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Expansion of Rosa rugosa and Hippophaë rhamnoides in coastal grey dunes: Effects at different spatial scales
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Flora 203 (2008) 273–280 www.elsevier.de/flora
Expansion of Rosa rugosa and Hippophae¨ rhamnoides in coastal grey dunes: Effects at different spatial scales Maike Isermann Vegetation Ecology and Conservation Biology, FB 2, University of Bremen, Leobener Strasse, 28359 Bremen, Germany Received 29 November 2006; accepted 31 March 2007
Abstract The study analysed the effects of shrub expansion on vegetation composition and plant species diversity in coastal grey dunes on the North Sea island Spiekeroog, comparing Rosa rugosa and Hippophae¨ rhamnoides. Species composition was recorded in plots of two spatial scales, 1 and 16 m2, considering the full range of shrub cover from less than 10 to almost 100%. Although R. rugosa and H. rhamnoides established and spread in the same grey dune environment, the vegetation of the two shrubland types was much different. While the H. rhamnoides plots were relatively species-rich, characterised by remnant grey dune vegetation with many small, often annual, light-demanding species except in the densest shrubs, the R. rugosa plots were clearly species-poorer due to the loss of many typical grey dune species, including only few shade-tolerant taxa. The total number of species, the number of herbaceous species and of species typical for grasslands decreased with increasing cover of H. rhamnoides and R. rugosa at both spatial scales. For the number of shrubs and shrubland species, hardly any significant effects of shrub cover were observed in R. rugosa, while there were positive effects in H. rhamnoides. Both the Shannon index and evenness decreased with increasing cover of the two shrub species at both spatial scales. Here, the decline in species diversity was more improved in R. rugosa than in H. rhamnoides. r 2008 Elsevier GmbH. All rights reserved. Keywords: Shading out; Shrub encroachment; Species diversity; Species richness
Introduction Shrub encroachment into open dune grasslands has been shown to have considerable effects on species richness and diversity (Fuller and Boorman, 1977; Isermann et al., 2007). In coastal grey dunes of the Wadden Sea Islands of the North Sea, Hippophae¨ rhamnoides and Rosa rugosa nowadays belong to the most frequent shrub species. Starting from plantations, they have, in the course of the second half of the 20th century, spread rapidly and at present dominate large E-mail address: [email protected]. 0367-2530/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2007.03.009
dune areas, forming dense, impenetrable thickets. As a consequence, the area of open grassland has declined (Isermann and Cordes, 1992), resulting in a change in environmental conditions and vegetation composition in the dune systems. An obvious change in the environment associated with the expansion of shrubs is a decline in light availability. For H. rhamnoides it has been shown that this increased shading leads to a decrease in the number of many typical, often annual, light-demanding dune species (Isermann et al., 2007). The extent of this effect depends on how fast light availability below the shrubs decreases with an increasing shrub cover. This decrease
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is stronger in the case of R. rugosa than in H. rhamnoides (Isermann, 2007), and different influences upon accompanying vegetation by shrubs have been reported similarly also for other species, e.g. Potentilla fruticosa and Juniperus communis (Rejma´nek and Rose´n, 1988; 1992). Other environmental changes connected to the expansion of shrubs into dune grasslands concern the soil; for example, soils under dense shrub thickets have been shown to have a higher proportion of organic matter, a higher water storage capacity and a different chemical composition than soils in open dune grasslands (Hodgkin, 1984). However, the effects of shrub expansion on the dune environment and eventually on species richness and diversity are likely to be scale-dependent, because the previously mentioned effects on the environment are scale-dependent, and because the relative importance of environmental factors varies with spatial scale (Auerbach and Shmida, 1987). In a study of H. rhamnoides shrublands on two islands of the Wadden Sea, it was shown that the number of species in 16 m2 plots (in total and for different species groups) mostly showed a humped-back relation with shrub cover (Isermann et al., 2007). If this pattern applies also to other regions, shrub species or spatial scales is not yet known, because the literature on the specific effects of expanding shrubs on species richness is scarce (but see Rejma´nek and Rose´n, 1988). The aim of this study was to examine whether the effects of shrub expansion on species richness and diversity differ between H. rhamnoides and R. rugosa, and whether such differences depend on the spatial scale examined. The expectation was that the general effects were more dramatic in R. rugosa, this species being broader-leaved and denser-growing than H. rhamnoides.
Materials and methods Species Since more than two centuries, shrubs with extensive root systems such as R. rugosa and H. rhamnoides were planted on coasts of the North Sea for coastal protection and sand stabilisation (Bruun, 2005; MeyerDeepen and Meijering, 1979; Pearson and Rogers, 1962). The subsequent expansion of shrubs was facilitated by a simultaneous decline in cattle grazing. H. rhamnoides is a deciduous shrub with narrow leaves, occurring along the coasts of Northwest and Central Europe and in mountainous areas in Europe and Asia. It is intolerant of shade (Pearson and Rogers, 1962), but able to establish on nutrient-poor, sandy and gravely soils with a high pH-value, including species-rich young grey dunes. After having established the species
can quickly increase in abundance and form dense thickets. Its ability to fix nitrogen by means of a symbiosis with micro-organisms in root nodules is likely to add to the nitrogen content of the dune soils. R. rugosa was introduced to Europe in the 18th century. Its original distribution area includes the coastal regions of the Northern Pacific, e.g. Alaska, Kamtchatka and Japan, where it grows mainly on dunes, along rocky shores and in species-rich meadows. The shrub established as a garden escape; it is naturalised in parts of northern, western and central Europe and is regarded an invasive species along the coasts of the Northern Atlantic, the North Sea and the Baltic Sea (Bruun, 2005). R. rugosa is a broad-leaved, multi-stemmed deciduous shrub and forms dense impenetrable thickets (Bruun, 2005). In North European coastal ecosystems R. rugosa occurs in yellow and grey dunes as well as in brown dunes, hence on a broader range of soils than H. rhamnoides, which shows a small pH-range and occurs mostly in yellow and young grey dunes (Isermann, 2007; Pearson and Rogers, 1962).
Sampling The study was carried out on Spiekeroog, a Wadden Sea island of about 21 km2 size. Plots were laid out exclusively in grey dunes that are largely characterised by grassland vegetation, avoiding species-poor yellow dunes of young successional stage and brown dunes dominated by heathland. In each plot (n ¼ 34 in H. rhamnoides and n ¼ 21 in R. rugosa) vegetation data were collected at two spatial scales, 1 and 16 m2. Plots were chosen as to enclose the full range of shrub cover from less than 10 to almost 100%. Three vegetation layers were distinguished: shrub layer, field layer with herbs, grasses and woody seedlings, and bottom layer with mosses and lichens. Only epigeic mosses and lichens were taken into account. Sampling included the percent cover of H. rhamnoides and R. rugosa, and a list of all species with their cover degree according to a refined Braun-Blanquet scale (Reichelt and Wilmanns, 1973). The nomenclature follows Wisskirchen and Haeupler (1998) for vascular plants, Koperski et al. (2000) for bryophytes and Wirth (1980) for lichens.
Statistical analysis For estimating general differences in species composition between the two shrubland types, a synoptic table with percent frequencies of all species was carried out on the large plot data. A species was defined as separating the two shrubland types if its frequency in one type was at least 20% and at the same time at least double the frequency in the second type (cf. Berg et al., 2004). To analyse whether the shrub expansion affected typical
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dune species and species of other habitat types differently, so-called ‘grassland’ and ‘shrubland’ species were distinguished according to Berg et al. (2001). Differences in vegetation parameters between H. rhamnoides and R. rugosa shrubland were analysed with t-test. To assess the effects of increasing cover of the shrub species on species richness and diversity, regression analysis was applied. Linear and quadratic regressions were compared by means of the percentage of variation explained (R2adj). Stepwise forward–backward regressions were used to check whether the quadratic term added significantly to the linear model. Species richness variables included the total number of species and the species number of different life form groups. Measures of species diversity were the Shannon index and evenness (Magurran, 2004). If not mentioned otherwise, tests were conducted with the program MINITAB (Anon, 1998).
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increasing cover of H. rhamnoides (but not of R. rugosa). In all cases with negative relationships between the number of species and shrub cover of both species, the results were more improved at the larger scale. In general, the negative effect of shrub cover was more pronounced with regard to the two diversity indices (Table 2). Both the Shannon index and evenness decreased with increasing cover of H. rhamnoides and R. rugosa. In one case (H. rhamnoides, evenness, 16 m2) a hump-backed curve (R2adj ¼ 0.28, p ¼ 0.002) described the relationship between diversity and shrub cover significantly better than a linear function. Comparing the linear regression (Table 2), the decline in species diversity was steeper in R. rugosa than in H. rhamnoides (Fig. 1). In the former species, values were reduced to approximately 50% when comparing plots with sparse and those with dense shrub cover.
Discussion Results Species composition and environment Species composition of both shrubland types was clearly different (Table 1). The number of separating species in the H. rhamnoides shrubland was more than twice as high as that in the R. rugosa shrubland (Table 1). The annual species of open dune grassland such as Arenaria serpyllifolia, Cerastium semidecandrum, Myosotis ramosissima, Phleum arenarium and Vicia lathyroides were almost exclusively found in H. rhamnoides shrubland, along with mosses such as Brachythecium albicans and Tortula ruraliformis. In contrast, R. rugosa shrubland had higher frequencies of perennial, more shade-tolerant species, including mosses such as Hypnum jutlandicum and Scleropodium purum (Table 1).
Species richness and diversity The total species richness, the number of herbaceous species, and (restricted to the large scale) typical grassland and shrubland species as well as mosses and lichens in the H. rhamnoides sites were higher than the one in the R. rugosa sites (Table 2). When comparing the values for the Shannon index and evenness, the H. rhamnoides plots were again clearly more diverse than the R. rugosa plots. The total number of species decreased with increasing shrub cover in R. rugosa and (restricted to the large scale) for H. rhamnoides (Table 2). As to the different life forms, the number of herbaceous species and typical grassland species declined in both shrublands. In contrast, the number of shrub species increased with
Species richness was higher in the Hippophae rhamnoides plots than in the Rosa rugosa plots. The latter species grows denser and has broader, more shading leaves, causing a stronger reduction in light intensity below the shrubs and thereby a decrease in many lightdemanding species (Isermann, 2007). In H. rhamnoides, in contrast, small gaps remain also in dense shrubland with a less shady interior due to the more narrow and sparser-growing leaves. This enables many species typical of open dune grasslands to persist, at least for some time (Isermann et al., 2007); furthermore gaps are important for the recruitment of herbaceous plants (Petru˚ and Menges, 2003). In general, species richness of gap-rich shrubland is obviously greater than in dense shrublands (Crawford and Young, 1998). Different effects on species richness related to different growth forms of shrubs were also observed in a comparison of Juniperus communis L. and Potentilla fruticosa L., where the latter species grows denser and reduces the number of herbaceous species more strongly than the juniper (Rejma´nek and Rose´n, 1988, 1992). In both shrubland types, the number of herbaceous and of typical grassland species declined with increasing shrub cover as an effect of out-shading. Mosses showed no consistent negative effects of increasing shrub, probably because this life form comprises high proportions of comparatively shade-tolerant species. In addition, R. rugosa shrubland often grows so dense that only few gaps are available for the germination of any species, which is already shown for other shrublands (Tyler and D’ Antonio, 1995). In contrast, an increase in H. rhamnoides cover had a positive effect on the number of further shrubs and other typical shrubland species. A possible explanation is that the fruits of H. rhamnoides
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Table 1.
M. Isermann / Flora 203 (2008) 273–280
Comparison of large shrubland plots dominated by Hippophae rhamnoides or Rosa rugosa H. rhamnoides scrub
Number of plots Hippophae¨ rhamnoides Brachythecium albicans Linaria vulgaris Cerastium semidecandrum Myosotis ramosissima Luzula campestris Epilobium montanum Rubus caesius Lotus corniculatus ssp. corniculatus Viola tricolor ssp. tricolor Senecio sylvaticus Rumex acetosella Hypnum cupressiforme var. lacunosum Arenaria serpyllifolia Rhinanthus minor Moehringia trinervia Leymus arenarius Tortula ruraliformis Sonchus arvensis Cardamine pratensis Phleum arenarium Hypnum cupressiforme var. cupressiforme Poa trivialis X Calammophila baltica Ceratodon purpureus Veronica arvensis Veronica officinalis Rosa rugosa Rhytidiadelphus squarrosus Holcus lanatus Anthoxanthum odoratum Sorbus aucuparia Agrostis capillaris Dicranum scoparium Galium album ssp. album Festuca rubra ssp. arenaria Ammophila arenaria Carex arenaria Poa pratense Hieracium umbellatum Hypochaeris radicata Brachythecium rutabulum Aira praecox Rosa canina Poa humilis Polypodium vulgare Viola canina ssp. canina Vicia lathyroides Rubus spec. Arabidopsis thaliana Sagina procumbens Corynephorus canescens Euphrasia stricta Taraxacum sect. Erythrosperma Elymus farctus ssp. boreoatlanticus
R. rugosa scrub
34
21
100 76 71 65 62 59 56 56 50 50 50 47 41 41 35 35 32 32 29 29 24 24 24 24 24 21 21 9 12 9 6 3
38 10 24 19
97 97 97 59 74 59 50 44 35 24 21 18 18 18 12 18 18 15 15 15 15
24 19 5 14 14 5 10 5 5 5 5 5
10 5 100 43 33 24 24 24 24 76 71 67 76 48 38 29 33 33 24 24 24 10 10 14
5 5
Grass/shrubland species
s g g g g g s s g g s g g g g s g g g x g g s g g g s s x s g s g x s g g g x g g s g s g s g g s x g g g g x
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Table 1. (continued ) H. rhamnoides scrub Cerastium holosteoides Jasione montana Sedum acre Hieracium pilosella Oenothera oakesiana Sambucus nigra Plantago lanceolata Scleropodium purum Epilobium angustifolium Dryopteris dilatata Crateagus monogyna Cladonia furcata Bromus hordeaceus Dactylis glomerata Hypnum jutlandicum
12 12 12 12 12 6
3
3
R. rugosa scrub 5 5 5
19 19 19 14 14 14 14 10 10 10
Grass/shrubland species g g g g s s g x s s s g g s x
H. rhamnoides scrub: Cardamine hirsuta (x), Cochlearia anglica (g), Eryngium maritimum (g), Eurhynchium praelongum (s), Urtica dioica 9 (s), Cirsium vulgare (s), Claytonia perfoliata (s), Pohlia nutans (g), Polytrichum juniperinum (g), Taraxacum sect. Ruderalia 6 (g), Anthyllis vulneraria (g), Lathyrus maritimus (g), Salix repens ssp. dunensis (s), Solanum dulcamara 3 (s); H. rhamnoides and R. rugosa scrub: Cerastium diffusum (g), Senecio vulgaris (x), Stellaria graminea 3, 5 (x); R. rugosa scrub: Cladonia arbuscula (g), Lonicera periclymenum (s), Stellaria pallida (s), Trifolium arvense (g), Trifolium campestre (g), Vicia cracca 5 (s). Percent frequencies of species occurrence in the plots are shown; low-frequent species (o10%) are given at the bottom of the table. Separating species are in bold. Furthermore, the classification of the species as belonging to shrubland (s), grassland (g) or indifferent (x) species is shown.
are in comparison to the fruits of R. rugosa attractive to and eaten by birds (smaller size and high contents of vitamine C), which may favour the dispersal and establishment of other shrub species, when birds rest in the H. rhamnoides shrubland. There are indeed observations that more shrub species can be found in the surrounding of fruit-bearing and bird-dispersed trees and shrubs (Suthers et al., 2000). Furthermore, H. rhamnoides shrubland in comparison to R. rugosa contains more gaps, where the seeds of other shrubs can germinate. Moreover, in the case of expansion of Juniperus communis in Swedish grasslands a positive effect on bird species richness could be registered (So¨derstro¨m et al., 2001). Hence, besides other environmental conditions, the combined effects of growth-form, gaps and seed dispersal by animals, do influence the succession of H. rhamnoides and R. rugosa to species-rich and to species-poor shrublands, respectively. The negative effects of shrub encroachment were more pronounced with regard to the two diversity indices than to species richness. The general effect of expanding shrubs may be the following: with the local establishment of single shrubs, the grassland vegetation starts to disintegrate, leading to a mosaic of patches with dominating shrubs and dominating herbaceous species side by side. This would mean that species richness first decreases only slowly, while evenness declines more rapidly. Only in the H. rhamnoides plots, there was a
humped-back relationship between evenness and shrub cover at the larger scale, perhaps because the disintegration of the dune vegetation proceeds less quickly in this less shading shrub species. The effects of R. rugosa on species diversity were more dramatic than that of H. rhamnoides, which again is best explained by the different growth forms of the two species. Similar effects of decrease in species richness were shown in a comparative study of Juniperus communis and Potentilla fruticosa L. (Rejma´nek and Rose´n, 1988, 1992). Considering the conditions within one vegetation type, for example dune slacks and grasslands, respectively, species diversity decreased with increasing plot size because of increasing small-scale habitat heterogeneity (Wilson et al., 1999). In the case of a transition from homogeneous grassland to H. rhamnoides shrubland, at larger scales evenness as mentioned above, at first increased and than decreased, probably because of increasing vegetation structure. In contrast, there was a monotonically decline in evenness with establishing of dominant R. rugosa shrubland. In general, species richness patterns are scale-dependent. In this study, the effects of shrub expansion on the species richness were, with few exceptions, more pronounced in the larger plot sizes. But at a small-scale R. rugosa stands showed a more improved linear decline in species diversity than H. rhamnoides stands, because R. rugosa showed already at low dominance levels stronger shading-out effects than H. rhamnoides.
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Table 2. Species richness and diversity (Shannon–Wiener-index and evenness) of H. rhamnoides and R. rugosa shrubland in relation to shrub cover examined at two spatial scales, 1 and 16 m2 Plot size
Hippophae¨ shrubland
Rosa shrubland
t-test
SD
b
R2adj
Species richness Total no. of species 1 13.03 16 22.03
4.75 9.01
0.05 0.12
0.02 0.13
0.184 0.020
9.95 12.86
4.23 4.75
0.09 0.10
0.42 0.53
0.001 0.000
No. of shrubs 1 1.74 16 2.38
1.50 0.98
0.03 0.01
0.23 0.11
0.002 0.030
1.48 2.12
0.87 1.84
0.01 0.02
0.03 0.05
0.206 0.169
No. of herbaceous species 1 9.63 4.48 16 17.18 7.74
0.07 0.10
0.09 0.14
0.038 0.018
6.91 8.76
3.87 4.54
0.09 0.12
0.58 0.80
0.000 0.000
* *
No. of mosses and lichens 1 1.71 1.34 16 2.74 1.91
0.01 0.03
0.00 0.16
0.493 0.011
1.57 1.71
1.47 1.65
0.00 0.00
0.00 0.00
0.833 0.736
*
No. of typical grassland species 1 8.11 4.11 16 14.32 7.12
0.08 0.14
0.22 0.33
0.003 0.000
6.19 7.57
4.14 5.05
0.09 0.13
0.53 0.75
0.000 0.000
*
No. of typical shrubland species 1 3.97 1.90 16 6.03 2.79
0.03 0.03
0.10 0.05
0.039 0.117
3.14 4.57
2.01 3.41
0.01 0.02
0.00 0.01
0.533 0.271
*
Mn
p
Mn
SD
b
R2adj
p
* *
Species diversity Shannon index 1 1.49 16 2.01
0.38 0.51
0.008 0.008
0.22 0.21
0.002 0.004
1.04 1.30
0.55 0.54
0.010 0.013
0.64 0.64
0.000 0.000
* *
Evenness 1 16
0.09 0.09
0.002 0.001
0.29 0.19
0.001 0.006
0.45 0.51
0.19 0.17
0.004 0.003
0.51 0.45
0.000 0.000
* *
0.59 0.66
Means (Mn) and standard deviations (SD) are given for both plot sizes. Linear regressions of species richness and diversity depending on shrub cover are compared by means of the percentage of variation explained (R2adj) and significance probabilities (p); b ¼ slope of regression. The t-test refers to the comparison of species richness and diversity between H. rhamnoides and R. rugosa plots, with significant results (po0.05) marked with an asterisk.
Other studies rendered also different result concerning scale dependence: Responses to changed environmental conditions often happen faster and more distinct at smaller spatial scales, as, for example, shown for calcareous grasslands on O¨land, Sweden (Huber, 1994, 1999; Rejma´nek and Rose´n, 1988). In a short grass steppe in Colorado, the dominant grass species Bouteloua gracilis (Kunth) Lag. ex. Griffiths and Buchloe dactyloides (Nutt.) Engelm. affected species richness only at small plot sizes (o3 m2), and species richness at small scales changed more rapidly than at larger scales due to stronger effects of altered biotic interactions such as competition (Singh et al., 1996). However, effects of scale are not always evident: in wet meadows in Wisconsin, there was a negative correlation between
species richness and the cover of Phalaris arundinacea L. both in small (1 m2) and large plots (4500 m2) (Kercher et al., 2004). Considering conservation aspects, the expansion of shrubs into species-rich grey dunes is highly problematic: Dune shrublands, which are characterised by the dominance of one or few species, a simple vegetation structure, the scarcity of gaps, and the absence of rare species, especially many typical elements of open dune grasslands, have a low conservation value compared to the more open grey dunes (Mortimer et al., 2000). These effects and consequences are even more pronounced in R. rugosa than in H. rhamnoides shrublands, because of the stronger decline of species diversity in the former case, due to a more intensified shading-out effect.
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3.0
Shannon Index
2.5 2.0 1.5 1.0 0.5 0.0
Hippophaë rhamnoides Rosa rugosa
20
0
40 60 Shrub cover [%]
80
100
80
100
0.8
Evenness
0.6 0.4 0.2 0
Hippophaë rhamnoides Rosa rugosa
0
20
40 60 Shrub cover [%]
Fig. 1. Relationship between Shannon index (above) and evenness (below) in large plots and shrub cover of H. rhamnoides (filled symbols) and R. rugosa (unfilled symbols). For regression statistics, see Table 2.
Acknowledgments The author expresses her thanks to the Administration of the Wadden Sea National Park of Lower Saxony for permission of access to the study area, to Sonja Heemann for field work in the H. rhamnoides shrubland; and to Martin Diekmann and two anonymous reviewers for critical comments on earlier drafts of the manuscript.
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Flora 203 (2008) 273–280 www.elsevier.de/flora
Expansion of Rosa rugosa and Hippophae¨ rhamnoides in coastal grey dunes: Effects at different spatial scales Maike Isermann Vegetation Ecology and Conservation Biology, FB 2, University of Bremen, Leobener Strasse, 28359 Bremen, Germany Received 29 November 2006; accepted 31 March 2007
Abstract The study analysed the effects of shrub expansion on vegetation composition and plant species diversity in coastal grey dunes on the North Sea island Spiekeroog, comparing Rosa rugosa and Hippophae¨ rhamnoides. Species composition was recorded in plots of two spatial scales, 1 and 16 m2, considering the full range of shrub cover from less than 10 to almost 100%. Although R. rugosa and H. rhamnoides established and spread in the same grey dune environment, the vegetation of the two shrubland types was much different. While the H. rhamnoides plots were relatively species-rich, characterised by remnant grey dune vegetation with many small, often annual, light-demanding species except in the densest shrubs, the R. rugosa plots were clearly species-poorer due to the loss of many typical grey dune species, including only few shade-tolerant taxa. The total number of species, the number of herbaceous species and of species typical for grasslands decreased with increasing cover of H. rhamnoides and R. rugosa at both spatial scales. For the number of shrubs and shrubland species, hardly any significant effects of shrub cover were observed in R. rugosa, while there were positive effects in H. rhamnoides. Both the Shannon index and evenness decreased with increasing cover of the two shrub species at both spatial scales. Here, the decline in species diversity was more improved in R. rugosa than in H. rhamnoides. r 2008 Elsevier GmbH. All rights reserved. Keywords: Shading out; Shrub encroachment; Species diversity; Species richness
Introduction Shrub encroachment into open dune grasslands has been shown to have considerable effects on species richness and diversity (Fuller and Boorman, 1977; Isermann et al., 2007). In coastal grey dunes of the Wadden Sea Islands of the North Sea, Hippophae¨ rhamnoides and Rosa rugosa nowadays belong to the most frequent shrub species. Starting from plantations, they have, in the course of the second half of the 20th century, spread rapidly and at present dominate large E-mail address: [email protected]. 0367-2530/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2007.03.009
dune areas, forming dense, impenetrable thickets. As a consequence, the area of open grassland has declined (Isermann and Cordes, 1992), resulting in a change in environmental conditions and vegetation composition in the dune systems. An obvious change in the environment associated with the expansion of shrubs is a decline in light availability. For H. rhamnoides it has been shown that this increased shading leads to a decrease in the number of many typical, often annual, light-demanding dune species (Isermann et al., 2007). The extent of this effect depends on how fast light availability below the shrubs decreases with an increasing shrub cover. This decrease
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is stronger in the case of R. rugosa than in H. rhamnoides (Isermann, 2007), and different influences upon accompanying vegetation by shrubs have been reported similarly also for other species, e.g. Potentilla fruticosa and Juniperus communis (Rejma´nek and Rose´n, 1988; 1992). Other environmental changes connected to the expansion of shrubs into dune grasslands concern the soil; for example, soils under dense shrub thickets have been shown to have a higher proportion of organic matter, a higher water storage capacity and a different chemical composition than soils in open dune grasslands (Hodgkin, 1984). However, the effects of shrub expansion on the dune environment and eventually on species richness and diversity are likely to be scale-dependent, because the previously mentioned effects on the environment are scale-dependent, and because the relative importance of environmental factors varies with spatial scale (Auerbach and Shmida, 1987). In a study of H. rhamnoides shrublands on two islands of the Wadden Sea, it was shown that the number of species in 16 m2 plots (in total and for different species groups) mostly showed a humped-back relation with shrub cover (Isermann et al., 2007). If this pattern applies also to other regions, shrub species or spatial scales is not yet known, because the literature on the specific effects of expanding shrubs on species richness is scarce (but see Rejma´nek and Rose´n, 1988). The aim of this study was to examine whether the effects of shrub expansion on species richness and diversity differ between H. rhamnoides and R. rugosa, and whether such differences depend on the spatial scale examined. The expectation was that the general effects were more dramatic in R. rugosa, this species being broader-leaved and denser-growing than H. rhamnoides.
Materials and methods Species Since more than two centuries, shrubs with extensive root systems such as R. rugosa and H. rhamnoides were planted on coasts of the North Sea for coastal protection and sand stabilisation (Bruun, 2005; MeyerDeepen and Meijering, 1979; Pearson and Rogers, 1962). The subsequent expansion of shrubs was facilitated by a simultaneous decline in cattle grazing. H. rhamnoides is a deciduous shrub with narrow leaves, occurring along the coasts of Northwest and Central Europe and in mountainous areas in Europe and Asia. It is intolerant of shade (Pearson and Rogers, 1962), but able to establish on nutrient-poor, sandy and gravely soils with a high pH-value, including species-rich young grey dunes. After having established the species
can quickly increase in abundance and form dense thickets. Its ability to fix nitrogen by means of a symbiosis with micro-organisms in root nodules is likely to add to the nitrogen content of the dune soils. R. rugosa was introduced to Europe in the 18th century. Its original distribution area includes the coastal regions of the Northern Pacific, e.g. Alaska, Kamtchatka and Japan, where it grows mainly on dunes, along rocky shores and in species-rich meadows. The shrub established as a garden escape; it is naturalised in parts of northern, western and central Europe and is regarded an invasive species along the coasts of the Northern Atlantic, the North Sea and the Baltic Sea (Bruun, 2005). R. rugosa is a broad-leaved, multi-stemmed deciduous shrub and forms dense impenetrable thickets (Bruun, 2005). In North European coastal ecosystems R. rugosa occurs in yellow and grey dunes as well as in brown dunes, hence on a broader range of soils than H. rhamnoides, which shows a small pH-range and occurs mostly in yellow and young grey dunes (Isermann, 2007; Pearson and Rogers, 1962).
Sampling The study was carried out on Spiekeroog, a Wadden Sea island of about 21 km2 size. Plots were laid out exclusively in grey dunes that are largely characterised by grassland vegetation, avoiding species-poor yellow dunes of young successional stage and brown dunes dominated by heathland. In each plot (n ¼ 34 in H. rhamnoides and n ¼ 21 in R. rugosa) vegetation data were collected at two spatial scales, 1 and 16 m2. Plots were chosen as to enclose the full range of shrub cover from less than 10 to almost 100%. Three vegetation layers were distinguished: shrub layer, field layer with herbs, grasses and woody seedlings, and bottom layer with mosses and lichens. Only epigeic mosses and lichens were taken into account. Sampling included the percent cover of H. rhamnoides and R. rugosa, and a list of all species with their cover degree according to a refined Braun-Blanquet scale (Reichelt and Wilmanns, 1973). The nomenclature follows Wisskirchen and Haeupler (1998) for vascular plants, Koperski et al. (2000) for bryophytes and Wirth (1980) for lichens.
Statistical analysis For estimating general differences in species composition between the two shrubland types, a synoptic table with percent frequencies of all species was carried out on the large plot data. A species was defined as separating the two shrubland types if its frequency in one type was at least 20% and at the same time at least double the frequency in the second type (cf. Berg et al., 2004). To analyse whether the shrub expansion affected typical
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dune species and species of other habitat types differently, so-called ‘grassland’ and ‘shrubland’ species were distinguished according to Berg et al. (2001). Differences in vegetation parameters between H. rhamnoides and R. rugosa shrubland were analysed with t-test. To assess the effects of increasing cover of the shrub species on species richness and diversity, regression analysis was applied. Linear and quadratic regressions were compared by means of the percentage of variation explained (R2adj). Stepwise forward–backward regressions were used to check whether the quadratic term added significantly to the linear model. Species richness variables included the total number of species and the species number of different life form groups. Measures of species diversity were the Shannon index and evenness (Magurran, 2004). If not mentioned otherwise, tests were conducted with the program MINITAB (Anon, 1998).
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increasing cover of H. rhamnoides (but not of R. rugosa). In all cases with negative relationships between the number of species and shrub cover of both species, the results were more improved at the larger scale. In general, the negative effect of shrub cover was more pronounced with regard to the two diversity indices (Table 2). Both the Shannon index and evenness decreased with increasing cover of H. rhamnoides and R. rugosa. In one case (H. rhamnoides, evenness, 16 m2) a hump-backed curve (R2adj ¼ 0.28, p ¼ 0.002) described the relationship between diversity and shrub cover significantly better than a linear function. Comparing the linear regression (Table 2), the decline in species diversity was steeper in R. rugosa than in H. rhamnoides (Fig. 1). In the former species, values were reduced to approximately 50% when comparing plots with sparse and those with dense shrub cover.
Discussion Results Species composition and environment Species composition of both shrubland types was clearly different (Table 1). The number of separating species in the H. rhamnoides shrubland was more than twice as high as that in the R. rugosa shrubland (Table 1). The annual species of open dune grassland such as Arenaria serpyllifolia, Cerastium semidecandrum, Myosotis ramosissima, Phleum arenarium and Vicia lathyroides were almost exclusively found in H. rhamnoides shrubland, along with mosses such as Brachythecium albicans and Tortula ruraliformis. In contrast, R. rugosa shrubland had higher frequencies of perennial, more shade-tolerant species, including mosses such as Hypnum jutlandicum and Scleropodium purum (Table 1).
Species richness and diversity The total species richness, the number of herbaceous species, and (restricted to the large scale) typical grassland and shrubland species as well as mosses and lichens in the H. rhamnoides sites were higher than the one in the R. rugosa sites (Table 2). When comparing the values for the Shannon index and evenness, the H. rhamnoides plots were again clearly more diverse than the R. rugosa plots. The total number of species decreased with increasing shrub cover in R. rugosa and (restricted to the large scale) for H. rhamnoides (Table 2). As to the different life forms, the number of herbaceous species and typical grassland species declined in both shrublands. In contrast, the number of shrub species increased with
Species richness was higher in the Hippophae rhamnoides plots than in the Rosa rugosa plots. The latter species grows denser and has broader, more shading leaves, causing a stronger reduction in light intensity below the shrubs and thereby a decrease in many lightdemanding species (Isermann, 2007). In H. rhamnoides, in contrast, small gaps remain also in dense shrubland with a less shady interior due to the more narrow and sparser-growing leaves. This enables many species typical of open dune grasslands to persist, at least for some time (Isermann et al., 2007); furthermore gaps are important for the recruitment of herbaceous plants (Petru˚ and Menges, 2003). In general, species richness of gap-rich shrubland is obviously greater than in dense shrublands (Crawford and Young, 1998). Different effects on species richness related to different growth forms of shrubs were also observed in a comparison of Juniperus communis L. and Potentilla fruticosa L., where the latter species grows denser and reduces the number of herbaceous species more strongly than the juniper (Rejma´nek and Rose´n, 1988, 1992). In both shrubland types, the number of herbaceous and of typical grassland species declined with increasing shrub cover as an effect of out-shading. Mosses showed no consistent negative effects of increasing shrub, probably because this life form comprises high proportions of comparatively shade-tolerant species. In addition, R. rugosa shrubland often grows so dense that only few gaps are available for the germination of any species, which is already shown for other shrublands (Tyler and D’ Antonio, 1995). In contrast, an increase in H. rhamnoides cover had a positive effect on the number of further shrubs and other typical shrubland species. A possible explanation is that the fruits of H. rhamnoides
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Table 1.
M. Isermann / Flora 203 (2008) 273–280
Comparison of large shrubland plots dominated by Hippophae rhamnoides or Rosa rugosa H. rhamnoides scrub
Number of plots Hippophae¨ rhamnoides Brachythecium albicans Linaria vulgaris Cerastium semidecandrum Myosotis ramosissima Luzula campestris Epilobium montanum Rubus caesius Lotus corniculatus ssp. corniculatus Viola tricolor ssp. tricolor Senecio sylvaticus Rumex acetosella Hypnum cupressiforme var. lacunosum Arenaria serpyllifolia Rhinanthus minor Moehringia trinervia Leymus arenarius Tortula ruraliformis Sonchus arvensis Cardamine pratensis Phleum arenarium Hypnum cupressiforme var. cupressiforme Poa trivialis X Calammophila baltica Ceratodon purpureus Veronica arvensis Veronica officinalis Rosa rugosa Rhytidiadelphus squarrosus Holcus lanatus Anthoxanthum odoratum Sorbus aucuparia Agrostis capillaris Dicranum scoparium Galium album ssp. album Festuca rubra ssp. arenaria Ammophila arenaria Carex arenaria Poa pratense Hieracium umbellatum Hypochaeris radicata Brachythecium rutabulum Aira praecox Rosa canina Poa humilis Polypodium vulgare Viola canina ssp. canina Vicia lathyroides Rubus spec. Arabidopsis thaliana Sagina procumbens Corynephorus canescens Euphrasia stricta Taraxacum sect. Erythrosperma Elymus farctus ssp. boreoatlanticus
R. rugosa scrub
34
21
100 76 71 65 62 59 56 56 50 50 50 47 41 41 35 35 32 32 29 29 24 24 24 24 24 21 21 9 12 9 6 3
38 10 24 19
97 97 97 59 74 59 50 44 35 24 21 18 18 18 12 18 18 15 15 15 15
24 19 5 14 14 5 10 5 5 5 5 5
10 5 100 43 33 24 24 24 24 76 71 67 76 48 38 29 33 33 24 24 24 10 10 14
5 5
Grass/shrubland species
s g g g g g s s g g s g g g g s g g g x g g s g g g s s x s g s g x s g g g x g g s g s g s g g s x g g g g x
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Table 1. (continued ) H. rhamnoides scrub Cerastium holosteoides Jasione montana Sedum acre Hieracium pilosella Oenothera oakesiana Sambucus nigra Plantago lanceolata Scleropodium purum Epilobium angustifolium Dryopteris dilatata Crateagus monogyna Cladonia furcata Bromus hordeaceus Dactylis glomerata Hypnum jutlandicum
12 12 12 12 12 6
3
3
R. rugosa scrub 5 5 5
19 19 19 14 14 14 14 10 10 10
Grass/shrubland species g g g g s s g x s s s g g s x
H. rhamnoides scrub: Cardamine hirsuta (x), Cochlearia anglica (g), Eryngium maritimum (g), Eurhynchium praelongum (s), Urtica dioica 9 (s), Cirsium vulgare (s), Claytonia perfoliata (s), Pohlia nutans (g), Polytrichum juniperinum (g), Taraxacum sect. Ruderalia 6 (g), Anthyllis vulneraria (g), Lathyrus maritimus (g), Salix repens ssp. dunensis (s), Solanum dulcamara 3 (s); H. rhamnoides and R. rugosa scrub: Cerastium diffusum (g), Senecio vulgaris (x), Stellaria graminea 3, 5 (x); R. rugosa scrub: Cladonia arbuscula (g), Lonicera periclymenum (s), Stellaria pallida (s), Trifolium arvense (g), Trifolium campestre (g), Vicia cracca 5 (s). Percent frequencies of species occurrence in the plots are shown; low-frequent species (o10%) are given at the bottom of the table. Separating species are in bold. Furthermore, the classification of the species as belonging to shrubland (s), grassland (g) or indifferent (x) species is shown.
are in comparison to the fruits of R. rugosa attractive to and eaten by birds (smaller size and high contents of vitamine C), which may favour the dispersal and establishment of other shrub species, when birds rest in the H. rhamnoides shrubland. There are indeed observations that more shrub species can be found in the surrounding of fruit-bearing and bird-dispersed trees and shrubs (Suthers et al., 2000). Furthermore, H. rhamnoides shrubland in comparison to R. rugosa contains more gaps, where the seeds of other shrubs can germinate. Moreover, in the case of expansion of Juniperus communis in Swedish grasslands a positive effect on bird species richness could be registered (So¨derstro¨m et al., 2001). Hence, besides other environmental conditions, the combined effects of growth-form, gaps and seed dispersal by animals, do influence the succession of H. rhamnoides and R. rugosa to species-rich and to species-poor shrublands, respectively. The negative effects of shrub encroachment were more pronounced with regard to the two diversity indices than to species richness. The general effect of expanding shrubs may be the following: with the local establishment of single shrubs, the grassland vegetation starts to disintegrate, leading to a mosaic of patches with dominating shrubs and dominating herbaceous species side by side. This would mean that species richness first decreases only slowly, while evenness declines more rapidly. Only in the H. rhamnoides plots, there was a
humped-back relationship between evenness and shrub cover at the larger scale, perhaps because the disintegration of the dune vegetation proceeds less quickly in this less shading shrub species. The effects of R. rugosa on species diversity were more dramatic than that of H. rhamnoides, which again is best explained by the different growth forms of the two species. Similar effects of decrease in species richness were shown in a comparative study of Juniperus communis and Potentilla fruticosa L. (Rejma´nek and Rose´n, 1988, 1992). Considering the conditions within one vegetation type, for example dune slacks and grasslands, respectively, species diversity decreased with increasing plot size because of increasing small-scale habitat heterogeneity (Wilson et al., 1999). In the case of a transition from homogeneous grassland to H. rhamnoides shrubland, at larger scales evenness as mentioned above, at first increased and than decreased, probably because of increasing vegetation structure. In contrast, there was a monotonically decline in evenness with establishing of dominant R. rugosa shrubland. In general, species richness patterns are scale-dependent. In this study, the effects of shrub expansion on the species richness were, with few exceptions, more pronounced in the larger plot sizes. But at a small-scale R. rugosa stands showed a more improved linear decline in species diversity than H. rhamnoides stands, because R. rugosa showed already at low dominance levels stronger shading-out effects than H. rhamnoides.
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Table 2. Species richness and diversity (Shannon–Wiener-index and evenness) of H. rhamnoides and R. rugosa shrubland in relation to shrub cover examined at two spatial scales, 1 and 16 m2 Plot size
Hippophae¨ shrubland
Rosa shrubland
t-test
SD
b
R2adj
Species richness Total no. of species 1 13.03 16 22.03
4.75 9.01
0.05 0.12
0.02 0.13
0.184 0.020
9.95 12.86
4.23 4.75
0.09 0.10
0.42 0.53
0.001 0.000
No. of shrubs 1 1.74 16 2.38
1.50 0.98
0.03 0.01
0.23 0.11
0.002 0.030
1.48 2.12
0.87 1.84
0.01 0.02
0.03 0.05
0.206 0.169
No. of herbaceous species 1 9.63 4.48 16 17.18 7.74
0.07 0.10
0.09 0.14
0.038 0.018
6.91 8.76
3.87 4.54
0.09 0.12
0.58 0.80
0.000 0.000
* *
No. of mosses and lichens 1 1.71 1.34 16 2.74 1.91
0.01 0.03
0.00 0.16
0.493 0.011
1.57 1.71
1.47 1.65
0.00 0.00
0.00 0.00
0.833 0.736
*
No. of typical grassland species 1 8.11 4.11 16 14.32 7.12
0.08 0.14
0.22 0.33
0.003 0.000
6.19 7.57
4.14 5.05
0.09 0.13
0.53 0.75
0.000 0.000
*
No. of typical shrubland species 1 3.97 1.90 16 6.03 2.79
0.03 0.03
0.10 0.05
0.039 0.117
3.14 4.57
2.01 3.41
0.01 0.02
0.00 0.01
0.533 0.271
*
Mn
p
Mn
SD
b
R2adj
p
* *
Species diversity Shannon index 1 1.49 16 2.01
0.38 0.51
0.008 0.008
0.22 0.21
0.002 0.004
1.04 1.30
0.55 0.54
0.010 0.013
0.64 0.64
0.000 0.000
* *
Evenness 1 16
0.09 0.09
0.002 0.001
0.29 0.19
0.001 0.006
0.45 0.51
0.19 0.17
0.004 0.003
0.51 0.45
0.000 0.000
* *
0.59 0.66
Means (Mn) and standard deviations (SD) are given for both plot sizes. Linear regressions of species richness and diversity depending on shrub cover are compared by means of the percentage of variation explained (R2adj) and significance probabilities (p); b ¼ slope of regression. The t-test refers to the comparison of species richness and diversity between H. rhamnoides and R. rugosa plots, with significant results (po0.05) marked with an asterisk.
Other studies rendered also different result concerning scale dependence: Responses to changed environmental conditions often happen faster and more distinct at smaller spatial scales, as, for example, shown for calcareous grasslands on O¨land, Sweden (Huber, 1994, 1999; Rejma´nek and Rose´n, 1988). In a short grass steppe in Colorado, the dominant grass species Bouteloua gracilis (Kunth) Lag. ex. Griffiths and Buchloe dactyloides (Nutt.) Engelm. affected species richness only at small plot sizes (o3 m2), and species richness at small scales changed more rapidly than at larger scales due to stronger effects of altered biotic interactions such as competition (Singh et al., 1996). However, effects of scale are not always evident: in wet meadows in Wisconsin, there was a negative correlation between
species richness and the cover of Phalaris arundinacea L. both in small (1 m2) and large plots (4500 m2) (Kercher et al., 2004). Considering conservation aspects, the expansion of shrubs into species-rich grey dunes is highly problematic: Dune shrublands, which are characterised by the dominance of one or few species, a simple vegetation structure, the scarcity of gaps, and the absence of rare species, especially many typical elements of open dune grasslands, have a low conservation value compared to the more open grey dunes (Mortimer et al., 2000). These effects and consequences are even more pronounced in R. rugosa than in H. rhamnoides shrublands, because of the stronger decline of species diversity in the former case, due to a more intensified shading-out effect.
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3.0
Shannon Index
2.5 2.0 1.5 1.0 0.5 0.0
Hippophaë rhamnoides Rosa rugosa
20
0
40 60 Shrub cover [%]
80
100
80
100
0.8
Evenness
0.6 0.4 0.2 0
Hippophaë rhamnoides Rosa rugosa
0
20
40 60 Shrub cover [%]
Fig. 1. Relationship between Shannon index (above) and evenness (below) in large plots and shrub cover of H. rhamnoides (filled symbols) and R. rugosa (unfilled symbols). For regression statistics, see Table 2.
Acknowledgments The author expresses her thanks to the Administration of the Wadden Sea National Park of Lower Saxony for permission of access to the study area, to Sonja Heemann for field work in the H. rhamnoides shrubland; and to Martin Diekmann and two anonymous reviewers for critical comments on earlier drafts of the manuscript.
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