Rates of small-scale species mobility in alvar limestone grassland

Journal of Vegetation Science 8: 199-208, 1997 IAVS; Opulus Press Uppsala. Printed in Sweden - Rates of small-scale species mobility in alvar grassland - 199 Rates of small-scale species mobility in alvar limestone grassland van der Maarel, Eddy 1 & Sykes, Martin T. 2 1 Department of Ecological Botany, Uppsala University, Villavägen 14, S-752 36 Uppsala, Sweden; Fax +46 18 182860; E-mail eddy.van_der_maarel@vaxtbio.uu.se; 2 Global Systems Group, Department of Ecology, Lund University, S-223 62 Lund, Sweden; Fax +46 46 2223742; E-mail martin@planteco.lu.se Abstract. Small-scale species frequency and cumulative species frequency were studied in four plots in limestone grassland of the Veronica spicata-avenula pratensis association on Stora Alvaret on the Baltic island of Öland, Sweden. Species mobility was expressed as increase in cumulative species frequency in 20 subplots of 100 cm 2. Observed cumulative frequencies from 1985-1989 in all four plots, and from 1985-1995 in one plot were compared with values following from two null models, a minimal mobility model and a random mobility model. In ca. 50 % of the cases the observed cumulative frequency was not significantly different from the random expectation. However, in many such cases the mean annual frequency was either very high or very low. Three ways of calculating the mobility rate are presented though only one is used: (observed cumulative frequency lowest annual frequency) / expected cumulative frequency. Values 100 range from 0 to 100. There were slight differences between the four plots which were interpreted in terms of differences in grazing intensity and soil depth. It is stressed that the idea of the Carousel model has never been meant to suggest that all species would show random mobility, which we now quantify, but that species differ in their mobility rate and that the mean rate is much higher than generally realized. Keywords: Carousel model; Cumulative frequency; Cumulative richness; Drought; Öland; Species mobility type; Species turnover; Null model. Introduction Using data from a 6-yr, fine-scale analysis of a limestone grassland, van der Maarel & Sykes (1993) introduced the Carousel model, a phenomenological model to elucidate how a homogeneous, species-rich, lownutrient, drought-prone and grazed plant community, the Veronica spicata-avenula pratensis association, can exhibit both high species richness on the community level and high species turnover at smaller scales. Plant communities which seem to be stable and homogeneous at the scale of the minimal area (2-10 m 2 for short grassland) appear to be continuously mobile at small scales (10-1000 cm 2 ). Similar changes appeared to occur in other grassland types as well (Herben et al. 1993; Sykes et al. 1994). The research described in this paper had two starting points: (1) to test to what extent species mobility is random, and (2) to devise an index of mobility in order to quantify differences between plant communities as to their internal dynamics. We now examine more precisely some of the possible processes involved in this mobility. We use data from a long-term project in semi-natural limestone grassland on the island of Öland in the Baltic Sea. This grassland is speciesrich, particularly at fine scales, with up to 30 species/ 0.25 m 2 and more than 20 species/100 cm 2 (shoot presence). Soils are relatively thin and nutrient-poor, and severe droughts in the growing season occur quite often. This project, which forms part of an international comparative research project (Peet et al. 1990), included the monitoring of the species composition of subplots from 10 cm 2 to 0.25 m 2 situated in plots subjected to different types of fertilization Species mobility can be expressed in different ways, including: (1) mean year-to-year species turnover on permanent small subplots; (2) mean species accumulation over a number of years; (3) cumulative frequency of species in series of small subplots. All three approaches are based on the appearance ( immigration ) and disappearance ( extinction ) of genets or ramets of species. The cumulative species number is obtained by summing up all species found on each subplot since the start of the observations. For one block on the Gettlinge site described by van der Maarel & Sykes (1993), the cumulative species number on 0.01m 2 was estimated to approach 30 after 15yr, which is not far below the yearly mean species number found on 2.5m 2. In line with our earlier papers (van der Maarel & Sykes 1993; Sykes et al. 1994) we will follow the third approach in the present paper, i.e. we will measure this turn-around mobility using frequency accumulation through time, but will link results to the second approach - species richness. In this way we check the

200 van der Maarel, E. & Sykes, M.T. earlier postulate that most species in this community can eventually reach most microsites within that community. In terms of niche differentiation this implies that the constituent species have virtually the same habitat niche, while their regeneration niches are so small in space and so ephemeral in time that the niche concept has little practical significance. In the present study, species mobility rate is approached by comparing observed and expected cumulative frequencies. Let us make clear that, in this approach, it is irrelevant which microsites will be newly occupied. The spatial extension may be directional, i.e. from nuclei of colonization already present at the beginning of an observation period. Or, a species can move to new microsites in a random way, as is often the case with annuals. In this paper we will only consider the frequency accumulation resulting from spatial and temporal processes. We consider three possible models of frequency accumulation, all constrained by the observed frequencies: (1) random accumulation - after J. B. Wilson, in line with his null model for species richness variance (Wilson et al. 1987, 1995), (2) minimal accumulation, and (3) maximum accumulation. The random model idea is based on the random allocation of species occurrences to calculate random accumulations over time; note that this procedure involves the random appearance and disappearance of species. Such a situation may be approached in communities consisting largely of annuals, as in Mediterranean semi-desert. The minimum mobility model assumes that occurrences are always in subplots where the species was found earlier unless there is an increase in frequency and new subplots have to be included. The maximum mobility model locates species always into new subplots until all available subplots are occupied. We will compare our field data with the model results and propose an index to measure the mobility rate. Material and Methods Sites and data sets The main site is situated on Gettlinge alvar, described in a previous paper (van der Maarel & Sykes 1993); it is one of three sites chosen on Stora Alvaret (the Great Alvar), the landscape on the vast limestone plateau in the southern part of the Baltic Island of Öland. On this plateau, at 30 m a.s.l., grassland assigned to the Veronica spicata - Avenula pratensis association (class Festuco-Brometea) occurs on 10-50 cm deep, slightly acid to neutral brown soils developed in reworked glaciofluvial deposits on Ordovician limestone (Krahulec et al. 1986). Mean annual precipitation is 430 mm; during the growing period - May to September - the grassland is often subjected to low water availability and roughly every 5-7 yr (most recently in 1992) the area undergoes severe drought (Rosén 1982, 1995). Most of the alvar grassland has been grazed for hundreds, perhaps thousands of years. The Gettlinge site (56 23' N, 16 27' E), is a small, slightly raised area with slightly acid nutrient-poor loamy soil, 15-30 cm deep; it is at present lightly grazed by cattle and some horses; the vegetation is dense and short, ca. 5-10 cm tall. Site 2 is a ridge at Kleva alvar (56 32' N, 16 30' E) where there has been no grazing since 1980. Site 3 is at Skarpa Alby (56 35' N, 16 39' E) on shallow soil (8-15 cm) and subject to light cattlegrazing. The plant community composition on these sites shows certain differences related to soil depth and grazing intensity, but is on the whole very uniform (van der Maarel et al. 1995). Two sets of data were used: (1) Species occurrences from 1985 to1989 in 20 sub plots of 100 cm 2 situated in the control plots of two of the three blocks at Gettlinge (GA1, GB1), one of the two blocks at Kleva (KA1) and the block at Skarpa Alby (SA1). (2) Species occurrences from 1985 to 1995 in 20 subplots of 100 cm 2 situated in the control plot (GA1) of one of the three blocks at Gettlinge. Observed and expected cumulative frequency For each plot the frequency of each species was determined for each year separately and as cumulative frequency over the years involved. The observed cumulative frequencies were compared with cumulative frequencies predicted by three different models, the random, low and high mobility models (Fig. 1). 1. Random mobility is approached by year-to-year random allocation of species over subplots taking their frequencies into account. This is done by applying a Monte Carlo simulation with 2000 randomizations. The number of new species is determined for each round and for each subplot and then averaged over the subplots. In this way expected accumulations for subsequent years were obtained. With mean frequencies from ca. 50 %, a random accumulation up to 100 % can be reached within four years. We calculated the number of times the expected cumulative species number was higher, lower or the same as the observed value and used the values to calculate significance with a two-tailed test. 2. In the minimum mobility model species are allocated each following year to the same subplots where they occurred earlier, unless the frequency increased and new subplots are needed. Hence, the lowest possible accumulated frequency is equal to the highest frequency found in any one year.

- Rates of small-scale species mobility in alvar grassland - 201 Random Yr 1 f = 6 1--1-1-1-----1--1--- cf = 6 Yr 2 f = 8 12-1------2--1--1-22 cf = 10 Yr 3 f = 7 ++-1-+3+-3+3-+-3+3+2 cf = 15 Minimum Yr 1 f = 6 1--1-1-1-----1--1--- cf = 6 Yr 2 f = 8 1--1-1-1-----12-1--2 cf = 8 Yr 3 f = 7 1--1-+-1-----12-+2-+ cf = 9 Maximum Yr 1 f = 6 1--1-1-1-----1--1--- cf = 6 Yr 2 f = 8 +22+2+-+--2-2+--+222 cf = 14 Yr 3 f = 7 +++++13+33+3++33++++ cf = 20 Fig. 1. Three alternatives for modelling the mobility of species, using the occurrences of a species in 6, 8, and 9 out of 20 plots in years 1, 2 and 3, with a. Random mobility, i.e. species are allocated randomly each year; b. Minimum mobility: species are allocated each following year to the same plots unless the frequency would increase; c. Maximum mobility, i.e. species are allocated each following year to unused plots, until in year 3 all 20 plots are used. 1 = occurring for the first time in year 1; 2 = occurring for the first time in year 2; 3 = occurring for the first time in year 3; + = earlier occurrence. 3. According to the maximum mobility model, species are allocated each following year to subplots not occupied before, until all subplots are used. Maximum mobility was usually higher than random mobility, and after 4 yr the level of 100% is reached for all species with a mean frequency of at least 25%. In order to keep the comparisons relatively easy, maximum mobility will not be considered any further. Table 1 elucidates the procedure for determining accumulated frequencies of Achillea millefolium in plot Gettlinge A, with a mean frequency of 65 % and a cumulative frequency increasing from 55 % in 1985 to a total accumulated frequency of 95 %, which was reached in 1989. The highest annual frequency was 90%, found in 1989 and the lowest value was 45 % in 1992. Using the random mobility model, the expected accumulation for 1986 is 26.9 % - against an observed accumulation of 20%. The expected accumulation decreases gradually to 0%. The differences between observed and expected accumulations are small and non-significant. Mobility rate Measures of the mobility rate MR of a species should be based on the difference between the observed cumulative frequency and an initial frequency. This can be the frequency in the starting year or the mean frequency over the years of observation. Such a difference should then be scaled to a maximum value obtained over the period of observation. The first index one could consider is: MR = (cf obs f 1 ) / (cf R f 1 ) (1) where cf obs is the observed cumulative frequency, i.e. the cumulative number of subplots in which the species was found over time, as a percentage of the total number of subplots (20 in our case); cf R is the expected cumulative frequency according to the random model; f 1 is the frequency in the first year included in the calculation. This index gives unrealistic results for species with a fluctuating annual frequency because these are strongly dependent on frequency in the first year. An alternative index suggested follows from MR = (cf obs cf L ) / (cf R cf L ) (2) where cf L is the lowest possible cumulative frequency, which is equal to the highest annual frequency observed. Table 1. An example of how frequency (%) can accumulate: Achillea millefolium in 20 100-cm 2 subplots in plot Gettlinge A1, 1985-1995. Expected values are based on 2000 randomizations. Year 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 Obs. frequency 55.0 60.0 60.0 60.0 90.0 60.0 70.0 45.0 75.0 75.0 55.0 Obs. accumulation 20.0 10.0 0.0 10.0 0.0 0.0 0.0 0.0 0.0 0.0 Obs. cumulative frequency 75.0 85.0 85.0 95.0 95.0 95.0 95.0 95.0 95.0 95.0 Exp. accumulation 26.9 10.8 4.4 2.6 0.2 0.1 0.0 0.0 0.0 0.0 Exp. cumulative frequency 55.0 81.9 92.7 97.1 99.7 99.9 100.0 100.0 100.0 100.0 100.0 In 1985 the species was found in 11 of the 20 100-cm 2 subplots, f = 55 %. In 1986, though the species frequency just increased from 55 to 60 %, four new subplots (20 %) had been occupied, implying that three previously occupied plots were now empty. The frequency varied from 90 % in 1989 to only 45 % in 1992. The total accumulated frequency is 95 %, which was reached in 1989, the year with the highest annual frequency. By that year only one subplot had not yet been reached by Achillea, and in 1995 this situation had not been changed.using the random mobility model with the yearly frequencies being the same as the observed values, and calculating averages of 2000 randomizations, the initial expected accumulation is equal to the frequency in 1985 and then drops gradually to 0 %, as soon as the maximum expected cumulative frequency = 100 % is reached, which happened in 1991.

202 van der Maarel, E. & Sykes, M.T. This ratio does not take into account that any increase in annual frequency is also a form oobility. Moreover, in many cases the lowest possible cumulative frequency cf L is as high as the observed cumulative frequency cf obs and hence the index has the value 0. In the third index cf obs is compared with in, the lowest annual frequency over the period included. The denominator to scale to is cf R. This gives: MR = (cf obs in ) / cf R (3) This third index is simple and appeared to give values with a wide range; thus it was chosen for further use. Results and Discussion Observed and expected frequency accumulation Table2 (below; next to Tables 4 and 5) presents the values for the observed and expected cumulative frequencies over 4 yr for 53 species found in any of the plots Gettlinge A (GA1), Gettlinge B (GB1), Kleva (KA1) and Skarpa Alby (SA1). Many species have a cumulative frequency which is much higher than the mean frequency; the most extreme cases are the winter annual Trifolium campestre in GA1: 60% against 19 %, the summer annual Euphrasia stricta in SA1: 65 % against 24 %, and the perennial Ranunculus bulbosus in GB1: 60 % against 22 %. On the other hand there are relatively immobile species for example the endemic species Helianthemum oelandicum (a character species of the Helianthemum oelandicum-galium oelandicum association of shallow, moist soils), which is often found in the immediate surroundings of the Avenetum (Krahulec et al. 1986). This species (not occurring in the no longer grazed plot Kleva) has a cumulative frequency far below the random expectation. A similar local behaviour is shown by Veronica spicata, but in contrast to H. oelandicum, V. spicata is a character species of the Avenetum association, the association we are studying here. In the 142 cases of species occurrence in Table 2, 50% of the o bserved cumulative frequencies are not significantly different from random expectation. However, most such cases concern species with either a very high mean frequency or a very low one (Table 2). Species such as Festuca ovina are constant species with an value of over 80% where cf obs and cf R are close to each other and close to 100 %. Their mobility cannot be estimated properly because we cannot check whether the continued occurrence in a quadrat is the result of perennation or of rapid disappearance and reappearance. On the other hand, the movements oany lowfrequent incidental (van der Maarel 1996) species which are not significantly different from random, such as the winter annuals Arenaria serpyllifolia and Veronica arvensis and the drought-sensitive perennial grass Danthonia decumbens, are ecologically less important because the species are too infrequent - and absent altogether in many years - and moreover show a broad phytosociological amplitude (Krahulec et al. 1986). Most species with intermediate mean frequencies have cumulative frequencies significantly below random expectation (Table 3). Still, they move around and make up most of the category circulating species (van der Maarel 1996). Most of the few medium-frequent species with a random movement are winter annuals, e.g. Cerastium semidecandrum and Trifolium campestre, or perennials which do not develop above-ground organs in certain years, e.g. Ranunculus bulbosus. Mobility rate The figures for the mobility rates are presented in Table 4. They vary considerably. In three cases, including the long-lived perennial Asperula tinctoria in GA1, MR was 0; this concerns low-frequent species which did not change position. In several cases MR was 100, for instance the winter annual Trifolium arvense in GA1. Most such cases are again found in low-frequent species, but one of them, Festuca ovina in GB1, is a highly frequent species. It is difficult to interpret the low MRvalues of highly constant species (see above) but it is reasonable to conclude that a species, once in a state of constancy, has low mobility. It would be useful to characterize the stand as a whole regarding species mobility, but in view of the occurrence of highly infrequent and highly frequent species the arithmetic (or geometric) mean may give unrealistic values. Instead the median value is used (Table 4). The variation in MR is easy to connect with the (non-)significance of the deviation between observed and expected accumulated frequency. Low values of MR (i.e. lower than the median) are associated with the significance of (cf R cf obs ) and high values of MR with non-significance (χ 2 test; p < 0.001). As Fig. 2 shows, MR values vary maximally in the mean-frequency interval 0-20% and gradually decrease for higher meanfrequency values. Species with a frequency accumulation not significantly different from random have MR values of at least 0.40, reached by species with higher mean frequencies, and higher values, up to 1.0 with lower mean frequencies. Species with a cumulative frequency significantly lower than random show a unimodal trend with MR values up to 0.70 in the middle mean species frequency range.

- Rates of small-scale species mobility in alvar grassland - 203 Comparison between the four plots Not only is the floristic composition of the four plots very much the same (van der Maarel & Sykes 1993; van der Maarel et al. 1995), but also the frequency and mobility patterns are similar. The number of species per plot is almost the same, as is the number of significant deviations from random cumulative frequency. However, the no longer grazed plot at Kleva, which has a coarser structure and a lower small-scale richness (Sykes et al. 1994), has a lower number of species in the medium frequency categories whose mobility is not significantly different from random, but also a lower number of such species anyway. Its median mobility rate is somewhat higher than in the grazed Gettlinge plots. The grazed vegetation on the shallow soil of Skarpa Alby, which is probably better drought-adapted, is a little less mobile than the vegetation on the deeper soil of Gettlinge. Most of the species occurring in three of four plots show a similar mobility pattern in these plots. If there are differences, they are related to the mean frequency. Achillea millefolium, for example, has a lower frequency in the no longer grazed plot (for unclear reasons) and is also less mobile there. Plant species mobility over a 10-yr period We also calculated values for the observed and expected cumulative frequencies over 10 yr for 38 species in plot GA1 (Table 5). One species, Polygala amarella, has entered one of the 20 subplots so that the total number of species increased from 37 to 38. The mean frequencies of several species changed since 1989, for instance Thymus serpyllum went down from 79 to 60 %, Trifolium repens increased from 15 to 33 %. The significance patterns oany species did not change much, but almost all MR values increased, some of them very much indeed, for instance Agrostis vinealis from 5 to 60%. This is the effect of a strong decrease in frequency in 1993. Some others, e.g. Anthoxanthum odoratum, which did not change in mean frequency, occupied relatively many new subplots and thus increased in mobility rate. Triggers of plant species mobility Many of these changes are related to the very dry summer of 1989 when many species died back fully or partly and did not recover completely, while others profited from the gaps left by the plants which died back that summer. After a return to a normal situation in June 1991 the summer of that year as well as the early summer of 1992 were again very dry as a result of which many species decreased strongly in frequency in 1992 and/or 1993 (van der Maarel 1996). More generally, changes in the small-scale occurrence of species can be related to year-to-year fluctuations in both high summer and early summer precipitation. In this respect the example presented in Fig. 1 is elucidating. The highest annual frequency of Achillea millefolium, 90 %, was found in 1989, which may be related to the very wet period July-August in the year before (for rainfall data, see van der Maarel 1996). The summer of 1989 was very dry, but the real drought started after we had finished the recordings. The lowest value found was only 45%; this was in June 1992, while the rainfall in the period May-June was extremely low, and moreover the period July-August 1991 had been extremely dry as well. Apparently the perennial A. millefolium produces above-ground shoots in spring in relation to the amount of soil moisture available then. By 1991 only one subplot had not yet been reached by Achillea. This situation had not changed up to 1995, but in June 1996 Achillea appeared to have a high frequency again (80 %), after the summer of 1995 had been wet and May 1996 had been extremely wet, and the only subplot which had remained empty so far was now occupied. Similar responses of species have been found to temperature conditions, both high and low temperatures, particularly in the previous year (Dai Xiaobing in prep.). Further disturbances such as activities of ants, earthworms and other small animals create small gaps. Gaps of a larger scale, ca. 20-50 cm, are created by patches of cow and horse dung. As we remarked in the beginning (van der Maarel & Sykes 1993), small-scale mobility of this kind may have the dieback of individuals as a trigger. However, in many cases we are dealing with the dieback of only parts of plants, notably relatively large leaves with a horizontal or oblique position. Many plant individuals may not develop above-ground parts in certain years. Anders Nilsson (pers. comm.), studying long-term dynamics of an Orchis morio population on the Great Alvar found that below-surface insect herbivory on Table 3. Data on the frequency distribution of average species frequency values and on the significance of differences between expected and observed cumulative frequencies; t = total; ns = number of non-significant cases. GA1 GA2 KA1 SA1 Total t ns t ns t ns t ns t ns % 80% 5 5 6 6 5 3 4 4 20 18 90 60-79 % 6 3 5 2 3 1 6 2 20 8 40 40-59 % 5 1 3 0 6 1 3 1 17 3 18 20-39 % 3 0 6 2 3 0 6 1 18 3 17 10-19 % 7 5 6 0 3 0 7 1 23 6 19 9 % 11 4 10 7 15 13 10 4 46 28 61 Total 37 18 36 17 35 18 36 13 144 66 46 Total 10-79 % 26 8 26 5 16 3 27 5 91 21 23

204 van der Maarel, E. & Sykes, M.T. Table 2. Cumulative frequencies (%) in 20 100-cm 2 subplots in plots Gettlinge A1, A2, Kleva and Skarpe Alby 1985-1989. = mean frequency; cf obs = observed cumulative frequency; cf L = expected cumulative frequency according to the minimum mobility model (with cf L = ax ) cf R = expected cumulative frequency following from 2000 randomizations; significance (* = p < 0.05; ** = p < 0.01; *** = p < 0.001) of the difference between cumulative observed and expected frequency (two-tailed test) after 2000 randomizations. lt = longevity type: a = annual; sp = short-lived perennial; p = long-lived perennial. Gettlinge A Gettlinge B Kleva Skarpa Alby Frequency lt cf obs cf L cf R cf obs cf L cf R cf obs cf L cf R cf obs cf L cf R Achillea millefolium p 65 95 90 99.7 86 100 95 100.0 28 55 45 82.7 *** 54 90 60 97.9 Agrostis capillaris p 0 44 70 65 95.6 0 04 15 10 18.8 A. vinealis p 99 100 100 100.0 93 100 100 100.0 72 100 90 99.9 95 100 95 100.0 Antennaria dioica p 17 25 25 61.3 *** 34 45 10 86.0 *** 0 09 15 15 37.8 *** Anthoxanthum odoratum sp 21 35 30 69.5 *** 04 10 10 18.7 * 57 95 90 99.6 15 40 20 55.9 * Anthyllis vulneraria sp 63 85 80 99.5 *** 62 100 85 99.7 0 22 50 35 72.4 ** Arabis hirsuta sp 0 0 02 10 10 10.0 11 15 15 44.0 *** Arenaria serpyllifolia a 03 15 10 14.5 03 15 15 15.0 01 05 05 05.0 02 10 10 10.0 Artemisia campestris p 0 0 01 05 05 22.6 *** 0 Asperula tinctoria p 10 10 10 40.9 *** 0 44 60 60 94.3 *** 60 75 70 99.1 *** Avenula pratensis p 88 100 100 100.0 89 100 100 100.0 94 100 100 100.0 69 95 80 99.8 A. pubescens p 0 0 01 05 05 05.0 0 Briza media sp 12 25 20 48.0 *** 16 25 20 58.3 *** 03 10 10 14.6 19 50 30 65.8 * Bromus hordeaceus a 10 25 25 42.2 *** 10 15 15 41.3 *** 02 10 10 10.0 0 Campanula rotundifolia p 0 0 16 25 20 58.6 *** 0 Carex caryophyllea 1 p 59 80 70 99.9 *** 67 90 90 99.8 *** 62 85 80 99.5 *** 71 90 85 99.9 *** Cerastium semidecandrum a 58 100 80 99.5 19 55 20 69.3 * 08 40 15 34.3 14 45 35 55.4 Cirsium acaule p 0 0 01 05 05 5.0 0 Danthonia decumbens p 01 05 05 5.0 0 04 20 10 19.0 0 Euphrasia stricta a 15 55 30 57.4 01 05 05 05.0 0 24 65 40 76.1 Festuca ovina p 98 100 100 100.0 100 100 100 100.0 99 100 100 100.0 98 100 100 100.0 Filipendula vulgaris p 96 100 100 100.0 84 100 100 100.0 65 90 85 99.6 ** 90 100 95 100.0 Galium verum p 62 80 70 99.3 *** 48 65 55 96.3 *** 89 95 95 100.0 *** 89 100 90 100.0 Globularia vulgaris p 0 0 0 05 05 05 22.6 *** Helianthemum nummularium p 65 85 85 99.6 *** 82 100 100 100.0 83 100 100 100.0 70 85 80 99.8 *** H. oelandicum p 05 05 05 22.7 *** 12 25 15 47.2 *** 0 11 20 15 44.4 *** Hieracium pilosella p 0 0 0 21 30 25 69.8 *** Linum catharticum sp 82 100 100 100.0 60 90 85 99.6 ** 10 25 20 42.4 *** 30 70 65 87.2 ** Lotus corniculatus p 38 75 55 91.4 ** 45 60 55 95.4 *** 01 05 05 5.0 06 30 20 44.8 * Luzula campestris p 41 70 45 91.9 *** 21 40 40 70.7 *** 16 35 25 58.6 *** 57 70 65 98.7 *** Oxytropis campestris p 0 0 36 55 25 89.3 *** 06 10 10 26.7 *** Phleum phleoides p 0 0 45 65 60 95.8 *** 09 25 15 38.0 * Plantago lanceolata p 48 80 80 98.0 77 90 80 99.9 *** 80 90 90 100.0 *** 75 100 85 99.9 Poa compressa p 0 03 15 15 15.0 0 0 Polygala amarella p 01 05 05 05.0 0 0 0 P. comosa p 0 08 15 15 34.6 *** 0 02 05 05 9.8 P. vulgaris p 03 10 10 14.5 06 15 15 27.3 ** 0 0 Potentilla tabernaemontani p 75 100 90 99.9 33 75 45 87.2 43 75 55 94.7 *** 61 80 65 99.1 *** Prunella grandiflora p 0 0 0 11 20 15 44.3 *** Pulsatilla pratensis p 47 85 65 96.6 * 01 05 05 05 0 51 70 60 97.3 *** Ranunculus bulbosus p 16 35 20 58.3 *** 22 60 45 73.8 01 05 05 05.0 05 20 15 23.4 Sedum acre p 07 15 15 30.7 *** 10 15 15 41.3 *** 05 05 05 22.7 *** 0 S. reflexum p 0 0 0 18 30 25 63.2 *** Stellaria graminea a 0 0 02 10 05 9.7 0 Taraxacum spec. p 04 05 05 18.5 *** 10 25 20 41.5 ** 26 45 35 78.4 *** 22 45 35 72.7 *** Thymus serpyllum p 79 100 100 100.0 79 100 100 100.0 59 80 70 98.9 *** 31 50 35 84.5 *** Trifolium arvense a 06 30 10 27.1 0 0 0 T. campestre 2 a 19 60 35 67.8 04 15 10 19.1 03 15 15 15.0 0 T. pratense p 0 01 05 05 05.0 0 0 T. repens p 33 75 60 88.8 * 36 65 60 92.0 *** 0 0 T. striatum a 07 25 20 31.9 0 0 0 Veronica arvensis a 01 05 05 05.0 08 30 20 35.0 04 20 10 18.8 0 V. spicata p 13 15 15 50.2 *** 24 35 35 75.5 *** 58 75 70 98.9 *** 07 15 10 30.5 *** Mean frequency 1985 (%) 39 42 37 37 Mean 1985-1989 (%) 37 36 32 35 Mean cf obs (%) 54 52 46 52 Nr. spec. 1985-1989 37 36 35 36 Nr. spec. with f 80 % 1985 4 3 3 4 Nr. spec. with cf 80 % 15 11 10 10 1 combined with Carex ericetorum; 2 combined with Trifolium dubium.

- Rates of small-scale species mobility in alvar grassland - 205 Table 4. Values for the Mobility Ratio MR (%) for species occurring in 20 100-cm 2 subplots in Gettlinge A1, Gettlinge A2, Kleva and Skarpa Alby. MR - = species absent from this plot. = increasing annual frequency; = decreasing annual frequency. Cases with 10%and < 80% and cf obs not significantly differing from cf R indicated in bold. GA1 GB1 KA1 SA1 in MR in MR in MR in MR Achillea millefolium 55 40 80 20 10 54 50 41 Agrostis capillaris 0-20 52 0-0 80 A. vinealis 95 5 75 25 50 50 95 05 Antennaria dioica 10 25 25 23 0-05 26 Anthoxanthum odoratum 21 27 0 53 0 95 5 26 Anthyllis vulneraria 45 49 20 80 0-5 62 Arabis hirsuta 0-0 - 0 100 10 11 Arenaria serpyllifolia 0 100 0 100 0 100 0 100 Artemisia campestris 0-0 - 0 22 0 - Asperula tinctoria 10 0 0-30 32 50 25 Avenula pratensis 75 25 85 15 80 20 55 40 Avenula pubescens 0-0 - 0 100 0 - Briza media 5 42 10 26 0 68 10 61 Bromus hordeaceus 0 59 10 16 0 100 0 - Campanula rotundifolia 0-0 - 5 26 0 - Carex caryophyllea 50 30 40 50 40 45 40 50 Cerastium semidecandrum 25 75 5 72 0 100 0 81 Cirsium acaule 0-0 - 0 100 0 - Danthonia decumbens 0 100 0-0 100 0 - Euphrasia stricta 0 96 0 100 0-5 79 Festuca ovina 95 05 100 0 95 5 95 05 Filipendula vulgaris 95 05 70 30 55 35 80 20 Galium verum 50 30 40 26 75 20 85 15 Globularia vulgaris 0-0 - 0-05 0 Helianthemum nummularium 55 30 70 30 65 35 55 30 H. oelandicum 5 0 10 32 0-5 34 Hieracium pilosella 0-0 - 0-10 29 Linum catharticum 45 55 10 80 0 59 05 75 Lotus corniculatus 30 49 35 26 0 100 0 67 Luzula campestris 25 49 10 42 0 60 35 35 Oxytropis campestris 0-0 - 39 28 05 19 Phleum phleoides 0-0 - 25 42 0 66 Plantago lanceolata 25 46 70 29 65 25 60 40 Poa compressa 0-0 100 0-0 - Polygala amarella 0 100 0-0 - 0 - P. comosa 0-0 43 0-0 49 P. vulgaris 0 69 0 55 0-0 - Potentilla tabernaemontani 60 40 20 57 30 48 55 25 Prunella grandiflora 0-0 - 0-10 23 Pulsatilla pratensis 25 62 0 100 0-45 26 Ranunculus bulbosus 15 34 0 87 0 100 0 85 Sedum acre 05 33 05 24 05 0 0 - S. reflexum 0-0 - 0-18 25 Stellaria graminea 0-0 - 0 100 0 - Taraxacum spec. 0 27 05 48 15 38 0 68 Thymus serpyllum 60 40 60 40 55 25 25 30 Trifolium arvense 0 100 0-0 - 0 - T. campestre 0 88 0 79 0 100 0 - T. pratense 0-0 100 0-0 - T. repens 15 68 0 71 0-0 - T. striatum 0 78 0-0 - 0 - Veronica arvensis 0 100 0 86 0 100 0 - V. spicata 10 10 20 20 45 30 0 49 Total no. of species 37-34 - 35-36 No. of species with fm 10 % 27 23 21 27 Median values of MR 42.0 42.5 48.0 34.5 shoots prevented certain individuals from developing an above-ground stem. The significant point is that in all these cases other plant species may, temporarily or Table 5. Cumulative frequeny (%) of 38 species in 20 100- cm 2 subplots in plot Gettlinge A1 1985-1995. = mean frequency; f l = lowest frequency in any year; cf L = lowest possible cumulative frequency); cf obs = observed cumulative frequency; cf R = mean cumulative frequency following from 2000 randomizations. Significance of the difference cumulative observed and expected (two-tailed test) after 2000 randomizations: *** = p < 0.001; ** = p < 0.05; p < 0.01 = **; * = p < 0.05. Mobility types (mt) according to van der Maarel (1996): co = constant; lo = local, ci = circulating; pu = pulsating; oc = occasional; MR values in %. Species arranged according to mobility type and MR value. Frequency mt f l cf L cf obs cf R MR Asperula tinctoria lo 8 0 10 10 59.2 *** 17 Helianthemum oelandicum lo 6 5 10 15 49.1 *** 20 Veronica spicata lo 16 10 30 35 85.5 *** 29 Sedum acre lo 4 0 15 15 40.6 *** 37 Antennaria dioica lo 13 0 25 30 78.5 *** 38 Festuca ovina co 88 75 100 100 100.0 25 Filipendula vulgaris co 84 65 100 100 100.0 35 Avenula pratensis co 80 65 100 100 100.0 35 Agrostis vinealis co 82 40 100 100 100.0 60 Achillea millefolium ci 64 45 90 95 100.0 *** 50 Carex caryophyllea ci 53 40 70 90 100.0 *** 50 Helianthemum nummularium ci 51 30 85 95 99.9 ** 55 Potentilla tabernaemontani ci 65 40 90 100 100.0 60 Galium verum ci 61 25 70 90 100.0 *** 65 Plantago lanceolata ci 40 20 80 90 99.8 *** 70 Pulsatilla pratensis ci 44 25 65 95 99.9 70 Luzula campestris ci 25 5 45 85 97.0 * 82 Lotus corniculatus ci 22 0 55 80 95.0 * 84 Thymus serpyllum ci 60 40 95 100 100 60 Trifolium striatum pu 17 0 55 65 91.8 *** 71 T. repens pu 15 0 60 75 89.2 * 84 Anthyllis vulneraria pu 46 10 80 95 100.0 ** 85 Euphrasia stricta pu 18 0 30 75 85.5 88 Trifolium campestre pu 25 0 60 90 97.5 93 Cerastium semidecandrum pu 42 5 80 100 99.9 95 Linum catharticum pu 48 0 100 100 100.9 100 Bromus hordeaceus oc 10 0 25 35 71.2 *** 49 Ranunculus bulbosus oc 14 5 25 45 82.5 *** 49 Briza media oc 8 0 20 30 60.3 *** 50 Taraxacum spec. oc 05 0 15 25 43.7 57 Anthoxanthum odoratum oc 17 0 45 65 89.3 *** 73 Polygala vulgaris oc 2 0 10 15 18.8 79 Arenaria serpyllifolia oc 6 0 25 45 51.3 88 Trifolium arvense oc 7 0 20 55 57.4 96 Agrostis capillaris oc 2 0 5 20 19.3 100 Danthonia decumbens oc 4 0 20 35 35.4 100 Polygala amarella oc 1 0 5 5 5.0 100 Veronica arvensis oc 2 0 15 20 19.3 100 Mean (MR: median) 14 38 80 61 71.1 67.5 more permanently, take part of the space becoming available. If large plants, or large leaves, for instance a rosette of Plantago lanceolata, disappear (or do not reappear), the space can be occupied by several seedlings or small shoots from nearby species. In this connection it is important to remember the variation in plant unit size (van der Maarel et al. 1995).

206 van der Maarel, E. & Sykes, M.T. 120 100 80 MR (%) 60 40 20 0 0 20 40 60 80 100 Mean frequency (%) Fig. 2. Mobility rate in relation to mean frequency for 37 species in plot GA1. = constant species; = species with random cumulative frequency not significantly different from random; = species with cumulative frequency significantly lower than random; and = annuals and shortlived perennials. Species mobility and mobility types Following up the typology of species mobility types presented by van der Maarel (1996) we allocated the species on plot GA1 to five groups of species (all examples mentioned being character species of the Veronica spicata-avenula pratensis association). In Table 5 the species are arranged according to their mobility type, while the types are ordered according to the range in mobility range. 1. Local species (5), e.g. Asperula tinctoria, with a low mean frequency and a low cumulative frequency, which is near to the lowest possible value. MR-values over the period 1985-1995 are less than 0.40. 2. Constant species (4). These are species with a high mean frequency, > 75 % such as Avenula pratensis, which easily reach a cumulative frequency of 100%, which is also the expected cumulative frequency under the random model. They are long-lived hemicryptophytes. Their mobility rate is low, usually below 0.40, but may rise after a catastrophic year (example Agrostis vinealis). 3. Circulating species (10), with a medium high mean frequency (ca. 20-75%) which reach a high cumulative frequency (90-100 %). Three of them reach a cumulative frequency which does not differ significantly from the random expectation, e.g. Pulsatilla pratensis. The others, though significantly less mobile than random, still have a high mobility ratio, most of them > 0.40. 4. Pulsating species (7), with a medium high mean frequency (usually < 50%) but with a low frequency in at least one year, and with a high cumulative frequency. Several winter annuals, e.g. Trifolium striatum belong to this group. MR-values are all higher than in the above categories. 5. Occasional species (12), with a low mean frequency, < 25 %. There are two subgroups, one with low MR-values and approaching the category local, and one with high random mobility, e.g. Polygala amarella. As a further indication of the high overall mobility, of the 38 species included in Table 4 no less than 20, including Lotus corniculatus, are absent in at least one year (f L = 0) and another six have a lowest frequency in any one year of 10 %. Cumulative species frequency and cumulative species richness The figures obtained on accumulated species frequency can easily be translated into species richness data so that we can investigate the development of cumulative richness under two null models. In this way

- Rates of small-scale species mobility in alvar grassland - 207 Species number 30 20 10 1985 1987 1989 1991 1993 1995 Year Fig. 3. Average species accumulation in 20 subplots in plot Gettlinge A1 1985-1995. C obs = Observed cumulative species number; C L = Species accumulation according to the minimual mobility model; C R = Species accumulation according to the random species mobility model. Logarithmic regression for observed values: C obs = 12.1 yr 0.305 ; R 2 = 0.98. we may expand our ideas on the maintenance of species richness (van der Maarel & Sykes 1993; Sykes et al. 1994). Mean species richness S m follows simply from: S m = Σ i / n (3) where i are the (absolute) frequencies of the various species and N is the number of subplots. Similarly, the cumulative species number C m follows from C m = Σ ci / n (4) In Fig. 3 we have plotted the cumulative species richness in plots GA1 from 1985 to 1995. One can regress C m on time (in yr) with a logarithmic function C m = 12.1 yr 0.305 (r 2 = 0.98). We have also indicated how the species accumulation would be under the conditions oinimal mobility and random mobility. The observed increase falls roughly between the two extremes. Some remarks on the random mobility model CR Cobs The Carousel model has been interpreted as a model for random mobility, leading to random increase in cumulative frequency and random increase of cumulative species number for all species participating in the model. This was unintended. Moreover, as we explained in the C L Introduction, the random accumulation model has no spatial component. Indeed, only part of the species involved have means for dispersal and extension enabling them to move freely, i.e. to cover any distance. In reality many species extend around subplots they already occupy. Although we do not yet have quantitative data on this aspect, it is clear from studying the distribution patterns that the spatial extension of species is often limited as is also demonstrated in Fig. 2 in van der Maarel & Sykes (1993) and by Herben et al. (1993). It would be possible to devise a spatially limited random model. So, in addition, we should follow and interpret the dynamics of individual species and build spatially explicit dynamic models (e.g. Czárán & Bartha 1989; Silvertown et al. 1992; Law et al. 1994; Herben et al. 1995). In such models the idea of guild proportionality (Wilson 1989; Wilson & Roxburgh 1992; Wilson et al. 1995) can be elaborated as well. Another limitation in the interpretation of the random model can be exemplified with Achillea millefolium. This species spread rapidly in GA1 from 1985 to 1989 and its mobility could not be distinguished from random. By 1989 it had reached all 20 subplots but one; logically, its speed of extension slowed done and, indeed, over the period 1985-1995 the species extension was not random. Irrespective of the ability of a species to exhibit a random mobility, it may or may not occupy new microsites in the community. Most species, however, appear to be able to reach new places. While the mean species frequency in 1985 was ca. 35 in the four plots (Table 2), the cumulative frequency values in 1989 have increased to ca. 50. In GA1 the values for 1985, 1989 cumulative and 1995 cumulative are 37 54 61. Another way to express the accumulation is to determine the number of species reaching a cumulative frequency of 80 %. While in 1985 3-4 species had a frequency of 80 % or higher in the four plots, in 1989 there were 10-15 species with a cumulative frequency of 80 % or higher. For GA1 the figures are 4 species in 1985, 15 in 1989 and 18 in 1995. One other aspect is that new species are immigrating all the time. For instance, since the 1985 analysis, four new species had entered one or more subplots of GA1 by 1989 and two more new species by 1995. This process of immigration is exactly what we expect according to the species pool concept (Cornell & Lawton 1992; Zobel 1992; Eriksson 1993), as elaborated and linked to the Carousel model by Pärtel et al. (1996). For such newcomers it may take many years to reach a high cumulative frequency. And, of course there are always the occasional species, which may enter the community but also disappear again soon. Finally we repeat (see van der Maarel & Sykes

208 van der Maarel, E. & Sykes, M.T. 1993) that the rate of species mobility is a function of the size of the subplots chosen to describe the internal community dynamics. Generally, the mobility is more pronounced in small subplots, but we have no data as yet on the relation between median mobility rate and subplot size. Concluding remarks Our results here do indeed show that many species show an increase in cumulative frequency not significantly different from random. The Avenetum grassland on Öland and probably other similar communities do show high internal dynamics, as we indicated earlier. With the mobility rate we now have a simple, relative, measure of the average turn-around rate for each of the participating species. On the other hand, many species move at a lower rate than expected on a random basis. This is no surprise and can easily be understood from the dispersal constraints many species have and the tendency of some species to stay in the same position from one year to the next. Our point has been, and still is, that each species turns around in the carousel with its own speed, varying from random-fast to slow, but, on average turning much faster than many of us seem to realize. The next step in the approach of species mobility will be at the community level and will concentrate on turn-around time in the carousel. Acknowledgements. We thank J.B. Wilson for assistance and advice on the original null model, and three referees for comments on the paper. References Cornell, H.V. & Lawton, J.H. 1992. Species interactions, local and regional processes, and limits to the richness of ecological communities: a theoretical perspective. J. Anim. Ecol. 61: 1-12. Czárán, T. & Bartha, S. 1989. The effect of spatial pattern on community dynamics; a comparison of simulated and field data. Vegetatio 83: 229-239. Eriksson, O. 1993. The species-pool hypothesis and plant community diversity. Oikos 68: 371-374. Herben, T., Krahulec, F., Hadincová, V. & Kovářová, M. (1993): Small-scale spatial dynamics of plant species in a grassland community over six years. J. Veg. Sci. 4: 171-178. Herben, T., During, H.J. & Krahulec, F. 1995. Spatiotemporal dynamics in mountain grasslands: species autocorrelations in space and time. Folia Geobot. Phytotax. 30: 185-196. Krahulec, F., Rosén, E. & van der Maarel, E. 1986. Preliminary classification and ecology of dry grassland communities on Ölands Stora Alvar (Sweden). Nord. J. Bot. 6: 797-809. Law, R., McLellan, A. & Mahdi, A.S. 1994. Spatiotemporal processes in a calcareous grassland. Plant Spec. Biol. 8: 175-193. Pärtel, M., Zobel, M., Zobel, K. & van der Maarel, E. 1996. The species pool and its relation to species richness: evidence from Estonian plant communities. Oikos 75: 111-117. Peet R.K., van der Maarel, E., Rosén, E., Willems, J.H., Norquist, C. & Walker, J. 1990. Mechanisms of coexistence in species-rich grasslands. Bull. Ecol. Soc. Am. 71: 283. Rosén, E. 1982. Vegetation development and sheep grazing in limestone grasslands of south Öland, Sweden. Acta Phytogeogr. Suec. 72: 1-104. Rosén, E. 1995. Periodic drought and long-term dynamics of alvar grassland vegetation on Öland, Sweden. Folia Geobot. Phytotax. 30: 131-140. Silvertown, J., Holtier, S., Johnson, J. & Dale, P. 1992. Cellular automaton models of interspecific competition for space - the effect of pattern on process. J. Ecol. 80: 527-534. Sykes, M.T., van der Maarel, E., Peet, R.K. & Willems, J.H. 1994. High species mobility in species-rich plant communities: an intercontinental comparison. Folia Geobot. Phytotax. 29: 439-448. van der Maarel, E. 1996.Pattern and process in the plant community: Fifty years after A.S. Watt. J. Veg. Sci. 7: 19-28. van der Maarel, E. & Sykes, M.T. 1993. Small-scale plant species turnover in grasslands: the carousel model and a new niche concept. J. Veg. Sci. 4: 179-188. van der Maarel, E., Noest, V. & Palmer, M.W. 1995. Variation in species richness on small grassland quadrats: niche structure or small-scale plant mobility. J. Veg. Sci. 6: 741-752. Wilson, J.B. 1989. A null model of guild proportionality, applied to stratification of a New Zealand temperate rain forest. Oecologia (Berl.) 80: 263-267. Wilson, J.B., Gitay, H. & Agnew, A.D.Q. 1987. Does niche limitation exist? Funct. Ecol. 1: 391-397. Wilson, J.B. & Roxburgh, S.H. 1994. A demonstration of guild-based assembly rules for a plant community, and determination of intrinsic guilds. Oikos 69: 267-276. Wilson, J.B., Sykes, M.T. & Peet, R.K. 1995. Time and space in the community structure of a species-rich grassland. J. Veg. Sci. 6: 729-740. Zobel, M. 1992. Plant species coexistence: The role of historical, evolutionary and ecological factors. Oikos 65: 314-320. Received 28 June 1996; Revision received 18 March 1996; Accepted 2 April 1997.