Variation in species richness within and between calcareous (alvar) grassland stands: the role of core and satellite species

Plant Ecology 157: 203 211, 2001. 2001 Kluwer Academic Publishers. Printed in the Netherlands. 203 Variation in species richness within and between calcareous (alvar) grassland stands: the role of core and satellite species Meelis Pärtel*, Mari Moora and Martin Zobel Institute of Botany and Ecology, University of Tartu, 40 Lai St., 51005, Tartu, Estonia; *Author for correspondence (e-mail: pmeelis@ut.ee; fax: + 372 7 376222.) Received 30 November 1999; accepted in revised form 15 December 2000 Key words: Alpha diversity, Beta diversity, Phylogenetically independent contrasts, Spatial turnover, Species pool, Species traits Abstract Sixteen stands of dry alvar grassland in Estonia, representing the same vegetation type in similar ecological conditions, were investigated in order to study a considerable variation in species richness within and between stands. Alpha diversity and within stand beta diversity (spatial turnover of species) were negatively correlated. The distribution of species frequencies across the stands was clearly U-shaped, which made it possible to distinguish core species (occurring in more than 75% of stands) and satellite species (occurring in less than 25% of stands), including most of species from the total species pool. Species richness showed significant nestedness scarce species occurred more often in species-richer stands. Both mean alpha diversity and the size of the community species pool were significantly positively correlated with the number of core species found in a stand, while beta diversity was correlated with the number of satellite species. Species frequencies across the stands were negatively correlated with species average height, seed mass and requirement for soil fertility. These differences were also evident in comparison of core and satellite species by 14 Phylogenetically Independent Contrasts. Also, satellite species had a significantly higher variation in average height and seed size than core species. It was concluded that the community matrix is made up of core species, which are better suited to dry oligotrophic conditions. Beta diversity is largely caused by satellite species, the optimum conditions of which may be found in other neighbouring communities. Further studies have to show whether stands with higher richness and thus a higher number of satellite species are those which were or are surrounded by communities which may potentially act as sources of satellite species. Introduction Alvar grasslands calcareous grasslands on thin soils (less than 20 cm) with underlying Ordovician or Silurian limestones are characterised by a very high species diversity both on a small (Rosén 1982; van der Maarel and Titlyanova 1989; Peet et al. 1990) and on a community scale (Pärtel et al. 1996). However, if alvar grasslands are studied in more detail, one sees that species richness varies considerably even between stands of one, environmentally homogeneous community type (Pärtel and Zobel 1999). Since habitat conditions are uniform, differences in species richness may be connected with different rates of colonisation and extinction, which, in turn, may be caused by different fragmentation and isolation of stands, now or in the past. Alvar grasslands are like islands in the sea of woody vegetation, rural landscapes and wetlands. Dispersal between different local populations in a fragmented landscape, which depends on species dispersal ability and community isolation, may be a process critical for survival for smaller local populations (Ouborg 1993). Partly isolated and partly connected local patches may constitute one metacommunity (Harrison 1999). However, the results of Dzwonko and Loster (1989, 1992); Eriksson et al. (1995) and Harrison (1997, 1999) do not advance much support

204 for this explanation in the case of vascular plants. Also, Pärtel and Zobel (1999) found that the total number of species in alvar grassland stands (community species pool Zobel et al. (1998)) was not dependent either on the current area of a stand, or on the current degree of isolation or current management conditions. To detect the reasons of species richness variability between stands of same community type, we have to study the variability in species composition. Do both species-rich and -poor stands represent a random subset of the regional species pool, or is a larger community species pool always associated with the presence of certain species? The question can be answered both on a community and on a species level. On the plant community level, several studies report nestedness, i.e. rarer species tended to be confined to more species-rich communities (Silvertown and Wilson 1994; Kadmon 1995; Weiher et al. 1998; Honnay et al. 1999). The next logical step is to find which species are responsible for nestedness in species richness. Several studies have reported the U-shaped distribution of species between stands, i.e. there were a set of species which occurred in most sites where the community type was found, called core species, and a number of species which occurred only in a few sites, called satellite species (Hanski 1982a, 1982b; Collins and Glenn 1991; Glenn and Collins 1993; Sætersdal 1994; Eriksson et al. 1995). However, this pattern is certainly not universal (e.g. Gaston and Lawton (1989)). But if such a distribution occurs, the variation in species richness may be dependent, as claimed also by Grubb (1986), namely on the presence or absence of sparsely distributed species. A comparison of the traits of species with contrasting frequencies, like core and satellite species, would enhance the understanding of the mechanisms behind patterns of species richness. However, the initial optimism of finding plant traits to explain the low local abundances (Hodgson 1986a, 1986b) has been replaced by the understanding that it is extremely difficult to explain low local abundance by inferior vegetative, reproductive or ecological attributes (e.g. Sætersdal (1994); Eriksson et al. (1995); Thompson et al. (1996); Witkowski and Lamont (1997)), the studies of Rees (1995) and Kunin and Shmida (1997) being positive exceptions. The present study was addressed first at describing the spatial variation in species richness, both within stands (alpha diversity and beta diversity or spatial turnover) and between stands. Second, we were interested in how the variation in species richness was built up, i.e. whether the relatively scarce species were confined to the highest diversity observations (i.e., community nestedness) or not. Third, we were interested in how relatively common (core) and scarce (satellite) species contribute to within and between stand variation in species diversity. Finally, we addressed the question whether core and satellite species differ in traits and the variability of the traits. Both cross-species analyses, where species are considered as independent data points, and the Phylogenetically Independent Contrasts (PIC), where possible effect of common phylogeny is removed (Silvertown and Dodd 1996; Harvey 1996; Eriksson and Jakobsson 1998) can be used for comparisons (Ricklefs and Starck 1996). Methods Study area Estonia is located on the eastern coast of the Baltic Sea, in Northern Europe. The vegetation of Estonia belongs to the boreo-nemoral zone (Sjörs 1965). We focus on one particular vegetation type thin-soil calcareous grasslands (called alvar grasslands). The history of alvar grasslands in Europe is largely connected with human influence (animal grazing and the collecting of firewood, Rosén (1982)), although species belonging to these communities have been known in Europe throughout the whole post-glacial period (Bush and Flenley 1987). In Estonia, the alvar vegetation type is spread sparsely across the western coastal zone and the islands of the Baltic Sea (Pärtel et al. 1999). Description of vegetation Alvar vegetation in Estonia has been classified numerically (Pärtel et al. 1999). Here we include only the stands which belonged to the same cluster in the numerical analysis, to guarantee that only stands of one community type are compared. The cluster in question contained 16 stands, which were located on the islands of Saaremaa and Muhu and on the western part of mainland. Geographical distances between stands varied from 1 km to 100 km. The area of stands varied between 1 to 150 ha. The soil was rendzic leptosol, the recent management history of

205 stands was uniform grazing pressure had gradually decreased during the last 15 20 years; presently only scattered grazing by sheep and cattle occurs. Each stand was sampled using 15 randomly located 1 m 1 m plots in which all vascular plant species were recorded. We calculated small-scale alpha diversity (mean number of species per plot) and beta diversity (or spatial turnover, mean dissimilarity between plots, calculated as 1 Jaccard similarity index, see Harrison (1999)). Community species pool was determined as the spatially cumulative number of species over all sample plots within a stand. Nomenclature follows Eesti NSV Floora (1959 1984). Core and satellite species We shall use the terms core and satellite species, following many authors like Hanski (1982b) or Collins and Glenn (1991). However, many other terms: dominant, matrix or common species, and subordinate, fugitive, interstitial, redundant, scarce or rare species, have been used in quite a similar sense (reviewed by Olff and Bakker (1998)). We defined core species as those occurring in more than 75% of stands and satellite species as those occurring in up to 25% of stands. These limitations are always artificial, other authors have used different criteria to determine core and satellite species, e.g. 90% and 10% (Collins and Glenn 1997). Our limits allowed to include most species from the total species pool, keeping the core and satellite group still well separated. The limit 25% corresponds to the criteria of rare species used in several cases (Kunin and Gaston 1997). Monte Carlo modelling (according to Pärtel et al. (1996) and Pärtel and Zobel (1999)) was used to estimate the strength of the relationships between richnesses at different levels (i.e. number of core and satellite species, and alpha diversity). These variables are not independent since richness on a small scale can never be higher than richness on a large scale, and traditional statistics cannot be used. Different solutions to overcome this problem have been proposed (Cresswell et al. (1995); Richardson et al. (1995); Pärtel et al. (1996); Caley and Schluter (1997); see Austin (1999) for review). In other comparisons, Pearson correlation was used. Spatial analyses In order to estimate the effect of spatial aggregation for species diversity measures, we used a Mantel type of test (Legendre 1993). All pairwise combinations between the 16 stands were established (120 combinations). Correlation coefficient was calculated between geographical distance and difference in species diversity values. Significance was calculated by a randomisation process where the geographical distance of the 120 combinations was randomly ordered and then correlation calculated. This process was iterated a 1000 times. The P value is the proportion of iterations where the calculated correlation was more negative than the correlation from empirical data. To analyse the nestedness of species richness, we used the index N of Patterson and Atmar (1986). All stands were ordered according to the size of the community species pool, from high to low values. For each species, we found the most species-poor stand where it occurred, and then counted all cases where this species was absent in more species-rich stands. The nestedness index is the sum of those counts over all species. A perfectly nested pattern results in a value of N = 0, higher values show deviance from nestedness. To provide a significance test, we randomised the whole table, keeping the original species frequencies. From the randomised tables, stands were ordered by species richness again and N was calculated using the same algorithm. Randomisation was iterated a 1000 times and the empirical P value is the proportion of iterations, where randomised N is smaller than the N calculated from the empirical table. Comparison of species traits The following traits were used for comparisons: 1. Mean local abundance of species in particular sites, calculated as mean number of plots (from the 15) where the species was recorded. Sites where a particular species was completely missing were not considered. 2. Mean height from local flora (Eesti NSV Floora 1959 1984). 3. Seed mass, using original data. 100 seeds (including morphological structures which were difficult to separate from the seed) of each species were weighed and a mean weight calculated. In some cases, if it was not possible to obtain original data,

206 data from literature was used (Hodgson et al. 1995; Bakker et al. 1996). 4. Ability to spread clonally (by Klimeš et al. (1997), including two categories: growing vegetatively more or less than 10 cm per year). 5. The position of the centre of the realised niche along four relative gradients: light, soil moisture, ph and nutrient status, according to the so-called Ellenberg et al. (1991) species indicator values. 6. Size of species distribution area in Eurasia by Hultén and Fries (1986). In the cross-species analyses, where all species were considered as independent data-points, the frequency of species across the studied stands was used as a continuous variable and Pearson correlation was used as a descriptive statistic. In the PIC analyses we compared taxonomically related species pairs where one species was classified as core and another as satellite. As detailed phylogenetic information was not available, we followed the example of many authors (e.g. Eriksson and Jakobsson (1998)) and assumed that species from the same genus or same family are more closely related to each other than to a species from another genus or family. The pair was chosen randomly from one genus or family (we took alphabetically the first core and the first satellite species). The family level was used only when it was not possible to choose any species pairs from this family at the genus level. The Wilcoxon test for paired samples was used to examine differences between species traits in interval and nominal scales (Zar 1996). If some data was not available (e.g. for ecological requirements the species was marked as indifferent), we still conducted all tests with a reduced number of species or species pairs. We also tested whether the traits for core or satellite species, included in the PIC analyses, differ in their variability. As the parameters of core and satellite species may be correlated due to phylogenetical relations, we used a modified variance-ratio test that takes into account the effect of correlation (Zar 1996). Results Mean alpha diversity over the sites was 27.4 ± 2.1 species per 1 m 2 ; mean within stand beta diversity (spatial turnover) was 0.43 ± 0.05 species, and mean community species pool was 53.1 ± 2.8 species per Figure 1. Distribution of species over 16 alvar grassland stands. Species occurring in up to 25% of stands (1 to 4) are defined as satellite group and species occurring in more than 75% of sites (13 to 16) are defined as core group of species. stand. There was a significant negative correlation between alpha and beta diversities (r = 0.514, P = 0.042). The frequency of a species was defined as its occurrence across 16 alvar stands. In total 122 species were recorded. The distribution of species between frequency classes was clearly U-shaped. Consequently, one may distinguish rather large groups of core and satellite species (Figure 1), while the amount of intermediate species was relatively small. The number of core and satellite species in particular stands were not correlated with each other (r = 0.199, P = 0.460). Community species pool was not spatially aggregated (Mantel test, P = 0.218), i.e. communities with a high number of species were not located close to each other in space. Number of core and satellite species showed no aggregated spatial pattern (P = 0.998 and P = 0.985, respectively). Neither alpha diversity nor beta diversity were spatially aggregated (P = 0.925 and P = 0.909, respectively). There was a significant nestedness of species richness among alvar grassland stands (P = 0.018). Scarce species occurred most often in more species-rich stands, and if the scarce species were missing, this occurred more often in species-poor stands. Alpha diversity was significantly positively related with the number of core species found in the stand (Monte Carlo modelling, P = 0.011, Figure 2). There was no relationship between the alpha diversity and the number of satellite species (P = 0.905). Beta diversity was correlated with the number of satellite species found in the stand (r = 0.652, P =

207 Figure 2. Relationship between the number of core species found in a stand and mean alpha diversity within stand (Monte Carlo modelling, P = 0.011). the difference in seed weight was marginally nonsignificant (T = 24, Z = 1.79, P = 0.074). No differences were found in vegetative growth ability. According to Ellenberg indicator values, core species were shown to prefer lower soil fertility than satellite species (T = 10, Z = 2.2, P = 0.025, Figure 4). No other ecological indicator values were statistically different between core and satellite species pairs. No differences were found in the area of the geographical distribution of species. The modified variance ratio test indicated that satellite species had higher variability in average height (F = 4.3, t = 3.0, P = 0.018) and seed size (F = 27.6, t = 9.0, P < 0.001) than core species. Other traits did not differ in their variance. Discussion Figure 3. Relationship between the number of satellite species found in a stand and beta diversity (spatial turnover) within stands (r = 0.652, P = 0.006). 0.006, Figure 3) and not with the number of core species (r = 0.228, P = 0.397). Cross-species analyses found a positive relationship between frequency across stands and mean local abundance (r = 0.803, P = 0.002). Species frequencies were negatively related to average height of species (r = 0.360, P = 0.004) and seed mass (r = 0.256, P = 0.046). Requirement for soil fertility also showed a negative relationship with frequency (r = 0.258, P = 0.041), while other ecological requirements did not show significant correlations. No correlations were found between vegetative growth ability or distribution area and frequency. Species traits were also compared in the case of 14 PIC-s (Table 1). The Wilcoxon test confirmed that core species were also locally significantly more abundant that satellite species (T =0,Z = 3.2, P = 0.001, Figure 4). Core species had, on average, lower height than satellite species (T =3,Z = 3.1, P = 0.002, Figure 4). Also, core species had smaller seeds, but Species richness on a plot (alpha diversity) and community species pool, as well as spatial turnover (beta diversity), varied greatly between alvar grassland stands of the same community type by Pärtel et al. (1999). The most species-rich stand had 1.5 times more vascular plant species altogether than the poorest stand. There was a lack of spatial aggregation between species-rich stands. Working with the same stands, Pärtel and Zobel (1999) did not find any correlation between species richness and characteristics like the stand size or the isolation from other communities of the same type. However, spatial aggregation may result from to the influence of common land use history or the presence of neighbouring communities, acting as diaspore donors, on a larger scale. Alpha and beta diversities were negatively correlated, showing that in cases of high species richness the community is close to have almost all species from the community species pool in all plots (high completeness or relative richness by Zobel and Liira (1997)) and there is little variability in species composition. There was a significant nestedness among alvar grassland stands species-poor or species-rich stands were not random subsets of the regional species pool. This is showing that variation in species richness is governed by assembly rules (sensu Weiher and Keddy (1999)). Also, there was a clear U-shaped distribution of species between stands, and it was easy to distinguish two groups with contrasting distribution core species and satellite species.

208 Table 1. Species pairs of core and satellite species in alvar grasslands for Phylogenetically Independent Contrasts analysis. Pair Family Core species Satellite species 1 Apiaceae Pimpinella saxifraga L. Anthriscus sylvestris (L.) Hoffm. 2 Asteraceae Centaureja jacea L. C. scabiosa L. 3 Asteraceae Hieracium pilosella L. H. umbellatum L. 4 Asteraceae Leontodon hispidus L. L. autumnalis L. 5 Campanulaceae Campanula rotundifolia L. C. persicifolia L. 6 Cyperaceae Carex caryophyllea Latourr. C. panicea L. 7 Fabaceae Medicago lupulina L. Melilotus albus Medik. 8 Lamiaceae Prunella vulgaris L. Origanum vulgare L. 9 Plantaginaceae Plantago lanceolata L. P. maritima L. 10 Poaceae Avenula pratensis (L.) Besser A. pubescens (Huds.) Pilg. 11 Poaceae Festuca ovina L. F. pratensis Huds. 12 Polygalaceae Polygala amarella Crantz P. comosa Schkuhr 13 Rosaceae Filipendula vulgaris Moench Agrimonia eupatoria L. 14 Violaceae Viola rupestris F.W.Schmidt V. collina Besser Due to the nestedness of species richness, we expected that the number of satellite species would be the significant determinator of the size of the alpha diversity. However, the results were different from our expectations, since the number of core species, and not of satellite species, was correlated with the mean number of species in plots. At the same time, the number of satellite species was significantly correlated with beta diversity within stands, while the number of core species was not. Consequently, our results are in general accordance with those of Glenn and Collins (1990, 1993), who found that in prairie grassland communities, actual patch structure was defined by satellite species, while core species are responsible for the stable community matrix. There was a strong relationship between local abundance and overall frequency of species. The possible reasons for such a pattern, which seems to be quite universal (Lawton 1999), have been discussed e.g. by Brown (1984); Hanski and Gyllenberg (1993); Gaston (1996); Gaston et al. (1997); Kunin and Shmida (1997). In the context of the present study we suggest that the fit of species requirements to abiotic and biotic conditions in alvar grasslands is responsible for the pattern. Core species were lower, on average, than satellite species, and they also had a lower soil fertility indicator value. These traits indicate, though indirectly, that the main difference between core and satellite species is their adaptation to lowfertility conditions. Alvar communities have low productivity (100 300 g/m 2 /yr, (Pärtel et al. 1999)) due to unfavourable soil conditions. The role of light competition is evidently nonsignificant in such communities with a low and sparse canopy (Wilson and Tilman 1993), and the most efficient adaptations in such conditions are those directed at overcoming environmental stress (sensu Grime (1979)). That is probably the reason why plant height, which is correlated with a plants ability to compete for light (Keddy 1989), and has explained species success as invaders on a larger scale (Crawley et al. 1996), does not show correlation with abundance in oligo- and mesotrophic temperate grasslands (Eriksson et al. 1995; Eriksson and Jakobsson 1998). Seed mass was negatively related to species frequencies in cross-species analyse, the relationship became marginally nonsignificant in PIC analyses. Controversial results have been received about the relationship between seed size and species frequency (e.g. Rees (1995); Eriksson and Jakobsson (1998)). Generally, germination of small seeds is favoured in gaps, while large seeds are able to germinate in dense turf (Burke and Grime 1996; Thompson et al. 1996; Eriksson 1997). As alvar grasslands are characterised by low and sparse vegetation, we suggest that ability to regenerate in the shade, which is associated with large seed mass, does not give species advantages in regeneration. Instead, species with small seeds may be favoured, both because of the larger number of seeds and because of the ability to form persistent seed bank (Thompson et al. 1997). Satellite species were more variable in their average height and seed size. This is an indication that the satellite group is a relatively incidental set of species compared with the core species, which have more consistent morphological traits.

209 abundant somewhere else across their geographical range. Consequently, alvar grassland species may quite easily be divided into two broad groups. Core species, occurring in many stands with high local abundances, are short and adapted to low soil fertility. This group of species is responsible for variation in species richness between stands and number of those species in a stand is determining its mean alpha diversity. Satellite species, occurring in a few stands with low local abundance, are responsible for spatial heterogeneity within stands. The preliminary study of the list of satellite species indicates that many of them are quite common in other more productive calcareous grasslands (Krall et al. 1980). The working hypothesis that the alvar stands with high species richness are those which are presently, or were in the past, surrounded by mesophytic calcareous grasslands needs to be checked in further studies. Acknowledgements Figure 4. Comparison between traits of core and satellite species using Phylogenetically Independent Contrast method (Wilcoxon matched pairs test). Lines are connecting values of phylogenetically independent species pairs where one species belongs into the core and another into the satellite group. Overlapping lines are arranged around their location to make them visible. a. Mean local abundance per site (T =0,Z = 3.2, P = 0.001). b. Mean plant height (T =3,Z = 3.1 P = 0.002). c. Requirement for soil fertility (T = 10, Z = 2.2, P = 0.025). Evidently, satellite species are those whose optimum conditions are realised in other, typically more fertile, environments. Literally speaking, core species occur in the right place, i.e. in oligotrophic dry calcareous grasslands, while satellite species may be more successful somewhere else, e.g. in more productive mesophyte calcareous grasslands. Brown (1995) refers to the possibility that locally rare species may be common somewhere else. Also, Lennon et al. (1997) discuss the possibility that core and satellite categorisation may be applied to a single species in different parts of its range. This idea is supported by a comprehensive work of Murray et al. (1999) where it was found that scarce species of Australian sclerophyll woodlands and temperate rainforests were The work was supported by the Estonian Science Foundation (Grants 2382, 2391 and 3280). R. Kalamees assisted during the fieldwork. L. Klimeš kindly provided data about vegetative growth. References Austin M.P. 1999. The potential contribution of vegetation ecology to biodiversity research. Ecography 22: 465 484. Bakker J.P., Bakker E.S., Rosén E., Verweij G.L. and Bekker R.M. 1996. Soil seed bank composition along a gradient from dry alvar grassland to Juniperus shrubland. Journal of Vegetation Science 7: 165 176. Brown J.H. 1984. On the relationship between abundance and distribution of species. American Naturalist 124: 255 279. Brown J.H. 1995. Macroecology. University of Chicago Press, Chicago. Burke M.J.W. and Grime J.P. 1996. An experimental study of plant community invasibility. Ecology 77: 776 790. Bush M.B. and Flenley J.R. 1987. The age of the British chalk grassland. Nature 329: 434 436. Caley M.J. and Schluter D. 1997. The relationship between local and regional diversity. Ecology 78: 70 80. Collins S.L. and Glenn S.M. 1991. Importance of spatial and temporal dynamics in species regional abundance and distribution. Ecology 72: 654 664. Collins S. and Glenn S.M. 1997. Effects of organismal and distance scaling on analysis of species distribution and abundance. Ecological Applications 7: 543 551.

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