modern analogues from the southern urals provide insights into biodiversity change in the early...

ORIGINALARTICLE

Modern analogues from the SouthernUrals provide insights into biodiversitychange in the early Holocene forests ofCentral Europe

Milan Chytry1*, Jirı Danihelka1,2, Michal Horsak1, Martin Kocı1, Svatava

Kubesova1,3, Zdenka Lososova1,4, Zdenka Otypkova1, Lubomır Tichy1,

Vasiliy B. Martynenko5 and El’vira Z. Baisheva5

1Department of Botany and Zoology, Masaryk

University, Kotlarska 2, CZ-611 37 Brno,

Czech Republic, 2Institute of Botany, Academy

of Sciences of the Czech Republic, Porıcı 3a,

CZ-603 00 Brno, Czech Republic, 3Department

of Botany, Moravian Museum, Hviezdoslavova

29a, CZ-627 00 Brno, Czech Republic,4Department of Biology, Masaryk University,

Porıcı 7, CZ-603 00 Brno, Czech Republic,5Institute of Biology, Ufa Scientific Center,

Russian Academy of Sciences, prosp. Oktyabrya

69, RU-450054 Ufa, Bashkortostan, Russia

*Correspondence: Milan Chytry, Department of

Botany and Zoology, Masaryk University,

Kotlarska 2, CZ-611 37 Brno, Czech Republic.

E-mail: [email protected]

ABSTRACT

Aim The diversity changes that occurred in Central European forests during the

early Holocene can be better understood using ecological knowledge of modern

analogues of these forests, which occur in far Eastern Europe. Here we compare

the diversity of vascular plants, bryophytes and snails among different forest types

of the Southern Urals to provide insights into the palaeoecology of the vanished

Central European forests.

Location Southern Ural Mountains, Bashkortostan, Russia.

Methods We recorded all species of vascular plants, ground-dwelling bryophytes

and land snails, and measured biotic and abiotic variables, in 100-m2 plots located

in four forest types dominated by different trees: Pinus sylvestris–Larix sibirica,

Betula pendula–Populus tremula, Quercus robur and Acer platanoides–Tilia cordata–

Ulmus glabra. These types correspond to the chronosequence of forest

communities that occurred in Central Europe in the early Holocene.

Results The species richness of herb-layer plants was most affected by the

canopy-transmitted light. The former three forest types had open canopy and

were rich in species, whereas the Acer–Tilia–Ulmus forests were darker and poor

in species. The species richness of ground-dwelling bryophytes decreased from

coniferous to broad-leaved deciduous forests. In contrast, the highest species

richness of snails was in the Acer–Tilia–Ulmus forests owing to the higher calcium

content in the litter of these trees.

Main conclusions Based on the modern analogue of the Southern Ural forests,

we propose the hypothesis that the late-glacial open-canopy pine and larch forests

of Central European lowlands were rich in light-demanding species of vascular

plants, many of which were also typical of tall-grass steppes or mesic grasslands.

They also contained several species of ground-dwelling bryophytes. The spread of

birch, aspen and oak in the early Holocene reduced the local species richness of

ground-dwelling bryophytes but not of vascular plants. The subsequent spread

of elm, lime, maple and ash caused canopy closure, a retreat of the light-

demanding herbs and a decline in the local species richness of vascular plants.

Besides the increased shading by these tree species, their litter enriched soils in

calcium, and enhanced decomposition and nutrient cycling. This supported an

increase in the species richness of land snails.

Keywords

Bryophytes, broad-leaved trees, canopy shading, mixed oak forests, palaeo-

ecology, Russia, snails, species richness, vascular plants, vegetation change.

Journal of Biogeography (J. Biogeogr.) (2010) 37, 767–780

ª 2010 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 767doi:10.1111/j.1365-2699.2009.02256.x

INTRODUCTION

Palynological and macrofossil charcoal evidence suggests that

in the full- and late-glacial, lowland areas of eastern Central

Europe were covered by a forest-steppe with open woodlands

of coniferous (Larix decidua, Pinus sylvestris) and small-leaved

deciduous (Betula pendula, Populus tremula) trees (Willis &

van Andel, 2004; Birks & Willis, 2008; Kunes et al., 2008;

Svenning et al., 2008). Following the climatic amelioration of

the early Holocene, these woodlands expanded at the expense

of open steppe, and simultaneously, or with some time lag,

were gradually invaded by broad-leaved deciduous trees, such

as Quercus, Ulmus, Tilia, Acer and Fraxinus (Huntley & Birks,

1983; Lang, 1994; Berglund et al., 1996; Willis et al., 1997).

Tree assemblages that developed in Central Europe by the

mid-Holocene are traditionally termed ‘mixed oak forest’

(Eichenmischwald, Quercetum mixtum) in the palynological

literature (e.g. Firbas, 1949); however, the actual structure of

such forests is unclear, because the stable coexistence of

light-demanding oaks with the shading broad-leaved trees is

unlikely (Ellenberg, 1988; Vera, 2000; Svenning, 2002).

The transition from the late-glacial open woodlands to the

mid-Holocene mixed oak forests was a major environmental

change, which probably had a significant effect on biodiversity.

However, it is very difficult to reconstruct the change in diversity

of forest plant communities from fossil records. There are

reasonably good fossil pollen or macrofossil data on the diversity

of Central European trees during the Holocene, but data for

forest herbs are deficient, as a result of the impossibility of pollen

identification to the species level in some genera and families

(Beug, 2004), the absence of long-distance pollen dispersal in

some (mainly insect-pollinated) herb species, and the low level

of deposition and poor preservation of plant macrofossils at

mesic and dry forest sites. It is herbaceous plants rather than

trees, however, that constitute the main component of the

vascular plant diversity in Central European forests (Ellenberg,

1988). Environmental conditions in the forest herb layer can be

better indicated by taxa that provide a more complete fossil

record, such as snails (Lozek, 1964, 2000), but it is unclear how

historical changes in the diversity of snails related to plant

diversity and vegetation change.

Our understanding of palaeoecological processes in the early

Holocene forests of Central Europe may be improved by

studies of modern analogues of the mixed oak forests.

However, these forests retreated from Central Europe owing

to the mid- to late Holocene spread of beech (Fagus sylvatica)

and hornbeam (Carpinus betulus; Kuster, 1997; Magri, 2008).

Both of these trees develop dense canopies, which prevent the

establishment of oak seedlings (Ellenberg, 1988), and thus

outcompete oak and most other trees, unless the forest is

disturbed by logging or grazing (Vera, 2000). Therefore, the

modern analogues of the mixed oak forests must be sought

outside the geographical ranges of beech and hornbeam,

possibly in the east, where the current continental climate

resembles the early Holocene climate of Central Europe (Davis

et al., 2003).

Beech reaches its eastern distribution limit on the eastern

fringes of the Carpathians, and hornbeam in the area of the

middle Dniepr River in the Ukraine (Walter, 1974; Gribova

et al., 1980). For the purpose of this paper, we interpret the

eastern limits of Central Europe as being identical with the

eastern limits of these species. Forests between the Dniepr

River and the Southern Ural Mountains are formed of broad-

leaved tree species that are considered typical of the Central

European early to mid-Holocene mixed oak forests (Gribova

et al., 1980; Bohn & Neuhausl, 2000–2003): oak (Quercus

robur), maple (Acer platanoides), lime (Tilia cordata), elm

(Ulmus glabra, U. laevis) and ash (Fraxinus excelsior). Except

for ash, which has its eastern distribution limit on the Volga

River, all of these species reach the Southern Urals, and T.

cordata extends even to western Siberia (Gorchakovskii, 1968).

The foothills of the Southern Urals provide perhaps the best

modern analogue of the Central European early Holocene

forests, because here the broad-leaved deciduous forests of

European temperate distribution meet with the small-leaved

deciduous and light-coniferous forests of Siberian distribution.

The latter are called hemiboreal forests (Ermakov et al., 2000),

or subtaiga in the Russian literature (e.g. Sochava, 1979), and

are dominated by birch (Betula pendula), aspen (Populus

tremula), pine (Pinus sylvestris) and, in some places, also by

larch (Larix sibirica). As the hemiboreal forests can be

considered as analogues of the late-glacial and preboreal

forests of the Central European lowlands (Kunes et al., 2008),

the Southern Ural foothills provide an excellent opportunity to

study, side by side, the analogues of the two forest types of

which one replaced the other in Central European post-glacial

vegetation history.

The analogue between the modern forests of the Southern

Urals and the early Holocene forests of Central Europe is

supported not only by the nearly identical assemblages of

forest trees but also by the compositional similarity of snail

faunas (Horsak et al., 2010). Rich fossil data on the early

Holocene snail faunas of Central Europe (e.g. Lozek, 1993,

2000) show a combination of drought-adapted steppe species

[e.g. Chondrula tridens (Muller, 1774)], species of boreal

forests [e.g. Discus ruderatus (Ferussac, 1821)] and species of

scrub and ecotones [e.g. Fruticicola fruticum (Muller, 1774)].

Such a combination has no modern analogue in Central

Europe. In contrast, thermophilous forest species such as

Discus perspectivus (M. von Muhlfeld, 1816), Platyla polita

(Hartmann, 1840) and many clausiliid species were absent in

Central Europe in the early Holocene and appeared only in the

mid-Holocene. Modern snail assemblages found in the

Southern Ural forests are remarkably similar to the Central

European early Holocene fossil record in terms of species

composition, richness and broader realized niches of some

species (Horsak et al., 2010). We acknowledge that modern

analogues are never perfect, because palaeoenvironments that

are not analogous to any present situation were common

(Monserud et al., 1993; Williams & Jackson, 2007) and the

space-for-time-substitution method of ecological enquiry

involves some interpretation risks (Pickett, 1989). At the same

M. Chytry et al.

768 Journal of Biogeography 37, 767–780ª 2010 Blackwell Publishing Ltd

time, however, we believe that carefully interpreted analogues

can significantly contribute to the ecological understanding of

past environments.

In this paper we aim to provide new insights into the early

Holocene biodiversity change in Central European forests

through a comparative study of their modern analogues –

different forest types occurring on the Southern Ural foothills.

We focus on the diversity of vascular plants and bryophytes,

both of which are very important for forest ecosystem

functioning, but each of them utilizes a different niche. In

addition, we focus on snails, which are well preserved in the

fossil record, and, therefore, frequently used as indicators of

past environmental conditions (Lozek, 1964; Rousseau, 1990).

STUDY AREA

This study was conducted on the western and eastern foothills

of the Southern Ural Mountains in the southern part of the

Bashkortostan Republic, Russian Federation (Fig. 1). The ridge

of the Southern Urals runs in an approximately NNE–SSW

direction and rarely reaches elevations over 700 m in this area;

our study sites were located at elevations of 168–932 m. The

landscape is predominantly gently undulating, but solitary

mountains and deep stream valleys occur in some places. The

central ridge of the Southern Urals is formed of Devonian and

Carboniferous base-poor sandstones and shales on the western

side and of Lower Palaeozoic slates on the eastern side. The

ridge is fringed by Devonian, Carboniferous and Permian

sandstones, limestones, conglomerates and other sedimentary

rocks (Yaparov, 2005). This geological setting includes a broad

spectrum of acidic and basic, and soft and hard rocks, which

provides a similar range of habitats for plant growth as

encountered in Central Europe. However, low-pH soils are

rare, even on base-poor rock, owing to limited cation leaching

in this continental area.

Mean July and January temperatures at the study sites range

from 17 to 20 �C and from )16 to )14.5 �C, respectively

(Yaparov, 2005). Annual precipitation is below 600 mm on the

summits and decreases to 450–500 mm on the western fringes

and to 400–450 mm on the eastern fringes of the mountain

range. Most precipitation falls in summer (Yaparov, 2005).

The landscape is a mosaic of natural forests, primary and

secondary steppes, and arable land, with forests being more

widely distributed at higher elevations. Basic descriptions of

forest vegetation diversity in the Southern Urals are found in

general overviews (Gribova et al., 1980; Popov, 1980) and

phytosociological studies (Schubert et al., 1979; Martynenko

et al., 2005; Mirkin, 2008). Broad-leaved forests of Acer

platanoides, Tilia cordata and Ulmus glabra prevail as zonal

forest vegetation on mesic soils on the western (European) side

of the Southern Ural range, whereas oak (Quercus robur)

forests are found as zonal vegetation in drier areas at the south-

eastern fringes of the range. Oak can also occur at drier or

formerly disturbed sites within the zone of the Acer–Tilia–

Ulmus forests. Hemiboreal coniferous forests of Pinus sylvestris

and Larix sibirica predominate in the summit area and on the

eastern (Siberian) side of the mountain range. Birch (Betula

pendula) and aspen (Populus tremula) forests often occur at

previously disturbed sites, but they can also form natural

forests in some places, especially on the eastern side of the

range. Floodplains are occupied by forests with Alnus incana,

A. glutinosa, Betula pendula, Quercus robur, Salix alba and

Ulmus laevis. In the hilly landscapes and lowlands, adjacent to

the Southern Urals from the west, south and east, the forested

landscape gradually changes to forest-steppe and steppe.

Human impact on forests is far less intense than in Central

Europe. There are almost no plantations of trees that are not

native to this area, and the species composition of forests is

near natural (Popov, 1980). Some forests are occasionally

grazed by domestic livestock. Forest fires may occur, some-

times caused by lighting ignition, especially in drier forest-

Figure 1 Location of the study area. Black dots indicate the

sampling sites.

Ural forests and early Holocene biodiversity change in Central Europe

Journal of Biogeography 37, 767–780 769ª 2010 Blackwell Publishing Ltd

steppe areas. After logging or burning, forests either regenerate

spontaneously or are being replanted with the same tree species

as occurred at the site before. Spontaneous regeneration often

leads to an increased dominance of birch or aspen, which are

replaced by competitively superior broad-leaved or coniferous

trees after a few decades (Khairetdinov, 2004). At some dry

sites, post-fire succession is dominated by oak, which is better

adapted to drought stress than maple, lime or elm.

MATERIALS AND METHODS

In July 2007 we sampled natural forests at 78 sites, using square

plots of 100 m2 placed in homogeneous vegetation, avoiding

plantations and disturbed or ecotonal situations. Floodplain

forests were not considered in this study.

In each plot we recorded all species of vascular plants

(taxonomy and nomenclature according to Cherepanov, 1995)

and ground-dwelling bryophytes and lichens, and estimated

their individual covers and total percentage covers of particular

vegetation layers. As ground-dwelling lichens were very rare in

these forests, they were not included in the analyses. In 52 of 78

sampled plots, we harvested the above-ground herb-layer

biomass within four square subplots of 0.25 m2 by clipping the

vegetation 1 cm above the soil surface. Biomass from these

four subplots was merged, and then separated into herbaceous

plants, wood (of seedlings, saplings and low shrubs) and leaves

of woody plants; they were then dried, weighed and analysed

for contents of total nitrogen (N), phosphorus (P), potassium

(K) and calcium (Ca). N was measured by the Kjehldahl

method, P spectrophotometrically, K by atomic emission

spectrophotometry and Ca by atomic absorption spectropho-

tometry (Zbıral, 1995).

In 37 of these plots, we recorded species of land snails. These

plots were selected to represent a geographical and habitat

range similar to that of the full sample set of 78 plots. For 2 h,

one person searched for snails by eye in all the appropriate

microhabitats. In addition, approximately 3 L of litter, moss

polsters and topsoil were sampled for recording small ground-

dwelling species and were processed immediately in the field,

using the wet sieving method (Horsak, 2003).

In all plots, we recorded the following environmental

variables. (1) Altitude was measured with a Global Positioning

System (GPS) receiver Garmin 60CSx (Garmin International

Inc., Olathe, KS). (2) Slope inclination was measured with a

Clino Master clinometer (Silva Sweden AB, Sollentuna,

Sweden). (3–4) Soil depth and litter depth were measured

using a metal rod in four places within each plot and averaged;

depths greater than 30 cm were given the value of 30 cm. (5)

Litter cover was estimated in percentage by eye. (6–7) Soil pH

and electrical conductivity: soil samples were taken in four

places within each plot, at 1–2 cm and 5–15 cm depth,

respectively, in order to assess separately the topmost soil layer,

which is more influenced by litter decomposition and directly

affects snails, and lower soil layer, which contains maximum

root biomass of herbaceous plants. A 2:5 soil-distilled water

solution was prepared from mixed samples from each depth

and measured after 24 h by a Greisinger GPRT 1400 AN pH-

meter (Greisinger Electronic GmbH, Regenstauf, Germany)

and a CM113 conductivity meter (Snail Instruments, Beroun,

Czech Republic). (8–9) Topographical indices of radiation and

heat were calculated from latitude, slope inclination and

aspect, according to McCune & Keon (2002, eq. 3). These two

indices differ in that the radiation index attains maximal values

on south-facing slopes and the heat index on south-west-facing

slopes. (10–13) Four measures of potential radiation were

derived from hemispherical photographs, taken in the vertical

direction at a height of 1.5 m above ground at three sites

within each plot. A Nikon CoolPix 4500 digital camera with a

fish-eye lens was used. Potential direct and total solar radiation

were calculated using the Gap Light Analyzer software (Frazer

et al., 1999) and averaged over the three photographs from

each plot. Latitude, slope inclination, aspect and shading by

the surrounding topography were considered in the calcula-

tions. We quantified potential radiation for 21 June above the

canopy (Above direct and Above total radiation) and below the

canopy (Transmitted direct and Transmitted total radiation),

(14–17). Mean temperature of July and January, and precipi-

tation sum for the periods April–October and November–March

were obtained from the climatic maps of Bashkortostan

(Yaparov, 2005).

Besides these abiotic variables, we used canopy covers of

individual tree species because of their potential effect on the

diversity of target taxa. As an additional environmental

variable, we used summed covers of Acer, Tilia and Ulmus,

because the leaves of these trees are rich in calcium citrate and

contribute significantly to calcium availability in the topsoil

(Wareborn, 1969, 1970) and, consequently, to litter decom-

position (Hobbie et al., 2006). The structure of variation in

environmental variables, both abiotic (1–17) and canopy

covers of individual trees, was simplified using principal

components analysis (PCA) of a correlation matrix from the

statistica 8 package (http://www.statsoft.com). The input

data for PCA was a matrix of 78 plots · 28 environmental

variables. Subsequently, the environmental variable that was

most strongly correlated with the first PCA axis was selected as

a representative of this axis, and characteristics of the target

taxa were related to it by correlation analysis.

For comparative purposes, plots were classified into four

types based on dominant tree species. These types roughly

corresponded to the temporal sequence in which tree species

replaced each other in Central Europe between the late-glacial

and mid-Holocene, as follows: (1) Pinus–Larix (n = 18):

hemiboreal open-canopy coniferous forests dominated by

pine (P. sylvestris) and/or, less frequently, by larch (L. sibirica).

(2) Betula–Populus (n = 20): open-canopy small-leaved decid-

uous forests dominated by birch (B. pendula) and/or, less

frequently, by aspen (P. tremula). (3) Quercus (n = 13): broad-

leaved deciduous forests dominated by oak (Q. robur). (4)

Acer–Tilia–Ulmus (n = 27): closed-canopy broad-leaved

deciduous forests dominated by maple (A. platanoides), lime

(T. cordata) and/or elm (U. glabra). Plots were assigned to

groups 1, 2 or 3 only if maple, lime or elm had a cover <5%.

M. Chytry et al.


Plant species composition of the four forest types was

summarized in a table, in which positive and negative

diagnostic species of the Acer–Tilia–Ulmus forests were

determined according to Tichy & Chytry (2006), using the

phi coefficient of association between species and site groups,

where the size of site groups was equalized and the statistical

significance of the association checked by Fisher’s exact test.

Table editing and calculation of diagnostic species were

performed with the juice program (Tichy, 2002). Selected

characteristics of the four forest types were compared with

ANOVA and Tukey post-hoc tests, using statistica 8. The

species richness of each forest type was expressed as the mean

and variation of the number of species in 100-m2 plots (a

measure of local species richness or alpha diversity) and as

sample-based rarefaction curves (a measure of total species

richness or species pool; Gotelli & Colwell, 2001). These curves

were computed as means of 10,000 sample-based species

accumulation curves that resulted from random ordering of all

plots belonging to each forest type. This calculation was

performed using the juice program. Rarefaction curves show

how the total number of species recorded in each forest type

increases with increasing number of sampled plots.

RESULTS

The PCA revealed a strong environmental gradient associated

with the first axis (Table 1), running from warmer areas, where

Acer, Tilia and Ulmus attained higher cover in the forest

canopy, which was consequently denser, to the cooler areas,

where these broad-leaved trees were absent or less prominent

and the canopy was therefore more open. Soil pH and

electrical conductivity were also associated with this gradient,

Table 1 Coordinates of environmental variables on the first two axes of principal components analysis (PCA) calculated from a matrix

of 78 sample plots · 28 environmental variables from the Southern Urals, and descriptive statistics of individual variables. As the PCA was

based on the correlation matrix, the coordinates are identical with the correlations between PCA axes and environmental variables.

Coordinates ‡|0.5| are set in bold. For soil pH and electrical conductivity, mean values from 1–2 and 5–15 cm depth were used. Means and

standard deviations (SD) of tree species covers were calculated only from plots where the particular species were present. See text for

explanation of variables.

Principal components Descriptive statistics

1 2

Mean SD Minimum Maximum

Eigenvalue 6.919 4.302

Percentage variance explained 24.7 15.4

Altitude (m a.s.l.) )0.640 )0.040 431 149 168 932

Slope (�) 0.412 )0.432 14 11 0 40

Soil depth (cm) )0.026 0.291 28 6 4 30*

Litter depth (cm) 0.033 )0.027 3 1 1 8

Litter cover (%) 0.119 0.402 84 17 0 98

Soil pH 0.672 0.299 6.3 0.5 5.1 7.6

Soil electrical conductivity (lS cm)1) 0.565 0.276 131 73 43 378

Radiation (topographical index) )0.470 0.829 0.73 0.16 0 0.9

Heat (topographical index) )0.504 0.744 0.73 0.17 )0.2 0.9

Above direct radiation (mol m)2 d)1) )0.446 0.831 19.1 2.6 8.5 22.2

Above total radiation (mol m)2 d)1) )0.487 0.825 38.1 3.8 18.6 41.5

Transmitted direct radiation (mol m)2 d)1) )0.729 0.111 5.9 2.3 1.2 12.1

Transmitted total radiation (mol m)2 d)1) )0.789 )0.028 11.6 3.8 2.6 23.6

Mean July temperature (�C) 0.692 0.370 18.3 0.5 17.2 19.7

Mean January temperature (�C) 0.588 0.207 )15.1 0.4 )15.7 )14.7

Precipitation April–October (mm) )0.009 )0.408 348 30 275 375

Precipitation November–March (mm) 0.202 )0.212 166 40 70 200

Cover of tree layer (%) 0.690 0.358 55 20 15 90

Cover of shrub layer (%) 0.429 0.279 9 12 0 60

Cover of Pinus sylvestris (%) )0.218 )0.203 21 16 0 63

Cover of Larix sibirica (%) )0.371 )0.235 15 13 0 39

Cover of Betula pendula (%) )0.368 )0.163 19 16 0 63

Cover of Populus tremula (%) 0.057 0.153 14 18 0 63

Cover of Quercus robur (%) 0.001 0.393 18 23 0 63

Cover of Acer + Tilia + Ulmus (%) 0.826 0.225 34 29 0 88

Cover of Acer platanoides (%) 0.694 0.269 22 25 0 88

Cover of Tilia cordata (%) 0.502 )0.066 20 19 0 64

Cover of Ulmus glabra + laevis (%) 0.472 0.223 16 16 0 63

*Soils deeper than 30 cm were arbitrarily given a value of 30 cm.



being higher in the Acer–Tilia–Ulmus forests. The second PCA

axis reflected insolation above the canopy, dependent on

differences in slope aspect, and was therefore less important for

the explanation of diversity in the forest sub-canopy layers.

Of the individual environmental variables, the summed

cover of Acer, Tilia and Ulmus was the most strongly correlated

with the first PCA axis. We therefore used it as a representative

of this axis, and correlated sub-canopy biotic variables with it

(Table 2). With the increasing cover of Acer, Tilia and Ulmus,

the biomass and cover of the herb layer decreased, but

nutrients (N, P, K and Ca) measured in herbaceous biomass

and calcium measured in leaves of the herb-layer woody plants

increased. The species richness of vascular plants in all layers

(except juvenile woody plants) decreased, and so did that of

ground-dwelling bryophytes. However, the species richness of

snails increased.

When forest types were divided into four groups and

compared, there was no difference in the transmitted total

radiation between the Pinus–Larix, Betula–Populus and Quer-

cus forests, but the Acer–Tilia–Ulmus forests had significantly

less light below the canopy (Fig. 2a). Soil pH and electrical

conductivity were lowest in the Pinus–Larix forests, interme-

diate in the Betula–Populus and Quercus forests, and highest in

the Acer–Tilia–Ulmus forests. There was no difference in pH

between depths of 1–2 and 5–15 cm, but conductivity was

higher closer to the soil surface in all forests types except for

the Pinus–Larix forests (Fig. 2b, c).

Herbaceous biomass was lowest in the Acer–Tilia–Ulmus

forests, highest in the Betula–Populus and Quercus forests, and

intermediate in the Pinus–Larix forests (Fig. 3a). It contained

least nutrients in the Pinus–Larix and Betula–Populus forests

and most nutrients in the Acer–Tilia–Ulmus forests (Fig. 4).

Local species richness of herb-layer vascular plants was high

and not significantly different among the Pinus–Larix, Betula–

Populus and Quercus forests, but it was lower in the Acer–Tilia–

Ulmus forests (Fig. 3b). There was also a remarkable difference

in the species composition of vascular plants between the

former three forests types and the Acer–Tilia–Ulmus forests

(Table 3). Species richness of ground-dwelling bryophytes was

highest in the Pinus–Larix forests and lowest in the Acer–Tilia–

Ulmus forests (Fig. 3c). Snail species richness was highest in

the Acer–Tilia–Ulmus forests and lowest in the Pinus–Larix

and Quercus forests (Fig. 3d). The total species richness of

larger areas estimated from the sample-based rarefaction

curves (Fig. 5) followed the same pattern as the local richness,

with fewer vascular plant species in the Acer–Tilia–Ulmus

forests (Fig. 5a), fewer bryophyte species in the Quercus and

Acer–Tilia–Ulmus forests (Fig. 5b), and fewer snail species in

the Pinus–Larix and Quercus forests. Less steep rarefaction

curves also indicate lower beta diversity (spatial turnover in

species composition) of the herb-layer plant species in the

Acer–Tilia–Ulmus forests and of bryophytes in the Quercus and

Acer–Tilia–Ulmus forests.

DISCUSSION

The analogue between the modern forests of the Southern

Urals and the early Holocene forests of Central Europe,

Table 2 Pearson correlations (r) of biotic variables measured in the Southern Ural forests with summed cover of Acer, Tilia and Ulmus, and

descriptive statistics of these variables. n = number of sampling plots where particular variables were measured. Significant correlations

(P < 0.05) are in bold.

n r Mean SD Minimum Maximum

Cover of herb layer (%) 78 )0.49 52 24 3 90

Cover of moss layer (%) 78 )0.14 2 8 0 70

Dry mass of herbs without graminoids (g m)2) 52 )0.64 82.8 47.8 0.2 208.8

Dry mass of graminoids (g m)2) 52 )0.16 1.4 2.7 0 56.2

Dry mass of all herbs (g m)2) 52 )0.66 83.2 48.7 0.2 208.8

Dry mass of woody plant leaves (g m)2) 52 )0.05 5.5 6.4 0 42.4

Dry mass of wood in herb layer (g m)2) 52 )0.21 12.5 16.6 0 138.0

Total dry mass of herb layer (g m)2) 52 )0.67 101.2 55.4 0.4 243.2

No. of species in herb layer 78 )0.75 37 17 5 79

No. of juvenile woody plants 78 0.39 2 1 0 6

No. of vascular plant species 78 )0.76 43 18 9 84

No. of bryophyte species 78 )0.28 2 3 0 16

No. of snail species 37 0.42 7 4 0 14

No. of snail individuals 37 0.21 32 21 0 84

Nitrogen in herbaceous plants (%) 52 0.74 1.96 0.53 1.09 3.14

Phosphorus in herbaceous plants (%) 52 0.39 0.25 0.10 0.11 0.49

Potassium in herbaceous plants (%) 52 0.48 3.23 1.27 1.60 7.23

Calcium in herbaceous plants (%) 52 0.54 1.33 0.61 0.49 3.00

Nitrogen in woody plant leaves (%) 30 0.12 2.58 0.42 1.87 3.45

Phosphorus in woody plant leaves (%) 30 0.15 0.28 0.11 0.12 0.53

Potassium in woody plant leaves (%) 30 0.05 1.66 0.67 0.48 3.33

Calcium in woody plant leaves (%) 30 0.49 1.80 0.44 1.02 2.78

M. Chytry et al.


proposed in this paper, is illustrated using a comparison of

four forest types with different dominant trees. These four

types, Pinus–Larix, Betula–Populus, Quercus and Acer–Tilia–

Ulmus, were studied at different sites at a single time, but we

interpret them hypothetically as a temporal sequence of post-

glacial colonization of Central Europe (Huntley & Birks, 1983;

Berglund et al., 1996). The analogue hypothesis is supported

by the fact that, in the Southern Urals, typical tree species of

late-glacial Central Europe (Larix, Pinus and Betula; Willis &

van Andel, 2004; Jankovska & Pokorny, 2008) occur in the

coolest areas whereas species that are typical of mid-Holocene

Central Europe (Acer, Tilia and Ulmus) occur in the warmest

areas (Table 1; see also Gorchakovskii, 1968). It must be noted

that Betula, Populus and Quercus forests often develop in

formerly disturbed places on the Southern Ural foothills, but

both the initial and the terminal types of this hypothetical

chronosequence analogue, the Pinus–Larix and Acer–Tilia–

Ulmus forests, are represented there by zonal natural forests.

In this sequence of forest types, ecosystem nutrient status

gradually improves: soil pH increases, as well as electrical

conductivity, which indicates soil enrichment in cations

(Fig. 2b, c). There is a parallel increase in soil nutrient uptake,

as suggested by increasing concentrations of nitrogen, phos-

phorus, potassium and calcium in the herbaceous biomass

(Fig. 4). The enhanced nutrient cycling in deciduous forests

probably results from the faster decomposition of the decid-

uous leaf litter than of conifer needles (Ellenberg, 1988; Hobbie

et al., 2006; Cornwell et al., 2008). The higher conductivity

found in the uppermost soil layer of 1–2 cm (as opposed to

that found in the slightly deeper layers; Fig. 2c) in deciduous

forests suggests that the higher cation concentration in the soil

is a result of litter decomposition rather than of bedrock

weathering. The highest soil pH, conductivity and biomass

nutrient contents were encountered in the Southern Ural

Acer–Tilia–Ulmus forests, although they often occurred on the

same bedrock as the other forest types. These trees are effective

in calcium uptake from the bedrock and contain high

concentrations of this element in their leaves and litter.

Moreover, they contain calcium in the soluble citrate form

rather than in the insoluble oxalate form (Wareborn, 1969,

1970), which supports activity of soil biota, including earth-

worms. As a result, the decomposition of leaf litter and its

translocation below-ground is faster for maple, lime and elm

than for oak, birch, aspen and conifers (Hobbie et al., 2006),

and forests dominated by maple, lime and elm are character-

ized by fast cycling of calcium and other nutrients. It was

probably the spread of these trees that enhanced nutrient

cycling in the early Holocene forests of Central Europe, as

supported by combined palynological and geochemical evi-

dence from a sedimentary sequence in eastern Hungary, where

the spread of these trees at about 9500 yr bp was followed by a

striking increase in calcium concentration (Willis et al., 1997).

In Central European forests, higher soil pH tends to be

positively related to higher species richness of vascular plants

(Chytry et al., 2003; Schuster & Diekmann, 2003), which is

explained by a historical and evolutionary effect of a larger

(a)

(b)

(c)

Figure 2 A comparison of (a) canopy-transmitted total radia-

tion, (b) soil pH and (c) soil electrical conductivity among four

forests types of the Southern Urals. Boxes and whiskers include

50% and 90% values, respectively, and white markers represent the

medians. Identical letters indicate homogeneous groups (Tukey

post-hoc test, P < 0.05). In (b) and (c), differences were tested

separately among the values measured at a depth of 1–2 cm

(homogeneous groups are indicated by letters on the first line at

the top of each graph), at a depth of 5–15 cm (homogenous

groups indicated on the second line at the top of each graph), and

between the two depths within each forest type (differences

indicated on the bottom of each graph: *, significant difference

at P < 0.01; n.s., no significant difference). Because of multiple

testing, significances are Bonferroni-corrected.



pool of calcicolous species (Partel, 2002; Ewald, 2003). This

relationship was also reported from forests of southern Siberia

(Chytry et al., 2007), but it does not occur on the Southern

Ural foothills, where the Acer–Tilia–Ulmus forests have the

highest pH, but fewest species of vascular plants (compare

Figs 2b and 3b). In this continental forest-steppe area, soil

leaching is limited by low precipitation. Consequently, very

acidic soils are rare or absent, even on base-poor bedrocks. The

most acidic plot that we encountered on a base-poor shale had

a pH of 5.1. In temperate and boreal Europe and southern

Siberia, species richness usually decreases only if soil pH is

below 5, owing to the increase of toxic aluminium in the soil

solution (Tyler, 1996; Schuster & Diekmann, 2003; Chytry

et al., 2007). On soils with pH > 5, species richness is usually

controlled by factors other than pH.

Our data suggest that it is because of the higher degree of

canopy shading that the Acer–Tilia–Ulmus forests of the

Southern Ural foothills usually have only about 12–20 vascular

plant species per 100 m2 in their herb layer whereas the other

forest types usually harbour 40–50 species in the same area

(compare Figs 2a and 3b). Acer, Tilia and Ulmus develop

denser canopies than Quercus, Betula, Populus, Pinus and Larix

(Ellenberg, 1988), which results in reduced light availability in

the herb layer. The herb layer of the Acer–Tilia–Ulmus forests

also produces the smallest biomass of the four forest types

(Fig. 3a), at least in the forest-steppe landscape analysed in this

study. Its lower productivity contrasts with the higher nutrient

content in the biomass and is obviously unrelated to water

availability, because all four types were sampled on mesic to

slightly dry soils of similar moisture status. Only some sites

with oak and pine were perhaps slightly drier. Thus, the most

probable reason for both lower productivity and lower species

richness of the herb layer in the Acer–Tilia–Ulmus forests is

canopy shading.

When applying this observation to the historical analogue

outlined above, we hypothesize that the open coniferous

forests of the Central European late-glacial forest-steppe were

rich in vascular plant species. Many of them were light-

demanding herbs that also occurred in tall-grass steppes (e.g.

Brachypodium pinnatum, Filipendula vulgaris, Origanum vul-

gare and Veronica teucrium) or in mesic, wet or intermittently

dry meadows (e.g. Bistorta major, Galium boreale, Sanguisorba

officinalis and Stachys officinalis; Table 3). Rich pools of

herbaceous species in these open coniferous forests evolved

and assembled over long time periods of the Pleistocene and

probably remained well preserved after the invasion of these

(a)

(c)

(b)

(d)

Figure 3 A comparison of (a) herbaceous biomass, and species richness of (b) herb layer, (c) ground-dwelling bryophytes and (d) snails

among four forest types of the Southern Urals. Boxes and whiskers include 50% and 90% values, respectively, and white markers represent

the medians. Identical letters indicate homogeneous groups (Tukey post-hoc test, P < 0.05).

M. Chytry et al.


forests by small-leaved deciduous trees, such as birch and

aspen, and even after the oak invasion in the early Holocene.

However, subsequent invasions by elm, maple, lime and

probably ash reduced light availability below the canopy and

resulted in a dramatic decline of the light-demanding herba-

ceous species, and consequently also in a decline of the total

vascular plant diversity.

From the mid-Holocene onwards, Neolithic agriculture

spread in the Central European lowlands and human impact

on forests increased (Ellenberg, 1988). As a result of forest

grazing, coppicing and support of oak as a valuable timber

species, the forest canopy was artificially open in some places

(Vera, 2000; Svenning, 2002). In such places a rich herb layer

with light-demanding species may have survived, even after the

invasion of Central Europe by strongly shading tree species,

namely beech and hornbeam. The early to mid-Holocene

‘mixed oak forest’ was probably partly dependent on distur-

bances, including fires, grazing and logging, which promoted

the coexistence of the light-demanding, competitively weak

oak with other broad-leaved species in the same stands. In

many areas, however, the ‘mixed oak forest’ may have been a

mosaic landscape of pure oak forests at drier sites and

Acer–Tilia–Ulmus–Fraxinus forests at mesic sites. Both these

situations occur in the modern landscape of the Southern

Urals: (1) some forests with a participation of oak are exposed

to grazing and logging; and (2) in the maple-, lime- and elm-

dominated landscapes, pure oak forests tend to occur at dry

sites with a shorter recurrence interval of wild fires.

We are not aware of any studies of deciduous forest

dynamics from the Southern Urals, but there are modern

Central European analogues of the spread of dense-canopy

trees into open oak forests. Some oak forests in Poland

and adjacent countries (e.g. Potentillo albae-Quercetum) were

traditionally maintained by livestock grazing and coppicing.

They had a rich herb layer with light-demanding species, many

of them with continental distribution ranges. When this

management ceased, approximately by the mid-20th century,

many of these forest sites were invaded by Carpinus betulus,

which formed a dense canopy, preventing oak regeneration

and causing a decline in the species richness of the herb-layer

(Kwiatkowska & Wyszomirski, 1988; Jakubowska-Gabara,

1996) and the retreat of some light-demanding invertebrates

(Benes et al., 2006).

Our data from the Southern Urals indicate that the loss of

light-demanding species owing to canopy shading is partly

compensated by the increase of shade-tolerant forest herbs,

such as Alliaria petiolata, Asarum europaeum and Galium

odoratum (Table 3). However, the pool of these species is

much smaller than that of light-demanding herbs. Thus, the

total species richness is low, both locally (Fig. 3b) and in the

(a)

(c)

(b)

(d)

Figure 4 A comparison of concentrations of (a) nitrogen, (b) phosphorus, (c) potassium and (d) calcium in herbaceous biomass among

four forest types of the Southern Urals. Statistical details are as in Fig. 3.



whole area of the Acer–Tilia–Ulmus forests (Fig. 5a). It should

be noted, however, that the pool of shade-tolerant forest

species in the Southern Urals is smaller than that in Central

Europe (e.g. Sadlo et al., 2007), probably as a result of the

more continental climate and the longer distance of the

Southern Urals from the assumed Southern European Pleis-

Table 3 Vascular plant species composition of the four forest

types studied in the Southern Urals. PiLa, Pinus–Larix; BePo,

Betula–Populus; Quer, Quercus; ATU, Acer–Tilia–Ulmus. Numbers

are percentage frequencies of species occurrence; dots indicate

absence. For trees, occurrences in both canopy and understorey

are counted. Shaded trees are those used to define vegetation types.

Shaded herbs and shrubs (negative and positive diagnostic species

of the Acer–Tilia–Ulmus forests) are those with the phi coefficient

of association value >0.3, calculated for equalized group size, and

with significant concentration of occurrence either within or

outside the Acer–Tilia–Ulmus forests. Non-shaded species have no

diagnostic value but occur with frequency >25% in the data set.

Forest type PiLa BePo Quer ATU

No. of plots 18 20 13 27

Trees

Pinus sylvestris 83 20 8 .

Larix sibirica 61 10 8 4

Betula pendula 50 85 31 19

Populus tremula 17 40 38 37

Betula pubescens . 5 . .

Quercus robur 61 40 100 52

Acer platanoides 39 35 69 100

Tilia cordata 28 15 46 67

Ulmus glabra 6 15 15 67

Padus avium 39 50 38 30

Herbs and shrubs

Negative diagnostic species of the Acer–Tilia–Ulmus forests

Geranium pseudosibiricum 72 65 62 .

Galium boreale 89 90 85 19

Seseli libanotis 78 55 62 4

Origanum vulgare 61 50 62 .

Lathyrus pisiformis 89 75 62 15

Stachys officinalis 50 50 69 .

Rosa majalis 89 80 62 22

Thalictrum minus 39 55 69 4

Pyrethrum corymbosum 78 55 92 19

Poa pratensis + angustifolia 33 35 77 .

Brachypodium pinnatum 83 75 92 30

Chamaecytisus ruthenicus 78 30 46 4

Trifolium medium 22 45 69 .

Filipendula vulgaris 28 40 62 .

Silene nutans 61 30 31 .

Campanula persicifolia 78 40 62 11

Calamagrostis arundinacea 89 90 62 33

Vicia tenuifolia 56 50 69 11

Fragaria vesca 83 55 . 7

Euphorbia subcordata 67 20 23 .

Bistorta major 39 35 38 .

Sanguisorba officinalis 33 40 38 .

Viola canina 28 35 46 .

Achillea millefolium 33 40 31 .

Veronica chamaedrys 67 40 54 11

Galium verum 39 15 54 .

Rubus saxatilis 89 95 69 44

Veronica teucrium 22 40 62 4

Calamagrostis epigeios 22 20 62 .

Hieracium umbellatum 50 25 38 4

Serratula coronata 17 55 38 4

Elytrigia repens 33 15 46 .

Table 3 Continued

Forest type PiLa BePo Quer ATU

No. of plots 18 20 13 27

Solidago virgaurea 56 50 54 15

Artemisia armeniaca 22 20 46 .

Inula salicina 22 20 46 .

Campanula bononiensis 17 30 38 .

Viola hirta 22 30 62 4

Lupinaster pentaphyllus 33 35 . .

Inula hirta 28 20 31 .

Carex supina 22 15 46 .

Dactylis glomerata 39 60 69 19

Aconitum nemorosum 22 25 23 .

Erysimum hieracifolium 39 15 15 .

Fragaria viridis 11 25 69 4

Primula macrocalyx 61 55 69 26

Festuca rupicola 17 20 31 .

Veronica spuria 22 15 31 .

Aconogonon alpinum 6 20 46 .

Phlomoides tuberosa 22 55 85 19

Pulmonaria mollis 44 60 46 19

Galium tinctorium 33 25 23 4

Positive diagnostic species of the Acer–Tilia–Ulmus forests

Galium odoratum . 10 23 85

Alliaria petiolata . . . 30

Asarum europaeum 11 15 15 52

Omphalodes scorpioides . . . 22

Euonymus verrucosa 6 . 8 30

Campanula trachelium 11 10 23 44

Lamium album . 5 8 26

Non-diagnostic species recorded in >25% of plots

Stellaria holostea 78 65 69 85

Lathyrus vernus 78 70 54 81

Poa nemoralis 78 60 54 44

Melica nutans 83 60 31 52

Viola mirabilis 39 60 46 74

Aegopodium podagraria 33 60 46 74

Geum urbanum 44 30 62 41

Viola collina 56 50 23 26

Vicia sepium 44 50 23 30

Heracleum sibiricum 28 70 38 19

Urtica dioica 11 35 23 52

Fallopia convolvulus + dumetorum 39 20 46 30

Polygonatum odoratum 61 45 8 15

Bromopsis inermis 17 50 46 22

Milium effusum 22 30 8 48

Bupleurum longifolium 22 35 15 30

Geranium sylvaticum 6 55 23 22

Galium aparine 17 10 46 37

Aconitum septentrionale 11 40 15 30

M. Chytry et al.


tocene refugia of broad-leaved forests (Birks & Willis, 2008;

Svenning et al., 2008; Willner et al., 2009). There is a striking

pattern of gradual depletion of the shade-tolerant forest flora

when moving from Central Europe to the east (Gorchakovskii,

1968; Walter, 1974; Gribova et al., 1980). Although small

refugia of broad-leaved forests may have existed in the

Southern Urals, as indicated by disjunct occurrences of some

European species and a few endemics related to the broad-

leaved forests in this area, the modern flora of the Southern

Ural broad-leaved forests is poorer than in Central Europe. In

particular, local species richness of the Southern Ural

Acer–Tilia–Ulmus forests is lower than that of comparable

types of Central European forests (Schubert et al., 1979). From

this perspective, the decline of local species richness in the

Central European forests after the early Holocene expansion of

broad-leaved trees may have been less striking than the

Southern Ural analogue would suggest. Nevertheless, broad-

leaved forests of Central Europe rarely contain as many herb-

layer species as the Southern Ural Pinus–Larix, Betula–Populus

or Quercus forests. The only exception is some species-rich

Central European oak forests that have maintained open

canopy as a result of past management by grazing and

coppicing. This suggests that the early Holocene diversity

decline in Central European forests may have been real,

although maybe less pronounced than the difference in

modern diversity between the Acer–Tilia–Ulmus and the other

forests in the Southern Urals.

Ground-dwelling bryophytes probably also experienced a

diversity decline during the transition from the late-glacial to

the mid-Holocene. They are represented by a few species in the

coniferous hemiboreal forests but are very rare in the broad-

leaved forests of the Southern Urals (Fig. 3c). Baisheva et al.

(2009) described the same pattern from another area in

Bashkortostan. An obvious reason is that the litter of broad-

leaved trees covers bryophytes with a thick layer in the

autumn, thus preventing photosynthesis (Ellenberg, 1988).

However, the diversity of epiphytic and epixylic bryophytes is

probably unaffected by the change in the tree-layer composi-

tion, because the species richness of these synusiae is similar

among different types of Southern Ural forests (Baisheva et al.,

2009).

Although the Southern Ural analogue suggests an early

Holocene diversity decline in vascular plants and bryophytes, it

suggests the opposite for land snails (Fig. 3d). Snails are

independent of light availability, but need calcium for the

development of their shells. Therefore, an increase in calcium

concentration in leaf litter resulting from the spread of

deciduous trees supports snail species richness. Of the four

forest types of the Southern Urals compared in this study, the

most diverse snail assemblages were recorded in the Acer–

Tilia–Ulmus forests, probably because they contain calcium in

soluble citrate form, which is directly available to snails

(Wareborn, 1969, 1970). Rich snail assemblages were also

found in the Southern Ural floodplain forests (Horsak et al.,

2010), which contain Ulmus laevis and are probably enriched

in calcium from the mineral accumulation in the floodplains.

The composition of the Southern Ural snail fauna is very

similar to that of the early Holocene fossil record from Central

Europe (Lozek, 1993, 2000; Horsak et al., 2010). Like the fossil

assemblages, this fauna is remarkably poor in species. We

recorded 28 snail species in total, and a maximum of 14

species at a single site. Twice as many species are usually

recorded in Central European forest plots of the same size as

we used in the Southern Urals (Cameron & Pokryszko, 2004;

Martin & Sommer, 2004; Sulikowska-Drozd & Horsak, 2007;

Cejka et al., 2008). As for the shade-tolerant vascular plants,

the limited species pool of snails in the Southern Urals

probably results from the larger distance of this region from

the Pleistocene refugia of broad-leaved forests. However, a

general increase in richness of snail assemblages from the

Pinus–Larix forests to the Acer–Tilia–Ulmus forests parallels

the gradual enrichment of the Central European snail fauna

between the late-glacial and mid-Holocene (Lozek, 1964, 1993,

2000).

(a) (b) (c)

Figure 5 Sample-based rarefaction curves showing an increase in the total number of species of (a) herb-layer vascular plants, (b) ground-

dwelling bryophytes and (c) snails encountered in four forest types of the Southern Urals with increasing number of plots sampled. Note the

different ranges on the vertical axes.



CONCLUSIONS

Using an analogue with the modern forests of the Southern

Ural foothills, we propose the hypothesis that the spread of

broad-leaved trees in the early Holocene forests of Central

Europe caused a profound environmental change. First, the

accumulation of leaf litter from birch, aspen and oak reduced

the diversity of ground-dwelling bryophytes. Later on, elm,

lime, maple and ash formed a dense canopy and caused a

decline of the light-demanding, species-rich herb layer, typical

of the previous open-canopy forests. However, the calcium-

rich litter of these trees enhanced nutrient cycling and

supported an increase in the species richness of land snails.

ACKNOWLEDGEMENTS

We thank Larisa Abramova, Amina Galeeva, Nikolai Ermakov,

Boris Mirkin and Al’bert Muldashev for supporting our

fieldwork; Michal Hajek and Jan Rolecek for comments and

discussions; Petra Makovcova for processing hemispherical

photographs; Ondrej Hajek for drawing the map; and Jens-

Christian Svenning and two anonymous referees for helpful

comments on the previous manuscript version. This study was

funded by the Grant Agency of the Academy of Sciences of the

Czech Republic (IAA6163303), the Ministry of Education of

the Czech Republic (MSM0021622416), the Academy of

Sciences of the Czech Republic (AV0Z60050516) and the

Russian Foundation for Basic Research RFBR (07-04-00030-a).

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BIOSKETCH

Milan Chytry is a professor of botany at Masaryk University,

Brno, Czech Republic. With a team of Czech, Russian and

Slovak plant ecologist, palynologists and a malacologist,

Michal Horsak, he is studying the diversity of the natural

ecosystems of southern Siberia and the Southern Ural

Mountains. This research focuses particularly on the determi-

nants of species diversity patterns and on the interpretation of

the full-glacial to early Holocene biota and environments of

eastern Central Europe using modern analogues from these

continental areas.

Author contributions: M.C. conceived the ideas and led the

writing; M.H. collected and processed the snail data and the

other authors collected and processed the botanical data;

J.D. and S.K. revised identifications of vascular plants and

bryophytes, respectively; M.C. and L.T. analysed the data; all

authors commented on the manuscript.

Editor: Jens-Christian Svenning

M. Chytry et al.


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