Acta Soc. Zool. Bohem. 74: 153–160, 2010
ISSN 1211-376X
Effects of secondary succession in abandoned grassland on the activity of
ground-foraging ant assemblages (Hymenoptera: Formicidae)
Michal WIEZIK1*), Adela WIEZIKOVÁ2) & Marek SVITOK2)
1) Department
of Applied Ecology, Faculty of Ecology and Environmental Science, Technical University in Zvolen,
T. G. Masaryka 24, SK–960 53 Zvolen, Slovakia
2) Department of Biology and General Ecology, Faculty of Ecology and Environmental Science,
Technical University in Zvolen, T. G. Masaryka 24, SK–960 53 Zvolen, Slovakia
*) corresponding author: [email protected]; [email protected]
Received 26 August 2009; accepted 1 December 2010
Published 20 December 2010
Abstract. The results of an assessment of the structural variations in ant assemblages in abandoned grasslands
in low-intensity farming areas of the Štiavnické Vrchy Mts and Strážovské Vrchy Mts in Central Slovakia, are
presented. In the Štiavnické Vrchy Mts. ant assemblages of managed and abandoned wet and mesic grasslands in the
initial stage of secondary succession were compared. Both species richness and epigaeic activity of ants increased
as a consequence of abandonment. The trend was independent of habitat moisture; however, this did affect species
composition. In the region of Strážovské Vrchy ant assemblages in mesic grasslands were assessed in a set of four
overgrown grasslands. An initial increase in the activity and species richness following abandonment was recorded
but after shrub cover exceeded 10% there was a distinct decrease in both these characteristics. If preservation of
ant diversity at these sites is important then they have to managed by keeping the shrub cover around 10% and
rehabilitating the ant assemblages in the initial stages of the succession.
Key words. Soil zoology, ecology, abandoned grasslands, secondary succession, management, Hymenoptera,
Formicidae, Slovakia, Carpathians.
INTRODUCTION
Cultivated grasslands are particularly sensitive to land-use change (Morris 2000). This is also the
case for grassland habitats, which have been abandoned as a consequence of the decline in agriculture in central Europe during the last two decades. After being abandoned, grasslands usually
undergo strong and relatively rapid succession. During the course of succession grassland becomes
overgrown with woody plants, which occurs in several stages. The final stage is usually a dense
forest. These changes have profound effects on plant and animal communities, including that of
soil arthropods. Ants are an important component of temperate grassland arthropod communities;
they are considered to be keystone species (Platner 2004) and ecosystem engineers (Folgarait
1998). However, there are surprisingly few studies on temperate grassland ant communities (e.g.
Gallé 1991, Dauber & Wolters 2005, Dahms et al. 2005) and no studies of secondary succession
of ant communities in the majority of European countries, including Slovakia. Thus, the aim of
this study was to examine the effect of secondary succession on grassland ant communities in
selected Slovak low-intensity farming areas. The effect grassland abandonment and subsequent
secondary succession has on ant (Hymenoptera: Formicidae) assemblages was studied. To achieve
this objective, the composition, species richness and epigaeic activity of ants, at managed and
Presented at the 10th Central European Workshop on Soil Zoology, České Budějovice, Czech Republic, 21–24 April 2009.
153
recently abandoned wet and mesic sites and at four distinct stages of colonization by shrubs,
were compared.
MATERIAL AND METHODS
This study was carried out on a set of managed and abandoned grasslands in the Štiavnické Vrchy and Strážovské Vrchy
Mts (Central Slovakia) (Fig. 1). Both regions have similar mean annual temperature and annual precipitation, being 7.6 °C
and 895 mm in the Štiavnické Vrchy (Hlavaček 1985) and 7–8 °C and 700–1000 mm in the Strážovské Vrchy Mts. The
geology and soils in the two regions are of volcanic and sedimentary origin, respectively. Rich brown soils overlaying
andesite bedrock and rendzina soils overlaying carbonates are most frequent (Lukniš 1972, Konečný 1998).
Twenty grassland plots representing managed and recently abandoned temperate grassland with wet and mesic soil
conditions in the Štiavnické Vrchy Mts were selected. In order to assess the effect of progressive overgrowing by shrubs
on ant assemblages another 12 grassland plots in the Stražovské Vrchy Mts were selected. These plots represent 4 different stages of successional overgrowing, defined by the proportion of woody species: managed grassland (A) without
woody species, recently abandoned grassland (B) with 0–10% shrubs, moderately overgrown grassland (C) with 30–50%
and heavily overgrown grassland (D) with >50% cover of woody species. All plots were situated on SE, S or SW facing
slopes, except the wet grassland plots that were situated on river terraces with no obvious slope.
In each plot a line of 10 traps, spaced at 3 m intervals, was established. The traps consisted of plastic cups (diameter
3 cm) buried level with the soil surface and filled with about 50 ml of 4% solution of formaldehyde. Each trap was left in
place for 7 days before being set in order to reduce digging-in effects (Greenslade 1973). In total, 320 traps were placed
in the field during late May 2008 and each trap remained open for a week. Sampling was repeated in late September 2008.
Workers of ants were identified to species level using the keys of Czechowski et al. (2002) and Seifert (2007).
Total species richness and epigaeic activity (pooled across two sample dates) were analysed using a hierarchical
ANOVA design. A mixed model that included the fixed effects of management (managed, abandoned), habitat moisture
(wet, mesic), their interaction and the random effects of plot, nested within interaction was fitted to the data from the
Štiavnické vrchy Mts. Furthermore, separate analyses were performed on richness and activity of two dominant functional
groups: opportunistic (Op) and cold climate specialists (CC) (sensu Andersen 2000). A model testing the fixed effect of
successional overgrowing (stages A, B, C, D) and random effect of plot was fitted to the data from the Strážovské vrchy
Mts. For significant effects, the relevant pair-wise comparisons were done using Tukey’s HSD tests. Prior to statistical
analysis, data were screened in diagnostic plots and logarithmically transformed when necessary. However, untransformed
data is presented in the figures to facilitate viewing and interpretation.
Fig. 1. Location of the study areas in the Štiavnické vrchy (right) and Strážovské vrchy Mountains (left) in Slovakia.
154
Table 1. Total activity of epigaeic ants of the family Formicidae and presence of species at replicated sites (upper index).
Habitat type based on cover of woody species: A – without woody species, B – 0–10%, C – 30–50%, D – >50% cover of
woody species. Type of management: m – managed, a – abandoned
habitat type
management
n
Myrmicinae
Myrmica gallienii Bondroit, 1920
Myrmica lobicornis Nylander, 1846
Myrmica lonae (Finzi, 1926)
Myrmica rubra (Linnaeus, 1758)
Myrmica ruginodis (Nylander, 1846)
Myrmica rugulosa Nylander, 1849
Myrmica sabuleti Meinert, 1861
Myrmica scabrinodis Nylander, 1846
Myrmica schencki Viereck, 1903
Myrmecina graminicola (Latreille, 1802)
Solenopsis fugax (Latreille, 1798)
Leptothorax acervorum (Fabricius, 1793)
Temnothorax interruptus (Schenck, 1852)
Tetramorium caespitum (Linnaeus, 1758)
Tetramorium impurum (Förster, 1850)
Dolichoderinae
Tapinoma ambiguum Emery, 1925
Tapinoma erraticum (Latreille, 1798)
Formicinae
Lasius flavus (Fabricius, 1782)
Lasius alienus (Förster, 1850)
Lasius niger (Linnaeus, 1758)
Lasius psammophilus Seifert, 1992
Camponotus ligniperdus (Latreille, 1802)
Formica cunicularia Latreille, 1798
Formica fusca (Linnaeus, 1758)
Formica pratensis Retzius, 1783
Formica rufa Linnaeus, 1761
Formica rufibarbis Fabricius, 1793
Formica sanguinea Latreille, 1798
total activity
species richness
Štiavnické vrchy
wet
mesic
m
a
m
a
5
5
5
5
A
m
3
Strážovské vrchy
B
C
a
a
3
3
D
a
3
31
–
–
2003
–
41
–
32
32
–
–
–
–
21
–
–
–
–
3385
–
21
–
1034
112
–
–
41
–
413
–
21
–
–
122
–
–
161
1184
–
–
42
–
–
32
11
–
51
–
–
–
–
533
24895
214
–
–
–
–
144
–
–
21
11
52
–
–
261
531
42
11
–
–
11
–
–
–
53
–
21
21
–
–
2043
62
–
–
–
–
71
–
71
31
–
–
61
–
32
2132
11
–
–
–
–
31
–
–
–
–
21
21
–
33
32
11
–
–
–
–
32
–
–
–
–
21
–
41
61
42
–
–
–
–
–
61
21
22
33
102
2285
81
–
33
–
–
–
42
–
224
–
4375
–
–
714
–
2012
51
22
–
21
1263
1934
202
–
83
–
4783
–
75
–
22
923
61
72
–
154
–
3474
–
43
11
–
21
1182
211
–
42
11
–
1901
92
–
11
11
593
191
22
–
–
933
–
11
1411
–
–
–
–
–
11
–
22
11
–
351
–
11
412
–
–
–
–
–
–
–
–
471
12
1239
13
994
15
3066
15
438
15
543
14
281
12
60
10
The same models were fitted to a community data matrix using distance-based MANOVA (Anderson 2001). The
analyses were based on Bray-Curtis distance (Bray & Curtis 1957). Species activities were log transformed to reduce
asymmetrical influence of the dominant species. P values were based on 9999 permutations of raw data using correct
permutable units (Anderson & ter Braak 2003). Non-metric multidimensional scaling (nMDS; Kruskal 1964) was used to
visualise differences in assemblage composition. Relationships between species and nMDS configuration were examined
using Spearman rank correlation.
RESULTS
A total of 5,770 ant workers of the family Formicidae belonging to 22 species were collected
in the Štiavnické Vrchy Mts, and 1,322 ant workers belonging to 24 species in the Strážovské
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Fig. 2. Differences in total activity of epigaeic ants and species richness of ants and selected functional groups at managed
and abandoned grassland sites. The column plots give the mean values ± SE. The ANOVA results are displayed.
Fig. 3. Results of nMDS analysis based on Bray-Curtis distance showing dissimilarity of ant assemblages in hygro- and
mesophilous habitats (left). Spearman correlation coefficients of species activities with nMDS configuration are presented
(right). Only species with a high correlation (r>0.4) are displayed.
156
Fig. 4. Column plots showing mean species richness (left) and activity of epigeic (right) ant assemblages (±SE) in different successional stages of grassland in the Strážovské vrchy Mts. Columns with the same lower case letters are not
significantly different (Tukey’s HSD test, p<0.05). For explanation of habitat types see Table 1.
Vrchy Mts (Table 1). The five most common species accounted for 87.2% of the total number of
ant workers: Myrmica scabrinodis Nylander, 1846, Lasius niger (Linnaeus, 1758) and Formica
pratensis Retzius, 1783 were dominant in both regions, Myrmica rubra (Linnaeus, 1758) and
Lasius alienus (Förster, 1850) were only recorded frequently in the Štiavnické vrchy Mts.
Fig. 5: Results of nMDS analysis based on Bray-Curtis distance showing dissimilarity of ant assemblages in the different successional stages of mesic grassland in the Strážovské Vrchy Mts. Notes: Grassland successional stages: managed
grassland (A) without woody species, recently abandoned grassland (B) with 0–10 % shrubs, moderately overgrown
grassland (C) with 30–50 %, and heavily overgrown grassland (D) with >50 % cover of woody species.
157
Management had a significant effect on total epigaeic activity and total species richness of
ants in the grasslands in the Štiavnické Vrchy Mts (Fig. 2). Recently abandoned grassland sites
were more species rich and the epigaeic activity of ants there was greater than in annually managed grasslands. This trend was even more pronounced for the Opportunist functional group,
which had a six times higher average activity and two times higher average species richness at
abandoned sites. Neither of these characteristics was significantly affected by moisture. Habitat
moisture, however, was shown to affect species composition (pseudo-F(1,16)=4.92; p<0.001). Wet
and mesic habitat plots tended to occur in different portions of the ordination space, suggesting
that the composition of ant assemblages in these grasslands differed (Fig. 3). Wet habitats were
characterized by an increased proportion of Lasius niger and Myrmica rubra – eurytopic species
that are moisture tolerant. Mesic habitats had higher proportions of Myrmica scabrinodis, Myrmica
sabuleti Meinert, 1861, Formica pratensis and two species of the Lasius alienus-group, all of
which belong among poly- and oligotopic species, which have a low moisture tolerance.
An increase in epigaeic activity and species richness of ants in the early stages of succession,
although not statistically significant, was also observed in mesic grasslands in the Strážovské Vrchy
Mts. However, at moderately and heavily overgrown sites, with shrub cover exceeding 10% of the
surface, a distinct decrease in epigaeic activity and species richness was recorded (Fig. 4). Within
the set of mesic grasslands, no significant differences in species composition between individual
overgrowing stages was recorded (pseudo-F(3,8) =1.56; p=0.069) (Fig. 5).
DISCUSSION
The results suggest that management and habitat moisture determine the ant assemblages in temperate grasslands specifically and independently. Management in general is considered one of the
main disturbance factors, i.e. the removal of biomass (Andersen 2000). Management practices
(in this case mainly mowing in combination with late summer grazing) have an adverse effect on
activity and species richness of ants, although management does not directly alter the composition of particular ant assemblages. When compared to early stages of succession of abandoned
grassland, managed plots host less abundant and less diverse ant assemblages. These results
further corroborate conclusions from several studies, which report that extensive management of
grassland has positive effects on biodiversity and insect abundance (Bignal & McCracken 1996,
Konvička et al. 2005, Krištín et al. 2005).
The Opportunist functional group proved to be especially sensitive to lack of management.
Species belonging to this group tend to benefit from disturbance (Gallé 1991, King et al. 1998,
Andersen 2000). In warmer regions, disturbance together with environmental stress enable the
Opportunist group to occupy habitats usually controlled by behaviourally dominant groups, such
as Dominant Dolichoderinae or Generalized Myrmicinae (Andersen 2000). In the temperate
zone, these groups are limited by a relatively cold macroclimate (Kunca et al. 2008) and hence
their competitive limitation of the Opportunist group is decreased. As a consequence, in such a
low-competition environment the Opportunist group might be able to prosper in habitats where
there is a low level of management-induced disturbance.
Indirect management-related disturbance is associated with the removal of plant biomass. Cutting the vegetation may reduce the numbers and diversity of invertebrates, as it causes a reduction
in food and shelter, and alters the microclimate (Morris 2000). Depending on intensity and scale,
such disturbance may vicariously increase environmental stress (Andersen 2000, Konvička et al.
2005). In temperate grasslands, ants as generally thermophilic organisms (Hölldobler & Willson
1990) have to adapt to relatively dense and tall vegetation, which due to shading of the soil surface,
158
acts as an important stress factor. After cutting, the vegetation is uniformly shortened to a few
centimeters, rapidly transforming formerly shaded conditions into extremely exposed, dry and hot
microclimate (Morris 2000). The negative effect of such a sudden alteration in the microclimate
on ants is reported for crops of perennial Lucerne (Medicago sativa) (Wieziková 2008).
Grasslands are widely accepted as being ecological systems in a state of dynamic equilibrium
in which secondary succession is kept in check mainly by management (Morris 2000). Although
management may have adverse effects on animal communities, it maintains typical grassland
structure and increases the productivity and quality of grassland. As most of the European
grasslands are semi-natural ecosystems (Morris 2000) or plagioclimax vegetation (Duffey et al.
1974), maintenance by human management is crucial for their long-tem existence. Unmanaged
grasslands usually revert to communities functionally and ecologically distinct from grassland
within several decades (Kunca et al. 2008), mainly as a consequence of colonization by shrubs.
Ants are particularly sensitive to the overgrowing of grassland, mainly because shading by shrubs
increases environmental stress (sensu Andersen 2000). Of the early stages in the succession of
grassland into forest, the stage when compact shrubs dominate is especially ant-poor (Goméz et
al. 2003). On the other hand, individual solitary trees and shrubs may have a positive effect on
ant communities, as they create an environment qualitatively and functionally different from the
open grassland habitat, which is preferred by several specialized ant species (Reyes-Lopéz et al.
2003). The results indicate that the adverse effects of shrubs colonizing and shading grassland on
ant assemblages occurred first when more than 10% of the grassland was covered with shrubs.
In such moderately and heavily overgrown grassland, ants no longer benefit from the absence
of management, as observed in the early stages of succession and species richness and activity
decreases as a consequence of increased environmental stress. In order to sustain a high diversity
of ant assemblages it is crucial to prevent an excessive overgrowing of grassland and ecourage the
regeneration of ants by disturbance. Such management consists of perpetuating a dynamic system
of short and tall vegetation through spatial variation in natural succession and selective management
(Morris 2000). Rotational management is recommended for the maintenance of grassland-scrub
mosaics (Ward 1990), which according to the results presented is the best compromise in terms
of human exploitation of grassland and conservation benefits of low intensity farming.
Acknowledgements
The study was funded by research grant no. 1/0557/10 of the Slovak Grant Agency for Science (VEGA) and institutional
grant no. I-09-003-00. We would like to acknowledge Martin Dovčiak for editing the English and Lenka Králiková for
assistance with the field work.
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