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Interspecific relationships in co-occurring populations of social parasites and their host ants
Abstract
Myrmica ant colonies host numerous insect species, including the larvae of Maculinea butterflies and Microdon myrmicae hoverflies. Little is known about the interspecific relationships among these social parasites and their host ants occurring in sympatric populations. We investigated communities of social parasites to assess the strategies allowing them to share the same pool of resources (i.e. Myrmica colonies). The present study was carried out at five sites inhabited by different social parasite communities, each comprising varying proportions of Maculinea teleius, Maculinea nausithous, Maculinea alcon, and Microdon myrmicae. We investigated their spatial distributions, host segregation, the degree of chemical similarity between social parasites and hosts, and temporal overlaps in colony resource exploitation. Spatial segregation among social parasites was found in two populations and it arises from microhabitat preferences and biological interactions. Local conditions can drive selection on one social parasite to use a Myrmica host species that is not exploited by other social parasites. Myrmica scabrinodis and Myrmica rubra nests infested by larvae of two social parasite species were found and the most common co-occurrence was between Ma. teleius and Mi. myrmicae. The successful coexistence of these two species derives
from their exploitation of the host colony resources at different times of the year. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 699–709.
ADDITIONAL KEYWORDS: competition – cuticular hydrocarbons – host–parasite interaction – Maculinea
– Microdon – Myrmica.
INTRODUCTION
Social parasites
... Data on the CHC profiles have shown that the post-adoption larvae of predatory M. teleius do not achieve the same level of chemical integration as cuckoo caterpillars. In a study conducted on two Polish populations the level of chemical similarity of the parasite caterpillars varied between 32 and 60% depending on the host species considered (Witek et al., 2013). This is in line with the fact that M. teleius is the most generalist species of the genus and is usually less locally specific to single Myrmica host (Witek et al., 2014;Tartally et al., 2019). ...
... Differently from cuckoo M. alcon, whose larvae acquire a limited number of CHCs (at maximum 28 peaks in the post-adoption phase), M. teleius caterpillars showed very complex profiles which ranged from 57 CHC peaks to more than 70, i.e., almost double than shown in the CHC profile of Myrmica workers. These results, even if derived from a limited number of samples, suggest that the predatory species may have evolved a different mechanism of integration, possibly based on the acquisition of compounds by contact with the host species or by feeding on the ant brood (Witek et al., 2013). ...
... Nevertheless, M. nausithous caterpillars do not acquire the same degree of chemical similarity as M. alcon does within its host colonies. This level (43%) is also lower than that of the M. teleius larvae, sharing the same M. rubra colonies, but higher than M. teleius caterpillars exploiting other Myrmica ants (Witek et al., 2013). In addition, its CHC profile seems intermediate between those of cuckoo and predatory species, suggesting that it may have evolved an intermediate strategy based both on mimicry of the host CHC profile and on chemical camouflage (Patricelli et al., 2010). ...
Ant nests and their surrounding territories represent a hoard of trophic resources, as well as of stable and protected environments for many arthropods involved in commensal, mutualistic, or parasitic associations. Among these organisms, called myrmecophiles, several are butterflies. Here, we explore the amazing diversity of strategies developed by myrmecophilous butterflies to “cheat” or manipulate ants and to elude the tough defenses of the colony. During oviposition, female butterflies use visual or plant volatile signals to identify the presence of ants, whereas chemical and vibroacoustic cues, either isolated or combined, are used by larvae and pupae to attract, deceive, or appease workers. Examples of mimicry and eavesdropping on both intraspecific and interspecific signals are discussed, primarily referring to the obligate-parasitic interactions involving Maculinea butterflies and Myrmica ants. Multimodal communication is crucial to maintaining the strong cohesion and social structure of ant societies, but its corruption is at the base of the evolution and persistence of interspecific associations, which can be beneficial or detrimental for the colony's fitness. In this framework, the remarkable complexity of signaling could have prompted the evolution of specialized life cycles enhancing the extraordinary butterfly diversity.
... Imperfect CHC mimicry in myrmecophileant systems is common, but the ultimate and proximate mechanisms behind a weak chemical host resemblance mostly remain speculative. Carrying only small quantities of CHCs compared to host ants has often been suggested to hamper recognition due to an inability of host ants to detect these cues (chemical insignificance sensu [19]; chemical hiding sensu [85]) (e.g., woodlice/ mites/phorid flies: [91]; syrphid flies: [92]; silverfish: [93]). On the contrary, the presence of only a few host CHCs in low quantities with slight compositional differences to the host has been suggested as a strategy of two parasitoid wasps to be detected by host ants [94]. ...
... In contrast to many of the unspecialized myrmecophiles of red wood ants [17], for example, the CHC profiles of Tetradonia beetles still resembled the CHC profiles of host ants fairly well in that they carried the exact same CHCs as host ants without possessing any idiosyncratic CHCs. The latter phenomenon is common among social insect symbionts (e.g., beetles: [95,96]; eucharitid wasps: [94,97]; silverfish: [41,98]; spiders: [58,98,99]; syrphid flies: [92,100]), most likely because a symbiont possessing components absent in the host cuticular profile would facilitate being recognized as an intruder. A very similar pattern to Tetradonia's chemical resemblancesame CHCs as host ants in non-integrated specieswas previously detected in staphylinid parasites of Southeast-Asian Leptogenys army ants [59,91]. ...
... We have compared the level of specialization in terms of social and chemical integration between army antassociated beetle specialists and beetle generalists. Our results support the hypothesis that the evolution of host-specialization in parasites is a trade-off between the range of potential host species and the level of specialization (see also [92]). However, the present study only focused on two beetle groups, and species within the groups were phylogenetically closely related. ...
Host-symbiont interactions are embedded in ecological communities and range from unspecific to highly specific relationships. Army ants and their arthropod guests represent a fascinating example of species-rich host-symbiont associations where host specificity ranges across the entire generalist - specialist continuum. In the present study, we compared the behavioral and chemical integration mechanisms of two extremes of the generalist - specialist continuum: generalist ant-predators in the genus Tetradonia (Staphylinidae: Aleocharinae: Athetini), and specialist ant-mimics in the genera Ecitomorpha and Ecitophya (Staphylinidae: Aleocharinae: Ecitocharini). Similar to a previous study of Tetradonia beetles, we combined DNA barcoding with morphological studies to define species boundaries in ant-mimicking beetles. This approach found four ant-mimicking species at our study site at La Selva Biological Station in Costa Rica. Community sampling of Eciton army ant parasites revealed that ant-mimicking beetles were perfect host specialists, each beetle species being associated with a single Eciton species. These specialists were seamlessly integrated into the host colony, while generalists avoided physical contact to host ants in behavioral assays. Analysis of the ants’ nestmate recognition cues, i.e. cuticular hydrocarbons (CHCs), showed close similarity in CHC composition and CHC concentration between specialists and Eciton burchellii foreli host ants. On the contrary, the chemical profiles of generalists matched host profiles less well, indicating that high accuracy in chemical host resemblance is only accomplished by socially integrated species. Considering the interplay between behavior, morphology, and cuticular chemistry, specialists but not generalists have cracked the ants’ social code with respect to various sensory modalities. Our results support the long-standing idea that the evolution of host-specialization in parasites is a trade-off between the range of potential host species and the level of specialization on any particular host.
Electronic supplementary material
The online version of this article (10.1186/s12983-018-0249-x) contains supplementary material, which is available to authorized users.
... In our definition, integrated species are able to penetrate into the dense brood chambers, whereas non-integrated species occur in sparsely populated nest chambers without brood at the periphery of the nest. There are indications that intraguild competition among social insect parasites can cause temporal niche specialization [13]. Alternatively, niche specialization can develop by a differential degree of tolerance of the host towards the symbionts. ...
... In several multi-symbiont systems, it has been reported that symbionts are not homogenously distributed within the host system but occupy different spatial and temporal niches [10,13,37]. This is further supported by our data on red wood ant symbionts. ...
... Niche selection in multiple symbiont systems can result from avoiding competition with other symbionts (described as niche partitioning) [4,13]. However, in several host-multiparasite systems, it has been reported that the host adjusts its defence to the potential negative impact of the symbiont [7][8][9][10]. ...
Background
A host infected with multiple parasitic species provides a unique system to test evolutionary and ecological hypotheses. Different parasitic species associated with a single host are expected to occupy different niches. This niche specialization can evolve from intraguild competition among parasites. However, niche specialization can also be structured directly by the host when its defence strategy depends on the parasite’s potential impact. Then it can be expected that species with low or no tendency to prey on host brood will elicit less aggression than severe brood parasitic species and will be able to integrate better in the host system.
We examined this hypothesis in a large community of symbionts associated with European red wood ants (Formica rufa group) by testing the association between 1) level of symbiont integration (i.e. presence in dense brood chambers vs. less populated chambers without brood) 2) level of ant aggression towards the symbiont 3) brood predation tendency of the symbiont.
Results
Symbionts differed vastly in integration level and we demonstrated for the first time that relatively unspecialized ant symbionts or myrmecophiles occur preferentially in brood chambers. Based on their integration level, we categorize the tested myrmecophiles into three categories: 1) species attracted to the dense brood chambers 2) species rarely or never present in the brood chambers 3) species randomly distributed throughout the nest. The associates varied greatly in brood predation tendency and in aggression elicited. However, we did not find a correlation for the whole myrmecophile community between a) brood predation tendency and host’s aggression b) integration level and host’s aggression c) integration level and brood predation tendency.
Conclusions
Our results indicate that red wood ants did not act more hostile towards species that have a high tendency to prey on brood compared to species that are less likely or do not prey on brood. We show that potentially harmful parasites can penetrate into the deepest parts of a social insect fortress. We discuss these seemingly paradoxical findings in relation to models on coevolution and evolutionary arms races and list factors which can make the presence of potentially harmful parasites within the brood chambers evolutionary stable.
... infected with R. wasmannii and parasitized by P. alcon was lower than expected if the two parasites were acting independently of each other. This pattern has also previously been found for co-infection of Myrmica colonies by different Phengaris species and/or Microdon myrmicae 24,25 .We also found that prepupal caterpillars of P. alcon were larger in nests where some caterpillars had already pupated, and there was a tendency for prepupal caterpillars to be larger in infected than uninfected ant nests ( Fig. 9). Putting these pieces of evidence together suggests that infection of an ant colony by R. wasmannii has a disproportionately large effect on the survival and development of smaller caterpillars of P. alcon, but rather little effect on larger caterpillars; this is what results in the somewhat larger sizes of prepupal caterpillars in infected nests. ...
... For wintering (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24) April, see below for details), the nests were moved to a climate-controlled chamber where the temperature was gradually decreased to 7 ± 2 °C, and then increased back to 22 ± 1 °C at the end of winter (Fig. 4). ...
Exploitation of organisms by multiple parasite species is common in nature, but interactions among parasites have rarely been studied. Myrmica ants are rich in parasites. Among others, the ectoparasitic Rickia wasmannii fungus and the parasitic caterpillars of myrmecophilous Phengaris butterflies often infect the same Myrmica colonies. In this study, we examined the effects of R. wasmannii on the adoption, long-term development, and survival of P. alcon. In laboratory conditions, caterpillars introduced into nests of Myrmica scabrinodis uninfected with R. wasmannii survived significantly longer compared to caterpillars introduced into infected nests. In the field, joint infection was less common than expected if both parasites exploited M. scabrinodis colonies independently. Pre-pupal caterpillars of P. alcon were somewhat larger in nests infected with R. wasmannii than those found in uninfected nests. Based on these results it seems that R. wasmannii infection of M. scabrinodis affects the survival and development of P. alcon caterpillars, suggesting competition between these two ant parasites.
... Myrmica individuals can be infected by parasitoid wasps (Hymenoptera: Eucharitidae and Ichneumonidae) and ies (Diptera: Phoridae), endoparasitic nematodes (Mermithidae, Rhabditidae and Steinernematidae), ecto-and endoparasitic fungi, and various bacteria [16][17][18][19] . While there is some information on the co-infection levels of Myrmica nests by different species of Phengaris butter ies and Microdon myrmicae 20,21 the consequences of these co-infections for the parasites themselves is poorly understood. ...
... When we examined colonies of M. scabrinodis in the eld, we found that the number of colonies simultaneously infected with R. wasmannii and parasitized by P. alcon was lower than expected if the two parasites were acting independently of each other. This pattern has also previously been found for co-infection of Myrmica colonies by different Phengaris species and/or Microdon myrmicae 20,21 .We also found that prepupal caterpillars of P. alcon were larger in nests where some caterpillars had already pupated, and there was a tendency for prepupal caterpillars to be larger in infected than uninfected ant nests (Fig. 9). ...
Exploitation of organisms by multiple parasite species is common in nature, but interactions among parasites have rarely been studied. Myrmica ants are rich in parasites. Among others, the ectoparasitic Rickia wasmannii fungus and the socially parasitic caterpillars of myrmecophilous Phengaris butterflies often infect the same Myrmica colonies. In this study, we examined the effects of R. wasmannii on the adoption, long-term development, and survival of P. alcon . In laboratory conditions, caterpillars introduced into nests of Myrmica scabrinodis uninfected with R. wasmannii survived significantly longer compared to caterpillars introduced into infected nests. In the field, joint infection was less common than expected if both parasites exploited M. scabrinodis colonies independently. Pre-pupal caterpillars of P. alcon were somewhat larger in nests infected with R. wasmannii than those found in uninfected nests. Based on these results it seems that R. wasmannii infection of M. scabrinodis affects the survival and development of P. alcon caterpillars, suggesting competition between these two ant associates.
... Mass spectral data were acquired in full scan mode over a range of 40 -600 m/z. Integration of chromatograms and the analysis of hydrocarbon was made following procedures described by Witek et al., (2013) 64 . The quantitative analyses were performed by GC coupled to a Flame Ionization Detector (FID) by using a Shimadzu gaschromatograph hi (GC-2010 Plus) at the same conditions and using the same column as described above. ...
... Mass spectral data were acquired in full scan mode over a range of 40 -600 m/z. Integration of chromatograms and the analysis of hydrocarbon was made following procedures described by Witek et al., (2013) 64 . The quantitative analyses were performed by GC coupled to a Flame Ionization Detector (FID) by using a Shimadzu gaschromatograph hi (GC-2010 Plus) at the same conditions and using the same column as described above. ...
The cuticular hydrocarbon (CHC) profile reflects the insect’s physiological states. These states include age, sex, reproductive stage, or gravidity. Environmental factors such as diet, relative humidity, or exposure to insecticides also affect the CHCs composition in mosquitoes. In this work, the CHC profile was analyzed in two Anopheles albimanus phenotypes with different degrees of susceptibility to Plasmodium : the susceptible-White and resistant-Brown phenotypes. The effects of the CHC profile were considered under a carbon-rich diet (sugar), a protein-rich diet (blood), and an infectious challenge (blood containing Plasmodium berghei ookinetes). The CHCs were analyzed by gas chromatography coupled with either mass spectrometry or flame ionization detection, identifying 19 CHCs with chain lengths ranging from 20 to 37 carbons. The qualitative and quantitative changes observed in the CHCs composition were dependent on the diet and parasite challenge, and independent of the phenotype. The exception was the challenged condition, where significant differences between the phenotypes were observed in Z-12 pentacosane, hexacosane 9-octyl, methyl-nonacosane, and methyl-hentriacontane. Since the lipid metabolism in Anopheles mosquitoes has been shown crucial for Plasmodium development, the changes in the CHC profiles associated with infection could have multiple effects on mosquito fitness and impacts on disease transmission.
... Interestingly, the survival of M. teleius larvae reared by colonies from infested, allopatric populations was similar to that obtained from colonies of the sympatric population and significantly higher than in one allopatric, unifested population. Our previous data collected on the variability of cuticular hydrocarbon profiles of M. scabrinodis from Kosyń and Kraków did not show a significant difference between the ant populations (Witek et al. 2013). Similarly, no difference was found for M. teleius larvae originating from these two sites, but we collected postadopted butterfly larvae (Witek et al. 2013). ...
... Our previous data collected on the variability of cuticular hydrocarbon profiles of M. scabrinodis from Kosyń and Kraków did not show a significant difference between the ant populations (Witek et al. 2013). Similarly, no difference was found for M. teleius larvae originating from these two sites, but we collected postadopted butterfly larvae (Witek et al. 2013). We do not have any data on the ant chemical profiles of the uninfested, allopatric populations, so we can only suppose that the cuticular hydrocarbon profiles of M. teleius larvae became more similar to infested ant populations compared to the ants from uninfested populations. ...
The arms race between Maculinea butterflies and Myrmica host ants leads to local host-parasite adaptations. In our study, we assessed whether sympatric and allopatric Myrmica scabrinodis populations exhibit behavioural differences towards Maculinea teleius larvae during the adoption-period when butterfly larvae need to be taken inside the Myrmica nest. The second aim was to assess the butterfly survival rate inside ant colonies from different populations. We used one sympatric host population and three allopatric populations: one infested by M. teleius and two uninfested populations. We found that ants from the sympatric population showed a higher number of positive behaviours toward M. teleius larvae during adoption than ants from the allopatric populations. There were no differences in the number of inspection or negative behaviour events. The survival of butterfly larvae was highest inside sympatric host colonies and differed from the survival of M. teleius reared by ants from the allopatric, uninfested populations. No difference was found for the survival rate of M. teleius raised by infested, allopatric host colonies compared to sympatric host populations. Our results suggest the lack of behavioural counter-adaptations of local hosts of M. teleius that more easily adopt and rear butterfly caterpillars compared to naive M. scabrinodis colonies. Our results may also have implications for Maculinea butterfly conservation, especially for reintroduction programmes. We suggest that the existence of behavioural host defences should be checked for the source host population, as well as for the Myrmica population from the reintroduction site. It may also be reasonable to introduce several Myrmica host colonies from the source butterfly host population.
... Studies on postadoption changes in the chemical signatures of Maculinea larvae and Myrmica hosts are scarce (e.g. Witek et al., 2013b), but we may assume that selection on hosts to avoid being parasitized fuels the co-evolutionary arms races, in which parasites evolve better mimicry and hosts improve their recognition of parasites (Foitzik et al., 2003). ...
... Moreover, these authors strongly suggest that the chemical mimicry of syrphid fly larvae is mediated by the biosynthesis of particular hydrocarbons (normal alkanes from C 22 to C 29 , a few methylalkanes and two alkenes, among others). In contrast, the chemical profile of Mi. myrmicae larvae is very poor, with an average of eight hydrocarbon peaks (Witek et al., 2013b). This low number of compounds, together with their low concentration, indicates that Mi. myrmicae might use the 'chemical insignificance' strategy (sensu Lenoir et al., 2001) to penetrate the host colony. ...
Myrmica ants have been model species for studies in a variety of disciplines, including insect physiology, chemical communication, ant social dynamics, ant population, community ecology, and ant interactions with other organisms. Species belonging to the genus Myrmica can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and systematics have been thoroughly studied. These ants serve as hosts to highly diverse parasitic organisms from socially parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in colony fitness. A comprehensive review of the parasitic organisms supported by Myrmica and the effects of these organisms on individuals and on whole ant colonies has not yet been compiled. Here, we provide a review of the interactions of these organisms with Myrmica ants by discussing host and parasite functional, behavioral or physiological adaptations. In addition, for all “symbiont groups” of Myrmica ants described in this paper, we examine the present limitations of the knowledge at present of their impact on individuals and host colony fitness. In conclusion, we argue that Myrmica ants serve as remarkable resource for the evolution of a wide variety of associated organisms.
M. Witek and F. Barbero equally contributed to the manuscript.
... Various authors [23,[29][30] have found evidence that chemical mimicry is used by Maculinea cuckoo species to bypass their host ants' recognition system. For predatory species only post-adoption data are available [31] showing that chemical mimicry is less specific than for cuckoo species. Only recently, the first case of acoustical mimicry in an ant social parasite has been demonstrated in the Maculinea rebeli/Myrmica schencki system [12] following a pilot study by DeVries et al. [32]. ...
... Maculinea alcon, Maculinea teleius and Microdon myrmicae, all of which exploit only one Myrmica species, M. scabrinodis [36]. Adults of the two Maculinea butterflies overlap in time and space and their initial food plants, respectively Gentiana pneumonanthe and Sanguisorba officinalis, grow largely in the same meadow, so that larvae of the two species could parasitize the same colony [31]. This co-occurrence represents a key factor in the regulation of the population dynamics of the two species [37]. ...
About 10,000 arthropods live as ants' social parasites and have evolved a number of mechanisms allowing them to penetrate and survive inside the ant nests. Many of them can intercept and manipulate their host communication systems. This is particularly important for butterflies of the genus Maculinea, which spend the majority of their lifecycle inside Myrmica ant nests. Once in the colony, caterpillars of Maculinea "predatory species" directly feed on the ant larvae, while those of "cuckoo species" are fed primarily by attendance workers, by trophallaxis. It has been shown that Maculinea cuckoo larvae are able to reach a higher social status within the colony's hierarchy by mimicking the acoustic signals of their host queen ants. In this research we tested if, when and how myrmecophilous butterflies may change sound emissions depending on their integration level and on stages of their life cycle. We studied how a Maculinea predatory species (M. teleius) can acoustically interact with their host ants and highlighted differences with respect to a cuckoo species (M. alcon). We recorded sounds emitted by Maculinea larvae as well as by their Myrmica hosts, and performed playback experiments to assess the parasites' capacity to interfere with the host acoustic communication system. We found that, although varying between and within butterfly species, the larval acoustic emissions are more similar to queens' than to workers' stridulations. Nevertheless playback experiments showed that ant workers responded most strongly to the sounds emitted by the integrated (i.e. post-adoption) larvae of the cuckoo species, as well as by those of predatory species recorded before any contact with the host ants (i.e. in pre-adoption), thereby revealing the role of acoustic signals both in parasite integration and in adoption rituals. We discuss our findings in the broader context of parasite adaptations, comparing effects of acoustical and chemical mimicry.
... The alimentary strategy of Maculinea nausithous has not yet been fully clarified, but some authors suggest the coexistence of both "cuckoo" and "predatory" strategies or the predominance of the "cuckoo" behaviour (Thomas & Settele 2004;Patricelli et al. 2010). Irrespective of the species, Maculinea larvae spend 11 or 23 months inside their host colonies mimicking their host ants by both chemical and acoustical cues Barbero et al. 2009aBarbero et al. , 2009bBarbero et al. 2012;Witek et al. 2013). ...
... On leaving its food plant, M. rebeli secretes a simple mixture of surface hydrocarbons that weakly mimic those of its host Myrmica ant, but it is sufficiently similar to all other Myrmica species for the larvae to be quickly retrieved by the first ant worker coming by. After adoption, the intruding larvae successfully integrate within colonies of the model host species, by synthesizing additional hydrocarbons that more precisely mimic their Myrmica host Witek et al. 2013). By contrast, caterpillars adopted within nests of other Myrmica species suppress their secretions and rely on the passive acquisition of their current host colony odour ). ...
Abstract
Although most conservationists claim to protect “species”, the conservation unit actually and practically managed is the
individual population. As resources are not unlimited, we need to focus on a restricted number of populations. But how can
we select them? The Evolutionarily Significant Unit (ESU), first conceptualised by Ryder in 1986, may offer some answer.
Several definitions have been proposed for the ESU, but all make reference to units “whose divergence can be measured or
evaluated by putting differential emphasis on the role of evolutionary forces at varied temporal scales”. Thus, an ESU might
be fully identical with a “species”, or a “species” could be composed of multiple ESUs. On the other hand, an ESU might
comprise single/multiple populations exchanging a degree of gene flow, such as meta-populations. In an attempt to show
strengths and weaknesses of ESU concepts, we present here, among several others, some case studies on the myrmecophilous
butterflies of the genus Maculinea. In particular, we analyse the apparently everlasting debate about Maculinea alcon and
M. rebeli, whose separation into separate species has been accepted by many authors, on mainly ecological criteria, but has
not been fully supported by molecular analyses. We also discuss how the tight association with host ants may have driven
selection for increasingly more strictly adapted Maculinea populations, arguably deserving specific taxonomic identity.
Finally we discuss how current DNA analyses may fail to detect critical information on differences between taxa recently
originated by the action of separate adaptive processes, which non-molecular studies can sometimes reveal. We conclude by
discussing some current and often conflicting taxonomic trends, in their relationships with conservation policies.
... Additionally, S. calyce caterpillars have facultative association with several species of ants, and they do not exploit ant nests (Callaghan 1986;Alves-Silva et al. 2018;Kaminski 2021). Previous studies demonstrating chemical mimicry between caterpillars and ants have typically involved obligate interactions with a few specific ant species, where the CHCs of caterpillars closely resemble those of the ants (Henning 1983;Elmes et al. 1991Elmes et al. , 2002Dettner and Liepert 1994;Akino et al. 1999;Schönrogge et al. 2004;Hojo et al. 2009Hojo et al. , 2014Thomas et al. 2013;Witek et al. 2013;Barbero 2016;Casacci et al. 2019). Chemical mimicry with attendant ants is an effective strategy for social parasitic caterpillars, as they typically inhabit ant nests and benefit from being perceived as members of the colony, allowing them to exploit valuable resources within the nest such as ant larvae or trophallaxis (Fiedler 1991;Barbero 2016;Casacci et al. 2019). ...
In myrmecophilous organisms, which live in symbiosis with ants, cuticular hydrocarbons (CHCs) play a pivotal role in interspecific communication and defense against chemical-oriented predators. Although these interactions form complex information webs, little is known about the influence of biotic environmental factors on the CHC profiles of myrmecophiles. Here, we analyzed the effect of different host plants and tending ants on the larval CHC profile of Synargis calyce (Lepidoptera: Riodinidae), a polyphagous species with facultative myrmecophily. Groups of caterpillars were fed individually with three host plant species (without tending ants), and with two tending ant species. Through gas chromatography analysis, we compared the cuticular profiles of treatments and found a high similarity between plants and caterpillars (65–82%), but a low similarity between caterpillars and their tending ants (30 − 25%). Cluster analysis showed that caterpillars, ants, and plants form distinct groups, indicating that S. calyce caterpillars have their own chemical profile. These results are similar to those observed for Lycaenidae caterpillars indicating that there is functional convergence in the chemical strategies used by myrmecophilous caterpillar species with similar ecology. Also, the results suggest that the cuticular compounds of S. calyce are primarily influenced by their host plants rather than their tending ants. Thus, we propose that these caterpillars present a trade-off between camouflage and directly informing their presence to ants, maintaining their unique chemical profile, though slightly affected by biotic environmental factors.
... 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. ...
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.
... Mass spectral data were acquired in full scan mode over a range of 40-600 m/z. Integration of chromatograms and the analysis of hydrocarbon was made following the procedures described by Witek et al. 62 . The quantitative analysis of epicuticular hydrocarbons was performed by GC coupled to a Flame Ionization Detector (FID) by using a Shimadzu gas chromatograph (GC-2010 Plus) at the same conditions and using the same column as described above. ...
The cuticular hydrocarbon (CHC) profile reflects the insects’ physiological states. These include age, sex, reproductive stage, and gravidity. Environmental factors such as diet, relative humidity or exposure to insecticides also affect the CHC composition in mosquitoes. In this work, the CHC profile was analyzed in two Anopheles albimanus phenotypes with different degrees of susceptibility to Plasmodium, the susceptible-White and resistant-Brown phenotypes, in response to the two dietary regimes of mosquitoes: a carbon-rich diet (sugar) and a protein-rich diet (blood) alone or containing Plasmodium ookinetes. The CHCs were analyzed by gas chromatography coupled to mass spectrometry or flame ionization detection, identifying 19 CHCs with chain lengths ranging from 20 to 37 carbons. Qualitative and quantitative changes in CHCs composition were dependent on diet, a parasite challenge, and, to a lesser extent, the phenotype. Blood-feeding caused up to a 40% reduction in the total CHC content compared to sugar-feeding. If blood contained ookinetes, further changes in the CHC profile were observed depending on the Plasmodium susceptibility of the phenotypes. Higher infection prevalence caused greater changes in the CHC profile. These dietary and infection-associated modifications in the CHCs could have multiple effects on mosquito fitness, impacts on disease transmission, and tolerance to insecticides.
... These species show highly peculiar parasitic interactions with ants (e.g. Witek et al. 2013;Filz and Schmitt 2015), but also their beauty was scored well above average in our enquiry. Due to their specific and highly sensitive life cycles, these species are vanishing across Europe, and consequently they are red-listed (Van Swaay et al. 2010). ...
Prioritization is crucial in nature conservation, as land and financial resources are limited. Selection procedures must follow objective criteria, and not primarily subjective aspects, such as charisma. In this study, we assessed the level of charisma for all European butterflies. Based on these data, we analysed the charisma values of the species listed on the annexes of the EU Habitats Directive and of the species being of conservation priority according to criteria derived by three objective criteria: Species ecological specialisation, distribution, and threat. The mean level of charisma was higher for species of the EU Habitats Directive than for species of conservation priority and for not-listed species. Five of the twenty most charismatic species were also listed on the EU Habitats Directive, but none occurred on the list of species being of conservation priority. A trait space analysis revealed remarkable differences between the different species assortments: The species listed on the EU Habitats Directive covered a large trait space and included many species with high charismatic value, but low ecological and biogeographical relevance, while species of high conservation priority covered a restricted trait space and did not overlap with charismatic species. According to our findings, the selection of species for nature conservation still follows a mix of being aesthetic combined with some ecological criteria.
... This habitat specificitypreference for Myrmica nests and habitat choices can explain the wide distribution on multiple Myrmica species and ant nest inquilines [53]. Moreover, the fact that there is overlap and even contact between Myrmica populations of different species [78] implies that regular or at least sufficient interspecific transfer of R. wasmannii occurs between host taxa. It also means that the different host taxa, their specific habitat choices, and the nature of their nests, allow the development of the fungus population. ...
Fungal species identities are often based on morphological features, but current molecular phylogenetic and other approaches almost always lead to the discovery of multiple species in single morpho-species. According to the morphological species concept, the ant-parasitic fungus Rickia wasmannii (Ascomycota, Laboulbeniales) is a single species with pan-European distribution and a wide host range. Since its description, it has been reported from ten species of Myrmica (Hymenoptera, Formicidae), of which two belong to the rubra-group and the other eight to the phylogenetically distinct scabrinodis-group. We found evidence for R. wasmannii being a single phylogenetic species using sequence data from two loci. Apparently, the original morphological description (dating back to 1899) represents a single phylogenetic species. Furthermore, the biology and host-parasite interactions of R. wasmannii are not likely to be affected by genetic divergence among different populations of the fungus, implying comparability among studies conducted on members of different ant populations. We found no differences in total thallus number on workers between Myrmica species, but we did observe differences in the pattern of thallus distribution over the body. The locus of infection is the frontal side of the head in Myrmica rubra and M. sabuleti whereas in M. scabrinodis the locus of infection differs between worker ants from Hungary (gaster tergites) and the Netherlands (frontal head). Possible explanations for these observations are differences among host species and among populations of the same species in (i) how ant workers come into contact with the fungus, (ii) grooming efficacy, and (iii) cuticle surface characteristics.
© D. Haelewaters et al., published by EDP Sciences, 2019.
... Despite using the same major hosts as Ma. alcon H, it does not seem to be able to use the related Myrmica species in the same way, suggesting that it does not rely on the same type of cuticular mimicry to gain access to its food [127]. This is possibly because its apparent need, when small, to eat ant eggs in the heavily protected host chambers that contain queens [40] requires closer host-specific mimicry of its main host that is simply ineffective with other Myrmica species. ...
The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris ) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe.
This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.
... Yet the low level of chemical similarity, coupled with poor discrimination by foraging workers, means that P. rebeli pre-adoption caterpillars are retrieved into nests by workers of any foraging Myrmica species that happen to encounter them 10,11,14,15 . Once inside ant colonies, the mimetic cocktail of hydrocarbons synthesised by caterpillars becomes more complex 11,15,16 , which, aided by acoustical mimicry [17][18][19] , not only enables the parasites to integrate closely with the societies of their primary ant host species but also identifies them as intruders to "non-host" species, where, in due course, either all or the large majority of individuals are killed or ejected by the more discriminatory nurse-workers 11,15,20,21 . Inside host ant nests, Phengaris larvae are fed mainly by the regurgitations of nurse ants, gaining about the 98% of their final body mass 4 over a period of either 11 or 23 months 4 , the result of a developmental polymorphism that exists in some populations. ...
In natural ecosystems, relationships between organisms are often characterised by high levels of complexity, where vulnerabilities in multi-trophic systems are difficult to identify, yet variation in specific community modules can be traceable. Within the complex community interactions, we can shed new light on dynamics by which co-evolutionary outcomes can inform science-led conservation. Here we assessed host-ant use in six populations of the butterfly Phengaris (=Maculinea) rebeli, an obligate social parasite of Myrmica ants and a model system in evolutionary and conservation ecology. Starting from the initial distribution of eggs, we estimated the survival of the parasite in the wild in nests of seven Myrmica ant species, and analysed the chemical cues evolved by the parasites to subvert its host defences. We found local variations in host specificity that are consistent with similarities found in the chemical profiles of hosts and parasites on different sites. At some sites, only one ant species is successfully exploited; at others, multiple-host populations are used. Understanding how stable or adaptable these associations are is essential knowledge when devising conservation measures to maintain keystone species of ant and locally adapted populations of Phengaris butterfly species, which are rare, threatened and a high priority for conservation worldwide.
... respectively, thanks to their ability to mimic ant brood CHC profile (Niphanda fusca [145]; Maculinea spp. [45,46,[146][147][148][149][150]). Once inside the host colony the epicuticular composition of N. fusca larvae gets a closer match of male ant profile by acquiring, through camouflage, specific blends of CHCs. ...
Even though insects and plants are distantly related organisms, they developed an integument which is functionally and structurally similar. Besides functioning as a physical barrier to cope with abiotic and biotic stress, this interface, called cuticle, is also a source of chemical signaling. Crucial compounds with this respect are surface lipids and especially cuticular hydrocarbons (CHCs). This review is focused on the role of CHCs in fostering multilevel relationships among ants, plants and Lepidoptera (primarily butterflies). Indeed, particular traits of ants as eusocial organisms allowed the evolution and the maintenance of a variety of associations with both plants and animals. Basic concepts of myrmecophilous interactions and chemical deception strategies together with chemical composition, biosynthetic pathways and functions of CHCs as molecular cues of multitrophic systems are provided. Finally, the need to adopt a multidisciplinary and comprehensive approach in the survey of complex models is discussed.
... alcon Denis and Schiffermüller 1775), one of the most endangered butterfly species in Europe (e.g. Munguira and Martin 1999), shows high variability in host hygrophilous ecotype in Europe [data sources: Austria (Steiner et al. 2003 and;Tartally et al. 2014);Belgium (van Dyck et al. 2000); Denmark (Als et al. 2001); Estonia (this study); France Stoeckel and Mercier 2001); Germany (Meyer-Hozak 2000; Küer and Fartmann 2005); Hungary (Tartally et al. 2008); Italy (Witek et al. 2013); Lithuania ); Netherlands (Thomas et al. 1989;Radchuk et al. 2012); Poland (Steiner et al. 2003;Stankiewicz 2004, 2007;Sielezniew et al. 2010b;Thomas et al. 2013); Portugal (Arnaldo et al. 2011); Romania (Tartally et al. 2008); Spain Thomas et al. 2013); Sweden ; Switzerland (Jutzeler 1989); Ukraine (Witek et al. 2008)] locations in Estonia where the species is known to occur. The landscape of the area is dominated by arable land and forests in which calcareous grasslands, potentially suitable for P. alcon X, form a mosaic of small discontinuous patches. ...
In myrmecophilous insects, interactions with ants are often a key factor determining persistence of their populations. Regional variation in host ant use is therefore an essential aspect to consider to provide adequate conservation practices for such species. In this study, we examined this important facet of species’ ecology in an endangered myrmecophilous butterfly Phengaris (=Maculinea) alcon (Lepidoptera, Lycaenidae). The investigations conducted in peripheral populations in Estonia allowed us to expand the knowledge of its host ant use to the northern distribution limit of the species. Our data indicate that in its northernmost populations, the xerophilous ecotype of Phengaris alcon is primarily parasitizing a single host ant species, Myrmica schencki. The data collected are in line with the emerging evidence suggesting that peripheral and core populations of P. alcon use different host ants, and peripheral populations tend to display higher host ant specificity. We also show that, at its northern range margin, P. alcon might be more limited by the availability of its sole larval food plant in the region, Gentiana cruciata, than the densities of its host ant. Finally, we found a strong negative correlation between Myrmica spp. and Lasius spp. colony densities, suggesting that interspecific competition between ants could have a substantial influence on host ant availability of Phengaris butterflies, and thus should be taken into account in conservation plans of these species.
... There are indications that intraguild competition among social insect parasites can cause temporal niche specialization (Witek et al. 2013). Alternatively, niche C H A P T E R 5 | 102 specialization can develop by a differential degree of tolerance of the host towards the symbionts. ...
... A few well-integrated myrmecophiles such as the larvae of Microdon albicomatus Novak and Microdon piperi Knab (Syrphidae), obligate predators of ant brood, attain perfect chemical mimicry by biosynthesizing de novo all of the CHCs of their hosts (Howard et al., 1990a,b) (''innate chemical mimicry'' sensu von Beeren et al., 2012b). However, it has recently been found that the chemical profile of M. myrmicae Schönrogge et al. which parasitizes several species of Myrmica, is composed of few CHCs, all at low concentrations, suggesting different strategies of social integration even in closely related species (Witek et al., 2013). Some other myrmecophiles vary in the level of social integration attained, in the aggressiveness they elicit in their ant hosts, and in their level of chemical mimicry (Lohman et al., 2006;Maruyama et al., 2009;von Beeren et al., 2011a). ...
Communication in ants is based to a great extent on chemical compounds. Recognition of intruders is primarily based on cuticular hydrocarbon (CHC) profile matching but is prone to being cheated. Eucharitid wasps are specific parasitoids of the brood of ants; the immature stages are either well integrated within the colony or are protected within the host cocoons, whereas adult wasps at emergence must leave their host nest to reproduce and need to circumvent the ant recognition system to escape unscathed. The behavioral interactions between eucharitid wasps and workers of their host, the Neotropical ant Ectatomma tuberculatum, are characterized. In experimental bioassays, newly emerged parasitoids were not violently aggressed. They remained still and were grabbed by ants upon contact and transported outside the nest; host workers were even observed struggling to reject them. Parasitoids were removed from the nest within five minutes, and most were unharmed, although two wasps (out of 30) were killed during the interaction with the ants. We analyzed the CHCs of the ant and its two parasitoids, Dilocantha lachaudii and Isomerala coronata, and found that although wasps shared all of their compounds with the ants, each wasp species had typical blends and hydrocarbon abundance was also species specific. Furthermore, the wasps had relatively few CHCs compared to E. tuberculatum (22-44% of the host components), and these were present in low amounts. Wasps, only partially mimicking the host CHC profile, were immediately recognized as alien and actively removed from the nest by the ants. Hexane-washed wasps were also transported to the refuse piles, but only after being thoroughly inspected and after most of the workers had initially ignored them. Being recognized as intruder may be to the parasitoids' advantage, allowing them to quickly leave the natal nest, and therefore enhancing the fitness of these very short lived parasitoids. We suggest that eucharitids take advantage of the hygienic behavior of ants to quickly escape from their host nests.
Copyright © 2015. Published by Elsevier Ltd.
... Altogether, 30 M. scabrinodis nests were dug up and in one of them a dealate M. karavajevi queen was found. Our previous study (Witek et al. 2013) indicated that M. scabrinodis was the most abundant Myrmica species but also other species such as M. rubra and M. gallienii were present there. In this situation it is enough to point a single spectacular morphological feature, which allow to explicitly distinguish M. karavajevi from any other Polish (and in general Central European) Myrmica species. ...
The ant Myrmica karavajevi is an extremely rarely found and poorly known workerless social parasite of ants of the Myrmica scabrinodis species group. Hereafter detailed information of its previously published findings from four geographical regions in Poland (Bieszczady Mts, Pieniny Mts, Pomeranian Lakeland and Mazovian Lowland) as well as data on three new records from the Roztocze Upland, Lubelska Upland and Krakowsko-Częstochowska Upland is given. The latter suggests higher than hitherto suspected degree of host species infestation by M. karavajevi. Use of M. rugulosa as a host by M. karavajevi is also discussed.
... 'Chemically insignificance' has been suggested to be a strategy for some intruders into the nests of social insects (Moritz et al., 1991;Lenoir et al., 2001;Witek et al., 2013). However, the present data provide support for a different strategy in the case of P. nausithous. ...
Phengaris (Maculinea) butterflies are social parasites of Myrmica ant colonies. Larvae of the parasite are adopted by the ant workers into the colonies. Apparently, chemical signals are used by Phengaris nausithous Bergsträsser larvae to mimic those of the host brood to be recognized by the ants. In the present study, chemical extracts of ant brood and butterfly larvae using four different solvents are tested in behavioural choice assays in search of compounds involved in the adoption process. Tetracosane is the main shared compound in all brood extracts of Myrmica rubra L. and in all larvae of P. nausithous. The attractiveness of tetracosane for M. rubra workers is confirmed by testing synthetic tetracosane in behavioural choice assays, suggesting that the adoption ritual may be initiated by tetracosane.
... Microdontine larvae resemble slugs or coccids, and have been described as molluscs in several instances (see Wheeler, 1908;Reemer, 2012). All of the species whose life histories are known have been found within ant nests or in their immediate vicinity (Cheng & Thompson, 2008;Reemer, 2012Reemer, , 2013a and some species are highly host-specific (Elmes et al., 1999;Witek et al., 2013). The nature of the feeding habits of the larvae of Microdontinae has long remained unclear. ...
Parasitoidism of ants by flies is known only for Phoridae and Tachinidae. We report the first record of a hoverfly (Syrphidae, Microdontinae, Hypselosyrphus) acting as a true primary parasitoid of ants. Previously, larvae of Microdontinae were known only as obligate predators of ant brood. This is also the first host record for any Hypselosyrphus species, the first reliable record of an association between a syrphid fly and a ponerine ant, and the first record of a dipteran parasitoid developing upon the immature stages of ants. We reared adults of Hypselosyrphus trigonus from cocoons of the arboreal ponerine ant, Pachycondyla villosa, nesting in Aechmea bracteata bromeliads in southern Quintana Roo, Mexico, and we succeeded in determining various aspects of the parasitoid's life history. The findings obtained in the present study provide novel insights into the evolutionary transformation and diversification of the feeding habits of microdontine syrphid larvae, from an obligatory, specific predatory association with the ant brood, to parasitoidism of ant prepupae. We also highlight the need for more detailed studies of the interactions of arboreal ants and their parasites. We conclude with an overview of the evolutionary transitions and diversification of larval feeding habits that have taken place within the family Syrphidae. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ●●, ●●–●●.
Ants use cuticular hydrocarbons (CHCs) as chemical cues for recognition, which are exploited by myrmecophiles to usufruct the benefits of the social habit. We aimed to identify the functional role of CHCs of two riodinid caterpillar species that obligately associate with different multitrophic ant-plant symbioses. Experiments of ant acceptance of caterpillars showed the concerted action of larval-ant-organs that produce liquid rewards (tentacle nectary organs, TNOs) and luring signals (anterior tentacle organs, ATOs) was key to ant appeasement and larval survival. Experiments changing the symbiosis were often lethal for the caterpillars, mainly after emptying the secretions of their TNOs and their ATOs were never activated. Chemical profiles of caterpillars were insignificant. Field bioassays with chemically insignificant palatable insect prey attracted fewer ants, indicating that insignificant cues may reduce the probability of ant attacks. Thus, caterpillars control the emission of signals of ant-organs during symbiosis, whereas the cues of CHCs are silenced. It is possible that a trade-off exists between signals under control and non-controlled cues. Chemical insignificance may allow for a crucial period for caterpillars to make tactical decisions to appease aggressive ants and could be extended to other communication channels according to the sensorial universe of the receiver.
Various organisms, especially arthropods, are able to live as parasites in ant nests and to prey upon ant broods without eliciting any aggressive behaviour in the hosts. Understanding how these intruders are able to break the ants’ communication codes in their favour represents a challenging and intriguing evolutionary question. We studied the chemical strategies of three European hoverfly species, Microdon mutabilis (parasitic on Formica cunicularia), M. analis (parasitic on Lasius emarginatus) and M. devius (parasitic on L. distinguendus). The peculiar slug-like larvae of these three species live inside ant nests feeding upon their broods. Gas chromatography-mass spectrometry analyses show that: 1) these parasites mimic the host brood rather than the ant workers, although each differs distinctly in the extent of chemical mimicry; 2) isolation experiments indicate that after 14 days the responsible cuticular hydrocarbons (CHCs) are not passively acquired but synthesized by the fly larvae. Additionally, Microdon larvae show an array of protective structural features, such as a thick and multi-layered cuticle, retractable head, dome-shaped tergum and a flat and strongly adhesive “foot” (sternum). This combination of protective chemical and structural features represents a successful key innovation by Microdon species, and one that may facilitate host switching. The results of a preliminary adoption analysis confirm that Microdon larvae of at least some species can readily be accepted by different species of ants.
We present a theory for the evolution of multiple host use in the parasite-host system Maculinea-Myrmica. A mathematical model supporting the theory is presented and some results from simulations discussed. Qualitative predictions from simulations of the model are tested using empirical data on the chemical profiles of population of hosts and parasites. The results show that increased similarity between the profiles of the host species is correlated with multiple host use, as predicted by the model. The model provides a theoretical framework which is totally coherent with: (1) patterns of host use by the Maculinea cuckoo species and (2) phylogenetic studies that suggest host shift during the evolutionary history of the species. The results also suggest that it might be possible to create a method to infer host use by the parasite species, based only on cuticular hydrocarbon profiles. Such method would be important for conservation measures.
Social insect colonies provide a valuable resource that attracts and offers shelter to a large community of arthropods. Previous research has suggested that many specialist parasites of social insects chemically mimic their host in order to evade aggression. In the present study, we carry out a systematic study to test how common such chemical deception is across a group of 22 arthropods that are associated with red wood ants (Formica rufa group). In contrast to the examples of chemical mimicry documented in some highly specialized parasites in previous studies, we find that most of the rather unspecialized red wood ant associates surveyed did not use mimicry of the cuticular hydrocarbon recognition cues to evade host detection. Instead, we found that myrmecophiles with lower cuticular hydrocarbon concentrations provoked less host aggression. Therefore, some myrmecophiles with low hydrocarbon concentrations appear to evade host detection via a strategy known as chemical insignificance. Others showed no chemical disguise at all and, instead, relied on behavioral adaptations such as particular defense or evasion tactics, in order to evade host aggression. Overall, this study indicates that unspecialized myrmecophiles do not require the matching of host recognition cues and advanced strategies of chemical mimicry, but can integrate in a hostile ant nest via either chemical insignificance or specific behavioral adaptations.
Studies investigating host-parasite systems rarely deal with multispecies interactions, and mostly explore impacts on hosts as individuals. Much less is known about the effects at colony level, when parasitism involves host organisms that form societies. We surveyed the effect of an ectoparasitic fungus, Rickia wasmannii, on kin-discrimination abilities of its host ant, Myrmica scabrinodis, identifying potential consequences at social level and subsequent changes in colony infiltration success of other organisms. Analyses of cuticular hydrocarbons (CHCs), known to be involved in insects’ discrimination processes, revealed variations in chemical profiles correlated with the infection status of the ants, that could not be explained by genetic variation tested by microsatellites. In behavioural assays, fungus-infected workers were less aggressive towards both non-nestmates and unrelated queens, enhancing the probability of polygyny. Likewise, parasitic larvae of Maculinea butterflies had a higher chance of adoption by infected colonies. Our study indicates that pathogens can modify host recognition abilities, making the society more prone to accept both conspecific and allospecific organisms.
Ant colonies provide well-protected and resource-rich environments for a plethora of symbionts. Historically, most studies of ants and their symbionts have had a narrow taxonomic scope, often focusing on a single ant or symbiont species. Here we discuss the prospects of studying these assemblies in a community ecology context using the framework of ecological network analysis. We introduce three basic network metrics that we consider particularly relevant for improving our knowledge of ant-symbiont communities: interaction specificity, network modularity, and phylogenetic signal. We then discuss army ant symbionts as examples of large and primarily parasitic communities, and symbiotic sternorrhynchans as examples of generally smaller and primarily mutualistic communities in the context of these network analyses. We argue that this approach will provide new and complementary insights into the evolutionary and ecological dynamics between ants and their many associates, and will facilitate comparisons across different ant-symbiont assemblages as well as across different types of ecological networks.
Host ant specificity of Maculinea teleius was investigated for the first time in Central Asia (northern Mongolia, Khentey Mountains). We found pupae of this butterfly just before its flying season in the nests of: Myrmica kamtschatica, M. forcipata and M. angulinodis. Soon after adoption the larva of this parasite was noted also in an M. eidmanni nest. This suggests low host specificity of M. teleius and suggests that other Myrmica species may also be suitable hosts. Our observations provide information about the presence of other Maculinea species in the investigated area and present data on M. teleius larval growth rates.
Maculinea teleius Bgstr. and M. nausithous Bgstr. larvae are obligatory social parasites of Myrmica Latr. ants spending most of their immature life inside ant nests and praying on ant brood. Studies were made to determine host-ant specificity of M. teleius and M. nausithous in Poland. Research was performed on: two isolated sites of M. teleius, one isolated site of M. nausithous and one site where populations of both species occurred as a part of the metapopulation system. Our findings showed that M. nausithous is the more specialized species living exclusively in nests of M. rubra L. while M. teleius seemed to be more plastic and adapted to local ants. Its larvae were recorded in nests of four Myrmica species with the highest frequency in M. rubra colonies. M. gallienii Bondr. was detected for the first time as a host-ant of M. teleius (or any Maculinea van Eecke species). The frequency of M. teleius larvae in M. gallienii nests was similar to that observed in M. scabrinodis Nyl. - the 'classic' host-ant of M. teleius in Europe. Results are discussed with respect to Maculinea biology and conservation.
The initially phytophagous caterpillars of Maculinea alcon and M. rebeli complete their development in Myrmica ant colonies as social parasites. Recent genetic studies show no differences at the species level among various populations of each butterfly taxa. Usually M. alcon and M. rebeli are identified by habitat and larval food plants (Gentianaceae) and host ant specificity is also considered to be an important feature. However most of the ecological characteristics overlap at least in some parts of their distributions. The developmental and survival characteristics of caterpillars reared by different Myrmica species were compared in laboratory experiments and in the field. Morphologically indistinguishable M. alcon and M. rebeli, which originated from Polish populations, are very similar in terms of host specificity i.e. larvae survived both with M. scabrinodis and M. sabuleti. However they showed different growth characteristics. The earlier flight period of M. rebeli, which is synchronized with the phenology of Gentiana cruciata, resulted from the quick growth of caterpillars in Myrmica nests in the pre-winter phase, when they gained about half of their final body biomass. After the end of winter they recommenced growth almost immediately. M. alcon larvae entered diapause shortly after adoption by ants and began to increase in weight significantly just one month after the onset of spring, which synchronized their development with that of their larval food plant, G. pneumonanthe. Therefore neither population group is transferable between habitats and should still be regarded, at least, as distinct conservational units.
In Europe there are only a few species of the syrphid fly Microdon, which live in the nests of various genera of ants. For most of these rare flies, details, of their biology, larval behaviour and relationships with their hosts are still not yet well known. In this paper we present data on the life cycle, feeding behaviour and growth pattern of Microdon myrmicae, a social parasite of Myrmica ants and compare it with two species of Maculinea butterflies similarly parasitizing Myrmica ant colonies. M myrmicae has three larval instars and overwinters as a third instar. Eggs and 1st instar larvae are ignored by ants, which indicate that they are "chemically insignificant". 2nd and 3rd instar larvae feed on small ant brood. M myrmicae larvae grow rapidly from May to July and later in the year the host colony only serves as shelter for overwintering. Like Maculinea alcon, larvae of M. myrmicae are numerous in Myrmica nests and more numerous than those of Maculinea teleius. Since the larvae of Microdon feed on an abundance of young ant brood, they experience low level of scramble competition and although many may develop in an ant's nest they have probably little effect on host colony fitness.
Of the four recognized Maculinea species that occur in Europe, three (M. teleius, M. nausithous, and M. alcon) are found on damp meadows, and may co-occur; sometimes their larval instars even occupy the same host ant nest. It is, therefore, important to be able to distinguish between the caterpillars of these species for effective conservation. We present the morphology of the larvae and pupae of these three species, and a simple key to their identification. Inter-specific differences among larvae and pupae, and within-species differences among larval instars, are underlined in order to enable their proper identification. The length, colour and distribution of bristles are considered the best features for species and instar identification. The morphology of the described species is compared with that of the other European species, M. arion.
Butterflies of the genus Phengaris have a highly specialised life cycle involving an obligatory relationship with Myrmica ants. A knowledge of the host ant specificity is essential for understanding the relationship between a particular Phengaris species and its hosts and also important for the conservation of these butterflies. Data on host ant specificity were collected in Poland, the Czech Republic, Slovakia and Ukraine. Five different Myrmica species were used by P. teleius as hosts (M. scabrinodis, M. rubra, M. ruginodis, M. rugulosa and M. gallienii) and at most localities it was not possible to distinguish a primary host - i.e. several Myrmica species were parasitized to similar extents. Three populations of P. nausithous were found in Poland and Ukraine. In every case, M. rubra was its primary host, although in the Krak-acow region (Poland) two nests of M. scabrinodis and two of M. ruginodis were infested by this butterfly species. P. alcon in the four populations investigated in Poland and Ukraine invariably only used M. scabrinodis as a host despite the presence of other Myrmica species. These results obtained suggest lack of host specificity in P. teleius and high host specificity in P. nausithous, which mainly uses M. rubra as its host across Europe. Moreover, the three populations of P. alcon investigated seem to be highly specific and use M. scabrinodis as a host, which confirms the high local specialisation of these populations.
Phengaris butterflies are social parasites of Myrmica ants. Previous studies on host ant specificity showed that P. nausithous is the most specific species among the genus and it uses M. rubra as host. Despite our relatively good knowledge of host specificity, the feeding strategy of this butterfly species inside the Myrmica host nests is still largely unknown. We collected data on host ant specificity of P. nausithous in two Polish sites during the early post-adoption larval phase and we compared them with some previous results obtained at the same sites in the end of larval development, i.e. at a time when larvae were fully integrated in their host colonies. The total number of investigated nests was 141 and they belong to four different Myrmica species. Even though the number of nests of M. rubra was proportionally very low at both sites, only colonies of this ant species were infested by P. nausithous larvae. All together 14 larvae of P. nausithous were found in 4 nests in the Kraków site, while 7 larvae were found in 4 nests in Kosyń. Our observation of such a high host ant specificity at the beginning of the in-nest larval development of P. nausithous suggests that the survival of this species during its initial integration phase is very high and similar in this to P. alcon and P. rebeli. We consider this as indirect indication that. P. nausithous is a cuckoo species. Key words: Phengaris, Myrmica, cuckoo strategy, social parasite, host-parasite integration * Note: We are fully aware that some molecular and cladistic studies indicate that Maculinea is congeneric with Phengaris. We will keep using the genus-1
In total, 58 overwintered Maculinea nausithous (BERGSTRÄSSER, 1779) larvae were found in nests of Myrmica rubra (LINNAEUS, 1758) from three sites in West Hungary. These results confirm that M. rubra is, in general, the host ant of M. nausithous. Twenty-eight larvae of M. nausithous and eight larvae of M. teleius (BERGSTRÄSSER, 1779) were found in a single M. rubra nest, which is a huge density for predacious butterfly species.
Host ant use of Maculinea teleius was investigated in 17 Hungarian and three Transylvanian (Romania) sites by opening Myrmica ant nests. A total of 856 nests of nine Myrmica species (M. contained 114 M. teleius specimens in to-tal. M. rubra and M. scabrinodis were the most frequently used host ants. M. rubra appeared to be more suitable in the western while M. scabrinodis proved to be more important in the east-ern sites. M. gallienii and M. salina were only locally important hosts on a few sites. M. specioides and M. vandeli were parasitized only once. Five Myrmica nests also contained lar-vae of other Maculinea species. These results show a less restricted host ant use of M. teleius in the central part of the Carpathian Basin than records from France. Our results correspond with the host ant use data recorded from Poland.
1. Phengaris butterflies are obligatory social parasites of Myrmica ants. Early research suggested that there is a different Myrmica host species for each of the five European Phengaris social parasites, but more recent studies have shown that this was an oversimplification.
2. The pattern of host ant specificity within a Phengaris teleius metapopulation from southern Poland is reported. A combination of studying the frequency distribution of Phengaris occurrence and morphometrics on adult butterflies were used to test whether use of different host species is reflected in larval development.
3. Phengaris teleius larvae were found to survive in colonies of four Myrmica species: M. scabrinodis, M. rubra, M. ruginodis, and M. rugulosa. Myrmica scabrinodis was the most abundant species under the host plant but the percentage of infested nests was similar to other host ant species at two sites and lower in comparison to nests of M. rubra and M. ruginodis at the other two sites. Morphometric measurements of adult butterflies reared by wild colonies of M. scabrinodis and M. ruginodis showed that wing size and number of wing spots were slightly greater for adults eclosing from nests of M. ruginodis.
4. Our results suggest that P. teleius in the populations studied is less specialised than previously suggested. The results are consistent with the hypothesis that P. teleius is expected to be the least specific of the European Phengaris species, as it has the largest and best defended fourth-instar caterpillars and, as a predatory species, it spends less time in the central larval chambers of the host colonies. The fact that individuals reared by M. ruginodis had wider hind wings may suggest that P. teleius had better access to resources in M. ruginodis than in M. scabrinodis colonies.
An important consequence of habitat fragmentation is the increase of edge habitats. Environmental factors in the edges are
different from those in the interiors, which causes changes in the distribution of plant and animal species. We aimed to study
how edges affect the distribution of two butterfly species within meadow fragments. We therefore investigated the effect of
distance from edge and edge type (road edge versus tree edge) on two sympatric large blue species (Maculinea teleius and M. nausithous). Our results showed that edge type had contrasting effects on the two species. M. teleius favoured both interiors and road edges, while M. nausithous preferred the tree edges. In the case of the latter species a strong positive edge effect was also found. This kind of within-habitat
niche segregation is probably related to the different microenvironmental conditions at the edges. Foodplant density did not
seem to limit the distribution of these species. Our results suggest that interiors of meadows are important for M. teleius, while tree edges maintain the habitats of the regionally rarer butterfly, M. nausithous.
The chemical signatures on the cuticles of five common Myrmica ant species were analysed (49 colonies of M.
rubra, M.
ruginodis, M.
sabuleti, M.
scabrinodis and M.
schencki), each ant being the specific host of one of the five threatened European species of Maculinea butterfly. The cuticular hydrocarbon profile (based on the relative abundance of each chemical) of each ant species was highly distinctive, even between the morphologically similar species M.
sabuleti and M.
scabrinodis. There was no significant difference in the chemical profiles of workers and larvae from any colony. Nor was there much pattern in the intraspecific variation: colonies from the same populations were significantly, but only slightly, more similar to each other than to colonies from distant populations. M.
rubra showed remarkably little variation between populations sampled widely from northern Russia, Ukraine, Scotland and southern England. The data were compared with published profiles of M.
rubra and two North American Myrmica species, and with a quantitative reanalysis of data for Maculinea
rebeli caterpillars. We conclude that the hydrocarbon profiles of Myrmica species are sufficiently and consistently different for chemical mimicry to explain the pattern of host specificity recorded for the European Maculinea butterflies. The optimum strategy for chemical mimicry in each of the two life-styles of Maculinea larvae is discussed: we suggest that predatory species might benefit from mimicking the median profile of their model whereas the "cuckoo" species would benefit when variation between siblings encompasses a large range of the variation recorded within a local population of the model species.
Butterflies of the genus Maculinea are highly endangered in Europe. The cuckoo species M. rebeli has been thoroughly investigated through both empirical and modelling studies, but less is known about the population ecology of predatory Maculinea. We present the findings of a 2-year research study on sympatric populations of two endangered butterflies: Maculinea teleius and M. nausithous in the Krakw region, southern Poland. The study comprised mark–release–recapture sampling and laboratory rearing of butterflies from larvae collected in the field. For both species the sex ratio was slightly, but consistently, female-biased and there was little year-to-year change in the seasonal population sizes. Daily numbers showed greater variation between the 2years of the study due to the differences in daily survival rate. The average life span of laboratory-raised butterflies kept in ideal conditions was more than 6days, compared to only 2–3days in the field. The recruitment of both males and females consistently followed a bimodal pattern. A small proportion of individuals (maximum 25%) changed sites, in spite of relatively short distances of ca. 100m separating them. The results indicate that populations of both species are typically stable within their sites, possibly due to larval polymorphism, but there is little inter-site mobility and thus landscape corridors seem necessary to enhance metapopulation viability. A further problem to be considered in the conservation of Maculinea butterflies is the fact that their very short life span in relation to flight-period length reduces the effective population size.
Maculinea butterflies in Europe, and probably most of Asia, are host specific social parasites of various species of Myrmica ants. The latest summary of field data showing the pattern of host specificity by Maculinea is presented. Myrmica ants have been well studied in the laboratory but much less is known about the ecology of their natural populations. While the former is important in understanding the adaptive evolution of Maculinea larval behaviours, the latter is of more practical importance to conservationists charged with the protection of specific populations of Maculinea. The current knowledge of habitat partition, colony growth and colony reproduction within communities of Myrmica ants is summarized in relation to the ecology of Maculinea species. Concepts used in current population simulation models are explained. A key concept is the idea that community structure (both number of species and size and abundance of nests) is controlled by the quantity and quality of suitable nest sites. Some advice is given to conservationists who might need to manipulate Myrmica ant populations in order to maintain a robust population of a Maculinea species. Rapid Science Ltd. 1998
Maculinea butterflies show social parasitism via obligatory myrmecophily as their larvae are adopted and raised to pupation by Myrmica ants. Suitable hosts differ for different Maculinea species, and host ant specificity can further differ at the population-level. Although early studies suggested single ant
species as main hosts for each Maculinea species, it has recently become clear that their host ant specificity is more complex. Maculinea alcon and Maculinea ‘rebeli’ have variously been separated according to adult and larval morphology, phenology, and their use of different ecosystems,
including host plant and host ant species. However, recent genetic evidence has questioned their separation as good species.
Here we compare the use of host ants by M. alcon and M. ‘rebeli’ at the regional scale in NE-Hungary and Transylvania (Romania), where molecular studies have found no species-level separation
between the two forms. We opened 778 nests of Myrmica ants and searched for Maculinea specimens (larvae, pupae and exuviae) shortly before imago emergence from the nest in seven M. alcon sites, six M. ‘rebeli’- sites and one site where both M. alcon and M. ‘rebeli’ are syntopic. In all, Maculinea caterpillars were found in the nests of seven different ant species (M. alcon was recorded mainly with Myrmica scabrinodis and occasionally with M. salina and M. vandeli; M. ‘rebeli’ used mainly M. scabrinodis, M. sabuleti and M. schencki and occasionally M. lonae and M. specioides). Myrmica scabrinodis was found to be a general host of both M. alcon and M. ‘rebeli’, which is the first record for a common host ant of these two closely related butterflies within the same region. However
there were also differences in host ant use patterns between the sites occupied by the two Maculinea taxa, which reflect differences in Myrmica communities between the two types of habitat. Possible explanations for the similar but not identical host use patterns of
M. alcon and M. ‘rebeli’, and their relevance for the question of whether they are separate species are discussed.
The myrmecophilous hoverfly, Microdon mutabilis, is listed as a 'Rare' or 'Nationally Notable Species' in UK Red Data Books. As an obligate social parasite, feeding only from ant colonies, its life-style satisfies theoretical conditions under which cryptic speciation is predicted to evolve; namely, strong selection for nonmorphological adaptations that enhance its exploitation of a local subspecies or populations of its host. Samples of larvae and pupae in Ireland, Scotland and England showed that M. mutabilis exploits a single and different host ant species on different sites across its range. In nine southern English colonies, 95.6% of infested nests were of Myrmica scabrinodis whereas in six Irish and two Scottish colonies 100% and 94.2%, respectively, of the infested nests were of Formica lemani, despite M. scabrinodis being common at all sites. Although the adults from 'scabrinodis' (and 'lemani) populations are cryptic, morphometric measurements of pupae showed consistent diagnostic characters that were sufficiently distinct for these ecotypes to be classed as separate species. We conclude that M. mutabilis is the 'lemani-type' and designate the 'scabrinodis-type' as a new species, Microdon myrmicae spec. nov. Thus, one of the listed threatened species of the British Isles becomes two species, each possessing about half the number of populations and occupying half the range of the original 'species'. Each also inhabits a different seral stage within grassland or heathland, and will require a different management regime if its declining populations are to be conserved. 'M. mutabills' is reported with other host ant species on the European continent. In the light of our results, these may prove to be additional cryptic species. We suggest that cryptic speciation is apt to evolve in species, such as myrmecophiles, endoparasites and koinobiont parasitoids, whose life-styles result in strong selection on their physiological or behavioural characters. The implications for Red Data Book classifications and for practical conservation are discussed.
These proceedings contain 18 papers that discuss topics on speciation and adaptation; life history, evolution, phenotypic plasticity and genetics; sexual selection and reproductive biology; insect-plant interactions; insect-natural enemy interactions; and social insects. A series of empirical case studies in evolutionary ecology using insects as model systems are also presented.
Maculinea butterflies are social parasites of Myrmica ants. Methods to study the strength of host ant specificity in the Maculinea–Myrmica association include research on chemical and acoustic mimicry as well as experiments on ant adoption and rearing behaviour of Maculinea larvae. Here we present results of laboratory experiments on adoption, survival, development and integration of M. teleius larvae within the nests of different Myrmica host species, with the objective of quantifying the degree of specialization of this Maculinea species. In the laboratory, a total of 94 nests of four Myrmica species: M. scabrinodis, M. rubra, M.
ruginodis and M. rugulosa were used. Nests of M. rubra and M. rugulosa adopted M. teleius larvae more readily and quickly than M. ruginodis colonies. No significant differences were found in the survival rates of M. teleius larvae reared by different ant species. Early larval growth of M. teleius larvae differed slightly among nests of four Myrmica host species. Larvae reared by colonies of M. rugulosa which were the heaviest at the beginning of larval development had the lowest mean larval body mass after 18 weeks compared to those reared by other Myrmica species. None of the M.
teleius larvae was carried by M. scabrinodis or M. rubra workers after ant nests were destroyed, which suggests a lack of integration with host colonies. Results indicate that Myrmica species coming from the same site differ in their ability to adopt and rear M. teleius larvae but there was no obvious adaptation of this butterfly species to one of the host ant species. This may explain why, under natural conditions, all four ants can be used as hosts of this butterfly species. Slight advantages of particular Myrmica species as hosts at certain points in butterfly larval development can be explained by the ant species biology and colony structure rather than by specialization of M. teleius.
Social insect colonies are like fortresses, well protected and rich in shared stored resources. This makes them ideal targets for exploitation by predators, parasites and competitors. Colonies of Myrmica rubra ants are sometimes exploited by the parasitic butterfly Maculinea alcon. Maculinea alcon gains access to the ants' nests by mimicking their cuticular hydrocarbon recognition cues, which allows the parasites to blend in with their host ants. Myrmica rubra may be particularly susceptible to exploitation in this fashion as it has large, polydomous colonies with many queens and a very viscous population structure. We studied the mutual aggressive behaviour of My. rubra colonies based on predictions for recognition effectiveness. Three hypotheses were tested: first, that aggression increases with distance (geographical, genetic and chemical); second, that the more queens present in a colony and therefore the less-related workers within a colony, the less aggressively they will behave; and that colonies facing parasitism will be more aggressive than colonies experiencing less parasite pressure. Our results confirm all these predictions, supporting flexible aggression behaviour in Myrmica ants depending on context.
A positive effect of (meta)population density on emigration has been predicted by many theoretical models and confirmed empirically in various organisms. However, in butterflies, the most popular species for dispersal studies, the evidence for its existence has so far been equivocal, with negative relationships between density and emigration being reported more frequently. We analysed dispersal in sympatric metapopulations of two Maculinea butterflies, intensively surveyed with mark–release–recapture methods for 7 years. Dispersal parameters, derived using the virtual migration model, were assessed against butterfly densities, which fluctuated strongly over the study period. Emigration was positively correlated with density, and this effect was particularly strong at densities above carrying capacity, when emigration increased up to threefold in females and twofold in males compared with the normal levels. In turn, density had little impact on other dispersal parameters analysed. Our findings provide good evidence for positive density-dependence of emigration in butterflies. Emigrating at high densities is particularly beneficial for females, because it gives them a chance to lay part of their egg-load in less crowded patches, where offspring survival is higher due to lower intraspecific competition. Even though the rise in emigration becomes considerable at densities exceeding carrying capacity, i.e. relatively infrequently, it still has serious implications for many ecological phenomena, such as species range expansions, gene flow, and metapopulation persistence. Consequently, instead of treating emigration as a fixed trait, it is worth allowing for its density-dependence in applications such as population viability analyses, genetic models or metapopulation models.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-011-2025-x) contains supplementary material, which is available to authorized users.
The relative contribution of density-dependent regulation and environmental stochasticity to the temporal dynamics of animal populations is one of the central issues of ecology. In insects, the primary role of the latter factor, typically represented by weather patterns, is widely accepted. We have evaluated the impact of density dependence as well as density-independent factors, including weather and mowing regime, on annual fluctuations of butterfly populations. As model species, we used Maculinea alcon and M. teleius living in sympatry and, consequently, we also analysed the effect of their potential competition. Density dependence alone explained 62 and 42% of the variation in the year-to-year trends of M. alcon and M. teleius, respectively. The cumulative Akaike weight of models with density dependence, which can be interpreted as the probability that this factor should be contained in the most appropriate population dynamics model, exceeded 0.97 for both species. In contrast, the impacts of inter-specific competition, mowing regime and weather were much weaker, with their cumulative weights being in the range of 0.08-0.21; in addition, each of these factors explained only 2-5% of additional variation in Maculinea population trends. Our results provide strong evidence for density-dependent regulation in Maculinea, while the influence of environmental stochasticity is rather minor. In the light of several recent studies on other butterflies that detected significant density-dependent effects, it would appear that density-dependent regulation may be more widespread in this group than previously thought, while the role of environmental stochasticity has probably been overestimated. We suggest that this misconception is the result of deficiencies in the design of most butterfly population studies in the past, including (1) a strong focus on adults and a neglect of the larval stage in which density-dependent effects are most likely to occur; (2) an almost exclusive reliance on transect count results that may confound the impact of environmental stochasticity on butterfly numbers with its impact on adult longevity.
Although it has always been assumed that chemical mimicry and camouflage play a major role in the penetration of ant societies by social parasites, this paper provides the first direct evidence for such a mechanism between the larvae of the parasitic butterfly Maculinea rebeli and its ant host Myrmica schencki. In the wild, freshly moulted fourth-instar caterpillars, which have no previous contact with ants, appear to be recognized as ant larvae by foraging Myrmica workers, which return them to their nest brood chambers. Three hypotheses concerning the mechanism controlling this behaviour were tested: (i) the caterpillars produce surface chemicals that allow them to be treated as ant larvae; (ii) mimetic compounds would include hydrocarbons similar to those employed by Myrmica to recognize conspecifics and brood; and (iii) the caterpillars' secretions would more closely mimic the profile of their main host in the wild, M. schencki, than that of other species of Myrmica. Results of behavioural bioassays and chemical analyses confirmed all three hypotheses, and explained the high degree of host specificity found in this type of highly specialized myrmecophile. Furthermore, although caterpillars biosynthesized many of the recognition pheromones of their host species (chemical mimicry), they later acquired additional hydrocarbons within the ant nest (chemical camouflage), making them near-perfect mimics of their individual host colony's odour.
Caterpillars of Maculinea rebeli have two growth strategies for living underground as social parasites of Myrmica ant colonies. Laboratory experiments and field data show that 25% of caterpillars live ten months with ants before pupating, whereas 75% grow slowly, parasitizing their hosts for 22 months. Both types of caterpillar form apparently identical similar-sized pupae. This may be the first description in the animal kingdom of polymorphic growth rates spanning different years within the same population, yet without resulting (as in salmonid fish) in two morphologically distinct adult types with obvious differences in behaviour. We suggest that a balanced polymorphism has evolved in M. rebeli growth rates, representing the most efficient way of exploiting the limited, yet steady, daily supply of food available to cuckoo-feeding parasites of long-lived ant societies. Bet-hedging benefits would also accrue to adult butterflies producing a mixture of annual and biennial offspring. Despite ergonomic and other benefits, partial biennialism is unlikely to evolve unless slow-growing individuals have enhanced survival and can remain attached to their mobile hosts. We show that caterpillars become so closely protected by, and integrated with, their host colonies that slow growers experience no greater mortality over two years than fast growers over one, and are transported in preference to the ants' own larvae when the host colony moves nest site.
A polymorphism in growth rates was recently described affecting the larval development of the myrmecophilous butterfly Maculinea rebeli, spanning different years in a single insect population. The close integration of M. rebeli into the host ant colonies, facilitated by adaptations in behaviour and chemical mimicry, make extended larval development a successful strategy. Here we present additional data for M. rebeli and new data for Maculinea alcon (another cuckoo-feeding lycaenid) and the two myrmecophilous predators Maculinea arion and Microdon mutabilis (Diptera: Syrphidae). As predicted, M. alcon shows the same growth pattern as M. rebeli with a proportion of caterpillars developing in one year and the remainder over two years. This pattern holds in both northern and southern European populations, where M. alcon exploits different species of host. Against expectation, the same bimodal distribution of pre-pupation body weights, indicating one and two year developers, was found for the larvae of M. arion and M. mutabilis. As predators, both species are less closely integrated in their host ant colonies, suggesting that the polymorphism in growth rates is a more general adaptation to a myrmecophilous life style, arrived at by convergent evolution between the Maculinea and Microdon species. For predatory species we suggest that biennialism is an adaptation to the migratory behaviour of the host made possible by the predators' ability to fast over extended periods. We also hypothesize that M. arion represents an ancestral strategy in Maculinea butterflies and that the growth polymorphism might have become genetically fixed in the cuckoo-feeding species.
The chemical strategies by which parasites manage to break into the social fortresses of ants offer a fascinating theme in chemical ecology. Semiochemicals used for interindividual nestmate recognition are also involved in the mechanisms of tolerance and association between the species, and social parasites exploit these mechanisms. The obligate parasites are odorless ("chemical insignificance") at the time of usurpation, like all other callow ants, and this "invisibility" enables their entry into the host colony. By chemical mimicry (sensu lato), they later integrate the gestalt odor of this colony ("chemical integration"). We hypothesize that host and parasite are likely to be related chemically, thereby facilitating the necessary mimicry to permit bypassing the colony odor barrier. We also review the plethora of chemical weapons used by social parasites (propaganda, appeasement, and/or repellent substances), particularly during the usurpation period, when the young mated parasite queen synthesizes these chemicals before usurpation and ceases such biosynthesis afterwards. We discuss evolutionary trends that may have led to social parasitism, focusing on the question of whether slave-making ants and their host species are expected to engage in a coevolutionary arms race.
The ant social parasite, Maculinea rebeli shows high levels of host specificity at a regional scale. While 68-88% of caterpillars in the field are adopted by nonhost Myrmica ants, 95-100% of the butterflies emerge from the natural host M. schencki the following year. While retrieval of preadoption caterpillars is specific to the genus Myrmica, it does not explain differential survival with different Myrmica species. We present survival data with host and nonhost Myrmica species suggesting that, with nonhosts (M. sabuleti and M. rubra), survival depends on the physiological state of the colony. We also compared the similarities of the epicuticular surface hydrocarbon signatures of caterpillars that were reared by host and nonhost Myrmica for 3 weeks with those from tending workers. Counterintuitively, the hydrocarbons of postadoption caterpillars were more similar (78%, 73%) to the ant colony profiles of the nonhost species than were caterpillars reared in colonies of M. schencki (42% similarity). However, caterpillars from M. schencki nests that were then isolated for 4 additional days showed unchanged chemical profiles, whereas the similarities of those from nonhost colonies fell to 52 and 56%, respectively. Six compounds, presumably newly synthesized, were detected on the isolated caterpillars that could not have been acquired from M. sabuleti and M. rubra (nor occurred on preadoption caterpillars), five of which were found on the natural host M. schencki. These new compounds may relate to the high rank the caterpillars attain within the hierarchy of M. schencki societies. The same compounds would identify the caterpillars as intruders in non-schencki colonies, where their synthesis appeared to be largely suppressed. The ability to synthesize or suppress additional compounds once adopted explains the pattern of mortalities found among fully integrated caterpillars in Myrmica colonies of different species and physiological states.
The presence of annual and biennial individuals within the same population has been recently demonstrated in the myrmecophilous butterflies Maculinea rebeli and Maculinea alcon, which present a cuckoo strategy inside Myrmica nests, and Maculinea arion which is a predatory species. Here, we present field and laboratory data on polymorphic larval growth in two other predatory species of Maculinea: M. teleius and M. nausithous. Body mass distributions of pre-pupation larvae were bimodal in both species. These results point to the existence of larvae that develop in 1 or 2 years. We also showed that the probability of pupation depended on larval body mass. In the case of M. teleius, the critical body mass at which larvae have a 50% probability of pupation is about 80 mg. We suggest that polymorphism in Maculinea may have evolved as an adaptation to life in ant nests, a habitat which protects them from predators and provides food. However, the quality of this resource is highly variable and unpredictable. According to the bet-hedging hypothesis, if the habitat is unpredictable, females should have an advantage by producing more variable offspring. In the case of Maculinea butterflies, this may involve maintaining larvae that develop in 1 or 2 years.
A new genus and species of flower flies is described from China (Furcantenna Cheng, type F. yangi Cheng). Another new genus is proposed for the Afrotropical species incorrectly placed in Ceratophya, Afromicrodon Thompson, type Microdon johannae Doesburg. A key is provided to the groups of the Subfamily Microdontinae, along with a checklist of genus-group names proposed within the subfamily and nomenclatural and taxonomic notes on them.
All parasites need to evade host defences to be successful. Social parasites, however, face unique challenges and opportunities. Their hosts are particularly well defended against intruders, but their social communication systems provide an alternative means of exploitation, if social parasites can evolve ways to subvert this system for their own ends. This chapter briefly reviews the range of tactics used by social parasites to exploit their hosts, and the communication channels and strategies used. Detailed analysis is presented of a few key systems that have been particularly well studied (Maculinea butterflies, Microdon flies, and slave-making and inquiline ants). The chapter examines general patterns of how social parasites use communication with their hosts to enhance their success, and the consequences that this has for the coevolutionary interaction between social parasites and their hosts.
1. Worldwide extinction of species due to habitat loss and habitat degradation can be recognised among butterflies pronouncedly. Therefore, conservation biologists devote special attention to identify the most important ecological factors affecting distribution and survival of butterflies. These efforts have been dominated by landscape-scale studies, although variation in habitat quality at smaller spatial scales may be of crucial importance. This applies for the highly specialised Maculinea species, which usually do not form classic metapopulations.
2. Maculinea nausithous and Maculinea teleius use the same larval food plant and usually occupy the same habitats in Europe. Afforestation of meadows due to abandonment is a major threat for these species. However, few if any studies have assessed the effects that proximity of forest edges may have on the habitat selection by adult butterflies at the scale of local populations. Here, we aimed to test these effects within one habitat fragment based on an intensive mark–release–recapture sampling.
3. Distribution of M. nausithous was aggregated and its density was highly positively influenced by the proportion of afforested meadow edges, while M. teleius showed no preference for afforested edges. Despite their different within-habitat distribution, the movement of both species was restricted to smaller parts of the habitat.
4. Our results suggest that M. nausithous has a narrower niche in the study region, which is most likely due to that its only host ant can find suitable microclimatic conditions at the afforested edges of wet meadows. This implies that habitat patches are not equally used by the two species and hence different management approaches are desirable for their conservation.
In 1979 the Nature Conservancy Council revealed that the large blue butterfly Maculinea arion was probably extinct in Britain, despite much research and valiant efforts to save it. The author, a member of the Institute of Terrestrial Ecology, who since 1972 has been engaged full time on the research and conservation work for the butterfly, tells the story as it is now known.
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@article{ORX:4970412,author = {Thomas,Jeremy},title = {Why Did the Large Blue Become Extinct in Britain?},journal = {Oryx},volume = {15},issue = {03},month = {4},year = {1980},issn = {1365-3008},pages = {243--247},numpages = {5},doi = {10.1017/S0030605300024625},URL = {http://journals.cambridge.org/article_S0030605300024625},}
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Why Did the Large Blue Become Extinct in Britain?
Jeremy Thomas (1980).
Oryx , Volume 15 , Issue03 , April 1980, pp 243-247
http://journals.cambridge.org/action/displayAbstract?aid=4970412
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Why Did the Large Blue Become Extinct in Britain?
Jeremy Thomas April 1980
Oryx,
,Volume15,
Issue03,
April 1980,
pp 243-247
http://journals.cambridge.org/abstract_S0030605300024625
Jeremy Thomas
(1980).
Why Did the Large Blue Become Extinct in Britain?.
Oryx,
15,
pp 243-247.
doi:10.1017/S0030605300024625.
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Maculinea rebeli caterpillars spend their final instar as specific parasites of colonies of the ant Myrmica schencki. This paper describes 14 experiments in which 604 caterpillars were reared with six species of Myrmica. About 40% of caterpillars died during an initial period of integration: survival was significantly greater among the larger caterpillars, in M. schencki nests, and in nests that had ant-brood present. The growth of the survivors was extremely variable. After three weeks they had gained 2–18 times their initial body weight and appeared to belong to two distinct types: fast and slow developers. Only 11% of caterpillars died during the next 37 days of growth, before a fall in temperature to below c. 14 d̀C caused them to overwinter. By then, the caterpillars weighed from 5–90 mg (mean 22 mg).
Caterpillars of all weights lost 33% of their mass during winter, and 8% died, before rising temperatures caused growth to resume in spring. Ofthe 363 that survived winter, 44% died during a period of spring growth and 12% pupated after about seven weeks. The latter came mainly from the largest caterpillars before winter and pupal size (mean weight 81 mg) was also related to prewinter caterpillar size. The remaining 44% of post-winter caterpillars continued to grow slowly and then entered another quiescent phase and were still alive after one year in the nest. A small number of these pupated in the second year, an average of 404 days after adoption.
It is calculated that an average-sized Myrmica schencki colony of 350 workers can produce 4–5 adult butterflies; this laboratory result agrees well with field observations. The results are discussed in the light of a previous behavioural study.
Caterpillars of the myrmecophilous butterfly Maculinea rebeli showed strong evidence of contest competition when introduced at high densities to laboratory nests of Myrmica ants.
This is attributed to the direct feeding of caterpillars by workers, which select a few individuals to nurture when food or ant numbers are limiting. It contrasts with published data for a congener, Maculinea arion , which has predacious larvae and experiences scramble competition in crowded ant nests.
Worker ants from two Myrmica rubra colonies (I and II) were used to found the laboratory nests hosting Maculinea rebeli. Nests from each source reared a similar biomass of Maculinea , but whereas those containing M. rubra I workers reared eight to ten lightweight caterpillars each, cultures from colony II reared half as many caterpillars, each of about double the weight.
Differences in nest capacity may be due to the different social structures of colonies I and II at the start of the experiment.
1. In 2002 Microdon myrmicae, a social parasite of Myrmica ants, was taxonomically separated from Microdon mutabilis. The original study in the U.K. found Microdon myrmicae to be specific to one ant species, Myrmica scabrinodis, yet it became apparent that the range of Microdon myrmicae includes at least the western Palaearctic.
2. Current knowledge of the European distributions of both Microdon myrmicae and Microdon mutabilis in Europe is reviewed. Also, in detailed studies of two Polish populations, Microdon myrmicae was found to survive equally well with two Myrmica ant species. We examine, however, the possibility that this reflects the presence of two separate Microdon species, each connected to one species of Myrmica.
3. Forty populations of Microdon myrmicae and 37 populations of Microdon mutabilis are currently known in Europe. All the populations in central and southern Europe that were visited after the separation of the two species were identified as Microdon myrmicae, while Microdon mutabilis’ recognised range is now restricted to the British Isles and Scandinavia. Myrmica scabrinodis was found to host Microdon myrmicae in 26 out of 31 populations investigated. Four other Myrmica species were identified to the host Microdon myrmicae: Myrmica gallienii (eight populations), Myrmica rubra (four), Myrmica vandeli (one), and Myrmica sabuleti (one). Microdon myrmicae occurs in waterlogged grassland habitats, mainly of the ‘Molinietum’ type, resulting in a patchy distribution relative to its host ants.
4. In two populations Myrmica scabrinodis and Myrmica gallienii are both abundant and rear Microdon myrmicae in equal proportions. Microdon myrmicae pupae from Myrmica gallienii nests were heavier and the anterior respiratory organs were of significantly different shape. In contrast, the comparisons of Microdon myrmicae pupae among all other populations showed no significant differences, suggesting only one species throughout the European range.
In recent spatial models describing interactions among a myrmecophilous butterfly Maculinea rebeli, a gentian Gentians cruciate and two competing species of Myrmica ant, we predicted that apparent competition should exist between gentians (the food of young M. rebeli caterpillars) and Myrmica schencki, which supports M. rebeli in its final instar. Here we extend and quantify model predictions about the nature of this phenomenon, and relate them to ecological theory. We predict that: (i) Within sites supporting the butterfly, fewer M. schencki colonies occur in sub-areas containing gentians than in identical habitat lacking this plant. (ii) Where G. cruciate and M. schencki do co-exist, the ant colonies will be less than half the size of those living > 1.5 m from gentians; (iii) The turnover of M. schencki colonies will be much greater than that of other Myrmica species in nest sites situated within 1.5 m of a gentian. All three predictions were supported in the field on 3-6 sites in two mountain ranges, although the exact strength of the apparent competition differed from some model predictions. Field data were also consistent with predictions about apparent mutualisms between gentians and other ants. We suggest that apparent competition is likely to arise in any system in which a specialist enemy feeds sequentially on two or more species during its life-cycle, as occurs in many true parasite-host interactions. We also predict that more complex patterns involving other Myrmica species and G. cruciate occur in our system, with apparent competition existing between them in some sub-areas of a site being balanced by apparent mutualism between them in other sub-areas.
A new genus and species of flower flies is described from China (Furcantenna Cheng, type F. yangi Cheng). Another new genus is proposed for the Afrotropical species incorrectly placed in Ceratophya, Afromicrodon Thompson, type Microdon johannae Doesburg. A key is provided to the groups of the Subfamily Microdontinae, along with a checklist of genus-group names proposed within the subfamily and nomenclatural and taxonomic notes on them.
1. Field studies were made of the benefits and costs of two feeding strategies in the genus Maculinea, whose final-instar larvae parasitise Myrmica ant colonies. Maculinea arion is an obligate predator of ant brood, whereas M. rebeli and M. alcon mimic ant larvae and are fed (like cuckoos) directly by the workers.
2. Samples of > 1500 Myrmica nests confirmed laboratory-based predictions that, by feeding at a lower trophic level, many (4.7-fold) more individuals of M. rebeli and M. alcon are supported per ant colony than M. arion.
3. Because of their efficient feeding, cuckoo species often occupied sites where their phytophagous early larval populations coincided to only a small extent (> 10%) with host Myrmica colonies, whereas all sites supporting M. arion had 50–100% of the phytophagous stages within foraging range of the host Myrmica species.
4. Greater host-specificity was identified as another consequence of cuckoo-feeding. The ecological cost of this is discussed.
5. The feeding of other Maculinea species had not been fully described: the data suggest that M. nausithous is a predator of ant brood and confirm that M. teleius is predacious.
Caterpillars of Maculinea arion are obligate predators of the brood of Myrmica sabuleti ants. In the aboratory, caterpillars eat the largest available ant larvae, although eggs, small larvae and prepupae are also palatable. This is an efficient way to predate. It ensures that newly-adopted caterpillars consume the final part of the first cohort of ant brood in a nest, before this pupates in early autumn and becomes unavailable as prey. At the same time, the fixed number of larvae in the second cohort is left to grow larger before being killed in late autumn and spring. Caterpillars also improve their feeding efficiency by hibernating for longer than ants in spring, losing just 6% of their weight while the biomass of ant larvae increases by 27%. Final instar caterpillars acquire more than 99% of their ultimate biomass in Myrmica nests, growing from 1.3 mg to an estimated 173 mg. A close correlation was found between the weights of caterpillars throughout autumn and the number of large ant larvae they had eaten. This was used to calculate the number of larvae eaten in spring, allowing both for the loss of caterpillar weight during winter and the increase in the size of their prey in spring. It is estimated that 230 of the largest available larvae, and a minimum nest size of 354 M. sabuleti workers, is needed to support one butterfly. Few wild M. sabuleti nests are this large: on one site, it was estimated that 85% of nests were too small to produce a butterfly, and only 5% could support two or more. This prediction was confirmed by the mortalities of 376 caterpillars in 151 wild M. sabuleti nests there. Mortalities were particularly high in nests that adopted more than two caterpillars, apparently due to scramble competition and starvation in autumn. Survival was higher than predicted in wild nests that adopted one caterpillar. These caterpillars seldom exhaust their food before spring, when there is intense competition among Myrmica for nest sites. Ants often desert their nests in the absence of brood, leaving the caterpillar behind. Vacant nests are frequently repopulated by a neighbouring colony, carrying in a fresh supply of brood. Maculinea arion caterpillars have an exceptional ability to withstand starvation, and sometimes survive to parasitize more than one Myrmica colony. Despite these adaptations, predation is an inefficient way to exploit the resources of a Myrmica nest. By contrast, Maculinea rebeli feeds mainly at a lower trophic level, on the regurgitations of worker ants. Published data show that Myrmica nests can support 6 times more caterpillars of Maculinea rebeli than of M. arion in the laboratory. This is confirmed by field data.
Ecological studies have been made of all 5 European species of Maculinea. These confirm that M. nausithous and M. rebeli live underground in Myrmica ant nests for 10 months of the year, as has long been known for the other 3 species. The main discovery was that each Maculinea species depends on a single, and different, host species of Myrmica. This specificity contradicts previous papers and scientific reviews of the relationship between Maculinea and ants. Therefore, early records are re-examined and 3 reasons are given to explain why most are misleading when applied to wild populations. Dependence on a single, rather than any, species of Myrmica explains why Maculinea populations exist in only a small minority of biotopes where their foodplants and Myrmica ants abound. It also explains the puzzling disappearance of Maculinea populations from apparently suitable sites. The discovery that M. alcon and M. rebeli depend on separate species of Myrmica that are not even closely related strengthens the argument that these butterflies are good species.
Classic metapopulation theory assumes relatively frequent population extinctions and colonisations on local habitat patches and consequently its interest is focused on spatial presence–absence patterns rather than on local population densities and their dynamics. However, the latter may also be important for metapopulation functioning, especially in the case of low turnover of local populations. We investigated spatial occurrence and abundance patterns of three species of endangered Maculinea butterflies in the Kraków region, southern Poland, in relation to various habitat parameters. For all three species investigated we found almost complete occupancy of their foodplant patches. The few patches lacking Maculinea populations were significantly smaller and more isolated. Foodplant availability proved to be the main factor limiting population densities for M. alcon, but not for M. teleius and M. nausithous, for which patch size and shape mattered the most. Small and highly internally fragmented patches supported higher densities of these two species. We hypothesise that the negative density–area relationship as well as positive impact of patch fragmentation on butterfly densities derive from differences in relative abundance of Myrmica ant hosts, which are a vital resource for myrmecophilous Maculinea butterflies. Since ants are under strong parasite pressure from Maculinea within their foodplant patches, and spread mainly through nest budding from surrounding refuge areas, their densities can be expected to be higher on small and fragmented patches. This underlines the importance of not only foodplant patches, but also their surroundings for the conservation of Maculinea butterflies.
Coevolution is one of the major processes organizing the earth's biodiversity. The need to understand coevolution as an ongoing process has grown as ecological concerns have risen over the dynamics of rapidly changing biological communities, the conservation of genetic diversity, and the population biology of diseases. The biggest current challenge is to understand how coevolution operates across broad geographic landscapes, linking local ecological processes with phylogeographic patterns. The geographic mosaic theory of coevolution provides a framework for asking how coevolution continually reshapes interactions across different spatial and temporal scales. It produces specific hypotheses on how geographically structured coevolution differs from coevolution at the local scale. It also provides a framework for understanding how local maladaptation can result from coevolution and why coevolved interactions may rarely produce long lists of coevolved traits that become fixed within species. Long-term field studies of the same interaction across multiple communities and spatially structured mathematical models are together beginning to show that coevolution may be a more important ongoing process than had been indicated by earlier empirical and theoretical studies lacking a geographic perspective.
Population growth and spread of recently reintroduced species is crucial for the success of their reintroduction. We analysed what limits the spread of two congeneric butterfly species Maculinea teleius and Maculinea nausithous, over 10 years following their reintroduction. During this time, their distributions appeared to be limited to a few sites although it was thought that more suitable habitats were available. Thus, we question, does the quality or the spatial arrangement of their habitat limit their spread? Although adult individuals of both species can select high-quality plots, we show that selection of suitable plots in the area of reintroduction is spatially constrained. A low colonization probability of unoccupied distant plots of high quality was found for both species. The abandonment of occupied plots in Ma. teleius was also found to be dependent on the distance to occupied plots. We conclude that the spatial distribution of the two species during the 10 years following reintroduction was limited by the spatial arrangement of their habitat, rather than by the availability of high-quality plots. The spatial constraints in movement can explain observed source–sink structures when female butterflies deposit their eggs on low-quality plots. We conclude that although these species have very similar life histories, they require different approaches to their conservation due to subtle differences in adult habitat use and movement. Conservation of Ma. teleius should concentrate on improving local habitat quality, whereas conservation of Ma. nausithous is predicted to be more effective by creating a spatial network of suitable habitat plots, such as along road verges
Understanding of ecosystem interactions and management has led to a major advance in the conservation of specialized insects.
Bringing Back the Large Blue
Flagship endangered species, such as the Large Blue butterfly have driven conservation programs worldwide. However, the Large Blue butterfly ( Maculinea arion ) became extinct in the United Kingdom. The apparent driver of this extinction was a complex set of events documented by Thomas et al. (p. 80 , published online 18 June; see the Perspective by Settele and Kühn ). Life-tables and modeling demonstrate how ecological changes, affecting multiple species, cascaded to negatively impact Large Blue populations. When the changes that cause these extinctions were addressed, reintroduction efforts proved successful. Other insects have experienced similar declines and, hopefully, on sites where their known resources remain abundant, a similar approach may be applied.