Journal of Biogeography (J. Biogeogr.

) (2005) 32, 985998

ORIGINAL ARTICLE

Multi-scale altitudinal patterns in species richness of land snail communities in south-eastern France
bastien Aubry1*, Fre de ric Magnin2, Ve ronique Bonnet2 and Richard C. Se 1 Preece

Department of Zoology, University Museum of Zoology, University of Cambridge, Cambridge, diterrane en dEcologie UK and 2Institut Me oe cologie, U.M.R. 6116 du CNRS, et de Pale timent Villemin, Europole de lArbois, Ba Aix-en-Provence Cedex, France

ABSTRACT

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 southeastern France, the altitudinal patterns of both at different spatial scales. Location The study was conducted on ve calcareous mountains in southeastern France (Etoile, Sainte Baume, Sainte Victoire, Ventoux and Queyras). Methods Stratied sampling according to vegetation and altitude was undertaken on ve 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 dened as the number of species found within quadrats of 25 m2. Species richness is dened 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 inuence on species density. The altitudinal pattern of species richness varies depending on the spatial resolution of the study. At ne 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. Species density decreases logarithmically with increasing altitude. Above a critical altitudinal threshold, this decrease lessens below the rate seen in the rst 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

bastien Aubry, Institut *Correspondence: Se diterrane en dEcologie et de Pale oe cologie, Me timent Villemin, U.M.R. 6116 du CNRS, Ba Europole de lArbois BP 80, F 13545 Aix-en-Provence Cedex 04, France. E-mail: sa257@cam.ac.uk

2005 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi

doi:10.1111/j.1365-2699.2005.01275.x

985

S. Aubry et al.

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.

INTRODUCTION Species richness, dened 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-shaped relationship 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 integrated into a theoretical hierarchical framework (Whittaker, 1960; Allen & Starr, 1982; Blondel, 1995; Willis & Whittaker, 2002). Willis & Whittaker (2002), while stressing the necessity of 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 986

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 independent 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 distribution 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 specic 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 rst studied at the restricted scale of the quadrat (25 m2). At this scale, the inuence 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. METHODS 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 sampling strategy has been devised to cover the full altitudinal range available in the region. This strategy produces a composite
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

Multi-scale altitudinal patterns in land snail species richness 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 ` gre, 1950; Barbero et al., 1978; to those of the Alpine zone (Ne 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 stratied strategy related to altitude and vegetation structure. When available, at least three types of habitat (grassland, shrubland and woodland) 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 chosen a priori on a location map. Twentyve 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 the present 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.
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

987

S. Aubry et al. ground cover is described. Sampling of molluscan communities 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 gur (1976), similar to those described by Evans (1972), Puisse (1981, 1982) and Magnin (1991) were used to collect Andre 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 difculty of sampling. Five turves were taken for Sainte Baume, four for Etoile, four for Sainte Victoire, four for Ventoux, two (four halves) for Queyras. The snails collected were then identied 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 signicant 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 ve 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 description, the standard procedure proposed by Godron (1968) was employed. The values of the environmental variables were measured in the eld, 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 signicant effect on species density and are not included in the present results. This lack of signicance 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. 988 The environmental heterogeneity was calculated with a ShannonWiener index, rst applied by MacArthur (1965) to study the inuence 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 called p1, p2, p3,p4, p5 and p6, and the formula: SCH
6 X i1

pi ln pi

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 the number 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 ve 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 rarefaction, 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 xed number of samples is recorded. Simultaneously, nine richness estimators are computed from the observed richness and abundance (Colwell & Coddington, 1994; Gotelli & Colwell, 2001). RESULTS Eighty-seven species of land snails were recorded in the ve 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 difcult to interpret directly as the sampling effort between altitudinal gradients was uneven. The observation of the accumulation curves of the ve mountains (not shown here) suggests that more species would have been
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

Multi-scale altitudinal patterns in land snail species richness 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 ve mountains are pooled together the number of land snail species per quadrat decreases with increasing altitude (Fig. 2). When a regression curve is tted to model the relationship between altitude and species density, it appears that density does not 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 signicant 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 elevations. Similarly, species density from Queyras conforms well
Table 1 Equations and signicance of regression lines between altitude (x in m) and species density (y) for each of the ve mountains
Mountains Etoile Ste Baume Ste Victoire Ventoux Queyras Relationships y y y y y 29.406 ) 0.018x 18.816 ) 0.003x 18.307 ) 0.009x 19.945 ) 0.008x 7.644 ) 0.001x r2 0.2064 0.0175 0.1910 0.5353 0.0919 n 15 30 49 67 48 P 0.0889 0.4854 0.0017* 0.0000* 0.0362*

*Signicant relationships.

30

Species density

20

10

0 0 1000 Altitude (m) 2000 3000

Figure 2 Species density (per 25 m2) of land snails vs. altitude for the ve mountains. Quadrats are distinguished by regions. Circles are for Provence and triangles for Queyras.
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

to the trend observed for the four other mountains. However, the logarithmic model is actually composed of two geographical 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 Sainte Baume and Sainte Victoire, where some quadrats at midelevation 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. Conversely, some quadrats are particularly species poor, independent 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 signicantly between classes of 5 mean annual temperature (ANOVA, F203 32:5, P < 0.0001). The mean species density of a class of mean annual temperature is always signicantly different from that of the second class of temperature next to it, and often signicantly different from that of the class next to it (LSD and Tukey HSD post hoc tests, 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, with rocks, 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 ve species. This sample came from dry managed woodland of Quercus ilex with 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 989

S. Aubry et al. 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 signicant (r2 0.66, n 29, P < 0.001). This certainly inuences 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 (samplebased 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 rst 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 midaltitudinal 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 extrapolation 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 based on 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 advantageous 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.
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

16

Mean species density

12

<4

47

79

911 1112.5 12.514

Mean annual temperature (C)

Figure 3 Mean species richness of land snails per quadrat for each class of mean annual temperature (C) derived from regional climatic maps. Error bars show 95% condence intervals of mean species richness per quadrat.

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 ve 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 signicant, 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 signicant rst explanatory variable only for Etoile and Ventoux (r2 0.52 and 0.07, respectively). On Etoile, species density is therefore mainly inuenced by the heterogeneity of the soil cover. On the three other Provenc al mountains, it is the interaction of altitude and SCH that governs species density. On Queyras, species density per quadrat 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 rst 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 rst 990

Multi-scale altitudinal patterns in land snail species richness

Table 2 LSD and Tukey HSD post hoc tests

(I) code temperature <4

(J) code temperature 47 79 911 1112.5 12.514 <4 79 911 1112.5 12.514 <4 47 911 1112.5 12.514 <4 47 79 1112.5 12.514 <4 47 79 911 12.514 <4 47 79 911 1112.5

Mean difference (I ) J) )1.9321 )5.5095 )7.9544 )11.0169 )10.8919 1.9231 )3.5864 )6.0313 )9.0938 )8.9688 5.5095 3.5864 )2.4449 )5.5074 )5.3824 7.9544 6.0313 2.4449 )3.0625 )2.9375 11.0169 9.0938 5.5074 3.0625 0.1250 10.8919 8.9688 5.3824 2.9375 )0.1250

SE 1.0627 1.0458 0.9091 1.0627 1.5689 1.0627 1.0842 0.9531 1.1005 1.5948 1.0458 1.0842 0.9342 1.0842 1.5836 0.9091 0.9531 0.9342 0.9531 1.4969 1.0627 1.1005 1.0842 0.9531 1.5948 1.5689 1.5948 1.5836 1.4969 1.5948

Signicance, Tukey HSD 0.459 0.000* 0.000* 0.000* 0.000* 0.459 0.012* 0.000* 0.000* 0.000* 0.000* 0.012* 0.093 0.000* 0.009* 0.000* 0.000* 0.093 0.017* 0.364 0.000* 0.000* 0.000* 0.017* 1.000 0.000* 0.000* 0.009* 0.364 1.000

Signicance, LSD 0.072 0.000* 0.000* 0.000* 0.000* 0.072 0.001* 0.000* 0.000* 0.000* 0.000* 0.001* 0.010* 0.000* 0.000* 0.000* 0.000* 0.010* 0.002* 0.051 0.000* 0.000* 0.000* 0.002* 0.938 0.000* 0.000* 0.001* 0.051 0.938

47

79

911

1112.5

12.514

*Signicant differences of species density between classes of temperature at the 0.05 level.

DISCUSSION The Mediterranean Basin is one of the worlds major centres for plant diversity, comprising 10% of the higher plants within dail & Que zel, 1997). It is also only 1.6% of its total surface (Me 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, zel (1997, 1999). However, with 87 dened by Medail & Que 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 dail & Que zel, 1999; Tzedakis of exchange and speciation (Me 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 mountains), and the southern part of the present study area in
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

particular, was also free of ice and outside the zone of , 2000). This ensured that the area permafrost (Van Vliet-Lanoe remained favourable for many species. Indeed, not only have land snails survived through the Quaternary in the surroundings 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 ndings of Magnin (1991) from Mont Ventoux. On a wider scale, the logarithmic shape of the relationship between species richness per quadrat and 991

S. Aubry et al.
Etoile
10.00

Ste Baume

Ste Victoire

Residuals

0.00

10.00

Ventoux
10.00

Queyras

0.00

10.00 0.50 1.00 1.50 0.50 1.00 1.50

SCH

SCH

Figure 4 Relationships between the heterogeneity of the soil cover (SCH) and species density of land snails represented by the residuals of the logarithmic model of regression between species density and altitude. Regression lines are tted: 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.).

Residuals

Figure 5 (ac) Species richness of land snails per segment of altitude for three different 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.

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 reect a climatic threshold above which species 992

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.
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

Multi-scale altitudinal patterns in land snail species richness

(a) 60

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50

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100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800

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Samples

Individuals

Figure 6 Land snail species numbers estimated by repeated and averaged sample-based rarefaction curves without replacement for each altitudinal belt of 100 m. The results shown are limited to the rst 1800 m. (a) The x-axis is the number of accumulated samples; the 200 m curve is above all others. (b) The x-axis is re-scaled to individuals; the 600 m curve now lies above all others and the 200 m curve now is in sixth position after 300, 400, 500, 600 and 700 m. Table 3 Observed species richness (Sobs) and values of nine species richness estimators calculated for a selected number of samples (10) and for a selected number of individuals (8000) for several altitudinal classes
Altitude (m) 10 samples 200 400 500 600 700 800 900 1000 1100 1400 8000 individuals 200 300 400 500 600 700 900 1000 1100 Sobs ACE ICE Chao1 Chao2 Jack1 Jack2 Bootstrap MMRuns MMMean

52.12 48.96 44.61 51.34 44.6 41.07 38.88 33.7 37.64 30

54.03 53.21 46.45 52.42 46.17 45.14 41.5 40.08 39.54 34.01

59.64 57.93 51.62 62.05 56.72 62.81 48.15 38.32 48.49 40.8

54.93 51.04 47.69 53.77 45.83 47.42 41.4 38.84 38.22 35.63

66.07 55.15 52.76 63.35 59.17 72.67 52.37 37.84 53.28 41.28

62.53 59.6 53.9 64.26 57.29 56.88 49.37 40.61 49.39 41.7

66.91 62.09 56.9 70.01 63.21 66.45 54.52 42.16 56.22 47.83

57.06 54.33 49.22 57.53 50.54 48.03 43.76 37.26 42.93 35.35

60.97 62.08 56.04 70.93 62.78 64.44 52.72 45.33 65.09 70.63

60.05 58.46 54.7 66.82 57.72 55.98 48.85 42.91 50.07 50.18

41.54 41 48.96 44.61 54 44.6 36.31 32.92 37.64

43.37 42.62 53.21 46.45 54.83 46.17 38.91 38.41 39.54

54.47 45.43 57.93 51.62 64.48 56.72 45.93 37.96 48.49

44.24 42.88 51.04 47.69 56 45.83 38.87 37.68 38.22

53.35 46.76 55.15 52.76 71.71 59.17 48.34 37.31 53.28

52.38 48 59.6 53.9 67.75 57.29 46.54 40.12 49.39

55.97 51.43 62.09 56.9 76.46 63.21 50.95 41.68 56.22

46.83 44.36 54.33 49.22 60.22 50.54 41.17 36.62 42.93

64.28 50.25 62.08 56.04 69.69 62.78 56.91 46.24 65.09

58.54 48.48 58.46 54.7 67.3 57.72 48.1 42.98 50.07

Altitude inuences many climatic variables, such that an increase in altitude leads to a decrease in temperature (mean annual, minimal, maximal), an increase in precipitation (rain and snow), a longer period of temperature below 0 C and a decrease in productivity. The speciesenergy relationship,
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

where an environment receiving a certain amount of energy can sustain a certain number of species, is thought to be an important factor in the explanation of the patterns (Gaston, 2000; Whittaker et al., 2001; Willis & Whittaker, 2002). Indeed, climate is a good predictor of species richness per 993

S. Aubry et al.
100

75

Estimators 50
ACE Bootstrap Chao1 Chao2 ICE Jack1 Jack2 MMmean MMruns

25

0 0 1000 2000 3000

Altitude (m)

Figure 7 Variation of estimated land snail species richness with altitude according to nine estimators using EstimateS v6.0 b1.

quadrat, but other factors, such as the heterogeneity of the environment or history, are also important at that scale of observation. Many studies have pointed to the signicance of environmental heterogeneity as one of the main explanations for species richness of various taxa such as birds (MacArthur, 1965; Blondel et al., 1973), freshwater molluscs (Harman, 1972) and lizards (Pianka, 1967), but almost no study includes land snail communities (Tews et al., 2004). Quadrats with a uniform structure harbour fewer species than quadrats with a diverse one. The effects of environmental heterogeneity are diverse. Principally, it increases the resource spectrum (habitat, food), therefore allowing different species to co-habit in a reduced space. It also allows the presence of species needing several micro-habitats to complete their life cycle. Environmental heterogeneity, often linked to patchiness (or spatial heterogeneity), can also lead to the coexistence of competing species when coupled to aggregative behaviour (Begon et al., 1996). No mid-altitudinal peak is observed, but the summits of Sainte Baume and Sainte Victoire are particularly interesting, as they show a wide range of species density, from the poorest to some of the richest quadrats. The particular conditions on these low altitude mountains, where the landscape is extremely heterogeneous, and where wooded quadrats are often only small patches of woodland in a mosaic of more or less high shrubs and grass, explain the high species richness occurring on the summits. This environmental heterogeneity is further increased by the rock structure, which forms cracks and provides many micro-habitats. These results suggest an inuence of the heterogeneity of the environment on the species density at a local scale. The results concerning the inuence of environmental heterogeneity on species density are consistent with the ndings of Labaune & Magnin (2002), who observed a decline in species density due to the environmental homogeneity caused by grazing on upland 994

grasslands, and a positive inuence of landscape heterogeneity on species density. The high species density on the ridges of Sainte Baume and Sainte Victoire, at 900 and 600 m, respectively, is explained by the extreme heterogeneity of these quadrats. However, it also results from the appearance at these altitudes of particular summit species, while lower altitude species are still present. Therefore, community overlap or an ecotone effect (Lomolino, 2001) is at least partly responsible for the observed pattern. It is noteworthy that the patterns for species richness (per altitudinal zone) and species density (per quadrat) observed for land snails show opposite trends to those observed by Terborgh (1977) or by Lee et al. (2004) for birds. Indeed, they found an overall decrease in species richness with increasing altitude, whereas species density showed a mid-altitudinal peak. Terborgh related the decrease in species richness (mainly that of insectivores and frugivores) to the decrease in foliage height diversity (ultimately linked to climate). For him, this decrease in heterogeneity leads to a decrease in the possibility of the partitioning of resources leading to a complex ecological cascade, in turn resulting in reduced species richness. He linked the peak in insectivore species density at mid-altitude to a peak in productivity. These results reect the importance of competition in the organization of bird species along the altitudinal gradient. For land snails, and for ectotherms in general, it appears that competition is not such an important factor in structuring communities but that these organisms are more sensitive to their abiotic environment (Hofer et al., 1999, but see Baur & Baur, 1990; Magnin, 1993). Indeed, as the present results suggest, climate and the opportunity to nd a suitable micro-habitat determine the number of species able to survive at one site and these show no peak at mid-altitude. Species richness Whereas in the previous section, the observed species richness per quadrat was considered the real species richness of the quadrat, it is likely that the recorded species richness for each altitudinal zone is only an approximation of its real species richness. The positive relationship between the number of species and the size of the area sampled is a fundamental pattern in ecology (Arrhenius, 1921). However, explanations for this relationship are still debated (MacArthur & Wilson, 1967; Connor & McCoy, 1979; Rahbek, 1997; Gaston, 2000; Whittaker et al., 2001; He & Legendre, 2002). In this study, area is used in two ways: (1) the area of the altitudinal belt, which decreases with increasing altitude, and (2) the area actually sampled from each altitudinal belt, which is directly related to the number of samples (each sample is 25 m2). The latter is an artefact linked to sampling effort that has to be taken into account when comparing the different altitudinal belts. The number of samples has three components. First, area per se has various ecological effects. Secondly, with a larger sample size more habitats are encountered and so more species are likely to be discovered. Thirdly, within a homogeneous habitat and independent of its actual area, an increased
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

Estimated species richness

Multi-scale altitudinal patterns in land snail species richness sampling effort is likely to yield more rare species. Unfortunately, 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 ve samples taken randomly within each 100 m altitudinal zone that decreases linearly with altitude. These results therefore validate on a larger scale (ve 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 per quadrat. 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 occupied 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 species richness along altitudinal gradient by using species altitudinal ranges (e.g. Sanders, 2002; Bhattarai et al., 2004; McCain, 2004). These ranges are dened 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, ination of species richness at midaltitude (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
Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd

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 conrm 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 ne resolution covering the full altitudinal gradient shows a mid-altitudinal peak in species richness (McCoy, 1990). CONCLUSIONS This baseline study on altitudinal patterns of land snail species richness on ve mountains in south-eastern France demonstrates that species density decreases logarithmically with altitude and that species richness peaks at mid-altitude. It also shows the difculty of determining precise patterns of richness. Indeed, this study, the rst large-scale analysis of land snail richness 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 heterogeneity 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, other rrez, 1997), the inuences, such as historical factors (Gutie 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). ACKNOWLEDGEMENTS The authors wish to thank Philip Roche and two anonymous referees for their constructive comments on a previous version 995

S. Aubry et al. of the manuscript. This work was supported by a European Union Training and Mobility of Researchers grant awarded to S. Aubry (contract no.: ENV4-CT98-5096). SUPPLEMENTARY MATERIAL The following material is available from http://www.blackwell publishing.com/products/journals/suppmat/jbi/jbi1275/ jbi1275sm.htm Appendix S1 Abundance of the 98 land snail species studied and number of samples where they occurred on each mountain in south-eastern France. Appendix S2 Species density (number of species per 25 m2) of land snails and altitude (m) for the 209 samples collected on the ve mountains in south-eastern France. REFERENCES Allen, T.F.H. & Starr, T.B. (1982) Hierarchy: perspectives for ecological complexity. Chicago University Press, Chicago. , J. (1981) Etude des peuplements malacologiques dune Andre ge tale post-culturale. Haliotis, 11, 1527. succession ve , J. 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S. Aubry et al. BIOSKETCHES bastien Aubry recently completed his PhD on the factors controlling the structure of land snail communities on limestone Dr Se mountains in south-eastern France at the Department of Zoology, University of Cambridge. He is now a post-doctorate researcher at diterrane en dEcologie et de Pale oecologie. His main research interest is the ecology of land snails. the Institut Me diterrane en dEcologie et de Pale oe cologie (CNRS, Marseille) working on the de ric Magnin is a researcher at the Institut Me Dr Fre ecology of both Recent and Quaternary land snails within the Mediterranean Basin. diterrane en dEcologie et de Pale oe cologie. Her main interest ronique Bonnet is a post-doctoral researcher at the Institut Me Dr Ve is community ecology, with a particular focus on the inuence 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

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Journal of Biogeography 32, 985998, 2005 Blackwell Publishing Ltd