Next Article in Journal
Population Density and Host Preference of the Japanese Pine Sawyer (Monochamus alternatus) in the Qinling–Daba Mountains of China
Previous Article in Journal
Managing Practical Resistance of Lepidopteran Pests to Bt Cotton in China
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

The Pattern of Social Parasitism in Maculinea teleius Butterfly Is Driven by the Size and Spatial Distribution of the Host Ant Nests

Magdalena Witek
Valentina La Morgia
Luca Pietro Casacci
3,* and
Francesca Barbero
Museum and Institute of Zoology, Polish Academy of Science, Wilcza 64, 00-679 Warszawa, Poland
Institute for Environmental Protection and Research (ISPRA), Via Ca’ Fornacetta 9, 40064 Ozzano Emilia, Italy
Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, 10123 Turin, Italy
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Insects 2023, 14(2), 180;
Submission received: 28 December 2022 / Revised: 6 February 2023 / Accepted: 7 February 2023 / Published: 12 February 2023
(This article belongs to the Topic Host–Parasite Interactions)



Simple Summary

Maculinea butterflies are endangered social parasites of Myrmica ants. In late summer, caterpillars abandon their foodplants and wait for a Myrmica worker to retrieve and carry them into the nest. Here the caterpillars spend 11 months consuming the ant brood or being fed by workers; then they pupate early in summer, and in one month the adults emerge. Our study aimed to assess the spatial relationship between nests parasitized by Maculinea teleius and those unparasitized and the factors influencing the parasite presence inside host nests. We searched for Ma. teleius caterpillars in ant nests in autumn, during the initial larval development, and in the following late spring. Unsurprisingly, we found a substantial decrease in the proportion of parasitized nests from autumn to late spring. The biggest Myrmica nests adopted a higher number of parasites, but mid-size nests provided the best trade-off between competition and resource availability, leading to high parasite survival observed in spring. The spatial distribution of parasitized nests in autumn was uniform, while the colonies in which Ma. teleius survived until pupation were grouped. Overall, our results suggest that host colonies’ features and spatial relationships should be considered when trying to preserve these rare butterflies.


The parasitic relationship between Maculinea butterflies and Myrmica ants has been extensively studied but little information is available on the spatial occurrence of Maculinea larvae. We searched for the presence of Maculinea teleius in 211 ant nests at two sites in two crucial phases of its life cycle, i.e., in autumn, during the initial larval development, and in the following late spring, before pupation. We assessed variations in the proportion of infested nests and factors correlated with spatial distributions of parasites in Myrmica colonies. The parasitism rate in autumn was very high (∼50% of infestation rate) but decreased in the following spring. The most important factor explaining parasite occurrence in both seasons was the nest size. Further factors, such as the presence of other parasites, the Myrmica species or the site, concurred to explain the differential survival of Ma. teleius until the final development. Irrespective of the host nest distribution, the parasite distribution changed from even in autumn to clumped in late spring. Our work showed that the survival of Ma. teleius is correlated with colony features but also with the nest spatial distribution, which therefore should be taken into consideration in conservation strategies aiming at preserving these endangered species.

1. Introduction

Many social insects, such as ants, live in colonies representing a forcefully protective environment as well as an abundant source of food. These traits make ant nests suitable to host many arthropods, either occasional visitors or steady guests fully dependent on the colony resources [1,2,3,4]. Obligate social parasites belong to the latter group, and, according to a broad definition, they are intruding arthropods that exploit any resources of an ant colony for some phases of their life cycle [5].
Myrmica Latreille, 1804 (Hymenoptera, Formicidae) ants are hosts to many parasitic ant species, primarily members of the same genus [6,7,8,9,10,11,12,13] but are also known for hosting immature instars of many other insects, such as Maculinea butterflies [14,15,16]. The survival of Maculinea Van Eecke, 1915 (Lepidoptera, Lycaenidae) larvae depends on the presence of their host ant nests but also on a specific food plant [17,18]. In Poland, females of Maculinea teleius Bergsträsser, 1779, the species surveyed in this work, lay their eggs in July-August, specifically on Sanguisorba officinalis Linné, 1753 (Rosales, Rosaceae). After feeding for three weeks on the foodplant, Maculinea larvae fall to the ground, where they are adopted by Myrmica workers thanks to the implementation of deceiving strategies based on multimodal signals [19], both chemical [20] and acoustical [21]. Once inside the host colony, larvae of Ma. teleius display a predatory strategy feeding on the ant brood, usually choosing the largest Myrmica larvae [22].
All Myrmica species that forage in the area beneath Maculinea food plants have the same probability of adopting butterfly larvae. Still, the survival probability of these larvae varies, depending on the adopting Myrmica species [23]. Many recent studies on host ant specificity have shown that Ma. teleius is among the most generalist species of its genus [15,24,25,26,27] and can survive inside nests of all available Myrmica species. Nevertheless, Myrmica scabrinodis Nylander, 1846 is the most common host of Ma. teleius populations in Europe [15].
Ant colony size is another critical factor playing a crucial role in the social parasite’s survival. By studying another Maculinea predatory species, Ma. arion Linné, 1758, Thomas & Wardlaw [22] estimated that Myrmica sabuleti colonies must contain a minimum number of 354 workers to rear one butterfly larva. Therefore, only a few Myrmica nests can support these parasites in nature. Inside host nests, Ma. teleius and Ma. arion larvae are subject to scramble competition because they compete for a finite resource which is equally accessible. Thus, the parasite survival rate drops along with the increase of caterpillar density in the same colony, often leading to only one or two Maculinea predatory larvae surviving until pupation [22].
Although the host and parasite relationship between Maculinea butterflies and Myrmica ants has been extensively studied, little information is available on the spatial pattern of Maculinea larvae occurrences with respect to their host ant nest distribution. In addition, the spatial pattern observed in the autumnal, first phase of adoption and in the post-hibernation phase have never been compared yet. In Ma. teleius, adult females evenly lay eggs on Sanguisorba officinalis and avoid food plants already carrying conspecific eggs [28]. Since S. officinalis is usually very abundant at sites with Ma. teleius [29], at least at the beginning of their larval development (autumn) parasitic larvae inside host colonies are also supposed to show an even distribution. In contrast, the parasite distribution found in late spring is linked to the survival of the parasites, which varies according to colony size, resource supply status and species identity of Myrmica nests [30].
In our study, we investigated factors affecting the rate of infestation of Myrmica nests and the micro-spatial distribution of the infested host colonies. In detail, the main aims of our study were to assess: (i) the spatial distribution of all Myrmica colonies, as well as of those infected by Ma. teleius, (ii) the infestation rate of Myrmica host nests, (iii) the influence of host species, nest size and presence of other competitors, e.g., larvae of other Maculinea species or Microdon myrmicae Schönrogge et al., 2002 (Diptera, Syrphidae) syrphid fly, on the occurrence of Ma. teleius larvae inside Myrmica colonies. We chose to focus our study on the occurrence of Ma. teleius because this parasite uses various Myrmica species as hosts, showing a high infestation rate that provides sufficient data to feed the statistical models. Moreover, the broad spatial distribution of S. officinalis allows for assessing potential variation in the parasite survival patterns from an initial even distribution due to its food plant occurrences.
We assessed spatial patterns of larval distribution within nests at the beginning of autumn, the parasite’s initial colonisation phase, and late spring when fully-grown Maculinea larvae are about to pupate. We expect infestation rates to be higher in autumn than in the following spring because of the high mortality rate faced by overwintering butterfly stages. Our hypothesis is that the colony size is a key factor affecting the presence of Ma. teleius larvae, with larger Myrmica colonies containing more parasitic larvae. Therefore, we envisage differences in Ma. teleius spatial distribution between the two phases of its life cycle, with an even distribution in autumn and a clumped pattern in spring, driven by intra-nest competition.

2. Materials and Methods

2.1. Study Areas

Studies were conducted at two sites: (1) Kosyń, in eastern Poland (51°23′ N/23°34′ E; 161 m a.s.l.) and (2) Kraków, in southern Poland (50°01′ N/19°53′ E; 220 m). Both sites are wet meadows dominated by Molinia Schrank, 1789 (Poales, Poaceae) spp. and are characterised by different communities of social parasites of Myrmica ants: (1) Maculinea teleius, Maculinea nausithous Bergstrasser, 1779 and Microdon myrmicae, in Kosyń; (2) Ma. teleius, Ma. nausithous, Maculinea alcon Denis & Schiffermüller, 1776 and Mi. myrmicae, in Kraków. Sanguisorba officinalis, the food plant of Ma. teleius (and Ma. nausithous), occurs at both study sites, and its density is 16 and 6 plants per m2, respectively, in Kraków and Kosyń. Gentiana pneumonanthe Linné, 1753 (Gentianales, Gentianaceae), the larval food plant of Ma. alcon, is present only in Kraków.
In both populations, adults of Ma. teleius are on the wing between the end of June and the end of August [31].

2.2. Field Survey

Data were collected at the beginning of October (hereafter “autumn”) and again in the middle of June (“late spring”), i.e., in the initial part and at the end of Ma. teleius development inside ant host colonies, respectively. Each area was an irregularly shaped grassland of 0.42 ha in Kosyń and 0.43 ha in Kraków (Figure 1). Within the grassland, S. officinalis was present in sub-areas with homogenous coverage. We surveyed for the presence of Myrmica ants by conducting a scrutiny search, sensu [32], along 2 m-width transects scattered only on the area covered by the food plant Sanguisorba officinalis. Therefore, all examined nests could be potentially infected by Maculinea teleius.
In our studied sites, Myrmica colonies build their nests in tufts of grass, which usually have different chimney sizes. Firstly, after finding the nest, data on ant nest size were collected following the method described by Nash et al. [33]. In brief, the number of Myrmica workers emerging when the nest was first opened (after splitting the grass tuft centre for the first time) were counted, allowing the classification of colonies into small (less than 20 workers), medium (20–100 workers), and large (>100 workers). Later, the nest was open, and all brood chambers were inspected for the presence of social parasite larvae. If necessary, we partially excavated the nest to reach the brood chamber. Thus, we counted Ma. teleius preimaginal instars, used as the dependent variable, and larvae or pupae of other social parasites (i.e., Maculinea spp. and Microdon myrmicae) as explanatory variables. From each ant colony, 10–20 workers were collected and preserved in 70% ethanol. The analytic key of Czechowski et al. [34] was used for ant species, while we used the key by Śliwinska et al. [35] for Maculinea larvae identification. The position of each Myrmica nest was determined by Garmin GPSMAP 60CSx and further recorded on a map. Information on the nest number and the composition of Myrmica ant communities, along with the infestation rates observed at the two study areas, is shown in Table 1.

2.3. Statistical Analyses

Chi-square tests were used to compare the degree of nest infestation between autumn and the following spring, for all studied populations. To analyse nests’ spatial distributions, we first considered the location of each ant nest within a 4 × 4 grid superimposed to the map of the study area grids, irrespectively of the ant species and of the presence/absence of social parasites’ larvae. We determined whether the pattern was consistent with Complete Spatial Randomness (CSR) using Monte Carlo quadrat tests and by calculating the Variance Mean Ratio (VMR) at different spatial scales, multiples of a 4 × 4 m sampling grid superimposed to the map of the study area for the analyses. We preferred quadrat count-based statistics to nearest-neighbour analyses since quadrat counts were more robust to errors in geolocation. Two-sided Monte Carlo tests were performed by generating 999 expected counts, according to a CSR hypothesis and comparing the corresponding Pearson chi-square statistic with the one for the observed point pattern. Secondly, we analysed nests’ association patterns via Monte Carlo tests based on random labelling and join count statistics [36,37]. Join count statistics (J) test whether or not the occurrence of categorical attributes at spatially adjacent sampling locations can be accounted for by randomness alone. To establish adjacency, the spatial neighbourhood of each nest was defined as the subset of the other nests falling within predefined, increasing distances, matching the scales of previous quadrat counts. For all categorical attributes (see further below), we directly performed the calculation of join count statistics, since a simple analysis of departure from CSR would be affected by the spatial distribution of nests. This approach was adopted to (1) detect patterns of association between My. scabrinodis nests (dominant Myrmica species) and those of other, less abundant Myrmica ant species, by calculating the join count statistics for pairs of adjacent My. scabrinodis nests (Jss), pairs of nests of other Myrmica species (Joo) and pairs with one nest of My. scabrinodis and one nest of other Myrmica species (Jso); (2) test the significance of aggregation of big/medium sized nests, by join count statistics focused on the Jbb statistics (pairs of big and medium nests as opposed to small nests); (3) test the spatial association of ant nests with and without social parasites (I - infested nests; E - empty nests, see also further below for details). The observed values of join count statistics were compared with those obtained from random re-labelling (999 replicates) of the ant nests, i.e., nest locations were fixed but labels indicating ant species/nest-size/parasitic infestation were redistributed [38]. To assess possibly positive spatial associations between nests of the same type (i.e., the same ant species/the same size or the same infestation state), we hypothesised that join count statistics should be higher than expected (“greater” hypothesis). The Monte Carlo p-value was thus estimated as: (random values equal to or greater than the observed one + 1)/(random values + 1). As concerns the other join count statistics (e.g., association of nests of different ant species, association of nests with different parasites), we were also interested in assessing possibly negative spatial association (or repulsion). In these cases, we tested the hypothesis that joint count statistics were lower than expected (“less” hypothesis) and the Monte Carlo p-value was estimated as: (random values equal to or less than the observed one + 1)/(random values + 1). The spatial distribution of nests belonging to different size groups was considered, since nest size was of interest for subsequent modelling (see further below). For infested nests, Monte Carlo analyses were performed (a) by grouping all infested nests regardless of the social parasite, (b) separately for Maculinea teleius and (c) to test for positive or negative association between Ma. teleius and larvae of other social parasites. All spatial statistics were calculated separately for each study site and sampling period. We also visually assessed distributions by plotting kernel smoothed probability density maps. These maps were obtained by R [39] adehabitatHR package [40], by estimating the smoothing parameter with the default ad hoc method [41].
The next step was to use several candidate mixed regression models to explain the occurrence of Ma. teleius larvae inside Myrmica colonies. We took “autumn” data collected in the initial part of the parasites’ larval development to reflect the ability of Myrmica colonies to adopt parasitic larvae, whereas data collected in late spring of the following year provided an indication of long-term conditions for larval survival within the nest. Thus, considering the same initial set of explanatory variables, we separately fitted models for autumn and late spring data to investigate possibly different seasonal processes. In particular, we related the presence of Ma. teleius larvae to the following fixed effects (1) Myrmica host ant species—a categorical variable with two levels: My. scabrinodis or other, less abundant, Myrmica species; (2) nest size—a categorical variable with three levels: large, medium, and small nests; (3) study site; (4) presence/absence of other social parasite larvae; (5) interaction between the nest size and presence/absence of other parasites. We verified the lack of relevant correlations between explanatory variables, and we then hypothesised various candidate models including different subsets of explanatory variables. We selected variables and interaction terms on a biological basis rather than evaluating all possible models in an automated selection framework, because the latter can result in selecting a “spurious” best model, and we then compared the candidate models in terms of AIC values [42], finally taking into account the regression coefficients obtained by averaging models with ΔAIC < 2. For model checking, given the potential problems arising from spatial autocorrelation of data, we fitted variograms to the residuals of our models, to check whether spatial autocorrelation was likely to impact the analyses [43], or whether to include an appropriate spatial correlation structure [44]. Statistical analyses were performed on R 4.2.2 [39].

3. Results

3.1. Infestation Rates

In Kraków, Maculinea teleius was the most abundant social parasite, both considering the number of infested nests as well as the number of larvae found inside Myrmica nests (Table 1). In Kosyń, Ma. teleius infested the highest number of Myrmica nests in both seasons compared to other social parasites but, in autumn, the highest number of larvae found inside the host nests belonged to Mi. myrmicae (Table 1). Only a small number of nests infested by Ma. nausithous and/or Ma. alcon were found (Table 1). In Kraków, 51% (n = 23) of Myrmica colonies were infested by larvae of Ma. teleius in autumn, and 43% (n = 21) in the late spring. For Kosyń the percentage of colonies infested by Ma. teleius was 40% (n = 23) and 15% (n = 9) in autumn and spring, respectively. The proportion of infested nests with first stages of larval development was significantly different than the proportion of nests parasitised by late instars found in the next spring in Kosyń (χ21 = 4.53, p = 0.03), whereas no difference was observed at the Kraków site (χ21 = 0.090, p = 0.765).
Irrespectively of the species, the estimated density of Myrmica nests was 0.2 nests/m2 in Kraków and 0.3 nests/m2 in Kosyń. A few Myrmica species were present in Kraków and Kosyń, but My. scabrinodis was the most abundant at both sites. In Kraków, the latter ant species was exploited by Ma. teleius, Ma. alcon and Mi. myrmicae and in both sampling periods, more than 60% of My. scabrinodis nests were infested (n = 20 in autumn, n = 22 in late spring). The second most abundant species was Myrmica ruginodis Nylander, 1846 (Table 1), whose nests (70% in autumn, n = 7, and 53% in late spring, n = 8) were infested only by Ma. teleius. In Kosyń, My. scabrinodis nests were infested by Ma. teleius and Mi. myrmicae with a significantly higher proportion of colonies (χ21 = 8.81, p = 0.003) infested in autumn (71.1%, n = 32) than in spring (17.1%, n = 7). A similar pattern was observed for nests of Myrmica rubra Linné, 1758, which were infested by larvae of Ma. teleius, Ma. nausithous and Mi. myrmicae and whose infestation rate was higher in autumn (90%, n = 9) than in the following spring (50%, n = 5) (χ21 = 0.23, p = 0.026).

3.2. Spatial Patterns

The VMRs calculated for each study site and season were always larger than 1, suggesting that the spatial distribution of Myrmica nests was clumped. Significant departures from CSR increased with quadrat size (e.g., in Kosyń in late spring, for quadrat width d = 12 m, VMR = 6.73, p = 0.002, for quadrat width d = 32, VMR = 8.69, p = 0.006). Because of the dominance of My. scabrinodis nests at all sites and periods, we performed the association analysis of My. scabrinodis with other Myrmica ants at both sites. In late spring, we observed a significant positive association of My. scabrinodis nests (e.g., at spatial distance d = 12 m, Jss Kraków = 260, p = 0.020; Jss Kosyń = 488, p = 0.009), and a significantly negative association of My. scabrinodis nests with colonies of other Myrmica species (d = 12 m, Jso Kraków = 74, p = 0.016; Jso Kosyń = 156, p = 0.008). These association patterns were detected at all scales in Kraków, and at small and intermediate scales (d < 20 m) in Kosyń.
Grouping all infested nests, no significant associations of infested or non-infested (hereafter called parasite-free nests) nests were detected in autumn for both Kraków and Kosyń sites (Figure S1a,b). In late spring, positive associations were detected at almost all scales for Kosyń (e.g., d = 16 m, JII = 54, p = 0.036; Figure 2a and Figure S1c,d).
A similar pattern emerged when we considered only the locations of Ma. teleius: a significant positive association of Ma. teleius larvae was detected at almost all scales in Kosyń (e.g., d = 20 m, JII Ma. teleius = 44, p = 0.025; Figure 2b, Figure 3b and Figure S2). In Kraków, we also detected an increase in the values of the JII Ma.teleius statistics in June (Figure 3a) with respect to October (Figure S2a,b), albeit the differences from expected values were not statistically significant. No patterns were detected when we considered only infested nests and we tested for segregation of Ma. teleius against all other larvae (Figure S3).
As concerns join count statistics for ant-colony size, the main result was that, in late spring, in Kosyń we observed significant segregation of big/medium nests (grouped together) with respect to the small ones, especially at intermediate and large scales (e.g., d = 20 m, Jsb = 44, p = 0.025; Figure 4).

3.3. Factors Correlated with the Presence of Ma. teleius and Mi. myrmicae Larvae Inside Myrmica Nests

For both seasons and parasite species we selected a base model including all explanatory variables as fixed effects (Myrmica species, study site, presence of other parasite larvae, colony size, interaction between colony size and the presence of other parasites, as well as interaction between ant species and the presence of other parasites). We then fitted candidate models including subsets of the explanatory variables, as shown in Table 2. According to information criteria, the most appropriate models (∆AIC < 2) differed among study sites and parasite species. For Ma. teleius, colony size was the only variable included in the model generating the lowest AIC in autumn and the estimated regression coefficient of big nests with respect to the small ones was statistically significant (β = 1.731 ± 0.719 SE, p = 0.016; Figure 5a). Equivalent models (in terms of AIC) also included site and ant species as explanatory variables (Table 2), but according to model averaging, colony size remained the most important variable (average βNest Size: big vs. small = 1.721 ± 0.723 SE, p = 0.019; average βNest Size: medium vs. small = 1.01 ± 0.715 SE, p = 0.163). At the end of larval development, variables involved in explaining the presence of Ma. teleius larvae included colony size, study site, ant species, presence of other parasites and its interaction with the ant species. According to the model with the lowest AIC, significant regression coefficients were detected for the nest size, especially for medium-sized nests (β = 1.428 ± 0.677 SE, p = 0.035; Figure 5b), compared to the small ones. When we compared big and small nests, the regression coefficient was β = 1.237 ± 0.845 SE (p = 0.143). The presence of Ma. teleius differed (β = −1.695 ± 0.562 SE, p = 0.003) between the Kosyń and the Kraków site. Accordingly, the colony size and study site were identified as the most important variables by model averaging (average βNest Size: big vs. small = 1.266 ± 0.865 SE, p = 0.148; average βNest Size: medium vs. small = 1.416 ± 0.696 SE, p = 0.044; average βSite: Kosyń vs. Kraków = −1.613 ± 0.561 SE, p = 0.004).

4. Discussion

Results presented in this paper indicate that several factors can affect the presence of Ma. teleius inside Myrmica nests but the most important is the colony size, which is pivotal both during the first phase of nest colonisation, in autumn, and for the parasite survival after the overwintering period, in late spring.
In detail, big colonies are infested more frequently by Ma. teleius in autumn and medium colonies in the spring. Indeed, big Myrmica colonies may adopt more parasite larvae since they include larger numbers of foraging workers (e.g., [45]), thus increasing the probability of finding Maculinea larvae within this kind of nests. It is also possible that bigger nests have higher within-colony genetic variation, perhaps linked to the presence of many queens, and are consequently more prone to social parasitism, thus adopting more larvae [45,46]. The finding that, at the end of their development, Ma. teleius larvae are found more often inside medium-sized nests suggests that the parasite survival is, on the one hand, dependent on food resources, still abundant in medium colonies [47] but, on the other side, can be affected by larval scramble competition [22]. The very high infestation rate of big colonies in autumn could lead to extremely high competition among Ma. teleius larvae and many (if not all) of them would not survive until the end of their development [22]. Therefore, medium-sized colonies can provide the optimal balance between the availability of resources and the level of scramble competition for the butterfly parasite to achieve the best survival.
In addition to the size, other colony features are correlated to the parasite occurrence, but their contribution is greater in explaining the larval survival in late spring than their initial infestation in autumn. The lack of a significant influence of Myrmica species on the presence of Ma. teleius larvae at the beginning of the butterfly cycle is consistent with previous studies showing that Maculinea caterpillars have the same probability of being adopted by any Myrmica species that forage in the surroundings of the food plants [23]. In contrast, we found that the species of Myrmica can partially explain Ma. teleius occurrence in late spring (Table 2). Still, this is not the most important variable explaining the parasite’s survival and it proves to be crucial when we consider its interaction with the presence of other parasites. This finding is not surprising as Ma. teleius is a rather generalist species, able to exploit several Myrmica species as hosts [15,24,26,27] while Mi. myrmicae and Ma. alcon are specialised to exploit only few or one species of Myrmica ants locally [15,23,48], primarily Myrmica scabrinodis in these two Polish populations. However, these two variables, i.e., Myrmica species and the other parasite occurrences, differ between the two sites, contributing to clarify why the “site” is another crucial variable explaining the survival of Ma. teleius in late spring. In Kraków three Myrmica species, i.e., My. scabrinodis, My. ruginodis and My. rubra, are present and used as hosts by Maculinea butterflies. My. rubra is very rare (only 5% in autumn and 2% in spring, among all Myrmica nests), but My. scabrinodis and My. ruginodis are abundant enough to compare their infestation rates between the two sampling events. Our results show that a similar proportion of My. scabrinodis and My. ruginodis nests is infested in autumn and in the end of the parasite development, thereby suggesting that Ma. teleius survival is high in both these ant species. This finding could indicate that in Kraków Ma. teleius population is truly generalist or that environmental conditions are particularly suitable for Myrmica colonies that are more prone to rear the parasite (see further below). In Kosyń, in contrast, the most abundant Myrmica species are My. scabrinodis and My. rubra with the former showing a substantial drop in the rate of parasitism by Ma. teleius from 42% in autumn to 7% in late spring. The high survival in the nest of My. rubra and the elevated mortality in the nests of My. scabrinodis in Kosyń explain the reason why “Myrmica species” is listed as a factor in the best models. Such a high survival rate of both Ma. teleius and Ma. nausithous larvae inside the nests of My. rubra can be explained by the highest similarities of chemical profiles between social parasites and this host ant species [49]. Our previous studies performed on the same populations showed that Ma. teleius cuticular hydrocarbon profile was 50% similar to that of My. rubra and only 38% similar to My. scabrinodis, which could suggest higher host specificity of Ma. teleius larvae toward My. rubra ants.
More in general, the occurrence of Ma. teleius in the host nest at the beginning and at the end of the butterfly development differ between the two sites, irrespective of the Myrmica species considered. Overall, the pressure of Ma. teleius we estimated in our work is very high since about half of the investigated ant colonies are infested in autumn (51% in Kraków and 43% in Kosyń). This scenario greatly changes at the end of the parasite development in Kosyń, where only a small proportion (15%) of host nests is still infested. Surprisingly, in Kraków, the proportion of nests with Ma. teleius does not differ between autumn and the following late spring (40%). While the proportion of nests parasitised by Maculinea teleius late instars in Kosyń is consistent with data gathered in other European populations [50], the parasitism rate (40%) of the Kraków population is particularly high also compared to previous observations performed in the same site (in 2003 and 2004, 11% and 12% of nests were infested by late Ma. teleius instars [27]). This result can be due to particularly benevolent conditions leading to well-fed colonies, which can support a higher number of parasites [22] or natural fluctuations in population size, frequently observed in Maculinea butterflies [51]. In addition, a study carried on in the same area showed that the probability of occurrence of Maculinea larvae and pupae in Myrmica nests was significantly higher in temporarily inundated meadows [52] than in control meadows. Unfortunately, we did not measure soil humidity systematically but, when we performed our field survey, meadows in Kraków were inundated. Even though how the presence of water can affect the ant colony performance is not straightforward, we tentatively concur with Kajzer-Bonk et al. [52] in pointing out that soil humidity may be one of the predictors for the presence of Ma. teleius in a mosaic landscape [53], see also 32 for the effect of soil moisture and temperature on ant niche selection.
Conversely, the spatial analysis is consistent at the two sites. If we consider all the Myrmica species found in a site, their nest distribution both in Kraków and Kosyń is clumped, even at small spatial scales. The same pattern is found when we compare the nest distribution of the most abundant species, My. scabrinodis, with other Myrmica species. My. scabrinodis nests have clumped distributions and are separated in space from nests belonging to My. rubra, My. ruginodis or Myrmica gallienii Bondroit, 1920. This kind of nest distribution suggests a polydomous structure for My. scabrinodis populations [54] but can also reflect distinct microclimatic niche preferences of each Myrmica species (e.g., [30,55]). Despite the fact that Myrmica colonies are clumped, in autumn, the distribution of Ma. teleius infested nests is even and does not show any spatial aggregation, suggesting that the infestation probability [23] is equal for all Myrmica nests and did not depend on their location. This result is in line with the expectation that early Ma. teleius distribution is based on the female oviposition pattern [28]. The most interesting finding is that in the course of its development we observe a variation in the spatial occurrences of the parasite, suggesting that the survival of Ma. teleius is also influenced by the position of the parasitised nest with respect to other Myrmica colonies. Although this result is significantly higher in Kosyń, at both sites we estimate an increase in the positive association of infested nests, leading to a change from an even (in autumn) to a clumped distribution of parasitised nests in late spring. This spatial heterogeneity, with patches where social parasite occurrence is higher than in others, is also correlated to the finding that big and medium-sized nests had clumped distributions. In other words, nests are grouped in habitat patches where conditions are apparently suitable to allow Myrmica colonies to grow to larger sizes, thereby generating more resources and better conditions for parasitic larval development. We should also mention that Myrmica colonies can constitutively differ in their susceptibility to infestation and nests more prone to social parasites may be grouped together as they can represent polydomous structures that promote social parasitism [1]. Overall, our results concur to support the general idea proposed by Hölldobler and Wilson [1] stating that hotspots of social parasites do not arise by chance and are promoted by several, peculiar ecological factors.

5. Conclusions

Our work indicates that the survival rate of obligate social parasites such as Ma. teleius depends on several ecological factors, among which the host ant colony size proved to be one of the most important. Of course, the colony size itself is affected by several factors such as the particular microclimatic conditions where the nest is found. These small-scale characteristics could eventually also explain the spatial distribution of these “optimal” (from the parasite’s point of view) nests [55]. Therefore, while the parasite occurrence in autumn is mainly driven by the female egg-laying behaviour and uniform host plant spreading, the survival of Ma. teleius late instars is correlated with many other variables related to the colony or population structure of the Myrmica ants [5]. Finally, the differences observed between the two Polish sites reveal that even though general patterns and paradigms of social parasitism hold across populations, local parasite adaptations to their ant hosts occur and temporal variation in environmental conditions (e.g., soil humidity) could also deeply influence the survival of these rare and endangered parasite species. Hence, conservation strategies implemented to preserve populations of Ma. teleius should also consider diverse factors affecting both the colony features but also to the nest spatial distribution.

Supplementary Materials

The following supporting information can be downloaded at:, Figure S1: Observed and expected values of the JII statistics based on empty and infested nests, regardless of parasite species; Figure S2: Observed and expected values of join count statistics calculated for nests infested by Ma. teleius, relative to empty nests; Figure S3: Observed and expected values of join count statistics calculated for nests infested by Ma. teleius and/or other parasites.

Author Contributions

Conceptualization, M.W., L.P.C. and F.B.; methodology, M.W., V.L.M., L.P.C. and F.B.; software, V.L.M.; validation, M.W., V.L.M. and F.B.; formal analysis, V.L.M.; investigation, M.W., L.P.C. and F.B.; resources, M.W., L.P.C. and F.B.; data curation, M.W., V.L.M. and F.B.; writing—original draft preparation, M.W., V.L.M. and F.B.; writing—review and editing, M.W., V.L.M., L.P.C. and F.B.; supervision, M.W., V.L.M., L.P.C. and F.B.; project administration, M.W., L.P.C. and F.B.; funding acquisition, M.W., L.P.C. and F.B. All authors have read and agreed to the published version of the manuscript.


This research was funded within the project CLIMIT (Climate Change Impacts on Insects and their Mitigation) 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). MW was funded by Polish National Science Centre (NCN) grant 2018/31/B/NZ8/03476.

Data Availability Statement

Data are available upon request.


We would like to thank Woyciechowski M., Sielezniew M., Amirowicz A., Rożej E., Kajzer J., and Mielczarek P. for their help during fieldwork in Kraków and Kosyń.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Hölldobler, B.E.; Wilson, E.O. The Ants; The Belknap Press of Harvard University Press: Cambridge, MA, USA, 1990. [Google Scholar]
  2. Pierce, N.E.; Dankowicz, E. Behavioral, ecological and evolutionary mechanisms underlying caterpillar-ant symbioses. Curr. Opin. Insect. Sci. 2022, 52, 100898. [Google Scholar] [CrossRef] [PubMed]
  3. New, T.R. Mutualisms and Insect Conservation; Springer: Cham, Switzerland, 2017. [Google Scholar]
  4. Hölldobler, B.; Kwapich, C.L. The Guests of Ants: How Myrmecophiles Interact with Their Hosts; Harvard University Press: Cambridge, MA, USA, 2022. [Google Scholar]
  5. Thomas, J.A.; Schönrogge, K.; Elmes, G.W. Specializations and host associations of social parasites of ants. In Insect Evolutionary Ecology; Fellowes, M.D.E., Holloway, G.J., Rolff, J., Eds.; Royal Entomological Society: London, UK, 2005; pp. 475–514. [Google Scholar]
  6. Radchenko, A.G.; Elmes, G.W. Myrmica (Hymenoptera: Formicidae) Ants of the Old World; Fauna Mundi 3; Natura Optima Dux Foundation: Warsaw, Poland, 2010; Volume 6, ISBN 9788393077311. [Google Scholar]
  7. Buschinger, A. Social parasitism among ants: A review (Hymenoptera: Formicidae). Myrmecol. News 2009, 12, 219–235. [Google Scholar]
  8. Bharti, H. Myrmica nefaria sp.n. (Hymenoptera: Formicidae)—A new social parasite from Himalaya. Myrmecol. News 2012, 16, 149–156. [Google Scholar]
  9. Bharti, H.; Radchenko, A.; Sasi, S. Socially-parasitic Myrmica species (Hymenoptera, Formicidae) of Himalaya, with the description of a new species. ZooKeys 2016, 605, 113. [Google Scholar] [CrossRef] [PubMed]
  10. Casacci, L.P.; Barbero, F.; Ślipiński, P.; Witek, M. The inquiline ant Myrmica karavajevi uses both chemical and vibroacoustic deception mechanisms to integrate into its host colonies. Biology 2021, 10, 654. [Google Scholar] [CrossRef] [PubMed]
  11. Kutter, H. Über die morphologischen Beziehungen der Gattung Myrmica zu ihren Satellitengenera Sifolinia Em., Symbiomyrma Arnoldi und Sommimyrma Menozzi. Mitt. Schweiz. entomol. Ges. 1973, 46, 253–268. [Google Scholar]
  12. Radchenko, A.G.; Elmes, G.W. A taxonomic revision of the socially parasitic Myrmica ants (Hymenoptera: Formicidae) of the Palaearctic region. Ann. Zool. 2003, 53, 217–243. [Google Scholar]
  13. Jansen, G.; Savolainen, R.; Vepsäläinen, K. Phylogeny, divergence-time estimation, biogeography and social parasite-host relationships of the Holarctic ant genus Myrmica (Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 2010, 56, 294–304. [Google Scholar] [CrossRef]
  14. Witek, M.; Barbero, F.; Markó, B. Myrmica ants host highly diverse parasitic communities: From social parasites to microbes. Insectes Soc. 2014, 61, 307–323. [Google Scholar] [CrossRef]
  15. Tartally, A.; Thomas, J.A.; Anton, C.; Balletto, E.; Barbero, F.; Bonelli, S.; Bräu, M.; Casacci, L.P.; Csősz, S.; Czekes, Z.; et al. Patterns of host use by brood parasitic Maculinea butterflies across Europe. Philos. Trans. R Soc. B Biol. Sci. 2019, 374, 20180202. [Google Scholar] [CrossRef]
  16. Thomas, J.A.; Settele, J. Butterfly mimics of ants. Nature 2004, 432, 283–284. [Google Scholar] [CrossRef] [PubMed]
  17. Thomas, J.A. Why did the large blue become extinct in Britain? Oryx 1980, 15, 243–247. [Google Scholar] [CrossRef]
  18. Thomas, J.A. The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In Ecology and Conservation of Butterflies; Pullin, A.S., Ed.; Chapman and Hall: London, UK, 1995; pp. 180–197. [Google Scholar]
  19. Casacci, L.P.; Bonelli, S.; Balletto, E.; Barbero, F. Multimodal signaling in myrmecophilous butterflies. Front. Ecol. Evol. 2019, 7, 454. [Google Scholar] [CrossRef]
  20. Elmes, G.W.; Akino, T.; Thomas, J.A.; Clarke, R.T.; Knapp, J.J. Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (Large Blue) butterflies. Oecologia 2002, 130, 525–535. [Google Scholar] [CrossRef] [PubMed]
  21. Schönrogge, K.; Barbero, F.; Casacci, L.P.; Settele, J.; Thomas, J.A. Acoustic communication within ant societies and its mimicry by mutualistic and socially parasitic myrmecophiles. Anim. Behav. 2017, 134, 249–256. [Google Scholar] [CrossRef]
  22. Thomas, J.A.; Wardlaw, J.C. The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. Oecologia 1992, 91, 101–109. [Google Scholar] [CrossRef]
  23. Thomas, J.A.; Elmes, G.W. Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. Ecol. Entomol. 1998, 23, 457–464. [Google Scholar] [CrossRef]
  24. Stankiewicz, A.; Sielezniew, M. Host specificity of Maculinea teleius Bgstr. and M. nausithous Bgstr. (Lepidoptera: Lycaenidae). The new sight. Ann. Zool. 2022, 52, 403–408. [Google Scholar]
  25. Woyciechowski, M.; Slowik, J.; Muehlenberg, M. Hosts of the butterfly, Maculinea teleius, among Myrmica ants in Northern Mongolia (Lepidoptera: Lycaenidae; Hymenoptera: Formicidae). Sociobiology 2006, 48, 493–502. [Google Scholar]
  26. Tartally, A.; Varga, Z. Host ant use of Maculinea teleius in the Carpathian Basin (Lepidoptera: Lycaenidae). Acta Zool. Acad. Sci. Hung. 2008, 54, 257–268. [Google Scholar]
  27. Witek, M.; Nowicki, P.; Sliwinska, E.B.; Skórka, P.; Settele, J.; Schönrogge, K.; Woyciechowski, M. Local host ant specificity of Phengaris (Maculinea) teleius butterfly, an obligatory social parasite of Myrmica ants. Ecol. Entomol. 2010, 35, 557–564. [Google Scholar] [CrossRef]
  28. Sielezniew, M.; Stankiewicz-Fiedurek, A.M. Behavioural evidence for a putative oviposition-deterring pheromone in the butterfly, Phengaris (Maculinea) teleius (Lepidoptera: Lycaenidae). Eur. J. Entomol. 2013, 110, 71–80. [Google Scholar] [CrossRef]
  29. Wynhoff, I.; Grutters, M.; Van Langevelde, F. Looking for the ants: Selection of oviposition sites by two myrmecophilous butterfly species. Anim. Biol. 2008, 58, 371–388. [Google Scholar] [CrossRef]
  30. Casacci, L.P.; Schönrogge, K.; Thomas, J.A.; Balletto, E.; Bonelli, S.; Barbero, F. Host specificity pattern and chemical deception in a social parasite of ants. Sci. Rep. 2019, 9, 1619. [Google Scholar] [CrossRef]
  31. Nowicki, P.; Witek, M.; Skórka, P.; Settele, J.; Woyciechowski, M. Population ecology of the endangered butterflies Maculinea teleius and M. nausithous and the implications for conservation. Popul. Ecol. 2005, 47, 193–202. [Google Scholar] [CrossRef]
  32. Seifert, B. The ecology of Central European non-arboreal ants—37 years of a broad-spectrum analysis under permanent taxonomic control. Soil Org. 2017, 89, 1–67. [Google Scholar]
  33. Nash, D.R.; Als, T.D.; Maile, R.; Jones, G.R.; Boomsma, J.J. A mosaic of chemical coevolution in a large blue butterfly. Science 2008, 319, 88–90. [Google Scholar] [CrossRef]
  34. Czechowski, W.; Radchenko, A.; Czechowska, W.; Vepsäläinen, K. The Ants of Poland with Reference to the Myrmecofauna of Europe; Fauna Poloniae (New Series); Natura optima dux Foundation: Warszawa, Poland, 2012; Volume 4, ISBN 978-83-930773-4-2. [Google Scholar]
  35. Śliwińska, E.B.; Nowicki, P.; Nash, D.R.; Witek, M.; Settele, J.; Woyciechowski, M. Morphology of caterpillars and pupae of European Maculinea species (Lepidoptera: Lycaenidae) with an identification Table. Entomol. Fenn. 2006, 17, 351–358. [Google Scholar] [CrossRef]
  36. Moran, P.A.P. The interpretation of statistical maps. J. R. Stat. Soc. Ser. B Methodol. 1948, 10, 243–251. [Google Scholar] [CrossRef]
  37. Cliff, A.D.; Ord, J.K. Spatial Processes: Models and Applications; Pion: London, UK, 1981. [Google Scholar]
  38. Fortin, M.J.; Dale, M. Spatial Analysis. A Guide for Ecologists; Cambridge University Press: Cambridge, UK, 2005. [Google Scholar]
  39. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2022. [Google Scholar]
  40. Calenge, C. The package adehabitat for the R software: A tool for the analysis of space and habitat use by animals. Ecol. Model. 2006, 197, 516–519. [Google Scholar] [CrossRef]
  41. Worton, B.J. Kernel methods for estimating the utilization distribution in home-range studies. Ecology 1989, 70, 164–168. [Google Scholar] [CrossRef]
  42. Burnham, K.P.; Anderson, D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach; Springer: New York, NY, USA, 2002. [Google Scholar]
  43. Dormann, C.F.; McPherson, J.M.; Araújo, M.B.; Bivand, R.; Bollinger, J.; Carl, G.; Davies, R.G.; Hirzel, A.; Jetz, W.; Kissling, W.D.; et al. Methods to account for spatial autocorrelation in the analysis of species distributional data: A review. Ecography 2007, 30, 609–628. [Google Scholar] [CrossRef]
  44. Zuur, A.F.; Ieno, E.N.; Walker, N.J.; Saveliev, A.A.; Smith, G.M. Mixed Effects Models and Extensions in Ecology with R.; Springer: New York, NY, USA, 2009. [Google Scholar]
  45. Maák, I.; Camera, J.; Casacci, L.P.; Barbero, F.; Trigos-Peral, G.; Ślipiński, P.; Bonelli, S.; Zaccagno, M.; Witek, M. The influence of colony traits on the collective behaviour of Myrmica scabrinodis ants. Insect Conserv. Diver. 2019, 12, 481–491. [Google Scholar] [CrossRef]
  46. Gardner, M.G.; Schönrogge, K.; Elmes, G.W.; Thomas, J.A. Increased genetic diversity as a defence against parasites is undermined by social parasites: Microdon mutabilis hoverflies infesting Formica lemani ant colonies. Proc. R. Soc. B. 2007, 274, 103–110. [Google Scholar] [CrossRef] [PubMed]
  47. Elmes, G.W. Temporal variation in colony populations of the ant Myrmica sulcinodis. II. Sexual production and sex ratios. J. Anim. Ecol. 1987, 56, 573–583. [Google Scholar] [CrossRef]
  48. Thomas, J.A.; Elmes, G.W.; Wardlaw, J.C. Contest competition among Maculinea rebeli butterfly larvae in ant nests. Ecol. Entomol. 1993, 18, 73–76. [Google Scholar] [CrossRef]
  49. Witek, M.; Casacci, L.P.; Barbero, F.; Patricelli, D.; Sala, M.; Bossi, S.; Maffei, M.; Woyciechowski, M.; Balletto, E.; Bonelli, S. Interspecific relationships in co-occurring populations of social parasites and their host ants. Biol. J. Linn. Soc. 2013, 109, 699–709. [Google Scholar] [CrossRef]
  50. Witek, M.; Śliwińska, E.B.; Skórka, P.; Nowicki, P.; Wantuch, M.; Vrabec, V.; Settele, J.; Woyciechowski, M. Host ant specificity of Large Blue butterflies Phengaris (Maculinea) (Lepidoptera: Lycaenidae) inhabiting humid grasslands in East-Central Europe. Eur. J. Entomol. 2008, 105, 871–877. [Google Scholar] [CrossRef]
  51. Nowicki, P.; Bonelli, S.; Barbero, F.; Balletto, E. Relative importance of density-dependent regulation and environmental stochasticity for butterfly population dynamics. Oecologia 2009, 161, 227–239. [Google Scholar] [CrossRef]
  52. Kajzer-Bonk, J.; Nowicki, P.; Bonk, M.; Skórka, P.; Witek, M.; Woyciechowski, M. Local populations of endangered Maculinea (Maculinea) butterflies are flood resistant. J. Insect Conserv. 2013, 17, 1105–1112. [Google Scholar] [CrossRef]
  53. Batáry, P.; Örvössy, N.; Körösi, Á.; Vályinagy, M.; Peregovits, L. Microhabitat preferences of Maculinea teleius (Lepidoptera: Lycaenidae) in a mosaic landscape. Eur. J. Entomol. 2007, 104, 731–736. [Google Scholar] [CrossRef]
  54. Pedersen, J.S.; Boomsma, J.J. Genetic analysis of colony structure in polydomous and polygynous ant populations. Biol. J. Linn. Soc. 1999, 66, 115–144. [Google Scholar] [CrossRef]
  55. Elmes, G.W.; Thomas, J.A.; Wardlaw, J.C.; Hochberg, M.E.; Clark, R.T.; Simcox, D.J. The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies. J. Insect Conserv. 1998, 2, 67–78. [Google Scholar] [CrossRef]
Figure 1. Distribution of infested (black dots) and non-infested (white dots) Myrmica nests in Kraków during (a) autumn and (b) late spring and in Kosyń during (c) autumn and (d) late spring. The Kernel-smoothed probability density of larvae is shown in the background (colour shades).
Figure 1. Distribution of infested (black dots) and non-infested (white dots) Myrmica nests in Kraków during (a) autumn and (b) late spring and in Kosyń during (c) autumn and (d) late spring. The Kernel-smoothed probability density of larvae is shown in the background (colour shades).
Insects 14 00180 g001
Figure 2. Observed and expected join count values (sum across nests) at different spatial distances (with standard deviation, SD, for expected values) in Kosyń in spring. The plots show the significance of the aggregation of infected nests by considering all parasites (JII, panel (a)) or only Ma. teleius (JII Ma. teleius, panel (b)). For positive spatial association, observed values must be significantly larger than expected.
Figure 2. Observed and expected join count values (sum across nests) at different spatial distances (with standard deviation, SD, for expected values) in Kosyń in spring. The plots show the significance of the aggregation of infected nests by considering all parasites (JII, panel (a)) or only Ma. teleius (JII Ma. teleius, panel (b)). For positive spatial association, observed values must be significantly larger than expected.
Insects 14 00180 g002
Figure 3. Kernel-smoothed density of Myrmica nests infested by Ma. teleius larvae, with superimposed locations of Ma. teleius larvae, in Kraków (a), or Kosyń (b), at the end of larval development.
Figure 3. Kernel-smoothed density of Myrmica nests infested by Ma. teleius larvae, with superimposed locations of Ma. teleius larvae, in Kraków (a), or Kosyń (b), at the end of larval development.
Insects 14 00180 g003
Figure 4. Kernel-smoothed density of large/medium Myrmica colonies at the end of larval development, in Kosyń (a). Panel (b) shows the significance of the segregation (join count statistics, Jsb) between big-medium nests (grouped together) and small nests. In case of significant segregation, observed values must be smaller than expected.
Figure 4. Kernel-smoothed density of large/medium Myrmica colonies at the end of larval development, in Kosyń (a). Panel (b) shows the significance of the segregation (join count statistics, Jsb) between big-medium nests (grouped together) and small nests. In case of significant segregation, observed values must be smaller than expected.
Insects 14 00180 g004
Figure 5. Occurrence of Ma. teleius larvae in nests of different size in (a) autumn, and in (b) spring.
Figure 5. Occurrence of Ma. teleius larvae in nests of different size in (a) autumn, and in (b) spring.
Insects 14 00180 g005
Table 1. Information on Myrmica host colonies and their social parasites in two sampled populations. Symbols: T—Maculinea teleius, N—Maculinea nausithous, A—Maculinea alcon, M—Microdon myrmicae. Some nests with double infestation were also observed.
Table 1. Information on Myrmica host colonies and their social parasites in two sampled populations. Symbols: T—Maculinea teleius, N—Maculinea nausithous, A—Maculinea alcon, M—Microdon myrmicae. Some nests with double infestation were also observed.
SiteAnt SpeciesNo. and (%) of Nests No. of Infested Nests and (Number of Larvae)
AutumnLate SpringAutumn Late Spring
KosyńMy. scabrinodis45 (79%)41 (68%)19T (48), 13M (61) 4T (6), 3M (4)
My. rubra10 (18%)10 (15%)3T (9), 3N (6), 3M (15)3T (62), 2N (36)
My. gallienii2 (3%)9 (17%)1T (3) 2T (3), 1N (1)
KrakówMy. scabrinodis33 (73%)33 (67%)15T (49), 2A (7), 3M (5) 12T (24), 1A (6), 9M (22)
My. ruginodis10 (22%)15 (31%)7T (17) 8T (15)
My. rubra2 (5%)1 (2%)1T (3), 1N (1) 1T (1)
Table 2. AIC values for models with different fixed structures fitted for the two study seasons. The base models relate the presence/absence of Ma. teleius larvae (dependent variable) to all explanatory variables included as fixed effects. Models selected according to information criteria (∆AIC < 2) are in bold.
Table 2. AIC values for models with different fixed structures fitted for the two study seasons. The base models relate the presence/absence of Ma. teleius larvae (dependent variable) to all explanatory variables included as fixed effects. Models selected according to information criteria (∆AIC < 2) are in bold.
Ma. teleius Presence
Model StructureAutumnLate Spring
Ant species × Other parasites + Site + Other parasites × Nest size146.1109.7
Ant species × Other parasites + Site + Nest size145.5108.0
Ant species + Site + Nest size × Other parasites144.2110.1
Ant species + Other parasites + Nest size + Site143.5108.9
Ant species × Other parasites + Nest size × Other parasites145.3117.5
Ant species + Nest size × Other parasites143.3116.6
Nest size + Site + Ant species142.1115.8
Nest size + Site140.2116.0
Nest size + Ant species141.0125.7
Nest size + Site + Other parasites141.6110.9
Ant species × Other parasites146.6118.2
Nest size × Other parasites141.4119.1
Nest size139.0126.0
Ant species144.1128.4
Other parasites143.8122.0
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Witek, M.; La Morgia, V.; Casacci, L.P.; Barbero, F. The Pattern of Social Parasitism in Maculinea teleius Butterfly Is Driven by the Size and Spatial Distribution of the Host Ant Nests. Insects 2023, 14, 180.

AMA Style

Witek M, La Morgia V, Casacci LP, Barbero F. The Pattern of Social Parasitism in Maculinea teleius Butterfly Is Driven by the Size and Spatial Distribution of the Host Ant Nests. Insects. 2023; 14(2):180.

Chicago/Turabian Style

Witek, Magdalena, Valentina La Morgia, Luca Pietro Casacci, and Francesca Barbero. 2023. "The Pattern of Social Parasitism in Maculinea teleius Butterfly Is Driven by the Size and Spatial Distribution of the Host Ant Nests" Insects 14, no. 2: 180.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop