Effects of Rosa rugosa invasion in different coastal dune vegetation types

Transcription

1 22.qxd:Isserman_q5.qxd :09 Pagina 289 Effects of Rosa rugosa invasion in different coastal dune vegetation types Maike Isermann Vegetation Ecology and Conservation Biology, University of Bremen, Leobener Strasse, Bremen, Germany; Abstract Rosa rugosa Thunb. has become naturalized in coastal dune vegetation. To assess the effects of R. rugosa invasion on different coastal dune vegetation types paired plots with and without R. rugosa were studied on the German North Sea islands Spiekeroog, Juist and Norderney. The complete dune series from Ammophila-dunes, through grey dunes with Corynephorus-swards, to brown dunes with Empetrum-heath were included. In general, both species richness and the major plant dune species declined with increasing shrub cover, and with differences among functional groups. Typical shrubland species increased slightly and typical grassland species decreased strongly, particularly in the grey dunes, where there was a sharp decline in the number of threatened species. The encroachment of species-poor shrubland types, e.g. with R. rugosa, which are characterized by the dominance of one or two shrub species, threatens dune vegetation. R. rugosa shrubland has a low conservation value and presents a serious conservation problem in dune habitats of the German North Sea region. Introduction Coastal dunes are one of the valuable habitat types in Europe, they are often species-rich and contain many regionally rare plants and animals not only in Europe, but also in other parts of the world such as in coastal sand plains of Massachusetts, USA (Dunwiddie 1997). Dunes represent a priority habitat type of the European Fauna Flora Habitats Directive 92/43/EEC (Council of the European Commission 1992). The preservation of semi-natural grass and heathland has a high conservation priority and the invasion of species-poor shrubland types poses a serious conservation problem, especially to open grassland communities (Hopkins 1996, Mortimer et al. 2000). Expansion of shrubs often reduces species richness of semi-natural vegetation types, for example by: Baccharis pilularis DC. in a Californian grassland, where herbaceous species richness was reduced (Hobbs & Mooney 1986, Williams et al. 1987, Sax 2002); Porlieria chilensis I.M. Johnst. in coastal shrub-grassland patches of Chile (Gutiérrez et al. 1993); a variety of alien shrubs and trees in the fynbos vegetation of South Africa (Richardson et al. 1989); Potentilla fruticosa L. and Juniperus communis L. in Swedish alvar vegetation (Rejmánek & Rosén 1988, 1992). Nitrogen-fixing shrubs like Hippophaë rhamnoides L., Myrica pensylvanica Mirb. and Porlieria chilensis are particularly significant in changing species com- Plant Invasions: Human perception, ecological impacts and management, pp Edited by B. Tokarska-Guzik, J.H. Brock, G. Brundu, L. Child, C.C. Daehler & P. Pyšek 2008 Backhuys Publishers, Leiden, The Netherlands

2 22.qxd:Isserman_q5.qxd :09 Pagina Maike Isermann position and environmental conditions of invaded dune ecosystems (Hodgkin 1984, Gutiérrez et al. 1993, Shumway 2000). In the past, due to changing land use, landscapes often changed from open grassland to areas increasingly covered with shrubland and woodland. Examples include the southern Swedish Göteborg archipelago (Herloff 2003) and the German Wadden Sea Island Spiekeroog (Isermann & Cordes 1992). The decline in species richness of native plants is one of the main effects related to the invasion of nonnative species all over the world (Richardson 2001). Invasive plants endanger valuable vegetation and displace rare plants in coastal dunes, e.g. the moss Campylopus introflexus (Hedw.) Brid. spreads into grey dunes and reduces natural diversity particularly of other mosses and lichens (Van der Meulen et al. 1987). On the Wadden Sea Islands, Rosa rugosa naturalized in dune vegetation, spread vegetatively by tillers and build large clones. Long-distance dispersal of fruits and seeds probably takes place as a result of dispersal in sea water and by birds. Dense invasive shrubs possibly also prevent development towards species-rich shrubland types. The objective of this study was to assess the effects of Rosa rugosa invasion on species richness, community structure and environmental factors in different coastal dune vegetation of the German North Sea islands Spiekeroog, Norderney and Juist. The following questions were addressed: (i) Were the effects of R. rugosa invasion on species richness and diversity similar in different coastal dune vegetation? (ii) Were functional groups or single species more affected by the invasion than others? (iii) Is the shading effect of the R. rugosa a possible reason for the changed vegetation parameters? Methods Study species Rosa rugosa Thunb. was introduced to Europe in the 18th century. Its natural distribution includes the coastal regions of the Northern Pacific, where it grows mainly on dunes, rocky shores and species-rich meadows. The shrub is naturalized in parts of northern, western and central Europe and is an invasive species along the coasts of the Northern Atlantic, the North Sea and the Baltic Sea (Bruun 2005). The time-lag of R. rugosa in Brandenburg, Germany was calculated at 199 years, in comparison that of Mahonia aquifolium (Pursh) Nutt. at 38 and that of Prunus laurocerasus L. at 319 years (Kowarik 2003). Rosa rugosa was planted in European coastal areas around the 19th century (Böcher 1952, Van Dieken 1970, Christensen & Johnsen 2001). In coastal dunes, R. rugosa was planted for sand stabilization and coastal protection (Eigner 1992, Dubra & Olšauskas 2002). In general, many alien plant species were used in dunes for coastal protection (Nordstrom et al. 2000) these include other woody plants such as Crataegus monogyna Jacq., Hippophaë rhamnoides and Lycium barbarum L. (Hansen & Vestergaard 1986, Vogt Andersen 1995). In northwest European coastal areas, both on islands and on the mainland, R. rugosa was also used as an ornamental plant in gardens (Østergaard 1954). From these introduced sites, it was

3 22.qxd:Isserman_q5.qxd :09 Pagina 291 Effects of Rosa rugosa invasion in different coastal dune vegetation types 291 distributed by animals into neighbouring dune areas. Today it is widely distributed, with the exception of small uninhabited islands like Lütje Hörn on the German Wadden Sea Islands (Dijkema & Wolf 1983). In Germany, R. rugosa is found in coastal areas where it is one of the most problematic invasive species (Kowarik 2003). Mechanical control or elimination of R. rugosa is difficult (Eigner 1992); published experiences with chemical destruction are not known and questionable; biological control (Bruun 2006) has a high risk of unforeseen negative effects, which are difficult to quantify. Sampling The study was carried out mainly on the German Wadden Sea Island, Spiekeroog. The dune vegetation was represented by a typical landward zonation from the beach across the yellow dunes dominated by Ammophila arenaria (L.) Link, to the semifixed grey dunes with Corynephorus canescens (L.) P. Beauv. and, in the oldest parts, brown dunes characterized by dwarf-shrub heath of Empetrum nigrum L. Vegetation data were collected from 16 m 2 plots of naturalized R. rugosa stands in all dune types, from the yellow to the brown dunes. Obvious planted stands were not included. The plots were placed in order to include the full range of R. rugosa cover. In connection with one or two Rosa plots, one paired plot without Rosa, but otherwise being as similar as possible to the Rosa plot with respect to aspect and inclination, was investigated. Three different vegetation layers were distinguished: a shrub layer, a surface layer with herbaceous species and woody seedlings, and a mosses and lichens surface layer. Epiphytic mosses and lichens were not considered. Data in each plot included, total cover of the respective vegetation layer in percentage terms, the percentage cover of R. rugosa, and a list of all species with their cover abundance according to a refined Braun-Blanquet-scale (Reichelt & Wilmanns 1973). Vascular plant nomenclature follows the Nomenclatural Data Base (TROPICOS) of the Missouri Botanical Garden ( and for mosses Koperski et al. (2000). To analyse shading effects, light (Lux) was measured with an illuminometer both beneath (at the bottom layer) and outside the Rosa stands. The relative irradiance beneath the shrub layer was used as a measure of light availability. Soil samples were taken from the upper 15 cm of soil. Chemical analyses were carried out on < 2 mm fraction of air-dried soil. Using standard techniques, soil ph (1:2.5 soil: CaCl 2 ratio) was analysed, total nitrogen and carbon were determined with a C/Nelementary analyser converted at 1010 ºC and gas-chromatographically separation, and organic matter (as loss on ignition at 550 ºC for 24 h). Water content in percent was measured as the weight difference of air-dried to 105 ºC dried-soil. Statistical analysis Vegetation parameters in most cases presented a normal distribution and were analysed by parametric methods. Statistical tests were carried out with the program MINITAB (Anon. 1998), unless indicated otherwise.

4 22.qxd:Isserman_q5.qxd :09 Pagina Maike Isermann To distinguish effects of R. rugosa on typical grassland and shrubland species, the species were divided into three types: grassland, shrubland and indifferent habitat connection, based on the frequency in the vegetation classes Koelerio- Corynephoretea and Rhamno-Prunetea according to Berg et al. (2001). To determine groups of species, the relevés were classified using PC-ORD (McCune & Mefford 1999). Differences in species composition among sites of shrubland and other vegetation types were shown using ordination analysis of the plots by Detrended Correspondence Analysis (DCA) running PC-ORD with its default options without downweighting for rare species. Regression analyses of the resulting scores of the ordination axes and species cover were used to find crucial species for interpretation of the ordination diagram. To examine differences in vegetation parameters among the four vegetation types (Ammophila-dune, Corynephorus-sward, Empetrum-heath, Rosa-scrub), oneway-anovas and Tukey-test were used. In connection with differences among vegetation types, the vegetation type R. rugosa-scrub was defined as having Rosa cover of at least 30 percent. Differences in vegetation parameters between scrub and related reference plots were analysed with a paired t-test, because of the sampling design. The shading effect of R. rugosa was shown by a regression analysis of relative irradiance. In addition, the light availability under R. rugosa and Hippophaë rhamnoides (Isermann et al. 2005) was compared. Regression analysis was used to access the impact of R. rugosa cover on vegetation parameters. Both linear and quadratic models were applied, comparing the R 2 adj. values and significance probabi - lities. Furthermore, significance of the quadratic model in relation to the linear one was tested by forward and backward stepwise regression. Results Species composition Species composition was different in all investigated plots (Fig. 1). The first axis of the ordination diagram is mostly characterized by an increase in Empetrum nigrum. (b = 0.41, R 2 adj. = 0.97, p < 0.001) and Hypnum jutlandicum Holmen & Warncke (b = 0.24, R 2 adj. = 0.61, p = 0.001), further by a decrease in Brachythecium albicans (Hedw.) Schimp. (b = 0.04, R 2 adj. = 0.61, p = 0.024) and Festuca arenaria Osbeck (b = 0.16, R 2 adj. = 0.42, p < 0.001). The second axis is primarily characterized by a decrease in Hippophaë rhamnoides (b = -0.26, R 2 adj. = 0.58, p = 0.002) and Ammophila arenaria (b = -0.06, R 2 adj. = 0.18, p = 0.005) as well as an increase in Carex arenaria L. (b = 0.18, R 2 adj. = 0.46, p < 0.001). Rosa rugosa has a quadratic relationship with the first axis (b = 0.88, c = , R 2 adj. = 0.60, p < 0.001) and a less pronounced quadratic relation with the second axis (b = 0.67, c = , R 2 adj. = 0.11, p = 0.029). Hence, the ordination diagram shows the differentiation among grey and brown dunes as well as yellow dune vegetation: along the first axis from yellow or young grey dunes to brown dunes and along the second axis from yellow to grey dunes. Rosa rugosa naturalized in all of the three investigated dry dune types; hence plots with high shrub cover are located mainly in the centre of the diagram.

5 22.qxd:Isserman_q5.qxd :10 Pagina 293 Effects of Rosa rugosa invasion in different coastal dune vegetation types 293 Fig. 1. DCA ordination of plots (axis 1: eigenvalue 0.812, length of gradient 4.276; axis 2: eigenvalue 0.480, length of gradient 3.678, n = 63). The size of the plot symbols reflects the percentage cover of R. rugosa. The white rhombus symbolizes plots of the Ammophila-dune, the grey quadrate those of the Corynephorus-sward and the black triangle reflects those of the Empetrum-heath. Three main species groups were classified and characterized by the three different dune types: Ammophila arenaria, Cerastium semidecandrum L., Festuca arenaria, Oenothera ammophila Focke and Brachythecium albicans were typical for the yellow dunes; Agrostis capillaris L., Aira praecox L., Carex arenaria, Corynephorus canescens, Galium album Mill., Poa pratensis L. agg. and Hypnum cupressiforme Hedw. var. lacunosum characterized the grey dunes and Empetrum nigrum, Polypodium vulgare L., Salix repens L. var. argentea and Hypnum jutlandicum were examples of the brown dunes. Rosa rugosa-scrub was often accompanied by Brachythecium rutabulum (Hedw.) Schimp. and is characterized by the absence of other species.

6 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann Vegetation cover Vegetation parameters of the dominant Rosa-scrub were, in general, similar on yellow, grey and brown dunes. There were differences among the four vegetation types (Table 1). Total vegetation cover of the Ammophila-dune was lower than in the other vegetation types. The cover of grasses and herbs was greater in the Ammophiladune and the Corynephorus-sward than in the Empetrum-heath and the Rosa-scrub. The cover of mosses and lichens was low in the Ammophila-dune as well as in the Rosa-scrub; furthermore, the cover of mosses and lichens was higher in the Corynephorus-sward and in the Empetrum-heath. With increasing shrub cover, total vegetation cover increased in the Ammophiladune (Table 3). The cover of herbaceous species decreased with increasing shrub cover, both in the Ammophila-dune and the Corynephorus-sward; and the cover of mosses and lichens decreased in the Empetrum-heath. Species richness Total species richness was highest in the Corynephorus-sward (Table 1). The number of herbaceous species and typical grassland species was higher both in the Ammophila-dune and the Corynephorus-sward when compared with the Empetrum-heath and the Rosa-scrub. The lowest number of mosses and lichens occurred in the Ammophila-dune. The Corynephorus-sward contained more threatened species than the other vegetation types (mean Ammophila-dune 0.8, Corynephorus-sward 1.0, Empetrum-heath 0.1, Rosa-scrub 0.1, ANOVA F = 5.9, p < 0.001). The total number of species decreased with increasing cover of R. rugosa (Fig. 2a) and declined in all vegetation types, especially in the case of the Ammophiladune and the Corynephorus-sward (Table 3). In more detail, the number of typical grassland species decreased strongly with increasing cover of R. rugosa (Fig. 2b) and the number of typical shrubland species increased slightly (Fig 2c). The decrease in the number of lichens was more pronounced in the Empetrum-heath when compared to the other vegetation types with increasing shrub cover. In addition, in the Ammophila-dune and the Corynephorus-sward the number of threatened species declined with increasing cover of the R. rugosa. Effect on single species The majority of species such as Festuca arenaria and Viola tricolor L., decreased with increasing cover of R. rugosa (Table 4), also impacted were herbs, grasses, mosses as well as dwarf shrubs such as Empetrum nigrum. Furthermore, Phleum arenarium L. occurred only in areas without R. rugosa. Only Stellaria media (L.) Vill., which is a typical shrubland species, increased with increasing shrub cover. Species diversity In the Ammophila-dune and the Corynephorus-sward, the Shannon index was higher than in the Empetrum-heath and the Rosa-scrub, and evenness decreased from

7 22.qxd:Isserman_q5.qxd :10 Pagina 295 Effects of Rosa rugosa invasion in different coastal dune vegetation types 295 Table 1. Descriptive statistics of vegetation cover, number of species and species diversity (Shannon-index and evenness) in the four vegetation types. For each vegetation type presented is the mean, the standard deviation (SD), and mean separation results the F and p-value of the one-way-anova. Means followed by the same letter are not significantly different (Number of investigated plots: total 63, Ammophila-dune 8, Corynephorus-sward 10, Empetrum-heath 9, Rosascrub 36). Mean SD ANOVA Mean SD ANOVA Mean SD ANOVA Total cover (%) Total no. of species No. of grassland species F = 7.7 F = 9.2 F = 16.1 Ammophila-dune 85.5 a 14.4 p < Ammophila-dune 14.8 ab 3.8 p < Ammophila-dune 10.8 a 4.8 p < Corynephorus-sward 95.6 b 6.4 Corynephorus-sward 18.4 b 4.1 Corynephorus-sward 15.0 a 4.6 Empetrum-heath b 0.0 Empetrum-heath 11.7 ac 3.5 Empetrum-heath 8.0 ab 2.9 Rosa-scrub 97.8 b 5.6 Rosa-scrub 11.5 ac 3.9 Rosa-scrub 5.8 a 3.6 Cover of shrubs (%) No. of shrubs No. of shrubland species F = 40.6 F = 2.1 F = 3.4 Ammophila-dune 33.1 a 31.4 p < Ammophila-dune 1.8 a 1.5 p = Ammophila-dune 3.4 ab 1.8 p = Corynephorus-sward 4.8 a 9.4 Corynephorus-sward 0.8 a 0.9 Corynephorus-sward 2.4 a 1.6 Empetrum-heath 13.6 a 29.3 Empetrum-heath 2.1 a 1.5 Empetrum-heath 3.0 ab 2.2 Rosa-scrub 80.8 b 22.9 Rosa-scrub 2.2 a 1.8 Rosa-scrub 4.9 b 3.0 Cover of herbaceous species (%) No. of herbaceous species Shannon-Index F = 31.0 F = 14.9 F = 8.2 Ammophila-dune 57.6 a 20.8 p < Ammophila-dune 12.1 a 4.3 p < Ammophila-dune 1.7 a 0.3 p < Corynephorus-sward 62.2 a 22.8 Corynephorus-sward 14.7 a 4.3 Corynephorus-sward 1.7 a 0.6 Empetrum-heath 4.0 b 4.5 Empetrum-heath 7.0 b 2.8 Empetrum-heath 1.1 b 0.3 Rosa-scrub 13.8 b 18.3 Rosa-scrub 7.4 b 3.1 Rosa-scrub 1.0 b 0.4 Cover of mosses, lichens (%) No. of mosses, lichens Evenness F = 12.9 F = 3.2 F = 5.8 Ammophila-dune 6.3 a 6.4 p < Ammophila-dune 0.9 a 0.9 p = Ammophila-dune 0.64 a 0.06 p = Corynephorus-sward 31.7 b 26.5 Corynephorus-sward 2.9 b 1.6 Corynephorus-sward 0.56 ab 0.18 Empetrum-heath 56.8 c 25.5 Empetrum-heath 2.6 b 1.5 Empetrum-heath 0.45 b 0.09 Rosa-scrub 17.3 ab 16.9 Rosa-scrub 1.9 b 1.6 Rosa-scrub 0.43 b 0.14

8 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann Fig. 2 (a) Relationship between the total number of species and the percent cover of Rosa rugosa (b = 0.07, R 2 adj = 0.33, p < 0.001, n = 63). (b) Regression between both typical grassland species and (c) typical shrubland species and the cover of R. rugosa in different habitat types (statistics see Table 3).

9 22.qxd:Isserman_q5.qxd :10 Pagina 297 Effects of Rosa rugosa invasion in different coastal dune vegetation types 297 the Ammophila-dune across the Corynephorus-sward to the Empetrum-heath and the Rosa-scrub (Table 1). Shannon-index and evenness declined linearly both in the Ammophila-dune and the Corynephorus-sward; but in the species-poor Empetrumheath, which was dominated by one species, there was a quadratic relationship (Table 3). Environment In general, relative irradiance decreased with increasing cover of R. rugosa (Fig. 3), but at low levels of shrub cover, there was no apparent effect. At approximately 20% cover, the light availability decreased strongly, and if the cover of R. rugosa reached 45 to 50%, relative irradiance was lower than 10%. Furthermore, there were no differences in relative light availability in the Rosa-scrub established in different vegetation types. The shading by R. rugosa was more pronounced than that of H. rhamnoides (Fig. 3). In the case of H. rhamnoides, the relative irradiance decreased to 20%, but in the case of R. rugosa the decrease was greater. The four vegetation types were characterized by different soil parameter values (Table 2). Carbon and water content were higher in the Empetrum-heath than in the Ammophila-dune as well as in the Corynephorus-sward and tended to be higher also in the Rosa-scrub. Likewise soil ph of Rosa-scrub was lower than in the Ammophila-dune and the Corynephorus-sward, and higher than in the Empetrumheath. Soil nitrogen content was highest in the Empetrum-heath. In general soils between shrubland and reference plots were quite similar. However, in the grey dunes, the water and carbon content of the Rosa-scrub were higher than in the related Corynephorus-sward (paired t-test, mean water (%) sward 0.49, scrub 0.87, t = -2.93, p = 0.015; mean carbon (%) sward 1.04, scrub 2.12, t = -2.52, p = 0.030). Fig. 3. Relationship between relative irradiance (ln %) and the cover of Hippophaë rhamnoides and Rosa rugosa (H. rhamnoides R 2 adj = 0.46, p < 0.001, n = 24, R. rugosa R2 adj = 0.69, p < 0.001, n = 58). Data of H. rhamnoides based on Isermann et al. (2005).

10 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann Table 2. Descriptive statistics of soil parameters in the four vegetation types. For each vegetation type presented is the mean, the standard deviation (SD), and mean separation results the F and p- value of the one-way-anova. Means followed by the same letter are not significantly different (Number of investigated plots: total 63, Ammophila-dune 8, Corynephorus-sward 10, Empetrumheath 9, Rosa-scrub 36). Mean SD ANOVA ph (CaCl 2 ) Ammophila-dune 5.9 a 0.8 F = 5.1 p = Corynephorus-sward 4.4 b 0.7 Empetrum-heath 3.8 b 0.3 Rosa-scrub 4.7 ab 0.9 Water content (%) Ammophila-dune 0.3 a 0.4 F = 4.3 p = Corynephorus-sward 0.3 a 0.2 Empetrum-heath 1.3 b 0.8 Rosa-scrub 0.6 ab 0.5 Carbon (%) Ammophila-dune 0.4 a 0.5 F = 3.8 p = Corynephorus-sward 0.8 a 0.4 Empetrum-heath 4.8 b 5.1 Rosa-scrub 1.9 ab 1.8 Organic matter (%) Ammophila-dune 4.9 a 0.1 F = 0.9 p = Corynephorus-sward 4.1 a 1.6 Empetrum-heath 4.5 a 0.5 Rosa-scrub 5.1 a 1.6 Nitrogen (%) Ammophila-dune 0.03 a 0.04 F = 3.1 p = Corynephorus-sward 0.06 a 0.02 Empetrum-heath 0.22 ab 0.17 Rosa-scrub 0.12 a 0.11 Discussion Environment The light availability beneath Rosa-scrub decreased strongly with increasing shrub cover. A similar negative exponential function was found in the case of Californian scrub, where light transmission declines sharply with horizontal distance inside the edge of shrub canopies (Alpert & Mooney 1996). Comparing grass and shrubland, light availability is generally lower beneath scrub, e.g. in the case of Myrica pensylvanica-scrub (Shumway 2000). Broad-leaved shrubs like R. rugosa shade more than small-leaved ones such as H. rhamnoides, therefore the effect of broad-leaved, especially evergreen shrubs like Rhododendron ponticum L. (Erfmeier & Bruelheide 2004) can be even greater. Different shading effects of broad and small leaf species also occur between Potentilla fruticosa and Juniperus communis in Sweden (Rejmánek & Rosén 1988,

11 22.qxd:Isserman_q5.qxd :10 Pagina 299 Effects of Rosa rugosa invasion in different coastal dune vegetation types 299 Table 3. Relationships between species richness, vegetation cover, species diversity and shrub cover of each vegetation type. Linear and quadratic regressions were compared, and significantly improved quadratic relations are shown in the second row (number of observations: Ammophiladune 18, Corynephorus-sward 24, Empetrum-heath 21; b = slope of linear regression; R 2 adj. = regression coefficient, p = probability) Significant relations are in bold. Ammophila-dune Corynephorus-sward Empetrum-heath b R 2 adj. p b R 2 adj. p b R 2 adj. p Total no. of species < < No. of herbaceous species < < No. of mosses, lichens No. of red-list-species < No. of shrubland species No. of grassland species < < Total cover Cover herbaceous species < < Cover mosses, lichens <0.001 Shannon-Index Shannon quadratic relation Evenness Evenness quadratic relation Relative irradiance < <0.001 ln relative irradiance < <0.001 Table 4. Effect of Rosa rugosa on the dominance of plant species in dunes (n = number of observations, b = slope of regression, R 2 adj. = regression coefficient, p = significance). n b R 2 adj. p Empetrum nigrum Festuca arenaria Galium album Hypnum jutlandicum Poa pratensis Veronica arvensis Viccia cracca Viola tricolor Stellaria media ). It is clear, that different shrub species affect the decline of light in different ways. Increasing Potentilla fruticosa causes a greater loss of species than increasing Juniperus communis (Rejmánek & Rosén 1988, 1992; Isermann et al. 2007). In addition, it should be considered that the relative proportion of thorny and evergreen species increases with the degree of invasiveness (Binggeli 1996). Rosa rugosa can become naturalized on various dune types, and soil parameters of the stands have a wide range. In comparison with other regions of Europe, soil ph of Rosa-scrub was similar (Bruun 2005) and in dunes it is comparable with that of the Corynephorus-sward. Therefore, open grey dunes are probably very endangered

12 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann by R. rugosa invasion. In contrast, Kollmann et al. (2007) showed that seedling emergence of R. rugosa, with the exception of undisturbed sites, was lowest in disturbed lichen-rich Corynephorus-sward and in Empetrum-heath. Considering that arbuscular mycorrhizae occurs with R. rugosa, the establishment, e.g. in Ammophila-dunes is encouraged, if soils already contain arbuscular mycorrhizae (Gemma & Koske 1997). On the other hand many introduced plants fail in the absence of mycorrhizal fungi or nitrogen-fixing bacteria (Richardson 2001). In contrast to nitrogen-fixing shrubs such as Myrica pensylvanica, Porlieria chilensis and Hippophaë rhamnoides (Pearson & Rogers 1962, Gutiérrez et al. 1993, Shumway 2000), only the total nitrogen content of Rosa-scrub in grey dunes was higher than in the reference plot. A similar result was also shown in the case of R. rugosa, which had invaded Carex arenaria grey dunes in Belgium (Vanderhoeven et al. 2005), although at the Belgian site soil ph was higher (7.02 KCl). Likewise total nitrogen in the topsoil was higher beneath the non-nitrogen-fixing Crataegus monogyna in dunes of Great Britain (Hodgkin 1984). Although it seems that there is a general trend of increased mineral nutrients in the topsoil under invasive species (Vanderhoeven et al. 2005), and it is important to distinguish among different habitats. Species composition and vegetation cover Rosa rugosa became naturalized in all studied dune types. The rather uniform soil parameters and the clear differentiation of the R. rugosa plots from the other vegetation types indicate that this shrubland occurs as a separate plant community. In all dune types, species number decreased with increasing cover of R. rugosa. However, the cover of herbs and grasses in general did not decrease in any dune vegetation type. Only the cover of the dominant vegetation layers decreased with increasing R. rugosa-scrub: this involved herbs and grasses in the Ammophila-dune and in the Corynephorus-sward, mosses and lichens in the Empetrum-heath. The stronger elimination effect on dominant life forms of the vegetation is also known from fynbos communities of South Africa (Richardson & Van Wilgen 1986). One important factor in the replacement of dune heath is probably root competition between Empetrum nigrum and R. rugosa. Both species have a shallow root system and occupy similar soil depths (Bell & Thallis 1973, Bruun 2005). Root competition for water is also observed between the invasive Carpobrotus edulis (L.) N.E. Br. and the native shrubs Haplopappus ericoides (Less.) Hook. & Arn. and H. venetus var. sedoides (Greene) Munz in Californian coastal areas (D Antonio & Mahall 1991), where the native shrubs (in response to alien invasion) shift their roots to a soil depth with lower water content. Species richness In general, in all dune types, species numbers of the characteristic vegetation declined with increasing R. rugosa. Nevertheless, it is necessary to distinguish between the vegetation types, because the intensity of the effects differed. For example, the decline of the number of typical grassland species was more noticeable in the Ammophila-dune and the Corynephorus-sward than in the Empetrum-

13 22.qxd:Isserman_q5.qxd :10 Pagina 301 Effects of Rosa rugosa invasion in different coastal dune vegetation types 301 heath. Differences in the degree of decline amongst habitat types is also known from the invasion by Delairea odorata Lem., an invasive evergreen vine, in woody vegetation of coastal California (Alvarez & Cushman 2002). However, overall species richness declined in each habitat type with increasing cover of the vine. The general relationship between reduction of species richness and shrub cover occurs in different ecosystems. Examples include the shrub invasion of Porlieria chilensis in coastal grasslands of Chile (Gutiérrez et al. 1993) and the invasion of alien shrubs and trees in the fynbos biome in the Cape Province, South Africa (Richardson et al. 1989). Furthermore, there is a linear decrease in the number of native plant species with up to 40% evergreen vine cover in the woody vegetation of coastal California (Alvarez & Cushman 2002). In addition to these general relations, there are different effects among functional groups, e.g. the number of typical grassland species declined and typical shrubland species increased with increasing cover of R. rugosa. Likewise, there is a negative relationship between the richness of herbaceous species in grassland and the cover of woody species in coastal sage scrub in California (Sax 2002). Other functional groups also show clear results: annuals were more abundant in open habitats and perennials more in scrub of coastal sand dune areas of Israel (Kutiel et al. 2000). In the German coastal dunes, vulnerable vegetation is endangered and typical dune species like Phleum arenarium, Veronica arvensis L. and Viola tricolor are displaced by R. rugosa. Moreover Empetrum-heath is endangered by the invasion of R. rugosa as well, and it should be noticed that heath and dry grassland habitats are the most invaded sites e.g. in Southwest Denmark (Vogt Andersen 1997). Invasiveness of Rosa rugosa The invasiveness of a species depends on different parameters (Drake & Mooney 1989). Rosa rugosa and Elaeagnus angustifolia L. (also planted in dunes) are salttolerant (Dirr 1978) and tolerant to sand cover (Belcher 1977). Both of these factors are important for establishment in coastal dune areas. Seeds of R. rugosa can germinate after being immersed for 6 weeks in 2.4 % sea water (Jessen 1958). Spread by vegetative tillers and dispersal by seeds, possibly long distance distribution by birds and sea currents, are effective in supporting the invasiveness of R. rugosa. In the case of Berberis thunbergii DC., invasiveness is also supported by a combination of vegetative and seed-based population growth (Ehrenberg 1999). Some attributes of R. rugosa are characteristic of other invasive woody species: dispersal by birds, a shrub height lower than 5 m and thorniness (Binggeli 1996). In addition, the ability to grow in a wide range of environmental situations supports the invasion of species. For example, the alien Berberis thunbergii replaces the native Berberis vulgaris L. in forests in the United States, grows under a broader range of light and soil moisture conditions than the native species (Silander & Klepeis 1999). Rosa rugosa also has a broad adaptability and because of its winter hardiness it grows throughout the north central United States (Epping & Hasselkus 1989, Widrlechner et al. 1998). Hybridization could strengthen invasion potential (Vilà et al. 2000). Along coastal areas different cultivars, variations and hybrids with native roses occur (Mang 1985, Epping & Hasselkus 1989, Eigner 1998, Nilsson 1999) that may help

14 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann support the success of alien species. Other examples include hybrids (R. majalis rugosa Thunb. ex. Murray, R. davurica Pall. rugosa Thunb. ex. Murray), which have become naturalized in Finland, following garden escapes (Palmén et al. 1996). The lack of herbivores in the invaded region or other animals able to damage R. rugosa probably is also a reason for its successful invasion (Bruun 2006). On the other hand, in Canada and the northern United States two species of gall-inducing wasps, normally found only on a native rose, attack R. rugosa (Bagatto et al. 1991). Because of the successful invasion and growth, Prunus serotina Ehrh., Pinus mugo Turra agg. and R. rugosa are the most widespread woody species in southwest Denmark (Vogt Andersen 1997). In addition, climatic change, especially the rise of temperatures, supports the northward distribution of species, such as the distribution of Beta maritima L., Crambe maritima L., Lepidium latifolium L. and R. rugosa in the coastal zone of South and West Norway (Lundberg 1996). The establishment process of R. rugosa in Germany has already overcome many environmental barriers; hence, the invasion in natural and semi-natural ecosystems is possible (Williamson 1999, Richardson et al. 2000b). Rosa rugosa-scrub changes the character, condition, form and nature of parts of the dune ecosystem. The species is one that can transform the environment not only by causing reduced light conditions but also as a sand stabilizer (Richardson et al. 2000a, Pyšek et al. 2004). The complete change of a community structure is further shown by the invasion of the shrub Baccharis pilularis into Californian grassland (Hobbs & Mooney 1986). In European dunes other woody invasive species occur that eliminate native, endangered species through competition, for example Acer pseudoplatanus L., Hippophaë rhamnoides, and Rhododendron ponticum (Martínez & García-Franco 2004). The planting of alien, especially woody species, in the NW-European region such as Amorpha fruticosa L., Elaeagnus angustifolia, Elaeagnus commutata Bernh. Ex Rydb., R. rugosa or Shepherdia argentea (Pursh) Nutt. or even some Populus species (Weeda 1987), often displaces native plant species in dunes. Invasibility of dune vegetation Invasibility of plant communities depends not only on the qualities of the successful invader (Rejmánek & Richardson 1996), but also on the invasibility of the community. This has a crucial influence on the process from initial establishment, through natu ralization to full-scale invasion (Drake & Mooney 1989). Attributes of environment and communities, such as species richness, nutrient status and disturbance regime can be determining factors of the invasibility (Drake & Mooney 1989, Levine & D Antonio 1999). The degree of disturbance to the ecosystem is one of the elementary drivers of plant invasions (Richardson 2001). Because of the dynamic nature of coastal dunes they are particularly prone to invasion (Martínez & García-Franco 2004). Nature conservation In the case of the German dune grassland, with increasing cover of R. rugosa, species richness and the number of rare species declined, which is also known from lichen-rich grey dunes on the isle of Anholt, Denmark (Christensen & Johnsen 2001). Similar negative effects of shrub invasion exist in Swedish alvar vegetation

15 22.qxd:Isserman_q5.qxd :10 Pagina 303 Effects of Rosa rugosa invasion in different coastal dune vegetation types 303 (Rejmánek & Rosén 1992). Scrub communities vary from relatively common, species-poor types through species-rich or rare shrubland types of great ecological interest; especially on calcareous dunes which are species-rich (Hopkins 1996, Mortimer et al. 2000). Rosa rugosa develops into a shrubland type with a low conservation value, because it becomes the single dominant species. The resulting R. rugosa community also has a simple three-dimensional vegetation structure with uniform height, canopy shape and age without gaps. Gaps in the shrub canopy are important microhabitats for the establishment of herbaceous plants, particularly those which are sensitive to competition for light (Petrů & Menges 2003). At landscape scales, plant species richness increases with moderate levels of disturbance, combined with high levels of habitat heterogeneity (Deutschewitz et al. 2003). The development of large, dominant Rosa-scrub reduces not only the species diversity, but also the landscape diversity of the dunes. Hence invasion of R. rugosa-scrub or other species-poor scrub into coastal dune vegetation, particularly into dry coastal grasslands with many rare species or notable species richness, poses a serious conservation problem. Encouraging the use of native species for dune stabilization, prohibition of planting alien species on dunes and a restriction of expansive species of species-poor shrubland types on dunes should be supported. Acknowledgements I express my thanks for advice in statistical questions to Martin Diekmann (Germany), for critical comments to two anonymous reviewers, furthermore to Hans Henrik Bruun (Sweden), Johannes Kollmann (Denmark), Silke Lütt (Germany) and David M. Richardson (South Africa) for posting articles and giving literature hints and for personal information to Julio R. Gutiérrez (Chile). I especially thank Pat Doody (UK) for the thorough linguistic revision of the manuscript. References Anon MINITAB. Minitab Inc., State College, PA. Alpert, P. and Mooney, H.A Resource heterogeneity generated by shrubs and topography on coastal sand dunes. Vegetatio 122: Alvarez, M.E. and Cushman, J.H Community-level consequences of a plant invasion: Effects on three habitats in coastal California. Ecological Applications 12: Bagatto, G., Zmijowskyj, T. and Shorthouse, J.D Galls induced by Diplolepis spinosa influence distribution of mineral nutrients in the shrub rose. Hortscience 26: Bell, J.N.B. and Thallis, J.H Biological flora of the British Isles. Empetrum nigrum L. Journal of Ecology 61: Belcher, C.R Effect of sand cover on the survival and vigor of Rosa rugosa Thunb. International Journal of Biometeorology 31: Berg, C., Dengler, J. and Abdank, A. (eds.) Die Pflanzengesellschaften Mecklenburg- Vorpommerns und ihre Gefährdung. Tabellenband. Weissdorn-Verlag, Jena. Binggeli, P A taxonomic, biogeographical and ecological overview of invasive woody plants. Journal of Vegetation Science 7: Böcher, T.W Vegetationsudvikling i forhold til marin akkumulation. I. Korshage ved indløbet til Isefjord. Botanisk Tidsskrift 49: Bruun, H.H Biological flora of the British Isles. Rosa rugosa Thunb. ex Murray. Journal of Ecology 93:

16 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann Bruun, H.H Prospects for biocontrol of invasive Rosa rugosa. Biocontrol 51: Christensen, S.N. and Johnsen, I The lichen-rich coastal heath vegetation on the isle of Anholt, Denmark conservation and management. Journal of Coastal Conservation 7: Council of the European Commission Council directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Official Journal of the European Communities. Series L. 206: D Antonio, C.M. and Mahall, B.E Root profiles and competition between the invasive exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. American Journal of Botany 78: Deutschewitz, K., Lausch, A., Kühn, I. and Klotz, S Native and alien plant species richness in relation to spatial heterogeneity on a regional scale in Germany. Global Ecology and Biogeography 12: Dijkema, K.S. and Wolff, W.J. (eds.) Flora and vegetation of the Wadden Sea and coastal areas. Report 9, Wadden Sea Working Group. Balkema, Rotterdam. Dirr, M.A Tolerance of seven woody ornamentals to soil-applied sodium chloride. Journal of Arboriculture 4: Drake, J.A. and Mooney, H.A. (eds.) Biological invasions: a global perspective. Wiley, Chichester. Dubra, J. and Olšauskas, A The main problems of the protection of the sand coasts in Lithuania. In: Gomes, V. (ed.), Littoral The changing coast. Vol. 3, pp EURO- COAST / EUCC, Porto. Dunwiddie, P.W Long-term effects of sheep grazing on coastal sandplain vegetation. Natural Areas Journal 17: Ehrenberg, J.G Structure and dynamics of populations of Japanese barberry (Berberis thunbergii DC.) in deciduous forests of New Jersey. Biological Invasions 1: Eigner, J Problems with the neophyt R. rugosa in dune landscapes of Schleswig-Holstein. In: Hilgerloh, G. (ed.), Proceedings of the Third Trilateral Working Conference on Dune Management in the Wadden Sea Area, pp Mettker & Söhne, Wilhelmshaven. Eigner, A Hybridisierung zwischen Rosa mollis (?) und R. rugosa auf der Geltinger Birk in Schleswig-Holstein. Acta Rhodologica 1: Epping, J.E. and Hasselkus, E.R Spotlight on shrub roses. American Nurseryman 170: Erfmeier, A. and Bruelheide, H Comparison of native and invasive Rhododendron ponticum populations: Growth, reproduction and morphology under field conditions. Flora 199: Gemma, J.N. and Koske, R.E Arbuscular mycorrhizae in sand dune plants of the North Atlantic Coast of the U.S.: Field and greenhouse inoculation and presence of mycorrhizae in planting stock. Journal of Environmental Management 50: Gutiérrez, J.R., Meserve, P.L., Contreras, L.C., Vásquez, H. and Jaksic, F.M Spatial distribution of soil nutrients and ephemeral plants underneath and outside the canopy of Porlieria chilensis shrubs (Zygophyllaceae) in arid coastal Chile. Oecologia 95: Hansen, K. and Vestergaard, P Initial establishment of vegetation in a man-made coastal ecosystem in Denmark. Nordic Journal of Botany 6: Herloff, B Floraförändringar i Göteborgs södra skärgård under 1900-talet. (Floristic changes during the twentieth century in the southern archipelago of Göteborg, SW Sweden). Svensk Botanisk Tidskrift 97: Hobbs, R.J. and Mooney, H.A Community changes following shrub invasion of grassland. Oecologia 70: Hodgkin, S.E Scrub encroachment and its effects on soil fertility on Newborough Warren, Anglesey, Wales. Biological Conservation 29: Hopkins, J Scrub ecology and conservation. British Wildlife 8: Isermann, M. and Cordes, H Changes in dune vegetation on Spiekeroog (East Frisian Islands) over a 30 year period. In: Carter, R.W.G., Curtis, T.G.F. and Sheehy-Skeffington, M.J. (eds.), Coastal dunes. Geomorphology, ecology and management for conservation, pp Balkema, Rotterdam. Isermann, M., Friedrichs, L., Grave, C. and Wagner, A Species richness in Sea-Buckthorn scrub. In: Herrier J.-L., Mees, J., Salman, A., Seys, J., Van Nieuwenhuyse, H. and Dobbelaere, I. (eds), Proceedings Dunes and Estuaries International Conference on Nature Restoration. Practices in European Coastal Habitats, pp Koksijde, Belgium. Isermann, M., Diekmann, M. and Heemann, S Effects of the expansion by Hippophaë rhamnoides on plant species richness in coastal dunes. Applied Vegetation Science 10:

17 22.qxd:Isserman_q5.qxd :10 Pagina 305 Effects of Rosa rugosa invasion in different coastal dune vegetation types 305 Jessen, K Om vandspredning af Rosa rugosa og andre arter af slægten. (On hydrochorous dissemination of Rosa rugosa and other species of the genus). Botanisk Tidsskrift 54: Kollmann, J., Frederiksen, L., Vestergaard, P. and Bruun, H.H Limiting factors for seedling emergence and establishment of the invasive non-native Rosa rugosa in a coastal dune system. Biological Invasions 9: Koperski, M., Sauer, M., Braun, W. and Gradstein, S.R Referenzliste der Moose Deutschlands. Schriftenreihe für Vegetationskunde 34: Kowarik, I Biologische Invasionen: Neophyten und Neozoen in Mitteleuropa. Ulmer. Stuttgart. Kutiel, P., Peled, Y. and Geffen, E The effect of removing shrub cover on annual plants and small mammals in a coastal sand dune ecosystem. Biological Conservation 94: Levine, J.M. and D Antonio, C.M Elton revisited: A review of evidence linking diversity and invasibility. Oikos 87: Lundberg, A Environmental change and nature management in Norway. Norsk Geografisk Tidsskrift 50: Mang, F Einige Bemerkungen über die Schädliche Rose, Rosa rugosa Thunb. in Schleswig-Holstein und Hamburg. Berichte des Botanischen Vereins Hamburg 7: Martínez, M.L. and García-Franco, J.G Plant-Plant interactions in coastal dunes. In: Martínez, M.L. and Psuty, N.P. (eds.), Coastal dunes: Ecology and conservation. Ecological Studies 171: McCune, B. and Mefford, M.J PC-ORD. Multivariate analysis of ecological data, Version 4. MjM Software Design, Gleneden Beach, Oregon, USA. Mortimer, S.R., Turner, A.J., Brown, V.K., Fuller, R.J., Good, J.E.G., Bell, S.A., Stevens, P.A., Norris, D., Bayfield, N. and Ward, L.K The nature conservation value of scrub in Britain. JNCC Report 308, JNCC, Peterborough. Nilsson, Ö Wild roses in Norden: Taxonomic discussion. Acta Botanica Fennica 162: Nordstrom, K.F., Lampe, R. and Vandemark, L.M Reestablishing naturally functioning dunes on developed coasts. Environmental Management 25: Østergaard, J Rosa rugosa. Botanisk Tidsskrift 50: Palmén, A., Hämet-Ahti, L. and Ahti, T Rosa glabrifolia, R. malyi, and other overlooked members of Rosa sect. Cassiorhodon (Rosaceae) as relicts of cultivation and established aliens in Finland. Acta Universitatis Upsaliensis Symbolae Botanicae Upsalienses 31: Pearson, M.C. and Rogers, J.A Biological flora of the British Isles. Hippophaë rhamnoides. Journal of Ecology 50: Petrů, M. and Menges, E.S Seedling establishment in natural and experimental Florida scrub gaps. Bulletin of the Torrey Botanical Club 130: Pyšek, P., Richardson, D.M., Rejmánek, M., Webster, G.L., Williamson, M. and Kirschner, J Alien plants in checklists and floras: towards better communication between taxonomists and ecologists. Taxon 53: Reichelt, G. and Wilmanns, O Vegetationsgeographie. Westermann, Braunschweig. Rejmánek, M. and Richardson, D.M What attributes make some plant species more invasive? Ecology 77: Rejmánek, M. and Rosén, E The effects of colonizing shrubs (Juniperus communis and Potentilla fruticosa) on species richness in the grasslands of Stora Alvaret, Öland (Sweden). Acta Phytogeographica Suecica 76: Rejmánek, M. and Rosén, E Influence of colonizing shrubs on species-area relationships in alvar plant communities. Journal of Vegetation Science 3: Richardson, D.M Plant invasions. In: Levin, S. (ed.). Encyclopaedia of biodiversity. Vol. 4. pp Academic Press, San Diego. Richardson, D.M. and Van Wilgen, B.W Effects of thirty-five years of afforestation with Pinus radiata on the composition of mesic mountain fynbos near Stellenbosch. South African Journal of Botany 52: Richardson, D.M., Macdonald, I.A.W. and Forsyth, G.G Reductions in plant species richness under stands of alien trees and shrubs in the fynbos biome. Southern African Forestry Journal 149: 1-8. Richardson, D.M., Allsopp, N., D Antonio, C.M., Milton, S.J. and Rejmánek, M. 2000a. Plant invasions the role of mutualisms. Biological Review 75: Richardson, D.M., Pyšek, P., Rejmánek, M., Barbour, M.G., Panetta, D.F. and West, C.J. 2000b. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6:

18 22.qxd:Isserman_q5.qxd :10 Pagina Maike Isermann Sax, D.F Native and naturalized plant diversity are positively correlated in scrub communities of California and Chile. Diversity and Distributions 8: Shumway, S.W Facilitative effects of a sand dune shrub on species growing beneath the shrub canopy. Oecologia 124: Silander, J.A. and Klepeis, D.M The invasion of Japanese barberry (Berberis thunbergii) in the New England landscape. Biological Invasions 1: Van der Meulen, F., Van der Hagen, H. and Kruijsen, B Campylopus introflexus. Invasions of a moss in Dutch coastal dunes. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen Series C 90: Van Dieken, J Beiträge zur Flora Nordwestdeutschlands unter besonderer Berücksichtigung Ostfrieslands. Mettcker & Söhne, Jever. Vanderhoeven, S., Dassonville, N. and Meerts, P Increased topsoil mineral nutrient concentrations under exotic invasive plants in Belgium. Plant and Soil 275: Vilà, M., Weber, E. and D Antonio, C.M.D Conservation implications of invasions by plant hybridisation. Biological Invasions 2: Vogt Andersen, U Invasive aliens: A threat to the Danish coastal vegetation? In: Healy, M.G. and Doody, J.P. (eds.), Directions in European coastal management, pp Samara Publishing Limited, Cardigan. Vogt Andersen, U Monitoring invasive weeds at landscape level in Denmark. In: Brock, J.H., Wade, M., Pyšek, P. and Green, D. (eds.), Plant invasions: Studies from North America and Europe, pp Backhuys Publishers, Leiden, The Netherlands. Weeda, E.J Invasions of vascular plants and mosses into the Netherlands. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen Series C 90: Widrlechner, M.P., Hebel, J.B., Herman, D.E., Iles, J.K., Kling, G.J., Ovrom, A.P., Pair, J.C., Paparozzi, E.T., Poppe, S.R., Rose, N., Schutzki, R.E., Tubesing, C. and Wildung, D.K Performance of landscape plants from northern Japan in the North Central United States. Journal of Environmental Horticulture 16: Williams, K., Hobbs, R.J. and Hamburg, S.P Invasion of an annual grassland in Northern California by Baccharis pilularis ssp. consanguinea. Oecologia 72: Williamson, M. (1999) Invasions. Ecography 22: 5-12.