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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. (buriana@sci.muni.cz) &
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. (daniel.dite@gmail.com) & Senko, D.
(dusan.senko@savba.sk) &Mele�ckov�a, Z.
(zuzana.meleckova@savba.sk): Institute of
Botany, Slovak Academy of Sciences,
D�ubravsk�a cesta 9, SK-845 23, Bratislava,
Slovakia
Eli�a�s, P. Jr. (pavol.elias.jun@gmail.com):
Department of Botany, Slovak University of
Agriculture, Tr. A. Hlinku 2, SK-94976, Nitra,
Slovakia
Sopotlieva, D. (dsopotlieva@gmail.com) &
Apostolova, I. (iva.apostolova@gmail.com):
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).
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 3
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
Applied Vegetation Science4 Doi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science
Vegetation of salt-rich grasslands P. Eli�a�s et al.
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
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 5
P. Eli�a�s et al. Vegetation of salt-rich grasslands
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
Applied Vegetation Science6 Doi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science
Vegetation of salt-rich grasslands P. Eli�a�s et al.
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)
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 7
P. Eli�a�s et al. Vegetation of salt-rich grasslands
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)
Applied Vegetation Science8 Doi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science
Vegetation of salt-rich grasslands P. Eli�a�s et al.
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.
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 9
P. Eli�a�s et al. Vegetation of salt-rich grasslands
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).
Applied Vegetation Science10 Doi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science
Vegetation of salt-rich grasslands P. Eli�a�s et al.
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.
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 11
P. Eli�a�s et al. Vegetation of salt-rich grasslands
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.
Applied Vegetation Science12 Doi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science
Vegetation of salt-rich grasslands P. Eli�a�s et al.
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.
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 13
P. Eli�a�s et al. Vegetation of salt-rich grasslands
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).
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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.
Applied Vegetation ScienceDoi: 10.1111/avsc.12017© 2012 International Association for Vegetation Science 17
P. Eli�a�s et al. Vegetation of salt-rich grasslands