The Interplay Between Scent Trails and Group-Mass Recruitment Systems in Ants

Large ant colonies invariably use effective scent trails to guide copious ant numbers to food sources. The success of mass recruitment hinges on the involvement of many colony members to lay powerful trails. However, many ant colonies start off as single queens. How do these same colonies forage efficiently when small, thereby overcoming the hurdles to grow large? In this paper, we study the case of combined group and mass recruitment displayed by some ant species. Using mathematical models, we explore to what extent early group recruitment may aid deployment of scent trails, making such trails available at much smaller colony sizes. We show that a competition between group and mass recruitment may cause oscillatory behaviour mediated by scent trails. This results in a further reduction of colony size to establish trails successfully.     

Tandem Recruitment and Foraging in the Ponerine Ant <Emphasis Type="Italic">Pachycondyla harpax</Emphasis> (Fabricius)

Tandem running is a common recruitment strategy in ant species with small colony sizes. During a tandem run, an informed leader guides a usually naïve nestmate to a food source or a nest site. Some species perform tandem runs only during house hunting, suggesting that tandem running does not always improve foraging success in species known to use tandem running as a recruitment strategy, but more natural history information on tandem running under natural conditions is needed to better understand the adaptive significance of tandem recruitment in foraging. Studying wild colonies in Brazil, we for the first time describe tandem running in the ponerine ant Pachycondyla harpax (Fabricius). We asked if foragers perform tandem runs to carbohydrate- (honey) and protein-rich (cheese) food items. Furthermore, we tested whether the speed and success rate of tandem runs depend on the foraging distance. Foragers performed tandem runs to both carbohydrate food sources and protein-rich food items that exceed a certain size. The probability to perform a tandem run and the travelling speed increase with increasing foraging distances, which could help colonies monopolize more distant food sources in a competitive environment. Guiding a recruit to a food source is costly for leaders as ants are ~66% faster when travelling alone. If tandem runs break up (~23% of all tandem runs), followers do not usually discover the food source on their own but return to the nest. Our results show that tandem running to food sources is common in P. harpax, but that foragers modify their behaviour according to the type of food and its distance from the nest. Competition with other ants was intense and we discuss how tandem running in P. harpax might help colonies to build-up a critical number of ants at large food items that can then defend the food source against competitors.     

The Regulation of Ant Colony Foraging Activity without Spatial Information

Many dynamical networks, such as the ones that produce the collective behavior of social insects, operate without any central control, instead arising from local interactions among individuals. A well-studied example is the formation of recruitment trails in ant colonies, but many ant species do not use pheromone trails. We present a model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies. This species forages for scattered seeds that one ant can retrieve on its own, so there is no need for spatial information such as pheromone trails that lead ants to specific locations. Previous work shows that colony foraging activity, the rate at which ants go out to search individually for seeds, is regulated in response to current food availability throughout the colony's foraging area. Ants use the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers available to leave the nest on the next foraging trip. Here we present a feedback-based algorithm that captures the main features of data from field experiments in which the rate of returning foragers was manipulated. The algorithm draws on our finding that the distribution of intervals between successive ants returning to the nest is a Poisson process. We fitted the parameter that estimates the effect of each returning forager on the rate at which outgoing foragers leave the nest. We found that correlations between observed rates of returning foragers and simulated rates of outgoing foragers, using our model, were similar to those in the data. Our simple stochastic model shows how the regulation of ant colony foraging can operate without spatial information, describing a process at the level of individual ants that predicts the overall foraging activity of the colony.     

Balancing organization and flexibility in foraging dynamics

Proper pattern organization and reorganization are central problems facing many biological networks which thrive in fluctuating environments. However, in many cases the mechanisms that organize system activity oppose those that support behavioral flexibility. Thus, a balance between pattern organization and pattern flexibility is critically important for overall biological fitness. We study this balance in the foraging strategies of ant colonies exploiting food in dynamic environments. We present discrete time and space simulations of colony activity that uses a pheromone-based recruitment strategy biasing foraging towards a food source. After food relocation, the pheromone must evaporate sufficiently before foraging can shift colony attention to a new food source. The amount of food consumed within the dynamic environment depends non-monotonically on the pheromone evaporation time constant—with maximal consumption occurring at a time constant which balances trail formation and trail flexibility. A deterministic, ‘mean field’ model of pheromone and foragers on trails mimics our colony simulations. This reduced framework captures the essence of the flexibility-organization balance, and relates optimal pheromone evaporation to the timescale of the dynamic environment. We expect that the principles exposed in our study will generalize and motivate novel analysis across a broad range systems biology.     

Microbial Community Structure of Leaf-Cutter Ant Fungus Gardens and Refuse Dumps

Background

Leaf-cutter ants use fresh plant material to grow a mutualistic fungus that serves as the ants'' primary food source. Within fungus gardens, various plant compounds are metabolized and transformed into nutrients suitable for ant consumption. This symbiotic association produces a large amount of refuse consisting primarily of partly degraded plant material. A leaf-cutter ant colony is thus divided into two spatially and chemically distinct environments that together represent a plant biomass degradation gradient. Little is known about the microbial community structure in gardens and dumps or variation between lab and field colonies.

Methodology/Principal Findings

Using microbial membrane lipid analysis and a variety of community metrics, we assessed and compared the microbiota of fungus gardens and refuse dumps from both laboratory-maintained and field-collected colonies. We found that gardens contained a diverse and consistent community of microbes, dominated by Gram-negative bacteria, particularly γ-Proteobacteria and Bacteroidetes. These findings were consistent across lab and field gardens, as well as host ant taxa. In contrast, dumps were enriched for Gram-positive and anaerobic bacteria. Broad-scale clustering analyses revealed that community relatedness between samples reflected system component (gardens/dumps) rather than colony source (lab/field). At finer scales samples clustered according to colony source.

Conclusions/Significance

Here we report the first comparative analysis of the microbiota from leaf-cutter ant colonies. Our work reveals the presence of two distinct communities: one in the fungus garden and the other in the refuse dump. Though we find some effect of colony source on community structure, our data indicate the presence of consistently associated microbes within gardens and dumps. Substrate composition and system component appear to be the most important factor in structuring the microbial communities. These results thus suggest that resident communities are shaped by the plant degradation gradient created by ant behavior, specifically their fungiculture and waste management.     

Information flow,opinion polling and collective intelligence in house-hunting social insects

The sharing and collective processing of information by certain insect societies is one of the reasons that they warrant the superlative epithet ''super-organisms'' (Franks 1989, Am. Sci. 77, 138-145). We describe a detailed experimental and mathematical analysis of information exchange and decision-making in, arguably, the most difficult collective choices that social insects face: namely, house hunting by complete societies. The key issue is how can a complete colony select the single best nest-site among several alternatives? Individual scouts respond to the diverse information they have personally obtained about the quality of a potential nest-site by producing a recruitment signal. The colony then deliberates over (i.e. integrates) different incoming recruitment signals associated with different potential nest-sites to achieve a well-informed collective decision. We compare this process in honeybees and in the ant Leptothorax albipennis. Notwithstanding many differences - for example, honeybee colonies have 100 times more individuals than L. albipennis colonies - there are certain similarities in the fundamental algorithms these societies appear to employ when they are house hunting. Scout honeybees use the full power of the waggle dance to inform their nest-mates about the distance and direction of a potential nest-site (and they indicate the quality of a nest-site indirectly through the vigour of their dance), and yet individual bees perhaps only rarely make direct comparisons of such sites. By contrast, scouts from L. albipennis colonies often compare nest-sites, but they cannot directly inform one another of their estimation of the quality of a potential site. Instead, they discriminate between sites by initiating recruitment sooner to better ones. Nevertheless, both species do make use of forms of opinion polling. For example, scout bees that have formerly danced for a certain site cease such advertising and monitor the dances of others at random. That is, they act without prejudice. They neither favour nor disdain dancers that advocate the site they had formerly advertised or the alternatives. Thus, in general the bees are less well informed than they would be if they systematically monitored dances for alternative sites rather than spending their time reprocessing information they already have. However, as a result of their lack of prejudice, less time overall will be wasted in endless debate among stubborn and potentially biased bees. Among the ants, the opinions of nest-mates are also pooled effectively when scouts use a threshold population of their nest-mates present in a new nest-site as a cue to switch to more rapid recruitment. Furthermore, the ants'' reluctance to begin recruiting to poor nest-sites means that more time is available for the discovery and direct comparison of alternatives. Likewise, the retirement of honeybee scouts from dancing for a given site allows more time for other scouts to find potentially better sites. Thus, both the ants and the bees have time-lags built into their decision-making systems that should facilitate a compromise between thorough surveys for good nest-sites and relatively rapid decisions. We have also been able to show that classical mathematical models can illuminate the processes by which colonies are able to achieve decisions that are relatively swift and very well informed.     

The Trail Less Traveled: Individual Decision-Making and Its Effect on Group Behavior

Social insect colonies are complex systems in which the interactions of many individuals lead to colony-level collective behaviors such as foraging. However, the emergent properties of collective behaviors may not necessarily be adaptive. Here, we examine symmetry breaking, an emergent pattern exhibited by some social insects that can lead colonies to focus their foraging effort on only one of several available food patches. Symmetry breaking has been reported to occur in several ant species. However, it is not clear whether it arises as an unavoidable epiphenomenon of pheromone recruitment, or whether it is an adaptive behavior that can be controlled through modification of the individual behavior of workers. In this paper, we used a simulation model to test how symmetry breaking is affected by the degree of non-linearity of recruitment, the specific mechanism used by individuals to choose between patches, patch size, and forager number. The model shows that foraging intensity on different trails becomes increasingly asymmetric as the recruitment response of individuals varies from linear to highly non-linear, supporting the predictions of previous work. Surprisingly, we also found that the direction of the relationship between forager number (i.e., colony size) and asymmetry varied depending on the specific details of the decision rule used by individuals. Limiting the size of the resource produced a damping effect on asymmetry, but only at high forager numbers. Variation in the rule used by individual ants to choose trails is a likely mechanism that could cause variation among the foraging behaviors of species, and is a behavior upon which selection could act.     

Trail Pheromone of the Argentine Ant,Linepithema humile (Mayr) (Hymenoptera: Formicidae)

The Argentine ant (Linepithema humile) is recognized as one of the world''s most damaging invasive species. One reason for the ecological dominance of introduced Argentine ant populations is their ability to dominate food and habitat resources through the rapid mobilization and recruitment of thousands of workers. More than 30 years ago, studies showed that (Z)-9-hexadecenal strongly attracted Argentine ant workers in a multi-choice olfactometer, suggesting that (Z)-9-hexadecenal might be the trail pheromone, or a component of a trail pheromone mixture. Since then, numerous studies have considered (Z)-9-hexadecenal as the key component of the Argentine ant trails. Here, we report the first chemical analyses of the trails laid by living Argentine ants and find that (Z)-9-hexadecenal is not present in a detectible quantity. Instead, two iridoids, dolichodial and iridomyrmecin, appear to be the primary chemical constituents of the trails. Laboratory choice tests confirmed that Argentine ants were attracted to artificial trails comprised of these two chemicals significantly more often than control trails. Although (Z)-9-hexadecenal was not detected in natural trails, supplementation of artificial dolichodial+iridomyrmecin trails with an extremely low concentraion of (Z)-9-hexadecenal did increase the efficacy of the trail-following behavior. In stark contrast with previous dogma, our study suggests that dolichodial and iridomyrmecin are major components of the Argentine ant trail pheromone. (Z)-9-hexadecenal may act in an additive manner with these iridoids, but it does not occur in detectable quantities in Argentine ant recruitment trails.     

Nest connectivity and colony structure in unicolonial Argentine ants

Unicolonial ant colonies occupy many nests and individuals rarely show aggression across large geographic distances. These traits make it difficult to detect colony structure. Here we identify colony structure at scales of hundreds of square-meters, within an invasive population of unicolonial Argentine ants. In experiments using labeled food, and in a 3-year census of nests and trails, we found that food was shared and nests were linked by trails at distances up to 50 meters. Food was not distributed to all nearby Argentine ant nests, showing that ants tend to share resources within a spatially bounded group of nests. The spatial extent of food sharing increased from winter to summer. Across different habitats and nest densities, nests were consistently aggregated at spatial scales of 3- 4 meters in radius. This suggests that new nests bud from old nests at short distances regardless of local conditions. We suggest that a ‘colony’ of Argentine ants could be defined as a group of nests among which ants travel and share food. In our study population, colonies occupy up to 650 m² and contain as many as 5 million ants. In combination with previous work showing that there is genetic differentiation among nests at similar spatial scales, the results suggest that Argentine ant populations do not function ecologically as single, large supercolonies, but instead as mosaics of smaller, distinct colonies consisting of groups of interacting nests. Received 6 June 2008; revised 30 June 2008; accepted 2 July 2008.     

Nest architecture shapes the collective behaviour of harvester ants

Structures influence how individuals interact and, therefore, shape the collective behaviours that emerge from these interactions. Here I show that the structure of a nest influences the collective behaviour of harvester ant colonies. Using network analysis, I quantify nest architecture and find that as chamber connectivity and redundancy of connections among chambers increase, so does a colony''s speed of recruitment to food. Interestingly, the volume of the chambers did not influence speed of recruitment, suggesting that the spatial organization of a nest has a greater impact on collective behaviour than the number of workers it can hold. Thus, by changing spatial constraints on social interactions organisms can modify their behaviour and impact their fitness.     

Predatory behavior of a seed-eating ant:Brachyponera senaarensis

The great flexibility of the feeding strategies exhibited by the ponerine ant Brachyponera senaarensis (Mayr) allows it to exploit either seeds or animal prey items as food resources. Predation is generally limited to small prey and is very similar to scavenging behavior. In laboratory conditions, the predatory behavior of B. senaarensis is not different in structure from that known in other carnivorous ants species. The workers forage individually and return to the nest using a series of cues involving light, a chemical graduated marking system near the nest entrance, and memory. During nest-moving, recruitment by tandem running was observed. However, in colonies where the food supply is regular, workers that discover food do not recruit nestmates, but make repeated trips between the nest and the food source. On the contrary, in starved colonies, the introduction of prey may produce a massive exit of foragers, corresponding to a primitive form of mass recruitment similar to that observed in some other ant species.     

The ecology and feeding habits of the arboreal trap-jawed ant Daceton armigerum

Here we show that Daceton armigerum, an arboreal myrmicine ant whose workers are equipped with hypertrophied trap-jaw mandibles, is characterized by a set of unexpected biological traits including colony size, aggressiveness, trophobiosis and hunting behavior. The size of one colony has been evaluated at ca. 952,000 individuals. Intra- and interspecific aggressiveness were tested and an equiprobable null model used to show how D. armigerum colonies react vis-à-vis other arboreal ant species with large colonies; it happens that D. armigerum can share trees with certain of these species. As they hunt by sight, workers occupy their hunting areas only during the daytime, but stay on chemical trails between nests at night so that the center of their home range is occupied 24 hours a day. Workers tend different Hemiptera taxa (i.e., Coccidae, Pseudococcidae, Membracidae and Aethalionidae). Through group-hunting, short-range recruitment and spread-eagling prey, workers can capture a wide range of prey (up to 94.12 times the mean weight of foraging workers).     

Seasonal spatial dynamics and causes of nest movement in colonies of the invasive Argentine ant (Linepithema humile)

Abstract.  1. Colony organisation and movement behaviour of the Argentine ant ( Linepithema humile ) was studied over 3 years in field populations in California and in captive colonies in the laboratory. This invasive species is highly polydomous and unicolonial; colonies consist of expansive and fluid networks of nests and trails. The spatial and temporal organisation of colonies may contribute to ecological dominance.
2. Argentine ant nests and inter-nest trails shift in size, abundance, and location, so that colony networks are spatially contracted in the winter and expanded spring to autumn. Colonies occupy permanent sites; ants migrated to and from the same winter nest locations year after year, and occupied 30% of the same nests repeatedly during seasonal migrations.
3. Nests were moved on average 2–3 m. Forty-two per cent were occupied less than 1 month, 4% the entire study, and the other 54% lasted 3.9 ± 2.3 months (mean ± SD).
4. Nests were located within 2–4 m of woody plants, in warm sites in the winter and cool sites in the summer. Both humidity and food availability influenced nest-site choice in laboratory colonies. However, when faced with a trade-off between factors, the ants chose humid nest boxes over nest boxes near food, and ants moved nests only in response to changes in humidity and not distance to food.
5. The results indicate that L. humile colonies are seasonally polydomous, and that nest movements are driven by changes in microclimate. Colony organisation maintains high local density and increases food supply, which may improve the competitive ability of L. humile colonies and reduce opportunities for species coexistence.     

Negative Feedback Enables Fast and Flexible Collective Decision-Making in Ants

Positive feedback plays a major role in the emergence of many collective animal behaviours. In many ants pheromone trails recruit and direct nestmate foragers to food sources. The strong positive feedback caused by trail pheromones allows fast collective responses but can compromise flexibility. Previous laboratory experiments have shown that when the environment changes, colonies are often unable to reallocate their foragers to a more rewarding food source. Here we show both experimentally, using colonies of Lasius niger, and with an agent-based simulation model, that negative feedback caused by crowding at feeding sites allows ant colonies to maintain foraging flexibility even with strong recruitment to food sources. In a constant environment, negative feedback prevents the frequently found bias towards one feeder (symmetry breaking) and leads to equal distribution of foragers. In a changing environment, negative feedback allows a colony to quickly reallocate the majority of its foragers to a superior food patch that becomes available when foraging at an inferior patch is already well underway. The model confirms these experimental findings and shows that the ability of colonies to switch to a superior food source does not require the decay of trail pheromones. Our results help to resolve inconsistencies between collective foraging patterns seen in laboratory studies and observations in the wild, and show that the simultaneous action of negative and positive feedback is important for efficient foraging in mass-recruiting insect colonies.     

Noise improves collective decision-making by ants in dynamic environments

Recruitment via pheromone trails by ants is arguably one of the best-studied examples of self-organization in animal societies. Yet it is still unclear if and how trail recruitment allows a colony to adapt to changes in its foraging environment. We study foraging decisions by colonies of the ant Pheidole megacephala under dynamic conditions. Our experiments show that P. megacephala, unlike many other mass recruiting species, can make a collective decision for the better of two food sources even when the environment changes dynamically. We developed a stochastic differential equation model that explains our data qualitatively and quantitatively. Analysing this model reveals that both deterministic and stochastic effects (noise) work together to allow colonies to efficiently track changes in the environment. Our study thus suggests that a certain level of noise is not a disturbance in self-organized decision-making but rather serves an important functional role.     

Dispersed central-place foraging in the polydomous odorous house ant, Tapinoma sessile as revealed by a protein marker

The odorous house ant, Tapinoma sessile, is a native ant species common throughout North America. In urban areas, this ant is classified a pest species and exhibits several attributes characteristic of invasive “tramp” ants (sensu Passera, 1994). These include: extreme polygyny, colony reproduction by budding, reduced internest aggression, generalist diet, and polydomy. Here we explore the organization of foraging and the pathways of food distribution in polydomous colonies of T. sessile in the laboratory and field using a novel marking technique (rabbit IgG protein) and enzyme linked immunosorbent assay (ELISA). Laboratory assays revealed patterns of food allocation from foragers to other castes and developmental stages. Foragers distributed the IgG- labelled sucrose to the majority of workers within 24 h, and workers retained significantly more sucrose than either queens or larvae. Approximately 50% of queens tested positive for the IgG marker and some queens received significantly more sucrose than others, indicating a possible reproductive dominance hierarchy. Larvae received little sucrose demonstrating their minor reliance on carbohydrates. The results of field experiments showed that odorous house ants are dispersed central-place foragers whereby ants from individual nests exhibit high foraging site fidelity, travel along well-established trails, and forage on a local scale. Dispersed central-place foraging most likely allows the odorous house ant to more efficiently secure both clumped and dispersed food sources and possibly increases its competitive ability. As a result, colonies become numerically large and ecologically dominant. The results of our study contribute to our understanding of the social behavior and colony organization in T. sessile. In addition, they provide a framework for designing more effective ant control programs based on liquid baits. Received 13 December 2005; revised 28 February 2006; accepted 3 March 2006.     

The Role of Non-Foraging Nests in Polydomous Wood Ant Colonies

A colony of red wood ants can inhabit more than one spatially separated nest, in a strategy called polydomy. Some nests within these polydomous colonies have no foraging trails to aphid colonies in the canopy. In this study we identify and investigate the possible roles of non-foraging nests in polydomous colonies of the wood ant Formica lugubris. To investigate the role of non-foraging nests we: (i) monitored colonies for three years; (ii) observed the resources being transported between non-foraging nests and the rest of the colony; (iii) measured the amount of extra-nest activity around non-foraging and foraging nests. We used these datasets to investigate the extent to which non-foraging nests within polydomous colonies are acting as: part of the colony expansion process; hunting and scavenging specialists; brood-development specialists; seasonal foragers; or a selfish strategy exploiting the foraging effort of the rest of the colony. We found that, rather than having a specialised role, non-foraging nests are part of the process of colony expansion. Polydomous colonies expand by founding new nests in the area surrounding the existing nests. Nests founded near food begin foraging and become part of the colony; other nests are not founded near food sources and do not initially forage. Some of these non-foraging nests eventually begin foraging; others do not and are abandoned. This is a method of colony growth not available to colonies inhabiting a single nest, and may be an important advantage of the polydomous nesting strategy, allowing the colony to expand into profitable areas.     

More food,less habitat: how necromass and leaf litter decomposition combine to regulate a litter ant community

1. In brown food webs of the forest floor, necromass (e.g. insect carcasses and frass) falling from the canopy feeds both microbes and ants, with the former decomposing the homes of the latter. In a tropical litter ant community, we added necromass to 1 m² plots, testing if it added as a net food (increasing ant colony growth and recruitment) or destroyer of habitat (by decomposing leaf litter). 2. Maximum, but not mean, colony growth rates were higher on +food plots. However, neither average colony size, nor density was higher on +food plots. In contrast, +food plots saw diminished availability of leaf litter and higher microbial decomposition of cellulose, a main component of the organic substrate that comprises litter habitat. 3. Furthermore, necromass acted as a limiting resource to the ant community only when nest sites were supplemented on +food plots in a second experiment. Many of these +food +nest plots were colonised by the weedy species Wasmannia auropunctata. 4. Combined, these results support the more food–less habitat hypothesis and highlight the importance of embedding studies of litter ant ecology within broader decomposer food web dynamics.     

The influence of forager number and colony size on food distribution in the odorous house ant, Tapinoma sessile

Stomodeal trophallaxis plays a major role in ant colony nutrition and communication. While the rate of food distribution at the individual level (worker to worker) is rapid, factors affecting the rate of food distribution at the colony level remain poorly understood. We used the odorous house ant, Tapinoma sessile (Say), as a model species to investigate the factors affecting the rate of spread of liquid carbohydrate food throughout a colony. To track the movement of the food we used protein marking and double antibody sandwich enzyme-linked immunosorbent assay, DAS-ELISA. Increasing colony size while keeping the number of donor workers constant significantly decreased the number of individuals testing positive for the marker. After 8 h of trophallactic interactions with ten donors, 92 ± 5% of recipient workers tested positive in a colony of 125 and 38 ± 5% tested positive in a colony of 1,000. Interestingly, as colony size increased and the percentage of workers testing positive decreased, the proportion of workers actually receiving food increased. Food originating from a single donor fed approximately 12 individuals in colonies comprised of 125 recipients and approximately 38 individuals in colonies comprised of 1,000 recipients. Thus, the per capita consumption of food decreased as colony size increased, most likely because the amount of food reaching the colony was limited. Increasing the number of donors while keeping colony size constant significantly increased the number of recipient ants testing positive for the marker. As the number of donor workers doubled, the percentage of recipients testing positive more than doubled suggesting that the number of individuals receiving food increases with increasing colony size, while the per capita amount of food decreases. When food was available ad libitum and in close proximity to the nest, numerous workers fed directly at the food source. This dramatically increased the rate and the extent of food distribution to both the workers and the queens and colony size had no significant effect on the spread of the marker in the workers or the queens. The rate and the extent of food distribution at the colony level may depend on a number of factors including the number of successful foragers, the size and density of the recipient colony, and the recipient caste.