background deposition levels of nutrients
Our data on both the quantity and composition of the bulk deposition (Table 1) differed from measurements at two nearby rainfall monitoring stations (Jordan 1997). Annual bulk deposition levels measured at the Kinnitty and Birr monitoring stations (at distances of 41 and 49 km, respectively) were two to three times lower than our measurements at Clara bog. The amount of oxidized N was comparable with the deposition levels that we measured, but the amount of reduced N was four- to fivefold higher at Clara bog. The elevated atmospheric ammonia deposition (NHx) levels we observed may have resulted from the extensive agricultural activities taking place in the immediate surroundings of Clara bog (Buijsman, Maas & Asman 1987). Compared with the bulk deposition levels of N in the Netherlands (2 g m−2 year−1; Table 1), levels in Ireland were four times lower. High N deposition levels in the Netherlands also resulted in significantly higher ammonium concentrations in the peat moisture compared with those measured in Irish bogs (Fig. 6).
Figure 6. Concentrations (mean ± 1 SE) of ammonium and phosphate at a depth of 0–10 cm in bogs in the Netherlands (NL; n = 12) and Ireland (IR; n = 7). *P = 0·05; **P = 0·001 (t-test).
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In areas with relatively low concentrations of atmospheric pollutants, bulk precipitation on Calluna-dominated vegetation amounts to approximately 60–75% of the total atmospheric input (R. Bobbink, personal communication). The calculated total atmospheric input on Clara bog must have been around 0·6–0·8 g N m−2 year−1, which is within the range of the empirically estimated critical load for ombrotrophic bogs (0·5–1·0 g N m−2 year−1; Bobbink & Roelofs 1995). This was as expected as no expansion of nitrophilous species in ombrotrophic vegetation has so far been observed. The total input levels of N on the experimental plots, including the current background deposition level, were approximately 0·7 (control), 2·7, 4·7 and 8·7 g N m−2 year−1. It must be noted that the annual N load was added in six applications, which is common in fertilization experiments, and this could have led to an imbalance between the supply and demand of nutrients in the vegetation. A laboratory experiment with weekly N applications, however, revealed comparable effects of high N addition rates on the growth of Molinia and Betula (Tomassen et al. 2003). Therefore we assume that the results of this experiment approached reality.
effect of n on rhizosphere chemistry
As N was applied only during the growing season, peat water N concentrations were higher during summer (Fig. 1). Although the vegetation takes up available N during this season, the applied N was completely taken up only at an addition rate of 2 g N m−2 year−1. At higher N addition rates, N was not completely taken up by the vegetation, partly because of the absence of a living Sphagnum layer. Incomplete N uptake by the vegetation was also indicated by the relatively higher fractions of ammonium adsorbed to the peat (Table 3) at addition rates of 4 g N m−2 year−1 and higher. In a similar experiment carried out in the same period at a location on Clara Bog dominated by Sphagnum mosses, addition of 4 g N m−2 year−1 for 3 years resulted in much lower peat moisture N concentrations (Limpens 2003). Sphagnum has a high N uptake rate, resulting in low N concentrations in the peat moisture (Lee & Woodin 1988; Jauhiainen, Wallén & Malmer 1998). In the Netherlands, with a total N deposition level of 4 g m−2 year−1, ammonium concentrations of up to 50 µmol l−1 have been measured. In our experiment, the availability of ammonium in the rhizosphere during winter was comparable with the concentrations measured in the Netherlands, but during the summer the availability of ammonium was much higher due to the N applications (Fig. 1) and the absence of a living Sphagnum layer. During the winter, when no nutrients were applied, the large amounts of precipitation (Fig. 1) probably flushed ammonium, nitrate and sulphate from the peat, resulting in lower concentrations.
The observed decrease in pH during the summer is probably due to increased (bio)geochemical oxidation processes in the dry peat. Oxidation processes generate protons and lead to acidification of the peat (Drever 1997). The addition of N further decreased the pH in the peat moisture. Uptake of ammonium by the vegetation (Raven 1985) and mobilization of protons from the peat cation exchange complex at high ammonium concentrations (Clymo & Hayward 1982), may have been responsible for the observed treatment effect.
As we expected, N addition significantly affected C : N and N : P ratios of the peat (Table 2). Peat C : P ratios, however, were also influenced by N addition. Increased N availability probably stimulated uptake of P, resulting in slightly lower peat P concentrations and significantly higher C : P ratios. The differences in C : N, C : P and N : P ratios of the peat had no significant effects on the mineralization rate (i.e. potential CO2 production). Several studies have found increased mineralization rates at low C : N and C : P ratios (Aerts & Chapin 2000) due to increased nutrient availability for micro-organisms. As the low pH of the peat probably caused the lack of stimulation of the mineralization rate by high N inputs, the potential CO2 production rate was significantly influenced by the pHNaCl of the peat (Fig. 2). An increased pH is known to enhance mineralization by stimulating microbial activity (Smolders et al. 2002). From the above we conclude that desiccation of the peat does not necessary lead to increased mineralization rates, because acidification of the peat as a result of oxidation processes, ammonium uptake by plants and proton exchange processes can inhibit mineralization.
effect of n addition on vascular plants
The above-ground biomass of Molinia increased with the N addition rate (Fig. 3), indicating limitation by N, as has also been found in earlier studies of heathlands (Berendse & Aerts 1984; Roelofs 1986; Heil & Bruggink 1987; Aerts & Berendse 1988). Growth limitation by N was also indicated by the constant foliar N concentrations in Molinia (Table 4), showing that extra available N was used for biomass production. However, foliar N : P ratios ranged from 41 to 52, suggesting that growth was severely limited by P (Koerselman & Meuleman 1996). Kirkham (2001) reported average N concentrations and N : P ratios of 18·5 mg g−1 DW and 21, respectively, in Molinia from upland regions in England and Wales. Foliar N concentrations of Molinia in our experiment were comparable to those measured by Kirkham (2001), but P concentrations were much lower, resulting in higher N : P ratios (Table 4). Despite these very high N : P ratios, the growth of Molinia was still stimulated, indicating that Molinia is a species well adapted to low P availability, as has been found elsewhere (Kirkham 2001; Tomassen et al. 2003).
In contrast, we found no N effect on Betula and E. vaginatum. It is likely that nutrients other than N were limiting to their growth. On drained mires in northern Finland, NPK and PK fertilization has been found to stimulate the growth of Betula pubescens, while N alone had no effect (Penttila & Moilanen 1997). N addition in our experiment significantly increased the foliar N concentration in Betula (Table 4), suggesting that its growth was not limited by N. The N : P ratios show that the growth of Betula was limited by P in all N treatments (Table 4; Koerselman & Meuleman 1996). Optimum nutrition levels for Betula pendula are known to be achieved at N : P ratios between 10 and 12 (Ericsson & Ingestad 1988). Hytönen & Kaunisto (1999) found growth limitation by P at foliar P concentrations below 2 mg g−1 DW. This indicates that the growth of Betula in our experiment was probably constrained by P. In a N addition experiment in the laboratory, growth of Betula in a wet Sphagnum fallax vegetation also seemed to be limited by P (Tomassen et al. 2003).
In our experiment, the growth of E. vaginatum was not stimulated by N addition. Redbo-Torstensson (1994), however, found increased densities of E. vaginatum at addition rates of 1 g N m−2 year−1 and more in central south Sweden, after 4 years. In contrast, fertilization experiments on drained peat sites in southern Norway and Sweden showed stimulated growth of E. vaginatum after NPK and PK fertilization, indicating P or K limitation (Finér & Brække 1991). As in the cases of Molinia and Betula, the N : P ratios suggested that E. vaginatum was limited by P (Table 4). P limitation was also observed in a study by Leith et al. (1999), in which tissue N concentrations of E. vaginatum increased at higher N input levels and were twice those measured in our experiment (19 mg N g−1 DW), while P concentrations decreased at high N deposition levels and were comparable with the concentrations we measured (0·5 mg P g−1 DW; Leith et al. 1999).
In our experiment, regrowth of Calluna was not significantly stimulated by N addition after 3 years, which has been found for Calluna growing in heathland vegetation (Roem, Klees & Berendse 2002). Foliar N concentrations of Calluna increased upon N addition (Table 4) and were in the same range as those measured in the UK, where N concentrations in shoots reached levels of 9 mg g−1 DW at additional N loads of 1·5 g m−2 year−1 (Power et al. 1995; Uren et al. 1997). In a large-scale study by Pitcairn, Fowler & Grace (1995), tissue N concentrations in mature Calluna growing on heathland soil were significantly correlated with the total deposition level of N, whereas Risager (1998) found no effect of N deposition levels on tissue N concentrations in Calluna growing on ombrotrophic bogs. This discrepancy could be explained by suppression of the growth by water shortage, which can only occur in heathland soils, but also by the presence of a Sphagnum layer on bogs, which limits the availability of N for Calluna (Risager 1998). The correlation between N deposition and foliar N concentrations of Calluna in our experiment is probably due to both the absence of a Sphagnum layer and the extremely high N inputs. In our experiment, tissue N : P ratios in Calluna indicated P limitation (29–54), which has been found for Calluna in heathlands (Roem, Klees & Berendse 2002).
Peat moisture P concentrations in the rhizosphere of Irish bogs were very low compared with those measured in Dutch bogs (Fig. 6). Beltman et al. (1996) also found P shortage in Irish blanket bogs. Molinia and Betula were both able to grow around wooden poles on Clara bog, where the availability of both N and P was high as a result of increased input by bird droppings (H.B.M. Tomassen & A.J.P. Smolders, unpublished data). The high P concentrations in Dutch bogs probably enabled the expansion of Molinia, Betula and E. vaginatum at high N deposition levels. Why most of the Dutch bogs are rich in P remains unclear. There is not much information about the input of atmospheric P, but it probably ranges from 0·01 to 0·1 g P m−2 year−1, the main sources being fine soil particles, pollen and the burning of plant material, coal and oil (Newman 1995). We did indeed measure higher P deposition levels in the Netherlands than in Ireland (Table 1). Increased P availability in Dutch bogs often results from former agricultural use, such as buckwheat fire cultivation (Joosten 1995) or from the inflow of nutrients from surrounding pastures, which are extensively fertilized (Koerselman, Bakker & Blom 1990). Several bogs are located in former heathland pools, which could have been enriched with P in the past by large numbers of waterfowl, as bird droppings contains high concentrations of P (H.B.M. Tomassen & A.J.P. Smolders, unpublished data).
effect of n on regrowth of lichens
Lichens are very sensitive to atmospheric pollution and have almost completely disappeared from ombrotrophic bogs in the Netherlands (H.B.M. Tomassen, personal observations), and Cladonia portentosa has declined under Dutch forest canopies since 1960 (Van Dobben, De Witt & Van Dam 1983). In our experiment, regrowth of Cladonia portentosa was suppressed at high N addition rates (Fig. 5). We cannot exclude the possibility that the low application frequency could have stimulated the detrimental effects of N on Cladonia portentosa, although the disappearance of lichens at high nutrient availability has been confirmed by various other studies (Press et al. 1998; Gordon, Wynn & Woodin 2001). Discoloration and die-back of Cladonia portentosa in Danish heathlands has been associated with atmospheric N pollution (Søchting & Johnsen 1987). Vagts & Kinder (1999) found that NPK fertilization stimulated the growth of Cladonia portentosa, but P or N alone had a negative effect. In addition to the effects of high N deposition levels, S pollution may also have had deleterious effects (Farmer, Bates & Bell 1992). Tissue N and S concentrations in Cladonia portentosa were significantly elevated at addition rates above 2 g N m−2 year−1 (Table 4). Several other studies have found an effect of N deposition levels on the tissue N concentrations in Cladonia portentosa (Søchting 1990; Hyvärinen & Crittenden 1998a). Cladonia portentosa transplanted to sites subjected to high N deposition levels had increased N concentrations in both apices and bases due to retarded growth at these locations (Hyvärinen & Crittenden 1998b). Because lichens are very sensitive to S as well as N pollution (Poikolainen et al. 1998), we think that both the high S and high N loads hampered the regrowth of Cladonia in our experiment. Fortunately, this seems to be a reversible process as a systematic mapping of epiphytic lichens on conifers in Finland in 1985–86 and 1995 showed an increase in lichen abundance due to decreasing S deposition levels (Poikolainen et al. 1998). The coverage of Cladonia in our experiment, however, had not yet changed a year after the experimental N additions had ended (data not shown).
invasion of bogs: desiccation or n effects?
Is the invasion of bogs in the Netherlands by species such as Betula and Molinia a result of desiccation or long-term high atmospheric N loads? The results of our experiment show that experimental elevation of N deposition to Dutch levels did indeed stimulate the growth of Molinia under desiccated conditions. However, this was not the case for Betula and E. vaginatum, most probably because their growth was limited by P instead of N. Foliar N : P ratios indicated that the growth of Molinia, Betula and E. vaginatum was limited by P. Despite this presumed P limitation, however, Molinia was able to increase its biomass at increased N addition rates, although Betula and Eriophorum clearly were not. The N : P ratio tool developed by Koerselman & Meuleman (1996) is based on results obtained at the vegetation level and not for individual plant species. Our results indicate that the N : P ratio is not a suitable tool for detecting the absence of N limitation in Molinia. This is in agreement with findings by Güsewell & Koerselman (2002), who found that the N : P ratios cannot predict the responses of individual plant species to fertilization.
The effects of desiccation on the invasion of bogs by Molinia and Betula are likely to be smaller than those of increased N availability. Experimental N fertilization of Molinia and Betula in a wet vegetation dominated by S. fallax revealed consistent effects of high N addition rates (Tomassen et al. 2003). Under wet conditions, growth of Molinia was also stimulated by N (4 g m−2 year−1), whereas that of Betula was probably limited by P instead of N. It is plausible that the drastic changes in vegetation composition in Dutch bogs can be ascribed to the combined effects of high N deposition levels and relatively high P availability. We propose that invasion of Betula in bogs can only take place in conditions of simultaneously high N and relatively high P availability. If N deposition levels increase while P availability remains extremely low, only Molinia is likely to be able to outcompete other species.