effects of the expansion by hippophaë rhamnoides on plant species richness in coastal dunes

- EFFECTS OF THE EXPANSION BY HIPPOPHAË RHAMNOIDES ON PLANT SPECIES RICHNESS - 33Applied Vegetation Science 10: 33-42, 2007© IAVS; Opulus Press Uppsala.

Effects of the expansion by Hippophaë rhamnoides on plant species richness in coastal dunes

Isermann, Maike*; Diekmann, Martin & Heemann, Sonja

Vegetation Ecology and Conservation Biology, Department of Ecology and Evolutionary Biology, FB 2, University of Bremen, Leobener Strasse, DE-28359 Bremen, Germany;

*Corresponding author; Fax +49 421 2187052; E-mail [email protected]

AbstractQuestion: Is the expansion of Hippophaë rhamnoides in coastal dunes associated with a decline in plant species richness, and is this decline best described by a hump-backed relationship between species number and shrub cover?Location: Grey and yellow dunes on the East Frisian islands Spiekeroog and Norderney.Methods: Total plant species richness as well as the number of herbaceous and cryptogam species were determined in 2001 using plots of 16 m2 size. We compared shrubland plots with varying cover of Hippophaë with neighbouring dune grassland plots without shrubs as reference sites. Soil samples were collected to determine the values of some important edaphic variables (pH, organic matter, nitrogen).Results: The shrubland plots with Hippophaë had or tended to have lower soil pH and C/N ratios and higher contents of organic matter and nitrogen than the grassland plots. Total spe-cies richness was marginally significantly related to the cover of Hippophaë in a hump-backed manner on both islands. The pattern was more pronounced for mosses and lichens than for herbaceous species. For all species groups on Spiekeroog and for the herbaceous species on Norderney, the hump-backed relationship was much improved when using the difference in species number between shrubland and grassland plot as a dependent variable. Relationships could be improved by including the soil parameters as co-variables. Species richness was highest at moderate levels of shrub expansion, while it was much reduced in very dense shrubland. The decrease in species number is caused by the decline in grassland species typical of the open dunes, including some rare taxa.Conclusions: The expansion of Hippophaë rhamnoides is a serious threat to the plant species richness of open coastal dunes, and needs to be counteracted by management measures.

Keywords: Grassland species; Grazing; Hump-backed rela-tionship; Rabbit; Shrub expansion.

Abbreviations: Nor = Norderney; Spi = Spiekeroog.

Nomenclature: Wisskirchen & Haeupler (1998).

Introduction

Natural and semi-natural, open grasslands are among the most species-rich plant communities in Central and Northwest Europe. This applies especially to chalk grass-lands, but also to acidic grasslands of mountainous areas and coastal dunes. Many rare plant and animal species are largely confined to these habitats. In most grassland types, the high plant species richness is maintained by management measures such as moderate grazing or mowing, which keep the grasslands open, enable the establishment of small, light-demanding species and exclude or suppress large, potentially dominant species (Provoost et al. 2002; Hellström et al. 2003; Fynn et al. 2004). Any relaxation or the abandonment of grazing and mowing is usually associated with an increase in tall grasses and forbs. Eventually, abandoned semi-natural pastures and meadows are invaded by woody species – notably shrubs, but also trees and vines, a process which is drastically changing the vegetation structure and abiotic conditions. The colonization of open grasslands by shrubs is often perceived as a serious threat to biodiversity (Fuller & Boorman 1977), because small and light-demanding plants cannot survive inside a dense and dark shrubland and/or cannot compete with taller and more shade-tol-erant species. Declines in plant species richness were observed, for example, in alvar grasslands of Sweden colonized by Juniperus communis and Potentilla fruti-cosa L. (Rejmánek & Rosén 1988, 1992), in grasslands of California invaded by Baccharis pilularis ssp. con-sanguinea (Williams et al. 1987), and in dry grasslands of continental Canada colonized by Populus tremuloides (Schwarz & Wein 1997). A decrease in plant species rich-ness caused by an expansion of shrubs was, for example, reported from the fynbos biome in the Cape Province of South Africa (Richardson et al. 1989), from coastal California (Alvarez & Cushman 2002), and from Ohio (Gould & Gorchov 2000; Collier et al. 2002). However, the evidence is not unequivocal: in semi-natural pastures of Sweden, increasing proportions of shrubs and trees had

34 ISERMANN, M. ET AL.

positive effects on the animal and plant species richness on a local scale (Söderström et al. 2001). A moderate level of shrub encroachment can be accompanied by an increase in species number (Rejmánek & Rosén 1988), indicating that the extent of shrub expansion has to be taken into account. In the dune systems of the Wadden Sea islands of Northwest Europe, grey dune grasslands represent a formerly widely distributed vegetation type. Grey dunes are characterized by an open, species-rich grassland veg-etation with Carex arenaria, Corynephorus canescens, Festuca rubra ssp. arenaria and various perennial herbs, e.g. Jasione montana, as well as annual species, e.g. Ph-leum arenarium, inhabiting bare patches of sand. Many regionally rare species, such as Anthyllis vulneraria ssp. maritima, Cerastium diffusum, Eryngium maritimum, Rhinanthus minor and Vicia lathyroides, are restricted to semi-fixed grey dunes (Garve 2004). The conservation of grey dune grasslands is an important task, because of their restricted coastal occurrence, their semi-natural conditions and high plant species richness. Therefore, they represent a priority habitat type of the EU Fauna Flora Habitats Directive 92/43/EEC (Anon. 1992). Aims of the directive are the preservation, protection and im-provement of the quality of the environment, including the conservation of natural and semi-natural habitats with their specific flora and fauna (Anon. 1992). Apart from coastal erosion, shrub expansion currently is one of the most serious threats to the grey dune vegetation of the Frisian Islands: For more than two centuries, shrubs with extensive root systems such as Rosa rugosa and Hippophaë rhamnoides have been planted for coastal protection and sand stabilization (Pearson & Rogers 1962; Meyer-Deepen & Meijering 1979). The expan-sion of shrubs was facilitated by a simultaneous decline in cattle grazing. On some islands, for example Norderney, this process was counteracted by dense populations of rab-bits. Where these are rare or were eliminated by hunting or myxomatosis, a considerable expansion of Hippophaë rhamnoides into the open dune areas has taken place (Fuller & Boorman 1977; Hodgkin 1984). On the island of Spiekeroog, for example, shrubland and heathland spread rapidly during the second half of the 20th century (Isermann & Cordes 1992). The main purpose of this study was to examine whether the expansion of Hippophaë rhamnoides in dunes affects plant species richness. Furthermore, we aimed to examine whether these effects differed between a grazed and an ungrazed dune system by comparing two islands with and without rabbits. We hypothesized that:1. A beginning colonization of shrubs will increase plant species richness, whereas the development of a dense shrub cover will result in a strong decline in plant species

richness. We therefore expected a hump-backed relation-ship between species number and shrub cover.2. The hump-backed pattern is less pronounced when the dunes are grazed by rabbits, because these will counteract the increase in tall-growing herbs associated with the expansion of Hippophaë.

Material and Methods

Hippophaë rhamnoides

Hippophaë rhamnoides is a deciduous shrub, occur-ring along the coasts of Northwest and Central Europe and throughout the mountain ranges of Europe and Asia. It is intolerant of shade (Pearson & Rogers 1962), but able to establish on nutrient-poor, sandy and gravelly soils with a high pH-value, including species-poor yellow dunes with Ammophila arenaria and Leymus arenarius and species-rich young grey dunes. Hippophaë is able to compete with herbs, grasses and low shrubs such as Salix repens, but not with trees and tall shrubs, because it does not tolerate shade (Pearson & Rogers 1962). Hav-ing established in herbaceous vegetation, the species can quickly increase in abundance and form dense thickets. Eventually, Hippophaë suffers from a gradual loss of vitality and is partly replaced by other shrub species such as Sambucus nigra and Rosa spp. (Oremus 1979). The expansion of dunes by Hippophaë rhamnoides causes a strong reduction in light intensity at the ground (Isermann et al. 2005) and, due to the ability of the species to fix nitrogen by means of a symbiosis with micro-organisms in root nodules, is likely to affect the nitrogen availability in the soil.

Sampling

The study was carried out on two Wadden Sea islands: Spiekeroog (21.3 km2 in size), since many decades devoid of rabbits, and Norderney (25.3 km2), inhabited by a dense rabbit population. Both islands are occupied by large dune areas showing a typical landward zonation: from the beach across the yellow dunes dominated by Ammophila arenaria, to the more stabilized grey dunes and, in the oldest parts, brown dunes characterized by dwarf-shrub heath with Empetrum nigrum. Field work took place between May and July 2001 and comprised the sampling of vegetation data and the collection of soil samples for chemical analysis. Vegetation data were collected in 16-m2 plots that were established predominantly in typical grey dunes, while only few were placed at the transition from the yellow to the grey dunes; for a survey of plots, see Table 1. The plots were laid out as to enclose the full range of

- EFFECTS OF THE EXPANSION BY HIPPOPHAË RHAMNOIDES ON PLANT SPECIES RICHNESS - 35

Hippophaë rhamnoides cover. In close vicinity of each Hippophaë shrubland plot, a neighbouring plot without shrubs – but otherwise being as similar as possible to the shrubland plot with respect to inclination and position along the dune slope – was analysed, in the following called grassland plot. In several cases, open spaces were reduced to such an extent that several shrubland plots had the same next available grassland plot as reference. In total, the number of shrubland plots on Spiekeroog and Norderney was 30 and 21, respectively, while 13 grassland plots were analysed on both islands (Table 1).We distinguished three vegetation strata: shrub layer, field layer with herbaceous plants and woody seedlings, and bottom layer with mosses and lichens (the latter being almost absent). Only epigeic mosses and lichens were taken into account. In each plot, we recorded the follow-ing variables: total cover of the vegetation layers (in %), percent cover of Hippophaë, and a list of all species with their cover degree according to a refined Braun-Blanquet scale (Reichelt & Wilmanns 1973). Soil samples were taken from the majority of plots (Table 1) and were composed of five soil cores from the upper 15 cm of the soil. Chemical analyses were con-ducted on the < 2 mm fraction of air-dried soil. Using standard techniques, we analysed soil pH (1:2.5 soil:H2O ratio), total nitrogen (Kjeldahl-method, mean of two replicates) and organic matter (as loss on ignition at 550 °C for 24 h, mean of two replicates; for details, see Steubing & Fangmeyer 1992).

Statistical analysis

The values for soil variables, plant cover and species number all showed a normal or regular distribution, and we therefore applied parametric methods in the statistical analysis. Differences in vegetation parameters and soil variables between grassland and shrubland sites were analysed with paired t-tests (comparing the shrubland plots with the corresponding grassland plots), as the data were collected in a pairwise design. This means that some of the ʻreference ̓grassland plots were used repeatedly in one and the same t-test, but we are convinced that this procedure was less problematic than the use of an un-paired t-test with unbalanced numbers of shrubland and grassland plots. The inter-correlation between soil factors was tested with Pearson correlation analysis.

To examine the impact of the cover of Hippophaë on species richness, regression analysis was applied. First, linear models were applied and the R2

adj values noted. Then, the quadratic term was added in a stepwise regression (back- and forward selection of variables, α = 0.05) to check whether it significantly added to the overall model. In addition, the relationship between species number and shrub cover was corrected for the effects of the measured soil parameters that were entered into the models as co-variables. A further refinement of the statistical analysis was made based on the following reflection: if Hippophaë tends to establish preferably on dune sites with specific abiotic conditions, the difference in the number of species between shrubland and grassland sites may not only reflect the effects of the shrub, but also those of differences in the primary environmental conditions. Therefore, we subtracted the number of spe-cies in the shrubland plot from the number of species in the corresponding grassland plot and conducted new regression analyses by relating this relative value to the cover of Hippophaë. To examine whether Hippophaë rhamnoides affected typical dune species and elements of other habitat types differently, all species were classified either as grassland species, shrubland species, or species with indifferent habitat requirements. This classification was based on the species ̓frequencies in synoptic tables of the vegetation classes Koelerio-Corynephoretea and Rhamno-Prunetea according to Berg et al. (2001). We also analysed the effect of Hippophaë cover on the cover of single plant species using linear regression analysis. To interpret the results ecologically, information on important species traits was extracted from the literature: mean height (Jäger & Werner 2002), ecological CRS-strategy (Klotz et al. 2002) and Ellenberg values for light (L) and nitrogen (N) (Ellenberg et al. 1991). All statistical analyses were carried out with the program MINITAB. To assess the general differences in species compo-sition between shrubland and grassland sites as well as between the islands, we applied Detrended Correspond-ence Analysis (DCA) on the total plot data set excluding Hippophaë rhamnoides, running PC-ORD (McCune & Mefford 1999) with its default options. The relative importance of Hippophaë and the environmental factors on the variation in species composition was examined by correlating the respective plot values with their cor-responding ordination scores along axes 1 and 2.

Table 1. Survey of the number of studied plots. Grassland: Grassland sites Grey-dune grassland sites Shrubland sites reference sites in yellow dunes No. plots No. soil samples No. plots No. soil samples Spiekeroog 13 2 11 9 30 17Norderney 13 3 10 10 21 13


Table 2. Number of species and values of soil variables in the two habitat types grassland and shrubland on the islands of Spiekeroog and Norderney. Mean, standard deviation (SD) and the number of observations (n) are shown. Species numbers in grasslands and shrublands are compared by paired t-tests, with significant results given in bold.

Grassland Shrubland Paired t-test Mean SD n Mean SD n t P

Spiekeroog Species number: total 22.0 9.7 13 20.1 8.5 30 0.83 0.416 Shrubs 0.8 0.9 13 2.0 1.1 30 -6.0 <0.001 Herbaceous species 18.1 8.0 13 16.2 7.4 30 1.47 0.155 Mosses & lichens 3.1 2.3 13 2.5 1.8 30 1.17 0.255 Grassland species 17.2 8.5 13 13.3 6.6 30 2.30 0.031 Shrubland species 3.2 2.5 13 5.9 3.2 30 –4.28 <0.001 Indifferent species 1.6 1.0 13 1.5 1.2 30 0.51 0.612 Soil parameters pH (H2O) 6.6 0.1 9 6.5 0.6 17 0.98 0.350 Organic matter [%] 0.5 0.3 9 0.7 0.4 17 -2.29 0.043 Total nitrogen [%] 0.01 0.008 9 0.02 0.014 17 -2.97 0.013 C/N ratio 47.6 30.8 9 37.3 18.1 17 2.61 0.024

Norderney Species number: total 21.2 5.7 13 22.3 4.3 21 –0.93 0.370 Shrubs 0.7 0.7 13 2.1 1.0 21 –6.55 <0.001 Herbaceous species 13.7 3.7 13 15.0 2.4 21 1.57 0.139 Mosses & lichens 6.8 4.3 13 5.2 3.1 21 1.93 0.073 Grassland species 17.0 4.4 13 14.9 3.7 21 1.88 0.081 Shrubland species 2.3 1.7 13 5.5 2.6 21 –4.93 <0.001 Indifferent species 1.8 0.9 13 1.9 0.7 21 –0.37 0.719 Soil parameters pH (H2O) 6.1 1.1 10 5.8 1.1 13 3.30 0.008 Organic matter [%] 0.7 0.4 10 0.9 0.4 13 –1.21 0.255 Total nitrogen [%] 0.02 0.01 10 0.03 0.01 13 –3.02 0.013 C/N ratio 48.3 28.3 10 34.5 3.9 13 1.63 0.133

Table 3. Inter-correlation between soil variables in the shrub-land plots from Spiekeroog (Spi; n = 17) and Norderney (Nor; n = 13). Pearson correlation coefficients r and significance levels: *** = P < 0.001; ** = P < 0.01; * = P < 0.05).

Organic Total pH matter nitrogen (H2O) [%] [%] C/N ratio

pH (H2O) Spi - –0.727 ** –0.765 *** 0.656 **Nor - –0.696 ** –0.695 ** 0.504 Organic matter [%] Spi - 0.965 *** –0.638 **Nor - 0.987 *** –0.372 Total nitrogen [%] Spi - –0.715 **Nor - –0.503

Results

Soils

On Spiekeroog, soil pH was between 5.2 - 7.5 (mean: 6.5) in the shrubland plots and 6.4 - 6.8 (6.6) in the grass-land plots (Table 2). On Norderney, pH ranged from 4.5 to 7.4 (5.7) and from 4.8 to 7.6 (5.9), respectively. For Norderney, the shrubland plots had significantly lower pH values than the corresponding grassland plots. Organic matter content was generally low, usually < 1% (Table 2). The values were (Spiekeroog) or tended to be (Nor-derney) higher in the shrubland plots. The differences between the plot types were even more pronounced for the nitrogen content; the N-values were generally very low (mean values differing between 0.02 and 0.03%), but significantly higher in the shrubland plots than in the grassland plots on both islands. The opposite trend was observed for the C/N ratio that showed overall very high values, with means differing between 34.3 and 49.3 and an absolute plot minimum of 26.3. The soil variables were closely inter-correlated (Ta-ble 3): on both islands organic matter and total nitrogen were highly positively correlated with each other, and on Spiekeroog the two variables were negatively related to both pH and C/N ratio.

Species composition

The open grassland plots comprised both mature yellow dunes with species such as Ammophila arenaria and Leymus arenarius and typical grey dunes with Aira praecox, Carex arenaria, Festuca rubra ssp. arenaria, Hieracium umbellatum and Polytrichum spp. In the shrubland plots, Hippophaë rhamnoides by definition played a dominant role. The ordination diagram (Fig. 1) reveals that the position of plots along DCA axis 1 is


mainly explained by the variable island (r = 0.88, P < 0.001). The sample plot scores along axis 2, on the other hand, were best correlated with the cover of Hippophaë (r = 0.41, P < 0.001). The strong effect of Hippophaë rhamnoides on the species composition is also reflected in its correlation with the occurrence of single species (Table 4). Several herbaceous species significantly increased in abundance with increasing cover of Hippophaë, for example Cir-sium vulgare, Moehringia trinervia and Urtica dioica on Spiekeroog, and Festuca rubra ssp. arenaria and Phleum arenarium (the latter in a hump-backed man-ner) on Norderney. Negative effects of Hippophaë were observed only on Spiekeroog, for example in Arenaria serpyllifolia, Cerastium semidecandrum, Jasione mon-tana, Tortula ruralis and Viola tricolor. Species with a positive relationship to shrub cover on Spiekeroog were on average taller (unpaired t-test: t = 2.43, P = 0.036) and more N-demanding (t = 9.13, P < 0.001) than those with a negative relation (Table 4). They also tended to have lower Ellenberg L-values (t = –1.50, P = 0.167). With respect to ecological strategy, most species increasing with an increasing cover of Hippophaë had a competi-tive or mixed-competitive behaviour, while most species with a negative relation to Hippophaë behaved, fully or partly, as ruderals (Table 4).

Fig. 1. DCA ordination diagram of dune plots on the islands Spiekeroog (S) and Norderney (N), based on cover-weighted species data. Hippophaë rhamnoides is excluded from the analysis; n = 77 plots. Eigenvalues: axis 1 = 0.497, axis 2 = 0.283; gradient lengths: axis 1 = 3.055 and axis 2 = 3.597. The abundance of Hippophaë is reflected by the size of the plot symbols and given by the cover values in %.

Table 4. Effect of the cover of Hippophaë rhamnoides on plant species cover in dunes on the two islands Spiekeroog and Norderney; only species with significant responses on at least one of the islands are considered. For each species, mean height (Jäger & Werner 2002), the ecological CRS-strategy (Klotz et al. 2002) and the Ellenberg values for light (L) and nitrogen (N) (Ellenberg et al. 1991) are given. The regression statistics include the direction of the relationship, R2

adj and P values (significant values in bold). If the quadratic term in the polynomial model added significantly to the linear model, the R2

adj value is marked with an ʻaʼ. --- = species lacking or present in only one plot, * = no data.

Spiekeroog Norderney Linear Quadratic Linear Quadratic Mean Ecological height [cm] strategy L N R2

adj P R2adj P R2

adj P R2adj P

Cirsium vulgare 0.95 cr 8 8 + 0.15 0.006 0.29a 0.000 0 0.767 0 0.658Epilobium montanum 0.45 cs 4 6 + 0.07 0.054 0.10 0.046 --- --- --- ---Festuca rubra ssp. arenaria 0.48 c 8 3 0 0.399 0 0.015 + 0.21 0.004 0.20 0.013Leymus arenarius 0.90 c 9 6 + 0.09 0.030 0.07 0.092 --- --- --- ---Moehringia trinervia 0.20 csr 4 7 + 0.33 0.000 0.31 0.000 0.04 0.123 0.04 0.203Phleum arenarium 0.15 sr 8 3 0 0.345 0 0.401 + 0.09 0.044 0.21a 0.010Poa trivialis 0.70 csr 6 7 + 0.15 0.007 0.15 0.016 0 0.945 0.03 0.241Rubus caesius * c 6 7 + 0.09 0.030 0.07 0.087 0 0.357 0 0.580Rubus spp. * * * * + 0.09 0.031 0.08 0.072 + 0.09 0.044 0.21a 0.010Urtica dioica 0.90 c x 8 + 0.09 0.032 0.12 0.029 0.03 0.161 0.04 0.355Aira praecox 0.09 sr 9 1 - 0.14 0.008 0.15 0.015 0 0.926 0 0.932Ammophila arenaria 0.80 cs 9 5 - 0.12 0.014 0.10 0.042 0.01 0.250 0.09 0.094Arenaria serpyllifolia 0.17 r 8 x - 0.23 0.001 0.22 0.003 0 0.839 0 0.602Cerastium semidecandrum 0.12 r 8 x - 0.20 0.002 0.20 0.004 0.02 0.223 0.03 0.239Hieracium umbellatum 0.65 cs 6 2 - 0.10 0.024 0.08 0.080 --- --- --- ---Hypochaeris radicata 0.38 csr 8 3 - 0.14 0.008 0.14 0.018 --- --- --- ---Jasione montana 0.28 csr 7 2 - 0.09 0.029 0.08 0.066 --- --- --- ---Lotus corniculatus 0.24 csr 7 3 - 0.14 0.007 0.14 0.018 --- --- --- ---Luzula campestris 0.15 csr 7 2 - 0.15 0.006 0.18 0.008 0 0.999 0 0.896Rumex acetosella 0.20 csr 8 2 - 0.19 0.002 0.17 0.009 0 0.703 0 0.866Tortula ruralis * * * * - 0.10 0.023 0.13 0.025 0 0.382 0 0.523Viola tricolor 0.20 r 8 3 - 0.12 0.015 0.10 0.042 --- --- --- ---


Species number

The total number of species per plot varied between 6 and 40. The average values for the two islands and the two habitat types, however, were fairly similar (Table 2). Shrubs were by definition more frequent in the shrubland plots. On both islands, herbaceous species tended to be more frequent in shrubland plots. In contrast, mosses and lichens tended to be more numerous in the grassland plots. In both plot types, herbaceous species were, both in absolute and relative numbers, more frequent on Spie-keroog than on Norderney, whereas the reverse pattern was observed for mosses and lichens. When comparing numbers of species with different habitat preferences, a clear pattern emerged: as expected, species largely con-fined to shrubs and forests were far more frequent in the shrubland plots, while typical grassland species prevailed

in the grassland plots (significantly so on Spiekeroog, Table 5). Total species richness was marginally significantly related to the cover of Hippophaë rhamnoides in a hump-backed manner (Table 5), i.e. the number of species first increased and then declined again with increasing shrub cover. For the sub-group of herbaceous species, a similar trend was observed for Spiekeroog. The quad-ratic relationship was more pronounced for mosses and lichens on both islands (P < 0.05). When using the dif-ference in the number of species between shrubland and grassland plot as a dependent variable, there was a clear hump-backed pattern on Spiekeroog for all measures of species richness. For total species number and the number of herbaceous species (Fig. 2), the quadratic term was found to be significant. On Norderney, in contrast, the

Fig. 2. Relationship between the differ-ence in the number of herbaceous species between shrubland and grassland plots and the cover of Hippophaë rhamnoides, ana-lysed separately for Spiekeroog (left) and Norderney (right). For regression statistics, see Table 5.

Table 5. Relationship between species number (total, herbaceous species, mosses and lichens) and shrub cover in dunes of the two islands Spiekeroog and Norderney. Linear and quadratic regressions are compared; regression statistics as in Table 4. The models were improved in two ways: by correcting for the effects of co-variables (indicated by ʻCoVʼ), and by using, instead of species number, the difference (Diff.) in species number between shrubland and grassland plot.

Spiekeroog Norderney Linear Quadratic Linear Quadratic R2

adj b P R2adj P n R2

adj b P R2adj P n

Total no. of species 0.09 –0.11 0.064 0.11a 0.083 30 0.0 –0.03 0.463 0.17 0.076 21CoV pH (H2O) 0.13 –0.12 0.094 0.24 0.066 16 0.22 0.07 0.059 0.16 0.165 13CoV organic matter 0.40 –0.16 0.005 0.43 0.010 16 0.12 0.07 0.134 0.06 0.300 13CoV total nitrogen 0.29 –0.15 0.019 0.36 0.022 16 0.07 0.05 0.192 0.0 0.410 13 CoV C/N ratio 0.16 –0.13 0.071 0.26a 0.055 16 0.04 –0.04 0.242 0.08 0.254 13 No. of herbaceous species 0.10 –0.10 0.054 0.11a 0.085 30 0.0 –0.02 0.439 0.0 0.698 21CoV pH (H2O) 0.12 –0.09 0.099 0.27 0.053 16 0.0 0.02 0.395 0.09 0.247 13CoV organic matter 0.35 –0.13 0.009 0.41 0.013 16 0.0 0.02 0.389 0.13 0.205 13CoV total nitrogen 0.24 –0.12 0.030 0.35a 0.025 16 0.0 0.02 0.384 0.15 0.178 13CoV C/N ratio 0.14 –0.10 0.084 0.28a 0.049 16 0.0 0.00 0.859 0.18 0.154 13 No. of mosses & lichens 0.10 –0.02 0.058 0.19a 0.025 30 0.0 –0.01 0.801 0.25 0.029 21CoV pH (H2O) 0.25 –0.03 0.029 0.32 0.031 16 0.15 0.05 0.108 0.11 0.230 13CoV organic matter 0.54 –0.04 0.001 0.56 0.002 16 0.04 0.04 0.256 0.16 0.167 13CoV total nitrogen 0.46 –0.04 0.002 0.50 0.005 16 0.0 0.03 0.365 0.11 0.229 13CoV C/N ratio 0.34 –0.03 0.011 0.39 0.016 16 0.0 –0.03 0.433 0.30 0.068 13 No. of grassland vs. shrubland speciesGrassland species 0.30 –0.14 0.001 0.30 0.004 30 0.04 –0.04 0.200 0.31 0.014 21Shrubland species 0.07 0.03 0.089 0.06 0.181 30 0.02 0.02 0.249 0.00 0.513 21Indifferent species 0.00 –0.01 0.656 0.04 0.234 30 0.01 –0.01 0.280 0.00 0.482 21 Diff. no. of species Total 0.16 0.11 0.031 0.41a 0.002 24 0.11 0.07 0.127 0.13 0.174 15Herbaceous species 0.25 0.11 0.008 0.41a 0.001 24 0.10 0.04 0.139 0.38 0.022 15Mosses & lichens 0.0 0.01 0.513 0.27 0.015 24 0.0 0.03 0.405 0.00 0.632 15


pattern became clearer only for the number of herbaceous species (Fig. 2), while it was still weak for total species number and disappeared for mosses and lichens (Table 5). When controlling for the effects of soil variables, the relationship between the number of species and shrub cover was much improved for Spiekeroog in both linear and quadratic models (Table 5). The polynomial models had throughout higher R2

adj than the linear models, and in several cases the quadratic term proved to be significant. For Norderney, in contrast, the inclusion of co-variables did not improve the coefficients of determination com-pared to the simple regressions. With few exceptions, quadratic regressions explained a higher amount of variation in species richness than the linear models, indicating that the relationship between the number of species and Hippophaë cover is gener-ally best described by a hump-backed curve. Maximum species richness was reached at cover values between 20 and 45%, i.e., at moderate levels of shrub expansion. The decrease in total species number with increasing cover of Hippophaë is mainly caused by the fairly steep decline in grassland species and is not compensated by the simultaneous, but only slight increase in shrubland species (Fig. 3).

Discussion

Soils

When comparing the soils of shrubland plots with Hippophaë rhamnoides with those of the grassland plots, pronounced differences were observed. On both islands, the shrubland plots showed higher values for both organic matter and nitrogen. With an increasing cover of shrubs, the leaf litter accumulates in low-fertil-ity sites such as dunes which results in a gradual carbon and nutrient enrichment of the soil (Hopkins 1996). High nitrogen contents of soils in dense stands of Hippophaë rhamnoides were reported by Pearson & Rogers (1962), and older stands were found to have twice the amount of nitrogen than young stands (Oremus & Otten 1981; Troelstra et al. 1987). In a related study of the N-fixing species Porlieria chilensis shrubland in coastal Chile, the

levels of soil nitrogen, phosphorus and organic matter were higher beneath the shrubs than in the surrounding area (Gutiérrez et al. 1993). The symbiosis of Hip-pophaë with the nitrogen-fixing actinomycete Frankia contributes to the relatively high N content of the soil. In a stand dominated by the legume Lupinus arboreus, the nitrogen content was up to four times higher than in the open grassland (Alpert & Mooney 1996). In humid regions the higher content of litter and or-ganic matter in the soil beneath the shrubs allows more water to be retained in the soil (Hodgkin 1984). The decomposition of litter and organic matter as well as the leaching of calcium and other base cations in older dunes may cause a decrease in soil pH (Oremus & Otten 1981; Rozema et al. 1985; Troelstra et al. 1987). In our study, however, a lower pH in the shrubland plots was only observed on Norderney.

Species composition

In agreement with other studies in dune systems (e.g. Pearson & Rogers 1962), on Spiekeroog the cover of several, mostly tall, herbaceous species was positively related to the cover of Hippophaë rhamnoides, includ-ing Cirsium vulgare, Leymus arenarius, Moehringia trinervia, Poa trivialis, Rubus caesius and Urtica dioica. These taxa are mostly N-demanding species (Ellenberg et al. 1991), and their association with Hippophaë may partly reflect the relatively high nitrogen content in the shrubland soils. In contrast, many typical, often annual, dune spe-cies (Aira praecox, Arenaria serpyllifolia, Cerastium semidecandrum, Luzula campestris, Rumex acetosella, Tortula ruralis, etc.) decreased on Spiekeroog with in-creasing shrub cover. These species often have a ruderal or mixed-ruderal strategy and are likely to be outcom-peted by the above-mentioned, more competitive species. They may also suffer from the reduced light intensity inside the shrubland (cf. Kutiel et al. 2000; Isermann et al. 2005). The dominance of shade-tolerant species beneath Hippophaë rhamnoides was also observed by Fuller & Boorman (1977). However, the shading effect of shrub expansion differs considerably between species: for example, the relative irradiance beneath Juniperus communis is

Fig. 3. Effect of the abundance of Hippophaë rhamnoides on the number of grassland and shrubland species on Spiekeroog (left) and Norderney (right). For regression statistics, see Table 5.


half that beneath Potentilla fruticosa L. (Rejmánek & Rosén 1988, 1992). Relative light intensity was found to decrease with increasing age of the evergreen Rhodo-dendron ponticum L. to only 2% in the oldest stands (Howard & Lee 2002). On Norderney, the effects of Hippophaë expansion on single species were weak: there was no increase in N-demanding species and no decrease in annual and light-demanding species. In contrast, the two grassland species Festuca rubra ssp. arenaria and Phleum are-narium showed a positive / hump-backed relation with the cover of Hippophaë. We believe that these marked differences between islands in the responses of species to the shrub expansion is best explained by the presence or absence of rabbits. Although an increase in Hippophaë creates environmental conditions, with regard to light and nutrient availability, which are suitable for the establish-ment of tall, N-demanding and relatively competitive species also on Norderney, these species cannot take advantage because they are preferably grazed by rab-bits and in general other herbivores (Wallage-Drees et al. 1986; Hartley & Jones 1997). The lack of a decrease in typical dune grassland species is difficult to explain: possibly this is an indirect effect of the weaker rabbit grazing pressure on these species, enabling them to use the increased nutrient availability close to the shrubs.

Species richness

On Spiekeroog we found, in accordance with our main hypothesis, a (marginally) significant, hump-backed rela-tionship between the number of species and the cover of Hippophaë rhamnoides. In most cases, maximum species richness was reached at about 30-40 % shrub cover, and species richness in the densest shrubland was throughout lower than in the open grassland. The decline of small and light-demanding species in dense Hippophaë stands thus is not fully compensated by an increase in taller, more shade-tolerant and nitrogen-demanding species. The results are in agreement with those found by Binggeli et al. (1992) in Northern Irish dunes where the total spe-cies number in Hippophaë shrubland decreased by 50%. They also conform with other studies on the effects of expansive shrubs on plant species richness: for example, in the understorey of North American forests the invasion of Lonicera maackii led to a decrease in species number of about 60% (Collier et al. 2002), and in coastal grass-land in California, species richness decreased up to 31% due to the encroachment of Delairea odorata (Alvarez & Cushman 2002). The invasion of non-native shrubs, e.g. Hippophaë rhamnoides, Rhododendron ponticum and Lupinus arboreus in Northern Irish dunes facilitates the establishment of other rapidly spreading, non-native plants such as Clematis vitalba and Rubus spectabilis

(Binggeli et al. 1992). We observed a strong decrease in species richness only at higher shrub density. In our study of Hippophaë rhamnoides, this is the case at cover values > 50%. In Swedish alvar grasslands overgrown by Juniperus com-munis and Potentilla fruticosa, a strong decline in the number of species was obvious only at very high cover values > 75% in the largest plots (256 m2), while in the smaller plots (4-64 m2) this decline was observed already at about 50% cover (Rejmánek & Rosén 1988). In the South African fynbos a decline in indigenous species was found when the cover of non-native shrubs and trees exceeded about 50%, irrespective of the plot size that varied between 4 and 256 m2 (Richardson et al. 1989). The hump-backed pattern observed in Hip-pophaë shrubland may be explained as follows: When the shrubs start to invade the dune area, soil organic matter and nitrogen accumulate, soil moisture avail-ability increases and light availability decreases. These conditions favour the establishment of shade-tolerant and relatively moisture- and nutrient-demanding species occurring side by side with typical dune species, which occupy the, still rather large, gaps not yet invaded by the shrubs (cf. Petrů & Menges 2003). Species richness thus rises due to an increased structural and environmental heterogeneity. As the shrubland becomes denser, the gaps become smaller or disappear, and as a consequence many light-demanding dune species start to disappear. This process eventually accelerates, especially if the seedling establishment of the dune species fails under the dense shrubs (Tyler & DʼAntonio 1995). We believe that this or a similar mechanism is responsible for the decrease in species number in most study systems of expanding or invading shrubs. When correcting for the effects of the soil co-variables (and of the grassland plots), the hump-backed pattern became much clearer in the case of Spiekeroog. The reason for these strong effects is that the gradient in Hippophaë rhamnoides cover is superimposed by the zonation gradient from the yellow across the grey to the brown dunes, which in turn is associated with a change in species richness in the form of an optimum curve (Isermann 2005). This means that the simple regression may be distorted because grey dunes with Hippophaë may be species-richer than yellow dunes without this species. For Norderney, however, the hump-backed pattern was, except for mosses and lichens, rather weak, and it was improved by the inclusion of co-variables only for the number of herbaceous species, which is largely in accordance with our second hypothesis. The above-given effects of Hippophaë may basically hold true, but are likely to be counteracted by rabbit grazing preventing the increase in tall, competitive species as caused by the


shrub expansion (see above).

Dune conservation

At a landscape level, the expansion of shrubs may result in a more varied habitat structure and thus environ-mental heterogeneity, which in turn may be associated with a higher species richness. In Swedish grasslands, the expansion of Juniperus communis was shown to have a positive effect on bird species richness (Söderström et al. 2001). In general, taxa confined to or associated with shrubs will be favoured by any shrub encroachment. Shrubland itself varies considerably in structure and com-position and can be of great ecological and conservation interest (Hopkins 1996; Mortimer et al. 2000). A moder-ate expansion of shrubs such as Hippophaë rhamnoides and Rosa rugosa (Isermann 2003) may well bring about a somewhat higher general species richness compared to the open dunes, but this is caused by an increase in highly common generalist species. Eventually, the shrub expansion leads to a much reduced species richness of the dune grasslands and also a reduced abundance of species with a high conservation value (according to the priorities stated in the FFH-Directive [Anon. 1992]). Shrubland with the above-mentioned species is characterized by the dominance of one or two species, a simple vegetation structure and few sunny glades, resulting in, compared to open dunes, low conservation value (Fuller & Boorman 1977; Binggeli et al. 1992; Hopkins 1996; Mortimer et al. 2000). This is likely to hold true not only for plants, but also for most animal taxa. In conclusion, dense or moderately dense Hippophaë shrubland (cf. Suthers et al. 2000) represents a serious conservation problem to the coastal habitats of the North Sea.

Acknowledgements. We are grateful to the Administration of the Wadden Sea National Park of Lower Saxony for permis-sion of access to the study areas. We thank three anonymous reviewers for many helpful comments on an earlier draft of the paper.

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Received 12 July 2005;Accepted 16 February 2006;

Co-ordinating Editor: J. Pfadenhauer.

effects of the expansion by hippophaë rhamnoides on plant species richness in coastal dunes

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