Traditionally managed mountain grasslands are biodiversity
hotspots in central Europe. However, socio-economic trends in agriculture
during the last decades have changed farming practices, leaving steep and remote
sites abandoned. Especially the abandonment of meadows is well known to
directly affect plant and insect diversity. However, not much is known about the
effects on soil processes and soil biota. To assess this, we studied four
extensively managed (mown once a year, no fertilization) and four abandoned
(no mowing, no fertilization) semi-dry meadows in a mountain region in
Austria. Plant species richness, plant cover, plant traits, plant biomass,
litter decomposition (tea bag index), and earthworm species richness and
density were assessed. Additionally, soil temperature, moisture and
electrical conductivity were measured. Results showed that managed meadows
contained more plant species than abandoned meadows (118 vs. 93 species,
respectively). We also observed different plant species assemblages between
the two management types. In managed meadows, hemirosette and ruderal plant
species were more abundant, while more plant species without rosettes and a
higher plant necromass were found in abandoned meadows. Additionally,
decomposition rate was higher in abandoned meadows. There was a trend
towards higher earthworm densities in managed meadows, but there was no difference in
earthworm species richness. We conclude that meadow management has effects
on both aboveground vegetation and belowground biota and processes. Both
abandoned and extensively managed meadows were important to sustain overall
biodiversity and ecosystem functioning in the study region.
Introduction
Mountain areas in central Europe consist of a high variety of natural
grasslands, managed meadows and pastures, and woody areas
(Schmitzberger et al., 2005). Most of the grasslands are traditionally managed and related to high species richness of, for example, plants (Schmitzberger
et al., 2005), bumblebees (Walcher et al., 2017) and hoverflies (Hussain et
al., 2018), thus forming biodiversity hotspots. Among these grasslands,
especially semi-dry, nutrient-poor meadows represent particularly species-rich plant agroecosystems inhabiting many rare and protected plant and
animal species (Bohner et al., 2003; Wilson et al., 2012). To protect these species-rich grasslands, regular extensive management is an important measure for nature conservation (Bohner et al.,
2003; Lundber et al., 2017; Moog et al., 2002). However, socio-economic
trends have led to a decline of traditional farming practices
(Hejcman et al., 2013).
Furthermore, small side-job farms are being replaced by more intensively
managed larger farms (Lieskovský et
al., 2015; Marini et al., 2011). Hence, two contrasting patterns can be
observed: intensification (increased fertilization and mowing frequency) of
easily accessible high-yielding areas on the one hand and abandonment in
areas that are difficult to manage with agricultural machinery on the other
hand (MacDonald et al., 2000; Niedrist et al., 2009; Tasser and Tappeiner, 2002). In this context, steep and remote mountain meadows have been increasingly abandoned (Niedrist et al., 2009) resulting in a reduction
of these semi-natural grasslands within Europe (Baur et al., 2006) and a loss of these biodiversity hotspots.
Land-use changes have been shown to be the most important driving force for
changes in the vegetation (Tasser and Tappeiner, 2002). These changes affect plant functional diversity and species composition (Bohner
et al., 2003; Maurer, 2005; Niedrist et al., 2009; Rolecek et al., 2014;
Tasser and Tappeiner, 2002) as well as the structure of plant biomass, as
abandonment increases litter accumulation
(Kelemen et al., 2014). Litter decomposition is
a key process in ecosystems that drives nutrient cycling. Decomposition
depends on changes in plant species composition, the functional
characteristics of plants (Hättenschwiler et al.,
2005; Meier and Bowman, 2008), the activity of soil biota such as earthworms,
and abiotic factors such as temperature and moisture (Lavelle
et al., 1998).
Generally, effects of grassland management on plant communities are well
studied, but little is known about management impacts on soil organisms and
processes and their interaction with vegetation, especially considering
mountain grasslands. In many grasslands, earthworms account for most of the
biomass of soil-dwelling fauna (Lavelle and Spain, 2001). They
are considered as ecosystem engineers, playing an important role in soil
formation and nutrient cycle (Blouin et al., 2013; Lavelle,
1997). Earthworms are known to influence the density, diversity, structure
and activity of microorganisms, and soil meso- and macrofauna
(Wurst et al., 2018). Earthworms have been shown
to react to changes in plant diversity and functional groups
(Piotrowska et al., 2013; Spehn et al., 2000; Zaller and Arnone III, 1999b), changes which have also been observed after abandonment of meadow management (e.g. changes in root biomass, nutrient supply and primary production). Consequently, we hypothesized for the current study that differences in meadow management may
alter soil biota and processes via changes in plant communities
(Hooper et al., 2005).
We expected that (i) mowing once a year will increase plant species
richness, alter vegetation structure and reduce plant necromass in managed
meadows compared to abandoned sites and that (ii) these changes in plant
communities and structure will stimulate earthworm abundance and increase
litter decomposition.
Material and methodsStudy sites
The study was conducted in the central Ennstal in the
Long-Term Socio-economic and Ecosystem Research (LTSER) region Eisenwurzen
(federal state of Styria, Austria) across eight study sites in the
municipalities of St. Gallen (47∘41′ N, 14∘37′ E), Pürgg (47∘31′ N, 14∘03′ E) and Stainach (47∘32′ N,
14∘06′ E) ranging from 660 to 790 m above sea
level. All sites are located in temperate sub-oceanic climate with a
long-term mean annual air temperature of 6.9 ∘C and a mean annual
precipitation of 1087 mm (ZAMG, 2018). Four extensively
managed and four abandoned meadows were studied in June and August 2016.
Study meadows were in close distance to each other with similar site
conditions such as meadow size, exposition, soil type and climate
(Table S1 in the Supplement). Each managed meadow was mown once a year without any fertilizer input for at least 20 years. They are assigned to the grassland type Bromion erecti (semi-dry grassland; Mucina et al., 1993),
with the grass species Bromus erectus Huds., the herb Astrantia major major L. and the grass Festuca rubra rubra L. as the dominant
plant species. The abandoned meadows were not mown for on average 30 years
and dominated by the tall grass Brachypodium pinnatum (L.) P. Beauv. Before abandonment,
grasslands were extensively mown but not grazed. All information about
management was obtained from interviews with land owners.
Plant species richness (a), Shannon index (b) and evenness (c) in
abandoned and managed meadows. * denotes significant difference between
management types (p<0.05). Means ± SD.
MeasurementsVegetation
For vegetation measurements four 1 m × 1 m study plots (distance 5 m) were randomly selected on each meadow. Vascular plant species within the plots were identified (Fischer et al., 2008) and plant cover
estimated using a modified Braun-Blanquet (1964) scale
containing three subdivisions per cover class (Bohner et al., 2012). Plant species frequency (rooted frequency) was counted per plot.
Plant biomass was assessed in June by cutting 50 cm × 50 cm subplots within the vegetation plots (4 cm above ground) and plant material separated into necromass and living biomass. In the laboratory, living biomass was further
separated in the functional groups grasses (Poaceae, Juncaceae and
Cyperaceae), legumes (Fabaceae) and non-legume herbs. Necromass and
functional groups were dried at 60 ∘C for 72 h and weighed.
Plant species were assigned into strategy types competitors,
stress tolerators and ruderals according to Grime (1977).
The management influence on plant architecture categories rosette,
hemirosette and erosulate (no rosette) was assessed according to
Klotz et al. (2002).
Litter decomposition
Following Keuskamp et al. (2013) the tea bag approach with two types of commercial tea bags (rooibos
tea – Lipton, EAN: 87 22700 18843 8 and green tea – Lipton, EAN: 87 22700
05552 5) was used to determine microbial and mesofaunal litter
decomposition. First, tea bags were dried for 1 h at 70 ∘C and
weighed. In June, 10 tea bag pairs of rooibos and green tea were buried in 8 cm depth in a circle of 2 m radius within a representative area in each
meadow considering exposition, slope, shading by trees. Second, after 68–71
days, tea bags were removed, cleaned from attached soil particles with a
toothbrush, dried for 48 h at 70 ∘C and weighed. Third, according
to the respective protocol
(http://www.teatime4science.org/method/stepwise-protocol/, last access: 10 May 2019),
decomposition rate k (rapidly decomposed plant material with easily
degradable compounds) and litter stabilization factor S (labile fraction,
which stabilize and become recalcitrant during decomposition) were
calculated. Thirteen pairs of tea bags in managed and 4 pairs in abandoned
meadows could not be found in August or were defective and not considered.
Earthworm sampling and soil properties
In each meadow, five sampling plots were randomly chosen at equal distance
of 5 m. Next, a 25 cm × 25 cm × 25 cm (length × width × depth) soil monolith was excavated with a spade. The excavated soil was carefully searched for earthworms on a plastic foil, and each earthworm found was preserved in 4 % formol.
In the laboratory, each sample was first washed under distilled water and
then separated into juvenile and adult earthworms. Juvenile earthworms
without a clitellum could not be identified at the species level but
were sorted into ecological groups endogeic, anecic and epigeic
(Bouché, 1977), counted and weighed. Adult earthworms with
a clitellum were identified after Brohmer (1984) and
Christian and Zicsi (1999), also allocated to the
ecological groups, counted and weighed.
Soil temperature, soil moisture and electrical conductivity were measured
in parallel with each earthworm sampling using the time domain reflectometry
(TRIME®-PICO 64/32, HD2, IMKO Micromodultechnik GmbH,
Ettlingen, Germany). Soil pH was determined using a glass electrode on mixed
soil samples (Karrer, 2015).
Statistical analyses
Effects of the management type (managed vs. abandoned) were examined using
generalized linear models (GLMs). A Poisson distribution was used for plant and earthworm species
richness, and a Gaussian distribution was used for Shannon index, evenness,
total plant biomass, necromass, legumes, herbs, grasses, plant cover, plant
strategy types, erosulate, hemirosette and rosette plants, decomposition
rate and stabilization factor, earthworm density, endogeic, anecic and
epigeic earthworms, soil electrical conductivity, pH, soil moisture, and
temperature. All statistical analyses were performed in R version 3.3.1 (R
Core Team, 2016) using an α<0.05 to be considered as
statistically significant and 0.05<α<0.10 to be
considered as marginally significant. To assess differences in species
assemblages of plants and earthworms between abandoned and managed meadows,
a principal coordinate analysis (PCoA) was conducted based on a resemblance
matrix of Bray–Curtis similarity measures. PERMANOVA was computed to test
for significant differences in species assemblages between abandoned and
managed meadows. Residuals were permuted 9999 times under a reduced model.
PCoA and PERMANOVA were performed in the Primer version 6.1.13 with
PERMANOVA+ (PRIMER-E Ltd., Plymouth, UK). Potential interrelations between
the tested parameters were analysed by Pearson correlations for normally
distributed variables and Spearman correlations for not normally distributed
variables (plant cover). Normality of distributions was checked using
a Shapiro test.
Results
In total, 93 plant species were recorded in abandoned and 118 plant species
in managed meadows. Plant species richness, Shannon index and evenness were
significantly higher in managed compared to abandoned meadows (Fig. 1a–c).
Plant species cover and frequency in abandoned and managed meadows.
Species are ordered by descending cover. Values are means.
Abandoned meadows Managed meadows SpeciesCover (%)Frequency (%)SpeciesCover (%)Frequency (%)Brachypodium pinnatum (L.)31.84100Bromus erectus Huds.8.8850P. Beauv.Laserpitium latifolium L.7.5025Astrantia major major L.7.8856Galium album Mill.6.5381Festuca rubra rubra L.6.18100Astrantia major major L.4.8544Rhinanthus glacialis Personnat4.9450Festuca rubra rubra L.4.2669Sesleria caerulea (L.) Ard.4.0025Trifolium medium medium L.1.3531Betonica alopecuros L.3.1025Betonica officinalis L.1.0838Thymus pulegioides pulegioides L.3.0163Rubus caesius L.1.006Medicago falcate (L.) Scholler2.5725Aegopodium podagraria L.0.9750Prunella grandiflora (L.) Scholler2.4844Clinopodium vulgare L.0.9463Euphorbia cyparissias L.2.3825Poa angustifolia L.0.8344Potentilla erecta (L.) Raeusch.2.1963
The dominant species in abandoned meadows was the grass B. pinnatum, which occurred in
all sampling plots with a mean cover of 31.8 %, followed by the herb
Laserpitium latifolium L. (mean cover 7.5 %; Table 1). In contrast, the cover of individual species in managed meadows was more equal. B erectus (grass), which was present in
half of the plots with a mean cover of 8.9 %, was the predominant species
in managed meadows, followed by the herb A. major major and the grass F. rubra rubra with a mean cover
of 7.9 % and 6.2 %, respectively. Plant cover was similar in abandoned and managed sites (GLM, p=0.260).
Principal coordinate analysis (PCO = PCoA) of plant species
assemblages between managed and abandoned meadows.
Structure of total plant biomass in abandoned and managed meadows.
* denotes significant difference between management types (p<0.05), • marginal difference (p<0.1), n.s. no
significant difference. Values are means.
PCoA (Fig. 2) revealed a clear and significant separation of species
assemblages between abandoned and managed meadows (PERMANOVA, p=0.028).
Total plant biomass was significantly higher in abandoned compared to
managed meadows (GLM, p=0.045). Furthermore, the structure of functional
groups in the plant assemblage was influenced by management (Fig. 3).
Abandoned meadows had significantly higher necromass and marginally higher
grass biomass. Herb and legume biomass showed no management-induced
differences.
Proportion of plant strategy types (a) and proportion of types of rosettes (b) in abandoned and managed meadows. * denotes significant difference between management types (p<0.05), n.s. no significant difference. Values are means.
Among the plant strategy types, ruderal plants had a significantly higher
proportion in managed meadows. Proportions of competitors and
stress tolerators were similar between management types (Fig. 4a). In
abandoned meadows, significantly more erosulate growing and less hemirosette
plant species were found. The predominant character states of rosettes in
both management types was hemirosette (Fig. 4b). A proportion of rosette
plant species showed no significant difference.
Decomposition rate k was significantly higher in abandoned meadows compared
to managed meadows (Fig. 5a). For stabilization factor S, no significant
difference was found (Fig. 5b).
Decomposition rate k(a) and stabilization factor S(b) measured
with tea bag index in abandoned and managed meadows. * denotes significant
difference between management types (p<0.05), n.s. no significant
difference. Values are means ± SD.
In total, seven earthworm species were found in all meadows (Table 2). The
endogeic species Aporrectodea rosea Sav. and Octolasion lacteum Oerl. were most abundant
across management types, followed by the endogeic Aporrectodea caliginosa Sav. in
abandoned meadows and epigeic Lumbricus rubellus Hoffm. in managed meadows. Only one species belonged to the ecological group anecic, with two recorded individuals in managed sites. Ecological groups (anecic and epigeic) did not significantly differ between meadow types. Neither species richness (GLM, p=0.866), nor earthworm assemblages were affected by management (PERMANOVA, p=0.642). Total earthworm density and endogeic earthworm density were marginally higher in managed compared to abandoned meadows (Fig. 6a, b).
Adult earthworm species found in abandoned and managed meadows with
mean density of individuals per species in June and August. Values are means ±
SD. Results do not include juvenile species with unclear identification.
Total earthworm density (a) and density of ecological groups (b)
in abandoned and managed meadows. Anecic earthworms are shown between
endogeics and epigeics but hardly depicted. • denotes marginally
significant difference between management types (p<0.1), n.s. no
significant difference. Values are means ± SD.
Soil temperature, soil moisture, electrical conductivity (EC) and pH did not
significantly differ between management types (GLM, psoil temperature=0.858, psoil moisture=0.742, pEC=0.276, ppH=0.563).
Earthworm density showed no significant correlations with other tested
parameters (Table 3). Plant species richness decreased with increasing
necromass (p=0.019), decomposition rate increased with increasing
necromass (p=0.004) and increasing grass biomass (p=0.014).
Decomposition rate was negatively correlated with plant species richness (p=0.007). All other correlations between the measured parameters were not
statistically significant.
Correlations between earthworm density, vegetation parameters and
litter decomposition. Pearson and Spearman (only for plant
cover) correlation coefficients. Missing results: no correlation was
calculated.
Symbols after values denote significant correlations: *p<0.05; **p<0.01.
Discussion
This is one of few studies considering effects of mountain meadow management
on interactions between above- and belowground ecosystem biota and
processes. An average of 54 plant species per square metre in extensively managed
and 38 species per square metre in abandoned meadows is representative of semi-dry
grasslands of the central Ennstal (Bohner et al., 2003).
Likewise, the Shannon index and evenness were higher in managed meadows. This
confirms other findings of decreased vascular plant species numbers due to
abandonment (Fontana et al., 2014; Jacquemyn et al., 2003; Niedrist et al., 2009; Tasser and Tappeiner, 2002; Wehn et al., 2017). Disturbances in managed meadows through mowing or driving with farm machinery reduce the competitive ability of dominant plant species and create gaps for the establishment of many other
species (Jacquemyn et al., 2003). The
higher light availability in managed meadows enables many meso- and
xerophilic, light-demanding species to co-exist, resulting in a higher
species richness (Bohner et al., 2003).
Pavlů et al. (2011) argue that the
principal effect of abandonment on plant species composition is based on a
change in the abundance of some dominant species. In abandoned meadows, some
species become dominant, forcing other species to decline
(Niedrist et al., 2009). This shift of species can
also be seen in abandoned meadows in the present work with a decline of the
grass B. erectus (cover of 8.9 % in managed and 0.1 % in abandoned meadows) and
an increase of the grass B. pinnatum (cover of 1.0 % in managed and 31.8 % in abandoned meadows). Similarly, Köhler et al. (2005)
observed a negative effect of abandonment on the tufts of B. erectus, whereas B. pinnatum
increased with ongoing abandonment due to benefits via more rhizomatous
growth. Bobbink and Willems (1987) related the dominance
of B. pinnatum to its tall growth form and aboveground phytomass. Furthermore, B. pinnatum is supposed to restrict the growth of most other plant species, resulting in a decrease of plant species diversity (Bobbink et al., 1987; Bobbink and Willems, 1987).
We also observed an accumulation of necromass in abandoned meadows and
accordingly higher total plant biomass in these sites. This has also been
observed by others (Kelemen et al., 2014) and
has been shown to have negative effects on plant species richness, e.g. due
to reduced solar irradiation on the surface, hindering germination and
establishment of many plant species (Kelemen et al., 2013). Also, tall
grasses are superior competitors in meadows and can suppress the biomass of
most herbs (Del-Val and Crawley, 2005). The
germination of grasses is less hindered by litter (Xiong and
Nilsson, 1999), which makes them more resistant to cessation of management.
The decline of ruderals during succession is in line with findings by
Prévosto et al. (2011), who related the
shift in strategy types to the lack of disturbances after abandonment.
Ruderal plants have a rapid growth rate and a high annual seed production,
allowing them to establish in frequently disturbed areas. Disturbances cause
a shift in the structure of the rosette types. In the present study,
erosulate species increased and hemirosette species decreased during
succession, suggesting that rosette plants are more sensitive to
abandonment. Prévosto et al. (2011) and
Weiss and Jeltsch (2015) obtained
similar results. Due to less light availability in the lower canopy layers,
plant types with leaves near the ground are discriminated by erosulate
plants (Pavlů et al., 2011; Peco et al., 2012).
While effects of grassland management on vegetation diversity and structure
have frequently been studied, little is known on potential impacts on
belowground fauna and processes. We found a higher decomposition rate in
abandoned than in managed meadows, indicating that a thicker layer of
necromass in abandoned sites may have improved the microenvironmental
conditions for decomposition (Facelli and Pickett, 1991).
Similarly, Liu et al. (2009) and Novara et al. (2015) found
that increasing litter quantity influences soil carbon and nitrogen cycles.
Meier and Bowman (2008) showed that the
composition and diversity of chemical compounds within plant litter mixtures
have important effects on decomposition. However, the chemical qualities of
plant litter were not considered in the present study.
Additionally, Scherer-Lorenzen (2008) observed that plant species diversity has rather weak effects on decomposition, while decomposition was found to increase with higher plant functional diversity. For example, legume abundance enhances decomposition via effects on litter quality and on the decomposition microenvironment. This is also in line with Milcu et al. (2008), who highlighted legumes as very important in grassland
decomposition processes. In the present study, we found a negative impact of
plant species richness on decomposition rate, while the positive effect
between legume biomass and decomposition could not be observed. However, in
the present results a higher biomass of grasses seemed to increase the
decomposition rate. Groffman et al. (1996), who
investigated the effects of grass species on microbial biomass, suggested
that different grass species may influence the microbial activity, but to a
lesser extent than soil type, which is considered a more important
controller of microbial biomass and activity. Clearly, these comparisons
should be made with caution as different approaches to determine litter
decomposition have been used and different ecosystems were investigated.
We found a total of seven earthworm species in the studied meadows, which is a
similar species richness than reported from grasslands of lower altitudes in
Europe (Cluzeau et al., 2012; Zaller and Arnone III, 1999b). Based on a long-term field
experiment, Pop (1997) concluded that 2–4 endogeic, 0–2 anecic
and 1–2 epigeic species are to be expected in mountain woody and grassland
ecosystems, which was also observed in the present study. In the current
study, earthworm species richness and species assemblages remained
unaffected by abandonment even if abandonment lasted for 20–40 years. This
indicated negligible effects on earthworms of an extensive management
including one annual mowing without any fertilizer input. Similarly,
Decaëns et al. (1997)
observed no changes in species richness during succession of a grazed chalk
grassland over 44 years. In the present study, the most common earthworm
species in both meadow types were A. rosea and O. lacteum, followed by A. caliginosa in abandoned sites and
L. rubellus in managed sites. This is in line with the species assemblages of mountain
grassland observed by Pop (1997). In the current study, managed
meadows showed a marginally higher total earthworm density compared to
abandoned ones, which is in contrast to other findings
(Decaëns et al., 1997; Józefowska et al., 2018; Pižl, 1992). These contrasting findings let us assume that several context-specific factors
such as species characteristics of the investigated plant and earthworm
communities or ecosystem characteristics alter these ecological
interactions. Earthworm abundance may be reduced via a decrease in nutrient
supply and primary production due to changes in the floral composition
(Scheu, 1992; Zaller and Arnone III, 1999a). Density of endogeic earthworms was marginally higher in managed meadows. Similarly,
Ponge et al. (2013) found endogeic
earthworms as K-selected species to be better adapted to disturbances than
r-selected anecic species with a higher sensitivity. This may emphasize the
marginally higher density of endogeic earthworms in managed sites, which are
disturbed by mowing (Ivask et al., 2012). As soil
properties between the abandoned and managed meadows were similar, it can be
suggested that characteristics of vegetation may have caused the differences
in earthworm populations. The marginally higher earthworm density in managed
meadows may be the result of a higher plant species richness. Other studies
reveal increasing earthworm density and biomass with higher plant species
richness (Spehn et al., 2000; Zaller and Arnone III,
1999b). A loss of plant species leads to changes in community fine root
biomass and negatively affects the food supply for earthworms
(Zaller and Arnone III, 1999b). However, different earthworm
densities in managed and abandoned meadows might have also affected root
growth and aboveground plant production (Arnone III and Zaller,
2014). Furthermore, Eisenhauer et al. (2009)
found the loss of key plant functional groups to be more important than
plant species richness in shaping the structure of earthworm communities.
Indeed, specific plant traits of functional groups appear to have a
considerable influence on earthworm community (Piotrowska et al., 2013). Grasses may reduce the abundance of earthworms primarily due to their dense root system in plant communities (Eisenhauer et al., 2009; Piotrowska et al., 2013).
Considering interactions between earthworms and litter decomposition we
observed contrasting patterns, i.e. less litter decomposition in mown
meadows where more earthworms were present. Earthworms influence soil
microbial communities and this affects microbial processes of soil organic
matter and nutrient dynamics (Lavelle et al., 1998), and
earthworms are considered important drivers of decomposition
(Milcu et al., 2008; Seeber et al., 2006). Also, Lubbers et al. (2017) found earthworms to stimulate the decomposition of freshly added and
older organic material rather than stabilize carbon inside biogenic
aggregates. We explain our current contrasting findings with the method used
to measure litter decomposition. Earthworms cannot pass through the mesh of
the tea bags; thus only the potential influence of earthworms on
microorganisms and mesofauna can be measured by tea bags
(Brown, 1995; Wurst et al., 2018). Therefore, in order to identify which soil organisms affected litter decomposition in our meadows, more classical approaches to assess litter decomposition with different mesh sizes would be necessary (Hättenschwiler et al., 2005).
Conclusion
Our findings showed that an extensive management consisting of one annual
mowing without fertilization of mountain meadows significantly increased the
diversity of plant communities but did not affect the diversity of earthworm
communities compared to leaving these meadows abandoned. Extensive meadow
management also led to a reduced aboveground plant biomass production,
increased earthworm densities and reduced litter decomposition. Aside from
these contrasting effects on these parameters of supporting ecosystem
services, effects on cultural ecosystem services such as health benefits of
more diverse, extensively managed meadows have been shown (Arnberger et al., 2018). As this is one of few studies considering effects of extensive mountain meadow management on above- and belowground ecosystem interactions, more studies investigating these aspects seem imperative. Based on our study it can be recommended that a mix of abandoned and extensively managed meadows seems important in order to sustain plant and earthworm biodiversity in the study region.
Data availability
Data are available upon request (contact: Ines Jernej, ines.jernej@gmx.net).
The supplement related to this article is available online at: https://doi.org/10.5194/we-19-53-2019-supplement.
Author contributions
IJ conducted the field work and further analyses. AB
supported IJ in identifying plant species. IJ wrote the manuscript; RW and
RIH assisted IJ with the field work and gave statistical advice. Project leaders JGZ, AA and TF designed and developed the “Healthy Alps” project.
All authors reviewed the manuscript.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
We express our thanks to Johannes Karrer for providing support and the evaluation scheme. Special thanks are owed to the farmers and land owners for their permission to carry out the studies on their land.
Financial support
This research has been supported by the Austrian Academy of Sciences (project: 10470 Healthy Alps). IJ was partly funded by Verband der Naturparke Österreichs and Österreichischen Bundesforste (research fund 2018/2019).
Review statement
This paper was edited by Jutta Stadler and reviewed by two anonymous referees.
ReferencesArnberger, A., Eder, R., Allex, B., Ebenberger, M., Hutter, H.-P., Wallner,
P., Bauer, N., Zaller, J. G., and Frank, T.: Health-related effects of short
stays at mountain meadows , a river and an urban site – results from a
field experiment, Int. J. Environ. Res. Public Health, 15, 1–19,
10.3390/ijerph15122647, 2018.Arnone III, J. A. and Zaller, J. G.: Earthworm effects on native grassland
root system dynamics under natural and increased rainfall, Front. Plant
Sci., 5, 1–9, 10.3389/fpls.2014.00152, 2014.Baur, B., Cremene, C., Groza, G., Rakosy, L., Schileyko, A. A., Baur, A.,
Stoll, P., and Erhardt, A.: Effects of abandonment of subalpine hay meadows
on plant and invertebrate diversity in Transylvania, Romania, Biol.
Conserv., 132, 261–273, 10.1016/j.biocon.2006.04.018, 2006.Blouin, M., Hodson, M. E., Delgado, E. A., Baker, G., Brussaard, L., Butt,
K. R., Dai, J., Dendooven, L., Peres, G., Tondoh, J. E., Cluzeau, D., and
Brun, J. J.: A review of earthworm impact on soil function and ecosystem
services, Eur. J. Soil Sci., 64, 161–182, 10.1111/ejss.12025, 2013.Bobbink, R. and Willems, J. H.: Increasing dominance of Brachypodium
pinnatum (L.) Beauv. in chalk grassland. A Threat to a species-rich
Ecosystem, Biol. Conserv., 40, 301–314, 10.1016/0006-3207(87)90122-4, 1987.
Bobbink, R., During, H. J., Schreurs, J., Willems, J., and Zielman, R.:
Effects of Selective Clipping and Mowing Time on Species Diversity in Chalk
Grassland, Folia Geobot. Phytotx., 22, 363–376, 1987.
Bohner, A., Grims, F., Sobotik, M., and Zechner, L.: Die
Trespen-Halbtrockenrasen (Mesobrometum erecti KOch 1926) im mittleren
steirischen Ennstal (Steiermark, Österreich) – Ökologie, Soziologie
und Naturschutz, Tuexenia, 23, 199–226,
2003.Bohner, A., Starlinger, F., and Koutecky, P.: Vegetation changes in an
abandoned montane grassland, compared to changes in a habitat with
low-intensity sheep grazing – A case study in Styria, Austria, Eco. Mont.,
4, 5–12, 10.1553/eco.mont-4-2s5, 2012.
Bouché, M. B.: Stratégies lombriciennes, in: Soil
Oranism as Components of Ecosystems, Ecol. Bull., 25, 122–132, 1977.
Braun-Blanquet, J.: Pflanzensoziologie, 3rd edn., Springer-Verlag, Wien,
1964.
Brohmer, P.: Fauna von Deutschland, Ein Bestimmungsbuch unserer heimischen
Tierwelt, Quelle & Meyer, Heidelberg, 1984.
Brown, G. G.: How do earthworms affect microflora and faunal community
diversity?, Plant Soil, 170, 209–231, 1995.Christian, E. and Zicsi, A.: Ein synoptischer bestimmungsschlussel der
regenwurmer Osterreichs (Oligochaeta: Lumbricidae), Die Bodenkultur, 50,
121–131, 10.1002/anie.200805838, 1999.Cluzeau, D., Guernion, M., Chaussod, R., Martin-Laurent, F., Villenave, C.,
Cortet, J., Ruiz-Camacho, N., Pernin, C., Mateille, T., Philippot, L.,
Bellido, A., Rougé, L., Arrouays, D., Bispo, A., and Pérès, G.:
Integration of biodiversity in soil quality monitoring: Baselines for
microbial and soil fauna parameters for different land-use types, Eur. J.
Soil Biol., 49, 63–72, 10.1016/j.ejsobi.2011.11.003, 2012.
Decaëns, T., Dutoit, T., and Alard, D.: Earthworm community
characteristics during afforestation of abandoned chalk grasslands (Upper
Normandy, France), Eur. J. Soil Biol., 33, 1–11, 1997.Del-Val, E. and Crawley, M. J.: What limits herb biomass in grasslands:
Competition or herbivory?, Oecologia, 142, 202–211,
10.1007/s00442-004-1719-8, 2005.Eisenhauer, N., Milcu, A., Sabais, A. C. W., Bessler, H., Weigelt, A.,
Engels, C., and Scheu, S.: Plant community impacts on the structure of
earthworm communities depend on season and change with time, Soil Biol.
Biochem., 41, 2430–2443, 10.1016/j.soilbio.2009.09.001, 2009.
Facelli, J. M. and Pickett, T. A.: Plant litter: Itsdynamics and effects on
plant communitystructure, Bot. Rev., 57, 1–32, 1991.
Fischer, M. A., Oswald, K., and Adler, W.: Exkursionsflora für
Österreich, Lichtenstein und Südtirol, 3rd edn., Land
Oberösterreich, Biologiezentrum der Oberösterreichischen
Landesmuseen, Linz, 2008.Fontana, V., Radtke, A., Walde, J., Tasser, E., Wilhalm, T., Zerbe, S., and
Tappeiner, U.: What plant traits tell us: Consequences of land-use change of
a traditional agro-forest system on biodiversity and ecosystem service
provision, Agric. Ecosyst. Environ., 186, 44–53,
10.1016/j.agee.2014.01.006, 2014.Grime, J. P.: Evidence for the Existence of Three Primary Strategies in
Plants and Its Relevance to Ecological and Evolutionary Theory, Am. Nat.,
111, 1169–1194, 10.1086/283244, 1977.Groffman, P. M., Eagan, P., Sullivan, W. M., and Lemunyon, J. L.: Grass
species and soil type effects on microbial biomass and activity, Plant Soil,
183, 61–67, 10.1007/BF02185565, 1996.Hättenschwiler, S., Tiunov, A. V., and Scheu, S.: Biodiversity and litter
decomposition in terrestrial ecosystems, Annu. Rev. Ecol. Evol. Syst., 36,
191–218, 10.1146/annurev.ecolsys.36.112904.151932, 2005.Hejcman, M., Hejcmanová, P., Pavlů, V., and Beneš, J.: Origin and
history of grasslands in Central Europe – A review, Grass Forage Sci.,
68, 345–363, 10.1111/gfs.12066, 2013.Hooper, D. U., III, F. S. C., Ewel, J. J., Hector, A., Inchausti, P.,
Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B.,
Setälä, H., Symstad, A. J., Vandermeer, J., and Wardle, D. A.:
Effects of biodiversity on ecosystem functioning: a consensus of current
knowledge, Ecol. Monogr., 75, 3–35, 10.1890/04-0922, 2005.Hussain, R. I., Walcher, R., Brandl, D., Jernej, I., Arnberger, A., Zaller,
J. G., and Frank, T.: Influence of abandonment on syrphid assemblages in
mountainous meadows, J. Appl. Entomol., 142, 450–456,
10.1111/jen.12482, 2018.
Ivask, M., Kuu, A., Truu, M., Kutti, S., Meriste, M., and Peda, J.: Earthworm
communities in soils of Estonian wooded meadows, Balt. For., 18, 111–118,
2012.Jacquemyn, H., Brys, R., and Hermy, M.: Short-term effects of different
management regimes on the response of calcareous grassland vegetation to
increased nitrogen, Biol. Conserv., 111, 137–147,
10.1016/S0006-3207(02)00256-2, 2003.Józefowska, A., Zaleski, T., Zarzycki, J., and Frączek, K.: Do mowing
regimes affect plant and soil biological activity in the mountain meadows of
Southern Poland?, J. Mt. Sci., 15, 2409–2421,
10.1007/s11629-018-4953-y, 2018.
Karrer, J.: Abandonment of nutrient poor montane meadows: impacts on
regulating ecosystem services (decomposition, greenhouse gas efflux) and
plant diversity, University of Natural Resources and Life Sciences, Vienna,
2015.
Kelemen, A., Török, P., Valkó, O., Miglécz, T. and Tóthmérész, B.: Mechanisms shaping plant biomass and species richness: Plant strategies and litter effect in alkali and loess grasslands, J. Veg. Sci., 24, 1195–1203, doi:10.1111/jvs.12027, 2013.Kelemen, A., Török, P., Valkó, O., Deák, B., Miglécz,
T., Tóth, K., Ölvedi, T., and Tóthmérész, B.: Sustaining
recovered grasslands is not likely without proper management: vegetation
changes after cessation of mowing, Biodivers. Conserv., 23, 741–751,
10.1007/s10531-014-0631-8, 2014.Keuskamp, J. A., Dingemans, B. J. J., Lehtinen, T., Sarneel, J. M., and
Hefting, M. M.: Tea Bag Index: a novel approach to collect uniform
decomposition data across ecosystems, Methods Ecol. Evol., 4,
1070–1075, 10.1111/2041-210X.12097, 2013.
Klotz, S., Kühn, I., and Durka, W.: BIOLFLOR-Eine Datenbank zu
biologisch-ökologischen Merkmalen der Gefäßpflanzen in
Deutschland, Schriftenr. für Veg., 2002.Köhler, B., Gigon, A., Edwards, P. J., Krüsi, B., Langenauer, R.,
Lüscher, A., and Ryser, P.: Changes in the species composition and
conservation value of limestone grasslands in Northern Switzerland after 22
years of contrasting managements, Perspect. Plant Ecol. Evol. Syst., 7,
51–67, 10.1016/j.ppees.2004.11.003, 2005.
Lavelle, P.: Biology and ecology of earthworms, 3rd edn., Chapman & Hall,
UK, 1997.
Lavelle, P. and Spain, A. V.: Soil Ecology, Kluwer Academic Publisher,
Netherlands, 2001.
Lavelle, P., Pashanasi, B., Charpentier, F., Gilot, C., Rossi, J.-P.,
Derouard, L., Andre, J., Ponge, J.-F., and Bernier, N.: Large-Scale Effects
of Earthworms on Soil Organic Matter and Nutrient Dynamics, in: Earthworm
Ecology, edited by: C. A. Edwards, St. Lucie Press, 103–122, 1998.Lieskovský, J., Bezák, P., Špulerová, J., Lieskovský,
T., Koleda, P., Dobrovodská, M., Bürgi, M., and Gimmi, U.: The
abandonment of traditional agricultural landscape in Slovakia – Analysis of
extent and driving forces, J. Rural Stud., 37, 75–84,
10.1016/j.jrurstud.2014.12.007, 2015.Liu, L., King, J. S., Booker, F. L., Giardina, C. P., Lee Allen, H., and Hu,
S.: Enhanced litter input rather than changes in litter chemistry drive soil
carbon and nitrogen cycles under elevated CO2: a microcosm study, Glob.
Chang. Biol., 15, 441–453, 10.1111/j.1365-2486.2008.01747.x, 2009.Lubbers, I. M., Pulleman, M. M., and Van Groenigen, J. W.: Can earthworms
simultaneously enhance decomposition and stabilization of plant residue
carbon?, Soil Biol. Biochem., 105, 12–24,
10.1016/j.soilbio.2016.11.008, 2017.
Lundber, A., Kapfer, J., and Måren, I. E.: Reintroduced mowing can
counteract biodiversity loss in abandoned meadows, Erdkunde, 71,
127–142, 2017.MacDonald, D., Crabtree, J. R., Wiesinger, G., Dax, T., Stamou, N., Fleury,
P., Gutierrez Lazpita, J., and Gibon, A.: Agricultural abandonment in
mountain areas of Europe: Environmental consequences and policy response, J.
Environ. Manage., 59, 47–69, 10.1006/jema.1999.0335, 2000.Marini, L., Klimek, S., and Battisti, A.: Mitigating the impacts of the
decline of traditional farming on mountain landscapes and biodiversity: a
case study in the European Alps, Environ. Sci. Policy, 14, 258–267,
10.1016/j.envsci.2010.12.003, 2011.
Maurer, K.: Natural and anthropogenic determinants of biodiversity of
grasslands in the Swiss Alps, Universität Basel, 2005.Meier, C. L. and Bowman, W. D.: Links between plant litter chemistry,
species diversity, and below-ground ecosystem function, P. Natl. Acad.
Sci. USA, 105, 19780–19785, 10.1073/pnas.0805600105, 2008.Milcu, A., Partsch, S., Scherber, C., Weisser, W. W., and Scheu, S.:
Earthworms and legumes control litter decomposition in a plant diversity
gradient, Ecology, 89, 1872–1882, 10.1890/07-1377.1, 2008.Moog, D., Poschlod, P., Kahmen, S., and Schreiber, K. F.: Comparison of
species composition between different grassland management treatments after
25 years, Appl. Veg. Sci., 5, 99–106,
10.1111/j.1654-109X.2002.tb00539.x, 2002.
Mucina, L., Grabherr, G., and Ellmauer, T.: Die Pflanzengesellschaften
Österreichs. Teil I: Anthropogene Vegetation, Gustav Fischer Verlag,
Jena, 1993.Niedrist, G., Tasser, E., Lüth, C., Dalla Via, J., and Tappeiner, U.:
Plant diversity declines with recent land use changes in European Alps,
Plant Ecol., 202, 195–210, 10.1007/s11258-008-9487-x, 2009.Novara, A., Rühl, J., La Mantia, T., Gristina, L., La Bella, S., and Tuttolomondo, T.: Litter contribution to soil organic carbon in the processes of agriculture abandon, Solid Earth, 6, 425–432, 10.5194/se-6-425-2015, 2015.Pavlů, L., Pavlů, V., Gaisler, J., Hejcman, M., and Mikulka, J.:
Effect of long-term cutting versus abandonment on the vegetation of a
mountain hay meadow (Polygono-Trisetion) in Central Europe, Flora – Morphol.
Distrib. Funct. Ecol. Plants, 206, 1020–1029,
10.1016/j.flora.2011.07.008, 2011.Peco, B., Carmona, C. P., de Pablos, I., and Azcárate, F. M.: Effects of
grazing abandonment on functional and taxonomic diversity of Mediterranean
grasslands, Agric. Ecosyst. Environ., 152, 27–32,
10.1016/j.agee.2012.02.009, 2012.Piotrowska, K., Connolly, J., Finn, J., Black, A., and Bolger, T.: Evenness
and plant species identity affect earthworm diversity and community
structure in grassland soils, Soil Biol. Biochem., 57, 713–719,
10.1016/j.soilbio.2012.06.016, 2013.Pižl, V.: Succession of earthworm populations in abandoned fields, Soil
Biol. Biochem., 24, 1623–1628, 10.1016/0038-0717(92)90160-Y, 1992.Ponge, J.-F., Pérès, G., Guernion, M., Ruiz-Camacho, N., Cortet, J.,
Pernin, C., Villenave, C., Chaussod, R., Martin-Laurent, F., Bispo, A., and
Cluzeau, D.: The impact of agricultural practices on soil biota: A regional
study, Soil Biol. Biochem., 67, 271–284, 10.1016/j.soilbio.2013.08.026,
2013.
Pop, V. V: Earthworm-Vegetation-Soil Relationships in the Romanian
Carpathians, Soil Biol. Biochem., 29(, 223–229, 1997.Prévosto, B., Kuiters, L., Bernhardt-Römermann, M., Dölle, M.,
Schmidt, W., Hoffmann, M., Van Uytvanck, J., Bohner, A., Kreiner, D.,
Stadler, J., Klotz, S., and Brandl, R.: Impacts of Land Abandonment on
Vegetation: Successional Pathways in European Habitats, Folia Geobot.,
46, 303–325, 10.1007/s12224-010-9096-z, 2011.R Core Team: A language and environment for statistical computing, Version v 3.1., Vienna, Austria, available at: http://www.R-project.org (last access: 23 August 2019), 2016.
Rolecek, J., Cornej, I. I., and Tokarjuk, A. I.: Understanding the extreme
species richness of semi-dry grasslands in east-central Europe: A
comparative approach, Preslia, 86, 13–34, 2014.Scherer-Lorenzen, M.: Functional diversity affects decomposition processes
in experimental grasslands, Funct. Ecol., 22, 547–555,
10.1111/j.1365-2435.2008.01389.x, 2008.Scheu, S.: Changes in the lumbricid coenosis during secondary succession
from a wheat field to a beechwood on limestone, Soil Biol. Biochem., 24,
1641–1646, 10.1016/0038-0717(92)90163-R, 1992.Schmitzberger, I., Wrbka, T., Steurer, B., Aschenbrenner, G., Peterseil, J.,
and Zechmeister, H. G.: How farming styles influence biodiversity
maintenance in Austrian agricultural landscapes, Agric. Ecosyst. Environ.,
108, 274–290, 10.1016/j.agee.2005.02.009, 2005.Seeber, J., Scheu, S., and Meyer, E.: Effects of macro-decomposers on litter
decomposition and soil properties in alpine pastureland: A mesocosm
experiment, Appl. Soil Ecol., 34, 168–175,
10.1016/j.apsoil.2006.02.004, 2006.Spehn, E. M., Joshi, J., Schmid, B., Alphei, J., and Körner, C.: Plant
diversity effects on soil heterotrophic activity in experimental grassland
ecosystems, Plant Soil, 224, 217–230, 10.1023/A, 2000.Tasser, E. and Tappeiner, U.: Impact of land use changes on mountain
vegetation, Appl. Veg. Sci., 5, 173–184,
10.1658/1402-2001(2002)005[0173:IOLUCO]2.0.CO;2, 2002.Walcher, R., Karrer, J., Sachslehner, L., Bohner, A., Pachinger, B., Brandl,
D., Zaller, J. G., Arnberger, A., and Frank, T.: Diversity of bumblebees,
heteropteran bugs and grasshoppers maintained by both: abandonment and
extensive management of mountain meadows in three regions across the
Austrian and Swiss Alps, Landsc. Ecol., 32, 1937–1951,
10.1007/s10980-017-0556-1, 2017.Wehn, S., Taugourdeau, S., Johansen, L., and Hovstad, K. A.: Effects of
abandonment on plant diversity in semi-natural grasslands along soil and
climate gradients, J. Veg. Sci., 28, 838–847, 10.1111/jvs.12543,
2017.Weiss, L. and Jeltsch, F.: The response of simulated grassland communities
to the cessation of grazing, Ecol. Modell., 303, 1–11,
10.1016/j.ecolmodel.2015.02.002, 2015.
Wilson, J. B., Peet, R. K., Dengler, J., and Pärtel, M.: Plant species
richness: The world records, J. Veg. Sci., 23, 796–802,
10.1111/j.1654-1103.2012.01400.x, 2012.
Wurst, S., Sonnemann, I., and Zaller, J. G.: Soil Macro-Invertebrates: Their
Impact on Plants and Associated Aboveground Communities in Temperate Regions
BT – Aboveground–Belowground Community Ecology, in Aboveground-Belowground
Community Ecology, edited by: Ohgushi, T., Wurst, S., and Johnson, S. N., Springer International Publishing,
175–200, 2018.
Xiong, S. and Nilsson, C.: The effects of plant litter on vegetation: a
meta-analys, J. Ecol., 87, 984–994, 1999.
Zaller, J. G. and Arnone III, J. A.: Earthworm and soil moisture effects on
the productivity and structure of grassland communities, Soil Biol.
Biochem., 31, 517–523, 1999a.Zaller, J. G. and Arnone III, J. A.: Earthworm responses to plant species'
loss and elevated CO2 in calcareous grassland, Plant Soil, 208, 1–8, 10.1023/A:1004424720523, 1999b.
Zentralanstalt für Meteorologie und Geodynamik (ZAMG): Klimamittel –
ZAMG, 2018.