SEARCH

SEARCH BY CITATION

Keywords:

  • chalk heath;
  • diversity;
  • edaphic factors;
  • grazing;
  • herbivore facilitation;
  • large herbivores;
  • plant species richness;
  • rabbit;
  • sheep;
  • soil heterogeneity

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

1. Both top-down and bottom-up influences, such as grazing herbivores and edaphic factors, may maintain species-rich vegetation by preventing dominant plants from reducing diversity. However, the interaction between grazing and other processes maintaining diversity, particularly in ecosystems with multiple herbivores, is poorly understood. We manipulated access by small and large vertebrate herbivores on an edaphically heterogeneous site. We investigated whether: (i) grazing and soil properties interacted in their impact on vegetation, (ii) the effects of herbivores on different plant functional groups depended on soil properties, and (iii) small and large herbivores were functionally equivalent.

2. Treatments allowed mixed rabbit and livestock grazing, rabbit grazing only or no grazing and were replicated within three areas differing in vegetation, soil nutrient availability and pH. Soil properties, plant species composition, vegetation height and above- and below-ground biomass were measured after 6 years.

3. Bottom-up and top-down impacts were both important, with soil properties and grazing explaining 42.1% and 9.2% of the variability in species composition between plots, respectively. Grazing enhanced the impact of soil properties on the plant community by preventing dominance by Ulex europaeus and maintaining differences in species composition between the areas.

4. Grazing consistently increased species richness across vegetation types, but the responses of different plant functional groups depended on area. For instance, grazing removal caused graminoid abundance to increase in the area where grasses were the dominant functional group, but to decrease in other areas.

5. Small herbivores (rabbits) were only partially functionally equivalent to larger grazing herbivores (livestock), as rabbit grazing pressure did not increase in plots ungrazed by large herbivores. The results suggested a facilitative relationship between large and small herbivores, with large herbivores improving forage quality and increasing access to plots by rabbits.

6.Synthesis. (i) Grazing and soil properties interacted in their impact on the composition and diversity of vegetation, (ii) the effects of herbivores on particular plant functional groups depended on the characteristics of the area, and (iii) small and large herbivores were not functionally equivalent, with small vertebrate herbivores unable to replace the impact of larger herbivores when these were removed.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Both top-down factors such as mammalian herbivory and bottom-up factors such as nutrient availability are key drivers of plant community composition, diversity and productivity, yet the relative impact of these factors varies between ecosystems (e.g. John & Turkington 1995; Alonso, Hartley & Thurlow 2001; Bakker et al. 2006). Many habitats with species-rich vegetation are of low fertility (Marrs 1993; Bobbink, Hornung & Roelofs 1998; Critchley et al. 2002) and grazed by mammalian herbivores (Dolman & Sutherland 1992; Loucougaray, Bonnis & Bouzille 2004), and their biodiversity is at risk when these factors change. Understanding the relative roles of herbivory and nutrients as drivers of community structure and composition in these systems is therefore of fundamental and applied importance (Olff & Ritchie 1998; Bokdam & Gleichman 2000).

The maintenance and restoration of species-rich vegetation often depends on the prevention of dominance by a few species (Bobbink & Willems 1993; Huisman et al. 1997). Both bottom-up mechanisms, such as low soil nutrient supply limiting the relative growth of potential dominants (Huisman et al. 1997; Lorenzo et al. 2007) and top-down mechanisms, such as herbivory, where dominant species have higher palatability or lower tolerance to grazing (Bakker et al. 1983; Bullock & Pakeman 1996) can have this effect, but interactions between herbivores and nutrient supply are also important (Proulx & Mazumder 1998; Hartley & Mitchell 2005; Denyer, Hartley & John 2007). For instance, Dutch salt marsh vegetation is species-rich and consists of small palatable species at low productivity (Kuijper, Nijhoff & Bakker 2004), but becomes dominated by a tall, relatively unpalatable grass (Elymus athericus, now Elytrigia atherica) at high productivity when not grazed. Bottom-up control prevents dominance of E. atherica at low productivity, where it is unable to compete for nutrients with the smaller species, whilst top-down control (grazing) prevents its dominance at higher levels of productivity, where herbivore numbers are highest.

The role of herbivory as a top-down factor maintaining species-rich vegetation also depends on the herbivore assemblage (Bakker et al. 2006). In particular, large (e.g. Putman, Fowler & Tout 1991; Loucougaray, Bonnis & Bouzille 2004) and small (e.g. Kuijper & Bakker 2005) mammalian herbivore species can differ in their impacts on vegetation. Small mammals (1–10 kg, Bakker et al. 2006) can strongly affect vegetation structure and species composition (e.g. Thomas 1960, 1963; Zeevalking & Fresco 1977; Bagchi, Namgail & Ritchie 2006), but their impact depends on habitat productivity (e.g. Bakker et al. 2006) and vegetation type (Cid et al. 1991; Bowers 1993; Bridle & Kirkpatrick 1999).

Differences in diet selection can lead to facilitative interactions between herbivores when one herbivore increases the access to a resource by another herbivore. An example is the relationship between geese and hares in a salt marsh system (van der Wal et al. 2000; Stahl et al. 2006). Hares consume the dominant plant, which is unpalatable to geese, thus improving the forage quality available to the geese. In contrast, negative interactions can occur when one herbivore changes the structure of vegetation and creates less favourable conditions for another. For example, Smith et al. (2001) reported that where large herbivores reduced vegetation height, they also reduced the cover and protection from predation for rodents sharing the same habitat. Thus, a mixed herbivore assemblage may exert different effects on vegetation than predicted from the impacts of separate herbivores (Smith et al. 2001). As small mammalian herbivores are present in many sites where livestock grazing maintains species-rich vegetation (Dolman & Sutherland 1992; Pakeman et al. 2003), it is important to determine the relative role of small herbivores as top-down controllers of vegetation composition and species richness, and whether they are functionally equivalent to livestock. Small herbivores tend to require high-energy diets and hence select plants with a high nutrient content, whilst large herbivores are able to gain sufficient energy from plants with a lower nutrient content (Demment & Van Soest 1985).

We investigated the impact of small and large herbivores on a natural productivity gradient on a single species-rich site after 6 years of an exclosure experiment. The vegetation at the site is chalk heath, mostly consisting of low-growing forbs and grasses interspersed with woody shrubs. In the absence of grazing the vegetation becomes overgrown, particularly by the leguminous woody shrub Ulex europaeus, and species richness is reduced. The soils are naturally nutrient-poor but where U. europaeus has been growing, the soil has lower pH (Grubb & Suter 1971) and elevated nutrient concentrations, creating heterogeneity in productivity across the site. We investigated whether (i) top-down (grazing) effects on different plant functional groups are consistent across vegetation, (ii) small herbivores (rabbits) are functionally equivalent to larger grazing herbivores when these are excluded and (iii) how top-down (grazing) impacts interact with bottom-up (soil properties) in this community.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Study site

This experiment was undertaken at Lullington Heath National Nature Reserve, East Sussex, UK (latitude 50.79, longitude 0.19). The reserve was established in 1954 to conserve one of the largest areas of chalk heath remaining in the UK. Chalk heath occurs where acid soils have been deposited over chalk bedrock (Grubb, Green & Merrifield 1969), and it supports both calcicole and calcifuge plants in species-rich vegetation. Sheep grazed the site until the 1920s and then, prior to the myxomatosis outbreak in the 1950s, open vegetation was maintained by the high rabbit numbers on the reserve. Livestock grazing was reintroduced in the 1970s and the site is now grazed all year round by a small flock of Hebridean sheep (c. 20 animals), and in the winter 2–3 native ponies (Exmoor and New Forest) have access to the site. The site is c. 12 ha. Rabbit numbers have recovered from the former decline (Tim Beech, pers. comm.).

The vegetation is spatially heterogeneous. There is a species-rich area of typical chalk heath (Area 1), on thinner soil, consisting of chalk grassland forbs and grasses with patches of Erica cinerea, Calluna vulgaris and other calcifuge plants. This area was never overgrown during the rabbit decline and therefore has been more consistently grazed by rabbits than the other, temporarily overgrown areas. In addition, there are areas of recovered chalk heath, on slightly deeper soil that contain a lower proportion of calcicole plants and are dominated either by thorny shrubs (Rosa pimpinellifolia, Rubus fruticosus agg. and sometimes U. europaeus (Area 2)) or heathers (C. vulgaris and E. cinerea (Area 3)). Species such as U. europaeus and C. vulgaris contribute to the lowering of pH as well as respond to it (Grubb & Suter 1971). The existence of the edaphic conditions that support chalk heath are themselves the result of a complex set of factors including grazing (management regimes) and topographical factors (Jenny 1941).

Experimental design

The grazing treatments were set-up in 1997 using two types of exclosures, with different mesh sizes, designed to either allow rabbit grazing only (large mesh of 16 × 16 cm) or no grazing (small mesh of 2 × 2 cm), hence excluding grazers stepwise from large to small. Similar control plots were established that were accessible to both livestock and rabbits. Each plot or exclosure measured 4 × 4 m. Within each of Areas 1, 2 and 3, the exclosures were positioned in four blocks, each block containing one plot of each treatment, giving a total of 12 blocks per area and 36 plots overall. Baseline vegetation composition data were recorded in 1997; all subsequent vegetation and soil sampling reported here was undertaken in September 2003, after 6 years.

Soil analysis

A soil sample, 10 cm in diameter, was taken from four random locations within each plot from a depth of 0–10 cm, depending on the depth of soil at each location. Samples were then combined to provide one sample of wet soil for analysis. Total extractable nitrate, total extractable ammonium, biologically available nitrogen, phosphorous, potassium and magnesium and pH were determined. For determination of nitrate, ammonium and available nitrogen, the samples were extracted in 2 M KCl and analysed using a colorimetric method; ammonium with an indophenol blue complex and nitrate with cadmium reduction and azo dye formation, both using a flow injection analyser. Nitrate nitrogen and ammonium nitrogen are given as mg kg−1 dry basis and available nitrogen is given as kg N ha−1. Available phosphorus was extracted with sodium bicarbonate ‘Olsens’ and given as mg L−1 on dry basis. Available potassium and available magnesium were extracted with ammonium nitrate and given as mg L−1 on dry basis.

Vegetation sampling

Vegetation height

Vegetation height was measured as the highest point at which vegetation touched a ruler placed vertically in the sward. Nine measurements were taken in each plot and the mean of these was used to estimate plot sward height.

Above-ground biomass

Above-ground biomass was harvested from four subplots of 0.25 × 0.25 m adjacent to the central 1 × 1 m plot within each exclosure to enable biomass (from a total area of 0.5 × 0.5 m) to be sampled without disturbing the central plot. Plant above-ground biomass was clipped at 2 cm above ground level. The biomass samples were sorted into groups prior to drying and the five main woody species at this site, U. europaeus, R. fruticosus agg., C. vulgaris, E. cinerea and R. pimpinellifolia were separated from all four subsamples per exclosure. The remaining non-woody biomass in two of the four subsamples was sorted into forb species, graminoids and bryophytes. The samples were then dried at 60 °C and weighed.

Below-ground biomass

Root biomass was harvested using a soil corer to collect soil from four randomly placed cores of 7 cm diameter and 5 cm depth from each exclosure. Five cm was the maximum depth that could be used because of the shallow nature of the soil across most of the site. The roots were washed with water to remove soil, and will have lost some fine roots in this process. They were then dried at 60 °C for 72 h and weighed.

Species composition

Species richness (presence of species in each plot recorded) was measured at the start of the experiment. Final species composition (6 years after application of grazing treatments) was measured as the percentage cover of all vascular plants and bryophytes (estimated by eye) in each experimental plot (centre 1 × 1 m of each exclosure). Nomenclature follows Stace (1997) for vascular plants and Smith (2004) for bryophytes.

Pellet count

The number of rabbit pellets in each grazed plot was counted in September 1998, 2001 and 2003. All pellets within the central 1 × 1 m plot were included.

Data analysis

All data excluding species cover data

Vegetation height, biomass and diversity data were analysed using a linear mixed-effect model fitted to the data by Restricted Maximum Likelihood, using the lme4 package in R (R Development Core Team, 2005). Fixed effects were treatment and its interaction with area, with block nested within area as a random effect. The results were summarized using an anova, and detailed post hoc (Tukey) tests were performed with the multcomp package in R. Rabbit pellet data were analysed using the above model with ungrazed plots removed from the analysis. For soil analysis and diversity, the effect of area alone was tested using a GLM, with pairwise comparisons of area × treatment undertaken using post hoc Tukey tests (Minitab 13.31; Minitab Ltd, Coventry, UK).

Species composition

The floristic data were analysed using multivariate analyses. Initially each data set was analysed using a detrended correspondence analysis, using Canoco for Windows (version 4.5) package (ter Braak & Šmilauer 2002). As the gradient lengths were short (<4.0 SD), subsequent analysis was undertaken using linear ordination methods (ter Braak & Šmilauer 2002): redundancy analysis (RDA) and principal components analysis (PCA). For all analyses, the species composition data were log-transformed (ln + 1) and standardized by sample norm.

Effects of grazing on species composition. Partial constrained RDAs were used to test whether the grazing treatments had a significant effect on species composition within each area. Significance was tested using restricted Monte Carlo permutation tests (499 permutations) with an appropriate randomization design. Permutations were restricted for a split-plot design (ter Braak & Šmilauer 2002); split plots (treatments) were freely permuted within whole plots (blocks). The significance of all canonical axes was tested together as generally the variability in species data (when constrained by environmental variables) is expressed by more than one canonical axis (Lepš & Smilauer 2003). The forward selection procedure in CANOCO was used to determine which treatments added significantly to the explanation of the observed species variance.

Relative contribution of grazing and soil to final species composition. To determine this, variance partitioning, a method to quantify the effects of two or more groups of ecologically distinct environmental variables (Lepš & Smilauer 2003), was used. The forward selection procedure in CANOCO was used to select a subset of soil properties that contributed to the explained variance (but were independent of each other) for inclusion in the ordination (Lepš & Smilauer 2003). These were soil pH, available magnesium, total nitrate and available phosphorus. Using a series of partially constrained ordinations on the floristic data (Borcard, Legendre & Drapeau 1992), the variation in these data was separated into four components; variation explained by (i) treatment alone, (ii) soil alone, (iii) these two factors combined and (iv) variation unexplained by either of these factors. All ordinations were tested with unrestricted Monte Carlo permutations (499 runs), with a Bonferroni-corrected significance level of 0.05/4 = 0.0125 (Borcard, Legendre & Drapeau 1992).

Diversity of species composition within and between the vegetation communities. To show how similar the plots are in species composition, an unconstrained analysis (PCA) was undertaken. In contrast to a constrained ordination (such as RDA), in a PCA the axes are not constrained by treatments, and hence the main variation in the species composition data (which may not be related to the treatments) is included (Lepš & Smilauer 2003). The environmental variables are then projected post hoc onto the ordination, giving an unbiased representation of the position of classes of samples (Lepš & Smilauer 2003). The significance of the first two principal components was tested using Parallel Analysis by generating 1000 artificial data sets (36 replicates of 58 variables) (Franklin et al. 1995). Each variable was independent and drawn from a standardized normal distribution.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Soil chemical properties

The three areas differed in fertility, pH and base ion concentration. The soils in Area 2 (thorny shrub-dominated area) and Area 3 (heather-dominated area) were more fertile than that in Area 1 (typical chalk heath area). Area 2 had significantly higher nitrate and total available nitrogen than the other two areas, whilst both Areas 2 and 3 had higher ammonium concentration (Table 1) than Area 1. Phosphorous levels did not differ between areas (Table 1). The soil was more base-rich (higher potassium, magnesium and pH) in Area 1 than in the other areas (Table 1). There was no significant effect of treatment on any of the measured soil variables (grazing, P > 0.05; grazing–area interaction, P > 0.05; for all variables).

Table 1.   Differences in measured soil variables between areas. Mean values for each area shown (±SE). +, data log-transformed. *P ≤ 0.05, ***P < 0.001, ns P > 0.05. Values not sharing common letters differ significantly
Soil variableArea 1Area 2Area 3F2,24P
Nitrate (mg kg−1)+1.15a (0.54)14.01b (2.93)0.98a (0.47)25.40***
Ammonium (mg kg−1)2.99a (0.47)15.18b (3.85)10.30b (3.59)4.04*
Available nitrogen (kg N ha−1)+8.27a (1.90)58.38b (12.37)22.56a (7.83)12.45***
Available phosphorus (mg L−1)+7.15 (0.28)7.33 (0.22)7.23 (0.18)0.20ns
Available potassium (mg L−1)+168.78a (17.33)61.73b (8.35)54.08b (5.00)33.91***
Available magnesium (mg L−1)+218.11a (8.59)106.13b (9.30)100.74b (8.48)39.95***
pH6.89a (0.12)4.67b (0.18)5.22b (0.21)43.14***

Vegetation structure and biomass

Vegetation height

Vegetation height was lowest in plots subjected to mixed grazing in all areas, was significantly higher in plots grazed by rabbits alone in Areas 2 and 3, and was greatest in the absence of grazing (Fig. 1) in all areas. Vegetation height was higher in Areas 2 and 3 (Fig. 1).

image

Figure 1.  Effect of grazing treatment on vegetation height (F2,36 = 102.33, < 0.001). Solid grey bar, mixed grazing; open bar, rabbit grazing only; hatched bar, no grazing. Error bars show ±SE. Bars not sharing common letters differ significantly (within-area comparisons only).

Download figure to PowerPoint

Above-ground biomass

Total above-ground biomass followed a similar pattern to height (Fig. 2c), although above-ground biomass was greater in Area 2 (F2,36 = 9.00, P = 0.001). The effect of grazing treatment was consistent across all areas. Examination of separate functional groups shows that woody species biomass (which forms the major part of the total biomass) responded in a similar direction to total biomass (Fig. 2a) in Areas 2 and 3, but there was no difference between the two grazed treatments. There was no effect of treatment on woody biomass in Area 1. In contrast, graminoid biomass responded positively to grazing removal in Area 1 but negatively in Areas 2 and 3 (Fig. 2b). There was a significant difference in graminoid biomass between mixed-grazed and rabbit-only grazed plots in Area 2. Non-woody forb biomass was unaffected by grazing treatment (grazing, P > 0.05; grazing–area interaction, P > 0.05).

image

Figure 2.  Comparison of the effects of grazing treatment on above-ground biomass of functional groups in each area: (a) woody species, (b) graminoids and (c) total biomass across all areas. Solid bars, mixed grazing; open bars, rabbit grazing only; hatched bars, no grazing. Error bars show ±SE. Bars not sharing common letters differ significantly (within-area comparisons only for (a) and (b)).

Download figure to PowerPoint

Ratio of below-ground to above-ground biomass

Overall, the ratio of below-ground to above-ground biomass decreased with grazer removal (Fig. 3). However, this response was much greater in Area 1 (Fig. 3), and in this area, the ratio was significantly different between the two grazing treatments.

image

Figure 3.  Effect of grazing treatment on ratio of below-ground to above-ground biomass in each area (grazing, F2,36 = 20.75, < 0.001; grazing–area interaction, F4,36 = 5.6, < 0.01). Solid bar, mixed grazing; open bar, rabbit grazing only; hatched bar, no grazing. Error bars show ±SE. Bars not sharing common letters differ significantly (within-area comparisons only).

Download figure to PowerPoint

Species composition

Effects on diversity

At the start of the experiment (year 0), there was no difference in species richness between the grazing treatments (F2,36 = 0.65, P > 0.05). As expected, the typical chalk heath area (Area 1) had greater initial species richness than the areas dominated by thorny shrubs (Area 2) and heather (Area 3) (F2,36 = 40.92, < 0.001). This difference was still present after 6 years of the experiment, with Area 1 having the highest species diversity (F2,36 = 9.272, = 0.001), total species richness (F2,36 = 35.92, < 0.001) and richness of graminoids (F2,36 = 29.64, < 0.001), non-woody forbs (F2,36 = 39.48, < 0.001) and bryophytes (F2,36 = 9.55, = 0.001). Woody species richness was higher in Areas 2 and 3 (F2,36 = 14.80, < 0.001). After 6 years, grazing treatment had an impact on species richness and diversity within each area (Table 2). Grazing removal reduced species diversity, total species richness and species richness of non-woody forbs and woody species in all areas (Table 2). Mixed grazing and grazing by rabbits alone maintained the same level of species richness and diversity in each area, except for woody species (which had greater richness in mixed-grazed plots) (Table 2). The response of graminoid species richness to grazing treatment and was not consistent across areas and in Area 2 was lower in rabbit-grazed plots than in mixed-grazed plots (Fig. 4).

Table 2.   Response of species diversity and richness to grazing treatment (d.f. for grazing is 2,36; no significant interaction between treatment and area for any response variable; *P 0.05, ***P < 0.001)
 GrazingMean (±SE) for each treatment
FPMixed grazingRabbit-only grazingNo grazing
  1. Values not sharing common letters differ significantly.

Species diversity20.70***2.15a (±0.14)2.00a (±0.18)1.15b (±0.24)
Species richness
 Total17.23***16.92a (±2.19)16.33a (±2.45)9.50b (±2.32)
 Non-woody forbs12.65***7.67a (±1.30)7.25a (±1.66)3.75b (±1.33)
 Woody species3.94*3.17a (±0.24)3.00ab (±0.33)2.42b (±0.26)
image

Figure 4.  Effect of grazing treatment on graminoid species richness M−2. Solid grey bar, mixed grazing; open bar, rabbit grazing only; hatched bar, no grazing. Error bars show ±SE. Bars not sharing common letters differ significantly (within-area comparisons only).

Download figure to PowerPoint

Effects on species composition

Grazing treatment had a significant effect on species composition in each area (Area 1, F = 2.349, < 0.05; Area 2, F = 2.264, < 0.05; Area 3, F = 2.74, < 0.01). In all areas, the primary gradient in the data (Axis 1) is associated with grazing removal, separating the grazed from the ungrazed plots (Fig. 5a–c). In Areas 1 and 3, only grazing removal contributed significantly to the explained species variance, showing that there was little difference in overall composition between the two grazing treatments. However, in Area 2, all treatments contributed significantly.

image

Figure 5.  Results of RDA ordination on final species composition data (see text for details). Separate species–environment biplot shown for each area. Data standardized and scaled for interspecies distance with environmental variables (grazing treatments) displayed as centroids. Species with >20% fit shown. Percentage of variation in the species composition data explained by axes 1 and 2: (a) 28.1 + 5.4 (33.5%), (b) 28.5 + 9.5 (38.0%) and (c) 24.6 + 13.2 (37.8%). Mixed = mixed grazing, Rabbit = rabbit grazing only, None = no grazing. Species abbreviations: Ac Asperula cynanchica, Am Achillea millefolium, Asp Agrostis spp., Be Bromopsis erecta, Bp Bellis perennis, Cc Carex caryophyllea, Cf Carex flacca, Cv Calluna vulgaris, Dd Danthonia decumbens, Dg Dactylis glomerata, Ds Dicranum scoparium, Ec Erica cinerea, Fsp Festuca spp., Gs Galium saxatile, Hl Holcus lanatus, Hpr Helictotrichon pratense, Hpul Hypericum pulchrum, Hr Hypochaeris radicata, Km Koeleria macrantha Lc Lotus corniculatus, Lh Leontodon hispidus, Pe Potentilla erecta, Prv Prunella vulgaris, Rf Rubus fruticosus agg., Sj Senecio jacobaea, Sm Sanguisorba minor, Sp Scleropodium purum, To Taraxacum officinale agg., Ts Teucrium scorodonia, Tsp Thymus spp., Ue Ulex europaeus, Vc Veronica chamaedrys, Vo Veronica officinalis, Vsp Viola spp.

Download figure to PowerPoint

The species most responsive to grazing removal in all areas was the woody shrub U. europaeus (positively associated with Axis 1) (Fig. 5a–c). In contrast, the woody shrubs R. fruticosus agg. in Area 3, C. vulgaris in Areas 1 and 3 and E. cinerea in Area 2, responded negatively to grazing removal (negatively associated with Axis 1).

All graminoids were negatively associated with grazing removal in Areas 2 and 3, but in Area 1 a few species had higher abundance in ungrazed plots; Helictotrichon pratensis, Bromopsis erecta and Dactylis glomerata. Some species, such as Festuca spp., the most abundant grasses at this site, showed the same direction of response (decreasing in the absence of grazing) in all areas. Dactylis glomerata, however, showed an inconsistent response to grazing treatment, having highest abundance in ungrazed plots in Area 1 and in mixed-grazed plots in Area 2 (Fig. 5a and b). As with graminoids, non-woody forbs only responded positively to grazing removal in Area 1 (Fig. 5a). All of the non-woody forb species that increased with grazing removal are either relatively tall compared with other species in this habitat (Achillea millefolium, Lotus corniculatus) or have a climbing habit (Galium saxatile). Smaller forbs, such as Asperula cynanchica, Bellis perennis and Prunella vulgaris had higher abundance in grazed than in ungrazed plots in Area 1, whereas all non-woody forbs (tall and short) had higher abundance in grazed than in ungrazed plots in Areas 2 and 3 (Fig. 5b and c).

In Area 2, rabbit-only grazed plots were more similar in species composition to ungrazed plots than mixed-grazed plots (Fig. 5b) with the woody species U. europaeus and the bryophytes Dicranum scoparium and Scleropodium purum positively associated with these plots. The main difference between the ungrazed and rabbit-only grazed plots was a higher abundance of bryophytes in the latter. In contrast, S. purum decreased after grazing removal in Areas 1 and 3 (Fig. 5a and c).

Relative contribution of grazing treatment to species composition

Variance partitioning analysis was used to determine the relative contributions of grazing treatment and soil properties to final species composition (after 6 years of the experiment). Both grazing treatment and soil were found to contribute significantly to final species composition, together explaining over half (52.6%) of the total variation in the floristic data (= 5.36, < 0.01). Grazing treatment explains 9.2% of total variation (= 2.82, < 0.01) with soil explaining a much greater proportion, 42.1% (= 42.10, < 0.01) and grazing and soil together 1.3%.

The consequence of this finding for vegetation heterogeneity between and within areas is shown in the results from a PCA on the final composition data (Fig. 6). This diagram shows that whether or not grazing is present, the plots in Area 1 are separated from those in Areas 2 and 3. As shown by the variance partitioning, soil is the major factor influencing species composition and this primary split in the data is associated with the amount of soil nitrogen (and ammonium and nitrate), K, Mg and soil pH. The second axis is associated with grazing removal; ungrazed plots in Area 1 are separated from grazed plots but there is little difference in composition between mixed-grazed and rabbit-only grazed plots. This similarity between grazed plots is also present in Area 3. However, in Area 2, plots from all treatments are distinct and rabbit-only grazed plots are more similar to ungrazed plots in Area 3 than to grazed plots. There are some differences in species response between this PCA diagram (Fig. 6) and the constrained ordination (Fig. 5a–c), demonstrating the importance of distinguishing between constrained and unconstrained ordinations when interpreting such analyses. For instance, Festuca spp. and Viola spp. are shown as being associated with mixed grazing in Areas 2 and 3 in Fig. 5 (constrained ordination), but with grazed plots in Area 1 in Fig. 6 (unconstrained ordination). Although these species increased in abundance in Areas 2 and 3 in response to grazing (Fig. 5), overall their cover was highest in Area 1 (Festuca spp.: F2,51 = 71.10, < 0.001; Viola spp.: F2,51 = 40.49, < 0.001).

image

Figure 6.  Results from PCA ordination of final species composition (see text for details). Experimental treatments and soil data displayed as supplementary variables (species–supplementary variable biplot). Data standardized and scaled for intersample distance, species with >50% fit shown. Arrows represent the soil variables and centroids represent the average species composition of all of the plots of each grazing treatment in each area. As the diagram is scaled for intersample distance, the proximity of centroids implies similarity of species composition (Lepš & Smilauer 2003). Axes 1 and 2 explain 54.8% and 43.8 + 11.0, respectively, of the variation in the species composition data. Eigenvalues for axes 1 and 2 are 0.44 and 0.11, respectively, and both axes are significant P < 0.001. Nominal environmental variables (area × treatment interactions) displayed as centroids, Mix = mixed grazing, Rab = rabbit grazing only, Non = no grazing, A1 = Area 1, A2 = Area 2, A3 = Area 3. Continuous variables (soil data) shown as arrows, nitrN = nitrate, AmmN = ammonium, = total available nitrogen, P = available phosphorous, K = available potassium, Mg = available Mg. Species abbreviations: Am Achillea millefolium, Cv Calluna vulgaris, Cf Carex flacca, Ec Erica cinerea, Fsp Festuca spp., Fv Filipendula vulgaris, Gs Galium saxatile, Hpr Helictotrichon pratense, Km Koeleria macrantha, Lc Lotus corniculatus, Lh Leontodon hispidus, Pe Potentilla erecta, Pl Plantago lanceolata, Po Pilosella officinarum, Prv Prunella vulgaris, Rf Rubus fruticosus agg., Sm Sanguisorba minor, Ts Teucrium scorodonia, Tsp Thymus spp., Ue Ulex europaeus, Vsp Viola spp.

Download figure to PowerPoint

Rabbit pellet count

In the early stages of the experiment, rabbit pellet counts did not differ between mixed-grazed plots and rabbit-only grazed plots (Fig. 7) or between Areas (post hoc Tukey tests, > 0.05). However, after 6 years of exclosure, there were fewer pellets in rabbit-only grazed plots than in mixed-grazed plots (treatment, F2,36 = 20.56, < 0.01) (Fig. 7).

image

Figure 7.  Differences in the mean number of rabbit pellets in the grazed plots (±SE), based on single counts in 1998, 2001 and 2003. Solid grey bars, mixed grazing; open bars, rabbit grazing only. The asterisk indicates a significant difference between the grazing treatments.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Are top-down (grazing) effects on different plant functional groups consistent across vegetation types?

After 6 years of an exclosure experiment, grazing had a positive effect on diversity in all areas by reducing the dominance of the main functional group, despite the differences in soil properties and species composition between the areas. Without top-down control from grazing, the main functional group in each area (graminoids in the area of low fertility and woody species in the more fertile areas) increased in above-ground biomass, leading to a decrease in total species diversity and richness. However, not all species within the dominant groups showed the same response to top-down control, and although woody dominance increased with grazing removal, this was due mainly to an increase in U. europaeus whilst other woody shrubs tended to decline, decreasing overall woody species richness. In the area of low fertility, there was a similar negative relationship between graminoid dominance and graminoid species richness, as the greater above-ground biomass in ungrazed plots resulted from an increase in a few dominant grasses such as Helictotrichon pratense and Bromopsis erecta. As each vegetation type was only represented by a single area in our experiment, we must apply some caution in making generalizations about the different responses of the vegetation in each area, but we believe the different responses we observed are informative.

Although grazing reduced the dominance of the main plant functional group in each area, this result reflects different responses to grazing by plant functional groups in each of the areas (Pakeman 2004). For instance, graminoid biomass only increased with grazing removal in the area where it was dominant and actually decreased with grazing removal in the more fertile, acidic areas. In these areas, woody species were dominant and prevented graminoid abundance from increasing in response to grazing removal. Therefore by influencing the dominant plant functional group, soil properties (nutrient richness and pH) can have an indirect effect on the responses of other functional groups to grazing.

The below-ground to above-ground biomass ratio decreased with the removal of grazing, most significantly in Area 1, which had the lowest above-ground biomass and where the above-ground biomass responded least to grazing. Other studies have found that grazing can have negative (Holland & Detling 1990), positive (Sims & Singh 1978) or little effect on root biomass, in either the short- (months) or long-term (years) (McNaughton, Banyikwa & McNaughton 1998), but that generally positive responses dominate (Milchunas & Lauenroth 1993). Our understanding of such responses is at an early stage.

Are rabbits functionally equivalent to larger grazing herbivores when these are excluded?

Grazer effects were found to be dependent upon herbivore assemblage, as rabbits were not able to completely functionally replace larger grazers in this system. Removal of large herbivores, allowing rabbit grazing only, led to an increase in vegetation height and above-ground biomass. However, rabbits were able to maintain species diversity and richness in all areas (Olofsson, de Mazancourt & Crawley 2008), suggesting a partial replacement of the role of larger herbivores. In Areas 1 and 3, the species composition of the plots grazed by the different assemblages was also similar. However, in Area 2, the most nutrient-rich area, the grazed plots became less similar in species composition than those in Areas 1 and 3. This was a result of less difference between rabbit-only grazed plots and ungrazed plots in this area (as a result of an increase in U. europaeus), implying that in this area, rabbit grazing could not compensate for the removal of large herbivores.

Grazing compensation can occur where herbivores consume similar plant species and therefore an increase in the consumption by one herbivore species can offset the removal of another (e.g. Bakker et al. 2004). In this study, rabbit use of rabbit-only grazed plots, estimated from pellet counts, was reduced after 6 years of grazing treatment. Pellet counts are a reliable indicator of rabbit density and thus grazing pressure (Wood 1988; Kolb 1991; Diaz 1998; Palomares 2001). However, our results indicate that rabbit grazing pressure has not increased in rabbit-only grazed plots and is unable to offset the removal of large herbivores.

Grazing pressure might not increase in response to the removal of another herbivore, if animals cannot increase consumption, e.g. because they are not competing for the same food source, or because individuals are limited in movement by factors such as territorial behaviour or predation risk. If facilitation occurs between herbivores, for instance ‘feeding facilitation’ (one species stimulates vegetation re-growth and improves the forage quality available to another species (van der Wal et al. 2000)), or ‘habitat facilitation’ (one species increases access to forage by altering habitat structure (Arsenault & Owen-Smith 2002)), then grazing pressure will also decrease in the absence of the facilitator, as was demonstrated by Bakker et al. (2004).

Rabbits are able to manipulate thorny plants (Belovsky et al. 1991), they can therefore graze U. europaeus (Bhadresa 1982) and control its abundance as they did on this site prior to the myxomatosis outbreak. However, once U. europaeus reaches a certain height, rabbits are unlikely to cause serious grazing damage to it (Mellanby 1968), whereas ruminants are able to consume such older growth and also break branches by feeding and trampling (Welch 1984). ‘Feeding facilitation’ by large herbivores may hence improve forage quality and access to rabbits. Furthermore, rabbits show a strong preference for shorter swards as they can spend longer foraging and less time scanning for predators (Iason et al. 2002), unlike sheep which are less influenced by sward height (Clarke, Welch & Gordon 1995). Rabbits tend to be restricted to grass-dominated habitats (Hulbert, Iason & Racey 1996; Fa, Sharples & Bell 1999), but avoid tall grass. Thus, both feeding facilitation and habitat facilitation for rabbits, by larger herbivores, are occurring at this site. We thus assume that both facilitation mechanisms are more important in woody shrub-dominated areas, and this may explain why rabbit grazing alone has least impact in the thorny shrub-dominated area. Such facilitation interactions are likely to be highly dynamic and change as time and the impact of the treatments progress. Kuijper et al. (2007) found that similar interactions between cattle and hares changed over a 30-year time span as the vegetation continued to respond to grazer removal.

How do top-down (grazing) impacts interact with bottom-up (soil properties) impacts in this community?

Despite the impact of grazing on vegetation at this site, both at present and historically (e.g. Thomas 1960, 1963), bottom-up factors (including soil fertility and pH) are dominant in determining species composition at local scales (cf. Ehrenfeld et al. 1997). Soil properties explain 42% of the variation in floristic data, and each vegetation community is characterized by a different combination of soil properties, such as pH and fertility. In both the presence and absence of grazing, the plots in the area of high pH and low fertility are distinct in their species composition from the plots in the more nutrient-rich and acidic areas.

Grazing is known to influence soil properties, particularly soil fertility, which is often increased by mammalian herbivores (Frank & Groffman 1998; Augustine, McNaughton & Frank 2003). In addition, grazing may increase or decrease the effects of soil properties on plant species composition. Gibson (1988) found a stronger relationship between soil heterogeneity and plant spatial patterns in ungrazed vegetation than in vegetation grazed by sheep. Similarly, in studies of rabbit grazing on different types of grass heath, ungrazed plots showed large differences in vegetation composition whereas rabbit-grazed plots were more alike (Tansley 1922; Watt 1957). However, Bakker (1985) showed that grazing could increase the influence of soil on vegetation, as in the absence of herbivory a single species became dominant and masked small underlying differences in soil properties. Similarly at Lullington, ungrazed plots in the more fertile and acidic areas have become more similar with time because of the dominance of U. europaeus. Although the current vegetation heterogeneity is largely determined by soil properties, the role of grazing in maintaining this heterogeneity is likely to become more important with time.

Although the primary determinants of composition at this site are bottom-up factors, herbivores maintain the short species-rich vegetation by reducing competition by taller species such as U. europaeus. This effect is greatest where soil fertility is high and the vegetation is potentially dominated by woody species. In these areas, absence of grazing leads rapidly (within 6 years) to domination by U. europaeus and reduction in species richness. This creates a positive feedback loop as U. europaeus further increases soil fertility and leads to reduced rabbit grazing; thus grazing by large herbivores becomes even more important as a top-down controller of this species.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Vegetation composition, species richness and biomass at this site are determined by interactions between the top-down effects of herbivory and bottom-up impacts of soil nutrient availability and pH. We found that whilst the top-down impacts (grazing) consistently increased species richness across vegetation types, the response of different plant functional groups to grazing was soil dependent. Rabbits were only partially functionally equivalent to larger grazing herbivores when these were excluded because rabbit grazing pressure did not increase in plots that were ungrazed by large herbivores. This suggests that there is a facilitative relationship between large and small herbivores, with large herbivores improving forage quality and increasing access to plots for rabbits. Despite the large impact of grazing at this site, bottom-up (soil properties) effects had greater impacts on vegetation than the grazers over the 6-year time-scale of this experiment. However, in areas of higher fertility, the correlation between soil properties and vegetation composition may be strengthened by grazing, as grazing prevents the homogenizing dominance of U. europaeus and maintains the difference in species composition between the areas.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

This field experiment was set-up in 1997 by Audra Hurst with the support of Malcolm Emery (Natural England) and has since then benefited from the help of many others including Hilary Orrom and Katherine Bass. We appreciated constructive comments on the manuscript from Robin Pakeman, Rob Marrs and two anonymous referees, assistance with data analysis from Jonathan Yearsley and suggestions on data presentation from Clare de Mazancourt and the members of the Ecology discussion group at the University of Sussex.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  • Alonso, L., Hartley, S.E. & Thurlow, M. (2001) Competition between heather and grasses on Scottish moorlands: interacting effects of nutrient enrichment and grazing regime. Journal of Vegetation Science, 12, 249260.
  • Arsenault, R. & Owen-Smith, N. (2002) Facilitation versus competition in grazing herbivore assemblages. Oikos, 97, 313318.
  • Augustine, D.J., McNaughton, S.J. & Frank, D.A. (2003) Feedbacks between soil nutrients and large herbivores in a managed savanna ecosystem. Ecological Applications, 5, 13251337.
  • Bagchi, S., Namgail, T. & Ritchie, M.E. (2006) Small mammalian herbivores as mediators of plant community dynamics in the high-altitude arid rangelands of Trans-Himalaya. Biological Conservation, 127, 438442.
  • Bakker, J.P. (1985) The impact of grazing on plant communities, plant populations and soil conditions on salt marshes. Vegetatio, 62, 391398.
  • Bakker, J.P., De Bie, S., Dallinga, J.H., Tjaden, P. & De Vries, Y. (1983) Sheep-grazing as a management tool for heathland conservation and regeneration in the Netherlands. Journal of Applied Ecology, 20, 541560.
  • Bakker, E.S., Olff, H., Boekhoff, M., Gleichman, J.M. & Berendse, F. (2004) Impact of small herbivores on nitrogen cycling: contrasting effects of small and large species. Oecologia, 138, 91101.
  • Bakker, E.S., Ritchie, M.E., Milchunas, D.G. & Knops, J.M.H. (2006) Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecology Letters, 9, 780788.
  • Belovsky, G.E., Schmitz, O.J., Slade, J.B. & Dawson, T.J. (1991) Effects of spines and thorns on Australian arid zone herbivores of different body masses. Oecologia, 88, 521528.
  • Bhadresa, R. (1982) Plant-rabbit interactions on a lowland heath. PhD Thesis, King’s College, University of London, London.
  • Bobbink, R., Hornung, M. & Roelofs, J.G.M. (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology, 86, 717738.
  • Bobbink, R. & Willems, J.H. (1993) Restoration management of abandoned chalk grassland in the Netherlands. Biodiversity and Conservation, 2, 616626.
  • Bokdam, J. & Gleichman, J.M. (2000) Effects of grazing by free-ranging cattle on vegetation dynamics in a continental north-west European heathland. Journal of Applied Ecology, 37, 415431.
  • Borcard, D., Legendre, L. & Drapeau, P. (1992) Partialling out the spatial component of ecological variation. Ecology, 73, 10451055.
  • Bowers, M.A. (1993) Influence of herbivorous mammals on an old-field plant communtiy: years 1-4 after disturbance. Oikos, 67, 129141.
  • Ter Braak, C.J.F. & Šmilauer, P. (2002) CANOCO Reference manual and CanoDraw for Windows User’s guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, NY.
  • Bridle, K.L. & Kirkpatrick, J.B. (1999) Comparative effects of stock and wild vertebrate herbivore grazing on treeless subalpine vegetation, Eastern Central Plateau, Tasmania. Australian Journal of Botany, 47, 817834.
  • Bullock, J.M. & Pakeman, R.J. (1996) Grazing of lowland heath in England: management methods and their effects on heathland vegetation. Biological Conservation, 79, 113.
  • Cid, M.S., Detling, J.K., Whicker, A.D. & Brizuela, M.A. (1991) Vegetational responses of a mixed-grass prairie site following exclusion of prairie dogs and bison. Journal of Range Management, 44, 100105.
  • Clarke, J.L., Welch, D. & Gordon, I.J. (1995) The influence of vegetation patterns on the grazing of heather moorland by red deer and sheep. I. The location of animals on grass/heather mosaics. Journal of Applied Ecology, 32, 166176.
  • Critchley, C.N.R., Chambers, B.J., Fowbert, J.A., Sanderson, R.A., Bhogal, A. & Rose, S.C. (2002) Association between lowland grassland plant communities and soil properties. Biological Conservation, 105, 199215.
  • Demment, M.W. & Van Soest, P.J. (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. American Naturalist, 125, 641671.
  • Denyer, J.L., Hartley, S.E. & John, E.A. (2007) Small mammalian herbivore determines vegetation response to patchy nutrient inputs. Oikos, 116, 11861192.
  • Diaz, A. (1998) Comparison of methods for measuring rabbit incidence on grasslands. Mammalia, 62, 205212.
  • Dolman, P.M. & Sutherland, W.J. (1992) The ecological changes of Breckland grass heaths and the consequences of management. Journal of Applied Ecology, 29, 402413.
  • Ehrenfeld, J.G., Han, X., Parsons, W.F.J. & Zhu, W. (1997) On the nature of environmental gradients: temporal and spatial variability of soils and vegetation in the New Jersey Pinelands. Journal of Ecology, 85, 785798.
  • Fa, J.E., Sharples, C.M. & Bell, D.J. (1999) Habitat correlates of European rabbit (Oryctolagus cuniculus) distribution after th.e spread of RVHD in Cadiz Province, Spain. Journal of the Zoological Society of London, 249, 8396.
  • Frank, D.A. & Groffman, P.M. (1998) Ungulate vs landscape control of soil C and N processes in grasslands of Yellowstone National Park. Ecology, 79, 22292241.
  • Franklin, S.B., Gibson, D.J., Robertson, P.A., Pohlmann, J.T. & Fralish, J.S. (1995) Parallel analysis: a method for determining significant principal components. Journal of Vegetation Science, 6, 99106.
  • Gibson, D.J. (1988) The relationship of sheep grazing and soil heterogeneity to plant spatial patterns in dune grassland. Journal of Ecology, 76, 233252.
  • Grubb, P.J., Green, H.E. & Merrifield, R.C.J. (1969) The ecology of chalk heath: its relevance to the calcicole-calcifuge and soil acidification problems. Journal of Ecology, 57, 175212.
  • Grubb, P.J. & Suter, M.B. (1971) The mechanism of acidification of soil by Calluna and Ulex and the significance for conservation. The Scientific Management of Animal and Plant Communities for Conservation, 11th Symposium of the British Ecological Society (eds E.Duffey & A.S.Watt), pp. 115133. Blackwell Scientific Publications, Oxford.
  • Hartley, S.E. & Mitchell, R.J. (2005) Manipulation of nutrients and grazing levels on heather moorland: changes in Calluna dominance and consequences for community composition. Journal of Ecology, 93, 9901004.
  • Holland, E.A. & Detling, J.K. (1990) Plant response to herbivory and belowground nitrogen cycling. Ecology, 71, 10401049.
  • Huisman, J., Grover, J.P., Van Der Wal, R. & Van Andel, J. (1997) Competition for light, plant-species replacement and herbivore abundance along productivity gradients. Herbivores: Between Plants and Predators (eds H.Olff, V.K.Brown & R.H.Drent), pp. 239269. Blackwell Science, Oxford.
  • Hulbert, I.A.R., Iason, G.R. & Racey, P.A. (1996) Habitat utilization in a stratified upland landscape by two lagomoprhs with different feeding strategies. Journal of Applied Ecology, 33, 315324.
  • Iason, G.R., Manso, T., Sim, D.A. & Hartley, F.G. (2002) The functional response does not predict the local distribution of European Rabbits (Oryctolagus cuniculus) on grass swards: experimental evidence. Functional Ecology, 16, 394402.
  • Jenny, H. (1941) Factors of Soil Formation A System of Quantitative Pedology. McGraw-Hill, New York. Accessed as the 1994 Dover Publications Inc, New York, edition at http://soilandhealth.org/.
  • John, E.A. & Turkington, R. (1995) Herbaceous vegetation in the understorey of the boreal forest: does nutrient supply or snowshoe hare herbivory regulate species composition and abundance? Journal of Ecology, 83, 581590.
  • Kolb, H.H. (1991) Use of burrows and movements by wild rabbits (Oryctolagus cuniculus) on an area of sand dunes. Journal of Applied Ecology, 28, 879891.
  • Kuijper, D.P.J. & Bakker, J.P. (2005) Top-down control of small herbivores on salt-marsh vegetation along a productivity gradient. Ecology, 86, 914923.
  • Kuijper, D.P.J., Nijhoff, D.J. & Bakker, J.P. (2004) Herbivory and competition slow down invasion of a tall grass along a productivity gradient. Oecologia, 141, 452459.
  • Kuijper, D.P.J., Beek, P., Van Wieren, S.E. & Bakker, J.P. (2007) Time-scale effects in the interaction between a large and a small herbivore. Basic and Applied Ecology, 9, 126134.
  • Lepš, J. & Smilauer, P. (2003) Multivariate Analysis of Ecological Data using CANOCO. Cambridge University Press, Cambridge.
  • Lorenzo, M., Scotton, M., Klimek, S., Isselstein, J. & Pecile, A. (2007) Effect of local factors on plant species richness and composition of Alpine meadows. Agriculture, Ecosystems and Environment, 119, 281288.
  • Loucougaray, G., Bonnis, A. & Bouzille, J.-B. (2004) Effects of grazing by horses and/or cattle on the diversity of coastal grasslands in western France. Biological Conservation, 116, 5971.
  • Marrs, R.H. (1993) Soil fertility and nature conservation in Europe: theoretical considerations and practical management solutions. Advances in Ecological Research, 24, 241300.
  • McNaughton, S.J., Banyikwa, F.F. & McNaughton, M.M. (1998) Root biomass and productivity in a grazing ecosystem: the Serengeti. Ecology, 79, 587592.
  • Mellanby, K. (1968) The effects of some mammals and birds on regeneration of oak. Journal of Applied Ecology, 5, 359366.
  • Milchunas, D.G. & Lauenroth, W.K. (1993) Quantitative effects of grazing on vegetation and soils over a global range of environments. Ecological Monographs, 63, 327366.
  • Olff, H. & Ritchie, M.E. (1998) Effects of herbivores on grassland plant diversity. Trends in Ecology and Evolution, 13, 261265.
  • Olofsson, J., De Mazancourt, C. & Crawley, M.J. (2008) Spatial heterogeneity and plant species richness at different spatial scales under rabbit grazing. Oecologia, 156, 825834.
  • Pakeman, R.J. (2004) Consistency of plant species and trait responses to grazing along a productivity gradient: a multi-site analysis. Journal of Ecology, 92, 893905.
  • Pakeman, R.J., Hulme, P.E., Torvell, L. & Fisher, J.M. (2003) Rehabilitation of degraded dry heather [Calluna vulgaris (L.) Hull] moorland by controlled sheep grazing. Biological Conservation, 114, 389400.
  • Palomares, F. (2001) Comparison of 3 methods to estimate rabbit abundance in a Mediterranean environment. Wildlife Society Bulletin, 29, 578585.
  • Proulx, M. & Mazumder, A. (1998) Reversal of grazing impact on plant species richness in nutrient poor vs. nutrient-rich ecosystems. Ecology, 79, 25812592.
  • Putman, R.J., Fowler, A.D. & Tout, S. (1991) Patterns of use of ancient grassland by cattle and horses and effects on vegetational composition and structure. Biological Conservation, 56, 329347.
  • R Development Core Team (2005) R: A Language and Environment for Statistical Computing, 2.2.1 edn. R Foundation for Statistical Computing, Vienna, Austria.
  • Sims, P.L. & Singh, J.S. (1978) The structure and function of ten western North American grasslands II. Intra seasonal dynamics in primary producer compartments. Journal of Ecology, 66, 547572.
  • Smith, A.J.E. (2004) The Moss Flora of Britain and Ireland, 2nd edn. Cambridge University Press, Cambridge.
  • Smith, R., Bokdam, J., Den Ouden, J., Olff, H. & Schot-Opschoor, H. (2001) Effects of introduction and exclusion of large herbivores on small rodent communities. Plant Ecology, 155, 119127.
  • Stace, C.A. (1997) New Flora of the British Isles, 2nd edn. Cambridge University Press, Cambridge.
  • Stahl, J., Van der Graaf, A.J., Drent, R.H. & Bakker, J.P. (2006) Subtle interplay of competition and facilitation among small herbivores in coastal grasslands. Functional Ecology, 20, 908915.
  • Tansley, A.G. (1922) Studies of the vegetation of the English chalk. II. Early stages of redevelopment of woody vegetation on chalk grassland. Journal of Ecology, 10, 168177.
  • Thomas, A.S. (1960) Changes in vegetation since the advent of myxomatosis. Journal of Ecology, 48, 287306.
  • Thomas, A.S. (1963) Further changes in vegetation since the advent of myxomatosis. Journal of Ecology, 51, 151183.
  • Van Der Wal, R., Van Winjen, H., Van Wieren, S.E., Beucher, O. & Bos, D. (2000) On facilitation between herbivores: how brent geese profit from brown hares. Ecology, 81, 969980.
  • Watt, A.S. (1957) The effect of excluding rabbits from Grassland B (Mesobrometum) in Breckland. Journal of Ecology, 45, 861878.
  • Welch, D. (1984) Studies in the grazing of heather moorland in north-east Scotland. II. Response of heather. Journal of Applied Ecology, 21, 197207.
  • Wood, D.H. (1988) Estimating rabbit density by counting dung pellets. Australian Wildlife Research, 15, 665671.
  • Zeevalking, H.J. & Fresco, L.F.M. (1977) Rabbit grazing and species diversity in a dune area. Vegetatio, 35, 193196.