europaea [31] and the names of syntaxa follow Jarolímek et al. [32], plant communities not included in the above-mentioned reference are supplied with author abbreviations.

Historical occurrence of Ludwigia palustris in Slovakia
Based on the herbarium collections, L. palustris was documented in four locations in Slovakia (Fig. 1): in the Borská Lowland (W Slovakia) on the bank of the Rudava River in an area near the Studienka settlement (Staněk 1948 BRNU, SLO, PR, PRC) and in the Východoslovenská Lowland (SE Slovakia) in two sites close to each other, Zatín, oxbow of the Latorica River in the confluence area with the Laborec River (Staněk 1947 BRNM) and Oborín, in the lower part of the woodlands in the confluence area of the above-mentioned rivers (Staněk 1947 BRNM, BRNU).The fourth historical locality was found also in the bank of the Latorica River near the bridge of the road to Kráľovský Chlmec (Holub 1952 ined. in [22]), however, herbarium specimen documenting this locality is missing.

Ludwigia palustris population and vegetation composition on recent locality No. 1
The first recent locality is situated near Zatín settlement in the dried oxbow of the Latorica River inundation area.After the water decrease shallow muddy banks of the internal oxbow were densely covered with Nuphar lutea, and L. palustris grew on the margins of the oxbow accompanied by other dwarf therophytes.Stands of L. palustris covered ca.70 × 20 m, while on a quarter of the occupied area its cover reached more than 25%.The populations were concentrated closer to the drier riverbank.The mentioned locality is identical with the historical site of L. palustris where original flow of the Latorica River was situated in the past (above-mentioned herbarium collection of Staněk).In spite of the river regulation, L. palustris has been preserved on the site.The vegetation is characterized by Relevés 1-3 in Tab. 1.According to the species composition, we assign Relevés 1 and 2 into the class Isoëto-Nanojuncetea, alliance Elatini-Eleocharition ovatae, association Ludwigio palustris-Lindernietum procumbentis Felzines, Loiseau & Portal 2002.On the same site, closer to the Magnocaricion belt among the dense stands of Scirpus radicans prostrate, low-herb stands of mudflat vegetation were found, together with a small population of L. palustris (Relevé 3; Tab. 1).The vegetation belongs to the association Scirpetum radicantis from the alliance Oenanthion aquaticae within the class Phragmito-Magnocaricetea.In this stand, L. palustris had only a marginal occurrence.

Ludwigia palustris population and vegetation composition on recent locality No. 2
The second recent locality was found between Kráľovský Chlmec and Veľké Kapušany at the bridge crossing the Latorica River.This recently found site is identical to locality mentioned by Holub.The species was observed within an 80-meter-long section of the river in about 10-18 meters wide belt of the exposed bottom reaching from the decreased water level to the oxbow shoreline overgrown with tussocks of perennial sedges (e.g., Carex acuta, C. acutiformis, C. melanostachya).Ludwigia palustris has occured here sporadically in small groups and also in large (>100 m 2 ) carpet-like stands depending to length of flood and bottom exposure.Carpet-like stands have occurred on dryer sites which were exposed for longer time; small groups of L. palustris individuals have occupied wet, shortly exposed parts of river bank closer to water level.The vegetation of Relevé 4 is similar to Relevés 1 and 2 (Tab.1), therefore, we included it to the association Ludwigo palustris-Lindernietum procumbentis.

Vegetation of Ludwigia palustris in Slovakia
There was not available phytosociological material about the vegetation of L. palustris in Slovakia.One remark gave Dostál [8] indicating it as part of the alliances Nanocyperion flavescentis, Elatini-Eleocharition ovatae, and Magnocaricion elatae, but it is not clear whether it is based on data from Slovakia.The only brief species list was available in labels of Staněk's herbarium vouchers of L. palustris.In SE Slovakia near Zatín, L. palustris occurred together with Trapa natans, Alisma plantago-aquatica, Oenanthe aquatica, and Echinochloa crus-galli (Staněk 1947 BRNM).From this poor list of species, is not clear what type of vegetation was occupied by L. palustris.In the same region, near Oborín, Staněk (1947 BRNM, BRNU) reported the species in low swards with Cyperus michelianus, C. fuscus, Lindernia procumbens, Gnaphalium uliginosum, Alisma plantago-aquatica, Echinochloa crus-galli, and Eleocharis acicularis.The species composition indicates a typical stand of the alliance Elatini-Eleocharition ovatae from the class Isoëto-Nanojuncetea.

Occurrence in Slovakia
In Slovakia, the oldest remark of L. palustris was published by Polívka et al. [20] from the Latorica River (SE Slovakia) without a particular localization and dating.Shortly after WWII, Staňek collected the most data (a single site in W Slovakia as well as in two sites in the south-east).The last historic data were given in early fifties from the Latorica River, near the bridge on the road to Kráľovský Chlmec (Holub 1952 in [22]).Since 1953, it has been considered as a missing species in Slovakia [8,23], or as probably extinct [24].Later, the botanical research in the area was scarce and has become more intensive again in the last 20 years.Several valuable records on rare plants of exposed bottoms were obtained, e.g., Carex bohemica [33], Lindernia procumbens, Cyperus michelianus, Heleochloa alopecuroides [34][35][36], Elatine hungarica [37], or Isolepis supina [38].However, the origin of L. palustris in both recent localities is more likely to be related to the synergic effect of favorable climatic conditions and persistent seed bank than the intensity of research in the area.The late summer of the year 2015 was characterized by extremely high temperatures in Central Europe [39].
The recent occurrence of L. palustris is associated with the persistent summer droughts when the river oxbows provided suitable conditions for the species with optimum on exposed bottoms of water bodies, including L. palustris.
Similarly as the re-discovery of Cyperus glomeratus in Slovakia, which was found after 60 years in exposed banks of the Danube River [36,40].Analogous examples are other rare hydrophilic plants, e.g., Elatine species, which occurrence significantly increased with high annual rainfall and the extent of inundated area [37,41].Extreme moist or dry conditions enable the species to supplement/renew the seed bank and increase the probability of their long-term survival [42].It is also well known that seeds of amphibian plants are able to germinate after several decades from the soil seed bank (e.g., [43][44][45][46]).
In the Sava River basin of Croatia, L. palustris is reported in the class Isoëto-Nanojuncetea, in the association Cyperetum flavescentis.It occupies wet margins of shallow flooded depressions after the water retreats.Besides L. palustris, Cyperus flavescens, Eleocharis acicularis, Juncus bufonius, and Hypericum humifusum occur [55].
In Western and Southern Europe, where L. palustris is more common, it has been recorded in numerous other communities of aquatic and wetland vegetation.A comprehensive revision of the class Isoëto-Nanojuncetea provided Brullo and Minissale [56].The alliance Elatino-Eleocharition ovatae is included in this class, in which L. palustris figures in six associations, in each case with high constancy (III).The highest constancy (IV) is found in the association Eleocharito acicularis-Lindernietum procumbentis Pignatti 1957.Ludwigia palustris is also present in another three associations in the alliance Verbenion supinae Slavnić 1951 within the mentioned class.Felzines et al. [57] described the association Ludwigio palustris-Lindernietum procumbentis based on vegetation occurred in the La Dordogne River basin (SW France), and included it in the alliance Elatini-Eleocharition ovatae.The vegetation occupies dried shores of river oxbows which are wet through the entire growing season.The exposed bottom is usually sandy to loamy and L. palustris prefers shaded areas.Both characteristic species, L. palustris and Lindernia procumbens, cover 5-75% of the patches areas [57].The third characteristic species is Callitriche brutia, but this species is found only with minimal cover.According to third version of the "International code of phytosociological nomenclature", this description is not valid for improper use for the type relevé name (holotype vs. holotypus) [58].However, some specialists suggest that essentially correctly described syntaxa would not be considered invalid for these formal errors in fourth version of the Code (L.Mucina, personal communication, 2016).
De Foucault [59] in his extensive study of periodically flooded habitats of France, added into the characteristic species of the Ludwigio palustris-Lindernietum procumbentis more taxa: Eleocharis ovata, Cyperus fuscus, and Persicaria hydropiper.He also included it in the alliance Elatini-Eleocharition ovatae.In the same alliance, he distinguishes one more association with dominance of L. palustris and determines it as Lythro portulae-Ludwigietum palustris Robbe ex J.-M.Royer, Felzines, Misset & Thévenin 2006.This thermophilous association was also recorded by Guillereme and Galtier [60], who observed it in periodically inundated riverbanks, depressions, and water reservoirs in the Loire River basin.
In Spain, Rivas Martinez et al. [61] described the association Ludwigio palustris-Cyperetum micheliani and assigned it to the alliance Nanocyperion flavescentis.It is included in the same alliance by Costa el at.[62].On the contrary, Brullo and Minissale [56] include this association in the alliance Verbenion supinae.In the published phytosociological relevés [61] of the association Ludwigio palustris-Cyperetum micheliani, Cyperus michelianus attains the highest cover, while C. fuscus reaches lower levels.Other constant but less dominant species are L. palustris, Cynodon dactylon, and Paspalum vaginatum.This vegetation consists mainly of therophytes and occupies sandy banks of rivers and flat depressions flooded until the beginning of summer [61,63].
Dimopoulos et al. [68] reported several communities with L. palustris over a large area of the Kalodiki Fen in Greece.As a characteristic species they indicate Phalaris arundinacea.The frame community of P. arundinacea occurs in nutrient-rich waters on mineral or organic soils with strongly fluctuating water level in summer.From the same area, they defined the plant community Ludwigia palustris and included it in the class Bidentetea tripartitae, alliance Bidention tripartitae.The species-poor stands are developed by the dominance of L. palustris and Agrostis stolonifera, while Utricularia australis appears less frequently.It occurs only rarely in moderately drying calciumpoor eutrophic marshes grazed by water birds.
From the Balkans (Skadar Lake on the Montenegro side), Lakušić and Pavlović [69] described new association Ludwigietum palustris as part of the class of strictly aquatic vegetation Potametea.This community is created by a significant dominance (>75%) of L. palustris and the dense stands of the submerged form of the plant are accompanied by low cover of Persicaria amphibia.Lakušić and Pavlović [69] mentioned several other associations of aquatic vegetation where L. palustris is present in low cover, for instance, Potametum perfoliati and Nyphoidetum peltatae.The cover of Nyphoides peltata exceeds 50% here, while Persicaria amphibia and L. palustris are less dominant.

Conclusions
Ludwigia palustris, a missing species of Slovak flora was recently confirmed at two historical localities in SE Slovakia (Zatín, Kráľovský Chlmec), over more than 60 years.It demonstrates the long-term survival of the species on the sites due to its persistent soil seed bank.Since the local habitat conditions changed rapidly, the occurrence is probably dependent on the particular climatic conditions.
Phytosociological relevés provide the first coenological data on L. palustris for Slovakia.After comparison with the available European phytosociological studies, we classified our relevés dominated by L. palustris as the association Ludwigio palustris-Lindernietum procumbentis (alliance Elatini-Eleocharition ovatae, class Isoëto-Nanojuncetea).This plant community was previously known neither from Slovakia nor from the other countries of Central Europe, therefore, our data enlarges the knowledge about its recent distribution.For the first time, the species is reported from the association Scirpetum radicantis (Phragmito-Magno-Caricetea class).Reasons why L. palustris was not yet recorded in this community are probably related to its limited distribution as well as quite scarce occurrence of Scirpetum radicantis even in the countries in which it is reported [70][71][72][73].
In eastern part of the Central Europe, on the western border of its European distribution, the species has narrower ecological and coenological amplitude.Although it was rarely recorded in stands of the class Phragmiteto-Magno-Caricetea (alliance Magnocaricion elateae), its optimal vegetation conditions are in the class Isoëto-Nanojuncetea, in two alliances: Nanocyperion flavescentis and Elatini-Eleocharition ovatae.These plant communities have recently become very rare due to habitat destruction, river regulation and eutrophication [43,53,74].Therefore, L. palustris is there more endangered than in Western and Southern Europe, where it occurs in a large variety of wetland vegetation [75], at least in five different classes (Isoëto-Nanojuncetea, Bidentetea tripartitae, Phragmito-Magnocaricetea, Potametea, and Litorelletea uniflorae).

Fig. 1
Fig. 1 Distribution of Ludwigia palustris in Slovakia: white circles -historical localities; black circles -recently confirmed localities.
Tab. 1 Phytosociological table of Ludwigia palustris relevés sampled during the study in Slovakia.