Vegetation changes over time
Complicating any vegetation responses to grazing treatment were the large changes in diversity over the whole grassland between 1990–91 and 1998: a 67% increase in species number per paddock and an 80% increase in the log normal diversity in the point quadrat survey. Such increases might be expected in extensified grasslands, where species number can increase rapidly after cessation of fertilizer inputs (Olff & Bakker 1991; Mountford, Lakhani & Holland 1996) as a result of declines in soil fertility and therefore productivity (Olff, Berendse & de Visser 1994). We found no declines over 12 years in the few nutrients measured, although the change in nitrogen, probably the limiting nutrient in such grasslands (Olff, Berendse & de Visser 1994), was not measured.
Despite these changes in species number per paddock, we found only 10 new species in the grassland since the 1990–91 surveys, including three sown by Tofts (1998). Furthermore, these new species were rare, having a total frequency of 0·3% in the point quadrat survey. Bullock et al. (1994a) suggested that colonization of the grassland at this site by new species would be slow because the seed bank and seed rain contained no species not already found in the vegetation. Therefore, while high soil fertility may be an important inhibitor of grassland diversification (Marrs 1993), dispersal limitation may also play a major role. The fact that three (Leontodon hispidus, Trifolium dubium, Cirsium eriophorum) of four (the fourth was Rumex obtusifolius) species artificially introduced by Tofts (1998) have established in the grassland supports this conclusion.
Community change was manifest mostly as increases or decreases in the abundance of the dominant species. Lolium perenne was still dominant, but nearly halved in abundance. It, and the second dominant Agrostis stolonifera, were generally replaced by other grasses. The greatest increases were by Cynosurus cristatus, Festuca rubra and Trisetum flavescens, finer grasses that, along with the increase in dicots, indicate change towards a plant community typical of slightly less fertile conditions (NVC MG6c Lolium perenne–Cynosurus cristatus grassland, Trisetum flavescens subcommunity; Rodwell 1992) and away from the community dominated by vigorous, agriculturally desirable, grasses that was present at the start of the experiment (NVC MG7 Lolium perenne ley). However, the grassland is still a long way short of dicot-rich diverse grassland (NVC MG5 Cynosurus cristatus–Centaurea nigra grassland or MG6 Lolium perenne–Cynosurus cristatus grassland) that may have been typical on these circum-neutral soils before the advent of intensive farming practises.
Grazing treatment effects over time
Comparison of the 1990–91 surveys with those in 1998 suggests that, to understand fully vegetation responses to grazing, it is important to continue experiments over a long period. Treatment effects in the point quadrat survey nearly tripled between 1990 and 1998 and had increased in significance; for example, nine were significant at P < 0·001 in 1998 compared with none in 1990. Furthermore, more species were affected by treatments in 1998, 17 compared with eight in 1990. The changes between the two surveys were caused mostly by strengthening of effects found in 1990 and emergence of new effects in 1998. However, five of 11 effects found in the 1990 point quadrat survey and four of nine in the 1991 dicot survey were lost in 1998. These discontinuities and the large number of new responses meant that vegetation responses in 1990 were poor predictors of responses in 1998, as shown by the poor correlations between the 1990 and 1998 grazing ratios.
We cannot predict when vegetation in the different paddocks will cease exhibiting new treatment effects over time, i.e. when treatment effects will stabilize. Hill, Evans & Bell (1992) reported on exclosure experiments in Welsh hill pastures that had lasted up to 33 years and found that, although most major changes occurred in the first 7 years, the vegetation continued changing throughout the recording period. However, ungrazed grassland undergoes succession to shrub-dominated vegetation, whereby there is a large change in species composition. Changes in response to different grazing intensities will be less profound and may therefore stabilize more rapidly.
The data presented are not a long time series, but from two points in time. It may be dangerous to assume that treatment responses in 1998 represent a gradual evolution since 1990–91. There is evidence that year-to-year fluctuations in plant communities can be large (Ward & Jennings 1990; Dodd et al. 1995), so an extreme scenario may be that differences between 1998 and 1990–91 represent variation around a mean that has stayed constant over the years. However, the great change over the whole grassland (see above) and the large increase in treatment effects suggest we are seeing a true time trend, although some individual species’ responses may be transitory. This conclusion is supported by the fact that surveys of frequencies in two 1-m2 quadrats per paddock showed increases in the number of treatment effects over time between 1986, 1987, 1989 and 1993 (Watt, Treweek & Woolmer 1996; Treweek, Watt & Hambler 1997). Furthermore, as found in the Park Grass experiment (Tilman et al. 1994), although there may be temporal variation in species’ abundances, responses of species to experimental treatments can be relatively consistent between years.
Grazing treatment effects on diversity and individual species
Where studies have compared grazed and ungrazed treatments it is usual to find that grazing increases plant species diversity (Hill, Evans & Bell 1992; Bullock & Pakeman 1997; Humphrey & Patterson 2000), and Olff & Ritchie (1998) have suggested this is a general effect of large grazers in temperate fertile systems. In our experiment, where all paddocks were grazed, but at different seasons and intensities, effects on diversity were not so straightforward. While winter and spring grazing increased dicot species number, the point quadrat survey showed no effect of winter grazing, a positive effect of spring grazing and a negative effect of heavier summer grazing on species number of all vascular plants. Most other studies have found no effect of grazing season or intensity on species richness: Smith & Rushton (1994) comparing autumn grazed only, spring grazed only and autumn and spring grazed treatments in a mesotrophic meadow; Smith et al. (1996) comparing autumn grazing vs. autumn and spring grazing treatments in another mesotrophic meadow; Gibson & Brown (1991) comparing autumn vs. spring grazing and long vs. short grazing periods on a chalk grassland. However, Smith et al. (2000) found that a combination of spring and autumn grazing increased species number in a mesotrophic meadow. We also found the log normal diversity index was unaffected by treatment. These complexities of diversity responses result from the variety of individual species’ responses to grazing treatments in different seasons. Thus, responses that might lead to higher species diversity under heavier grazing, such as increase of the uncommon Trisetum flavescens under winter grazing or the decline of the dominant Agrostis stolonifera under heavier grazing in any season, were counteracted by effects such as the increase of the dominant Lolium perenne under heavier summer grazing. The rare species showed a similar variety of responses: the coarse grass Elytrigia repens was nearly 20 times more abundant in non-spring grazed paddocks, but the low-growing dicot Medicago lupulina was found only in spring grazed paddocks.
Aside from community-level responses, the treatment effects on particular species may be important in terms of management requirements. While the general increase in dicot species number and abundance of individual dicots under heavier grazing pressure (see also Bullock, Clear Hill & Silvertown 1994c) might be seen as desirable for biodiversity, the enormous increase in Cirsium vulgare under heavier grazing in any season is undesirable in terms of stock management and animal production (Hartley 1983). In one particular paddock that was grazed in winter and spring and heavy grazed in the summer, Cirsium vulgare was found in 82 of the 100 dicot survey quadrats. This level of infestation reflects the emerging weed problems in heavily grazed pastures that have been extensified as a result of the UK government's Environmentally Sensitive Areas scheme (Pywell et al. 1998).
Marrs (1993) suggested grazing might be used to decrease soil nutrients in extensified pastures and other fertile systems to allow development of more desirable plant community types, but the lack of grazing responses by most soil nutrients in this study indicates this is not a useful method. In fact nitrogen was higher under heavier grazing. This is commonly found and is probably the result of excretal return increasing available nitrogen (Dormaar & Willms 1998).
Species’ traits and responses to grazing
Wishing to describe vegetation responses to grazing in terms of functional groups, Lavorel et al. (1997) suggested that responses to grazing can be correlated to life history (grazing increases short-lived species), morphology (grazing increases short and rosette species) and regeneration type. This implies responses to grazing are controlled mostly by: (i) grazer selectivity, in that shorter plants avoid biomass removal by large grazers; and (ii) disturbance, in that short-lived plants or good dispersers can colonize disturbances caused by grazers, while longer-lived plants are damaged by grazing and cannot exploit openings. This classification has been supported by studies comparing grazed vs. ungrazed or light vs. heavy grazed temperate (Trémont 1994; McIntyre, Lavorel & Trémont 1995; Lavorel, McIntyre & Grigulis 1999), mediterranean (Noy Meir, Gutman & Kaplan 1989; Sternberg et al. 2000) and arid (Landsberg et al. 1999) grasslands, which have shown that grazing encourages species that are short-lived, have a flat-rosette growth form and/or have seeds that disperse well (for example are small or have pappi). Correlating grazing response with coarse classes of growth form and life history may be useful where extremes of grazed vs. ungrazed or very heavily vs. lightly grazed are compared. However, this may be irrelevant within the usual range of grazing regimes imposed by agricultural or conservation managers on temperate pastures. In our grassland, which is typical of temperate improved pasture, there were few species and few functional groups; almost all species were polycarpic perennial hemicryptophytes (perennial buds in the soil surface), with a few short-lived species and some chamaephytes (perennial buds just above the soil surface). This suggests grazing per se has already restricted the range of life forms in the pasture (see also Tofts & Silvertown 2000). The less extreme variations in grazing intensity of our study produce more subtle correlations. The use of functional groups is useful where there is a diversity of groups (for example Sternberg et al. 2000 had 10 functional groups and 166 species) and poor quantitative information on species’ traits. However, functional groups are distinguished using an array of traits and so it is difficult to determine exactly which traits are determining the response to grazing. The use of quantitative traits is more informative and rigorous than the use of functional groups.
Briske (1996) and Augustine & McNaughton (1998) considered traits rather than functional groups and suggested there are two conflicting mechanisms causing community change under grazing compared with no grazing. (i) Avoidance, whereby species less preferred by grazers increase under grazing. Selection is controlled by biochemical deterrents (for example secondary chemicals) and/or morphology (for example growth form). (ii) Tolerance, whereby species more able to regrow, and regrow more rapidly, after grazing are able to dominate. One factor controlling the balance between these two mechanisms is the possibility that fast regrowers may gain an advantage under the greater nitrogen availability under heavier grazing.
This dichotomy may be too simplistic. Our study suggests the mechanism of response can vary, even within the same grassland, depending on the type of grazing contrast considered. The lack of a correlation of the summer ratios with those for winter or spring grazing suggests the mechanism controlling community responses to summer grazing treatment was different to that controlling responses to winter or spring grazing. However, the latter two responses were correlated, suggesting a common mechanism.
The summer grazing mechanism was clearly through the opening of vegetation gaps, and superior gap colonizers showed a more positive response to heavier grazing. Our direct measure of gap colonization ability was the best predictor of summer grazing response. However, the fact that Grime's ruderality score (Grime, Hodgson & Hunt 1988) was also significant and was correlated with our gap colonization ability measure means that there is a generally available measure that might be used to predict response to grazing. The negative effect of competitive ability, as measured by Grime's C-value, on summer grazing response probably does not indicate a second mechanism. This is because the other measures of competitive ability were not correlated with response to grazing and the C-value and R-value were negatively correlated (Pearson r =−0·84, d.f. = 15, P < 0·001). The latter finding is a general problem caused by the constrained geometry of Grime's triangular model (Loehle 1988), which reduces its usefulness for a study such as ours.
The surprising positive correlations of spring and winter grazing ratios with grazing selectivity may be spurious. Accurate measures of selection are extremely hard to make, and grazer choice can vary depending on a wide range of factors, including animal condition, previous grazing environment, season, and species, breed and gender of grazer (Illius & Gordon 1993). However, the correlation of the Davies (Davies 1925) and Spedding (Spedding & Diekmahns 1972) selectivity values indicates they have some generality for large grazers (the Diaz & Ford 2000 data suggest rabbits use different criteria). Another explanation for the positive correlation is that selectivity score may be a surrogate for another process that controlled response to grazing. In a review of studies of a wide range of habitats, Augustine & McNaughton (1998) found some cases of increases in biochemically unpalatable species under grazing, but other cases of no change, or even an increase in more palatable species. They explained the latter case by suggesting there is a trade-off between biochemical palatability and regrowth ability, which means that avoidance and tolerance may be alternative strategies. There is ample evidence of a negative relationship between a plant's growth rate and its ability to defend itself chemically (Hartley & Jones 1997). In our system, where grazing is intense during winter and spring grazing, and we have observed sheep eating even well-defended species such as Urtica dioica and Cirsium vulgare, tolerance may be a more successful strategy than avoidance.
Over and above these correlations of particular traits with performance under grazing was the difference between dicots and grasses, with the former generally increasing, and the latter generally decreasing, under winter grazing or heavy summer grazing. This seemed to be a general difference between the taxa because the sum of the frequencies of the rarer 17 dicots (i.e. those not included in the trait analysis) was increased by grazing in any season (mean ratio = 2·93) whereas the sum of the frequencies of the rarer four grasses was decreased by grazing (mean ratio = 0·81; paired t-test on ratios for each main grazing treatment, t = 4·1, d.f. = 2, P < 0·05). The positive effect of grazing on dicots was noted in the previous surveys (Bullock et al. 1994a) but, given the wide range of life histories exhibited by the dicot species, it is unclear why this should be such a general effect. It does mean, however, that heavier grazing in any season will move the grassland towards the more dicot-rich community desired by conservationists.
This study has shown that vegetation changes due to grazing will differ depending on the exact grazing regime, season and intensity being important. These differences are due to changes in the mechanism of response to grazing. An ability to adjust the grazing regime in order to direct vegetation change towards particular targets, such as increasing dicot diversity or weed control, will require greater understanding of the mechanisms by which plants are responding to grazing.