A temporary social parasite of tropical plant-ants improves the fitness of a myrmecophyte

Myrmecophytes offer plant-ants a nesting place in exchange for protection from their enemies, particularly defoliators. These obligate ant–plant mutualisms are common model systems for studying factors that allow horizontally transmitted mutualisms to persist since parasites of ant–myrmecophyte mutualisms exploit the rewards provided by host plants whilst providing no protection in return. In pioneer formations in French Guiana, Azteca alfari and Azteca ovaticeps are known to be mutualists of myrmecophytic Cecropia (Cecropia ants). Here, we show that Azteca andreae, whose colonies build carton nests on myrmecophytic Cecropia, is not a parasite of Azteca–Cecropia mutualisms nor is it a temporary social parasite of A. alfari; it is, however, a temporary social parasite of A. ovaticeps. Contrarily to the two mutualistic Azteca species that are only occasional predators feeding mostly on hemipteran honeydew and food bodies provided by the host trees, A. andreae workers, which also attend hemipterans, do not exploit the food bodies. Rather, they employ an effective hunting technique where the leaf margins are fringed with ambushing workers, waiting for insects to alight. As a result, the host trees’ fitness is not affected as A. andreae colonies protect their foliage better than do mutualistic Azteca species resulting in greater fruit production. Yet, contrarily to mutualistic Azteca, when host tree development does not keep pace with colony growth, A. andreae workers forage on surrounding plants; the colonies can even move to a non-Cecropia tree.     

When attempts at robbing prey turn fatal

Because group-hunting arboreal ants spread-eagle insect prey for a long time before retrieving them, these prey can be coveted by predatory flying insects. Yet, attempting to rob these prey is risky if the ant species is also an effective predator. Here, we show that trying to rob prey from Azteca andreae workers is a fatal error as 268 out of 276 potential cleptobionts (97.1?%) were captured in turn. The ant workers hunt in a group and use the “Velcro?” principle to cling firmly to the leaves of their host tree, permitting them to capture very large prey. Exceptions were one social wasp, plus some Trigona spp. workers and flies that landed directly on the prey and were able to take off immediately when attacked. We conclude that in this situation, previously captured prey attract potential cleptobionts that are captured in turn in most of the cases.     

Nest site selection and induced response in a dominant arboreal ant species

It is well known that arboreal ants, both territorially dominant species and plant ants (e.g., species associated with myrmecophytes or plants housing them in hollow structures), protect their host trees from defoliators. Nevertheless, the presence of an induced defense, suggested by the fact that the workers discovering a leaf wound recruit nestmates, is only known for plant ants. Based on the results from a field study, we show here (1) that colonies of Azteca chartifex, a territorially dominant, neotropical arboreal ant species, mostly selected Goupia glabra (Goupiaceae) trees in which to build their principal carton nests and (2) that plant signals induced workers to recruit nestmates, which patrol the leaves, likely providing the plant with a biotic defense. Furthermore, the number of recruited workers was clearly higher on G. glabra, their most frequently selected host tree species, than on other tree species. These results show that contrary to what was previously believed, induced responses are also found in territorially dominant arboreal ants and so are not limited to the specific associations between myrmecophytes and plant ants.     

An absence of aggression between non-nestmates in the bull ant <Emphasis Type="Italic">Myrmecia nigriceps</Emphasis>

The ability of social insects to discriminate against non-nestmates is vital for maintaining colony integrity, and in most social insect species, individuals act aggressively towards non-nestmates that intrude into their nest. Our experimental field data revealed that intra-colony aggression in the primitive bulldog ant Myrmecia nigriceps is negligible; our series of bioassays revealed no significant difference in the occurrence of aggression in trials involving workers from the same, a close (less than 300 m) or a far (more than 1.5 km) nest. Further, non-nestmate intruders were able to enter the nest in 60% of our trials; a similar level was observed in trials involving nestmates. These results suggest that workers of M. nigriceps are either unable to recognize alien conspecifics or that the costs of ignoring workers from foreign colonies are sufficiently low to favor low levels of inter-colony aggression in this species.     

Workers select mates for queens: a possible mechanism of gene flow restriction between supercolonies of the invasive Argentine ant

Some invasive ants form large networks of mutually non-aggressive nests, i.e., supercolonies. The Argentine ant Linepithema humile forms much larger supercolonies in introduced ranges than in its native range. In both cases, it has been shown that little gene flow occurs between supercolonies of this species, though the mechanism of gene flow restriction is unknown. In this species, queens do not undertake nuptial flight, and males have to travel to foreign nests and cope with workers before gaining access to alien queens. In this study, we hypothesized that male Argentine ants receive interference from workers of alien supercolonies. To test this hypothesis, we conducted behavioral and chemical experiments using ants from two supercolonies in Japan. Workers attacked males from alien supercolonies but not those from their own supercolonies. The level of aggression against alien males was similar to that against alien workers. The frequency of severe aggression against alien males increased as the number of recipient workers increased. Cuticular hydrocarbon profiles, which serve as cues for nestmate recognition, of workers and males from the same supercolony were very similar. Workers are likely to distinguish alien males from males of their own supercolony using the profiles. It is predicted that males are subject to considerable aggression from workers when they intrude into the nests of alien supercolonies. This may be a mechanism underlying the restricted gene flow between supercolonies of Argentine ants. The Argentine ant may possess a distinctive reproductive system, where workers participate in selecting mates for their queens. We argue that the aggression of workers against alien males is a novel form of reproductive interference.     

Knowing your enemies: seasonal dynamics of host–social parasite recognition

Despite its evolutionary significance, behavioural flexibility of social response has rarely been investigated in insects. We studied a host–social parasite system: the slave-making ant Polyergus rufescens and its host Formica rufibarbis. Free-living host workers from parasitized and from unparasitized areas were compared in their level of aggression against the parasite and alien conspecifics. We expected that a seasonal change would occur in the acceptance threshold of F. rufibarbis workers from a parasitized area towards the parasite, whereas F. rufibarbis workers from an unparasitized area would not show substantial changes connected with the parasites peak in activity (raiding and colony-founding season). The results showed a significant adaptive behavioural flexibility of host species workers and are consistent with the acceptance threshold models (Reeve 1989) prediction that recognition systems are not fixed but context-dependent. In particular, host workers from the unparasitized area were highly aggressive towards the parasite regardless of the season, whereas host workers from the parasitized area significantly increased their aggression towards the parasite during its raiding and colony-founding season. Being able to detect and possibly kill a Polyergus scout searching for host nests can be an effective strategy for a Formica colony to avoid being raided or usurped by a parasite queen.     

Shell colour,temperature, (micro)habitat structure and predator pressure affect the behaviour of <Emphasis Type="Italic">Cepaea nemoralis</Emphasis>

Although shell colour polymorphism of the land snail Cepaea nemoralis is a well-known phenomenon, proximate and ultimate factors driving its evolution remain uncertain. Polymorphic species show variation in behavioural responses to selective forces. Therefore, we estimated effects of various environmental factors (temperature, humidity, food availability, (micro)habitat structure and predatory pressure) on behavioural response (frequency of locomotion, climbing and hiding) of C. nemoralis morphs, in experimental and natural conditions. In the experimental part of study, the frequency of locomotion was negatively affected by temperature and the presence of food and positively influenced by the presence of light. Morphs significantly differed in behavioural responses to environmental variability. Pink mid-banded and yellow five-banded morphs climbed less often and hide in shelter more often than yellow and pink unbanded individuals when temperature was low and food was absent. Snails fed most often at moderate temperature compared to low and high temperatures. Field investigations partially confirmed differences among morphs in frequency of climbing, but not in terms of probability of hiding in sheltered sites. In natural colonies, temperature and (micro)habitat structure significantly affected frequency of climbing as well as hiding in shelter. Snails more often hid in sheltered sites where thrushes preyed on Cepaea. Tendency of unbanded morphs to climb trees may have evolved under avian predatory pressure as thrushes forage on a ground. Tendency of banded morphs to hide in sheltered sites may reflect prey preferences for cryptic background. The results implicate that differential behaviour of C. nemoralis morphs compensate for their morphological and physiological limitations of adaptation to habitat.     

Nest- and colony-mate recognition in polydomous colonies of meat ants (Iridomyrmex purpureus)

Workers of polydomous colonies of social insects must recognize not only colony-mates residing in the same nest but also those living in other nests. We investigated the impact of a decentralized colony structure on colony- and nestmate recognition in the polydomous Australian meat ant (Iridomyrmex purpureus). Field experiments showed that ants of colonies with many nests were less aggressive toward alien conspecifics than those of colonies with few nests. In addition, while meat ants were almost never aggressive toward nestmates, they were frequently aggressive when confronted with an individual from a different nest within the same colony. Our chemical analysis of the cuticular hydrocarbons of workers using a novel comprehensive two-dimensional gas chromatography technique that increases the number of quantifiable compounds revealed both colony- and nest-specific patterns. Combined, these data indicate an incomplete transfer of colony odor between the nests of polydomous meat ant colonies.     

Two pathways ensuring social harmony

Reproductive division of labour is a characteristic trait of social insects. The dominant reproductive individual, often the queen, uses chemical communication and/or behaviour to maintain her social status. Queens of many social insects communicate their fertility status via cuticle-bound substances. As these substances usually possess a low volatility, their range in queen–worker communication is potentially limited. Here, we investigate the range and impact of behavioural and chemical queen signals on workers of the ant Temnothorax longispinosus. We compared the behaviour and ovary development of workers subjected to three different treatments: workers with direct chemical and physical contact to the queen, those solely under the influence of volatile queen substances and those entirely separated from the queen. In addition to short-ranged queen signals preventing ovary development in workers, we discovered a novel secondary pathway influencing worker behaviour. Workers with no physical contact to the queen, but exposed to volatile substances, started to develop their ovaries, but did not change their behaviour compared to workers in direct contact to the queen. In contrast, workers in queen-separated groups showed both increased ovary development and aggressive dominance interactions. We conclude that T. longispinosus queens influence worker ovary development and behaviour via two independent signals, both ensuring social harmony within the colony.     

Aggressions and size-related fecundity of queenless workers in the ant <Emphasis Type="Italic">Cataglyphis cursor</Emphasis>

In social hymenoptera, the reproductive division of labor is often linked to differences in individual body size with the reproductive caste (the queen) being larger than the workers. Likewise, the reproductive potential may vary with size within the worker caste and could affect the evolution of worker size in social insects. Here, we tested the relationship between worker size and reproductive potential in the facultative parthenogenetic ant Cataglyphis cursor. Colonies are headed by a multiply mated queen, but workers can produce gynes (virgin queens) and workers by thelytokous parthenogenesis after the queen's death. We observed the behaviour of workers (n = 357) until the production of gynes (212 h over 3 months) in an orphaned colony (mated queen not present). The size of workers was measured, and their paternal lineage determined using six microsatellite markers, to control for an effect of patriline. Larger workers were more likely to reproduce and lay more eggs indicating that individual level selection could take place. However, paternal lineage had no effect on the reproductive potential and worker size. From the behavioural and genetic data, we also show for the first time in this species, evidence of aggressive interactions among workers and a potential for nepotism to occur in orphaned colonies, as the five gynes produced belonged to a single paternal lineage.     

Docile sitters and active fighters in paper wasps: a tale of two queens

Ropalidia marginata and Ropalidia cyathiformis are sympatric, primitively eusocial paper wasps widely distributed in peninsular India. We compare the two species, especially their queens, in an attempt to begin to understand the role of the power of queens over their workers, in social organisation and evolution. Queens of R. marginata have lower levels of activity, rates of interactions and dominance behaviour, compared with queens of R. cyathiformis. For the same variables, R. marginata queens are either indistinguishable from or have lower values than their workers, while R. cyathiformis queens have higher values than their workers. R. marginata queens never occupy the top rank while R. cyathiformis queens are always at the top of the behavioural dominance hierarchies of their colonies. R. marginata queens thus do not appear to use dominance behaviour to suppress reproduction by their workers, while R. cyathiformis queens appear to do so. These different mechanisms used by the two queens to regulate worker reproduction give them different powers over their workers, because R. marginata queens are completely successful in suppressing reproduction by their nestmates while in R. cyathiformis colonies, other individuals also sometimes lay eggs. There is also some evidence that the different powers of the queens result in different mechanisms of regulation of worker foraging in the two species--decentralised, self-regulation in R. marginata and relatively more centralised regulation by the queen in R. cyathiformis. Thus we show here, perhaps for the first time, that the power of the queens over their workers can have important consequences for social organisation and evolution.     

Potential increase in mating frequency of queens in feral colonies of Bombus terrestris introduced into Japan

With the exception of several species, bumblebees are monandrous. We examined mating frequency in feral colonies of the introduced bumblebee Bombus terrestris in Japan. Using microsatellite markers, genotyping of sperm DNA stored in the spermatheca of nine queens detected multiple insemination paternities in one queen; the others were singly mated. The average effective paternity frequency estimated from the genotypes of queens and workers was 1.23; that estimated from the workers’ genotype alone was 2.12. These values were greater than those of laboratory-reared colonies in the native ranges of B. terrestris. The genotypes of one or two workers did not match those of their queens or showed paternities different from those of their nestmates; this may have arisen from either queen takeover or drifting of workers. These alien workers were responsible for the heterogeneous genotype distribution within each B. terrestris colony, resulting in higher estimates of paternity frequency than of insemination frequency. The high mating frequency of introduced B. terrestris may have occurred by artificial selection through mass breeding for commercialization. Moreover, polyandrous queens may be selectively advantageous, because reproduction by such queens is less likely to be disturbed by interspecific mating than that by monandrous queens.     

Conservation of Bio synthetic pheromone pathways in honeybees Apis

Social insects use complex chemical communication systems to govern many aspects of their life. We studied chemical changes in Dufours gland secretions associated with ovary development in several genotypes of honeybees. We found that C28–C38 esters were associated only with cavity nesting honeybee queens, while the alcohol eicosenol was associated only with their non-laying workers. In contrast, both egg-laying anarchistic workers and all parasitic Cape workers from queenright colonies showed the typical queen pattern (i.e. esters present and eicosenol absent), while egg-laying wild-type and anarchistic workers in queenless colonies showed an intermediate pattern, producing both esters and eicosenol but at intermediate levels. Furthermore, neither esters nor eicosenol were found in aerial nesting honeybee species. Both esters and eicosenol are biosynthetically similar compounds since both are recognizable products of fatty acid biosynthesis. Therefore, we propose that in honeybees the biosynthesis of esters and eicosenol in the Dufours gland is caste-regulated and this pathway has been conserved over evolutionary time.     

Colony size affects division of labour in the ponerine ant<Emphasis Type="Italic"> Rhytidoponera metallica</Emphasis>

In theory, larger colonies of social insects should have greater colony organisation. While inter-specific comparative studies provide support for this idea, there is little direct intra-specific evidence. We investigated differences in task specialisation between large (>450 workers) and small (<80 workers) colonies of the ponerine ant Rhytidoponera metallica. Observations of individually marked young or old workers revealed greater task specialisation in large colonies. Age polyethism was detected in large but not small colonies. In large colonies, old workers spent significantly more time foraging than young workers did, while young workers spent more time caring for brood. In small colonies, young and old workers spent a similar amount of time foraging and caring for brood. This difference in task allocation patterns in large and small colonies was associated with a difference in contact rates between workers. Workers in small colonies have a lower contact rate between nestmates and a greater variability in time between contacts than workers from large colonies.     

A unique strategy of host colony exploitation in a parasitic ant: workers of<Emphasis Type="Italic"> Polyrhachis lama</Emphasis> rear their brood in neighbouring host nests

The formicine ant Polyrhachis lama is a social parasite, exploiting its ponerine host ant species Diacamma sp. In most social parasitic associations, the parasitic species are closely related to their host species group, evolving directly from independent ancestors of the host species. However, in the Polyrhachis lama–Diacamma sp. association, the associated species belong to different ant subfamilies. Based on preliminary field surveys, we had presumed that P. lama might have given up its reproductive division of labour, i.e. workers would be able to produce males as well as workers and females parthenogenetically. In this study, this hypothesis was disproved: Polyrhachis lama workers cannot be fertilized and are only able to produce males. In the host–parasite association originating from nests possessing a P. lama queen, workers penetrate surrounding Diacamma sp. nests, carrying brood for rearing within these satellite nests. In this peculiar way, a single P. lama colony is able to exploit several Diacamma sp. colonies simultaneously.     

Altruism during predation in an assassin bug

Zelus annulosus is an assassin bug species mostly noted on Hirtella physophora, a myrmecophyte specifically associated with the ant Allomerus decemarticulatus known to build traps on host tree twigs to ambush insect preys. The Z. annulosus females lay egg clutches protected by a sticky substance. To avoid being trapped, the first three instars of nymphs remain grouped in a clutch beneath the leaves on which they hatched, yet from time to time, they climb onto the upper side to group ambush preys. Long-distance prey detection permits these bugs to capture flying or jumping insects that alight on their leaves. Like some other Zelus species, the sticky substance of the sundew setae on their forelegs aids in prey capture. Group ambushing permits early instars to capture insects that they then share or not depending on prey size and the hunger of the successful nymphs. Fourth and fifth instars, with greater needs, rather ambush solitarily on different host tree leaves, but attract siblings to share large preys. Communal feeding permits faster prey consumption, enabling small nymphs to return sooner to the shelter of their leaves. By improving the regularity of feeding for each nymph, it likely regulates nymphal development, synchronizing molting and subsequently limiting cannibalism.     

The hunter becomes the hunted: when cleptobiotic insects are captured by their target ants

Here we show that trying to rob prey (cleptobiosis) from a highly specialized predatory ant species is risky. To capture prey, Allomerus decemarticulatus workers build gallery-shaped traps on the stems of their associated myrmecophyte, Hirtella physophora. We wondered whether the frequent presence of immobilized prey on the trap attracted flying cleptoparasites. Nine social wasp species nest in the H. physophora foliage; of the six species studied, only Angiopolybia pallens rob prey from Allomerus colonies. For those H. physophora not sheltering wasps, we noted cleptobiosis by stingless bees (Trigona), social wasps (A. pallens and five Agelaia species), assassin bugs (Reduviidae), and flies. A relationship between the size of the robbers and their rate of capture by ambushing Allomerus workers was established for social wasps; small wasps were easily captured, while the largest never were. Reduviids, which are slow to extract their rostrum from prey, were always captured, while Trigona and flies often escaped. The balance sheet for the ants was positive vis-à-vis the reduviids and four out of the six social wasp species. For the latter, wasps began by cutting up parts of the prey’s abdomen and were captured (or abandoned the prey) before the entire abdomen was retrieved so that the total weight of the captured wasps exceeded that of the prey abdomens. For A. pallens, we show that the number of individuals captured during attempts at cleptobiosis increases with the size of the Allomerus’ prey.     

A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking early observations with recent findings

Myrmecophily provides various examples of how social structures can be overcome to exploit vast and well-protected resources. Ant nest beetles (Paussinae) are particularly well suited for ecological and evolutionary considerations in the context of association with ants because life habits within the subfamily range from free-living and predatory in basal taxa to obligatory myrmecophily in derived Paussini. Adult Paussini are accepted in the ant society, although parasitising the colony by preying on ant brood. Host species mainly belong to the ant families Myrmicinae and Formicinae, but at least several paussine genera are not host-specific. Morphological adaptations, such as special glands and associated tufts of hair (trichomes), characterise Paussini as typical myrmecophiles and lead to two different strategical types of body shape: while certain Paussini rely on the protective type with less exposed extremities, other genera access ant colonies using glandular secretions and trichomes (symphile type). We compare these adaptations with other taxonomic groups of insects by joining contemporary research and early sources and discuss the possibility of an attracting or appeasing effect of the secretion. Species that are ignored by their host ants might use chemical mimicry instead. Furthermore, vibrational signals may contribute to ant–beetle communication, and chemical signals have proven to play a role in host finding. The powerful defense chemistry of paussines as “bombardier beetles” is not used in contact with host ants. We attempt to trace the evolution of myrmecophily in paussines by reviewing important aspects of the association between paussine beetles and ants, i.e. morphological and potential chemical adaptations, life cycle, host specificity, alimentation, parasitism and sound production.

Thelytokous parthenogenesis by queens in the dacetine ant Pyramica membranifera (Hymenoptera: Formicidae)

Thelytokous parthenogenesis in which diploid females are produced from unfertilized eggs, was recently reported for some ant species. Here, we document thelytokous reproduction by queens in the polygynous species Pyramica membranifera. Queens that emerged in the laboratory were kept with or without workers under laboratory conditions. Independent colony founding was successful for a few queens if prey was provided. All artificial colonies, which started with a newly emerged queen and workers produced new workers and some of the colonies also produced female sexuals. Some of the female sexuals shed their wings in the laboratory and started formation of new polygynous colonies. Workers had no ovaries and thus, were obligatorily sterile.     

Temperature and parasitism by <Emphasis Type="BoldItalic">Asobara tabida</Emphasis> (Hymenoptera: Braconidae) influence larval pupation behaviour in two <Emphasis Type="BoldItalic">Drosophila</Emphasis> species

In holometabolous insects, pupation site selection behaviour has large consequences for survival. Here, we investigated the combined effects of temperature and parasitism by the parasitoid Asobara tabida on larval pupation behaviour in two of its main Drosophila sp. hosts differing in their climate origin. We found that larvae of Drosophila melanogaster—a species with a (sub)tropical origin—placed at 25°C pupated higher in rearing jars than those placed at 15°C. The opposite pattern was observed for Drosophila subobscura larvae—a species from temperate regions—which pupated lower, i.e. on or near the substrate at 25°C, than those placed at 15°C. When placed at 25°C, parasitized larvae of both species pupated closer to the substrate than unparasitized ones. Moreover, the Drosophila larvae that had been exposed and probably stung by A. tabida, but were not parasitized, pupated lower than the control unparasitized larvae. These results provide new insights of host behaviour manipulation by A. tabida larvae.