Ant Queens Research Articles

Comparative morpho-physiology of the metapleural glands of two Atta leaf-cutting ant queens nesting in clayish and organic soils

Queens of leaf-cutting ants found their nests singly, each consisting of a vertical tunnel and a final horizontal chamber. Because of the claustral mode of nest founding, the queen and/or her initial fungus garden are exposed to threats imposed by several soil pathogens, and the antibiotic secretions produced by their metapleural glands are considered a main adaptation to deal with them. Nests of two Atta leaf-cutting ant species, Atta vollenweideri and Atta sexdens rubropilosa, occur in different soil types, alfisols and oxisols. Their queens are known to excavate the initial nest in different soil horizons, clayish and organic, respectively, which differ in their fertility and associated microbiota. The aim of the present study was to comparatively investigate the morpho-physiology of the metapleural glands in queens of A. vollenweideri and A. sexdens rubropilosa, addressing the question whether the distinct selective pressure imposed by the microbiota in the two different soil types led to morpho-physiological differences in the metapleural glands that were consistent with their antiseptic function. The results revealed that metapleural glands of A. sexdens rubropilosa have a larger number of secretory cells, and consequently a higher production of antibiotic secretions, which may have been selected to allow nest founding at the superficial horizon of oxisols rich in organic matter and microorganisms. Glands of A. vollenweideri, on the contrary, presented fewer secretory cells, suggesting less production of antibiotic secretions. We argue that the excavation of deep founding nests in A. vollenweideri was primarily selected for during evolution to avoid the risk posed by flooding, and further hypothesize that a reduced number of cells in their metapleural glands occurred because of a weak pathogen-driven selective pressure at the preferred soil depth.

Benomyl treatment decreases fecundity of ant queens

Methyl benzimidazole carbamate fungicides, including benomyl, are widely used in agriculture, and to eliminate entomopathogenic infections. We treated queens of Myrmica rubra (Hymenoptera:Formicidae) infected or not by Rickia wasmannii (Laboulbeniales:Laboulbeniaceae) with benomyl, 1mg/ml p.o. for six weeks. Benomyl did not treat the infection, and the treatment alone caused strong decrease in the fecundity of control healthy queens from 18.0±8.4 to 3.7±5.2eggs per healthy queen. This is the first evidence on severe adverse effects of methyl benzimidazole carbamate fungicide on the fecundity of insects, which might be responsible for altered species composition of ant assemblages in the cultural landscape.

Mating with an allopatric male triggers immune response and decreases longevity of ant queens.

In species with lifelong pair bonding, the reproductive interests of the mating partners are aligned, and males and females are expected to jointly maximize their reproductive success. Mating increases both longevity and fecundity of female reproductives (queens) of the ant Cardiocondyla obscurior, indicating a tight co-evolution of mating partners. Here, we show that mating with a male from their own population increases lifespan and reproductive success of queens more than mating with a male from a different population, with whom they could not co-evolve. A comparison of transcriptomes revealed an increased expression of genes involved in immunity processes in queens, which mated with males from a different population. Increased immune response might be proximately associated with decreased lifespan. Our study suggests a synergistic co-evolution between the sexes and sheds light on the proximate mechanisms underlying the decreased fitness of allopatrically mated queens.

Transport and Dispersal of Stictococcus Vayssierei (Hemiptera, Stictococcidae) by Anoplolepis Tenella (Hymenoptera, Formicidae)

Dispersal can be a crucial factor affecting fitness in insects. We conducted a series of experiments and observations with the aim of determining the dispersal mode of the African root and tuber scale Stictococcus vayssierei, a pest on cassava in the Congo Basin. We monitored the main options of dispersal that occurred in scale insects: wandering of first-instar nymphs (crawlers), active dispersal by ant workers, phoresis on colony-founding queen ants, and passive dispersal by wind. Results showed that A. tenella workers are actively involved in the transport and dissemination of scale crawlers. When ants were excluded, crawlers could move by themselves for a short distance to find the host plant. In the presence of ants, crawlers were transported by ant workers for longer distance across the bridge and established on scale-free plants. Scales transport increased with the duration of the experiment and ant density. Neither a case of phoresis nor dispersal by wind was recorded, suggesting that passive dispersal is rare. These results outline the active role of A. tenella workers in the dispersal of immature stages of S. vayssierei in Southern Cameroon and have implication in the management of the scale on cassava.

Consequences of Nosema apis infection for male honey bees and their fertility.

The queens of eusocial bees, ants and wasps mate only during a very short period early in life and males therefore produce ejaculates consisting of large numbers of high quality sperm. Such extreme selection for high fecundity resulted in males investing minimally into their somatic survival, including their immune system. However, if susceptible males are unable to protect their reproductive tissue from infections, they compromise queen fitness if they transfer pathogens during mating. We used the honey bee Apis mellifera and investigated the course of infection of the sexually transmitted pathogen Nosema apis. We predicted that honey bee males are susceptible but protect their reproductive tissues from infections. We investigated the effects of N. apis infections on the midgut, the accessory glands and the accessory testes and quantified the consequences of infection on male survival and fecundity. We found that N. apis is able to infect males, and as infections progressed, it significantly impacted fertility and survival in older males. Even though we confirm males to be able to minimize N. apis infections of their reproductive tissues, the parasite is present in ejaculates of older males. Consequently N. apis evolved alternative routes to successfully infect ejaculates and get sexually transmitted.

Avoid mistakes when choosing a new home: Nest choice and adoption of Leptothorax ant queens

In ants, mating and colony founding are critical steps in the life of ant queens. Outside of their nests, young queens are exposed to intense predation. Therefore, they are expected to have evolved behavior to accurately and quickly locate a nesting place. However, data on the early life history of female reproductives are still lacking. Leptothorax gredleri is a suitable model organism to study the behavior of young queens. Reproductives can be reared under artificial conditions and readily mate in the laboratory. After mating, L. gredleri queens have the options to found solitarily, seek adoption into another colony, or return into their natal nest. In this study, we investigated the decision-making processes of female sexuals before and after mating. In particular, we tested whether female sexuals use chemical cues to find their way back to the nest, studied if they prefer their own nest over other nesting sites and followed the adoption dynamics of mated queens over 8weeks (plus hibernation and spring). We showed that female sexuals and freshly mated queens spent more time on substrate previously used by workers from their own colony and from another colony than on a blank substrate. This discriminatory capability of queens appears to be lost in old, reproductive queens. Nest choice experiments showed that female sexuals and freshly mated queens can distinguish their own nest while old mated queens’ do not. When reintroduced in their maternal colony, young queens were readily adopted, but a few weeks later aggression against young queens led to their emigration from the maternal nest and eventually also death.

Octopamine and cooperation: octopamine regulates the disappearance of cooperative behaviours between genetically unrelated founding queens in the ant.

We investigated whether octopamine (OA) is associated with the disappearance of cooperation in Polyrhachis moesta ant queens. Queens of P. moesta facultatively found the colony with genetically unrelated queens. The founding queens perform frequent food exchange with these non-related queens and partake in cooperative brood rearing, whereas single colony queens exclude non-related queens via aggressive behaviour. Thus, aggression is a factor that reduces cooperation. Given that aggression is generally associated with brain OA in insects, we hypothesized that OA controls the behavioural change in cooperation in the ant queen, via an increase in aggression. To test this hypothesis, we compared the amounts of OA and related substances in the brain between founding and colony queens, and observed the interaction of founding queens following oral OA administration. The brain OA levels in colony queens were significantly higher than those in founding queens. Oral administration of OA to founding queens caused significantly less trophallaxis and allogrooming behaviour than in the control founding queens, but with no significant increase in aggression. These results suggest that OA promotes the disappearance of cooperation in founding queens of P. moesta. This is the first study to reveal the neuroendocrine mechanism of cooperation in ant queens.

Ant sperm storage organs do not have phenoloxidase constitutive immune activity

The prophenoloxidase system (proPO-AS) is a primordial constituent of insect innate immunity. Its broad action spectrum, rapid response time, and cytotoxic by-products induced by phenoloxidase (PO) production contribute to the effective clearing of invading pathogens. However, such immune reactions may not be optimal for insect organs that evolved to have mutualistic interactions with non-self-cells. Ant queens are long-lived, but only mate early in adult life and store the sperm in a specialized organ, the spermatheca. They never re-mate so their life-time reproductive success is ultimately sperm-limited, which maintains strong selection for high sperm viability before and after storage. The proPO-AS may therefore be inappropriate for the selective clearing of sexually transmitted infections, as it might also target sperm cells that cannot be replaced.We measured PO enzymatic activity in the sperm storage organs of three ant species before and after mating. Our data show that no PO is produced in the sperm storage organs, relative to other somatic tissues as controls, and that these negative results are not due to non-detection in small volumes as non-immune-relevant catalase activity in single spermatheca fluid samples of both virgin and mated queens was significant. The lack of PO activity in sperm storage organs across three different ant species may represent an evolutionarily conserved adaptation to life-long sperm storage by ant queens. We expect that PO activity will be similarly suppressed in queen spermathecae of other eusocial Hymenoptera (bees and wasps) and, more generally, of insect females that store sperm for long periods.

Butterflies that trick ants with sound

Larvae of parasitic Maculinea butterflies use acoustic mimicry to induce host ants to adopt and care for them.

Long live the wasp: adult longevity in captive colonies of the eusocial paper wasp Polistes canadensis (L.).

Insects have been used as an exemplary model in studying longevity, from extrinsic mortality pressures to intrinsic senescence. In the highly eusocial insects, great degrees of variation in lifespan exist between morphological castes in relation to extreme divisions of labour, but of particular interest are the primitively eusocial insects. These species represent the ancestral beginnings of eusociality, in which castes are flexible and based on behaviour rather than morphology. Here we present data on the longevity of the primitively eusocial Neotropical paper wasp P. canadensis, in a captive setting removed of environmental hazards. Captive Polistes canadensis had an average lifespan of 193 ± 10.5 days; although this average is shorter than most bee and ant queens, one individual lived for 506 days in the lab—longer than most recorded wasps and bees. Natal colony variation in longevity does exist between P. canadensis colonies, possibly due to nutritional and genetic factors. This study provides a foundation for future investigations on the effects of intrinsic and extrinsic factors on longevity in primitively eusocial insects, as well as the relationship with natal group and cohort size.

Reproduction-dispersal tradeoffs in ant queens

Organisms often experience reproduction–dispersal tradeoffs mediated by body size. In ants (Hymenoptera: Formicidae) the Found or Fly (FoF) Hypothesis states that dispersing queens face an ecological tradeoff between colony founding and flight success mediated by abdominal nutrient loading. If expressed interspecifically, such a tradeoff implies biomechanical costs to more energetically demanding life history strategies. Claustrally founding queens, who carry the entire resource load necessary to fuel early colony growth, may incur flight costs. We characterized the flight morphology of 21 Neotropical species representing four major subfamilies, spanning four orders of magnitude in body mass and practicing several colony founding strategies. Flight morphologies were compared in a phylogenetic context to evaluate how they varied with body size and reproductive ecology. Consistent with FoF, claustral founders had 30 % lower flight muscle ratios (FMR) and trended toward higher abdomen drag than species in which founding queens feed. The two strategies did not differ in wing loading. Instead, claustral founders evolved larger wings, counteracting the effect of heavier abdomens. Heavy nutrient loads pushed several claustral species to theoretical limits of flight by lowering FMR to levels which cause flightlessness in other insects. Selection for higher nutrient loads related to colony founding is a possible mechanism for the recurrent evolution of flightlessness in ants. The importance and conflicting demands of nutrient storage and flight make ant queens ideal organisms for modeling reproduction–dispersal tradeoffs. By emphasizing the role of flight in ant biology, the FoF Hypothesis highlights this tradeoff and provides novel insights into ant evolution.

Founding weaver ant queens (Oecophylla longinoda) increase production and nanitic worker size when adopting non-nestmate pupae.

Weaver ants (Oecophylla longinoda Latreille) are used commercially to control pest insects and for protein production. In this respect fast colony growth is desirable for managed colonies. Transplantation of non-nestmate pupae to incipient colonies has been shown to boost colony growth. Our objectives were to find the maximum number of pupae a founding queen can handle, and to measure the associated colony growth. Secondly, we tested if transplantation of pupae led to production of larger nanitic workers (defined as unusually small worker ants produced by founding queens in their first batch of offspring). Forty-five fertilized queens were divided into three treatments: 0 (control), 100 or 300 non-nestmate pupae transplanted to each colony. Pupae transplantation resulted in highly increased growth rates, as pupae were readily adopted by the queens and showed high proportions of surviving (mean = 76%). However, survival was significantly higher when 100 pupae were transplanted compared to transplantation of 300 pupae, indicating that queens were unable to handle 300 pupae adequately and that pupae require some amount of nursing. Nevertheless, within the 60-day experiment the transplantation of 300 pupae increased total colony size more than 10-fold whereas 100 pupae increased the size 5.6 fold, compared to control. This increase was due not only to the individuals added in the form of pupae but also to an increased per capita brood production by the resident queen, triggered by the adopted pupae. The size of hatching pupae produced by the resident queen also increased with the number of pupae transplanted, leading to larger nanitic workers in colonies adopting pupae. In conclusion, pupae transplantation may be used to produce larger colonies with larger worker ants and may thus reduce the time to produce weaver ant colonies for commercial purposes. This in turn may facilitate the implementation of the use of weaver ants.

Protein content of leaf-cutting ant queens before the nuptial flight and during the post-claustral phase

Protein content of leaf-cutting ant queens before the nuptial flight and during the post-claustral phase. This study evaluated the crude protein content of queens of Atta sexdens before the nuptial flight and after the claustral phase in laboratory and field colonies. The hypothesis was that protein is used for survival of the queen and for early colony growth during the claustral phase. Additionally, the nest morphology, live biomass and adult population of field colonies were evaluated. Crude protein was determined by digestion of the organic material with sulfuric acid at high temperatures. The mean crude protein content was 123.23 ± 11.20 mg for females before the nuptial flight and 70.44 ± 12.21 mg for laboratory-reared queens after the claustral phase. The post-claustral crude protein content of field-collected queen was 55.90 ± 9.18 mg. With respect to the loss of crude protein as a function of duration of the claustral phase, laboratory-reared queens lost 52.79 mg and field-collected queens lost 67.33 mg compared to females before the nuptial flight. A positive linear correlation was observed between the weight of field-collected queens (256.4 ± 36.3 mg) and colony biomass (13.02 ± 9.12 g), but there was no correlation between biomass and nest depth (13.11 ± 3.82 cm). As expected, the present results support the hypothesis that protein is used for survival of the queen and for early colony growth, as demonstrated by the reduction in crude protein content as a function of duration of the claustral phase. To our knowledge, this is the first study to provide data of the dynamics of protein reserves in leaf-cutting ant queens during the claustral phase.

Dispatches

Dispatches

Temporary sterilization behavior of mutualistic partner ants in a Southeast Asian myrmecophyte

AbstractObligate ant–plant interactions are known to be mutualistic but plant‐ants that destroy flowers of their hosts have been reported. They were regarded as parasites in myrmecophytic systems. The mechanisms that lead to flower damage (sterilization) by plant‐ants are not easy to understand as most sterilizing ants are actually regular colonizers of their plants and normally offer protection against herbivores and/or plant competition. It is difficult to find general patterns of ant or plant traits even in the few yet known associations of flower sterilization. We here present the first study from Southeast Asia where flower sterilizing occurs in the complex mutualistic Macaranga–Crematogaster system that differs from other cases. Flowers of M. hullettii in the Gombak Valley were destroyed by all three associated specific and otherwise protective Crematogaster species. The hypotheses that limitation of nesting space or food are main proximate factors for flower destruction were not strongly supported in our study system. Ants are even attracted to flowers by special food bodies produced by the plants. Only younger, not yet reproductive colonies were found to destroy flowers but not colonies with alates, indicating that flower sterilization behavior may only occur when the onset of host reproduction precedes ant reproduction, perhaps leading to a change in ant behavior. Fruit set always occurred in larger trees, and saplings for colonizing ant queens were therefore always present in the local population, stabilizing the association.

Behavioral plasticity in ant queens: environmental manipulation induces aggression among normally peaceful queens in the socially polymorphic ant Leptothorax acervorum.

The behavioral traits that shape the structure of animal societies vary considerably among species but appear to be less flexible within species or at least within populations. Populations of the ant Leptothorax acervorum differ in how queens interact with other queens. Nestmate queens from extended, homogeneous habitats tolerate each other and contribute quite equally to the offspring of the colony (polygyny: low reproductive skew). In contrast, nestmate queens from patchy habitats establish social hierarchies by biting and antennal boxing, and eventually only the top-ranking queen of the colony lays eggs (functional monogyny: high reproductive skew). Here we investigate whether queen-queen behavior is fixed within populations or whether aggression and high skew can be elicited by manipulation of socio-environmental factors in colonies from low skew populations. An increase of queen/worker ratio and to a lesser extent food limitation elicited queen-queen antagonism in polygynous colonies from Nürnberger Reichswald similar to that underlying social and reproductive hierarchies in high-skew populations from Spain, Japan, and Alaska. In manipulated colonies, queens differed more in ovarian status than in control colonies. This indicates that queens are in principle capable of adapting the magnitude of reproductive skew to environmental changes in behavioral rather than evolutionary time.

Immune priming and pathogen resistance in ant queens.

Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life-history theory predicts that immune priming and large investment in immunity should be more frequent in long-lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditions or species. In both ant species, mated queens showed higher pathogen resistance than virgin queens, which suggests that mating triggers an up-regulation of the immune system. Overall, mated ant queens combine high reproductive output, very long life span, and elevated investment in immune defense. Hence, ant queens are able to invest heavily in both reproduction and maintenance, which can be explained by the fact that mature queens will be protected and nourished by their worker offspring.

Variation in Butterfly Larval Acoustics as a Strategy to Infiltrate and Exploit Host Ant Colony Resources

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.

Performance of the species-typical alarm response in young workers of the ant Myrmica sabuleti (Hymenoptera: Formicidae) is induced by interactions with mature workers.

Young workers of the ant Myrmica sabuleti (Hymenoptera: Formicidae) Meinert 1861 perceived nestmate alarm pheromone but did not display normal alarm behavior (orientation toward the source of emission, increased running speed). They changed their initial behavior when in the presence of older nestmates exhibiting normal alarm behavior. Four days later, the young ants exhibited an imperfect version of normal alarm behavior. This change of behavior did not occur in young ants, which were not exposed to older ants reacting to alarm pheromone. Queen ants perceived the alarm pheromone and, after a few seconds, moved toward its source. Thus, the ants’ ability to sense the alarm pheromone and to identify it as an alarm signal is native, while the adult alarm reaction is acquired over time (= age based polyethism) by young ants. It is possible that the change in behavior observed in young ants could be initiated and/or enhanced (via experience-induced developmental plasticity, learning, and/or other mechanisms) by older ants exhibiting alarm behavior.

Virgin ant queens mate with their own sons to avoid failure at colony foundation

Mother-son mating (oedipal mating) is practically non-existent in social Hymenoptera, as queens typically avoid inbreeding, mate only early in life and do not mate again after having begun to lay eggs. In the ant genus Cardiocondyla mating occurs among sib in the natal nests. Sex ratios are extremely female-biased and young queens face the risk of remaining without mating partners. Here, we show that virgin queens of Cardiocondyla argyrotricha produce sons from their own unfertilized eggs and later mate with them to produce female offspring from fertilized eggs. Oedipal mating may allow C. argyrotricha queens to found new colonies when no mating partners are available and thus maintains their unusual life history combining monogyny, mating in the nest, and low male production. Our result indicates that a trait that sporadically occurs in solitary haplodiploid animals may evolve also in social Hymenoptera under appropriate ecological and social conditions.