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This is the accepted version of the following article: Witek M., Casacci L.P., Barbero F., Patricelli D., Sala M., Woyciechowski M., Balletto E., Bonelli S. 2013. Interspecific relationships in sympatric populations of ant social parasites. Biol J Linnean Society. 109 (3): 699–709,

which has been published in final form at http://onlinelibrary.wiley.com/doi/10.1111/bij.12074/abstract
Title: Interspecific relationships in co-occurring populations of ants’ social parasites

Running title: Co-occurring of ant’s social parasites

Authors: Magdalena Witek1, Luca Pietro Casacci2, Francesca Barbero2, Dario Patricelli2, Marco Sala2, Simone Bossi3, Massimo Maffei3, Michal Woyciechowski4, Emilio Balletto2, Simona Bonelli2
1 Museum and Institute of Zoology, Polish Academy of Science, Wilcza 64, 00-679 Warszawa, Poland
2 Zoology Unit, Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, 10123 Torino, Italy
3 Plant Physiology Unit, Department of Life Sciences and Systems Biology, University of Turin, Innovation Centre, Via Quarello 11/A, 10135 Torino, Italy
4 Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland

*Corresponding author:

Magdalena Witek, Muzeum and Institute of Zoology, Polish Academy of Science, Wilcza 64, 00-679 Warszawa, Poland

Tel: +48 22 629 32 21

E-mail: mawitus@yahoo.co.uk


Abstract

Myrmica ant colonies host numerous insect species, including the larvae of Maculinea butterflies and Microdon myrmicae hoverflies. Little is known about the interspecific relationships among these social parasites and their host ants occurring in sympatric populations. We investigated communities of social parasites to assess the strategies allowing them to share the same pool of resources, i.e. Myrmica colonies. Our study was carried out at five sites inhabited by different social parasite communities, each comprising varying proportions of Maculinea teleius, Maculinea nausithous, Maculinea alcon and Microdon myrmicae. We investigated their spatial distributions, host segregation, the degree of chemical similarity between social parasites and hosts and temporal overlaps in colony resource exploitation. Spatial segregation among social parasites was found in two populations and it arises from microhabitat preferences and biological interactions. Local conditions can drive selection on one social parasite to use Myrmica host species that is not exploited by other social parasites. My. scabrinodis and My. rubra nests infested by larvae of two social parasite species were found and the most common co-occurrence was between Ma. teleius and Mi. myrmicae. The successful coexistence of these two species derives from their exploitation of the host colony resources at different times of the year.

Key-words: competition; cuticular hydrocarbons; host-parasite interaction; Maculinea; Microdon; Myrmica; social parasites co-occurrence

Introduction

Social parasites exploit the resources of an entire insect colony (Nash & Boomsma 2008). Many organisms have evolved to live within ant societies showing various degrees of interaction, ranging from mutualism to parasitism (Hölldobler & Wilson 1990). An estimated 10,000-20,000 morpho-species of arthropods, most of which are ants themselves (Hölldobler & Wilson 1990), have evolved as ant social parasites (Thomas, Schönrogge & Elmes 2005). Numerous other insects also exploit ant colonies, e.g., Myrmecophila spp. (crickets), Atemeles spp. (beetles), Microdon spp. (hoverflies) and Maculinea spp. (butterflies) (Henderson & Akre 1986; Thomas, Schönrogge & Elmes 2005).



Among ant social parasites one of the best studied systems is the interaction between Maculinea butterflies and Myrmica ants. Maculinea butterflies are obligate social parasites for which larval survival depends on specific food plants and the presence of Myrmica ants (Thomas 1980). Maculinea larvae are adopted by Myrmica foragers from early to late summer and then live inside ant colonies for 11 or 23 months (Thomas, Elmes &Wardlaw 1998; Schönrogge et al., 2000; Witek et al., 2006). Once inside the ant colony, butterfly larvae use different types of feeding strategies: Maculinea teleius (Bergsträsser 1779) and Maculinea arion (Linnaeus 1758) are predators that actively prey on ant brood (Thomas & Wardlaw 1992), whereas Maculinea alcon (Denis & Schiffermüller 1775) and Maculinea rebeli Hirschke 1904 are considered cuckoo feeders because their larvae are fed directly by ant workers (Elmes, Wardlaw &Thomas 1991; Thomas & Elmes 1998). The feeding behaviour of Maculinea nausithous (Bergsträsser 1779) has not been fully clarified (Thomas & Elmes 1998) but recent studies suggest that it is more similar to the cuckoo strategy (e.g. Patricelli et al., 2010). Each feeding method implies particular costs and benefits. Cuckoo feeders as Ma. alcon larvae have higher larval survival rates inside the host colony (Thomas & Elmes 1998), but this strategy apparently results in higher host specificity, at least on a local scale. In contrast, Ma. teleius predatory caterpillars have lower larval survival rates inside Myrmica nests, although the parasite may be less specialised towards a single ant host species (Thomas & Elmes 1998).

Microdon myrmicae Schönrogge et al., 2002 (Schönrogge et al., 2002) is another social parasite that exploits Myrmica ants. This syrphid fly belongs to the Microdontinae subfamily, whose members have various levels of association with ants (Cheng & Thompson 2008). Similarly to many other Microdon species, Mi. myrmicae larvae and pupae are known to live inside ant colonies, whereas adults are free-flying organisms (Duffield 1981; Witek et al., 2012). In May and June, Mi. myrmicae females lay their eggs on the surface of Myrmica ant nests (Witek et al., 2012). Detailed studies on host ant specificity across Europe have shown that Mi. myrmicae exploits various Myrmica species, although Myrmica scabrinodis Nylander 1846 is the most frequently used (Bonelli et al., 2011).

Most of the previous studies have dealt with the interactions between a single social parasite species and its host ant and investigations on social parasite communities are scarce, particularly those addressing potential competition among parasites (Johnson & Herbers 2006). This is probably due to the fact that social parasites of ants are very rare and restricted to much smaller areas when compared to the distribution of their hosts (Thomas et al., 2005). Nevertheless, in wet meadows typically dominated by Molinia spp. a few social parasite species of Myrmica ants can coexist on a local scale. In previous studies many localities were found where at least two, but sometimes three or even four, species of social parasites of Myrmica ants occur together (Stankiewicz & Sielezniew 2002; Zakšek et al., 2005; Tartally 2008; Tartally et al., 2008; Witek et al., 2008; Batáry et al., 2009; Van Langevelde & Wynhoff 2009; Nowicki et al., 2009; Bonelli et al., 2011; Nowicki & Vrabec 2011; Kőrösi et al., 2012). These sites are usually preferred habitats for three Maculinea butterfly species (i.e. Ma. teleius, Ma. nausithous and Ma. alcon) as well as for the hoverfly Mi. myrmicae (Stankiewicz 2003; Nowicki et al., 2007; Witek et al., 2008; Bonelli et al., 2011). The number of such sympatric populations might be underestimated, as it is known that at least Ma. teleius and Ma. nausithous often co-occur in Europe and in the western parts of Central Asia (Woyciechowski et al. 2006). Little is known about the distribution of Mi. myrmicae except that it was frequently found at places inhabited by Maculinea butterflies (Bonelli et al., 2011). Some authors suggests that various ecological factors may be responsible for the emergence of social parasite “hot-spots” by making ant populations or individual colonies more vulnerable to social parasitism (Thomas et al., 2005; Fürst, Durey & Nash 2011). In our study, we investigated several sympatric populations of Maculinea butterflies and Mi. myrmicae hoverfly to assess how these parasites share the same pool of resources, i.e. Myrmica colonies. When more than one conspecific parasite enters the same ant nest there can be competition between them. In the case of Maculinea caterpillars either “scramble” or “contest” competition can arise, depending on the life history traits of the butterfly (Thomas, Elmes & Wardlaw 1993). Such competition can affect host and parasite population dynamics (Thomas et al., 1997), as well as larval developmental strategies (Hovestadt et al., 2007). Given the importance of competition between conspecific social parasites, we can predict that effects on the population dynamics of the interacting species should be detectable also when heterospecific social parasites using the same resources coexist in the same ant population. We hypothesised that competing populations of social parasites might be separated in space, either: i) by using different parts of the habitat; or ii) by exploiting different host species, showing different strategies of chemical integration; or temporally iii) by infesting the same Myrmica nests but using colony resources at different times of the year. The above hypotheses are not mutually exclusive.

Materials and Methods

Study sites

Studies were conducted at five sites: 1) Kosyń (Eastern Poland, 51º23'N/23º34'E), 2) Aleksandrówka (Eastern Poland in 51º33'N/23º 33'E), 3) Wojciechów (Eastern Poland, 51º34'N/23º 32'E) 4) Kraków (South Poland, 50º01'N/19º53'E) and 5) Caselette, (North-western Italy, 45º 70'N/07º29E). These study sites were characterized by different communities of social parasites (Table 1 in Supporting Information). All sites were wet meadows dominated by Molinia caerulea. Sanguisorba officinalis, the larval food plant of Ma. teleius and Ma. nausithous, was present at four sites (excluding Wojciechów), whereas Gentiana pneumonanthe, the larval food plant of Ma. alcon, was present at Caselette, Kraków and Wojciechów.



Data collection

To establish the host ant specificity and survival rates of parasitic larvae, data were collected at the end of the parasite larval development (June). At Caselette, Aleksandrówka and Wojciechów, Maculinea food plants had patchy and restricted distributions, meaning that some parts of the habitat had no, or contained only single individuals of Maculinea food plants. At these three sites, we collected data both within and outside the food plant patches. Maculinea larvae could be found only in patches covered by their food plants, whereas Mi. myrmicae was able to infest any Myrmica colony. We tested for possible spatial segregation between Maculinea and Mi. myrmicae on the basis of butterfly food plants distributions. In contrast, at Kraków and Kosyń, S. officinalis was widespread, and all investigated ant nests were inside Maculinea food plant patches.

At all sites within Maculinea food plant patches, we searched for Myrmica ant colonies located within 2 m of the butterfly food plants (S. officinalis and/or G. pneumonanthe), as this is the average foraging distance of Myrmica ants (Elmes et al., 1998). This procedure allowed us to assume that all examined nests were potentially available for all social parasite species occurring at the site. Myrmica nests located outside Maculinea butterfly food plant patches and potentially infested only by Mi. myrmicae were searched for in a random way. During sampling procedures, Myrmica nests were opened to determine the presence/absence of Maculinea (Śliwinska et al., 2006) and Mi. myrmicae larvae, pupae and exuviae. From each Myrmica colony, 10-20 ant workers were collected and preserved in 70% ethanol. The key proposed by Czechowski, Radchenko & Czechowska (2002) was used for ant species identification. A total of 656 Myrmica nests were studied. Details on the spatial distribution and composition of the Myrmica ant communities are described in Table 1 (see the Supporting Information).

Comparison of Mi. myrmicae and Ma. teleius life cycle

Data for the comparison of Mi. myrmicae and Ma. teleius life cycle focused on larval development inside Myrmica colonies are coming from our former studies (Witek et al., 2011; 2012).



Surface chemistry

Social parasite integration into host colonies can be reflected in chemical profile similarities between social parasite larvae and their Myrmica host ants. Therefore, we sampled cuticular chemical profiles of individual larvae and host ants from Kraków and Kosyń (Poland) in June 2010. Ant workers’ cuticular chemicals were sampled from six colonies of My. scabrinodis, five colonies of My. rubra (Linnaeus 1758) and two colonies of My. ruginodis Nylander 1846. Surface chemicals were also sampled from parasitic larvae: three of Ma. alcon (all found inside My. scabrinodis nests), four of Ma. nausithous (collected from My. rubra colonies), 16 of Ma. teleius (eight in My. scabrinodis, six in My. rubra, two in My. ruginodis colonies) and three of Mi. myrmicae (collected from My. scabrinodis colonies). Cuticular hydrocarbons were extracted in the laboratory from single post-adoption caterpillars as well as from five Myrmica workers from each colony. Extracts were analysed by gas-chromatography/mass spectrometry (GC-MS) using standard methods (for further information see to the Supporting Information).



Statistical analysis

Fisher’s exact test was used to compare the degree of nest infestation among habitat patches in Caselette. The ant host specificity of Ma. teleius in the Kraków and Kosyń populations was calculated by two separate tests: 1) Fisher’s exact test: the proportion of available nests of each Myrmica species (expected value) was compared with the proportion containing Ma. teleius larvae/pupae (observed value), 2) general linear model for overdispersed data (negative binominal distribution) comparing the numbers of Ma. teleius specimens found within the nests of each Myrmica species. Data concerning My. ruginodis nests from Kosyń were excluded from this analysis because only two nests were found. GLM analysis allows to tests for quantitative differences between the numbers of Ma. teleius reared by different Myrmica species. Methods used to analyse data on cuticular hydrocarbons are described in the Supporting Information.


Results

Spatial segregation of social parasites

Spatial segregation was tested for three populations: Caselette, Aleksandrówka and Wojciechów. In Caselette only My. scabrinodis colonies were present. In an area containing both species of Maculinea food plants we found 15 (30%) nests exploited by Ma. alcon, two nests (4%) infested by Mi. myrmicae (one of them also contained Ma. alcon) and one nest (2%) with Ma. teleius. In the area where only S. officinalis was present, 10 nests (20%) were infested by Ma. teleius and four (8%) by Mi. myrmicae. In the area lacking any butterfly food plants and hence having no Maculinea, 25 (25%) Myrmica colonies were infested by Mi. myrmicae. The proportion of nests infested by Ma. teleius was significantly higher in the part of the meadow where only S. officinalis was present as compared with the zone where both Maculinea food plants were present (Fisher’s exact test, P = 0.003). Significant differences in the proportion of nests infested by Mi. myrmicae were observed across the three zones (Fisher’s exact test, P < 0.001). Pairwise comparisons demonstrated that the proportion of nests infested by Mi. myrmicae was significantly higher outside of the area with butterfly food plants than in the area where both plants were present (Fisher’s exact test, P = 0.004).

At Aleksandrówka only My. scabrinodis nests were infested by social parasites. In the area containing S. officinalis, 98% of the nests were of My. scabrinodis. Six (12%) of these nests were exploited by Ma. teleius and none contained Mi. myrmicae, whereas in the area lacking Ma. teleius food plant, only 74% of the Myrmica colonies belonged to My. scabrinodis and 6 of these (8%) were infested by Mi. myrmicae (Table 1, Supporting Information).

Also at Wojciechów only My. scabrinodis colonies were exploited by social parasites. All infested nests were found in an area where G. pneumonanthe was growing; My. scabrinodis formed 95% of the nest population, two nests (3%) were infested by Ma. alcon larvae and another two (3%) by Mi. myrmicae.



Double infestations

Nests with double infestations were found at Caselette (3 nests), Kosyń (3 nests) and Kraków (6 nests) and they belonged to either My. scabrinodis or to My. rubra. Depending on ant species and population the percentage of double infestation among parasitised nests ranged from 6 to 40 (Table 1). Also the proportion of parasitic larvae reared in nests with double infestation was high and in some situations all larvae of a particular social parasite species were found in such colonies (Table 1). The most common co-occurrence was found between Mi. myrmicae and Ma. teleius (nine out of 12 cases) and the mean number of parasitic larvae (±SD) was 4.8 ± 2.18.



Comparison of Mi. myrmicae and Ma. teleius life cycle

A comparison of the life cycle of Mi. myrmicae and Ma. teleius is shown in Fig. 1. The most intensive Ma. teleius larval growth connected with exploitation of host colony resources occurs from April to June, which corresponds to period when Mi. myrmicae is present in the stage of pupa, adult or egg and it is not using colony resources. Mi. myrmicae larvae mostly grow from the beginning of July to September, which is a time when Ma. teleius is present in the stage of pupae, adults, eggs and I-III instar larvae feeding on the specific food plants (Fig. 1).



Segregation among host ant species

My. scabrinodis was the only host ant species exploited by social parasites at Caselette, Wojciechów and Aleksandrówka. At Caselette, My. scabrinodis was the only Myrmica species present, whereas at the other two sites it was the most abundant species (83% in Aleksandrówka and 81.5% in Wojciechów). Similarly, My. scabrinodis was the dominant species at Kraków and Kosyń, but also other Myrmica species were used as hosts in these areas.

At Kraków My. scabrinodis was the only host exploited by Ma. alcon and Mi. myrmicae (Table 1, Supporting Information), whereas Ma. teleius exploited all Myrmica species present. The proportion of Ma. teleius larvae/pupae reared by various Myrmica host species differed significantly (Fisher exact test, P = 0.01), although pairwise comparisons among Myrmica host species did not reveal any significant differences. Results obtained by the general linear model did not reveal any significant difference in the numbers of Ma. teleius reared by various Myrmica host species (Table 2).

In Kosyń four Myrmica species were found, three of which were exploited by resident social parasites (Table 1, Supporting Information). Mi. myrmicae exclusively exploited My. scabrinodis, whereas Ma. nausithous was found only inside My. rubra nests. Ma. teleius exploited three Myrmica species: My. rubra, My. scabrinodis and My. gallienii Bendroit 1920. The proportion of Ma. teleius larvae/pupae reared by the various Myrmica host species differed significantly (Fisher exact test, P < 0.001) and pairwise comparisons performed by Fisher exact test indicated that Ma. teleius larvae exploited My. rubra nests to a significantly greater degree than nests of My. scabrinodis (P < 0.001) or My. gallienii (P < 0.001). Similar results were obtained by the general linear model (Table 2).

Surface chemistry

A GC analysis revealed a total of 111 compounds across the pooled samples, with branched alkanes being the most abundant hydrocarbons. We did not find any significant difference in the variability of cuticular hydrocarbon profiles of samples (My. scabrinodis, My. rubra, Ma. teleius) collected from different sites with respect to samples obtained from the same site (P-valuesANOSIM > 0.05 for each species). Data collected from Kraków and Kosyń were therefore pooled for analysis.

A cluster representation of the 39 samples, based on the fourth root-transformed relative abundances of all recorded hydrocarbons, yielded a good discrimination between the three Myrmica ant species and the four parasite species (Fig. 2a). Pairwise within-species comparisons showed that My. scabrinodis had the lowest within-species similarity (ca. 67%), whereas My. rubra and My. ruginodis had high within-species similarities (ca. 78% and 89%, respectively). ANOSIM determined that six out of the seven analysed species were significantly distinct from each other (P < 0.05), except Ma. alcon, which clustered together with My. scabrinodis, its host ant species (Fig. 2a). The hydrocarbon samples of Ma. teleius, which was the only parasite found within the nests of three different Myrmica species presented a rich chemical profile (Ma. teleiusruginodis: 57.0 ± 0.0 peaks; Ma. teleiusscabrinodis: 69.0 ± 7.8 peaks; Ma. teleiusrubra: 69.0 ± 7.8 peaks) . Also Ma. nausithous chemical profiles were characterised by a high number of hydrocarbons (50 ± 13 peaks), while Ma. alcon larvae had considerably fewer cuticular hydrocarbons (a maximum of 28 peaks) than Ma. teleius or Ma. nausithous. Ma. teleius chemical profile was 32% similar to that of My. ruginodis workers and 50% similar to that of My. rubra. Ma. nausithous, which exclusively exploits My. rubra colonies, clustered together with Ma. teleius samples, but had lower chemical similarity (43%) with its host species than was observed for Ma. teleius caterpillars (51%). Ma. alcon showed the highest pairwise similarity (ca. 67%) with its exclusive host ant, My. scabrinodis (Fig. 2b). The parasite species showing the most peculiar and simple hydrocarbon profile, with an average of just eight hydrocarbon peaks, was Mi. myrmicae, which exclusively infested My. scabrinodis colonies.
Discussion

Sympatric populations of ant social parasites use a number of ways to share the same pool of resources, which are colonies of their host ants. The spatial distribution of Maculinea butterflies is strictly connected to the presence of their food plants. As a consequence, only Myrmica nests located in the vicinity of these plants can be infested by butterfly larvae. In contrast, Mi. myrmicae females may apparently lay their eggs on the surface of any Myrmica nest occurring in any part of the meadow. At three out of five study sites the distribution of Maculinea food plants allows us to test the spatial distributions of various social parasite species and data collected at two of these sites clearly showed that they can be spatially segregated. At Caselette we distinguished three zones, each dominated by one social parasite species. A similar spatial segregation pattern was detected at Aleksandrówka, where no Myrmica colonies were infested by Mi. myrmicae in the part of the meadow where Ma. teleius food plants were present. Spatial segregation can result from a mixture of various factors and the simplest explanation can be connected with slightly different microhabitat preferences since, for example, Mi. myrmicae females prefer to lay their eggs in very humid habitat patches (Bonelli et al., 2011). Another possible explanation might be a consequence of competition among different species of social parasites as well as their influence on host colony behaviour but in order to explain these possible mechanisms, further investigations are needed.



In our study, only at Caselette it was possible to detect spatial segregation between different Maculinea species. In other places only Ma. teleius was abundant enough, whereas samples of other butterfly species were too small to make any spatial analysis. Nevertheless, previous studies (Nowicki et al., 2005, 2007; Batáry et al., 2009; Van Langevelde & Wynhoff 2009; Kőrösi et al., 2012), based on data obtained on adult butterflies, showed that in sympatric populations of Ma. teleius and Ma. nausithous these two species are spatially separated, mostly because of their different microhabitat preferences. These results can be viewed both in connection with the use of different hosts ants and with the implementation of different strategies of chemical integration into the host colonies corresponding to different degrees of host-specificity. Our data clearly show that Ma. alcon and Mi. myrmicae are highly specific with respect to My. scabrinodis, whereas Ma. nausithous is specific to My. rubra. Ma. teleius is considered the most generalist species among all Maculinea butterflies (Stankiewicz & Sielezniew 2002; Woyciechowski et al., 2006; Tartally & Varga 2008; Witek et al., 2010). At Kraków and Kosyń, where several Myrmica species were abundant, Ma. teleius uses all available host species. Our data concur with some previous studies carried out in the Kraków region (Witek et al., 2010) which indicating that colonies of My. rubra and My. ruginodis can be used by Ma. teleius larvae even more successfully than nests of My. scabrinodis. It should be noticed that, in these populations, Ma. teleius competes with Ma. alcon and Mi. myrmicae larvae for access to My. scabrinodis colonies. In such situations should competition pose strong enough selection on Ma. teleius population to use Myrmica host species not exploited by other social parasites. More in general, one can ask whether the local patterns of host ant specificity observed in Ma. teleius may vary depending on the presence/absence of other competitors. According to predictions of the geographical mosaic model (Thompson 1999); geographic variation in the strengths of coevolution may lead to differences in host ant use at both the local and regional level. Thus, in some cases not only the availability of host species but also the presence of other competitors might shape coevolution between particular species of social parasites and of their hosts.

Although the sample size for some of the species considered in our study is small, results obtained from the analysis of post-adoption chemical profiles reflect degrees of integration inside the host colony and well explain the level of species-specificity observed for the various social parasites in study populations. It is known that Maculinea caterpillars infiltrate Myrmica colonies mostly by mimicking the cuticular hydrocarbon composition used by the ants for nest mate recognition (Akino et al., 1999; Schönrogge et al., 2004; Nash et al., 2008). Abandoning the food plant, Maculinea larvae possess a chemical profile that weakly mimics that of their host ants (Nash et al., 2008). Such behaviour has been demonstrated for the cuckoo feeders (Akino et al., 1999; Elmes et al., 2002; Schönrogge et al., 2004) but it is also conceivable for the predatory species. Once the caterpillars are retrieved to inside the ant colonies, the chemical composition of their cuticle changes and the number of hydrocarbons increases to mimic more closely the host ant’s profile (Akino et al., 1999; Elmes et al., 2002; Schönrogge et al., 2004). In both populations, Ma. alcon and Mi. myrmicae exclusively exploit My. scabrinodis colonies. Data on the chemical profiles of their post-adoption larvae show two different patterns of chemical similarity with respect to this Myrmica host species. Ma. alcon larvae are highly integrated within their host colonies and achieve almost 70% of chemical similarity with their host workers (Fig. 2), comparable to the degree of similarity found among My. scabrinodis colonies. Even if we do not have any data on the chemical profiles occurring during the pre-adoption phase, it is possible to assume that after adoption Ma. alcon caterpillars developed more complex chemical profiles either through the acquisition of hydrocarbons, by inducing direct feeding by worker ants, or perhaps through the synthesis of new hydrocarbons. Schönrogge et al., (2004) demonstrated that the latter option is implemented in Ma. alcon’s sister species, Maculinea rebeli , which in this way improves and amplifies its mimicry to My. schencki. The chemical similarity between Mi. myrmicae and its host ants is much lower than that of Ma. alcon, but its hydrocarbon profile is still more similar to My. scabrinodis than to any other Myrmica species. Relative to Maculinea larvae and Myrmica workers, the chemical profile of Mi. myrmicae exhibits few cuticular hydrocarbons, all at low concentrations, thereby indicating that it uses an improved “chemical insignificance” strategy (Lenoir et al., 2001) to survive within Myrmica colonies. Such a poorly developed chemical profile might be explained by the fact that, after summer, Mi. myrmicae larvae seem to stop feeding on the ant brood and do not have many further contacts with workers, becoming therefore unable to acquire the more complex chemical profiles characteristic for Ma. teleius and Ma. nausithous. Moreover, in analogy to Mi. mutabilis, which parasitises colonies of Formica lemani (Schönrogge et al., 2008), we can assume that Mi. myrmicae females, following the olfactory trace of one or more specific chemicals, may recognise and lay their eggs in the host nests of My. scabrinodis to thereby maximising the fitness of their offspring. For this reasons, it is likely that larvae having developed in the “correct” host colony do not need to be chemically mimetic to integrate inside it, but simply use a chemical insignificance strategy to prey on ant brood undisturbed. In our study, Ma. nausithous was observed only at Kosyń but our previous investigation that it exploited My. rubra also in the Kraków (Witek et al., 2008; Patricelli et al., 2010). Ma. nausithous, in fact, is highly specific to My. rubra colonies (Thomas et al., 1989; Stankiewicz & Sielezniew 2002; Tartally & Varga 2005; Witek et al., 2008). Yet, its larvae do not reach the same level of chemical similarity as Ma. alcon does within My. scabrinodis colonies and is also lower than that of Ma. teleius larvae, which share the same My. rubra colonies. Nevertheless, its chemical similarity is high enough (ca. 43%) to successfully exploit colony resources. The cuticular hydrocarbon profiles of post-adoption Ma. teleius larvae achieved the highest degree of similarity with the host workers of My. rubra colonies (Fig. 2), which may explain why Ma. teleius is able to successfully exploit colonies of this ant species both at Kraków and Kosyń, and might also indicate an ancestral association with this Myrmica species. Various chemical integration strategies could therefore have stabilized over time thereby allowing a variety of social parasites to survive at the expenses of the same ant community of the genus Myrmica.

Our results showed that social parasites are able to exploit the same Myrmica colonies and most doubly-infested nests belong to My. scabrinodis, which was the most abundant Myrmica species in all study sites. This is not surprising because this ant species is the only host of Ma. alcon and Mi. myrmicae and is also used by Ma. teleius. Another Myrmica species that could be potentially infested by more than one parasite species is My. rubra, which is a host of Ma. nausithous and Ma. teleius. The highest number of parasitised nests were found at Kraków, where almost half of the My. scabrinodis colonies were infested by parasitic larvae and among them 19% were doubly infested. The percentage of Ma. teleius and Mi. myrmicae larvae reared by these colonies was also high and respectively 33% and 46% of larvae were found inside doubly infested nests. This result shows that double infestation is not such a rare phenomenon and is particularly interesting because even intra-species competition among Maculinea larvae has crucial consequences for both larval survival and population dynamics (Thomas et al., 1993). The most commonly observed double parasitic co-existing observed inside Myrmica nests was between Mi. myrmicae and Ma. teleius. Because our data were collected at the end of the larval development period, the co-occurrence of these social parasites indicates that they were able to share the resources afforded by the same host colony. We found Mi. myrmicae exuviae in most of these nests, indicating that this social parasite successfully completed its life cycle inside the host colonies. The ability to coexist in the same host colony might result from temporal segregation in resource exploitation. The highest feeding activity of Mi. myrmicae larvae occurs from July to September (Witek et al., 2012), when Maculinea butterflies are present as pupae, imagoes and early instar larvae feeding at specific foodplants and are therefore not yet exploiting colony resources (Fig. 1). In contrast, the most intensive feeding activity found for the majority of Maculinea larvae occurs before pupation, between the end of April until middle of June (Thomas et al., 1998; Schönrogge et al., 2000; Witek et al., 2006; Sielezniew & Stankiewicz 2007) which is a time when Mi. myrmicae is present as pupa, imago or egg and does not use host colonies resources. Therefore, this temporal segregation of feeding activities might allow both social parasite species to undergo larval development inside the same host colony. It is important to notice that in some populations of Ma. teleius and Mi. myrmicae, especially those from northern Europe, one- and two-year developed larvae can coexist (Schönrogge et al., 2000; Witek et al., 2006). Therefore, the mechanism of interaction between these two social parasites as well as their population dynamics might vary across their ranges.

To our knowledge for the first time it was investigated how ant social parasites occurring in sympatric populations share the same pool of resources, which are ant colonies. Although the database presented in this paper is not very powerful, mostly because of difficulties in collecting materials of social parasites, and although most of our conclusions are based on field observations, we have been able to distinguish patterns of sharing Myrmica colonies among different social parasite species. It is supposed that the effect of Maculinea butterfly larvae on host colony fitness is severe (Thomas &Wardlaw 1992; Nash et al., 2008), so that strong competition among larvae of these social parasites is expected to occur. As hypothesized, we found context-dependent segregation among social parasites either by space and host-ant species, as well as by temporal segregation in colony resource exploitation. In the case of spatial segregation, probably a mixture of various ecological factors is responsible for the observed pattern. When environmental conditions do not allow for spatial segregation, the populations of some social parasite species may be forced to use Myrmica host species not exploited by other more specialised competitors. Finally, the most common co-occurrence between social parasites was found for species that exploit host resources in different times of the year. Thus, temporal segregation allows them to survive inside the same host nest and avoiding direct competition for resources.


Acknowledgements

We would like to thank Anna Amirowicz, Elżbieta Rożej, Joanna Kajzer and Paweł Mielczarek for their help with the fieldwork in Kraków as well as Graham Elmes and four anonymous referees for providing valuable comments on earlier version of manuscript. This research was funded within the project CLIMIT (Climate Change Impacts on Insects and their Mitigation; Settele and Kühn 2009; Thomas et al., 2009) funded by DLR-BMBF (Germany), NERC and DEFRA (UK), ANR (France), Formas (Sweden), and Swedish EPA (Sweden) through the FP6 BiodivERsA Eranet” as well as by the project “A multitaxa approach to study the impact of climate change on the biodiversity of Italian ecosystems” of the Italian Ministry of Education, University and Research (MIUR). M. Witek was financially supported by grant from Polish National Science Centre (post-doctoral internship-No. DEC-2012/04/S/NZ8/00218).



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Table 1. Number and percentage of nests, and number and percentage of social parasite larvae reared by Myrmica colonies showing single and double infestation. Symbols: Ma. teleius (tel), Ma. nausithous (nau), Ma. alcon (alc), Mi. myrmicae (mic).




Site and ant sp.

No. of infested nests

No. (%) of single infested nests

No. (%) of double infested nests

No. (%) of larvae inside single infested nests

No. (%) of larvae inside double infested nests



















Kraków

My. scabrinodis

32

26 (81%)

6 (19%)

34 (67%)tel,

13 (54%)mic


17 (33%)tel,

11 (46%)mic


Kosyń

My. scabrinodis

My. rubra

12

5


11 (92%)


3 (60%)

1 (8%)


2 (40%)

10 (77%)tel,

3 (60%)mic
9 (14%)tel

3 (23%)tel,

2 (40%)mic
55 (86%)tel,

36 (100%)nau



Caselette

My. scabrinodis

(zone with both Maculinea food plants)


My. scabrinodis (zone with S. officinalis)

17

12




16 (94%)


10 (83%)

1 (6%)


2 (17%)

52 (94.5%)alc,

5(100%)mic

9 (60%)tel,

6 (54.5%)mic

3 (5.5%)alc,

5 (100%)tel

6 (40%)tel,

5 (45.5%)mic

Table 2. Results of GLM analysis comparing the numbers of Ma. teleius specimens found within the nests of each Myrmica species at Kraków and Kosyń (k- dispersion parameter of the negative binomial distribution was 0.725 for Kraków and 0.158 for Kosyń). Significant results in bold. Results showing the mean (± SE ) number of Ma. teleius larvae refer to Myrmica species mentioned in the first column (host species*).



Site

Host species*




Host species

No. of Ma. teleius larvae inside host* nests (mean ± SE)

Likelihood ratio

d.f.

P

Kosyń

My. rubra

vs

My. gallieni

4.57 ± 3.10

6.618

1

0.010




My. gallieni

vs

My. scabrinodis

0.19 ± 0.14

0.000

1

0.984




My. scabrinodis

vs

My. rubra

0.19 ± 0.07

15.142

1

<0.001

























Kraków

My. rubra

vs

My. ruginodis

1.00 ± 0.33

0.237

1

0.627




My. ruginodis

vs

My. scabrinodis

0.63 ± 0.04

0.148

1

0.700




My. scabrinodis

vs

My. rubra

0.73 ± 0.02

0.119

1

0.731



























Figure legends

Figure 1. Comparison of the life cycle of Ma. teleius (inner circle) and Mi. myrmicae (outer circle). Dark grey colour - intensive larval growth of social parasite inside Myrmica colony connected with high exploitation of host colony resources. Mi. myrmicae: II and III instar larvae. Ma. teleius: IV instar larva. Light grey colour – diapause, larvae of social parasite stay inside host nest but slightly use colony resources. Mi. myrmicae: III instar larva. Ma. teleius: IV instar larva. White colour – during this period the social parasite does not use host colony resources. Mi. myrmicae: pupa, adult, egg, I instar larva. Ma. teleius: pupa, adult, egg, I-III instar larvae. Data used for this comparison were published by Witek et al., (2011; 2012).


Figure 2. a) Dendrogram representing the relationship between the hydrocarbon signatures of the three ant species (My. scabrinodis, My. rubra, and My. ruginodis) and the larvae of the four social parasite species found inside these Myrmica host colonies: Ma. alcon (alc), Ma. teleius (tel), Ma. nausithous (nau) and Mi. myrmicae (mic). b) The figure shows mean Bray-Curtis similarities (% ± SE) between the chemical profiles of the host ant species (squares) and their parasites (circles). Overlapping circles indicate the parasite species that were found together in the same colonies.


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