Interspecific relationships in co‐occurring populations of social parasites and their host ants

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.     

A biotrophic fungal infection of the great burnet Sanguisorba officinalis indirectly affects caterpillar performance of the endangered scarce large blue butterfly Phengaris teleius

Interactions between ecological communities of herbivores and microbes are commonly mediated by a shared plant. A tripartite interaction between a pathogenic fungus-host plant-herbivorous insect is an example of such mutual influences. In such a system a fungal pathogen commonly has a negative influence on the morphology and biochemistry of the host plant, with consequences for insect herbivore performance. Here we studied whether the biotrophic fbngus Podosphaera ferruginea, attacking the great burnet Sanguisorba officinalis, affects caterpillar performance of the endangered scarce large blue butterfly Phengaris teleius. Our results showed that the pathogenic ftmgus affected the number and size of inflorescences produced by food-plants and, more importantly, had in direct, plant-mediated effects on the abun dance, body mass and immune response of caterpillars. Specifically, we found the relationship between caterpillar abundance and variability in inflorescence size on a plant to be positive among healthy food-plants, and negative among infected food-plants. Caterpillars that fed on healthy food-plants were smaller than those that fed on infected food-plants in one studied season, while there was no such difference in the other season. We observed the relationship between caterpillar immune response and the proportion of infected great burnets within a habitat patch to be positive when caterpillars fed on healthy food-plants, and negative when caterpillars fed on infected food-plants. Our results suggest that this biotrophic fungal infection of the great burnet may impose a significant indirect influence on P. teleius caterpillar performance with potential consequences for the population dynamics and structure of this endangered butterfly.     

Dinucleotide microsatellite DNA loci from the ant Myrmica scabrinodis

We describe the isolation and characterization of five dinucleotide microsatellite loci in the ant Myrmica scabrinodis, which were obtained using a magnetic bead hybridization selection protocol. The PCR primers were tested on nine to 11 individuals. The number of alleles ranged from two to 13, and the observed heterozygosity from 0.200 to 0.778.     

Reproductive compensation of a perennial plant Sanguisorba tenuifolia to herbivory by Phengaris teleius

Plants that are consumed by herbivores incur a reduction in fitness. Therefore, plants need to prepare to defend against and/or avoid herbivory using ‘resistance’ and/or ‘tolerance’ systems. Phengaris teleius is a specialist herbivore of Sanguisorba tenuifolia. Phengaris teleius lays eggs in the flower buds of S. tenuifolia and the larvae of P. teleius feed on the ovaries and ovules of S. tenuifolia. In order to clarify the extent of herbivory damage by P. teleius and effect on reproduction in S. tenuifolia, we conducted field observations and artificial cutting experiments carried out in the natural habitat where both P. teleius and S. tenuifolia live sympatrically. Phengaris teleius often lays one egg per spike, and about half of the total eggs were laid on the spike that developed at the shoot apex and was largest in size. The fruits were damaged most heavily in the spike in which an egg was laid. However, the number of fruits was almost the same between individuals with no damage and individuals with a feeding damage rate of 40% or less. This showed that compensation would be achieved by increasing the number of fruits in other spikes without damage. On the other hand, because no compensation was detected in the cutting experiments, it was considered that compensation may be induced by biological stimuli produced by P. teleius. These responses may be one of the mechanisms for continuing the interspecific relationship between S. tenuifolia (host plant) and P. teleius (herbivore insect).     

Basal hatching by Maculinea butterfly eggs: a consequence of advanced myrmecophily?

Larvae of Maculinea alcon and M. rebeli are unique among Holarctic Lycaenidae in hatching through the base of the eggshell and emerging on the opposite side of the leaf to the egg. This occurs because the exposed upper surfaces of their eggs have exceptionally thick shells. Other species of Maculinea have normal or unusually thin-shelled eggs. It is suggested that both types of Maculinea eggshell have evolved to reduce mortalities from parasitoids and predators. Maculinea alcon and M. rebeli are forced to lay in exposed places due to the structure of their foodplants, and protect their eggs with thick shells. The other three species hide their eggs deep within the inflorescences of their foodplants; M. nausithous and M. teleius require thin flexible shells to achieve this. These adaptations are necessary because Maculinea eggs often occur at much higher densities on their initial foodplants and are hence more vulnerable—than is the case with other Lycaenidae. This is a consequence of myrmecophily. Maculinea population size is regulated more by the status of the ant host than by that of the initial foodplant. Large Maculinea populations, and high densities of eggs, occur on the many sites where the ant is abundant but the foodplant is scarce. Maculinea alcon and M. rebeli eggs occur at the highest densities, and need the greatest protection, due to the advanced form of myrmecophily found in these species. Whereas M. anon, M. teleius and M. nausithous larvae are predators of ant brood, M. alcon and M. rebeli feed mainly at a lower trophic level on ant regurgitations. This leads to roughly seven times more M. alcon and M. rebeli adults emerging per ant nest, and to a similar increase in egg densities per foodplant.     

Nine polymorphic microsatellite loci for the parasitic wasp Neotypus melanocephalus (Hymenoptera: Ichneumonidae)

Nine polymorphic microsatellite loci were isolated from Neotypus melanocephalus (Gmelin), a parasitoid of the parasitic large blue butterfly Maculinea nausithous. Allelic diversity and heterozygosity were quantified in samples from the Upper Rhine valley in Southwest Germany.     

Population structure of a large blue butterfly and its specialist parasitoid in a fragmented landscape

Habitat fragmentation may interrupt trophic interactions if herbivores and their specific parasitoids respond differently to decreasing connectivity of populations. Theoretical models predict that species at higher trophic levels are more negatively affected by isolation than lower trophic level species. By combining ecological data with genetic information from microsatellite markers we tested this hypothesis on the butterfly Maculinea nausithous and its specialist hymenopteran parasitoid Neotypus melanocephalus. We assessed the susceptibility of both species to habitat fragmentation by measuring population density, rate of parasitism, overall genetic differentiation (theta(ST)) and allelic richness in a large metapopulation. We also simulated the dynamics of genetic differentiation among local populations to asses the relative effects of migration rate, population size, and haplodiploid (parasitoid) and diploid (host) inheritance on metapopulation persistence. We show that parasitism by N. melanocephalus is less frequent at larger distances to the nearest neighbouring population of M. nausithous hosts, but that host density itself is not affected by isolation. Allelic richness was independent of isolation, but the mean genetic differentiation among local parasitoid populations increased with the distance between these populations. Overall, genetic differentiation in the parasitoid wasp was much greater than in the butterfly host and our simulations indicate that this difference is due to a combination of haplodiploidy and small local population sizes. Our results thus support the hypothesis that Neotypus parasitoid wasps are more sensitive to habitat fragmentation than their Maculinea butterfly hosts.     

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 modelling of the spatial interactions between Maculinea rebeli their initial foodplant Gentiana cruciata and Myrmica ants within a 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     

Performance of Myrmica ant colonies is correlated with the presence of social parasites

1. The performance of ant colonies depends on different factors such as nest site, colony structure or the presence of pathogens and social parasites. Myrmica ants host various types of social parasites, including the larvae of Maculinea butterflies and Microdonmyrmicae (Schönrogge) hoverfly. How these social parasites affect host colony performance is still unexplored. 2. It was examined how the presence of Maculinea teleius Bergsträsser, Maculinea alcon (Denis & Schiffermüller), and M. myrmicae larvae, representing different feeding and growth strategies inside host colonies, is associated with worker survival, the number of foragers, and colony productivity parameters such as growth and reproduction. 3. It was found that the presence of social parasites is negatively associated with total colony production and the production of ant larvae and gynes. Male production was lower only in nests infested by M. teleius, whereas the number of worker pupae was significantly higher in all types of infested colonies than in uninfested colonies. Laboratory observations indicated that nests infested by Maculinea larvae are characterised by a higher number of foragers compared to uninfested nests but we did not find differences in worker survival among nest types. 4. The observed pattern of social parasite influence on colony productivity can be explained by the feeding strategies of parasitic larvae. The most negative effect was found for M. teleius, which feeds on the largest host brood and eliminates a high number of sexual forms. The strong, adverse influence of all studied parasite species on gyne production may result in low queen production in Myrmica populations exposed to these social parasites.