Habitats of relict terrestrial snails in southern Siberia: lessons for the reconstruction of...

ORIGINALARTICLE

Habitats of relict terrestrial snails insouthern Siberia: lessons for thereconstruction of palaeoenvironmentsof full-glacial Europe

Michal Horsak1*, Milan Chytry1, Beata M. Pokryszko2, Jirı Danihelka1,3,

Nikolai Ermakov4, Michal Hajek1,3, Petra Hajkova1,3, Katerina Kintrova1,

Martin Kocı1, Svatava Kubesova1,5, Pavel Lustyk1, Zdenka Otypkova1,

Barbora Pelankova1,3 and Milan Valachovic6

1Department of Botany and Zoology, Masaryk

University, Kotlarska 2, CZ-611 37 Brno,

Czech Republic, 2Museum of Natural History,

Wrocław University, Sienkiewicza 21, PL-50-

335 Wrocław, Poland, 3Institute of Botany,

Academy of Sciences of the Czech Republic,

Porıcı 3a, CZ-603 00 Brno, Czech Republic,4Central Siberian Botanical Garden, Russian

Academy of Sciences, Zolotodolinskaya 101,

Novosibirsk, 630090, Russia, 5Department of

Botany, Moravian Museum, Hviezdoslavova

29a, CZ-627 00 Brno, Czech Republic,6Institute of Botany, Slovak Academy of

Sciences, Dubravska cesta 14, SK-845 23

Bratislava, Slovakia

*Correspondence: Michal Horsak, Department

of Botany and Zoology, Masaryk University,

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

E-mail: [email protected]

ABSTRACT

Aim Shells of fossil molluscs are important for palaeoecological reconstructions.

However, the habitat requirements of snail species typical of central European

full-glacial loess sediments are poorly known because most of them became very

rare or extinct in Europe. The recent discovery of an almost complete extant

assemblage of such species in mountainous regions of central Asia enables more

precise characterization of their habitats, which may significantly improve

reconstructions of Pleistocene environments.

Location Altai Mountains, Russia.

Methods Terrestrial snail assemblages, vegetation composition and selected

environmental variables were recorded at 118 sites along a gradient of climatic

continentality in the Russian Altai. Habitat characteristics of sites where species

typical of the full-glacial period occurred were described using a classification

tree.

Results Seven of the eight species that are typical of central European full-glacial

loess sediments were found in the study area. They were confined to cool areas

with January mean temperatures below )17 �C, but occurred mainly in sheltered

habitats with a warmer microclimate, such as scrub or open woodland. Pupilla

loessica and Vallonia tenuilabris had the broadest habitat range, occurring from

woodland to dry steppe. Unexpectedly, Columella columella, Pupilla alpicola,

Vertigo genesii, V. parcedentata and V. pseudosubstriata were found mainly in

wooded fens and shrubby tundra rather than in open steppe. Most of these seven

species were recorded in base-rich wooded fens. Very dry open steppe habitats

usually supported no snails.

Main conclusions Habitat ranges of the studied snails in the Altai indicate that

the full-glacial landscapes of central European lowlands that harboured these

species were not completely dominated by open and dry loess steppe. Most

probably they contained a significant component of shrubby vegetation, patches

of wet habitats, and probably also areas of woodland at sites with a favourable

mesoclimate.

Keywords

Altai Mountains, climate, Gastropoda, habitat preferences, index species, loess

steppe, palaeoreconstruction, Pleistocene analogue, Russia, vegetation.

Journal of Biogeography (J. Biogeogr.) (2010) 37, 1450–1462

1450 www.blackwellpublishing.com/jbi ª 2010 Blackwell Publishing Ltddoi:10.1111/j.1365-2699.2010.02280.x

INTRODUCTION

Ecological studies of extant faunas and floras that are similar to

species assemblages found in the Pleistocene fossil record

provide important lessons for an understanding of glacial

environments (Anderson et al., 1989; Rousseau, 1991; Moine

& Rousseau, 2002; Schofield et al., 2007; Fløjgaard et al.,

2009). Landscapes of the modern boreal and arctic zones of

northern Europe suggest some similarities to the full-glacial

landscape of central Europe, because they harbour many

species of the central European full glacial, such as Scots pine

(Pinus sylvestris), Norway spruce (Picea abies), dwarf birch

(Betula nana) (Meusel et al., 1965–1992; Willis et al., 2000;

Willis & van Andel, 2004), reindeer (Rangifer tarandus),

muskox (Ovibos moschatus), wolverine (Gulo gulo), Arctic fox

(Alopex lagopus), Norway lemming (Lemmus lemmus) (Ho-

racek & Lozek, 1988; Mitchell-Jones et al., 1999; Musil, 2003;

Pazonyi, 2004; Sommer & Nadachowski, 2006) and several

species of snails (e.g. Columella columella and Vertigo genesii;

Lozek, 1964, 2001; Kerney et al., 1983). However, the northern

European climate, with its low summer temperatures, low

temperature sums of the growing season, and a low ratio of

summer temperatures and precipitation (Rivas-Martınez et al.,

2004), may not be the best modern analogue of the full-glacial

climates for the subcontinental south-eastern part of central

Europe (Frenzel et al., 1992; Guthrie, 2001; Barron & Pollard,

2002; Jost et al., 2005). Indeed, Fennoscandia lacks many

species of the central European full glacial, such as Swiss pine

(Pinus cembra) and European larch (Larix decidua) (Willis

et al., 2000; Willis & van Andel, 2004), the rodents Allactaga

major, Cricetulus migratorius, Lagurus lagurus and Microtus

gregalis (Horacek & Lozek, 1988; Pazonyi, 2004; Sommer &

Nadachowski, 2006) and some species of land snails that are

regarded as index (i.e. indicator) fossils of full-glacial loess

sediments in central Europe, for example Pupilla loessica and

Vallonia tenuilabris (Lozek, 1964, 2001).

The modelled full-glacial climate of central Europe (Barron

& Pollard, 2002; Jost et al., 2005) corresponds closely to the

modern climate in Siberia (Fløjgaard et al., 2009). This

climatic analogue has recently been supported by biological

data. Kunes et al. (2008) demonstrated a close similarity

between full- and late-glacial pollen samples from central

Europe and modern surface-pollen spectra from the Western

Sayan Mountains in southern Siberia. Similar spectra have also

been found in surface pollen from the adjacent Russian Altai

Mountains (Pelankova & Chytry, 2009). These mountain

ranges contain several vegetation types that are dominated by

sibling species (or subspecies) of the trees and shrubs that were

widespread across full-glacial central Europe (Willis & van

Andel, 2004) but retreated to the mountains after the Holocene

climate amelioration. These species include Siberian pine

(Pinus sibirica, related to European P. cembra), Siberian larch

(Larix sibirica, related to European L. decidua) and dwarf birch

(Betula rotundifolia, related to B. nana). Moreover, in the

Altai-Sayan region, vegetation types of taiga, open woodland

and tundra dominated by these species occur in close

proximity to the steppes (Kuminova, 1960), as they did in

full-glacial central Europe (Willis et al., 2000; Jankovska &

Pokorny, 2008).

The Altai Mountains also hold mammal assemblages that

are very similar to the fossil fauna of the European ‘mammoth

steppe’, including Equus spp., Rangifer tarandus, Saiga tatarica,

Gulo gulo, Lepus timidus, Ochotona spp., Allactaga major,

Cricetulus migratorius, Lagurus lagurus, Marmota spp. and

Microtus gregalis (Yudin et al., 1979; Horacek & Lozek, 1988;

Musil, 2003; Pazonyi, 2004; Agadjanian & Serdyuk, 2005;

Ricankova, 2008). This evidence suggests that the Altai-Sayan

region is probably the most significant modern refugium of the

central European full-glacial biota. Its refugial character is also

supported by the fact that fossil pollen spectra from the Altai

and adjacent regions indicate little difference between modern

biomes of this region and those reconstructed for the Last

Glacial Maximum (Tarasov et al., 2000). There was a rapid

spread of coniferous trees at the Pleistocene/Holocene bound-

ary, and an increase in forested area at the expense of treeless

formations (Blyakharchuk et al., 2004). However, there is no

evidence in the available fossil pollen data for the complete

disappearance or new emergence of any major vegetation type

in the Altai-Sayan region. The environment of this region can

be thus considered as rather conservative and stable, at least in

comparison with central Europe.

Recently, the view of the Altai and adjacent mountain ranges

as a refugium of European glacial biota has been confirmed by

a discovery in this area of extant snail assemblages that contain

nearly all the index species from full- and late-glacial central

Europe, including Columella columella, Pupilla alpicola,

P. loessica, Vallonia tenuilabris, Vertigo genesii, V. parcedentata

and V. pseudosubstriata (Pokryszko & Horsak, 2007; Meng,

2008, 2009; Meng & Hoffmann, in press).

Because terrestrial snails are common fossils in all types of

calcium-rich sediments, particularly loess (Lozek, 1964, 2001;

Rousseau, 1990), they are frequently used for the reconstruc-

tion of Quaternary palaeoenvironments (Krolopp, 1983;

Horacek & Lozek, 1988; Rousseau, 1991; Willis et al., 2000;

Moine & Rousseau, 2002; White et al., 2008). Snail fossils have

several important advantages over other types of fossil

material. First, snail shells can be easily identified to species,

whereas plant pollen is often identifiable only to genus or

family. Second, each shell represents one individual, which

enables an accurate estimation of population density. Third,

unlike pollen or vertebrate remains, snail fossils are usually

deposited in places where they lived, thus enabling a fine

spatial resolution of the resulting palaeoenvironmental recon-

struction. Fourth, snail fossils are well preserved in conditions

that are usually poor in other fossils, especially in dry and

calcium-rich sediments.

However, the use of a species for palaeoenvironmental

reconstruction can only be successful if its habitat range and

environmental affinities are sufficiently well known. So far this

has not been the case for several of the index snail species from

European full-glacial loess sediments, because modern ecolog-

ical studies either were confined to restricted parts of their

Snails of glacial Europe extant in southern Siberia

Journal of Biogeography 37, 1450–1462 1451ª 2010 Blackwell Publishing Ltd

range in central European mountains and Fennoscandia (e.g.

Columella columella, Pupilla alpicola, Vertigo genesii and V.

parcedentata; e.g. Kerney et al., 1983; Pokryszko, 1993; Horsak

et al., 2007) or have never been undertaken (e.g. Pupilla

loessica, Vallonia tenuilabris and Vertigo pseudosubstriata).

Some of these species were first described from the fossil

record and extant populations were discovered only some

decades later (e.g. Pokryszko, 1993; Pokryszko & Horsak, 2007;

Meng, 2009; Meng & Hoffmann, in press). The first reports on

the habitats in which some of these species (Vallonia tenui-

labris and Vertigo spp.) live in central Asia have become

available only recently (Meng, 2008, 2009; White et al., 2008).

In this study we attempt to identify and describe the habitats

that harbour the index snail species found in central European

full-glacial loess sediments in their modern refugium in the

Russian Altai Mountains. We describe the vegetation types,

climate and environmental conditions associated with the

occurrence of these species in order to obtain information

necessary for palaeoecological reconstructions of landscapes,

environments and vegetation during the cold periods of the

Pleistocene.

MATERIALS AND METHODS

Study area

This study was undertaken along an approximately 300-km-

long NNW–SSE transect (49�56¢–52�19¢ N, 85�35¢–88�31¢ E,

260–2570 m a.s.l.) running across the Russian part of the Altai

Mountains in the Altai Republic, part of the Russian Feder-

ation, in southern Siberia (Fig. 1). The mountains are formed

of Proterozoic to Devonian siliceous bedrocks such as mica

and chlorite schist and slate, together with local beds of

limestone and some intrusions of granite and other plutonic

rocks (Nekhoroschev, 1966). The high ranges of the Altai

Mountains strongly affect the distribution of precipitation,

which comes mostly with fronts from the north-west. In the

northern Altai foothills, mean annual precipitation locally

exceeds 800 mm, but it decreases sharply with every sub-

sequent mountain range crossed when moving south or south-

east (Gidrometeoizdat, 1966–1970; Polikarpov et al., 1986).

Particularly dry conditions occur in the intermontane basins in

the south-eastern part of the Russian Altai, which receive less

than 180 mm of annual precipitation (Beresneva, 2006). Most

precipitation falls in the summer, but in the south-eastern

basins it comes very irregularly with thunderstorms, and

therefore long periods of drought occur. Temperatures are

generally higher in the northern Altai foothills, and decrease

towards the south-east. Most of the study area is covered with

natural vegetation, which is weakly influenced by humans,

except for grazing in steppes and forest-steppes. Vegetation

varies strongly in response to the NW–SE climatic gradient

(Kuminova, 1960; Walter, 1974).

The northern part of the studied transect includes the Biya

river basin in the northern foothills of the Altai at elevations of

300–700 m. This is the most oceanic part of the study area,

with an annual precipitation of 450–800 mm and mean

January and July temperatures of )14 to )10 �C and 15 to

21 �C, respectively. It is dominated by taiga and hemiboreal

forests, with Abies sibirica, Betula pendula, Picea obovata, Pinus

sibirica, P. sylvestris and Populus tremula. Treeless areas are

covered by mesic meadows. Bogs and mineral-poor fens are

more common in this region than elsewhere in the study area.

The north-western part of the transect includes the Katun’

river valley and adjacent mountain ranges up to the Seminskii

Range in the south. At lower elevations in the Altai foothills

(250–1000 m), annual precipitation is 400–700 mm and mean

temperatures for January and July are )16 to )7 �C and 14 to

21 �C, respectively. There is a forest-steppe landscape consist-

ing of a mosaic of hemiboreal forests with Pinus sylvestris and

Betula pendula and meadow steppes. At higher elevations

(1400–2100 m), annual precipitation is 1200–1400 mm and

mean temperatures for January and July are )24 to )21 �C

and 7 to 10 �C, respectively. Mountain ranges are covered

mainly by sparse Pinus sibirica taiga and, above the timberline,

by shrubby tundra dominated by Betula rotundifolia.

The central part of the transect includes the Katun’ river

valley south of the Seminskii range and the lower part of the

Chuya valley. Owing to its leeward position, annual precip-

itation is only 250–400 mm in the valley bottoms and on the

lower slopes (at 700–1000 m a.s.l.) and about 800–900 mm at

higher elevations (1300–1400 m). Temperatures are )18 to

)15 �C in January and 11 to 15 �C in July. The landscape is a

forest-steppe consisting of a mosaic of Larix sibirica hemibo-

real forests and short-grass steppe, with Picea obovata

occurring in wetter sites of valley bottoms and on north-

facing slopes, and Pinus sibirica at higher elevations, where

it is associated with alpine tundra dominated by Betula

rotundifolia.

Figure 1 Studied sites in the Altai Republic (Russia). Black

squares indicate sites with at least one of the full-glacial index snail

species; white squares are other studied sites.

M. Horsak et al.

1452 Journal of Biogeography 37, 1450–1462ª 2010 Blackwell Publishing Ltd

The south-eastern part of the transect includes the large

intermontane basins along the Chuya River and their adjacent

mountain ranges. The bottom of the Kurai Basin (c. 1500 m

a.s.l.) receives about 150–180 mm of annual precipitation, and

the bottom of the Chuya Basin (c. 1750 m a.s.l.) less than

150 mm. We sampled sites at elevations of 1300–2600 m,

where annual precipitation was 150)550 mm and mean

temperatures of January and July were )23 to )18 �C, and 5

to 12 �C, respectively. There are generally the same vegetation

types as in the central part of the transect, but the area of forest

decreases and that of steppe increases towards drier regions.

The bottoms of the Kurai and Chuya basins are extensive

treeless areas with a short-grass steppe. On some mountain

slopes around the Chuya Basin, forest is entirely absent and

steppe borders directly on alpine tundra.

Sampling

We sampled snail assemblages, vegetation and environmental

variables at 118 sites along the environmental transect of

increasing climate continentality across the Russian Altai

Mountains in August 2005 and July 2006. The sites were

selected to include the whole regional range of habitat types,

determined by physiognomy and dominant plant species.

Sampling plots of 10 · 10 m2 were located in the central parts

of physiognomically and ecologically homogeneous vegetation

stands. Places affected by recent disturbance, for example early

stages of post-fire succession or ruderal vegetation near human

settlements, were not sampled. Multiple sampling of a single

habitat was avoided at nearby sites with similar elevation, slope

and aspect in order to avoid pseudo-replications.

Within each plot, snails were searched for by eye and

collected in appropriate microhabitats for 2 h. In addition, a

5-L sample of leaf litter, moss polsters and topsoil was collected

within each plot from several patches, especially those

considered most favourable for snails. The samples were

washed through a sieve with a 0.6 · 0.6 mm mesh in the field

immediately after sampling, using the wet-sieving method

(Horsak, 2003). Live snails and shells were extracted during

washing and preserved in 80% ethanol or dried out.

Sites were classified into the following 13 habitat types

according to vegetation structure, plant species composition

and abiotic environmental factors. The number of sampled

sites (in brackets) approximately reflects the frequency of a

particular habitat in the landscape. Taiga (n = 11): mesic to

wet coniferous forest with a species-poor herb layer and a well-

developed moss layer, usually dominated by Abies sibirica,

Larix sibirica, Picea obovata or Pinus sibirica. Hemiboreal

forest (n = 22): dry to mesic coniferous or deciduous forest

with a species-rich herb layer and a sparse moss layer, usually

dominated by Betula pendula, Larix sibirica or Pinus sylvestris.

Wooded fen (n = 2): wet woodland with accumulation of

base-rich organic sediment, dominated by Picea obovata.

Treeless fen (n = 4): open base-rich fen with sedges and

mosses. Acidic mire (n = 7): bogs and mineral-poor fens.

Alluvial scrub (n = 3): riverine woody vegetation with willows

(Salix spp.). Tall-forb vegetation (n = 5): tall herbaceous

vegetation in wet places, usually along mountain streams.

Alpine grassland (n = 3): short herbaceous vegetation above

the timberline. Shrubby tundra (n = 8): low-shrub vegetation

above the timberline, dominated mainly by Betula rotundifolia

(= B. nana s.l.), in places also by Dryas oxyodonta. Steppe

(n = 36): both short-grass steppe and tall-grass (meadow)

steppe, in places with low shrubs such as Caragana or Spiraea.

Saline grassland (n = 4): grassland on soils with elevated salt

concentration, usually in shallow depressions in steppe land-

scapes. Meadow (n = 8): mesic grassland used for regular or

occasional hay-making. Scree (n = 5): treeless talus slopes.

In each plot, all species of vascular plants and ground-

dwelling bryophytes and lichens were recorded, with their

cover-abundances estimated on the Braun-Blanquet scale (van

der Maarel, 1979). The following environmental variables were

compiled for each plot (Table 1). (1) Elevation, measured with

a GPS receiver (Garmin 60CSx) in the field. (2–7) Climatic

data, including annual, winter (November–March) and su-

mmer (April–October) precipitation sums and mean annual,

January and July temperatures, were taken from a spatially

explicit climatic model (Chytry et al., 2007) based on climate-

station data interpolated over a digitized 1:200,000 map using

the ArcGIS 8.2 Geographic Information System (ESRI, 2003).

Temperature interpolations considered local topography,

using an adiabatic lapse rate of 0.65 �C per 100 m of altitude.

Precipitation was computed from the precipitation-elevation

charts compiled for each of the aridity-humidity sectors of the

Altai-Sayan region (Polikarpov et al., 1986). Summer and

winter precipitation were strongly correlated (r = 0.992,

P < 0.001), as were January and July temperatures (r =

0.710, P = 0.001). (8) Slope inclination was measured in the

field with a clinometer (Clino Master, Silva, Sollentuna,

Sweden). (9) Radiation index was calculated from slope

inclination and aspect according to McCune & Keon (2002,

eq. 3). The values of this index are high on steep south-facing

slopes, low on steep north-facing slopes and medium on flat

land, gentle slopes, and steep east- or west-facing slopes. (10–

12) Potential radiation, accounting for shading by adjacent

topographic features and forest canopy, was calculated from

hemispheric photographs taken in the vertical direction at a

height of 1.5 m above ground in each plot, using a Nikon

CoolPix 4500 digital camera with a fish-eye lens. Radiation was

estimated as a daily sum of direct, diffuse, and total (= direct +

diffuse) radiation for 21 June in mol m)2 day)1. (13–16)

Percentage covers of trees, shrubs, herbs and bryophytes/

lichens were estimated by eye in the field. (17–19) Depths of

soil, peat and litter layers were measured using a metal rod.

(20) Percentage cover of litter was estimated by eye. (21–22)

Soil pH and electrical conductivity were measured in a 2:5

soil:water solution of mixed soil samples taken at four places in

each plot from a depth of 5–10 cm or less if the soil was very

shallow. A GPRT 1400 AN pH-meter (Greisinger Electronic

GmbH, Regenstauf, Germany) and a CM113 conductivity

meter (Snail Instruments, Beroun, Czech Republic) were used,

respectively. Conductivity caused by H+ ions was subtracted



according to Sjors (1952). (23–24) Numbers of tree species and

vascular plant species were recorded for each plot.

Data analysis

To define indicator snail species of the full-glacial landscapes

of central Europe we adopted Lozek’s classification of fossil

molluscs and his concept of index species (Lozek, 2001). The

vast majority of fossil records of full-glacial index species are

confined to loess sediments, and at present these species

are either extinct or survive in remote areas with a climate

different from the modern climate of central Europe (Lozek,

2001). We considered the following seven species as full-glacial

index species: Columella columella, Pupilla alpicola, P. loessica,

Vallonia tenuilabris, Vertigo genesii, V. parcedentata and

V. pseudosubstriata (Fig. 2). Vertigo genesii was included, even

though it is very rare in loess sediments (Lozek, 2001);

however, it became more common during the Late Glacial

period (Lozek, 1964). Its rarity in the dry full-glacial

landscapes was probably linked to the rarity of suitable

habitat, namely calcareous marshes.

The 118 plots were classified into three categories: (1) plots

containing at least one of the seven index species; (2) plots

containing other snails only; and (3) plots containing no snails.

Hereafter, these categories of plots are termed Index, Others

and None.

The relationships between these three categories, habitat

types and environmental variables were analysed using classi-

fication trees (CART; Breiman et al., 1984; De’ath & Fabricius,

2000). This method is suitable for exploratory analysis

of complex unbalanced data sets that involve higher-order

interactions and nonlinear relationships between predictor

variables. It reveals ecologically meaningful relationships that

might remain hidden if standard techniques, such as linear

models, were used. To select the optimal tree size (with the

optimal number of nodes) we used a complexity parameter (cp)

that weighs both the tree complexity and the sum of errors in

the classification of a new set of sites (i.e. a test data set). This is

usually computed in a cross-validation process that enables the

utilization of all information available. We worked with a

cross-validation function of the rpart package, R 2.9.2

software (R Development Core Team, 2009) with 10 subsets,

and built the tree with constraints on the minimal number of

sites to be divided (10) and the minimal number of sites in

terminal nodes (5). The cross-validation process was repeated

500 times with random data subsets in each repetition, and the

complexity parameter for every node of all 500 trees was

recorded. The complexity level of the tree that most often

reached the lowest cp-value was chosen. For each node of the

tree, apart from the primary splitter variable, surrogates (i.e.

variables allocating at least 90% of the cases similarly to the

primary splitter) were identified.

RESULTS

The misclassification rate of the classification tree was 17.8%;

that is, 97 out of 118 sites were successfully classified based on

splitting criteria into the Index (n = 18), Others (n = 71) or

None (n = 29) category (Fig. 3). The model revealed that the

occurrence of the index snail species of central European loess

sediments is confined to macroclimatically cool areas with

January, July and annual temperature means lower than )17.9,

10.4 and )3.3 �C, respectively. Such conditions are found

especially in the Kurai and Chuya basins and the adjacent

mountain ranges in the south-eastern Russian Altai at

elevations higher than c. 1400 m (Figs 1 and 4). In these cool

areas, snails are mostly absent from open exposed sites, living

Table 1 Descriptive statistics for the environmental variables

established for the 118 sample plots in the Russian Altai

Mountains.

Mean

Standard

deviation Minimum Maximum

Elevation (m a.s.l.) 1257 660 262 2570

Annual precipitation

(mm)

572 333 165 1399

Winter precipitation

(mm)

159 124 33 477

Summer precipitation

(mm)

413 213 132 922

Annual temperature (�C) )1.7 4.9 )9.0 7.4

January temperature (�C) )17.1 4.3 )23.1 )7.6

July temperature (�C) 12.2 4.3 5.0 20.9

Inclination (�) 14 12 0 43

Radiation index 0.81 0.13 0.40 0.96

Transmitted direct

radiation

(mol m)2 day)1)

15.5 6.5 2.0 22.1

Transmitted diffuse

radiation

(mol m)2 day)1)

14.2 5.5 3.0 20.1

Transmitted total

radiation

(mol m)2 day)1)

29.7 11.8 5.1 41.2

Tree cover (%) 10 16 0 70

Shrub cover (%) 18 18 0 75

Herb cover (%) 63 26 10 100

Bryophyte/lichen

cover (%)

29 32 0 100

Soil depth (cm) 23 8 3 30*

Peat depth (cm) 3 9 0 30*

Litter depth (cm) 2 1 0 10

Litter cover (%) 21 25 0 95

Soil pH 6.4 1.0 4.0 8.6

Soil conductivity

(lS cm)1)

163 155 17 1176�

No. of tree species 0.6 1.1 0 4

No. of vascular plant

species

40.8 19.4 8 90

*Soils and peat accumulations deeper than 30 cm were arbitrarily given

a value of 30 cm.

�In one plot where the soil contained NaCl the value was above

10,000 lS cm)1, which is the upper limit of the conductivity

meter used.

M. Horsak et al.


(a)

(d) (e) (f) (g)

(b) (c)

Figure 2 Index species of the central Euro-

pean full glacial that are extant in central

Asia. Most of them are typical fossils of

European loess sediments (a–f) and some of

them are currently extinct in Europe (a, d, f).

All shells were collected in the studied sites

in the Altai Republic, Russia. (a) Vallonia

tenuilabris (2.31 mm); (b) Columella

columella (2.95); (c) Pupilla alpicola (3.55);

(d) Pupilla loessica (2.67); (e) Vertigo

parcedentata (2.22); (f) Vertigo pseudosub-

striata (2.04); (g) Vertigo genesii (1.91). The

largest dimension of each shell is given in

parentheses. Photos by M. Horsak.

Figure 3 Classification tree for the occurrence of index, other and no snail species at 118 study sites in the Russian Altai Mountains.

Numbers at each node indicate the number of plots with the occurrence of index/other/no snails and the total number of sites assigned

to that node. The primary splitter variable and its split value at each node are shown in bold. Surrogates (i.e. variables that allocate at

least 90% of the cases to the same group as the primary splitter) are given in smaller letters below the primary splitter. Identification numbers

of nodes used in the text are given in circles. Habitat types and index species that belong to particular terminal nodes are shown below

these nodes, with their frequencies in parentheses. Branch lengths are proportional to the classification improvement at a particular node.

Species abbreviations: ColCol, Columella columella; PupAlp, Pupilla alpicola; PupLoe, Pupilla loessica; ValTen, Vallonia tenuilabris; VerGen,

Vertigo genesii; VerPar, Vertigo parcedentata; VerPse, Vertigo pseudosubstriata.



mainly in places protected by tree canopy or adjacent

topographic features (Fig. 3, node 2) and containing at least

5% of shrub cover (node 4). The index species prevailed in

areas with mean annual precipitation lower than 290 mm or

outside woodlands in areas with higher precipitation (nodes 5

and 6), whereas other species were more common in

woodlands in areas of higher precipitation (node 6).

Wooded fens dominated by Picea obovata, although repre-

sented by only two sites, harboured all the index species except

Pupilla loessica (Table 2, Fig. 4). Four of the seven index

species were also recorded in tundra with low shrubs such as

Betula rotundifolia and in places also B. humilis, Dryas

oxyodonta, Pentaphylloides fruticosa and Salix spp. The other

habitats contained only 1–3 index species. Pupilla loessica was

the most frequent index species, recorded at 13 sites and in

seven habitats. Two other index species, Vertigo genesii (8 sites)

and Vallonia tenuilabris (7 sites), were also relatively common,

found in four and five habitats, respectively. The remaining

four species were recorded at fewer than four sites and in fewer

than three habitats.

Full-glacial index species were most often found in wood-

lands with Larix sibirica or Picea obovata as well as in shrubby

habitats with the above-mentioned tundra shrubs, or in steppe

landscapes, with drought-adapted shrubs such as Caragana

Table 2 Habitat types and ranges of environmental variables associated with the occurrence of the studied index snail species in the Russian

Altai Mountains. For each species and habitat the range of the number of individuals found at particular sites is given. For snail species

authorities see Appendix S1.

Columella

columella

Pupilla

alpicola

Pupilla

loessica

Vallonia

tenuilabris

Vertigo

genesii

Vertigo

parcedentata

Vertigo

pseudosubstriata

Total no. of sites/individuals 2/83 1/33 13/133 7/90 8/650 3/23 3/28

Habitat type (number of sites/total number of all snail species)

Shrubby tundra (3/11) 0 0 3–7 0 1–4 2–17 23

Taiga (1/8) 0 0 1–8 2 4 0 0

Hemiboreal forest (3/9) 0 0 3–18 29 0 0 0

Wooded fen (3/11) 21–62 33 0 15–18 37–410 4 4

Alpine grassland (1/7) 0 0 6 3 0 0 0

Treeless fen (2/3) 0 0 0 0 73–116 0 0

Meadow (1/7) 0 0 0 0 0 0 1

Steppe (3/13) 0 0 1–53 9 0 0 0

Saline grassland (1/4) 0 0 8 14 5 0 0

Environmental variable

Elevation (m a.s.l.) 1354–1731 1731 1342–2490 1342–2059 1330–1998 1731–1994 1354–1994

Annual precipitation (mm) 196–522 195 205–879 195–522 195–880 195–821 522–821

Winter precipitation (mm) 41–164 40.9 45–308 44–164 41–308 41–308 164–283

Summer precipitation (mm) 154–358 154 160–572 154–358 154–572 154–538 358–586

Annual temperature (�C) )5.3–()3.9) )5.3 )8.2–()0.7) )7.8–()3.1) )8.2–()3.1) )8.2–()5.3) )7.5–1.0

January temperature (�C) )19.5–()18.0) )19.5 )22.2–()17.1) )21.9–()17.1) )22.1–()17.1) )22.1–()19.5) )21.4–()18.0)

July temperature (�C) 8.3–10.1 8.3 5.7–11.1 6.1–10.8 5.7–10.8 5.7–8.3 6.4–11.4

Inclination (�) 1–2 1 0–33 0–33 0–19 1–19 2–19

Radiation index 0.86–0.87 0.86 0.45–0.95 0.45–0.90 0.84–0.88 0.84–0.87 0.82–0.87

Transmitted direct radiation

(mol m)2 day)1)

5.3–13.4 13.4 4.4–21.7 4.4–21.3 5.3–21.2 13.4–21.2 5.3–21.2

Transmitted diffuse radiation

(mol m)2 day)1)

5.7–11.6 11.6 5.0–19.9 5.0–19.9 5.7–19.2 11.6–19.2 5.7–19.2

Transmitted total radiation

(mol m)2 day)1)

10.9–25.0 25 9.4–40.4 9.4–39.6 10.9–40.4 25.0–40.4 11.0–40.4

Tree cover (%) 15–20 15 0–35 0–35 0–20 0–15 0–20

Shrub cover (%) 25–40 25 0–70 0–50 0–70 25–70 5–70

Herb cover (%) 30–60 60 10–95 10–80 10–95 60–95 30–100

Bryophyte/lichen cover (%) 70–80 70 5–90 5–90 5–90 40–70 40–80

Soil depth (cm) ‡30 ‡30 5 to ‡30 5 to ‡30 5 to ‡30 10 to ‡30 10 to ‡30

Peat depth (cm) 0 to ‡30 ‡30 0–12 0 to ‡30 0 to ‡30 0 to ‡30 15 to ‡30

Litter depth (cm) 3–15 3 1–10 1–15 1–15 1–3 1–15

Litter cover (%) 10–30 30 1–80 1–30 1–30 3–30 3–15

Soil pH 6.8–7.5 6.8 5.4–8.6 6.1–8.6 5.4–8.6 5.4–6.8 5.8–7.5

Soil conductivity (lS cm)1) 318–408 408 40–1176 40–1176 56–1176 56–408 17–318

No. tree species 2–3 3 0–2 0–3 0–3 0–3 0–2

No. vascular plant species 34–35 35 25–58 33–56 25–55 35–43 34–45

M. Horsak et al.


Figure 4 Habitats harbouring the studied index snail species in the Russian Altai Mountains. 1, taiga; 2, hemiboreal forest; 3, wooded

fen; 4, treeless fen; 5, alpine grassland; 6, shrubby tundra; 7, steppe; 8, saline grassland; 9, meadow. Photos by P. Hajkova (1–5, 7, 8),

Z. Otypkova (6) and M. Chytry (9). A detailed description and a list of snail species recorded at each site are available in Appendix S1 in the

Supporting Information.



arborescens, Cotoneaster uniflorus, Rosa pimpinellifolia and

Spiraea media (68% of all records, see Fig. 4). Only two

species, Pupilla loessica and Vallonia tenuilabris, were also

frequently recorded in treeless habitats, although they were still

more frequent in woodlands and scrub. At two sites we

sampled both a wooded fen and an adjacent open fen lacking

trees and shrubs. In both cases, wooded fens were richer in

snail species and contained several index species, whereas the

treeless areas of the same fen contained fewer than four species

of land snails, of which only one, Vertigo genesii, was an index

species. However, this species occurred there in high densities.

DISCUSSION

Our data confirm that the Altai Mountains are an important

refugium for full-glacial snail faunas, as recently documented

by Pokryszko & Horsak (2007), Meng (2008, 2009) and Meng

& Hoffmann (in press). Extant populations of index snail

species of the central European full glacial are significantly

associated with a cold macroclimate in the southern part of the

Russian Altai. Of the 18 sites where these species were found,

16 had a mean January temperature below )17.9 �C and for

the other two it was below )17.1 �C. None of these sites had

mean July and annual temperatures higher than 11.4 and

1.0 �C, respectively (Table 2). These values correspond to

those modelled for the central European full-glacial period

(Barron & Pollard, 2002). The temperature limitation of the

full-glacial index snail species suggests that their niches, like

those of plants (Martınez-Meyer & Peterson, 2006), mammals

(Martınez-Meyer et al., 2004) and probably other animal

groups, remained relatively stable over several millennia.

However, their affinity to cool environments contrasts with

the fact that land snails, as poikilotherms, are generally

favoured by warmer conditions (e.g. Bishop, 1977; Cameron

& Greenwood, 1991) because of their sensitivity to superco-

oling. It is known that small snail species are able to survive

under cold conditions better that those with large bodies

(Ansart & Vernon, 2003), but both groups need specific shelter

to survive. This raises the question why these species were not

also found in warmer areas of the Altai Mountains in spite of

the fact that suitable habitats and source populations were

available in adjacent areas and that sites from warmer areas

were well represented in our samples. This pattern can be

explained either by physiological constraints on the species

fundamental niche, or by biotic interactions. Physiological

constraints that exclude these species from warmer areas may

have evolved in the full-glacial landscapes, which probably

contained few microclimatically warmer or otherwise favour-

able habitats. Competitive exclusion of the index snail species

by other snails in warmer areas is unlikely, because snail

assemblages of warmer areas, although richer in species than

those of cold areas, are still distinctly poorer in species than the

snail assemblages of temperate Europe (e.g. Martin & Sommer,

2004; Sulikowska-Drozd & Horsak, 2007) and include species

that would hardly be able to outcompete all the index species of

the region. However, further biotic mechanisms could control

this distributional pattern, for example competitive pressure of

snail predators (Barker, 2004) occurring only in warmer areas.

An important finding for the reconstruction of full-glacial

environments is the preference of index snail species for wet or

microclimatically favourable wooded or shrubby habitats.

Meng (2008, 2009) observed a similar pattern in various

mountain ranges of central Asia, where 70% of all records of

Vallonia tenuilabris and most records of Vertigo genesii and V.

parcedentata were from wet habitats. Vallonia tenuilabris has

also been previously reported from various forest habitats in

southern Siberia (Schileyko, 1984, p. 169; White et al., 2008).

Although it has traditionally been believed that trees were

virtually absent in central European full-glacial landscapes with

loess accumulation, the above-mentioned data indicate the

existence of patches of open woodland or scrub in the loess

sites from which fossils of the index snails are known. This is in

accordance with recent palaeobotanical evidence of several tree

species occurring in the full-glacial landscapes of eastern-

central Europe (Rybnıckova & Rybnıcek, 1991; Willis et al.,

2000; Jankovska et al., 2002; Willis & van Andel, 2004; Birks &

Willis, 2008; Jankovska & Pokorny, 2008). Modelling exercises

also indicated the climatic suitability of full-glacial central

Europe for coniferous trees and other species with modern

boreal distributions (Alfano et al., 2003; Svenning et al., 2008;

Fløjgaard et al., 2009). We found the index snail species to

occur in Altaian woodlands dominated by Larix sibirica and

Picea obovata, that is, by sibling species of European L. decidua

and P. abies, respectively, which are both reported from central

European full-glacial fossil pollen and charcoal. Thus, our data

on the Altai snail assemblages provide further evidence of

northern tree refugia in full-glacial Europe. They are consistent

with the reconstruction of the full-glacial landscape in central

Europe as a mosaic of loess steppes, shrubby tundra, and

woodland patches in mesoclimatically suitable pockets (Rud-

ner & Sumegi, 2001; Kunes et al., 2008).

Shrubby or woodland vegetation with a favourable micro-

climate in the undergrowth may have been the main full-

glacial habitat of all snail species included in the present study

except Vertigo genesii. In the full-glacial sediments this snail is

known only from calcareous fens and very wet habitats (Lozek,

1964). The same pattern was observed in the extant snail

assemblages in the Altai, where the most abundant populations

of this species were encountered in treeless, calcium-rich fens.

In northern Europe this species is also characteristic of base-

rich treeless fens (Speight et al., 2003), but it is also reported

from wooded mires (Valovirta, 2003). Preferences for wet,

base-rich fens are also known for northern European popu-

lations of Columella columella and Vertigo parcedentata,

although the former occurs also in wet subarctic woodlands,

grey willow thickets and alpine meadows (Kerney et al., 1983;

Pokryszko, 1990, 1993). In central European high mountains,

C. columella can also inhabit grasslands on limestone outcrops

above 1500 m a.s.l. (Lozek, 1964; Pokryszko, 1990).

Another full-glacial index snail species that may not

necessarily have been linked with woody vegetation is Pupilla

loessica. This species was described from the central European

M. Horsak et al.


fossil record (Lozek, 1954) and its extant populations were

reliably recognized only recently in central Asia (Meng, 2009;

Meng & Hoffmann, in press). It seems to be the species most

tolerant of cold conditions, which are unfavourable for the

other index snail species. Pupilla loessica was more often

recorded at open steppe sites. This observation is in accor-

dance with the fossil record, because this snail is most

abundant in loess sediments from the Last Glacial Maximum

(e.g. Lozek, 1964, 2001). The areas and sites in the Altai

Mountains with the exclusive occurrence of this snail have a

fossil analogue in the drier phases of full-glacial loess steppes

(e.g. Lozek, 1989). We also found that this species can occupy a

broad range of habitats, including all types of habitats

supporting the other index species except fens. This is in

accordance with its abundant occurrence in most loess

sediments from central Europe (Lozek, 1964, 2001). A

similarly broad range of habitats was found for Vallonia

tenuilabris, which is another very common species associated

with loess sediments (Table 2). The broad niche of both

species in cool climatic conditions could be the reason why

they survived glacial periods of the European Pleistocene. They

also occurred in drier phases, which were characterized by

species-poor assemblages dominated by Pupilla spp. (Lozek,

1964; Willis et al., 2000). This Pupilla-rich fauna is conse-

quently regarded as aridity-tolerant. In contrast, the other

index species were mostly characteristic of the youngest loess

deposits (30,000–14,000 yr bp; Lozek, 2001). The basal part of

this thick depositional sequence includes several horizons of

pale grey tundra gley soils, indicating a wetter climate (Klıma,

1958) than in previous glacial periods. This basal part is

characterized by rich snail assemblages with all the loess index

species (Lozek, 2001). This corresponds perfectly to the

modern situation observed in the Altai, where dry steppe

habitats are inhabited mostly by species-poor Pupilla/Vallonia

faunas. However, the driest steppes at exposed sites, which

contain no or an insignificant cover of shrubs, are usually

devoid of all snail species. This indicates that the environ-

mental conditions at the bottoms of the driest basins in the

south-eastern Russian Altai (Kurai and Chuya Basins) are

probably harsher than those of many full-glacial landscapes of

central Europe.

It should be noted that there are some differences between

the studied snail faunas and the full-glacial snail assemblages of

central Europe (see Lozek, 2001 and lists of species recorded in

the Altai in Appendix S1 in the Supporting Information).

There are several species unique to each of these two contexts;

however, most differences can be easily explained by a limited

distribution or different biogeography of the higher taxa to

which these species belong. For example, one of the most

abundant species of European loess sediments was Helicopsis

striata, which has never occurred outside Europe. Indeed, there

are about 5000 km between central Europe and the Altai – a

distance that could cause differences in species composition

even within the environmentally homogeneous loess steppe

biome. However, an important finding is that, except for one

index species of the full-glacial loess sediments of central

Europe, Catinella antiqua, all index species were found extant

in the study area.

In conclusion, the occurrence of relict snail assemblages,

coupled with relict assemblages of plants and mammals,

confirms that the landscape of the Altai Mountains can be

regarded as the best known modern analogue of the last full-

glacial period of central Europe. Even within this region of

continental climate, the index snail species of the full-glacial

loess sediments are limited to colder areas. In these areas their

current habitat ranges suggest that the full-glacial landscapes of

central European lowlands very probably contained a signif-

icant component of shrub vegetation, patches of wet habitats,

and probably also patches of woodland at sites with a

favourable mesoclimate (Fig. 4). These results add to the

growing body of literature demonstrating that full-glacial

landscapes of the central European lowlands were not com-

pletely treeless as had traditionally been believed.

ACKNOWLEDGEMENTS

We thank the local staff of our expeditions for their varied

support, the employees of the Kamlak field station for

accommodation and a warm welcome, Vojen Lozek for

inspiring discussions, Katrin Karimova for processing the

hemispheric photographs, Ondrej Hajek for preparing the map

and Denis Popov for developing the climatic models. Very

useful comments and editorial work from John Birks, Pim van

der Knaap, Richard Preece and Vera Ricankova are greatly

appreciated. This research was funded by the Ministry of

Education of the Czech Republic (MSM0021622416) and the

Academy of Sciences of the Czech Republic (IAA6163303,

AVOZ60050516).

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the

online version of this article:

Appendix S1 Detailed location and species data of the 18

study sites in the Altai Mountains, with occurrences of index

snail species of full-glacial central Europe.

As a service to our authors and readers, this journal

provides supporting information supplied by the authors.

Such materials are peer-reviewed and may be re-organized for

online delivery, but are not copy-edited or typeset. Technical

support issues arising from supporting information (other

than missing files) should be addressed to the authors.

BIOSKETCHES

Michal Horsak and Beata Pokryszko are malacologists,

Katerina Kintrova is a statistician, Barbora Pelankova

is a palynologist, and the other team members are botanists

and plant ecologists. In a project of Masaryk University, Brno,

Czech Republic, coordinated by Milan Chytry, this team

studied the diversity of natural ecosystems in the Altai and

Western Sayan Mountains of southern Siberia in 2003–2006.

This research focused on patterns of species richness, their

determinants, and on the interpretation of full-glacial envi-

ronments of eastern-central Europe using modern analogues

from these continental areas. Particular attention was paid to

the calibration of the fossil record using modern pollen

deposition and modern assemblages of land snails.

Author contributions: M. Horsak and M. Chytry conceived

the ideas and led the writing; M. Horsak collected and

identified all snail samples; B. Pokryszko helped with the

identification of some problematic snail species; K. Kintrova

analysed the data using a classification tree; and the other co-

authors collected and processed environmental and botanical

data and commented on the manuscript.

Editor: John Birks

M. Horsak et al.


1

M. Horsák et al.: Habitats of relict terrestrial snails in southern Siberia: lessons for the reconstruction of palaeoenvironments of full-glacial Europe

Appendix S1 Detailed description of the 18 study sites in the Russian Altai Mountains with occurrences of index snail species of full-glacial loess sediments of central Europe. All recorded snail species and plant species with cover > 5% are given for each site. Plants are ordered by vegetation layers (tree, shrub, herb and moss layer), with layer separated by semicolons and species within layers ranked by decreasing cover. The taxonomy and nomenclature of vascular plants, bryophytes and lichens follow Cherepanov (1995), Ignatov & Afonina (1992) and Andreev et al. (1996), respectively. The first nine sites are shown in Figure 4; their numbers match the figure numbers.

1 – 50°07’06”N; 87°48’18”E; Kosh-Agach distr., Kurai: Northern Chuya Ridge, Bol’shoi Akturu river valley 14 km SSW of the village, valley bottom with open subalpine taiga, 1950 m a.s.l., 5 Aug 2005, field no. PH121. Snails: Columella intermedia Schileyko et Almuhambetova, 1984, Deroceras altaicum (Simroth, 1886), Euconulus fulvus (O.F. Müller, 1774), Vallonia tenuilabris (Al. Braun, 1842), Vertigo genesii (Gredler, 1856), Vitrina rugulosa Martens, 1874, Pupilla loessica Ložek, 1954, P. muscorum (Linné, 1758). Dominant plants: Larix sibirica; Betula rotundifolia; Hylocomium splendens, Aulacomnium palustre, Cladonia arbuscula, Dicranum spadiceum. 2 – 50°10’01”N; 87°48’37”E, Kosh-Agach distr., Kurai: SW margin of the Kurai steppe 12 km SW of the settlement, hemiboreal forest on a N facing slope, 1676 m, 4 Aug 2005, field no. PH120. Snails: Vertigo alpestris Alder, 1838, V. ronnebyensis (Westerlund, 1871), Euconulus fulvus (O.F. Müller, 1774), Pupilla loessica Ložek, 1954. Dominant plants: Larix sibirica; Caragana arborescens, Cotoneaster uniflorus; Bromopsis inermis, Iris ruthenica; Rhytidium rugosum. 3 – 50°09’04”N; 88°18’10”E, Kosh-Agach distr., Chagan-Uzun: Chuya river valley near the mouth of the Kuyuktanar valley 2 km NW of the settlement, wooded fen on a valley bottom, 1731 m, 3 Aug 2005, field no. PH117. Snails: Columella columella (G. v. Martens, 1830), Euconulus fulvus (O.F. Müller, 1774), Oxyloma sarsii (Esmark, 1886), Pupilla alpicola (Charpentier, 1837), Vallonia tenuilabris (Al. Braun, 1842), Vertigo genesii (Gredler, 1856), V. parcedentata (Al. Braun, 1847). Dominant plants: Picea obovata; Carex enervis, C. nigra, Equisetum pratense, E. scirpoides, Bryum pseudotriquetrum, Drepanocladus aduncus, Limprichtia cossoni, Sanionia uncinata. 4 – 50°09’16”N; 88°18’30”E; Kosh-Agach distr., Chagan-Uzun: Chuya river valley near the mouth of the Kuyuktanar valley 2 km NW of the settlement, base-rich fen, 1740 m, 2 Aug 2005, field no. PH113. Snails: Deroceras altaicum (Simroth, 1886), Oxyloma sarsii (Esmark, 1886), Vertigo genesii (Gredler, 1856). Dominant plants: Carex curaica, C. enervis, C. nigra, Equisetum variegatum, Juncus triglumis, Salix divaricata, Triglochin palustre; Hamatocaulis vernicosus, Aulacomnium palustre, Campylium stellatum. 5 – 50°06’02”N; 87°47’48”E; Kosh-Agach distr., Kurai: Northern Chuya Ridge, Bol’shoi Akturu river valley 17 km SSW of the village, wet alpine meadow on a gentle SSE

slope near the valley bottom, 2059 m, 5 Aug 2005, field no. PH123. Snails: Euconulus fulvus (O.F. Müller, 1774), Fruticicola schrenkii (Middendorff, 1851), Novisuccinea altaica (Martens, 1879), Perpolita hammonis (Ström, 1765), Pupilla loessica Ložek, 1954, Vallonia tenuilabris (Al. Braun, 1842), Vitrina pellucida (O.F. Müller, 1774). Dominant plants: Bupleurum longifolium, Carex pediformis s. l., Festuca sphagnicola, Pentaphylloides fruticosa, Trollius asiaticus. 6 – 50°28’32”N; 87°37’54”E; Ulagan distr., Ulagan: Ulagan plateau near Uzunkel’ lake, 28 km SW of the village, shrubby tundra, 1998 m, 18 Jul 2006, field no. MC202. Snails: Columella intermedia Schileyko et Almuhambetova, 1984, Euconulus fulvus (O.F. Müller, 1774), Novisuccinea altaica (Martens, 1879), Perpolita hammonis (Ström, 1765), Pupilla loessica Ložek, 1954, Vertigo genesii (Gredler, 1856), V. parcedentata (Al. Braun, 1847). Dominant plants: Betula rotundifolia; Aulacomnium palustre, Cladonia rangiferina, Polytrichum commune, Sphagnum warnstorfii, Tomenthypnum nitens. 7 – 50°09’52”N; 87°48’31”E; Kosh-Agach distr., Kurai: SW margin of the Kurai steppe 12 km SW of the settlement, steppe on a steep ESE-facing slope on limestone bedrock, 1693 m, 4 Aug 2005, field no. PH119. Snails: Pupilla alluvionica Meng et Hoffmann, 2008, P. altaica Meng et Hoffmann, 2008, P. loessica Ložek, 1954, P. muscorum (Linné, 1758), Vallonia costata (O.F. Müller, 1774). Dominant plants: Potentilla acaulis, Thymus serpyllum s. l. 8 – 50°18’27”N; 87°38’46”E; Ulagan distr., Aktash: Menka river valley 2 km E of the settlement, saline meadow grazed by horses, 1342 m, 6 Aug 2005, field no. PH126. Snails: Deroceras altaicum (Simroth, 1886), Pupilla loessica Ložek, 1954, Vallonia tenuilabris (Al. Braun, 1842), Vertigo genesii (Gredler, 1856). Dominant plants: Carex enervis, Cirsium esculentum, Deschampsia cespitosa, Glaux maritima, Halerpestes salsuginosa, Potentilla anserina. 9 – 50°59’06”N; 85°40’30”E; Ongudai distr., Zaisan’skaya Elan’: Seminskii Ridge, above the right bank of the Tuekta creek 2 km NW of the settlement, irregularly mown meadow, 1349 m, 12 Aug 2005, field no. MC150. Snails: Chilanodon bicallosa (L. Pfeiffer, 1853), Euconulus fulvus (O.F. Müller, 1774), Lindholmomneme altaica (Westerlund, 1896), Perpolita petronella (L. Pfeiffer, 1853), P. hammonis (Ström, 1765), Vertigo pseudosubstriata Ložek, 1954, V. substriata (Jeffreys, 1833).

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Dominant plants: Deschampsia cespitosa, Cirsium heterophyllum, Geranium pseudosibiricum; Brachythecium salebrosum, Rhytidiadelphus triquetrus. 10 – 49°56’40”N; 88°00’47”E; Kosh-Agach distr., Chuya steppe, Bel’tir: Imele brook valley (right-side tributary of the Taldura river) 12 km WSW of the village, alpine tundra on a N facing slope, 2450 m, 1 Aug 2005, field no. PH106. Snails: Pupilla loessica Ložek, 1954. Dominant plants: Dryas oxyodonta, Betula rotundifolia, Salix alpina, S. arctica, S. glauca; Abietinella abietina, Aulacomnium palustre, A. turgidum, Dicranum sp., Tortula ruralis. 11 – 49°57’03”N; 88°01’06”E; Kosh-Agach distr., Chuya steppe, Bel’tir: slopes above the right bank of the Taldura river near Oimok settlement, subalpine forest on a steep NNW facing slope near the timberline, 2490 m, 1 Aug 2005, field no. PH110. Snails: Pupilla loessica Ložek, 1954. Dominant plants: Larix sibirica; Arctous alpina, Dryas oxyodonta, Hedysarum neglectum, Pyrola rotundifolia, Abietinella abietina, Aulacomnium turgidum, Rhytidium rugosum, Sanionia uncinata, Tortula ruralis. 12 – 50°08’56”N; 87°48’58”E; Kosh-Agach distr., Kurai: SW margin of the Kurai steppe 12 km SW of the settlement, shruby steppe, 1726 m, 4 Aug 2005, field no. PH118. Snails: Euconulus fulvus (O.F. Müller, 1774), Pupilla loessica Ložek, 1954, Vallonia kamtschatica Likharev, 1963, V. tenuilabris (Al. Braun, 1842), Vertigo ronnebyensis (Westerlund, 1871). Dominant plants: Caragana arborescens, Rosa pimpinellifolia, Spiraea media; Artemisia sericea, Carex pediformis, Festuca valesiaca, Iris ruthenica; Rhytidium rugosum. 13 – 50°14’57”N; 87°41’32”E; Ulagan distr., Chuya valley, Aktash: right bank of the Chuya river 9.5 km SE of the village, spruce forest with a well-developed shrub layer on a steep NNW facing slope with open boulder patches, 1472 m, 30 Jul 2005, field no. MC102. Snails: Euconulus fulvus (O.F. Müller, 1774), Pupilla alluvionica Meng et Hoffmann, 2008, P. altaica Meng et Hoffmann, 2008, P. loessica Ložek, 1954, Vallonia costata (O.F. Müller, 1774), V. ladacensis (Nevill, 1878), V. tenuilabris (Al. Braun, 1842), Vertigo alpestris Alder, 1838, V. ronnebyensis (Westerlund, 1871). Dominant plants: Picea obovata; Caragana arborescens; Carex macroura; Rhytidium rugosum, Abietinella abietina. 14 – 49°57’14”N; 88°02’17”E; Kosh-Agach distr., Chuya steppe, Bel’tir: above the right bank of the Taldura river 10 km W of the village, near Oimok settlement, larch forest on a steep N facing slope, 2199 m, 31 Jul 2005, field no. MC105.

Snails: Pupilla loessica Ložek, 1954, Vallonia ladacensis (Nevill, 1878). Dominant plants: Larix sibirica; Abietinella abietina, Rhytidium rugosum. 15 – 50°26’50”N; 87°36’28”E; Ulagan distr., Aktash: near the road to Ulagan 16 km N of the town, south of the Ulagan pass, species-rich grassland on a steep slope, 1976 m, 19 Jul 2006, field no. MC209. Snails: Novisuccinea altaica (Martens, 1879), Perpolita hammonis (Ström, 1765), Pupilla loessica Ložek, 1954, P. muscorum (Linné, 1758), Vallonia kamtschatica Likharev, 1963, V. ladacensis (Nevill, 1878), Vertigo sp. (undescribed species). Dominant plants: Artemisia laciniata, Aster alpinus, Astragalus austrosibiricus, Carex pediformis s. l., Iris ruthenica, Pentaphylloides fruticosa, Saussurea controversa. 16 – 50°18’27”N; 87°38’22”E; Ulagan distr., Aktash: Menka river valley 2 km E of the settlement, treeless calcareous fen in a river floodplain, 1330 m, 6 Aug 2005, field no. PH125. Snails: Oxyloma sarsii (Esmark, 1886), Vertigo genesii (Gredler, 1856). Dominant plants: Blysmus rufus, Carex enervis, C. nigra, Eleocharis quinqueflora, Primula nutans; Limprichtia cossoni, Bryum pseudotriquetrum, Campylium stellatum, Pseudocalliergon turgescens. 17 – 50°28’36”N; 87°37’48”E; Ulagan distr., Ulagan: plateau near Uzunkel’ lake 28 km SW of the village, shrubby tundra, 1994 m, 18 Jul 2006, field no. PH201. Snails: Columella intermedia Schileyko et Almuhambetova, 1984, Deroceras altaicum (Simroth, 1886), Euconulus fulvus (O.F. Müller, 1774), Novisuccinea altaica (Martens, 1879), Pupilla loessica Ložek, 1954, P. muscorum (Linné, 1758), Vertigo sp. (undescribed species), V. genesii (Gredler, 1856), V. parcedentata (Al. Braun, 1847), V. pseudosubstriata Ložek, 1954. Dominant plants: Betula humilis, B. rotundifolia, Pentaphylloides fruticosa; Lagotis integrifolia; Sanionia uncinata. 18 – 50°18’25”N; 87°38’55”E; Ulagan distr., Aktash: Menka river valley 2 km E of the settlement, base-rich wooded fen on a valley bottom, 1354 m, 6 Aug 2005, field no. PH127. Snails: Columella columella (G. v. Martens, 1830), Deroceras altaicum (Simroth, 1886), Pupilla muscorum (Linné, 1758), Punctum pygmaeum (Draparnaud, 1801), Vallonia tenuilabris (Al. Braun, 1842), Vertigo genesii (Gredler, 1856), V. pseudosubstriata Ložek, 1954. Dominant plants: Picea obovata; Salix divaricata, S. pyrolifolia; Comarum palustre, Deschampsia cespitosa, Equisetum scirpoides; Helodium blandowii, Plagiomnium affine, Tomenthypnum nitens.

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Bryologist, 99, 137–169. Cherepanov, S.K. (1995) Sosudistye rasteniya Rossii i sopredel’nykh gosudarstv (Vascular plants of Russia and adjacent

countries). Mir i sem’ya-95, Sankt-Peterburg. Ignatov, M.S. & Afonina, O.M. (Eds) (1992) Check-list of mosses of the former USSR. Arctoa, 1, 1–58.

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