SEARCH

SEARCH BY CITATION

Keywords:

  • above-ground biomass;
  • competition;
  • mycorrhizal infection;
  • nutrient uptake;
  • root length

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1 The role of nutrient supply and defoliation on the competitive interactions between pot-grown Calluna vulgaris and Nardus stricta plants was investigated.WP leading adjustment

2 Young plants were grown alone and together in pots under a combination of fertilizer and defoliation treatments. After 18 months, parameters reflecting both above- and below-ground performance were measured, namely: total above-ground biomass, shoot nitrogen and phosphorus content, root length and the extent of mycorrhizal infection of the roots.

3 In the pots that received fertilizer, the shoot nutrient content and above-ground biomass of Nardus plants increased to a greater extent than those of Calluna plants; this effect was more marked for Nardus plants growing with Calluna plants than for those growing with other Nardus plants. In contrast, Calluna plants growing in competition with Nardus failed to respond to the addition of nutrients. However, in unfertilized pots, Calluna gained more above-ground biomass during the experimental period than Nardus.

4Calluna had greater root length than Nardus, but Nardus had a higher proportion of its root length infected by mycorrhizal fungi. In both plants, the addition of fertilizer reduced the mycorrhizal infection and increased the root length. Nardus root length was decreased when grown in competition with Calluna only in pots where no nutrients were added. Defoliation decreased the extent of mycorrhizal infection in Calluna roots but not in those of Nardus; defoliation decreased the shoot nutrient content in Calluna plants, but not in Nardus plants.

5 These results suggest that the competitive balance between Nardus and Calluna may be altered by the addition of nutrients, and by defoliation, which may have serious implications for the future dominance of Calluna in heathland ecosystems, particularly those where nutrient inputs are increasing significantly or where grazing pressures are high.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Resource-based competition can be a major structuring force in plant communities (Berendse & Elberse 1990; Goldberg 1990; Tilman 1997) but its effects on plant community structure may be modified by other processes, particularly herbivory, which may shift the competitive balance between species if they differ in their palatability or in their regrowth capacity (Berendse 1985; Louda et al. 1990; Crawley 1997). Relatively few studies have attempted to quantify the interacting effects of herbivory and resource availability on the competitive balance between plant species in terms of below-ground growth parameters as well as above-ground ones, but knowledge of the differential effects of herbivory and nutrient availability on plant performance is important in understanding the mechanisms by which one species replaces another.WP leading adjustment

Calluna vulgaris (L.) Hull-dominated moorland is in decline in many areas of Scotland (Sydes 1988; Marrs 1993; Welch & Scott 1995). Overgrazing by sheep and deer is thought to be a major cause of the loss of Calluna cover to grass species, particularly to Nardus stricta L., a species which is relatively unpalatable to sheep (Welch 1986; Marrs & Welch 1991; Welch & Scott 1995). The decrease in Calluna cover is more rapid in some places than in others. This may simply reflect uneven grazing pressures, but it is also possible that herbivory has a more adverse effect on Calluna where the soils have a relatively high nutrient value, because this may further favour grasses (Heil & Bruggink 1987; Aerts & Berendse 1988; Berendse et al. 1994; Bobbink et al. 1998). To understand more about the mechanisms by which Calluna is being replaced by Nardus, the factors affecting their competitive interactions above- and below-ground need to be examined.

Calluna and Nardus have different growth strategies. Calluna is a slow-growing evergreen dwarf shrub (Gimingham 1972) and, typical of woody plants with long-lived leaves that are adapted to growing in low nutrient environments (Coley et al. 1985), it contains high levels of carbon-based secondary metabolites such as phenolics and tannins (Iason et al. 1993). If Calluna is grazed, the meristems at the tip of the shoots are lost, and recovery from browsing is therefore slow. In contrast, Nardus seedlings have a slightly faster relative growth rate than those of Calluna (Grime et al. 1988), and Nardus is better able to regrow after browsing because its meristems are found at the bases of the leaves. It has lower levels of tannins and lignin than Calluna, but the mature leaves are unpalatable to sheep due to high levels of silica (Welch 1986).

In addition to these different above-ground strategies of growth and defence, Nardus and Calluna have different below-ground growth forms and mycorrhizal associations. Calluna roots grow mainly in a dense mat in the upper organic layer of soil (Gimingham 1960). The bulk of the nutrient absorption by Calluna takes place via fine hair roots that are always infected with the ericoid mycorrhizal fungus Hymenoscyphus ericae (Gimingham 1972; Read & Stribley 1973). This mycorrhizal association may confer an advantage to the host-plant by improving access to nutrients held in forms unobtainable to other plants, e.g. proteins and amino acids (Read & Stribley 1973; Read & Bajwa 1985), and by improved tolerance of low pH and toxic elements in the soil, such as phenolic acids and heavy metals (Leake et al. 1989; Hashem 1995). In contrast to ericoid species, Nardus has an association with two types of arbuscular mycorrhizae (AM) (Ali 1996). These are thought to increase nutrient absorption area (and thus uptake), particularly for phosphorus (Read et al. 1976; Abbot & Robson 1985), and to improve both resistance to pathogens (Fitter 1985; Sharma et al. 1992) and drought tolerance (Allen & Allen 1986). The dominance of Calluna in low nutrient soils may owe much to the mycorrhizal association it holds, but there have been few studies on the effects of grazing and increased nutrient availability on the relationship between Calluna and its mycorrhizal fungus, and none which addresses the effects of these factors on this association relative to the mycorrhizal association of competing grass species.

In this study we examined potential competitive interactions between Nardus and Calluna, specifically the effects of nutrient addition and defoliation upon this interaction, both above- and below-ground. In order to assess the relative abilities of each species to utilize additional nutrients, we measured changes in above-ground biomass and shoot nutrient content, as well as changes in below-ground factors, namely mycorrhizal infection levels and root length, in response to fertilizer. We also investigated how these parameters were modified by defoliation.WP leading adjustment

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Treatments

Nardus stricta tussocks and small C. vulgaris plants, approximately 3–5 years old, were collected from a recently burned area on the Cairn o’ Mount, Kincardineshire (grid reference NO648805) and potted into a mixture (4 : 1) of peat and sand in March 1994. The plants were grown either with the same species or mixed with the other species at densities of four plants (four Calluna plants, four Nardus tussocks, or two of each) to a pot 25 cm in diameter by 22 cm deep. At the start of the experiment, the plants were sufficiently small (c. 3 cm diameter and 5 cm tall) that they could be spaced far enough apart to ensure minimum competition for light. They were allowed to establish for 3 months prior to each pot receiving one of four treatments: control (no treatment), fertilized with NPK, defoliated, or both fertilized and defoliated. NPK was applied as ammonium nitrate (1.1 g pot−1 year−1), as superphosphate (0.6 g pot−1 year−1) and as sulphate of potash (0.6 g pot−1 year−1). This fertilizer application is approximately equivalent to 75 kg N, 25 kg P and 50 kg K ha−2 year−1. Fertilizer was applied in three doses during the growing season and watered in. The defoliation treatment removed approximately half of the current year's growth by clipping at three times during the growing season. There were 12 species × treatment combinations (Calluna, Nardus, or both, × four fertilizer/ defoliation treatments) in each of seven replicate blocks, each block consisting of 12 pots and 48 plants (24 Nardus and 24 Calluna), four pots containing Nardus plants only, four containing Calluna plants only, and four containing both species. All pots were kept in a hard standing at ITE Banchory (grid reference NO677984) and were regularly watered and weeded.

Harvesting

All plants were destructively harvested in August 1995. The above-ground growth of each plant was dried in an oven at 80 °C for 48 h and weighed. The dry plant material was milled and analysed for total nitrogen and phosphorus content using a continuous flow colorimetric autoanalyser (Segmented Flow Autoanalyser, Burkard Scientific, Uxbridge, UK), following wet acid digestion (Allen 1989). The nitrogen content was measured as ammonium by a modified Bertholet reaction (Hinds & Lowe 1980; Rowland 1983), and phosphorus was measured as phosphate by the ‘Molybdenum blue’ method (Burkard Scientific, personal communication; Allen 1989).WP leading adjustment

A root core (c. 15 cm deep by 5 cm diameter) was taken from the centre of each pot and frozen prior to analysis. For analysis of root length, the soil from each core was defrosted overnight and allowed to dry until friable, then two 5-g subsamples (c. 5 cm deep by 2 cm diameter) were removed. The roots were removed from the soil by washing in a 1-mm mesh sieve, then cleared in 2–5% potassium hydroxide at 90 °C for 30 min. The roots were washed thoroughly in several changes of deionized water, bleached in hydrogen peroxide for 10 min, then acidified in 1% hydrochloric acid for a further 10 min. They were stained for mycorrhizal infection using 0.05% trypan blue in acidic glycerol for 15 min at 90 °C, then destained overnight in acidic glycerol. Both the root length and percentage mycorrhizal infection were assessed by a modified line intersect method (Brundrett et al. 1975; Tennant 1975) using a ×40 magnification under a dissecting microscope (Leica Wild M3Z Type-S, Leica UK Ltd, Milton Keynes, UK).

Statistical analysis

The results were analysed using the glm procedure in Minitab. All the results were expressed as mean values of all plants per species per pot. All seven blocks were harvested and analysed for the above-ground measurements (apart from a small number of pots with insufficient material for shoot analyses), giving up to 56 replicates per species (7 blocks × 8 pots per block which contained that species). Due to the labour-intensive nature of the below-ground measurements, only five randomly selected replicate blocks were sampled, giving 40 replicates per species.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Above-ground measurements

The addition of fertilizer significantly increased the above-ground biomass of both Calluna and Nardus, with the exception of Calluna plants growing in competition with Nardus (Table 1 and Fig. 1). The response of the two species to fertilizer differed according to whether they were grown in competition with each other or with conspecifics. Fertilizer increased biomass to a greater extent in those Nardus plants grown with Calluna than in those grown with other Nardus plants. The effect of the type of competition was in the reverse direction in Calluna: fertilizer had an effect only when the competitors were conspecifics (i.e. the pots did not contain Nardus plants). There was therefore a significant pot type (i.e. mixed vs. alone)–fertilizer interaction for both species (Table 1). Calluna plants growing in the absence of fertilizer were slightly larger in the mixed species pots than when growing with conspecifics, but this was not statistically significant. Fertilizer increased the shoot nitrogen and phosphorus content of both Calluna and Nardus plants (Table 1 and Fig. 2a,b) but, as with above-ground biomass, the relative size of the increase depended on whether the plants were grown with conspecifics or in mixtures. Nardus plants had a greater increase in tissue nitrogen and phosphorus content when growing in competition with Calluna plants than with other Nardus plants (Fig. 2a). In contrast, Calluna plants showed an increase in nitrogen and phosphorus content in response to nutrient addition when they were growing alone, but a much smaller increase when growing with Nardus (Fig. 2b). There was therefore a significant pot type–fertilizer interaction for both species (Table 1).WP leading adjustment

Table 1.  The results of glm analyses on the effects of fertilizer, defoliation, and growing with conspecifics or in mixtures, on the above-ground biomass, shoot nitrogen and phosphorus content, root length and mycorrhizal infection of Calluna and Nardus plants. F-values and significance levels for the main effects and the interaction between them are given. n = the number of replicate pots sampled for each species (see text for details)
Above-ground measurements
Above-ground biomassmg N per plantmg P per plant
 Nardus (n = 56)Calluna (n = 56)Nardus (n = 53)Calluna (n = 52)Nardus (n = 53)Calluna (n = 52)
Pot typeF  = 11.2 P < 0.01F  = 4.86 P < 0.05F  = 2.58 NSF  = 6.56 P < 0.05F  = 2.48 NSF  = 5.56 P < 0.05
FertilizerF  = 138 P < 0.001F  = 19.5 P < 0.001F  = 6.6 P < 0.001F  = 35.51 P < 0.001F  = 39.4 P < 0.001F  = 14.95 P < 0.001
DefoliationF  = 8.8 P < 0.01F  = 37.91 P < 0.001F  = 0.27 NSF  = 11.52 P < 0.001F  = 0.16 NSF  = 12.52 P < 0.001
Pot type × fertilizerF  = 10.2 P < 0.01F  = 18.53 P < 0.001F  = 1.46 NSF  = 14.12 P < 0.001F  = 0.44 NSF  = 10.89 P < 0.01
Pot type × defoliationF  = 0.02 NSF  = 1.43 NSF  = 1.65 NSF  = 0.04 NSF  = 1.5 NSF  = 0.56 NS
Fertilizer × defoliationF  = 2.22 NSF  = 4.92 P < 0.05F  = 0.00 NSF  = 6.41 P < 0.05F  = 0.54 NSF  = 1.46 NS
 Below-ground measurements
 Root lengthProportion mycorrhizal infection  
 Nardus (n = 40)Calluna (n = 40)Nardus (n = 40)Calluna (n = 40)  
Pot typeF  = 6.84 P < 0.05F  = 5.15 P < 0.05F  = 0.77 NSF  = 0.00 NS  
FertilizerF  = 26.52 P < 0.001F  = 2.02F  = 43.12 P < 0.001F  = 0.73 NS  
DefoliationF  = 0.33 NSF  = 6.61 P < 0.05F  = 3.23 NSF  = 10.85 P < 0.01  
Pot type × fertilizerF  = 2.37 NSF  = 5.17 P < 0.05F  = 2.28 NSF  = 0.00 NS  
Pot type × defoliationF  = 0.01 NSF  = 0.12 NSF  = 0.18 NSF  = 0.03 NS  
Fertilizer × defoliationF  = 0.09 NSF  = 0.56 NSF  = 16.54 P < 0.001F  = 0.14 NS  
image

Figure 1. Above-ground biomass (dry weight in g) of Nardus (n = 56) and Calluna (n = 56) plants, grown in pots in monocultures (alone) or in mixtures (+ Calluna, or + Nardus). Shaded bars are values for plants grown in pots with added fertilizer, unshaded bars are values for plants from control pots with no fertilizer added. Mean values ± SE are shown.

Download figure to PowerPoint

imageimage

Figure 2. Nitrogen and phosphorus contents (as total nitrogen or phosphorus in mg per plant) of Nardus and Calluna plants grown in monocultures or in mixtures, in pots with (shaded bars) or without (unshaded bars) fertilizer addition. Mean values ± SE are shown. (a) Nardus plants (n = 53), (b) Calluna plants (n = 52).

Defoliation obviously reduced above-ground biomass in both species (Table 1), but it also prevented Calluna from increasing its above-ground biomass in response to fertilizer: even in Calluna-only pots defoliated plants were the same size irrespective of fertilizer addition. This was not the case for Nardus plants, which increased in above-ground biomass in response to fertilizer whether they were defoliated or not, leading to a significant fertilizer–defoliation interaction for Calluna but not Nardus (Table 1).

These effects of defoliation on above-ground biomass may reflect the effect of defoliation on nutrient uptake in the two species. Defoliation reduced the nitrogen and phosphorus content of Calluna shoots (particularly in fertilized pots), but the nutrient content of Nardus shoots was not significantly affected by defoliation (Table 1 and Fig. 3a,b for nitrogen levels), suggesting that the effect of defoliation on the ability of plants to take up nutrients was more marked in Calluna than in Nardus. For Nardus, whether growing in monoculture or in mixtures with Calluna, defoliation did not affect the increase in shoot nitrogen content in response to fertilizer (Fig. 3a). Thus there were no significant pot type–defoliation or fertilizer–defoliation interactions for Nardus (Table 1), and neither defoliated (F = 0.31, P = 0.58) nor control (F = 1.15, P = 0.29) plants showed a significant pot type–fertilizer interaction. In contrast, the addition of fertilizer to Calluna produced a much smaller increase in shoot nitrogen content in defoliated plants than in control ones, both for Calluna growing in monoculture and in competition with Nardus (Fig. 3b). There was a significant fertilizer–defoliation interaction term for Calluna nitrogen content (Table 1), and both defoliated (F = 10.7, P = 0.003) and undefoliated (F = 6.06, P = 0.02) Calluna plants showed a significant fertilizer–pot type interaction for shoot nitrogen content. In summary, the increase in tissue nitrogen content produced by fertilizer in plants growing in mixtures was slightly greater for defoliated Nardus plants but significantly reduced in defoliated Calluna plants, relative to control plants (Fig. 3a,b).

imageimage

Figure 3. The nitrogen content (mg per plant) of shoot tissue in control and defoliated plants grown in monocultures (Alone) or with the other species (Mixed). Shaded bars are values for plants from fertilized pots; unshaded bars are values for plants from control pots. Mean values ± SE are shown. (a) Nardus plants (n = 26), (b) Calluna plants (n = 26).

Below-ground measurements

Fertilizer increased the root length of Nardus (Table 1 and Fig. 4 and Fig. 5), particularly when the plants were growing in monocultures, although the pot type–fertilizer interaction was non-significant. Regardless of fertilizer treatment, Nardus plants tended to have a greater root length growing in monoculture than when growing with Calluna plants, hence there was a significant effect of pot type on root length (Table 1 and Fig. 4). Overall, fertilizer had no significant effect on the root length of Calluna, but there was a significant effect of pot type on Calluna root length (Table 1): in monocultures, fertilizer increased root length, but decreased it when Calluna was growing with Nardus. In unfertilized pots, Calluna root length was the same whether the plants were grown alone or in mixtures with Nardus (Fig. 4). There was therefore a significant pot type–fertilizer interaction on Calluna root length. Defoliation had no effect on the root length of Nardus plants but caused a marked decrease in the root length of Calluna (Table 1 and Fig. 5).WP leading adjustment

image

Figure 4. Root length (cm) of Nardus and Calluna plants, grown in pots in monocultures (alone) or in mixtures (mixed). Shaded bars are values for plants grown in pots with added fertilizer, unshaded bars are values for plants from control pots with no fertilizer added. Mean values (n = 40) ± SE are shown.

Download figure to PowerPoint

image

Figure 5. The root length (cm) of Nardus plants (unshaded bars) and Calluna plants (shaded bars) receiving no treatment (control), fertilizer, defoliation, or both fertilizer and defoliation treatments. Mean values (n = 40) ± SE are shown, calculated irrespective of whether the plants were in mixtures or in monocultures (see Fig. 4 for monoculture vs. mixture effects).

Download figure to PowerPoint

Nardus plants had a higher proportion of root length infected by mycorrhizal fungi than Calluna plants, regardless of treatment (Fig. 6). Defoliation alone increased the mycorrhizal infection rate of Nardus plants, while fertilizer (with or without defoliation) significantly decreased it. The large decrease in infection rates in fertilized Nardus plants as a result of defoliation led to a significant fertilizer–defoliation interaction on infection rates. Fertilizer tended to reduce the infection rate in Calluna slightly, while defoliation caused a more marked decrease (Table 1 and Fig. 6).

image

Figure 6. Proportional mycorrhizal infection of Nardus plants (unshaded bars) and Calluna plants (shaded bars) receiving no treatment (control), fertilizer, defoliation, or both fertilizer and defoliation treatments. Mean values (n = 40) ± SE are shown, calculated irrespective of whether the plants were in mixtures or in monocultures.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

All the treatments applied to the Calluna and Nardus plants in this experiment, namely fertilizer, defoliation and being grown in competition with conspecifics vs. mixtures, produced significant effects on at least some aspects of their above- and below-ground growth. In addition, there were interactions between the treatments: for example, the effects of fertilizer on the plants were modified by defoliation and the identity of the competing species. The treatments altered plant growth and nutrient acquisition by the two species to differing extents, suggesting that the competitive balance between Nardus and Calluna may be altered by nutrient availability and herbivory.WP leading adjustment

Under three of the four treatments, Nardus was the superior competitor, which explains why Nardus performed better in mixtures than in monocultures, while the reverse was true for Calluna. Only in unfertilized and undefoliated pots did the competitive advantage lie with Calluna. In unfertilized pots Calluna produced more biomass growing with Nardus than alone, and Nardus plants were the same size growing with Calluna as with conspecifics. In addition, Nardus root length was lower in unfertilized pots where Calluna was present. However, when fertilizer was added, the competitive balance changed and Nardus seemed better able to take advantage of the nutrient addition than Calluna. Calluna plants did not increase in size if they were fertilized when growing with Nardus, but Nardus plants showed a greater response to fertilizer when growing with Calluna than when grown in monoculture. The same pattern occurred in shoot nutrient content as in biomass, with a greater benefit to Nardus from fertilizer addition in mixtures than monocultures, but the reverse was the case for Calluna. Furthermore, the competitive disadvantage to Calluna extended below-ground, because fertilizer increased Nardus root length in both monocultures and mixtures, but Calluna root growth only increased in monocultures.

These results are similar to those from experiments with Erica tetralix and Molinia caerulea (Berendse & Aerts 1984). In unfertilized conditions, the growth of Erica was similar in mixtures and in monocultures, but when nitrogen was added Erica's productivity and shoot nitrogen content were decreased in the presence of Molinia. The superior competitive ability of both Erica and Calluna to Molinia in unfertilized conditions has also been demonstrated in the field (Aerts et al. 1990); Calluna also outcompeted Molinia at high fertility, although Erica did not. However, several other studies have found that high fertility does favour Molinia over ericaceous species (Heil & Bruggink 1987; Aerts 1989; Aerts et al. 1991; Berendse et al. 1994).

This study suggests Calluna has a slight advantage over Nardus when the plants are competing without the addition of fertilizer. Although it is difficult to extrapolate from pots to the field situation, this is what might be expected on upland moorlands, with Calluna and its mycorrhizal endophyte Hymenoscyphus ericae better able to overcome the nutrient limitations of the soil (Stribley & Read 1980; Read 1983; Leake & Read 1991). However, when nutrient availability is increased, Nardus benefits to a greater extent than Calluna because it acquires the nutrients more rapidly, possibly because of differences in the effect of fertilizer on the root growth of the two species. Root length was increased in the fertilized pots to a greater extent for Nardus than for Calluna, especially when they were growing together. This may reflect the different strategies of the two plants for acquiring nutrients: Nardus has fibrous roots that go deep in the soil, while Calluna has fine roots close to the soil surface (Gimingham 1960). In the pot system used here, in which peat and soil were mixed homogeneously, Nardus roots may have been able to colonize to a greater depth and so have access to more of the added nutrients. Generally grasses distribute their roots more evenly in the soil profile than ericoid species, which concentrate their roots in the top 10 cm of soil (Aerts 1993). Aerts et al. (1991) found that Molinia allocated more than twice as much biomass to its root system than did Calluna when they were growing in competitive mixtures. Furthermore, the root biomass of Molinia present in the soil compartment of competing Calluna plants was three times as high in fertilized turves as in unfertilized ones. The authors concluded that the high competitive ability of Molinia at high nutrient supply was due to its large biomass allocation to the roots and a root system that can exploit a large soil volume. However, in heather moorlands the soil substrate is more heterogeneous than in turves or pots, and nutrients are concentrated in the organic layer very close to the soil surface. This is where Calluna roots form a dense mat, so the advantage to Nardus and other grasses may not be so apparent under field conditions. There is evidence from root box experiments using a separate peat layer at the soil surface, that this is indeed the case: Calluna is a better competitor for nitrogen than Nardus in spatially heterogeneous substrates (I. J. Alexander & S. E. Hartley, unpublished data).

The decrease in mycorrhizal infection rates in both species in the fertilized pots may be due to a direct effect of nutrients on the ability of mycorrhizae to infect successfully, or it may simply reflect ‘dilution’ of infection by increasing root growth. However, there are results from other pot studies that support the idea that mycorrhizal infection is reduced by increased soil nutrient levels (Stribley & Read 1976; Yesmin et al. 1996), although results from field trials have been less consistent (Caporn et al. 1995). Infection is costly to the host in terms of carbon, so if soil nutrient levels are such that adequate nutrients can be obtained by the plant without the aid of the mycorrhizae, it seems likely that there is a mechanism by which the plant can reduce infection. There are a number of published experiments on the effects of mycorrhizal infection on the outcome of competition (Allen & Allen 1990; Watkinson & Freckleton 1997), but these have usually used plants that have vesicular-arbuscular (VA) mycorrhizae (West 1996). There seem to be few studies, if any, comparing the performance of plants that have VA mycorrhizae with that of plants with ericoid mycorrhizae. In this study we did not manipulate the levels of infection, so we can make no inference on the importance of either sort of mycorrhizal infection on the competitive ability of plants. Indeed, the interpretation of the results from experiments that do compare plants with and without mycorrhizal infection in order to assess the effects on competition is complex, and effects are often found to be dependant on plant density (Watkinson & Freckleton 1997).

Nardus was a better competitor than Calluna not only under conditions of high nutrient supply, but also when defoliation shifted the competitive balance in its favour: defoliation had more adverse effects on Calluna than on Nardus, in terms of shoot nutrient content, mycorrhizal infection and root length. Defoliation reduced the increase in shoot nutrient content produced by fertilizer to a greater extent in Calluna than in Nardus, particularly when Calluna was grown in competition with Nardus. Defoliation decreased both root length and mycorrhizal infection in Calluna, but did not decrease root length and actually increased mycorrhizal infection in Nardus. The lower levels of shoot resources in defoliated Calluna plants, but not in defoliated Nardus plants, suggest that Nardus may be quicker to recover from defoliation than Calluna, reinforcing the advantage Nardus already gains from having basal meristems. Heavy grazing is thought to be a major cause of the loss of Calluna-dominated moorland in recent years (Welch 1986; Hartley 1997).

Although in these pot experiments both fertilizer and defoliation seemed to shift the competitive balance towards Nardus, in the field these factors may not necessarily favour Nardus to the same extent, as soil type, the nature of the grazing pressure, and the structure (and hence invasibility) of the Calluna canopy will all play a role in modifying their effects (Hartley 1997). For example, the effect of nutrients on the competitive balance between the two species may depend on the extent to which their relative palatability to grazing animals alters in response to increasing nutrient inputs. Any competitive advantage to Nardus from increased shoot nutrient concentrations might be lost were it to become a more preferred food for grazing animals. On Scottish moorlands, however, it was found that nitrogen addition benefited Nardus, but only in heavily grazed areas where its resistance to grazing gave it a competitive advantage. If grazing animals were excluded by fencing, Calluna cover increased in response to fertilizer and its increased growth, in response to both the extra nutrients and the lack of browsing, allowed it to close its canopy over the Nardus plants and shade them out (Hartley 1997). This field experiment highlighted the importance of canopy structure in competitive interactions between Calluna and Nardus: the smaller stature and shade intolerance of the latter species does not come into play in experiments using small transplanted plants in pots.

The results presented here show that the competitive ability of Nardus with respect to Calluna was enhanced by the addition of fertilizer, as a result of the superior ability of Nardus to acquire the added nutrients. Simulated grazing also benefited Nardus, due to its more adverse effects on Calluna's root and shoot resources. These results suggest that both grazing and nitrogen inputs could reduce the competitive ability of Calluna, particularly below-ground, which may have implications for the future dominance of Calluna in heathland ecosystems, particularly those where nutrient inputs are increasing significantly, or where grazing pressures are high.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We are indebted to the following people for their help on this project: Ann Davies, Caroline Young and Susie Macintosh for harvest measurements; Maddie Thurlow for nitrogen and phosphorus analysis; Jim Kerslake and Dave Dare for potting up the plants; Paul Taylor for mycorrhizal analysis; and Professor Ian Alexander and Dorothy Mackinnon for advice on methods. Sarah Woodin, Richard Bardgett and Rob Marrs provided helpful comments on earlier drafts of the manuscript. Financial support was provided by a Royal Society of Edinburgh Research Fellowship to S. E. Hartley, funded by the James Weir Foundation, and by the Natural Environment Research Council.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Abbot, L.K. & Robson, A.D. 1985 Formation of external hyphae in soil by four species of vesicular–arbuscular mycorrhizal fungi. New Phytologist, 99, 245 255.
  • Aerts, R. 1989 Aboveground biomass and nutrient dynamics of Calluna vulgaris and Molinia caerulea in a dry heathland. Oikos, 56, 31 38.
  • Aerts, R. 1993 Biomass and nutrient dynamics of dominant plant species from heathlands. Heathlands: Patterns and Processes in a Changing Environment (eds R.Aerts & G.W.Heil), pp. 51 84. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  • Aerts, R. & Berendse, F. 1988 The effect of increased nutrient availability on nutrient dynamics in wet heathlands. Vegetatio, 76, 63 69.
  • Aerts, R., Berendse, F., De Caluwe, H., Schmitz, M. 1990 Competition in heathland along an experimental gradient of nutrient availability. Oikos, 57, 310 318.
  • Aerts, R., Boot, R.G.A., Van Der Aart, P.J.M. 1991 The relation between above- and belowground biomass allocation patterns and competitive ability. Oecologia, 87, 551 559.
  • Ali, B. 1996 Occurrence and characteristics of the vesicular–arbuscular endophyte of Nardus stricta. Nova Hedwigia, XVII. 409–425.
  • Allen, S.E. 1989Chemical Analysis of Ecological Materials, 2nd edn. Blackwell Scientific Publications, Oxford, UK.
  • Allen, E.B. & Allen, M.F. 1986 Water relations of xeric grasses in the field: interactions of mycorrhizae and competition. New Phytologist, 104, 559 571.
  • Allen, E.B. & Allen, M.F. 1990 The mediation of competition by mycorrhizae in successional and patchy environments. Perspectives in Plant Competition (eds J.B.Grace & D.Tilman), pp. 367 390. Academic Press, San Diego, CA.
  • Berendse, F. 1985 The effect of grazing on the outcome of competition between plant species with different nutrient requirements. Oikos, 44, 35 39.
  • Berendse, F. & Aerts, R. 1984 Competition between Erica tetralix L. & Molinia caerulea (L.) Moench as affected by the availability of nutrients. Acta Oecologica, 5, 3 14.
  • Berendse, F. & Elberse, W.T. 1990 Competition and nutrient availability in heathland and grassland ecosystems. Perspectives in Plant Competition (eds J.B.Grace & D.Tilman), pp. 93 116. Academic Press, San Diego, CA.
  • Berendse, F., Schmitz, M., De Visser, W. 1994 Experimental manipulation of succession in heathland ecosystems. Oecologia, 100, 38 44.
  • Bobbink, R., Hornug, M., Roelofs, J.G.M. 1998 The effects of airborne pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology, 86, 717 738.
  • Brundrett, M., Melville, L., Peterson, L. 1975 Practical methods in mycorrhizal research. Workshop in Conjunction with the 9th North American Conference on Mycorrhizae, Ontario, Canada. Mycologue Publications, Waterloo, Canada.
  • Caporn, S.J.M., Song, W., Read, D.J., Lee, J.A. 1995 The effect of repeated nitrogen fertilization on mycorrhizal infection in heather (Calluna vulgaris (L.) Hull). New Phytologist, 129, 605 609.
  • Coley, P.D., Bryant, J.P., Chapin, F.S. 1985 Resource availability and plant antiherbivore defense. Science, 230, 895 899.
  • Crawley, M.J. 1997 Plant–herbivore dynamics. Plant Ecology (ed. M.J.Crawley), pp. 410 472. Blackwell Science, Oxford, UK.
  • Fitter, A.H. 1985 Functioning of vesicular–arbuscular mycorrhizas under field conditions. New Phytologist, 99, 257 265.
  • Gimingham, C.H. 1960 Biological flora of the British Isles: Calluna vulgaris (L.) Hull. Journal of Ecology, 48, 455 483.
  • Gimingham, C.H. 1972Ecology of Heathlands. Chapman & Hall, London, UK.
  • Goldberg, D.E. 1990 Components of resource competition in plant communities. Perspectives in Plant Competition (eds J.B.Grace & D.Tilman), pp. 27 50. Academic Press, San Diego, CA.
  • Grime, J.P., Hodgson, J.G., Hunt, R. 1988Comparative Plant Ecology. Unwin Hyman, London, UK.
  • Hartley, S.E. 1997 The effects of grazing and nutrient inputs on grass–heather competition. Botanical Journal of Scotland, 49, 317 326.
  • Hashem 1995 The role of mycorrhizal infection in the tolerance of Vaccinium macrocarpon to iron. Mycorrhiza, 5, 451 454.
  • Heil, G.W. & Bruggink, M. 1987 Competition for nutrients between Calluna vulgaris (L.) Hull and Molinia caerulea (L.) Moench. Oecologia, 73, 105 107.
  • Hinds, A.A. & Lowe, L.E. 1980 Application of the Berthelot reaction to the determination of ammonium-N in soil extracts and soil digests. Communications in Soil Science and Plant Analysis, 11, 469 475.
  • Iason, G.R., Hartley, S.E., Duncan, A.J. 1993 Chemical composition of Calluna vulgaris (Ericaceae): does response to fertiliser vary with phenological stage? Biochemical Systematics and Ecology, 21, 315 321.
  • Leake, J.R. & Read, D.J. 1991 Proteinase activity in mycorrhizal fungi. III. Effect of protein, protein hydrolysate, glucose and ammonium on production of extracellular proteinase by Hymenoscyphus ericae (Read) Korf and Kernan. New Phytologist, 117, 309 317.
  • Leake, J.R., Shaw, G., Read, D.J. 1989 The role of ericoid mycorrhizas in the ecology of ericaceous plants. Agriculture, Ecosystems and the Environment, 29, 237 250.
  • Louda, S.M., Keeler, K.H., Holt, R.D. 1990 Herbivore influences on plant performance and competitive interactions. Perspectives in Plant Competition (eds J.B.Grace & D.Tilman), pp. 414 444. Academic Press, San Diego, CA.
  • Marrs, R.H. 1993 Soil fertility and nature conservation in Europe: theoretical considerations and practical management solutions. Advances in Ecological Research, 24, 241 300.
  • Marrs, R.H. & Welch, D. 1991Moorland Wilderness: the Potential Effects of Removing Domestic Livestock, Particularly Sheep. ITE Report to Department of the Environment. Huntingdon, Cambs.
  • Read, D.J. 1983 The biology of the mycorrhiza in the Ericales. Canadian Journal of Botany, 61, 985 1004.
  • Read, D.J. & Bajwa, R. 1985 Some nutritional aspects of the biology of ericaceous mycorrhizas. Proceedings of the Royal Society of Edinburgh, 85B, 317 332.
  • Read, D.J., Koucheki, H.K., Hodgson, J. 1976 Vesicular–arbuscular mycorrhiza in natural vegetation systems. I. The occurrence of infection. New Phytologist, 77, 641 653.
  • Read, D.J. & Stribley, D.P. 1973 Effect of mycorrhizal infection on nitrogen and phosphorus nutrition of ericaeceous plants. Nature, 244, 81 82.
  • Rowland, A.P. 1983 An automated method for the determination of ammonium-N in ecological materials. Communications in Soil Science and Plant Analysis, 13, 49 63.
  • Sharma, A.K., Johri, B.N., Gianinazzi, S. 1992 Vesicular–arbuscular mycorrhizae in relation to plant disease. World Journal of Microbiology and Biotechnology, 8, 559 563.
  • Stribley, D.P. & Read, D.J. 1976 The biology of mycorrhiza in the Ericacae. VI. The effect of mycorrhizal infection and concentration of ammonium nitrogen on growth of cranberry (Vaccinium macrocarpon) in sand culture. New Phytologist, 77, 63 73.
  • Stribley, D.P. & Read, D.J. 1980 The biology of mycorrhiza in the Ericacae. VII. The relationship between mycorrhizal infection and the capacity to utilize simple and complex organic nitrogen sources. New Phytologist, 86, 365 371.
  • Sydes, C. 1988 Recent Assessments of Moorland Losses in Scotland. CSD Notes 43. Nature Conservancy Council, Edinburgh, UK.
  • Tennant, D. 1975 A test of a modified line intersect method of estimating root length. Journal of Ecology, 63, 995 1001.
  • Tilman, D. 1997 Mechanisms of plant competition. Plant Ecology (ed. M.J.Crawley), pp. 239 261. Blackwell Science, Oxford, UK.
  • Watkinson, A.R. & Freckleton, R.P. 1997 Quantifying the impact of arbuscular mycorrhiza on plant competition. Journal of Ecology, 85, 541 546.
  • Welch, D. 1986 Studies in the grazing of heather moorland in north-east Scotland. V. Trends in Nardus stricta and other unpalatable graminoids. Journal of Applied Ecology, 23, 1047 1058.
  • Welch, D. & Scott, D. 1995 Studies in the grazing of heather moorland in north-east Scotland. VI. Twenty-year trends in botanical composition. Journal of Applied Ecology, 32, 596 611.
  • West, H.M. 1996 Influence of arbuscular mycorrhizal infection on competition between Holcus lanatus and Dactylis glomerata. Journal of Ecology, 84, 429 438.
  • Yesmin, L., Gamack, S.M., Cresser, M.S. 1996 Effects of atmospheric nitrogen deposition on ericoid mycorrhizal infection of Calluna vulgaris grown in peat soils. Applied Soil Ecology, 4, 49 60.

Received 15 April 1998revision accepted 3 November 1998