insects
Article
A Unique Population in a Unique Area: The Alcon
Blue Butterfly and Its Specific Parasitoid in the
Białowieża Forest
Izabela Dziekańska 1, * , Piotr Nowicki 2 , Ewa Pirożnikow 3 and Marcin Sielezniew 4
1
2
3
4
*
Division of Molecular Biology, Faculty of Biology, University of Bialystok, Ciołkowskiego 1J,
15-245 Białystok, Poland
Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland;
piotr.nowicki@uj.edu.pl
Institute of Forest Sciences, Bialystok University of Technology, Wiejska 45 E, 15-351 Białystok, Poland;
e.piroznikow@pb.edu.pl
Laboratory of Insect Evolutionary Biology and Ecology, Faculty of Biology, University of Bialystok,
Ciołkowskiego 1J, 15-245 Białystok, Poland; marcins@uwb.edu.pl
Correspondence: i.dziekanska@uwb.edu.pl
Received: 31 August 2020; Accepted: 8 October 2020; Published: 12 October 2020
Simple Summary: Caterpillars of the Alcon blue butterfly Phengaris alcon feed initially inside flowerheads
of Gentiana plants but complete their development as ‘cuckoos’ in nests of Myrmica ants being fed by
workers. Social parasitism protects larvae from most natural enemies and only specialized ichneumon
wasps are able to infiltrate host colonies and parasitize them. Across its range P. alcon forms different
ecotypes adapted to specific ants and plants. Complicated ecological requirements make the butterfly a
very local and threatened species and sensitive to environmental changes. We investigated an isolated and
previously unknown population in the high nature value area, i.e., the Białowieża Forest (NE Poland).
Using the marking technique we estimated the seasonal number of adults at 1460 individuals and the
density (850/ha) showed to be the highest among all hygrophilous populations studied so far. Premature
P. alcon were found exclusively in nests of M. scabrinodis and from as many as 75.5% pupae Ichneumon cf.
eumerus wasps were reared. The exceptional abundance of both P. alcon and its parasitoid (its population
could be estimated at about 4500 adults) can be explained by a high density of nests host ants in vicinity of
host plants. This unique system deserves special conservation care.
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. Its specific and complicated ecological requirements
make P. alcon a very local, threatened species, sensitive to environmental changes. We investigated
an isolated and previously unknown population in an area of high nature value—the Białowieża
Forest (NE Poland). Using the mark–release–recapture method we estimated the seasonal number of
adults at 1460 individuals, and their density (850/ha) was the highest among all populations using
G. pneumonanthe studied so far. The site is also unique due to the presence of the specific parasitoid
Ichneumon cf. eumerus, and parasitoids are considered the ultimate indicators of the biodiversity
of Phengaris systems. Since 75.5% of P. alcon pupae were infested we could estimate the seasonal
population of adult wasps at about 4500 individuals. The high abundance of both P. alcon and its
parasitoid may be explained by favorable habitat characteristics, i.e., the strong presence of host plants
and the high density of nests of Myrmica scabrinodis, which is the only local host ant of the butterfly.
Keywords: adult demography; Ichneumon eumerus; Maculinea alcon; Myrmica scabrinodis; host-ant
specificity; life span; mark–recapture; population size; temporal fragmentation
Insects 2020, 11, 687; doi:10.3390/insects11100687
www.mdpi.com/journal/insects
Insects 2020, 11, 687
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1. Introduction
European representatives of the genus Phengaris Doherty (Lepidoptera, Lycaenidae), which is a
senior synonym of Maculinea Van Eecke [1], are considered as flagship priorities in butterfly conservation,
along with Queen Alexandra’s birdwing of Papua New Guinea, and the Mexican overwintering sites
of monarchs [2]. All four European species are threatened on a continental scale [3] and three of
them are also listed in the Annexes of the Habitat Directive. Large blues attract the attention not
only of conservationists but also scientists due to their complicated and peculiar life history related to
obligatory myrmecophily [4–6].
In contrast to most other butterflies they require two different resources to complete their
development. Caterpillars are initially endophytic, feeding on specific plants, but in the fourth (final)
instar they become social parasites of red ants (Myrmica Latr.). Infiltration of host colonies is enabled
by sophisticated adaptations, including chemical and acoustical mimicry [7–9]. Three of the four
European species exploit ants as predators feeding on their brood, while the Alcon blue Phengaris
alcon (Denis and Schiffermüller, 1775) is mostly fed directly by ants through trophalaxis or by insect
prey. This sophisticated strategy is believed to be the most advanced and also the most effective,
i.e., more ‘cuckoo’ larvae can develop in a single colony compared to predatory species [10].
Phengaris alcon shows considerable ecological variation across its range, being locally adapted to
different larval food plants and host ants. Populations inhabiting contrasting biotopes even used to
be regarded as different species, e.g., those dependent on Gentiana cruciata, which grows mostly on
xerothermal calcalerous grasslands, were commonly separated out as P. rebeli, while the nominative
occurred on wet meadows with Gentiana pneumonanthe. However genetic studies showed that this
approach was unreasonable, and moreover the number of larval food plants used is even higher [11–15].
In the European lowlands the most common ecotype is that dependent on G. pneumonanthe.
Quite often it exists in very small and spatially isolated local populations, however, large metapopulation
systems with many connected populations are also known [16–22]. Two host ant races could be
distinguished in Europe, i.e., north-western populations depending on Myrmica rubra and Myrmica
ruginodis, while the remaining ones mostly exploit the nests of Myrmica scabrinodis [23].
In 2016 we discovered a large population in an area of high nature value—the Białowieża Forest
(NE Poland). The area is believed to be the best preserved forest complex in temperate lowland Europe.
It is known as the most important refuge for primeval forest entomofauna, and saproxylic species
(especially beetles) are considered the most valuable component [24]. Less common knowledge is that
the Białowieża Forest is also considered one of the best explored and richest areas in Poland as far
as Lepidoptera are concerned [25–28], being one of the prime butterfly areas [29]. A total number of
110 species have been recorded from the Białowieża Forest so far, i.e., more than 2/3 of Polish fauna,
but there are no data concerning the presence of P. alcon there.
The aim of the present study was to estimate the demographic parameters of the adult population
at this isolated site. We also identified host ants and assessed density in the vicinity of food plants
as one of the key parameters determining the habitat quality of the butterfly. Finally we studied the
infestation of P. alcon pupae by Ichneumon cf. eumerus, which was recorded during a preliminary survey.
This rare and specific parasitoid attacks butterfly larvae when they are in the socially parasitic part of
their development [30]. Simultaneous studies performed in the same season enabled us to estimate the
seasonal population size both of adult butterflies and ichneumon wasps, for the first time.
2. Materials and Methods
2.1. Study Site
We conducted our study on an isolated site of P. alcon near the village of Budy (52◦ 44′ 10′′ N,
E; 150 m above sea level), situated in one of the large clearings in the Białowieża Forest and
surrounded by compact forest stands (Figure 1). This open area surrounded by forest had an area of
about 120 ha and nearly 90% of it was covered by grasslands and fallow land. The area with Gentiana
23◦ 44′ 7′′
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pneumonanthe (Figure 2) covered only 1.71 ha and encompassed parts of six plots of land differing with
regard to management. Three of them were irregularly mown once a year and on three others no signs
of recent (i.e., within at least the last five years) management
could be seen. In the past the whole area
–
was probably extensively mown.
Figure 1. Outline
map
of the
Białowie
ża Forest
(NE
Poland)
with
thethe
location
of the
study
sitesite
(red
Outline
map
of the
Białowieża
Forest
(NE
Poland)
with
location
of the
study
(red
arrow). The color green represents area covered by forest.
Figure 2. The study site of Phengaris alcon in the Białowieża Forest.
in the Białowieża Forest
The biotope of the butterfly could be classified as a mesotrophic fen-meadow community of
Molinietum caeruleae W. Koch 1926 (Molinietum medioeuropaeum W. Koch 1926; ‘litter meadows’),
with somewhat impoverished species composition. The phytocoenoses was dominated by grasses,
– Agrostis
– capillaris, and with a smaller proportion of
i.e., mainly Phleum pratense, Festuca rubra and
Deschampsia caespitosa and Briza media. In some patches the development of aggregations of Calamagrostis
epigejos was observed. Juncus effusus and Juncus conglomeratus could be also mentioned, among other
–
–
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monocots. The meadows were characterized by a high species richness of dicotyledonous plants,
and the most common were Centaurea jacea, Lathyrus pratensis, Viola canina, Potentilla erecta and Lychnis
flos-cuculi, and G. pneumonanthe in some parts. Local aggregations of Betonica officinalis, Succisa pratensis
and Rhinanthus serotinus were also remarkable. In wetter places Lysimachia vulgaris and Filipendula
ulmaria were also present.
The abundance of the host plant was quite high, an estimated 3000 individuals at least, based on
counts of individuals present in six random plots (50–100 m2 ). Only a few single plants were localized
outside the study area.
2.2. 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. A mark–release–recapture (MRR) study to estimate population
size and adult life span was conducted in 2019, when we sampled the population on 11 occasions
between 19 July and 12 August. The sampling covered almost the entire flight period of the focal
species, i.e., it was started on the second or third day of the emergence of the first adults and the site was
visited every 2–5 days if the weather was favorable (i.e., sunny and not very windy), between 10 am
and 5 pm. Two people spent 2–3 h on the site during each sampling day. The end of the flight period
was estimated at around 16 August, so its total duration was ca. 30 days. Butterflies were captured
with an entomological net, marked on the underside of their hind-wings with unique identity numbers
(Figure 3) using a fine-tipped waterproof pen, and then immediately released at the place of capture.
Date, time and patch number and the sex and ID number of each butterfly were recorded.
Figure 3. A marked individual of Phengaris alcon on a flower of Gentiana pneumonanthe.
We analyzed our data with the Jolly-Seber model [31] using Program MARK, version 8.0 [32].
The model represents a well-established standard for estimating the population size in open populations,
and it has been frequently applied in butterfly studies [33–35]. Based on the lowest value of the Akaike
information criterion corrected for small sample size (AICc ) [36], the best-performing model variant
was ϕ (.) p (s + t) B (s*t), i.e., the model assuming a constant (and equal for both sexes) survival rate (ϕ),
but sex-dependent and freely time-varying (thus differing between capture days) recruitments of new
individuals into the population (B), and sex-dependent and time-varying capture probabilities (p) with
a constant difference between sexes. 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. For comparative purposes we also
derived mean capture probabilities for males and females across the entire season and mean adult life
span, estimated from the survival rate as e = (1 − φ)−1 − 0.5 [37]. Besides, we calculated the temporal
Insects 2020, 11, 687
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fragmentation index, i.e., ratio of the flight period length to the adult life span, which is considered an
indicator of species vulnerability [38].
2.3. Studies of Premature Individuals in Ant Nests
In late August 2018, patches with larval food plants bearing eggs/eggshells of P. alcon were marked
with GPS, and additionally using wooden tags. In late June and early July 2019 we searched for
Myrmica ants in those patches in a radius of 1 m from plants, i.e., certainly within the foraging zone of
Myrmica workers [39]. All nests found were very carefully opened and examined for the presence of
P. alcon. 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. Nests in which we could not find any larvae/pupae were searched more thoroughly.
Finally we covered the nests and restored the arrangement of the surrounding vegetation as exactly as
possible to minimize the impact of our investigation.
When we found prepupae and/or pupae, they were put into plastic containers with some wet
moss and transferred to the lab. 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 m2 each) were surveyed to estimate the average
density of Myrmica colonies in the vicinity of G. pneumonanthe plants. Ants were preliminarily identified
in the field with hand lenses, but voucher samples of 5–10 workers were collected to confirm this
determination in the laboratory, according to Czechowski et al. [41].
3. Results
3.1. Adult Demography
We captured and marked a total of 854 individuals (505 males and 349 females). Only 154 of them
(18%) were recaptured. The proportion of recaptured males and females was almost identical (17.8%
and 18.3% respectively). 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 2.63 for males and 2.86 for
females respectively, whereas the maximum duration between captures of an individual reached six
days for both sexes. The daily survival rate obtained with the Jolly-Seber model was 0.558 ± 0.021
(95% Confidence Interval [CI]: 0.517–0.579), which corresponds to the estimated adult life span
of 1.76 ± 0.11 days (95% CI: 1.57–1.99 days). Taking into consideration the estimated flight period
(ca. 30 days) the temporal fragmentation index was calculated at 17.05.
The mean capture probability was slightly higher in males (0.617 ± 0.078; 95% CI: 0.457–0.755)
than in females (0.547 ± 0.069; 95% CI: 0.412–0.675). In the first week of sampling, a clear dominance of
males was observed with the peak of abundance on July 23rd (164 ± 12.8). The highest number of
females was estimated eight days later (132 ± 11.2). 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).
The seasonal population size was estimated at 1460 adults (95% CI: 1358–1582), including 793 males
(95% CI: 722–886) and 667 females (95% CI: 599–753) giving a slightly male-biased sex ratio (1.19:1).
The density was estimated as 854 adults per hectare.
–
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3.2. Host Ants and Parasitoids
– The most common
A total number of 135 colonies of Myrmica ants was found and inspected.
species was M. scabrinodis
Nyl. (87 nests) and the other four
–
– species recorded there were: M. ruginodis
Nyl. (25), M. rubra (L.) (12), M. gallieni Bondr. (10) and M. lobicornis Nyl. (1) (Figure 5).
Figure 4. Dynamics of daily numbers of males and females throughout the flight period based on
Jolly-Seber model estimates. Error bars represent SEs.
–
Figure 5. Myrmica ant species composition at the site of Phengaris alcon in the Białowieża Forest and
proportion of Myrmica scabrinodis nests infested by the butterfly.
in the Białowieża Forest and
–
Premature P. alcon were found exclusively in colonies of M. scabrinodis (Figure 5) and the difference
in the rate of parasitism between this species and the three other most common species was significant
according to the Fisher exact test: M. scabrinodis/M. ruginodis (p < 0.00001), M. scabrinodis/M. rubra
(p = 0.0003) and M. scabrinodis/M. gallieni (p = 0.0013).
We found a total number of 94 premature individuals: larvae, prepupae and pupae (1–13 in
individual nests and 2.29 on average). 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 (75.51%) from 21 nests (1–6 parasitized pupae per a nest) were
finally shown to be parasitized by Ichneumon cf. eumerus Wesmael, 1857 (Figure 7). This indicates
Insects 2020, 11, 687
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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. alcon (1460),
in the
the Białowieża
Białowieża Forest
Forest and
and
in
the seasonal number of adult wasps could be estimated at ca. 4500 individuals.
Figure 6. Parasitized (marked with arrows) and unparasitized pupae of Phengaris alcon in a nest of
Myrmica scabrinodis.
Figure 7. A female Ichneumon cf. eumerus reared from a pupa of Phengaris alcon.
The mean density of Myrmica nests near gentians was 1.86/m2 and density of colonies of the only
recorded host ant, i.e., M. scabrinodis, was estimated at 1.34/m2 . Up to four nests were found in a single
1 m2 square.
4. Discussion
4.1. The Alcon Blue Butterfly in the Białowieża Forest
Surprisingly P. alcon has never been recorded in the Białowieża Forest before, including the
Belarussian part of the area [42]. We hypothesized that the presently studied site was simply
overlooked in the past due to its small area and inconspicuous surroundings. Recent colonization is
Insects 2020, 11, 687
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not likely, taking into consideration the very specific and complex habitat requirements of P. alcon
and restricted colonization abilities [16]. Some butterfly species colonized the area of the Białowieża
Forest recently, following a range expansion, as, e.g., observed for the generalistic Melanargia galathea.
There are also records concerning habitat specialists, namely Lycaena helle, which became extinct at
a historical site, although several populations have recently been discovered in other parts of the
Białowieża Forest. 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. helle is
relatively widespread compared to G. pneumonanthe, which is rare, local and declining in the Białowieża
Forest [44]. Moreover species like P. alcon, due to its absence in Annex II of the Habitat Directive,
are not included in management plans for Natura 2000 sites, and are therefore neglected by most
inventory and monitoring activities.
4.2. 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). If we also consider the xerothermophilous form of P. alcon dependent on G. cruciata
(formerly known as P. rebeli) only one single German population reached a higher abundance per
hectare [45]. 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].
Table 1. Estimated adult population sizes (N) and densities derived from MRR studies of Phengaris
alcon across Europe.
Ecotype of
Phengaris alcon
Site
Country
Higrophilous
(Gentiana
pneumonanthe)
Budy
Caselette
Mottarone
Rauzes
Fanatele
Bokiny
Poland
Italy
Italy
France
Romania
Poland
Talesberg
Rimetea
Schmandberg
Sengenberg
Wiedberg
Fanatele Domnesc
Rieseler Berg
Germany
Romania
Germany
Germany
Germany
Romania
Germany
Xerothermophilous
(Gentiana cruciata)
Year(s)
N
2019
1460
1997–2010
1600
2009–2010 346–388
2004–2007 281–1222
2010
1313
2015
40
1993
2012
1990
1990
1993
2010
1990
496
699
108
262
85
1073
38
Area
(ha)
Density
(N/ha)
Source
1.71
2.9
1.2
13
40
5.47
854
52–552
288–323
22–94
33
7
present study
[20,47]
[47]
[48]
[49]
[20]
0.36
0.93
0.5
1.5
0.58
40
2.25
1378
752
216
175
147
27
17
[45]
[35]
[50]
[50]
[45]
[49]
[50]
The high density of adults reflects two favorable habitat characteristics, i.e., (i) high and relatively
even coverage by initial larval food plants and (ii) the high density of host ants. If we compare
our results with data concerning other Phengaris species, especially for P. teleius and P. nausithous,
even higher densities (ca 1000 adults per hectare) are found on some sites [19,37]. 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. pneumonanthe, which usually forms local
clusters. 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. alcon in our study (1.7 days) was relatively low but not
exceptional if compared with available data [20,22,47,48,51,52], and Phengaris butterflies are generally
considered short-lived insects (see [38]). Their short life expectancy is compensated for by high
fecundity, and in the case of P. alcon a female can lay 19 eggs/h and 80–100 eggs per day [51].
Interestingly, the estimated life span (4.9 days) of another isolated population studied in the same
region was nearly three times longer [22]. This discrepancy could be related to the high density of
Insects 2020, 11, 687
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adults at the presently investigated site, which could trigger emigration [34] and therefore affect the
recorded residency time. The population in the Białowieża Forest was clearly isolated, but at the same
time the occupied patch of habitat was situated in an open area of grassland and fallow land without
clear barriers and such conditions favor dispersal [17]. 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. arion, which in contrast shows weak sexual dimorphism and usually occurs in
lower vegetation [35]. This may suggests that flight activity is the most important factor influencing
probability of encountering a Phengaris of a given sex.
4.3. 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. Myrmica scabrinodis is the only host ant of P. alcon on the vast majority of Polish
sites where G. pneumonanthe is the larval food plant [53]. 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. scabrinodis [54]. Among hundreds of nests searched across the country there
was just a single case of the use of an untypical host (i.e., Myrmica schencki) by the hygrophilous
ecotype [55]. A more complicated pattern of host use is observed in the case of populations dependent
on G. cruciata [23].
The density of host nests was relatively high, i.e., >1 colony of M. scabrinodis was recorded per
square meter on average in the vicinity of gentians. There is an ongoing debate over whether females
of P. alcon are able to detect their host, and the results are ambiguous [56–58]. 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. alcon may switch between ant nests during its
development, e.g., a weak colony with the butterfly’s caterpillars inside raided by a stronger colony [59].
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. alcon population from the Białowieża Forest unique
and deserving of conservational concern. 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]. A more widespread species
is Neotypus melanocephalus Gmelin, 1790, a specific parasitoid of Phengaris nausithous (Bergsträsser,
1779), which may be quite common at some localities [62]. This wasp can also occasionally parasitize
Phengaris teleius (Bergsträsser, 1779) [63], which in turn can be a rare host of Ichneumon fulvicornis
Gravenhorst 1829 and I. eumerus Wesmael 1857 [60].
Insects 2020, 11, 687
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As far as I. eumerus is concerned it is known mostly as a spectacular and famous specific parasitoid
of P. alcon. 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. alcon parasitized by Ichneumon balteatus Wesmael 1845, known as a parasitoid of some other
unrelated butterfly species [65].
Data on the occurrence of populations of P. alcon infected by parasitoids are scarce. In Poland
hygrophilous populations have been recorded so far only from a single region in the south situated
about 300 km from the presently studied site. The parasitization rate of pupae found in nests of M.
scabrinodis and M. vandeli was also high there, estimated at 62% [54]. Moreover there is a record from
the site of the xerothermophilous form using G. cruciata where just a single nest with infested pupae
was recorded among many dozens surveyed [66].
In addition, parasitoids of P. alcon have been reported from the Spanish Pyreenes [30], Hungary [67],
Portugal [68] and from the Austrian Alps [69], where quantitative data concerning the parasitization
rate are available—60% and 77.6% of pupae of P. alcon rebeli and P. alcon X were infested by I. cf eumerus
respectively. It should be mentioned here that there are some uncertainties concerning the identity
of Ichneumon wasps parasitizing different ecotypes/subspecies of P. alcon [60], and this is why we
identified the reared wasps as I. cf eumerus. Genetic studies are desirable, to look for possibilities of
cryptic speciation among populations adapted to different biotopes.
4.4. 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. Butterflies requiring grasslands have suffered a severe decline in the Białowieża Forest
and some species (including habitat directive species, i.e., Parnassius mnemosyne, Colias myrmidone,
Polyommatus eros, Phengaris arion, Coenonympha hero and Coenonympha oedippus) have become extinct
at least in the Polish part [28]. 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. alcon (when G. pneumonanthe is cut too early
caterpillars are not able to finish the phytophagous part of their development) and it is difficult to
distinguish natural cycles of abundance from anthropogenic factors. Moreover the analysis of the
available orthophotomaps indicates that recent successional changes clearly reduced the P. alcon habitat
at one of the plots of land, where just a single large oak was present for the past 15 years, and now
scrubs and trees cover a significant part of the area. 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. alcon [71], and indeed we
noticed that M. scabrinodis became less frequent in unmanaged patches in higher vegetation.
The site in the Białowieża Forest creates the potential for further studies, since it consists of distinct
meadow stripes, and the suitability of managed plots changes from year to year due to differences in
mowing. 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
Insects 2020, 11, 687
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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.
5. Conclusions
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. alcon is not a habitat
directive species, and therefore is a secondary target of conservation in the Natura 2000 site Puszcza
Białowieska.
Author Contributions: Conceptualization, I.D., P.N., and M.S.; Methodology, I.D., P.N., and M.S.; Formal Analysis,
I.D., P.N., and M.S.; Investigation, I.D., E.P., and M.S.; Resources, I.D.; Data Curation, I.D., M.S.; Writing—Original
Draft Preparation, I.D., P.N., E.P., and M.S.; Writing—Review and Editing, I.D., M.S.; Visualization, I.D., M.S.;
Supervision, I.D., M.S.; Project Administration, I.D., M.S.; Funding Acquisition, I.D., P.N. All authors have read
and agreed to the published version of the manuscript.
Funding: This research was funded by Polish Ministry of Science and Higher Education, under the subsidy for
maintaining the research potential of the Faculty of Biology, University of Bialystok, grant number BMN-1 obtained
by I.D. P.N. was supported by the Polish National Science Centre through its grant UMO-2019/33/B/NZ9/00590.
Acknowledgments: Aurelia and Gustaw Sielezniew helped in field studies. Sarah Luczaj made linguistic
improvements on the manuscript. The Regional Director for Environmental Protection in Białystok provided
relevant permissions for the studies of P. alcon. We thank three anonymous reviewers for constructive comments
on our manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Fric, Z.; Wahlberg, N.; Pech, P.; Zrzavý, J. Phylogeny and classification of the Phengaris-Maculinea clade
(Lepidoptera: Lycaenidae): Total evidence and phylogenetic species concepts. Syst. Entomol. 2007, 32,
558–567. [CrossRef]
Thomas, J.A.; Settele, J. Butterfly mimics of ants. Nature 2004, 432, 283–284. [CrossRef]
Maes, D.; Verovnik, R.; Wiemers, M.; Brosens, D.; Beshkov, S.; Bonelli, S.; Buszko, J.; Cantú-Salazar, L.;
Cassar, L.F.; Collins, S.; et al. Integrating national Red Lists for prioritising conservation actions for European
butterflies. J. Insect Conserv. 2019, 23, 301–330. [CrossRef]
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. ISBN 978-9401045599.
Settele, J.; Kühn, E.; Thomas, J.A. (Eds.) Studies in the Ecology and Conservation of Butterflies in Europe. Species
Ecology along a European Gradient: Maculinea Butterflies as a Model, Volume 2; Pensoft Publishers: Sofia, Bulgaria,
2005; ISBN 978-9546422569.
Thomas, J.A.; Simcox, D.J.; Clarke, R.T. Successful conservation of a threatened Maculinea butterfly. Science
2009, 325, 80–83. [CrossRef]
Barbero, F.; Thomas, J.A.; Bonelli, S.; Balletto, E.; Schönrogge, K. Queen ants make distinctive sounds that are
mimicked by a butterfly social parasite. Science 2009, 323, 782–785. [CrossRef]
Thomas, J.A.; Elmes, G.W.; Sielezniew, M.; Stankiewicz–Fiedurek, A.; Simcox, D.J.; Settele, J.; Schönrogge, K.
Mimetic host shifts in an endangered social parasite of ants. Proc. R. Soc. Lond. B 2013, 280, 2012233.
[CrossRef]
Casacci, L.P.; Bonelli, S.; Balletto, E.; Barbero, F. Multimodal signaling in myrmecophilous butterflies. Front.
Ecol. Evol. 2019, 7, 454. [CrossRef]
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. [CrossRef]
Als, T.D.; Vila, R.; Kandul, N.P.; Nash, D.R.; Yen, S.H.; Hsu, Y.F.; Mignault, A.A.; Boomsma, J.J.; Pierce, N.E.
The evolution of alternative parasitic life histories in large blue butterflies. Nature 2004, 432, 386–390.
[CrossRef] [PubMed]
Insects 2020, 11, 687
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
12 of 15
Pecsenye, K.; Bereczki, J.; Tihanyi, B.; Toth, A.; Peregovits, L.; Varga, Z. Genetic differentiation among the
Maculinea species (Lepidoptera: Lycaenidae) in eastern Central Europe. Biol. J. Linn. Soc. 2007, 91, 11–21.
[CrossRef]
Sielezniew, M.; Rutkowski, R.; Ponikwicka-Tyszko, D.; Ratkiewicz, M.; Dziekańska, I.; Švitra, G. Differences
in genetic variability between two ecotypes of endangered myrmecophilous butterfly Phengaris (=Maculinea)
alcon—The setting of conservation priorities. Insect Conserv. Divers. 2012, 5, 223–236. [CrossRef]
Koubínová, D.; Dincă, V.; Dapporto, L.; Vodă, R.; Suchan, T.; Vila, R.; Alvarez, N. Genomics of extreme
ecological specialists: Multiple convergent evolution but no genetic divergence between ecotypes of Maculinea
alcon butterflies. Sci. Rep. 2017, 7, 13752. [CrossRef] [PubMed]
Bereczki, J.; Pecsenye, K.; Varga, Z.; Tartally, A.; Tóth, J.P. Maculinea rebeli (Hirschke)—A phantom or reality?
Novel contribution to a long-standing debate over the taxonomic status of an enigmatic Lycaenidae butterfly.
Syst. Entomol. 2018, 43, 166–182. [CrossRef]
Vanden Broeck, A.; Maes, D.; Kelager, A.; Wynhoff, I.; WallisDeVries, M.F.; Nash, D.R.; Oostermeijer, J.G.B.;
Van Dyck, H.; Mergeay, J. Gene flow and effective population sizes of the butterfly Maculinea alcon in a highly
fragmented, anthropogenic landscape. Biol. Conserv. 2017, 209, 89–97. [CrossRef]
Maes, D.; Vanreusel, W.; Talloen, W.; Van Dyck, H. Functional conservation units for the endangered Alcon
Blue butterfly Maculinea alcon in Belgium (Lepidoptera: Lycaenidae). Biol. Conserv. 2004, 120, 233–245.
[CrossRef]
WallisDeVries, M.F. A quantitative conservation approach for the endangered butterfly Maculinea alcon.
Conserv. Biol. 2004, 18, 489–499. [CrossRef]
Nowicki, P.; Pepkowska, A.; Kudlek, J.; Skórka, P.; Witek, M.; Settele, J.; Woyciechowski, M. From
metapopulation theory to conservation recommendations: Lessons from spatial occurrence and abundance
patterns of Maculinea butterflies. Biol. Conserv. 2007, 140, 119–129. [CrossRef]
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. [CrossRef]
[PubMed]
Radchuk, V.; WallisDeVries, M.F.; Schtickzelle, N. Spatially and financially explicit population viability
analysis of Maculinea alcon in The Netherlands. PLoS ONE 2012, 7, e38684. [CrossRef] [PubMed]
Nowicki, P.; Deoniziak, K.; Dziekańska, I.; Kostro-Ambroziak, A.; Plazio, E.; Rutkowski, R.; Sielezniew, M.
What keeps “living dead” alive: Demography of a small and isolated population of Maculinea (=Phengaris)
alcon. J. Insect Conserv. 2019, 23, 291–300. [CrossRef]
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. [CrossRef] [PubMed]
Jaroszewicz, B.; Cholewińska, O.; Gutowski, J.J.; Samojlik, T.; Zimny, M.; Latałowa, M. Białowieża Forest—A
relic of the high naturalness of European forests. Forests 2019, 10, 849. [CrossRef]
Krzywicki, M. Fauna Papilionoidea i Hesperioidea (Lepidoptera) Puszczy Białowieskiej. Ann. Zool. 1967, 25,
1–213.
Krzywicki, M. Stan fauny motyli dziennych Lepidoptera, Diurna Puszczy Białowieskiej. Parki Nar. Rez.
Przyr. 1986, 7, 69–76.
Buszko, J.; Kokot, A.; Palik, E.; Śliwiński, Z. Motyle wi˛eksze (Macrolepidoptera) Puszczy Białowieskiej. Parki
Nar. Rez. Przyr. 1996, 15, 3–46.
Jaroszewicz, B. Stan zachowania na terenie Puszczy Białowieskiej gatunków motyli z załaczników
˛
II i IV
Dyrektywy Siedliskowej i propozycje działań ochronnych. Parki Nar. Rez. Przyr. 2010, 29, 29–50.
Buszko, J. Poland. In Prime Butterfly Areas in Europe. Priority Sites for Conservation; van Swaay, C.A.M.,
Warren, M., Eds.; National Reference Centre for Agriculture, Nature and Fisheries, Ministry of Agriculture,
Nature Management and Fisheries: Wageningen, The Netherlands, 2003; pp. 399–401. ISBN 978-9072578242.
Thomas, J.A.; Elmes, G.W. Specialized searching and the hostile use of allomones by a parasitoid whose host,
the butterfly Maculinea rebeli, inhabits ant nests. Anim. Behav. 1993, 45, 593–602. [CrossRef]
Arnason, A.N.; Schwarz, C.J. Using POPAN-5 to analyse banding data. Bird Study 1999, 46, 157–168.
[CrossRef]
White, G.C.; Burnham, K.P. Program MARK: Survival estimation from populations of marked animals. Bird
Study 1999, 46, 120–138. [CrossRef]
Insects 2020, 11, 687
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
13 of 15
Schtickzelle, N.; Le Boulenge, E.; Baguette, M. Metapopulation dynamics of the bog fritillary butterfly:
Demographic processes in a patchy population. Oikos 2002, 97, 349–360. [CrossRef]
Nowicki, P.; Vrabec, V. Evidence for positive density-dependent emigration in butterfly metapopulations.
Oecologia 2011, 167, 657–665. [CrossRef] [PubMed]
Osváth-Ferencz, M.; Bonelli, S.; Nowicki, P.; Peregovits, L.; Rákosy, L.; Sielezniew, M.; Kostro-Ambroziak, A.;
Dziekańska, I.; Kőrösi, A. Population demography of the endangered large blue butterfly Maculinea arion in
Europe. J. Insect Conserv. 2017, 21, 411–422. [CrossRef]
Hurvich, C.M.; Tsai, C. Regression and time series model selection in small samples. Biometrika 1989, 76,
297–307. [CrossRef]
Nowicki, P.; Witek, M.; Skorka, 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. [CrossRef]
Bubová, T.; Kulma, M.; Vrabec, V.; Nowicki, P. Adult longevity and its relationship with conservation status
in European butterflies. J. Insect Conserv. 2016, 20, 1021–1032. [CrossRef]
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. [CrossRef]
Als, T.D.; Nash, D.R.; Boomsma, J.J. Geographical variation in host-ant specificity of the parasitic butterfly
Maculinea alcon in Denmark. Ecol. Entomol. 2002, 27, 403–414. [CrossRef]
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.
Kulak, A.W. Phengaris alcon (Denis & Schiffermüller, 1775). In Krasnaya Kniga Respubliki Belarus′ . Zhivotnyye,
4th ed.; Katchanovski, I.M., Nikiforov, M.E., Parfienov, W.I., Eds.; Belorusskaya Entsiklopediya im. Petrusja
Brovki: Minsk, Belarus, 2015; pp. 211–212. ISBN 978-985-11-0844-8.
Sielezniew, M.; Dziekańska, I.; Bystrowski, C. Czerwończyk fioletek Lycaena helle (Lepidoptera, Lycaenidae)
w polskiej cz˛eści Puszczy Białowieskiej. Parki Nar. Rez. Przyr. 2017, 36, 87–94.
Karczewska, M.; Michalska-Hejduk, D.; Kucharski, L. The Non-Forest Land Ecosystems of Białowieża National
Park; Karczewska, M., Kucharski, L., Eds.; Białowieża National Park: Białowieża, Poland, 2016; pp. 37–139.
ISBN 978-8364513169.
Nowicki, P.; Richter, A.; Glinka, U.; Holzschuh, A.; Toelke, U.; Henle, K.; Woyciechowski, M.; Settele, J. Less
input same output-simplified approach for population size assessment in Lepidoptera. Popul. Ecol. 2005, 47,
203–212. [CrossRef]
Nowicki, P. Survey precision moderates the relationship between population size and stability. Biol. Conserv.
2017, 212, 310–315. [CrossRef]
Cerrato, C.; Lai, V.; Balletto, E.; Bonelli, S. Direct and indirect effects of weather variability in a specialist
butterfly. Ecol. Entomol. 2016, 41, 263–275. [CrossRef]
Baliteau, L. Suivi des insectes à la tourbière de la plaine des Rauzes (Aveyron) et gestion conservatoire de
l’entomofaune. Master’s Thesis, Université de Toulouse, Toulouse, France, 2012.
Timus, , N.; Craioveanu, C.; Sitaru, C.; Rus, A.; Rákosy, L. Differences in adult phenology, demography,
mobility and distribution in two syntopic ecotypes of Maculinea alcon (cruciata vs. pneumonanthe) (Lepidoptera:
Lycaenidae) from Transilvania (Romania). Entomol. Romanica 2013, 18, 21–30.
Meyer-Hozak, C. Population biology of Maculinea rebeli (Lepidoptera: Lycaenidae) on chalk grasslands of
Eastern Westphalia (Germany) and implications for conservation. J. Insect Conserv. 2000, 4, 63–72. [CrossRef]
Van Dyck, H.; Regniers, S. Egg spreading in the ant-parasitic butterfly, Maculinea alcon: From individual
behaviour to egg distribution pattern. Anim. Behav. 2010, 80, 621–627. [CrossRef]
Osváth-Ferencz, M.; Czekes, Z.; Molnár, G.; Markó, B.; Vizauer, T.Z.; Rákosy, L.; Nowicki, P. Adult population
ecology and egg laying strategy in the “cruciata” ecotype of the endangered butterfly Maculinea alcon
(Lepidoptera: Lycaenidae). J. Insect Conserv. 2016, 20, 255–264. [CrossRef]
Sielezniew, M.; Stankiewicz-Fiedurek, A.M. Host ant use by Phengaris (=Maculinea) alcon in Poland. Pol. J.
Entomol. 2009, 78, 323–335.
Sielezniew, M.; Stankiewicz, A. Simultaneous exploitation of Myrmica vandeli and M. scabrinodis (Hymenoptera:
Formicidae) colonies by the endangered myrmecophilous butterfly Maculinea alcon (Lepidoptera: Lycaenidae).
Eur. J. Entomol. 2004, 101, 693–696. [CrossRef]
Insects 2020, 11, 687
55.
56.
57.
58.
59.
60.
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
14 of 15
Sielezniew, M.; Bystrowski, C.; Deoniziak, K.; Da Costa, J.M. An unexpected record of Myrmica schencki
Emery, 1895 as a secondary host ant of the hygrophilous form of a small and isolated population of the Alcon
Blue butterfly Phengaris (=Maculinea) alcon (Denis et Schiffermüller, 1775) (Lepidoptera, Lycaenidae) in NE
Poland. Pol. J. Entomol. 2015, 84, 49–59. [CrossRef]
Van Dyck, H.; Talloen, W.; Oostermeijer, J.G.B.; Feenstra, V.; Van der Hidde, A.; Wynhoff, I. Does the presence
of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly? Proc. R. Soc. B 2000,
267, 861–866. [CrossRef]
Fürst, M.; Nash, D.R. Host ant independent oviposition in the parasitic butterfly Maculinea alcon. Biol. Lett.
2010, 6, 174–176. [CrossRef]
Wynhoff, I.; Bakker, R.B.; Oteman, B.; Arnaldo, P.S.; Van Langevelde, F. Phengaris (Maculinea) alcon butterflies
deposit their eggs on tall plants with many large buds in the vicinity of Myrmica ants. Insect Conserv. Divers.
2015, 8, 177–188. [CrossRef]
Tartally, A.; Somogyi, A.; Révész, T.; Nash, D. Host ant change of a socially parasitic butterfly (Phengaris
alcon) through host nest take-over. Insects 2020, 11, 556. [CrossRef] [PubMed]
Shaw, M.R.; Stefanescu, C.; van Nouhuys, S. Parasitism of European butterflies (Hesperioidea and
Papilionoidea). In Ecology of Butterflies in Europe; Settele, J., Shreeve, T.G., Konvicka, M., van Dyck, H., Eds.;
Cambridge University Press: Cambridge, UK, 2009; pp. 130–156. ISBN 978-0521766975.
Sielezniew, M.; Włostowski, M.; Dziekańska, I. Myrmica schencki (Hymenoptera: Formicidae) as the primary
host of Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae) at heathlands in eastern Poland. Sociobiology
2010, 55, 95–106.
Anton, C.; Zeisset, I.; Musche, M.; Durka, W.; Boomsma, J.J.; Settele, J. Population structure of a large blue
butterfly and its specialist parasitoid in a fragmented landscape. Mol. Ecol. 2007, 16, 3828–3838. [CrossRef]
[PubMed]
Tartally, A. Neotypus melanocephalus (Hymenoptera: Ichneumonidae): The first record of a parasitoid wasp
attacking Maculinea teleius (Lycaenidae). Nota Lepidopterol. 2005, 28, 65–67.
Thomas, J.A.; Knapp, J.J.; Akino, T.; Gerty, S.; Wakamura, S.; Simcox, D.J.; Wardlaw, J.C.; Elmes, G.W.
Parasitoid secretions provoke ant warfare. Nature 2002, 417, 505–506. [CrossRef]
Timus, , N.; Constantineanu, R.; Rákosy, L. Ichneumon balteatus (Hymenoptera: Ichneumonidae)—A new
parasitoid species of Maculinea alcon butterflies (Lepidoptera: Lycaenidae). Entomol. Romanica 2013, 18,
31–35.
Sielezniew, M.; Stankiewicz, A.M.; Górnicki, A. Modraszek Rebela Maculinea rebeli w Przemyślu. Ekologia i
perspektywy ochrony populacji. Rocz. Przemys. 2006, 42, 73–88.
Tartally, A. Myrmecophily of Maculinea butterflies in the Carpathian Basin (Lepidoptera: Lycaenidae). Ph.D.
Thesis, University of Debrecen, Debrecen, Hungary, 2008.
Tartally, A.; Rodrigues, M.C.; Brakels, P.; Arnaldo, P.S. Myrmica aloba (Hymenoptera: Formicidae) hosts
isolated populations of a hoverfly, a butterfly and an ichneumon species in NE-Portugal. J. Insect Conserv.
2013, 17, 851–855. [CrossRef]
Tartally, A.; Koschuh, A.; Varga, Z. The re-discovered Maculinea rebeli (Hirschke, 1904): Host ant usage,
parasitoid and initial food plant around the type locality with taxonomical aspects (Lepidoptera, Lycaenidae).
Zookeys 2014, 406, 25–40. [CrossRef]
Thomas, J.A.; Clarke, R.T.; Elmes, G.W.; Hochberg, M.E. Population dynamics in the genus Maculinea
(Lepidoptera: Lycaenidae). In Insect Population Dynamics: In Theory and Practice; Dempster, J.P., McLean, I.F.G.,
Eds.; Symposia of the Royal Entomological Society 19; Chapman & Hall: London, UK, 1998; pp. 261–290.
ISBN 978-0412832604.
Tartally, A.; Nash, D.R.; Varga, Z.; Lengyel, S. Changes in host ant communities of Alcon Blue butterflies in
abandoned mountain hay meadows. Insect Conserv. Divers. 2019, 12, 492–500. [CrossRef]
Hochberg, M.E.; Elmes, G.W.; Thomas, J.A.; Clarke, R.T. Effects of habitat reduction on the persistence of
Ichneumon eumerus (Hymenoptera: Ichneumonidae), the specialist parasitoid of Maculinea rebeli (Lepidoptera:
Lycaenidae). J. Insect Conserv. 1998, 2, 59–66. [CrossRef]
Munguira, M.L.; Martín, J. Action Plan for the Maculinea Butterflies in Europe; Nature and Environment, No.
97; Council of Europe Publishing: Strasbourg, France, 1999; ISBN 978-9287139931.
Anton, C.; Musche, M.; Settele, J. Spatial patterns of host exploitation in a larval parasitoid of the predatory
Dusky Large Blue, Maculinea nausithous. Basic Appl. Ecol. 2007, 8, 66–74. [CrossRef]
Insects 2020, 11, 687
15 of 15
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