Does organic grassland farming benefit plant and arthropod diversity at the expense of yield and soil fertility?

Agriculture, Ecosystems and Environment 177 (2013) 1–9

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Does organic grassland farming benefit plant and arthropod diversity at the expense of yield and soil fertility? Valentin H. Klaus a,∗ , Till Kleinebecker a , Daniel Prati b , Martin M. Gossner c , Fabian Alt d , Steffen Boch b , Sonja Gockel c , Andreas Hemp e , Markus Lange f , Jörg Müller g , Yvonne Oelmann d , Esther Paˇsalic´ f , Swen C. Renner h , Stephanie A. Socher b , Manfred Türke c , Wolfgang W. Weisser c , Markus Fischer b,g , Norbert Hölzel a a

Universität Münster, Institute of Landscape Ecology, Robert-Koch-Str. 28, 48149 Münster, Germany Universität Bern, Institute of Plant Sciences, Altenbergrain 21, 3013 Bern, Switzerland c Technische Universität München, Department of Ecology and Ecosystem Management, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany d Universität Tübingen, Geoecology/Geography, Rümelinstr. 19-23, 72070 Tübingen, Germany e Universität Bayreuth, Department of Plant Systematics, Universitätsstr. 30-31, 95440 Bayreuth, Germany f Friedrich-Schiller-Universität Jena, Institute of Ecology, Dornburger Strasse 159, 07743 Jena, Germany g Universität Potsdam, Institute of Biochemistry and Biology, Maulbeerallee 1, 14469 Potsdam, Germany h Universität Ulm, Institute of Experimental Ecology, Albert-Einstein Allee 11, 89069 Ulm, Germany b

a r t i c l e

i n f o

Article history: Received 4 January 2013 Received in revised form 15 May 2013 Accepted 18 May 2013 Keywords: Agri-environmental schemes Fertilization Fodder quality Land-use intensity Nitrogen Biomass nutrient concentrations Organic farming Phosphorus Species richness Nutrient availability

a b s t r a c t Organic management is one of the most popular strategies to reduce negative environmental impacts of intensive agriculture. However, little is known about benefits for biodiversity and potential worsening of yield under organic grasslands management across different grassland types, i.e. meadow, pasture and mown pasture. Therefore, we studied the diversity of vascular plants and foliage-living arthropods (Coleoptera, Araneae, Heteroptera, Auchenorrhyncha), yield, fodder quality, soil phosphorus concentrations and land-use intensity of organic and conventional grasslands across three study regions in Germany. Furthermore, all variables were related to the time since conversion to organic management in order to assess temporal developments reaching up to 18 years. Arthropod diversity was significantly higher under organic than conventional management, although this was not the case for Araneae, Heteroptera and Auchenorrhyncha when analyzed separately. On the contrary, arthropod abundance, vascular plant diversity and also yield and fodder quality did not considerably differ between organic and conventional grasslands. Analyses did not reveal differences in the effect of organic management among grassland types. None of the recorded abiotic and biotic parameters showed a significant trend with time since transition to organic management, except soil organic phosphorus concentrations which decreased with time. This implies that permanent grasslands respond slower and probably weaker to organic management than crop fields do. However, as land-use intensity and inorganic soil phosphorus concentrations were significantly lower in organic grasslands, overcoming seed and dispersal limitation by re-introducing plant species might be needed to exploit the full ecological potential of organic grassland management. We conclude that although organic management did not automatically increase the diversity of all studied taxa, it is a reasonable and useful way to support agro-biodiversity. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Organic management has become one of the most popular sustainable strategies to produce agricultural goods but reduce negative environmental effects of intensive agriculture such as biodiversity decline (Zechmeister et al., 2003; Tscharntke et al.,

∗ Corresponding author. Tel.: +49 251 8339770; fax: +49 251 8338338. E-mail address: [email protected] (V.H. Klaus). 0167-8809/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.agee.2013.05.019

2005; Whittingham, 2011). To achieve this goal, organic management abandons pesticides and synthetic fertilizers, and restricts livestock density and the use of organic fertilizers from animal husbandry (maximum of 170 kg N ha−1 a−1 ) (European Union, 2008). Hence, the resulting lower pressure of land-use intensity can benefit agro-biodiversity (Gomiero et al., 2011). However, critics of organic management argue that especially restricted fertilizer input may significantly reduce quantity and quality of yields (Offermann and Nieberg, 2000). Furthermore, it is debated, whether organic management decreases nutrient availability in

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soils leading to additional long-term economical deterioration (Gosling and Shepherd, 2005; Hathaway-Jenkins et al., 2011). It is therefore important to carefully assess not only potential benefits of organic management, but also to quantify decreasing quantity and quality of yield associated with organic management. However, such negative effects have hardly been quantified for grasslands on a larger scale, which is necessary to account for the wide range of grassland productivity found among different environmental conditions. Grasslands are among the most species rich habitats in the world (Wilson et al., 2012), and the proportion of organic farms and organic markets grow rapidly. From 2008 to 2011 the area of organically managed grasslands in Germany increased by 9.2% resulting in 11.5% organic grasslands of the total grassland area (Schaack et al., 2010). Nevertheless, compared with well studied crop fields, where biodiversity in general increased on multiple scales (Hole et al., 2005; Geiger et al., 2010), the effect of organic management in permanent grasslands has yielded equivocal results (Manusch and Pieringer, 1995; Haas et al., 2001; Kleijn and Sutherland, 2003; Mayer et al., 2008; Batáry et al., 2012). Grassland types can be categorized as meadows (mowing only), pastures (grazing only) and mown pastures where mowing and grazing are combined. However, such differences were consistently neglected although mowing and grazing are known to have distinct effects on biodiversity (Zahn et al., 2010; Socher et al., 2012). Furthermore, studies are at risk to overestimate ecological benefits of organic management, because organic plots have often a lower agronomic potential and are thus per se less intensively used and more diverse which can skew the outcomes of these surveys (Kleijn and Sutherland, 2003; Dahms et al., 2010). Therefore, we conducted a study on effects of organic management in grasslands located in different landscapes taking into account both the overall land-use intensity at the plot scale and differences in the management type. We compared (i) diversity measures of vascular plants, (ii) diversity measures of foliage-living arthropod taxa, (iii) soil P concentrations, (iv) quantity and fodder quality of yield (aboveground biomass) and (v) land-use intensity of organic and conventional grasslands in three regions in Germany. Plots were selected randomly stratified and subsequently reduced according to soil type, grazing animal type and grassland type. Furthermore, we related all diversity and abiotic variables to the time since conversion to organic management because effects on ecosystem properties may need some time to turn out (Gosling and Shepherd, 2005; Hole et al., 2005). In this study, we hypothesized that (1) land-use intensity, yield and fodder quality as well as soil nutrient availability are lower, whereas (2) the diversity of plants and foliage-living arthropods (both herbivorous and predatory taxa) is higher in organic compared with conventional grasslands, although (3) this might differ among grassland types; and (4) the time since conversion to organic management has a positive effect on species diversity but a negative on yield and soil P concentrations.

2. Materials and methods 2.1. Plot selection and land-use intensity The study took place in grasslands within three regions in Germany that are part of the Biodiversity Exploratories project (Fischer et al., 2010): (1) the UNESCO Biosphere Reserve Schorfheide-Chorin, in North-Eastern Germany, (2) the National Park Hainich and surrounding areas (Hainich-Dün) in Central Germany and (3) the UNESCO Biosphere Reserve Schwäbische Alb in South-Western Germany. In each region, we selected and sampled 50 grassland plots according to a randomly stratified

Table 1 Study plots arranged according to grassland type, organic management and study region. Meadows

Pastures

Mown pastures

Sum

Org.

Conv.

Org.

Conv.

Org.

Schwabische Alb Hainich-Dün Schorfheide-Chorin

3 – 2

13 – 2

– 5 –

– 1 –

1 5 2

5 7 2

22 18 8

Total

5

15

5

1

8

14

48

Conv.

procedure with strata representing the range of land-use intensities to create representative gradients of Central European land use. For further details on study regions and plot selection see Fischer et al. (2010). The intensity of land use varied strongly among grasslands. From these 150 plots, we selected all organic grasslands, which were at least managed for two years according to the standards of an organic management certificate (e.g. European Union, 2008). In turn, conventional grasslands were defined by management, which is not conforming to organic management guidelines, e.g. application of synthetic fertilizers. This led to the exclusion of many unfertilized but not certified (conventional) plots Table 1. To compare organic and conventional grasslands, two subsets of plots were sub-selected according to study region, grassland type, grazing animal type, soil type and soil depth. This resulted in a dataset of 18 organic grasslands from 13 different farms and 30 conventional grasslands (Table 1). At the time of sampling (2009), the time of organic grassland management ranged from 2 to 18 years (including time in conversion). Field size did not significantly differ between organic and conventional grasslands (Table 2). To quantify land-use intensity, we used questionnaires to gather information from farmers on the amount of fertilizer application (kg N ha−1 ) (F), the frequency of mowing (cuts y−1 ) (M) and the livestock density (livestock units × days ha−1 ) (G) in 2007, 2008 and 2009. For each plot [i], an index of mean land-use intensity LUI[i] was calculated as LUI[i] =



F[i] : Fmean + M[i] : Mmean + G[i] : Gmean ,

where Fmean , Mmean and Gmean are respective means values of all 50 plots of each study region (Blüthgen et al., 2012). 2.2. Field surveys and chemical analyses Soil samples for pH and phosphorus (P) analysis were taken with a soil corer (∅ 55 mm, Eijkelkamp, Giesbeek, The Netherlands) in Schorfheide-Chorin and Hainich-Dün from May to June 2008, and in the Schwäbische Alb in April 2009 as mixed samples from five sub-samples. Soil samples were air-dried and sieved to <2 mm. 0.5 g of sieved soil were sequentially extracted for 30 min with 20 mL 0.5 mol L−1 NaHCO3 (adjusted to pH 8.5 with 1 M NaOH) and thereafter for 16 h with 30 mL 0.1 mol L−1 NaOH to estimate the labile (NaHCO3 -P) and moderately labile-bonded (NaOH-P) P fractions in soil (Negassa and Leinweber, 2009). Phosphorous concentrations in the extraction solutions were determined colorimetrically by the phosphomolybdate blue method after Murphy and Riley (1962) using a continuous flow analyzer (CFA, Bran+Luebbe, Norderstedt, Germany). Organic P concentrations were calculated as the difference between total and inorganic P concentrations. Further details on soil sampling are given in Alt et al. (2011). From mid of May to beginning of June 2009, we identified all vascular plant species and estimated their abundance on 4 m × 4 m sub-plots in the grassland center and harvested aboveground

V.H. Klaus et al. / Agriculture, Ecosystems and Environment 177 (2013) 1–9

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Table 2 Land use, species richness and abiotic characteristics of organically and conventionally managed grasslands. pc

Organic management

Land use Field size (ha) Land-use intensity indexa Fertilizer application (N ha−1 a−1 ) Cuts (a−1 ) Grazing intensity (a−1 ) Vegetation parameters Shannon diversity vascular plants Vascular plant species richness Number grass species Number legume species Number herb species (non legumes) Abundance grasses Abundance legumes Abundance herbs (non legumes) Abundance bryophytes Ellenberg nutrient values (mN) Arthropod parameters Shannon diversity all arthropod species Species richness all arthropod species Abundance all arthropod species Shannon diversity herbivorous arthropods Species richness herbivorous arthropods Abundance herbivorous arthropods Shannon diversity predatory arthropods Species richness predatory arthropods Abundance predatory arthropods Shannon diversity beetles (Coleoptera) Species richness beetles Abundance beetles Shannon diversity herbivorous beetles Species richness herbivorous beetles Abundance herbivorous beetles Shannon diversity predatory beetles Species richness predatory beetles Abundance predatory beetles Shannon diversity spiders (Araneae) Species richness spiders Abundance spiders Shannon diversity cicada (Auchenorrhyncha) Species richness cicada Abundance cicada Shannon diversity bugs (Heteroptera) Species richness bugs Abundance bugs Soil characteristics pH Inorganic phosphorus (mg kg−1 )b Organic phosphorus (mg kg−1 )b Biomass characteristics Yield (aboveground biomass) (g sqm−1 ) K (g kg−1 ) P (g kg−1 ) N (g kg−1 ) N:P ratio NDF (neutral detergent fiber) (% DW) ADF (acid detergent fiber) (% DW) ADL (lignin) (% DW) Ash content (% DW)

n

Min/max

Mean

SE

18 18 18 18 18

1.56/65 0.82/2.22 0/90.5 0/2.7 0/366.8

18 1.61 23.4 1.1 108.9

4.6 0.1 9.1 0.2 30.1

18 18 18 18 18 18 18 18 18 18

5.0/24.5 14/57 3/15 1/7 9/35 28/103 0.5/31 5/72.5 0/60 4.6/6.8

12.0 27.6 7.9 2.6 17.1 65.2 9.8 35.6 15.3 6.0

0.9 2.3 0.7 0.4 1.6 4.1 1.9 4.1 3.9 0.1

18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18 18

1.5/3.1 13/54 31/448 1.5/2.77 10/43 26/421 0/2.16 0/10 0/21 0.69/2.69 2/23 2/173 0.69/2.42 2/16 2/155 0/2.16 0/9 0/17 0/1.56 0/5 0/7 0.84/2.09 3/14 3/242 0/1.86 1/13 1/364

17 16 16

5.2/6.7 4.1/24.1 8.3/35.7

18 18 18 18 18 18 18 18 18

123.7/496.2 5.3/39.3 2/3.6 13.6/29.6 4.4/12.4 38.3/54.8 21/29.5 3.9/8.4 5.1/11.9

2.5 28 136 2.26 21 121 1.37 5 7.9 2.0 11 31.3 1.6 8 24.8 0.6 3 4.6 0.7 2 2.9 1.4 7 46.0 1.1 6 45.9 6.2 11.2 17.9 299.81 23.7 2.9 20.7 7.4 46.5 24.5 6.1 9.2

0.1 2 28.6 0.1 2 25.9 0.1 1 1.3 0.1 1 9.2 0.1 1 8.3 0.2 1 1.1 0.1 0 0.5 0.1 1 13.9 0.2 1 19.6 0.1 1.6 2.0 28.9 2.5 0.1 1.1 0.6 1.2 0.6 0.4 0.5

(***) (***) (**)

*** *

** ** * * * * ** ** ** **

*

Conventional management n

Min/max

Mean

30 30 30 30 30

2.5/30 1.67/3.18 34.3/230.6 0/3 0/767

10.2 2.20 69.6 1.7 89.0

1.4 0.1 7.7 0.1 30.3

30 30 29 29 29 29 29 29 23 30

4.5/16.4 12/41 6/13 0/4 3/29 58/134.5 0/40 10.5/59.5 0/35 5.5/6.7

10.4 24.1 8.2 2.2 13.9 88.1 8.3 33.8 8.9 6.1

0.6 1.1 0.4 0.2 0.9 3.2 2.0 3.1 2.0 0.1

29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29

1.1/2.6 7/38 19/735 1.02/2.34 6/30 14/720 0/2.03 0/9 0/17 0/2.54 0/18 0/51 0/2.43 0/16 0/42 0/0.96 0/3 0/15 0/1.61 0/7 0/13 0.16/1.86 3/14 5/635 0/1.72 0/8 0/355

2.1 22 205 1.92 18 199 0.90 3 5.1 1.5 7 17 1.3 6 13.9 0.3 1 2.5 0.5 2 2.4 1.2 7 125.2 0.9 5 56.5

29 28 28

4.7/7.2 25.9/45.3 9.9/46.8

6.5 24.2 23.2

29 30 30 30 30 30 30 30 30

77.84/717.54 6.2/33 1.7/4.1 1.47/3.52 5.2/13.9 35.1/62.3 18.5/31.9 3/9.1 4.4/11.8

335.15 20.5 2.90 22.6 8.0 52.3 26.8 5.8 8.3

SE

0.1 2 36.2 0.1 1 35.9 0.1 0 0.8 0.1 1 2.5 0.1 1 2.2 0.1 0 0.6 0.1 0 0.5 0.1 1 29.9 0.1 0 12.5 0.1 2.4 1.8 28.4 1.4 0.1 0.9 0.4 1.4 0.7 0.3 0.4

a LUI is the sum of fertilization intensity (fertilizer application in kg N ha−1 y−1 ), mowing intensity (cuts per year) and grazing intensity (number of livestock units × days grazing ha−1 y−1 ) (see Blüthgen et al., 2012). b Inorganic and organic P concentrations given are the sum of extractions with NaHCO3 und NaOH. c Significance levels derived from regression models (see Appendix 1): ***, p < 0.001; **, 0.001 < p < 0.01; *, 0.01 < p < 0.05. No star: no significant differences. In brackets: significance levels of Mann–Whitney U-tests.

community biomass as mixed samples of four randomly placed quadrates of 0.25 m2 each. Temporary fences ensured that plots were not mown or grazed before biomass sampling took place. After harvesting, material was dried for 48 h at 80 ◦ C, weighed and ground. Total nitrogen (N) concentrations were determined using

an element auto analyzer (NA 1500, Carlo Erba, Milan, Italy). For the analyses of phosphorus (P) and potassium (K), samples were digested with concentrated nitric acid and hydrogen peroxide and determined by ICP-OES analyses (Vista-PRO Axial, Varian, Palo Alto, USA). Neutral detergent fiber (NDF), acid detergent fiber (ADF) and

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V.H. Klaus et al. / Agriculture, Ecosystems and Environment 177 (2013) 1–9

lignin (ADL) contents were measured gravimetrically (Naumann and Bassler, 1976) (Fibertec 2010, Foss, Höganäs, Sweden). Ash content was determined as the percentage of residue remaining after dry oxidation at 545 ◦ C in a muffle furnace relative to the 105 ◦ C oven dry weight of the sample. Following studies from Olde Venterink et al. (2003) and Güsewell (2004), we used nutrient ratios in biomass to estimate the type of nutrient limitation (NP-co limitation = 10 < N:P < 16; N limitation = N:P ≤ 10; K or K (co) limitation = N:K > 2.1 and K:P < 3.4; P limitation = N:P > 16). Further details are given in Klaus et al. (2011). Foliage-living arthropods were collected by sweep-net (circular, ∅ 30 cm) samples, standardized to 60 double-sweeps per plot (20 along three transects) in the grassland center in June and August 2009. All arthropods were transferred to 70% ethanol in the field. In the laboratory, arthropods were sorted to the order-level and all specimens of the taxa Araneae, Heteroptera, Coleoptera, Neuroptera, Auchenorrhyncha, Symphyta and Orthoptera subsequently identified to species level by taxonomic specialists. As species of different trophic levels might respond differently to organic management (Batáry et al., 2012), all species were classified as herbivores (Heteroptera in partim, Auchenorrhyncha, Coleoptera in partim, Symphyta, Orthoptera) and predators (Araneae, Heteroptera in partim, Coleoptera in partim, Neuroptera) based on data provided by the taxonomic specialists. Species that likewise feed on plants and animals (13 species of Heteroptera) as well as Coleoptera species that do not feed mainly on plants (excl. xylophages) or other arthropods were excluded from this grouping. Details on trophic guild classification are given in Appendix 1. 2.3. Data analyses Exponential Shannon diversity indices (H) were calculated for vascular plants and different arthropod taxa according to Jost (2006) with the formula H = exp −

 S 

 (pi × ln pi )

i=1

where pi is the cover or abundance of the i-th species and S is the total number of species in the record. As an indirect measure of nutrient availability, we calculated mean Ellenberg indicator values for nutrients (mN) from vegetation records without cover-weighting. A linear regression model (y-variable ∼ grassland type + management + grassland type:management) was used to separate effects of grassland type (meadow, pasture or mown pasture) and organic vs. conventional management including the interaction on plant and arthropod diversities and soil and biomass characteristics. Soil pH was involved as an explanatory variable in the analysis of organic and inorganic P concentrations (without interactions), but it was finally removed as it was not significant in both cases. Regression analyses were performed using R version 2.12.2 (R Development Core Team, 2011) with “lm” and “step” functions for stepwise reduction of predictor variables according to the Akaike information criterion (AIC). Models were re-run after removing all non significant variables (p > 0.05). To account for spatial autocorrelation we also performed generalized least squares models (“gls”) with exponential spatial correction (Zuur et al., 2009). As gls results were consistent with those obtained by lm analyses, we decided to present the result of the lm-models which have the advantage of model R2 and p-values. Normal distribution of regression residuals was checked using quantile–quantile plots. For land-use intensity and its components grazing, mowing and fertilization, Mann–Whitney U-tests were used to detect significant group differences. All biotic and abiotic variables were related to

the time since conversion to organic management using Spearman correlation coefficients. To account for differences among study regions, variables were centered prior to statistical analyses by subtracting the regional mean. This disabled the analysis of regional peculiarities in order to strengthen the generality of the observed patterns. Except regression models, all analyses and graphics were gained using IBM SPSS 20. 3. Results 3.1. Land-use intensity, yield, fodder quality and nutrient availability Based on the calculated land-use intensity index, organic grasslands were spread over the whole gradient of land-use intensities, but most frequent at the low middle of the gradient (Fig. 1). Nevertheless, land-use intensity in organic grasslands was 27% lower compared to conventional grasslands (Fig. 2 and Table 2). This was due to considerably lower application of fertilizer (only one third!) and cutting frequencies in organic grasslands, while grazing intensity did not differ between organic and conventional management (Table 2 and Fig. 3b). Linear regression revealed that the yield did not respond to grassland type and organic management (Fig. 2 and Appendix 2). Under organic management, higher lignin (ADL) and lower NDF concentrations and a weak but significant interaction of organic management and grassland type for organic P concentrations in soil were found. Nevertheless, nutrient concentrations and fiber fractions in aboveground biomass were statistically not different in organic and conventional grasslands (Table 2 and Appendix 2). Nutrient limitation, estimated via nutrient ratios, was also similar in organic and conventional grasslands, with slightly more cases of N limitation in organic and slightly more cases of NP co-limitation in conventional grasslands. Strict P limitation with a N:P ratio above 16 was not observed (Fig. 3). While organic P concentrations in soil exhibited only a weak interactional effect of organic management with grassland types, inorganic P concentrations were significantly lower under organic management. In contrast, Ellenberg mN values did not show any significant difference according to grassland types and organic management. (Table 2 and Appendix 2). In summary, organic and conventional grasslands differed in land-use intensity and soil fertility, while no such differences could be observed for the quantity and quality of the yield. 3.2. Species diversity Shannon diversity of vascular plants differed between grassland types but was not significantly affected by organic management (Fig. 2 and Table 2). Similarly, total vascular plant species richness as well as richness of grass, herb and legume species did not differ between organic and conventional grasslands. Nevertheless, organic grasslands were characterized by lower grass and higher herb abundance, while legume and bryophyte abundance were unaffected by organic management (Table 2 and Appendix 2). Generally, we observed quite similar result for different measures of arthropod diversity, therefore we only use the term diversity hereafter to represent both species number and Shannon diversity. The total diversity of foliage-living arthropods did not differ among grassland types, but was significantly higher under organic management (Fig. 2 and Table 2). While on the scale of single taxa beetle diversity

100%

Conventional 90%

Unf ertilized conventional

80% 70%

Organic 60% 50% 40% 30% 20% 10% 0% 0.5

1.0

(n = 25)

1.5 (n = 49)

2.0 (n = 38)

2.5 (n = 23)

3.3 (n = 15)

Land-use intensity Fig. 1. Cumulative frequency of land-use intensity of 150 organic and conventional grasslands along a land-use gradient in three German regions according to Blüthgen et al. (2012). Land-use intensity (LUI) was calculated as the sum of fertilization, grazing and mowing intensity (see Table 2).

V.H. Klaus et al. / Agriculture, Ecosystems and Environment 177 (2013) 1–9

5

Fig. 2. Vascular plant and arthropod species richness, yield, land-use intensity (LUI), Ellenberg mean nutrient values (mN) and inorganic P concentrations in soils of organic and conventional grasslands. Values given have been centered according to the mean in each study region. The box represents values within the 25th to 75th percentiles with the median as thick line. The whiskers range from the highest to the lowest values with outliers and extreme values as dots (1.5–3 times box length outside box) and stars (more than 3 times box length outside box). Stars represent significant group differences according to regression analyses or Mann–Whitney U-tests (see Table 2 and Appendix 2).

(especially of herbivorous Coleoptera) was also more diverse in organic than in conventional grasslands; this was not the case for spider (Araneae), cicada (meaning plant- and leafhoppers; Auchenorrhyncha) and bug (Heteroptera) diversities. Both groups of all herbivorous as well as all predatory arthropod species were significantly more diverse in organic grasslands, although this was barely statistically significant. Arthropod abundances did not show any differences among grassland types or organic versus conventional management, irrespective of taxon or functional group (Table 2 and Appendix 2). 3.3. Effect of time since conversion to organic management Correlation analyses revealed that only organic P concentrations in soil (n = 18; rS = −0.68; p = 0.004) decreased significantly after conversion to organic management (Fig. 4). In contrast, diversities of vascular plants and foliage-living arthropods and all other abiotic variables were not significantly related to the time since conversion (p > 0.05) indicating fairly slow response of studied grasslands to implementation of organic management.

A)

Nutrient limitation

100%

NP-co li mitation

80%

N lim itation

70%

4.1. Land-use intensity, yield, fodder quality and nutrient availability Organic grasslands were characterized by lower land-use intensity, especially due to decreased fertilization and cutting frequency. The drastic reduction of 2/3 of conventional fertilizer applications is in any case environmentally favorable because it can minimize losses of N to the groundwater, to neighboring habitats and as greenhouse gases to the air (Hopkins and Wilkins, 2006). Furthermore, Haas et al. (2001) underlined reduced eutrophication potential and resource consumption of organic grassland management.

B) K (co) li mitation

90%

4. Discussion

100%

>150 kg

90%

101-150 kg

80%

51-100 kg

70%

60%

60%

50%

50%

40%

40%

30%

30%

20%

20%

10%

10%

0%

Fertilizer (N kg*ha-1*a-1)

1-50 kg 0 kg

0% Organic

Conventional

Management

Organic

Conventional

Management

Fig. 3. Cumulative frequency of (A) nutrient limitation of grasslands estimated by N:P, K:P and N:K ratios in aboveground biomass and (B) amount of fertilizer applied as nitrogen per hectare and year (organic n = 18, conventional n = 30).

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V.H. Klaus et al. / Agriculture, Ecosystems and Environment 177 (2013) 1–9

Fig. 4. The effect of the duration of organic management on vascular plant and arthropod species richness, yield (all n = 18) and organic phosphorus concentrations in topsoil (n = 16). Values were standardized to study region prior to analysis. Regression line only shown for significant Spearman correlation rs = −0.68; p = 0.004.

Although organic grasslands received considerably less fertilizer, yield was not significantly lower compared to conventional grasslands. In contrast, Haas et al. (2001), Mäder et al. (2002) and Nemecek et al. (2011) found a reduction of 10–20% grassland yield under organic management in agricultural experiments or regional comparisons in Southern Germany and Switzerland. Other studies found significantly reduced productivity after the complete cessation of fertilization in grasslands, although effects of former nutrient addition on productivity were still apparent after more than 15 years (Willems and van Nieuwstadt, 1996; Hrevuˇsová et al., 2009). Probably due to a wider range of grassland types and environmental variability in our study, effects of organic management on yield were less significant. Fodder quality did also not substantially differ between organic and conventional grasslands. Instead of mineral fertilizer, N2 -fixing legumes such as white clover (Trifolium repens L.) are of high relevance for N supply and soil fertility in organic grasslands (Manusch and Pieringer, 1995). However, a higher abundance of legumes in organic grasslands could not be found. While Ellenberg mN values and nutrient limitation did not differ, we found significantly lower inorganic P concentrations in organic soils, indicating less nutrient-rich conditions in organic than in conventional grasslands. These findings are in line with Gosling and Shepherd (2005) reporting reduced P availability in arable soils after long-term organic management, whereas Wachendorf and Taube (2001) and Hathaway-Jenkins et al. (2011) found no such differences in soil P concentrations of organically and conventionally managed grassland soils after decades of organic management. Although our data gave no clear indication of this, on the very long run P might get significantly limiting plant growth. However, as yield and fodder value of organic grasslands are still as high as those from conventional grasslands, our study disproved concerns of serious economic losses associated with organic management, at least for the studied time span of 18 years. 4.2. Vascular plant diversity Vascular plant diversity was not significantly higher under organic management, which was consistent for all grassland types.

Other studies comparing organic and conventional grasslands revealed ambiguous results. While Wachendorf and Taube (2001), Mayer et al. (2008), Batáry et al. (2012) and found organic grassland management to promote plant species richness, Manusch and Pieringer (1995), Hole et al. (2005) and Batáry et al. (2010) detected no such differences. In contrast to arable weeds, which clearly benefit from the disuse of herbicides in organic arable fields and which have a higher dispersal potential due to their life strategy (Hole et al., 2005; Rundlöf et al., 2010), grassland plants are considered to respond much slower, most likely due severe seed, dispersal and micro site limitation (Bakker and Berendse, 1999; Donath et al., 2003, 2007; Stein et al., 2008). In our study, neither organic nor conventional grasslands were treated with herbicides, as reported by the farmers. The extent to which plant diversity is positively affected by organic management heavily depends on differences in land-use intensity among grasslands under consideration (Marini et al., 2011). In studies with drastic differences among organic and conventional management, floristic changes were much more distinct than in studies with less variation in land use and without herbicide applications (Dietschi et al., 2007; Power et al., 2012). However, our study indicated that comparing only extremes (highly intensive conventional and lowest-intensive organic grasslands) does not reflect reality, as organic land use at the plot scale can also be quite intensive. Although diversities of plant functional groups did not respond to organic management either, lower grass and higher herb (but not legume) abundance may indicate less competitive conditions among plant species in grasslands communities under organic compared to conventional management. This is consistent with finding of studies by Willems and van Nieuwstadt (1996) and Batáry et al. (2012). 4.3. Arthropod diversity The total diversity of foliage-living arthropods was significantly higher under organic than conventional management, regardless of different grassland types. Similarly, the diversity of herbivorous species, especially beetles (Colepotera), was higher in organic compared with conventional grasslands, while this was only true for the diversity of all predatory species together. Diversities of single taxa of spiders (Araneae), bugs (Heteropera), cicada (meaning plant- and leafhoppers; Auchenorrhyncha) and predatory beetles (Coleoptera) did not differ between organic and conventional grasslands. Other studies on effects of organic management on arthropods mostly considered arable fields. Authors found both, several taxa to be more species-rich under organic management, and also some taxa to be more species-rich under conventional management (Weibull et al., 2003; Bengtsson et al., 2005; Fuller et al., 2005; Hole et al., 2005). A study of Batáry et al. (2012) in grasslands in Germany found neither epigaeic (predatory) beetles, nor spiders to be more species rich under organic management, while diversity of epigaeic non-carnivore beetles were positively affected by organic management in grasslands. Especially such herbivorous species strongly rely on resource supply and quality such as N concentrations in biomass (Siemann, 1998; Morris, 2000). As in our study resource supply was found to be similar in organic and conventional grasslands, a decrease in herbivore abundance due to reduced fertilizer application as supposed by Albrecht et al. (2010) is unlikely. Higher lignin (ADL) concentrations in organic plant biomass, which are typical for the yield of low-intensively used grasslands (Klaus et al., 2011), did apparently not generally negatively influence resource supply for herbivorous arthropods. Several studies reported negative effects of intensive management on foliage-living arthropod diversity (e.g. Foster et al.,

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2010; Zahn et al., 2010), especially intensive application of fertilizers, which can exceed positive effects of higher productivity on arthropod species richness by moderate fertilization as reported by Siemann (1998). Moderate fertilization under organic management seems to be sufficient to provide high quality fodder for these taxa. Moreover, significantly lower cutting frequencies have favored especially foliage-living (herbivorous) arthropods in our study. The increased abundance of herbs in organic grasslands may also have positively influenced the diversity of herbivorous arthropods, although plant diversity itself was not higher under organic management. Higher herbivorous species diversity may then have positively affected predatory species diversity, although positive effects of diversity dampen with higher trophic levels (Scherber et al., 2010). Meanwhile, the abundance of any arthropod taxa in the herb layer including herbivores was not affected by organic management, although this was reported previously (e.g. Hole et al., 2005; Birkhofer et al., 2008; Batáry et al., 2012). Thus, although herbivory was not measured directly, the danger of increasing plant damage under organic management is rather unlikely. Banning herbicides and pesticides has strong direct and indirect effects on arthropods. However, this is much more important in crop fields (Hole et al., 2005; Geiger et al., 2010), as the application of pesticides in grasslands is less common. In our study, farmers did not report the usage of pesticides for any conventional grassland (data not shown). Finally, whether a positive (or negative) effect of organic grassland management on a single arthropod taxa can be found may also strongly depend on a multiplicity of direct and indirect effects such as species specific interactions (Joern and Laws, 2013) or the position of the sampling transect in the grasslands (edge vs. center) (Power et al., 2012) and on site specific characteristics such as the landscape setting (Schweiger et al., 2005; Winqvist et al., 2011).

response to organic management as especially for plant diversity more time is required to recover from former intensive use (Jonason et al., 2011). However, lower land-use intensity and lower soil P concentrations in organic grasslands are potentially favorable for higher plant diversity, but active re-introduction of plant species by propagule transfer might be needed to overcome seed and dispersal limitation (Hölzel and Otte, 2003; Bakker and ter Heerdt, 2005; Donath et al., 2007). By a successful increase in plant diversity also a further increase in arthropod diversity can be expected. Such measures directly assisting the restoration of biodiversity in organic grasslands open a new perspective and could become an integral part of organic management. We suggest that although organic management in grasslands did not automatically increase the diversity of all studied taxa within the time of consideration, it still can be considered as a reasonable and useful way to effectively produce agricultural goods while enhancing the overall perspectives of agro-biodiversity.

4.4. Time since conversion to organic management

Appendix A. Supplementary data

Except organic P concentrations in soil, none of the recorded parameters showed a significant trend with time since conversion to organic management. Although yield and fodder quality were not affected by lower P concentrations in soil, we cannot rule out that decreasing soil fertility might negatively affect yield of organic grasslands in the very long run. However, within the analyzed time span of 18 years no such trend was found. Our findings underline that especially plant diversity takes long to recover after intensive land use and heavy fertilization (Walker et al., 2004; Poptcheva et al., 2009). Additionally, further abiotic site factors such as drainage of fen grasslands can suppress re-colonization of species-poor but nowadays low-intensively managed grasslands (Klaus et al., 2013).

Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.agee.2013.05.019.

5. Conclusions Our study showed positive and neutral, but no negative effects of organic grassland management within the analyzed time span of 18 years. All these patterns were consistent for different grassland types. However, although surprisingly even yield did not differ between organic and conventional grasslands, for the future, as indicated by our data, considerably lower organic P concentrations in organic grassland soils can be expected. While the diversity – especially of herbivorous foliage-living arthropods – was clearly higher under organic management, no trend towards higher plant diversity was found after 18 years. This indicates that permanent grasslands significantly differ from crop fields in

Acknowledgments We thank the local management teams of the three exploratories, especially Steffen Both, Martin Gorke, Ralf Lauterbach, Uta Schumacher, Konstans Wells and Kerstin Wiesner. Furthermore, we thank Simone Pfeiffer for their work in maintaining plot and project infrastructure and Dominik Hessenmöller, the late Elisabeth Kalko, Eduard Linsenmair, Jens Nieschulze, Ingo Schöning and ErnstDetlef Schulze for their role in setting up the exploratories project. The work has been funded by the DFG Priority Program 1374 “Infrastructure-Biodiversity-Exploratories” (grants FI 1246/6-1, FI 1246/9-1, HO 3830/2-1, OE 516/1-1, WE 3081/21-1). Field work permits were given by the responsible state environmental offices of Baden-Württemberg, Thüringen and Brandenburg (according to § 72 BbgNatSchG).

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