Nutrient impoverishment and limitation of productivity after 20 years of conservation management in wet grasslands of north-western Germany

Biological Conservation 142 (2009) 2941–2948

Contents lists available at ScienceDirect

Biological Conservation journal homepage: www.elsevier.com/locate/biocon

Nutrient impoverishment and limitation of productivity after 20 years of conservation management in wet grasslands of north-western Germany Yvonne Oelmann a,*, Gabriele Broll b, Norbert Hölzel c, Till Kleinebecker c, Andreas Vogel c, Peter Schwartze d a

Professorship of Soil Geography/Soil Science, Geographic Institute, Johannes Gutenberg University Mainz, Johann-Joachim-Becher-Weg 21, 55128 Mainz, Germany Institute for Spatial Analysis and Planning in Areas of Intensive Agriculture (ISPA), University of Vechta, P.O. Box 1553, 49364 Vechta, Germany c Institute of Landscape Ecology, University of Münster, Robert-Koch-Str. 26-28, 48149 Münster, Germany d Biological Station of the County Steinfurt, Bahnhofstr. 71, 49545 Tecklenburg, Germany b

a r t i c l e

i n f o

Article history: Received 20 February 2009 Received in revised form 8 July 2009 Accepted 25 July 2009 Available online 20 August 2009 Keywords: Wet meadows Nutrient impoverishment PK fertilization N:P ratio N:K ratio

a b s t r a c t European wet grasslands are characterized by high diversity of plant and animal species but are threatened by intensive land use. Although preservation or restoration of species-rich wet grasslands requires low nutrient availability that could be achieved by long-term management, studies monitoring nutrient removal are lacking. Our objective was to assess the long-term effect of management (mowing twice a year without or with PK fertilization for 20 years) on (i) productivity and nutrient removal with the harvest, (ii) the type of nutrient limitation, and (iii) plant species richness in wet grasslands in north-western Germany considering the differences between organic and mineral soils. Initially low nutrient availability in soil led to decreased productivity and base cation removal with harvest particularly on mineral soils after six years of mowing twice a year without fertilization. On mineral soils, N:K ratios indicated limitation of plant growth by K. On organic soils, neither productivity nor K removal with the harvest changed with time suggesting additional K input probably caused by rising groundwater. On organic soils, K:P ratios and a significant decrease of productivity with increasing N:P ratios suggested P limitation. Plant species richness was maintained or even slightly increased by mowing twice a year without fertilization but mainly comprised species that were already present at the study sites. Productivity and N, P, K, and Mg removal with the harvest was significantly increased by mowing twice a year with PK fertilization while species richness was maintained. After 10 years, N:K ratios indicate K limitation even for mowing twice a year with PK fertilization. In case of initially low nutrient availability in soil, cautious PK fertilization and mowing can be recommended to meet demands of agriculture and nature conservation. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction European wet grasslands characterized by groundwater levels near the soil surface on acidic to calcareous soils serve as a habitat for many endangered plant and animal species such as meadow birds (Bakker and Berendse, 1999; Liira et al., 2008). Seminatural species-rich grasslands depend on farming systems of low intensity. Consequently, these ecosystems are threatened by intensification of agricultural management such as high fertilizer application rates or deep drainage (Bakker and Berendse, 1999; Bakker et al., 2002). Nutrient impoverishment to conserve or restore speciesrich wet grasslands might result in positive feedbacks on the

* Corresponding author. Tel.: +49 61313922137; fax: +49 61313926861. E-mail addresses: [email protected] (Y. Oelmann), gbroll@ispa. uni-vechta.de (G. Broll), [email protected] (N. Hölzel), [email protected] (T. Kleinebecker), [email protected] (A. Vogel), biologische. [email protected] (P. Schwartze). 0006-3207/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2009.07.021

vertebrate and invertebrate fauna (Plum, 2005; Broll et al., 2002), however, opposing effects of rewetting and reduced nutrient availability in soil complicate predictions (Ilg et al., 2009; Felske et al., 2000; Broll et al., 2002; Hemerik and Brussaard, 2002). The success of measures to conserve or restore species-rich wet grasslands is controlled by complex interactions among many factors: (i) nutrient availability in soil associated with soil substrates, i.e. organic or mineral soils, or with intensity of former land use (Berendse et al., 1992; Pegtel et al., 1996), (ii) atmospheric nutrient deposition (Bobbink et al., 1998; Wassen et al., 2005), (iii) nutrient concentrations in groundwater – in case of rewetting – (Bakker and Berendse, 1999), (iv) seed bank and recruitment conditions (Isselstein et al., 2002; Hölzel, 2005), or (v) dispersal limitation, i.e. distance to neighboring species-rich grasslands (Bakker and Berendse, 1999; Bakker et al., 2002; Rosenthal, 2006). Predictions on the success of management measures based on short-term studies may not correctly reflect future developments of the wet grasslands, if only few of the relevant factors are considered

2942

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948

(Bakker et al., 1996). However, long-term studies might facilitate evaluation of management measures even if restricted to a subset of relevant factors highlighting the importance of long-term studies. There are some long-term studies on effects of different management on plant species composition and successional changes in dry to mesic grasslands (Hansson and Fogelfors, 2000; Moog et al., 2002; Silvertown et al., 2006), but only few in wet speciesrich grasslands (Bakker, 1989; Bakker et al., 2002; Güsewell et al., 1998). Although the establishment and persistence of plant species in species-rich grasslands are positively affected by low nutrient availability (Janssens et al., 1998; McCrea et al., 2004; Wassen et al., 2005), studies on long-term effects of management measures on nutrient removal with the harvest as an indicator of nutrient impoverishment are rare. Findings in other types of grasslands (e.g., Smits et al., 2008) cannot be transferred to wet grasslands, since in wet grasslands nutrient availability is mainly controlled by high groundwater levels that induce anaerobic conditions in soil and, thus, influence uptake of nutrients by plants (Keplin and Broll, 2002). To our knowledge, there are no long-term studies on nutrient removal with the harvest in wet grasslands. However, to balance requirements of nature conservation (e.g., increasing the number of total species or of endangered species) and requirements of low-intensity agriculture (e.g., yield and fodder quality for ruminants, Donath et al., 2004), profound knowledge on nutrient removal with the harvest is of crucial importance. Hay-making will lead to nutrient impoverishment in the long run, particularly for K and Mg (Olde Venterink et al., 2002; McCrea et al., 2004), thereby improving conditions for establishment and persistence of endangered plant species. On the other hand, one of these nutrients may limit plant growth resulting in reduced yield and fodder quality. Therefore, not only nutrient impoverishment but also the identification of the nutrient limiting plant growth needs to be addressed if aiming to improve management in nature conservation. Our objective was to assess the long-term effect of management (mowing twice a year without [2xM0] or with PK fertilization [2xMPK] for 20 years) in wet grasslands in north-western Germany on (i) productivity and nutrient removal with the harvest, (ii) the type of nutrient limitation, and (iii) plant species richness. A particular focus was given to differences between organic and mineral soils. 2. Materials and methods 2.1. Study sites and sampling In 1987, experiments were established to study the effects of different management treatments in wet meadows in north-western Germany (Schwartze, 1992). Seven study sites in four nature reserves in the ‘‘Münsterland” region were selected on mineral (n = 4) and organic soils (n = 3, Table 1). The study area is charac-

terized by an oceanic climate with a precipitation of 700– 850 mm per annum evenly distributed throughout the year and a mean annual temperature of 9.0 °C (DWD, 2007). Inundation of the study sites (= water table reached soil surface) occurred during 4–11 months mainly from autumn to spring. During the growing season, water tables of the study sites were below the soil surface (Table 1). Further details on initial vegetation and successional changes in vegetation during the study period can be found in Schwartze (1992, 2003) and Poptcheva et al. (2009). For all seven study sites, plots that were mown twice a year without fertilization (2xM0) were established on an area of 1000 m2 (Table 1). Because of time and money constraints on three of the seven study sites, fertilized plots that were also mown twice a year (2xMPK) were established on an area of 50 m2 in addition to the non-fertilized plots (Table 1). Fertilization of 2xMPK started in 1989 and included 2.62 g P m 2 and 9.96 g K m 2 applied once a year in early spring on the whole area of the plot. During the experimental course, cover abundance classes for individual vascular plant species were recorded visually at four fixed 4 m2 subplots for each study site and management treatment (2xM0 n = 7, 2xMPK n = 3). To document initial site conditions, soil was sampled as one composite sample per plot comprising 30 individual and randomly distributed soil cores (diameter 0.02 m; soil depth 0–0.05 m) in October 1988. To determine productivity aboveground biomass was harvested by cutting eight randomly selected quadrats of 0.25 m2 for each plot in 1987, 1988, 1993, 1998, and 2007. Harvested biomass was dried at 80 °C for 48 h and weighted.

2.2. Chemical analyses Field-fresh soil samples were sieved to <2 mm. The pH of fieldfresh soil samples was analyzed with a glass electrode (type E 50, WTW, Weilheim, Germany) in a soil: water suspension (w/v 1:2.5). To determine P and K availability in soil, sieved samples were air dried and extracted with Calcium lactate solution (DL method, Neyroud and Lischer, 2003). After drying, three out of eight samples of harvested biomass per plot were ground with a vibrating cup mill (Siebtechnik GmbH, Mühlheim a. R., Germany). Samples were digested by heating to 450 °C and 600 °C followed by addition of 0.5 M HCl (Jones et al., 1991). Digests were heated in a sand-bath and after cooling filtered through ashfree paper filters (Schleicher and Schuell 790, Germany). Samples collected in 2007, were ground to pass a 1-mm screen using a Cyclotec 1093 mill (Foss, Höganäs, Sweden) and digested in a microwave (MLS Start 1500, Milestone, Bergamo, Italy) with concentrated nitric acid (65%) and hydrogen peroxide (35%). We might have introduced an error by switching to another digestion procedure during the experimental course. However, this error was supposed to be very small, because Mingorance (2002) did not find significant differences between nutrient concentra-

Table 1 Characterization of the experimental sites. Former land use, initial vegetation, and soil types (FAO, 2006) were extracted from Schwartze (1992). Maximum water table depth during the growing season according to Ruville-Jackelen (1994). 2xM0 = mown twice a year without fertilization; 2xMPK = mown twice a year with PK fertilization.

a

Nature reserve

Former land use

Initial vegetation

Soil

Water tablea

Management

Heubachwiesen Düsterdiek Düsterdiek Strönfeld Strönfeld Saerbeck Saerbeck

Mown pasture/meadow Meadow Meadow Permanent pasture Mown pasture/meadow Mown pasture Permanent pasture

Bromo-Senecionetum caricetosum nigrae Bromo-Senecionetum typicum Carex acutiformis community Lolio-Cynosuretum typicum and lotetosum Bromo-Senecionetum caricetosum nigrae Bromo-Senecionetum caricetosum nigrae Lolio-Cynosuretum typicum

Histosol Histosol Histosol Gleyic Podzol Gleyic Podzol Eutric Gleysol Eutric Gleysol

<0.5 <0.9 <0.4 <1.7 <1.4 <0.8 <1.7

2xM0 2xM0, 2xMPK 2xM0 2xM0 2xM0 2xM0, 2xMPK 2xM0, 2xMPK

Below surface (m).

2943

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948

A 1000 harvested biomass (g m-2 a -1)

tions in digests of a microwave procedure and of conventional wet digestion. Because soils did not contain carbonates (Schwartze, 1992), organic C (Corg) concentrations were equal to total C concentrations which were analyzed with an elemental analyzer (NA 1500, Carlo Erba, Milan, Italy). Similarly, N concentrations in soils and harvested biomass were measured by means of the elemental analyzer. In the digests of harvested biomass and in the extracts of soil samples, P concentrations were determined photometrically (550 SE, Perkin Elmer, Waltham, USA) as phosphate forming a molybdenum blue complex (Murphy and Riley, 1962). We measured K concentrations in digests and in soil extracts with a flame photometer (PFP 7, Jenway, Essex, UK). Calcium and Mg concentrations in digests were determined by means of atomic absorption spectrometry (AAS 1100, Perkin Elmer, Waltham, USA).

900

a

A

1998 2007

800

A a

700 a

a

600

a

ab

500

b

a

b

400

a a

c

300

B

2.3. Calculations and statistical analyses

1987 1988 1993

18 a

16

a

14

A

a

10

A

a

12 a

ab

a

b

a

8

b b

6 4 2 0

C

3 a a

harvested P (g m-2 a -1)

Nutrient removal with the harvest was calculated as the product of the mass of harvested biomass and the respective nutrient concentrations. Nitrogen:P, N:K, and K:P ratios were calculated based on the respective nutrient concentrations in harvested biomass. For the calculation of species richness per site and treatment the four 4 m2 vegetation sampling subplots were pooled together. We used the SPSS software package for all statistical analyses (SPSS 15.0 SPSS Inc., Chicago, IL, USA). To elucidate differences between mineral and organic soils a t test was performed adjusted to heterogeneous variances if required. For comparison of fertilized versus non-fertilized plots, we considered the paired plots (2xM0, 2xMPK) for the sites where both management measures were established (n = 3, Table 1). We conducted a t test for paired samples to test for significant differences between non-fertilized and fertilized plots. Significant differences among years were assessed using a least square differences (LSD) post hoc test. If data sets showed heteroscedasticity (Ca removal with the harvest, Corg concentrations of 2xM0, N:K ratios of 2xMPK), data were log transformed. Harvested biomass, N:P ratios, N:K ratios and plant species numbers were related using linear regression after logarithmic data transformation.

harvested N (g m -2 a -1)

a

AB a

2

AB

b

a a

1

ab

ab

ab b

b

b

3. Results 0 2xM0 mineral soil

3.1. Nutrient impoverishment In 1988, plant-available P and K concentrations in soil were in a range of 1–90 mg P kg 1 soil and 24–116 mg K kg 1 soil, respectively (Table 2). During the experiment, productivity in terms of harvested biomass of non-fertilized sites ranged from 236 to 1022 g m 2 on mineral and organic soils. On mineral soils, productivity of non-fertilized sites has continuously decreased since 1988 (Fig. 1). Nutrients differed with respect to the period of time until management effects were observed. Nitrogen and Mg concentrations in harvested biomass of non-fertilized sites significantly decreased in

Table 2 Mean pH in water, organic C (Corg), N, P, and K concentrations of soils (0–0.05 m depth) of the non-fertilized sites in 1988. The standard error is given in brackets (not possible for pH values).

pH (H2O) Corg (g kg 1) N (g kg 1) P (mg kg 1) K (mg kg 1)

Mineral soils

Organic soils

5.0 57.5 4.8 33.5 56.2

5.0 182.3 13.8 10.5 33.8

(9.9) (1.1) (19.2) (13.1)

(61.6) (5.3) (5.4) (5.0)

2xM0 organic soil

2xMPK both

Fig. 1. Biomass (A), N (B), and P (C) removed with the harvest (g m 2 a 1) by mowing twice a year without fertilization (2xM0) of sites on mineral soils (n = 4) and on organic soils (n = 3) and with PK fertilization (2xMPK, n = 3) from 1987 to 2007. Note that fertilization started in 1989 so that data of 1988 reflect initial conditions of PK-fertilized sites (1987 not available). Whiskers refer to the standard error. Significant differences among years are indicated by different lowercase letters. Uppercase letters in italics and in bold refer to marginally significant (p < 0.1) and significant differences (p < 0.05), respectively, between the plots with and without fertilization.

2007 compared to previous years on mineral as well as on organic soils (Table 2). In 2007, P concentrations of non-fertilized sites on organic soils were lower than in previous years (Table 2). Generally, nutrient removal with the harvest of non-fertilized sites decreased on mineral as well as on organic soils from 1987 to 2007 (Figs. 1 and 2). On mineral soils, six years without fertilization (1987–1993) resulted in a significantly decreased removal of Ca and Mg with the harvest (Fig. 2). Removal of N, P, and K was significantly lower after 20 years (1987–2007; Figs. 1 and 2). On organic soils, Ca and Mg removed with the harvest significantly decreased after six years without fertilization (1987–1993; Fig. 1), whereas N and P removal was significantly lower after 11 years (1987–1998; Fig. 2). Removal of K was not affected by mowing twice a year

2944

A

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948 14

harvested K (g m-2 a-1)

12 10

A

1993

A

a

1998 2007

8 6

3.2. Nutrients limiting plant growth

1987 1988

A

a ab

a

a

a b

ab ab

4

b

a

2 0

B

12

harvested Ca (g m-2 a-1)

10 a

8 a

a a

6

a

4

a

ab

a b

b

a

b

Nutrient ratios in harvested biomass indicate elements limiting plant growth. Generally, N:P and N:K ratios in harvested biomass on non-fertilized mineral and organic soils were below 14.0 and above 1.2, respectively (Table 2). On one organic site, K:P ratios were consistently above 3.4 (mean of all years: 8.8 ± SE 3.3). Nitrogen:P ratios in harvested biomass on non-fertilized organic soils marginally increased from 1987 to 2007, though not significantly. Fertilization of PK significantly decreased N:K ratios compared to non-fertilized sites (Table 2). However, on two of the three sites fertilized with PK (including mineral and organic soils) we observed N:K ratios of harvested biomass above 1.2 in 1998 and 2007. The relationship between N:P or N:K ratios and productivity might further indicate the nutrient that limits plant growth if PK-fertilized sites (ideally not limited by either P or K) and non-fertilized sites are included. On mineral soils, N:K ratios of harvested biomass of fertilized and non-fertilized sites were negatively correlated with productivity (Fig. 3). On organic soils, productivity of fertilized and non-fertilized sites correlated negatively with N:P ratios in harvested biomass (Fig. 3). 3.3. Plant species richness

b b

2

Management in nature conservation areas primarily aims at preserving or increasing species richness. We observed maximum and minimum plant species richness of 41 and 18, respectively, on nonfertilized sites (mineral and organic soils). Fertilization of PK maintained plant species richness compared to the respective non-fertilized sites where on organic soils a slight increase could be observed from 1993 to 2007 (Fig. 4). Plant species richness of fertilized and non-fertilized sites on organic soils was also positively correlated with N:P ratios in harvested biomass (r = 0.44, p < 0.05).

0

harvested Mg (g m-2 a-1)

C

6

4 a ab a

a

a

4. Discussion

a b

2 b

a b

a

b

4.1. Nutrient impoverishment

b c

0 2xM0 mineral soil

2xM0 organic soil

2xMPK both

Fig. 2. Potassium (A), Ca (B), and Mg (C) removed with the harvest (g m 2 a 1) by mowing twice a year without fertilization (2xM0) of sites on mineral soils (n = 4) and on organic soils (n = 3) and with PK fertilization (2xMPK, n = 3) from 1987 to 2007. Note that fertilization started in 1989 so that data of 1988 reflect initial conditions of PK-fertilized sites (1987 not available). Whiskers refer to the standard error. Significant differences among years are indicated by different lowercase letters. Lowercase letters in italics and in bold refer to marginally significant (p < 0.1) and significant differences (p < 0.05), respectively, between the paired plots with and without fertilization.

without fertilization on organic soils during the experiment (Fig. 2). In 2007, fertilization of PK more than doubled productivity compared to the respective non-fertilized sites (significant increase of 131%; Fig. 1). Potassium concentrations in harvested biomass were higher if PK fertilizer was applied (Table 2). As expected, mainly removal of P and K with the harvest was significantly higher on fertilized than on non-fertilized sites (Figs. 1 and 2). Related to the average removal of P with the harvest (=100%) of fertilized sites, more P was fertilized (130% ± standard error [SE] 10%) than was removed with the harvest from 1993 to 2007. For K, the amount of applied fertilizer K was equal to the average removal of K with the harvest (99 ± SE 13%). In 2007, fertilization of PK significantly increased N and Mg removal with the harvest (Fig. 2).

Initial nutrient availability of the studied wet grasslands was low and comparable to other European species-rich grasslands (Janssens et al., 1998; McCrea et al., 2004). On both, mineral and organic soils, low levels of plant-available nutrient concentrations in combination with mowing twice without fertilization resulted in a significant and continuous decrease of productivity in our study. Similarly, Berendse et al. (1992) found decreasing productivity with high inter-annual variability during more than 15 years of mowing twice without fertilization on acidic sandy soils. In a comparison of long- and short-term effects of management, Güsewell et al. (1998) found arbitrary trends in productivity of calcareous fens within the first four or up to 14 years. Their results might not be transferable to acidic wet grasslands because of probably constant influx of nutrients with water movement. Nevertheless, high inter-annual variability and differences between long- and short-term effects of management measures indicate that shortterm studies representing the majority of publications are of limited value to investigate management effects in species-rich meadows in the long run. Most studies on long-term management effects in species-rich meadows focus on productivity. Less information is available on the long-term effects on nutrient cycling. To our knowledge, only one long-term study on nutrient removal with the harvest in species-rich meadows has been published so far. In this study, Smits et al. (2008) found significant effects of time (1970–2006) on N, P, and K removal with the harvest of non-fertilized calcareous

2945

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948

A

log productivity

3.0

B

3.0

2.8

2.8

2.6

2.6 r = -0.71**

2.4

2.4 2xM0 2xMPK

2.2

2.2

3.2

C

2xM0

3.2

D

log productivity

2xMPK

3.0

3.0

2.8

2.8

2.6

2.6 r = -0.59*

2.4

2.2 0.6

0.7

0.8

0.9

1.0

1.1

1.2

log N:P

2.4

1.3

2.2 -0.2

0.0

0.2

0.4

0.6

0.8

1.0

log N:K

Fig. 3. Relationship between N:P (A, C) and N:K (B, D) ratios in harvested biomass and productivity (both log transformed) on mineral soils (diamonds; A, B) and on organic soils (triangles; C, D). 2xM0 = mowing twice a year without fertilization; 2xMPK = mowing twice a year with PK fertilization. Note that regressions include non-fertilized and PK-fertilized sites. * p < 0.05; ** p < 0.01. Dashed lines refer to the logarithm of the threshold values of 14.0 (N:P) and 1.2 (N:K) above which N or P limitation of plant growth, respectively, was suggested by Koerselman and Meuleman (1996) and Van Duren et al. (1997).

40 a a

species number

35 30

a

a

a

a a

a

a a

1987 1988 1993 1998

a

a

a

2007

25 20 15 10 5 0 2xM0 mineral soils

2xM0 organic soils

2xMPK both

Fig. 4. Number of species of sites without fertilization (2xM0; mineral soils n = 4, organic soils n = 3) and of sites with PK fertilization (2xMPK; n = 3). Note that PK fertilization started in 1989. Whiskers refer to the standard error. Significant differences among years are indicated by different lowercase letters.

grasslands that were mown once a year. Because of differences in soil substrate and moisture as well as in site and land use history temporal trends in nutrient removal of Smits et al. (2008) cannot be linked to our study. Therefore, we can only use implications of nutrient budget calculations in species-rich wet meadows to interpret our findings. We observed decreasing N removal with the harvest in the long term particularly on organic soils (Fig. 1). For low productive wetlands, Olde Venterink et al. (2002) and Wassen and Olde Venterink (2006) calculated that N removal with the harvest was counterbalanced by atmospheric input and N mineralization in soil. It is very

unlikely that the atmospheric N input recently has decreased, thus, mineralization of organic matter in soil has probably decreased since the establishment of the experiment particularly on organic soils. Olde Venterink et al. (2002) reported negative budgets of P and K in wetland ecosystems of low productivity i.e., ecosystem input (sum of atmospheric deposition, groundwater and surface water input, release by net mineralization) was less than ecosystem output (sum of leaching and removal by haymaking). Negative P and K budgets can explain decreased removal of P and K observed in our study. Potassium and Mg removal with the harvest was particularly affected by mowing twice without fertilization on mineral soils, which confirms the importance of K and Mg in mowed ecosystems (Tallowin and Jefferson, 1999; Olde Venterink et al., 2002), but also highlights the need to differentiate among soil substrates. During our study, removal of K with the harvest did not change on organic soils. Increased K availability in soil might be caused by additional K input due to rising groundwater levels or lateral flow, which applies for all our study sites (Ruville-Jackelen, 1994) and is also indicated by increasing cover-weighted means of Ellenberg indicator values for moisture of the vegetation samples with time (Poptcheva et al., 2009). Rising groundwater levels and the related input of K into soil particularly increases K availability in organic soils because of the higher cation exchange capacity associated with increased organic C concentrations in organic soils (Bruckert et al., 1992). Therefore, the supply of K on the studied organic soils seems to be constantly high due to the retention from groundwater. Calcium and Mg removal with the harvest significantly decreased after six years, whereas significant effects on removal of N and P (and K on mineral soils only) became obvious after more than six years of mowing twice a year without fertilization (Figs.

2946

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948

1 and 2). These temporal trends of nutrient removal with the harvest are not necessarily reflected by productivity, which might be strongly affected by the inter-annual variation in precipitation and temperature. Nevertheless, impoverishment in terms of nutrient removal with the harvest indicate that the contribution of plant species adapted to nutrient-poor conditions increased in our study. This is also reflected by Ellenberg N values of vegetation of our sites that constantly decreased with time (Poptcheva et al., 2009). Therefore, other organisms that are either specialized on these plant species or that are generally adapted to nutrient-poor conditions might profit from nutrient impoverishment (Broll et al. 2002; Ilg et al., 2009). However, positive effects of nutrient impoverishment on invertebrates and vertebrates might be counterbalanced by negative effects of rewetting on reproduction of these species (Ausden et al., 2001; Davis et al., 2006). Phosphorus fertilized as PK was not completely taken up by the vegetation. The remaining 30% are most probably retained in soil as Fe or Al phosphates of low solubility according to the range of pH values in soil (Table 2). Although fertilizer P might induce P accumulation in soil, the low solubility of phosphate minerals probably results in a minor role of P dissolution for P release as compared to mineralization of the great organic matter pool in soils of our study. Nearly 100% of fertilized K was taken up by the vegetation of fertilized sites. Smits et al. (2008) applied comparable amounts of K fertilizer and found significant effects restricted to the first two years after cessation of fertilization in calcareous grasslands corroborating complete uptake of fertilizer K by the vegetation. The high mobility of K+ ions in ecosystems favours leaching of K to the groundwater and could represent another mechanism behind short-term responses of K fertilizer (Kayser and Isselstein, 2005). Fertilization of PK adjusted to the respective removal with the harvest increased productivity compared to nonfertilized sites and maintained the initial level of nutrient removal with the harvest (Figs. 1 and 2). In species-rich and nutrient-poor grasslands mainly located in nature reserves, agricultural use of adequately fertilized sites might reduce costs (Isselstein et al. 2005) associated with a continuous management by increasing the amount and quality of harvested biomass, thus, improving attractiveness to local farmers. 4.2. Nutrients limiting plant growth On the studied non-fertilized mineral soils, N:K ratios of harvested biomass indicated limitation of plant growth by K (Van Duren et al., 1997; Hoosbeek et al., 2002). This finding is corroborated by a significant relationship between N:K ratios and harvested biomass of the respective sites (Fig. 3). Although particularly on soils with reduced availability of base cations, the importance of K, Ca, or Mg for plant growth seems obvious, few authors addressed limitation of plant growth by e.g., K (Olde Venterink et al., 2001a; Hoosbeek et al., 2002; Olde Venterink et al., 2002). If harvested bio-

mass is of agricultural value in species-rich grasslands, K should be considered as a possibly limiting element reducing plant growth particularly on acidic mineral soils. Based on the initially suggested threshold of N:P ratios of 14 above which limitation of plant growth is assumed to be caused by P (Koerselman and Meuleman, 1996), N:P ratios in our study did not indicate P limitation on any site (Table 3). Nitrogen:P ratios were even more below the threshold of 20 proposed by Güsewell et al. (2003) and Güsewell (2004). However, on organic soils in our study N:P ratios correlated negatively with productivity (Fig. 3) and one site suggested P limitation as indicated by K:P ratios above 3.4 (Olde Venterink et al., 2003) or even above 8.2 (Pegtel et al., 1996). Because the significant regression between N:P ratios and productivity was even consistent if excluding this site, we infer that plant growth could be limited by P on organic soils despite the N:P ratios not supporting this hypothesis. Because no other elemental ratio (N:Ca, N:Mg) was significantly correlated with plant growth, elements not included in our study might play an important role for plant nutrition in wet grasslands on organic soils. Therefore, N:P ratios in aboveground biomass of grasslands must be cautiously applied also considering productivity and other nutrients possibly limiting plant growth. Increased productivity of sites fertilized with PK compared to their non-fertilized counterparts confirms the limitation of plant growth by either P or K. However, we cannot completely rule out the possibility of industrial fertilizer containing other potentially limiting (trace) elements. Although fertilization of PK temporarily decreased N:K ratios in harvested biomass (Table 3), two of three fertilized sites showed N:K ratios above the critical threshold of K limitation in 2007 (Fig. 3). As fertilized K was nearly completely taken up by the vegetation, the amount of fertilized K should be slightly increased. The effect of fertilizer on productivity could be improved by also considering N:P or N:K ratios. 4.3. Species richness In 1988, availability of P and K in soil of non-fertilized sites (Table 2) was in the optimal range of less than 50–70 mg P kg 1 soil and 100–300 mg K kg 1 soil, respectively, reported for conserving or restoring species-rich grasslands across western and central Europe (Janssens et al., 1998; McCrea et al., 2001). Species numbers ranged between 18 and 41, which is in accordance with wet species-rich grasslands on mineral and organic soils in Europe (Berendse et al., 1992; Olde Venterink et al., 2001b; Olde Venterink et al., 2003). Despite considerable changes in floristic composition and an increase in abundance of stress-tolerant plant species with low nutrient demands (Poptcheva et al., 2009), total species richness rose only insignificantly. This is most likely due to seed and dispersal limitation, which means that only few new species could enter the community (Bakker et al., 1996; Hölzel, 2005). Such phenomena have been reported from many other studies on wet

Table 3 Nutrient concentrations and nutrient ratios in harvested biomass of sites without fertilization (2xM0) and with PK fertilization (2xMPK). Note that fertilization started in 1989 so that data of 1988 reflect initial conditions of PK-fertilized sites (1987 not available). Significant differences among years are indicated by different lowercase letters. Uppercase letters in italics and in bold refer to marginally significant (p < 0.1) and significant differences (p < 0.05), respectively, between the plots with and without fertilization. 2xM0 mineral soils

1

N (mg g ) P (mg g 1) K (mg g 1) Ca (mg g 1) Mg (mg g 1) N:P N:K

2xM0 organic soils

2xMPK mineral and organic soils

1987

1988

1993

1998

2007

1987

1988

1993

1998

2007

1988

1993

1998

2007

16.8b 2.7a 9.2a 9.5a 2.8a 6.1a 2.3a

18.1ab 2.8a 9.8a 8.4a 4.1a 6.8a 2.1a

20.1a 2.9a 8.0a 7.2a 3.0a 7.4a 2.8a

22.3a 3.5a 6.2a 6.9a 3.0a 7.0a 4.0a

15.8b 2.2a 4.7a 6.2a 1.8b 7.5a 4.0a

21.3ab 2.8a 8.3a 9.5a 4.2a 7.6a 4.1a

24.1ab 3.0a 6.6a 11.1a 5.2ab 8.0a 5.2a

26.7a 3.1a 7.8a 9.7a 3.1ab 8.7a 4.2a

21.5ab 2.3ab 9.6a 9.8a 2.9b 10.4a 2.9a

15.8b 1.7b 10.2a 8.4a 2.3b 10.7a 1.9a

22.4a 3.1a 6.3a 11.4a 4.7a 7.5a 4.7a

18.5a 3.3a 18.5A 7.5a 2.2A 5.7a 1.0A

18.4a 3.4a 16.4A 7.1a 2.5a 5.5a 1.2A

14.6a 2.6a 12.3a 6.5a 2.1a 5.8a 1.3a

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948

grasslands that found dispersal limitation to be the main obstacle for species-enrichment in fragmented cultural landscapes despite favourable site conditions (in terms of productivity e.g., Bakker 1989). However, to test this hypothesis experimental introduction of plant species to our study sites would be necessary (Turnbull et al., 1999; Schmid, 2002; Donath et al., 2007; Stein et al., 2008). On organic soils, we found a significantly positive correlation between N:P ratios in harvested biomass and plant species numbers, which is in accordance with Ertsen (1998). Fertilization of PK resulted in low N:P ratios and species diversity on organic soils (Table 3, Fig. 4). In combination with the negative relationship between N:P ratios (>14) and plant species richness observed by Roem and Berendse (2000), maximum species richness is to be expected at intermediate N:P ratios (Wassen et al., 2005). However, threatened plant species richness was shown to exponentially increase with increasing N:P ratios (Wassen et al., 2005). Thus, nature conservation of species-rich wet meadows should aim at reducing or maintaining low levels of P supply particularly on organic soils. Acknowledgements We thank Andrea Scheideler who collected, prepared, and analyzed the biomass samples of 1993. Kathrin Poptcheva took the biomass samples of 2007 and Sebastian Schmidt and Anja Berndt prepared and analyzed them for which we are very grateful. Thanks to Melanie Tappe, Ulrike Berning-Mader, and Madeleine Supper for their assistance in the laboratory. References Ausden, M., Sutherland, W.J., James, R., 2001. The effects of flooding lowland wet grassland on soil macroinvertebrate prey of breeding wading birds. Journal of Applied Ecology 38, 320–338. Bakker, J.P., 1989. Nature management by grazing and cutting. Kluwer Academic Publishers, Dordrecht. Bakker, J.P., Poschlod, P., Strykstra, R.J., Bekker, R.M., Thompson, K., 1996. Seed banks and seed dispersal: important topics in restoration ecology. Acta Botanica Neerlandica 45, 461–490. Bakker, J.P., Berendse, F., 1999. Constraints in the restoration of ecological diversity in grassland and heathland communities. Trends in Ecology & Evolution 14, 63– 68. Bakker, J.P., Elzinga, J.A., de Vries, Y., 2002. Effects of long-term cutting in a grassland system: perspectives for restoration of plant communities on nutrient-poor soils. Applied Vegetation Science 5, 107–120. Berendse, F., Oomes, M.J.M., Altena, H.J., Elberse, W.T., 1992. Experiments on the restoration of species-rich meadows in the Netherlands. Biological Conservation 62, 59–65. Bobbink, R., Hornung, M., Roelofs, J.G.M., 1998. The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology 86, 717–738. Broll, G., Merbach, W., Pfeiffer, E.-M., 2002. Wetlands in Central Europe: Soil Organisms. Soil Ecological Processes and Trace gas Emissions. Springer, Berlin. 250 pp. Bruckert, S., Villemin, P., Kubler, B., 1992. Potassium forms in aerated and anoxic soils of different management and potassium fertilizer history. Plant and Soil 147, 225–233. Davis, C.A., Austin, J.E., Buhl, D.A., 2006. Factors influencing soil invertebrate communities in riparian grasslands of the central Platte River floodplain. Wetlands 26, 438–454. Donath, T.W., Hölzel, N., Bissels, S., Otte, A., 2004. Perspectives for incorporating biomass from non-intensively managed temperate flood meadows into farming systems. Agriculture, Ecosystems and Environment 104, 439–451. Donath, T.W., Bissels, S., Hölzel, N., Otte, A., 2007. Large scale application of diaspore transfer with plant material in restoration practice - impact of seed and site limitation. Biological Conservation 138, 224–234. DWD, 2007. Climate data of the stations Schöppingen, Reken, Westerkappeln, and Ladbergen-Overbeck. Deutscher Wetterdienst Online. Ertsen, A.C.D., 1998. Ecohydrological response modelling. University of Utrecht, The Netherlands. FAO, 2006. World reference base for soil resources, World soil resources reports, Rome, pp. 145. Felske, A., Wolterink, A., Van Lis, R., De Vos, W.M., Akkermans, A.D.L., 2000. Response of a soil bacterial community to grassland succession as monitored by 16S rRNA levels of the predominant ribotypes. Applied and Environmental Microbiology 66, 3998–4003.

2947

Güsewell, S., Buttler, A., Klötzli, F., 1998. Short-term and long-term effects of mowing on the vegetation of two calcareous fens. Journal of Vegetation Science 9, 861–872. Güsewell, S., Koerselman, W., Verhoeven, J.T.A., 2003. Biomass N: P ratios as indicators of nutrient limitation for plant populations in wetlands. Ecological Applications 13, 372–384. Güsewell, S., 2004. N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266. Hemerik, L., Brussaard, L., 2002. Diversity of soil macro-invertebrates in grasslands under restoration succession. European Journal of Soil Biology 38, 145– 150. Hölzel, N., 2005. Seedling recruitment in flood-meadow species - effects of gaps, litter and vegetation matrix. Applied Vegetation Science 8, 115–124. Hansson, M., Fogelfors, H., 2000. Management of a semi-natural grassland; results from a 15-year-old experiment in southern Sweden. Journal of Vegetation Science 11, 31–38. Hoosbeek, M.R., Van Breemen, N., Vasander, H., Buttler, A., Berendse, F., 2002. Potassium limits potential growth of bog vegetation under elevated atmospheric CO2 and N deposition. Global Change Biology 8, 1130–1138. Ilg, C., Foeckler, F., Deichner, O., Henle, K., 2009. Extreme flood events favour floodplain mollusc diversity. Hydrobiologia 621, 63–73. Isselstein, J., Tallowin, J.R.B., Smith, R.E.N., 2002. Factors affecting seed germination and seedling establishment of fen-meadow species. Restoration Ecology 10, 173–184. Isselstein, J., Jeangros, B., Pavlu, V., 2005. Agronomic aspects of biodiversity targeted management of temperate grasslands in Europe – A review. Agronomy Research 3, 139–151. Janssens, F., Peeters, A., Tallowin, J.R.B., Bakker, J.P., Bekker, R.M., Fillat, F., Oomes, M.J.M., 1998. Relationship between soil chemical factors and grassland diversity. Plant and Soil 202, 69–78. Jones, J.B., Wolf, B., Mills, H.A., 1991. Plant analysis handbook. Micro Macro Publishing, Athens, Georgia. pp. 213. Kayser, M., Isselstein, J., 2005. Potassium cycling and losses in grassland systems: a review. Grass and Forage Science 60, 213–224. Keplin, B., Broll, G., 2002. Earthworm coenosis in wet grassland of NorthwestGermany. Effects of restoration management on a Histosol and a Gleysol. In: Broll, G., Merbach, W., Pfeiffer, E.-M. (Eds.), Wetlands in Central Europe. Springer, Berlin - Heidelberg - New York, pp. 11–34. Koerselman, W., Meuleman, A.F.M., 1996. The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33, 1441– 1450. Liira, J., Schmidt, T., Aavik, T., Arens, P., Augenstein, I., Bailey, D., Billeter, R., Bukacek, R., Burel, F., De Blust, G., De Cock, R., Dirksen, J., Edwards, P.J., Hamersky, R., Herzog, F., Klotz, S., Kuhn, I., Le Coeur, D., Miklova, P., Roubalova, M., Schweiger, O., Smulders, M.J.M., Van Wingerden, W., Bugter, R., Zobel, M., 2008. Plant functional group composition and large-scale species richness in European agricultural landscapes. Journal of Vegetation Science 19, 3–14. McCrea, A.R., Trueman, I.C., Fullen, M.A., Atkinson, M.D., Besenyei, L., 2001. Relationships between soil characteristics and species richness in two botanically heterogeneous created meadows in the urban English West Midlands. Biological Conservation 97, 171–180. McCrea, A.R., Trueman, I.C., Fullen, M.A., 2004. Factors relating to soil fertility and species diversity in both semi-natural and created meadows in the West Midlands of England. European Journal of Soil Science 55, 335–348. Mingorance, M.D., 2002. Focused microwave-assisted digestion of vegetal materials for the determination of essential mineral nutrients. Analytical and Bioanalytical Chemistry 373, 153–158. Moog, D., Poschlod, P., Kahmen, S., Schreiber, K.F., 2002. Comparison of species composition between different grassland management treatments after 25 years. Applied Vegetation Science 5, 99–106. Murphy, J., Riley, J.P., 1962. A modified single solution method for determination of phosphate in natural waters. Analytica Chimica Acta 26, 31–36. Neyroud, J.A., Lischer, P., 2003. Do different methods used to estimate soil phosphorus availability across Europe give comparable results? Journal of Plant Nutrition and Soil Science 166, 422–431. Olde Venterink, H., van der Vliet, R.E., Wassen, M.J., 2001a. Nutrient limitation along a productivity gradient in wet meadows. Plant and Soil 234, 171–179. Olde Venterink, H., Wassen, M.J., Belgers, J.D.M., Verhoeven, J.T.A., 2001b. Control of environmental variables on species density in fens and meadows: importance of direct effects and effects through community biomass. Journal of Ecology 89, 1033–1040. Olde Venterink, H., Pieterse, N.M., Belgers, J.D.M., Wassen, M.J., de Ruiter, O.D., 2002. N, P and K budgets along nutrient availability and productivity gradients in wetlands. Ecological Applications 12, 1010–1026. Olde Venterink, H., Wassen, M.J., Verkroost, A.W.M., de Ruiter, P.C., 2003. Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84, 2191–2199. Pegtel, D.M., Bakker, J.P., Verweij, G.L., Fresco, L.F.M., 1996. N, K and P deficiency in chronosequential cut summer-dry grasslands on gley podzol after the cessation of fertilizer application. Plant and Soil 178, 121–131. Plum, N., 2005. Terrestrial invertebrates in flooded grassland: A literature review. Wetlands 25, 721–737. Poptcheva, K., Schwartze, P., Vogel, A., Kleinebecker, T., Hölzel, N., 2009. Changes in wet meadow vegetation after 20 years of different management in a field experiment. Agriculture Ecosystems & Environment in press; doi:10.1016/ j.agee.2009.06.004.

2948

Y. Oelmann et al. / Biological Conservation 142 (2009) 2941–2948

Roem, W.J., Berendse, F., 2000. Soil acidity and nutrient supply ratio as possible factors determining changes in plant species diversity in grassland and heathland communities. Biological Conservation 92, 151–161. Rosenthal, G., 2006. Restoration of wet grasslands–Effects of seed dispersal, persistence and abundance on plant species recruitment. Basic and Applied Ecology 7, 409–421. Ruville-Jackelen, F., 1994. Untersuchungen zum Bodenwasserhaushalt und zum Bioelementtransport an ausgewählten Standorten des Feuchtgrünlandes im Münsterland. PhD Thesis, University of Münster, 252 pp. Schmid, B., 2002. The species richness – productivity controversy. Trends in Ecology and Evolution 17, 113–114. Schwartze, P., 1992. Nordwestdeutsche Feuchtgrünlandgesellschaften unter kontrollierten Nutzungsbedingungen, Dissertationes Botanicae. Cramer, Berlin–Stuttgart, pp. 204. Schwartze, P., 2003. Einfluss von Brache und Nutzung auf Feuchtgrünlandvegetation im Münsterland. Kieler Notizen zur Pflanzenkunde. Schleswig-Holstein Hamburg 31, 185–196. Silvertown, J., Poulton, P., Johnston, E., Edwards, G., Heard, M., Biss, P.M., 2006. The Park Grass Experiment 1856–2006: Its contribution to ecology. Journal of Ecology 94, 801–814.

Smits, N.A.C., Willems, J.H., Bobbink, R., 2008. Long-term after-effects of fertilisation on the restoration of calcareous grasslands. Applied Vegetation Science 11, 279–292. Stein, C., Auge, H., Fischer, M., Weisser, W.W., Prati, D., 2008. Dispersal and seed limitation affect diversity and productivity of montane grasslands. Oikos 117, 1469–1478. Tallowin, J.R.B., Jefferson, R.G., 1999. Hay production from lowland semi-natural grasslands: a review of implications for ruminant livestock systems. Grass and Forage Science 54, 99–115. Turnbull, L.A., Rees, M., Crawley, M.J., 1999. Seed mass and the competition/ colonization trade-off: a sowing experiment. Journal of Ecology 87, 899–912. Van Duren, I.C., Pegtel, D.M., Aerts, B.A., Inberg, J.A., 1997. Nutrient supply in undrained and drained Calthion meadows. Journal of Vegetation Science 8, 829–838. Wassen, M.J., Venterink, H.O., Lapshina, E.D., Tanneberger, F., 2005. Endangered plants persist under phosphorus limitation. Nature 437, 547–550. Wassen, M.J., Olde Venterink, H., 2006. Comparison of nitrogen and phosphorus fluxes in some European fens and floodplains. Applied Vegetation Science 9, 213–222.