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8/13/2019 Snails and Altitude South France
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O R I G I N A LA R T I C L E
Multi-scale altitudinal patterns in species
richness of land snail communities
in south-eastern France
Sebastien Aubry1*, Frederic Magnin2, Veronique Bonnet2 and Richard C.
Preece1
1Department of Zoology, University Museum of
Zoology, University of Cambridge, Cambridge,
UK and 2Institut Mediterraneen dEcologie
et de Paleoecologie, U.M.R. 6116 du CNRS,
Batiment Villemin, Europole de lArbois,
Aix-en-Provence Cedex, France
*Correspondence: Sebastien Aubry, Institut
Mediterraneen dEcologie et de Paleoecologie,
U.M.R. 6116 du CNRS, Batiment Villemin,
Europole de lArbois BP 80, F 13545
Aix-en-Provence Cedex 04, France.
E-mail: [email protected]
ABS T RACT
Aim Species richness is an important feature of communities that varies along
elevational gradients. Different patterns of distribution have been described in the
literature for various taxonomic groups. This study aims to distinguish between
species density and species richness and to describe, for land snails in south-
eastern France, the altitudinal patterns of both at different spatial scales.
Location The study was conducted on five calcareous mountains in south-
eastern France (Etoile, Sainte Baume, Sainte Victoire, Ventoux and Queyras).
Methods Stratified sampling according to vegetation and altitude wasundertaken on five mountains, forming a composite altitudinal gradient
ranging from 100 to 3100 m. Visual searching and analysis of turf samples
were undertaken to collect land snail species. Species density is defined as the
number of species found within quadrats of 25 m 2. Species richness is defined as
the number of species found within an elevation zone. Different methods
involving accumulation curves are used to describe the patterns in species
richness. Elevation zones of different sizes are studied.
Results Eighty-seven species of land snails were recovered from 209 samples
analysed during this study. Land snail species density, which can vary between
29 and 1 species per 25 m2, decreases logarithmically with increasing altitude
along the full gradient. However, on each mountain separately, only a linear
decrease is observable. The climatic altitudinal gradient can explain a large part
of this pattern, but the great variability suggests that other factors, such as
heterogeneity of ground cover, also exert an influence on species density. The
altitudinal pattern of species richness varies depending on the spatial resolution
of the study. At fine resolution (altitudinal zones of 100 m) land snail species
richness forms a plateau at altitudes below 1000 m, before decreasing with
increasing altitude. At coarse resolution (altitudinal zones of 500 and 1000 m)
the relationship becomes linear.
Main conclusions This study reveals that land snail species density and land
snail species richness form two different altitudinal patterns. Species density
exhibits strong variability between sites of comparable altitude. A large number of
samples seem necessary to study altitudinal patterns of species density. Speciesdensity decreases logarithmically with increasing altitude. Above a critical
altitudinal threshold, this decrease lessens below the rate seen in the first 1500 m.
Different methods exist to scale-up species density to species richness but these
often produce different patterns. In this study, the use of accumulation curves has
yielded a pattern of species richness showing a plateau at low altitude, whereas
simple plotting of known altitudinal ranges from single mountains would have
produced stronger mid-altitudinal peaks. This study shows that not only factors
Journal of Biogeography(J. Biogeogr.) (2005) 32, 985998
2005 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi doi:10.1111/j.1365-2699.2005.01275.x 985
8/13/2019 Snails and Altitude South France
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INT RO DUCT IO N
Species richness, defined as the number of species, is the
simplest way to describe communities at local and regional
scales (Magurran, 1988). The study of patterns of species
richness is pervasive in ecology and biogeography and it is well
established in the literature that increased altitude generally
results in reduced species richness in both plants and animals
(MacArthur, 1972; McCoy, 1990). However, two main
patterns have been documented, a monotonic decrease in
species richness with increasing altitude and a hump-shapedrelationship with a peak in richness at intermediate altitude
(Rahbek, 1995). Both patterns have been observed for species
richness per quadrat, also called species density, as well as for
the richness of an entire elevational zone (Lomolino, 2001).
The shape of the relationship depends on the taxa studied, the
latitude and the ecological conditions of the investigated area
(Sfenthourakis, 1992) but it also depends on the sampling
strategy, which can also lead to a biased description of the
pattern (McCoy, 1990). Furthermore, despite a large number
of publications (Rahbek, 1995) and the suggestion of several
explanatory hypotheses for these patterns (MacArthur, 1972;
Terborgh, 1977; Lawton et al., 1987; McCoy, 1990; Stevens,
1992; OBrien, 1993, 1998; Colwell & Lees, 2000; Gaston, 2000;
Lomolino, 2001), the effect of altitude remains controversial
(Stevens, 1992; Rahbek, 1995). Data, collected with adapted
methods, from new communities and new regions at different
levels are needed if the distribution pattern of montane taxa is
to be properly understood (Lomolino, 2001; Li et al., 2003).
Ecological factors and species interact at different scales in
space and time. At the same time, the scale of observation will
lead to the recognition of different factors and reveal different
patterns. These scales and factors therefore need to be integ-
rated into a theoretical hierarchical framework (Whittaker,
1960; Allen & Starr, 1982; Blondel, 1995; Willis & Whittaker,
2002). Willis & Whittaker (2002), while stressing the necessityof controlling area, highlighted the advantage of studying
diversity at different scales to reveal where in the continuum
particular factors have greatest relevance.
The distinction between species richness and species density
is rarely made in the literature although the shape of the
altitudinal pattern is strongly dependent on this difference
(Lomolino, 2001). The description of species density patterns
is relatively straightforward and usually results from the
measurements of species richness within plots along altitudinal
transects. However, by using only a few plots, this method
usually ignores the strong variability that exists between plots
at the same altitude (but see Lee et al., 2004). The description
of altitudinal patterns of species richness, supposedly inde-
pendent of the sampled area as well as of the actual area of the
elevation zone, is more complex. Indeed, species density is
often measured from only a few plots within a habitat type per
elevation zone and assumed to correspond to species richness
(e.g. McCoy, 1990). Classically, a second method, computing
species richness from the species elevation ranges, either
derived from the literature or from new sampling, is used to
scale-up to the richness of an entire elevation zone (e.g.Sanders, 2002; Bhattarai et al., 2004). Although the distribu-
tion of land snail species in France is relatively well known
(Kerney et al., 1999), the altitudinal distribution of most of
them has yet to be established, especially in the specific context
of the Mediterranean region. Furthermore, the use of such
species altitudinal ranges can produce spurious patterns of
richness (Zapata et al., 2003).
The main objective of the present study is to describe the
altitudinal patterns of both species density and species richness
of land snail species on the mountains of south-eastern France.
A large number of quadrats were sampled to take into account
the large variability of species density while controlling for
sampling effort and area (Whittaker et al., 2001; Lee et al.,
2004). In the present work, the relationship between land snail
species density and altitude is first studied at the restricted
scale of the quadrat (25 m2). At this scale, the influence of
habitat heterogeneity on the number of species is tested. An
attempt is then made to scale species richness up to the
landscape scale and to describe the patterns of the overall
number of species per elevation zones of different sizes.
M E T HO DS
Study area
This study was undertaken in south-eastern France, where
many of the mountains are not only composed of calcareous
bedrock, which supports thriving land snail communities, but
also cover an extensive altitudinal gradient from sea level to
elevations above 3000 m. Furthermore, the land snails of this
region are reasonably well known, in terms of distribution as
well as taxonomically, which provides a good foundation for
assessment of diversity, distribution and abundance. A samp-
ling strategy has been devised to cover the full altitudinal range
available in the region. This strategy produces a composite
such as temperatures and habitat heterogeneity, but also an ecotone effect, are
responsible for the observed patterns.
Keywords
Elevation gradient, France, land snails, Mediterranean mountains, rarefaction,
species accumulation curves, species density, species richness.
S. Aubry et al.
986 Journal of Biogeography32, 985998, 2005 Blackwell Publishing Ltd
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altitudinal gradient associating mountains with overlapping
altitudinal ranges. Five mountains were chosen from the
Etoile mountain range, bordering the Mediterranean, to the
Southern Alps region, 130 km inland (Fig. 1). Together, these
mountains cover an altitudinal gradient ranging from 100 to
3100 m a.s.l. and a southnorth distance of 200 km. Mean
annual temperatures range from 14 C at the base of the
southernmost mountain to below 4 C at the top of the
Queyras mountains (CNRS, 1970, 1972, 1975a,b). Similarly,
the number of cold months (T< 7 C) per year increases from
two to three at the base, to eleven at the summit, whereas the
number of dry months (P< 2T) decreases from three to none.
Consequently, altitudinal zones of vegetation range from plant
associations belonging to the Mediterranean vegetation zone
to those of the Alpine zone (Negre, 1950; Barberoet al., 1978;
Lavagne et al., 1984). Whereas the four southern mountains
are isolated and belong to the Mediterranean or Pre-alpine
biogeographical domain, the Queyras is situated within the
Alpine chain and belong to the Internal Alps biogeographical
domain (Ozenda, 1985).
Sampling strategy
Each mountain was sampled according to a stratified strategy
related to altitude and vegetation structure. When available, at
least three types of habitat (grassland, shrubland and wood-
land) were sampled per altitudinal zone of 100 m on each
mountain. In order to study and compare different sites, a
standardized sampling method was used. A standardized
sample of soil and litter, from an area of 25 m2, enables a
quantitative characterization of the malacological communities
from a variety of micro-habitats. Sampling undertaken
between March and November during three consecutive years
(1999, 2000 and 2001), led to the collection of 209 samples:
15 on Etoile, 30 on Sainte Baume, 49 on Sainte Victoire, 67 on
Mont Ventoux and 48 in the Queyras region. In order to
increase the number of samples, and therefore to have a better
image of the diversity at low altitude, samples collected during
an earlier study (Aubry, 2003) of the region of Auriol, a
lowland area between Sainte Baume, Sainte Victoire and Etoile
(Fig. 1), are included. During this earlier study, samples were
taken according to a systematic sampling strategy whereby
sampling sites were chosena priorion a location map. Twenty-
five samples aligned on a grid were taken between September
and October 1995. These sites covered an altitudinal gradient
between 220 and 750 m, and included all types of vegetation
from grassland to woodland. Eleven additional species were
recorded, leading to the recovery of a total of 98 species in thepresent work (Appendix S1).
Land snail sampling
Each sampling unit (hereafter referred to as a quadrat or site)
is a 5 5 m square taken from a habitat type for which the
Figure 1 Location map of southern France
showing sampling sites: Etoile, Sainte Baume,
Sainte Victoire, Ventoux and Queyras. One
other site from a previous unpublished study
is also included: Auriol. Land above 1000 m
a.s.l. shaded.
Multi-scale altitudinal patterns in land snail species richness
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ground cover is described. Sampling of molluscan commu-
nities in each quadrat was performed in two ways. First, a
visual search involving the collection of all living, fresh or old
dead snails, was undertaken for 30 min over the entire 25 m2
area. This involved searching beneath fallen logs and stones,
investigating crevices and under the bark of trees. Methods
similar to those described by Evans (1972), Puissegur (1976),
Andre (1981, 1982) and Magnin (1991) were used to collect
shells < 5 mm diameter. Vegetation, litter and surface soil
covering an area of 25 25 cm and a depth of 5 cm (turves)
were collected at different points within the quadrat, bagged
and brought back to the laboratory. There, samples were
dried in an oven (4075 C), then immersed in water.
Floating material was collected in a 0.5 mm mesh sieve and
dried again. The sieved samples were separated into four
fractions using a set of graded soil sieves (10, 2, 1 and
0.5 mm). Shells were then separated from plant material,
using a binocular microscope for the smallest fractions.
Different numbers of turves per quadrat were collected for
each mountain, depending on the difficulty of sampling. Five
turves were taken for Sainte Baume, four for Etoile, four forSainte Victoire, four for Ventoux, two (four halves) for
Queyras. The snails collected were then identified in the
laboratory and counted. The results presented here consider
the snails collected during both the visual search and the
turves analysis. The difference in number of turves per
quadrats on different mountains has not led to a significant
bias because similar results were obtained when only the
individuals collected during the visual search were examined.
A similar method was used at Auriol where five turves were
also taken. However, these turves were collected within a
400 m2 area (quadrats of 20 20 m). This difference in size of
the sampling units implies that these results cannot be
included in the study of species density.
Environmental records
Variables covering the entire range highlighted by Menez
(2002) as being relevant for the description of habitat of
molluscan communities were recorded. As regards site des-
cription, the standard procedure proposed by Godron (1968)
was employed. The values of the environmental variables were
measured in the field, except for soil pH (varying between 5.5
and 8.6) and CaCO3, which were measured in the laboratory
from soil samples. These two variables showed no significant
effect on species density and are not included in the presentresults. This lack of significance is not surprising in the context
of the present study which deals essentially with limestone
mountains where calcium is always present in a form available
for organisms and is therefore rarely a limiting factor. Altitude
was measured with an altimeter calibrated with a topographic
map (1 : 25,000). Mean annual temperatures were attributed
to each site according to the four climatic maps covering the
area (CNRS, 1970, 1972, 1975a,b). The percentages of ground
cover of the different variables were assessed with the help of a
visual chart and a ruler.
The environmental heterogeneity was calculated with a
ShannonWiener index, first applied by MacArthur (1965) to
study the influence of the diversity of foliage height on bird
species richness. The ShannonWiener index is used as follows.
For each quadrat the percentage of cover of six variables was
recorded: bedrock, boulder, stones, vegetation, leaf-litter and
bare soil. The proportion of these variables (sum 1) were
calledp1, p2, p3,p4, p5 and p6, and the formula:
SCH X6
i1
pilnpi
was used to compute the soil cover heterogeneity (SCH). This
index varies between 0, when only one component is present
and covers the whole quadrat, and 1.792 when the six
components are present and evenly distributed. In no case
(all mountains together or separately) is SCH correlated with
altitude but it is noticeable that the most heterogeneous sites
on Sainte Baume are found along its ridge.
Analyses
The patterns in species density are observed by plotting thenumber of species collected in each quadrat according to the
altitude of that quadrat. The scaling-up, from species density
(each quadrat) to species richness (altitudinal zones), is
achieved by grouping all the samples from a same range of
altitude into one unit. Therefore, this method also merges
different types of habitat and creates a composite landscape at
the regional scale. Three different scales of observations
(altitudinal classes) have been chosen to describe altitudinal
patterns: every 100, 500 and 1000 m. Species richness was
calculated for each of them, with all the samples from the five
mountains taken together, plus those of Auriol.
Randomized species accumulation curves (sample-based
rarefaction curves) were calculated using the EstimateS v6.0 b1
software (Colwell, 2000) for each altitudinal band of the three
scales of observation. Repeated, averaged sample-based rare-
faction, allows standardization of sampling by producing
smooth curves for comparison (Gotelli & Colwell, 2001).
Species richness of a random selection of a set number of
samples per altitudinal segment was computed. After 500
iterations of this randomization, a mean richness per
altitudinal segment for a fixed number of samples is recorded.
Simultaneously, nine richness estimators are computed from
the observed richness and abundance (Colwell & Coddington,
1994; Gotelli & Colwell, 2001).
RE S ULT S
Eighty-seven species of land snails were recorded in the five
mountain ranges (Appendix S1). The total number of species
on each mountain varied between 39 on Queyras, 47 on Etoile
and Sainte Victoire, 56 on Sainte Baume and 55 on Ventoux.
These differences are difficult to interpret directly as the
sampling effort between altitudinal gradients was uneven. The
observation of the accumulation curves of the five mountains
(not shown here) suggests that more species would have been
S. Aubry et al.
988 Journal of Biogeography32, 985998, 2005 Blackwell Publishing Ltd
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recovered if more samples had been taken. Indeed, when the
25 samples from Auriol are included, the number of species
increases to 98. However, the present study does not attempt
to obtain the complete list of species in the region but rather to
describe patterns using a sampling strategy with known
properties on the number of collected species. In the present
study, habitats such as riparian zones, human habitations, or
agricultural areas have been deliberately ignored, leading to an
under-representation of certain species. However, the results
concerning species density and the nature of the patterns
should nevertheless be of interest.
Species density
In the study area, species density ranges between 29 and 1
species per 25 m2. When all the individuals sampled in
quadrats (visual search and turves) from the five mountains
are pooled together the number of land snail species per
quadrat decreases with increasing altitude (Fig. 2). When a
regression curve is fitted to model the relationship between
altitude and species density, it appears that density doesnot decrease linearly but rather logarithmically (higher r2,
density )7.5 ln(altitude) + 63; r2 0.508; d.f. 207;
P< 0.0001).
When each mountain is examined individually (Appendix
S2), the relationships seem to be linear (Table 1). However,
this relationship is statistically significant only for Sainte
Victoire, Mont Ventoux and Queyras. The values of species
density correspond well between mountains. Species density
at the bottom of Mont Ventoux is comparable with that
occurring on the southernmost mountains at similar eleva-
tions. Similarly, species density from Queyras conforms well
to the trend observed for the four other mountains. However,
the logarithmic model is actually composed of two geo-
graphical components, Provence and Queyras. Species density
exhibits differences between these two regions; it decreases
linearly with altitude in both but has a much steeper slope in
Provence. On Mont Ventoux, the negative relationship
between species richness per quadrat and altitude is perfectly
linear whereas there is much more variability for SainteBaume and Sainte Victoire, where some quadrats at mid-
elevation yielded high species richness. In particular, species
density is surprisingly high on the ridges of Sainte Baume
and Sainte Victoire, at 900 and 600 m, respectively. Con-
versely, some quadrats are particularly species poor, inde-
pendent of altitude.
Mean annual temperature is strongly correlated with
altitude and can explain most of the relationship between
species richness and altitude (Fig. 3). Indeed, the mean species
richness per quadrat differs significantly between classes of
mean annual temperature (ANOVA, F5203 32:5, P< 0.0001).
The mean species density of a class of mean annual
temperature is always significantly different from that of the
second class of temperature next to it, and often significantly
different from that of the class next to it (LSD and Tukey HSD
post hoctests, Table 2).
Altitude or mean annual temperature are good predictors of
species richness but the wide range of species densities for
comparable altitudes or temperatures, and the overlap between
these classes, indicates that other factors must be operating.
The highest species richness per quadrat is found at 400 m
but outlier samples with extreme values of species richness are
also observed. Indeed, there is a structural component to the
species richness per quadrat. On Sainte Baume, the sample
with the greatest richness at high altitude is a woodland, withrocks, litter and different vegetation strata in a small valley
facing north, whereas lower altitude sites are mainly covered
with leaf-litter and harbour fewer species. Similarly, on Sainte
Victoire a quadrat at 435 m yielded only five species. This
sample came from dry managed woodland ofQuercus ilexwith
only one vegetation stratum and a uniform leaf-litter. On the
contrary, the site with the greatest richness, occurring at
740 m, is a diverse woodland in a humid valley. In general,
species richness per quadrat increases with an increased
heterogeneity of the soil cover (SCH). Once the effect of
0
10
20
30
0 1000 2000 3000
Altitude (m)
Speciesdensity
Figure 2 Species density (per 25 m2) of land snails vs. altitude for
the five mountains. Quadrats are distinguished by regions. Circles
are for Provence and triangles for Queyras.
Table 1 Equations and significance of regression lines between
altitude (xin m) and species density (y) for each of the five
mountains
Mountains Relationships r2 n P
Etoile y 29.406 ) 0.018x 0.2064 15 0.0889
Ste Baume y 18.816 ) 0.003x 0.0175 30 0.4854
Ste Victoire y 18.307 ) 0.009x 0.1910 49 0.0017*
Ventoux y 19.945)
0.008x 0.5353 67 0.0000*Queyras y 7.644 ) 0.001x 0.0919 48 0.0362*
*Significant relationships.
Multi-scale altitudinal patterns in land snail species richness
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altitude has been taken into account, inspection of the
residuals of the regression can highlight this other factor.
The residuals of the logarithmic model of regression between
altitude and species richness per quadrat of the five mountains
together were calculated and plotted against the SCH of the
corresponding quadrat (Fig. 4). After removal of the effect of
altitude, the positive relationships between species richness and
SCH are all significant, except for Queyras (Fig. 4). The results
are the same when the residuals of the quadratic model are
taken into account. These residuals are not evenly distributed
between mountains. It is clear that quadrats from Etoile and
Sainte Baume have a higher richness than those of the other
mountains at comparable altitudes, as residuals are mainly > 0
for these two mountains. When the effect of altitude is not
accounted for, SCH is a significant first explanatory variable
only for Etoile and Ventoux (r2 0.52 and 0.07, respectively).
On Etoile, species density is therefore mainly influenced by the
heterogeneity of the soil cover. On the three other Provencal
mountains, it is the interaction of altitude and SCH that
governs species density. On Queyras, species density perquadrat is consistently low and independent of altitude or
SCH.
Species richness
Land snail species richness decreases with increasing altitude
for the three scales of observation (Fig. 5ac). However, for the
first two of these scales (Fig. 5a,b), species richness forms a
mid-altitudinal peak or plateau between 200 and 900 m, and
then decreases. There are 85 snail species present in the first
1000 m. The maximum species richness for an altitudinal band
of 100 m is 58 species and occurs between 100 and 200 m.
When only three altitudinal classes are chosen (every 1000 m),
species richness decreases linearly from 85 to 30 species with
increasing altitude. However, species richness is strongly linked
to the number of samples collected within each altitudinal
class, which is also maximal at mid-altitude.
Not surprisingly, the positive relationship between number
of samples taken in an altitudinal zone and its recorded species
richness (not shown here) is highly significant (r2 0.66,
n 29, P< 0.001). This certainly influences the observed
patterns in Fig. 5ac. This effect is particularly relevant in the
present study, where more samples have been collected at low
and mid-altitude than at higher altitude. It might therefore
account for the strong decrease in species richness with
increasing altitude, as well as for the plateau at mid-altitude.
However, in those zones where the sampling intensity is
comparable, the effect of altitude is nevertheless observable as
the high altitude zones invariably support fewer species.
In order to overcome the bias linked to the number of
samples, randomized species accumulation curves (sample-based rarefaction curves) have been calculated using the
EstimateS v6.0 b1 software (Colwell, 2000). After this process,
species richness appears to decrease linearly for all scales of
observation (Fig. 5d,f), as the low richness of the first 100 m
certainly results from the small number of samples (i.e. n 1).
Another way to compare communities is to look at the
overall rarefaction curves. Inspection of these curves (Fig. 6,
Table 3) indicates more clearly a mid-altitudinal peak between
500 and 1000 m, as there is a strong overlap of curves when a
low number of samples is studied. Species richness is always
higher for the altitudinal belt between 100 and 200 m, but
richness at 600 m (500600 m) does not seem to have reached
its asymptote (Fig. 6a). When the curves are re-scaled for the
mean number of individuals per sample (Gotelli & Colwell,
2001), the picture changes radically (Fig. 6b) and this mid-
altitudinal peak is even more striking. For a comparable
number of individuals sampled, species richness becomes
higher in the 500600 m belt and that of the 100200 m
segment now falls into sixth position.
These interpolations allow a comparison of small samples
with the larger ones. An alternative approach is by extrapo-
lation via the statistical estimation of the real species richness
from the observed richness and abundance as described by
Colwell & Coddington (1994) and Gotelli & Colwell (2001).
These authors reviewed nine species richness estimators basedon the occurrence of rare species in collected samples. These
estimators had the advantage of reaching their asymptote
(estimated real richness) quicker than the accumulation curves
(maximal observed richness), therefore providing an expected
number of species with fewer samples. Despite this advanta-
geous property, the results are still dependent on the number
of samples taken into account. However, the plateau at low
altitude, or the hump-shaped curve with a peak at 600 m, were
more apparent (Fig. 7, Table 3), even with a small number of
samples for some estimators.
Mean annual temperature (C)
16
12
8
4
< 4 47 79 911 1112.5 12.514
Meanspeciesd
ensity
Figure 3 Mean species richness of land snails per quadrat foreach class of mean annual temperature (C) derived from regional
climatic maps. Error bars show 95% confidence intervals of mean
species richness per quadrat.
S. Aubry et al.
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DIS CUS S IO N
The Mediterranean Basin is one of the worlds major centres
for plant diversity, comprising 10% of the higher plants within
only 1.6% of its total surface (Medail & Quezel, 1997). It is also
a global hotspot for a large array of other taxa (Myers et al.,
2000). The region considered in this study does not belong to
one of the more local hotspots within the Mediterranean Basin,
defined by Medail & Quezel (1997, 1999). However, with 87
species of land snails recovered in 209 quadrats of 25 m2,
which increases to 98 species when the results of an earlier
study are included, this region is undoubtedly rich in species.This number is especially high when compared with the 279
species present in north-west Europe (area covered in Kerney
& Cameron, 1979). The high species richness of the
Mediterranean Basin is often explained by its Quaternary
history. The Mediterranean Basin is both a refuge and a place
of exchange and speciation (Medail & Quezel, 1999; Tzedakis
et al., 2002). The role of the Mediterranean peninsular regions
as refugia has long been recognized (Taberlet et al., 1998) but
during the last glacial stage, the whole basin (except moun-
tains), and the southern part of the present study area in
particular, was also free of ice and outside the zone of
permafrost (Van Vliet-Lanoe, 2000). This ensured that the area
remained favourable for many species. Indeed, not only have
land snails survived through the Quaternary in the surround-
ings of Marseille by shifting their altitudinal ranges accordingly
to climate, but there is also evidence that refugia for cold
intolerant snail species were also present in the area (Magnin,
1991; Pfenninger et al., 2003). Furthermore, this species
richness is explained by the variety of habitats encountered
in a small area due to the heterogeneity of the Mediterranean
landscapes and the elevational gradient.
Species density
The number of land snail species in a quadrat of 25 m2
decreases logarithmically with increasing altitude. This
decrease conforms to the general law observed for all kingdoms
in all environments (McCoy, 1990; Gaston, 2000). The linear
decrease in species richness per quadrat on each of the
mountains is consistent with the findings of Magnin (1991)
from Mont Ventoux. On a wider scale, the logarithmic shape
of the relationship between species richness per quadrat and
Table 2 LSD and Tukey HSD post hoc
tests (I) code
temperature
(J) code
temperature
Mean
difference (I ) J) SE
Significance,
Tukey HSD
Significance,
LSD
< 4 47 )1.9321 1.0627 0.459 0.072
79 )5.5095 1.0458 0.000* 0.000*
911 )7.9544 0.9091 0.000* 0.000*
1112.5 )11.0169 1.0627 0.000* 0.000*
12.514 )10.8919 1.5689 0.000* 0.000*
47 < 4 1.9231 1.0627 0.459 0.07279 )3.5864 1.0842 0.012* 0.001*
911 )6.0313 0.9531 0.000* 0.000*
1112.5 )9.0938 1.1005 0.000* 0.000*
12.514 )8.9688 1.5948 0.000* 0.000*
79 < 4 5.5095 1.0458 0.000* 0.000*
47 3.5864 1.0842 0.012* 0.001*
911 )2.4449 0.9342 0.093 0.010*
1112.5 )5.5074 1.0842 0.000* 0.000*
12.514 )5.3824 1.5836 0.009* 0.000*
911 < 4 7.9544 0.9091 0.000* 0.000*
47 6.0313 0.9531 0.000* 0.000*
79 2.4449 0.9342 0.093 0.010*
1112.5 )3.0625 0.9531 0.017* 0.002*
12.514 )2.9375 1.4969 0.364 0.051
1112.5 < 4 11.0169 1.0627 0.000* 0.000*
47 9.0938 1.1005 0.000* 0.000*
79 5.5074 1.0842 0.000* 0.000*
911 3.0625 0.9531 0.017* 0.002*
12.514 0.1250 1.5948 1.000 0.938
12.514 < 4 10.8919 1.5689 0.000* 0.000*
47 8.9688 1.5948 0.000* 0.000*
79 5.3824 1.5836 0.009* 0.001*
911 2.9375 1.4969 0.364 0.051
1112.5 )0.1250 1.5948 1.000 0.938
*Significant differences of species density between classes of temperature at the 0.05 level.
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altitude suggests that in this region, the 1500 m contour
constitutes a threshold above which species density declines
only slightly to the summit. However, it also seems that species
density behaves differently between two regions. In Provence,
the decrease is steep and linear with some variations depending
on the heterogeneity of the soil cover and on the number of
species present at any altitude. In Queyras, on the other hand,
the decrease is gentle and progressive. This difference is
thought to reflect a climatic threshold above which species
density remains relatively constant. Indeed, if Mont Ventoux
were a 1000 m higher, it is unlikely that no land snail species
would actually occur there. In fact, it is likely that the same few
species as those present from 1600 m would be found
continuously up to the summit. However, a biogeographical
pattern is also responsible for this regional difference, as alpine
species absent in Provence occur on Queyras along the entire
altitudinal gradient and contribute to the relative stability of
species density.
Etoile
Ventoux
SCH0.50 1.00 1.50
SCH
Residuals
Residuals
0.50 1.00 1.50
10.00
0.00
10.00
10.00
0.00
10.00
Queyras
Ste Baume Ste Victoire
Figure 4 Relationships between the hetero-geneity of the soil cover (SCH) and species
density of land snails represented by the
residuals of the logarithmic model of regres-
sion between species density and altitude.
Regression lines are fitted: Etoile (r2 0.45,
n 15, P< 0.01), Ste Baume (r2 0.21,
n 30, P< 0.05), Ste Victoire (r2 0.10,
n 49, P< 0.05), Ventoux (r2 0.12,
n 67, P< 0.01), Queyras (r2 0.05,
n 48, n.s.).
Figure 5 (ac) Species richness of land
snails per segment of altitude for three dif-
ferent scales of observation (100, 500 and
1000 m); (df) after random selection of
limited number of samples. Means for 5, 22
and 30 samples are chosen for classes of 100,
500 and 1000 m, respectively, when possible.
Circles are number of species and stars are
number of samples.
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sampling effort is likely to yield more rare species. Unfortu-
nately, these three components cannot be easily disentangled
and have to be considered together when studying the effect of
the number of samples.
The patterns obtained with a set number of samples also
refer to species density. Indeed, it is the species richness of five
samples taken randomly within each 100 m altitudinal zone
that decreases linearly with altitude. These results therefore
validate on a larger scale (five quadrats correspond to 125 m2)
the pattern obtained for quadrat of 25 m2. The intersection of
the accumulation curves indicates that the inspection of the
full curves is a better approach for comparing the species
richness from different elevational zones (Lande et al., 2000).
In that case a peak in species richness is suggested. On the
other hand, the rescaling of species richness per number of
individuals collected, recommended by Gotelli & Colwell
(2001) when comparing species richness, has two effects. First,
it transforms values of species density (number of species per
quadrat) into values of species richness (number of species
independent of the surface sampled). Secondly, by the same
process, it lowers the effect of number of soil samples perquadrat. In this case, species richness peaks, or at least forms a
plateau, at mid-altitude. The same is true for the estimators of
estimated real species richness.
The area of the altitudinal bands must also be taken into
account. The results obtained after rescaling per number of
individuals are dependent on the area of the altitudinal zone
where these snails were collected. In the broader sense these
results still refer to species density concept (Lomolino, 2001).
As no speciesarea curves for each altitudinal belt (cf. Rahbek,
1997) can be calculated, the effect of area per se cannot be
factored out of the relationship between altitude and species
richness. Nevertheless, knowing that area decreases with
altitude and has a positive effect on richness, it can be
suggested that species richness at low altitude is actually lower
than that at higher altitude. In the region, area decreases
linearly between 0 and 800 m, with the area occupied by the
600800 m belt approximately being two-third of that occu-
pied by the one between 0 and 200 m. This enhances the
possibility that, once the effect of area is removed, species
richness at low altitude is lower than it appears, when
compared with the higher belt.
The mid-altitudinal peak in species richness reported in the
literature is usually more pronounced than the one described
here. The method used here can explain this difference as the
result of two factors. First, other works might explore speciesrichness along altitudinal gradient by using species altitudinal
ranges (e.g. Sanders, 2002; Bhattarai et al., 2004; McCain,
2004). These ranges are defined by upper and lower elevation
limits of species, which are assumed to occur everywhere
within this range. This assumption, and the use of these ranges
to calculate species richness at different elevations, leads to an
automatic, but spurious, inflation of species richness at mid-
altitude (Zapata et al., 2003). Secondly, the use of several
mountains to describe the species richness pattern over the
entire gradient (from sea level to 3100 m), results in a wide
plateau (sum of smaller peaks at different altitudes), instead of
a strong peak.
The patterns observed for species richness depend on the
scale of resolution. McCoy (1990) argued that most studies
that had not found a mid-altitudinal peak in species richness
had used an inappropriate sampling regime. Our results seem
to confirm this suggestion, showing that studies with a coarse
resolution will tend to demonstrate a linear decrease in species
richness with increasing altitude (e.g. Mylonas et al., 1995),
whereas a fine resolution covering the full altitudinal gradient
shows a mid-altitudinal peak in species richness (McCoy,
1990).
CO NCLUS IO NS
This baseline study on altitudinal patterns of land snail species
richness on five mountains in south-eastern France demon-
strates that species density decreases logarithmically with
altitude and that species richness peaks at mid-altitude. It also
shows the difficulty of determining precise patterns of richness.
Indeed, this study, the first large-scale analysis of land snailrichness patterns with elevation, aided by a large number of
samples, shows the strong variation in species richness between
sites, as well as the importance of the choice of methods used to
describe them. Despite these problems, it seems that land snail
species richness genuinely does peak at an altitude between 500
and 900 m in montane regions of south-eastern France.
The present study attempted to describe altitudinal patterns
of land snail species richness without providing an explanation
of them. Species richness is controlled by a wealth of factors,
operating at different scales on individual species. Each of the
observed global patterns of species richness, themselves
dependent on the scale of observation, can be explained by
different factors, but no consensus has emerged about the
mechanisms involved (Gaston, 2000). These effects, sometimes
similar and sometimes divergent, can all take place at the same
time and it appears that no factor can be singled out to explain
the general pattern (Lomolino, 2001). Indeed, in the present
study, mean annual temperature and area have been shown to
be potential explanations, but at the restricted scale of the
quadrat it has also been shown that environmental heterogen-
eity is a factor responsible for low densities at low altitude or
high densities at high altitude. This is further increased by what
can be called an ecotone effect or community overlap on the
ridges of the lower mountains, where faunas with different
ecologies can meet in a single quadrat. Certainly, otherinfluences, such as historical factors (Gutierrez, 1997), the
extension of Rapoports rule to elevational gradient (Stevens,
1992) or the geometric effect (Colwell & Lees, 2000) have to be
studied and might also provide partial explanation for these
patterns (Sanders, 2002; Bhattarai et al., 2004).
ACK NO W LE DGE M E NT S
The authors wish to thank Philip Roche and two anonymous
referees for their constructive comments on a previous version
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B I O S K E T C H E S
Dr Sebastien Aubry recently completed his PhD on the factors controlling the structure of land snail communities on limestone
mountains in south-eastern France at the Department of Zoology, University of Cambridge. He is now a post-doctorate researcher at
the Institut Mediterraneen dEcologie et de Paleoecologie. His main research interest is the ecology of land snails.
Dr Frederic Magninis a researcher at the Institut Mediterraneen dEcologie et de Paleoecologie (CNRS, Marseille) working on the
ecology of both Recent and Quaternary land snails within the Mediterranean Basin.
Dr Veronique Bonnetis a post-doctoral researcher at the Institut Mediterraneen dEcologie et de Paleoecologie. Her main interest
is community ecology, with a particular focus on the influence of perturbations.
Dr Richard C. Preece is the Watson Curator of Malacology at the University Museum of Zoology, Cambridge. His main research
interest is malacology in general, but especially the use of non-marine Mollusca in reconstructing environments and climates during
the Quaternary (and Tertiary).
Editor: Robert Whittaker
S. Aubry et al.
998 Journal of Biogeography32, 985998, 2005 Blackwell Publishing Ltd