LAND SNAIL FAUNAS ALONG AN ENVIRONMENTAL GRADIENT
IN THE ALTAI MOUNTAINS (RUSSIA)
MATTHIAS H. HOFFMANN 1, STEFAN MENG 2 , PJOTR A. KOSACHEV 3,
TATJANA A. TERECHINA 3 AND MARINA M. SILANTEVA 3
1
Martin Luther University Halle-Wittenberg, Institute of Geobotany and Botanical Garden, Am Kirchtor 3, D-06108 Halle, Germany;
Ernst-Moritz-Arndt University Greifswald, Institute of Geography and Geology, Friedrich-Ludwig-Jahn-Str. 17a, D-17487 Greifswald, Germany; and
3
Altai State University, Dimitrova str. 66, Barnaul 656099, Russia
2
Correspondence: M.H. Hoffmann; e-mail: [email protected]
(Received 4 September 2009; accepted 29 September 2010)
ABSTRACT
Many land snail species of the European Pleistocene have recently been reported from Central Asia.
The ecological conditions in which they live, however, are little known. We studied vascular plants
and land snails along a climatic gradient in the Russian Altai Mountains. We recorded 566 plant
and 40 mollusc species. In the most continental part of the Altai we discovered living Pupilla loessica,
a land snail now extinct in Europe and which is an important indicator of palaeoenvironments of the
European Pleistocene. We inferred thermal ranges of the snail species in the Altai and observed considerable differentiation among the species. Moisture requirements of the species were indirectly estimated by using moisture indicator values of plant species co-occurring with the snails. They reveal
local moisture requirement patterns that cannot be inferred from climate data. Snails are sorted
along our transect; only a few species occur throughout the Altai. Many snails are able to occupy
various plant communities. A few species may be indicators of vegetation types. For palaeoreconstructions, mollusc species are apparently good indicators for climate but less so for vegetation types.
INTRODUCTION
Central Asian landscapes may be considered a proxy or analogue of European Pleistocene periglacial landscapes, which
were probably dominated by cold, dry steppes (e.g. Guthrie,
2001). Plants were rarely conserved in the fossil record during
dry periods around the glacial maxima, but terrestrial snails
are frequent. They are important indicator species of European
loess deposits. In particular, Pupilla loessica Ložek is a typical
species that was first described from fossil loess deposits of
Central Europe. It was considered to be extinct, although
Ložek (1986) speculated that P. loessica might still occur in the
Central Asian mountains, which was later confirmed (Meng &
Hoffmann, 2009a). Other species of the fossil snail communities
of the glacial maxima are also still extant in the northern
hemisphere. Examples are Vallonia tenuilabris (Braun), Columella
columella (von Martens) and Pupilla muscorum (L.) (Meng, 1995,
1998, 2009; Rousseau, 2001; Meyrick, 2002; White et al., 2008).
A comparative analysis of fossil and extant snail assemblages
shows that the qualitative and quantitative composition of
species varies over a wide range (Meng, 2009). Some species
frequently co-occurred in fossil assemblages, such as Oxyloma
elegans (Risso) and Vallonia pulchella (O.F. Müller), but have
not been observed living together in Central Asia (Meng,
2009). Species like V. tenuilabris, C. columella and others have
been found co-occurring in fossil as well as extant communities. These different co-occurrences, as well as presence/
absence patterns, may be indicators for large-scale environmental conditions and support the analyses of entire extant
and fossil faunistic groups instead of single species.
Information on the ecology of these molluscs, particularly
their affinity to vegetation, is available mainly from Europe
(e.g. Boycott, 1934; Kerney, Cameron & Jungbluth, 1983) and
is rare from Central Asia, where analogues to the periglacial
environments have been suspected. The Altai Mountains
provide a suitable area for studying plants and snails along a
steep climatic gradient (Modina, 1997), ranging from a more
moderately continental climate type along the humid northwestern margin of the mountain system with species-rich forests
and meadows, to a strong continental and dry climate in the
southeastern interior of the Altai with predominant desert
steppes and relict-like forests along the bases of the mountain
ranges. In this area the cold, dry steppe sometimes intergrades
with alpine vegetation (Kuminova, 1960; Hoffmann,
Telyatnikov & Ermakov, 2001; Kamelin et al., 2005).
Our working hypothesis was that we might encounter snail
and plant communities in the Altai Mountains that could
serve as close analogues with those of the European
Pleistocene. For this purpose snail and plant species were
studied along a steep climatic gradient. Species are commonly
sorted along environmental gradients, leading to spatially
different community assemblages (Ackerly, 2003). Plants and
snails are considered to be largely independent of each other,
because plants frequently provide snails only with shelter and
an appropriate microclimate (humidity) for their home ranges
(Boycott, 1934; Horsák et al., 2007). Thus plants and snails
may be sorted independently along environmental gradients or
during changing climates and may be quite independent of
each other. On the other hand, one group of organisms might
also be an indicator for the other group and vice versa. As
already mentioned, snails are abundant in European glacial
deposits, whereas plants are scarce. If snails reported as fossils
could be shown to be indicators for plant species or vegetation
types, one could obtain an indirect and complementary
picture of palaeoenvironments.
The main goals of this study were: (1) to reveal distribution
patterns of plants and snails along a strong environmental gradient in the Altai Mountains; (2) to find climatic and environmental factors that control the pattern; (3) to study the snail
species distribution along the climatic gradient and determine
Journal of Molluscan Studies (2011) 77: 76– 86. Advance Access Publication: 7 January 2011
# The Author 2011. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.
doi:10.1093/mollus/eyq039
SNAILS AND PLANTS IN THE ALTAI
if snails can be indicators for plant communities and particular
regions (i.e. climatic conditions along the transect).
A parallel study to our own is that of Horsák et al. (2010).
They reported the distribution of seven ‘full-glacial index
species’ in the Altai Mountains that are frequent species of
Pleistocene deposits in Europe: Columella columella, Pupilla alpicola, P. loessica, Vallonia tenuilabris, Vertigo genesii, V. parcedentata
and V. pseudosubstriata. However, the fossil assemblages comprise many more species that are also present in the Altai
Mountains, which may give hints on Pleistocene environmental
conditions. Although superficially similar the two studies differ
in the environmental variables and sampling areas used.
Siberian pine (Pinus sibirica) forests and moist mountain
meadows.
(3) Onguday. Steppes and riverine forests dominate the vegetation along the Ursul river. At the other places we collected over a larger altitudinal range and in more diverse
habitats. Here, this was not possible because of difficult
access. However high true steppes and rocky true steppes
were present here, so we sampled them too.
(4) Aygulakskiy Khrebet. Located in the Central Altai, the
region is moderately moist. Larch (Larix sibirica) is a dominant species in this region.
(5) Saylyugem. Situated in the southeastern Russian Altai
close to the border with Mongolia, the Saylyugem is a prominent mountain area emerging from the surrounding
high plateau. Larch forests are confined in this area to a
small belt on the lower slopes of the massif.
MATERIAL AND METHODS
Study area
We studied vegetation and snail communities in August 2006
at five places along a northwest to southeast transect through
the Russian Altai, collecting at the following places (Fig. 1,
Table 1):
Climatic data for the sampling regions were obtained from
the closest station available (Fig. 1, Table 1). We obtained
data from Modina (1997) for three stations: Onguday
(833 m a.s.l.) for the Onguday collection locality, Ust-Ulagan
(1,241 m a.s.l.) for the Aygulakskiy Khrebet and Kosh-Agach
(1,757 m a.s.l.) for the Saylyugem. Data for the remaining two
regions were obtained from the ‘Russia’s weather’ server (http://
meteo.infospace.ru): Charyshskoje (429 m a.s.l.) for the
Korgonskiy Khrebet (Ust-Kan station in Modina, 1997, was
not useful because it is in the rain shadow of the Korgonskiy
Khrebet and is considerably drier than the sampled area) and
Shebalino (860 m a.s.l.) for the Seminskiy Khrebet.
(1) Korgonskiy Khrebet. This mountain ridge is in the
Altaiyskiy Kray in the most oceanic sector of the Altai.
The vegetation is mainly mixed coniferous forests and
meadows at lower elevations, and alpine meadows on the
high mountains.
(2) Seminskiy Khrebet. This and the following places are in
the Republic of Altai. The landscapes at the Seminskiy
Khrebet (a low mountain range) are dominated by
Figure 1. The study area in the Russian Altai. Circles indicate the regions we have sampled, triangles gives the location of the closest weather
stations.
Table 1. Descriptive data for the study regions and climate data from the closest weather stations (see text for details).
Region
No. of
Altitude (m)
plots
Altitude
Weather
January
July temp
Mean annual
Temp
Mean annual
range (m)
station
temp (8C)
(8C)
temp (8C)
range (8C)
precipitation (mm)
Korgonskiy Khrebet
12
872 – 1,775
903
Charyshskoye
212.3
17.7
3.9
30.3
717
Seminskiy Khrebet
18
1,203 – 1,937
734
Shebalino
212.6
15.3
2.4
28
487
8
725 – 762
37
Onguday
222.1
16.2
21.1
38.5
345
Aygulakskiy Khrebet
22
1,269 – 2,094
825
Ust-Ulagan
225.5
13.6
24.2
39.1
292
Saylyugem
51
2,132 – 2,648
516
Kosh-Agach
232.1
13.8
26.7
45.9
110
Onguday
77
M. H. HOFFMANN ET AL.
Temperatures for the sampling sites were calculated using a correction of 0.58C/100 m (Modina, 1997). For precipitation no
such rule exists so the precipitation at sampling sites cannot be
estimated. Precipitation is thus omitted from most of the calculations. Temperatures and precipitation decrease towards the
southeastern Altai, whereas the annual temperature amplitude
increases.
Although no sufficient data on precipitation are available for
most of our plots, moisture preferences of snails may be estimated in an indirect way. It may be assumed that plant communities reflect the moisture of a given site, because plant
species track habitats (Ackerly, 2003). However, this tracking is
not perfect because of the more or less wide ecological amplitude of the species. It is commonplace that plant species may
be indicators of local conditions, e.g. moisture conditions and
nutrient supply. According to their optima they may be
assessed as indicators. In a given plot with a definite water
regime and species composition several plant species co-occur:
species whose optima almost perfectly match this place, but
also species whose optima do not perfectly match the local conditions. Averaging indicator values of all plants in a given
assemblage may thus provide an indirect measure of that community’s water regime. This method may not be useful for the
determination of the amount of precipitation at a given site,
but it may be used for comparisons of plots. Korolyuk (2006)
provides indicator values for Southern Siberian plants on a
scale from 0 (desert plants) to 100 (submerged water plants)
that were used for estimations of snail moisture requirements.
For each plot the average of the indicator values was calculated and subsequently used for ranking the vegetation units
along the moisture gradient. The average value of moisture at
a locality was then assigned to all snail species in this plot.
Across all samples the relative moisture preferences of each
snail species could then be calculated.
1999). The communities were named according to the nomenclature of Kuminova (1960).
Monthly means of temperature and precipitation, annual
precipitation, annual temperature and temperature amplitude
were analysed by principal component analysis (PCA) to
reveal correlated values that could be omitted from further
analyses (SPSS for Windows, 2004). Indicator species analysis
(ISA) is commonly used to detect characteristic species in
groups of sample units. This is based on their abundances and
constancy (fidelity) in the units. The method, as implemented
in PC-ORD (McCune & Mefford, 1999), was applied here to
identify snail species that were statistically significantly characteristic of regions and/or plant communities. The indicator
values were statistically tested with 5,000 Monte Carlo randomizations. Floristic and faunistic similarities among regions
were calculated with the Sørensen index on the transformed
presence/absence data.
RESULTS
Species richness and patterns of diversity
We recorded three new Pupilla species (Gastropoda,
Stylomatophora): Pupilla alluvionica and P. altaica from
Onguday and the Aygulakskiy Khrebet (Meng & Hoffmann,
2008) and P. seminskii from the Seminskiy Khebet (Meng &
Hoffmann, 2009b). Further, we confirmed the occurrence of
P. loessica Ložek in the Altai (Meng & Hoffmann, 2009a).
In total, we recorded 566 plant species and 40 snail species in
the plots, the latter with a total of 2,278 individuals
(Supplementary material Tables S1 –3). For each organism
group about half of the species were recorded in only one of the
five regions. Plant species number and number of unique snail
species are positively correlated with the number of plots
sampled per region ( plants: n ¼ 5, Pearson’s correlation
coefficient ¼ 0.966, P ¼ 0.007; snails: n ¼ 5, Pearson’s correlation coefficient ¼ 0.92, P ¼ 0.027). This indicates that
additional rare species may be expected. To address this issue,
rarefaction plots with ‘occurrences’ as abscissa were calculated
to standardize comparisons of snail and plant species richness
(Gotelli & Colwell, 2001; Pfeiffer, Chimedregzen & Ulykpan,
2003). If the graphs reach an asymptote as numbers of samples
increase, it may be assumed that the region is exhaustively
sampled. This saturation was only obtained for the Saylyugem,
both for plants and snails. At the sample size of eight plots (the
number of plots at Onguday, the lowest number among the five
regions), species richness may be estimated from the rarefaction
diagram and compared among the regions (Table 2). Species
richness is highest at Onguday for plants and Aygulakskiy
Khrebet for snails. The species number ranks obtained from
rarefaction and observation are congruent; the ranks from estimates of the Michaelis– Menten equation (MMMeans,
Table 2) agree largely with the others. Species richness of
plants and snails among the regions are not correlated (n ¼ 5,
Pearson’s correlation coefficient ¼ 20.089, P ¼ 0.887).
Data collection and statistical analysis
We sampled at different numbers of sites in each region
(Table 1). We characterized each site as forested or nonforested. At each nonforested site we recorded vegetation and
snail species composition in a single 16 m2 plot. At each
forested site we recorded plant species in a 100 m2 area to get
an adequately representative sample of the vegetation, while
snails were collected in the centre of this area in a 16 m2 plot.
In total we analysed 111 plots in the five regions. Occurrences
and abundances of the plants were recorded using the Londo
scale (Dierschke, 1994). Nomenclature of plants follows Flora
Sibiri (Krasnoborov et al., 1988 –1997). To sample snails, one
of us (S.M.) collected all snails he could gather in 30 min,
making the samples comparable across the study.
Species richness and other community parameters were estimated with the programs EcoSim 7 (Gotelli & Entsminger,
2001) and EstimateS (Colwell, 2006). Rarefaction curves
(Gotelli & Colwell, 2001) were produced to compare expected
with observed species richness of the five regions and to standardize comparisons among regions, because the number of
sites differed among regions. From the smoothed
species-accumulation curves, the species richness of each region
was estimated as the Michaelis–Menten mean (MMMean)
using EstimateS (Colwell, 2006). Clustering of species and nestedness were calculated with the program package prabclus
(Hennig & Hausdorf, 2007), an add-on package for the statistical software R (R Development Core Team, 2008). Significant
species clustering allows the inference of communities. Plant
communities were defined by cluster analysis of the plant
species data using the flexible beta method (b ¼ 20.25) with
the Sørensen similarity index (PC-ORD, McCune & Mefford,
Climatic gradient
The first three axes of the PCA explained 99% of the variance
of the climatic parameters obtained from the weather stations.
Most of the temperature and precipitation values are correlated. From the component plot we have extracted for further
analysis five climate variables that are widely separated and
are correlated only to a low degree: annual precipitation and
mean annual temperature, mean January and July temperatures, and annual temperature range (Table 1). This table
reveals the general climatic gradient of our sample area
(Fig. 1). Temperatures and precipitation decrease from
78
SNAILS AND PLANTS IN THE ALTAI
Northwest
(Korgonskiy Khebet) to the Southeast
(Saylyugem). Thermal continentality, in terms of the annual
temperature amplitude, increases in this direction.
Using the lapse rates of temperature and altitudes of the
plots allows inferences of the snail species distribution along
the thermal gradient of the Altai Mountains (Fig. 2). Pupilla
loessica and Vallonia tenuilabris are the species having their main
distribution in the areas with the most severe winter cold.
Judging from the main precipitation gradient in the Altai
these species also appear to be confined to the areas with driest
winters. In addition P. alluvionica, V. genesii and C. columella live
in the areas of coldest winter, although at least the latter two
species occur in a wider range. In conditions c. 208C warmer
during the winter P. seminskii occurs, along with those species
observed only in true steppe habitats, i.e. Gastrocopta theeli and
V. kamtschatica. Some species, like Perpolita harmmonis and
Novisuccinea altaica, occur in a wide range of winter temperatures, but seem to avoid the coldest areas.
The differences between the species with respect to July
temperatures are not as large as those for the winter temperatures. The winter temperatures span a range of about 20 K, for
summer most plots span a range of only about 7 K. With the
exception of G. theeli, Punctum pygmaeum and V. pygmaea that
were observed only in the warmest places, most species have
overlapping thermal niches between about 10 and 158C July
temperature.
The indicator value method for inferring moisture values of
the plots was validated by the vegetation communities.
Figure 3 shows the average moisture amplitude of the plant
communities. The ranking of the communities by the mean of
the species indicator values closely reflects the vegetation
change along the moisture gradient in the Altai Mountains
(Kuminova, 1960). The driest vegetation units are rocky true
and desert steppes followed by more mesic true steppes. The
communities with apparently most mesophilic species are
larch-Siberian pine communities, taiga, subalpine tall forb
Table 2. Summary statistics for plant and snail species richness and diversity.
Region
No. of plots
No. of
Rarefied plant
No. of local
No. of
Rarefied mollusc
No. of local unique
MMMeans
with
plant
species number
unique plant
mollusc
species number
mollusc species
(max. sample)
molluscs
species
(8 samples)
species
species
(8 samples)
molluscs
Korgonskiy Khrebet
9
145
135.6
53
16
15.1
4
26
Seminskiy Khrebet
12
146
117.4
31
13
12.4
1
20
8
153
153
62
15
15
3
37
Aygulakskiy Khrebet
22
203
109.7
59
27
17.1
9
41
Saylyugem
38
221
132.4
86
8
5.3
2
8
Total
89
566
291
40
Onguday
19
Figure 2. Distribution of the snail species occurring in more than one plot along the temperature gradient in the Russian Altai. Because of a high
autocorrelation of the monthly values January temperatures were chosen as representatives of winter conditions and July temperatures for summer
conditions. The species are sorted according to their median value: (the small horizontal line within the box plot). The box represents the
interquartile range (25th to the 75th percentile of the data), outliers (whiskers) and extreme values (open circles and asterisks).
79
M. H. HOFFMANN ET AL.
Figure 4. Relative moisture preferences of the snail species in the
Russian Altai, inferred from the mean indicator values of the plots
vegetation community. Species are sorted by the median. Species on
the left are those occurring in dry places, those of the right side were
found only at moist places (for further explanation, see text).
Figure 3. Indicator values of moisture for the vegetation communities
in the Russian Altai. Communities on the left are those from dry
places, towards the right side of the diagram moisture increases (for
further explanation, see text).
Table 3. P-values for clustering of species occurrences.
Considering
Not considering
geographical structure
geographical structure
Plants
0.001
0.001
Snails
0.838
0.826
Plants
0.001
0.001
Snails
0.628
0.649
Plants
0.001
0.001
Snails
0.199
0.209
Plants
0.037
0.015
Snails
0.517
0.522
Plants
0.024
0.024
Snails
0.179
0.157
Korgonskiy Khrebet
communities and willow communities along rivers. All other
plant communities rank between these two ends of the moisture gradient in our transect.
Most snail species span a wider range of moisture than vegetation types (Fig. 4). This is in accordance with the observation
that many snail species occur in different vegetation types. The
diagram reveals that many species appear to have quite similar
moisture requirements (species from P. seminskii to the right in
Fig. 4). Species in the most moist habitats are, for example,
V. geyeri, P. petronella and P. pygmaeum. On the left are species
able to deal with drier conditions although most also span a
wide moisture range. Species confined to the drier habitats are,
for example, Pupilla altaica and G. theelii. Pupilla loessica, P. alluvionica and V. tenuilabris appear in an intermediate position in the
moisture gradient; they may occupy dry habitats but are
seemingly missing in moist vegetation communities.
Seminskiy Khrebet
Onguday
Aygulakskiy Khrebet
Saylyugem
Characteristic snail species for the regions and plant communities
were not observed by a few spot checks (e.g. desert steppes and
vegetation types at the upper altitudinal margin of the vegetation). In contrast to plants, clustering of snail species was
not significant; there are too few species available (Hausdorf &
Hennig, 2007; Table 3). Therefore, no snail communities can
be inferred.
Only six plant species were found in all five regions: Bistorta
vivipara, Poa altaica, Galium boreale, Festuca ovina, Campanula glomerata and Thesium repens. Euconulus fulvus was the only snail
Clustering of plant species is significant within regions
(Hausdorf & Hennig, 2007; Table 3) allowing the determination of plant communities. Clusters at about 50% of the
information remaining (half of the objective distance function)
could easily be assigned to 21 vegetation types, which were
described by Kuminova (1960; for names see Fig. 3). We
sampled in all major vegetation units of the Altai with an
under-representation of those vegetation types in which snails
80
SNAILS AND PLANTS IN THE ALTAI
Figure 5. Distribution and abundances of some snail species in the vegetation types in the Russian Altai. The first columns indicate the regions in
that the plant communities were observed. The bars indicate the number of snail individuals observed in the vegetation communities. Note the
different scales. Abbreviations: Ko, Korgonskiy Khrebet; Se, Seminskiy Khrebet; On, Onguday; Ay, Aygulakskiy Khrebet; Sa, Saylyugem.
species observed in all regions, but it was most abundant at the
Aygulakskiy Khrebet. The abundances of different snail species
are not evenly distributed along our transect (Fig. 5). For
example, Fruticicola schrenki was observed in low abundance in
four regions (four to nine individuals each), but not in the
Saylyugem. Similarly distributed are Vertigo alpestris Alder or,
slightly less widely distributed, Vallonia tenuilabris and Perpolita
hammonis (Ström). Pupilla loessica is most abundant in the
Saylyugem, with occurrences in lower abundance also in the
Aygulakskiy Khrebet.
ISA was used to test the significance of mollusc species being
typical for either regions or vegetation communities (Table 4).
This table reveals the geographically structured distribution of
the vegetation communities along the transect. Some plant
communities are more widespread, for example the shrub
tundra community or rocky true steppes. Most of the other
communities are confined to one region, at least in our
sampling range. Five snails are characteristic for both region
and plant community. The most characteristic species,
Gastrocopta theeli and Vallonia kamtschatica, were found in tall
true steppes at Onguday, and P. loessica may be typical for the
continental region of the Saylyugem, where it was frequently
observed in rocky desert steppes and low true steppes, i.e.
rather dry vegetation types (Supplementary material Fig. S1).
Other species are either characteristic for a region (e.g. Vallonia
tenuilabris of the Saylyugem) or vegetation type (e.g. Pupilla
alluvionica of alluvions, Supplementary material Fig. S1).
biogeographical point of view, this disjunction between Central
Europe and Central Asia can be seen in several disjunct patterns
of other species that did not go extinct in Europe. For plants,
the most prominent examples may be Artemisia rupestris and
Carex obtusata, widespread species of Central Asia that still occur
in a few places in Europe (Meusel, Jäger & Weinert, 1965;
Hultén & Fries, 1986; Jäger, 1987). Among animals a similar
disjunct pattern is observed, for example, in the butterfly
Parnassius phoebus (Higgins & Riley 1978).
Snail and plant assemblages change considerably along the
gradient through the Russian Altai. With increasing distance
plant and snail communities become dissimilar, suggesting that
the species were sorted along the temperature and precipitation
gradient (Ackerly, 2003; Cameron & Pokryszko, 2004). Only a
few species were present in all regions. Some snail and plant
species, as well as plant communities, were observed only at
some sections of the gradient. Plant species numbers and plant
community numbers do not explain the species richness patterns for snails of our study area, in contrast to such explanations that have been reported for aquatic snail –plant
assemblages, New Zealand mollusc diversity or island faunas
(Costil & Clement, 1996; Barker & Mayhill, 1999; Triantis
et al., 2005).
Snails sometimes show coincidence with plant communities
in their distributions (e.g. Ant, 1969; Kralka, 1986; Barker &
Mayhill, 1999; Horsák & Hájek, 2003; Martin & Sommer,
2004; Horsák et al. 2007; but see Čejka, Horsák & Némethová,
2008). The ISA reveals some snail species that are significantly
characteristic of regions (comprising several plant communities
and a variety of habitats) as well as vegetation types. Most of
the observed snail species may thus cope with a variety of habitats. This may, however, only be possible around the species
environmental optima. At the Saylyugem, Pupilla loessica
occurs in almost all vegetation types from steppes to forest to
high mountain forb communities, although the snail assemblage including this species is most characteristic for steppes
(Supplementary material Fig. S1). In the adjacent region, the
Aygulakskiy Khrebet, this species appears restricted to only
one vegetation type (degraded places with former Siberian
pine forests). This may perhaps be an indication of an environmental optimum for P. loessica in the Saylyugem, where the
species is able to live in very different habitats. Outside these
DISCUSSION
Our samples contain a mixture of Eastern and Western
Eurasian plant and mollusc species co-occurring in the Altai
Mountains. For plants, Kuminova (1960) and Hoffmann et al.
(2001) have discussed the various geographical elements contributing to the high plant diversity of the Altai in comparison
with the lower species numbers of the surrounding areas
(Barthlott, Lauer & Placke, 1996). For the land snails a similar,
but less well-known pattern appears. We observed many
Western Eurasian species, like Euconulus fulvus and Vertigo alpestris, but also many Siberian and East Asian species, like Vallonia
kamtschatica, V. tenuilabris, Gastrocopta theeli and Lindholmomneme
spp. (Udaloi & Novikov, 2005; Meng, 2008, 2009). From a
81
Table 4. Significant results of the ISA for the snail species.
Korgonskiy Khrebet
Subalpine tall forb
Deroceras altaicum
communities
R52%, V31.4%
Shrub tundra
2
High mountain forb tundra
1
Seminskiy Khrebet
Onguday
Aygulakskiy Khrebet
Saylyugem
Total
3
3
1
6
4
5
(oceanic type)
Alpine meadows
3
Dark coniferous taiga
1
Logged secondary birch
2
3
1
3
5
forests
Rock formations
Pupilla seminskii
8
R25.0%, V 50%
Siberian pine forests
5
Tall true steppes
5
3
Gastrocopta theeli R50%, V98.6%,
V43.9%
Rocky true steppes
2
2
4
Pupilla altaica
V75%
Fruticicola
schrenkii
V52.2%
82
Willow communities along
1
2
3
rivers
Columella
columella
Cochlicopa
lubrica V15%
V30.4%
Valley spruce forests
5
5
Degraded places with
2
2
Succinella
oblonga V50%
former Siberian pine
forest
Oceanic alluvions
Cochlicopa lubrica
3
R18.2%, V51.3%
Larch-Siberian pine forests
V. geyeri R22.7%,
5
V47.6%
Meadow steppes
10
10
Continental alluvions
3
3
Low true steppes
10
10
High mountain forb tundra
14
14
8
8
Pupilla alluvionica
V56.3%
Pupilla loessica
V21%
(continental type)
Larch forests
Columella
columella
V12%
Rocky desert steppes
Pupilla loessica
5
R94.3%, V42.3%
Total
12
18
8
22
51
111
M. H. HOFFMANN ET AL.
Vallonia kamtschatica R43%,
Euconulus fulvus R20%
R28%
R29.9%
Lindholmomneme sp.
Perpolita petronella
climatic conditions, in a northwesterly direction, P. loessica
becomes much rarer and occurs only in restricted habitats.
Vallonia tenuilabris is very similar to P. loessica in its distribution
across the vegetation types and regions, although it was always
recorded in lower numbers than P. loessica. It also occurred
more frequently in alluvions. In the Saylyugem, V. tenuilabris
occurred mostly in open vegetation types like steppes, continental high mountain tundra and meadow steppes. At
Onguday and the Aygulakskiy Khrebet it was found almost
exclusively in forests bordering rivers, revealing also a narrowing of the habitat types that can be occupied. Perhaps the
species is at its distribution limit here. Other species have
broader amplitudes, like the infrequent Columella columella that
is also typical of Pleistocene deposits, and is to be found further
north also in other snail and plant assemblages. It shows a preference for moist Larix sibirica or Picea obovata forests and continental high mountain tundra. Euconulus fulvus, in contrast to
the above-mentioned species, seems not to have such a distribution centre and occurs more or less evenly throughout the
vegetation types and regions (with the exception of alluvions).
In forests of Europe it appears to be much more abundant
(e.g. Martin & Sommer, 2004; Hylander et al., 2005) than in
Central Asia.
A few snail species were identified as characteristic of particular vegetation types in our study area. For example,
Pupilla alluvionica is a typical component of river gravels
(alluvions). Oxyloma sarsii was observed only once in gravel
with loose meadow vegetation along alluvions. Cochlicopa
lubrica appears in the Altai to be characteristic of alluvions
and shrub communities along rivers (Supplementary
material Fig. S2). However, in Europe this species is very
widespread and occurs in a wide variety of mesic habitats
(Wäreborn, 1970; Kerney et al., 1983; Martin & Sommer,
2004; Čejka et al., 2008). Our study suggests that snails may
occupy a much wider range of habitats at their optima
than at the boundary of their distribution ranges, where
they become rare (Martin & Sommer, 2004) and are confined to certain vegetation communities.
Direct inferences about physical factors were only possible
for the temperatures as they could be calculated from the lapse
rates and plot altitudes. Most snail species span rather wide
ranges of temperatures although a few were observed to occur
only in a narrow thermal range (Fig. 2). This figure suggests
that in the Altai Mountains most species cannot live where
winter temperatures fall below 2308C. However, January
temperatures below –30 8C were only inferred for the
Saylyugem, where many of these species were absent. Because
precipitation declines towards this region it cannot be decided
if these species show a lower temperature limit or if precipitation becomes the limiting factor. Lower temperature limits
may, nevertheless, be surmized for P. pygmaeum, V. kamtschatica
and others that do not occupy the coldest places within an
area (whiskers in the box plots). On the other hand, species
like P. loessica, V. tenuilabris and P. altaica seem to show an
upper temperature limit. These species seem not to live in the
warmer places within some regions.
Regarding the moisture amplitudes of the snail species it
appears that most have wider amplitudes than for the vegetation types. This can also be inferred from the occurrences of
the species in different vegetation types. Most snail species
appear to have rather similar moisture requirements, as
inferred from their occurrence at higher relative moistures.
Nevertheless, the ranking of the species reveals different moisture requirements of snails in continental climatic conditions. It
is interesting that snails living in the overall driest area
(Saylyugem) are not necessarily the species living in vegetation
types of the driest places as inferred from the plant species
composition of the plots. For example, G. theelii and P. altaica
The columns refer to the regions and the rows to the vegetation types. Grey cells are the realized combinations of region × vegetation community that were observed in our study. The row and column totals refer to the
numbers of plots. If a snail species is a significantly characteristic species for region and vegetation community, it is printed in the centre of the table. If a snail species is typical either for a region or a vegetation type, it
is printed at the right or lower margin. The percentage values give the relative importance of the species for the region (R) or the vegetation type (V). Species in italics are those, which are significant for one region and
vegetation type, but also have a relatively high indicator value for another region or vegetation community.
R44.7%
R34.8%
R37.5%
R49.9%
Novisuccinea altaica
Perpolita hammonis
Vertigo pygmaea R15.3%
Euconulus fulvus
Vallonia tenuilabris
SNAILS AND PLANTS IN THE ALTAI
83
M. H. HOFFMANN ET AL.
were found in the relatively moist Onguday and Aygulakskiy
Khrebet in steppe habitats, but appear to be more drought
resistant than P. loessica that was almost exclusively observed at
the overall drier Saylyugem. This suggests that moisture
requirements of snails as inferred from plant species composition may reflect more finely their ecological amplitudes than
data from weather stations. Unfortunately, direct estimation of
the amount of precipitation from these data seems to be difficult. Calibrating local direct measurements of precipitation
within communities and subsequent regressions may be useful.
The observation that some snail species occur at their putative ecological optima within a wide range of vegetation types
brings some problems for palaeontological reconstructions.
Joint occurrences of snail species in the fossil deposits may not
reveal particular ancient vegetation types. For example, shared
occurrence of P. loessica, V. tenuilabris and others in the fossil
deposits reveals a vegetation of continental climates, i.e. steep
annual temperature amplitude, cold and dry winter, extensive
drought and high evapotranspiration. Whether steppes or
larch forests were the prevailing vegetation types can hardly be
inferred, perhaps only that a mosaic of these vegetation types
was present. In the Altai Mountains such a mosaic of continental vegetation types occurs presently within short distances.
How these vegetation types occur in extensive lowland areas
needs to be determined. Other frequent species of glacial
deposits, like Pupilla muscorum or Vertigo geyeri (Horsák et al.,
2007), are restricted to continental Siberian larch and Siberian
pine forest at higher elevations, perhaps serving as better indicators of vegetation types in continental climates. The high
indicator value may, however, result from a narrowing of the
distribution in our study area due to suboptimal conditions.
Therefore, these indicator values may only be applicable for
particular continental conditions. The combination of the
species with broad amplitudes under those environmental conditions and species that are locally restricted may, however, be
suitable for inferences on palaeoenvironments.
Horsák et al. (2010) for January temperatures in a range from
about 222 to 2178C. Figure 2 shows that we observed these
species mainly between 236 and 2348C with a few outliers
between 229 and 2268C. The higher temperatures recorded
in the other study may thus result from outpost occurrences of
these species. The study at the Saylyugem reveals that some
species may have their centre of distribution in distinctly colder
conditions during the winter, such as for example P. loessica,
V. tenuilabris and Columella columella. For the July temperatures
the differences between the studies are not that large, because
of the smaller temperature amplitude across the Altai
Mountains. Clearly, caution is needed in defining tolerance
ranges from limited studies.
Horsák et al. (2010) indicated widely overlapping ranges of
precipitation for the seven index species, that do not differentiate among their particular requirements. Using our indirect
measurement of moisture requirements, some species were also
shown to have rather similar niches, e.g. P. loessica and V. tenuilabris. Although overlapping with these two species, C. columella
and V. genesii seem both to prefer vegetation types of moister
conditions. This differentiation was not discernable from the
range of the precipitation and may point to the importance of
microclimate.
For many other environmental variables the ranges in which
the index species occurred were also reported by Horsák et al.
(2010). Five out of 24 environmental variables were most
useful for the classification tree of the snail species (January
temperature, habitat type, transmitted diffuse radiation, shrub
cover, annual precipitation). In this scheme some of the index
species are scattered along the branches. For example,
P. loessica and V. tenuilabris occur in four out of seven terminal
branches. Only P. alpicola is confined to one branch. We used
an ISA to reveal typical snail species for vegetation types and
regions. Among the index species P. loessica is typical for the
most continental region (Saylyugem) and, to a lesser degree,
for two dry steppe types (rocky desert steppe and low true
steppe). Vallonia tenuilabris is also typical for the most continental region, but not significantly characteristic of a particular
vegetation type. Columella columella is more widespread and
characteristic for willow communities along rivers, which are
among the most moist vegetation types in our samples, as well
as for larch forests that are drier. This species thus lives in significantly more moist conditions than the former two species.
The ISA reveals also the indicator value of other species frequently found together with P. loessica and V. tenuilabris in the
fossil deposits, like Vertigo pygmaea, Euconulus fulvus and Succinella
oblonga. These may point, beside the index species, to a vegetation mosaic in the palaeo-landscapes. Due to the steep climatic gradient and relief diversity in the Altai Mountains the
species characteristic of different vegetation types can occur
close together. How this vegetation mosaic looked in the periglacial landscapes of European lowlands, which led to the joint
deposition of snails presently not living together, remains enigmatic. Perhaps small climatic fluctuations not resolved in the
fossil record have led to this pattern.
In summary, snail species have the potential to be excellent
indicators of ancient large-scale environments (e.g. Rousseau,
1991, 2001), but their contribution requires very careful evaluation. The joint occurrence of many species from the European
Pleistocene in the Altai Mountains and surely also in adjacent
areas of Middle and Central Asia makes this area suitable for
further studies of analogues of European glacial landscapes.
Comparisons of snail studies in the Altai Mountains
Two independent studies have dealt with snail distributions in
the Altai Mountains and their correlation with environmental
conditions; Horsák et al. (2010) were concerned only with the
factors affecting seven species indicative of periglacial conditions in Central Europe; our study encompasses all species
found. The sampling schemes differed between the two studies.
Horsák et al. (2010) sampled more in the Northern and
Central Altai with spatially scattered sites, whereas we focused
on four regions that were sampled more in detail. We had also
the opportunity to study snail distributions in the most continental part of the Altai Mountains (Saylyugem), a region
probably crucial for the understanding of European fossil snail
assemblages. Here, we observed the centre of distribution and
highest abundances of P. loessica, V. tenuilabris and V. genesii,
but also a high abundance of C. columella which is more widespread across the Altai Mountains. Other species frequently
found in fossil assemblages together with the above-mentioned
species, like P. hammonis and Vallonia costata, could not be
observed in the most continental part of the Altai Mountains,
which makes this region valuable for palaeontological
reconstructions.
Horsák et al. (2010) provided much environmental information on ranges within which the seven index species occur.
In our study we focused on thermal conditions and indirect
estimations of moisture requirements. The box plots for the
January and July mean temperatures shown in Figure 2
display the same trend, but the widespread of values indicates
that caution is required in interpreting simple ranges of temperature. Pupilla loessica and V. tenuilabris were reported by
SUPPLEMENTARY MATERIAL
Supplementary material is available at Journal of Molluscan
Studies online.
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ACKNOWLEDGEMENTS
We are very grateful to Alexander I. Shmakov for his help and
support in organizing the expedition. Many thanks for
Mischa’s continuous help during the field trip. Igor Volkov
(Tomsk) and Nikolas Prechtel (Dresden) helped to gather the
climate data. Karsten Wesche (Halle) and Christian Hennig
(London) helped with the statistical analyses. Many thanks to
Dietmar Brandes (Braunschweig) and Klaus-Dieter Jäger
(Berlin) for their encouragement to conduct this study. The
German Academic Exchange Programme (DAAD) supported
the field work.
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