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Keywords:

  • fertilization experiment;
  • herbivory;
  • nitrogen;
  • plant–species interactions;
  • plant succession

Abstract

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

1 A factorial fertilizer experiment was conducted in a 15-year-old coastal barrier salt marsh with a low soil nitrogen content, and in an older 100-year-old marsh with a higher nitrogen content. Plots were fertilized at high and low marsh elevations in both marshes. Nitrogen and phosphorus were applied at low and high concentrations both separately and in combination in each of 3 successive years.

2 Nitrogen limited above-ground plant growth in both young and old salt marshes in all years. Phosphorus limitation of plant growth was apparent in the first year in the young marsh and in the last year in both marshes. In young marshes with low soil organic matter, phosphorus limitation may occur. In addition, phosphorus limitation occurs at both successional stages when a marsh is saturated with nitrogen.

3 Plant species that are typical of nitrogen-rich habitats and late successional stages significantly increased in biomass after fertilization. Limonium vulgare, a low stature species of early and intermediate successional stages, decreased in biomass, whereas the taller Elymus pycnanthus and Artemisia maritima increased. After 3 years of fertilization, plant species composition in a young marsh was similar to the species composition in an unfertilized older marsh. Fertilization of a 100-year-old marsh, however, still resulted in a change in plant species composition, suggesting that succession was still occurring and that, overall, plants in marshes of different age are similar in their response to fertilization.


Introduction

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

Measurements of nutrient limitation are important in understanding the mechanisms involved in plant competition and vegetation succession (DiTommaso & Aarssen 1989). Such studies provide data on the importance of nutrients as an ecological factor (Lee et al. 1981) and allow the prediction of changes in both plant production and species composition over time. Most studies of primary succession show an increase in resource availability and plant standing crop over time (Crocker & Major 1955; Bormann & Sidle 1990; Gerlach et al. 1994; Olff et al. 1997). According to Tilman's resource-ratio hypothesis, competition for nutrients will be important at early successional stages where the majority of plants are relatively small. Competition for light becomes more important at late successional stages where tall growing plants become dominant (Tilman 1985, 1988). Fertilization studies can simulate the successional pathway by increasing nutrient availability, thus allowing tall growing plants to become dominant and competition for light to increase.

Although salt marshes are relatively rich in nutrients, plants have to cope with salinity and flooding that results in high costs for maintenance processes (Adam 1990). Some studies have shown that plant production in west European salt marshes is limited by nitrogen (Jefferies & Perkins 1977; Kiehl et al. 1997), which is needed for the synthesis of osmotically active compounds (Stewart & Lee 1974; Jefferies 1980). Others have reported phosphorus limitation (Tyler 1967; Pigott 1969). During succession, salt marshes accumulate organic matter, in part due to the input of nutrients via atmospheric deposition, and in part as a consequence of tidal inundation (Osgood & Zieman 1993; Olff et al. 1997). By artificially enhancing nutrient availability, succession may be accelerated (DiTommaso & Aarssen 1989).

Plant species composition has been described along a successional gradient in a coastal-barrier salt marsh in the Netherlands (Bakker et al. 1993; Olff et al. 1997; van Wijnen & Bakker 1997). As natural accumulation of nitrogen may have led to changes in production and in plant species composition in this coastal barrier salt marsh, it may be an important factor determining the rate of vegetation succession (Marrs et al. 1983). This study was devised to test experimentally whether nitrogen and phosphorus limit plant production along the successional gradient, and whether vegetation succession can be mimicked by artificially enhancing nitrogen and phosphorus availability. As the early successional stages are low in soil organic matter content, we assume that nitrogen or phosphorus limitation of plant growth occurs at these stages (Morris 1991). After fertilization, plant species composition is expected to change towards dominance of those taller growing species that occur naturally at late successional stages in this coastal barrier marsh.

Materials and methods

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

Site description

The experiment was conducted in a coastal barrier salt marsh on the island of Schiermonnikoog in the Netherlands (53°30′N, 6°10′E). Several successional stages occur on this island (Olff et al. 1997). Vegetation succession starts on a bare sandbank and marshes can then develop in areas that are sheltered by dunes created by wind deposition of sand. Because the marsh is expanding eastwards, young marshes are located in the eastern part, whereas older marshes are located in the western part of the island. Nitrogen content in the upper 50 cm of the soil in young marshes is c. 200 g N m−2 but rises to more than 600 g N m−2 in older parts (Olff et al. 1997; van Wijnen & Bakker 1997). The net N-mineralization rate is c. 2.5 g N m−2 year−1 in young marshes and increases towards 12.7 g N m−2 year−1 in older marshes (H.J. van Wijnen, unpublished data). Soil salinity is relatively high in older marshes. Salinity of soil water is higher at low elevations in the marsh (13.3 g NaCl l−1–20.6 g NaCl l−1, compared with 2.8 g NaCl l−1–10.1 g NaCl l−1 at higher elevations; H.J. van Wijnen, unpublished data; de Leeuw et al. 1990). Soil pH varies between 7 and 8 at all successional stages (H.J. van Wijnen, unpublished data). Plant species composition changes from dominance by Spergularia media, Limonium vulgare and Festuca rubra at early successional stages, towards Artemisia maritima, Halimione portulacoides and Elymus pycnanthus at later stages (Olff et al. 1997; nomenclature of plant species follows Tutin et al. 1964–80). Distribution of each of these species appears to be mainly dependent on marsh elevation. Herbivores such as geese, hares and rabbits forage mainly in young marshes in the east (van de Koppel et al. 1996). Recently, hares were found to retard vegetation succession by c. 30 years by preventing Halimione portulacoides and Artemisia maritima from reaching dominance, mainly as a result of grazing during the winter period (van der Wal 1998).

Experimental procedure

Two successional stages were selected for the fertilization experiment: a young 15-year-old marsh, and an older 100-year-old marsh. At each stage, four sites were chosen that were representative of that stage with respect to plant species composition. Two of these four sites were located at a high marsh elevation (80 cm above mean high tide level) and two at a low marsh elevation (40 cm above mean high tide level). This resulted in two replicated sites per elevation and successional stage that were at least 20 m apart. At each site, nine fertilization treatments were applied to an experimental block, with each treatment replicated three times within a block (Fig. 1). Fencing excluded geese, hares and rabbits from each block. Plots within a block measured 1 × 1 m and were 10 cm apart from each other, except where a path, 0.5 m wide, was established to allow us to walk through the centre of each block.

image

Figure 1. Fertilization scheme, indicating the block design that was used. C = control plot; n = low concentration of nitrogen; N = high concentration of nitrogen; p = low concentration of phosphorus; P = high concentration of phosphorus. Three replicates per treatment were used in each block.

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Where appropriate, nitrogen was applied in solution as NH4NO3 at a low (5 g N m−2 year−1) or high concentration (25 g N m−2 year−1). Phosphorus was also applied in solution as NaH2PO4 at a low (2 g P m−2 year−1) or high concentration (10 g P m−2 year−1). A single solution of the two salts was used on plots that received additions of both nitrogen and phosphorus. Plots were fertilized in early May in 3 consecutive years from 1994 when 1 L of fertilizer solution was applied followed by 1 L of fresh water; control plots received 2 L of fresh water.

In early August, above-ground biomass was sampled in a 10 × 25-cm area of each plot, using a different portion of the plot in each year. In August 1995, root samples were also collected in control plots and in high fertilizer (NP) treatment plots by sampling a soil core of 6.5 × 6.5 × 25 cm deep. Dead roots were not separated from living roots. Above-ground plant samples were separated into dead and living shoots. In control plots and in NP treatment plots, living shoots were sorted per species in 1995 and 1996. Roots and above-ground plant parts were rinsed, dried at 70 °C for 48 h and weighed.

Statistical procedure

The package SPSS/PC+ (Norusis 1990) was used for statistical analyses. When necessary, data were transformed to meet statistical assumptions. A three-way anova that included block effects was used to calculate main effects, two-way interactions and three-way interactions of N, P and elevation on above-ground plant biomass. Data were analysed separately for each successional stage and each year.

A Tukey test was used after one-way anova to test for differences in above-ground biomass in the control plot between the 3 years of the study. The test was done separately for both the young and old marsh. Similarly, the Tukey test was used to test for differences in above-ground biomass and root biomass in the control plots between successional stages. Tests for shoot biomass were done for each year separately; root biomass was tested for 1995 only. When multiple comparisons were made, the significance level was reduced to 0.01 in order to meet Bonferonni adjustments.

The response of individual plant species to a high concentration of fertilizer was calculated by taking the difference in their mean biomass between the control plots and the NP plots in 1995 and 1996. A similar root response was calculated, but for 1995 only and for all species combined. A Tukey test was used after one-way anova to test for differences in these responses.

Results

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

Plant biomass: a test of the assumption that marshes are nutrient limited

Nitrogen limited above-ground plant biomass production at both successional stages and in all years (Table 1). Phosphorus limited plant biomass production in the young marsh in 1994 and in both marshes in 1996. High and low marshes differed significantly at both successional stages in 1995 but only in the old marsh in 1994. No interaction effects were significant, except for the N × elevation interaction in the old marsh in 1996.

Table 1.  Effects of nitrogen (N), phosphorus (P) and marsh elevation (elevation) on total above-ground biomass at two successional stages and 3 consecutive years. F-values of a three-way anova with block as a factor
Young marshOld marsh
Source of variationd.f.199419951996199419951996
  • *

    P  < 0.05,

  • * *

    P  < 0.01,

  • * * *

    P  < 0.001.

N229.95***32.62***15.11***19.02***18.64***42.31***
P23.19*3.073.85*0.710.454.98**
Elevation10.0623.42***0.1414.64***121.11***0.98
N × P41.151.310.761.061.072.07
N × elevation20.440.670.391.112.4911.11***
P × elevation20.022.080.141.050.522.55
N × P × elevation40.100.261.340.341.692.07
Block29.56***1.577.74***4.53*0.229.06***

Biomass production was stimulated most in high nitrogen treatments (Fig. 2). Effects of phosphorus addition alone were relatively small compared with additions of phosphorus and nitrogen in combination. Mean litter and shoot biomass in the unfertilized plot significantly increased at the 0.01 significance level in the young marsh only during the experimental period (one-way anova; young marsh: F2,33 = 14.6, P < 0.0001; old marsh: F2,33 = 3.9, P = 0.0294). Because geese, hares and rabbits were excluded from the experimental plots at the beginning of the experiment, these results indicate that grazing by these herbivores had a strong impact on above-ground biomass in the young marsh. Differences in total above-ground biomass between successional stages for unfertilized plots were only significant in 1994 (one-way anova; 1994: F1,22 = 33.0, P < 0.0001; 1995: F1,22 = 4.0, P = 0.0582; 1996: F1,22 = 1.6, P = 0.2159). This indicates that initial differences between successional stages were mainly due to the higher grazing intensity that occurs in the young marsh. After 3 years without grazing, both marshes were similar in total biomass production and in their response to fertilization.

image

Figure 2. Mean above-ground biomass (litter + living shoot) for each treatment (±SEM; n = 12), presented for each successional stage and year of fertilization.

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Plant-species composition: a test of mimicking succession in response to fertilizers

Most of the plant species that occur naturally in fertile habitats and that are dominant at later successional stages showed an increase in above-ground biomass after fertilization, although few results were statistically significant (Table 2). However, biomass of Elymus pycnanthus increased at both successional stages, whereas biomass of Artemisia maritima and Atriplex prostrata increased in the old marsh only. One species, Limonium vulgare, which was dominant at early successional stages, significantly decreased in biomass after fertilization. Fertilization had no significant effect on overall root biomass of plants at either stage in 1995. Root biomass in the older marsh was approximately twice as high as that in the young marsh (Fig. 3). Differences between successional stages in total root biomass were significant (one-way anova; F1,22 = 21.3, P < 0.0001).

Table 2.  Mean plant response of individual species (g m−2) and standard error of the mean (SE) after fertilization with nitrogen and phosphorus at a high concentration (see text). F-values of a one-way anova
Young marshOld marsh
 Marsh elevationResponseSEFResponseSEF
  • *

    P  < 0.05;

  • * *

    P  < 0.01.

RootsBoth198.4119.13.20 −124.394.10.15
Festuca rubraHigh  18.451.00.14 −8.519.60.22
Agrostis stoloniferaHigh −10.614.00.52   
Glaux maritimaLow0.91.40.164.58.20.22
Juncus gerardiLow    −34.435.91.02
Limonium vulgareLow −65.522.38.66** −19.39.83.78
Plantago maritimaLow −23.225.01.01   
Puccinellia maritimaLow  65.588.20.44   
Spergularia mediaLow −12.96.93.374.25.20.66
Elymus pycnanthusHigh208.960.15.22*  286.993.14.92*
Artemisia maritimaLow  59.844.01.49  486.6180.05.74*
Halimione portulacoidesLow  58.246.31.7469.469.41.00
Atriplex prostrataLow2.41.91.57  194.074.26.82*
image

Figure 3. Mean rhizome and root biomass (±SEM; n = 12) in control and fertilized plots for each successional stage in 1995.

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The relative contribution of each species to the total biomass changed after fertilization (Fig. 4). At high marsh elevations Elymus pycnanthus became abundant at the expense of Festuca rubra, especially in the young marsh where Elymus was not abundant previously. Plant species composition in the young marsh was more similar to that in the old marsh after fertilization. Plant species composition at the low-marsh elevation also changed. In the young marsh, Limonium vulgare decreased in abundance and Festuca rubra increased. In the old marsh, however, Festuca rubra and Juncus gerardi decreased after fertilization, whereas Artemisia maritima and Atriplex prostrata (indicated as ‘other’) increased in abundance.

image

Figure 4. Relative contribution as percentages of different plant species to the total above-ground living biomass for both successional stages in 1996, which was the last year of fertilization. Species distributions for a high and low marsh are presented separately.

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Discussion

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

As expected, we found a clear effect of nitrogen addition on plant biomass and species composition. Differences between successional stages, however, were small and only significant in the first year of fertilization. In addition, we found phosphorus limitation in the young marsh, which was attributed to a lack of soil organic matter. No effect of treatments on root biomass was found. Plant species responded to nutrient addition as predicted. Plants with a tall growth habit increased in biomass after fertilization, whereas other species either failed to respond or else decreased in biomass. Nitrogen appears to play a major role in plant succession on these coastal barrier marshes even after 100 years of natural succession.

We have to emphasize that the two replicated sites at each successional stage are in fact pseudoreplicates and therefore no statistical distinction can be made between site effects and marsh-age effects (Berendse et al. 1998). We believe, however, that these stages represent succession on this coastal barrier island. Measurements in permanent quadrats that remained in place for 37 years on another coastal-barrier island in the Netherlands revealed similar transitions in plant species composition that represented the different successional stages on Schiermonnikoog (Leendertse et al. 1997a). In addition, successional stages on two other Wadden Sea coastal barrier salt marshes were very similar to the stages on Schiermonnikoog with respect to soil nitrogen content and plant species composition (van Wijnen & Bakker 1997). Comparison of successional stages, however, should be done carefully. Climatological conditions, the mineral substrate and flooding regime should be comparable between stages. In our study, the sites were situated close together (within 8000 m), making climatological differences unlikely, and the mineral substrate always consisted of a sandy sublayer with a layer of clay on top. Because sites of similar elevation were studied (80 cm or 40 cm above mean high tide level), we assumed that the successional stages experienced a similar flooding regime.

Phosphorus limitation

When soil pH is high (7–8), which is the case in most salt marsh soils, calcium phosphate is a dominant form of inorganic P (Broome et al. 1975). This form of phosphorus is probably not directly available for plant uptake (Olff et al. 1993). Other forms of phosphorus are iron and aluminium phosphates. These forms of phosphorus become more soluble, and therefore more available to plants, when reducing conditions in the salt marsh soil increase due to clay deposition (Broome et al. 1975). Thus the phosphorus limitation at the early successional stage may have been caused by a relatively low clay content (Olff et al. 1997; van Wijnen & Bakker 1997). During salt marsh development, clay is deposited on the marsh surface and this may increase the amount of available phosphorus, leading to the absence of phosphorus limitation in the older marsh (Olff et al. 1997). In plots that received nitrogen for 3 years, plant standing crop was limited by phosphorus at both successional stages. This indicates that when nitrogen supply is sufficient, phosphorus becomes limiting in salt marshes (Cargill & Jefferies 1984).

Nitrogen limitation

Nitrogen limitation of plant growth occurs at both successional stages. As the rate of clay accretion in coastal barrier marshes is low compared to that of other European (mainland) salt marshes (Bakker et al. 1993), soil nitrogen content is also low in this type of marsh, even after 100 years of clay accumulation. Although nitrogen mineralization rate increased along the same successional gradient (van Wijnen et al. 1999), above-ground biomass production remained limited by nitrogen. Biomass production may also be inhibited by factors other than nitrogen and phosphorus. Salinity and soil moisture content in particular may limit plant production in years when rainfall deficit is high (de Leeuw et al. 1990; Kiehl et al. 1997). Some plants in a saline environment may increase their salt tolerance by producing nitrogen-based, osmotically active compounds (Stewart & Lee 1974). Nitrogen fertilization may result in an increased production of these compounds that enables plants to reallocate internal nitrogen for growth (Cavalieri & Huang 1981). It remains questionable, therefore, whether the availability of either nitrogen or salt limits the growth of these plants.

Grazing effects appeared to be mainly responsible for the observed differences in above-ground standing crop between successional stages (Fig. 5). As grazing intensity of hares, rabbits and geese was higher in young marshes (van de Koppel et al. 1996), the effect on shoot biomass was more pronounced there. When neither marsh was grazed by herbivores, shoot biomass was similar between successional stages. When fertilization increased nitrogen availability, shoot growth was stimulated to the same extent at both successional stages, whereas no effect on root biomass was observed.

image

Figure 5. Schematic changes in shoot and root biomass production during succession. In addition, the potential shoot biomass is indicated when the marsh is not grazed (grazing effect) and when nutrients are in abundance (NP effect).

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Plant succession

Vegetation succession on coastal barrier salt marshes in Europe has been studied extensively (Roozen & Westhoff 1985; Bakker 1989; Leendertse et al. 1997a; Olff et al. 1997; van Wijnen & Bakker 1997). Tall growing species such as Elymus pycnanthus, Artemisia maritima and Halimione portulacoides dominate late successional stages and it has been suggested that nitrogen is a critical factor in the development of these plant communities (Leendertse et al. 1997b; Olff et al. 1997; van Wijnen & Bakker 1997). In these studies, however, direct evidence was lacking. In the present study we found a change in plant species composition and in production when nitrogen and phosphorus availability was enhanced artificially, both in a young and an old marsh. Successional change in plant community composition was therefore accelerated by artificially increasing nitrogen and phosphorus availability in the young marsh. Others have reported similar changes in plant species composition towards species that are characteristic of more fertile sites when plots are fertilized for a long time (Chapin et al. 1986; DiTommaso & Aarssen 1989; Elberse & Berendse 1993).

According to Tilman's resource-ratio hypothesis, competition for nutrients changes to competition for light at late successional stages. Our results indicate that at least competition for nutrients is present at both successional stages, because the biomass of tall growing plants increased when fertilized. This implies that the smaller plants may have been limited by another factor. Differences in phenology, however, may be involved too. The increase in biomass of tall growing plants irrevocably results in a further decrease in the amount of available light for other species. Competition for light therefore may become more important at late successional stages.

Our results support the hypothesis that nitrogen is an important determinant of successional processes in these marshes (Lee et al. 1981). Because both successional stages responded similarly to nitrogen addition, both stages appear to be transitional phases (Chapin et al. 1986). In time, we predict that these marshes may be released from nutrient limitation and extensive areas will be covered by tall growing plants such as Artemisia maritima and Elymus pycnanthus.

Acknowledgements

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

We would like to thank Bas Kers and Edwin van Hooff for their help with the separation of plant species, and Jelte van Andel, Wim Wolff and two anonymous referees for critical comments on earlier versions of the manuscript. We are especially grateful to Bob Jefferies and Lindsay Haddon, who improved the manuscript considerably.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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Received 24 April 1998revision accepted 19 September 1998