Invasive moss alters patterns in life-history traits and functional ...

Invasive moss alters patterns in life-history traits and functional diversity of spiders and carabids Jens Schirmel & Sascha Buchholz

Biological Invasions ISSN 1387-3547 Volume 15 Number 5 Biol Invasions (2013) 15:1089-1100 DOI 10.1007/s10530-012-0352-4

1 23

Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be selfarchived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”.

1 23

Author's personal copy Biol Invasions (2013) 15:1089–1100 DOI 10.1007/s10530-012-0352-4

ORIGINAL PAPER

Invasive moss alters patterns in life-history traits and functional diversity of spiders and carabids Jens Schirmel • Sascha Buchholz

Received: 18 April 2012 / Accepted: 19 November 2012 / Published online: 29 November 2012 Ó Springer Science+Business Media Dordrecht 2012

Abstract Invasive plants can modify terrestrial habitats and affect the natural faunal composition. In acidic coastal dunes the invasive moss Campylopus introflexus can form dense carpets that largely replace native vegetation. As shown in a previous study, moss invasion affects habitat structure and ground-dwelling arthropod diversity. We suggested that including the functional diversity concept in the analysis of moss invasion impacts may offer further insights. We used pitfall trap data to compare trait composition and functional diversity of spiders and carabids in (a) invaded, moss-rich (C. introflexus) and (b) native, lichen-rich (Cladonia spp.) acidic coastal dunes. Moss invasion induced shifts in the trait values body size and feeding preference (carabids) and hunting mode (spiders): Species were smaller in native sites, and the percentages of web-building spiders and phytophagous beetles

J. Schirmel (&) Biological Station Hiddensee, University of Greifswald, Biologenweg 15, 18565 Hiddensee, Germany e-mail: [email protected] Present Address: J. Schirmel Ecosystem Analysis, Institute of Environmental Science, University of Koblenz-Landau, Fortstraße 7, 76829 Landau, Germany S. Buchholz Department of Ecology, TU Berlin, Rothenburgstraße 12, 12165 Berlin, Germany e-mail: [email protected]

were reduced in invaded sites. Furthermore, moss invasion led to a more heterogeneous trait composition for spiders, and changed functional diversity of both arthropod groups, although with the opposite effects: While spiders were functionally more diverse in invaded sites, moss invasion reduced carabid beetles’ functional diversity. We also observed changes in the relationship between species richness and functional diversity that indicate a high functional similarity for spiders but a lower one for carabid beetles in native grey dunes. C. introflexus invasion not only alters the arthropod diversity and assemblage structure of endangered acidic coastal dunes but also interferes at a functional level. These results provide further insight into the way plant invasions might alter the structure and function of ecosystems. Keywords Araneae Campylopus introflexus Carabidae Functional dispersion Functional similarity

Introduction Invasions by alien plant species present a major threat to global biodiversity (Sala et al. 2000). At a large scale, plant invasion results in a homogenised flora, and at the community level, invasive plants often build dominant and homogeneous stands (Hejda et al. 2009) (although regional or local species richness can also be enhanced; Davis 2009). Alien plants modify terrestrial

123

Author's personal copy 1090

habitats due to their impact on plant diversity (KetnerOostra and Sykora 2004), vegetation composition (Mack and D’Antonio 2003; Hejda et al. 2009), microclimate conditions (Schirmel et al. 2011), nutrient cycles and soil conditions (Ehrenfeld 2003; Jordan et al. 2008; Weidenhamer and Callaway 2010). Consequently, invasive alien plants affect the natural faunal composition and food-web structures (Wolkovich et al. 2009; Litt and Steidl 2010; Pe´tillon et al. 2010). Effects of invasive plants on faunal components have been analysed for several taxonomic groups on a broad range of spatial scales. For example, smooth cordgrass (Spartina alterniflora) has a negative effect on specialised saltmarsh birds in China (Ma et al. 2010), carabid beetle assemblages are affected by giant knotweed (Reynoutria spp.) invasion in Germany (Topp et al. 2008), abundance and diversity of forest floor spiders are negatively affected by Vinca minor in the USA (Bultman and DeWitt 2008), and in riparian ecosystems in California (USA) the perennial grass Arundo donax has a negative impact on a broad range of invertebrate groups (Herrera and Dudley 2003). Even small-scale invasions can influence the native fauna, as shown for the invasion by the moss Campylopus introflexus in European acidic coastal dunes (grey dunes), which has a negative impact on ground-dwelling arthropods (Schirmel 2011; Schirmel et al. 2011). Besides effects on abiotic conditions and taxonomic components, invasions by alien species have an effect on functional diversity, for example by changing the composition of functional groups/guilds or life-history traits (Gratton and Denno 2006; Pe´tillon et al. 2006; Topp et al. 2008; Wu et al. 2009). Functional diversity is a key driver of several ecosystem functions such as productivity (Tilman 1997) or resilience against invasive species (Folke et al. 2004). Thus, invasive alien plants may change several ecosystem functions (D’Antonio and Vitousek 1992; Mack and D’Antonio 2003; Pritekel et al. 2006) and have strong impacts on ecosystem services (Villa` et al. 2010). In recent years, the functional diversity concept has expanded rapidly as a tool for analysing the functioning of ecological communities (Petchey and Gaston 2006; Violle et al. 2007; Mokany et al. 2008; II Choi et al. 2010). Functional diversity (FD) can be seen as a biodiversity component that reveals insights into functional interactions of organisms with their environment. FD therefore goes beyond traditional

123

J. Schirmel, S. Buchholz

diversity concepts that examine the taxonomic richness of species communities (Petchey et al. 2009) as it integrates life-history and functional trait information, e.g. morphological, phenological, and physiological characteristics (Violle et al. 2007). FD can be defined as the range, dispersion, and relative abundance of functional traits of organisms in ecosystems (Diaz et al. 2007) and can provide a useful approach to integrating biodiversity research into the broader context of ecosystem processes (Loreau 2010). In our study we focussed on the impact of the invasive moss species C. introflexus on the functional diversity of spiders and carabid beetles. C. introflexus originates from the Southern Hemisphere and is listed among the 100 worst invasive plant species in Europe (DAISIE project, http://www.europe-aliens.org). In nutrient-poor and acidic habitats it is able to alter habitat conditions by building homogeneous and dense carpets (Biermann and Danie¨ls 2001; KetnerOostra and Sykora 2008). In a previous study Schirmel et al. (2011) showed that mean species richness of spiders and carabids was reduced in moss-invaded grey dunes as compared to native, lichen-rich sites. In addition, species composition differed between invaded and native sites, which was explained by different responses of species to modified habitat parameters (e.g. reduced grass cover). In this study we perform a detailed analysis of C. introflexus’s impact on the life history trait composition and functional diversity of spiders and carabids by investigating three hypotheses: 1.

Trait proportion hypothesis: Moss invasion alters the proportion of life-history trait categories in the assemblage. We hypothesise the following shifts: Body size (hypothesis 1a): the proportion of large species will be higher in invaded sites compared to native, lichen-rich sites. C. introflexus create a distinct two-dimensional surface compared to the highly branched native Cladonia-lichens—this might reduce spatial resistance; Hunting/feeding (hypothesis 1b): for spiders, due to the loss of a three-dimensional vegetation architecture the proportion of web builders will decrease in Campylopus sites, while the proportion of actively hunting species will increase; for carabids, the proportion of phytophagous species will decrease since moss carpets hinder the germination of grasses (Schirmel et al.

Author's personal copy Invasive moss alters patterns

2.

3.

2011); Daily activity (hypothesis 1c): the proportion of diurnal species will increase in Campylopus sites due to a less variable and therefore a more moderate microclimate (Schirmel et al. 2011). Trait composition hypothesis: The native and lichen-rich grey dunes contain a specific assemblage of highly specialised species adapted to local habitat conditions (=habitat filtering). Spider and carabid assemblages living on native grey dunes therefore show a more homogeneous trait composition (i.e. the relative frequencies of selected traits). In contrast, the moss invasion favours the occurrence of species with different traits, which leads to a broader spectrum of traits and a more heterogeneous trait composition of the assemblages. Functional diversity hypothesis: As the trait composition is more heterogeneous in invaded sites (hypothesis 2), functional diversity is higher in these sites. Functional diversity is lower in native sites because many specialised dune species are functionally similar. Functional diversity is expressed as functional dispersion which is a measure of multiple traits that can estimate the dispersion of species in a trait space (Laliberte´ and Legendre 2010).

Materials and methods Study area The study area is an anthropo-zoogenic coastal heathland on the German Baltic island of Hiddensee (54°320 N, 13°500 E). The average annual temperature in this region is 7.5 °C and the average precipitation is 547 mm (Reinhard 1962). The vegetation on the acidic, nutrient-poor and sandy soils (Bauer 1972) is dominated by extensive dwarf-shrub stands (mainly Calluna vulgaris and Empetrum nigrum) and, to a lesser extent, by grey dunes. The grey dunes predominantly feature Corynephorus canescens, Carex arenaria, and cryptogams. Lichens of the genus Cladonia are particularly frequent (more than ten species; Remke, pers. comm.). The coastal heathland was used as a grazing ground until the beginning of the last century (Ministry of Environment of MecklenburgWestern Pomerania 2003) and is currently kept open

1091

by management measures such as shrub clearing, mowing, sod cutting and, since 2004, sheep grazing. Since the 1980s the exotic moss C. introflexus has been found on the island of Hiddensee (Schubert pers. comm.), where it has mainly invaded lichen-rich grey dunes (grey dunes). While lichens are very sensitive to trampling and grazing, C. introflexus has an effective vegetative propagation (shoot fragments) and grows quickly (Biermann and Danie¨ls 2001). The spreading of C. introflexus in the lichen-rich grey dunes on the island might therefore be favoured by tourist trampling and the increased grazing pressure since the reintroduction of sheep. Plot selection and characteristics We selected a total of 22 grey dune plots within the coastal heathland area. The minimum distance among the plots amounted to 20 m. The plots were almost level, had a homogeneous vegetation structure and were surrounded by dwarf-shrub vegetation. Eleven of the plots had been invaded by C. introflexus which had reached a cover of [85 % (henceforth referred to as invaded plots). As reference, eleven native, lichen-rich plots with a Cladonia spp. cover of [85 % of (henceforth referred to as native plots) were selected (Table 1). Based on findings of a prior study (Schirmel et al. 2011) the 22 grey dune plots contained 66 spider (native: 52, invaded: 49) and 39 carabid species (native: 32, invaded: 32), and mean species richness of spiders and carabids was significantly higher in native than in invaded grey dunes. For both groups, species composition showed a dissimilarity between native and invaded sites (Jaccard’s index, spiders = 0.5; carabids = 0.6). Further information and statistical analyses on species data, vegetation structure and environmental parameters of invaded and native plots are given in Schirmel et al. (2011). Sampling and identification of spiders and carabid beetles Spiders and carabid beetles were sampled between 19 May and 28 July, 2009, using unroofed pitfall traps. In each of the 22 plots three traps were set level with the soil surface. Within plots, the minimum distance between traps was 2 m. Traps were 6.5 cm in diameter and 7.5 cm deep and were filled to 1/3 of the volume with an 80 % ethylene–glycol-solution with a few

123



Table 1 The main characteristics of grey dunes invaded by Campylopus introflexus and native, lichen-rich grey dunes studied on the Baltic Island of Hiddensee, Germany (original data from Schirmel et al. 2011) Habitat

Vegetation and environment

Invaded by Campylopus introflexus

Mean cover of C. introflexus was 93 % and of Cladonia-lichens 1.5 %. Graminoids (mainly Corynephors canescens and Carex arenaria) had a mean cover of 9 % and a mean height of 9 cm Mean temperature was 21 °C, maximum temperature was 52 °C. Mean air humidity was 72 %

Native and lichen-rich

Cladonia-lichens had a mean cover of 91 % and C. introflexus of\1 %. Mean cover of graminiods was 16 % and the mean height was 14 cm Mean temperature was 23 °C and maximum temperature was 62 °C. Mean air humidity was 65 %

For further information see Schirmel et al. (2011)

drops of detergent. Traps were emptied fortnightly (five collections) and catches were stored in 70 % alcohol. Specimens were identified to the species level following Roberts (1987, 1996), Heimer and Nentwig (1991), and Almquist (2005) for spiders, and Mu¨llerMotzfeld (2006) for carabid beetles. Life-history traits Morpho-physiological and daily activity traits may have an effect on the occurrence patterns of spiders and carabid beetles (Ribera et al. 2001; Lambeets et al. 2009). As a result, species collected in the pitfall traps were assigned to categories of three life-history traits, based on published information: ‘body size’, ‘hunting’ (spiders) or ‘feeding’ (carabids), and ‘daily activity’ (Table 2). Data analysis Analyses were carried out at the plot level, pooling catches from the three pitfall traps and five collections. Both plot types were characterised by a different

species richness of spiders and carabids (see section 2.2 and Schirmel et al. 2011). Hence, we used proportional rather than count data to test for shifts in life-history trait values between the species assemblages of invaded and native plots. Therefore, we applied generalised linear models (GLM) with the frequency of a trait category within a plot as response variable and the plot type as predictor variable. For GLMs we used a binomial error function and, due to overdispersion, a quasi-binomial (proportions) model was applied. F-statistics were evaluated using an analysis of deviance. Results were visualised using modified plots as in Sax et al. (2005). To test if the moss invasion has a significant effect on the trait composition of spiders and carabids we performed a permutational multivariate Analysis of variance using the Bray-Curtis similarity measure (using the ‘adonis’ in the R package ‘vegan’). To test if C. introflexus invasion leads to more heterogeneous trait composition we analysed the multivariate dispersion based on the Bray-Curtis similarity of traits for both habitat types. To do this we used a traitabundance per plot matrix (using the command

Table 2 Life-history traits of carabid beetles and spiders based on literature data Trait

Attributes

Reference

Spiders

Carabids

Body size*1

Very small (\3.1 mm), small (3.1–4.5 mm), medium (4.6–8.4 mm), large ([8.5 mm)

Very small (\5 mm), small (5–9 mm), medium (9–15 mm), large ([15 mm)

4, 5

1, 2

Hunting/ feeding

Web-building, wanderer (active hunting)

Collembola-specialist, generalist predator, phytophagous

4, 6

3

Daily activity

Diurnal, nocturnal

Diurnal, nocturnal

4, 6, 7, 8, 9, 10

3

*

Spiders

Carabids

Female body size was used for spiders. 1 = Mu¨ller-Motzfeld (2006), 2 = Ribera et al. (1999), 3 = Turin (2000), 4 = Nentwig et al. (2010); 5 = Ruzicka (1985), 6 = Roberts (1987), 7 = Roberts (1996), 8 = Henatsch and Blick (1993), 9 = Kreuels (2001), 10 = Buchholz (2010b)

123


‘betadisper’ in the R package ‘vegan’; Anderson et al. 2006). An ANOVA was used to test for differences between the multivariate homogeneity of dispersions of invaded and native sites. We chose functional dispersion (FDis) to express changes in functional diversity. FDis is a measure of multiple traits that can estimate the dispersion of species in a trait space (Laliberte´ and Legendre 2010). Mathematically, FDis is the weighted mean distance of individual species to the weighted centroid of all species in a multidimensional trait space, where weights correspond to the relative species abundances. FDis has several advantages over other functional diversity indices such as functional richness (sensu Ville´ger et al. 2008) as it is unaffected by species richness, can handle any number or type of traits, and is not strongly influenced by outliers. Moreover, FDis can be computed from any distance or dissimilarity measure (Anderson et al. 2006). FDis has no upper limit, and high values should correspond to high numbers of functionally different species with more or less even abundances. For more detailed information on FDis see Laliberte´ and Legendre (2010). We calculated Gaussian error structures of GLMs and identity link function to detect possible effects of C. introflexus and used FDis as response and plot type as predictor variable. All analyses were performed in R 2.11.1 (R Development Core Team 2010) using the FD (Laliberte´ and Legendre 2010; Laliberte´ and Shipley 2011) and Vegan (Oksanen et al. 2011) packages.

Results Proportions of life-history trait categories in species assemblages of invaded and native sites Significant shifts in the proportion of trait categories were observed for all life-history traits of both spiders and carabids except for daily activity (Fig. 1). The proportion of very small spiders and small carabids was significantly lower in invaded plots (GLM, spiders: F = 4.9, p = 0.040; carabids: F = 24.7, p \ 0.001). In contrast, the proportion of medium carabids was higher in invaded plots (F = 13.4, p = 0.002). Web-building spiders contributed less to the spider assemblage of invaded plots as compared to native plots (F = 13.8, p = 0.001), and there was a

1093

higher proportion of actively hunting species in invaded as compared to native plots (F = 12.0, p = 0.002). Carabid assemblages contained lower proportion of phytophagous species (F = 11.1, p = 0.003) and higher proportion of Collembolafeeders in invaded plots (F = 7.1, p = 0.010). Trait composition For both spiders and carabids, the trait compositions between invaded sites and native sites were different (Fig. 2). Plot type (invaded or native) had a significant effect on trait composition of spiders (permutational multivariate ANOVA with 999 permutations, F = 5.299, p = 0.01) and on carabids (F = 10.158, p = 0.01). For spiders, homogeneity of multivariate dispersion of traits differed significantly (ANOVA, F = 6.630, p = 0.018). The average distance to the centroid was 0.188 in invaded and 0.135 in native grey dunes (Fig. 2). No differences were found for carabids (F = 1.3, p = 0.268), where the distances to the centroid were 0.143 in invaded and 0.111 in native grey dunes (Fig. 2). Functional diversity For spiders, functional diversity (=functional dispersion) was significantly higher in invaded grey dunes (0.21 ± 0.01) compared to native grey dunes (0.16 ± 0.01) (GLM, F = 10.1, p = 0.005). In contrast, the functional diversity of carabid beetles was significantly higher in native grey dunes (0.30 ± 0.01) than in invaded sites (0.25 ± 0.01) (GLM, F = 10.9, p = 0.004). Assemblages above the line contained species with less similar traits and low redundancy, which means that species are more scattered in the functional trait space (Fig. 3). Assemblages below the line contained species with more similar traits; this pattern was given for the spider assemblages in native grey dunes.

Discussion Trait proportion hypothesis The Campylopus invasion has induced shifts in trait values in both spider and carabid beetle assemblages:

123



Fig. 1 Proportions (%) of categories of the life-history traits ‘body size’, ‘hunting’ or ‘feeding’, and ‘activity’ of spiders (left) and carabids (right) in invaded sites (grey dunes invaded by Campylopus introflexus) and native sites (lichen-rich grey dunes). Points near the line show a similar proportion in both habitat types. An arrow indicates a significant difference of a life-history trait proportion between native and invaded sites (binomial GLM at p \ 0.05)

Body size (Hypothesis 1a) We found evidence to support our first hypothesis, since native sites contained a higher proportion of very

123

small (spider) and small (carabid) species, suggesting body size shifts due to moss invasion. C. introflexus is able to build dense and uniform two-dimensional moss carpets which can have a negative impact on the


1095

Fig. 2 Multivariate homogeneity of dispersion of spider (top) and carabid (bottom) traits in invaded and native sites. Multivariate dispersion is measured by calculating the Bray Curtis distance of group members to the group centroid (either invaded or native sites). Original distances were reduced to principal coordinates (spiders: eigenvalue of the first axis = 0.400, second axis = 0.176; carabids: first axis = 0.417, second axis = 0.057). Distances differ significantly for spiders (F = 6.630, p = 0.018) but not for carabids (F = 1.3, p = 0.268)

germination of higher plants (Biermann and Danie¨ls 2001) and could lead to a reduced graminoid cover (or cover of other herbs) (Schirmel et al. 2011). This, in turn, could lead to a reduction in spatial resistance compared to native plots with highly branched native Cladonia-lichens. A higher spatial resistance might favour the occurrence of smaller species in native plots. For spiders, this was apparently related to the higher proportion of web-building species in native sites (see

below), since most dune-dwelling web builders found in our study were small bodied (e.g. Hahnia montana, Tenuiphantes tenuis). Native sites provided a more diverse vegetation structure and therefore essential habitat requirements for web builders (Scheidler 1990). However, the proportion of large species was evenly distributed in invaded and native sites which might suggest that larger species are not directly negatively affected by a higher spatial resistance. A

123



Fig. 3 Relationship between species richness and functional diversity (=functional dispersion, FDis) of spider and carabids assemblages in grey dunes invaded by Campylopus introflexus (top) and in native, lichen-rich grey dunes (bottom). The line shows the hypothetical relationship when every species contributes to functioning and enhances functional diversity. An increase of species richness has only little effect on functional diversity when more similar traits occur in the assemblage and species show a high functional similarity (points under the line). If changes in functional diversity are greater than changes in species richness, traits are less similar (points above the line)

higher proportion of medium carabids in invaded sites could be explained by high abundances of one single medium sized species (Calathus erratus). Hunting/feeding (Hypothesis 1b) As hypothesised, actively hunting species were dominant in invaded sites, which could on the one hand be associated with lower spatial resistance (see above). On the other hand, loss of the three-dimensional vegetation architecture—due to the loss of highly branched lichens and a lower graminoid cover—could decrease habitat suitability for many web builders. Shifts in the spider hunting mode were accompanied by shifts in the feeding behaviour of carabid beetles, since phytophagous species were more abundant in native sites. A higher graminoid cover in native sites (twice as high) and therefore higher availability of seeds might be an explanation for this, as already

123

discussed by Schirmel et al. (2011). The higher proportion of Collembola-specialists in invaded sites might be explained by higher humidity and lower temperature in moss carpets, which generally favours the occurrence of springtails (Badejo et al. 1998). Higher springtail abundances might also have attracted actively hunting spiders, as Collembola contribute considerably to the diet of spiders (Foelix 1996). Thus, both for body size and hunting mode/ feeding preference we found shifts due to moss invasion. Daily activity (Hypothesis 1c) We had to reject our third hypothesis as we did not find any effects of moss invasion on daily activity. Although microclimate was significantly drier and hotter in native and more balanced (less extreme) in Campylopus sites (air humidity: invaded: 72 %, native


65 %; temperature: invaded: 21 °C, native 23 °C; Schirmel et al. 2011), differences might be too small to favour nocturnal activity. Dune species are well adapted to higher temperatures as they, for example, seek for shelter, burrows or migrate to densely vegetated patches (Almquist 1970, 1971, 1973). Trait composition hypothesis Trait composition of both spiders and carabids differed between invaded and native sites. Native sites showed a more homogeneous trait composition for spiders (corroboration of hypothesis ii). One explanation might be that habitat filtering has led to the appearance of similar traits (Ulrich et al. 2010). Besides alteration in the vegetation structure, the moss invasion resulted in a more balanced microclimate (Schirmel et al. 2011). Therefore, the extreme habitat conditions that are normally found in grey dunes could be attenuated. While (grey) dune species assemblages generally consist of a high number of habitat specialists (Buchholz 2010a), lower spatial resistance, lower temperatures and higher air humidity might favour comprehensive migration of species from neighbouring habitat types and migration of generalist species from neighbouring habitat types into Campylopus sites (Heydemann 1957; Duffey 1968; Bonte et al. 2003, 2004). This, in turn, could explain a higher variation in life-history traits and might have led to a less even trait distribution. C. introflexus might therefore be regarded as an ‘ecosystem engineer’ species which is able to change the availability of resources to other species (Jones et al. 1994). Functional diversity hypothesis The effect of moss invasion on spider functional diversity was opposite to the effect on carabid beetles. For spiders, invasion enhanced functional diversity. Lower functional diversity in native sites could be due to very high abundances of one single species, the common grey dune wolf spider Pardosa monticola (Schirmel et al. 2011). As our measure for functional diversity FDis takes relative species abundances into account (Laliberte´ and Legendre 2010), functional diversity decreases with increasing dominance of single species. Consequently, a higher functional diversity in invaded sites could be related to the decrease of P. monticola abundances (analysis of FDis

1097

without P. monticola revealed results with a significantly higher value in native sites; Appendix). For carabid beetles, the moss invasion reduced functional diversity. This means that native sites exhibited an assemblage in which species were more scattered in trait space and were less dominated by single species (see also rank-abundance plots in Schirmel et al. 2011). Besides impacts on the mean values of functional diversity, we observed changes in the relationship between species richness and functional diversity in native and invaded sites. This relationship is indicative for the distribution of traits in the assemblage (Petchey et al. 2007). If an increase of species richness has only little effect on functional diversity, this might be an indication that more similar traits occur in the assemblage and that species show a high functional similarity. If changes in functional diversity are greater than changes in species richness, traits are less similar (Petchey et al. 2007). The latter might occur if functionally different species immigrate to a community (in the case of grey dunes, generalist species)—and therefore add new traits to the system— while other species with similar traits disappear (for example xerophilic habitat specialists). In contrast, if functional similarity is high, habitat filtering might induce species sorting which favours distinct lifehistory traits. In that case, dune-dwelling communities are mostly made up of xerophilic habitat specialists. Our results showed that spiders in native grey dunes had a higher functional similarity compared to invaded sites. We explained this by habitat filtering (e.g. Weiher and Keddy 1999; Cornwell et al. 2006) and which seems to structure the assemblage. Species occurring in sites with habitat filtering are particularly well adapted to the predominating environmental conditions and show more or less similar traits that are best adapted to this habitat (Holdaway and Sparrow 2006; Petchey et al. 2007). In the case of native grey dunes, it seems likely that many species were highly specialised to living in the three-dimensional lichen branches, to the special food resources, and to the extreme microclimatic conditions. After moss invasion, species traits became less similar, which might have reduced the functional similarity (Petchey et al. 2007). This might be explained by character displacements and by changes in the composition of spider assemblages. As indicated by the more heterogeneous trait composition among spiders in invaded sites, less specialised species (generalists)

123



might have been able to immigrate due to lower environmental filtering effects. In contrast, carabid beetles showed no clear patterns in similarity (if any, a very low similarity in both grey dune types seemed to exist). Habitat filtering in grey dunes might therefore be less apparent for carabid beetles than it is for spiders. One reason might be that the moss invasion occurred only at a very small scale. Many carabid beetles are very mobile (able to fly and run) and might have larger activity ranges than most web building spiders and ambush hunters. Except for wandering species, niche differentiation and microhabitat use might therefore be more natural for spiders that depend on a three-dimensional habitat structure (Scheidler 1990).

Conclusion Moss invasion by Campylopus introflexus induced changes in functional composition of spiders and carabids by creating more heterogeneous trait communities, as suggested by diminished trait similarities (most obvious for spiders). The latter is thought to result from species immigration, a crucial aspect, as it might indicate a weakening of the habitat filtering effects that normally regulate typical and specialised dune arthropod assemblages in non-invaded habitats. In this context, we found evidence which suggests that spiders are more sensitive than carabids, since a loss of (dune) species accompanies a diversification of traits. Finally, moss invasion influenced functional diversity. Acknowledgments We thank Lars Timler for help with the field work and Martin Entling and two anonymous reviewers for helpful comments on a previous version of the manuscript. The study was in part financially supported by the Bauer-Hollmann foundation.

Appendix See Table 3. Table 3 Analysis of functional dispersion (FDis) of spiders excluding the dominant species P. monticola (GLM)

FDis

123

Invaded

Native

F

p

0.23

0.28

23.06

0.0001

References Almquist S (1970) Thermal tolerances and preferences of some dune-living spiders. Oikos 21:230–236 Almquist S (1971) Resistance to desiccation in some dune-living spiders. Oikos 22:225–229 Almquist S (1973) Habitat selection by spiders on coastal sand dunes in Scania, Sweden. Entomol Scand 4:134–154 Almquist S (2005) Swedish Araneae, part 1: families Atypidae to Hahniidae (Linyphiidae excluded). Insect Syst Evol Suppl 62:1–284 Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9: 683–693 Badejo MA, Nathaniel TI, Tian G (1998) Abundance of springtails (Collembola) under four agroforestry tree species with contrasting litter quality. Biol Fertil Soils 27:15–20 Bauer L (1972) Handbuch der Naturschutzgebiete der Deutschen Demokratischen Republik. Band 1: Bezirke Rostock, Schwerin und Neubrandenburg. Urania-Verlag, Leipzig Biermann R, Danie¨ls FJA (2001) Vegetationsdynamik im Spergulo-Corynephoretum unter besonderer Beru¨cksichtigung des neophytischen Laubmooses Campylopus introflexus. Braunschweiger Geobot Arb 8:27–37 Bonte D, Criel P, Van Thournout I, Maelfait JP (2003) Regional and local variation of spider assemblages (Araneae) from coastal grey dunes along the North Sea. J Biogeogr 30: 901–911 Bonte D, Baert L, Lens L, Maelfait JP (2004) Effects of aerial dispersal, habitat specialisation, and landscape structure on spider distribution across fragmented grey dunes. Ecography 27:343–349 Buchholz S (2010a) Ground spider assemblages as indicators for habitat structure in inland sand ecosystems. Biodivers Conserv 19:2565–2595 Buchholz S (2010b) Factors determining daily rhythms of epigeic arthropods—activity patterns of spiders in dry open habitats. Entomol Gen 32:251–264 Bultman TL, DeWitt DJ (2008) Effect of an invasive ground cover plant on the abundance and diversity of a forest floor spider assemblage. Biol Invasions 10:749–756 Choi W II, Choi KS, Lyu DP, Lee JS, Lim J, Lee S, Shin SC, Chung YJ, Park YS (2010) Seasonal changes of functional groups in coleopteran communities in pine forests. Biodivers Conserv 19:2291–2305 Cornwell WK, Schwilk DW, Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471 D0 Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87 Davis MA (2009) Invasion biology. Oxford Univ Press, Oxford Diaz S, Lavorel S, de Bello F, Quetier F, Grigulis K, Robson M (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci USA 104:20684–20689 Duffey E (1968) An ecological analysis of the spider fauna of sand dunes. J Anim Ecol 37:641–674 Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

Author's personal copy Invasive moss alters patterns Foelix R (1996) Biology of spiders. Oxford University Press, Oxford Folke CS, Carpenter S, Walker B, Scheffer M, Elmquist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Syst 35:557–581 Gratton C, Denno RF (2006) Arthropod food web restoration following removal of an invasive wetland plant. Ecol Appl 16:622–631 Heimer S, Nentwig W (1991) Spinnen Mitteleuropas: ein Bestimmungsbuch. Parey, Berlin Hejda M, Pysˇek P, Pergl J, Sa´dlo J, Chytry´ M, Jarosˇ´ık V (2009) Invasion success of alien plants: do habitat affinities in the native distribution range matter? Global Ecol Biogeogr 18:372–382 Henatsch B, Blick T (1993) Zur tageszeitlichen Laufaktivita¨t der Laufka¨fer, Kurzflu¨gelka¨fer und Spinnen in einer Hecke und einer angrenzenden Brachfla¨che (Carabidae, Staphylinidae, Araneae). Mitt Dtsch Ges All Angew Ent 8: 529–536 Herrera AM, Dudley TL (2003) Reduction of riparian arthropod abundance and diversity as a consequence of giant reed (Arundo donax) invasion. Biol Invasions 5:167–177 Heydemann B (1957) Die Biotopstruktur als Raumwiderstand und Raumfu¨lle fu¨r die Tierwelt. Verh Dtsch Zool Ges 1956:332–347 Holdaway RJ, Sparrow AD (2006) Assembly rules operating along a primary riverbed-grassland successional sequence. J Ecol 94:1092–1102 Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386 Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190 Ketner-Oostra R, Sykora KV (2004) Decline of lichen-diversity in calcium-poor coastal dune vegetation since the 1970 s, related to grass and moss encroachment. Phytocoenologia 34:521–549 Ketner-Oostra R, Sykora KV (2008) Vegetation change in a lichen-rich inland drift sand area in the Netherlands. Phytocoenologia 38:267–286 Kreuels M (2001) Die Tagespha¨nologie epiga¨ischer Spinnen (Arachnida: Araneae) im NSG Hasental-Kregenberg bei Marsberg (NRW). Arachnol Mitt 22:19–28 Laliberte´ E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305 Laliberte´ E, Shipley B (2011) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-11 Lambeets K, Vandegehuchte ML, Maelfait JP, Bonte D (2009) Integrating environmental conditions and functional lifehistory traits for riparian arthropod conservation planning. Biol Conserv 142:625–637 Litt AR, Steidl RJ (2010) Insect assemblages change along a gradient of invasion by a nonnative grass. Biol Invasions 12:3449–3463 Loreau M (2010) Linking biodiversity and ecosystems: towards a unifying ecological theory. Philos T R Soc B 365:49–60 Ma Z, Gan X, Cai Y, Chen J, Li B (2010) Effects of exotic Spartina alterniflora on the habitat patch associations of

1099 breeding saltmarsh birds at the Chongming Dongtan in the Yangtze River estuary, China. Biol Invasions 13: 1673–1686 Mack MC, D’Antonio CM (2003) Exotic grasses alter controls over soil nitrogen dynamics in Hawaiian woodland. Ecol Appl 13:154–166 Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893 Mu¨ller-Motzfeld G (2006) Band 2, Adephaga 1: Carabidae (Laufka¨fer). In: Freude H, Harde KW, Lohse GA, Klausnitzer B (eds) Die Ka¨fer Mitteleuropas. SpektrumVerlag Nentwig W, Ha¨nggi A, Kropf C, Blick T (2010) Spiders of Europe. www.araneae.unibe.ch Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MH, Wagner H (2011) The vegan Package Version 1.17-11. http://CRAN. R-project.org/package=vegan Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758 Petchey OL, Evans KL, Fishburn IS, Gaston KJ (2007) Low functional diversity and no redundancy in British avian assemblages. J Anim Ecol 76:977–985 Petchey OL, O’Gorman EJ, Flynn DFB (2009) A functional guide to functional diversity measures. In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C (eds) Biodiversity, ecosystem functioning and human wellbeing: an ecological and economic perspective. Oxford University Press, Oxford, pp 49–60 Pe´tillon J, Canard A, Ysnel F (2006) Spiders as indicators of microbabitat changes after a grass invasion in salt-marshes: synthetic results from a case study in the Mont-SaintMichel Bay. Cah Biol 47:11–18 Pe´tillon J, Lambeets K, Montaigne W, Maelfait JP, Bonte D (2010) Habitat structure modified by an invasive grass enhances inundation withstanding in a salt-marsh wolf spider. Biol Invasions 12:3219–3226 Pritekel C, Whittemore-Olson A, Snow N, Moore JC (2006) Impacts from invasive plant species and their control on the plant community and belowground ecosystem at Rocky Mountain National Park, USA. Appl Soil Ecol 32:132–141 Reinhard H (1962) Klimatologie. Atlas der Bezirke Rostock, Schwerin und Neubrandenburg. VEB, Rostock Ribera I, Foster GN, Downie IS, McCracken DI, Abernethy VJ (1999) A comparative study of the morphology and life traits of Scottish ground beetles (Coleoptera, Carabidae). Ann Zool Fenn 36:21–37 Ribera I, Dole´dec S, Downie IS, Foster GN (2001) Effect of land disturbance and stress on species traits of ground beetle assemblages. Ecology 82:1112–1129 Roberts MJ (1987) The spiders of Great Britain and Ireland. Volume 2: Linyphiidae and checklist. Harley Books Roberts MJ (1996) Spiders of Britain and Northern Europe. Collins Ruzicka V (1985) The size groups in the spiders (Araneae) and carabids (Col. Carabidae). Acta Univ Carolinae Biol 1982–1984:77–107 Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Osterheld M,

123

Author's personal copy 1100 LeRoy Poff N, Sykes MT, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774 Sax DF, Kinlan BP, Smith KF (2005) A conceptual framework for comparing species assemblages in native and exotic habitats. Oikos 108:457–464 Scheidler M (1990) Influence of habitat structure and vegetation architecture on spiders. Zool Anz 225:333–340 Schirmel J (2011) Response of the grasshopper Myrmeleotettix maculatus (Orthoptera: Acrididae) to invasion by the exotic moss Campylopus introflexus in acidic coastal dunes. J Coast Conserv 15:159–162 Schirmel J, Timler L, Buchholz S (2011) Impact of the invasive moss Campylopus introflexus on carabid beetles (Coleoptera: Carabidae) and spiders (Araneae) in acidic coastal dunes at the southern Baltic Sea. Biol Invasions 13:605–620 R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org Tilman D (1997) The influence of functional diversity and composition on ecosystem processes. Science 277: 1300–1302 Topp W, Kappes H, Rogers F (2008) Response of grounddwelling beetle (Coleoptera) assemblages to giant knotweed (Reynoutria spp.) invasion. Biol Invasions 10: 381–390 Turin H (2000) De Nederlandse Loopkevers. Verspreiding en oecologie (Coleoptera: Carabidae). European Invertebrate Survey Nederland

123

J. Schirmel, S. Buchholz Ulrich W, Hajdamowicz I, Zalewski M, Stanska M, Ciurzycki W, Tykarski P (2010) Species assortment or habitat filtering: a case study of spider communities on lake islands. Ecol Res 25:375–381 Villa` M, Basnou C, Pyesˇek P, Josefsson M, Genovesi P, Gollasch S, Nentwig W, Olenin S, Roques A, Roy D, Hulme P and DAISE partners (2010) How well do we understand the impacts of alien species on ecosystem services? A panEuropean, cross-taxa assessment. Front Ecol Environ 8: 135–144 Ville´ger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301 Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892 Weidenhamer JD, Callaway RM (2010) Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol 36:59–69 Weiher E, Keddy PA (1999) Ecological assembly rules: perspectives, advances, retreats. Cambridge University press, Cambridge Wolkovich EM, Bolger DT, Holway DA (2009) Complex responses to invasive grass litter by ground arthropods in a Mediterranean scrub ecosystem. Oecologia 161:697–708 Wu YT, Wang CH, Zhang XD, Zhao B, Jiang LF, Chen JK, Li B (2009) Effects of saltmarsh invasion by Spartina alterniflora on arthropod community structure and diets. Biol Invasions 11:635–649