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Species diversity of remnant calcareous grasslands in south eastern Germany depends on litter cover and landscape structure
Acta Oecologica 83 (2017) 48e55
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Species diversity of remnant calcareous grasslands in south eastern Germany depends on litter cover and landscape structure Stephanie Huber a, Birgit Huber a, Silvia Stahl a, Christoph Schmid b, Christoph Reisch a, *, 1 a b
University of Regensburg, Institute of Plant Sciences, 93040 Regensburg, Germany €dter Landstr. 1, 85764 Neuherberg, Germany German Research Center for Environmental Health, Research Unit Comparative Microbiome Analysis, Ingolsta
a r t i c l e i n f o
a b s t r a c t
Article history: Received 13 December 2016 Received in revised form 21 June 2017 Accepted 29 June 2017
Species diversity depends on, often interfering, multiple ecological drivers. Comprehensive approaches are hence needed to understand the mechanisms determining species diversity. In this study, we analysed the impact of vegetation structure, soil properties and fragmentation on the plant species diversity of remnant calcareous grasslands, therefore, in a comparative approach. We determined plant species diversity of 18 calcareous grasslands in south eastern Germany including all species and grassland specialists separately. Furthermore, we analysed the spatial structure of the grasslands as a result of fragmentation during the last 150 years (habitat area, distance to the nearest calcareous grassland and connectivity in 1830 and 2013). We also collected data concerning the vegetation structure (height of the vegetation, cover of bare soil, grass and litter) and the soil properties (content of phosphorous and potassium, ratio of carbon and nitrogen) of the grassland patches. Data were analysed using Bayesian multiple regressions. We observed a habitat loss of nearly 80% and increasing isolation between grasslands since 1830. In the Bayesian multiple regressions the species diversity of the studied grasslands depended negatively on cover of litter and to a lower degree on the distance to the nearest calcareous grassland in 2013, whereas soil properties had no significant impact. Our study supports the observation that vegetation structure, which strongly depends on land use, is often more important for the species richness of calcareous grasslands than fragmentation or soil properties. Even small and isolated grasslands may, therefore, contribute significantly to the conservation of species diversity, when they are still grazed. © 2017 Elsevier Masson SAS. All rights reserved.
Keywords: Extinction debt dry grasslands Land use Litter Grazing Soil nutrients
1. Introduction Calcareous grasslands belong to the most species-rich ecosystems in Central Europe and are, therefore, under a strong conservation focus (Poschlod and Wallis De Vries, 2002; Wallis De Vries et al., 2002). The species diversity of these local biodiversity hotspots depends on multiple ecological drivers, which often interfere and fragmentation has been identified as one of the most important factors reducing species richness within small and isolated habitat patches (Debinski and Holt, 2000; Fahrig, 2003; Saunders et al., 1991). Due to land use changes, calcareous grasslands strongly
* Corresponding author. University of Regensburg, Institute of Plant Sciences, D93040 Regensburg, Germany. E-mail address: [email protected] (C. Reisch). 1 Declaration of authorship: SH, BH and SS collected the data, CS conducted the statistical analyses, CR designed the study and wrote the manuscript. http://dx.doi.org/10.1016/j.actao.2017.06.011 1146-609X/© 2017 Elsevier Masson SAS. All rights reserved.
declined in Europe during the last 150 years (Poschlod, 2015). Agricultural intensification, the application of fertilizer, and afforestation caused a loss of grasslands, which reached locally up to 90% (Cousins et al., 2007). As a result calcareous grasslands are often highly fragmented, which means that the area of the grassland patches continuously decreased while their spatial isolation increased (Krauss et al., 2004). The impact of fragmentation on plant species diversity is derived from the theory of island biogeography (Brown and KodricBrown, 1977), since populations within the remnants will only survive when they are large enough to support a viable population and/or when re-immigration after extinction from a nearby grassland patch is possible (Zulka et al., 2014). Cessation of traditional land use and the connected loss of dispersal vectors, such as migrating sheep, additionally impedes the exchange of seeds between fragmented grasslands (Poschlod and Bonn, 1998; Poschlod et al., 1998; Poschlod and Wallis De Vries, 2002). As a consequence
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specialist plant species become extinct and the species richness of € cklin, fragmented calcareous grassland decreases (Fischer and Sto 1997). However, fragmentation effects on plant species diversity may be delayed, which has previously been described as “extinction debt” (Helm et al., 2006). Besides habitat area and isolation, land use by grazing strongly affects species diversity of fragmented grasslands. Lack of grazing due to abandonment completely changes vegetation structure (Bobbink and Willems, 1987; Wells, 1969), leads to the dominance of grasses and causes the loss of the typical open short-grass condition of calcareous grasslands (Zulka et al., 2014). Moreover, it can cause the encroachment of shrubs and increase competition (Gazol et al., 2012). Especially ground shadowing due to the dominance of grasses and litter accumulation causes reduction of species having a demand for light at germination (Jensen and Gutekunst, 2003; Piqueray et al., 2015). Moreover, litter hinders the germinating , 2012). Beyond seeds to reach the soil surface (Ruprecht and Szabo grazing and its impact on vegetation structure, species diversity may, however, also depend on soil properties. Calcareous grassland species are generally adapted to low levels of nutrients and the increasing deposition of nitrogen from the air and fertilised agricultural land is known to cause a decrease in species richness (Bobbink et al., 2010) and shifts in the species composition (Diekmann et al., 2014). Although the impact of increased nitrogen input has been studied more intensively (Bobbink et al., 2010), it has been reported that phosphorous content has long-term effects on species composition (Smits et al., 2008) and species diversity (Janssens et al., 1998) and that enhanced phosphorous is more likely to be the cause of species loss than nitrogen enrichment (Wassen et al., 2005). The impact of fragmentation, land use or soil properties on species diversity is, as mentioned above, beyond all question. However, these environmental factors operate simultaneously and maybe also interactively, which may be the reason for the ambignez et al., 2014). Recently, it has uous results of different studies (Iba for example been stated, “….that broad generalizations about the effects of fragmentation on remnant vegetation may not be possible due to the large variety of processes and responses associated with nez et al., 2014). Comprehensive approaches fragmentation” (Iba are, hence, strongly needed to analyse the mechanisms determining species diversity of calcareous grasslands. More recent studies follow these comprehensive approaches and combine historical data, patch quality data and landscape data to analyse the impact of land use and fragmentation on species richness of calcareous grasslands (Gazol et al., 2012; Reitalu et al., 2010, 2014; Zulka et al., 2014). In the study presented here, we took on this idea and used Bayesian multiple regressions to analyse the species diversity of calcareous grasslands in a comprehensive approach. More specifically, our aim was to identify the parameters determining species richness within isolated grassland patches in south eastern Germany. 2. Methods 2.1. Fragmentation For our study we selected randomly 18 remnant calcareous grasslands in the valleys of the rivers Naab and Laber on the Franconian Alb in south eastern Germany near Regensburg (Table 1, Fig. 1). In this region the climate is subcontinental with an annual precipitation of 649 mm and a mean annual temperature of 7.4 C (BayKLIMFOR, 1996). The calcareous grasslands belong to the phytosociological association Gentiano-Koelerietum (Sendtko, 1993). The study sites were vectorised using GIS (Arc Info 10.0, Esri) based upon corrected aerial photos (orthophotos) from 2013
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and using historical maps from 1830. We studied fragmentation and vectorised, therefore, all other grasslands occurring within a radius of 3 km around the selected study sites in 2013 and 1830. We chose this value, since 3 km are a realistic migration distance for many species of dry grasslands that are dispersed by sheep from one grassland to another (Helm et al., 2006). Vectorised data were used to calculate the current and previous habitat area (HA2013 and HA1830), the distance to the nearest calcareous grassland in 2013 and 1830 (D2013 and D1830) and the connectivity of each fragment to all other fragments (CO2013 and CO1830) within the 3 km radius in P 2013 and 1830 according to Hanski (1994) as Si ¼ exp(adij)Aj jsi distance bewhere Si is the connectivity of the patch i, dij is the tween patches i and j and Aj is the area of the patch j. Additionally we compared the area covered by calcareous grassland in 1830 and 2013 and calculated the habitat loss (HL) within the 3 km radius around each of our study sites as percentage of the grassland area lost since 1830 and we characterized the shape of the study sites in 2013 by the ratio of habitat area and perimeter (HA/P2013), which is small for narrow, stretched and large for round, compact grasslands. Based upon the historical maps grasslands were classified as historically old, when they were already grassland in 1830, and historically young grasslands, when they originated only after 1830.
2.2. Land use, vegetation structure and soil properties It is assumed that the selected grasslands date back to the Roman Empire period (Poschlod and Baumann, 2010). They have been grazed frequently until the 1960s, as most other grasslands in central Europe (Poschlod, 2015). Meanwhile, they are abandoned or infrequently grazed. Detailed information about the grazing history is, however, not available. For our study, we established 10 study plots with the size of 2 2 m at each of the selected grasslands to analyse the impact of the habitat conditions on species diversity. In each plot we determined the vegetation height (VH) as well as the cover of grass (CG), litter (CL) and bare soil (BS). Furthermore, we took five soil samples at each study site with a core sampler, which were then pooled, in order to analyse nutrient content of the soil. Pooled samples were dried in a heating cabinet at 50 C for several days, cleaned by sieving with 2 mm mesh size and then stored at 4 C until they were subjected to a soil chemical analysis following the procedures described by Bassler et al. (2003). We determined the content of phosphorous (P) and potassium (K), as well as the carbon to nitrogen ratio (C/N) as described previously (Karlík and Poschlod, 2009).
2.3. Species diversity Two different estimates of species diversity were used: total species richness (SR) and species density (SD) (Cousins et al., 2007). Total species richness of the grasslands was surveyed by recording all occurring species while walking through the study sites. In contrast species density was determined based upon the plant species growing within the 10 study plots per site. Since herbs are most indicative for vegetation changes in calcareous grasslands we recorded all herb species occurring at the study sites and within the plots. Since dry grassland specialists and other ecologically more generalist species may react differently on environmental parameters, we separated dry grassland specialists from all other recorded species and calculated total species richness and species density separately for all species (SRall, SDall) and for dry grassland specialists (SRspec, SDspec). We considered all species as specialists, which were assigned to the phytosociological class FestucoBrometea following the flora of Oberdorfer (2001).
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Table 1 Geographic location of the selected study sites, the area of the grasslands in m2 in 1830 and 2013 (HA1830 and HA2013), the distance to the nearest calcareous grassland (D1830 and D2013) within a radius of 3 km in 1830 and 2013 in meter, and the loss of calcareous grasslands within this radius since 1830 in % (HL) and the area/perimeter ratio (HA/ P2013) in 2013. St. 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18
Name Eichelberg Münchsried Oel Staudenberg Eitelberg Kühschlag Kallmünz Kronbuckel Ziegelhütte Weichseldorf Fuchsenbügl Undorf Schafbuckel Goldberg €nhofen Scho Traidendorf €nsleite Ga Pfaffenberg
Lat. (N)
49 49 49 49 49 49 49 49 49 49 49 49 49 49 49 49 49 49
Mean SE
0
05 040 060 070 010 000 090 040 040 080 090 010 040 010 000 100 080 020
Long. (N) 26 16 01 39 49 12 35 39 22 08 42 43 41 57 36 11 59 35
11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11
0
49 560 580 570 550 570 580 520 530 560 580 550 590 590 570 570 570 540
15 29 10 60 43 20 29 53 28 37 00 53 13 47 20 01 26 28
HA
2013
HA
1830
D2013
D1830
HL
HA/P2013
445 631 763 1020 1399 1440 1546 1695 2495 5659 6211 8009 12033 22160 21894 24405 64984 91067
715410 0 6725 0 0 3308 11072 1176 0 37519 13243 0 17338 0 58015 134710 440768 631523
58 980 391 97 117 340 175 382 41 290 60 91 150 32 211 58 222 87
129 133 81 70 97 98 168 62 24 273 15 59 192 121 251 44 63 94
83.01 79.12 61.88 67.04 84.25 82.43 83.75 80.55 78.33 71.19 83.21 84.49 77.90 66.83 81.99 84.95 78.88 85.32
2.41 3.95 3.44 5.31 8.56 8.25 6.67 4.79 4.69 12.26 11.22 20.89 17.12 12.31 23.84 15.02 23.17 24.87
14881 ±5828
115045 ±53938
210 ±53
110 ±17
78.62 ±1.67
11.60 ±1.79
2.4. Bayesian multiple regression We applied Bayesian multiple regressions to identify the parameters determining species diversity of isolated grassland patches in south eastern Germany. The Bayesian framework enables a more detailed interpretation of the data while being more flexibly adaptable to the data structure than methods testing the significance of null hypotheses (NHST methods). Especially when analysing data sets consisting of many parameters yet a comparatively low sample size, Bayesian methods are superior to NHST methods. This allows us to present a robust, yet powerful analysis of the mechanisms regulating species diversity of the selected calcareous grasslands. Predictor variables were grassland fragmentation parameters (fragment area, area/perimeter ratio as well as distance to the nearest calcareous grassland and the loss of calcareous grassland within a 3 km radius since 1830 around the selected study sites), vegetation structure parameters (vegetation height, cover of grass, litter and bare soil) and soil properties (contents of P, K and C/N ratio). As habitat age was different in our selection of field sites, this variable was at first included as a factor in the model according to the available data. There was no credible influence of habitat age detectable by the model and, hence, the corresponding model parameters were difficult to estimate. Accordingly, habitat age as a parameter hampered model interpretation and was, therefore, excluded from the final analysis. A Bayesian approach was chosen for being flexibly adjustable to the situation at hand, e.g. it can be easily modified to reduce false positives in parameter estimation or improved to better handle outliers in the data. Besides that, results from Bayesian models have a higher informative value than classical NHST methods as they provide full probability distributions on the estimated parameters. Modelling and interpretation were carried out using the software packages R 3.2.1 (R-Core-Team, 2013) and JAGS 3.4.0 for Markov Chain Monte Carlo (MCMC) sampling (Plummer, 2003) as well as utility functions provided by Kruschke (2015). Errors were modelled as being t-distributed in order to accommodate outliers. Regression parameters were regularised using mildly informed, t-distributed priors with normality parameters set to 5 thereby reducing chances for false positives. These settings are known as the Bayesian Lasso (Park and Casella, 2008)
and avoid overfitting in complex models, which reduces the overestimation effects that can happen in AIC-based model selection procedures. The complete and commented JAGS model specification is available from the supplementary material. Sampling was carried out with four MCMC chains with 500k steps each, a burn-in period of 1000 steps and 500 steps for adaption. All parameters were checked for chain convergence using trace plots, thereby ensuring none of the chains got stuck at local maxima. Autocorrelation was assessed as the effective sample size (ESS) aiming at a lower limit of 10k for the relevant parameters in order to assure that a representative part of the posterior distribution was sampled. Predictor variables were checked for multicollinearity before model interpretation using pairwise Pearson correlations (maximum observed < 0.7) and checking the marginal posterior distributions of regression parameters for strongly increased uncertainties. Multicollinearity was, however, not present in the data set. Highest density intervals (HDIs) were computed for the regression coefficients to check if coefficients were credibly non-zero. The predictors’ relative influences were assessed using standardised regression coefficients. Graphs were produced by fixing all but the predictors of credible influence to their mean, resulting in two dimensional scatter plots.
3. Results 3.1. Fragmentation In 2013 the area of the selected grasslands ranged from 445 to 91067 m2 with a mean of 14881 m2 (Table 1). In contrast the mean area of the study sites amounted to 115045 m2 in 1830 which is nearly ten times as much as 2013. In 2013 the mean distance to the nearest calcareous grassland patch within a 3 km radius was 210 m and ranged from 32 m to 980 m. In 1830 the mean distance was with 110 m only half as much and ranged from 15 m to 273 m. Mean habitat loss since 1830 within the 3 km radius around the study sites was 78.62% and varied between 61.8% and 85.32%. The ratio of habitat area and perimeter, as indicator for the shape of the patch, ranged from 2.41 to 24.87 with a mean of 11.60 (Table 1). Connectivity among all calcareous grasslands was in 1830 nearly three times higher as connectivity in 2013 (Table 2).
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Table 2 Connectivity among calcareous grasslands within the 3 km radius around the selected study sites in 1830 and 2013. St.
Name
CO2013
CO1830
01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18
Eichelberg Münchsried Oel Staudenberg Eitelberg Kühschlag Kallmünz Kronbuckel Ziegelhütte Weichseldorf Fuchsenbügl Undorf Schafbuckel Goldberg €nhofen Scho Traidendorf €nsleite Ga Pfaffenberg
8.35 2.34 1.96 11.65 44.65 26.52 48.29 13.94 15.55 9.24 66.19 50.75 3.60 7.19 32.96 71.44 48.36 38.90
100.90 23.89 9.76 37.16 130.80 62.28 82.16 59.55 70.72 43.21 101.79 132.94 13.19 21.15 78.99 97.91 97.09 183.16
Mean SE
27.90 ±5.38
74.81 ±11.01
3.2. Vegetation structure and soil properties Vegetation height on the study sites was between 0.51 m and 1.18 m with a mean of 0.93 m (Table 3). The grass cover varied between 48.0% and 90.0% and was on average 76.5%, while the litter cover ranged from 7.7% to 38.0% with a mean of 20.4%. The minimum proportion of bare soil was 0% and the maximum 5.5% with an average value of 0.7%. The content of phosphorous differed strongly between sites and ranged from 8.04 mg/kg soil to 53.76 mg/kg soil with a mean of 26.47 mg/kg soil (Table 3). Similarly, the content of potassium varied between 101.22 mg/kg soil and 319.02 mg/kg soil. On average we observed potassium content of 211.06 mg/kg soil. Finally, we determined the carbon to nitrogen ratio, which ranged from 10.9 to 42.0 with a mean of 19.6 (Table 3).
3.3. Species diversity Total species richness varied between 30 and 63 with a mean of 45.1 for all species occurring at the study sites. Considering only dry grassland specialists it ranged from 10 to 31 with a mean of 25.3. The species density of the studied calcareous grasslands ranged from 14.2 to 26.9 and was on average 18.5 when all reported species were included (Table 3). Restricting the calculation to grassland specialists, species density varied between 4.6 and 13.0 with a mean of 10.6.
3.4. Bayesian multiple regression
Fig. 1. Geographic location of the 18 selected study sites (labelled dots) in the valleys of Naab and Laber on the Franconian Alb in south eastern Germany near Regensburg and all other calcareous grasslands (grey areas) within a radius of 3 km around the study sites in 1830 and 2013 (© Bayerische Vermessungsverwaltung) (from Reisch et al. 2017, BMC Ecol (2017) 17:19 DOI 10.1186/s12898-017-0129-9).
Bayesian multiple regressions revealed a credible negative impact of the cover of litter on total species richness considering all occurring species, whereas the total species richness of the dry grassland specialists depended negatively on the current distance to the nearest grassland (Table 4, Fig. 2). The density of all species and of the dry grassland species also depended negatively on the cover of litter (Table 5, Fig. 3).
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Table 3 Species diversity of the selected study sites measured as total species richness and species density for all species (SRall/SDall) and the dry grassland specialists (SRspec/SDspec), the height of the vegetation in meter (VH), the cover of litter in % (CL), the cover of grass in % (CG), the cover of bare soil in % (BS) as well as the content of phosphorous in mg/kg soil (P), potassium in mg/kg soil (K) and the ratio of carbon and nitrogen (C/N). St.
Name
SRall
SRspec
SDall
SDspec
VH
CG
CL
BS
P
K
C/N
01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18
Eichelberg Münchsried Oel Staudenberg Eitelberg Kühschlag Kallmünz Kronbuckel Ziegelhütte Weichseldorf Fuchsenbügl Undorf Schafbuckel Goldberg €nhofen Scho Traidendorf G€ ansleite Pfaffenberg
42 35 37 30 47 52 39 49 50 43 50 52 63 42 47 44 45 44
25 15 18 10 26 27 22 21 32 31 29 27 29 25 29 29 29 31
18.0 15.8 15.7 14.2 21.6 21.6 19.5 19.8 19.4 22.8 19.1 15.4 26.9 11.9 18.6 17.7 18.7 16.1
10.3 07.8 07.7 04.6 10.3 10.1 11.8 09.4 13.5 17.2 12.9 06.9 13.0 07.1 11.9 12.9 12.4 10.9
1.18 0.95 0.94 1.54 1.08 0.91 0.77 1.13 0.93 0.51 1.15 1.13 1.01 1.13 0.43 0.31 0.98 0.65
92.8 62.5 90.0 67.0 88.2 87.0 82.5 88.8 84.5 63.0 74.5 90.3 78.0 62.0 73.0 48.0 66.0 78.0
23.0 19.0 24.0 29.0 16.6 30.5 15.0 10.3 17.5 14.5 19.0 25.5 07.7 29.0 20.5 38.0 17.0 10.4
0.0 0.3 0.0 0.0 0.0 0.3 5.5 0.4 0.8 0.8 0.1 0.1 0.0 0.2 0.2 1.5 1.8 0.5
14.70 15.66 36.48 53.76 14.18 26.63 12.70 23.85 37.63 16.25 31.92 41.19 37.90 37.57 37.63 09.62 20.67 08.04
369.53 101.22 232.81 272.77 130.26 192.97 195.62 220.63 169.02 135.42 249.64 173.90 240.98 127.73 247.30 319.02 294.17 126.00
18.3 13.7 15.6 16.0 22.6 42.0 17.6 16.6 21.8 20.1 19.0 37.4 18.1 19.9 17.6 13.9 10.9 11.1
Mean SE
45.1 ±1.76
25.3 ±1.41
18.5 ±0.8
10.6 ±0.7
0.93 ±0.1
76.5 ±3.0
20.4 ±1.9
0.7 ±0.3
26.47 ±3.11
211.06 ±17.52
19.6 ±1.9
Table 4 Results of the Bayesian multiple regression on total species richness. Modal values of marginal distributions of each standardised regression coefficient (RC) are given together with the effective sample size (ESS) of all parameters. A 95% highest density interval (HDI) was computed for each model parameter. The cover of litter (CL) and the habitat area in 2013 (HA2013) exhibited a credible impact on the total species richness at the selected study sites (in bold letters) as its HDI excludes zero. For a detailed explanation of the abbreviations please see Tables 1e3. SRall
Intercept HA1830 HA2013 HA/P P K C/N VH CG CL BS D1830 D2013 CO1830 CO2013 Variance parameter Normality parameter
SRspec
RC
ESS
HDIlow
HDIup
RC
ESS
HDIlow
HDIup
0,00 0,15 0,09 0,36 0,23 0,25 0,58 0,23 0,03 ¡0,65 0,26 0,24 0,27 0,33 0,05 0,59 5,95
231702,30 40557,90 37207,60 33129,60 44447,00 55258,70 48577,30 83381,60 55534,30 46897,00 99925,50 44474,80 89065,00 35472,60 39147,50 31505,90 85829,40
0,39 0,78 0,78 0,30 0,81 0,27 0,04 0,69 0,48 ¡1,13 0,66 0,76 0,69 1,02 0,57 0,28 1,00
0,38 0,49 0,59 1,10 0,38 0,71 1,06 0,30 0,59 ¡0,02 0,19 0,28 0,20 0,41 0,73 1,27 90,52
0,01 0,20 0,05 0,14 0,13 0,03 0,43 0,51 0,13 0,48 0,20 0,18 ¡0,48 0,17 0,12 0,55 5,63
239025,70 30942,80 36933,00 36958,30 51553,70 52077,80 55829,90 58003,60 56200,60 46514,70 97162,80 47452,50 96050,80 32985,20 35249,60 32397,00 75462,50
0,36 0,45 0,71 0,46 0,71 0,49 0,13 1,00 0,62 0,90 0,57 0,65 ¡0,86 0,88 0,52 0,26 1,00
0,36 0,86 0,62 0,82 0,42 0,43 0,87 0,03 0,40 0,11 0,24 0,35 ¡0,01 0,49 0,77 1,19 89,51
4. Discussion 4.1. Impact of fragmentation Taking into account the strong decline of calcareous grasslands within our study region, in the past 200 years, we expected a significant impact of fragmentation on the species diversity of the selected grasslands. Indeed, nearly 80% of the habitat disappeared, patch size often decreased and the distance to the nearby grassland increased during the fragmentation process. Declining species diversity due to reduced habitat area and increasing isolation has been proven in many investigations (Adriaens et al., 2006; Bruun, 2000; Cousins et al., 2007; Krauss et al., 2004). However, in our study species diversity was generally independent from current habitat area, as previously reported k et al. (2016b). This may be due to the fact that despite by Dea different grassland area all study sites must be considered as small
k et al., 2016b). Moreover, edge effects may increase the islands (Dea species richness especially of small patches due to the immigration of plant species from other surrounding habitats such as forests or arable fields (Murcia, 1995). Excluding these edge effects by considering only dry grassland species, total species richness decreased, however, credibly with increasing distance to the nearest calcareous grassland in 2013, indicating an impact of fragmentation and the present landscape configuration on species richness. Our results support, therefore, the assumption derived from the theory of island biogeography (Brown and Kodric-Brown, 1977), that the immigration likelihood of species in isolated fragments decreases with increasing distance to potential source populations. In contrast to total species richness, species density did not depend on fragmentation, which has already been reported and can be explained by the fact that species density is more sensitive to land use and its continuity (Cousins et al., 2007). We observed no evidence for an extinction debt as previously
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Fig. 2. Relationship between total species richness of all species (SRall) and the cover of litter (CL) in % (a), as well as between the total species richness of the dry grassland specialists (SRspec) and the distance to the nearest calcareous grassland in 2013 (D2013) in m (b) on 18 selected calcareous grasslands in south eastern Germany displayed as two dimensional scatter plots based upon the results of the Bayesian multiple regression. Dashed lines represent twenty randomly chosen steps from the MCMC chains and are added to depict the variability in the posterior distribution of the regression parameters.
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Fig. 3. Relationship between species density of all species (SDall) (a) as well as the dry grassland specialists (SDspec) (b) and the cover of litter in % (CL) in % on 18 selected calcareous grasslands in south eastern Germany displayed as two dimensional scatter plots based upon the results of the Bayesian multiple regression. Dashed lines represent twenty randomly chosen steps from the MCMC chains and are added to depict the variability in the posterior distribution of the regression parameters.
Table 5 Results of the Bayesian multiple regression on species density. Modal values of marginal distributions of each standardised regression coefficient (RC) are given together with the effective sample size (ESS) of all parameters. A 95% highest density interval (HDI) was computed for each model parameter. The cover of litter (CL) exhibits a credible impact on the species density at the selected study sites (in bold letters) as its HDI excludes zero. For a detailed explanation of the abbreviations please see Tables 1e3. SDall
Intercept HA1830 HA2013 HA/P P K C/N VH CG CL BS D1830 D2013 CO1830 CO2013 Variance parameter Normality parameter
SDspec
RC
ESS
HDIlow
HDIup
RC
ESS
HDIlow
HDIup
0,00 0,21 0,08 0,00 0,33 0,42 0,46 0,18 0,08 ¡0,75 0,16 0,08 0,17 0,20 0,07 0,67 7,12
260827,70 46693,70 48136,50 47159,90 56601,10 55052,30 53409,10 94932,10 65628,20 52530,50 114524,50 78637,80 119004,10 50744,50 49199,00 41778,40 95681,40
0,42 0,89 0,81 0,68 0,94 0,18 0,19 0,70 0,62 ¡1,30 0,58 0,41 0,61 0,92 0,56 0,35 1,00
0,42 0,46 0,59 0,67 0,29 0,92 0,97 0,34 0,50 ¡0,09 0,32 0,62 0,33 0,50 0,78 1,36 91,43
0,01 0,10 0,15 0,14 0,14 0,15 0,32 0,61 0,32 ¡0,71 0,10 0,05 0,33 0,22 0,18 0,59 7,57
229949,40 34169,00 42774,50 36386,70 50543,60 62242,30 44089,70 53474,70 45798,10 35554,30 99073,20 62360,70 109804,40 40356,40 37488,80 32441,30 91461,40
0,38 0,55 0,83 0,79 0,75 0,32 0,29 1,07 0,84 ¡1,22 0,48 0,51 0,73 0,88 0,49 0,29 1,00
0,39 0,76 0,52 0,56 0,40 0,64 0,79 0,01 0,26 ¡0,05 0,37 0,50 0,16 0,48 0,86 1,25 91,69
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reported in other studies (Alofs et al., 2014; Guardiola et al., 2013; Helm et al., 2006; Krauss et al., 2010; Piqueray et al., 2011), since species diversity did not depend on former habitat area or isolation. In this context it should, however, be considered that the detection of an extinction debt may depend on the spatial scale (Cousins and Vanhoenacker, 2011; Guardiola et al., 2013). It is, therefore, possible, that an extinction debt occurs at a landscape level we did not analyse in our study. 4.2. Impact of vegetation structure and land use It has already been demonstrated, that land use and its continuity can play an important role for the species diversity and composition of calcareous grasslands (Johannson et al., 2008; Karlík and Poschlod, 2009; Reitalu et al., 2010). In our study we observed, however, no differences in species diversity between historically old and young grasslands. Maybe such differences could be revealed by a more detailed analysis including further time periods. Nevertheless, land use had a large impact on species diversity, since both total species richness of all species and species density depended on the cover of litter and, therefore, indirectly on land use by grazing. Typical grasslands specialists missing at study sites with a low species richness and an increased cover of litter are e.g. Pulsatilla vulgaris, Globularia punctata, Anthyllis vulneraria or Pimpinella saxifraga. It is already known, that grazing strongly affects vegetation structure (Bobbink and Willems, 1987; Wells, 1969) and has thus an enormous impact on the species diversity of calcareous grasslands (Reitalu et al., 2010, 2014). Lack of grazing leads to the dominance of competitive grasses suppressing the small, lightdemanding herbs (Bobbink and Willems, 1987). However, the most important effect of abandonment is litter accumulation (Foster and Gross, 1998), which strongly affected species density here. Although depending on the productivity of the habitat, the accumulation of biomass may have several negative consequences for calcareous grasslands (Kelemen et al., 2013). Litter can decrease solar irradiation on the soil surface (Amatangelo et al., 2008), acts as a mechanical barrier impeding seedling establishment (Ruprecht , 2012) and might decrease the number of flowering and Szabo shoots, which lowers seed production and may lead to a seed limitation over generations (Bischoff et al., 2005). Especially, ground shadowing due to increasing vegetation height, dominance of grasses and litter accumulation conducts to the regression of species having a demand for light at germination (Jensen and Gutekunst, 2003; Piqueray et al., 2015). This is most probably leading to the observed decline in plant species diversity of the calcareous grasslands we studied here. 4.3. Impact of soil properties In contrast to our expectations, we detected no credible impact of soil properties on total species richness or species density. The contents of phosphorous and potassium at our study sites were maximum 53 mg (P) and 370 mg (K) per kilogram soil respectively and were within the range reported previously for calcareous grasslands in Belgium (Jacquemyn et al., 2003). The observed level of nutrients may be the reason why we found no significant impact on species diversity. As already reported by Janssens et al. (1998), species diversity is not related to phosphorous content under 50 mg P per kilogram soil. Furthermore, high potassium contents are just like that compatible with high levels of species diversity. This means that the levels of P and K are so low in the soils of the analysed grasslands, that they have no impact on species diversity. Similarly to our results, Cousins et al. (2009) found a strong impact of land use but no relationship between the content of nitrogen, phosphorous and the species richness of calcareous grasslands. Our
results support, therefore, other studies, concluding that land use by grazing and the related export of nutrients with migrating sheep flocks may buffer the effects of increasing soil nutrients (Newton et al., 2012; Poschlod and Wallis De Vries, 2002). 5. Conclusions The impact of fragmentation on species diversity has been studied elaborately and is widely accepted in conservation. However, it has also been stated recently that “broad generalizations about the effects of fragmentation” remain difficult (Ib anez et al., 2014), especially due to the effects of different habitat conditions. In the study presented here, vegetation structure had a stronger impact on species diversity than fragmentation and soil properties. Consequently, it can be concluded, that even small and isolated grasslands may contribute significantly to the conservation of species diversity, when they are still grazed. The reestablishment of grazing is, therefore, the most promising approach to preserve the species richness of fragmented calcareous grasslands. However, the management of isolated grassland fragments by grazing is a challenging task for nature conservation. Nevertheless, the restoration of landscape connectivity is crucial for the long-term preservation of small isolated grasslands (De ak et al., 2016a). Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements Special thanks go to Christina Putz for her support with the selection of the study sites, to Sabine Fischer for her help with GIS, to Günther Kolb for technical assistance during soil analyses and to Peter Poschlod for his generous support. References Adriaens, D., Honnay, O., Hermy, M., 2006. No evidence of a plant extinction debt in highly fragmented calcareous grasslands in Belgium. Biol. Conserv. 133, 212e224. lez, A.V., Fowler, N.L., 2014. Local native plant diversity responds Alofs, K.M., Gonza to habitat loss and fragmentation over different time spans and spatial scales. Plant Ecol. 215, 1139e1151. Amatangelo, K.L., Dukes, J.S., Field, C.B., 2008. Responses of a California annual grassland to litter manipulation. J. Veg. Sci. 19, 605e612. Bassler, R., Schmitt, L., Siegel, O., 2003. Methodenbuch/Verband Deutscher Landwirtschaftlicher Untersuchungsanstalten, 4. Auflage ed.. VDLUFA-Verlag, Darmstadt. BayKLIMFOR, 1996. Klimaatlas von Bayern, München. Bischoff, A., Auge, H., Mahn, E.G., 2005. Seasonal changes in the relationship between plant species richness and community biomass in early succession. Basic Appl. Ecol. 6, 385e394. Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmett, B., Erisman, J.W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., De Vriess, W., 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30e59. Bobbink, R., Willems, J.H., 1987. Increasing dominance of Brachypodium pinnatum (L.) Beauv. In: Chalk Grasslands: a Threat to a Species-rich Grassland. Biol Conserv, vol. 40, pp. 301e314. Brown, J.H., Kodric-Brown, A., 1977. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58, 445e449. Bruun, H.H., 2000. Patterns of spceis richness in dry grassland patches in an agricultural landscape. Ecography 23, 641e650. Cousins, S.A.O., Lindborg, R., Mattson, S., 2009. Land use history and site location are more important for grassland species richness than local soil properties. Nord. J. Bot. 27, 483e489.
S. Huber et al. / Acta Oecologica 83 (2017) 48e55 Cousins, S.A.O., Ohlson, H., Eriksson, O., 2007. Effects of historical and present fragmentation on plant species diversity in semi-natural grasslands in Swedish rural landscapes. Landsc. Ecol. 22, 723e730. Cousins, S.A.O., Vanhoenacker, D., 2011. Detection of extinction debts depends on scale and specialisation. Biol. Conserv. 144, 782e787. thme re sz, B., Valko , O., Sudnik-Wo jcikowska, B., Moysiyenko, I.I., De ak, B., To €ro €k, P., 2016a. Cultural Bragina, T.M., Apostolova, I., Dembicz, I., Bykov, N.I., To monuments and nature conservation: a review of the role of kurgans in the conservation and restoration of steppe vegetation. Biodivers. Conserv. 25, 2473e2490. , O., To €ro €k, P., To thme re sz, B., 2016b. Factors threatening grassland De ak, B., Valko specialist plants - a multi-proxy study on the vegetation of isolated grasslands. Biol. Conserv. 204, 255e262. Debinski, D.M., Holt, R.D., 2000. A survey and overview of habitat fragmentation experiments. Conserv. Biol. 14, 342e355. Diekmann, M., Jandt, U., Alard, D., Bleeker, A., Corcket, E., Gowing, D.J.G., , C., 2014. Long-term changes in calcareous grassland vegeStevens, C.J., Dupre tation in North-western Germany - no decline in species richness, but a shift in species composition. Biol. Conserv. 172, 170e179. Fahrig, L., 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Syst. 34, 487e515. €cklin, J., 1997. Local extinctions of plants in remnants of extensively Fischer, M., Sto used calcareous grasslands 1950-1985. Conserv. Biol. 11, 727e737. Foster, B.L., Gross, K.L., 1998. Species richness in a successional grassland: effects of nitrogen enrichment and plant litter. Ecology 79, 2593e2602. Gazol, A., Tamme, R., Takkis, K., Kasari, L., Saar, L., Helm, A., P€ artel, M., 2012. Landscape- and small-scale determinants of grassland species diversity: direct and indirect influences. Ecography 35, 944e951. Guardiola, M., Pino, J., Rod a, F., 2013. Patch history and spatial scale modulate local plant extinction and extinction debt in habitat patches. Divers. Distrib. 19, 825e833. Hanski, I., 1994. Patch occupancy dynamics in fragmented landscapes. Trend Ecol. Evol. 9, 131e135. Helm, A., Hanski, I., P€ artel, M., 2006. Slow response of plant species richness to habitat loss and fragmentation. Ecol. Lett. 9, 72e77. nez, I., Katz, D.S.W., Peltier, D., Wolf, S.M., Connor Barrie, B.T., 2014. Assessing the Iba integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess-multiresponse dynamics. J. Ecol. 102, 882e895. Jacquemyn, H., Brys, R., Hermy, M., 2003. Short-term effects of different management regimes on the response of calcareous grassland vegetation to increased nitrogen. Biol. Conserv. 111, 137e147. 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 Soil 202, 69e76. Jensen, K., Gutekunst, K., 2003. Effects of litter on establishment of grassland plant species: the role of seed size and successional status. Basic Appl. Ecol. 4, 579e587. €m, M., Johannson, L.J., Hall, K., Prentice, H.C., Ihse, M., Reitalu, T., Sykes, M.T., Kindstro 2008. Semi-natural grassland continuity, long-term land-use and plant species € richness in an agricultural landscape on Oland. Swed. Landsc. Urban Plan. 84, 200e211. Karlík, P., Poschlod, P., 2009. History of abiotic filter: which is more important in determining the species composition of calcareous grasslands. Preslia 81, 321e340. €ro €k, P., Valko , O., Migle cz, T., To thme re sz, B., 2013. Mechanisms Kelemen, A., To shaping plant biomass and species richness: plant strategies and litter effect in alkali and loess grasslands. J. Veg. Sci. 24, 1195e1203. Krauss, J., Bommarco, R., Guardiola, M., Heikkinen, R.K., Helm, A., Kuusaari, M., € €rtel, M., Pino, J., Po €yry, J., Raatikainen, K.M., Sang, A., Lindborg, R., Ockinger, E., Pa Stefanescu, C., Teder, T., Zobel, M., Steffan-Dewenter, I., 2010. Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol. Lett. 13, 597e605. Krauss, J., Klein, A.-M., Steffan-Dewenter, I., Tscharntke, T., 2004. Effects of habitat area, isolation, and landscape diversity on plant species richness of calcareous grasslands. Biodivers. Conserv. 13, 1427e1439. Kruschke, J.K., 2015. Doing Bayesian Data Analysis - a Tutorial with R, JAGS, and
55
Stan. Academic Press, Waltham. Murcia, C., 1995. Edge effects in fragmented forests: implications for conservation. Trend Ecol. Evol. 10, 58e62. Newton, A.C., Walls, R.M., Golicher, D., Keith, S.A., Diaz, A., Bullock, J.M., 2012. Structure, composition and dynamics of a calcareous grassland metacommunity over a 70-year interval. J. Ecol. 100, 196e209. Oberdorfer, E., 2001. Pflanzensoziologische Exkursionsflora für Deutschland und angrenzende Gebiete (Ulmer, Stuttgart). Park, T., Casella, G., 2008. The Bayesian Lasso. J. Am. Stat. Assoc. 103, 681e686. Piqueray, J., Bisteau, E., Cristofoli, S., Palm, R., Poschlod, P., Mahy, G., 2011. Plant species extinction debt in a temperate biodiversity hotspot: community, species and functional traits approaches. Biol. Conserv. 144, 1619e1629. Piqueray, J., Ferroni, L., Delescaille, L.-M., Speranza, M., Mahy, G., Poschlod, P., 2015. Response of plant functional traits during the restoration of calcareous grasslands from forest stands. Ecol. Indic. 48, 408e416. Plummer, M., 2003. JAGS: a Program for Analysis of Bayesian Graphical Models Using Gibbs Sampling. Poschlod, P., 2015. Geschichte der Kulturlandschaft (Eugen Ulmer, Stuttgart). Poschlod, P., Baumann, A., 2010. The historical dynamics of calcareous grasslands in the Central and Southern Franconian jurassic mountains e a comparative pedoanthracological and pollen analytical study. Holocene 20, 13e23. Poschlod, P., Bonn, S., 1998. Changing dispersal processes in the central European landscape since the last ice age: an explanation for the actual decrease of plant species richness in different habitats? Acta Bot. Neerl 47, 27e44. €nkle, U., Fischer, S.F., Bonn, S., 1998. Plant species richness Poschlod, P., Kiefer, S., Tra in calcareous grasslands as affected by dispersability in space and time. Appl. Veg. Sci. 1, 75e90. Poschlod, P., Wallis De Vries, M.F., 2002. The historical and socioeconomic perspective of calcareous grasslands - lessons from the distant and recent past. Biol. Conserv. 104, 361e376. R-Core-Team, 2013. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project. org/. € pplein, Q., Meyer, C., Hums, C., Putz, C., Reisch, C., Schmidkonz, S., Meier, K., Scho Schmid, C., 2017. Genetic diversity of calcareous grassland plant species depends on historical landscape configuration. BMC Ecol. 17, 19. http://dx.doi.org/ 10.1186/s12898-017-0129-9. €rtel, M., Bengtsson, K., Gerhold, P., Rose n, E., Takkis, K., Reitalu, T., Helm, A., Pa Znamensky, S., Prentice, H.C., 2014. Determinants of fine-scale plant diversity in dry calcareous grasslands within the Baltic Sea region. Agric. Ecosyst. Environ. 182, 59e68. Reitalu, T., Johannson, L.J., Sykes, M.T., Hall, K., Prentice, H.C., 2010. History matters: village distances, grazing and grassland species diversity. J. Appl. Ecol. 47, 1216e1224. , A., 2012. Grass litter is a natural seed trap in long-term unRuprecht, E., Szabo disturbed grassland. J. Veg. Sci. 23, 495e504. Saunders, D.A., Hobbs, R.J., Margules, C.R., 1991. Biological consequences of ecosystem fragmentation: a review. Conserv. Biol. 5, 18e32. Sendtko, A., 1993. Die Flora und Vegetation der Kalkmagerrasen am Schloßberg und Hutberg bei Kallmünz (Landkreis Regensburg). Hoppea 54, 393e454. Smits, N.A.C., Willems, J.H., Bobbink, R., 2008. Long-term after-effects of fertilisation on the restoration of calcareous grasslands. Appl. Veg. Sci. 11, 279e286. Wallis De Vries, M.F., Poschlod, P., Willems, J.H., 2002. Challenges for the conservation of calcareous grasslands in northwestern Europe: integrating the requirements of flora and fauna. Biol. Conserv. 104, 265e273. Wassen, M., Venterinck, H.O., Lapshina, E.D., Tanneberger, F., 2005. Endangered plants persist under phosphorus limitation. Nature 437, 547e550. Wells, T.C.E., 1969. Botanical aspects of conservation management of chalk grasslands. Biol. Conserv. 2, 36e44. Zulka, K.P., Abensberg-Traun, M., Milasowszky, N., Bieringer, G., Gereben-Krenn, B.€ lzler, G., Rabitsch, W., Reischütz, A., Querner, P., A., Holzinger, W., Ho Sauberer, N., Schmitzberger, I., Willner, W., Wrbka, T., Zechmeister, H.G., 2014. Species richness in dry grassland patches of eastern Austria: a multi-taxon study on the role of local, landscape and habitat quality variables. Agric. Ecosyst. Environ. 182, 25e36.
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Acta Oecologica journal homepage: www.elsevier.com/locate/actoec
Species diversity of remnant calcareous grasslands in south eastern Germany depends on litter cover and landscape structure Stephanie Huber a, Birgit Huber a, Silvia Stahl a, Christoph Schmid b, Christoph Reisch a, *, 1 a b
University of Regensburg, Institute of Plant Sciences, 93040 Regensburg, Germany €dter Landstr. 1, 85764 Neuherberg, Germany German Research Center for Environmental Health, Research Unit Comparative Microbiome Analysis, Ingolsta
a r t i c l e i n f o
a b s t r a c t
Article history: Received 13 December 2016 Received in revised form 21 June 2017 Accepted 29 June 2017
Species diversity depends on, often interfering, multiple ecological drivers. Comprehensive approaches are hence needed to understand the mechanisms determining species diversity. In this study, we analysed the impact of vegetation structure, soil properties and fragmentation on the plant species diversity of remnant calcareous grasslands, therefore, in a comparative approach. We determined plant species diversity of 18 calcareous grasslands in south eastern Germany including all species and grassland specialists separately. Furthermore, we analysed the spatial structure of the grasslands as a result of fragmentation during the last 150 years (habitat area, distance to the nearest calcareous grassland and connectivity in 1830 and 2013). We also collected data concerning the vegetation structure (height of the vegetation, cover of bare soil, grass and litter) and the soil properties (content of phosphorous and potassium, ratio of carbon and nitrogen) of the grassland patches. Data were analysed using Bayesian multiple regressions. We observed a habitat loss of nearly 80% and increasing isolation between grasslands since 1830. In the Bayesian multiple regressions the species diversity of the studied grasslands depended negatively on cover of litter and to a lower degree on the distance to the nearest calcareous grassland in 2013, whereas soil properties had no significant impact. Our study supports the observation that vegetation structure, which strongly depends on land use, is often more important for the species richness of calcareous grasslands than fragmentation or soil properties. Even small and isolated grasslands may, therefore, contribute significantly to the conservation of species diversity, when they are still grazed. © 2017 Elsevier Masson SAS. All rights reserved.
Keywords: Extinction debt dry grasslands Land use Litter Grazing Soil nutrients
1. Introduction Calcareous grasslands belong to the most species-rich ecosystems in Central Europe and are, therefore, under a strong conservation focus (Poschlod and Wallis De Vries, 2002; Wallis De Vries et al., 2002). The species diversity of these local biodiversity hotspots depends on multiple ecological drivers, which often interfere and fragmentation has been identified as one of the most important factors reducing species richness within small and isolated habitat patches (Debinski and Holt, 2000; Fahrig, 2003; Saunders et al., 1991). Due to land use changes, calcareous grasslands strongly
* Corresponding author. University of Regensburg, Institute of Plant Sciences, D93040 Regensburg, Germany. E-mail address: [email protected] (C. Reisch). 1 Declaration of authorship: SH, BH and SS collected the data, CS conducted the statistical analyses, CR designed the study and wrote the manuscript. http://dx.doi.org/10.1016/j.actao.2017.06.011 1146-609X/© 2017 Elsevier Masson SAS. All rights reserved.
declined in Europe during the last 150 years (Poschlod, 2015). Agricultural intensification, the application of fertilizer, and afforestation caused a loss of grasslands, which reached locally up to 90% (Cousins et al., 2007). As a result calcareous grasslands are often highly fragmented, which means that the area of the grassland patches continuously decreased while their spatial isolation increased (Krauss et al., 2004). The impact of fragmentation on plant species diversity is derived from the theory of island biogeography (Brown and KodricBrown, 1977), since populations within the remnants will only survive when they are large enough to support a viable population and/or when re-immigration after extinction from a nearby grassland patch is possible (Zulka et al., 2014). Cessation of traditional land use and the connected loss of dispersal vectors, such as migrating sheep, additionally impedes the exchange of seeds between fragmented grasslands (Poschlod and Bonn, 1998; Poschlod et al., 1998; Poschlod and Wallis De Vries, 2002). As a consequence
S. Huber et al. / Acta Oecologica 83 (2017) 48e55
specialist plant species become extinct and the species richness of € cklin, fragmented calcareous grassland decreases (Fischer and Sto 1997). However, fragmentation effects on plant species diversity may be delayed, which has previously been described as “extinction debt” (Helm et al., 2006). Besides habitat area and isolation, land use by grazing strongly affects species diversity of fragmented grasslands. Lack of grazing due to abandonment completely changes vegetation structure (Bobbink and Willems, 1987; Wells, 1969), leads to the dominance of grasses and causes the loss of the typical open short-grass condition of calcareous grasslands (Zulka et al., 2014). Moreover, it can cause the encroachment of shrubs and increase competition (Gazol et al., 2012). Especially ground shadowing due to the dominance of grasses and litter accumulation causes reduction of species having a demand for light at germination (Jensen and Gutekunst, 2003; Piqueray et al., 2015). Moreover, litter hinders the germinating , 2012). Beyond seeds to reach the soil surface (Ruprecht and Szabo grazing and its impact on vegetation structure, species diversity may, however, also depend on soil properties. Calcareous grassland species are generally adapted to low levels of nutrients and the increasing deposition of nitrogen from the air and fertilised agricultural land is known to cause a decrease in species richness (Bobbink et al., 2010) and shifts in the species composition (Diekmann et al., 2014). Although the impact of increased nitrogen input has been studied more intensively (Bobbink et al., 2010), it has been reported that phosphorous content has long-term effects on species composition (Smits et al., 2008) and species diversity (Janssens et al., 1998) and that enhanced phosphorous is more likely to be the cause of species loss than nitrogen enrichment (Wassen et al., 2005). The impact of fragmentation, land use or soil properties on species diversity is, as mentioned above, beyond all question. However, these environmental factors operate simultaneously and maybe also interactively, which may be the reason for the ambignez et al., 2014). Recently, it has uous results of different studies (Iba for example been stated, “….that broad generalizations about the effects of fragmentation on remnant vegetation may not be possible due to the large variety of processes and responses associated with nez et al., 2014). Comprehensive approaches fragmentation” (Iba are, hence, strongly needed to analyse the mechanisms determining species diversity of calcareous grasslands. More recent studies follow these comprehensive approaches and combine historical data, patch quality data and landscape data to analyse the impact of land use and fragmentation on species richness of calcareous grasslands (Gazol et al., 2012; Reitalu et al., 2010, 2014; Zulka et al., 2014). In the study presented here, we took on this idea and used Bayesian multiple regressions to analyse the species diversity of calcareous grasslands in a comprehensive approach. More specifically, our aim was to identify the parameters determining species richness within isolated grassland patches in south eastern Germany. 2. Methods 2.1. Fragmentation For our study we selected randomly 18 remnant calcareous grasslands in the valleys of the rivers Naab and Laber on the Franconian Alb in south eastern Germany near Regensburg (Table 1, Fig. 1). In this region the climate is subcontinental with an annual precipitation of 649 mm and a mean annual temperature of 7.4 C (BayKLIMFOR, 1996). The calcareous grasslands belong to the phytosociological association Gentiano-Koelerietum (Sendtko, 1993). The study sites were vectorised using GIS (Arc Info 10.0, Esri) based upon corrected aerial photos (orthophotos) from 2013
49
and using historical maps from 1830. We studied fragmentation and vectorised, therefore, all other grasslands occurring within a radius of 3 km around the selected study sites in 2013 and 1830. We chose this value, since 3 km are a realistic migration distance for many species of dry grasslands that are dispersed by sheep from one grassland to another (Helm et al., 2006). Vectorised data were used to calculate the current and previous habitat area (HA2013 and HA1830), the distance to the nearest calcareous grassland in 2013 and 1830 (D2013 and D1830) and the connectivity of each fragment to all other fragments (CO2013 and CO1830) within the 3 km radius in P 2013 and 1830 according to Hanski (1994) as Si ¼ exp(adij)Aj jsi distance bewhere Si is the connectivity of the patch i, dij is the tween patches i and j and Aj is the area of the patch j. Additionally we compared the area covered by calcareous grassland in 1830 and 2013 and calculated the habitat loss (HL) within the 3 km radius around each of our study sites as percentage of the grassland area lost since 1830 and we characterized the shape of the study sites in 2013 by the ratio of habitat area and perimeter (HA/P2013), which is small for narrow, stretched and large for round, compact grasslands. Based upon the historical maps grasslands were classified as historically old, when they were already grassland in 1830, and historically young grasslands, when they originated only after 1830.
2.2. Land use, vegetation structure and soil properties It is assumed that the selected grasslands date back to the Roman Empire period (Poschlod and Baumann, 2010). They have been grazed frequently until the 1960s, as most other grasslands in central Europe (Poschlod, 2015). Meanwhile, they are abandoned or infrequently grazed. Detailed information about the grazing history is, however, not available. For our study, we established 10 study plots with the size of 2 2 m at each of the selected grasslands to analyse the impact of the habitat conditions on species diversity. In each plot we determined the vegetation height (VH) as well as the cover of grass (CG), litter (CL) and bare soil (BS). Furthermore, we took five soil samples at each study site with a core sampler, which were then pooled, in order to analyse nutrient content of the soil. Pooled samples were dried in a heating cabinet at 50 C for several days, cleaned by sieving with 2 mm mesh size and then stored at 4 C until they were subjected to a soil chemical analysis following the procedures described by Bassler et al. (2003). We determined the content of phosphorous (P) and potassium (K), as well as the carbon to nitrogen ratio (C/N) as described previously (Karlík and Poschlod, 2009).
2.3. Species diversity Two different estimates of species diversity were used: total species richness (SR) and species density (SD) (Cousins et al., 2007). Total species richness of the grasslands was surveyed by recording all occurring species while walking through the study sites. In contrast species density was determined based upon the plant species growing within the 10 study plots per site. Since herbs are most indicative for vegetation changes in calcareous grasslands we recorded all herb species occurring at the study sites and within the plots. Since dry grassland specialists and other ecologically more generalist species may react differently on environmental parameters, we separated dry grassland specialists from all other recorded species and calculated total species richness and species density separately for all species (SRall, SDall) and for dry grassland specialists (SRspec, SDspec). We considered all species as specialists, which were assigned to the phytosociological class FestucoBrometea following the flora of Oberdorfer (2001).
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Table 1 Geographic location of the selected study sites, the area of the grasslands in m2 in 1830 and 2013 (HA1830 and HA2013), the distance to the nearest calcareous grassland (D1830 and D2013) within a radius of 3 km in 1830 and 2013 in meter, and the loss of calcareous grasslands within this radius since 1830 in % (HL) and the area/perimeter ratio (HA/ P2013) in 2013. St. 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18
Name Eichelberg Münchsried Oel Staudenberg Eitelberg Kühschlag Kallmünz Kronbuckel Ziegelhütte Weichseldorf Fuchsenbügl Undorf Schafbuckel Goldberg €nhofen Scho Traidendorf €nsleite Ga Pfaffenberg
Lat. (N)
49 49 49 49 49 49 49 49 49 49 49 49 49 49 49 49 49 49
Mean SE
0
05 040 060 070 010 000 090 040 040 080 090 010 040 010 000 100 080 020
Long. (N) 26 16 01 39 49 12 35 39 22 08 42 43 41 57 36 11 59 35
11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11
0
49 560 580 570 550 570 580 520 530 560 580 550 590 590 570 570 570 540
15 29 10 60 43 20 29 53 28 37 00 53 13 47 20 01 26 28
HA
2013
HA
1830
D2013
D1830
HL
HA/P2013
445 631 763 1020 1399 1440 1546 1695 2495 5659 6211 8009 12033 22160 21894 24405 64984 91067
715410 0 6725 0 0 3308 11072 1176 0 37519 13243 0 17338 0 58015 134710 440768 631523
58 980 391 97 117 340 175 382 41 290 60 91 150 32 211 58 222 87
129 133 81 70 97 98 168 62 24 273 15 59 192 121 251 44 63 94
83.01 79.12 61.88 67.04 84.25 82.43 83.75 80.55 78.33 71.19 83.21 84.49 77.90 66.83 81.99 84.95 78.88 85.32
2.41 3.95 3.44 5.31 8.56 8.25 6.67 4.79 4.69 12.26 11.22 20.89 17.12 12.31 23.84 15.02 23.17 24.87
14881 ±5828
115045 ±53938
210 ±53
110 ±17
78.62 ±1.67
11.60 ±1.79
2.4. Bayesian multiple regression We applied Bayesian multiple regressions to identify the parameters determining species diversity of isolated grassland patches in south eastern Germany. The Bayesian framework enables a more detailed interpretation of the data while being more flexibly adaptable to the data structure than methods testing the significance of null hypotheses (NHST methods). Especially when analysing data sets consisting of many parameters yet a comparatively low sample size, Bayesian methods are superior to NHST methods. This allows us to present a robust, yet powerful analysis of the mechanisms regulating species diversity of the selected calcareous grasslands. Predictor variables were grassland fragmentation parameters (fragment area, area/perimeter ratio as well as distance to the nearest calcareous grassland and the loss of calcareous grassland within a 3 km radius since 1830 around the selected study sites), vegetation structure parameters (vegetation height, cover of grass, litter and bare soil) and soil properties (contents of P, K and C/N ratio). As habitat age was different in our selection of field sites, this variable was at first included as a factor in the model according to the available data. There was no credible influence of habitat age detectable by the model and, hence, the corresponding model parameters were difficult to estimate. Accordingly, habitat age as a parameter hampered model interpretation and was, therefore, excluded from the final analysis. A Bayesian approach was chosen for being flexibly adjustable to the situation at hand, e.g. it can be easily modified to reduce false positives in parameter estimation or improved to better handle outliers in the data. Besides that, results from Bayesian models have a higher informative value than classical NHST methods as they provide full probability distributions on the estimated parameters. Modelling and interpretation were carried out using the software packages R 3.2.1 (R-Core-Team, 2013) and JAGS 3.4.0 for Markov Chain Monte Carlo (MCMC) sampling (Plummer, 2003) as well as utility functions provided by Kruschke (2015). Errors were modelled as being t-distributed in order to accommodate outliers. Regression parameters were regularised using mildly informed, t-distributed priors with normality parameters set to 5 thereby reducing chances for false positives. These settings are known as the Bayesian Lasso (Park and Casella, 2008)
and avoid overfitting in complex models, which reduces the overestimation effects that can happen in AIC-based model selection procedures. The complete and commented JAGS model specification is available from the supplementary material. Sampling was carried out with four MCMC chains with 500k steps each, a burn-in period of 1000 steps and 500 steps for adaption. All parameters were checked for chain convergence using trace plots, thereby ensuring none of the chains got stuck at local maxima. Autocorrelation was assessed as the effective sample size (ESS) aiming at a lower limit of 10k for the relevant parameters in order to assure that a representative part of the posterior distribution was sampled. Predictor variables were checked for multicollinearity before model interpretation using pairwise Pearson correlations (maximum observed < 0.7) and checking the marginal posterior distributions of regression parameters for strongly increased uncertainties. Multicollinearity was, however, not present in the data set. Highest density intervals (HDIs) were computed for the regression coefficients to check if coefficients were credibly non-zero. The predictors’ relative influences were assessed using standardised regression coefficients. Graphs were produced by fixing all but the predictors of credible influence to their mean, resulting in two dimensional scatter plots.
3. Results 3.1. Fragmentation In 2013 the area of the selected grasslands ranged from 445 to 91067 m2 with a mean of 14881 m2 (Table 1). In contrast the mean area of the study sites amounted to 115045 m2 in 1830 which is nearly ten times as much as 2013. In 2013 the mean distance to the nearest calcareous grassland patch within a 3 km radius was 210 m and ranged from 32 m to 980 m. In 1830 the mean distance was with 110 m only half as much and ranged from 15 m to 273 m. Mean habitat loss since 1830 within the 3 km radius around the study sites was 78.62% and varied between 61.8% and 85.32%. The ratio of habitat area and perimeter, as indicator for the shape of the patch, ranged from 2.41 to 24.87 with a mean of 11.60 (Table 1). Connectivity among all calcareous grasslands was in 1830 nearly three times higher as connectivity in 2013 (Table 2).
S. Huber et al. / Acta Oecologica 83 (2017) 48e55
51
Table 2 Connectivity among calcareous grasslands within the 3 km radius around the selected study sites in 1830 and 2013. St.
Name
CO2013
CO1830
01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18
Eichelberg Münchsried Oel Staudenberg Eitelberg Kühschlag Kallmünz Kronbuckel Ziegelhütte Weichseldorf Fuchsenbügl Undorf Schafbuckel Goldberg €nhofen Scho Traidendorf €nsleite Ga Pfaffenberg
8.35 2.34 1.96 11.65 44.65 26.52 48.29 13.94 15.55 9.24 66.19 50.75 3.60 7.19 32.96 71.44 48.36 38.90
100.90 23.89 9.76 37.16 130.80 62.28 82.16 59.55 70.72 43.21 101.79 132.94 13.19 21.15 78.99 97.91 97.09 183.16
Mean SE
27.90 ±5.38
74.81 ±11.01
3.2. Vegetation structure and soil properties Vegetation height on the study sites was between 0.51 m and 1.18 m with a mean of 0.93 m (Table 3). The grass cover varied between 48.0% and 90.0% and was on average 76.5%, while the litter cover ranged from 7.7% to 38.0% with a mean of 20.4%. The minimum proportion of bare soil was 0% and the maximum 5.5% with an average value of 0.7%. The content of phosphorous differed strongly between sites and ranged from 8.04 mg/kg soil to 53.76 mg/kg soil with a mean of 26.47 mg/kg soil (Table 3). Similarly, the content of potassium varied between 101.22 mg/kg soil and 319.02 mg/kg soil. On average we observed potassium content of 211.06 mg/kg soil. Finally, we determined the carbon to nitrogen ratio, which ranged from 10.9 to 42.0 with a mean of 19.6 (Table 3).
3.3. Species diversity Total species richness varied between 30 and 63 with a mean of 45.1 for all species occurring at the study sites. Considering only dry grassland specialists it ranged from 10 to 31 with a mean of 25.3. The species density of the studied calcareous grasslands ranged from 14.2 to 26.9 and was on average 18.5 when all reported species were included (Table 3). Restricting the calculation to grassland specialists, species density varied between 4.6 and 13.0 with a mean of 10.6.
3.4. Bayesian multiple regression
Fig. 1. Geographic location of the 18 selected study sites (labelled dots) in the valleys of Naab and Laber on the Franconian Alb in south eastern Germany near Regensburg and all other calcareous grasslands (grey areas) within a radius of 3 km around the study sites in 1830 and 2013 (© Bayerische Vermessungsverwaltung) (from Reisch et al. 2017, BMC Ecol (2017) 17:19 DOI 10.1186/s12898-017-0129-9).
Bayesian multiple regressions revealed a credible negative impact of the cover of litter on total species richness considering all occurring species, whereas the total species richness of the dry grassland specialists depended negatively on the current distance to the nearest grassland (Table 4, Fig. 2). The density of all species and of the dry grassland species also depended negatively on the cover of litter (Table 5, Fig. 3).
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S. Huber et al. / Acta Oecologica 83 (2017) 48e55
Table 3 Species diversity of the selected study sites measured as total species richness and species density for all species (SRall/SDall) and the dry grassland specialists (SRspec/SDspec), the height of the vegetation in meter (VH), the cover of litter in % (CL), the cover of grass in % (CG), the cover of bare soil in % (BS) as well as the content of phosphorous in mg/kg soil (P), potassium in mg/kg soil (K) and the ratio of carbon and nitrogen (C/N). St.
Name
SRall
SRspec
SDall
SDspec
VH
CG
CL
BS
P
K
C/N
01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16 17 18
Eichelberg Münchsried Oel Staudenberg Eitelberg Kühschlag Kallmünz Kronbuckel Ziegelhütte Weichseldorf Fuchsenbügl Undorf Schafbuckel Goldberg €nhofen Scho Traidendorf G€ ansleite Pfaffenberg
42 35 37 30 47 52 39 49 50 43 50 52 63 42 47 44 45 44
25 15 18 10 26 27 22 21 32 31 29 27 29 25 29 29 29 31
18.0 15.8 15.7 14.2 21.6 21.6 19.5 19.8 19.4 22.8 19.1 15.4 26.9 11.9 18.6 17.7 18.7 16.1
10.3 07.8 07.7 04.6 10.3 10.1 11.8 09.4 13.5 17.2 12.9 06.9 13.0 07.1 11.9 12.9 12.4 10.9
1.18 0.95 0.94 1.54 1.08 0.91 0.77 1.13 0.93 0.51 1.15 1.13 1.01 1.13 0.43 0.31 0.98 0.65
92.8 62.5 90.0 67.0 88.2 87.0 82.5 88.8 84.5 63.0 74.5 90.3 78.0 62.0 73.0 48.0 66.0 78.0
23.0 19.0 24.0 29.0 16.6 30.5 15.0 10.3 17.5 14.5 19.0 25.5 07.7 29.0 20.5 38.0 17.0 10.4
0.0 0.3 0.0 0.0 0.0 0.3 5.5 0.4 0.8 0.8 0.1 0.1 0.0 0.2 0.2 1.5 1.8 0.5
14.70 15.66 36.48 53.76 14.18 26.63 12.70 23.85 37.63 16.25 31.92 41.19 37.90 37.57 37.63 09.62 20.67 08.04
369.53 101.22 232.81 272.77 130.26 192.97 195.62 220.63 169.02 135.42 249.64 173.90 240.98 127.73 247.30 319.02 294.17 126.00
18.3 13.7 15.6 16.0 22.6 42.0 17.6 16.6 21.8 20.1 19.0 37.4 18.1 19.9 17.6 13.9 10.9 11.1
Mean SE
45.1 ±1.76
25.3 ±1.41
18.5 ±0.8
10.6 ±0.7
0.93 ±0.1
76.5 ±3.0
20.4 ±1.9
0.7 ±0.3
26.47 ±3.11
211.06 ±17.52
19.6 ±1.9
Table 4 Results of the Bayesian multiple regression on total species richness. Modal values of marginal distributions of each standardised regression coefficient (RC) are given together with the effective sample size (ESS) of all parameters. A 95% highest density interval (HDI) was computed for each model parameter. The cover of litter (CL) and the habitat area in 2013 (HA2013) exhibited a credible impact on the total species richness at the selected study sites (in bold letters) as its HDI excludes zero. For a detailed explanation of the abbreviations please see Tables 1e3. SRall
Intercept HA1830 HA2013 HA/P P K C/N VH CG CL BS D1830 D2013 CO1830 CO2013 Variance parameter Normality parameter
SRspec
RC
ESS
HDIlow
HDIup
RC
ESS
HDIlow
HDIup
0,00 0,15 0,09 0,36 0,23 0,25 0,58 0,23 0,03 ¡0,65 0,26 0,24 0,27 0,33 0,05 0,59 5,95
231702,30 40557,90 37207,60 33129,60 44447,00 55258,70 48577,30 83381,60 55534,30 46897,00 99925,50 44474,80 89065,00 35472,60 39147,50 31505,90 85829,40
0,39 0,78 0,78 0,30 0,81 0,27 0,04 0,69 0,48 ¡1,13 0,66 0,76 0,69 1,02 0,57 0,28 1,00
0,38 0,49 0,59 1,10 0,38 0,71 1,06 0,30 0,59 ¡0,02 0,19 0,28 0,20 0,41 0,73 1,27 90,52
0,01 0,20 0,05 0,14 0,13 0,03 0,43 0,51 0,13 0,48 0,20 0,18 ¡0,48 0,17 0,12 0,55 5,63
239025,70 30942,80 36933,00 36958,30 51553,70 52077,80 55829,90 58003,60 56200,60 46514,70 97162,80 47452,50 96050,80 32985,20 35249,60 32397,00 75462,50
0,36 0,45 0,71 0,46 0,71 0,49 0,13 1,00 0,62 0,90 0,57 0,65 ¡0,86 0,88 0,52 0,26 1,00
0,36 0,86 0,62 0,82 0,42 0,43 0,87 0,03 0,40 0,11 0,24 0,35 ¡0,01 0,49 0,77 1,19 89,51
4. Discussion 4.1. Impact of fragmentation Taking into account the strong decline of calcareous grasslands within our study region, in the past 200 years, we expected a significant impact of fragmentation on the species diversity of the selected grasslands. Indeed, nearly 80% of the habitat disappeared, patch size often decreased and the distance to the nearby grassland increased during the fragmentation process. Declining species diversity due to reduced habitat area and increasing isolation has been proven in many investigations (Adriaens et al., 2006; Bruun, 2000; Cousins et al., 2007; Krauss et al., 2004). However, in our study species diversity was generally independent from current habitat area, as previously reported k et al. (2016b). This may be due to the fact that despite by Dea different grassland area all study sites must be considered as small
k et al., 2016b). Moreover, edge effects may increase the islands (Dea species richness especially of small patches due to the immigration of plant species from other surrounding habitats such as forests or arable fields (Murcia, 1995). Excluding these edge effects by considering only dry grassland species, total species richness decreased, however, credibly with increasing distance to the nearest calcareous grassland in 2013, indicating an impact of fragmentation and the present landscape configuration on species richness. Our results support, therefore, the assumption derived from the theory of island biogeography (Brown and Kodric-Brown, 1977), that the immigration likelihood of species in isolated fragments decreases with increasing distance to potential source populations. In contrast to total species richness, species density did not depend on fragmentation, which has already been reported and can be explained by the fact that species density is more sensitive to land use and its continuity (Cousins et al., 2007). We observed no evidence for an extinction debt as previously
S. Huber et al. / Acta Oecologica 83 (2017) 48e55
Fig. 2. Relationship between total species richness of all species (SRall) and the cover of litter (CL) in % (a), as well as between the total species richness of the dry grassland specialists (SRspec) and the distance to the nearest calcareous grassland in 2013 (D2013) in m (b) on 18 selected calcareous grasslands in south eastern Germany displayed as two dimensional scatter plots based upon the results of the Bayesian multiple regression. Dashed lines represent twenty randomly chosen steps from the MCMC chains and are added to depict the variability in the posterior distribution of the regression parameters.
53
Fig. 3. Relationship between species density of all species (SDall) (a) as well as the dry grassland specialists (SDspec) (b) and the cover of litter in % (CL) in % on 18 selected calcareous grasslands in south eastern Germany displayed as two dimensional scatter plots based upon the results of the Bayesian multiple regression. Dashed lines represent twenty randomly chosen steps from the MCMC chains and are added to depict the variability in the posterior distribution of the regression parameters.
Table 5 Results of the Bayesian multiple regression on species density. Modal values of marginal distributions of each standardised regression coefficient (RC) are given together with the effective sample size (ESS) of all parameters. A 95% highest density interval (HDI) was computed for each model parameter. The cover of litter (CL) exhibits a credible impact on the species density at the selected study sites (in bold letters) as its HDI excludes zero. For a detailed explanation of the abbreviations please see Tables 1e3. SDall
Intercept HA1830 HA2013 HA/P P K C/N VH CG CL BS D1830 D2013 CO1830 CO2013 Variance parameter Normality parameter
SDspec
RC
ESS
HDIlow
HDIup
RC
ESS
HDIlow
HDIup
0,00 0,21 0,08 0,00 0,33 0,42 0,46 0,18 0,08 ¡0,75 0,16 0,08 0,17 0,20 0,07 0,67 7,12
260827,70 46693,70 48136,50 47159,90 56601,10 55052,30 53409,10 94932,10 65628,20 52530,50 114524,50 78637,80 119004,10 50744,50 49199,00 41778,40 95681,40
0,42 0,89 0,81 0,68 0,94 0,18 0,19 0,70 0,62 ¡1,30 0,58 0,41 0,61 0,92 0,56 0,35 1,00
0,42 0,46 0,59 0,67 0,29 0,92 0,97 0,34 0,50 ¡0,09 0,32 0,62 0,33 0,50 0,78 1,36 91,43
0,01 0,10 0,15 0,14 0,14 0,15 0,32 0,61 0,32 ¡0,71 0,10 0,05 0,33 0,22 0,18 0,59 7,57
229949,40 34169,00 42774,50 36386,70 50543,60 62242,30 44089,70 53474,70 45798,10 35554,30 99073,20 62360,70 109804,40 40356,40 37488,80 32441,30 91461,40
0,38 0,55 0,83 0,79 0,75 0,32 0,29 1,07 0,84 ¡1,22 0,48 0,51 0,73 0,88 0,49 0,29 1,00
0,39 0,76 0,52 0,56 0,40 0,64 0,79 0,01 0,26 ¡0,05 0,37 0,50 0,16 0,48 0,86 1,25 91,69
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S. Huber et al. / Acta Oecologica 83 (2017) 48e55
reported in other studies (Alofs et al., 2014; Guardiola et al., 2013; Helm et al., 2006; Krauss et al., 2010; Piqueray et al., 2011), since species diversity did not depend on former habitat area or isolation. In this context it should, however, be considered that the detection of an extinction debt may depend on the spatial scale (Cousins and Vanhoenacker, 2011; Guardiola et al., 2013). It is, therefore, possible, that an extinction debt occurs at a landscape level we did not analyse in our study. 4.2. Impact of vegetation structure and land use It has already been demonstrated, that land use and its continuity can play an important role for the species diversity and composition of calcareous grasslands (Johannson et al., 2008; Karlík and Poschlod, 2009; Reitalu et al., 2010). In our study we observed, however, no differences in species diversity between historically old and young grasslands. Maybe such differences could be revealed by a more detailed analysis including further time periods. Nevertheless, land use had a large impact on species diversity, since both total species richness of all species and species density depended on the cover of litter and, therefore, indirectly on land use by grazing. Typical grasslands specialists missing at study sites with a low species richness and an increased cover of litter are e.g. Pulsatilla vulgaris, Globularia punctata, Anthyllis vulneraria or Pimpinella saxifraga. It is already known, that grazing strongly affects vegetation structure (Bobbink and Willems, 1987; Wells, 1969) and has thus an enormous impact on the species diversity of calcareous grasslands (Reitalu et al., 2010, 2014). Lack of grazing leads to the dominance of competitive grasses suppressing the small, lightdemanding herbs (Bobbink and Willems, 1987). However, the most important effect of abandonment is litter accumulation (Foster and Gross, 1998), which strongly affected species density here. Although depending on the productivity of the habitat, the accumulation of biomass may have several negative consequences for calcareous grasslands (Kelemen et al., 2013). Litter can decrease solar irradiation on the soil surface (Amatangelo et al., 2008), acts as a mechanical barrier impeding seedling establishment (Ruprecht , 2012) and might decrease the number of flowering and Szabo shoots, which lowers seed production and may lead to a seed limitation over generations (Bischoff et al., 2005). Especially, ground shadowing due to increasing vegetation height, dominance of grasses and litter accumulation conducts to the regression of species having a demand for light at germination (Jensen and Gutekunst, 2003; Piqueray et al., 2015). This is most probably leading to the observed decline in plant species diversity of the calcareous grasslands we studied here. 4.3. Impact of soil properties In contrast to our expectations, we detected no credible impact of soil properties on total species richness or species density. The contents of phosphorous and potassium at our study sites were maximum 53 mg (P) and 370 mg (K) per kilogram soil respectively and were within the range reported previously for calcareous grasslands in Belgium (Jacquemyn et al., 2003). The observed level of nutrients may be the reason why we found no significant impact on species diversity. As already reported by Janssens et al. (1998), species diversity is not related to phosphorous content under 50 mg P per kilogram soil. Furthermore, high potassium contents are just like that compatible with high levels of species diversity. This means that the levels of P and K are so low in the soils of the analysed grasslands, that they have no impact on species diversity. Similarly to our results, Cousins et al. (2009) found a strong impact of land use but no relationship between the content of nitrogen, phosphorous and the species richness of calcareous grasslands. Our
results support, therefore, other studies, concluding that land use by grazing and the related export of nutrients with migrating sheep flocks may buffer the effects of increasing soil nutrients (Newton et al., 2012; Poschlod and Wallis De Vries, 2002). 5. Conclusions The impact of fragmentation on species diversity has been studied elaborately and is widely accepted in conservation. However, it has also been stated recently that “broad generalizations about the effects of fragmentation” remain difficult (Ib anez et al., 2014), especially due to the effects of different habitat conditions. In the study presented here, vegetation structure had a stronger impact on species diversity than fragmentation and soil properties. Consequently, it can be concluded, that even small and isolated grasslands may contribute significantly to the conservation of species diversity, when they are still grazed. The reestablishment of grazing is, therefore, the most promising approach to preserve the species richness of fragmented calcareous grasslands. However, the management of isolated grassland fragments by grazing is a challenging task for nature conservation. Nevertheless, the restoration of landscape connectivity is crucial for the long-term preservation of small isolated grasslands (De ak et al., 2016a). Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements Special thanks go to Christina Putz for her support with the selection of the study sites, to Sabine Fischer for her help with GIS, to Günther Kolb for technical assistance during soil analyses and to Peter Poschlod for his generous support. References Adriaens, D., Honnay, O., Hermy, M., 2006. No evidence of a plant extinction debt in highly fragmented calcareous grasslands in Belgium. Biol. Conserv. 133, 212e224. lez, A.V., Fowler, N.L., 2014. Local native plant diversity responds Alofs, K.M., Gonza to habitat loss and fragmentation over different time spans and spatial scales. Plant Ecol. 215, 1139e1151. Amatangelo, K.L., Dukes, J.S., Field, C.B., 2008. Responses of a California annual grassland to litter manipulation. J. Veg. Sci. 19, 605e612. Bassler, R., Schmitt, L., Siegel, O., 2003. Methodenbuch/Verband Deutscher Landwirtschaftlicher Untersuchungsanstalten, 4. Auflage ed.. VDLUFA-Verlag, Darmstadt. BayKLIMFOR, 1996. Klimaatlas von Bayern, München. Bischoff, A., Auge, H., Mahn, E.G., 2005. Seasonal changes in the relationship between plant species richness and community biomass in early succession. Basic Appl. Ecol. 6, 385e394. Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmett, B., Erisman, J.W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., De Vriess, W., 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30e59. Bobbink, R., Willems, J.H., 1987. Increasing dominance of Brachypodium pinnatum (L.) Beauv. In: Chalk Grasslands: a Threat to a Species-rich Grassland. Biol Conserv, vol. 40, pp. 301e314. Brown, J.H., Kodric-Brown, A., 1977. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58, 445e449. Bruun, H.H., 2000. Patterns of spceis richness in dry grassland patches in an agricultural landscape. Ecography 23, 641e650. Cousins, S.A.O., Lindborg, R., Mattson, S., 2009. Land use history and site location are more important for grassland species richness than local soil properties. Nord. J. Bot. 27, 483e489.
S. Huber et al. / Acta Oecologica 83 (2017) 48e55 Cousins, S.A.O., Ohlson, H., Eriksson, O., 2007. Effects of historical and present fragmentation on plant species diversity in semi-natural grasslands in Swedish rural landscapes. Landsc. Ecol. 22, 723e730. Cousins, S.A.O., Vanhoenacker, D., 2011. Detection of extinction debts depends on scale and specialisation. Biol. Conserv. 144, 782e787. thme re sz, B., Valko , O., Sudnik-Wo jcikowska, B., Moysiyenko, I.I., De ak, B., To €ro €k, P., 2016a. Cultural Bragina, T.M., Apostolova, I., Dembicz, I., Bykov, N.I., To monuments and nature conservation: a review of the role of kurgans in the conservation and restoration of steppe vegetation. Biodivers. Conserv. 25, 2473e2490. , O., To €ro €k, P., To thme re sz, B., 2016b. Factors threatening grassland De ak, B., Valko specialist plants - a multi-proxy study on the vegetation of isolated grasslands. Biol. Conserv. 204, 255e262. Debinski, D.M., Holt, R.D., 2000. A survey and overview of habitat fragmentation experiments. Conserv. Biol. 14, 342e355. Diekmann, M., Jandt, U., Alard, D., Bleeker, A., Corcket, E., Gowing, D.J.G., , C., 2014. Long-term changes in calcareous grassland vegeStevens, C.J., Dupre tation in North-western Germany - no decline in species richness, but a shift in species composition. Biol. Conserv. 172, 170e179. Fahrig, L., 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Syst. 34, 487e515. €cklin, J., 1997. Local extinctions of plants in remnants of extensively Fischer, M., Sto used calcareous grasslands 1950-1985. Conserv. Biol. 11, 727e737. Foster, B.L., Gross, K.L., 1998. Species richness in a successional grassland: effects of nitrogen enrichment and plant litter. Ecology 79, 2593e2602. Gazol, A., Tamme, R., Takkis, K., Kasari, L., Saar, L., Helm, A., P€ artel, M., 2012. Landscape- and small-scale determinants of grassland species diversity: direct and indirect influences. Ecography 35, 944e951. Guardiola, M., Pino, J., Rod a, F., 2013. Patch history and spatial scale modulate local plant extinction and extinction debt in habitat patches. Divers. Distrib. 19, 825e833. Hanski, I., 1994. Patch occupancy dynamics in fragmented landscapes. Trend Ecol. Evol. 9, 131e135. Helm, A., Hanski, I., P€ artel, M., 2006. Slow response of plant species richness to habitat loss and fragmentation. Ecol. Lett. 9, 72e77. nez, I., Katz, D.S.W., Peltier, D., Wolf, S.M., Connor Barrie, B.T., 2014. Assessing the Iba integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess-multiresponse dynamics. J. Ecol. 102, 882e895. Jacquemyn, H., Brys, R., Hermy, M., 2003. Short-term effects of different management regimes on the response of calcareous grassland vegetation to increased nitrogen. Biol. Conserv. 111, 137e147. 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 Soil 202, 69e76. Jensen, K., Gutekunst, K., 2003. Effects of litter on establishment of grassland plant species: the role of seed size and successional status. Basic Appl. Ecol. 4, 579e587. €m, M., Johannson, L.J., Hall, K., Prentice, H.C., Ihse, M., Reitalu, T., Sykes, M.T., Kindstro 2008. Semi-natural grassland continuity, long-term land-use and plant species € richness in an agricultural landscape on Oland. Swed. Landsc. Urban Plan. 84, 200e211. Karlík, P., Poschlod, P., 2009. History of abiotic filter: which is more important in determining the species composition of calcareous grasslands. Preslia 81, 321e340. €ro €k, P., Valko , O., Migle cz, T., To thme re sz, B., 2013. Mechanisms Kelemen, A., To shaping plant biomass and species richness: plant strategies and litter effect in alkali and loess grasslands. J. Veg. Sci. 24, 1195e1203. Krauss, J., Bommarco, R., Guardiola, M., Heikkinen, R.K., Helm, A., Kuusaari, M., € €rtel, M., Pino, J., Po €yry, J., Raatikainen, K.M., Sang, A., Lindborg, R., Ockinger, E., Pa Stefanescu, C., Teder, T., Zobel, M., Steffan-Dewenter, I., 2010. Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol. Lett. 13, 597e605. Krauss, J., Klein, A.-M., Steffan-Dewenter, I., Tscharntke, T., 2004. Effects of habitat area, isolation, and landscape diversity on plant species richness of calcareous grasslands. Biodivers. Conserv. 13, 1427e1439. Kruschke, J.K., 2015. Doing Bayesian Data Analysis - a Tutorial with R, JAGS, and
55
Stan. Academic Press, Waltham. Murcia, C., 1995. Edge effects in fragmented forests: implications for conservation. Trend Ecol. Evol. 10, 58e62. Newton, A.C., Walls, R.M., Golicher, D., Keith, S.A., Diaz, A., Bullock, J.M., 2012. Structure, composition and dynamics of a calcareous grassland metacommunity over a 70-year interval. J. Ecol. 100, 196e209. Oberdorfer, E., 2001. Pflanzensoziologische Exkursionsflora für Deutschland und angrenzende Gebiete (Ulmer, Stuttgart). Park, T., Casella, G., 2008. The Bayesian Lasso. J. Am. Stat. Assoc. 103, 681e686. Piqueray, J., Bisteau, E., Cristofoli, S., Palm, R., Poschlod, P., Mahy, G., 2011. Plant species extinction debt in a temperate biodiversity hotspot: community, species and functional traits approaches. Biol. Conserv. 144, 1619e1629. Piqueray, J., Ferroni, L., Delescaille, L.-M., Speranza, M., Mahy, G., Poschlod, P., 2015. Response of plant functional traits during the restoration of calcareous grasslands from forest stands. Ecol. Indic. 48, 408e416. Plummer, M., 2003. JAGS: a Program for Analysis of Bayesian Graphical Models Using Gibbs Sampling. Poschlod, P., 2015. Geschichte der Kulturlandschaft (Eugen Ulmer, Stuttgart). Poschlod, P., Baumann, A., 2010. The historical dynamics of calcareous grasslands in the Central and Southern Franconian jurassic mountains e a comparative pedoanthracological and pollen analytical study. Holocene 20, 13e23. Poschlod, P., Bonn, S., 1998. Changing dispersal processes in the central European landscape since the last ice age: an explanation for the actual decrease of plant species richness in different habitats? Acta Bot. Neerl 47, 27e44. €nkle, U., Fischer, S.F., Bonn, S., 1998. Plant species richness Poschlod, P., Kiefer, S., Tra in calcareous grasslands as affected by dispersability in space and time. Appl. Veg. Sci. 1, 75e90. Poschlod, P., Wallis De Vries, M.F., 2002. The historical and socioeconomic perspective of calcareous grasslands - lessons from the distant and recent past. Biol. Conserv. 104, 361e376. R-Core-Team, 2013. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project. org/. € pplein, Q., Meyer, C., Hums, C., Putz, C., Reisch, C., Schmidkonz, S., Meier, K., Scho Schmid, C., 2017. Genetic diversity of calcareous grassland plant species depends on historical landscape configuration. BMC Ecol. 17, 19. http://dx.doi.org/ 10.1186/s12898-017-0129-9. €rtel, M., Bengtsson, K., Gerhold, P., Rose n, E., Takkis, K., Reitalu, T., Helm, A., Pa Znamensky, S., Prentice, H.C., 2014. Determinants of fine-scale plant diversity in dry calcareous grasslands within the Baltic Sea region. Agric. Ecosyst. Environ. 182, 59e68. Reitalu, T., Johannson, L.J., Sykes, M.T., Hall, K., Prentice, H.C., 2010. History matters: village distances, grazing and grassland species diversity. J. Appl. Ecol. 47, 1216e1224. , A., 2012. Grass litter is a natural seed trap in long-term unRuprecht, E., Szabo disturbed grassland. J. Veg. Sci. 23, 495e504. Saunders, D.A., Hobbs, R.J., Margules, C.R., 1991. Biological consequences of ecosystem fragmentation: a review. Conserv. Biol. 5, 18e32. Sendtko, A., 1993. Die Flora und Vegetation der Kalkmagerrasen am Schloßberg und Hutberg bei Kallmünz (Landkreis Regensburg). Hoppea 54, 393e454. Smits, N.A.C., Willems, J.H., Bobbink, R., 2008. Long-term after-effects of fertilisation on the restoration of calcareous grasslands. Appl. Veg. Sci. 11, 279e286. Wallis De Vries, M.F., Poschlod, P., Willems, J.H., 2002. Challenges for the conservation of calcareous grasslands in northwestern Europe: integrating the requirements of flora and fauna. Biol. Conserv. 104, 265e273. Wassen, M., Venterinck, H.O., Lapshina, E.D., Tanneberger, F., 2005. Endangered plants persist under phosphorus limitation. Nature 437, 547e550. Wells, T.C.E., 1969. Botanical aspects of conservation management of chalk grasslands. Biol. Conserv. 2, 36e44. Zulka, K.P., Abensberg-Traun, M., Milasowszky, N., Bieringer, G., Gereben-Krenn, B.€ lzler, G., Rabitsch, W., Reischütz, A., Querner, P., A., Holzinger, W., Ho Sauberer, N., Schmitzberger, I., Willner, W., Wrbka, T., Zechmeister, H.G., 2014. Species richness in dry grassland patches of eastern Austria: a multi-taxon study on the role of local, landscape and habitat quality variables. Agric. Ecosyst. Environ. 182, 25e36.