Micro-topographic heterogeneity increases plant diversity in old stages of restored grasslands

Basic and Applied Ecology 16 (2015) 291–299

Micro-topographic heterogeneity increases plant diversity in old stages of restored grasslands Balázs Deáka , Orsolya Valkóa,∗ , Péter Törökb , András Kelemena , Tamás Miglécza , Szilárd Szabóc , Gergely Szabóc , Béla Tóthmérésza a

MTA-DE Biodiversity and Ecosystem Services Research Group, Egyetem tér 1, Debrecen H-4032, Hungary Department of Ecology, University of Debrecen, Egyetem tér 1, Debrecen H-4032, Hungary c Department of Physical Geography and Geoinformatics, Egyetem tér 1, Debrecen H-4032, Hungary b

Received 29 August 2014; accepted 20 February 2015 Available online 27 February 2015

Abstract It is a truism in ecology that environmental heterogeneity increases diversity. Supporting field studies are mostly concerned with a large-scale topographic heterogeneity, ranging from a couple of metres to landscape-scale gradients. To test the role of fine-scale micro-topography on plant diversity, we studied the initial vegetation of recently filled (1-year-old), and established vegetation on old (7-year-old) soil-filled channels in an alkali landscape, East-Hungary. We hypothesised that (i) recently filled channels are characterised by a high cover of ruderal species and high species diversity and (ii) high micro-topographic heterogeneity increases the diversity of species and plant strategy types (mixed C–S–R categories) in early stages but later on this effect diminishes. We found that diversity of species and plant strategy types was higher in recently filled channels compared to old filled channels. Micro-topographic heterogeneity had no effect on the studied vegetation parameters in recently filled channels. Conversely, in old filled channels higher micro-topographic heterogeneity resulted in higher diversity and lower cover of the dominant grass Festuca pseudovina. Higher micro-topographic heterogeneity resulted in increased ruderality and decreased stress-tolerance, but it did not increase the diversity of plant strategy types. In contrast with former studies, we found that a couple of centimetres of micro-topographic heterogeneity had no effect on vegetation in recently filled channels, but supported a high diversity in old filled channels. An important practical implication of our study is that in grassland restoration projects, micro-topographic heterogeneity has a crucial role in sustaining biodiversity.

Zusammenfassung Es ist eine einfache ökologische Wahrheit, dass eine heterogene Umwelt die Diversität steigert. Freilandstudien, die dies unterstützen, betrachten meist großskalige topographische Heterogenität von einigen Metern bis hin zu Landschaftsgradienten. Um die Bedeutung feinskaliger Mikro-Topographie auf die Pflanzendiversität zu überprüfen, untersuchten wir, die anfängliche Vegetation von kürzlich (1 Jahr) verfüllten Entwässerungskanälen und die etablierte Vegetation von alten (7 Jahre) verfüllten Kanälen in einer Alkalilandschaft (Ost-Ungarn). Wir postulierten, dass (i) kürzlich verfüllte Kanäle durch eine hohe Bedeckung von Ruderalpflanzen und hohe Artendiversität charakterisiert sein sollten, dass (ii) hohe mikro-topographische Heterogenität die Artendiversität und die Diversität der Pflanzenstrategietypen (C–S–R-Kategorien) in frühen Stadien steigern sollte,

∗ Corresponding

author. Tel.: +36 52 512 900/22631; fax: +36 52512743. E-mail address: [email protected] (O. Valkó).

http://dx.doi.org/10.1016/j.baae.2015.02.008 1439-1791/© 2015 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

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während dieser Effekt später geringer wird. Wir fanden, dass die Diversität der Pflanzenarten und Strategietypen bei kürzlich verfüllten Kanälen höher war als bei alten Kanälen. Die mikro-topographische Heterogenität hatte bei kürzlich verfüllten Kanälen keinen Effekt auf die untersuchten Vegetationsparameter. Dagegen resultierte bei alten verfüllten Kanälen eine höhere mikrotopographische Heterogenität in höherer Diversität und geringerer Bedeckung durch das dominante Gras Festuca pseudovina. Höhere mikro-topographische Heterogenität bewirkte vermehrte Ruderalität und verminderte Stresstoleranz, aber sie erhöhte nicht die Diversität der Pflanzenstrategietypen. Im Gegensatz zu früheren Studien fanden wir, dass mikro-topographische Heterogenität von ein paar Zentimetern bei kürzlich verfüllten Kanälen keinen Einfluss auf die Vegetation hatte, dass aber eine hohe Diversität in alten verfüllten Kanälen unterstützt wurde. Eine wichtige praktische Schlussfolgerung aus unserer Studie ist, dass die mikro-topographische Heterogenität eine entscheidende Rolle für den Erhalt der Biodiversität in GraslandRestaurationsprojekten spielt. © 2015 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

Keywords: Alkali landscape; C–S–R strategies; Elevation; Functional diversity; Grassland restoration; Plant trait; Soil disturbance; Succession, Topography

Introduction Understanding processes shaping the spatial pattern of vegetation has been in the focus of vegetation science for decades (Newman 1982). In this respect the relationship between environmental heterogeneity and diversity is of crucial importance (Sebastiá 2006; Tamme, Hiiesalu, Laanisto, Szava-Kovats & Pärtel 2010). Heterogeneity of abiotic environment generally supports high species diversity at multiple scales (Lundholm 2009; Stein, Gerstner & Kreft 2014). The niche theory suggests that species with different resource preferences can co-exist in a heterogeneous environment due to niche differentiation (Newman 1982; Tamme et al. 2010; Richardson, MacDougall & Larson 2012). Smallscale environmental heterogeneity is often represented by micro-topographic heterogeneity (Rose & Malanson 2012). Micro-topographic heterogeneity enables diverse germination and establishment conditions for a wide range of species providing safe sites in various quality and quantity (Tilman 1994). Micro-topographic heterogeneity has also several indirect effects on diversity by affecting other environmental variables like soil moisture (Vivian-Smith 1997; Moeslund, Arge, Bøcher, Dalgaard, Ejrnæs et al. 2013), light availability and solar radiation (Hough-Snee, Long, Jeroue & Ewing 2011), soil salt-content (Valkó, Tóthmérész, Kelemen, Simon, Miglécz et al. 2014) or nutrient availability (Loiseau, Louault, Le Roux, & Bardy 2005). By creating various micro-sites, micro-topographic heterogeneity is considered to increase plant diversity both in natural (Moeslund, Arge, Bøcher, Nygaard & Svenning 2011) and experimental ecosystems (Vivian-Smith 1997; Biederman & Whisenant 2011). Although the link between environmental heterogeneity and diversity is a hot topic in community ecology, opinion and review papers have pointed out that most of the published literature focused on the beneficial effects of large-scale (sampling unit bigger than 200 m2 ) environmental heterogeneity on diversity (Stein et al. 2014; Lundholm 2009). There are some fine-scale field studies testing this

relationship (Moeslund, Arge, Bøcher, Dalgaard, Ejrnæs et al. 2013; Moeslund, Arge, Bøcher, Dalgaard, Odgaard et al. 2013), but most of these studies focus on wetlands. Recent reviews found only one experimental and four field studies on fine-scale micro-topography – plant diversity relationships (sampling unit smaller than 200 m2 ; Lundholm 2009). Most of these studies are either experimental ones or focus on restored ecosystems, likely because these systems are more dynamic compared to permanent plant communities. In most cases the effects of micro-topographic heterogeneity were studied only for a short time, thus temporal effects could not be considered. Although in the few cases when temporal patterns were considered, it was found that microtopographic heterogeneity supports diversity only in the short run in the first few years after disturbance; however, later its effect diminishes (Ewing 2002; Biederman & Whisenant 2011). There is a growing consensus that trait-based analyses contribute to a better understanding of community assembly processes (Lavorel & Garnier 2002). The competitor–stress–ruderal (C–S–R) classification of plant strategy types (Grime 2002) is frequently used to explore the functional composition of vegetation, reflecting environmental conditions and biotic interactions in plant communities (Hunt, Hodgson, Thompson, Bungener, Dunnett et al. 2004; Cerabolini, Brusa, Ceriani, De Andreis, Luzzaro et al. 2010). Grime (2002) classified species into three main functional groups based on their tolerance to disturbance and stress, i.e. competitors (C), stress-tolerators (S) and ruderals (R). Competitors are generally perennial, large-sized plants with dense canopy structure and high ability of rapid lateral spread. Stress-tolerators are often slow-growing species with a high root-shoot ratio. Ruderals are generally short-lived small-sized herbs with limited lateral spread, characterised by sparse canopy structure and increased rate of seed production (Grime 2002; Kelemen, Török, Valkó, Miglécz & Tóthmérész 2013). Micro-topography can be a crucial driver of local patterns in soil moisture in habitats located within a few metres

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in vertical distance from a water table (Moeslund, Arge, Bøcher, Dalgaard & Svenning 2013). Alkali landscapes of Central-Europe provide an excellent opportunity to study the effects of fine-scale micro-topographic heterogeneity on diversity. Alkali grasslands are characterised by high microtopographic heterogeneity; various types of grasslands and marshes form a complex and dynamic mosaic structure driven by the differences in the soil salt-content and water table. These two crucial environmental factors correlate strongly with micro-topography (Deák, Valkó, Alexander, Mücke, Kania et al. 2014a). In alkali grasslands even minor changes in micro-topography (a few centimetres) result in considerable changes in these environmental parameters (Valkó et al. 2014). Thus, micro-topography is responsible for the spatial distribution of grassland types and fine-scale species composition of pristine alkali grasslands (Valkó et al. 2014). In the Hortobágy region (East-Hungary) in the 1950s and 1960s landscape-scale networks of drainage channels were established to support crop-production and agricultural intensification. In recent years, several landscape-scale restoration projects were started to eliminate these channels. The goal of these restoration projects was to restore former landscape connectivity and support grazing regimes. The overall aim is to suppress ruderal species and to recover grassland vegetation characterised by perennial grasses and target species of alkali grasslands. Grassland restoration projects in the study region reported on fast grassland recovery, but the initial vegetation was generally characterised by a high cover and diversity of ruderal species, which were able to rapidly colonise recently disturbed areas (Török, Deák, Vida, Valkó, Lengyel et al. 2010). We tested the relationship of micro-topography and diversity in a highly heterogeneous alkali landscape. To test the role of micro-topography and its temporal aspects on fine-scale plant diversity, we studied the initial vegetation of recently filled channels (1-year-old vegetation) and established vegetation on old filled channels (7-year-old vegetation). We aimed at to test the following hypotheses:

(i) After disturbance (soil filling and levelling) vegetation is generally characterised by a high cover of ruderal species and high species diversity in the initial year, but later on with increasing perennial cover the species diversity decreases (e.g. Bonet & Pausas 2004). Thus, we hypothesised that recently filled channels would be characterised by ruderal species, and high diversity of species and plant strategy types. (ii) Micro-topographic heterogeneity was found to increase diversity in early stages by providing a variety of microhabitats (Ewing 2002; Biederman & Whisenant 2011). Thus, we hypothesised that high micro-topographic heterogeneity would increase diversity of species and of plant strategy types in early stages, but later on this effect diminishes.

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Fig. 1. Sketch map of a filled channel showing the sampling design.

Materials and methods Study sites Our study sites are in the Hortobágy National Park (EastHungary) (N 47◦ 30 E 21◦ 12 ). The Hortobágy region is characterised by alkali grasslands, marshes and loess grasslands, forming one of the largest open habitat complex in Europe (Deák, Valkó, Török & Tóthmérész 2014b). Short alkali grasslands are typical on meadow solonetz soils. Their vegetation is generally species-poor, characterised by the short grass species Festuca pseudovina and salttolerant forbs, such as Artemisia santonicum, Aster tripolium ssp. pannonicum, Limonium gmelinii ssp. hungaricum and Podospermum canum (Kelemen, Török, Valkó, Deák, Tóth et al. 2015). For the present study, we selected 12 soil-filled former drainage channels. The width of the filled channels was 8 m; the depth of the channels was approximately 0.8 m. The channels were filled with the soil of the embankments (constructed from the excavated soil). There were no other restoration measures applied after soil-filling and levelling of the soil surface. The filled channels were surrounded by pristine alkali grasslands on both sides, which were managed by moderate cattle grazing.

Sampling design We selected six recently (1-year-old) and six old (7-yearold) filled channels. We designated three cross-sections per channel; the distance between cross-sections was 200 m. On each cross-section we surveyed four 1 m × 1 m plots; altogether 12 plots were surveyed per channel (see Fig. 1). The percentage cover of vascular plants was recorded in each plot in June 2012. Fine-scale micro-topography was measured by a high-precision geodetic survey using TRIMBLE S9 GPS devices in June 2012. Elevation was measured in the centroid

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Table 1. Effects of vegetation age and elevation range (as predictors) and their interaction on vegetation characteristics (dependent variables) considering the location of the channels as a random factor (GLMM). Vegetation characteristic

Predictors

Shannon diversity

Age Elevation range A × ER

Festuca pseudovina cover

Coefficient ± SE

t

p

0.524 ± 0.183 3.365 ± 1.550 −4.041 ± 1.980

2.856 2.171 −2.041

0.007 0.037 0.050

Age Elevation range A × ER

−57.347 ± 13.304 −297.285 ± 129.290 292.944 ± 129.995

−4311 −2.299 2.253

0.000 0.028 0.031

Shannon diversity of CSR strategies

Age Elevation range A × ER

0.513 ± 0.183 2.900 ± 1.503 −3.254 ± 1.902

2.806 1.929 −1.711

0.008 0.063 0.097

Cover-weighted C-coordinates

Age Elevation range A × ER

0.068 ± 0.145 2.266 ± 1.260 −0.621 ± 1.670

0.472 1.798 −0.372

0.640 0.082 0.712

Cover-weighted S-coordinates

Age Elevation range A × ER

−0.718 ± 0.207 −2.609 ± 1.772 5.880 ± 2.286

−3.476 −1.472 2.537

0.001 0.151 0.016

Cover-weighted R-coordinates

Age Elevation range A × ER

1.220 ± 0.270 3.461 ± 2.182 −5.694 ± 2.749

4.511 1.586 −2.071

0.000 0.123 0.046

Significant effects are marked with boldface.

of each plot with an accuracy of 1 cm, thus we had 4 discrete elevation data for each cross-section.

C–S–R classification Grime’s C–S–R strategy system (Grime 2002) was finetuned by Hodgson, Wilson, Hunt, Grime, and Thompson (1999), who built up a system containing 19 mixed C–S–R category types. We classified all species into these mixed C–S–R categories, based on our own plant trait measurements. The classification followed Hodgson et al. (1999) and Kelemen et al. (2013). We used seven plant traits as predictor variables (canopy height, leaf dry matter content, flowering period, flowering start, lateral spread, leaf dry weight and specific leaf area). The result of the classification was a mixed C–S–R category type determined by three coordinates describing competitiveness, stress-tolerance and ruderality (C-, S- and R-coordinates, respectively) for each species. The score for each coordinate was an integer between −2 and +2; higher scores refer to higher competitiveness, stress-tolerance or ruderality respectively. The species classifications are listed in Appendix A. We calculated the cover-weighted average of the coordinates and also the Shannon diversity of mixed C–S–R categories for each plot.

Data processing Micro-topographic heterogeneity along a cross-section can be expressed by the elevation range (i.e. the elevation

difference between the lowest- and highest-elevated points) and the standard deviation of elevation scores. Before model fitting, we calculated the Pearson correlation coefficient between the elevation range and standard deviation of the elevation, in order to avoid the inclusion of highly correlated predictors within the same model. As the two parameters showed a significant positive correlation (R = 0.981; p < 0.001) we decided to use only elevation range for further calculations. Differences between the elevation range scores of the recently- and old filled channels were analysed by independent samples t-test. For all calculations we used pooled vegetation data from the four plots along each cross-section (n = 36). Generalized Linear Mixed Model (GLMM; McCulloch & Neuhaus 2001) was calculated for exploring the effect of vegetation age and elevation range (predictors) and their interaction on the vegetation characteristics (dependent variables; i.e. Shannon diversity, cover of F. pseudovina, Shannon diversity of mixed C–S–R categories, cover-weighted C-, S- and R-coordinates). In the GLMMs, location of the channels was considered as a random factor. Species composition (based on the percentage cover of the ˇ species) was plotted by a PCA ordination (Lepˇs & Smilauer 2003). Elevation range, Shannon diversity and the coverweighted C-, S- and R-coordinates were included as overlay using weighted averages. Univariate statistics were calculated using SPSS 20.0 program package, PCA was calculated using CANOCO 4.5 program package.

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Fig. 2. Relationship between elevation range and Shannon diversity in the studied channels. Recently filled channels are denoted by empty symbols and dashed line, while old filled channels are denoted by full symbols and continuous line. Lines are used to demonstrate the trends. Linear regression; R2 = 0.02, p = 0.557 for recently filled channels and R2 = 0.42; p = 0.004 for old filled channels.

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Fig. 3. Relationship between elevation range and the cover of Festuca pseudovina in the studied channels. Recently filled channels are denoted by empty symbols and dashed line, while old filled channels are denoted by full symbols and continuous line. Lines are used to demonstrate the trends. Linear regression; R2 = 0.01, p = 0.732 for recently filled channels and R2 = 0.69; p < 0.001 for old filled channels.

Results Diversity and age We recorded altogether 77 vascular plant species in the study sites, from which 75 were present in the recently filled channels and 28 in the old filled channels. Shannon diversity was significantly higher in the recently filled channels compared to the old filled channels (Table 1). The cover of F. pseudovina was significantly higher, whereas Shannon diversity of mixed C–S–R categories was significantly lower in the old filled channels than in the recently filled ones (Table 1). The cover-weighted C-coordinates were not different between the recently and old filled channels. The cover-weighted S-coordinates were significantly lower, while the cover-weighted R-coordinates were significantly higher in the recently filled channels compared to the old filled channels (Table 1).

Diversity and micro-topographic heterogeneity Elevation range along cross-sections was between 2–16 cm in recently filled channels, and 2–15 cm in old filled channels. Elevation range along cross sections was not different between recently and old filled channels (t-test; t = 0.089; df = 34; p = 0.93). We found that increasing elevation range increased significantly Shannon diversity and decreased the cover of F. pseudovina (Table 1; Figs. 2 and 3). There was a significant interaction between vegetation age and elevation range on Shannon diversity, the cover of F. pseudovina, coverweighted S- and R-coordinates (Table 1). Cover-weighted

S-coordinates decreased, while cover-weighted Rcoordinates increased with increasing elevation range in the old filled channels (Fig. 4). Elevation range had no effect on the Shannon diversity of mixed CSR categories (Fig. 5). In the case of the recently filled channels the ordination showed that elevation range had only a slight influence on the species composition (Fig. 6A). Species in the recently filled channels were randomly scattered throughout the PCA space. The ordination of the old filled channels showed that Shannon diversity, ruderality and competitiveness (expressed as cover weighted C- and R-coordinates) increased with increasing elevation range, while stress-tolerance (expressed as coverweighted S-coordinates) decreased with increasing elevation range (Fig. 6B). The majority of the species were also plotted towards the direction of C and R and were positively correlated with elevation range. The cover of the dominant grass F. pseudovina was negatively correlated with elevation range.

Discussion Diversity and age Supporting our first hypothesis we found higher species richness and Shannon diversity scores in recently filled channels compared to old filled channels. In our study sites, there is a high diaspore availability in the landscape, thus propagule limitation likely did not hamper the colonisation of the newly

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Fig. 4. Relationship between elevation range and the cover-weighted C-, S-, and R-coordinates in the studied channels. Recently filled channels are denoted by empty symbols and dashed line, while old filled channels are denoted by full symbols and continuous line. Lines are used to demonstrate the trends. Linear regression; C-coordinates: R2 = 0.11, p = 0.178 for recently filled channels and R2 = 0.28; p = 0.025 for old filled channels; S-coordinates: R2 = 0.20, p = 0.062 for recently filled channels and R2 = 0.28; p = 0.025 for old filled channels; R-coordinates: R2 = 0.22, p = 0.055 for recently filled channels and R2 = 0.47; p = 0.002 for old filled channels.

created soil surfaces. These results also support the general finding that after soil disturbance, a wide set of species with effective dispersal in space (mostly anemo- or hydrochory) or time (e.g. possessing persistent seed banks) can establish rapidly on newly created open soil surfaces (Bischoff, Warthemann & Klotz 2009). We found that total species richness was approximately three times higher in recently filled channels compared to old ones. In contrast, the cover of F. pseudovina, the dominant perennial grass of alkali grasslands was significantly higher in old filled channels compared to recently filled ones. Thus, in old filled channels, establishment of further species was likely limited by the biotic

filtering effect of F. pseudovina (see also Myers & Harms 2009). We found that recently filled channels were characterised by ruderal species, and high diversity of plant strategy types, which confirmed our first hypothesis. The magnitude of ruderality was lower in old filled channels compared to recently filled ones, also supporting the importance of biotic filtering (Myers & Harms 2009; Kelemen et al. 2013). The high variability in plant strategies and high number of co-existing species is likely due to random establishment processes provided both by seed banks and spatial dispersal. High diversity was likely also supported by the lack of well developed biotic interactions and also the lack of late-succession competitor species which hamper the establishment of subordinate species by biotic filtering (Wellstein, Campetella, Spada, Chelli, Mucina et al. 2014). On the contrary, in old filled channels, diversity of mixed C–S–R categories decreased likely because of the developed dense canopy of F. pseudovina (belonging to the S/SC group).

Diversity and micro-topographic heterogeneity

Fig. 5. Relationship between elevation range and the diversity of mixed C–S–R categories in the studied channels. Recently filled channels are denoted by empty symbols and dashed line, while old filled channels are denoted by full symbols and continuous line. Lines are used to demonstrate the trends. Linear regression; R2 = 0.06, p = 0.336 for recently filled channels and R2 = 0.24; p < 0.042 for old filled channels.

In spite of the similar ranges of micro-topographic heterogeneity detected in recently and old filled channels, its effect on diversity was different. We found that micro-topographic heterogeneity increased Shannon diversity in the old filled channels, but had no effect in recently filled ones. This partly confirmed our second hypothesis and conclusions of Biederman and Whisenant (2011) and Ewing (2002). The likely explanation could be, that vegetation composition in recently filled channels was predominantly driven by ‘random’ auto- and allogenic species establishment processes driven by local propagule banks and spatial dispersal (Rebele 1992; Wilson 1992). Thus the species composition was a mixture of the species pool of the site and surroundings proposed also by the neutral theory of co-existence (Hubbell 2001). Several other studies (Bissels, Donath, Hölzel & Otte 2006; Moeslund, Arge, Bøcher, Dalgaard, & Svenning 2013)

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Fig. 6. PCA ordination plot on the species composition of recently (A) and old filled channels (B). Elevation range, Shannon diversity and the cover-weighted C-, S- and R-coordinates were included as overlay. Species are abbreviated by the first four letters of their genus and species names respectively. Numbers represent the average of the four plots at one cross-section. Cumulative percentage variance of species data were 44.5 and 62.6 in recently filled channels and 49.1 and 71.9 in old filled channels for the first and second axis, respectively.

found that spatial heterogeneity supports diversity in the early years of succession, as micro-depressions can protect seeds from herbivores and wind, which increases seedling establishment. The effect of biotic filter was also low, because the recently filled channels were characterised by open soil surfaces (Myers & Harms 2009). We found that micro-topographic heterogeneity increased Shannon diversity in old filled channels. Micro-topographic heterogeneity generally supports the co-existence of species with a wide range of environmental needs by providing

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various micro-sites which can lead to effective niche differentiation (Wacker, Baudois, Eichenberger-Glinz & Schmid 2008; Tamme et al. 2010). In old filled channels, microtopographic heterogeneity likely provided a mosaic of relatively moist micro-sites at low and dry micro-sites at high elevations due to different local drainage patterns (Moeslund, Arge, Bøcher, Dalgaard, Odgaard et al. 2013). Increased micro-topographic heterogeneity also suppressed the dominant species (F. pseudovina) of alkali grasslands in old filled channels. Increased heterogeneity of microsites with a mosaic of suitable and unsuitable (moist) micro-sites likely acted as an abiotic filter for the establishment of the dry grassland species F. pseudovina (see also Moeslund, Arge, Bøcher, Dalgaard, Odgaard et al. 2013). Thus, it likely affected biotic relationships by shifting competitive interactions between species (Wacker et al. 2008; Myers & Harms 2009). It seems that even these very small, few-centimetre differences in micro-topographic heterogeneity provide heterogeneous mosaics representing alternative states for species assemblages resulting in a higher number of co-existing species. These results support the multistate model of community assembly (Drake, Zimmermann, Purucker & Rojo 1999). Micro-topographic heterogeneity determined the distribution of mixed C–S–R strategy types in old filled channels. Competitiveness was not affected, but stresstolerance decreased and ruderality increased with increasing micro-topographic heterogeneity. The main reason for decreased stress-tolerance might be that the dominant F. pseudovina belonging to the S/SC group was suppressed by increased micro-topographic heterogeneity. Micro-topographic heterogeneity resulted in a fine-scale mosaic, where stress-tolerators were probably restricted to highly stressed micro-sites which were suboptimal for other species (Grime 2002). A possible reason for the increased ruderality might be that micro-topographic heterogeneity hindered the development of a closed vegetation. Thus more micro-sites were available for ruderals which require open surfaces for germination and establishment (Kelemen et al. 2013). In spite of the detected positive effect of microtopographic heterogeneity on species diversity we found no effect of micro-topographic heterogeneity on the diversity of mixed C–S–R categories in old filled channels. The most likely explanation is that the decrease of stress-tolerator strategies was balanced by the increase of ruderals. Our results showed that after the filling of the channels, a random assemblage characterised by high ruderality emerged from local seed banks and micro-topographic heterogeneity had no effect on the species diversity in recently filled channels. In old filled channels we found that fine-scale (a couple of centimetres) micro-topographic heterogeneity was a crucial factor controlling diversity. Our findings are in contrast with former studies, which found that immediately after soil disturbance high micro-topographic heterogeneity supports the establishment of a wide range of species, but later on biotic filters likely obscure these effects (Biederman & Whisenant

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2011; Ewing 2002). An important practical implication of our study is that in grassland restoration actions microtopographic heterogeneity can have contradictory effects on restoration success. On the one hand, high micro-topographic heterogeneity is beneficial for sustaining a high diversity and increasing the local species pool. On the other hand, we found that high micro-topographic heterogeneity decreased the establishment success of F. pseudovina, a characteristic species of the target grasslands. Thus, precise soil levelling is essential when eliminating landscape scars and restoring perennial grass cover is needed.

Acknowledgements We are thankful to I. Kapocsi, Sz. G˝ori, and L. Gál for their help in fieldwork. Authors were supported by TÁMOP4.2.4.A/2-11-1-2012-0001, TÁMOP-4.2.1./B-09/1/KONV2010-0007, TÁMOP-4.2.2/B-10/1-2010-0024 and TÁMOP4.2.2/C-11/1/KONV-2012-0010 projects, OTKA PD 100192, OTKA PD 111807 and by the Internal Research Grant of the Debrecen University.

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.baae.2015.02.008.

References Biederman, L. A., & Whisenant, S. G. (2011). Using mounds to create microtopography alters plant community development early in restoration. Restoration Ecology, 19, 53–61. Bischoff, A., Warthemann, G., & Klotz, S. (2009). Succession of floodplain grasslands following reduction in land use intensity: The importance of environmental conditions, management and dispersal. Journal of Applied Ecology, 46, 241–249. Bissels, S., Donath, T. W., Hölzel, N., & Otte, A. (2006). Effects of different mowing regimes on seedling recruitment in alluvial grasslands. Basic and Applied Ecology, 7, 433–442. Bonet, A., & Pausas, J. G. (2004). Species richness and cover along a 60-year chronosequence in old-fields of southeastern Spain. Plant Ecology, 174, 257–270. Cerabolini, B. E. L., Brusa, G., Ceriani, R. E., De Andreis, R., Luzzaro, A., & Pierce, S. (2010). Can CSR classification be generally applied outside Britain? Plant Ecology, 210, 253–261. Deák, B., Valkó, O., Alexander, C., Mücke, W., Kania, A., Tamás, J., et al. (2014). Fine-scale vertical position as an indicator of vegetation in alkali grasslands – Case study based on remotely sensed data. Flora, 209, 693–697. Deák, B., Valkó, O., Török, P., & Tóthmérész, B. (2014). Solonetz meadow vegetation (Beckmannion eruciformis) in East-Hungary – An alliance driven by moisture and salinity. Tuexenia, 34, 187–203.

Drake, J. A., Zimmermann, C. R., Purucker, T., & Rojo, C. (1999). On the nature of the assembly trajectory. In E. Weiher, & P. Keddy (Eds.), Ecological assembly rules: Perspectives, advances, retreats (pp. 233–250). Cambridge: Cambridge University Press. Ewing, K. (2002). Mounding as a technique for restoration of prairie on a capped landfill in the Puget Sound lowlands. Restoration Ecology, 10, 289–296. Grime, J. P. (2002). Plant strategies and vegetation processes. New York: John Wiley and Son. Hodgson, J. G., Wilson, P. J., Hunt, R., Grime, J. P., & Thompson, K. (1999). Allocating C–S–R plant functional types: A soft approach to a hard problem. Oikos, 85, 282–296. Hough-Snee, N., Long, L. A., Jeroue, L., & Ewing, K. (2011). Mounding alters environmental filters that drive plant community development in a novel grassland. Ecological Engineering, 37, 1932–1936. Hubbell, S. P. (2001). The unified neutral theory of biodiversity and biogeography. Princeton, NJ, US: Princeton University Press. Hunt, R., Hodgson, J. G., Thompson, K., Bungener, P., Dunnett, N. P., & Askew, A. P. (2004). A new practical tool for deriving a functional signature for herbaceous vegetation. Applied Vegetation Science, 7, 163–170. Kelemen, A., Török, P., Valkó, O., Deák, B., Tóth, K., & Tóthmérész, B. (2015). Both facilitation and limiting similarity shape the species coexistence in dry alkali grasslands. Ecological Complexity, 21, 34–38. Kelemen, A., Török, P., Valkó, O., Miglécz, T., & Tóthmérész, B. (2013). Mechanisms shaping plant biomass and species richness: Plant strategies and litter effect in alkali and loess grasslands. Journal of Vegetation Science, 24, 1195–1203. Lavorel, S., & Garnier, E. (2002). Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the Holy Grail. Functional Ecology, 16, 545–556. ˇ Lepˇs, J., & Smilauer, P. (2003). Multivariate analysis of ecological data using CANOCO. Cambridge: Cambridge University Press. Loiseau, P., Louault, F., Le Roux, X., & Bardy, M. (2005). Does extensification of rich grasslands alter the C and N cycles, directly or via species composition? Basic and Applied Ecology, 6, 275–287. Lundholm, J. T. (2009). Plant species diversity and environmental heterogeneity: Spatial scale and competing hypotheses. Journal of Vegetation Science, 20, 377–391. McCulloch, C., & Neuhaus, J. (2001). Generalized linear mixed models. John Wiley & Sons, Ltd. Moeslund, J. E., Arge, L., Bøcher, P. K., Dalgaard, T., Ejrnæs, R., Odgaard, M. E., et al. (2013). Topographically controlled soil moisture drives plant diversity patterns within grasslands. Biodiversity and Conservation, 22, 2151–2166. Moeslund, J. E., Arge, L., Bøcher, P. K., Dalgaard, T., Odgaard, M. V., Nygaard, B., et al. (2013). Topographically controlled soil moisture is the primary driver of local vegetation patterns across a lowland region. Ecosphere, 4(7), article number 91 Moeslund, J. E. M., Arge, L., Bøcher, P. K., Dalgaard, T., & Svenning, J.-C. (2013). Topography as a driver of local terrestrial vascular plant diversity patterns. Nordic Journal of Botany, 31, 129–144. Moeslund, J. E., Arge, L., Bøcher, P. L., Nygaard, B., & Svenning, J. C. (2011). Geographically comprehensive assessment of

B. Deák et al. / Basic and Applied Ecology 16 (2015) 291–299

salt-meadow vegetation-elevation relations using LiDAR. Wetlands, 31, 471–482. Myers, J. A., & Harms, K. E. (2009). Seed arrival, ecological filters, and plant species richness: A meta-analysis. Ecology Letters, 12, 1250–1260. Newman, E. I. (1982). The plant community as a working mechanism. Oxford: Blackwell Science Publisher. Rebele, F. (1992). Colonization and early succession on anthropogenic soils. Journal of Vegetation Science, 3, 201–208. Richardson, P. J., MacDougall, A. S., & Larson, D. W. (2012). Fine-scale spatial heterogeneity and incoming seed diversity additively determine plant establishment. Journal of Ecology, 100, 939–949. Rose, J. P., & Malanson, G. P. (2012). Microtopographic heterogeneity constrains alpine plant diversity, Glacier National Park, MT. Plant Ecology, 213, 955–965. Sebastiá, M. T. (2006). Role of topography and soils in grassland structuring at the landscape and community scales. Basic and Applied Ecology, 5, 331–346. Stein, A., Gerstner, K., & Kreft, H. (2014). Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters, 17, 866–880. Tamme, R., Hiiesalu, I., Laanisto, L., Szava-Kovats, R., & Pärtel, M. (2010). Environmental heterogeneity, species diversity and co-existence at different spatial scales. Journal of Vegetation Science, 21, 796–801.

299

Tilman, D. (1994). Competition and biodiversity in spatially structured habitats. Ecology, 75, 2–16. Török, P., Deák, B., Vida, E., Valkó, O., Lengyel, Sz., & Tóthmérész, B. (2010). Restoring grassland biodiversity: Sowing low-diversity seed mixtures can lead to rapid favourable changes. Biological Conservation, 143, 806–812. Valkó, O., Tóthmérész, B., Kelemen, A., Simon, E., Miglécz, T., Lukács, B., et al. (2014). Environmental factors driving vegetation and seed bank diversity in alkali grasslands. Agriculture, Ecosystems and Environment, 182, 80–87. Vivian-Smith, G. (1997). Microtopographic heterogeneity and floristic diversity in experimental wetland communities. Journal of Ecology, 85, 71–82. Wacker, L., Baudois, O., Eichenberger-Glinz, S., & Schmid, B. (2008). Environmental heterogeneity increases complementarity in experimental grassland communities. Basic and Applied Ecology, 9, 467–474. Wellstein, C., Campetella, G., Spada, F., Chelli, S., Mucina, L., Canullo, R., et al. (2014). Context-dependent assembly rules and the role of dominating grasses in semi-natural abandoned sub-Mediterranean grasslands. Agriculture, Ecosystems and Environment, 182, 113–122. Wilson, J. B. (1992). Egler’s concept of ‘Initial floristic composition’ in succession – Ecologists citing it don’t agree what it means. Oikos, 64, 591–593.

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