Quorum sensing, recruitment, and collective decision-making during colony emigration by the ant Leptothorax albipennis

When its nest is damaged, a colony of the ant Leptothorax albipennis skillfully emigrates to the best available new site. We investigated how this ability emerges from the behaviors used by ants to recruit nestmates to potential homes. We found that, in a given emigration, only one-third of the colony's workers ever recruit. At first, they summon fellow recruiters via tandem runs, in which a single follower is physically led all the way to the new site. They later switch to recruiting the passive majority of the colony via transports, in which nestmates are simply carried to the site. After this switch, tandem runs continue sporadically but now run in the opposite direction, leading recruiters back to the old nest. Recruitment accelerates with the start of transport, which proceeds at a rate 3 times greater than that of tandem runs. The recruitment switch is triggered by population increase at the new site, such that ants lead tandem runs when the site is relatively empty, but change to transport once a quorum of nestmates is present. A model shows that the quorum requirement can help a colony choose the best available site, even when few ants have the opportunity to compare sites directly, because recruiters to a given site launch the rapid transport of the bulk of the colony only if enough active ants have been "convinced" of the worth of the site. This exemplifies how insect societies can achieve adaptive colony-level behaviors from the decentralized interactions of relatively poorly informed insects, each combining her own limited direct information with indirect cues about the experience of her nestmates.     

Rules of supply and demand regulate recruitment to food in an ant society

The process by which ant scouts move a group of nestmates toward a newly discovered food site is called recruitment. In this paper, I report on the interactions between scouts and nestmates that result in a graded recruitment response to graded food quality in the fire ant, Solenopsis invicta. Twelve experimental groups composed of 100 fire ant workers and 50 fire ant larvae were established (three experimental groups per colony × four stock colonies). Each experimental group was placed in a shallow, artificial nest with a glass cover. After a 48-h period of food deprivation, experimental groups were exposed to one of three concentrations of sugar water. Behavioral interactions between scouts and nestmates in each group were videotaped at 10× magnification for 20 min. Detailed behavioral data on a total of 120 scouts (10 scouts per experimental group) and ~1,000 nestmates (~90 nestmates per experimental group) were transcribed from the videotapes using standard play and frame-by-frame techniques. Throughout the recruitment process, scouts employed six discrete behaviors to inform nestmates of the location and quality of a food site. Scouts laid incoming trails, waggled their heads, increased walking tempo, stroked nestmates with their antennae, advertised with a brief food display, and led groups of nestmates to the food site by laying outgoing trails. In turn, nestmates assessed the food sample with antennae, then responded to or resisted recruitment based on the quality of food advertised, their employment status and their level of hunger. In summary, recruitment was an emergent property based on competent supply and demand decisions made face-to-face inside the nest rather than on the trail or at the food site.Communicated by J. Heinze     

The migrating herdsman Dolichoderus (Diabolus) cuspidatus: an ant with a novel mode of life

Summary The Malayan ant Dolichoderus cuspidatus lives in obligatory symbiosis with the pseudococcid Malaicoccus formicarii and other species of the same genus. The assemblies, which may be encountered up to 25 m away from the nest, are constantly covered with a great number of worker ants who protect them and receive honeydew. In the event of heavy rain the workers from a dense protective cluster, clinging to each other on top of the mealybugs. Neither hunting behavior nor active search for protein sources was observed in D. cuspidatus, although dead insects were accepted as food. When not searching for new plants, the activity of the ants outside the colony is limited to visiting the mealybugs. During the night and parts of the day the ants stay in their nest. Ant colonies deprived of their mealybugs are not viable due to their dependence on the symbiosis and because of the competition of other ants. Antless M. formicarii are likewise not viable. The mealybugs are extremely polyphagous and feed on many different monocotylous and dicotylous angiosperms. They feed exclusively on the phloem sap of young plant parts which are rich in amino acids. Dolichoderus cuspidatus workers carry the mealybugs to such locations. During the picking up and carrying process both partners display typical behavioral patterns. The colonization of new feeding sites takes place in well organized mass processions. During the foundation or disintegration of large feeding complexes, provisional depots with waiting mealybugs and ants are set up. The pseudococcids are carried not only while shifting the feeding sites, but also whenever the colony leaves its former nesting site and especially when any kind of disturbance occurs. They are even carried about without any apparent external cause, which leads to the fact that, at all times of trail activity, on average more than 10% of all ants using the trails carry mealybugs. Mealybugs are also present within the nest, especially adult females which are viviparous and give birth to their offspring there. Censused colonies each consisted of over 10 000 workers, about 4000 larvae and pupae, more than 5000 mealybugs and one ergatoid queen. Male winged ants were observed in large numbers during the dry season (January–February) and during the rainy season (September–October). The colonies form typical clumplike bivouac nests consisting of clusters of workers clinging to each other, thereby covering the brood and the mealybugs. The nesting site is in no way altered by constructive measures and is mostly found close to the ground. The preferred nesting sites are clusters of leaves, and cavities in wood or soil, although a freely hanging bivouac between a few branches may be set up as well. As soon as the distance between the nest and the feeding site is too great the colony moves to the feeding site, whereby the brood and the mealybugs are carried along in a well organized manner. During such nest-moving the establishment of intermediate depots can be observed. A shift of nest sites can also be induced by disturbances or by a change in the microclimate in the vicinity of the nest. Colonies multiply by budding. The tropical rain forest continuously offers different sprouting plants, the utilization of which requires extreme mobility on the part of the consumer. The unique behavioral strategy of D. cuspidatus, to carry constantly their polyphagous mealybug partners to new feeding sites and to take the whole colony there has enabled this ant and its symbiont to occupy this rich food niche. Dolichoderus cuspidatus is the first true nomad found in ants.     

Modulation of individual behavior and collective decision-making during aggregation site selection by the ant<Emphasis Type="Italic"> Messor barbarus</Emphasis>

Insect societies are often confronted with choices among several options such as food sources of different richness or potential nest sites with different qualities. The mechanisms by which a colony as a whole evaluates these situations and takes the appropriate decision are of crucial importance for its survival. Here we studied how collective decisions arise from individual behaviors when a group of workers of the ant Messor barbarus is given a choice between two aggregation sites. Two hundred ants were introduced into an arena and given a choice between two tubes connected to the arena. The tubes had different physical properties: dry and transparent (termed as dry), humid and transparent (termed as humid), or dry and dark (termed as dark). After 30 min, most ants were found to be aggregated in a humid tube when paired with a dry tube, or in a dark tube when paired with a humid one. When two humid tubes were in competition, ants aggregate more in one of the sites. The choice of ants was consistent throughout experiments. An analysis of individual behaviors shows that the probability of an ant recruiting and the intensity of its trail-laying behavior strongly depend on the quality of the tubes. Our study suggests that the selection of an aggregation site does not require that individual ants directly compare sites, but rather relies on the synergy between amplification processes involving recruitment by chemical trails, and a modulation of the individual resting time in a site as a function of its population.Communicated by L. Sundström     

Blinkered teaching: tandem running by visually impaired ants

During tandem runs, one ant worker recruits another to an important resource. Here, we begin to investigate how dependent are tandem leaders and followers on visual cues by painting over their compound eyes to impair their vision. There are two ways in which Temnothorax albipennis might use vision during tandem running. First, the follower might track the movements of the leader by keeping it in sight. Our results suggest that the ants do not use vision in this way. For example, in all four classes of tandem run (those with either leader or follower, both, or neither of their participants with visual impairments) progress was most smooth at about 3 mm/s. This suggests that communication between leaders and followers during tandem runs is not based on vision and is purely tactile and pheromonal. Second, the leader and the follower might be using vision to navigate and our results support this possibility but also suggest that these ants have other methods of navigation. Ants with visual impairments were more likely to follow than to lead, but could occupy either role, even though they had many fully sighted nestmates. This might help to explain why the ants did not focus grooming on their most visually impaired nestmates. Wild-type tandem runs, with both participants fully sighted and presumably taking time to learn landmarks, were overall significantly slower, smoother, and a little less tortuous, than the other treatments. All four classes of tandem run significantly increased mean instantaneous speeds and mean absolute changes in instantaneous acceleration over their journeys. Moreover, tandems with sighted followers increased their speed with time more than the other treatments. In general, our findings suggest that eyesight is used for navigation during tandem running but that these ants also probably use other orientation systems during such recruitment and to learn how to get to new nest sites. Our results suggest that the ants’ methods of teaching and learning are very robust and flexible.     

Information transfer during recruitment in the ant<Emphasis Type="Italic"> Lasius niger</Emphasis> L. (Hymenoptera: Formicidae)

In this paper, we used the food-correlated search behavior observed in foraging ants returning to a previously rewarding site to study information transfer during recruitment in the ant Lasius niger. We hypothesized that, if information about the characteristics of the food is conveyed during recruitment, food-correlated search tactics should also be observed in recruited workers. Our results show that the characteristics of the trajectories of recruited workers are comparable to those of scout ants returning to a site or prior food find and depend more on the type (prey/sugar) than on the quality (sugar concentration) of the food discovered by the scouts. Independent of sugar concentration, workers recruited to a source of sugar search with a greater sinuosity than workers recruited to a prey. Experimental manipulation of the recruitment signals (chemical trail and contact between ants) shows that the trail pheromone laid down by recruiting ants does not play a role in the modification of trajectory sinuosity. This change appears to be most likely triggered by a direct perception of the residue of sugar smeared on the body of the recruiting workers coming back to the nest.Communicated by J. Heinze     

Better the nest site you know: decision-making during nest migrations by the Pharaoh’s ant

Animals frequently have to decide between alternative resources and in social insects these individual choices produce a colony-level decision. The choice of nest site is a particularly critical decision for a social insect colony to make, but the decision making process has still only been studied in a few species. In this study, we investigated nest selection by the Pharaoh’s ant, Monomorium pharaonis, a species renowned for its propensity to migrate and its use of multi-component trail pheromones to organise decision-making in other contexts. When presented with the choice of familiar and novel nests of equal quality in a Y set-up, colonies preferentially migrated towards the familiar nest, suggesting a form of colony-level ‘memory’ of potential nest sites. However, if the novel nest was superior to the familiar nest, then colonies began migrating initially to the familiar nest, but then redirected their migration to the superior quality novel nest. This may be an effective method of reducing colony exposure while searching for an optimum nest site. Branches that had previously led to a selected nest were attractive to ants in subsequent migrations, suggesting that trail pheromones mediate the decision making process. The adaptive, pheromone-based organisation of nest-site selection by Pharaoh’s ants matches their ephemeral environment and is likely to contribute to their success as a 'tramp' species.     

Consensus building during nest-site selection in honey bee swarms: the expiration of dissent

This study addresses a question that lies at the heart of understanding how the scouts in a honey bee swarm achieve unanimity in their dances, and so reach agreement in their choice of a future nest site: what causes the scouts that perform dances for the non-chosen sites to stop dancing for these sites? One possibility is that a scout stops dancing for a non-chosen site only after she follows a lively dance for another site, such as the site that is ultimately chosen. This hypothesis is contradicted by the finding that 23 out of 27 scouts (in 6 swarms) that danced initially for a non-chosen site stopped their dancing before they followed a dance for another site. Evidently, a scout that supports initially one of the non-chosen sites is likely to withdraw her support for this site even before she learns about another site. What causes her to do so? Close examination of the behavior of scouts revealed that they reduce the strength of their dancing (waggle runs/return to the swarm) for a given site over consecutive returns to the swarm. On average, the pattern of this reduction in dancing is strikingly linear, which suggests that it arises from an internal, neurophysiological process that automatically drives down a scout's motivation to dance for a site. Other results suggest that scouts from inferior sites start their dancing less strongly, and so cease their dancing more rapidly, than do scouts from superior sites. If so, then during the consensus-building process of the scouts, it is the support (the dancing) for inferior sites that is most likely to die out while it is the support for a superior site that is most likely to prevail.     

Choosing a home: how the scouts in a honey bee swarm perceive the completion of their group decision making

This study considers the mystery of how the scout bees in a honey bee swarm know when they have completed their group decision making regarding the swarm's new nest site. More specifically, we investigated how the scouts sense when it is appropriate for them to begin producing the worker piping signals that stimulate their swarm-mates to prepare for the flight to their new home. We tested two hypotheses: "consensus sensing," the scouts noting when all the bees performing waggle dances are advertising just one site; and "quorum sensing," the scouts noting when one site is being visited by a sufficiently large number of scouts. Our test involved monitoring four swarms as they discovered, recruited to, and chose between two nest boxes and their scouts started producing piping signals. We found that a consensus among the dancers was neither necessary nor sufficient for the start of worker piping, which indicates that the consensus sensing hypothesis is false. We also found that a buildup of 10–15 or more bees at one of the nest boxes was consistently associated with the start of worker piping, which indicates that the quorum sensing hypothesis may be true. In considering why the scout bees rely on reaching a quorum rather than a consensus as their cue of when to start preparing for liftoff, we suggest that quorum sensing may provide a better balance between accuracy and speed in decision making. In short, the bees appear to begin preparations for liftoff as soon as enough of the scout bees, but not all of them, have approved of one of the potential nest sites.

Foraging and spatiotemporal territories in the honey ant Myrmecocystus mimicus wheeler (Hymenoptera: Formicidae)

Summary The honey ant Myrmecocystus mimicus is a scavenger, forages extensively on termites, collects floral nectar, and tends homoptera. Individual foragers of M. mimicus usually disperse in all directions when leaving the nest, but there are also groups of foragers that tend to swarm out of the nest primarily in one direction. Such massive departues are usually at irregular intervals, which may last several hours. The results of field and laboratory experiments suggest that these swarms of foragers are organized by a group recruitment process, during which recruiting scout ants lay chemical orientation trails with hindgut contents and simultaneously stimulate nestmates with a motor display and secretions from the poison gland. Usually these columns travel considerable distances (4–48 m) away from the nest, frequently interfering with the foraging activity of conspecific neighboring colonies.To prevent a neighboring colony from access to temporal food sources or to defend spatiotemporal borders, opposing colonies engage in elaborate display tournaments. Although hundreds of ants are often involved during these tournaments almost no physical fights occur. Instead, individual ants confront each other in highly sterotyped aggressive displays, during which they walk on stilt legs while raising the gaster and head. Some of the ants even seem to inflate their gasters so that the tergites are raised and the whole gaster appears to be larger. In addition, ants involved in tournament activities are on average larger than foragers.The dynamics of the tournament interactions were observed in several colonies over several weeks-mapping each day the locations of the tournaments, the major directions of worker routes away from the nest, and recording the general foraging activities of the colonies. The results indicate that a kind of dominance order can occur among neighboring colonies. On the other hand, often no aggressive interactions among neighboring colonies can be observed, even though the colonies are actively foraging. In those cases the masses of foragers of each colony depart in one major direction that does not bring them into conflict with the masses of foragers of a neighboring colony. This stability, however, can be disturbed by offering a new rich food source to be exploited by two neighboring colonies. This invariably leads to tournament interactions.When a colony is considerably stronger than the other, i.e., with a much larger worker force, the tournaments end quickly and the weaker colony is raided. The foreign workers invade the nest, the queen of the resident colony is killed or dirven off, while the larvae, pupae, callow workers, and honey pot workers are carried or dragged to the nest of the raiders. From these and other observations we conclude that young M. mimicus queens are unlikely to succeed in founding a colony within approximately 3 m of a mature M. mimicus colony because they are discovered and killed, or driven off by workers of the resident colony. Within approximately 3–15 m queens are more likely to start colonies, but these incipient groups run a high risk of being raided and exterminated by the mature colony.Although populations of M. mimicus and M. depilis tend to replace each other, there are areas where both species overlap marginally. Foraging areas and foraging habitats of both species also overlap broadly, but we never observed tournament interactions between M. mimicus and M. depilis.The adaptive significance of the spatiotemporal territories in M. mimicus is discussed.     

Quorum sensing during nest-site selection by honeybee swarms

This study addresses a question about the nest-site selection process of honeybee swarms: how do the scout bees know when to initiate the preparation for their swarm’s move to their new home? We tested the quorum-sensing hypothesis: that the scouts do this by noting when one of the potential nest sites under consideration is being visited by a sufficiently large number of scouts. A falsifiable prediction of this hypothesis is that delaying the formation of a quorum of scout bees at a swarm’s chosen nest cavity, while leaving the rest of the decision-making process undisturbed, should delay the start of worker piping (the prepare-for-takeoff signal) and thus the takeoff of the swarm. In paired trials, we presented each of four swarms once with five nest boxes close to each other at a site and once with a single nest box. The multiple nest boxes caused the scouts visiting the site to be dispersed among five identical nest cavities rather than concentrated at one. We observed long delays in the start of piping and the start of takeoff in the five-nest-box trials relative to the one-nest-box trials. These results provide strong support for the quorum-sensing hypothesis.     

Repeated training does not improve the path integrator in desert ants

Desert ants, Cataglyphis fortis, return to their nest by means of path integration vectors. By using the reversal of these vectors, they approach previously visited feeding sites again. They adjust these vectors whenever outbound and inbound vector are set into conflict or when they make use of external cues. Here, we examine the influence of repeated training on the accuracy, precision, and straightness of outbound and inbound vectors. We trained desert ants to forage to and fro between their nest and a feeder and made sure that they relied exclusively on their path integrator. Neither the ants’ outbound nor their inbound runs, which, in general, are straighter than the outbound runs, become more accurate, precise, or straighter during repeated training. Hence, repeated training does not improve the path integrator in desert ants.     

Individual and collective decision-making during nest site selection by the ant Leptothorax albipennis

Social insect colonies possess remarkable abilities to select the best among several courses of action. In populous societies with highly efficient recruitment behaviour, decision-making is distributed across many individuals, each acting on limited local information with appropriate decision rules. To investigate the degree to which small societies with less efficient recruitment can also employ distributed decision-making, we studied nest site selection in Leptothorax albipennis. Colonies were found to make sophisticated choices, taking into account not only the intrinsic qualities of each site, but also its value relative to the available options. In choices between two sites, individual ants were able to visit both sites, compare them and choose the better one. However, most ants encountered only one site in the course of an emigration. These poorly informed ants also contributed to the colony's decision, because their probability of initiating recruitment to a site depended on its quality. This led to shorter latencies between discovery and recruitment to a superior site, and so created greater amplification via positive feedback of the population at the better site. In short, these small colonies make use of a distributed mechanism of information processing, but also take advantage of direct decision-making by well-informed individuals. The latter feature may in part stem from the limitations of their social structure, but may also reflect the stringent demand for unanimous decisions by house-hunting colonies of any size.     

What makes a honeybee scout?

A honeybee colony needs to divide its workforce so that each of the many tasks it performs has an appropriate number of workers assigned to it. This task allocation system needs to be flexible enough to allow the colony to quickly adapt to an ever-changing environment. In this study, we examined possible mechanisms by which a honeybee colony regulates the division of labor between scouts (foragers that search for new food sources without having been guided to them) and recruits (foragers that were guided via recruitment dances toward food sources). Specifically, we examined the roles that the availability of recruitment dances and worker genotype has in the colony-level regulation of the number of workers engaged in scouting. Our approach was threefold. We first developed a mathematical model to demonstrate that the decision to become a scout or a recruit could be regulated by whether a potential forager can find a recruitment dance within a certain time period. We then tested this model by investigating the effect of dance availability on the regulation of scouts in the field. Lastly, we investigated if the probability of being a scout has a genetic basis. Our field data supported the hypothesis that scouts are those foragers that have failed to locate a recruitment dance as predicted by our model, but we found no effect of genotype on the propensity of foragers to become scouts.     

Chemical trail communication in the amblyoponine species Mystrium rogeri Forel (Hymenoptera, Formicidae, Ponerinae)

Summary. Workers of the amblyoponine species Mystrium rogeri employ trail communication during recruitment to food sources and new nest sites. The trail pheromone originates from a hitherto unknown sternal gland located in the 7th abdominal sternite. The recruiting ant deposits the gland secretions by a special gaster-dragging behavior. The recruitment behavior can be complemented by a rapid vertical body shaking performed by some recruiting ants inside the nest. M. rogeri workers possess a large pygidial gland, the secretion of which elicits a repellent response in other ant species. Received 25 May 1998; accepted 15 June 1998.     

Orientation and recruitment behavior in the ponerine ant Pachycondyla tesserinoda (Emery): laying of individual-specific trails during tandem running

Summary Tandem leaders of Pachycondyla tesserinoda mark their way during nest moving. While scouting and foraging for food in an unknown area, chemical orientation is used as well. The origin of the trail substance could not be identified. Secretions of gastral exocrine glands did not induce trail following behavior. Nor do these secretions elicit tandem-following reactions; rather the latter is released by the general body surface odor. The trail substance and the substance used for marking the nest entrance are colony-specific. Moreover, individual tandem leaders recognize and show a preference for their own trails. This extraordinary effect is independent of the age of the trail. P. tesserinoda workers search individually for food and new nest sites. Targets which are important for the colony are directly shown to nestmates by tandem running. Due to this type of foraging and scouting individual-specific trails may be advantageous for this ant.     

Dominance and fertility in a functionally monogynous ant

Summary Colonies of some leptothoracine ants may contain several inseminated but sterile females in addition to a single, fertile queen (functional monogyny). We here report the first observations on the behavior of these supernumerary females in the nearctic ant Leptothorax sp.A, a species belonging to the L. muscorum complex.In four colonies, each with up to eight intermorphic females, ritualized or openly aggressive interactions between individuals were observed, similar to those among workers of some other leptothoracine ants. The responses of individual females during encounters with nestmates apparently reflect the existence of linear dominance hierarchies. In each colony, the highest ranking individual was fed and groomed significantly more often than other females, and was the only one to oviposit after hibernation and to become fully physogastric during the first weeks of spring. When these -females were removed from three colonies, several other females started to lay eggs. However, in each colony only the highest ranking individual remained fertile; the others either were pushed out of the nest and finally killed by the workers, or their ovaries degenerated again.Aggressive interactions among females may also play an important role in the foundation of new colonies either by inducing intermorphs to leave the maternal nest to found new colonies solitarily or by inducing colony fission. Offprint requests to: J. Heinze at his new address     

The evolution of worker–queen polymorphism in Cataglyphis ants: interplay between individual- and colony-level selections

In many ants, young queens disperse by flying away from their natal nest and found new colonies alone (independent colony founding, ICF). Alternatively, in some species, ICF was replaced by colony fission, in which young queens accompanied by workers found a new colony at walking distance from the mother nest. We compared the queen morphology of Cataglyphis floricola, which disperses by fission, with that of its most likely living ancestor, Cataglyphis emmae, which disperses by ICF. As in other species, the transition from ICF to fission is associated with queen miniaturization. Interestingly, C. floricola presents two types of small queens: brachypters (with short non-functional wings) and ergatoids (worker-like apterous queens). Ergatoids are, on average, 2.8 mg lighter and have half the number of ovarioles than brachypters, which limits the advantage for a colony to produce ergatoids instead of brachypters. Furthermore, more ergatoids are produced than brachypters, but their individual survival rate is lower. During colony fission, 96% of the cocoons containing brachypters but only 31% of those containing ergatoids are transferred to the daughter nests where, after emergence, they compete for becoming the next queen. The remaining queen cocoons, which stay in the mother queen's nest, are eliminated by workers upon emergence, probably to maintain monogyny. This waste of energy suggests that producing ergatoids instead of brachypters is unlikely to increase colony efficiency. We argue that the evolution of ergatoids could derive from a selfish larval strategy, developing into worker-like queens in spite of the colony interest.     

Ecology of<Emphasis Type="Italic"> Leptothorax</Emphasis> ants: impact of food,nest sites,and social parasites

In a long-term field manipulation, we demonstrate strong reactions of Leptothorax longispinosus ant colonies to food- and nest-site supplementation. Demographic and genetic responses varied over small geographic scales, and the two ecological factors interacted with the presence of the social parasite Protomognathus americanus. We conducted a 2×2 experiment in three blocks and found that the blocks, which were less than 100 m apart, reacted very differently to the treatments. Blocks differed in degree of polygyny, intranest relatedness, colony size, productivity, and sexual investment. Furthermore, these differences were associated with the presence of slave-making ants and the local availability of nest sites. Nest-site supplementation had a strong effect only in the site with the highest prevalence of social parasites, influencing there the density and investment patterns of colonies. L. longispinosus ants in the least parasitized area were strongly affected by both food- and nest-site supplementation. There, food supplementation led to a decrease in the number of queens per colony and consequently to an increase in intranest relatedness, while colonies in nest-site-supplemented areas invested fewer resources in males and produced a female-biased allocation ratio. By contrast, in a third block with a very low intracolonial relatedness, food supplementation induced an absolute and relative higher investment in males. We conclude that ecological factors influencing social organization in insect societies cannot be studied in isolation, because the interactions among factors produce far richer responses than any one variable.Communicated by L. Sundström