Differential impact of two dominant Formica ant species (Hymenoptera, Formicidae) on subordinates in temperate Europe

Abstract

Competition is one of the basic mechanisms shaping ant assemblages. Dominant territorial species are known to restrictively influence the traits of subordinates in various ways. However, there could be differences in the effects of dominants due to differences in their colony structure, lifestyle and also behaviour. We tested this hypothesis in natural circumstances in an area where a Formica exsecta Nyl. supercolony neighbours a strong population of the European slave-maker F. sanguinea Latr. For the purpose of our study three different sites were selected: one dominated by F. exsecta, a neighbouring site dominated by F. sanguinea, and a third site where both species co-occurred. We analyzed the structure of subordinate ant communities based on nest counts, and by recording the activity of ants at baits. Based on our findings the structure of ant communities differed significantly among the three sites. The F. exsecta site was characterized by the lowest nest density of subordinates, especially in the case of aggressive species as Lasius platythorax Seifert. At baits even the simple presence of the dominant limited the abundance and occurrence of subordinates. In contrast, no such negative effect could be revealed at the F. sanguinea site. The community of the mixed site showed intermediate features in many respects. Generally, the supercolonial F. exsecta had a bigger influence on the ant community than the slave-making F. sanguinea. On the other hand, our findings revealed a slight protective role of the territorial F. exsecta for potential slave species to F. sanguinea. The current study underlines the importance of differences between dominant ant species in shaping differentially ant communities even within the same restricted area.

Full text

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 97
Differential impact of two dominant Formica
ant species (Hymenoptera, Formicidae) on
subordinates in temperate Europe
Gema Trigos Peral1, Bálint Markó2,3, Hanna Babik1, Ioan Tăuşan4, István Maák3,
Zsóa Pál5, Piotr Ślipiński1, Zsolt Czekes2, Wojciech Czechowski1
1 Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza St 64, 00-679 Warsaw, Poland 2Hunga-
rian Department of Biology and Ecology, Babeş-Bolyai University, Clinicilor St 5–7, 400006 Cluj-Napoca,
Romania 3 Department of Ecology, University of Szeged, PO Box 51, H-6701 Szeged, Hungary 4 Department
of Environmental Sciences and Physics, Faculty of Sciences, Lucian Blaga University of Sibiu, Dr. Raţiu St 5–7,
550012 Sibiu, Romania 5 School of Environmental Sciences, Charles Stuart University, PO Box 789, NSW
2640 Albury, Australia
Corresponding author: Gema Trigos Peral (getriral@googlemail.com)
Academic editor: Jack Ne |Received 29 February 2016|Accepted 17 April 2016| Published 27 June2016
http://zoobank.org/F8E45D32-7A35-40C9-A10A-07FBD7A0B871
Citation: Trigos Peral G, Markó B, Babik H, Tăuşan I, Maák I, Pál Z, Ślipiński P, Czekes Z, Czechowski W (2016)
Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae) on subordinates in temperate
Europe. Journal of Hymenoptera Research 50: 97–116. doi: 10.3897/JHR.50.8301
Abstract
Competition is one of the basic mechanisms shaping ant assemblages. Dominant territorial species are
known to restrictively inuence the traits of subordinates in various ways. However, there could be die-
rences in the eects of dominants due to dierences in their colony structure, lifestyle and also behaviour.
We tested this hypothesis in natural circumstances in an area where a Formica exsecta Nyl. supercolony
neighbours a strong population of the European slave-maker F. sanguinea Latr. For the purpose of our
study three dierent sites were selected: one dominated by F. exsecta, a neighbouring site dominated by
F. sanguinea, and a third site where both species co-occurred. We analyzed the structure of subordinate
ant communities based on nest counts, and by recording the activity of ants at baits. Based on our nd-
ings the structure of ant communities diered signicantly among the three sites. e F. exsecta site was
characterized by the lowest nest density of subordinates, especially in the case of aggressive species as Lasius
platythorax Seifert. At baits even the simple presence of the dominant limited the abundance and occur-
rence of subordinates. In contrast, no such negative eect could be revealed at the F. sanguinea site. e
community of the mixed site showed intermediate features in many respects. Generally, the supercolonial
JHR 50: 97–116 (2016)
doi: 10.3897/JHR.50.8301
http://jhr.pensoft.net
Copyright Gema Trigos Peral et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
RESEARCH ARTICLE

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
98
F. exsecta had a bigger inuence on the ant community than the slave-making F. sanguinea. On the other
hand, our ndings revealed a slight protective role of the territorial F. exsecta for potential slave species to
F. sanguinea. e current study underlines the importance of dierences between dominant ant species in
shaping dierentially ant communities even within the same restricted area.
Keywords
Formica exsecta, Formica sanguinea, baits, community structure, competition, interspecic hierarchy, nest
density, slavery, territoriality
Introduction
Most of the concepts regarding the assembly rules of animal communities point to
competition as a crucial factor in shaping their composition and structure (MacArthur
1972, Wiens 1983, Farris et al. 2015, McFarlane Tranquilla et al. 2015, Sunarto et
al. 2015). is is supported for ants as well by several case studies (e.g. Savolainen
and Vepsäläinen 1988, Pisarski and Vepsäläinen 1989, Cerdá et al. 1998, Parr and
Gibb 2010, Czechowski et al. 2013, Maák et al. 2014, Ślipiński et al. 2014, Dejean
et al. 2015, Spotti et al. 2015) and the work reviewed quite recently by Cerdá et al.
(2013). Specically, ant communities in temperate zones are organized hierarchically
and a crucial role in shaping them can be attributed to ecologically and behaviourally
dominant species. Dominant species can restrictively structure local communities in
various ways, from interference and exploitative competition to direct predation on
lower-ranked species, both quantitatively (decreasing nest densities and colony sizes
of subordinates) and qualitatively (reducing species richness by competitive exclusion
and altering the dominance structure), but also with regards to the spatial patterns
of the nests (e.g. by forced resource partitioning, nest moving, etc.) (Higashi and
Yamauchi 1979, Cherix and Bourne 1980, Pisarski 1982, Pisarski and Vepsäläinen
1989, Savolainen and Vepsäläinen 1988, 1989, Savolainen et al. 1989, Savolainen
1990, 1991, Vepsäläinen and Savolainen 1990, Hölldobler and Wilson 1990, Punttila
et al. 1991, 1996, Sanders and Gordon 2003, Czechowski and Markó 2005, Adler et
al. 2007, Czechowski et al. 2013, Markó et al. 2013, Rzeszowski et al. 2013, Ślipiński
et al. 2014).
Typically, at least in Euro-Asian boreal and temperate zones, the top dominants of
ant communities are territorial species (sensu Pisarski 1982), i.e. those which actively
protect the boundaries of their whole foraging areas against other territorials (Pisarski
1980, Vepsäläinen and Pisarski 1982, Pisarski and Vepsäläinen 1989). In temperate
Europe, such territorial dominants, already well-known for their competitive impact
on subordinate ants, are the wood ant species of the Formica rufa group (subgenus
Formica s. str. L.) (Savolainen and Vepsäläinen 1988, 1989, Savolainen et al. 1989,
Savolainen 1990, 1991, Punttila et al. 1991, 1996, Czechowski and Markó 2005),
species of the subgenus Coptoformica Müll. (genus Formica L.) (Czechowski 1975,
Pisarski 1982, Pisarski and Vepsäläinen 1989), the dendrophilic Lasius (Dendrolasius)
fuliginosus (Latr.) (Czechowski et al. 2013, Markó et al. 2013, Ślipiński et al. 2014),

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 99
and Liometopum microcephalum (Panzer) (Petráková and Schlagamerský 2011). Colo-
nies of territorial species (either allo- or conspecic) do not share the same territory,
but non-territorial species can nest and forage within the dominant’s territory, how-
ever with diverse limitations. eir colonies are the centres of the spatial organization
in ant communities through their dierential eects on subordinate species, which are
‘allowed’ only to nest at certain distances from the nest of the territorial species – the
farther away are the nests of the subordinates, the stronger could be the competition
between the two species (Savolainen and Vepsäläinen 1988, Pisarski and Vepsäläinen
1989). e impact of territorials on subordinates may further be enhanced by specic
social strategies, such as the formation of new colonies through budding, which leads
to the development of a network of related nests over a larger area (so-called supercolo-
nies – see e.g. Helanterä et al. 2009, Robinson 2014 for reviews), a well-known strategy
in many territorial wood ants (Higashi and Yamauchi 1979, Cherix and Bourne 1980,
Rosengren et al. 1985), but also in members of the subgenus Coptoformica (Pisarski
1982, Czechowski 1975, 1977, Markó et al. 2012).
Within subordinates, two competition levels are distinguished: (a) encounter spe-
cies, which are fairly aggressive and usually manage to monopolize (defend) single food
sources, and (b) submissive species, which defend only their nests (Vepsäläinen and
Pisarski 1982). Although they can manage to survive in the territory of dominants,
subordinates are restrictively aected by territorials, and, in general, they fare bet-
ter outside than within territories of dominant species (Savolainen 1990, 1991). On
the other hand, in certain situations, nesting inside a dominant territory can even be
good for certain species. Members of the subgenus Serviformica For. (genus Formica)
are slave species for the facultative slave-maker Formica (Raptiformica) sanguinea Latr.
Potential slave colonies may prot from the proximity of strong dominants since these
can stop the raiding columns of F. sanguinea or force them to change their route when
protecting their own territory. Such a positive eect of territorials has been reported
for several species of wood ants of the F. rufa group (F. rufa L., F. polyctena Först., F.
aquilonia Yarr., F. lugubris Zett.) for F. fusca L. and F. lemani Bondr., and known slave
species F. sanguinea (Punttila et al. 1996, Czechowski 1999, 2000, Czechowski and
Vepsäläinen 2001, Czechowski and Markó 2006, Väänänen et al. 2010). A similar
mechanism may also work, at least to some extent, in the case of Serviformica species
enslaved by the obligate slave-maker Polyergus rufescens (Latr.) (Czechowski 2006).
e dierences among dominant species regarding their eect on subordinates
may vary depending on their lifestyle (slave-maker vs non-slave-maker), colony struc-
ture (mono- vs polydomous), and on their foraging strategies (narrow vs wide food
spectrum). e dierential eect of dominants on subordinates are best revealed when
dominant species occur syntopically (in the same habitat), consequently, the basic
species pool that could make up the ant community is the same. erefore, if the dif-
ferences between the dominants are negligible, the dierences between the ant com-
munities occurring in their territories/areas should also be minor. In order to test this
hypothesis, an appropriate natural set-up is needed, with the long-term co-occurrence
of territorial allospecic neighbours (see e.g. Czechowski et al. 2013). Recent eld

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
100
studies performed on the largest European polydomous system of the territorial For-
mica exsecta (Markó et al. 2012) yielded the discovery of a large population of the
slave-maker F. sanguinea, also a dominant species, neighbouring the above-mentioned
supercolony. is unique natural set-up of two dominant neighbours from the same
genus, yet with a dierent colony structure (supercoloniality vs mono- or oligodomy)
and lifestyle (non slave-maker vs slave-maker) oered the chance to perform a com-
parative study. In the framework of the current study, we proposed an analysis of the
structure of ant communities in the area of these two dominants, and formulated the
following questions: (1) are there any dierences between the structure of ant commu-
nities of the two neighbouring dominant Formica species’ territory/area, (2) are there
any dierential eects of these two dominants on the foraging strategies of subordi-
nate species, (3) do the abundance and foraging strategy of members of the subgenus
Serviformica, known as a slave species of F. sanguinea, dier within and outside the F.
sanguinea area?
Materials and methods
Study species and sites
e main subjects of the study are two dominant ant species: Formica (Coptoformica)
exsecta and Formica (Raptiformica) sanguinea.
Formica exsecta is a fairly common North-Palaearctic mound-building territorial
species, a typical forest-ecotone polytope dwelling in forest margins and clearings,
thinned young growth, overgrowing meadows and glades, etc. Its colonies number
several thousand to tens of thousands of workers and occur in two, mono- and po-
lygynous social forms. Polygynous colonies may grow through nest splitting into poly-
domous systems, often with more than 100 nests (so-called supercolonies). Addition-
ally, colonies may be established through the temporary social parasitism of members
of the subgenus Serviformica. e optimal home range of foraging workers from a
single nest does not exceed a few meters. ey are aggressive and predacious ants,
which also feed on honeydew (Pisarski 1982, Seifert 2000, Hughes 2006, Erős et al.
2009, Csata et al. 2012).
Formica sanguinea is a common South-Palaearctic species, a polytope of warm and
dry habitats, both forested and open areas; generally its ecological preferences widely
overlap with those of the former species. It nests in decaying tree stumps, partly cov-
ered with dry plant material and also in the ground, often under stones. In general,
colonies, usually functionally monogynous, number up to several tens of thousands
of workers. It is a facultative socially parasitic species which enslaves workers of the
subgenus Serviformica; the range of its slave raids may reach 100 m (usually < 50 m).
ey are very aggressive and predatory ants; during their raiding period they do not
respect the boundaries of other species’ territories (Czechowski 2000, Hughes 2006).
e territoriality of F. sanguinea is a moot point (see the Discussion).

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 101
As habitat niches of Formica exsecta and F. sanguinea overlap each other to a con-
siderable degree, colonies of these two species often co-occur.
Our study area was a vast semi-moist meadow of the Molinion caeruleae W. Koch
alliance [with, among others, Molinia caerulea (L.) Moench, Deschampsia caespitose
(L.) P. B., Festuca pratensis Huds., Nardus stricta L. and Juncus sp.], densely overgrown
with small birch saplings, located in the southern part of the Giurgeului depression
(46°36'N; 25°36'E; 780 m a.s.l.) in the eastern Carpathians, Transylvania, Romania.
e meadow is fairly intensely grazed by cows for most of the year. is is the location
of the largest known European polydomous system of Formica exsecta. e supercolo-
ny contains 3,347 permanent nests over an area of nearly 22 ha (i.e. the nest density is
ca. 153/ha) (Markó et al. 2012). A population of F. sanguinea was recently detected,
with a small number of F. cunicularia Latr. and F. rubarbis F. slaves, within the same
habitat near the area occupied by the supercolony.
ree sites were selected within the area for the purpose of our study (Fig. 1): (1)
a site clearly dominated by Formica sanguinea right at the border of the F. exsecta poly-
domous system (referred to as the F. sanguinea site; 32 F. sanguinea nests on ca. 3210
m2 with 0.01 nests/m2, and four F. exsecta nests with 0.001 nests/m2), (2) a neighbour-
ing patch within the F. exsecta territory with a single F. sanguinea nests (referred to as
the F. exsecta site; 68 nests on ca. 5780 m2 with 0.012 F. exsecta nests/m2, and one F.
sanguinea nest with 0.0002 nest/m2) and (3) a site with interspersed nests of both F.
sanguinea and F. exsecta (referred to as the mixed site; eight F. sanguinea on ca. 2685
m2 with and 0.003 nests/m2, and 80 F. exsecta nests with 0.03 nests/m2). Within the
whole study area, the meadow was homogeneous in respect of the vegetation, surface
conguration and sun exposure.
e study area was not part of any nature protection area and no specic permits
were required to carry out the eld studies.
Sampling methods
Nest densities of dierent subordinate ant species were obtained using the biocoenom-
etric method, by carefully investigating 15 quadrats of 9 m2 at each of the three study
sites. e quadrats were randomly selected by a blindfolded person in the eld, they
did not border each other, and they were at least 2 m from any Formica exsecta nest
(Fig. 1). A sample of workers was collected for precise identication from each nest
found. Identication of ant species was carried out with the key of Czechowski et al.
(2012). Field work was carried out between 17 and 21 June 2010.
Baiting is commonly used to study the foraging pattern of ants around their nests
and species’ foraging strategies. It is also an appropriate method for determining the
hierarchical positions of particular species within an assemblage (e.g. Czechowski
1979, 1985, Czechowski and Pisarski 1988, Parr and Gibb 2010, Petráková and
Schlaghamerský 2011, Markó and Czechowski 2012). As the food preferences of
ants may change seasonally, we provided a mixture of two dierent kinds of bait:

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
102
Figure 1. Map of the study area (F. exsecta nests outside the delineated sites are not marked out; grey
area – compact area of the F. exsecta supercolony).
tuna sh akes as a source of animal protein food and a water solution of mixed-
ower honey as a source of carbohydrates. Altogether, 10 observation plots were
distributed along linear transects at each of the three study sites (Fig. 1), and the
baits were put out in the centre of each plot, separated from the next plot by 2 m,
and placed at least 2 m from any Formica exsecta or F. sanguinea nest and any previ-
ously surveyed plot. e bait portions of ca. 3 cm diameter were placed in the centre
of a round green plastic plate of 10 cm diameter. Baiting observations were carried
out on 8 July 2010. Observations were carried out in two periods: between 1000 and
1200 AM, and between 520 and 720 PM. Each period consisted of six observations of

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 103
1 min, separated by 20 minute breaks. During each observation, the number and
species of ants appearing at the baits were recorded, with the exception of Myrmica
spp., where species level identication could not be performed under eld condi-
tions. e baits were put out 10 minutes before each period of observation (morning
and afternoon) and left there until the end of the period when they were retrieved
and the plates cleaned.
Data analyses
e dierences in the abundance of dierent ant species among sites were revealed by
the use of the Kruskal-Wallis test, followed by Tukey and Kramer post-hoc tests. e
diversity of ant communities was calculated with the Shannon-Wiener entropy index
(log2), using data for individual quadrats and baits respectively for nest count and
bait data, while dierences among sites for these parameters were revealed by using
the Kruskal-Wallis test, followed by the Tukey and Kramer post-hoc tests separately
for nest count and bait data. In order to determine the dierences among the ant
assemblages of the three sites, permutational multivariate ANOVA (perMANOVA,
10000 permutations) was applied both for nest count and bait data, while Nonmetric
Multidimensional Scaling (NMDS) was used to visualize the three assemblages, both
in the case of nest and bait data. e SIMPER test was performed to determine the
contribution of each species to dissimilarities between ant communities.
e Generalized Linear Mixed Model approach (GLMM, binomial, maximum
likelihood) was applied to analyze the eect of dominant species on the presence and
absence of subordinate species at baits. e abundance of Formica sanguinea and F.
exsecta workers present at baits were introduced as variables, along with their pres-
ence vs absence data as factors, next to the type of the site (F. sanguinea, F. exsecta,
mixed) as a factor. e period and time of the observation as well as bait ID were
introduced as nested random factors. A similar approach (GLMM, Poisson error,
maximum likelihood) was applied to separately test the eect of dominants on the
abundance of subordinates. e number of all subordinates was pooled together,
since they showed a low abundance separately (see the Results). e same model
structure was used as above.
All statistical analyses were carried out using the R 3.1.2 statistical package (R
Core Team 2015). Multiple pairwise comparisons in the case of the Kruskal-Wallis
tests concerning diversity indices were performed using the Tukey and Kramer post-
hoc test after Nemenyi with the PMCMR R-package (Pohlert 2015). Permutational
multivariate ANOVA, NMDS and the SIMPER test were carried out with the vegan
R-package (Oksanen et al. 2013). GLMMs were performed using the glmer function
in the lme4 R-package (Bates et al. 2014). Post-hoc Tukey-tests for sequential com-
parison among factor levels when performing GLMM were carried out with the glht
function in the multcomp R-package (Hothorn et al. 2015).

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
104
Results
Species composition and abundance
During the quadrat survey, 171 nests were found belonging to 11 subordinate ant
species in addition to the two dominant species (i.e. Formica sanguinea and F. exsecta)
(Table 1). Five subordinate species occurred at every site studied [Tetramorium cf. caes-
pitum (L.), Myrmica scabrinodis Nyl., M. vandeli Bondr., M. schencki Viereck, and
Lasius avus (F.)]. Total nest density of co-occurring ant species was 1.8 times higher
at the F. sanguinea than at the F. exsecta site, whereas it was intermediate at the mixed
site (Table 1). e most abundant subordinate species was the subterranean L. avus
followed by M. scabrinodis on every study site (Table 1).
Only three aggressive encounter species were found: Lasius platythorax, Tetramo-
rium cf. caespitum and Formica rubarbis, and none of them were present in high
densities at the site (territory) of F. exsecta. e three sites diered mainly in the nest
density of two encounter species: L. platythorax and T. cf. caespitum (Table 1). Nest
density of the former was relatively high at the F. sanguinea site, whereas the latter had
a higher density at the mixed site. Nest density of all submissive species [Myrmica spp.,
Leptothorax acervorum (F.) and Serviformica spp.] taken together was the highest at the
F. sanguinea site, owing mainly to the trends noticeable in Myrmica species (Table 1).
e ant community of the Formica sanguinea site was signicantly more diverse
than the F. exsecta site, while the mixed site had an intermediate position (Kruskal-
Wallis χ2 = 7.83, p = 0.02; Fig. 2). e structure of the ant assemblages also diered
signicantly among the three studied sites (perMANOVA F1,40 = 3.51, p = 0.006),
mostly with regards to the ant community of the F. sanguinea site, while seemingly the
communities of the other two sites were quite similar (Fig. 3). According to the results
of the SIMPER analysis, most of the dissimilarities (ca. 70%) among the three sites
could be contributed mostly to three common species: Lasius avus, Myrmica scabrino-
dis and L. platythorax, except for the F. exsecta vs mixed site, where T. cf. caespitum
took the place of L. platythorax in this respect (Table 2).
Foraging strategies and competitive eects
Besides Formica sanguinea and F. exsecta, foragers of other species were also present
at the baits (Table 3). e highest abundance of ants at baits was observed at the F.
exsecta site, exclusively due to the ecient recruitment of F. exsecta workers to the food
sources (Table 3). As expected, F. sanguinea was present at baits in its site, though in a
surprisingly low number, whereas it was totally absent from the F. exsecta site; in turn,
F. exsecta was absent in the F. sanguinea site. Both species exploited baits, though, at
the mixed site (Table 3).
Dierent trends were detected in the abundance of two aggressive (encounter) spe-
cies: Lasius platythorax and Tetramorium cf. caespitum. e former occurred in similar

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 105
Table 1. Nest densities (mean number per 9 m2 ± SD) of subordinate ant species and their proportions
(%) in the three study sites.
Species
F. sanguinea site F. exsecta site Mixed site
mean ± SD
%
mean ± SD
%
mean ± SD
%
Tetramorium cf. caespitum (L.) 0.33 ± 0.49
6.4
0.2 ± 0.56
7
0.67 ± 1.05
20
Leptothorax acervorum (F.) – 0.07 ± 0.26
2.3 –
Myrmica scabrinodis Nyl. 1.13 ± 1.13
21.8
0.53 ± 0.92
18.6
0.73 ± 1.1
22
Myrmica vandeli Bondr. 0.47 ± 0.99
9.0
0.47 ± 0.74
16.3
0.13 ± 0.35
4.0
Myrmica schencki Viereck 0.27 ± 0.8
5.1
0.07 ± 0.26
2.3
0.13 ± 0.35
4
Myrmica lobicornis Nyl. – 0.13 ± 0.35
4.7
0.07 ± 0.26
2
Myrmica ruginodis Nyl. 0.07 ± 0.26
1.3 – –
Lasius avus (F.) 2.00 ± 1.81
38.5
1.33 ± 1.54
46.5
1.40 ± 0.99
42
Lasius platythorax Seifert 0.87 ± 0.74
16.7
0.07 ± 0.26
2.3 –
Formica cunicularia Latr. 0.07 ± 0.26
1.3 –0.13 ± 0.35
4
Formica rubarbis F. – – 0.07 ± 0.26
2
All subordinate species 5.21 2.87 3.33
All epigean subordinate species 3.21 1.54 1.93
Table 2. Results of the SIMPER analysis: the overall dissimilarity between study sites, the average contri-
bution of subordinated ant species to overall dissimilarity (Dissimilarity contribution), their mean abun-
dances in the compared sites (Mean 1 and Mean 2), and the cumulative percentages of contributions.
Sites (dissimilarity) Species Dissimilarity
contribution (%) Mean 1 Mean 2 Cumulative
contribution (%)
F. sanguinea vs. F.exsecta
(70.13)
L. avus 20.95 2 1.54 29.88
M. scabrinodis 13.49 1.13 0.62 49.13
L. platythorax 12.27 0.87 0.08 66.63
M. vandeli 9.44 0.47 0.54 80.11
T. cf. caespitum 6.13 0.33 0.23 88.85
F. sanguinea vs. Mixed
(67.83)
L. avus 18.83 2 1.5 27.76
M. scabrinodis 13.11 1.13 0.78 47.1
L. platythorax 12.21 0.87 0 65.11
T. cf. caespitum 9.33 0.33 0.71 78.88
M. vandeli 6.18 0.47 0.14 88
F. exsecta vs. Mixed
(65.81)
L. avus 20.35 1.54 1.5 30.92
M. scabrinodis 14.38 0.62 0.79 52.79
T. cf. caespitum 11.16 0.23 0.71 69.75
M. vandeli 8.48 0.54 0.14 82.64
M. schencki 3.46 0.08 0.14 87.91

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
106
Table 3. Mean number of ant individuals per baits (± SD) for each study site and their relative propor-
tions (%) to other ant species at the same site.
Species
F. sanguinea site F. exsecta site Mixed site
mean ± SD
%
mean ± SD
%
mean ± SD
%
Tetramorium cf. caespitum 31.6 ± 96.78
36.5 –10.6 ± 21.49
32.0
Myrmica spp. 2.1 ± 3.96
2.4
0.2 ± 0.42
0.1
4.0 ± 3.83
12.1
Lasius platythorax 52.2 ± 83.48
60.3
52.2 ± 120.86
29.6 –
Formica cunicularia 0.6 ± 1.9
0.7
3.4 ± 4.03
1.9
1.8 ± 3.16
5.4
Formica sanguinea 0.1 ± 0.32
0.1 –1.9 ± 2.56
5.7
Formica exsecta –120.4 ± 100.65
68.3
14.8 ± 35.67
44.7
All subordinate species 86.5 ± 111.43 55.8 ± 121.5 16.5 ± 22.75
99.9 31.6 49.7
All species 86.6 ± 111.35 176.6 ± 102.94 33.2 ± 36.19
100 100 100
Figure 2. Diversity of the ant communities within the study sites based on nest surveys (medians, quartiles,
min–max values and outliers). Survey performed on 9 m2 quadrats (N = 15 in each site). Dierent letters
indicate signicant dierences among groups.

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 107
Figure 3. NMDS graph of the ant communities within the study sites based on nest survey (stress = 0.172).
numbers at baits in the Formica exsecta and F. sanguinea sites, whereas it was absent
from the mixed site (Table 3). In turn, Tetramorium cf. caespitum was absent from the
F. exsecta site, while it was the second most abundant ant in the two other sites (Table
3). e abundance of potential F. sanguinea slave species, such as F. cunicularia, gradu-
ally increased from the F. sanguinea site to the mixed one and then to the F. exsecta
site (Table 3).
e highest diversity was found at baits in the mixed site (Kruskal-Wallis χ2 =
9.11, p = 0.011) followed by the signicantly lower diversities of Formica sanguinea
and F. exsecta sites, which did not dier signicantly from each other based on the
post-hoc test result (Fig. 4). ere were no dierences between the three sites in the
qualitative-quantitative composition of foraging ants (perMANOVA F1,29 = 1.83, p =
0.12), however, baits in the F. exsecta territory seemed to stand apart from all other
sites due to the marked presence of F. exsecta, while the presence of subordinate species
was more characteristic for the F. sanguinea and the mixed sites (Fig. 5).
According to the results of the GLMM analysis, Formica exsecta’s abundance (z =
–3.09, p = 0.002) and presence (z = –2.32, p = 0.02) had a signicant negative eect
on the occurrence of subordinates at baits, while the abundance of F. sanguinea did
not play a major role (z = –1.72, p = 0.08), but its presence did have a positive inu-
ence on the occurrence of subordinates (z = 2.13, p = 0.033). ere were no dierences

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
108
between the F. sanguinea and the F. exsecta sites with regards to the frequency of the
occurrence of subordinates (z = 1.99, p = 0.11). Also, no dierence was found between
the F. sanguinea and the mixed site in this respect (z = –1.8, p = 0.16), but subordinates
were signicantly less frequent at baits in the mixed site compared to the F. exsecta site
(z = –3.18, p = 0.004).
Generally, a similar pattern with smaller adjustments was found when analyzing
the eect of dominants on the abundance of subordinates at baits. In addition to the
abundance of Formica exsecta (z = –8.33, p < 0.0001), even its simple presence (z =
–2.01, p = 0.044) had a signicant negative eect on the abundance of subordinates.
On the other hand, F. sanguinea’s abundance (z = 0.04, p = 0.96) and presence (z =
0.96, p = 0.33) had no signicant eect. e abundance of subordinates also showed
signicant dierences among the three study sites (z ≥ 9.92, p < 0.0001).
Discussion
e main factors which shape biodiversity and structure of animal communities are,
besides habitat heterogeneity (see e.g. MacArthur and MacArthur 1961, Hölldobler
Figure 4. Diversity of the ant communities within the study sites based on bait observations (medians,
quartiles, min–max values and outliers). Dierent letters indicate signicant dierences among groups.

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 109
and Wilson 1990, Tews et al. 2004, Ossola et al. 2015), intra- and interspecic rela-
tionships, such as competition and social parasitism. e importance of the latter is
well known in ants (Savolainen and Vepsäläinen 1988, Hölldobler and Wilson 1990,
Andersen 1992, Ryti and Case 1992, Cerdá et al. 1997, Czechowski and Markó 2006,
Scharf et al. 2011, Ślipiński et al. 2011, 2014). Colonies of dominant species, espe-
cially territorial ones, play a crucial role, as organizing centres of the ant community, by
limiting the establishment of colonies of subordinate species within dominant territo-
ries or by managing their accessibility to various resources (Savolainen and Vepsäläinen
1988, Pisarski and Vepsäläinen 1989, Andersen 1992, Bestelmeyer 2000, Lester et al.
2010, Cerdá et al. 2012, 2013, Czechowski et al. 2013). In our study, we revealed con-
siderable dierences among ant communities living in areas within the same habitat,
but dominated by two dominant species with clearly dierent features.
e species composition of the studied ant communities was quite similar among
all three sites, but dierences were found in the abundance of dierent ant species,
and also in the diversity of ant communities. In almost all respects the Formica san-
guinea site was superior housing the most diverse ant community. us, despite the
low chance of interaction with Lasius avus due to its subterranean lifestyle, the lowest
density of L. avus nests was recorded in the Formica exsecta territory, which could be
Figure 5. NMDS graph of the ant communities within the study sites based on bait observations (stress
= 0.114).

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
110
the result of the establishment of F. exsecta colonies on the top of their soil mounds,
with the gradual extermination of L. avus colonies (Pisarski 1982). is species was
followed by Myrmica spp. with a low level of aggression compared to L. platythorax
and Tetramorium cf. caespitum, while the lowest abundance was recorded for members
of the subgenus Serviformica, being both a slave species to F. sanguinea and the host of
temporary social parasitism caused by F. exsecta fundatrices (Czechowski et al. 2012).
Generally speaking, there was an increase in the abundance of aggressive and submis-
sive species in the mixed territory where F. exsecta and the slave maker species showed
lower abundance or were absent.
Usually, the exploitation patterns of food resources at the Formica exsecta site was
in agreement with the general rules concerning hierarchy patterns, where the dominant
species, especially a territorial one, monopolizes the area and its resources (Savolainen
and Vepsäläinen 1988, Savolainen et al. 1989). In the F. exsecta site the absence of T. cf.
caespitum at baits, known as an aggressive species (e.g. Brian et al. 1966, 1979) with a
quick reaction towards intruders (Dobrzański and Dobrzańska 1975) and with the abil-
ity to exploit habitat resources eectively (Brian et al. 1966), might have been caused by
its general avoidance of the dominant species during foraging (see Cerdá et al. 2012). On
the other hand, contrary to Formica exsecta, as other authors have already shown before
(e.g. Czechowski 1999, 2000, Czechowski and Markó 2006, Ślipiński et al. 2011), F.
sanguinea behaved as a considerably weaker competitor, exploiting the baits much less
actively than e.g. Lasius platythorax and Tetramorium cf. caespitum, which succeeded in
exploiting the baits within its area quite heavily. e strongest dierence in the exploita-
tion pattern of baits is shown by the results obtained from the mixed territory, where the
presence of almost all species at baits increased, with the exception of Formica exsecta,
which exhibited the highest frequency and abundance in its own exclusive territory.
e low number ofFormica sanguineaforagers at baits, especially in relation to
the numbers of workers of other ant species, requires additional explanations. Recent
studies on the foraging strategy ofF. sanguineahave already shown, that this species
seems to be less competitive towards subordinates to the south (e.g. Romania) than in
the northern parts of the species range in Europe (e.g. Finland) (P. Ślipiński et al., in
prep). One of the major signs of its weaker competitiveness is its reduced presence at
articialbaits, as also conrmed by our present observations. However, it is possible
that at least some of the F. cunicularia workers present at baits were individuals en-
slaved byF. sanguinea,and these de facto acted as foragers of the latter. Since,generally,
slaves fulll intranest tasks in colonies (Kharkiv 1979a,b, see also Czechowski 1996),
the abundance of slaves foraging at baits could anyhow be quite low.
Territorial ants can hold o raiding columns of Formica sanguinea to some extent,
and in this way directly protect possible slave species against their enslaver. is pro-
tective eect would manifest itself when there was a signicantly greater abundance
of slave species within, rather than outside of wood ant territories of the F. rufa group
(Punttila et al. 1996, Czechowski 2000, Czechowski and Vepsäläinen 2001, Czechows-
ki and Markó 2006, Väänänen et al. 2010). However, this is not generally valid for all
territorials, since, e.g., no measurable protective eect of the territorial Lasius fuliginosus

Dierential impact of two dominant Formica ant species (Hymenoptera, Formicidae)... 111
towards the F. fusca slave species was detected by Ślipiński et al (2014), despite cases of
direct interference of the latter during F. sanguinea raids (Czechowski 1999, 2000). In
our study area, two potential slave ant species (and, at the same time, potential hosts of
the temporary social parasitism of F. exsecta) occurred, both members of the subgenus
Serviformica: F. cunicularia and F. rubarbis. e former is a typical submissive species,
the latter is an aggressive encounter species. Due to this, the relations of each of them
with both local dominant species, i.e. F. exsecta and F. sanguinea, might proceed dier-
ently. On one hand, the submissive, weakly competitive F. cunicularia should be less
restrictively treated by the territorial F. exsecta than the more competitive F. rubarbis.
On the other hand, colonies of the aggressive F. rubarbis (see Mori et al. 2001) should
be much less prone to being destroyed by F. sanguinea, and they should also be more re-
sistant to being taken over by young F. exsecta queens than colonies of the submissive F.
cunicularia. So, one could expect that these dierences in behaviour might be reected
in dierences in the distribution of the two subordinate species. However, both species
were very scarce in the study area. In total, only three nests of F. cunicularia and one
nest of F. rubarbis were found. At the baits, only F. cunicularia foragers occurred, most
abundantly within the F. exsecta site. At the remaining sites (both with F. sanguinea),
they were generally scarce, and what is more, at least some of them may have been F.
sanguinea slaves. is result may suggest some type of protective eect of the territorial
F. exsecta on this slave species against the slave-maker.
While the decisive eect of Formica exsecta as a typically territorial species on the
structure of ant communities is quite evident, this question still remains open regard-
ing F. sanguinea. In the literature, the latter is commonly handled in a similar manner
as the territorial Formica s. str. and Coptoformica species (Vepsäläinen and Pisarski
1982, Savolainen et al. 1989, Punttila et al. 1996, Czechowski 2000, Czechowski and
Markó 2006, Väänänen et al. 2010). However, our ndings seem to contradict the
similarly strong territorial (sensu Pisarski 1982) nature of F. sanguinea. e fact that
some F. sanguinea nests can occur in the vicinity of F. exsecta nests (see the mixed site)
also emphasizes the reduced territoriality of F. exsecta. Other eld observations point
in this direction as well. For example, in the Białowieża Forest (N-E Poland), a very
strong F. sanguinea colony was observed to peacefully coexist with a fairly large F. ex-
secta colony over several years, nesting just ca. 3 m from an edge of the mound of the
latter (W. Czechowski, unpubl.). Also, the above mentioned recent case study on the
competitive strategy of F. sanguinea (P. Ślipiński et al., in prep.) strongly suggests the
non-territoriality of this aggressive and undoubtedly inuential species.
e results of this study underscore the importance of dierences between dominant
ant species in dierentially shaping ant communities, even within the same limited area.
Acknowledgements
We are indebted for the Apáthy István Society for the housing during the eld works.
e study was carried out with the support of scientic cooperation between the Polish

Gema Trigos Peral et al. / Journal of Hymenoptera Research 50: 97–116 (2016)
112
Academy of Sciences and the Romanian Academy. is work was supported by a grant
of the Romanian National Authority for Scientic Research and Innovation, CNCS –
UEFISCDI, project number PN-II-RU-TE-2014-4-1930.
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