ISSN 0013-8738, Entomological Review, 2015, Vol. 95, No. 3, pp. 370–387. © Pleiades Publishing, Inc., 2015. Original Russian Text © S.V. Stukalyuk, 2015, published in Entomologicheskoe Obozrenie, 2015, Vol. 94, No. 1, pp. 67–89.
Structure of the Ant Assemblages (Hymenoptera, Formicidae) in the Broad-Leaved Forests of Kiev S. V. Stukalyuk Institute for Evolutionary Ecology, National Academy of Sciences of Ukraine, Kiev, Ukraine e-mail:
[email protected] Received January 28, 2014
Abstract—In 2012–2013, six parks and urban forests in Kiev with a different level of anthropogenic load were investigated. Twenty-six species of ants from three subfamilies were found in the studied localities with oak (Quercus robur) forests and parks. The ant assemblages are classified into three types according to the number of dominants and their territoriality: (a) mono- and bidominant continuums of associations with weakly territorial dominants Lasius emarginatus and L. fuliginosus, having the highest population densities, and the “behavioral” dominant Camponotus ligniperdus; (b) monodominant associations with a territorial dominant (species of the Formica rufa group); (c) degraded associations in the parks where the dominants are absent and are substituted by the influents Lasius niger and Myrmica rubra. Continuums of associations with weakly territorial dominants have a more developed structure as compared with a monodominant association with the territorial dominant F. rufa producing considerable pressure on the subordinate species. Dominants, subdominants, and influents manifest different types of foraging strategy. A dominant and a subdominant can interchange individual foraging strategy and mobilization; in influents, the strategy remains constant. When the mobilization strategy is used by an influent, only the number of the mobilized workers can be modified, especially in the association without a dominant. Thus, dominants and subdominants have a more flexible foraging strategy due not only to the environmental conditions, but also to the more tight interrelations between the species. With the growth of anthropogenic load the territorial dominant F. rufa increases its pressure upon the subordinate ant species, reducing the intensity of mobilization of their workers to bait. Ant assemblages in the broad-leaved forests of Kiev consist of five chorological complexes, where the leading and layer-connecting role is played by the climbing herpetobiont Lasius emarginatus and the multilayer species F. rufa and L. fuliginosus. Degradation of the associations leads to the disappearance of the species of the two above complexes, disconnection of the layers, and, following the impoverishment of the association structure, weakening and disappearance of hierarchical links. As compared with other cities studied, Kiev has less anthropogenically disturbed ant assemblages with distinct hierarchical structure where the typical forest species F. rufa, L. fuliginosus, L. emarginatus, and C. ligniperdus may act as dominants. Preservation of ant assemblages in Kiev is ensured by the forests and parks present within the city. DOI: 10.1134/S0013873815030094
The multi-species ant associations are used as indicators of the state of the environment (Kaspari and Majer, 2000; Andersen et al., 2002; Ribas et al., 2012). The ant complexes were recently studied in the urban territories of Warsaw (Czechowski and Slipinski, 2008; Slipinski et al., 2012), Helsinki (Vepsäläinen et al., 2008), Sofia (Antonova and Penev, 2006), San Francisco (Clarke et al., 2008), New York (Pećarević et al., 2010), São Paulo (Angilletta et al., 2007), Tokyo (Yamaguchi, 2004), and other large cities. A number of similar studies were performed in the Russian Federation (Sorokina, 1998; Bugrova, 2001; Volkova, 2009; Zryanina, 2009; Omelchenko et al., 2010).
In Ukraine and its largest city Kiev (843 km2) such research has not been performed before. Since Kiev differs from other large European cities in the species composition of ants and, consequently, the structure of their multi-species associations, the study of this problem is of considerable interest. Vegetation covers a large part (55%) of the city area of Kiev, 44% being occupied by forests (Didukh and Alioshkina, 2012). Correspondingly, one may expect a higher species richness of ants in Kiev as compared with other large cities, since ant complexes in urban ecosystems stem from the associations of the natural biotopes around the city (Antonov, 2008). Considerable areas of coniferous, mixed, and broad-leaved forests surrounding
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Kiev and fragmentarily occurring in its territory may serve as refugia for many ant species, including rare ones. Ant complexes of broad-leaved forests with participation of the English oak Quercus robur are convenient study objects which allow one to carry out comparative analysis of different localities. The broadleaved forests of the study region belong to the class Querco-Fagetea Braun-Blanquet et Vlieger in Vlieger, 1937 (Alioshkina, 2011). Having assessed the structure of ant complexes of broad-leaved forests and plantings with oak, we can characterize the organization of multi-species ant associations in the green zone of Kiev as a whole, with the exception of mixed forests and also pine forests and plantations. The goal of the present research was to study the structure of ant complexes and estimate their state in broad-leaved forests and plantings within the boundaries of Kiev. We set ourselves the following tasks: (a) to reveal the species composition of ants in broadleaved forests in the territory of Kiev; (b) to determine the types of multi-species associations in this territory; (c) to study the hierarchical structure of ant complexes; (d) to compare the foraging strategies of ant species of different hierarchical ranks in broad-leaved forest areas and forest plantings with different degrees of anthropogenic transformation; e) to assess the distribution of ant species over the chorological complexes in different types of multi-species associations. MATERIALS AND METHODS Research was carried out in the June and July of 2012–2013, in the territory of six parks and recreational forests of Kiev: the Svyatoshino forest, the Feofaniya and Syretsky Gai landscape memorials, the Lysa Hora area, and also the Peremoha (Victory) and Partizanskaya Slava parks (Fig. 1). The areas of Lysa Hora and Feofaniya are characterized by the lowest level of anthropogenic disturbance. Feofaniya is protected by the Ukrainian law, whereas Lysa Hora had the status of a restricted military area till the middle of the 1980s, which was conducive to the better preservation of its nature. The nature of Syretsky Gai is more anthropogenically disturbed than that of Feofaniya or Lysa Hora: uncontrolled recreation there leads to tramping down and ruderalization of the grass layer while the tree species are preserved. Most (up to 70%) of the territory of Feofaniya, Lysa Hora, and Syretsky Gai is covered with oak-hornbeam ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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and oak-hornbeam-maple forests of natural origin. Peremoha and Partizanskaya Slava parks are fully open to visitors and intensive recreation. The oak occurs there as plantings, the grass cover is strongly degraded, and the soil is compacted. To assess the species composition, hierarchical relations, the size of foraging areas, and the density and arrangement of nests of different ant species, we used an original “attracting tape” method (Ivanov and Stukalyuk, 2003). The attracting tape (AT) was a linen ribbon 5 cm wide and 10 m long, marked into 50-cm segments and permeated with 20% sugar solution. After a 30-min exposure of the AT in the test site, we determined the number of ants of different species, the nature of their interactions, the direction of their movement from the nest, and the position of worker parties of different species. These parameters were used to calculate the number of workers and worker parties for each ant colony. Based on the mean number of workers from one party attracted to the AT and the mean number of such parties per colony, it was possible to determine which foraging strategy is more characteristic of the given species: individual or mobilization one. We follow the classification of foraging strategies used by Dlussky (1981) and Beckers and co-authors (1989), which includes the two above strategies. The simplified description of the mobilization types is due to the fact that the different types of mobilization cannot be reliably differentiated by the worker parties recorded on the AT; no relevant method has so far been developed. The species with expressed mobilization typically have a small (1–2) number of parties and a greater (from 3 to several tens) number of workers from one colony. In species with solitary foraging, foragers may appear on the AT in many (up to 8–10) points but there is rarely more than one worker in each point. In such species as Formica rufa Linnaeus, 1761, single workers from adjoining elementary search areas (ESA, according to Zakharov, 1991) may interact. Whether the workers or parties on the AT belonged to the same or different colonies could be easily determined by their behavior, either aggressive or loyal. Altogether, we used 71 AT in the study territory: 20 in Feofaniya, 21 in Lysa Hora, 12 in the Svyatoshino forest, and 6 in Syretsky Gai and each of the two parks. Such a number of AT was sufficient for the parks with their uniform plant associations and small areas as compared to the forests. Altogether, 602 ant colonies were recorded on the AT.
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The species composition was determined by route collections and AT observations. The species richness was determined by counts in plots measuring 10 × 10 m (Zakharov and Sablin-Yavorsky, 1998), with not less than 3 counts made for each type of ant associations. Since workers of the genera Myrmica and Temnothorax are difficult to identify to species under the field conditions, we present generalized parameters for the several species from each of these genera inhabiting the given biotope (Myrmica spp., Temnothorax spp.). The associations studied by us included only one dominant species Lasius fuliginosus (Latreille, 1798) which preferred protein baits and practically did not start mobilization to carbohydrate bait; thus, its role in the multi-species association could not be adequately assessed by the method used. In 2013 we determined the dynamic density of the dominants Lasius fuliginosus, L. emarginatus (Olivier, 1792), and Formica rufa Linnaeus, 1761. Counts were performed on 53 plots measuring 0.5 × 0.5 m, and subsequently they were carried out on the same plots but with carbohydrate and protein baits (for method, see Czhechowski et al., 2013) for the foraging territories of 5 colonies of L. fuliginosus, 2 colonies of F. rufa, and 14 colonies of L. emarginatus in the oak-maple-hornbeam forest of Feofaniya. The dynamic density surveys were carried out for 2 min each with three replications, during three days. The following parameters of dynamic density of workers on the foraging territory (FT) were calculated: the mean total number of workers of each species during 2 min of survey, the mean number of workers on the foraging trails, the mean number of workers in the central part of the FT, and that on the periphery of FT. The dynamic density parameters of F. rufa were calculated only for single colonies but not for the nonfederated complex. Data on the dynamic density and on the number of workers attracted to bait are presented as the mean values for the general sample, rather than for one colony. The hierarchical rank of each ant species was determined by several characters: advantage in fights, the presence of a defended area and the complexity of the foraging territory, the colony size, and the possibility of co-occurrence of species. We distinguished the following hierarchical ranks: dominant (territorial or weakly territorial); subdominants of the 1st and 2nd order; influents of the 1st, 2nd, and 3rd order. Subdivision of the dominant rank into subcategories was pre-
viously used in our earlier work carried out in the Mountainous Crimea (Stukalyuk and Radchenko, 2010). We consider such a subdivision to be justified since the dominants in the ant associations studied may be represented both by species with aggressive behavior but small colonies, such as Camponotus ligniperdus (Latreille, 1802), and by species with large colonies: F. rufa, L. emarginatus, L. fuliginosus. Of them, C. ligniperdus may be regarded as a behavioral dominant (Davidson, 1998; Segev and Ziv, 2012), whereas the other species are numerical dominants in the classification of the cited authors. All the dominant species except F. rufa were placed in the “weakly territorial” group in our classification, since they could co-occur on the same AT. By contrast, F. rufa was never recorded simultaneously with other dominant species, and was therefore regarded as a territorial dominant. Camponotus ligniperdus was considered separately, as a weakly territorial behavioral dominant. Lasius emarginatus and L. fuliginosus were regarded as weakly territorial dominants according to the number of workers in their colonies. Such classification reflects better the dominant properties of these species and, consequently, the structural peculiarities of multi-species ant associations as a whole. The tables contain the mean values of parameters (the number of workers and parties mobilized from one colony) significant at p < 0.05. RESULTS The Species Composition We found 26 ant species belonging to three subfamilies in the territory of broad-leaved forests and plantations with participation of oak in Kiev (Table 1). Of the species shown in Table 1, the geobionts were placed in a separate category. Due to their cryptic mode of life, geobionts have weak connections with the rest of the species in ant complexes. Some subdominant species can change their rank and become dominants under favorable conditions. For instance, the subdominant F. cinerea can switch from monocalic to polycalic settlements at the primary federation level (Zakharov, 1991); yet in the biotopes studied by us it had only monocalic colonies. Federations of F. cinerea are characteristic of pine forests and also of intrazonal forests in the Dnieper floodland. Among the dominants, F. rufa and L. emarginatus were more common, whereas other dominant species were recorded in less than 20% of the samples. As can ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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Table 1. The species composition of ants in the studied forest and woodland park localities of Kiev Species Camponotus fallax (Nylander, 1856) C. ligniperdus (Latreille, 1802) C. vagus (Scopoli, 1763) Dolichoderus quadripunctatus (Linnaeus, 1771) Formica cunicularia Latreille, 1798 F. cinerea Mayr, 1853 F. fusca Linnaeus, 1758 F. polyctena Förster, 1850 F. rufa Linnaeus, 1761 F. pratensis Retzius, 1783 Lasius brunneus (Latreille, 1798) L. emarginatus (Olivier, 1792) L. flavus (Fabricius, 1782) L. fuliginosus (Latreille, 1798) L. niger (Linnaeus, 1758) Lasius platythorax Seifert, 1991 L. umbratus (Nylander, 1846) Leptothorax muscorum (Nylander, 1846) Myrmica rubra (Linnaeus, 1758) M. ruginodis Nylander, 1846 M. scabrinodis Nylander, 1846 M. sabuleti Meinert, 1861 Solenopsis fugax (Latreille, 1798) Temnothorax crassispinus (Karavaiev, 1926) T. tuberum (Fabricius, 1775) Tetramorium caespitum (Linnaeus, 1758) Total number of species in locality Mean number of species per sample plot
Groups
Localities studied
1
2
3
4
5
6
7
8
1b 1a 1b 1c
S BD BD S
– – – –
– – – –
– – – –
– – – +
+ – + +
+ + + +
1c 1c 1c 1b 1b 1b 1c 1c 1c 1c 1c 1c 1c 1c 1c 1c 1c 1b 1b 1c
S S, STD I STD STD STD S WTD G WTD I I G I I I I I G I
– – – – – – – – – – + – – – + – – – – +
+ – – – – – – – – – + – – – + + – – – +
+ + + + + – – – + + + + – – + + – – – +
+ – + – – – + + – + + – + + + + + – – +
+ + + – + + + + + + + + + + + + + + + +
+ + + – – + + + + + + + + + + + + + + +
1c 1c – –
I I – –
– + 4
– + 6
– + 13
+ + 15
+ + 24
+ + 24
2.0 ± 0.3 2.6 ± 0.4 3.8 ± 0.2 4.0 ± 0.6 5.1 ± 0.3
7.3 ± 0.2
1, ecological valence: 1a, stenotopic; 1b, oligotopic; 1c, eurytopic, according to Antonov, 2008; 2, hierarchical status: I, influent; G, geobiont (with a cryptic mode of life and no expressed hierarchical relations with other species); S, subdominant; BD, weakly territorial behavioral dominant; WTD, weakly territorial dominant (by the number of workers in colonies); STD, territorial dominant; 3–8, localities studied: 3, Peremoha Park; 4, Partizanskaya Slava Park; 5, Svyatoshino Forest; 6, Syretsky Gai; 7, Feofaniya; 8, Lysa Hora.
be seen from Table 1, the species composition of ants is the poorest in parks and the richest in Feofaniya and Lysa Hora which still have some forest patches little disturbed by anthropogenic activity. In parks, 3–4 times less ant species per sample plot were recorded than in Feofaniya or Lysa Hora. In the total number of ant species the parks were 4–6 times inferior to Feofaniya and Lysa Hora. ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
In classifying the species of the studied ant complexes by their ecological valence (according to Antonov, 2008), a clear predominance of eurytopic species (18) over oligotopic ones (7) was revealed, and only one stenotopic species C. ligniperdus was found. Five of the eurytopic species occurred in all the ant complexes studied: Lasius niger, Myrmica rubra, M. ruginodis, Temnothorax crassispinus, and Tetra-
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Table 2. The mean number of workers per party mobilized to FT and the mean number of parties per colony for the subdominant Formica cunicularia Latr. and the influent species Ant species
Type of association
Locality
Plant community
I
X
x
none
4
1.2 ± 0.1
2.5 ± 0.3
Formica cunicularia Latr.
1
Lysa Hora
Lasius niger (L.)
3
Syretsky Gai Oak-hornbeam forests with ruderal herbaceous vegetation
none
7
13.4 ± 2.3
1.6 ± 0.4
4
Peremoha Park
Oak plantings
none
11
35.6 ± 8.1
2.0 ± 0.3
Partizanskaya Oak plantings Slava Park
none
6
6.9 ± 1.2
1.5 ± 0.5
1
Lysa Hora
none
14
1.7 ± 0.2
6.0 ± 0.6
2
Svyatoshino
none
8
2.1 ± 0.2
4.1 ± 0.9
1
Lysa Hora
Hornbeam-oak, none oak-maple, and oak-maple-hornbeam forests
98
7.7 ± 0.7
1.9 ± 0.1
2
Svyatoshino
Oak-hornbeam and oak-pine forests
none
43
6.9 ± 0.9
1.7 ± 0.1
2
Feofaniya
Oak-hornbeam forests with prevalence of ruderal herbaceous vegetation
with F. rufa at the forest edge
13
4.9 ± 1.0
1.5 ± 0.2
with F. rufa under forest canopy
15
3.2 ± 0.5
1.3 ± 0.1
Oak-hornbeam forests with prevalence of ruderal herbaceous vegetation
with L. emarginatus at the forest edge
14
7.1 ± 0.7
1.5 ± 0.2
with L. emarginatus under forest canopy
56
6.8 ± 0.5
2.1 ± 0.1
6.7 ± 0.9
2.1 ± 0.2
Formica fusca L. Myrmica spp.
3
Feofaniya
Hornbeam-oak forest
Type of relative position
Hornbeam-oak forest
without dominants Syretsky Gai Oak-hornbeam forests with prevalence of ruderal herbaceous vegetation
without dominants
22
7.1 ± 0.8
1.5 ± 0.1
4
Peremoha Park
without dominants
19
13.7 ± 1.7
2.0 ± 0.1
4
Partizanskaya Slava Park
without dominants
28
4.3 ± 0.3
2.2 ± 0.1
Oak plantings
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Table 2 (Contd.) Ant species
Type of association
Temnothorax spp.
1
Lysa Hora
2
Svyatoshino
2
Feofaniya
3
3
4
Locality
Plant community Hornbeam-oak, oak-maple, and oakmaple-hornbeam forests Oak-hornbeam and oak-pine forests Oak-hornbeam forests with prevalence of ruderal herbaceous vegetation
Type of relative position
I
X
x
without dominants
106
5.4 ± 0.4
1.1 ± 0.03
without dominants with F. rufa in the forest with L. emarginatu s in the forest none
41
2.8 ± 0.2
1.0 ± 0.02
2
1.3 ± 0.3
1.0 ± 0.01
33
2.4 ± 0.2
1.0 ± 0.01
9
3.1 ± 0.5
1.0 ± 0.01
5
2.4 ± 0.2
1.0 ± 0.01
Syretsky Gai Oak-hornbeam forests with prevalence of ruderal herbaceous vegetation Partizanskaya Oak and pine plantings none Slava Park
Types of associations: 1, bidominant with weakly territorial dominants (L. emarginatus and L. fuliginosus, C. ligniperdus); 2, monodominant with a territorial dominant (F. rufa); 3, monodominant with a weakly territorial dominant (L. emarginatus); 4, without expressed hierarchy. I, number of ant colonies of this category; X, mean number of workers per party; x, mean number of parties per colony.
morium caespitum. Thus, ant complexes in the territory of Kiev mainly consisted of widespread eurytopic species in the rank of influents. Some forest species (usually dominants and subdominants) were reduced in abundance while some disappeared from the complexes. Types of Multi-Species Ant Associations and Their Characteristics The following characteristics of each type of ant associations will be considered below: (a) the number of dominant species or the total number of ant species per sample site (a 10 × 10-m plot) for each type of associations; (b) the specific traits of foraging strategy (if there are any) of the same species in different biotopes; (c) the most species-rich ecological group (in terms of the preferred layers for nesting and foraging). The characteristic feature of ant associations in the territory of Kiev was the presence of the dominant species Lasius emarginatus. This dominant actively competing with L. fuliginosus considerably changed the structure of associations by complicating the interactions between the species. We have distinguished two main types of ant associations in the territory of Kiev: monodominant with ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
a territorial dominant (F. rufa) and monodominant with a weakly territorial dominant (usually L. emarginatus). The territorial dominant F. rufa or F. polyctena occupied the most productive areas of the biotope and was the main consumer of its resources. Bidominant associations with weakly territorial dominants occurred within the same biotope as monodominant ones with a weakly territorial dominant; therefore, in subsequent analysis we consider them jointly. For instance, the hornbeam-oak-maple forest of Lysa Hora revealed associations both with one (L. emarginatus) and two (L. emarginatus and L. fuliginosus or L. emarginatus and C. ligniperdus) weakly territorial dominants. Lasius emarginatus occurred in most of the samples in the absence of F. rufa; it visited and controlled the greater fraction of trees than other dominants. Thus, this species was the main component of the dominant group. The dominant C. ligniperdus occurred rarely and, as a rule, in the same association as L. emarginatus, without forming separate associations. The most degraded park associations in which the interspecific interaction was practically absent are considered separately below.
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Table 3. The mean number of workers per party mobilized to FT and the mean number of parties per colony for the territorial and weakly territorial dominants Ant species Formica rufa L.
Lasius emarginatus (Ol.)
Type of association
Locality
Type of relative position
Plant community
I
X
x
2
Feofaniya
Oak-hornbeam forests none with ruderal herbaceous vegetation
8
8.1 ± 1.0
10.6 ± 0.7
2
Svyatoshino
Oak-hornbeam and oakpine forests
none
9
2.9 ± 0.2
8.5 ± 0.9
1
Lysa Hora
Oak-birch-maple forest
in areas with C. ligniperdus
3
3.8 ± 0.8
2.3 ± 0.3
3
Oak-hornbeam and oak- without maple-hornbeam forests C. ligniperdus
15
4.3 ± 0.6
4.2 ± 0.9
1
Oak-maple forest
2
7.8 ± 1.7
3.0 ± 0.5
in areas with L. fuliginosus
3
Feofaniya
Oak-hornbeam forests in areas with ruderal herbaceous without F. rufa vegetation
7
14.5 ± 2.8
4.1 ± 0.8
3
Syretsky Gai
Oak-hornbeam forests none with ruderal herbaceous vegetation
4
7.9 ± 1.6
2.5 ± 0.5
Types of associations: 1, bidominant with weakly territorial dominants (Lasius emarginatus and L. fuliginosus, C. ligniperdus); 2, monodominant with a territorial dominant (F. rufa); 3, monodominant with a weakly territorial dominant (L. emarginatus). I, number of ant colonies of this category; X, mean number of workers per party; x, mean number of parties per colony.
1. Monodominant associations with a territorial dominant. They were characterized by: (a) territoriality of the only obligate dominant; (b) the possibility of subdominants dropping out of the hierarchy; (c) stability of foraging strategy; (d) prevalence of herpetobionts and practically complete absence of dendrobionts (dominants and subdominants) due to the influence of the multilayer territorial dominant. Each type of associations is considered in detail below. 1a. Territoriality of the obligate dominant may considerably reduce the abundance of other ant species. Associations of this type had 4–5 ant species at one site, other species with a high hierarchical status being either absent or present at the periphery. The dominant F. rufa formed non-federated complexes in the oakhornbeam forests of Feofaniya. In the oak-pine and oak-hornbeam forests of Svyatoshino with a single dominant (F. rufa, seldom L. fuliginosus), a distinct hierarchy of the subordinate species was preserved. 1b. Subdominants may drop out of the hierarchy. This was most typical of the oak-hornbeam forests of Feofaniya with the dominance of F. rufa, in which degradation processes had commenced (including the
appearance of ruderal herbaceous vegetation represented by the invasive species Impatiens parviflora). Formica rufa existed there on the verge of its requirements, which resulted in an almost complete disappearance of influents. This was expressed in the reduced number of the workers of influent species attracted to bait (Table 2), shifting of the zones of their high dynamic density to the road edges where the presence of the dominant was minimal, and also in the absence of the weakly territorial dendrobiont dominant L. emarginatus within the foraging territory of F. rufa. As compared with the population parameters in Svyatoshino, the parties of F. rufa in the forests of Feofaniya included more workers (Table 3), which ensured faster coordination of the actions of foragers at the finding of prey. Such a strategy of the dominant agrees with the data of Zakharov and Sablin-Yavorsky (1998), according to which a decrease in biodiversity in the multi-species associations may be compensated for by expansion of the foraging and nesting zones, and also by the general increase in abundance of the multilayer species, to which F. rufa also belongs. In the Svyatoshino forest, F. rufa constituted 12–40% of ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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Figs. 1–6. The localities studied in Kiev: (1–4) the right bank of the Dnieper: (1) Syretsky Gai; (2) Svyatoshino forest; (3) Lysa Hora; (4) Feofaniya. (5, 6) the left bank of the Dnieper: (5) Peremoha Park; (6) Partizanskaya Slava Park.
all the ants attracted to baits, whereas in Feofaniya its fraction was as great as 92–96%. In our opinion, this difference in abundance is related to the fact that only single nests of F. rufa were recorded in Svyatoshino, whereas in Feofaniya there were also non-federated complexes, implying larger colonies and a greater density of nests in the territory and workers on FT. The presence of the influent F. fusca in Svyatoshino may be accounted for by richer food resources as compared with Feofaniya, since the former is less disturbed by human activities. 1c. The foraging strategies of the ant species included in the association remained stable. The dominant F. rufa with the secondary subdivision of the territory mobilized small (several workers) but numerous parties to the bait (Table 3) from the adjoining ESA. The influent F. fusca (if present) foraged only singly. In the presence of the territorial dominant, the influents Myrmica spp. in Svyatoshino forest preserved mobilization, and so did the influents Temnothorax spp. (Table 2). The parameters of Temnothorax spp. were reduced as compared with those in the bidominant associations of Lysa Hora. It is possible that some workers of Temnothorax spp. moved into the litter layer to reduce ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
competition with Myrmica spp. The parameters of Temnothorax spp. were the lowest in the forests of Feofaniya. There the pressure of the dominant F. rufa was the most expressed, which was also indirectly manifested in the lower parameters of Myrmica spp. (Table 2). 1d. With the exception of the multilayer dominant, herpetobionts prevailed among the biological morphs. These associations typically included one multilayer dominant species, from 2 to 5 herpetobions, and 1 dendrobiont (Lasius brunneus). The parameters of the subordinate species in these associations were inversely proportional to the activity of the multilayer dominant. 2. Monodominant and bidominant associations with weakly territorial dominants. Associations of the hornbeam-oak, oak-maple, oak-maple-hornbeam, and oak-birch-maple forests of Lysa Hora and Feofaniya were the richest in species and the most complicated in structure. 2A. Bidominant associations with weakly territorial dominants. Associations of this type were characterized by the following features: (a) the presence of several, usually two dominant species in one sample (on one AT); (b) the constant fractions of workers of one dominant species and one influent species at-
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tracted to bait; (c) the possibility of changes in the type of foraging strategy or mobilization intensity in some high-rank species, caused by their interactions with other dominants; (d) the prevalence of dendrobionts by the number of species. 2Aa. Due to the absence of the obligate territorial dominant F. rufa, several weakly territorial dominants, usually dendrobionts, may be present simultaneously. Such associations also included 2 or 3 subdominants and influents, so that up to 8 or 9 species co-occured at one site. The dominants were usually representatives of the genera Camponotus (C. ligniperdus, C. vagus) or Lasius (L. emarginatus, L. fuliginosus). 2Ab. The number of workers of one of the dominants and an influent attracted to bait remained a constant. For example, associations of the hornbeam-oak, oak-maple, and oak-maple-hornbeam forests of Lysa Hora and Syretsky Gai were characterized by a constant fraction of workers of the dominant L. emarginatus (11–13% of all the ants attracted to bait). In the presence of the co-dominant C. ligniperdus, the fraction of L. emarginatus doubled and reached 28%, which was also reflected in the change of the foraging strategy type (see below). The same regularity held for influents of the genus Myrmica (41–61%, this fraction being the same as in the oak-maple-birch forest where there was one more co-dominant, C. ligniperdus). 2Ac. The type of foraging activity of some ant species, first of all, high-rank ones, may change depending on the composition of the association. For example, L. emarginatus could change its foraging strategy type in the presence of species of the genus Camponotus. In the oak-birch-maple forest, the weakly territorial dominant L. emarginatus did not suffer much pressure from the co-dominant C. ligniperdus, the average number of its workers attracted to bait from one colony remaining approximately the same (Table 3). At the same time, the average number of worker parties was somewhat changed. In all probability, L. emarginatus switched from solitary foraging to mobilization when in the presence of C. ligniperdus many workers concentrated in parties on the periphery of the forage plot. In the oak-maple forest, in the presence of the dominant L. fuliginosus, the mean number of workers of the dominant L. emarginatus increased; its foragers formed large parties on bait (Table 2), which may be a situational way of opposing L. fuliginosus.
Thus, comparison of the behavior of L. emarginatus in the presence of the dominants C. ligniperdus and L. fuliginosus revealed a trend for increasing the mean number of workers in the party, when other dominants appeared in the territory or when their dynamic density increased. According to our observations, the dominants L. emarginatus and L. fuliginosus never co-occurred on the forage trees if their FTs overlapped in the surface layer. If the trees were positioned not far apart, parties of workers of both species were usually present at the boundary of their territories; conflicts occurred rather rarely, mainly in spring. A similar situation was also observed in the case of adjoining territories of L. fuliginosus and F. rufa; however, conflicts were not characteristic of these species, either (Czechowski et al., 2013). The subdominants preferred to settle close to the FTs of the dominants but not within them, whereas the colonies of influents might be also located inside the dominants’ territories, experiencing minimal pressure on the part of the latter. In such cases the interaction between subdominants and weakly territorial dominants was shifted onto the periphery of the latter’s FT. Lasius fuliginosus had the highest dynamic densities of workers in all the parts of the FT and the highest intensity of movement along forage trails (Table 4). We did not measure the parameters of F. rufa within the non-federated nest complex; therefore, data for F. rufa in Table 4 refer only to single small colonies, which are not to be compared with the complex that includes millions of individuals and naturally has the highest parameters as compared with other, weakly territorial dominant species. As can be seen from Table 4, the parameters of movement along forage trails and the dynamic density of workers of L. emarginatus were only twice as small as those of L. fuliginosus. Taking into account the absence of dominants below L. emarginatus in the hierarchy, it can be supposed that such values were the lower limit for effective use of the defended FT in weakly territorial dominants. This threshold would be higher for territorial dominants. The dominant L. fuliginosus visited protein baits more often than carbohydrate ones (Table 5) and got mobilized to carbohydrate baits less frequently than other dominants. As can be seen from Table 5, the influents Myrmica spp. and L. niger mobilized approximately the ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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Table 4. Dynamic density of workers of dominant species in FT Species Formica rufa L.
Lasius fuliginosus (Latr.)
Lasius emarginatus (Ol.)
Parameters
I
Number of workers / 2 min
1 2 3 4 1 2 3 4 1 2 3 4
21 3 4 14 55 5 23 27 76 6 4 66
26.6 ± 9.9 129.6 ± 17.0 30.5 ± 4.3 3.5 ± 0.7 36.2 ± 5.5 139.8 ± 18.4 44.0 ± 4.3 10.2 ± 1.0 10.7 ± 2.1 67.5 ± 5.4 23.5 ± 1.3 4.8 ± 0.5
1, total number of workers for the given species; 2, number of workers on foraging trails; 3, number of workers in the central part of the FT; 4, number of workers in the peripheral parts of the FT; I, number of measurements in sample plots 0.5 × 0.5 m.
Table 5. Attractivity of carbohydrate and protein baits for the dominant and influent ant species Species Formica rufa L. Lasius fuliginosus (Latr.) Lasius emarginatus (Ol.) Myrmica spp. Lasius niger (L.)
Type of bait
I
Number of workers on bait
C P C P C P C P C P
5 11 24 31 30 29 16 13 5 8
2.8 ± 1.5 6.4 ± 2.2 2.8 ± 0.3 67.0 ± 7.4 6.6 ± 1.4 14.2 ± 3.0 8.8 ± 2.4 5.8 ± 1.8 10.0 ± 3.9 13.8 ± 4.4
C, carbohydrate baits; P, protein baits; I, number of measurements in sample plots 0.5 × 0.5 m.
same number of workers to carbohydrate and protein baits. The dominants could occupy nearly all the baits presented within their FTs. The presence of protein baits is an obligatory condition for assessing the role of L. fuliginosus in the association. The mobilization parameters of Myrmica spp. remained unchanged within the FT of L. fuliginosus. They were reduced only in the territory of the nest complexes of F. rufa (Table 2), which also testified to its highest territoriality among the dominants. The co-dominant C. ligniperdus foraged singly, rarely in groups of 2 or 3 workers, although large colonies established forage trails leading to the stable food resources, such as aphid colonies. ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
The solitary foraging subdominant F. cunicularia (Table 2) was characteristic of sparse forest areas with the crown density up to 50–60%. In shaded areas (the crown density up to 85–90%), the influent F. fusca was also characterized by solitary foraging but it had a greater number of parties (represented in this case by solitary workers) per colony. Formica fusca foraged singly, rarely in groups of 2 or 3 workers, in all the biotopes where it was present. Settlement in areas with different vegetation within the biotope allowed the species with a similar worker size (class IV in F. cunicularia and F. fusca), foraging type, and social organization of colonies to avoid competition.
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The subdominant Lasius brunneus occurred rarely, mainly on old drying oak and hornbeam trees. This species could mobilize large parties (on average, 1 or 2 parties and 25–50 workers per colony). Mobilization allowed L. brunneus to compete effectively with both the influent F. fusca, which co-occurred regularly with the former species and which had solitary foraging, and with the influents Myrmica spp. which used mass mobilization (Table 2). On average, the influents Temnothorax spp. mobilized one party to each bait (see Table 2). 2Ad. Dendrobionts prevailed by the number of species (up to 8 species in each locality studied), followed by herpetobionts (up to 5 species). Dendrobionts were dominants or subdominants while herpetobionts were, as a rule, influents. Associations of this type were characterized by weakly expressed (as compared to the monodominant associations with a territorial dominant) interaction of the subdominant species with the dominant. The situational nature of this interaction as well as dominance was earlier noted by Zakharov and Sablin-Yavorsky (1998) in their discussion of the characteristics of facultative dominants. 2B. Monodominant associations with weakly territorial dominants (oak-hornbeam forests plots with prevalence of ruderal herbaceous vegetation in Feofaniya and Syretsky Gai). They were characterized by: (a) the presence of up to 5–6 species at one site, with a single weakly territorial dominant; (b) the invariable type of foraging strategy in all the species; (c) the prevalence of herpetobionts (up to 4 species). 2Ba. Due to the absence of the territorial dominant and the presence of only one weakly territorial dominant L. emarginatus, there was a somewhat greater number of ant species present (up to 5 or 6 per site). 2Bb. The foraging strategy remained unchanged in the ant species of all the hierarchical ranks. For example, mobilization of the influent Myrmica spp. was at the same level in the sparse (the crown density up to 64%) and dense (80% and higher) areas of the forest, regardless of the illumination regime and the presence of the weakly territorial dominant L. emarginatus. In this association the parameters of the influents (Myrmica spp. and Temnothorax spp.) within the FT of L. emarginatus were twice as high as within the FT of F. rufa (Table 2). Thus, in the absence of the territorial multilayer dominant, influents reached greater mobili-
zation parameters without changing their strategy type. The oak-hornbeam forest areas with prevalence of ruderal vegetation in Syretsky Gai were characterized by the mobilization parameters of the influent species similar to those in Feofaniya (Table 2). For the dominant L. emarginatus, mobilization to bait was somewhat lower (Table 3). 2Bc. Herpetobionts prevailed among the ecological groups (up to 4 species), with the exception of the dendrobiont dominant or subdominant species. These associations had a somewhat greater fraction of dendrobionts as compared with monodominant associations with a territorial dominant, since the latter was absent. 3. Degraded ant associations (pine, oak, and locust plantations in the Peremoha and Partizanskaya Slava parks). In the oak plantings most subject to anthropogenic influence (tramping, soil compaction, ruderalization of the herbaceous layer), the structure of the ant complexes has degraded due to disappearance of species of high hierarchical ranks. These associations were characterized by: (a) the lowest species richness (2–4 species); (b) the quantitative prevalence of one species which usually acted as an influent in other associations; (c) sometimes more extensive mobilization, possibly due to the greater size of colonies in the absence of dominants. 3a. These associations typically included 2 or 3, less frequently 4 ant species. Most often, one species prevailed in the samples (up to 80–95% of the total number). All the members of such associations were herpetobionts; less frequently one dendrobiont species was present. Their distribution was determined by their biotopic preferences, whereas in all the other types of associations it was more or less strongly affected by the distribution of the dominant. 3b. The degraded associations included some species (most often, Lasius niger and Myrmica rubra) which in other associations act as influents and are adapted to existing under the anthropogenic impact; this fact was earlier noted by Sorokina (1998). Both species were herpetobionts. 3c. Correspondingly, the foraging strategy did not depend on the high-rank species. The mean number of workers and parties attracted to bait in the Peremoha Park were the greatest in L. niger and M. rubra (see Table 2). In the absence of dominants, these influents ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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Table 6. Distribution of chorological complexes in different types of multi-species ant associations within the city limits of Kiev Type of multispecies association
Chorological complex
Dominant
Subdominant
Influent
1
HDC (I)
0 2–3
1–2 1–3
0 0
2
3
CHC (IV) HHC (V) SLC (VI) MLC (VII) HDC (I) CHC (IV) HHC (V) SLC (VI) MLC (VII) HDC (I) CHC (IV) HHC (V) SLC (VI) MLC (VII)
4 HDC (I) CHC (IV) HHC (V) SLC (VI) MLC (VII)
0 0–1 0 0 0 0 0 0 0 0–1 0 0–1 0 0 1 0 0 0–1 1 0 0 0–1 0 0 0 Hierarchy of species is not expressed 0 1 1–2 0–1 0
1–2 1–2 0 0 0 1–2 1–2 0 0 0 1–3 1–3 0
Types of multi-species ant associations: 1, bidominant with weakly territorial dominants (L. emarginatus and L. fuliginosus, C. ligniperdus); 2, monodominant with a territorial dominant (F. rufa); 3, monodominant with a weakly territorial dominant (L. emarginatus); 4, degraded. Chorological complexes: HDC, horizontal dendrobiont complex; CHC, climbing herpetobiont complex; HHC, horizontal herpetobiont complex; SLC, soil and litter complex; MLC, complex of multilayer species (according to Zakharov, 1994). Figures correspond to the total number of ant species for the given type of association in the studied territory. The chorological complexes which include the dominant species of the given type of association are shown in bold.
could either form larger colonies (judging by the greater number of mobilized workers) or have a greater density of colonies as compared with other associations. The mobilization parameters of M. rubra in the Partizanskaya Slava park were low, close to those within the FT of F. rufa in the forests of Feofaniya. The parameters of L. niger were also minimal. The multi-species ant associations in this park were in the most degraded state, the foraging activity being minimal even in the species with a high adaptive potential.
of the settlement of the remaining ant species in the territory. In such associations, the interspecific connections, weak as they already are, may become practically absent, primarily due to the small density of nests. A similar structure of ant settlements was observed by Dlussky (1981) under natural conditions in the north; the FTs in such settlements did not overlap and interspecific interactions were absent.
The lower limit of functional integrity or the very existence of the most degraded ant associations seems to be determined by the minimal values of the number of workers and their parties, the density and regularity
In total, we have distinguished 5 chorological complexes of ants. This number is comparable with that reported by Zakharov and Sablin-Yavorsky (1998) for the mixed forests, and by Putyatina (2008) for the pine
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forests of Moscow region (4 complexes each). Besides the above 4 types of chorological complexes (CHC, HHC, SLC, and MLC; the acronyms are explained in notes to Table 6), one of the associations studied by us included one more complex, HDC, with two species: Camponotus fallax and Dolichoderus quadripunctatus.
The presence of Temnothorax spp. of SLC was also possible.
From the data in Table 6 it can be seen that the bidominant and monodominant associations with weakly territorial dominants typically included 3 or 4 chorological complexes, the monodominant ones with territorial dominants, 3 (rarer, 4) complexes, and the degraded associations, 2 or 3 complexes.
Formica rufa has all the characteristics of a territorial dominant, especially in the case of formation of colony federations (in the sense of Zakharov, 1991). Ants of this species, similar to F. polyctena and F. aquilonia Yarrow, 1955, visit and defend all the layers of the FT. By contrast, L. fuliginosus visits and defends the central part of its territory as well as areas along the trails and around the trees housing aphid colonies (Czechowski et al., 2013). Thus, F. rufa may exert a more substantial action on other ant species, forming monodominant associations of nests (Zakharov and Sablin-Yavorsky, 1998), where other ant species either occur sporadically within the dominant’s FTs (such as L. fuliginosus), or are forced out into the neutral areas if such areas are available. In this way F. rufa mostly affects the species with high hierarchical ranks but fewer workers in the colonies (in our case, the weakly territorial dominants). Species which have no defended territory but only defend their nests are not, as a rule, subjected to this pressure (Vepsäläinen and Pisarski, 1982).
The first 3 types of ant associations occurred under natural conditions. In bidominant associations, the FTs of dominants were spatially separated, so that penetration into the neighbor’s FT was possible only at the periphery. The territories of species with larger colonies and FTs (L. fuliginosus) could be surrounded by the FT of the dominant with smaller colonies (L. emarginatus). The dominants and subdominants of bidominant associations belonged to CHC. The species of this complex acted as a link between the herpetobiont and dendrobiont complexes. A greater number of CHC species in bidominant and monodominant associations with weakly territorial dominants may reflect the strengthening of connections between ant species from different layers. There was also a relatively autonomous complex of dendrobionts (HDC, Table 6). Influents belonging to HHC and SLC (Myrmica spp. and Temnothorax spp., respectively) interacted only on the soil surface. The monodominant association with the territorial dominant F. rufa included a somewhat smaller number of species since some high-rank dominants were absent. The interaction of species there was mostly mediated by the multilayer dominant (MLC) F. rufa. The subdominant, if present, belonged to CHC (F. cunicularia). The influents (including F. fusca of HHC) were represented by species of the same chorological complexes as in the bidominant association. The monodominant associations with a weakly territorial dominant included L. emarginatus (CHC) as the prevalent species. Its less expressed territoriality as compared with F. rufa was conducive to the presence of a greater number of species, first of all, influents of HHC and SLC. Finally, the degraded associations included only species of CHC (L. niger) and HHC (Myrmica spp.).
DISCUSSION The Influence of the Dominant’s Territoriality upon the Structure of Multi-Species Ant Associations
The subordinate species, as noted by Zakharov and Sablin-Yavorsky (1998), mainly inhabit neutral areas if such areas have not disappeared due to the establishment of the secondary federation of F. rufa. In the hornbeam-oak forests of Feofaniya, the association generally preserved its mosaic structure with nonfederated nest complexes of F. rufa and single nests of L. fuliginosus in the neutral areas. The term “nonfederated” refers to the nests complexes of F. rufa in which neutral territories are still present and which have not yet started the formation of secondary federations (Zakharov and Sablin-Yavorsky, 1998). The ant associations in the hornbeam-oak forests of Feofaniya give a typical example of the influence of this dominant upon the subordinate species at high settlement density. The mobilization parameters of Myrmica spp. and Temnothorax spp. are the lowest, whereas Temnothorax spp. forages only in the litter layer that cannot be easily accessed by the dominant. Under the conditions of increased anthropogenic impact in the form of uncontrolled recreation, the dominant may still be preserved but the subdominant disapENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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pears from the association. Similar results were obtained by Vepsäläinen and co-authors (2000) for the areas of high dynamic density of F. aquilonia, in which only 2 ant species were found. In the complex of 25 nests of F. rufa located in the oak-hornbeam forest in Feofaniya, we observed a gradual decrease in the size and number of nests, which was reduced by 30% during 2009–2013. This was related to gradually increasing recreation pressure, road building, and construction activity which damaged some nearby nests. Subsequently, with the disappearance of F. rufa from the association, L. fuliginosus will remain in it and the number of ant species will somewhat increase due to their settling in the vacated and neutral areas. In associations with one or several weakly territorial dominants the influence on the subordinate species is less considerable. The overlapping of the FTs of most species, including the dominant ones, allows more species with high hierarchical ranks to coexist. The Foraging Strategy As can be seen from Tables 2 and 3, differences between the types of associations by the mean number of workers per party and the number of parties per colony were maximal in the high-rank species F. rufa and L. emarginatus. As already noted, differences in the number of workers and their parties per colony of F. rufa in Svyatoshino and Feofaniya may result from different levels of anthropogenic impact. If resources become insufficient due to anthropogenic degradation of plant communities, the dominant species builds up a high dynamic density of workers and can faster mobilize large parties to the food source. Red wood ants were shown to be able to exist under the conditions of a megalopolis (Volkova, 2009) in the presence of a sufficient number of trees and also grass and litter, providing the food resources, building material, and microclimate. Settlements of F. rufa can be preserved in habitats with a high recreational load (Samoshilova and Reznikova, 1979), yet under these conditions this species cannot fully perform its regulatory functions in the forest ecosystem. In dominants with a high level of social organization, one of the mechanisms of adaptation to the changing environmental conditions (including the anthropogenic factor) is their ability to change the ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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foraging strategy from the solitary to mobilization one and vice versa. The best example of foraging strategy change may be the dominant Lasius emarginatus. In associations of the oak-hornbeam and oak-maple-hornbeam forests of Lysa Hora this species foraged singly, whereas in the oak-hornbeam forest of Feofaniya it used mobilization of parties (Table 3). In the other localities studied in Kiev L. emarginatus used strategies intermediate between the above, such as foraging in small parties (the oak-maple forest in Lysa Hora and the oak-hornbeam forest in Feofaniya). Formica rufa, with its secondarily structured FT, can change the number of foragers attracted to bait by directing workers from the varying number of adjacent ESA. The influents do not change their foraging strategy type. All the four species listed in Table 2 consistently used either individual foraging (F. fusca) or mobilization (the rest of the species). Only the scale of mobilization varied depending on the biotope and the degree of territoriality of the dominant. Dependence on territoriality was observed only regarding the dominant F. rufa, at the level corresponding to its nest complexes. Considerable fluctuations in the number of influent workers mobilized were recorded only in the Peremoha Park (Table 2). In the oak-hornbeam forests of Feofaniya the minimal parameters of Myrmica spp. were characteristic of areas with an obligate territorial dominant F. rufa. The parameters of Myrmica spp. were higher in the areas with a facultative dominant L. emarginatus, and the highest in the absence of the dominant’s influence (Peremoha Park). Changes in the Composition of Chorological Complexes during Degradation of Multi-Species Ant Associations under Urban Conditions In the monodominant association with a territorial dominant, the lower parameters of mobilization of the subordinate ant species resulted from the dominant’s territoriality, whereas in degraded associations, impoverishment of the species composition was caused by the increasing anthropogenic impact. The bidominant association with weakly territorial dominants was characterized by a mosaic spatial distribution of species and expressed vertical connections due to the CHC species of higher ranks. During degradation of such associations, the dominance system was preserved while the vertical connections between species of the terrestrial and arboreal layers weakened.
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The horizontal connections between ant species of HHC and SLC did not suffer any considerable changes following changes in the species composition. In the monodominant association with a territorial dominant, connections between species from different layers were mediated by the dominant of MLC. The mean number of workers and their parties per colony was inversely proportional to the corresponding parameters of the dominant which was present in all the layers and interacted with other components of the association. Such associations included no species of HDC (they may occur only in the absence of the dominant’s nest complexes), whereas the CHC component was weakened due to a rarer occurrence or absence of the subdominant species. This was caused by the aggressiveness of the territorial dominant toward the high-rank ant species under the conditions of limited resources. Finally, the degraded associations had no vertical connections between species since they included no dendrobionts and no members of MLC and CHC. The only representative of CHC is L. niger. Horizontal connections could take the form of occasional fights for abundant resources. Thus, during degradation of associations the number of ant species belonging to CHC was gradually reduced, which was accompanied by the weakening of connection between species from different layers. The Role of Lasius emarginatus in Multi-Species Ant Associations Lasius emarginatus is unique in its broad adaptation abilities as compared with other dominant species. The FT of L. emarginatus is structured, and its large colonies have foraging pathways which may partly run underground as tunnels. The intensity of movement along these pathways (up to 85 ind. in 2 min) was only twofold inferior to that in L. fuliginosus. All the other species lower in hierarchy, with the exception of L. brunneus, had no structured FTs. In the absence of L. emarginatus in the association, the interactions between species were strongly weakened, which may result in its further degradation. The Significance of the Urban Green Zones for Preservation of the Species Composition and Structure of Multi-Species Ant Associations Zryanina (2009) emphasized the significance of the netlike structure of green zones for the penetration of
forest species into cities. The significance of refugia preserving both the dominant species and the ants of other hierarchical ranks for restoration of the species composition and association structure in disturbed biotopes was also noted in earlier works (Zakharov and Sablin-Yavorsky, 1998). In the territory of Kiev, such refugia were Feofaniya, Lysa Hora, and Svyatoshino where Lasius emarginatus, L. fuliginosus, Camponotus ligniperdus, and Formica rufa occurred. However, red wood ants may disappear from the associations of Feofaniya in the near future. Urgent measures should be taken to protect the nests of this complex and to restrict the recreational load in the adjoining zone. The increasing recreational load causes impoverishment of the species composition, reduction of nest density in the territory (Zyuzgina, 1998), and disappearance of the structure-forming dominant species, which leads to its further degradation. Peculiarities of the Structure of Ant Complexes in Kiev as Compared with Other Cities Comparison of the composition and structure of ant complexes in Kiev and some other large cities, such as Warsaw, Sofia, and Helsinki, has revealed considerable differences between them. In Helsinki, Lasius niger was the most common species, followed by Myrmica rubra, Formica fusca, Lasius flavus, and L. platythorax (87% of the total number). The species L. niger, L. flavus, and Myrmica rugulosa Nylander, 1849 were the most resistant to urban conditions, whereas such forest species as Camponotus herculeanus and ants of the Formica rufa group had minimal abundance or were entirely absent (Vepsäläinen et al., 2008). Species with defended territories and those inhabiting wood were rare or absent. The most common species on lawns and in parks of Warsaw was L. niger, whereas M. rubra occurred most often in the preserved patches of forest vegetation (Slipinski et al., 2012); F. cunicularia, Solenopsis fugax, and L. flavus were also frequent in parks while Tetramorium caespitum and M. rugulosa were more typical of alleys. The invasive species L. neglectus prevailed in some districts of Warsaw (Czechowska and Czechowski, 2003). Within the city limits of Sofia, the abundance of widespread species was twice as high as in the suburbs (Antonova and Penev, 2006). The most common species were T. caespitum, L. niger, F. cinerea, and Temnothorax affinis (Mann, 1920). ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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Lasius emarginatus, L. brunneus, Camponotus fallax, Dolichoderus quadripunctatus, and Temnothorax crassispinus were common in the forest and woodland park areas of Kiev. These dendrobionts had the ranks of dominants or subdominants, or, as T. crassispinus, high abundance. Lasius niger and M. rubra occurred in Kiev in great numbers only in degraded park communities. This situation was possible only in the absence of species that act as dominants in forest areas. If trophic resources were limited, Lasius niger gradually replaced M. rubra, which could be seen by its increasing mobilization parameters. An important factor under urban conditions is the shortage of places suitable for nesting. The highest values of nesting parameters and highest plasticity with respect to biotic factors (Zakharov and Sablin-Yavorsky, 1998) were characteristic of L. niger. Typically forest territorial species (the Formica rufa group, etc.) were also recorded within the Kiev city area; some of them were common (L. emarginatus) and formed the core of multi-species ant associations in the fragmented forest areas. The multi-species ant associations in Kiev are less disturbed and more structured than those in other cities considered above. Their structure and preservation is ensured by the presence of considerable forest areas within the city limits. CONCLUSIONS (1) A total of 26 ant species from 3 subfamilies were recorded in the broad-leaved forests with participation of the English oak and in the oak plantings within the green zones of Kiev. (2) Three types of multi-species ant associations were distinguished: (a) mono- and bidominant continuums of associations with weakly territorial dominants Lasius emarginatus and L. fuliginosus, and also the behavioral dominant Camponotus ligniperdus; (b) a monodominant association with a territorial dominant of the Formica rufa group; (c) degraded associations of city parks in which these dominants were absent, being replaced by the influents Lasius niger and Myrmica rubra. (3) The dominant and subdominant species could change their foraging strategy depending on external factors, such as the level of anthropogenic impact, etc. The foraging strategy of influents remained of the ENTOMOLOGICAL REVIEW Vol. 95 No. 3 2015
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same type, though the number of workers attracted to bait could change in case of a mobilization strategy. Thus, the dominants and subdominants had more flexible foraging strategies, which was related not only to external conditions but also to more intensive interactions between them. (4) In case of increasing anthropogenic impact, the territorial dominant F. rufa intensified its influence on the subordinate species, reducing the intensity of their mobilization to bait. (5) The studied multi-species ant associations in the broad-leaved forests of the Kiev green zone were formed by five chorological complexes in which the leading and integrative role belonged to species of the climbing herpetobiont complex (CHC; Lasius emarginatus) and multilayer species (MLC; F. rufa, L. fuliginosus). (6) During degradation of associations, species of CHC and MLC disappeared from it, the vertical connections between the layers were disrupted; finally, the decreasing complexity of the association led to weakening and disappearance of the species hierarchy. (7) On the whole, as compared with other cities, Kiev has less anthropogenically disturbed ant complexes with a hierarchical structure including typically forest species in the dominant position. Their existence is to a considerable degree ensured by the forests and forest parks present within the limits of the city. ACKNOWLEDGMENTS The author is deeply grateful to A.G. Radchenko (Institute of Zoology, National Academy of Sciences of Ukraine, Kiev) and A.A. Ignatyuk (Institute for Evolutionary Ecology, NAS, Kiev) for valuable advice and comments. REFERENCES 1. Alioshkina, U.M., “Plant Associations of the Green Zone of the City of Kiev,” in Russian Geobotany: the Main Landmarks and Perspectives, Vol. 1: Variability of Types of Plant Associations and the Problems of Their Protection. Geography and Cartography of Vegetation. The History and Prospects of Geobotanical Research (St. Petersburg, 2011), pp. 7–10 [in Russian]. 2. Andersen, A.N., Hoffmann, B.D., Müller, W.J., and Griffiths, A.D., “Using Ants as Bioindicators in Land
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