Alain Lenoir

Individuality and colonial identity in ants: the emergence of the social representation concept

Colonial identity in social insects is based on nestmate recognition which is mediated through cuticular substances. Although this is considered to be distinct from kin recognition, it is possible that through evolution the signal mediating kinship was replaced by the signal mediating “nestmateship”. Cuticular hydrocarbons in Cataglyphis niger are responsible for modifying the ant’s aggressive behavior and are considered to have a similar function in other ants species. In ants, the postpharyngeal gland (PPG) serves as a storage organ for these cues and functions as a “gestalt” organ, with the gestalt being permanently updated. Its content is constantly being exchanged with nestmates through trophallaxis and allogrooming. We hypothesize that already in the primitive ponerine ants the PPG evolved as a gestalt organ even without trophallaxis. We discuss two alternative primary selective pressures for the evolution of trophallaxis: facilitating food exchange versus exchanging recognition cues. Callow workers seem to be characterized by a “cuticular chemical insignificance” followed by a “chemical integration” period when they acquire the gestalt of the colony and learn the associated template. We hypothesize that the template has evolved from a simple personal chemical reference in primitive species with small colonies to an internal representation of the colonial identity in larger colonies.

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.

Fertility signalling and reproductive skew in queenless ants

Social insects often show an extreme reproductive skew. In queenless ants, colonies consist of morphologically identical workers that can all potentially reproduce sexually. Similarly to that in social vertebrates, aggression in these ants functions to select the reproductive(s). We investigated the mechanisms underlying reproductive skew in the monogynous queenless ant Streblognathus peetersi. Behavioural observations of disturbed hierarchies were integrated with physiological measures of fertility (vitellogenin titre in the haemolymph) and chemical analysis of cuticular hydrocarbons, which are putative fertility pheromones. This multifaceted approach revealed that the colony reproductive is determined as a result of aggression between high-ranking workers, but once an alpha is established, chemical signalling is enough to maintain reproductive skew. As already reported in several species of ants and also in a social wasp, egg layers have distinct profiles of cuticular hydrocarbons compared with infertile workers. Importantly, ‘high rankers’ who are unable to lay eggs also have a specific cuticular profile; this is consistent with their intermediate state of fertility indicated by vitellogenin levels. Rather than just ovarian activity, the cuticular hydrocarbon profile thus reveals the individual hormonal state that underlies reproductive activity. We compare the fertility signal in queenless ants with the ‘badge of status’ reported in various birds. We discuss the evolutionary stability of this communication system and give special emphasis to ecological constraints and the high degree of intracolonial relatedness typical of social insects.

Hydrocarbons in the ant Lasius niger: from the cuticle to the nest and home range marking.

The cuticular hydrocarbons (CHCs) of the ant Lasius niger are described. We observe a high local colony specificity of the body cuticular profile as predicted for a monogynous and multicolonial species. The CHCs show a low geographical variation among different locations in France. The CHCs on the legs also are colony specific, but their relative quantities are slightly different from those on the main body. For the first time, we demonstrate that the inner walls of the ant nest are coated with the same hydrocarbons as those found on the cuticle but in different proportions. The high amount of inner-nest marking and its lack of colony-specificity may explain why alien ants are not rejected once they succeed in entering the nest. The cuticular hydrocarbons also are deposited in front of the nest entrance and on the foraging arena, with a progressive increase in n-alkanes relative amounts. Chemical marks laid over the substrate are colony specific only when we consider methyl-branched alkanes. Our data confirm that these “footprint hydrocarbons” are probably deposited passively by the contact of ant tarsae with the substrate. These results suggest that the CHCs chemical profiles used by ants in colony recognition are much more complex than a single template: ants have to learn and memorize odors that vary depending on their context of perception.

Nest separation and the dynamics of the Gestalt odor in the polydomous ant Cataglyphis iberica (Hymenoptera, Formicidae)

Abstract In the polydomous ant species Cataglyphis iberica, nests belonging to the same colony are completely separated during hibernation. In order to examine whether this separation induces changes both in the hydrocarbon profile and in recognition ability between adult nestmates, we separated groups of workers for several months under two different conditions: at hibernation temperature and at room temperature. At room temperature, recognition remained unchanged but separation led to longer mutual antennations relative to non-separated controls. When half of a colony was placed under hibernation conditions, antennal interactions also increased in duration and a few aggressive interactions emerged between separated ants. This aggressiveness never reached the intercolonial level observed in this species. In both cases, the hydrocarbon profiles showed differences between individuals after separation while remaining homogeneous within each nest. This chemical modification may induce the longer antennations observed. After separated groups were reunited, individuals recovered their previous antennation pattern and a convergence in hydrocarbon profiles was again observed. These concurrent observations suggest that hydrocarbons are transferred between nestmates. In C. iberica, the formation of the colonial odor seems to follow the “Gestalt” model which allows all satellite nests of a colony to have a common colonial odor. In the field, temporary nest isolation during hibernation may induce divergence between satellites. The role of adult transport in connecting nests during the active season to obtain an efficient Gestalt odor is discussed.

Comparative dynamics of gestalt odour formation in two ant species Camponotus fellah and Aphaenogaster senilis (Hymenoptera: Formicidae)

Abstract. Ant colonies experience continuous shifts in worker populations, which may affect odour composition in the nest. A major question regarding the dynamics of gestalt formation is that of the speed at which the scent of a new individual will be incorporated into the gestalt. It is predicted from the gestalt model of colony odour that workers have to exchange recognition cues continuously to maintain themselves within the gestalt and become well integrated within their colony. Using radioactive tracers the rates of transfer were measured between a labelled donor ant and one or 10 recipient ants, as a close approximation to the within‐nest situation. The labelled hydrocarbons were first transferred to a small number of individuals and progressively to all the individuals of the group so that the distribution of hydrocarbon transfer rate approached a normal distribution. Furthermore, in Camponotus fellah Dalla Torre, which performs trophallaxis, homogeneity was reached more rapidly than in Aphaenogaster senilis Mayr, which does not show this behaviour. In the latter species, the gestalt seems to be maintained mainly by allogrooming. These experiments were accompanied by behavioural observations to ascertain the respective importance of trophallaxis and allogrooming in the behavioural time‐budget of the ants. In A. senilis, allogrooming was more frequent than in ants that trophallax, which corroborates the role of allogrooming in the establishment of the gestalt in this species.

Effects of social isolation on hydrocarbon pattern and nestmate recognition in the ant Aphaenogaster senilis (Hymenoptera, Formicidae)

Summary. In the non-trophallacting ant Aphaenogaster senilis, a change over time was observed in cuticular and postpharyngeal gland hydrocarbon profiles. A change was also observed after individual social isolation. Short periods of isolation induced amicable reaction, such as allogrooming, which may have facilitated re-integration of the isolated ants into their mother colonies. Longer periods of isolation, on the other hand, caused overt aggression towards the isolated ants when reintroduced into their mother colonies, and also resulted in higher changes in cuticular hydrocarbon profile. This correlation suggests a link between these two phenomena. We suggest that in A. senilis, in the absence of cue transfer by trophallaxis: a) colony odour constitutes a gestalt, and b) the major means of cue transfer is allogrooming. The possible evolution of allogrooming and trophallaxis as cue transfer modalities is discussed.

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.

Trophallaxis mediates uniformity of colony odor in Cataglyphis iberica ants (Hymenoptera, Formicidae)

We studied the effect of nestmate separation on trophallaxis in the polydomous ant Cataglyphis iberica. After dividing three colonies into two equivalent subgroups, one queenright and one queenless, we quantified the frequency of trophallaxis within each subgroup, between the workers from the two subgroups (“mixed” trophallaxis), and trophallaxis involving the queen. Observations of trophallaxis were conducted over four periods of time: for 2 weeks before the separation of the two subgroups, 8 weeks during separation, immediately after reunification, and 3 weeks following reunification. Subgroups were identically fed on the eve of each day of observation. Group separation induced an increase in “mixed” frequencies of trophallaxis just after reunification, after which trophallaxis returned to the initial level observed before separation. Previous results showed that group separation in C. iberica induces hydrocarbon profile divergence and that reunification restores this chemical modification. The current results seem to indicate that increased trophallaxis permits a uniform odor to be reestablished among previously separated ants. Trophallaxis involving the queen is infrequent and does not seem to be crucial in the process of odor exchange. Our data confirm that trophallaxis plays a key role in establishing the “Gestalt” colony odor, particularly among naturally separated satellite nests in a polydomous species like C. iberica.