Bryophyte biomass and species richness on the Park Grass ...

Plant Ecology 151: 129–141, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.

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Bryophyte biomass and species richness on the Park Grass Experiment, Rothamsted, UK R. Virtanen1 , A. E. Johnston2, M. J. Crawley3 & G. R. Edwards4 1 Department

of Biology, University of Oulu, Oulu, Finland (E-mail: [email protected]); 2 Rothamsted Experimental Station, Harpenden, Herts, UK; 3 Imperial College, Department of Biology, Silwood Park, Ascot, UK; 4 Thomas Huxley School of the Environment, Earth Sciences and Engineering, Imperial College, Wye College Campus, Ashford, Kent, UK Received 29 October 1999; accepted in revised form 20 June 2000

Key words: pH, Acidity, Community, Diversity, Grassland, Long-term effect, Nutrients, Transient dynamics

Abstract The relationships between bryophyte biomass and species richness and soil pH, nutrient applications and vascular plant biomass and species richness were analyzed for the Park Grass Experiment (Rothamsted, UK). The study examined the abundance of bryophytes in relation to long-term fertilizer and lime application and to fertilizer treatments recently being ceased on some plots. The probability of bryophytes being present on a plot increased with increasing soil pH, and on plots at soil pH 3.3–4.5, the lowest values in this experiment, there were virtually no mosses present. Total bryophyte biomass decreased with increasing vascular plant biomass and vascular plant richness. Both bryophyte biomass and species richness showed a curvilinear response to soil pH. Bryophyte biomass was markedly increased on plots where nitrogen (N) fertilization had recently been ceased. The abundance of the common bryophyte species showed individualistic responses to treatments. N had a negative effect on the abundance of Brachythecium rutabulum. Increasing soil pH, and the application of phosphorus (P) and potassium (K) fertilizer together, had a positive effect on Eurhynchium praelongum. This species was also negatively affected by N, but tolerated larger amounts of it (100–150 kg ha−1 N) than B. rutabulum. An ephemeral moss, Bryum subapiculatum, had a unimodal response to soil pH but showed no response to N, P, K or other explanatory variables. Nomenclature: Blockeel & Long (1998).

Introduction Determining which factors control the number, identity and relative abundance of plant species remains a central goal in ecology. The role of soil resource availability has attracted much attention (Tilman 1988). Both observational and theoretical studies have suggested that nutrient supply rates can control the abundance of species in communities (Snaydon 1962; Thurston 1969; Tilman 1982, 1988; Carson & Pickett 1990). These suggestions have been reinforced by experimental studies showing dramatic effects of fertilizer and lime application on community composition (Silvertown 1980; Tilman & Olff 1991). These

responses reflect differences in the capacity of plants to tolerate, assimilate and use nutrients (Kellner 1993; Turkington et al. 1998), as well as indirect effects of nutrients on other factors controlling competition and composition. These factors include the levels of herbivory (John & Turkington 1995) and the amount of plant litter (Tilman 1993). Many studies highlighting the importance of resource supply rate have been conducted with vascular plants (Crawley 1997). Much less is known for bryophytes, even though they are a widespread group of plants, have a considerable role in many ecosystems and can react rapidly to environmental changes (Longton 1984; Huntley et al. 1998).

130 In temperate grasslands, bryophytes are an inconspicuous group of plants for most of the year. They reach peak abundance in the moist cool seasons of autumn-spring and have a low abundance in the summer months (Al-Mufti et al. 1977; van Tooren et al. 1988; van der Hoeven & During 1997). Grassland bryophytes are generally viewed as being poor competitors with vascular plants; their abundance declining as vascular plant cover increases (Watson 1960; van Tooren et al. 1988). Previous studies have shown that bryophytes are sensitive to acid deposition and the level of nutrients in the atmosphere (Bates 1992, 1994; Brown 1992; Farmer et al. 1992). Nitrogen fertilization is also known to have negative impacts on some bryophytes (Mickiewicz 1976; Bakken 1994). To date these fertilization studies have been short-term, and so they would typically measure the transient dynamics that inevitably follow the imposition of a novel fertilizer treatment (Tilman et al. 1994; Crawley 1997). No data exist on how long-term variation in nutrient supply rates and soil pH affect the equilibrium composition of bryophytes. The Park Grass Experiment (PGE), begun at Rothamsted, England in 1856 and still running, affords a unique opportunity to examine the influence of long-term differences in nutrient (N, P and K) supply rate, soil pH and community structure on bryophytes. Regular schedules of fertilizer and chalk (calcium carbonate referred to as liming) have created plots with marked differences in vascular plant species richness and biomass. The botanical composition of vascular plants for many of the plots has been in dynamic equilibrium since about 1900 (Silvertown 1980; Silvertown et al. 1994; Dodd et al. 1995). However, some recent changes in fertilizer treatments on some subplots make it possible to estimate transient dynamics of bryophytes in response to changing nutrient levels. This paper uses data on bryophyte abundance from the PGE to examine how the number, identity and relative abundance of bryophytes is related to - long-term differences in soil pH and soil nutrient status; - cessation of nutrient inputs; and - differences in community structure of variables like vascular plant biomass and species richness.

Material and methods The Park Grass Experiment The Park Grass Experiment was started in 1856 and 1872 on a flat 4 ha field at Rothamsted Experimental Station, Harpenden, 40 km north of London, England. The field was of comparatively uniform vegetation and soil type, and had been under permanent grass for at least 200 years. The British National Vegetation Classification (Rodwell 1992) that most closely matched the original field was MG5 (Cynosurus cristatusCentaurea nigra grassland) (Dodd et al. 1994). The plots are harvested twice each year, once as summer (June) and then in late autumn. The cut herbage is taken as silage. The field was divided into 20 plots between 0.1 and 0.2 ha. Inorganic and organic fertilizers were applied to 18 plots and 2 plots (3 and 12) were left as unfertilized controls. On many plots the same fertilizers continue to be applied annually. The P, K, Mg and Na are applied in late winter and the N in early spring. Farmyard manure (FYM) and fishmeal are applied every fourth year in winter. Liming was first tested in the late 19th century but it was not until 1903 that nearly all the plots were halved to test applying chalk every 4th year. For details of the changes in manuring and liming until 1963 see Warren & Johnston (1964) and Johnston et al. (1986). In 1965, the plots were subdivided again to give four sub-plots of which three (a, b, c) are now limed. The rate and frequency of lime application is controlled to achieve target pH levels of 7, 6 and 5 for sub-plots a, b and c, respectively. Subplot d has never been limed (Warren et al. 1965). For details of treatments see Figure 1. Some further changes to the fertilizer treatments have been made in the last 10 years (see Figure 1). In 1989, N fertilizer application was ceased on one half of two plots receiving N, P, K fertilizers (9 and 14, see Figure 1). The soil pH of these no-N half plots, now designated as 9/1 and 14/1 is predicted to converge. Of interest is whether the species composition of these two half plots converges towards that on plots 7 and is which only get P and K. In 1994, FYM and fishmeal application was ceased on one half of plot 13; the noFYM half is now designated as 13/1. Of interest is whether the species composition of this plot converges towards plot 7 which just gets just P and K fertilizer. Plot 7 is used as the endpoint rather than the control plots (3 and 12) as the FYM has built up reserves of P and K in the soil. In addition, since 1996, K fertil-

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Figure 1. The Park Grass Experiment with details of fertilizer and liming treatments. For further details of treatments and changes from 1856 to 1963, see Warren & Johnston (1964).

132 izer has been applied to one half of plot 2 plot 2/1). This allows the short-term effects of K application on bryophyte abundance to be examined. Sampling The sampling for the study reported was carried out in late February 1997 to coincide with the time of peak bryophyte biomass in grasslands. Six 25 × 25 cm quadrats were randomly located in 87 of the 97 subplots. Plots 5 and 6c-d are no longer in experimental use, and plots 11/1, 19/1-3 and 20/1-3 were not sampled. The metal quadrats were thrown and left to bounce freely. Bryophytes were manually scraped up and put into plastic bags. In the laboratory, soil and vascular plant debris were removed before the bryophytes were air dried for 5–7 days and identified to species level. The identifications were made with the help of Smith (1978,1990). Nomenclature of taxa follows Blockeel & Long (1998). The taxon referred to as Bryum subapiculatum may include some other species of the Bryum erythrocarpum complex (Smith 1978). Samples were then oven dried at 80 ◦ C for 24 hours and weighed. Statistical analyses Data were analyzed by multiple regression using generalized linear models (Payne 1986; McCullagh & Nelder 1989; Crawley 1993). The minimum adequate model for each response variable was found by deleting variables with no significant effect from the maximal model, which left those factors whose deletion caused significant effects (Crawley 1993). At all stages, control of the model was manual (i.e, an automatic stepwise deletion was not used). Unless specified otherwise in the results section, the maximal model included the following predictor variables: P (none, P applied); K (none, K applied); FYM (no FYM, FYM applied every 4th year, FYM not applied after 1994); N type (no N, N applied as ammonium sulphate, N applied as sodium nitrate, N not applied after 1989); N rate (0, 48, 96 and 144 kg N ha−1 ); soil pH; vascular plant biomass (mean hay yield from the June harvest); and vascular plant species richness (no of species in each sub-plot in summer 1994, M.J. Crawley, unpublished). Quadratic terms of continuous response variables were also fitted in the maximal model. As a large number of significance tests were conducted we chose to use α = 0.01 as our level of significance for retaining factors in the model. Two approaches were adopted to analyze total bryophyte

Figure 2. The presence of bryophytes on the 89 sub-plot of Park Grass Experiment in relation to soil pH (1 = present, 0 = absent). The line represents fitted values for the relationship between the presence of bryophytes and soil pH back-transformed from the logit-scale on which the analysis was carried out.

biomass summed across all species. First, the presence/absence of bryophytes on each sub-plot was analyzed using binomial errors with a logit link function. Second, a data set was constructed that included only those sub-plots where bryophytes were found and the mean dry weight of bryophytes, averaged across the six quadrats in each sub-plot, was analyzed using normal errors. Three different link functions (square root, log and identity; Crawley 1993) were used. All produced the same minimum adequate model, and the model using normal errors and identity link is presented in the results. The number of species found in the six quadrats in each sub-plot was analyzed using Poisson errors with a log link function. The data set for this analysis excluded those plots where no bryophytes were found. To allow investigation of the relationship between biomass and species richness (Grime 1979), the maximal model fitted also included linear and quadratic effects of bryophyte dry weight. Brachythecium rutabulum, Bryum subapiculatum and Eurhynchium praelongum occurred frequently enough to analyze the effects of treatments on their distribution. For each species, the number of quadrats out of the six sampled on each sub-plot where the species was present was analyzed using binomial errors with a logit link function. Where models were over-dispersed (i.e, residual deviance was greater than residual degrees of freedom), an empirical scale parameter was estimated, and F -tests rather than χ 2 -tests were carried out (Crawley 1993). The maximal model

133 included bryophyte species richness in order to investigate relationships between local species richness and abundance of a particular species. The species richness value fitted was the number of species on a plot excluding the species being analyzed. To further analyze the response to the cessation of fertilizer application, the biomass of bryophytes on the half of the plot where fertilizer had been ceased (transient plot) was compared using t-tests with the half of the plot where the fertilizer had continued (start plot) and with the plot which already had the fertilizer treatments of the transient plot (end plot) (Figure 1). This was done by contrasting plot 9/1 (N last applied 1989) with 9/2 and 7, plot 14/1 (N last applied 1989) with 14/2 and 15, and plot 13/1 (FYM/fishmeal last applied 1994) with 13/2 and 7. The effect of the recent application of K fertilizer was examined using t-tests to compare bryophyte biomass on plots 2/2 and 2/1 (K first applied 1996). Results Total bryophyte biomass There was a significant effect of soil pH on the presence of any bryophyte on a sub-plot (Figure 2, χ 2 = 21.1, df = 1, P < 0.001). The probability that a bryophyte was present on a sub-plot increased with soil pH. There were no significant effects of the fertilizer treatments, vascular plant biomass or species richness on the presence of a bryophyte on a sub-plot. Analysis of sub-plots where bryophytes were present showed that the dry weight of bryophyte decreased as vascular plant biomass increased (Figure 3a, F1,68 = 11.6, P < 0.01) and as vascular plant species richness increased (Figure 3b, F1,68 = 7.2, P < 0.01) and was a unimodal function of soil pH (Figure 3c, F1,68 = 11.4, P < 0.01), although there was considerable scatter in these relationships. There was a significant effect of N fertilizer type on bryophyte biomass (Figure 3d, F1,68 = 10.4, P < 0.01), with higher biomass where N fertilization had been ceased (e.g., plot 9/1 and 14/1 than where N was applied as sodium nitrate or ammonium sulphate. The plots where N was applied as sodium nitrate or ammonium sulphate did not differ in bryophyte biomass. There was also a significant effect of FYM application on bryophyte biomass (F2,68 = 5.2, P < 0.01). The biomass was greater on plots where FYM was applied than on plots where it was not applied or where application had been ceased (Figure 3e).

Species richness A total of 24 species were found on the 87 subplots sampled (Appendix), with a maximum of 8 species on one sub-plot. The analysis of those subplots where bryophyte occurred showed there was significant quadratic effect of soil pH on the number of bryophyte species on each sub-plot although there was considerable scatter among data points (Figure 4, χ 2 = 7.1, df = 1, P < 0.01). Fertilizer application, vascular plant species richness, vascular plant biomass and bryophyte biomass had no significant effect on bryophyte species richness. Relative abundance of common species There was a significant effect of N fertilizer type on the proportion of quadrats in each sub-plot where Brachythecium rutabulum was present (Figure 5a, F3,72 = 4.6, P < 0.01). The proportion was lower on plots receiving N as ammonium sulphate than sodium nitrate, but this effect was not significant. The proportion was lower for both nitrogen fertilizer types than for plots receiving no N, with the plots where N application had recently been stopped having intermediate values. The proportion of quadrats in each sub-plot where B. rutabulum was present declined as N rate increased (Figure 5b, F3,72 = 5.0, P < 0.001). The proportion of quadrats in each sub-plot where Eurhynchium praelongum was present increased as soil pH increased (Figure 6a, F1,71 = 7.6, P < 0.01). There was significant effect of N rate (F3,71 = 10.2., P < 0.01) and the P × K interaction (F1,73 = 8.3, P < 0.01) on the proportion of quadrats where E. praelongum was present. The proportion was higher at the two lower N rates than the higher two N rates (Figure 6b). The addition of K fertilizer had a negative impact on the proportion of quadrats where E. praelongum was present when no P was applied, but a positive impact when P was applied (Figure 6c). The proportion of quadrats where Bryum subapiculatum was present increased with soil pH up to a pH 5.7 and then declined as soil pH increased further (χ 2 = 16.3, df = 1, P < 0.01), although the relationship was not strong (Figure 7). This moss showed no statistically significant response to N, P, K or other explanatory variables. Transient plots Analyses of plots where fertilizer treatments had been ceased show further details on how bryophyte biomass

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Figure 3. Bryophyte biomass (g dry weight 0.0625 m−2 ) on the Park Grass Experiment in relation to (a) hay yield, (b) vascular plant richness, (c) soil pH, (d) nitrogen fertilizer type, and (e) farmyard manure application. The lines in (a)–(c) represent fitted value for each relationship. The values in (d) and (e) are means (± SE), and bars with different letters are significantly different according to LSD-test.

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Figure 4. Bryophyte species richness on the Park Grass Experiment in relation to soil pH. The sub-plots where no bryophytes were found are not included in this figure. The line represents fitted values for the relationship between species richness and soil pH back-transformed from the log-scale on which analysis was carried out.

and species react to changes in nutrient levels. The ‘transient’ sub-plot 9/1, not receiving N any more, had a greater bryophyte biomass than the plot 9/2 receiving N at soil pH 6 (pH level b; Table 1). Here the species increased was obviously Eurhynchium praelongum which was present in all quadrats on this sub-plot (Table 2). Bryophyte biomass on the ‘end’ plot 7, where Brachythecium rutabulum and E. praelongum both occurred (Table 2), tended to be less than on the transient plots, although this was not significant (Table 1). On plot 14/1 at soil pH 5 or less (c and d), ceasing the N application in 1989, resulted in an increase in bryophyte biomass in 1997 compared to both the plot it had come from and the plot it was converging to. B. rutabulum appeared to have become more common on transient plot 14/1 than on start plot 14/2, whereas there seemed to be no marked difference in the occurrence of B. rutabulum and E. praelongum between plot 14/1 and plot 15 (Table 2). The cessation of the FYM/fishmeal treatment did not have significant across-liming level effects on bryophyte biomass (Figure 3e). However, at pH 7 (pH level a), the sub-plot no longer receiving FYM/fishmeal had a much smaller bryophyte biomass than the expected endpoint (plot 7) (Table 1). There were no clear differences in the occurrence of different bryophyte species among plots receiving FYM, ceased FYM and expected endpoint (Table 2). Two applications of K to plot 2/1 had not caused any changes in bryophyte biomass by spring 1997 (Table 1).

Figure 5. The effect of (a) nitrogen fertilizer type and (b) nitrogen fertilizer rate on the proportion of quadrats in each sub-plot where Brachythecium rutabulum was present. The values are means (± SE) back-transformed from the logit-scale on which analysis was carried out. Bars with different letters are significantly different.

Discussion Effect of soil pH The dominant variable affecting the distribution of bryophytes on the Park Grass Experiment was soil pH. Bryophytes were virtually absent from plots with soil pH < 4.5. This suggests that the most acidic plots are beyond the tolerance limits of most grassland bryophytes. The precise mechanism by which bryophytes are excluded from acid plots is unclear. In some experiments simulating acid rain, very acid conditions have reduced photosynthetic rates and accelerated evapotranspiration of feather moss (Hutchinson & Scott 1988), but experimental data on acid tolerance of grassland bryophytes are scarce. It is

136 Table 1. Bryophyte biomass in relation to recent changes in treatments of the Park Grass Experiment. The soil pH in sub-plots a, b and c, are 7, 6 and 5. respectively. pH levels are still lower in sub-plot d, which has never been limed. Significant changes indicated as bold text. The biomass of vascular plants (g 0.125 m−2 ) in June 1996 given in parentheses. Start: plot before fertilizer treatment has been changed; Transient: plot where fertilizer treatment has been changed; End: plot which has received for long periods the same fertilizer treatment as the transient plot (e.g. start plot minus fertilizer treatment stopped). Change of treatment

Mean bryophyte biomass in 6 plots sampled (g DW 0.0625 m−2 ), (vascular plant biomass)

t-test (P values)

Start

Transient

End

Start vs. transient

Transient vs. end

a b c d mean

9/2 0.019 (67.4) 0.063 (66.3) 0.012 (30.9) 0 (31.6) 0.024

9/1 (ceased) 0.897 (59.4) 4.825 (65.1) 1.967 (23.2) 0.306 (22.9) 1.999

7 0.343 (50.2) 0.247 (57.4) 0.381 (53.2) 0.221 (32.0) 0.298

0.121 0.050 0.216 0.282 0.096

0.323 0.058 0.311 0.761 0.141

a b c d mean

14/2 0.052 (93.7) 0.416 (76.6) 0.366 (72.2) 0.098 (98.9) 0.233

14/1 (ceased) 0.374 (49.9) 0.514 (54.9) 4.525 (42.1) 3.023 (46.5) 2.109

15 0.242 (49.7) 0.432 (49.8) 0.131 (25.3) 0.189 (24.5) 0.249

0.161 0.820 0.011 0.022 0.114

0.645 0.842 0.008 0.025 0.116

a b c d mean

13/2 2.279 (39.6) 1.647 (56.9) 0.251(42.8) 0.050 (38.0) 1.057

13/1 (ceased) 2.084 (50.9) 0.071 (51.7) 0.804 (44.6) 0.091 (47.4) 0.762

7 0.343 (50.2) 0.247 (57.4) 0.381 (53.2) 0.221 (32.0) 0.298

0.854 0.267 0.450 0.501 0.696

0.007 0.182 0.566 0.068 0.369

a b c d mean

2/2 0.126 (25.3) 0.114 (42.2) 0.033 (18.6) 0.022 (24.1) 0.074

2/1 (added) 0.062 (32.2) 0.210 (36.6) 0.010 (26.0) 0.185 (23.9) 0.139

Soil pH level

N (ammonium sulphate)

N (sodium nitrate)

FYM

K

also possible that the high concentrations of soluble aluminum in acid environments reduce bryophyte survival (Büscher et al. 1990). In addition, dense layers of non-decomposed litter accumulated on acid plots (M.J. Crawley, unpublished data) may prevent bryophyte growth. The absence of bryophytes on the most acid plots suggests that bryophytes, as a group, have narrower pH amplitude than the vascular plants of the Park Grass Experiment (Tilman et al. 1994). This result may partly reflect a ‘pool size’ effect in that there are

0.271 0.361 0.218 0.137 0.190

relatively few bryophyte species in the Hertfordshire area adapted to soil pH < 4.5, and they may exhibit very slow immigration rates (Cornish 1954; During 1990). The mosses on the Park Grass Experiment characteristic of acid heathlands include Rhytidiadelphus squarrosus and Scleropodium purum, and these were present in low abundance on a few sub-plots. Species characteristic of acid grassland sites (e.g., Campylopus introflexus, C. pyriformis and Pleurozium schreberi) were not found.

137 Table 2. The occurrences of two common species, Brachythecium rutabulum (Br) and Eurhynchium praelongum (Ep), in plots with recent changes in treatments (soil pH levels as in Table 3). The numbers after species code indicate the occurrence in plots out of the 6 plots sampled. In 9/2d, 9/1c, 2/2c and 2/1c,d other moss species were recorded. For additional details, see Table 1. Change of treatment

Soil pH level

N (ammonium sulphate) a b c d N (sodium nitrate)

Presence in 0.0625 m−2 plots Start Transient End

9/2 Ep 3 Ep 4 Ep 2

9/1 (ceased) Br 1 Ep 5 Ep 6 Br 1 Ep 4

7 Br 5 Ep 2 Br 6 Ep 6 Br 2 Ep 4 Br 1 Ep 5

a b c d

14/2 Ep 5 Br 1 Ep 6 Br 1 Ep 5 Br 2 Ep 4

14/1 (ceased) Br 1 Ep 4 Br 3 Ep 5 Br 5 Ep 6 Br 6 Ep 6


a b c d

13/2 Br 6 Ep 5 Br 5 Ep 1 Br 3 Ep 4 Br 2 Ep 5

13/1 (ceased) Br 5 Ep 1 Br 3 Ep 1 Br 3 Ep 4 Br 1 Ep 5


2/2 Br 6 Ep 2 Br 5

2/1 (added) Br 4 Ep 4 Br 4 Ep 1

FYM

K a b c d

On plots at pH 4.5–6.5 bryophyte biomass and species richness was at highest. At this intermediate pH range the soil chemical properties allow a higher number of species to survive. In addition, here earthworms produce fresh soil on the ground and thus create suitable growing substrates for bryophytes. At highest pH, in turn, shading by dense vascular plants cover (Silvertown 1980) may reduce bryophyte abundance. In addition, the surface application of CaCO3 may kill most bryophytes, except for calcicolous or calciphilous species such as Tortula acaulon found on some of the ‘a’ sub-plots of the Park Grass. Such detrimental effects of CaCO3 application have been seen with some vascular plants (Tilman et al. 1994). The detected curvilinear relationship between bryophyte species richness and pH matches well with a similar relationship found for vascular plants of northern England (Grime 1979). Instead, there was no apparent relationship between bryophyte species

Br 1

richness and bryophyte biomass. In the Park Grass Experiment, the greatest species richness occurred where the bryophyte biomass is also greatest. In other words, the relationship between bryophyte biomass and richness, if anything, is positive. This contrasts with the pattern detected for vascular plants of the Park Grass Experiment (Silvertown 1980; Crawley 1997) and also mismatches with a curvilinear relationship between biomass and species richness in a manner presented by Grime (1979). Effect of vascular plants on bryophytes Two effects of vascular plants on the Park Grass bryophytes were observed. First, total bryophyte biomass declined as vascular plant biomass increased. This result is consistent with previous studies that have documented increases in bryophyte biomass with events that reduce vascular plant biomass (e.g., grazing, Watson 1960; During & Willems 1986; van

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Figure 7. The proportion of quadrats in each sub-plot where Bryum subapiculatum was present in relation to soil pH. The line represents fitted values for the relationship backtransformed from the logit-scale on which analysis was carried out.

Tooren et al. 1988, 1990; Common et al. 1991). It also supports the common notion that bryophytes are competitively inferior to vascular plants. Second, bryophyte biomass decreased as vascular plant species richness increased. It seems that small and tightly packed vascular plants characteristic of control plots (M. J. Crawley, unpublished data) may leave little space for bryophytes to grow (see also Watson 1960; During & Lloret 1996). These results suggest that bryophytes on Park Grass are limited by competition for space and that the bryophyte responses depend on vascular plants and changes in resource levels can be mediated via changes in the vascular plant community. Effect of P and K

Figure 6. The effect of (a) soil pH, (b) nitrogen fertilizer rate and (c) phosphorus and potassium fertilizer on the proportion of quadrats in each sub-plot where Eurhynchium praelongum was present. The line in (a) represents the fitted values for the relationship from the logit-scale on which analysis Was carried out. The values in (b) and (c) are means (± SE) back-transformed from the logit-scale on which analysis was carried out. Bars with different letters are significantly different.

There was little apparent effect of the P and K status of the soil on bryophyte abundance. Only E. praelongum was positively affected where both K and P were applied. Furthermore, the recent application of K to plot 2/1 showed no effect on bryophyte biomass. The fact that Park Grass bryophytes have only a small response to P and K, is surprising because many vascular plants seem to respond and even vascular plant species richness declines when P and K are added (Williams 1978; Tilman et al. 1994). Moreover, previous studies in boreal forests and peatlands have normally shown negative effects of P and K on bryophytes. In a dry bog addition of rapidly soluble P and K fertilizers had negative effects particularly on a spruce site (Jäppinen & Hotanen 1990). Similarly, negative effects of P and K were found by Vasander et al. (1993). However, Dirkse & Martakis (1992) and Finér & Braekke (1991)

139 have found positive effects of P and K on bryophyte abundance. Effect of FYM and fishmeal There was a marked increase in total bryophyte biomass on plots where FYM and fishmeal are each applied once every four years. The bullock manure (35 t ha−1 applied every fourth year, has many pieces of manure up to 30 cm in diameter and 5 cm thick. These pieces cover and kill vascular plants, creating sites free of large vascular plants which bryophytes could colonize. These sites sometimes last up to a year (G. R. Edwards, unpublished data). Effects of N rate, N fertilizer type and cessation of N fertilizer application There was no effect of N fertilizer rate on bryophyte biomass. This contrasts with previous shorter-term studies showing a negative effect of N fertilizer application on bryophyte abundance (Mickiewicz 1976; Kellner 1993; Vasander et al. 1993; Turkington et al. 1998). In addition, there was no statistically significant difference in total biomass, species richness or abundance of common species between plots given the same rate of N but as sodium nitrate and ammonium sulphate. This contrasts with studies of vascular plants on the Park Grass Experiment (Tilman et al. 1994). The lack of significant correlation between bryophyte species richness and N rate also contrasts with studies showing clearly negative effect of N rate on vascular plant species richness (e.g., Tilman 1982, 1993). Individual bryophyte species showed different species-specific responses to N. Bryum subapiculatum showed no response. This moss is a short-lived species that produces copious vegetative propagules (size 190–260 µm), a typical character of an ephemeral colonist species dispersing from patch to patch (During 1979, 1992; Herben 1994). According to During (1979) this strategy fits to a habitat which is present only for a short period but which predictably reappears in the same community. Diaspore bank probably plays an important role for the long-term persistence of this species in grasslands (During & ter Horst 1983). This moss appears to strongly trade-off its competitive-persistence ability against its colonization ability, which may be one reason why it does not show any distinct response in relation to varying resource levels. The abundance of Brachythecium rutabulum decreased linearly with increasing N rate, being absent

on plots receiving 144 kg N ha−1 . Eurhynchium praelongum also declined with increasing N rate but was still present where N was applied at 96 and 144 kg N ha−1 . It thus seems that E. praelongum can be regarded as a more nitrotolerant moss than B. rutabulum. In another study, E. hians (E. swartzii), a related species to E. praelongum (Stech & Frahm 1999), was more tolerant of large amounts of NPK than B. rutabulum (Mickiewicz 1976). Furthermore, an Eurhynchium species has also colonized NPK fertilized drained bog sites in Norway (Finér & Braekke 1991) and E. praelongum is often found on N-rich bird-cliffs (Watson 1971) and productive grasslands. Rather unexpectedly, the cessation of N fertilizer application led to dramatic increase of bryophyte biomass. The increase in bryophyte biomass was pronounced on the plots of intermediate soil pH. Besides any direct effect of withholding N, a reduction in the vascular plant biomass on some plots (particularly on plot 14/1), and therefore increased availability of suitable microsites and light, may have led to the increased bryophyte biomass. The finding that the largest response to stopping N was at the medium soil pH levels is not fully consistent with the general response of vascular plant biomass. At low soil pH (e.g., 9/1 d; 14/1d) there are few bryophytes, so making it difficult to detect any effect. At high pH (e.g., 9/1 a; 14/1a) the response may be small because vascular plant biomass is still large on these plots. There are few similar studies to compare these results. Ingerpuu et al. (1998) found that bryophyte species richness increased and cover decreased in an experiment where fertilizing was conducted 1961-1981 and where bryophytes were sampled in 1995. There are differences in species’ responses to the cessation of N fertilizer application. E. praelongum grows on transient plots that have previously received either sodium nitrate or ammonium sulphate. This probably reflects the fact that this moss have grown on these plots when still fertilized. B. rutabulum is virtually absent on plots fertilized by ammonium sulphate and it has immigrated the transient plots very poorly. There is no direct evidence how possible differences in dispersal capacity or some other mechanisms could account for the differences in distributions of these two species. These results, nevertheless, suggest that the full recovery of the species composition of grassland bryophyte community from long-term application of ammonium sulphate treatment may take over ten years even though viable moss populations occur in the vicinity.

140 Acknowledgements This work was supported by a research grant from the Finnish Research Council for Environment and Natural Resources (to R.V.). We thank all persons at Silwood Park who assisted in bryophyte sampling. We also thank two anonymous refererees for constructive comments.

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Appendix The bryophyte species recorded in the Park Grass Experiment. In the parentheses the names used in Smith (1978). Ditrichaceae Pleuridium subulatum (Hedw.) Rabenh. Dicranaceae Dicranum scoparium Hedw. Fissidentaceae Fissidens bryoides Hedw. F. cf. celticus Paton Pottiaceae Barbula unguiculata Hedw. Didymodon insulanus (De Not.) M.O. Hill (Barbula cylindrica) Tortula acaulon (With.) R.H. Zander (Phascum cuspidatum) Funariaceae Funaria hygrometrica Hedw. Bryaceae Bryum argenteum Hedw. B. capillare Hedw. B. subapiculatum Hampe (B. microerythrocarpum) Mniaceae Plagiomnium cuspidatum (Hedw.) T.J. Kop. P. undulatum (Hedw.) T.J. Kop. Aulacomniaceae Aulacomnium androgynum (Hedw.) Schwägr. Brachytheciaceae Brachytecium albicans (Hedw.) Bruch, Schimp. & W. Gümbel B. rutabulum (Hedw.) Bruch, Schimp. & W. Gümbel Eurhynchium praelongum (Hedw.) Bruch, Schimp. & W.Gümbel E. pulchellum (Hedw.) Jenn. Scleropodium purum (Hedw.) Limpr. (Pseudoscleropodium purum) Plagiotheciaceae Plagiothecium sp. Hypnaceae Calliergonella cuspidata (Hedw.) Loeske (Calliergon cuspidatum) Hypnum cupressiforme Hedw. Rhytidiadelphus squarrosus (Hedw.) Warnst. Geocalycaceae Lophocolea bidentata (L.) Dumort.