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1. The six papers in this Special Issue of Insect Conservation and Diversity are presented as a gedenkschrift honouring ground‐breaking contributions made by the late Graham Elmes towards understanding the biology of Myrmica ants and their social parasites. 2. A common theme is that each research paper contributes new knowledge applicable to the future survival of Maculinea (= Phengaris) species of butterflies, which have become flagships for insect conservation across Europe. All Maculinea species are highly specialised, with larvae that feed briefly on a specific foodplant before living underground for 11–23 months as social parasites of Myrmica colonies. 3. This introductory overview provides a brief history of the research that has led to the current collection, with emphasis on Graham Elmes' life and work. It is followed by three research papers that illustrate the diversity, socio‐biology and ecology of Myrmica ants. A fourth describes an extreme adaptation that increases the efficiency with which some populations of Maculinea larvae exploit the resources within Myrmica nests. A fifth, more theoretical, paper models the constraints that typically lead to host specificity among social parasites and explores why host switches are rare and quick.

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’.

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.

SUMMARY Rapid, effective communication between colony members is a key attribute that enables ants to live in dominant, fiercely protected societies. Their signals, however, may be mimicked by other insects that coexist as commensals with ants or interact with them as mutualists or social parasites. We consider the role of acoustics in ant communication and its exploitation by social parasites. Social parasitism has been studied mainly in the butterfly genus Maculinea, the final instar larvae of which are host-specific parasites of Myrmica ants, preying either on ant grubs (predatory Maculinea) or being fed by trophallaxis (cuckoo Maculinea). We found similar significant differences between the stridulations of model queen and worker ant castes in both Myrmica sabuleti and Myrmica scabrinodis to that previously reported for Myrmica schencki. However, the sounds made by queens of all three Myrmica species were indistinguishable, and among workers, stridulations did not differ significantly in two of three species-pairs tested. Sounds recorded from the predatory caterpillars and pupae of Maculinea arion had similar or closer patterns to the acoustics of their host Myrmica sabuleti than those previously reported for the cuckoo Maculinea rebeli and its host Myrmica schencki, even though Maculinea rebeli caterpillars live more intimately with their host. We conclude that chemical mimicry enables Maculinea larvae to be accepted as colony members by worker ants, but that caterpillars and pupae of both predatory and cuckoo butterflies employ acoustical mimicry of queen ant calls to elevate their status towards the highest attainable position within their host's social hierarchy.

International audience; Caterpillars of the butterfly Maculinea rebeli develop as parasites inside ant colonies. In intensively studied French populations, about 25% of caterpillars mature within 1 year (fast‐developing larvae [FDL]) and the others after 2 years (slow‐developing larvae [SDL]); all available evidence indicates that this ratio is under the control of egg‐laying females. We present an analytical model to predict the evolutionarily stable fraction of FDL (pESS). The model accounts for added winter mortality of SDL, general and kin competition among caterpillars, a competitive advantage of SDL over newly entering FDL (priority effect), and the avoidance of renewed infection of ant nests by butterflies in the coming season (segregation). We come to the following conclusions: (1) all factors listed above can promote the evolution of delayed development; (2) kin competition and segregation stabilize pESS near 0.5; and (3) a priority effect is the only mechanism potentially selecting for . However, given the empirical data, pESS is predicted to fall closer to 0.5 than to the 0.25 that has been observed. In this particular system, bet hedging cannot explain why more than 50% of larvae postpone growth. Presumably, other fitness benefits for SDL, for example, higher fertility or longevity, also contribute to the evolution of delayed development. The model presented here may be of general applicability for systems where maturing individuals compete in small subgroups.

Summary Chemical communication plays a major role in the organisation of ant societies, and is mimicked to near perfection by certain large blue (Maculinea) butterflies that parasitise Myrmica ant colonies. The recent discovery of differentiated acoustical communication between different castes of ants, and the fact that this too is mimicked by the butterflies, adds a new component of coevolutionary complexity to a fascinating multitrophic system of endangered species, and it could inspire new ways to engage the public in their conservation.

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.

Ants dominate terrestrial ecosystems through living in complex societies whose organization is maintained via sophisticated communication systems. The role of acoustics in information exchange may be underestimated. We show that Myrmica schencki queens generate distinctive sounds that elicit increased benevolent responses from workers, reinforcing their supreme social status. Although fiercely defended by workers, ant societies are infiltrated by specialist insects that exploit their resources. Sounds produced by pupae and larvae of the parasitic butterfly Maculinea rebeli mimic those of queen ants more closely than those of workers, enabling them to achieve high status within ant societies. We conclude that acoustical mimicry provides another route for infiltration for ∼10,000 species of social parasites that cheat ant societies.

We develop a “case model” approach to investigate how conservation measures may affect the ecology of a community module, defined as a small number of tightly interacting species. The community module consists of a parasitic butterfly and its two hosts, a plant and an ant. The butterfly Maculinea alcon and its host plant Gentiana pneumonanthe have long been used as indicators of high-quality Palearctic heath and moist grassland ecosystems, and both species have been targeted for ecological research and specific conservation management. We constructed a mechanistic model of this community module, including dynamics for the three species, and conducted simulation studies of different conservation strategies (burning, sod cutting, mowing, and grazing). We identified several key parameters for the conservation of Maculinea alcon and its host plant as well as the most efficient conservation strategies for their dual long-term persistence. Our results show that the conditions that optimize the size of the butte...

Final instar larvae of Maculinea rebeli Hirschke (Lepidoptera, Lycaenidae) are social parasites of Myrmica Latreille (Hymenoptera, Formicidae) nests. In the populations of the southern French Alps and Spanish Pyrenees, >95% adult M. rebeli emerge from colonies of Myrmica schencki Emery, despite >60% caterpillars being adopted by other Myrmica species (non-hosts). However, in laboratory culture caterpillars can be reared successfully by many of the non-host species. This contradiction, which has led some to question the existence of host specificity, has been explained by the lack of stress, particularly food stress, in laboratory cultures compared to wild conditions. Here, we report the results of an experiment that tested the survival of M. rebeli caterpillars that had been growing well, after being socially integrated into a series of host and non-host cultures, and were then subjected to a 4-week period of stress induced by a 'starvation diet' estimated to be less than the minimum for ant survival. Significantly more M. rebeli survived in M. schencki cultures than with any of the other Myrmica species (all died in most non-host cultures). Under a starvation diet, caterpillars are killed and eaten along with dead workers - this never happens under an ample diet - rather than simply starving to death. It was noted that the proportion of young M. rebeli caterpillars that survived initial integration into an ant colony (including some M. schencki colonies) was a good predictor of subsequent survival under starvation conditions. We concluded that two key phases of host specificity exist in the life of this social parasite: initial integration, in which the caterpillar simply has to be accepted into a host society, followed by full integration, when a relatively high hierarchical status within the host society becomes essential for a caterpillar's survival during periods when the host colony is stressed, e.g., by food shortage. This experimental regime provides a useful bioassay for testing host specificity in other populations of Maculinea.

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.

Fourth instar larvae of Maculinea species of lycaenid butterfly live as social parasites insideMyrmica ant nests. They show highly unusual growth patterns, with small but regular growth in early phytophagous instars, followed by >10 times the growth predicted by extrapolating the early growth rate (following Dyar's rule) during the final carnivorous instar. This produces striking allometry between head and body size in full-grown larvae (ratios of 4–5% compared with 8–10%). Larvae of the Myrmica ant hosts have a similar growth. Data for c. 150 other lycaenid species showed that species with similar life-histories exhibit the same unusual growth pattern (Phengaris sppLepidochrysops spp Niphanda fusca); all others have regular growth throughout their larval life, including the carnivorous species that are parasitic on ants from the first instar. It is suggested that Maculinea -type growth pattern has arisen convergently in at least three unrelated lineages of lycaenids. Selection pressures might include the need for reduced early growth to produce late instars that are small enough to be integrated as brood mimics into ant social systems, combined with the need to achieve at least the same adult size as the ancestral species. Trophic pressures that operate on both sedentary ant and butterfly larvae, which must survive long periods of starvation and grow rapidly when food is abundant, may also be involved.

Recent recordings of the stridulations of Myrmica ants revealed that their queens made distinctive sounds from their workers, although the acoustics of queens and workers, respectively, were the same in different species of Myrmica. Queen recordings induced enhanced protective behavior when played to workers in the one species tested. Larvae and pupae of the butterfly genus Maculinea inhabit Myrmica colonies as social parasites, and both stages generate sounds that mimic those of a Myrmica queen, inducing similar superior treatments from workers as their model. We discuss how initial penetration and acceptance as a colony member is achieved by Maculinea through mimicking the species-specific semio-chemicals of their hosts, and how acoustical mimicry is then employed to elevate the parasite's membership of that society towards the highest attainable level in their host's hierarchy. We postulate that, if acoustics is as well developed a means of communication in certain ants as these studies suggest, then others among an estimated 10,000 species of ant social parasite may supplement their well-known use of chemical and tactile mimicry to trick host ants with mimicry of host acoustical systems.

Caterpillars of the lycaenid butterfly Maculinea rebeli Hirschke (Lepidoptera: Lycaenidae) live for 11–23 months as social parasites in Myrmica (Hymenoptera: Formicidae) red ant nests, a trait that is believed to have evolved from mutualistic myrmecophilous ancestry. Although Maculinea rebeli caterpillars harm Myrmica larvae, they simultaneously produce copious secretions which the adult worker ants imbibe, perhaps representing a vestige of the ancestral mutualism. We report the results of laboratory experiments designed to test alternative hypotheses: (i) Maculinea rebeli caterpillars provide a beneficial source of sugar in return for being tended by Myrmica workers; (ii) Maculinea rebeli harms its host by stressing the workers by competing for available sugar. Comparisons were made of Myrmica worker fitness after 90–450 days under all possible combinations of three experimental treatments: ±M. rebeli caterpillars, ± sucrose and ± ant brood. Caterpillars always reduced the survival of both ant workers and their larvae, even when sugar was not provided, suggesting that M. rebeli is wholly parasitic on all stages in its host colony. The results also confirmed the importance of sucrose in the diet of Myrmica, and showed that M. rebeli caterpillars which eat ant brood to supplement their normal trophallactic feeding by workers develop more quickly - but have the same survival and pupal weights – as caterpillars that are fed solely by worker ants.

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 caterpillar–s 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.

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 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 spatial computer simulation model has been developed to assist our understanding of the ways in which Maculinea butterflies depend upon the spatial distribution and abundance of their initial foodplant and their Myrmica host ant. It was initially derived for the Maculinea rebeli-Myrmica schencki-Gentiana cruciata system. It relates the population processes of the competing host and other ant species to an underlying gradient of habitat quality and incorporates the impact of adopted Maculinea caterpillars on the growth and survival of individual ant nests. The model was initially calibrated for a large site in the Spanish Pyrenees, but has since been successfully tested on 12 French sites and another in Spain. On such sites, with M. rebeli present, there is a close relationship between Maculinea population density and the density of the early larval foodplant G. cruciata. Optimum gentian density is estimated to be about 1500 plants ha-1 on sites with the natural clumping of gentians found. However, any site management which added extra gentians, especially if filling the gaps, is predicted to reduce the Maculinea population. Meta-population studies of single species have shown that the size and spatial arrangement of patches of assumed uniformly ‘suitable’ habitat can influence their population dynamics and persistence. Our modelling suggests that the spatial pattern of ‘suitable’ habitat of varied quality within a single site can influence the local butterfly population size and perhaps also persistence. Despite being free-ranging over the whole area, the butterfly's dynamics may depend on the arrangement of habitat quality at a finer spatial scale, due to its interactions with ant species possessing narrower habitat niches and more localized dispersal. © Rapid Science Ltd. 1998

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

In recent spatial models describing interactions among a myrmecophilous butterfly Maculinea rebeli , a gentian Gentiana cruciata 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. cruciata 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. cruciata 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.

An emerging problem in conservation is whether listed morpho-species with broad distributions, yet specialized lifestyles, consist of more than one cryptic species or functionally distinct forms that have different ecological requirements. We describe extreme regional divergence within an iconic endangered butterfly, whose socially parasitic young stages use non-visual, non-tactile cues to infiltrate and supplant the brood in ant societies. Although indistinguishable morphologically or when using current mitochondrial and nuclear sequence-, or microsatellite data, Maculinea rebeli from Spain and southeast Poland exploit different Myrmica ant species and experience 100 per cent mortality with each other's hosts. This reflects major differences in the hydrocarbons synthesized from each region by the larvae, which so closely mimic the recognition profiles of their respective hosts that nurse ants afford each parasite a social status above that of their own kin larvae. The two host ants occupy separate niches within grassland; thus, conservation management must differ in each region. Similar cryptic differentiation may be common, yet equally hard to detect, among the approximately 10 000 unstudied morpho-species of social parasite that are estimated to exist, many of which are Red Data Book listed.

1 Caterpillars of the myrmecophilous butterfly Maculinea rebeli showed strong evidence of contest competition when introduced at high densities to laboratory nests of Myrmica ants. 2 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. 3 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. 4 Differences in nest capacity may be due to the different social structures of colonies I and II at the start of the experiment.

Large blue butterflies are notable for their rarity and ability to dupe ants, and they are endangered. A genetic reconstruction of how social parasitism evolved among them will overturn conservation priorities.

Caterpillars of the butterfly, Maculinea rebeli, feed sequentially in flower-buds of Gentiana cruciata and in nests of Myrmica schencki ants, with which they have a sort of'cuckoo bird' relationship. Ants feed them in preference to their own larvae, reducing the production of new workers and hence the colony size the following year. Other Myrmica compete with M. schencki for nest-sites. They adopt caterpillars with equal facility, but fail to rear them to maturity and are consequently less damaged. Using a mathematical model we explore how species interactions can influence the populations of the butterfly, M. schencki, and other Myrmica species. The model assumes a 1 ha square of 900 cells with a fixed population of gentians

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.