A Biogeographic Delineation of the European Alpine System Based on a Cluster

Flora 207 (2012) 168–178

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Flora

jo urnal homepage: www.elsevier.de/flora

A biogeographic delineation of the European Alpine System based on a cluster

analysis of Carex curvula-dominated grasslands

a,∗ b

Mihai Pus¸ cas¸ , Philippe Choler

A. Borza Botanical Garden, Babes¸ -Bolyai University, 400015 Cluj-Napoca, Romania

Laboratoire d’Ecologie Alpine UMR 5553 UJF-CNRS and Station Alpine J. Fourier UMS 3370 UJF-CNRS, Université de Grenoble, F-38041 Grenoble, France

a r t i c l e i n f o

a b s t r a c t

Article history: Biogeographic delineations within the European temperate mountains remain poorly understood, as

Received 28 June 2011

there has been little effort to assemble and analyze vegetation relevés covering Pyrenees, Alps, Carpathi-

Accepted 4 October 2011

ans and Balkans altogether. Our study tackles this issue by focusing on the widely distributed alpine acidic

grasslands dominated by Carex curvula. Cluster analysis of more than 800 vegetation relevés revealed the

Keywords:

European-scale spatial patterns of vascular plant diversity in these alpine grasslands. The geographical

Alpine grasslands

distribution of ﬂoristic clusters was partly congruent with the physiography of European mountains.

Species richness

Southern European ranges (Southern Balkans and Pyrenees) exhibit a high level of endemism and corre-

Distribution patterns

Phytogeography sponding ﬂoristic clusters are well separated from the others. Marked ﬂoristic similarities between the

Endemism Easternmost Alps, the Carpathians, and the Northern Balkans (Stara Planina) supported a major ﬂoristic

Indicator species boundary that runs through the Austrian Alps and that is likely the legacy of a shared Quaternary his-

tory. Within the Alps, ﬂoristic clustering was mainly driven by ecological drivers and not geography. This

paper presents the ﬁrst detailed study of spatial patterns of species distribution within the European

Alpine System, based on a comprehensive analysis of within- and between-community species diversity.

It shows that the quantitative analysis of large and consistent data sets may question the traditional

delineations of biogeographic regions within European mountains.

Introduction patches (Kreft et al., 2008). Previous works have shown that spa-

tial arrangement of these islands differs considerably among the

Temperate mountains of Europe share a number of common various mountain ranges of the EAS (Pus¸ cas¸ et al., 2008b). This has

features – ﬂora, vegetation, fauna – that prompted biogeographers important consequences on species dispersal constraints and geo-

to include Pyrenees, Alps, Carpathians and Northern Balkans into graphical ranges (Svenning and Skov, 2004). In addition, a number

a same biogeographic region, the so-called European Alpine Sys- of phylogeographic studies have shown that the glaciations of the

tem (EAS: Ozenda, 1985, 2009). The EAS is a well-known hotspot Quaternary period have had contrasting impacts on the alpine ﬂora

of plant diversity (Barthlott et al., 2007; EEA, 2005). At the regional of the EAS mountains (Comes and Kadereit, 2003; Kadereit et al.,

scale, steep environmental gradients produce complex patterns of 2004). For example, it is likely that only a few mountain ranges of

diversity and high turnover in species composition across short dis- the EAS were signiﬁcant refuges for alpine plants during ice ages

tances (Barthlott et al., 2005; Körner, 2007). At the continental scale, and this is a key issue to understand the current spatial distribu-

favorable habitats for mountain plants are separated by unfavor- tion of genetic diversity within these species (Schönswetter et al.,

able, lowland habitats, resulting in a highly fragmented distribution 2005; Tribsch, 2004). Most of these studies have focused on the

of alpine vegetation and a high degree of endemism (Coldea et al., infra-speciﬁc level of diversity using a limited number of taxa (but

2009; Ozenda, 2009; Pauli et al., 2003; Pawłowski, 1970). Moun- see Alvarez et al., 2009). By contrast, there has been less effort to

tains of the EAS are examples of sky islands system (Heald, 1951) examine how geography and post-glacial history have inﬂuenced

that offer large opportunities to examine how history and ecology diversity patterns at the level of species assemblages, including

have shaped species distribution. within- and between-community species diversity.

Species diversity within and among islands of alpine habi- The mountain ﬂora of Europe has been explored for more than

tat is primarily controlled by the area and the isolation of the two centuries (e.g. Allioni, 1785; Baumgarten, 1816; de Lapeyrouse,

1818; Rochel, 1838; von Crantz, 1769). Biogeographers have early

addressed ﬂoristic similarities and dissimilarities among the moun-

∗ tain ranges of the EAS (Braun-Blanquet, 1923, 1930; Gaussen and

Corresponding author.

Lerendde, 1949; Wołoszczak, 1895). Despite of a large number of

E-mail address: [email protected] (M. Pus¸ cas¸ ).

M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178 169

Fig. 1. (a) Distribution of Carex curvula subsp. curvula in the European temperate mountains (dark gray) and location of the grid cells (6 latitude and 10 longitude resolution)

where vegetation relevés are available (white squares). Light gray is for the areas above 800 m. (b) The number of relevés available in each grid cell (gray circles) and the

total number of relevés for each mountain range.

local and regional studies (e.g. Lüth et al., 2011; mountain grass- characteristic plant communities of the higher European mountain

lands of Eastern Alps), very few comparative analyses of alpine ranges, ﬂoristic data are available in a large number of regional

plant communities have covered large areas of the whole EAS monographs. Moreover, these high-elevation grasslands have not

(e.g. Horvat et al., 1974; but see Sibíkˇ et al., 2010, for subalpine been severely affected by land use and the current ﬂoristic diver-

vegetation). However, most recent studies have put emphasis on sity patterns mostly reﬂect the outcome of long-term evolutionary

the statistical analysis of vegetation relevés without performing a history (Grabherr et al., 2000). All these features make these grass-

detailed analysis of spatial patterns of species distribution. Rather lands an excellent model to delineate biogeographic regions within

ironically, the delineation of biogeographic regions within the the EAS. Based on clustering analysis of a very comprehensive syn-

EAS remains poorly understood, especially because of the absence thesis of vegetation relevés, we addressed the following questions:

of comparative ﬂoristic data between the different ranges. Only (1) what are the species diversity patterns of C. curvula-dominated

recently, the detailed mapping of the ﬂora of the Alps was linked grasslands in the mountain ranges of the EAS? (2) where are the

with the species chorology inside the EAS (Aeschimann et al., 2004), main ﬂoristic boundaries located and do the biogeograhic regions

but an overall analysis of the alpine plant species distribution in this correspond to natural entities (i.e. the mountain ranges)? and (3)

range is still needed. what are the indicator species of each identiﬁed cluster?

Latest advances in multivariate analysis and computational

power now allow a more robust delineation of biogeographic Materials and methods

regions based on quantitative analysis of large data sets (Kreft and

Jetz, 2010). In this study, we addressed this issue by focusing on Vegetation data

the alpine grasslands dominated by the sedge Carex curvula All.

subsp. curvula, hereafter C. curvula. These alpine grasslands are Carex curvula is endemic to the EAS. It is the dominant species

widely distributed in the EAS (Pus¸ cas¸ , 2005) where they repre- of extensive swards mainly occurring between ca. 2200 and

sent the typical late-successional communities of the alpine belt 2700 m a.s.l. in the Pyrenees, the Alps, the Carpathians and the

on acidic substrates (Choler and Michalet, 2002; Niederfriniger- mountains from Balkans (Stara Planina, Rila, Pirin) and the Dinar-

Schlag and Erschbamer, 2000; Pus¸ cas¸ et al., 2008b). The very few ides (Fig. 1a, Pus¸ cas¸ , 2005). The plant communities dominated by

C. curvula-dominated grasslands that were described in the Alps C. curvula were among the ﬁrst to be described by European phy-

on dolomites and shales (Erschbamer, 1992) have been shown to togeographers (the so-called “Curvuletum” of Brockmann-Jerosch,

be dominated by introgressed forms between C. curvula All. subsp. 1907; Rübel, 1911), and the ﬂoristic composition of these alpine

curvula and C. curvula All. subsp. rosae, an edaphically differentiated grasslands has been studied in the ﬁrst surveys of the alpine vege-

ecotype that occurs on base-rich substrates (Choler et al., 2004). tation of the Carpathians (Borza, 1934), the Balkans (Horvat et al.,

Because C. curvula-dominated alpine grasslands is one of the most 1937), and the Pyrenees (Braun-Blanquet, 1948). Since then, a large

170 M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178

number of monographs have described ﬂoristic diversity of these algorithm allows the use of various distances. Our ﬁnal results were

grasslands in various regions of the EAS (see Appendix 1 for an not signiﬁcantly different when other distance metrics (e.g. Sokal

extended list). However, existing phytogeographic syntheses are and Michener, 1958) were used (data not shown). Exploratory anal-

restricted to one mountain range only (Coldea, 1991; Pus¸ cas¸ et al., yses of the ﬂoristic data set were conducted using a varying number

2005; Roussakova, 2000; Theurillat, 1996). To our best knowledge, of prescribed groups (values of k ranging from 2 to 7). The number

there has been no comprehensive analysis of these grasslands at of times a given relevé was assigned to a given cluster was com-

the EAS scale. puted. A relevé was ﬁnally assigned to the cluster to which it was

We assembled 853 relevés of alpine vegetation dominated by the most frequently associated.

C. curvula coming from 59 different local monographs (Appendix Further analyses on indicator species were done with k = 5 that

1 for a list of references). The data set comprises 86 of our own provided an ecologically and biogeographically meaningful parti-

relevés. The assembled data set covers the whole distribution range tion (see Results and Discussion). The strength of the association

of the species (Fig. 1). Floristic surveys were conducted using stan- between a species and a group and the signiﬁcance level of this

dard phytosociological procedures (Braun-Blanquet, 1932), with a association were estimated using Indicator Species Analysis (ISA).

6-level scale for vascular plant species cover: +: <5%; 1: 5–10%; Following each partitioning, we calculated the indicator index pro-

2: 10–25%; 3: 25–50%; 4: 50–75%; and 5: >75%. We only selected posed by Dufrêne and Legendre (1997) and implemented in the

relevés for which the abundance of C. curvula was superior or equal R package INDICSPECIES (de Caceres and Legendre, 2009). For the

to two. We paid special attention not to add relevés including Carex signiﬁcance test, the null ecological hypothesis says that the fre-

curvula subsp. rosae (Gilomen, 1938). The two closely related sub- quency of the species in a given group is due to chance only, i.e. it

species exhibit contrasting distributions along soil acidity gradients is not lower or higher than in the other groups of the partitioning.

and to a lesser extent disturbance and meso-topographical gra- The estimated P-value was based on 1000 permutations.

dients (Choler and Michalet, 2002; Choler et al., 2004). C. rosae Following Chytry´ et al. (2002), we also calculated the hyper-

is primarily calcicole and is found only in the Alps and the Pyre- geometrical value (uhyp) as a measure of ﬁdelity of a species to a

nees (Chater, 1980). Relevés on non-acidic rocks were disregarded given group. The uhyp metric has positive or negative values that

unless authors have speciﬁcally referred to C. curvula. indicate the strength of association or disassociation, respectively,

Because ﬂoristic data were collected by different authors, the between a species and a group. All indicator species obtained with

area of the relevés exhibited some variation (3–160 m ). Within this method were in the list resulting from the ISA approach (data

each mountain range, we examined whether species richness was not shown).

dependent upon the area of the relevés and found no signiﬁcant All statistical analyses were performed with the open-source

relationships (linear regression, p > 0.05). From a ﬂoristic point R-cran software (R Development Core Team, 2007: www.R-

of view, C. curvula grasslands are rather uniform and the results project.org).

strongly suggested that the area of the relevés was large enough

to sample the within-community ﬂoristic diversity. These ﬁndings

were in concordance with the results of Virtanen et al. (2002), who Results

reported no congruence between the sampling scale and the esti-

mating of species diversity in alpine communities on siliceous soils Partitioning relevés into ﬁve clusters yielded a clear geograph-

in European mountains. ical structure of the spatial diversity patterns of the C. curvula

Taxonomy and nomenclature of the species follow Flora grasslands within the EAS (Fig. 2g and h). Each cluster had a rela-

Europaea (Tutin et al., 1964–1980). Some taxonomically prob- tionship with the main mountain ranges of the EAS: Pyrenees

lematic, or easily misidentiﬁed species were lumped into broadly (hereafter cluster Pyr), Alps (two clusters, Alp1 and Alp2), Carpathi-

deﬁned taxa (Appendix 2). In this paper, we used the term ‘Curvule- ans (cluster Car) and Balkans (cluster Bal). All relevés from the

tum’ to refer to any alpine grassland dominated by C. curvula and Carpathians and the Pyrenees were consistently assigned to the

not to a given phytosociological plant association. corresponding clusters Car and Pyr, respectively. Relevés from the

Balkan mountains showed a more complex picture. Grasslands

Data analysis from Rila and Pirin formed a well deﬁned group (Bal) but the North-

ern part of the range (Stara Planina) and the very few relevés

Obviously, data collated from independent sources do not meet from the Prokletije (Dinarides) were assigned to the Carpathian

the criteria of a sampling protocol for a spatial analysis conducted cluster Car. In the Alps, the pattern was even more complex:

at the European scale. In particular, the oversampling in some areas (i) the two exclusively Alpine groups (Alp1 and Alp2) did not

may seriously inﬂuence the ﬁnal results (Knollová et al., 2005). To exhibit any noticeable geographic structure; (ii) all the relevés

overcome this issue, we randomly sampled a maximum of 5 relevés from the easternmost part of the Alps (Austria) were assigned

within each cell of a geographic grid of 6 latitude and 10 longitude to the Carpathian cluster; and (iii) a small percentage (3%) of

resolution covering the EAS. We had 204 grid cells in total of which the relevés from the Alps were assigned to the Pyrenean cluster.

50 include at least 5 relevés with C. curvula (Fig. 1a). The resulting Finally, the two relevés from Massif Central (France) were more

data subsets comprised 430 relevés. A total of 100 different data closely related to Pyrenean grasslands than to grasslands from

subsets were analyzed. the Alps.

We conducted a similarity-based cluster analysis on each data The delineation of biogeographic regions within the EAS was

subset. Distances among relevés were estimated with the Jaccard’s also investigated by increasing sequentially the number of clusters

index (Jaccard, 1901). For the clustering, we used the Partition- from 2 to 5 (Fig. 2). When a two-group partitioning was prescribed,

ing Around Medoids (PAM) algorithm which is an agglomerative the ﬁrst split in the Curvuletum was between an Eastern group

(or bottom-up) clustering technique. We used the pam function including the Easternmost Alps, the Carpathians, the Balkans and

(Kaufman and Rousseeuw, 1990) as implemented in the R package the Dinarides and a Western group including the rest of the Alps

CLUSTER ver. 1.11.9 (Maechler et al., 2005). The method is based on and the Pyrenees. The second split led to the separation of Pyrenees

the search for a selected k representative objects or medoids among from the Alps and the third one to the Bal cluster. Further separation

the observations. Then, k clusters are constructed by assigning within the Alps became only distinguishable in the ﬁve-group par-

each observation to the nearest medoid. The goal is to ﬁnd k clus- titioning. Geographical consistency in the distribution of clusters

ters that minimize the sum of dissimilarities between groups. The was lost with increased number of clusters (data not shown).

M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178 171

Fig. 2. (Left) Geographical location of the clusters and delineation of the biogeographic regions within the European Alpine System. (Right) Distribution of the relevés from

each mountain range in the clusters. red – Pyr, gray – Alp1, green – Alp2, black – Car, white – Bal. The number of clusters is prescribed in the partitioning analysis. Results are

shown for 2 (a–b), 3(c–d), 4 (e–f) and 5 (g–h) clusters.

Detailed accounts of the ﬂoristic diversity and indicator species

of the ﬁve clusters were as follows.

The Pyr cluster (167 relevés in 36 grid cells, 206 species) com-

prised relevés of high species richness (Fig. 3) and showed a high

number of indicator species (43) – Table 1. Many of these species are

endemic to Pyrenees (e.g. Leontodon pyrenaicus, Oreochloa blanka,

Pedicularis pyrenaica, Thymus nervosus, Hieracium breviscapum, Fes-

tuca eskia, F. glacialis and Ranunculus pyrenaeus) or are also found in

nearby mountains (e.g. Gentiana alpina, Agrostis schleicheri, Helic-

totrichon sedenense, Jasione crispa, Plantago monosperma, Selinum

pyrenaeum and Primula integrifolia). Another important set of indi-

cator species included widely distributed taxa growing on rocky

places, screes or shallow soils (e.g. Arenaria grandiﬂora, A. ciliata,

A. gothica ssp. moehringioides, Minuartia recurva, Potentilla crantzii,

Saxifraga exarata ssp. moschata, Silene ciliata, Polygonum viviparum,

Fig. 3. Species richness per relevé. Means and standard errors are shown per cluster

Linaria alpina, Carex rupestris, Leucanthemopsis alpina and Lychnis

for k = 5 (see Fig. 2g and h). Bars with the same letters are not signiﬁcantly different

alpina). at P < 0.05 (results from a post hoc Tukey test).

172 M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178

Table 1

List of indicator species for each cluster. The ISA metric is the mean of the 100 data subsets analyses (see “Material and methods” section for details).

Cluster Alp1 Alp2 Bal Car Pyr

***

Antennaria carpatica (Wahlenb.) Bluff & Fingerh. 0.45 – – – –

*** ***

Avenula versicolor (Vill.) M. Laínz 0.51 0.53 – – –

*** ***

Leontodon pyrenaicus Gouan ssp. helveticus (Mérat) Finch & P.D. Sell 0.53 0.61 – – –

*** **

Leucanthemopsis alpina (L.) Heywood 0.51 – – – 0.37

*** ***

Potentilla aurea L. ssp. aurea 0.42 0.63 – – –

***

Pulsatilla vernalis (L.) Miller 0.36 – – – –

***

Salix herbacea L. 0.49 ––––

***

Senecio incanus L. ssp. carniolicus (Willd.) Braun–Blanquet 0.45 – – – –

***

Veronica bellidioides L. 0.49 – – – –

Hieracium piliferum Hoppe 0.57 – – – –

Kobresia myosuroides (Vill.) Fiori 0.37 – – – –

** * ***

Phyteuma hemisphaericum L. 0.45 0.40 – – 0.57

** *

Euphrasia minima Jacq. ex DC. 0.45 0.40 –––

Luzula lutea (All.) DC. 0.43 ––––

Primula glutinosa Jacq. 0.30 – – – –

Festuca halleri All. 0.58 – – – –

Phyteuma globulariifolium Sternb. & Hoppe 0.29 – – – –

** **

Poa alpina L. 0.43 – – – 0.38

Phyteuma globulariifolium Sternb. & Hoppe ssp. pedemontanum (R. 0.31 – – – –

Schulz) Becherer

** **

Gentiana punctata L. 0.34 0.38 – – –

Pedicularis kerneri Dalla Torre 0.37 – – – –

Ligusticum mutellinoides (Crantz) Vill. 0.41 ––– –

Agrostis alpina Scop. 0.35 – – – –

** **

Oreochloa disticha (Wulfen) Link 0.41 – – 0.42 –

Lloydia serotina (L.) Reichenb. 0.28 – – – –

** ***

Minuartia sedoides (L.) Hiern 0.47 – – – 0.49

Juncus jacquinii L. 0.35 – – – –

Potentilla frigida Vill. 0.25 – – – –

Androsace obtusifolia All. 0.33 – – – –

** *

Homogyne alpina (L.) Cass. 0.38 0.54 – – –

Primula hirsuta All. 0.21 – – – –

Primula daonensis (Leyb.) Leyb. 0.20 – – – –

Salix serpyllifolia Scop. 0.22 – – – –

* *

Sibbaldia procumbens L. 0.29 ––– 0.26

Saxifraga bryoides L. 0.31 – – – –

Doronicum clusii (All.) Tausch. 0.18 – – – –

Cardamine resedifolia L. 0.20 – – – –

Sempervivum montanum L. 0.37 – – – –

Sesleria caerulea (L.) Ard. 0.21 – – – –

Festuca quadriﬂora Honckeny 0.23 – – – –

Minuartia verna (L.) Hiern 0.20 ––– –

Saxifraga exarata Vill. 0.15 – – – –

Carex sempervirens Vill. – 0.42 – – –

Arnica montana L. – 0.42 – – –

* **

Ligusticum mutellina (L.) Crantz – 0.41 – 0.34 –

Vaccinium myrtillus L. – 0.37 – – –

Pulsatilla alpina (L.) Delarbre ssp. apiifolia (Scop.) Nyman – 0.22 – – –

Plantago alpina L. – 0.39 – – –

Anthoxanthum alpinum Löve et Löve – 0.57 – – –

Campanula scheuchzeri Vill. – 0.49 – – –

Geum montanum L. – 0.44 – – –

Gentiana acaulis L. – 0.49 – – –

Nardus stricta L. – 0.46 – – –

***

Campanula alpina Jacq. ssp. orbelica (Panciˇ c)´ Urum. – – 0.94 – –

***

Dianthus microlepis Boiss. – – 0.93 – –

***

Leontodon croceus Haenke ssp. rilaensis (Hajek) Finch – – 0.57 – –

***

Poa media Schur – – 0.65 – –

***

Ranunculus crenatus Waldst. & Kit. – – 0.58 – –

***

Sesleria comosa Velen. – – 0.78 – –

Festuca riloensis (Hack. ex Hayek) Markgr.–Dann. – – 0.54 – –

Ranunculus pseudomontanus Schur – – 0.40 – –

Alopecurus gerardii Vill. – – 0.38 – –

Scleranthus perennis L. ssp. marginatus (Gauss) Arcangeli – – 0.37 – –

Omalotheca supina (L.) DC. – – 0.48 – –

Achillea clusiana Tausch – – 0.26 – –

Pedicularis verticillata L. – – 0.30 – –

Juniperus communis L. ssp. nana Syme – – 0.33 – –

Arenaria biﬂora L. – – 0.28 – –

Saxifraga pedemontana All. ssp. cymosa Engler – – 0.25 – –

Jasione bulgarica Stoj. & Stef. – – 0.26 – –

Hieracium alpicola Schleich. ex Gaudin – – 0.28 – –

Pedicularis orthantha Griseb. – – 0.28 – –

Jasione laevis Lam. ssp. orbiculata (Griseb. ex Velen.) Tutin – – 0.25 – –

M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178 173

Table 1 (Continued)

Cluster Alp1 Alp2 Bal Car Pyr

***

Campanula alpina Jacq. – – – 0.69 –

*** **

Festuca airoides Lam. – – – 0.65 0.35

***

Juncus triﬁdus L. – – – 0.57 –

***

Phyteuma confusum A. Kerner – – – 0.69 –

***

Potentilla aurea L. ssp. chrysocraspeda (Lehm) Nyman – – – 0.58 –

***

Primula minima L. – – – 0.61 –

***

Rhododendron myrtifolium Schott & Kotschy – – – 0.52 –

Anthemis carpatica Willd. – – – 0.29 –

Veronica baumgartenii Roemer & Scultes – – – 0.21 –

Vaccinium vitis–idaea L. – – – 0.39 –

Dianthus glacialis Haenke ssp. gelidus (Schott, Nyman & Kotschy) Tutin – – – 0.17 –

Pulsatilla alba Rchb. – – – 0.36 –

Viola declinata Waldst. & Kit. – – – 0.17 –

Poa laxa Haenke – – – 0.16 –

Soldanella rugosa L.B. Zhang – – – 0.19 –

Hieracium villosum Jacq. – – – 0.15 –

***

Arenaria grandiﬂora L. – – – – 0.36

***

Armeria alpina Willd. – – – – 0.46

***

Carex ericetorum Pollich – – – – 0.35

***

Gentiana alpina Vill. – – – – 0.84

***

Helictotrichon sedenense (DC.) Holub – – – – 0.39

***

Hieracium breviscapum DC. – – – – 0.32

***

Jasione crispa (Pourr.) Samp. – – – – 0.57

***

Leontodon pyrenaicus Gouan – – – – 0.86

***

Minuartia recurva (All.) Schinz & Thell. – – – – 0.46

***

Oreochloa blanka Deyl – – – – 0.56

***

Pedicularis pyrenaica J. Gay – – – – 0.65

***

Plantago monosperma Pourr. – – – – 0.27

***

Polygonum viviparum L. – – – – 0.70

***

Primula integrifolia L. – – – – 0.52

***

Saxifraga exarata Vill. ssp. moschata (Wulfen) Cavillier – – – – 0.51

***

Silene ciliata Pourr. – – – – 0.34

***

Thymus nervosus J. Gay ex Willk. – – – – 0.53

***

Lychnis alpina L. – – – – 0.30

Ranunculus pyrenaeus L. – – – – 0.29

Festuca eskia Ramond ex DC. – – – – 0.33

Gentianella campestris (L.) Börner – – – – 0.26

Festuca glacialis (Miégev. ex Hack.) K. Richt. – – – – 0.27

Linaria alpina (L.) Miller – – – – 0.25

Festuca nigrescens Lam. – – – – 0.24

Selinum pyrenaeum (L.) Gouan – – – – 0.21

Carex pyrenaica Wahlenb. – – – – 0.23

Carex rupestris All. – – – – 0.22

Arenaria ciliata L. – – – – 0.19

Oxytropis campestris (L.) DC. – – – – 0.2

Agrostis schleicheri Jord. & Verl. – – – – 0.19

Arenaria gothica Fries ssp. moehringioides (J. Murr) Wyse Johnson – – – – 0.17

Hieracium lactucella Wallr. – – – – 0.17

Calluna vulgaris (L.) Hill – – – – 0.20

Antennaria dioica (L.) Gaertner – – – – 0.22

Bellardiochloa variegata (Lam.) Kerguélen – – – – 0.18

Potentilla crantzii (Crantz) G. Beck ex Fritsch – – – – 0.17

Agrostis rupestris All. – – – – 0.39

p < 0.5.

p < 0.01.

***

p < 0.001.

The Car cluster (258 relevés in 40 grid cells, 194 species) Festuca riloensis, Jasione bulgarica, Pedicularis orthantha and Sesleria

included species-poor Curvuletum communities (Fig. 3). The lim- comosa. Other taxa restricted to the Eastern part of the EAS have

ited number of indicator species (18) are distributed in the higher ﬁdelity to the Bal cluster (e.g. Leontodon croceus ssp. rilaen-

Carpathians and the neighboring mountains (e.g. Primula minima, sis, Poa media, Ranunculus crenatus, R. pseudomontanus, Saxifraga

Pulsatilla alba and Phyteuma confusum in Carpathians, Balkans and pedemontana ssp. cymosa) (Fig. 4).

Eastern Alps, Potentilla aurea ssp. chrysocraspeda, Veronica baum- The Alp1 (297 relevés in 67 grid cells, 277 species) and Alp2

gartenii and Rhododendron myrtifolium in Carpathians and Balkans, clusters (52 relevés in 28 grid cells, 171 species) included the

Campanula alpina in Carpathians and Eastern Alps) (Fig. 4; Table 1). species-richest Curvuletum communities of the EAS (Fig. 3). The

Few of these species are Carpathian endemites (Dianthus glacialis distinction between the two clusters was not geographical (Fig. 2g).

ssp. gelidus, Viola declinata and Soldanella rugosa). Examination of indicator species lists rather suggests an ecologi-

The small Bal cluster (79 relevés in 9 grid-cells, 85 species) cal partitioning. Indicator species of Alp1 (42) occur in the upper

included grasslands from the Rila and Pirin Mountains. Species rich- part of the alpine belt, and are mostly found on shallow soils

ness in these grasslands is the lowest of the EAS (Fig. 3). The set of of summits and ridges (e.g. Antennaria carpatica, Veronica bellid-

indicator species (20) comprised taxa endemic to Balkan moun- ioides, Oreochloa disticha, Kobresia myosuroides, Minuartia sedoides,

tains such as Campanula alpina ssp. orbelica, Dianthus microlepis, Hieracium piliferum, Senecio incanus ssp. carniolicus, Lloydia serotina,

174 M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178

Fig. 4. The geographical distribution of the indicator species identiﬁed for each cluster (the size of the circle is proportional to the percentage of indicator species that occur

in the grid cell; colors as in Fig. 2).

Androsace obtusifolia, Salix serpyllifolia, Saxifraga bryoides, S. exarata, Large geographical distances that separate mountain ranges

Doronicum clusii, Sempervivum montanum, Leucanthemopsis alpina). of the EAS did not always translate into marked ﬂoristic dis-

Indicator species of Alp2 (18) include species from the lower similarities. The most striking example of disconnection between

part of the alpine belt and the ecotone with subapine grasslands geography and ﬂoristic diversity was the delineation of a major

(e.g. Homogyne alpina, Nardus stricta, Plantago alpina, Anthoxan- ﬂoristic boundary that separates the group of Easternmost Alps,

thum alpinum, Ligusticum mutellina, Campanula scheuchzeri, Arnica Carpathian and Northernmost Balkan grasslands (Car) from that

montana, Vaccinium myrtillus, Pulsatilla alpina ssp. apiifolia, Geum of Western Europe and the Southern Balkans. The alpine vegeta-

montanum and Gentiana acaulis). These taxa have a wide dis- tion from Stara Planina shows closer similarities with Carpathian

tribution range in the mountains of EAS (Fig. 4) and were less grasslands than with the nearby Rila and Pirin grasslands. Previ-

discriminant for the cluster (Table 1). The number of local endemics ous phytogeographical studies have acknowledged the existence

among the indicator species was particularly low for Alp1 with of ﬂoristic similarities between the mountain ﬂoras of the east-

only Festuca halleri, Primula glutinosa, P. daonensis and Phyteuma ernmost part of the EAS and a core group of “Carpatho-Balkanic”

globulariifolium. There was no species endemic to Alps among the elements has been proposed (Coldea, 1991). Our large synthe-

indicator species of Alp2. sis of Curvuletum relevés supports this hypothesis. Roussakova

(2000) has also highlighted the important dissimilarities between

Discussion the vegetation of the alpine belts of Rila and Stara Planina. Notice-

ably, Carpathian populations of C. curvula are genetically closely

related to the populations from Stara Planina (Pus¸ cas¸ et al., 2008a).

Species diversity patterns of the Carex curvula-dominated grass-

From both geographic and ﬂoristic point of view, the Dinar-

lands allow to delineate biogeographic regions within the alpine

ides have an intermediate position between the Alps, Carpathians

system of European temperate mountains. The partitioning of veg-

and Balkan mountains (Fig. 1, Lakusiˇ c,´ 1970). Our analysis shows

etation relevés into ﬁve clusters was partly congruent with the

that the Dinaric acidic alpine grasslands are also closer to the

physiography of European mountains.

Carpathian group. However, we only had a limited number of

Congruence between geography and ﬂoristic diversity was

vegetation relevés for the high mountains of Macedonia and

strong for the Pyrenees and the Southern Balkans (Pirin and

Bosnia-Hercegovina, and this preliminary result will have to be

Rila). These southern mountain ranges that are under Mediter-

conﬁrmed by including more data from this area.

ranean inﬂuence exhibit a high level of endemism (Küpfer, 1974;

Our analysis clearly assigned the easternmost alpine Curvule-

Roussakova, 2000; Stojanov and Kitanov, 1926). Several of these

tum to the Carpathian-centered cluster. The major ﬂoristic

endemic taxa occur in the acidic alpine grasslands we focused on

boundary separating it from acidic grasslands in the central and

and this explains the agreement between geography and ﬂoristic

clustering. western parts of the Alps runs between the Niedere Tauern (to

M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178 175

the East) and the Hohe Tauern (to the West). The Curvuletum sites slopes and wind-blown crests. C. curvula grasslands in the Pyrenees

from the Lavanttaler Alpen and the Wölzer, Triebner and Seckauer are also generally found in the uppermost part of the alpine belt.

Tauern in the Niedere Tauern have been included in the Phyteu- They are developed on shallower soils than in the Alps (M. Pus¸ cas¸

mato confusi – Caricetum curvulae by Theurillat (1996). Existence and Ph. Choler, unpublished). Because of severe summer drought

of ﬂoristic similarities between the Carpathian and Eastern Alps and rapid snow melt in the spring, the Curvuletum communities of

ﬂora has already been recognized (Schneeweiss and Schönswetter, the Pyrenees tend to exhibit more stress-tolerant species as com-

1999). Recently, Finnie et al. (2007) analyzed the spatial distribu- pared with what is observed in the acidic alpine grasslands of the

tion of about 20% of the European Flora and pointed to the existence Alps (Braun-Blanquet, 1948; Negre, 1969).

of one Carpathian ﬂoristic element (“Rumex alpinus”) that is well

represented in the easternmost part of the Alps. Thiel-Egenter et al. Conclusion

(2011), analyzing the distribution of a large dataset of acidic high

mountain species in the Alps, also conﬁrmed an important break

This study presents the ﬁrst comprehensive analysis of

zone in this area (the “Salzburg-Trieste break-line”), and explained

community-related species distribution patterns within the alpine

this by the large presence of Carpathian species in easternmost part

belt of the EAS. Our ﬁndings are based on the cluster analysis of an

of the Alps. Our results conﬁrm the importance of this boundary,

exhaustive ﬂoristic data set of acidic alpine grasslands dominated

and moreover, show that it represents the most important dividing

by Carex curvula. Spatial patterns of diversity in these grasslands

zone for the acidic alpine ﬂora inside of the EAS. To our knowledge,

are driven by an intricacy of local-scale ecological drivers and large-

our study is the ﬁrst one supporting this ﬁnding at the level of plant

scale historical drivers. We found that the high level of endemism

communities.

in alpine communities can explain the ﬂoristic separation of the

Surprisingly, none of the seven North to South phytogeographi-

Southernmost ranges (the Balkans and the Pyrenees). We hypoth-

cal boundaries proposed for the Alps (Ozenda, 1985) corresponds to

esize that the ﬂoristic similarities between the alpine vegetation of

this major ﬂoristic boundary. Our ﬁndings and others indicate that

the Easternmost Alps, the Carpathians, and the Northern Balkans

these delineations should be reconsidered at least when examining

can be explained by a shared Quaternary history. Finally, the large

high-elevation vegetation.

elevational amplitude of alpine acidic grasslands in the Alps must

It is usually hypothesized that ﬂoristic similarities between dis-

be emphasized, explaining why the primary factor of between-

tant areas reﬂect some shared history (Ron, 2000). The last major

community diversity is ecological and not geographical in this

events that inﬂuenced species diversity and species assemblages

mountain range.

within the EAS were the climatic oscillations during the Pleis-

The delineation of biogeographical regions within the EAS has

tocene (Comes and Kadereit, 1998; Taberlet et al., 1998). While

mainly been based on qualitative approaches with emphasis given

most of the Alps were almost entirely covered by a large ice-

to the distribution of particular species (especially endemics)

sheet during the glaciations, the Eastern part of Austrian Alps

and/or vegetation ecology. Our statistical approach using quanti-

remained almost ice free (Voges, 1995). The same situation also

tative data from relevés across the whole EAS range provides new

characterized the Carpathians and the Balkans, where only local-

insights on the alpine biogeography of European temperate moun-

ized glaciers were present on the highest summits (Bazilova and

tains and supports the existence of overlooked ﬂoristic boundaries

Tonkov, 2000; Pawłowski, 1970; Ronikier, 2011). In these mountain

in the European Alpine System.

ranges the alpine species have responded to the cooling climate by

a local downward shift of their altitudinal distribution (Pus¸ cas¸ et al.,

Acknowledgements

2008b; Tribsch and Schönswetter, 2003), and this has probably

facilitated species migration between different mountain ranges

We are grateful to Corina Bas¸ nou, Michał Ronikier, Jozef

of the EAS, even distant ones (Mráz et al., 2007; Schönswetter

Sibík,ˇ Gheorghe Coldea, Harald Pauli, Peter Schönswetter, Tenyo

et al., 2003; Zhang et al., 2001). Noticeably, alpine communities

Meshinev, Tone Wraber, Rolland Douzet, Serge Aubert and the

from the Easternmost Alps included in Car cluster are precisely

staff from the Conservatoire Botanique National Alpin (Gap, France)

located in an area considered as the largest glacial refugium

for their valuable help in collating data. We are also indebted to

for acidic alpine species (refugium S1, Tribsch and Schönswetter,

several anonymous referees for their comments on previous ver-

2003) and the ﬂoristic boundary identiﬁed here approximately

sions of the manuscript. M. Pus¸ cas¸ was funded by the Romanian

matches the maximum extent of the glaciers during the last

glaciation. Ministry of Education, Research and Innovation (CNCSIS-UEFISCSU,

project PNII-Resurse Umane, PD 405/2010). Logistical support was

Species distribution patterns result from a combination of local

provided by the Alpine ﬁeld station of the University of Greno-

scale environmental factors and larger scale evolutionary and his-

ble and the A. Borza Botanical Garden (Babes¸ -Bolyai University in

torical factors (Finnie et al., 2007). Our results show that the local

Cluj-Napoca).

habitat characteristics are to be considered even in large-scale com-

parative studies. The Alp1 cluster is the largest cluster revealed

by our analysis (Fig. 2). It comprises two phytosociological asso- Appendix 1. The list of the monographs used for the

ciations described for the Alps by Theurillat (1996), namely the synthesis of Carex curvula dominated grasslands.

Senecioni incani-Caricetum curvulae for the Western Alps and the

typical Caricetum curvulae from the Central Alps. Our cluster anal- Alexiu, V., 1998. Vegetat¸ia Masivului Iezer-Papus˘ ¸ a. Studiu Fito-

ysis of C. curvula-dominated grasslands at the entire range of EAS cenologic. Editura Cultura, Pites¸ ti.

did not support this East-West distinction within the Alps. The Ascaso, J., 1992. Estudio Fitocenològico y Valoración de los

main ﬂoristic dissimilarity within alpine grasslands of the Alps was Pastos de Puerto del Valle de Benasque (Pirineo Oscense). Tesis

primarily related to elevation. The Alp2 cluster assembles low ele- Doctoral, Universidad de Zaragoza.

vation C. curvula grasslands, and many of its indicator species are Ballesteros, E., Canalís, V., 1991. La vegetació culminal dels Mas-

abundant in the subalpine acidic grasslands (Nardion) and widely sissos de Besiberri i de Mulleres (Pirineus centrals catalans). Butlletí

distributed in the Alps (Coldea, 1991; Theurillat et al., 1994). de la Institució Catalana d’Història Natural, Secció Botànica 59,

Ecological factors also explain the clustering of a small set of 95–106.

relevés from the Alps with the Pyrenees. These grasslands are found Baudière, A., 2000. La Haute Vallée de Carenc¸ a (Pyrénées-

in the highest part of the alpine belt (ca. 3000 m), mainly on rocky Orientales). Le Monde des Plantes 469, 12–20.

176 M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178

Baudière, A., Bonnet, A.L.-M., 1965. Etude phytogéographique Hartl, H., 1963. Die Vegetation des Eisenhutes im Kärntner Nock-

de la Haute-Vallée de Carenc¸ a (Pyrénées-Orientales). Deuxième gebiet. Carinthia II, 293–336.

inventaire ﬂoristique. Vie et Milieu 16, 599–630. Hartmann, H., 1972. Die azidophilen Pﬂanzengesellschaften

Baudière, A., Gauquelin, T., Serve, L., 1985. La régression des in der alpinen Stufe des westlichen Rätikons und der Schesa-

pelouses culminales et les facteurs de la géomorphologie sur les planagruppe. Jahresbericht der Naturforschenden Gesellschaft

hautes surfaces planes oriento-pyrénéennes. Colloques Phytosoci- Graubündens 94, 1–81.

ologiques 13, 149–171. Horvat, I., Pawlowski, B., Walas, J., 1937. Phytosoziologische

Baudière, A., Serve, L., 1975. Les groupements à Carex curvula Studien über die Hochgebirgsvegetation der Rila Planina in Bulgar-

subsp. curvula All. des Pyrénées Orientales et leur interprétation ien. Bulletin de l’Académie Polonaise des Sciences et des Lettres,

phytogéographique. Colloques Phytosociologiques, 1–8. Classe des Sciences Mathématiques et Naturelles, Série B: Sciences

Baudière, A., Serve, L., 1975. Les landes rases à Loiseleuria Naturelles, 159–189.

procumbens en Pyrénées Orientales et leur intérêt phytogéo- Klein, J.-C., 1979. Application de l’analyse factorielle des cor-

graphique. Colloques Phytosociologiques, 337–347. respondances à l’étude phytosociologique de l’étage alpin des

Borza, A., 1934. Studii ﬁtosociologice în Munt¸ii Retezatului. Pyrénées centrales. Phytocoenologia 5, 125–188.

Buletinul Gradinii˘ Botanice s¸ i al Muzeului Botanic Cluj 14, 1–84. Lakusic, R., 1970. Die Vegetation der südöstlichen Dinariden.

Bos¸ caiu, M., Bos¸ caiu, N., Ehrendorfer, F., 1998. The Cerastium Vegetatio 21, 321–373.

alpinum group (Caryophyllaceae) in the South Eastern Carpatians. Malinovsky, K.A., Diduck, Y.P., 2000. High mountain vegetation.

Contribut¸ii Botanice, 5–39. In: Vegetation of the Ukraine. Solomakha, V.A. (Ed.). Phytosocio-

Bos¸ caiu, N., 1971. Flora s¸ i Vegetat¸ia Munt¸ilor T¸ arcu, Godeanu s¸ i centre, Kiev, pp. 1–230.

Cernei. Editura Academiei Republicii Socialiste România, Bucures¸ ti. Meshinev, T., Apostolova, I., Kachaunova, E., Velchev, V., Bondev,

Braun-Blanquet, G., Braun-Blanquet, J., 1931. Recherches phy- I., 2000. Flora and plant communities. In: High Mountain Treeless

togéographiques sur le massif du Gross Glockner (Hohe Tauern). Zone of the Central Balkan National Park. Biological Diversity and

Communication S.I.G.M.A. 13, 1–65. Problems of its Conservation. Popov, A., Meshinev, T. (Eds.). BSBCP,

Braun-Blanquet, J., 1948. La végétation alpine et nivale des Soﬁa, pp. 1–337.

Pyrénées Orientales. Communication S.I.G.M.A. 98, 1–306. Michalet, R., Philippe, T., 1995. Les landes et pelouses acidiphiles

Braun-Blanquet, J., 1969. Die Pﬂanzengesellschaften der Rätis- de l’étage subalpin des Monts Dore (Massif Central Franc¸ ais):

chen Alpen im Rahmen ihrer Gesamtverbreitung Bischofberger, Syntaxonomie et potentialités dynamiques. Colloques Phytosoci-

Chur. ologiques 25, 433–471.

Braun-Blanquet, J., Jenny, H., 1926. Vegetations-Entwicklung Mondino, G.P., 1966. Cenosi a Carex curvula All. in alta Val d’Ala

und Bodenbildung in der alpinen Stufe der Zentralalpen (Klimaxge- (Valli di Lanzo – Alpi Graie). Allionia 12, 103–117.

biet des Caricion curvulae). Denkschriften der Schweizerischen Mustin, L., 1983. Contribution a l’Etude de la Végétation des

Naturforschenden Gesellschaft 63, 183–349. Milieux Supraforestiers Pyrénéens: le Vallon de Laurenti (Ariege).

Buia, A., 1943. Contribut¸iuni la studiul ﬁtosociologic al pas˘ ¸ unilor PhD Thesis, Université Paul Sabatier, Toulouse.

din Munt¸ii Carpat¸i. Buletinul Facultat˘ ¸ii Agricole Cluj-Timis¸ oara 10, Negre, R., 1969. Le Gentiano-Caricetum curvulae dans

143–168. la région Louchonaise (Pyrénées centrales). Vegetatio 18,

Buia, A., Paun,˘ M., Pavel, C., 1962. Studiul geobotanic al pajis¸ tilor. 167–201.

In: Pajis¸ tile din Masivul Parâng s¸ i Îmbunat˘ at˘ ¸irea lor. Editura Agro- Negre, R., 1970. La végétation du bassin de l’One (Pyrénées cen-

Silvica,˘ Bucures¸ ti, pp. 143–274. trales). Portugaliae Acta Biologica (B) 11, 51–166.

Buia, A., Paun,˘ M., Safta, I., 1959. Contribut¸iigeobotanice asupra Niculescu, M., 2006. Flora s¸ i Vegetat¸ia Bazinului Superior al

pas˘ ¸ unilor s¸ i fânet¸elor din Oltenia. Lucrarile˘ S¸ tiintiﬁce ale Institutu- Luncavat˘ ¸ului (Judet¸ulVâlcea). PhD Thesis, Babes¸ -Bolyai University,

lui Agronomic Craiova, 93–183. Cluj-Napoca.

Caccianiga, M., Armiraglio, S., Andreis, C., 2000. Le formazioni Pauli, H., 1993. Untersuchungen zur Phytosoziologischen und

con Carex curvula e i microarbustei a Loiseleuria procumbens del Ökologischen Stellung von Festuca pseudodura in den Niederen

versante meridionale delle Alpi Orobie. Fitosociologia 37, 21–38. Tauern. Diplomarbeit, Universität Wien.

Carreras, J., Carrillo, E., Masalles, R., Ninot, J.M., Vigo, J., 1993. El Pignatti, E., Pignatti, S., 1958. Un’escursione al Passo di Gavia.

poblament vegetal de les valls de Barravés i de Castanesa. I – Flora Archivio Botanico e Biogeograﬁco Italiano 34, 137-153.

i vegetacio. Acta Botanica Barcinonensia 42, 1–392. Poldini, L., Oriolo, G., 1997. La vegetazione dei pascoli a Nar-

Carrillo, E., Ninot, J.M., 1992. Flora y vegetatio de les valls d’Espot dus stricta e delle praterie subalpine acidoﬁle in Friuli (NE-Italia).

i de Boi. Institut d’Estudis Catalans, Barcelona. Fitosociologia 34, 127–158.

Coldea, G., 1990. Munt¸ii Rodnei, Studiu Geobotanic. Editura Pus¸ caru, D., Pus¸ caru-Soroceanu, E., Pauca,˘ A., et al., 1956.

Academiei Române, Bucures¸ ti. Pas˘ ¸ unile Alpine din Munt¸ii Bucegi. Editura Academiei Republicii

Coldea, G., Pînzaru, G., 1986. La végétation de la Réserve Bila-Lala Populare Române, Bucures¸ ti.

des Monts Rodnei. Contribut¸ii Botanice, 153–169. Reisigl, H., Pitschmann, H., 1958. Obere Grenzen von Flora und

Csurös, I., 1957. Adatok a Fogarasi havasok központi része alpin Vegetation in der Nivalstufe der Zentralen Ötzatler Alpen (Tirol).

vegetaciojanak ismeretèhez. A Kolozsvari V. Babes¸ es Bolyai Egyete- Vegetatio 8, 93–129.

mek Közlémenyei, Természettudomanyi sorozat, 303–329. Resmerit¸a,˘ I., 1974. Cl. Juncetea triﬁdi, Hadac in Klinka et Hadac

Csurös, S¸ ., Kovacs, A., Moldovan, I., 1964. Cercetari˘ de vegetat¸ieîn 44 din Parcul Nat¸ional Retezat. Sargetia, Acta Musei Devensis, Ser.

rezervat¸ia s¸ tiintiﬁca˘ a Parcului National Retezat. Contribut¸iiBotan- Scientia Naturae 10, 112–129.

ice, 167–188. Resmerit¸a,˘ I., 1981. Vegetat¸ia rezervat¸iei naturale “Pietrosul

Eggler, J., 1954. Vegetationsaufnahmen alpiner Rasenge- Rodnei”. Studia Universitatis Babes¸ -Bolyai, Biologia, 3–12.

sellschaften in Oberkärnten und Osttirol. Carinthiaca II 64, 99–105. Resmerit¸a,˘ I., Rat¸iu, O., 1983. Contribut¸ii la cunoas¸ terea

Flütsch, P., 1930. Über die Pﬂanzengesellschaften der alpinen vegetat¸iei alpine din Munt¸ii Rodnei. Contribut¸ii Botanice,

Stufe des Berninagebietes. Jahresbericht der Naturforschenden 99–110.

Gesellschaft Graubündens 68, 37–88. Rivas-Martinez, S., 1974. Los pastizales del Festucion supinae y

Ghis¸ a, E., 1940. Contribut¸iuni la studiul ﬁtosociologic al Munt¸ilor Festucion eskiae (Juncetea triﬁdi) en el Pirineo Central. Collectanea

Fag˘ aras˘ ¸ ului. Buletinul Gradinii˘ Botanice Cluj 20, 127–141. Botanica 9, 5–23.

M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178 177

Rivas-Martinez, S., Bascones, J.C., Diaz, T.E., Fernandez-Gonzales,

Aggregates or groups of taxa Taxa included

F., Loidi, J., 1991. Vegetacion del Pirineo occidental y Navarra. Itinera

Hieracium praecox agg. Hieracium praecox Sch. Bip.

geobotanica 5, 5–456.

Hieracium schmidtii Tausch

Roussakova, V., 2000. Végétation alpine et sous-alpine

Leontodon hispidus agg. Leontodon hispidus L.

supérieure de la montagne de Rila (Bulgarie). Braun-Blanquetia 25,

Leontodon hispidus L. subsp. alpinus (Jacg.)

1–132.

Finch & P.D. Sell

Rübel, E., 1911. Pﬂanzengeographische Monographie des

Lotus corniculatus agg. Lotus alpinus (DC.) Schleicher cx Ramond

Bernina-Gebietes. Botanische Jahrbücher für Systematik,

Lotus corniculatus L.

Pﬂanzengeschichte und Pﬂanzengeographie 47, 1–296.

Luzula campestris agg. Luzula campestnis (Ehrh.) Lej.

Schneeweiss, G.M., Schönswetter, P., 1999. Feinverbreitung,

Luzula multiﬁora (Ehrh.) Lej.

Ökologie und Gesellschaftsanschluß reliktischer Gefäßpﬂanzen der

Luzula sudetica (Willd.) DC. in Lam. & DC.

Niederen Tauern östlich des Sölkpasses (Steiermark, Österreich). [1815]

Staphia 61, 1–242.

Luzula spicata group Luzula spicata (L.) DC.

Schneider-Binder, E., Voik, W., 1979 Asociat¸iile din Clasa Sal-

Luzula italica Parl.

icetea herbaceae Br.-Bl. 1947 în Carpat¸ii Meridionali cu privire Luzula hispanica Chrtek & KrIsa

speciala˘ asupra celor din Munt¸ii Fag˘ aras˘ ¸ ului. Studii s¸ i Comunicari,˘

Sesleria coerulans agg. Sesleria bielzii Schur

S¸ tiint¸ele Naturii, Muzeul Brukenthal 23, 221–237. Sesleria coerulans Friv.

Serve, L., 1989. Recherches Ecologiques sur Quelques Groupe-

Silene acaulis agg. Silene acaulis (L.) Jacq.

ments Végétaux de l’Etage Alpin des Pyrénées Orientales thèse,

Silene acaulis (L.) Jacq. subsp. bryoides (Jordan)

Université de Perpignan, Perpignan. Nyman

Simon, T., 1958. Über die alpinen Pﬂanzengesellschaften des

Solidago virgaurea agg. Solidago virgaurea L.

Pirin-Gebirges. Acta Botanica Academiae Scientiarum Hungaricae

Solidago virgaurea L. subsp. alpestris (Waldst. &

4, 159–190. Kit. ex Walld.) Gremli

Stancu, D.I., 2002. Flora s¸ i Vegetat¸ia Munt¸ilor Râiosu s¸ i Buda,

Taraxacum sp. Taraxacum apenninum gr.

Masivul Fag˘ aras˘ ¸ teza˘ de doctorat, Academia Româna,˘ Bucures¸ ti. Taraxacum alpinum Weber

Wikus, E., 1961. Die Vegetation der Lienzer Dolomiten (Osttirol). Taraxacum nigricans (Kit.) Rchb.

Taraxacum ofﬁcinale Weber

Arch. Bot. Biogeogr. Ital. 37, 13–35.

Taraxacum dissectum (Ledeb.) Ledeb.

Appendix 2. List of taxa that were taxonomically References

reconsidered for the numerical analysis.

Aeschimann, D., Lauber, K., Moser, D.M., Theurillat, J.-P., 2004. Flora Alpina. Belin,

Paris.

Aggregates or groups of taxa Taxa included

Allioni, C., 1785. Flora Pedemontana sive enumeratio methodica stirpium indige-

narum pedemontii. Augustae Taurinorum, Ioannes Michael Briolus, Torino.

Androsace carnea agg. Androsace carnea L.

Alvarez, N., et al. (20 authors), 2009. History or ecology? Substrate type as a major

Androsace carnea L. subsp. laggeri (A. Huet)

driver of spatial genetic structure in Alpine plants. Ecol. Lett. 12, 632–640.

Nyman

Barthlott, W., Mutke, J., Raﬁqpoor, D., Kier, G., Kreft, H., 2005. Global centers of

Androsace adﬁnis Biroli

vascular plant diversity. In: Endress, P.K., Lüttge, U., Parthier, B. (Eds.), From

Plant Taxonomy to Evolutionary Biology. Nova Acta Leopoldina N.F. 92, Nr. 342.

Anthyllis vulneraria agg. Anthyllis vulneraria L. subsp. vulnerarioides

Wissensch, Verlagsgesellsch, Stuttgart, pp. 61–83.

(All.) Arcang.

Barthlott, W., et al. (8 authors), 2007. Geographic patterns of vascular plant diversity

Anthyllis vulneraria L. subsp. alpestris (Kit.)

at continental to global scales. Erdkunde 61, 305–315.

Aseherson & Graebner

Baumgarten, J.C.G., 1816. Enumeratio stirpium magno Transsilvaniae principatui

Anthyllis vulneraria L. subsp. iberica (W. Becker)

praeprimis indigenarum in usum nostratum botanophilorum conscripta inque

Jalas

ordinem sexualinaturalem concinnata. Libraria Camesianae, Vindebonae.

Bazilova, E.D., Tonkov, S.B., 2000. Pollen from Lake Sedmo Rilsko reveals southeast

Carex atrata agg. Carex atrata L.

European postglacial vegetation in the highest mountain area of the Balkans.

Carex atrata L. subsp. aterrima (Hoppe) Celak.

New Phytol. 148, 315–325.

Borza, A., 1934. Studii ﬁtosociologice în Munt¸iiRetezatului. Bul. Grad.˘ Bot. Muz. Bot.

Carex bigelowii agg. Carex bigelowii Torr. cx Schw.

Cluj 14, 1–84.

Carex bigelowii Torr. cx Schw. subsp. rigida

Schultze-Motel Braun-Blanquet, J., 1923. L’Origine et le Développement des Flores dans le Massif

Central de France avec Aperc¸ u sur les Migrations des Flores dans l’Europe Sud-

Carex nigra agg. Carex nigra (L.) Reichard Occidentale. Léon Lhomme, Beer et Cie, Paris, Zürich.

Carex nigra (L.) Reichard subsp. alpina (Gaudin) Braun-Blanquet, J., 1930. Zentralalpen und Tatra, eine pﬂanzensoziologische Paral-

Lemke lele. Veröff. Geobot. Inst. Rübel Zürich 6, 1–43.

Braun-Blanquet, J., 1932. Plant Sociology. McGraw-Hill, New York.

Carex ornithopoda agg. Carex ornithopoda Willd. Braun-Blanquet, J., 1948. La végétation alpine et nivale des Pyrénées Orientales.

Carex ornithopoda Willd. subsp. Commun. SIGMA 98, 1–306.

ornithopodioides (Hausm.) Nyman Brockmann-Jerosch, H., 1907. Die Pﬂanzengesellschaften der Schweizeralpen.

Engelmann, Leipzig.

Cerastium alpinum agg. Cerastium alpinum L.

Chater, A.O., 1980. Carex L. In: Tutin, T.G., Heywood, V.H., Burges, N.A., et al. (Eds.),

Cerastium alpinum L. subsp. lanatum (Lam.)

Flora Europaea. Cambridge University Press, Cambridge, pp. 290–323.

Ascherson & Graebner Choler, P., Michalet, R., 2002. Niche differentiation and distribution of Carex curvula

along a bioclimatic gradient in the southwestern Alps. J. Veg. Sci. 13, 851–858.

Erigeron uniﬁorus agg. Erigeron uniﬁorus L.

Choler, P., Erschbamer, B., Tribsch, A., Gielly, L., Taberlet, P., 2004. Genetic introgres-

Erigeron aragonensis Vierh.

sion as a potential to widen species’ niche: insights from alpine Carex curvula.

Proc. Natl. Acad. Sci. U.S.A. 101, 171–176.

Gentiana verna agg. Gentiana brachyphylla Vill.

Chytry,´ M., Tichy,´ L., Holt, J., Botta-Dukát, Z., 2002. Determination of diagnostic

Gentiana verna L.

species with statistical ﬁdelity measures. J. Veg. Sci. 13, 79–90.

Gentiana orbicularis Schur

Coldea, G., 1991. Prodrome des associations végétales des Carpates du Sud-Est

(Carpates Roumaines). Doc. Phytol. 13, 317–539.

Hieracium alpinum agg. Hieracium alpinum L.

Coldea, G., Stoica, I.A., Pus¸ cas¸ , M., Ursu, T., Oprea, A., + IntraBioDiv Consortium, 2009.

Hieracium halleri Vill.

Alpine-subalpine species richness of the Romanian Carpathians and the current

Hieracium pilosella agg. Hieracium pilosella L. conservation status of rare species. Biodiv. Conserv. 18, 1441–1458.

Hieracium pilosella L. subsp. tnichosoma Peter Comes, H.P., Kadereit, J.W., 1998. The effect of quaternary climatic changes on plant

distribution and evolution. Trends Plant. Sci. 3, 432–438.

178 M. Pus¸ cas¸ , P. Choler / Flora 207 (2012) 168–178

Comes, H.P., Kadereit, J.W., 2003. Spatial and temporal patterns in the evolution of Pawłowski, B., 1970. Remarques sur l’endémisme dans la ﬂore des Alpes et des

the ﬂora of the European Alpine System. Taxon 52, 451–462. Carpates. Vegetatio 21, 181–243.

de Lapeyrouse, P.P., 1818. Histoire abrégée des plantes des Pyrénées et itinéraire des Pus¸ cas¸ , M., 2005. Carpathian chorology of Carex curvula All., within European alpine

botanistes dans ses montagnes. Bellegarrigue, Toulouse. system. Contrib. Bot. 40, 5–14.

de Caceres, M., Legendre, P., 2009. Associations between species and groups of sites: Pus¸ cas¸ , M., Gafta, D., Cristea, V., 2005. L’analyse èco-coenotique des prairies èdiﬁèes

indices and statistical inference. Ecology 90, 3566–3574. par Carex curvula All. des Carpates roumaines. Acta. Bot. Gall. 152, 497–506.

Dufrêne, M., Legendre, P., 1997. Species assemblages and indicator species: the need Pus¸ cas¸ , M., Choler, P., Tribsch, A., Gielly, L., Rioux, D., Gaudeul, M., Taberlet, P., 2008a.

for a ﬂexible asymetrical approach. Ecol. Monogr. 67, 345–366. Post-glacial history of the dominant alpine sedge Carex curvula in the European

EEA, 2005. Biogeographical Regions, Europe 2005. European Environment Agency, Alpine System inferred from nuclear and chloroplast markers. Mol. Ecol. 17,

Copenhagen. 2417–2429.

Erschbamer, B., 1992. Zwei neue Gesellschaften mit Krummseggen (Carex curvula Pus¸ cas¸ , M., Taberlet, P., Choler, P., 2008b. No positive correlation between species

ssp. rosae, Carex curvula ssp. curvula) aus den Alpen: ein Beitrag zur Klärung and genetic diversity in European alpine grasslands dominated by Carex curvula.

eines alten ökologischen Rätsels. Phytocoenologia 21, 91–116. Divers. Distrib. 14, 852–861.

Finnie, T.J.R., Preston, C.D., Hill, M.O., Uotila, P., Crawley, M.J., 2007. Floristic ele- Rochel, A., 1838. Botanische Reise in das Banat im Jahre 1835. Heckenast, Leipzig.

ments in European vascular plants: an analysis based on Atlas Florae Europaeae. Ron, S.R., 2000. Biogeographic area relationships of lowland Neotropical rainforest

J. Biogeogr. 34, 1848–1872. based on raw distributions of vertebrate groups. Biol. J. Linn. Soc. 71, 379–402.

Gaussen, H., Lerendde, C., 1949. Les endémiques pyrénéo-cantabriques dans la Ronikier, M., 2011. Biogeography of high-mountain plants in the Carpathians: an

région centrale des Pyrénées. Bull. Soc. Bot. Fr. 96, 57–83. emerging phylogeographical perspective. Taxon 60, 373–389.

Gilomen, H., 1938. Carex curvula All. sp. nov. rosae (Kalk-Krummsegge). Ber. Geobot. Roussakova, V., 2000. Végétation alpine et sous-alpine supérieure de la montagne

Forsch. Inst. Rübel Zürich, 77–104. de Rila (Bulgarie). Braun-Blanquetia 25, 1–132.

Grabherr, G., Gottfried, M., Pauli, H., 2000. GLORIA: a global observation research Rübel, E., 1911. Pﬂanzengeographische Monographie des Bernina-Gebietes. Bot.

initiative in Alpine environments. Mt. Res. Dev. 20, 190–191. Jahrb. Syst. Pﬂanzengesch. Pﬂanzengeogr. 47, 1–296.

Heald, W.F., 1951. Sky islands of Arizona. Nat. Hist. 60, 56–63. Schneeweiss, G.M., Schönswetter, P., 1999. Feinverbreitung, Ökologie und

Horvat, I., Glavac, V., Ellenberg, H., 1974. Vegetation Südosteuropas. G. Fischer, Jena. Gesellschaftsanschluß reliktischer Gefäßpﬂanzen der Niederen Tauern östlich

Horvat, I., Pawłowski, B., Walas, J., 1937. Phytosoziologische Studien über die des Sölkpasses (Steiermark Österreich). Stapﬁa 61, 1–242.

Hochgebirgsvegetation der Rila Planina in Bulgarien. Bull. Int. Acad. Pol. Sci. Lett., Schönswetter, P., Paun,˘ O., Tribsch, A., Niklfeld, H., 2003. Out of the Alps: coloniza-

Cl. Sci. Math. Nat., Ser. B, 159–189. tion of Northern Europe by East Alpine populations of the Glacier Buttercup

Jaccard, P., 1901. Distribution de la ﬂore alpine dans le bassin des Dranses et dans Ranunculus glacialis L. (Ranunculaceae). Mol. Ecol. 12, 3373–3381.

quelques régions voísines. Bull. Soc. Vaudoise Sci. Nat. 37, 241–272. Schönswetter, P., Stehlik, I., Holderegger, R., Tribsch, A., 2005. Molecular evidence

Kadereit, J.W., Griebeler, E.M., Comes, H.P., 2004. Quaternary diversiﬁcation in Euro- for glacial refugia of mountain plants in the European Alps. Mol. Ecol. 14,

pean alpine plants: pattern and process. Phil. Trans. R. Soc. Lond. B 359, 265–274. 3547–3555.

Kaufman, L., Rousseeuw, P.J., 1990. Finding Groups in Data: An Introduction to Clus- Sibík,ˇ J., Sibíkova,ˇ I., Kliment, J., 2010. The subalpine Pinus mugo-communities of the

ter Analysis. John Wiley & Sons, New York. Carpathians with a European perspective. Phytocoenologia 40, 155–188.

Knollová, I., Chytry,´ M., Tichy,´ L., Hájek, O., 2005. Stratiﬁed resampling of phytosoci- Sokal, R.R., Michener, C.D., 1958. A statistical method for evaluating systematic rela-

ological databases: some strategies for obtaining more representative data sets tionships. Univ. Kans. Sci. Bull. 38, 1409–1438.

for classiﬁcation studies. J. Veg. Sci. 16, 479–486. Stojanov, N., Kitanov, B., 1926. Phytogeographical and ﬂoristic characteristics of the

Körner, C., 2007. The use of ‘altitude’ in ecological research. Trends Ecol. Evol. 22, Pirin Mountains. Annu. Univ. Soﬁa 18, 1–27.

569–574. Svenning, J.C., Skov, F., 2004. Limited ﬁlling of the potential range in European tree

Kreft, H., Jetz, W., 2010. A framework for delineating biogeographical regions based species. Ecol. Lett. 7, 565–573.

on species distributions. J. Biogeogr. 37, 2029–2053. Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G., Cosson, J.-F., 1998. Comparative phylo-

Kreft, H., Jetz, W., Mutke, J., Kier, G., Barthlott, W., 2008. Global diversity of island geography and postglacial colonization routes in Europe. Mol. Ecol. 7, 453–464.

ﬂoras from a macroecological perspective. Ecol. Lett. 11, 116–127. Theurillat, J.-P., 1996. Les pelouses à Carex curvula subsp. curvula (Caricion curvulae)

Küpfer, P., 1974. Recherches sur les liens de parenté entre la ﬂore orophile des Alpes dans les Alpes. Diss. Bot. 258, 267–294.

et celle des Pyrénées. Boissiera 23, 11–322. Theurillat, J.-P., Aeschimann, D., Küpfer, P., Spichiger, R., 1994. The higher vegetation

Lakusiˇ c,´ R., 1970. Die Vegetation der südöstlichen Dinariden. Vegetatio 21, units of the Alps. Colloq. Phytol. 23, 189–239.

321–373. Thiel-Egenter, C., et al. (20 authors), 2011. Break zones in the distributions of alleles

Lüth, C., Tasser, E., Niedrist, G., Dalla Via, J., Tappeiner, U., 2011. Plant communities and species in alpine plants. J. Biogeogr. 38, 772–782.

of mountain grasslands in a broad cross-section of the Eastern Alps. Flora 206, Tribsch, A., 2004. Areas of endemism of vascular plants in the Eastern Alps in relation

433–443. to Pleistocene glaciation. J. Biogeogr. 31, 747–760.

Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., 2005. Cluster Analysis Basics and Tribsch, A., Schönswetter, P., 2003. Patterns of endemism and comparative phylo-

Extensions, http://cranr-projectorg/web/packages/cluster/. geography conﬁrm palaeoenvironmental evidence for Pleistocene refugia in the

Mráz, P., Gaudeul, M., Rioux, D., Gielly, L., Choler, P., Taberlet, P., IntraBioDiv Con- Eastern Alps. Taxon 52, 477–497.

sortium, 2007. Genetic structure of Hypochaeris uniﬂora (Asteraceae) suggests Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M.,

vicariance in the Carpathians and rapid post-glacial colonization of the Alps from Webb, D.A. (Eds.), 1964–1980. Flora Europaea. Cambridge University Press, Cam-

an eastern Alpine refugium. J. Biogeogr. 34, 2100–2114. bridge.

Negre, R., 1969. Le Gentiano-Caricetum curvulae dans la région Louchonaise Virtanen, R., Dirnböck, T., Dullinger, S., Pauli, H., Staudinger, M., Grabherrm, G.,

(Pyrénées centrales). Vegetatio 18, 167–201. 2002. Multi-scale patterns in plant species richness of European high mountain

Niederfriniger-Schlag, R.N., Erschbamer, B., 2000. Germination and establishment vegetation. In: Körner, C., Spech, E.M. (Eds.), Mountain Biodiversity – A Global

of seedlings on a glacier foreland in the central Alps, Austria. Arct. Ant. Alp. Res. Assessment. Parthenon Publ., London/New York, pp. 91–101.

32, 270–277. Voges, A., 1995. International Quaternary map of Europe. Bundesanstalt für Geowis-

Ozenda, P., 1985. La Végétation de la Chaîne Alpine dans l’Espace Montagnard senschaften und Rohstoffe. Hannover, Germany.

Européen. Masson, Paris. von Crantz, H.J.N., 1769. Stirpium austriacarum. Impensis Ioannis Pauli Kraus, Bib-

Ozenda, P., 2009. On the genesis of the plant population in the Alps: new or critical liopalae Vienn.

aspects. C. R. Biol. 332, 1092–1103. Wołoszczak, E., 1895. Z granicy ﬂory zachodnio- i wschodnio-karpackiej. Spraw.

Pauli, H., Gottfried, M., Dirnböck, T., Düllinger, S., Grabherr, G., 2003. Assessing the Kom. Fizjogr. 31, 119–159.

long-term dynamics of endemic plants at summit habitats. In: Nagy, L., Grabherr, Zhang, L.B., Comes, H.P., Kadereit, J.W., 2001. Phylogeny and quaternary history of

G., Körner, C., Thompson, D.B.A. (Eds.), Alpine Biodiversity in Europe. Springer, the European montane/alpine endemic Soldanella (Primulaceae) based on ITS

Berlin, pp. 195–207. and AFLP variation. Am. J. Bot. 88, 2331–2345.