Data on terrestrial snail species composition and abundance were obtained for 17 islands in the central part of lake Mälaren, Sweden in 1981 (Nilsson et al. 1988). The islands are located within an area of approximately 1062 km2, they have been formed by land uplift and are, depending on island height, 1000–4000 years old. They are covered with mature unmanaged forest, and their edaphic conditions are heterogeneous with the proportion of morainic soil, exposure of bedrock and sediments varying among the islands (Fig. 1). Some islands (mostly smaller ones) are part of an esker ridge (Högholmen, Hargen, Grävlingen, Benklädet, and Räfsgarn) with a more lime-rich, coarse-grained soil that is highly permeable (Kers 1978). The islands differ in size, distance to the mainland, habitat diversity, plant diversity, amount of deciduous and coniferous forest, and tree cover, creating several environmental gradients that influence land snails (Nilsson et al. 1988).
Figure 1. (A) The smallest island, Benklädet (0.7 ha), covered with mixed deciduous forest. (B) Scree in mixed deciduous forest on the island Alholmen (9.4 ha). (C) The snail Helicigona lapicida on Alholmen. (D) Snail sampling square (0.1 m2) showing how the litter and uppermost soil layers were collected. The material was placed in plastic bags, brought to the laboratory, dried and sieved, after which snails were extracted by hand sorting.
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On each island, ground-living snails were sampled on five occasions from May to September 1981. Both living and recently dead snails (empty fresh shells) were collected because empty shells represent individuals from the year of the sampling or the year before (due to rapid decomposition older shells are not present) and can therefore be considered to represent the current community. The snails were sampled by collecting litter and the uppermost soil layer from five to seven randomly placed 0.1 m2 squares within 10 × 10 m plots. The counts from each small square were lumped together to give one count per species for each plot. The number of plots (10 × 10 m) on the islands varied from one on the smallest islands to four on the largest ones (see Table A9 in the supplementary material and Nilsson et al. 1988 for more details on the sampling). The litter samples were dried at 50°C, and the snails were hand-sorted after sieving (Nilsson et al. 1988). Slugs (nonshelled Gastropods) were not included in the sampling campaign, because they could not be sampled adequately with the same methods that were used for the sampling of shelled snails. In total, 33 snail species were found (Appendix S1, Table A1). The number of species found per island ranged from 9 to 26. A jackknife estimate of the number of species revealed that on average, two species per island were not included in the samples (see Nilsson et al. 1988). As our trait analyses are based on abundance-weighted trait values, missing a few rare species should not influence our results.
Selection and use of traits
Trait information was taken from a database of shelled snails containing information on traits ranging from macro- and microhabitat occurrences to physiological and biological traits of 270 European snail species (Falkner et al. 2001). To our knowledge, this is currently the most comprehensive collection of trait data available for snails. The database also comprises information on the potential range of the trait values within species. Even though traits such as shell size or shape may vary under different environmental conditions, the difference in trait values for the traits we selected is larger between species than within species, which justifies the use of such published traits in our analysis.
From the species present in the former study, we excluded Succinea sp. because it was not determined to species level. For the remaining species, we selected traits that are related to dispersal, environmental tolerance, and niche differentiation (Table 1).
Dispersal ability and abiotic environmental conditions both can lead to a reduction in trait range (i.e., trait underdispersion). Together they determine whether a species can colonize an island, because to be present a species should have to be both able to reach the island, and have the right set of traits to be able to survive the abiotic conditions. Important traits here are dispersal traits, tolerance traits and habitat occurrences (reflecting the environmental conditions needed for survival). During the establishment phase, traits related to reproduction can also be important.
Large-bodied snail species are often found to be more mobile and better dispersers (Sutherland et al. 2000; Brouwers and Newton 2009). However, snails are poor active dispersers (Schilthuizen and Lombaerts 1994) and even larger species, such as Arianta arbustorum, Cepaea nemoralis, or Cepaea hortensis do not disperse more than 12–86 m per year (Day and Dowdeswell 1968; Baur and Baur 1993). Instead, passive dispersal or accidental dispersal by birds has been suggested as the main dispersal mechanism for terrestrial snails (Schilthuizen and Lombaerts 1994; Gittenberger et al. 2006). In case of passive dispersal, small-bodied species may be more easily dispersed (Hausdorf 2000). Indeed, small shell size has been recognized as a dispersal trait for terrestrial snails (Vagvolgyi 1975). Apart from shell size, there is hardly any information available on which traits are related to the dispersal ability of snails (but see Baur 1991 for intraspecific influence of life history traits on range expansion). Studies from various animal groups suggest that species with high reproductive potential, for example, number of offspring (Stevens et al. 2012), broad tolerance to abiotic conditions (Martin and Sommer 2004), and generalist species (Baur and Bengtsson 1987; Jocque et al. 2010) are more likely to successfully establish a population on an empty site; hypotheses related to the classical idea of r-selected species (MacArthur and Wilson 1967). Humidity is an important abiotic factor influencing abundance and diversity of snails (Martin and Sommer 2004). Hence, we included the traits humidity preference and tolerance to dry conditions. Shell size and shell shape could be constrained by environmental factors (Schamp et al. 2010) and habitat structure (Cain 1977; Heller 1987) and are regarded as traits indicating environmental filtering (for detailed predictions see Table 1).
Diet (Bowers and Brown 1982), shell size (Chiba 1996; Lee and Silliman 2006), and shell shape (Cain and Cowie 1978; Cameron and Cook 1989) have been found to be involved in competition and niche differentiation. Therefore, if competition plays a major role, it is likely that communities exhibit overdispersion in those traits. Body size has been linked to niche partitioning via specialization on different resources (Bowers and Brown 1982). Shell shape is indicative of the preferred microhabitats (Cain and Cowie 1978; Cameron and Cook 1989), as snails with flat shells tend to prefer horizontal structured habitats such as litter, whereas elongated snails tend to prefer vertical surfaces (Cain and Cowie 1978) such as tree trunks. In addition, microhabitat occurrences reflect where the species prefer to live on a small scale, such as on trees, in the litter layer or on mosses. At this, small-scale species can potentially interact and compete which might lead to niche partitioning (for detailed predictions see Table 1).
We used the information in Falkner et al. (2001) to calculate average values for each species and trait. Each trait in the database consists of several categories wherein each entry describes the degree of association between a species and the trait category. The degree of association can take values from 0 to 3, with 0 defined as no association, one as weak association, two as moderate association and three as strong association to the respective category. This means that the categories are not always mutually exclusive, but have a fuzzy coding structure (see Appendix S1, Table A8.2 for an example). The number of reproduction periods was calculated by counting the occurrences in the corresponding main reproduction period categories within a year (Appendix S1, Table A8.1). As we did not use all the food-type categories present in the database due to redundancy among some categories, we could not keep the original scoring but converted the categories to a binary multichoice variable (Appendix S1, Table A4). The same was carried out for the ecosystem occurrence and microhabitat occurrence (Appendix S1, Table A5 and Table A6). For all other traits, we calculated a mean trait value from the fuzzy coded entries (see Appendix S1, Table A8b for an example). In the original data set, carnivorous and saprophagous species were grouped into one category. We separated this category into two new categories because carnivory and saprophagy are two different strategies. To the category “carnivorous,” we assigned species for which carnivorous behavior is reported in the literature (Taylor 1914; Rondelaud 1977; Badie and Rondelaud 1985). Of these, only Zonitoides nitidus is an efficient active predator (Rondelaud 1978). All other species in this category can be considered as facultative carnivores (Barker and Efford 2004). Also note that food niche breadth might be underestimated for some species because many macrodetritivores including snails do not eat primarily pure litter, but ingest the microbial biofilm attached to it as an important part of their diet (Hax and Golladay 1993).
Twelve environmental variables (Table 2) were used to test for a link between traits and environmental variables. The theory of island biogeography (MacArthur and Wilson 1967) considers island area and distance to the mainland to be two central factors affecting the number of species on an island. Those might also affect the functional richness and composition. Distance to the mainland is an isolation measure and affects the immigration rate, whereas area affects the probability of persistence, that is, extinction rate on an island. We also considered the distance to the next largest island as an additional measure for isolation. Land snail species richness has previously been found to be related to plant diversity (Barker and Mayhill 1999). As humidity has also been shown to be important for species richness and abundance of snails (Martin and Sommer 2004), we included a habitat wetness index based on indicator plants of the ground vegetation (Nilsson et al. 1988). In addition, we tested several environmental variables that might reflect habitat quality and heterogeneity (leaf dry matter content, basal area of deciduous trees, number of habitats per island, woody plant richness, location on esker ridge, and a measure for productivity based on indicator plants of the ground vegetation (Nilsson et al. 1988). Indices like the wetness and productivity index are based on indicator species as proxies for environmental variables. Therefore, they have limitations because species not always are found at their environmental optimum. However, these proxies may still give a good indication of major differences in humidity and productivity between islands, in the absence of more detailed information. Leaf dry matter content might be important for snails that feed on leaves or leaf litter. Leaves with a high LDMC are less palatable compared to leaves with a low LDMC. Average leaf dry matter content (LDMC; mg/g) of tree species was compiled from data gathered at 17 other forest sites around Lake Mälaren Sweden in 2008. At each site, 12 leaves from all species of trees and shrubs were collected in spring and autumn and LDMC measured in the laboratory following the guidelines from Cornelissen et al. (2003). Using data for each tree and shrub species, an average LDMC was calculated for each sampling plot on each island. The remaining variables were taken from Nilsson et al. (1988).
Table 2. List of environmental predictor variables included in the CWM-RDA and regression analysis. For more detailed description of the variables, see Nilsson et al. (1988).
|Environmental predictor variables||Range||Source|
|Island area [ha]||0.6–74.3||(Nilsson et al. 1988)|
|Distance to the mainland [m]||200–4050||(Nilsson et al. 1988)|
|Distance to the next largest island [m]||50–1650||(Nilsson et al. 1988)|
|Average tree cover [%]a||64.4–97.5||(Nilsson et al. 1988)|
|Woody plant richness||19–23||(Nilsson et al. 1988)|
|Number of habitats per islandb||2–7||(Nilsson et al. 1988)|
|Mean basal area of deciduous trees (BADT) [% of living basal area]||53.65–98.87||(Nilsson et al. 1988)|
|Productivity of ground vegetationc||0–14.70||(Nilsson et al. 1988)|
|Wetness index of ground vegetationc||0–29.70||(Nilsson et al. 1988)|
|Leaf dry matter content (LDMC) [mg/g]||259.7–312.1|| |
|Esker ridge||0 or 1|| |