Trophic interactions in an ant nest microcosm: a combined experimental and stable isotope (δ13C/δ15N) approach

Living in close association with other organisms has proven to be a widespread and successful strategy in nature. Some communities are completely driven by symbiotic associations and therefore, intimate relationships among the partners can be expected. Here, we analyzed in‐depth the food web of a particularly rich community of arthropods found in strict association with European red wood ants (Formica rufa group). We studied the trophic links between different ant‐associated myrmecophiles and food sources associated with the host ant, but also tested predator–prey links among myrmecophiles themselves. Our approach combined direct feeding tests and stable carbon and nitrogen isotope analyses for a large number of myrmecophiles. The results of the direct feeding tests reveal a complex food web. Most myrmecophiles were found to parasitize on ant brood. Moreover, we encountered multiple trophic predator– prey links among the myrmecophiles. The results of the stable isotope analyses complement these findings and indicate the existence of multiple trophic levels and trophic isotopic niche compartmentalization. δ¹⁵N values were strongly correlated with the trophic levels based on the direct tests, reflecting that δ¹⁵N values of myrmecophiles increased with higher trophic levels. This strong correlation underlines the strength of stable isotopes as a powerful tool to assess trophic levels. In addition, the stable isotope data suggest that most species only facultatively prey on ant brood. The presence of numerous trophic interactions among symbionts clearly contrasts with the traditional view of social insects nests as offering an enemy‐free space for symbionts. Interestingly, the ant host can indirectly benefit from these interactions because brood predators are also preyed upon by other myrmecophiles. Overall, this study provides unique insights into the complex interactions in a small symbiont microcosm system and suggests that the interactions between host and symbiont might be mediated by other symbionts in the same community.     

Strategies of the beetle Oochrotus unicolor (Tenebrionidae) thriving in the waste dumps of seed-harvesting Messor ants (Formicidae)

1. A diverse group of arthropods have adapted to the niches found inside the nests of social insects. Studies mostly focused on very specialised parasites residing in the brood chambers. However, the biology and strategies of symbionts occupying other niches, such as waste dumps, are underexplored. 2. Using a series of complementary experiments, this study demonstrated that the Mediterranean beetle Oochrotus unicolor has adapted to the waste dump niche found in the nests of Messor harvester ants. 3. Laboratory experiments confirmed field observations that the beetle preferentially resided in the refuse pits. Next, it was shown that the beetles readily consumed seeds and flour, whereas other food sources were poorly accepted and ant brood was never even eaten. The beetles did not elicit a strong aggression response in Messor ants, and they could tolerate very high densities of workers without clear costs. The beetles modestly mimicked the nest recognition cues of their Messor host. This imperfect mimicry could promote the adoption of the beetle in the ant colony, in concert with mechanical defence generated by its tank-like body. Isolation of the beetle from its host did not significantly affect the beetle's chemical cuticular profile nor did it provoke elevated ant aggression, indicating that the beetle does not acquire the chemicals passively from its host. 4. This paper discusses the fact that waste dumps in social insect nests are hotspots for arthropod symbionts. It shows that symbionts in this niche may employ behavioural, trophic and chemical strategies that are different from those found in other niches of social insect nests.     

Diversity and morphology of abdominal glands in workers of the ant genus Myopias (Formicidae,Ponerinae)

Histological examination of serial sections through the abdomen of workers of three species of Myopias ants revealed the presence of several exocrine glands. These include the common venom and Dufour glands as well as the pygidial gland, but also more specific sternal glands and glands associated with the sting base and the gonostyli. Two of these glands have not been reported previously among ants: one is the paired oblong plate gland, that occurs next to the oblong plate and may have a pheromonal function. The other novel gland is the paired sting shaft gland, that occurs at the dorsal side in the proximal region of the sting shaft. A remarkable characteristic of these Myopias ants is that all glands of class-3 show ducts with gradually widening internal diameter. Myopias emeryi shows a clearly more simple variety of abdominal glands than Myopias maligna and M. sp.1.     

Successful maintenance of a stingless bee population despite a severe genetic bottleneck

Stingless bees play an important ecological role as pollinators of many wild plant species in the tropics and have significant potential for the pollination of agricultural crops. Nevertheless, conservation efforts as well as commercial breeding programmes require better guidelines on the amount of genetic variation that is needed to maintain viable populations. In this context, we carried out a long-term genetic study on the stingless bee Melipona scutellaris to evaluate the population viability consequences of prolonged breeding from a small number of founder colonies. In particular, it was artificially imposed a genetic bottleneck by setting up a population starting from only two founder colonies, and continued breeding from it for a period of over 10?years in a location outside its natural area of occurrence. We show that despite a great reduction in the number of alleles present at both neutral microsatellite loci and the sex-determining locus relative to its natural source population, and an increased frequency in the production of sterile diploid males, the genetically impoverished population could be successfully bred and maintained for at least 10?years. This shows that in stingless bees, breeding from a small stock of colonies may have less severe consequences than previously suspected. In addition, we provide a simulation model to determine the number of colonies that are needed to maintain a certain number of sex alleles in a population, thereby providing useful guidelines for stingless bee breeding and conservation efforts.     

Deleterious Wolbachia in the ant Formica truncorum

Wolbachia is a maternally inherited bacterium that may manipulate the reproduction of its arthropod hosts. In insects, it is known to lead to inviable matings, cause asexual reproduction or kill male offspring, all to its own benefit, but to the detriment of its host. In social Hymenoptera, Wolbachia occurs widely, but little is known about its fitness effects. We report on a Wolbachia infection in the wood ant Formica truncorum, and evaluate whether it influences reproductive patterns. All 33 colonies of the study population were infected, suggesting that Wolbachia infection is at, or close to, fixation. Interestingly, in colonies with fewer infected workers, significantly more sexuals are produced, indicating that Wolbachia has deleterious effects in this species. In addition, adult workers are shown to have significantly lower infection rates (45%) than worker pupae (87%) or virgin queens (94%), suggesting that workers lose their infection over life. Clearance of Wolbachia infection has, to our knowledge, never been shown in any other natural system, but we argue that it may, in this case, represent an adaptive strategy to reduce colony load. The cause of fixation requires further study, but our data strongly suggest that Wolbachia has no influence on the sex ratio in this species.     

Nepotism absent in insect societies — or is it?

Inclusive fitness theory, put forward by English biologist William Hamilton in 1964, is considered by many as the most important addition to the theory of natural selection since Darwin. One prediction of the theory is that animals should often show a tendency to nepotistically favour close relatives. Goodisman et al. (2007 ) test this theory for the first time using molecular methods in a vespine wasp, the eastern yellowjacket, Vespula maculifrons. Somewhat surprisingly, nepotism was found to be absent. This begs the question why nepotism is predicted by theory, yet in a growing list of species is shown to be absent. Is inclusive fitness theory in trouble? As we show, it is not: costs and constraints explain the general absence of queen rearing nepotism, and nepotism in insect societies in fact is well supported in the context of male rearing and manipulation of colony sex ratios.     

Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton''s theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.     

No Evidence of Enemy Release in Pathogen and Microbial Communities of Common Wasps (Vespula vulgaris) in Their Native and Introduced Range

When invasive species move to new environments they typically experience population bottlenecks that limit the probability that pathogens and parasites are also moved. The invasive species may thus be released from biotic interactions that can be a major source of density-dependent mortality, referred to as enemy release. We examined for evidence of enemy release in populations of the common wasp (Vespula vulgaris), which attains high densities and represents a major threat to biodiversity in its invaded range. Mass spectrometry proteomic methods were used to compare the microbial communities in wasp populations in the native (Belgium and England) and invaded range (Argentina and New Zealand). We found no evidence of enemy release, as the number of microbial taxa was similar in both the introduced and native range. However, some evidence of distinctiveness in the microbial communities was observed between countries. The pathogens observed were similar to a variety of taxa observed in honey bees. These taxa included Nosema, Paenibacillus, and Yersina spp. Genomic methods confirmed a diversity of Nosema spp., Actinobacteria, and the Deformed wing and Kashmir bee viruses. We also analysed published records of bacteria, viruses, nematodes and fungi from both V. vulgaris and the related invader V. germanica. Thirty-three different microorganism taxa have been associated with wasps including Kashmir bee virus and entomophagous fungi such as Aspergillus flavus. There was no evidence that the presence or absence of these microorganisms was dependent on region of wasp samples (i.e. their native or invaded range). Given the similarity of the wasp pathogen fauna to that from honey bees, the lack of enemy release in wasp populations is probably related to spill-over or spill-back from bees and other social insects. Social insects appear to form a reservoir of generalist parasites and pathogens, which makes the management of wasp and bee disease difficult.     

The effect of host plants on genotype variability in fitness and honeydew composition of Aphis fabae

Aphid species can be polyphagous, feeding on multiple host plants across genera. As host plant species can have large variation in their phloem composition, this can affect aphid fitness and honeydew composition. Previous research showed significant intraspecific genotype variation in the composition of the honeydew carbohydrates of the black bean aphid Aphis fabae, with the ant attractant trisaccharide melezitose showing especially large variation across different genotypes. In this study, we test if variation in melezitose and carbohydrate composition of aphid honeydew could be linked to the adaptation of specific aphid genotypes to particular host plants. To this end, 4 high and 5 low melezitose secreting genotypes of the black bean aphid Aphis fabae were reared on 4 common host plants: broad bean, goosefoot, beet, and poppy. The carbohydrate composition, and in particular melezitose secretion, showed important aphid genotype and host plant interactions, with some genotypes being high melezitose secreting on 1 host plant but not on another. However, the interaction effects were not paralleled in the fitness measurements, even though there were significant differences in the average fitness across the different host plants. On the whole, this study demonstrates that aphid honeydew composition is influenced by complex herbivore–plant interactions. We discuss the relevance of these findings in the context of ant–aphid mutualisms and adaptive specialization in aphids.