response to individual treatments
Nitrogen deposition on lowland Calluna vulgaris-dominated communities is commonly associated with increased graminoid abundance, becoming dominant over dwarf shrubs in the long term (Heil & Diemont 1983; Aerts & Heil 1993; Bobbink, Hornung & Roelofs 1998). The graminoid component of the vegetation at this alpine site was initially very small, although several species were present as isolated individuals, and no evidence of an expansion was seen. This result is similar to that of Power, Ashmore & Cousins (1998), who saw no grass invasion of Calluna vulgaris-dominated lowland heathland after 7 years of nitrogen addition; their plots, however, were undisturbed. Transition from shrub to graminoid dominance is generally associated with disturbance, such as heather beetle Lochmaea suturalis attacks opening the dwarf shrub canopy (Berdowski & Zeilinga 1987). In alpine heathland the dense mat of dwarf shrubs and lichens covering the ground may reduce the availability of gaps for establishment and, in combination with a low seed input, limit the potential for graminoid expansion. Burned plots, however, had a large proportion of bare ground for several years but still did not see a significant increase in graminoid cover; thus it seems more likely that seed availability is the limiting factor. Species such as Deschampsia flexuosa do not form a seed bank (Grime, Hodgson & Hunt 1990) and this would give the dominant dwarf shrubs, with a large long-lived seed bank and/or the ability to spread rapidly through vegetative means, a competitive advantage during regeneration. When nitrogen was added to similar alpine lichen–dwarf shrub vegetation in Norway over a 10-year period (Fremstad, Paal & Möls 2005), Festuca ovina was the only higher plant species that responded, showing a slight increase in cover. The initial cover of Festuca ovina was higher in that study, however, so the potential for vegetative expansion may have been greater.
While the higher plant component of the vegetation appeared resilient to change and showed only small responses to the nitrogen treatments, the lower plant component of the community was more sensitive to the effects of nitrogen deposition. Lichen cover declined on nitrogen-treated plots, a response that was also reported in the Norwegian study (Fremstad, Paal & Möls 2005) and in studies of heathlands and arctic tundra vegetation (Bobbink, Hornung & Roelofs 1998; Lee & Caporn 1998; Press et al. 1998; Gordon, Wynn & Woodin 2001). As there was no obvious change in vegetation structure that might have reduced light availability to lichens or increased competition with higher plants, it seems likely that the reduction was a direct effect of the nitrogen deposition. Lichens and mosses are extremely efficient at retaining applied nitrogen (Curtis et al. 2005), and reductions in Cladonia growth in response to nitrogen exposure have previously been reported in heathland habitats (Vagts & Kinder 1999). Species reacted individually to the treatments, with Cladonia furcata and Cladonia ‘arbuscula’ showing a significant response to the nitrogen treatments while Ochrolechia frigida and Cetraria islandica did not. Lichen species richness was also reduced and was the main driver of reductions in total community species richness. This reduction in species richness in response to low levels of nitrogen addition appears to be a general response and has been observed in a wide range of communities (Gough et al. 2000). This suggests that lichen diversity could be used as an effective indicator of the impacts of nitrogen deposition in alpine lichen-rich communities. What cannot be determined from this study is whether the observed effects of the nitrogen treatments are a result of the total nitrogen load or the concentration of the treatments. Because of practical constraints on the frequency and volume of nitrogen treatment applications, most studies of this type, including this one, expose the vegetation to much higher ion concentrations than would typically be found in rainfall or cloud water. Further work is needed to separate these two effects and to improve understanding of what drives the effects of nitrogen deposition on both higher and lower plants.
The burning treatment had the greatest effect on species richness and composition of the vegetation in the short term. The recovery of the vegetation following this treatment, however, was relatively rapid. Although burning caused a large drop in species richness at the beginning of the experiment, species were quick to recolonize the plots, and species richness had recovered to unburned levels within 4 years. Total cover of lichens and shrubs was still below unburned levels in 2004, but looked likely to recover fully within 7 years if the current trajectory was continued. Species composition data indicated that species from the original species pool were recolonizing, and little invasion of new species occurred despite a high cover of bare ground within the plots for several years. Lichen species quickly recolonized, possibly because of their ability to disperse by wind-blown fragments, but as they are generally slow growing it is likely that lichen cover will take longer to recover. This relatively direct return towards the initial species composition is in contrast to Calluna heaths at lower altitude, where temporary increases of Vaccinium species or graminoids often follow management fires (Gimingham 1972). However, such management fires would generally be more intense than burns in the alpine zone, as a result of the higher fuel load present in lower altitude heaths, giving other species the opportunity to establish while the slow-growing Calluna vulgaris regenerates.
Although sufficiently large that the majority of the regeneration of higher plants following the fire was from seed rather than from lateral expansion of surrounding individuals (A. Britton, personal observation), the small plot size (1·125 m2) used here may also have contributed to the rapid return of the vegetation to its original composition. Small plots are more sheltered and less exposed to the effects of winter frost heave, which is the predominant cause of winter mortality in seedlings at this altitude (Miller & Cummins 1987), thus allowing vegetation to re-establish more quickly. Where larger areas of alpine heath have been burned, frost heave and exposure may reduce or delay dwarf shrub regeneration and make initiation of erosion likely (Moorland Working Group 1998). While the nature of the experimental site precluded using larger plots, this interaction between plot size, dispersal and physical disturbance, along with fire intensity, must be taken into account when applying results at larger scales to ensure that potential effects are not underestimated (Strengbom, Englund & Ericson 2006).
Although the clipping rate of 12% of the current year growth removed that was applied in this experiment is approximately double the amount of biomass removed by grazing on low-alpine heaths in the Scottish Highlands (A. Britton, unpublished data), Calluna vulgaris withstood this amount of offtake without obvious damage and vegetation diversity was unaffected. This treatment does not completely simulate the selective effects of grazing herbivores, or the effects of trampling and nutrient deposition which result from their presence, but it does show that the vegetation can withstand a significant level of biomass removal without damage. Effects of trampling and nutrient deposition by grazers may therefore be more important in causing the reductions in alpine dwarf shrub heath extent in areas of high grazing pressure.
interactions between treatments and between treatments and climate
The strong interaction seen in this study between burning and nitrogen addition, in terms of effects on community composition, has previously been documented for higher plant species in lower altitude heathland communities subject to a variety of nitrogen-removing management treatments (Diemont 1994; Britton et al. 2001; Barker et al. 2004). However, for lichens, which grow on the soil substrate but do not obtain their nutrients from it, the mechanism for this effect is not clear. In unburned plots, reductions in lichen species richness were seen with nitrogen additions as low as 10 kg N ha−1 year−1, while only non-significant trends towards a reduction were seen in burned plots. Further studies are needed to investigate the reason for this difference.
The severe winter browning and subsequent death of Calluna vulgaris in the 50 kg N ha−1 year−1 plots, which occurred during winter 2002–03 appeared to have the potential to cause significant changes in species composition, which until then had shown little response to nitrogen treatments. The effect of exposure to pollutant nitrogen on dwarf shrub frost and drought tolerance has been the subject of a number of studies (Bobbink, Hornung & Roelofs 1998). However, results have varied. Where the effect of nitrogen on frost tolerance has been measured directly, it has been shown variously to increase tolerance (Caporn, Risager & Lee 1994; Taulavuori et al. 1997, 2001), decrease tolerance (Power et al. 1998; Caporn, Ashenden & Lee 2000 found a reduction in hardening in spring) or have no effect (Sæbøet al. 2001; Power et al. 1998 found no effect in early winter). Effects on drought tolerance appear to be more consistent, with most authors finding an increased sensitivity to drought (including winter drought as a result of soil freezing) in plants exposed to elevated nitrogen levels (van der Eerden et al. 1991; Fangmeier et al. 1994; Lee & Caporn 1998; Gordon et al. 1999). Fangmeier et al. (1994) have suggested that this increased susceptibility to drought is a result of increased carbon demand in plants exposed to high levels of nitrogen leading to increased stomatal opening and hence increased water loss. Reductions in root : shoot ratios are another potential explanation (van der Eerden et al. 1991). Whether the result of reduced freezing tolerance or increased susceptibility to drought, increased winter browning in Calluna vulgaris exposed to elevated nitrogen deposition has been reported from both experimental studies and in field situations (e.g. Dutch heathlands; Bobbink, Hornung & Roelofs 1998). In the case of alpine Calluna heathlands, which experience particularly severe winter conditions and potentially high rates of evapotranspiration as a result of high mean wind speeds, the interaction between nitrogen deposition and drought and frost tolerance has the potential to be a critical one for determining biodiversity responses to nitrogen deposition.