Simona Bonelli

Queen ants make distinctive sounds that are mimicked by a butterfly social parasite.

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.

Relative importance of density-dependent regulation and environmental stochasticity for butterfly population dynamics

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.

Acoustical mimicry in a predatory social parasite of ants.

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 hosts social hierarchy.

Selection on dispersal in isolated butterfly metapopulations

In most metapopulation models dispersal is assumed to be a fixed species-specific trait, but in reality dispersal abilities are highly sensitive to various selective pressures. Strict isolation of a metapopulation, which precludes any influx of immigrants (and their genes) from outside and makes it impossible for emigrants to reach other localities with suitable habitat, thus reducing fitness benefits of long-distance dispersal to zero, may be expected to impose strong selection against dispersal. We tested the above prediction by comparing dispersal parameters derived with the Virtual Migration model for isolated and non-isolated metapopulations of two species of large blue Maculinea (= Phengaris) butterflies, surveyed with intensive mark-recapture. Mortality during dispersal was found to be twice (in M. teleius) to five times higher (in M. arion) in isolated metapopulations. Isolation also resulted in significantly reduced dispersal distances in isolated metapopulations, with the effect being particularly strong in M. arion females. Apart from its evolutionary and ecological consequences, dispersal depression in isolated butterfly metapopulations implied by our results has serious conservation implications. It provides a clear argument against using parameter values obtained in a different environmental setting in modelling applications, e.g., Population Viability Analyses or environmental impact assessment. Furthermore, it underlines the importance of establishing well-connected networks of suitable habitats prior to species release in areas where reintroductions are planned.

Population extinctions in the Italian diurnal lepidoptera: an analysis of possible causes

In depth studies of patterns of extinction are fundamental to understand species vulnerability, in particular when population extinctions are not driven by habitat loss, but related to subtle changes in habitat quality and are due to ‘unknown causes’. We used a dataset containing over 160,000 non-duplicate individual records of occurrence (referred to 280 butterflies and 43 zygenid moths), and their relative extinction data, to carry out a twofold analysis. We identified ecological preferences that influence extinction probability, and we analysed if all species were equally vulnerable to the same factors. Our analyses revealed that extinctions were non-randomly distributed in space and time, as well as across species. Most of the extinctions were recorded in 1901–1950 and, as expected, populations at their range edges were more prone to become extinct for non-habitat-related causes. Ecological traits were not only unequally distributed between extinction and non-extinction events, but also not all ecological features had the same importance in driving population vulnerability. Hygrophilous and nemoral species were the most likely to experience population losses and the most prone to disappear even when their habitat remained apparently unchanged. Species vulnerability depends on both ecological requirements and threat type: in fact, each species showed a distinct pattern of vulnerability, depending on threats. We concluded that the analysis may be an important step to prevent butterfly declines: species that are strongly suffering due to ‘unknown changes’ are in clear and urgent need of more detailed auto-ecological studies.

When the Rule Becomes the Exception. No Evidence of Gene Flow between Two Zerynthia Cryptic Butterflies Suggests the Emergence of a New Model Group

There is increasing evidence that most parapatric cryptic/sister taxa are reproductively compatible across their areas of contact. Consequently, the biological species concept, which assumes absence of interbreeding, is becoming a not so effective criterion in evolutionary ecology. Nevertheless, the few parapatric sister taxa showing complete reproductive barriers represent interesting models to study speciation processes and the evolution of reproductive isolation. In this study, we examined contact populations in northwestern Italy of two butterfly species, Zerynthia polyxena and Z. cassandra, characterized by different genitalic morphotypes. We studied levels of divergence among 21 populations distributed from Sicily to France using three genetic markers (the mitochondrial COI and ND1 genes and the nuclear wingless gene) and genitalic geometric morphometrics. Moreover, we performed species distribution modelling to estimate different climatic requirements of Z. polyxena and Z. cassandra. We projected climatic data into glacial maximum scenarios in order to verify if and to which extent glacial cycles could have contributed to speciation processes. Genetic and morphometric analyses identified two main groups. All specimens showed a concordant pattern of diversification, including those individuals sampled in the contact area. Haplotype distribution and climatic models showed that during glacial maxima both species experienced a strong range contraction and presumably remained separated into different microrefugia in southern France, in the Italian Peninsula and on the islands of Elba and Sicily. Long term separation was probably favoured by reduced dispersal ability and high phylopatry, while genitalic diversification probably favoured interbreeding avoidance. Conversely, the aposematic wing pattern remained almost identical. We compared our results with those obtained in other species and concluded that Z. polyxena and Z. cassandra represent a valuable model in the study of speciation.

Ant Pupae Employ Acoustics to Communicate Social Status in Their Colony’s Hierarchy

The possession of an efficient communication system and an ability to distinguish between young stages are essential attributes that enable eusocial insects to live in complex integrated societies. Although ants communicate primarily via chemicals, it is increasingly clear that acoustical signals also convey important information, including status, between adults in many species. However, all immature stages were believed to be mute. We confirm that larvae and recently formed pupae of Myrmica ants are mute, yet once they are sclerotized, the pupae possess a fully functioning stridulatory organ. The sounds generated by worker pupae were similar to those of workers but were emitted as single pulses rather than in the long sequences characteristic of adults; both induced the same range and intensity of benevolent behaviors when played back to unstressed workers. Both white and sclerotized pupae have a higher social status than larvae within Myrmica colonies, but the latters status fell significantly after they were made mute. Our results suggest that acoustical signals supplant semiochemicals as a means of identification in sclerotized pupae, perhaps because their hardened integuments block the secretion of brood pheromones or because their developing adult secretions initially differ from overall colony odors.

Hotspots of biodiversity and conservation priorities: a methodological approach

This is a methodological paper aimed at comparing methods to assess regional biodiversity. In more detail we compared the effectiveness of hotspots of species richness, of rarity and complementarity in evaluating local animal diversity. Species distributions were sampled over a 10×10 km UTM grid across the Italian territory. We considered 471 species of zygaenids, butterflies, carabines, amphibians and reptiles. Hotspots were analysed at national and regional levels and considered taxa either all together, or separately. To test the predictive value of complementarity analysis, we initially excluded zygaenids. At national level, of 3218 10×10 km UTM quadrats sampled, 161 (5% of total) had highest species richness. Islands included only 1 hotspot (Sicily). Sixty‐eight species (14.4%) were not represented. They were mainly endemic (65%), insular (73.5%), or rare (25%). Working taxon by taxon, hotspots numbered 433. Only 85 (19.6%) were hotspots contemporaneously for two taxa and only 9 were hotspots for 3 taxa. Missing species were fundamentally insular species. The regional‐level approach generated 467 hotspots. Eleven species were not represented (2.3%). They had marginal distributions, or were insular endemites. Hotspots of rarity numbered 235 and 10 species were not included. Results demonstrated that hotspots are poor predictors of overall biodiversity. The complementarity method identified 67 quadrats. By definition, these quadrats accounted for all species investigated. They failed, however, to predict the occurrence of three zygaenids. As expected, complementarity provided better results than hotspots analysis. Combining the two methods assures that areas having the highest biodiversity are identified, even working with incomplete databases. Regional or rarity hotspots should generally be preferred to hotspots of species richness.

Corruption of ant acoustical signals by mimetic social parasites: Maculinea butterflies achieve elevated status in host societies by mimicking the acoustics of queen ants

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.

Plant defences against ants provide a pathway to social parasitism in butterflies

Understanding the chemical cues and gene expressions that mediate herbivore–host-plant and parasite–host interactions can elucidate the ecological costs and benefits accruing to different partners in tight-knit community modules, and may reveal unexpected complexities. We investigated the exploitation of sequential hosts by the phytophagous–predaceous butterfly Maculinea arion, whose larvae initially feed on Origanum vulgare flowerheads before switching to parasitize Myrmica ant colonies for their main period of growth. Gravid female butterflies were attracted to Origanum plants that emitted high levels of the monoterpenoid volatile carvacrol, a condition that occurred when ants disturbed their roots: we also found that Origanum expressed four genes involved in monoterpene formation when ants were present, accompanied by a significant induction of jasmonates. When exposed to carvacrol, Myrmica workers upregulated five genes whose products bind and detoxify this biocide, and their colonies were more tolerant of it than other common ant genera, consistent with an observed ability to occupy the competitor-free spaces surrounding Origanum. A cost is potential colony destruction by Ma. arion, which in turn may benefit infested Origanum plants by relieving their roots of further damage. Our results suggest a new pathway, whereby social parasites can detect successive resources by employing plant volatiles to simultaneously select their initial plant food and a suitable sequential host.