Raphaël Boulay

Camponotus fellah colony integration : worker individuality necessitates frequent hydrocarbon exchanges

Our aim was to test the existence of Gestalt colony odour in Camponotus fellah. We isolated individual workers to prevent trophallaxis, allogrooming and body contact. After 20 days, the cuticular hydrocarbon profile of the isolated ants diverged from that of the parent colony. Moreover, each isolated individual had its own specific blend. This procedure showed that after about 20 days of isolation there was a turnover of the colony odour, revealing the genetically expressed hydrocarbon profile of each individual. It also showed that the cuticular hydrocarbon profile is polymorphic, and that its homogeneity within a colony is maintained by frequent exchanges of hydrocarbons between workers. Behavioural observations of resident workers, in their nest, towards nestmates reintroduced after isolation indicated that a short isolation period (3-5 days), which induced a minor change in hydrocarbon profile, provoked frequent trophallactic solicitations. These were likely to permit the isolated ants to readjust their hydrocarbon profile to that of the ants in the mother colony. Longer isolation periods (20-40 days) induced a greater change in hydrocarbon profile and made the residents intolerant towards their introduced nestmates. Therefore, our results clearly support the existence of a Gestalt colony odour in C. fellah. They also show that since individual hydrocarbon production is dynamic, workers are obliged to exchange hydrocarbons continually (mainly by trophallaxis) in order to be in the Gestalt, and properly integrate into the colony. Copyright 2000 The Association for the Study of Animal Behaviour.

Individual and collective foraging decisions: a field study of worker recruitment in the gypsy ant Aphaenogaster senilis

In social insects, the decision to exploit a food source is made both at the individual (e.g., a worker collecting a food item) and colony level (e.g., several workers communicating the existence of a food patch). In group recruitment, the recruiter lays a temporary chemical trail while returning from the food source to the nest and returns to the food guiding a small group of nestmates. We studied how food characteristics influence the decision-making process of workers changing from individual retrieving to group recruitment in the gypsy ant Aphaenogaster senilis. We offered field colonies three types of prey: crickets (cooperatively transportable), shrimps (non-transportable), and different quantities of sesame seeds (individually transportable). Colonies used group recruitment to collect crickets and shrimps, as well as seeds when they were available in large piles, while small seed piles rarely led to recruitment. Foragers were able to “measure” food characteristics (quality, quantity, transportability), deciding whether or not to recruit, accordingly. Social integration of individual information about food emerged as a colony decision to initiate or to continue recruitment when the food patch was rich. In addition, group recruitment allowed a fast colony response over a wide thermal range (up to 45°C ground temperature). Therefore, by combining both advantages of social foraging (group recruitment) and thermal tolerance, A. senilis accurately exploited different types of food sources which procured an advantage against mass-recruiting and behaviorally dominant species such as Tapinoma nigerrimum and Lasius niger.

Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size

Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour’s and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colony-level recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen’s influence, creating a second mode of colony fission.

Social Hybridogenesis in the Clonal Ant Cataglyphis hispanica

With a few rare exceptions, the vast majority of animals reproduce sexually. Some species have, however, evolved alternative modes of reproduction by shifting from classical bisexuality to unorthodox reproductive systems, like parthenogenesis, gynogenesis, or hybridogenesis. Under hybridogenesis, both the maternal and paternal genomes are expressed in somatic tissues, whereas the germline is purely maternal. Recently, a form of hybridogenesis at the level of the society has been reported in some ants, where purebred females develop into reproductive queens and interlineage hybrids into sterile workers. Here, we report a unique case of social hybridogenesis in the desert ant Cataglyphis hispanica. Workers are produced exclusively from interbreeding between two distinct genetic lineages, whereas male and female sexuals are produced by asexual reproduction through parthenogenesis. As a consequence, all workers are pure hybridogens, and only maternal genes are perpetuated from one generation to the next. Thus, queens of C. hispanica use sexual reproduction for colony growth, whereas they reproduce asexually through parthenogenesis for germline production.

Colony insularity through queen control on worker social motivation in ants

We investigated the relative contribution of the queen and workers to colony nestmate recognition cues and on colony insularity in the Carpenter ant Camponotus fellah. Workers were either individually isolated, preventing contact with both queen and workers (colonial deprived, CD), kept in queenless groups, allowing only worker-worker interactions (queen deprived, QD) or in queenright (QR) groups. Two weeks post-separation QD and QR workers were amicable towards each other but both rejected their CD nestmates, which suggests that the queen does not measurably influence the colony recognition cues. By contrast, aggression between QD and QR workers from the same original colony was apparent only after six months of separation. This clearly demonstrates the power of the Gestalt and indicates that the queen is not a dominant contributor to the nestmate recognition cues in this species. Aggression between nestmates was correlated with a greater hydrocarbon (HC) profile divergence for CD than for QD and QR workers, supporting the importance of worker-worker interactions in maintaining the colony Gestalt odour. While the queen does not significantly influence nestmate recognition cues, she does influence colony insularity since within 3 days QD (queenless for six months) workers from different colony origins merged to form a single queenless colony. By contrast, the corresponding QR colonies maintained their territoriality and did not merge. The originally divergent cuticular and postpharyngeal gland HC profiles became congruent following the merger. Therefore, while workers supply and blend the recognition signal, the queen affects worker-worker interaction by reducing social motivation and tolerance of alien conspecifics.

Odour convergence and tolerance between nestmates through trophallaxis and grooming in the ant Camponotus fellah (Dalla Torre)

SummarySocial isolation provides a useful tool to study nestmate recognition in ants. In Camponotus fellah, reintroduction of 10-day isolated (IS) workers to their colony resulted in intensive trophallaxis and grooming, while longer isolation periods generally provoked rejection of the IS ants. In the first experiment the behaviour of queenless (QL) and queenright (QR) workers towards 10-day IS workers was tested. Trophallaxis of QL or QR with IS workers was of similar magnitude, but was significantly higher than that among the QL or QR, or that between QL and QR workers. Allogrooming was mostly initiated by the resident non-isolated ants (QL or QR) possibly because they detected a slight mismatch between the IS ant’s odour and their own template, which represents the group odour. It appears that the presence/absence of the queen did not affect nestmate recognition cues of workers.The second experiment demonstrated that 20-day IS workers were strongly aggressed by colony guards, irrespective of whether they were QL or QR. However, if they were permitted to exchange trophallaxis and grooming with 5 young nestmates (companion ants) for 5 days before reintroduction to their colony, aggression was greatly reduced, irrespective of the origin of the companion ants (QR or QL). Chemical analysis showed a significant divergence between the hydrocarbon profiles of IS and both QL and QR groups, but a prior contact of the IS workers with companion ants resulted in re-convergence of their profile with that of the colony. These results demonstrate that nestmate recognition cues are exchanged between workers via trophallaxis and grooming and that they are not dominated by queen cues, two conditions that fulfil Gestalt nestmate recognition signals requirements.

Intraspecific competition in the ant Camponotus cruentatus: should we expect the ‘dear enemy’ effect?

The mechanisms of competition and resource domination were analysed in the Mediterranean ant Camponotus cruentatus. In a plot located in southern Spain mature colonies are overdispersed, which is indicative of territoriality in other species. Unexpectedly, however, workers from neighbouring colonies commonly foraged in areas that overlapped by more than 44%. This suggests that while mature colonies possibly prevent the establishment of new colonies in the vicinity of their nests, they do not limit the intrusion of alien foragers. In contrast, rich food sources located in common foraging areas are aggressively defended, generally leading to their domination by the nest that discovered them first. Resource exploitation further requires rapid recruitment of foragers and soldiers to transport food as well as to exclude competitors. Complementary to the field experiments we conducted laboratory bioassays to assess intercolonial aggression. Group encounters showed that workers of C. cruentatus were equally aggressive towards alien ants irrespective of whether they were sympatric neighbours (and had possibly had contact), sympatric nonneighbours (which had probably had no contact), or allopatric. This was corroborated by analysis of the hydrocarbons that generally serve as colony recognition cues. This mixture, which contains an unusual proportion of trimethylalkanes, showed important colony specificity. The high intraspecific aggression shown indiscriminately by workers indicates that the ‘dear enemy’ effect does not exist in this species and suggests that scarce resources are worth defending against intraspecific competitors. We discuss several proximate and ultimate constraints that may prevent the general occurrence of this process in ants.

Synchrony between fruit maturation and effective dispersers' foraging activity increases seed protection against seed predators

The evolution of pollination and seed dispersal mutualisms is conditioned by the spatial and temporal co-occurrence of animals and plants. In the present study we explore the timing of seed release of a myrmecochorous plant (Helleborus foetidus) and ant activity in two populations in southern Spain during 2 consecutive years. The results indicate that fruit dehiscence and seed shedding occur mostly in the morning and correspond to the period of maximum foraging activity of the most effective ant dispersers. By contrast, ant species that do not transport seeds and/or that do not abound near the plants are active either before or after H. foetidus diaspores are released. Experimental analysis of diet preference for three kinds of food shows that effective ant dispersers are mostly scavengers that readily feed on insect corpses and sugars. Artificial seed depots suggest that seeds deposited on the ground out of the natural daily time window of diaspore releasing are not removed by ants and suffer strong predation by nocturnal rodents Apodemus sylvaticus. Nevertheless, important inter-annual variations in rodent populations cast doubts on their real importance as selection agents. We argue that traits allowing synchrony between seed presentation and effective partners may constitute a crucial pre-adaptation for the evolution of plant–animal mutualisms involving numerous animal partners.

Brood development into sexual females depends on the presence of a queen but not on temperature in an ant dispersing by colony fission, Aphaenogaster senilis

Abstract. 1. In eusocial insects, colony fission is a mode of dispersal by which a young queen leaves her nest with some workers to found a new colony. In these species, adult females (workers and the queen) should allocate most resources to increasing their colony size, which constrains the possibility of fission. In contrast, developing diploid larvae should have a preference for becoming a queen and having their own offspring, rather than becoming workers and rearing the offspring of other females.

Geographic variations in seed dispersal by ants: are plant and seed traits decisive?

The effect of local ant species on the dispersal success of a myrmecochorous plant, Helleborus foetidus, was analyzed in two populations of the Iberian Peninsula (Caurel and Cazorla, respectively). The contribution of the various local ant species to dispersal was very unequal. While 5 and 19 ant taxa visited the plants of Caurel and Cazorla, respectively, most removal activity (67 and 80%) was performed by two species only (Formica lugubris and Camponotus cruentatus, respectively). Visits by dispersers were also unequally distributed between neighboring plants. While some plants were always visited during the period of seed release, others were never visited. A regression model indicated that this pattern might be explained by two plant traits: ants preferred to visit plants that released more seeds and whose elaiosomes were richer in oleic acid. Although it has long been known that this compound triggers removal by ants, it is the first demonstration that quantitative variations in elaiosome traits contribute to variation in dispersal success. Finally, other variables being equal, morphological traits (seed size, elaiosome size, and elaiosome/seed size ratio) did not affect ant behavior. Although myrmecochory has long been considered a diffuse interaction, our results support the idea that, at local scale, a limited number of ant species may be decisive to its evolution.