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We thus used this model to obtain the estimates of daily numbers of males and females as well as their seasonal population sizes. Subsequently, we estimated the total population size as the sum of the male and female population sizes. Besides, we calculated the temporal fragmentation index, i. In late June and early July we searched for Myrmica ants in those patches in a radius of 1 m from plants, i.
All nests found were very carefully opened and examined for the presence of P. It is known that full-grown larvae are carried by workers to upper chambers during the day and that pupation takes place there as well [ 40 ], therefore there was no necessity for the excavation and destruction of colonies. For conservational reasons the sensitivity of an isolated population we did not try to find all the premature individuals, which could be present in deeper chambers if a colony was infested.
Finally we covered the nests and restored the arrangement of the surrounding vegetation as exactly as possible to minimize the impact of our investigation. They were maintained there at room temperature until adult butterflies or wasps emerged. The proportion of parasitized pupae enabled us to estimate the population size of adult parasitoids, based on the estimation of the butterfly population derived from the MRR study. Additionally, 50 randomly chosen squares 1 m 2 each were surveyed to estimate the average density of Myrmica colonies in the vicinity of G.
Ants were preliminarily identified in the field with hand lenses, but voucher samples of 510 workers were collected to confirm this determination in the laboratory, according to Czechowski et al.
We captured and marked a total of individuals males and females. The proportion of recaptured males and females was almost identical The maximum number of recaptures on different days was four for males and three for females.
Most of the capture events occurred in more sheltered places, surrounded by trees and shrubs. The mean number of days between first and last captures was 2. The daily survival rate obtained with the Jolly-Seber model was 0. Taking into consideration the estimated flight period ca. The mean capture probability was slightly higher in males 0. Generally the dominance of females in the second half of the flight period was less evident compared to that previously observed for males Figure 4.
Dynamics of daily numbers of males and females throughout the flight period based on Jolly-Seber model estimates. Error bars represent SEs. The density was estimated as adults per hectare.
A total number of colonies of Myrmica ants was found and inspected. The most common species was M. We found a total number of 94 premature individuals: larvae, prepupae and pupae 113 in individual nests and 2. However, as far as infested colonies are concerned our search was restricted to surface chambers so as not to disturb them excessively and to minimize our impact on the population.
Therefore, it is possible that further larvae were present there. The larvae we found were left with their hosts, but prepupae and pupae Figure 6 were collected and kept in captivity to assess the parasitization rate.
A total number of 49 individuals were collected from 27 different nests, and 37 pupae This indicates that the population of adult wasps could be three times more numerous than the population of adult butterflies. Based on this rate and an estimation of the adult population size of P. Parasitized marked with arrows and unparasitized pupae of Phengaris alcon in a nest of Myrmica scabrinodis.
The mean density of Myrmica nests near gentians was 1. Up to four nests were found in a single 1 m 2 square. Surprisingly P. We hypothesized that the presently studied site was simply overlooked in the past due to its small area and inconspicuous surroundings. Recent colonization is not likely, taking into consideration the very specific and complex habitat requirements of P.
It is suggested that it could have colonized some sites as a consequence of actions aimed at the restoration of meadows in river valleys [ 43 ]. However the larval food plant of L. Moreover species like P.
The most unique trait of the presently studied population is the density of adults, which is the highest of all populations of Phengaris alcon using Gentiana pneumonanthe studied so far with the MRR method Table 1. If we also consider the xerothermophilous form of P. However it occupied an area that was a few times smaller, and the overall number of adults was lower. Another method of estimation of adult populations is based on egg counts but the maximum result for hygrophilous populations was clearly lower [ 46 ].
The high density of adults reflects two favorable habitat characteristics, i. If we compare our results with data concerning other Phengaris species, especially for P.
One has to keep in mind that the larval food plant of congeneric species Sanguisorba officinalis is often abundant and evenly distributed in favorable biotopes, in contrast to G.
Therefore the importance of host plant availability in determining of habitat quality may vary between species [ 19 ]. The estimated life span of adults of P.
Their short life expectancy is compensated for by high fecundity, and in the case of P. Interestingly, the estimated life span 4. This discrepancy could be related to the high density of adults at the presently investigated site, which could trigger emigration [ 34 ] and therefore affect the recorded residency time. As a consequence many individuals could leave the site relatively freely. In contrast, the previously studied population was very small and its site was surrounded by a clearly distinct biotope of wetlands with tall vegetation of sedges and Phragmites [ 22 ].
The calculated value of the temporal fragmentation index was then relatively high and typical for a species of conservation concern see [ 38 ] for a review , suggesting that the population could be under threat.
However, taking into consideration the high density of adults and weak protandry we could assume that the chance for individuals to find a mate was high for most of the flight period and the effective population was not reduced. The slightly higher capture probability of males that we recorded is not surprising taking into consideration the brighter colouration of this sex and its patrolling behavior. Females are less conspicuous when they are flying low and looking for larval food plants or ovipositing on gentians, which are frequently still not flowering.
Tall grasses in some parts of the habitat made the detection of females even harder. On the other hand the higher catchability of patrolling males was also observed for the congeneric P. This may suggests that flight activity is the most important factor influencing probability of encountering a Phengaris of a given sex.
Host ant specificity turned out to be typical for this part of the European range [ 23 ], and for Poland in particular. Myrmica scabrinodis is the only host ant of P. The exceptions are habitats where Myrmica vandeli also co-occurs, but this ant is a closely related species and moreover suspected to be a temporary social parasite of M. Among hundreds of nests searched across the country there was just a single case of the use of an untypical host i.
A more complicated pattern of host use is observed in the case of populations dependent on G. The density of host nests was relatively high, i. There is an ongoing debate over whether females of P. In the case of the presently studied site this potential ability seems to be less important, taking into consideration the high availability of hosts.
Moreover it was found that P. In that case a high density of host colonies increases the probability that readopted caterpillars will be moved to a nest where they will be able to complete their development. Not only its high abundance makes the P. The presence of a specific parasitoid was detected and its impact on the population is likely to be significant taking into consideration that as many as three quarters of the pupae were infested.
This means that the adult population of this wasp is around three times more numerous compared to adult butterflies. Parasitoids are important factors influencing the population size of butterflies.
However, socially parasitic Phengaris butterflies are known as regular hosts of specific ichneumonid parasitoids of the subfamily Ichneumoninae, almost exclusively [ 60 ]. Three species are attacked when they are still in the flowerheads of larval food plants. Phengaris arion is infested by Neotypus coreensis but data on its occurrence are very rare [ 61 ]. As far as I. Females localize their host only in ant colonies and produce specific allomones, causing fights among workers to parasitize butterfly caterpillars with impunity [ 30 , 64 ].
There are anecdotal records of P. Data on the occurrence of populations of P. In Poland hygrophilous populations have been recorded so far only from a single region in the south situated about km from the presently studied site.
The parasitization rate of pupae found in nests of M. Moreover there is a record from the site of the xerothermophilous form using G. In addition, parasitoids of P. Genetic studies are desirable, to look for possibilities of cryptic speciation among populations adapted to different biotopes.
Despite the positive features discussed above, the investigated population may be at risk of extinction given factors including isolation, successional changes and unpredictability of management practices. They were mainly affected by intensification of management or abandonment.
Many open areas have become overgrown and invasive plants are also a real problem. Our one-year study does not enable evaluation of the long-term trend of the investigated population. However, it is worth noting that populations of Phengaris species are considered as relatively stable compared to other butterflies [ 70 ]. There is no doubt, however, that certain conditions are not stable at the presently studied site.
Irregular mowing of managed plots every year affects to a greater or lesser extent the population of premature P. Moreover the analysis of the available orthophotomaps indicates that recent successional changes clearly reduced the P.
Other meadows were still open but encroachment of the invasive Lupinus was observed and goldenrods could be problematic in the future, taking into consideration that they were widespread in the vicinity. It is known that long term abandonment may lead to adverse changes in ant species composition in the habitats of P.
Studies of the effects of different management practices on particular parts of this unique system butterflies, plants, ants and parasitoids are vital in order to recommend optimum management. Although our results suggest that the seasonal adult population of the parasitoid wasp is much more numerous than the host population in fact it may be even more at risk in case of habitat reduction [ 72 ]. Parasitoids are considered ultimate indicators of the biodiversity of Phengaris Maculinea systems, and their presence proves high habitat quality and the existence of large, functional metapopulations [ 73 , 74 ].
The presently studied site is highly isolated and there is little doubt that its relatively large area is a key factor in making it unique. The investigated population is remarkable due to its exceptionally high density of adults and simultaneously high infestation rate by a specific parasitoid.
We hope that the results of the present study will help to attract attention to the protection of this site, even though P. Aurelia and Gustaw Sielezniew helped in field studies. Sarah Luczaj made linguistic improvements on the manuscript.
We thank three anonymous reviewers for constructive comments on our manuscript. Conceptualization, I. All authors have read and agreed to the published version of the manuscript. Published online Oct Author information Article notes Copyright and License information Disclaimer.
Received Aug 31; Accepted Oct 8. Abstract Caterpillars of the Alcon blue butterfly Phengaris alcon are initially endophytic and feed inside the flowerheads of Gentiana plants, but complete their development as social parasites in the nests of Myrmica ants, where they are fed by workers.
Keywords: adult demography, Ichneumon eumerus , Maculinea alcon , Myrmica scabrinodis , host-ant specificity, life span, markrecapture, population size, temporal fragmentation. Materials and Methods 2. Study Site We conducted our study on an isolated site of P. Open in a separate window.
Figure 1. Figure 2. Studies of Adult Demography The study population was monitored every year since its discovery, and in every season adults were observed numerously at the site. Figure 3. A marked individual of Phengaris alcon on a flower of Gentiana pneumonanthe. Results 3. Adult Demography We captured and marked a total of individuals males and females. Figure 4. Host Ants and Parasitoids A total number of colonies of Myrmica ants was found and inspected.
Figure 5. Figure 6. Figure 7. A female Ichneumon cf. Discussion 4. Adult Demography The most unique trait of the presently studied population is the density of adults, which is the highest of all populations of Phengaris alcon using Gentiana pneumonanthe studied so far with the MRR method Table 1. Host Ants and Parasitoids Host ant specificity turned out to be typical for this part of the European range [ 23 ], and for Poland in particular.
Implications for Conservation Despite the positive features discussed above, the investigated population may be at risk of extinction given factors including isolation, successional changes and unpredictability of management practices. Conclusions The investigated population is remarkable due to its exceptionally high density of adults and simultaneously high infestation rate by a specific parasitoid.
Acknowledgments Aurelia and Gustaw Sielezniew helped in field studies. Author Contributions Conceptualization, I. Conflicts of Interest The authors declare no conflict of interest.
References 1. Fric Z. Phylogeny and classification of the Phengaris-Maculinea clade Lepidoptera: Lycaenidae : Total evidence and phylogenetic species concepts. Thomas J. Butterfly mimics of ants. Maes D. Integrating national Red Lists for prioritising conservation actions for European butterflies. Insect Conserv.
The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In: Pullin A. Ecology and Conservation of Butterflies.
Chapman and Hall; London, UK: Settele J. Studies in the Ecology and Conservation of Butterflies in Europe. Pensoft Publishers; Sofia, Bulgaria: Successful conservation of a threatened Maculinea butterfly.
Barbero F. Data provider:. National Agricultural Library. Active Data provider submitted metadata in the last calendar year. Journal Article. Access the full text Link. Lookup at Google Scholar. Soares, P. This butterfly species maintains a complex relationship with its host plant marsh gentian Gentiana pneumonanthe L. This study involved a multivariate analysis of the relationship between M.
Three habitats were distinguished in terms of their floristic combinations: density of ferns more humid and deep soils, Habitat A , size of grasses left wetlands, Habitat B and shrubs productive wetland, Habitat C. In these habitats, several G. Taller plants and higher number of Maculinea eggs were observed in the habitats with higher values ofshrubs and grasses cover Habitats B and C , whereas the higher number of plants was stimulated by higher values of shrub cover Habitat C.
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From Wikipedia, the free encyclopedia. Species of butterfly. Conservation status. For a key to the terms used, see Glossary of entomology terms. Retrieved 8 May Band 1: Abt. Bibcode : Natur. PMID S2CID Systematic Entomology. ISSN Molecular Phylogenetics and Evolution. Insectes Sociaux. Bibcode : Oecol.. ISBN Ecological Entomology.
Wardlaw Journal of Insect Conservation. ISSN X. Bibcode : Sci CiteSeerX Nature News. PMC Bibcode : Oecol. In three Ma. Wikimedia Commons has media related to Maculinea alcon. Brood parasites. Black-headed duck. Honeyguide Thick-billed honeyguide Greater honeyguide. Cuckoo catfish. Pungtungia herzi. Phengaris alcon Phengaris arion Phengaris rebeli. J Insect Conserv Myrmecologische Nachrichten Syst Entomol Ekologia Bratislava Accessed 12 July Larval feeding and oviposition preferences.
Eur J Entomol Nash DR MacSamp version: 1. Accessed 25 November Lepidoptera: Lycaenidae; Hymenoptera: Formicidae. Sociobiology Science Pensoft, Sofia, Moscow. Pol J Entomol Plant Biosystems in press. Insect Soc Oecologia Download references. Elmes determined the first M.
Nash, E. Varga revised the manuscript. Dutch Butterfly Conservation, P. You can also search for this author in PubMed Google Scholar. Reprints and Permissions. Arnaldo, P. Maculinea alcon exploits Myrmica aloba in Portugal: unusual host ant species of a myrmecophilous butterfly in a peripheral region.
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