Vegetation diversity of salt-rich grasslands in Southeast Europe

Applied Vegetation Science && (2012)

SPECIAL FEATURE: GRASSLAND CLASSIFICATIONVegetation diversity of salt-rich grasslands inSoutheast Europe

Pavol Eli�a�s Jr, Desislava Sopotlieva, Daniel D�ıt�e, Petra H�ajkov�a, Iva Apostolova,Du�san Senko, ZuzanaMele�ckov�a &Michal H�ajek

Keywords

Balkan region; Classification; Europe;

Grassland; Halophytic habitats; Pannonian

region; Saline habitats; Vegetation survey

Nomenclature

Tutin et al. (1964–1980, 1993)

Received 2 January 2012

Accepted 16 November 2012

Co-ordinating Editor: Wolfgang Willner

Virtual Special Feature “Towards a consistent

classification of European grasslands”

(Eds. Jurgen Dengler, Erwin Bergmeier,

Wolfgang Willner & Milan Chytry)

H�ajek, M. (corresponding author, hajek@sci.

muni.cz), H�ajkov�a, P. ([email protected]) &

Sopotlieva, D: Department of Botany and

Zoology, Faculty of Science, Masaryk

University, Kotl�a�rsk�a 2, CZ-61137, Brno, Czech

Republic

D�ıt�e, D. ([email protected]) & Senko, D.

([email protected]) &Mele�ckov�a, Z.

([email protected]): Institute of

Botany, Slovak Academy of Sciences,

D�ubravsk�a cesta 9, SK-845 23, Bratislava,

Slovakia

Eli�a�s, P. Jr. ([email protected]):

Department of Botany, Slovak University of

Agriculture, Tr. A. Hlinku 2, SK-94976, Nitra,

Slovakia

Sopotlieva, D. ([email protected]) &

Apostolova, I. ([email protected]):

Institute of Biodiversity and Ecosystem

Research, Bulgarian Academy of Sciences,

2 Gagarin Street, BG-1113, Sofia, Bulgaria

H�ajek, M. &H�ajkov�a, P.: Department of

Vegetation Ecology, Institute of Botany,

Academy of Sciences of the Czech Republic,

Po�r�ı�c�ı 3b, CZ-60300, Brno, Czech Republic

Abstract

Question: How does the plant species composition of Pontic–Pannonian salt-

rich habitats vary on a large geographical scale? Do the floristic differences

between Pannonia and the Balkans correspond to the current phytosociological

classification?

Location: Pannonia (Hungary, Slovakia, Austria, Czech Republic, Croatia, Ser-

bia, Romania) and the Balkans (Bulgaria, Macedonia, Greece).

Methods: Two thousand four hundred and thirty-seven relev�es from halo-

phytic and sub-halophytic habitats were classified using a modified TWINSPAN.

The crispness of classification was checked. DCA and CCA with climate data as

explanatory variables were applied.

Results: The classification was best interpreted at the level of 15 clusters. The

vegetation changed along the salinity gradient from sub-halophytic grasslands

(including Trifolion resupinati alliance of the Molinio-Arrhenatheretalia class and

Beckmannion eruciformis and Festucion pseudovinae p. p. alliances of the Festuco-

Puccinellietea class) and reed beds (Bolboschoenion maritimi p. p. alliance; the

Phragmito-Magnocaricetea class), through steppe and wet inland halophytic veg-

etation (Festucion pseudovinae p. p., Puccinellion limosae, Pucinellion convolutae, Bol-

boschoenion maritimi p. p. and Juncion gerardii of the Festuco-Puccinellietea class)

towards the extreme halophytic vegetation of the Thero-Salicornietea, Crypsietea

and Juncetea maritimi classes. This gradient was longer in the Balkan region,

where it spanned from the sub-mediterranean salt-rich grasslands to the extre-

mely halophytic vegetation at the Black Sea coast. The second most important

gradient coincided with the water regime. Some vegetation types appeared to

be confined to either the Pannonian or the Balkan region (especially within

dry sub-halophytic and steppe halophytic grasslands), while others were dis-

tributed across the entire study area. The above-mentioned pattern did not

always correspond with current classification systems.

Conclusions: Variation in salt-rich vegetation predominantly follows the

salinity and water regime gradients. Geographical variation, generally coincid-

ing with climatic and historical effects, is also important, especially in drier

salt-rich habitats. Our large-scale analysis of the floristic variation of salt-rich

habitats might be useful for the unification of classification systems that differ

substantially between the countries involved. In addition, the analysis may be

useful for adjustment of a classification system in the poorly explored Balkan

region, where particular vegetation types were identified with, or delimited

from, Central European vegetation types without detailed comparative

analysis until now.

Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 1

Introduction

During the last decade, developments in the compilation

of vegetation plot databases (Schamin�ee et al. 2009) have

led to an effort to create classification systems valid across

large areas that would serve, for example, as a basis for

interpretation of the habitats of European conservation

interests within the Natura 2000 network (Council Direc-

tive 92/43/EEC 1992). In such a way, vegetation survey

was integrated into applied vegetation science, and started

to focus on analysing large data sets that span national

boundaries (Botta-Duk�at et al. 2005; Illy�es et al. 2007;

D�ubravkov�a et al. 2010; Michl et al. 2010; Rozbrojov�a

et al. 2010; Sekulov�a et al. 2011). So far, these studies

have been strongly biased towards Central Europe, where

the most complete vegetation databases exist. In addition,

some threatened habitats, such as inland halophytic wet-

lands, have not yet been included in trans-national vegeta-

tion surveys, including those of Central Europe. Although

there is a series of large-scale trans-national vegetation sur-

veys of halophytic vegetation published (Golub 1994;

Golub et al. 2001, 2003), only the survey of the Festuco-

Puccinellietea class comprises the territory of Central and

Southern Europe (Golub et al. 2005). The latter study,

however, used an analysis of published synoptic tables in

order to present a vegetation synthesis and to describe new

higher-rank syntaxa. Any study using individual relev�es is

still missing.

The lack of detailed knowledge about the large-scale

variation of inland halophytic vegetation is caused by two

interacting factors. First, this vegetation is rare, geographi-

cally restricted to relatively small areas and recently disap-

pearing as a result of human pressure, such as afforestation

and land reclamation. This pattern especially holds in the

otherwise well-explored region of Central Europe, where

halophytic vegetation is most abundant in Hungary

(Moln�ar & Borhidi 2003). Second, vegetation plot databas-

es have not yet been created in some European regions,

especially in Southeast Europe, where a traditional Braun-

Blanquet phytosociological approach has been less fre-

quently applied in the past (Tzonev et al. 2009). When the

classification system of halophytic vegetation started to be

created in SE Europe (Tzonev et al. 2008, 2009), particular

vegetation types were only identified with, or delimited

from, Central European vegetation types without detailed

comparative analysis. Some salt-rich habitats (e.g. sub-hal-

ophytic grasslands with Beckmannia eruciformis or vegeta-

tion with Carex divisa and Juncus gerardii) were never

sampled in SE Europe using the phytosociological

approach.

Large-scale patterns in halophytic and sub-halophytic

vegetation were not sufficiently analysed in the well-

explored Pannonian region of Central Europe. Although

many local and regional vegetation studies were published

in most countries of the Pannonian region (Wendelberger

1943; So�o 1947; Slavni�c 1948; Bodrogk€ozy 1962, 1965a,b,

1970; Bodrogk€ozy & Gy€orffy 1970; Vicherek 1973;Mucina

1993; Pop 2002; Moln�ar & Borhidi 2003; D�ıt�e et al. 2010),

only one complete vegetation survey of the entire territory

was published, based on data from Austria and Hungary

(Wendelberger 1950). Thus, not only a detailed compara-

tive analysis between Central and Southern Europe, but

also a current synthesis of halophytic and sub-halophytic

vegetation of Pannonia is needed.

The problems with habitat rarity in Central Europe and

the lack of vegetation data from SE Europe imply that a

detailed large-scale vegetation survey requires field

research in order to fill in missing data, together with

efforts to digitize the scarce literature data. Here a trans-

national vegetation survey of Pannonian and Balkan halo-

phytic and sub-halophytic vegetation is presented, which

covers the territory of ten European countries and uses

both database data from Central Europe, and a large

amount of originally gathered field data and originally digi-

tized literature data from SE Europe. Considering the large

vegetation variability and large geographical area covered,

this paper is not ultimately aimed at creating a final syn-

taxonomical system, but rather at exploring how the plant

species composition of salt-rich habitats varies on a large

geographical scale, including regions that are largely unex-

plored so far. A further aim is to determine whether floris-

tic similarities or differences between Pannonian and

Balkan halophytic vegetation correspond to current phyto-

sociological classifications applied in different countries.

Methods

Study area

In SE Europe, halophytic vegetation is developed predomi-

nantly in the continental Pannonian Basin, where it has

been described in detail, especially for Hungary, and in the

Eastern Balkan region, where only scarce local studies

have been performed so far. This Pannonian–Balkan

region forms a large but rather compact area, where a large

amount of vegetation data from a wide set of spatially

explicit localities are available, either from our own

research or from vegetation-plot databases (Fig. 1).

Geographically, the Pannonian Basin is situated at the

boundary between Central Europe, Eastern Europe and

the Balkans. It forms a topographically discrete unit set

within the European landscape, surrounded by obvious

geographic boundaries – the Carpathian Mountains, the

Alps, the Dinarides and the BalkanMountains (Hoffman &

Davies 1983). It consists of a large Neogene basin, which

spans ca. 600 km from east towest and 500 km from north

to south, and was recently filled by a thick layer of fluvial

Applied Vegetation Science2 Doi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science

Vegetation of salt-rich grasslands P. Eli�a�s et al.

and aeolian sediments (Fodor et al. 1999; Nem�cok et al.

2006). The Balkan Peninsula constitutes an irregular trian-

gle situated in SE Europe. While southern and eastern

boundaries are relatively clear, the northern and western

boundaries have been treated differently (Reed et al.

2004). The salt-affected soils are predominantly situated in

lowlands to the north and east. These lowlands are usually

covered by thick layers of Tertiary and Quaternary sedi-

ments (Reed et al. 2004), and reach the southernmost

extension of the Pannonian Basin to the west.

From the climate point of view, the Pannonian Basin is

included in a temperate, continental steppic bioclimatic

region (Rivas-Martınez & Rivas-Saenz 2009). This conti-

nental climate zone usually has cold, snowy winters and

hot, dry summers. The average annual temperature is

about 10 °C, and annual precipitation is ca. 400–500 mm

in the central region (the Great Hungarian Plain) and 500–

600 mm in the northwest area (the Danube lowland).

Severe droughts may occur in the summer (Borhidi 1961;

Mikl�os 2002). In the Balkans, the prevailing mountainous

character of the region determines the significant climate

diversity. The mean annual temperature of the lowlands is

between 10 and 13 °C (Nikolova 2002); precipitationmax-

imum for central parts of the Balkans occurs during spring,

and for most of the region ranges between 500 and

750 mm. In the southern parts (Tracian plane, Eastern

Rhodopes, Strandja) rainfall is of the Mediterranean type

and is at a maximum during the autumn and winter

(Mateeva 2002). In the mountains, the temperature tends

to fall with altitude, while precipitation increases.

Salt-affected soils, as an essential element for the forma-

tion of halophytic and sub-halophytic vegetation, occur

particulary in arid and semi-arid regions where the strong

concentration of salts in the soil is caused by high evapora-

tion of water in the summer (negative balance of precipita-

tion) and specific geological and geomorphological

conditions of the area. Formation of the saline soil is also

supported by the chemical composition of the parent rock

(Abrol et al. 1988). In Pannonia, salt-affected soils are nat-

urally more common than in the Balkans (Panagos et al.

2012; Fig. 1). They are found in the zone between cher-

nozems and meadow soils, where a seasonal fluctuation of

groundwater levels frequently occurs. Solonchaks pre-

dominate in the coarse-grained calcareous sediments of

the Danube River, while in the acidic, fine-grained sedi-

ments of the Tisza River Solonetz soil is formed (Szabolcs

1974). The supposed age of salt-affected soils in the Panno-

nian basin is 7000–5000 yrs in most cases (Stefanovits

1981). In the Balkans, salt-rich soils are of natural origin

but expand as a consequence of anthropic influence in

some cases. Areas of salt-rich soils are not extensive. In the

Republic of Macedonia, for example, they cover ca.

11 000 ha (Mitkova & Mitrikeski 2005). The formation of

these soils is determined by the basic rock influence com-

bined with topographic–hydrographic conditions and,

especially, saline groundwaters. In Ovche Pole (Republic

of Macedonia) there are the most salinized groundwaters

found in the Balkans, with predominant Na2SO4 (Mitkova

& Mitrikeski 2005). In Bulgaria, saline soils constitute two

main types (Solonetz and Solonchaks), which are mainly

distributed in southeast Bulgaria and in one region of the

Danube lowland (Fig. 1). The salinization in Bulgaria is

mostly of the sulphate–chloride type (Ninov 2002).

Study vegetation, vegetation sampling and re-sampling

We focused on all vegetation types with the occurrence of

sub-halophytic and halophytic species, regardless of the

Fig. 1. Distribution of salt-affected soils in the study area and localities of

analysed relev�es. The map shows the distribution area of saline, sodic and

potentially salt-affected areas within the European Union. The accuracy of

input data only allows the designation of salt-affected areas with a limited

level of reliability (e.g. <50% or >50% of the area). The data were digitized

from the ‘Map of Saline and Sodic Soils in the EU’ created by Gergely Toth,

Land Management and Natural Hazards Unit, Institute for Environment &

Sustainability, European Commission DG Joint Research Centre in 2008

(Panagos et al. 2012).


P. Eli�a�s et al. Vegetation of salt-rich grasslands

traditional syntaxonomic classification. This object delimi-

tation therefore comprises, in this study area, the truly

halophytic classes Thero-Salicornietea, Crypsietea, Juncetea

maritimi and Festuco-Puccinellietea, as well as different

vegetation types from the Molinio-Arrhenatheretea and

Phragmito-Magnocaricetea classes, which were assigned as

sub-halophytic in the literature (Wendelberger 1950;

Micevski 1965; Vicherek 1973; Mucina 1993; Pop 2002;

Borhidi 2003; Tzonev et al. 2009). Therefore also grassland

or reed (e.g. Bolboschoenus maritimus, Cyperus longus, Scirpus

lacustris subsp. tabernaemontani) vegetation was sampled

when it occurred in salt marsh complexes and contained

sub-halophytic or halophytic species. At each location vis-

ited, particular zones of vegetation were recognized, and

only one vegetation plot of 4 9 4 m was sampled from

each vegetation zone. Vegetation zones were usually

defined by the dominance of some species. Because only

one plot per vegetation type at each locality was sampled,

the data set was not stratified.

In the next step, the data set was enlarged using the

unpublished historical vegetation plot records (relev�es) of

Ji�r�ı Vicherek in Bulgaria, in order to cover vegetation types

and localities that could have become extinct during the

last few decades. Altogether, 897 new and 272 of Vicherek′

s relev�es were collected. Databases and published sources

were only used to fill in certain gaps in the research,

because these generally suffer from many inconsistencies

(Jansen & Dengler 2010; Michalcov�a et al. 2011). Pub-

lished relev�es from Bulgaria (Tzonev 2002, 2009; Tzonev

et al. 2008), Macedonia (Micevski 1964, 1965, 1978) and

Greece (Raus 1983) originate from regions and localities

different from those that we explored. They were therefore

digitized and used in this study. Furthermore, the Czech

National Phytosociological Database (Chytr�y & Rafajov�a

2003) was used to obtain relev�es from the Moravian part

of the Pannonian lowland (Czech Republic), where most

localities have already disappeared and only historical plots

are available. From this source, relev�es of all target vegeta-

tion types were taken (halophytic Thero-Salicornietea, Cryp-

sietea, Festuco-Puccinellietea, sub-halophytic Bolboschoenion

and Potentillion anserinae). Finally, relev�es of the sub-halo-

phytic vegetation were taken from the Central Database of

Phytosociological Samples (CDF) of Slovakia (Heged€u�sov�a

2007), using the same units as for the Czech Republic plus

Beckmannion eruciformis. Truly halophytic vegetation in

Slovakia was sampled from research of D.D., P.E. and Z.M.

After merging all of our field data and that from the lit-

erature, the nomenclature of all species was checked and

synonyms merged appropriately. In addition, the taxa

whose correct determination in the literature data or

taxonomic status was unclear were merged with allied

species (e.g. Taraxacum species; Achillea millefolium

agg. = A. collina, A. millefolium, A. pannonica, A. setacea;

Agrostis stolonifera agg. = A. canina, A. stolonifera; Arenaria

serpyllifolia agg. = A. serpyllifolia, A. leptoclados; Aster novi-

belgii agg. = A. novi-belgii, A. laevis, A. lanceolatus; Bolbo-

schoenus maritimus agg. = B. maritimus, B. yagara, B. ko-

shewnikowii; Carex vulpina agg. = C. otrubae, C. vulpina;

Eleocharis palustris agg. = E. palustris, E. uniglumis; Galium

palustre agg. = G. palustre, G. uliginosum; G. verum agg.

= Galium verum, G. wirtgenii; Glyceria fluitans agg. = G. flui-

tans, G. nodosa; Chenopodium album agg. = C. album, C. stric-

tum, C. suecicum; Juncus bufonius agg. = J. bufonius, J.

ranarius; Leucanthemum vulgare agg. = L. ircutianum, L. vulg-

are; Myosotis palustris agg. = M. palustris, M. scorpioides, M.

laxiflora, M. nemorosa, M. sicula; Orchis laxiflora agg. = O. lax-

iflora, O. elegans, O. palustris; Pimpinella saxifraga agg. =P. saxifraga, P. major; Polygonum aviculare agg. = P. aviculare,

P. rurivagum; Salicornia europaea agg. = S. europaea, S. herba-

cea; Poa pratensis agg. = Poa pratensis, P. angustifolia, P. hum-

ilis; Puccinellia distans agg. = P. distans, P. limosa, P. peisonis;

Thymus pannonicus agg. = T. pannonicus, T. glabrescens).

The first run of numerical classification created some

clusters that contained no relev�es with either halophytic or

sub-halophytic species (e.g. monospecific growths of Bolbo-

schoenus maritimus agg. from published relev�es), which

were deleted from the data set. Some clusters were further

composed of relev�es sampled in a few over-sampled locali-

ties (especially from the literature sources Vicherek 1973

and Tzonev et al. 2008). In that case, the data from these

clusters were re-sampled through random selection of

three relev�es from each locality. After these modifications,

the data set contained 1268 relev�es from the literature.

The total number of analysed relev�es was 2437, with 795

species or aggregate species involved. For each relev�e, the

climate data were obtained from the WorldClim model

(variables BIO1-BIO19; Hijmans et al. 2005).

Numerical analyses

Modified TWINSPAN (Role�cek et al. 2009) was used, with

three pseudo-species cut-off levels (0%, 5% and 25%) and

total inertia as a heterogeneity measure. The crispness of

classification was checked using the method in Botta-

Duk�at et al. (2005), and the OptimClass1 method (Tich�y

et al. 2010). The first method revealed the highest crisp-

ness at the level of four clusters and it decreased gradually

when the number of clusters increased. The peak of the

OptimClass1 curve, with Fisher′s exact test cut-off level

P = 10�30, appeared at the level of 17 clusters. From these

clusters, one cluster contained only four species-poor

relev�es with Petrosimonia triandra and Artemisia santonicum

from the literature, which was merged with the closest

cluster (cluster 6 characterized by A. santonicum) in order

to simplify the results. Further, two clusters characterized

by Puccinellia distans, appearing after the last division, were



merged into a single cluster because we did not find any

ecological, geographical or syntaxonomical intepretations

for them. We created a synoptic table, in which frequency

values are shown. We show those diagnostic species with

the Φ-coefficient of association to at least one cluster

� 0.4. The size of the clusters was standardized to equal

size of 15% of the data set (Tich�y & Chytr�y 2006). Only

species with statistically significant affinity to a cluster

according to Fisher′s exact test with P < 0.001 were con-

sidered.

The entire final data set was subjected to detrended cor-

respondence analysis (DCA) with the same three pseudo-

species cut-off levels, without down-weighting rare

species, and centroids were calculated for each of the 15

clusters. The distribution of Pannonian and Balkan relev�es

was also shown in ordination space. Because the ordina-

tion of the complete data set might only show a very gen-

eral pattern, the major gradients were also explored for a

restricted data set, where some clusters representing the

extreme ends of the gradient were omitted. Using canoni-

cal correspondence analysis (CCA), with log-transformed

plant cover values, the relationships between large-scale

climate data and species composition of the vegetation data

were tested. The explanatory power of each climate vari-

able was also tested with the Monte Carlo permutation test

(reduced model, 499 permutations) and a manual forward

selection procedure was used to select the twomost impor-

tant variables. These two important predictors were then

mapped in order to describe the most important inter-

regional differences in climate.

Results

Classification

Although 15 clusters were interpreted in a finer classifica-

tion (Table 1, see full version in Appendix S1, distribution

maps in Fig. 2 and photos in Appendix S2), the most crisp

classification occurred at the level of four clusters (Fig. 3),

and can be interpreted as follows: A – vegetation of sub-

halophytic habitats (clusters 1–4), B – vegetation of steppe

halophytic habitats (clusters 5–9), C – vegetation of wet

halophytic habitats (10–13), and D – vegetation of extreme

halophytic habitats (clusters 14, 15).

Group A includes vegetation of sub-halophytic habitats.

However, while the vegetation in cluster 1 was rather

evenly distributed across the regions, three other clusters

are clearly defined geographically. Cluster 1 represents the

sub-halophytic wetlands with tall graminoids, which is

traditionally classified within the Beckmannion eruciformis

alliance and the Loto-Trifolienion suballiance of Agropyro-

Rumicion crispi. They are developed on meadows and pas-

tures of moist or wet slightly saline soils in the floodplains

in steppe zones of both the Pannonian (Romania, Slovakia)

and Balkan regions (Bulgaria, Greece, Macedonia). Physi-

ognomy of the communities is determined by tall, usually

persistent, plants such as Alopecurus pratensis, A. creticus,

Beckmannia eruciformis, Cirsium brachycephalum, Eleocharis pa-

lustris agg. and Scirpus lacustris subsp. tabernaemontani. Cluster

2 represents the Balkan sub-halophytic wet grasslands of

the Trifolion resupinati alliance, with a few exceptions. The

stands are developed in meadows occurring at periodically

flooded, slightly saline soils in SE Europe (Bulgaria, Mace-

donia, Greece). The physiognomy of Trifolion resupinati

communities is similar to those classified in cluster 1, but

their stands are lower in height, and are formed by a differ-

ent functional species group. Among them, clovers are

particularly important (Trifolium balansae, T. micranthum,

T. nigrescens, T. resupinatum, T. striatum, T. subterraneum);

grasses and sedges may also reach a high abundance

(e.g. Agrostis stolonifera agg., Alopecurus utriculatus, Carex

distans, Hordeum maritimum, Poa sylvicola). Cluster 3 repre-

sents exclusively more types of Balkan sub-halophytic,

intermittently wet grasslands, mostly belonging to the alli-

ance Trifolio-Cynodontion. Further studies on its syntaxo-

nomic interpretation are needed, however. The data were

sampled in Bulgaria, Macedonia and Serbia. Communities

dominated by perennial rhizomatous grasses (Agrostis stolo-

nifera, Cynodon dactylon) and some annual (Centaurea calcit-

rapa, Crepis setosa) or perennial herbs (Cichorium intybus,

Potentilla anserina, P. reptans, Trifolium fragiferum) developed

in compact, slightly saline soils and trampled more or less

ruderal habitats. On the other hand, Cluster 4 covered only

Pannonian sub-halophytic, intermittently wet grasslands of

the alliance Festucion pseudovinae (especially ass. Centaureo-

Festucetum pseudovinae). This vegetation is developed on rel-

atively slightly saline solontchak soils in the Czech Repub-

lic, Hungary, NW Romania and Slovakia. The stands are

species-rich and rather dense with a low abundance of

therophytes. Except for the occurrence of dominant halo-

phytes such as Artemisia santonicum and Festuca pseudovina, a

rather low salt content in the soil is mirrored in the pres-

ence of many grassland species with a broad realized niche,

such as the dry grassland species Asperula cynanchica, Aster li-

nosyris, Centaurea pannonica, Galium verum, Euphorbia cyparis-

sias or the mesic grassland species Dactylis glomerata, Daucus

carota and Poa pratensis agg. Intense grazing leads to the

occurrence of ruderal species such as Cirsium arvense and

Dipsacus fullonum.

Group B formed steppe vegetation on salt-affected soils.

This vegetation is developed on soils with a higher content

of salts as compared to the previous group. Cluster 5 consti-

tutes Pannonian vegetation close to the Achilleo-Festucetum

pseudovinae association from the alliance Festucion pseudovi-

nae. It represents the transition between halophytic

vegetation and dry and mesic meadow vegetation (the

Molinio-Arrhenatheretea class). In the spring, the soils are



Table 1. Synoptic table of halophytic and sub-halophytic vegetation in the Pannonian lowland and the Eastern Balkans. The table shows modified TWIN-

SPAN classification at the level of four vegetation types (A–D) and at the level of 15 clusters (1–15). The frequency values are shown, with background shad-

ing indicating the cases whenΦ � 0.4. Percentage representation of relev�es across the countries and regions, rounded to 0.1%, is shown

Higher level cluster code (A–D) A A A A B B B B B C C C C D D

Cluster No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

No. of relev�es 58 201 154 51 167 183 111 75 196 154 178 251 51 356 251

% Pannonian relev�es 26 2.8 0 100 100 92.4 97.4 0 93.8 100 73 99 100 69 9

% Balkan relev�es 74 97.2 100 0 0 7.6 2.6 100 6.2 0 27 1 0 31 91

% relev�es for countries:

Czech Republic 0 2.2 0 5 0.9 0 0 0 0 69 47 16 0 15 5

Slovakia 26 0.6 0 83 42 58 31 0 53 22 16 39 16 9 0

Austria 0 0 0 0 0 5.9 0 0 1 6.2 10 5.2 31 9.1 0

Hungary 0 0 0 2 14 6.5 42 0 22 1.4 0 14 37 22.6 0.5

Serbia 0 0 4 0 5.1 4 2.6 0 5.7 1.4 0 6 14 13 2

Croatia 0 0 0 0 0 0 1.8 0 2.1 0 0 2.8 2 0 0

Romania 13 0 0 10 38 18 20 0 10 0 0 16 0 0.3 1.5

Bulgaria 20 23 83 0 0 7.6 0 69 3.6 0 27 1 0 27 88

Macedonia 0 69 13 0 0 0 2.6 31 2.6 0 0 0 0 4 3

Greece 41 5.2 0 0 0 0 0 0 0 0 0 0 0 0 0

A: Sub-halophytic habitats

Plantago lanceolata 3 65 55 63 47 12 1 25 2 2

Lolium perenne 47 62 59 16 2 3 13 6 4 4

Ranunculus marginatus 34 45 2

Galium palustre agg. 34 44 1 8 1 1

Taraxacum species 2 64 23 75 26 5 1 3 1 16 1 5

Cluster 1: Beckmannia eruciformis–Eleocharis palustris (tall grass sub-halophytic wetlands)

Eleocharis palustris agg. 41 27 1 10 1 10 2 25 1 1

Beckmannia eruciformis 40 2 2 1 5

Rumex conglomeratus 36 13 1 0

Veronica anagalloides 26 1 1

Ranunculus ophioglossifolius 22 1

Alopecurus creticus 21 1

Cluster 2: Trifolium resupinatum–Poa sylvicola (Balkan sub-halophytic wet grasslands)

Poa sylvicola 28 80 29 1 1

Alopecurus rendlei 26 67 1

Trifolium resupinatum 26 65 14 1 7

Bromus racemosus 53 2 1 1

Carex hirta 2 43 1 20 6

Tragopogon pratensis 42 5

Potentilla reptans 10 41 15 33 4 1 1 2

Trifoliummicranthum 38 2 1

Carex distans 9 37 6 6 24 4

Cynosurus cristatus 35 1

Anthoxanthum odoratum 34 1 2 5

Orchis laxiflora agg. 2 33 2 3

Oenanthe silaifolia 21 33 7 1 2

Trifolium patens 3 32 2

Moenchia mantica 31 3

Cyperus longus 5 26

Hordeum secalinum 25 18 1

Trifolium balansae 24

Ranunculus velutinus 23

Medicago polymorpha 21 3

Oenanthe stenoloba 21 2

Cluster 3: Cynodon dactylon–Hordeum hystrix (Balkan sub-halophytic intermittently wet grasslands)

Cynodon dactylon 16 50 70 31 22 14 4 40 5 10 3 8 2 3 1

Cichorium intybus 2 42 49 39 8 1 7 5 4 1

Hordeum hystrix 33 48 34 4 22 19 7 3 7 1 2



Crepis setosa 26 37 2 2 1 11

Centaurea calcitrapa 1 27 1

Bromus arvensis 2 4 27 1 1

Festuca pseudovina grasslands accross higher rank clusters (clusters 4, 5)

Achillea millefolium agg. 2 9 30 90 74 29 4 1 2 14 3 2

Cluster 4: Trifolium repens–Festuca pseudovinae (Pannonian sub-halophytic intermittently wet grasslands)

Trifolium repens 2 31 43 75 30 3 3 1 3

Poa pratensis agg. 10 29 69 34 9 5 6 1 2

Lotus corniculatus 2 22 44 69 23 1 2 1

Centaurea jacea 9 1 63 29 3 2 8 4 1

Trifolium pratense 2 27 9 53 5 2 1 1 3

Festuca pratensis agg. 29 8 51 4 2 4 1

Leontodon autumnalis 9 1 49 9 2 2 4 1

Cerastium holosteoides 5 1 45 13 3

Ranunculus acris 7 11 41 6

Pimpinella saxifraga agg. 35 14 1 1

Daucus carota 6 12 35 9 22 2 2

Ononis spinosa 7 3 29 11 2 5 1 1

Dactylis glomerata 2 2 4 27 4 3 1 1 1

Carex caryophyllea 2 1 27 14 1

B: Steppe halophytic habitats

Cluster 5: Festuca pseudovina–Hordeum hystrix (Pannonian steppe halophytic grasslands)

Scorzonera cana 3 11 6 37 69 58 37 19 8 3 3 16

Poa bulbosa 2 12 20 53 7 12 48 11 1 1

Festuca pseudovina 76 92 83 32 24 5 3 15 2 1

Bromus hordeaceus 1 1 2 53 17 8 6 2

Scleranthus annuus 3 4 37 5 2

Carex stenophylla 1 6 34 5 23 1 1 5

Trifolium retusum 9 33 8 2 21 1 1

Koeleria macrantha 2 31 3

Ornithogalum kochii 10 29 8 1 1

Ranunculus pedatus 6 28 10 3

Polycnemum arvense 26 3

Trifolium species 1 22 2 1

Cluster 6: Artemisia santonicum (continental steppe halophytic grasslands)

Artemisia santonicum 1 46 92 50 17 30 6 2 21 6 1 6

Cluster 7: Plantago tenuiflora–Pholiurus pannonicus (Pannonian low-productive steppe halophytic grasslands)

Plantago tenuiflora 3 10 8 87 4 23 2 1 4 1

Pholiurus pannonicus 1 9 2 74 5 5 1 2 1

Polygonum aviculare agg. 5 2 12 4 43 10 62 4 4 19 2 15 3 1

Cluster 8: Camphorosmamonspeliaca–Plantago coronopus (Balkan sub-Mediterranean steppe halophytic grasslands)

Camphorosmamonspeliaca 5 100 1 1

Puccinellia *convoluta 4 21 5 2 52 5 16 1 22 41

Plantago coronopus 4 40 3 4

Trigonella monspeliaca 1 1 20

Cluster 9: Camphorosma annua (Pannonian and Balkan steppe halophytic grasslands with Camphorosma annua)

Camphorosma annua 0 11 4 5 3 96 1 9 47 1

C: Wet halophytic habitats.

Puccinellia distans agg 7 1 1 16 38 76 9 76 55 34 98 96 26 17

Cluster 10: Lotus tenuis–Bolboschoenus maritimus (wet and moist halophytic grasslands at the Pannonian margin)

Lotus tenuis 10 26 10 39 34 14 3 1 78 51 24 1 2

Potentilla anserina 12 2 20 68 34 7 1

Atriplex prostrata 1 61 5 14 7 1

Bolboschoenus maritimus agg. 9 13 3 1 57 30 6 2 11 2

Melilotus dentata 2 1 43 21 1

Cluster 11: Scorzonera parviflora–Juncus gerardii

Juncus gerardii 12 23 17 18 4 11 1 1 1 54 78 22 5 9

Table 1. (Continued)



wet but not flooded, and they later dry out so that the soil

can be polygonally fractured. Due to the lower salt con-

tent, precipitation of salts on the soil surface never occurs.

The stands of this cluster were found in all Pannonian

countries. Communities are characterized by rather dense

stands of low grasses, dominated by Festuca pseudovina;

halophytes are usually replaced by grassland species,

including Bromus hordeaceus, Poa bulbosa and, less com-

monly, Elymus repens and Alopecurus pratensis; Achillea mil-

lefolium agg., Inula britannica and Plantago lanceolata are

frequent, while obligate halophytes occur rarely. Cluster 6

corresponds with the same alliance. Most relev�es belong to

the steppe halophytic vegetation of the Artemisio-Festucetum

pseudovinae association. This differs from cluster 5 in a

slightly higher salinity and lower soil moisture content.

Soils dry out during the summer and are strongly polygo-

nally fractured; salt efflorescence could also be rarely

found. Therefore, the halophyte species Artemisia santoni-

cum and Festuca pseudovina usually dominate. Other obli-

gate and facultative halophytes are also represented (e.g.

Aster tripolium, Cerastium dubium, Plantago maritima, Puccin-

ellia distans agg. and Scorzonera cana). Most of the relev�es

came from Pannonia (Hungary, Romania, Slovakia), but

Bulgarian salt steppes are also represented. Cluster 7 also

represents Pannonian vegetation (NE Croatia, Hungary,

NW Romania, N Serbia, Slovakia) and corresponds to the

Plantagini-Pholiuretum pannonici association, developed in

shallow depressions of the salt solonetz steppe, which is

flooded with water in spring, then stays dry for a long per-

iod before drying out during the summer. This association,

however, was also recorded in the Balkans (Macedonia).

The community is characterized by common occurrence of

two dominant species, Plantago tenuiflora and Pholiurus pan-

nonicus, which are frequently accompanied by the obligate

halophytes Artemisia santonicum and Puccinellia distans agg.,

as well as salt-tolerant sub-halophytes such as Polygonum

aviculare, Carex stenophylla and Gypsophila muralis. Both

of the dominant species can grow in many types of

halophytic vegetation, but they reach the highest cover in

Plantagini-Pholiuretum pannonici. The stands are of low

height and are species-poor, with the total number of spe-

cies per relev�e usually being below ten. Cluster 8 comprises

exclusively Balkan steppe halophytic grasslands from the

class Festuco-Puccinellietea, especially Camphorosmetum mons-

peliaceae and floristically similar associations. This vegeta-

tion was documented only in Bulgaria andMacedonia. It is

formed of the perennial plants Camphorosma monspeliaca

and Plantago coronopus, frequently accompanied by Bupleu-

rum tenuissimum,Hedysarum bulgaricum, Puccinellia festucifor-

mis subsp. convoluta and Trigonella monspeliaca. The stands

develop on extremely salt-affected solonetz soils as well as

on steep slopes on the basis of open, Cretaceous clay marls

in small patches with diameters of 1–3 m. Cluster 9 com-

prises structurally similar vegetation of the Camphorosme-

tum annue association, which was found in all Pannonian

countries except the Czech Republic and Bulgaria and

Macedonia. This vegetation is formed of rather dense,

monodominant low carpets of the succulent annual plant

Camphorosma annua. The dominant species is accompanied

by other obligate halophytes (Artemisia santonicum, Plantago

maritima, P. tenuiflora, Puccinellia spp.), which reach only a

low abundance. This vegetation is developed on strongly

salt-affected solonetz soils and indicates the most salinized

andmost extreme habitats of the salt steppes.

Group C includes vegetation of wet halophytic habitats.

Cluster 10 represents different vegetation types of wet and

moist sub-halophytic and halophytic grasslands at the

Pannonian margins of the Potentillion anserinae and Juncion

gerardii alliances. Their common feature is the relatively

long-term flooding and low to medium salt content in soil.

The vegetation is not of a uniform physiognomy. It is

composed of either high or low plants, most frequently of

Atriplex prostrata, Bolboschoenus maritimus agg., Cirsium

brachycephalum, Lotus tenuis, Melilotus dentata and Potentilla

Phragmites australis 10 4 2 1 5 1 40 53 8 6 8 8

Scorzonera parviflora 5 1 19 49 8 1 1

Triglochin maritima 2 2 48 8 1

Cluster 12: Aster tripolium–Puccinellia distans (subcontinental wet low-grass halophytic grasslands)

Aster tripolium 3 1 1 4 4 21 12 0 5 71 54 84 43 27 27

Cluster 13: Lepidium cartilagineum–Puccinellia distans (Pannonian wet halophytic Lepidium grasslands)

Lepidium cartilagineum 1 4 9 1 61 1

D: Extreme halophytic habitats

Cluster 14: Crypsis aculeata–Suaeda pannonica (low-productive salt-rich marshes)

Crypsis aculeata 1 3 1 17 2 2 57 4

Cluster 15: Salicornia europaea–Suaedamaritima (the most extreme salt-rich marshes)

Salicornia europaea agg. 1 1 2 5 17 74

Suaeda maritima 2 1 1 2 2 6 57

Bassia hirsuta 1 22

Table 1. (Continued)



Fig. 2. The distribution of relev�es included in the individual clusters: cluster 1 Beckmannia eruciformis-Eleocharis palustris (Bec. eruc.-Eleo. pal.), cluster 2

Trifolium resupinatum-Poa sylvicola (Tri. res.-Poa syl.), cluster 3 Cynodon dactylon-Hordeum geniculatum (Cyn. dac.-Hord. gen.), cluster 4 Trifolium repens-

Festuca pseudovina (Tri. rep.-Fes. pseu.), cluster 5 Festuca pseudovina-Hordeum geniculatum (Fes. pseu.-Hor. gen.), cluster 6 Artemisia santonicum-

Festuca pseudovina (Art. san.-Fes. pseu.), cluster 7 Plantago tenuiflora-Pholiurus pannonicus (Pla. ten.-Pho. pan.), cluster 8 Camphorosma monspeliaca-

Plantago coronopus (Cam. mons.-Pla. cor.), cluster 9 Camphorosma annua (Cam. annua), cluster 10 Lotus tenuis-Bolboschoenus maritimus (Lot. ten.-Bolb.

mar.), cluster 11 Scorzonera parviflora-Juncus gerardii (Scor. par.-Junc. ger.), cluster 12 Aster tripolium-Puccinellia distans (Trip. pan.-Pucc. dis.), cluster 13

Lepidium cartilagineum-Puccinellia distans (Lep. cart.-Pucc. dis.), cluster 14 Crypsis aculeata-Suaeda pannonica (Cryp. acu.-Suae. pann.), cluster 15:

Salicornia europaea-Suaedamaritima (Sal. eur.-Suae. mar.). Hatched areas refer to regions with extremely high concentration of localities.



anserina. It was found in Austria, NE Croatia, the

Czech Republic, Hungary, N Serbia and Slovakia, and its

syntaxonomy is not consistent accross the countries

and deserves further study. Cluster 11 shows vegetation

developed on wet solonchak soils from the Juncion gerardii

alliance. It represents a transition between the salt marsh

andwet grassland vegetation. The halophytic species Triglo-

chin maritima, Juncus gerardii, Scorzonera parviflora and Aster

tripolium dominate, alongwithwetland generalists, indicat-

ing permanently wet soils and seasonal flooding at least

(Phragmites australis, Bolboschoenus maritimus agg., Eleocharis

palustris). The water table is permanently near the soil sur-

face or is only reduced for a short time. This vegetation is

represented especially in Pannonia (Austria, the Czech

Republic, Slovakia), but has been recorded in Bulgaria as

well. Cluster 12 comprises sub-continental wet low-grass

halophytic grassland vegetation of the Puccinellietum limosae

association from the Puccinellion limosae alliance. This vege-

tation is rather sparse and dominated by the perennial grass

Puccinellia distans agg.Obligate halophytes such as Artemisia

santonicum,Aster tripolium, Plantagomaritima and Spergularia

media are also abundant. The community develops in flat

depressions on clayey and strongly saline solontchak and

solonetz soils. Soils are moist for most of the year. The soil

surface dries out strongly during the summer, so that it is

hardened and polygonally fragmented. This vegetationwas

found predominantly in Pannonia (Austria, NE Croatia,

Czech Republic, W Romania, N Serbia, Slovakia). Cluster 13

comprises Pannonian wet halophytic vegetation of the

Lepidietum crassifolii association. This sparse and low-herb

vegetation is developed in large depressions on strongly

salt-affected solonchak soils. The obligate halophyte species

Lepidium cartilagineum subsp. crassifolium dominate, accom-

panied by Camphorosma annua and Puccinellia distans agg.

This vegetation occurs in thewestern part of the Pannonian

Basin (NEAustria,WHungary, N Serbia).

The last group, group D, includes vegetation of extreme

halophytic habitats. Cluster 14 represents both the inland

vegetation of extremely salt-rich and periodically flooded

habitats developed in the exposed bottoms of salt lakes in

SW Pannonia (Hungary, N Serbia) and the coastal and

slightly inland vegetation in the Black Sea region. The

vegetation belongs to the Crypsietea aculeatae class and two

associations from the Thero-Salicornietea class: Suaedetum

pannonicae and Crypsido aculeatae-Suaedetum maritimae. Clus-

ter 15 represents vegetation types occurring predominantly

on the Black Sea coast in Bulgaria, but the Pannonian veg-

etation of exposed bottoms of saline lakes is also included.

This group includes plant associations from the classes

Thero-Salicornietea and Juncetea maritimi (predominantly

the Salicornietum prostratae, Crypsido aculeatae-Suaedetum ma-

ritimae, Suaedo maritimae-Bassietum hirsutae and Juncetum

maritimi associations). Vegetation is sparse and species-

poor, usually with dominance of the particular succulent

taxa of Salicornia and Suaeda. Generally, Thero-Salicornietea

vegetation occupies more nutrient-poor soils than the

Crypsietea aculeatae vegetation.

Ordination analyses

The first DCA axis of the complete data set described the

salinity gradient from sub-halophytic grasslands and reed

beds (clusters 1–4), through steppe and wet inland halo-

phytic vegetation (clusters 5–9), towards extreme halo-

phytic species-poor vegetation (clusters 14, 15). This

gradient was longer in the Balkan region, where it spanned

from sub-Mediterranean, salt-rich grasslands to extremely

halophytic vegetation at the Black Sea coast. The second

most important gradient coincided with the water regime

and spans from the wettest sub-halophytic grasslands with

Beckmannia eruciformis and Eleocharis palustris (cluster 1) to

the driest steppe-like Camphorosma monspeliaca vegetation

(cluster 8; Fig. 4). When the restricted data set without the

extreme ends of the salinity and water level gradients,

comprising clusters B and C without cluster 8, was analy-

sed, two major gradients were identified, again related to

salinity and water regime. The first, however, clearly coin-

cided more with the water regime than with salinity

(Appendix S3) and sorted the sites from dry, steppe-like

habitats to wet and simultaneously salt-rich habitats with

Triglochin maritima and Scorzonera parviflora. The second

axis sorted drier habitats along the salinity gradient from

Festuca pseudovina, Artemisia santonicum and Hordeum hystrix

grasslands to extremely halophyte Camphorosma annua

vegetation. The importance of salinity clearly increased

towards drier habitats.

The Monte Carlo permutation test in CCA showed that

all climate variables obtained from the WorldClim model

were significant. The strongest, and nearly equal, relation-

Fig. 3. Dendrogram of the modified TWINSPAN analysis. The number of

clusters corresponds to synoptic table (Table 1).



ships with the species composition were found with vari-

ables BIO18 (Precipitation of Warmest Quarter, explaining

14.3% of the variation explained by all variables), BIO9

(Mean Temperature of Driest Quarter; 13.9%), BIO8

(Mean Temperature of Wettest Quarter; 13.8%) and

BIO11 (Mean Temperature of Coldest Quarter; 13.4%).

When the most important variable (BIO18) was included

in the model, the residual variation was best explained by

the variable BIO7 (Temperature Annual Range). Putting

these variables into the map showed that BIO18 corre-

sponds to the division of the data set into the sub-Mediter-

ranean region (Macedonia, Greece, SE Bulgaria and Black

Sea coast) and the continental region with a more Central

European climate (Pannonian basin and Middle Danube

plain in Bulgaria; Appendix S4a), while BIO7 corresponds

to the gradient from themaritime climate (Black Sea coast)

to the strongly continental regions of Eastern Pannonia,

the Middle Danube plain and the Thracian lowland

(Appendix S4b).

Discussion

Vegetation gradients

Salinity and water regime were found to be the most

important factors governing species composition in the

analysed large-scale data set, where inland salt marshes

predominate over coastal marshes. The same two most

important gradients also appeared when only core halo-

phytic grasslands, without the extreme ends of the gradi-

ents, were analysed. Nevertheless, the water regime

overrode the salinity gradient, which appeared important

only in drier grasslands. Analogous results, with the same

principal gradients, were reported from a wide set of other

studies dealing with coastal (Mesl�eard et al. 1991; Pen-

nings & Ragan 1992; Alvarez Rogel et al. 2000; Dubyna &

Neuh€auslov�a 2000; Freitag et al. 2001; van Kley & Scham-

in�ee 2003; Pandža et al. 2007; Apaydin et al. 2009) or inland(Wendelberger 1943; Bodrogk€ozy 1970; Piernik 2003, 2005;Wei-Qiang et al. 2008) salt marshes.

Adam (1978) reported that the past and present land

use is the most important determinant of vegetation vari-

ability of salt marshes in Great Britain. The land-use effects

are also important in the region studied here. Heavy graz-

ing, for example, leads to the development of Hordeum hys-

trix-dominated vegetation (Eli�a�s et al. 2013), and soil

mining for brick production can preserve open salt pans,

which are necessary for development of Camphorosmetum

annuae association in desalinated salt steppes (D�ıt�e et al.

2008). However, these effects became obscured in the

analysis of this study, covering wide geographic, climatic

and salinity gradients. The above-mentioned Hordeum hys-

trix-dominated vegetation was clustered together with the

vegetation from which it usually develops. In both ordina-

tion and classification analyses, Hordeum hystrix grasslands

displayed a tight floristic similarity to Festuca pseudovina

and Artemisia santonicum steppe grasslands. This suggests

that this type of grassland also develops from the latter and

not only from Puccinellia grasslands, as was previously

thought (see also Eli�a�s et al. 2013).

The salinity gradient was longer in the Balkan region

than in Pannonia. This difference can be explained by

the fact that the major vegetation gradient corresponding

to salinity level also coincides with climate. The most

salt-rich grasslands develop under a maritime climate,

whereas drier types of sub-halophytic vegetation, occur-

ring exclusively in the Balkans, develop under a (sub)

Mediterranean–(sub)continental climate. The climate of

the Pannonian basin and the Danube lowland in Bulgaria

is, on the other hand, rather continental, with a higher

annual temperature range (Appendix S4b). As a result,

sub-Meditteranean sub-halophytic grasslands do not

occur in continental regions of Central Europe, where

they are replaced with different vegetation types not

belonging to the sub-halophytic vegetation types at all,

such as Deschampsion caespitosi alliance (Botta-Duk�at et al.

2005; H�ajek et al. 2008) or Cynodon dactylon-dominated

vegetation from the Lolio-Plantaginetea class (Tzonev et al.

2009). The reasons for this phenomenon are the climate

conditions that prevent the occurrence of sub-Mediterra-

nean sub-halophytic taxa in the area of the Pannonian

basin. However, longer vegetation gradients in the Bal-

kans do not mean that Balkan halophytic vegetation is

more diverse than that of Pannonia. Continental types of

halophytic vegetation are extremely rare in the Balkans

Fig. 4. Detrended correspondence analysis of all samples, with centroids

of particular clusters, and the distribution of Balkan and Pannonian relev�es

along the first two ordination axes. Eigenvalues of axes: 1st axis 0.799. 2nd

axis 0.691, total inertia 50.065.



and some vegetation types (e.g. those involved in clusters

4, 5, 10 and 13) are even absent in the Balkans.

Higher rank syntaxa

The vegetation survey presented in this paper should be

understood as a description of the large-scale vegetation

pattern that might serve as a support for certain syntaxo-

nomical decisions, rather than for rigorous syntaxonomic

revision. The results of any numerical classification are

strongly dependent on the context of the study, including

the diversity of vegetation types involved, the rarity of

some vegetation types in a study area, the weighting of

cover data, the classificationmethod and the stopping rules

used. It is therefore impossible to consider resulting clus-

ters as discrete units of the same rank of the hierarchical

syntaxonomical system, and further effort is needed to cre-

ate a final syntaxonomical decision (Willner 2006; Michl

et al. 2010). In this heterogeneous data set, particular clus-

ters corresponded to one or even more traditionally delim-

ited classes, while another with only one association was

found in a separate case (e.g. Plantagini-Pholiuretum panno-

nici, cluster 7). This pattern was evidently not caused by

sporadic mis-classified relev�es. Some clusters containing

more associations traditionally classified within different

classes had not split even at the very fine level of division.

This pattern might be further caused through using total

inertia as a heterogeneity measure in a modified TWIN-

SPAN analysis (Role�cek et al. 2009), because it depends on

species richness and thus shows higher heterogeneity in

species-rich clusters. However, when cluster analyses were

used instead of TWINSPAN analyses (data not shown), the

results were similar, and clusters comprising more orders

or even classes were still created. Hence, this result reflects,

at least partially, the inconsistent weighting of physiog-

nomy and total species composition in traditional syntaxo-

nomic systems (Ot’ahel’ov�a & Valachovi�c 2001; Borhidi

2003; Moln�ar & Borhidi 2003; �Sumberov�a 2007; Jarol�ımek

et al. 2008; Tzonev et al. 2008; Hroudov�a 2011). Although

considering physiognomy in classification is important for

practical purposes, it has some shortcomings. First, it is

unclear which physiogonomic features should be preferred

in the classification. As a result, some vegetation types (e.g.

Crypsietum aculeatae) are classified in different classes by dif-

ferent authors. Second, classification based predominantly

on dominance can poorly coincide with ecological condi-

tions, preventing the use of phytosociological classification

in bioindication. For example, particular species of tall

graminoids may dominate in very different ecological con-

ditions, covering nearly complete major environmental

gradients (e.g. Carex lasiocarpa and the pH gradient in fens).

In halophytic grasslands, dominance-based classifications

may also not be appropriate, as demonstrated for Beckman-

nia eruciformis in D�ıt�e et al. (2012). Our analysis has identi-

fied two similar problems. First, the vegetation dominated

by Bolboschoenus maritimus or Scirpus lacustris subsp. taber-

naemontani and simultaneously containing sub-halophytic

or halophytic species, traditionally classified within the

Phragmito-Magnocaricetea class, was not classified into sepa-

rate clusters and became a part of the clusters correspond-

ing to Festuco-Puccinellietea. The Bolboschoenus maritimus-

dominated vegetation had not split from clusters 10 and

11, corresponding to Juncion gerardii, even when very fine

classification and/or a very strong weighting of dominance

was used. This suggests that placing this vegetation into Fe-

stuco-Puccinellietea would be more ecologically reasonable

than creating separate alliances or associations within the

Phragmito-Magnocaricetea class (Ot’ahel’ov�a & Valachovi�c

2001; Moln�ar & Borhidi 2003). Second, Carex divisa-domi-

nated communities fell into more clusters, giving no sup-

port for delimiting the Caricetum divisae association based

on themere dominance of the species.

The survey outlined here also demonstrates heterogene-

ity of the Puccinellion limosae alliance. The clusters that cor-

respond to this alliance are distributed across higher rank

clusters B and C, and some of them display a floristic simi-

larity to Festucion pseudovinae (cluster B), while others are

similar to Scorzonero-Juncion (cluster C). The Hordeetum

hystricis association, traditionally classified within Puccinel-

lion, had not even split from cluster 5, which contains the

most Festucion pseudovinae relev�es. Clusters 6 and 7, corre-

sponding to two different alliances, Festucion pseudovinae

and Puccinellion limosae, are not separated along the first

two ordination axes. These results call into question the

concept of the Puccinellion limosae alliance. On the other

hand, the results of this analysis support the classification

of Camphorosma annua and C. monspeliaca communities into

Puccinellion limosae and Puccinellion convolutae (Micevski

1965; Tzonev et al. 2008, 2009), rather than creating a sep-

arate alliance Plantagi coronopodo-Camphorosmion monspelia-

cae (Golub et al. 2005), or even placing Camphorosmetum

annuae into Thero-Salicornietea (Moln�ar & Borhidi 2003).

Cluster 8 contains the Balkan steppe halophytic grass-

lands from the class Festuco-Puccinellietea. It covers vegeta-

tion units occurring under a wide range of environmental

gradients, especially soil salinity. This cluster also involves

theHedysaro bulgarici-Camphorosmetummonspeliacae associa-

tion, which is included in the Artemisio-Kochion prostratae

alliance from the Artemisietea vulgaris class (Tzonev et al.

2009). The occurence of obligate halophytes (Artemisia san-

tonicum, Camphorosma monspeliaca, Puccinellia festuciformis

subsp. convoluta) as well as the results of our analysis sug-

gest that it would still belong to the Puccinellion convolutae

alliance. Nevertheless, further research is needed, because

the relev�es of this association had outlying positions along

the second DCA axis.



Vegetation types new to Bulgaria

One of themain goals of this studywas to compare the spe-

cies composition of analogous vegetation types between

well-explored Pannonia and the newly explored Balkan

region. Here, particular vegetation types were identified

with, or delimited from, Central European vegetation

types without detailed comparative analysis, until now.

Our results suggest that identifying the Balkan vegetation

dominated by Hordeum hystrix with Pannonian Hordeetum

hystricis (compare Tzonev et al. 2009) may not be appropri-

ate. We therefore suggest a preliminary description of a

vicarious association. On the other hand, unifying the

maritime extreme halophytic vegetation at the Black Sea

Coast with analogous Pannonian inland communities, as

well as differentiating vegetation with Pucinellia festucifor-

mis subsp. convoluta into different associations (Tzonev

et al. 2009), is supported by our data. Furthermore, the

vegetation dominated by Artemisia santonicum, which Tzo-

nev et al. (2009) assigned only as a community, could be

classified within the same associations as analogous Pan-

nonian vegetation, but further research is needed.

One of the most important results of this analysis is the

discovery of a clearly delimited Juncion gerardii alliance in

the Balkans. These relev�es were sampled during our own

field research (M.H., P.H., D.S. and I.A.) in eastern Bul-

garia and are usually dominated either by Carex divisa or

Table 2. Synopsis of halophytic vegetation in the Pannonian–Balkan

region based on a literature review and our results.

Junceteamaritimi Br.-Bl. ex Tx. et Oberd. 1952

Juncetalia maritimi Br.-Bl. ex Horvati�c 1934

Juncion maritimi Br.-Bl. ex Horvati�c 1934

Oenantho lachenalii-Juncetummaritimi Tx. 1937

Thero-Salicornietea Tx. in Tx. et Oberd. 1958

Thero-Suaedetalia Br.-Bl. et O. de Bol�os 1958

Salicornion fruticosae Br.-Bl. 1933

Crypsido aculeatae-Suaedetummaritimae (Bodrogk€ozy 1966)

Mucina1993

Salicornietum prostratae So�o 1964

Suaedetum pannonicae (So�o 1933) Wendelberger 19431Salsoletum sodae Slavni�c 1948

Suaedo-Bassietum hirsutae Br.-Bl. 1928

Crypsietea aculeatae Vicherek 1973

Crypsietalia aculeatae Vicherek 1973

Crypsietum aculeataeWenzl 19342Atriplicetum prostrataeWenzl 1934 corr. Gutermann & Mucina

1993

Atriplici prostratae-Chenopodietum crassifolii Slavni�c 1948 corr.

Gutermann et Mucina 1993

Acorelletum pannoniciWendelberger 19433Heleochloetum alopecuroidis Rapaics ex Ubrizsy 1948

Heleochloetum schoenoidis T�opa 19394Chenopodietum urbici Kopeck�y 1981

Festuco-Puccinellietea So�o ex Vicherek 1973

Puccinellietalia distantis So�o 19475Pucinellion limosae So�o 1933

Puccinellietum limosae So�o 19333Chenopodio-Puccinellietum limosae So�o 19476,7Lepidietum crassifoliiWenzl 1934

Plantagini-Pholiuretum pannoniciWendelberger 1943

Matricario-Plantaginetum tenuiflorae (So�o 1933) Borhidi 1996

Puccinellietum limosae So�o 19333Bassietum sedoidis Ubrizsy 1948 corr. So�o 1964

Camphorosmetum annuae Rapaics ex So�o 1933

Artemisietum santonici So�o 1927 corr. Gutermann et Mucina 1993

Pucinellion convolutaeMicevski 1965

Diantho pallidiflori-Puccinellietum convolutae Tzonev et al. 2008

CamphorosmetummonspeliacaeMicevski 19653Bupleuro tenuissimi-Camphorosmetummonspeliacae Tzonev et al.

20083Petrosimono brachyatae-Puccinellietum convolutae Tzonev et al.

2008

Hedysaro bulgarici-Camphorosmetummonspeliacae Tzonev 2009

Puccinellio convolutae-Hordeetum hystricis assoc. nova prov.

Artemisio-Festucetalia pseudovinae So�o ex Vicherek 1973

Festucion pseudovinae So�o in M�ath�e 1933

Achilleo-Festucetum pseudovinae So�o 1947

Artemisio santonici-Festucetum pseudovinae So�o in M�ath�e 1933 corr.

Borhidi 1996

Centaureo-Festucetum pseudovinae Klika et Vlach 1937

Hordeetum hystricisWendelberger 1943

Peucedano officinalis-Asterion sedifolii Borhidi 1996

Peucedano-Asteretum punctati So�o 1947

Scorzonero-Juncetalia gerardii Vicherek 1973

Juncion gerardiiWendelberger 1943

8Caricetum divisae Slavni�c 1948

Scorzonero parviflorae-Juncetum gerardii (Wenzl 1934)

Wendelberger 1943

Carici distantis-Eleocharitetum quinqueflorae (Wendelberger 1950)

Mucina 1993

Loto tenuis-Potentilletum anserinae Vicherek 1973

Agrostio stoloniferae-Juncetum ranarii Vicherek 1962

Astero pannonici-Bolboschoenetum compacti Hejn�y et Vicherek ex

Ot’ahel’ov�a et Valachovi�c 20019Beckmannion eruciformis So�o 1933

Agrostio-Alopecuretum pratensis So�o 1933

Agrostio-Beckmannietum eruciformis Rapaics ex So�o 1930

Eleocharito-Alopecuretum geniculati So�o 1947

Rorippo-Ranunculetum lateriflori (So�o 1947) Borhidi 1996

Molinio-Arrhenatheretea Tx. 1937

Trifolio-Hordeetalia Horvati�c 196310Trifolion resupinatiMicevski 1957

Hordeo-Caricetum distantisMicevski 1957

Cynosuro-Caricetum hirtaeMicevski 1957

Trifolietum resupinati-balansaeMicevski 1959

Trifolietum nigrescentis-subterraneiMicevski 1957

Bromo commutati-Alopecuretum utriculatiMicevski 1965

Alopecuro-Ranunculetummarginati Zeidler 1954

Scirpo-Alopecuretum creticiMicevski 1957

Narcisso tazetae-Caricetum distantis (Economidou 1969) Raus 1983

Footnotes (see Appendix S5) are used when further studies are needed

before definitive syntaxonomical decision. Footnotes 1–10: seeAppendix S5.



Juncus gerardii, sometimes by Plantago coronopus. These do-

minants are accompanied by Spergularia media, Aster tripoli-

um, Puccinellia festuciformis subsp. convoluta, Trifolium

fragiferum and, especially in the past (J. Vicherek, unpubl.

data), Triglochin maritima. Neither this alliance nor any

association that could be assigned to it is reported for Bul-

garia in Tzonev et al. (2009).

Significant new insights were also obtained in the case

of sub-halophytic vegetation. Cluster 1 contained both

Pannonian and Balkan relev�es from wet sub-halophytic

grasslands. Many of them have been previously classified

within the Beckmannion eruciformis alliance, either with

Beckmannia eruciformis from Pannonia or even those with-

out Beckmannia from Greece (Raus 1983). Although the

Beckmannion eruciformis alliance had not been reported in

Bulgaria so far (Tzonev et al. 2009), this cluster also con-

tains a few relev�es with Beckmannia from Bulgaria. How-

ever, the same cluster contains relev�es resembling the

Loto-Trifolienion sub-alliance of the Agropyro-Rumicion crispi

(Vicherek 1973; Sykora 1982). D�ıt�e et al. (2012) drew

attention to the fact that the Beckmannia-dominated vege-

tation that is traditionally classified within Beckmannion is

often floristically distinct from the original diagnosis of the

alliance, and shows similarity to different alliances.

Because the syntaxonomy of wet sub-halophytic grasslands

is generally not clear in Europe, resolving the syntaxomic

position of Balkan relev�es will require further studies.

Cluster 2 predominantly contains vegetation belonging to

the Trifolion resupinati alliance, evidencing a clear delimita-

tion of this vegetation, not only from theDeschampsion caespi-

tosae alliance, as demonstrated by H�ajek et al. (2008), but

also from Pannonian sub-halophytic grasslands of the Loto-

Trifolienion sub-alliance. In addition, the Trifolion resupinati

alliance appeared to be delimited also from the more widely

distributed south European alliance Trifolio-Cynodontion,

which is reported for Bulgaria by Tzonev et al. (2009) and

whose relev�es formed a part of the separate cluster 3. How-

ever, cluster 3 is rather heterogeneous and also contains

Balkan vegetationwithHordeum hystrix and Puccinellia festuci-

formis subsp. convoluta as well as vegetation poor in halo-

phytes, developed in strongly managed or disturbed places,

such as those assigned as Plantagini majoris-Lolietum perennis

(Sopotlieva 2008). This suggests that further research, which

will includemore disturbed and less salt-rich plots from Pan-

nonia as well as the Balkan region, would lead to different

results regarding the distribution and delimitation of the Tri-

folio-Cynodontion alliance. In the European perspective,

detailed revisionof theTrifolion resupinati alliance and its rela-

tionships to Trifolio-Cynodontion,Molinio-Hordeion secalini and

Alopecurion utriculati is needed (L.Mucina, pers. comm.).

Based on a literature review and personal results, we

propose a united syntaxonomic synopsis of halophytic

grasslands in the Pannonian–Balkan region, and have

identified syntaxonomic problems that deserve further

studies (Table 2, Appendix S5).

Acknowledgements

We are indebted to Ji�r�ı Vicherek for providing unpublished

relev�es, Laco Mucina for help with nomenclature, Borja

Jim�enez-Alfaro for technical help and all colleagues who

helped in the field, herbaria or with literature. Editors (W.

Willner, M. Chytr�y) and anonymous referees provided

useful comments. Research in Pannonia was supported by

the grants VEGA No. 2/0030/09 and 2/0003/12. Research

in Bulgaria and data processing were supported by the

exchange project of the Czech and Bulgarian Academy of

Sciences (Diversity patterns of moist and mesophytic semi-

natural grassland vegetation in Bulgaria, 2008–2010), the

post-doc stay of D.S. at Masaryk University and the long-

term research plan of the Czech Academy of Sciences

(AV0Z60050516). Analysis of data from the Czech

National Phytosociological Database was supported by

Czech Science Foundation (GA206/09/0329).

References

Abrol, I.P., Yadav, J.S.P. & Massoud, F.I. 1988. Salt-affected soils

and their management. FAO Soils Bulletin 39: 1–131.

Adam, P. 1978. Geographical variation in British saltmarsh vege-

tation. Journal of Ecology 66: 339–366.

Alvarez Rogel, J.A., Alcaraz Ariza, F. & Ortiz Silla, R.O. 2000. Soil

salinity and moisture gradients and plant zonation in

Mediterranean salt marshes of southeast Spain. Wetlands 20:

357–372.

Apaydin, Z., Kutbay, H.G., Ozbucak, T., Yalcin, E. & Bilgin, A.

2009. Relationships between vegetation zonation and

edaphic factors in a salt-marsh community (Black Sea coast).

Polish Journal of Ecology 57: 99–112.

Bodrogk€ozy, G. 1962. Die standorts€okologischen Verh€altnisse

der halophilen Pflanzengesellschaften des Pannonicum I.

Untersuchungen an den Solontschak-Szikb€oden des s€udli-

chen Kiskuns�ag.Acta Botanica Hungarica 8: 1–37.

Bodrogk€ozy, G. 1965a. Ecology of the halophylic vegetation of

the Pannonicum III. Correlation between alkali (“szik”)

plant communities and genetic soil classification in the

Northern Hortob�agy.Acta Botanica Hungarica 11: 11–51.

Bodrogk€ozy, G. 1965b. Ecology of the halophylic vegetation of

the Pannonicum IV. Results of the investigation on the solo-

netz meadow soils of Orosh�aza. Acta biologica Szegediensis 11:

207–227.

Bodrogk€ozy, G. 1970. Ecology of the halophilic vegetation of the

Pannonicum VI. Effect of the soil-ecological factors on the

vegetation of the reserve of lake “Dong�er” at Pusztaszer. Acta

biologica Szegediensis 16: 21–41.

Bodrogk€ozy, G. & Gy€orffy, B. 1970. Ecology of the halophilic

vegetation of the Pannonicum VII. Zonation study along the



Bega-Backwaters in the Voivodina (Yugoslavia). Acta Biolog-

ica Szegediensis 16: 25–41.

Borhidi, A. 1961. Klimadiagramme und Klimazonale Karte Un-

garns. Annales Universitatis Scientiarum Budapestinensis Sectio

Biologia 4: 21–50.

Borhidi, A. 2003. Magyarorsz�ag n€ov�enyt�arsul�asai. Akad�emiai

Kiad�o, Budapest, HU.

Botta-Duk�at, Z., Chytr�y, M., H�ajkov�a, P. & Havlov�a, M. 2005.

Vegetation of lowland wet meadows along a climatic conti-

nentality gradient in central Europe. Preslia 77: 89–111.

Chytr�y, M. & Rafajov�a, M. 2003. Czech National Phytosociologi-

cal Database: basic statistics of the available vegetation-plot

data. Preslia 75: 1–15.

D�ıt�e, D., Eli�a�s, P. Jr & S�adovsk�y, M. 2008. Camphorosmetum annu-

ae Rapaics ex So�o 1933 – vanishing plant community of sal-

ine habitats in Slovakia. Thaiszia 18: 51–64.

D�ıt�e, D., Eli�a�s, P. Jr, �Suvada, R. & Szombathov�a, N. 2010. The

ecology and the coenotic characteristics of Pholiuro pannonici-

Plantaginetum tenuiflorae in the Pannonian Basin. Phyton 49:

295–315.

D�ıt�e, D., Hrivn�ak, R., Mele�ckov�a, Z., Eli�a�s, P. Jr & Daji�c-Stevano-

vi�c, Z. 2012. Beckmannia eruciformis vegetation in the Panno-

nian Basin (Central and South-Eastern Europe). Phyton.

In press.

D�ubravkov�a, D., Chytr�y, M., Willner, W., Illy�es, E., Jani�sov�a, M.

& K�allayn�e Szer�enyi, J. 2010. Dry grasslands in the Western

Carpathians and the northern Pannonian Basin: a numerical

classification. Preslia 82: 165–221.

Dubyna, D.V. & Neuh€auslov�a, Z. 2000. Salt meadows (Festuco-

Puccinellietea) of the Biryuchij Island Spit in the Azov Sea,

Ukraine. Preslia 72: 31–48.

Eli�a�s, P. Jr, D�ıt�e, D., �Suvada, R., P�ı�s, V. & Ikr�enyi, I. 2013. Horde-

um geniculatum in the Pannonian Basin: ecological require-

ments and grassland vegetation on salt-affected soils. Plant

Biosystems. In press.

Fodor, L., Csontos, L., Bada, G., Gy€orfi, I. & Benkovics, L. 1999.

Tertiary tectonic evolution of the Pannonian Basin system

and neighbouring orogens: a new synthesis of palaeostress

data. In: Durand, B., Jolivet, L., Horvath, F. & Seranne, M.

(eds.) The Mediterranean basins: Tertiary extension within the

Alpine orogen. pp. 295–334. Geological Society, London, UK.

Freitag, H., Golub, V.B. & Yuritsina, N.A. 2001. Halophytic plant

communities in the northern Caspian lowlands: 1. Annual

halophytic communities. Phytocoenologia 31: 63–108.

Golub, V.B. 1994. Class Asteretea tripolium on the territory of the

former USSR and Mongolia. Folia Geobotanica et Phytotaxono-

mica 29: 15–54.

Golub, V.B., Rukhlenko, I.A. & Sokoloff, D.D. 2001. Survey of

communities of the class Salicornietea fruticosae. Rastitel’nost’

Rossii 2: 87–95.

Golub, V.B., Karpov, D.N., Lysenko, T.M. & Bazhanova, N.B.

2003. Conspectus of communities of the class Scorzonero-

Juncetea gerardii Golub et al. 2001 on the territory of the

Commonwealth of Independent States and Mongolia. Sa-

marskaya Luka 13: 88–140.

Golub, V.B., Karpov, D.N., Sorokin, A.N. & Nikolajchuk, L.F.

2005. Soobshchestva klasa Festuco-Puccinellietea Soό ex Vic-

herek 1973 na teritorii Evrazii. Rastitel’nost’ Rossii 7: 50–75.

H�ajek, M., H�ajkov�a, P., Sopotlieva, D., Apostolova, I. & Velev, N.

2008. The Balkan wet grassland vegetation: a prerequisite to

better understanding of European habitat diversity. Plant

Ecology 195: 197–213.

Heged€u�sov�a, K. 2007. Centr�alna datab�aza fytocenologick�ych

z�apisov (CDF) na Slovensku. Bulletin Slovenskej Botanickej

spolo�cnosti 29: 124–129.

Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A.

2005. Very high resolution interpolated climate surfaces for

global land areas. International Journal of Climatology 25: 1965

–1978.

Hoffman, G.W. & Davies, Ch.S. (eds.) 1983. A geography of Eur-

ope: problems and prospects. Wiley, New York, NY, US.

Hroudov�a, Z. 2011. Svaz MCB Meliloto dentati-Bolboschoenion

maritimi Hroudov�a et al. 2009. In: Chytr�y, M. (ed.) Vegetation

of the Czech Republic. 3. Aquatic and wetland vegetation. pp. 428–

440. Academia, Praha, CZ.

Illy�es, E., Chytr�y, M., Botta-Duk�at, Z., Jandt U., �Skodov�a, I.,

Jani�sov�a, M., Willner, W. & H�ajek, O. 2007. Semi-dry grass-

lands along a climatic gradient across central Europe: vegeta-

tion classification with validation. Journal of Vegetation Science

18: 835–846.

Jansen, F. & Dengler, J. 2010. Plant names in vegetation databas-

es – a neglected source of bias. Journal of Vegetation Science 21:

1179–1186.

Jarol�ımek, I., �Sib�ık, J., Heged€u�sov�a, K., Jani�sov�a, M., Kliment,

J., Ku�cera, P., M�ajekov�a, J., Mich�alkov�a, D., Sadlonov�a, J.,�Sib�ıkov�a, I., �Skodov�a, I., Uhl�ı�rov�a, J., Ujh�azy, K., Ujh�azyov�a,

M., Valachovi�c, M. & Zaliberov�a, M. 2008. A list of vegeta-

tion units of Slovakia. In: Jarol�ımek, I. & �Sib�ık, J. (eds.) Diag-

nostic, constant and dominant species of the higher vegetation units

of Slovakia. pp. 295–329. Veda, Bratislava, SK.

van Kley, J.E. & Schamin�ee, J.H.J. 2003. Large-scale ordination

and gradient analysis of salt-marsh communities in theNeth-

erlands in the light of the Dutch National Vegetation Classifi-

cation. Phytocoenologia 33: 335–347.

Mateeva, Z. 2002. Precipitation and snow cover. In: Kopralev, I.

(ed.) Geography of Bulgaria. Physical geography. Socio-economic

geography. pp. 152–154. ForComPublishingHouse, Sofia, BG.

Mesl�eard, F., Grillas, P. & Lepart, J. 1991. Plant community suc-

cession in a coastal wetland after abandonment of cultiva-

tion: the example of the Rhone delta. Vegetatio 94: 35–45.

Micevski, K. 1964. Tipoloshki istrazhuvana na vegetacijata na

nizinskite livadi voMakedonija. Annuaire de la Faculte′ des Sci-

ences de l’Universite′ de Skopje 15: 121–173.

Micevski, K. 1965. Halofitska vegetacija Ovche Polja. Acta Musei

Macedonici Scientiarum Naturalium 10: 67–90.

Micevski, K. 1978. Tipoloshki istrazhuvana na vegetacijata na li-

vadite i pasishtata vo Males i Pijanec. In: Filipovski, G.,

Micevski, K. & Panov, M. (eds.) Males i Pijanec. pp. 9–41.

Makedonska akademija na naukite i umetnostite, Skopje,

MK.



Michalcov�a, D., Lvon�c�ık, S., Chytr�y, M. & H�ajek, O. 2011. Bias

in vegetation databases? A comparison of stratified-random

and preferential sampling. Journal of Vegetation Science 22:

281–291.

Michl, T., Dengler, J. & Huck, S. 2010. Montane–subalpine tall-

herb vegetation (Mulgedio-Aconitetea) in central Europe:

large-scale synthesis and comparison with northern Europe.

Phytocoenologia 40: 117–154.

Mikl�os, L. (ed.) 2002. Atlas krajiny Slovenskej republiky. M�ZP SR,

Bratislava & A�ZP SR, Bansk�a Bystrica, SK.

Mitkova, T. & Mitrikeski, J. 2005. Soils of the Republic of Mace-

donia: present situation and future prospects. In: Jones, R.J.

A., Hou�skov�a, B., Bullock, P. & Montanarella, L. (eds.) Soil

resources of Europe. pp. 225–234. 2nd ed. European Soil

Bureau Research Report No.9, EUR 20559 EN, Office for

Official Publications of the European Communities, Luxem-

bourg, LU.

Moln�ar, Z. & Borhidi, A. 2003. Hungarian alkali vegetation: ori-

gins, landscape history, syntaxonomy, conservation. Phyto-

coenologia 33: 377–408.

Mucina, L. 1993. Puccinellio-Salicornietea. In: Mucina, L., Grabh-

err, G. & Ellmauer, T. (eds.) Die Pflanzengesellschaften €Osterr-

eichs, Teil 1. pp. 522–549. Fischer, Stuttgart, DE.

Nem�cok,M., Pog�acs, G. & Posp�ı�sil, L. 2006. Activity timing of the

main tectonic systems in theCarpathian-Pannonian region in

relation to the rollbackdestruction of the lithosphere. In: Gol-

onka, J. & P�ıcha, F.J. (eds.) The Carpathians and their foreland:

geology andhydrocarbon resources.AAPGMemoir84: 743–766.

Nikolova, M. 2002. Air and soil temperatute. In: Kopralev, I.

(ed.) Geography of Bulgaria. Physical geography. Socio-economic

geography. pp. 146–149. ForCom Publishing, Sofia, BG.

Ninov, N. 2002. Soils. In: Kopralev, I. (ed.) Geography of Bulgaria.

Physical geography. Socio-economic geography. pp. 277–315. For-

ComPublishing, Sofia, BG.

Ot’ahel’ov�a, H. & Valachovi�c, M. 2001. Bolboschoenetalia. In: Va-

lachovi�c, M. (ed.) Plant communities of Slovakia. 3. Wetland veg-

etation. pp. 161–164. VEDA, Bratislava, SK.

Panagos, P., Van Liedekerke, M., Jones, A. & Montanarella, L.

2012. European soil data centre: response to European policy

support and public data requirements. Land Use Policy 29:

329–338.

Pand�za, M., Franji�c, J. & �Skvorc, Z. 2007. The salt marsh vegeta-

tion of the East Adriatic coast. Biologia 62: 24–31.

Pennings, S.C. & Ragan, M.R.M. 1992. Salt marsh plant zona-

tion: the relative importance of competition and physical fac-

tors. Ecology 73: 681–690.

Piernik, A. 2003. Inland halophilous vegetation as indicator of

soil salinity. Basic and Applied Ecology 4: 525–536.

Piernik, A. 2005. Vegetation–environment relations on inland

saline habitats in Central Poland. Phytocoenologia 25: 19–37.

Pop, I. 2002. Vegetatia solurior saraturoase den Romania. Con-

tributii Botanice 35: 287–332.

Raus, Th. 1983. Wechselnasse Wiesen in Griechenland. Tuexenia

3: 259–270.

Reed, J., Kry�stufek, B. & Eastwood, W. 2004. The physical geog-

raphy of the Balkans and nomenclature of place names. In:

Griffiths, H., Kry�stufek, B. & Reed, J. (eds.) Balkan biodiver-

sity. Pattern and process in the European hotspot. pp. 9–22. Klu-

wer Academic, Dordrecht, NL.

Rivas-Mart�ınez, S. & Rivas-Saenz, S. 2009. Worldwide biocli-

matic classification system 1996–2009. Phytosociological

Research Center, Madrid, ES. Available at http://www.

globalbioclimatics.org, accessed on November 15, 2011.

Role�cek, J., Tich�y, L., Zelen�y, D. & Chytr�y, M. 2009. Modified

TWINSPAN classification in which the hierarchy respects

cluster heterogeneity. Journal of Vegetation Science 20: 596–

602.

Rozbrojov�a, Z., H�ajek, M. & H�ajek, O. 2010. Vegetation diversity

of mesic meadows and pastures in the West Carpathians.

Preslia 82: 307–332.

Schamin�ee, J.H.J., Hennekens, S.M., Chytr�y, M. & Rodwell, J.S.

2009. Vegetation plot data and databases in Europe: an over-

view. Preslia 81: 173–185.

Sekulov�a, L., H�ajek, M., H�ajkov�a, P., Mikul�a�skov�a, E. & Ro-

zbrojov�a, Z. 2011. Alpine wetlands in the West Carpathians:

vegetation survey and vegetation–environment relation-

ships. Preslia 83: 1–24.

Slavni�c, �Z. 1948. Slaninska vegetacija Vojvodine. Arhiv za pol-

joprivredne nauke i tehniku 3: 1–80.

So�o, R. 1947. Conspectus des groupements v�eg�etaux dans les Bassins

Carpathiques. I. Les associations halophiles. Institut Botanique

de l’Universit�e �a Debrecen,, Debrecen, HU.

Sopotlieva, D. 2008. Sintaksonomichna harakteristika na trevnata

rastitelnost v Straldzhansko-Ajtoski geobotanichen okrag. PhD

Thesis, Institute of Botany, Bulgarian Academy of Sciences,

Sofia, BG.

Stefanovits, P. 1981. Soil science. Mez}ogazdas�agi Kiad�o, Budapest,

HU.

�Sumberov�a, K. 2007. Vegetation of annual graminoids in saline

habitats (Crypsietea aculeatae). In: Chytr�y, M. (ed.) Vegetation

of the Czech Republic. 1. Grassland and heathland vegetation. pp.

132–142. Academia, Praha, CZ.

Sykora, K.V. 1982. Syntaxonomic status of the Junco-Menthetum

longifoliae Lohmeyer 1953, the Junco-Menthetum rotundifoliae

Oberdorfer (1952) 1957, and the Caricetum vulpinaeNowinski

1927.Acta Botanica Neerlandica 31: 391–416.

Szabolcs, I. 1974. Salt-affected soils in Europe. Martinus Nijhoff,

The Hague, NL.

Tich�y, L. & Chytr�y, M. 2006. Statistical determination of

diagnostic species for site groups of unequal size. Journal of

Vegetation Science 17: 809–818.

Tich�y, L., Chytr�y, M., H�ajek, M., Talbot, S.S. & Botta-Duk�at,

Z. 2010. OptimClass: using species-to-cluster fidelity to

determine the optimal partition in classification of

ecological communities. Journal of Vegetation Science 21:

287–299.

Tutin, T.G., Burgess, N.A., Chater, A.O., Edmonson, J.R., Hey-

wood, V.H., Moore, D.M., Valentine, D.H., Walters, S.M. &



Webb, D.A. (eds.) 1993. Flora Europaea. Vol. 1, 2nd edn.

Cambridge University Press, Cambridge, UK.

Tutin, T.G., Heywood, V.H., Burgess, N.A., Moore, D.M., Valen-

tine, D.H., Walters, S.M. & Webb, D.A. (eds.) 1964–1980.

Flora Europaea. Vols. 1–5. Cambridge University Press, Cam-

bridge, UK.

Tzonev, R. 2002. Flora i rastitelnost na Sredna Dunavska ravnina.

PhD Thesis, Biological Faculty, University of Sofia, Sofia, BG.

Tzonev, R. 2009. Plant communities, habitats and ecological

changes in the vegetation on territory of three propected

areas along the Danube River. In: Ivanova, D. (ed.) Plant,

fungal and habitat diversity investigation and conservation. Pro-

ceedings of IV Balkan Botanical Congress, 20–26 June 2006,

Sofia. pp. 321–331. Institute of Botany, Sofia, BG.

Tzonev, R., Lysenko, T., Gussev, Ch. & Zhelev, P. 2008. The hal-

ophytic vegetation in South-East Bulgaria and along the

Black Sea coast.Hacquetia 7: 95–121.

Tzonev, R., Dimitrov, M. & Roussakova, V. 2009. Syntaxa

according to the Braun-Blanquet approach in Bulgaria. Phyt-

ologia Balcanica 15: 209–233.

Vicherek, J. 1973. Die Pflanzengesellschaften der Halophyten - und

Subhalophytenvegetation der Tschechoslowakei. Academia,

Praha, CZ.

Wei-Qiang, L., Xiao-Jing, L., Khan, M.A. & Gul, B. 2008.

Relationship between soil characteristics and halophytic

vegetation in coastal region of North China. Pakistan Journal

of Botany 40: 1081–1090.

Wendelberger, G. 1943. Die Salzpflanzengesellschaften des

Neusiedler Sees.Wiener botanische Zeitschrift 92: 124–144.

Wendelberger, G. 1950. Zur Soziologie der kontinentalen

Halophytenvegetation Mitteleuropas. Denkschriften der Oster-

reichischen Adademie der Wissenschaften 108: 1–180.

Willner, W. 2006. The association concept revisited. Phytocoenolo-

gia 36: 67–76.

Supporting information

Additional supporting information may be found in the

online version of this article:

Appendix S1. Full synoptic table in pdf and csv

format.

Appendix S2. Photographs depicting some of the

vegetation types.

Appendix S3. DCA ordination of the restricted data

set, without extreme ends of the salinity and water level

gradients.

Appendix S4. The variability in the precipitation of

the warmest quarter (a) and temperature annual range

(b), the most important climatic predictors in CCA in the

study area.

Appendix S5. Footnotes for the synopsis of halo-

phytic vegetation in the Pannonian–Balkan region.



Vegetation diversity of salt-rich grasslands in Southeast Europe

Documents

Transcript of Vegetation diversity of salt-rich grasslands in Southeast Europe