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1.  The Regulation of Ant Colony Foraging Activity without Spatial Information 
PLoS Computational Biology  2012;8(8):e1002670.
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.
Author Summary
Social insect colonies operate without any central control. Their collective behavior arises from local interactions among individuals. Here we present a simple stochastic model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies, which forage for scattered seeds that one ant can retrieve on its own, so there is no need for pheromone trails to specific locations. Previous work shows that colony foraging activity is regulated in response to current food availability, using the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers. Our feedback-based algorithm estimates the effect of each returning forager on the rate at which foragers leave the nest. The 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.
doi:10.1371/journal.pcbi.1002670
PMCID: PMC3426560  PMID: 22927811
2.  Harvester ants use interactions to regulate forager activation and availability 
Animal behaviour  2013;86(1):197-207.
Social groups balance flexibility and robustness in their collective response to environmental changes using feedback between behavioural processes that operate at different timescales. Here we examine how behavioural processes operating at two timescales regulate the foraging activity of colonies of the harvester ant, Pogonomyrmex barbatus, allowing them to balance their response to food availability and predation. Previous work showed that the rate at which foragers return to the nest with food influences the rate at which foragers leave the nest. To investigate how interactions inside the nest link the rates of returning and outgoing foragers, we observed outgoing foragers inside the nest in field colonies using a novel observation method. We found that the interaction rate experienced by outgoing foragers inside the nest corresponded to forager return rate, and that the interactions of outgoing foragers were spatially clustered. Activation of a forager occurred on the timescale of seconds: a forager left the nest 3–8 s after a substantial increase in interactions with returning foragers. The availability of outgoing foragers to become activated was adjusted on the timescale of minutes: when forager return was interrupted for more than 4–5 min, available foragers waiting near the nest entrance went deeper into the nest. Thus, forager activation and forager availability both increased with the rate at which foragers returned to the nest. This process was checked by negative feedback between forager activation and forager availability. Regulation of foraging activation on the timescale of seconds provides flexibility in response to fluctuations in food abundance, whereas regulation of forager availability on the timescale of minutes provides robustness in response to sustained disturbance such as predation.
doi:10.1016/j.anbehav.2013.05.012
PMCID: PMC3767282  PMID: 24031094
collective behaviour; complex system; flexibility; foraging; interaction rate; Pogonomyrmex barbatus; regulation; robustness; temporal dynamics; timescale
3.  Interactions with Combined Chemical Cues Inform Harvester Ant Foragers' Decisions to Leave the Nest in Search of Food 
PLoS ONE  2013;8(1):e52219.
Social insect colonies operate without central control or any global assessment of what needs to be done by workers. Colony organization arises from the responses of individuals to local cues. Red harvester ants (Pogonomyrmex barbatus) regulate foraging using interactions between returning and outgoing foragers. The rate at which foragers return with seeds, a measure of food availability, sets the rate at which outgoing foragers leave the nest on foraging trips. We used mimics to test whether outgoing foragers inside the nest respond to the odor of food, oleic acid, the odor of the forager itself, cuticular hydrocarbons, or a combination of both with increased foraging activity. We compared foraging activity, the rate at which foragers passed a line on a trail, before and after the addition of mimics. The combination of both odors, those of food and of foragers, is required to stimulate foraging. The addition of blank mimics, mimics coated with food odor alone, or mimics coated with forager odor alone did not increase foraging activity. We compared the rates at which foragers inside the nest interacted with other ants, blank mimics, and mimics coated with a combination of food and forager odor. Foragers inside the nest interacted more with mimics coated with combined forager/seed odors than with blank mimics, and these interactions had the same effect as those with other foragers. Outgoing foragers inside the nest entrance are stimulated to leave the nest in search of food by interacting with foragers returning with seeds. By using the combined odors of forager cuticular hydrocarbons and of seeds, the colony captures precise information, on the timescale of seconds, about the current availability of food.
doi:10.1371/journal.pone.0052219
PMCID: PMC3540075  PMID: 23308106
4.  Harvester Ant Colony Variation in Foraging Activity and Response to Humidity 
PLoS ONE  2013;8(5):e63363.
Collective behavior is produced by interactions among individuals. Differences among groups in individual response to interactions can lead to ecologically important variation among groups in collective behavior. Here we examine variation among colonies in the foraging behavior of the harvester ant, Pogonomyrmex barbatus. Previous work shows how colonies regulate foraging in response to food availability and desiccation costs: the rate at which outgoing foragers leave the nest depends on the rate at which foragers return with food. To examine how colonies vary in response to humidity and in foraging rate, we performed field experiments that manipulated forager return rate in 94 trials with 17 colonies over 3 years. We found that the effect of returning foragers on the rate of outgoing foragers increases with humidity. There are consistent differences among colonies in foraging activity that persist from year to year.
doi:10.1371/journal.pone.0063363
PMCID: PMC3662670  PMID: 23717415
5.  Differential regulation of the foraging gene associated with task behaviors in harvester ants 
BMC Ecology  2011;11:19.
Background
The division of labor in social insect colonies involves transitions by workers from one task to another and is critical to the organization and ecological success of colonies. The differential regulation of genetic pathways is likely to be a key mechanism involved in plasticity of social insect task behavior. One of the few pathways implicated in social organization involves the cGMP-activated protein kinase gene, foraging, a gene associated with foraging behavior in social insect species. The association of the foraging gene with behavior is conserved across diverse species, but the observed expression patterns and proposed functions of this gene vary across taxa. We compared the protein sequence of foraging across social insects and explored whether the differential regulation of this gene is associated with task behaviors in the harvester ant, Pogonomyrmex occidentalis.
Results
Phylogenetic analysis of the coding region of the foraging gene reveals considerable conservation in protein sequence across insects, particularly among hymenopteran species. The absence of amino acid variation in key active and binding sites suggests that differences in behaviors associated with this gene among species may be the result of changes in gene expression rather than gene divergence. Using real time qPCR analyses with a harvester ant ortholog to foraging (Pofor), we found that the brains of harvester ant foragers have a daily fluctuation in expression of foraging with mRNA levels peaking at midday. In contrast, young workers inside the nest have low levels of Pofor mRNA with no evidence of daily fluctuations in expression. As a result, the association of foraging expression with task behavior within a species changes depending on the time of day the individuals are sampled.
Conclusions
The amino acid protein sequence of foraging is highly conserved across social insects. Differences in foraging behaviors associated with this gene among social insect species are likely due to differences in gene regulation rather than evolutionary changes in the encoded protein. The task-specific expression patterns of foraging are consistent with the task-specific circadian rhythms observed in harvester ants. Whether the molecular clock plays a role in regulating foraging gene expression (or vice versa) remains to be determined. Our results represent the first time series analysis of foraging gene expression and underscore the importance of assaying time-related expression differences in behavioral studies. Understanding how this gene is regulated within species is critical to explaining the mechanism by which foraging influences behavior.
doi:10.1186/1472-6785-11-19
PMCID: PMC3180247  PMID: 21831307
6.  Information Needs at the Beginning of Foraging: Grass-Cutting Ants Trade Off Load Size for a Faster Return to the Nest 
PLoS ONE  2011;6(3):e17667.
Background
Acquisition of information about food sources is essential for animals that forage collectively like social insects. Foragers deliver two commodities to the nest, food and information, and they may favor the delivery of one at the expenses of the other. We predict that information needs should be particularly high at the beginning of foraging: the decision to return faster to the nest will motivate a grass-cutting ant worker to reduce its loading time, and so to leave the source with a partial load.
Principal Findings
Field results showed that at the initial foraging phase, most grass-cutting ant foragers (Acromyrmex heyeri) returned unladen to the nest, and experienced head-on encounters with outgoing workers. Ant encounters were not simply collisions in a probabilistic sense: outgoing workers contacted in average 70% of the returning foragers at the initial foraging phase, and only 20% at the established phase. At the initial foraging phase, workers cut fragments that were shorter, narrower, lighter and tenderer than those harvested at the established one. Foragers walked at the initial phase significantly faster than expected for the observed temperatures, yet not at the established phase. Moreover, when controlling for differences in the fragment-size carried, workers still walked faster at the initial phase. Despite the higher speed, their individual transport rate of vegetable tissue was lower than that of similarly-sized workers foraging later at the same patch.
Conclusions/Significance
At the initial foraging phase, workers compromised their individual transport rates of material in order to return faster to the colony. We suggest that the observed flexible cutting rules and the selection of partial loads at the beginning of foraging are driven by the need of information transfer, crucial for the establishment and maintenance of a foraging process to monopolize a discovered resource.
doi:10.1371/journal.pone.0017667
PMCID: PMC3052370  PMID: 21408014
7.  The Organization of Foraging in the Fire Ant, Solenopsis invicta  
Although natural selection in ants acts most strongly at the colony, or superorganismal level, foraging patterns have rarely been studied at that level, focusing instead on the behavior of individual foragers or groups of foragers. The experiments and observations in this paper reveal in broad strokes how colonies of the fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), allocate their available labor to foraging, how they disperse that force within their territory, and how this force changes with colony size, season and worker age. Territory area is positively related to colony size and the number of foragers, more so during the spring than fall. Changes of colony size and territory area are driven by seasonal variation of sexual and worker production, which in turn drive seasonal variation of worker age-distribution. During spring sexual production, colonies shrink because worker production falls below replacement. This loss is proportional to colony size, causing forager density in the spring to be negatively related to colony and territory size. In the fall, colonies emphasize worker production, bringing colony size back up. However, because smaller colonies curtailed spring worker production less than larger ones, their fall forager populations are proportionally greater, causing them to gain territory at the expense of large colonies. Much variation of territory area remains unexplained and can probably be attributed to pressure from neighboring colonies. Boundaries between territories are characterized by “no ants' zones” mostly devoid of fire ants. The forager population can be divided into a younger group of recruitable workers that wait for scouts to activate them to help retrieve large food finds. About one-third of the recruits wait near openings in the foraging tunnels that underlie the entire territory, while two-thirds wait in the nest. Recruitment to food is initially very rapid and local from the foraging tunnels, while sustained recruitment gradually involves the recruits waiting in the nest. As recruits age, they become scouts searching for food on the surface, and die about two weeks later. Foraging tunnels decrease in cross-sectional area with distance from the nest, in keeping with the gradual bleeding off of workers to the surface with distance. Foragers lack route-faithfulness, and having been marked and released at one point within the territory, they can be recaptured at any other point a day later. The size of the territory actually occupied may be limited during dry weather, resulting in very large no-ants' zones.
doi:10.1673/031.011.0126
PMCID: PMC3391925  PMID: 21529150
colony census; colony growth; division of labor; forager density; foraging tunnels; labor allocation; ortstreue; route faithfulness; seasonality; superorganism; territory; trail recruitment; worker age
8.  The Dynamics of Foraging Trails in the Tropical Arboreal Ant Cephalotes goniodontus 
PLoS ONE  2012;7(11):e50472.
The foraging behavior of the arboreal turtle ant, Cephalotes goniodontus, was studied in the tropical dry forest of western Mexico. The ants collected mostly plant-derived food, including nectar and fluids collected from the edges of wounds on leaves, as well as caterpillar frass and lichen. Foraging trails are on small pieces of ephemeral vegetation, and persist in exactly the same place for 4–8 days, indicating that food sources may be used until they are depleted. The species is polydomous, occupying many nests which are abandoned cavities or ends of broken branches in dead wood. Foraging trails extend from trees with nests to trees with food sources. Observations of marked individuals show that each trail is travelled by a distinct group of foragers. This makes the entire foraging circuit more resilient if a path becomes impassable, since foraging in one trail can continue while a different group of ants forms a new trail. The colony’s trails move around the forest from month to month; from one year to the next, only one colony out of five was found in the same location. There is continual searching in the vicinity of trails: ants recruited to bait within 3 bifurcations of a main foraging trail within 4 hours. When bait was offered on one trail, to which ants recruited, foraging activity increased on a different trail, with no bait, connected to the same nest. This suggests that the allocation of foragers to different trails is regulated by interactions at the nest.
doi:10.1371/journal.pone.0050472
PMCID: PMC3509047  PMID: 23209749
9.  Differences in Forage-Acquisition and Fungal Enzyme Activity Contribute to Niche Segregation in Panamanian Leaf-Cutting Ants 
PLoS ONE  2014;9(4):e94284.
The genera Atta and Acromyrmex are often grouped as leaf-cutting ants for pest management assessments and ecological surveys, although their mature colony sizes and foraging niches may differ substantially. Few studies have addressed such interspecific differences at the same site, which prompted us to conduct a comparative study across six sympatric leaf-cutting ant species in Central Panama. We show that foraging rates during the transition between dry and wet season differ about 60 fold between genera, but are relatively constant across species within genera. These differences appear to match overall differences in colony size, especially when Atta workers that return to their nests without leaves are assumed to carry liquid food. We confirm that Panamanian Atta specialize primarily on tree-leaves whereas Acromyrmex focus on collecting flowers and herbal leaves and that species within genera are similar in these overall foraging strategies. Species within genera tended to be spaced out over the three habitat categories that we distinguished (forest, forest edge, open grassland), but each of these habitats normally had only a single predominant Atta and Acromyrmex species. We measured activities of twelve fungus garden decomposition enzymes, belonging to the amylases, cellulases, hemicellulases, pectinases and proteinases, and show that average enzyme activity per unit of fungal mass in Atta gardens is lower than in Acromyrmex gardens. Expression profiles of fungal enzymes in Atta also appeared to be more specialized than in Acromyrmex, possibly reflecting variation in forage material. Our results suggest that species- and genus-level identities of leaf-cutting ants and habitat-specific foraging profiles may give predictable differences in the expression of fungal genes coding for decomposition enzymes.
doi:10.1371/journal.pone.0094284
PMCID: PMC3981799  PMID: 24718261
10.  Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant Pogonomyrmex barbatus 
PLoS Genetics  2013;9(8):e1003730.
The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker division of labor. Support for this hypothesis in honeybees is provided by studies demonstrating that the reproductive potential of workers, assessed by the levels of vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honeybees that have a single Vg ortholog and potentially fertile nurses, the genome of the harvester ant Pogonomyrmex barbatus harbors two Vg genes (Pb_Vg1 and Pb_Vg2) and nurses produce infertile trophic eggs. P. barbatus, thus, provides a unique model to investigate whether Vg duplication in ants was followed by subfunctionalization to acquire reproductive and non-reproductive functions and whether Vg reproductive function was co-opted to regulate behavior in sterile workers. To investigate these questions, we compared the expression patterns of P. barbatus Vg genes and analyzed the phylogenetic relationships and molecular evolution of Vg genes in ants. qRT-PCRs revealed that Pb_Vg1 is more highly expressed in queens compared to workers and in nurses compared to foragers. By contrast, the level of expression of Pb_Vg2 was higher in foragers than in nurses and queens. Phylogenetic analyses show that a first duplication of the ancestral Vg gene occurred after the divergence between the poneroid and formicoid clades and subsequent duplications occurred in the lineages leading to Solenopsis invicta, Linepithema humile and Acromyrmex echinatior. The initial duplication resulted in two Vg gene subfamilies preferentially expressed in queens and nurses (subfamily A) or in foraging workers (subfamily B). Finally, molecular evolution analyses show that the subfamily A experienced positive selection, while the subfamily B showed overall relaxation of purifying selection. Our results suggest that in P. barbatus the Vg gene underwent subfunctionalization after duplication to acquire caste- and behavior- specific expression associated with reproductive and non-reproductive functions, supporting the validity of the RGPH in ants.
Author Summary
One of the main features of social insects is the division of labor, whereby queens monopolize reproduction while sterile workers perform all of the tasks related to colony maintenance. The workers usually do so in an age-dependent sequence: young workers tend to nurse the brood inside the nest and older workers are more likely to forage for food. Previous studies revealed that vitellogenin, a yolk protein typically involved in the regulation of reproduction in solitary insects, has been co-opted to regulate division of labor in the honeybee. In this study, we investigate such a role of vitellogenin in another group of social insects: the ants. We first use phylogenetic analyses to reveal the existence of multiple vitellogenin genes in most of the sequenced ant genomes. Then we compare the expression of the two vitellogenin genes (Pb_Vg1 and Pb_Vg2) among queens, nurses and foragers in the seed-harvester ant Pogonomyrmex barbatus. Our results suggest that, after the initial duplication in ants, the vitellogenin genes acquired caste and behavioral specific expression associated with reproductive and non-reproductive nutritionally related functions. This study also shows that ants and bees, despite having evolved sociality independently, have conserved similar mechanisms to regulate division of labor.
doi:10.1371/journal.pgen.1003730
PMCID: PMC3744404  PMID: 23966882
11.  Quantifying the Effect of Colony Size and Food Distribution on Harvester Ant Foraging 
PLoS ONE  2012;7(7):e39427.
Desert seed-harvester ants, genus Pogonomyrmex, are central place foragers that search for resources collectively. We quantify how seed harvesters exploit the spatial distribution of seeds to improve their rate of seed collection. We find that foraging rates are significantly influenced by the clumpiness of experimental seed baits. Colonies collected seeds from larger piles faster than randomly distributed seeds. We developed a method to compare foraging rates on clumped versus random seeds across three Pogonomyrmex species that differ substantially in forager population size. The increase in foraging rate when food was clumped in larger piles was indistinguishable across the three species, suggesting that species with larger colonies are no better than species with smaller colonies at collecting clumped seeds. These findings contradict the theoretical expectation that larger groups are more efficient at exploiting clumped resources, thus contributing to our understanding of the importance of the spatial distribution of food sources and colony size for communication and organization in social insects.
doi:10.1371/journal.pone.0039427
PMCID: PMC3393712  PMID: 22808035
12.  Expression patterns of a circadian clock gene are associated with age-related polyethism in harvester ants, Pogonomyrmex occidentalis 
BMC Ecology  2009;9:7.
Background
Recent advances in sociogenomics allow for comparative analyses of molecular mechanisms regulating the development of social behavior. In eusocial insects, one key aspect of their sociality, the division of labor, has received the most attention. Age-related polyethism, a derived form of division of labor in ants and bees where colony tasks are allocated among distinct behavioral phenotypes, has traditionally been assumed to be a product of convergent evolution. Previous work has shown that the circadian clock is associated with the development of behavior and division of labor in honeybee societies. We cloned the ortholog of the clock gene, period, from a harvester ant (Pogonomyrmex occidentalis) and examined circadian rhythms and daily activity patterns in a species that represents an evolutionary origin of eusociality independent of the honeybee.
Results
Using real time qPCR analyses, we determined that harvester ants have a daily cyclic expression of period and this rhythm is endogenous (free-running under dark-dark conditions). Cyclic expression of period is task-specific; foragers have strong daily fluctuations but nest workers inside the nest do not. These patterns correspond to differences in behavior as activity levels of foragers show a diurnal pattern while nest workers tend to exhibit continuous locomotor activity at lower levels. In addition, we found that foragers collected in the early fall (relative warm, long days) exhibit a delay in the nightly peak of period expression relative to foragers collected in the early spring (relative cold, short days).
Conclusion
The association of period mRNA expression levels with harvester ant task behaviors suggests that the development of circadian rhythms is associated with the behavioral development of ants. Thus, the circadian clock pathway may represent a conserved 'genetic toolkit' that has facilitated the parallel evolution of age-related polyethism and task allocation in social insects.
doi:10.1186/1472-6785-9-7
PMCID: PMC2676274  PMID: 19374755
13.  A quantification of predation rates, indirect positive effects on plants, and foraging variation of the giant tropical ant, Paraponera clavata 
While a clear consensus is emerging that predators can play a major role in shaping terrestrial communities, basic natural history observations and simple quantifications of predation rates in complex terrestrial systems are lacking. The potential indirect effect of a large predatory ant, Paraponera clavata Fabricius (Formicidae: Ponerinae), on herbivores was determined on rainforest trees at La Selva Biological Station in Costa Rica and Barro Colorado Island in Panama. Prey and other food brought back to nests by 75 colonies of P. clavata were quantified, taking into account temporal, seasonal, and microhabitat variation for both foraging activity and composition of foraging booty. The dispersion and density of ant colonies and combined density with the mean amounts of prey retrieval were used to calculate rates of predation per hectare in the two forests. In addition, herbivory was measured on trees containing P. clavata and on trees where the ants were not foraging. Colonies at La Selva brought back significantly more nectar plus prey than those at Barro Colorado Island, but foraging patterns were similar in the two forests. At both forests, the ants were more active at night, and there was no significant seasonal or colonial variation in consumption of nectar, composition of foraging booty, and overall activity of the colonies. At La Selva, trees containing P. clavata colonies had the same levels of folivory as nearest neighbor trees without P. clavata but had significantly lower folivory than randomly selected trees. Predation by this ant was high in both forests, despite its omnivorous diet. This insect predator is part of potentially important top-down controls in these wet and moist forests.
PMCID: PMC355916  PMID: 15455052
La Selva; Costa Rica; Barro Colorado Island; Panama; foraging; predation; larvae; herbivory; indirect effects
14.  Does an ecological advantage produce the asymmetric lineage ratio in a harvester ant population? 
Oecologia  2013;173(3):849-857.
In dependent-lineage harvester ant populations, two lineages interbreed but are genetically distinct. The offspring of a male and queen of the same lineage are female reproductives; the offspring of a male and queen of different lineages are workers. Geographic surveys have shown asymmetries in the ratio of the two lineages in many harvester ant populations, which may be maintained by an ecological advantage to one of the lineages. Using census data from a long-term study of a dependent-lineage population of the red harvester ant, Pogonomyrmex barbatus, we identified the lineage of 130 colonies sampled in 1997–1999, ranging in age from 1 to 19 years when collected, and 268 colonies sampled in 2010, ranging in age from 1 to 28 years when collected. The ratio of lineages in the study population is similar across an 11-year interval, 0.59 J2 in 1999 and 0.66 J2 in 2010. The rare lineage, J1, had a slightly but significantly higher number of mates of the opposite lineage than the common lineage, J2, and, using data from previous work on reproductive output, higher male production. Mature colonies of the two lineages did not differ in nest mound size, foraging activity, or the propensity to relocate their nests. There were no strong differences in the relative recruitment or survivorship of the two lineages. Our results show no ecological advantage for either lineage, indicating that differences between the lineages in sex ratio allocation may be sufficient to maintain the current asymmetry of the lineage ratio in this population.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-013-2690-z) contains supplementary material, which is available to authorized users.
doi:10.1007/s00442-013-2690-z
PMCID: PMC3824609  PMID: 23715745
Skewed lineage ratio; Pogonomyrmex; Sex ratio
15.  Resource redistribution in polydomous ant nest networks: local or global? 
Behavioral Ecology  2014;25(5):1183-1191.
Lay Summary
Wood ants nests share resources with neighboring nests, not the whole colony. A single ant colony can either live all in one nest, or split into several separate, but communicating, nests. How and why ant colonies do this is unknown. By treating these separated colonies as networks we show that wood ants exchange food locally, with neighboring nests, without a colony-level plan.
An important problem facing organisms in a heterogeneous environment is how to redistribute resources to where they are required. This is particularly complex in social insect societies as resources have to be moved both from the environment into the nest and between individuals within the nest. Polydomous ant colonies are split between multiple spatially separated, but socially connected, nests. Whether, and how, resources are redistributed between nests in polydomous colonies is unknown. We analyzed the nest networks of the facultatively polydomous wood ant Formica lugubris. Our results indicate that resource redistribution in polydomous F. lugubris colonies is organized at the local level between neighboring nests and not at the colony level. We found that internest trails connecting nests that differed more in their amount of foraging were stronger than trails between nests with more equal foraging activity. This indicates that resources are being exchanged directly from nests with a foraging excess to nests that require resources. In contrast, we found no significant relationships between nest properties, such as size and amount of foraging, and network measures such as centrality and connectedness. This indicates an absence of a colony-level resource exchange. This is a clear example of a complex behavior emerging as a result of local interactions between parts of a system.
doi:10.1093/beheco/aru108
PMCID: PMC4160112  PMID: 25214755
Formica lugubris; levels of selection; network analysis; polydomy; self-organization; wood ants.
16.  Nest site and weather affect the personality of harvester ant colonies 
Behavioral Ecology  2012;23(5):1022-1029.
Environmental conditions and physical constraints both influence an animal's behavior. We investigate whether behavioral variation among colonies of the black harvester ant, Messor andrei, remains consistent across foraging and disturbance situations and ask whether consistent colony behavior is affected by nest site and weather. We examined variation among colonies in responsiveness to food baits and to disturbance, measured as a change in numbers of active ants, and in the speed with which colonies retrieved food and removed debris. Colonies differed consistently, across foraging and disturbance situations, in both responsiveness and speed. Increased activity in response to food was associated with a smaller decrease in response to alarm. Speed of retrieving food was correlated with speed of removing debris. In all colonies, speed was greater in dry conditions, reducing the amount of time ants spent outside the nest. While a colony occupied a certain nest site, its responsiveness was consistent in both foraging and disturbance situations, suggesting that nest structure influences colony personality.
doi:10.1093/beheco/ars066
PMCID: PMC3431114  PMID: 22936841
behavioral syndromes; collective behavior; harvester ant; Messor andrei; nest structure; personality; plasticity; social insects; temperament
17.  The hidden cost of information in collective foraging 
Many animals nest or roost colonially. At the start of a potential foraging period, they may set out independently or await information from returning foragers. When should such individuals act independently and when should they wait for information? In a social insect colony, for example, information transfer may greatly increase a recruit's probability of finding food, and it is commonly assumed that this will always increase the colony's net energy gain. We test this assumption with a mathematical model. Energy gain by a colony is a function both of the probability of finding food sources and of the duration of their availability. A key factor is the ratio of pro-active foragers to re-active foragers. When leaving the nest, pro-active foragers search for food independently, whereas re-active foragers rely on information from successful foragers to find food. Under certain conditions, the optimum strategy is totally independent (pro-active) foraging because potentially valuable information that re-active foragers may gain from successful foragers is not worth waiting for. This counter-intuitive outcome is remarkably robust over a wide range of parameters. It occurs because food sources are only available for a limited period. Our study emphasizes the importance of time constraints and the analysis of dynamics, not just steady states, to understand social insect foraging.
doi:10.1098/rspb.2005.3137
PMCID: PMC1559855  PMID: 16087424
collective foraging; optimal foraging; information transfer; recruitment; division of labour; social insect
18.  Specialization Does Not Predict Individual Efficiency in an Ant 
PLoS Biology  2008;6(11):e285.
The ecological success of social insects is often attributed to an increase in efficiency achieved through division of labor between workers in a colony. Much research has therefore focused on the mechanism by which a division of labor is implemented, i.e., on how tasks are allocated to workers. However, the important assumption that specialists are indeed more efficient at their work than generalist individuals—the “Jack-of-all-trades is master of none” hypothesis—has rarely been tested. Here, I quantify worker efficiency, measured as work completed per time, in four different tasks in the ant Temnothorax albipennis: honey and protein foraging, collection of nest-building material, and brood transports in a colony emigration. I show that individual efficiency is not predicted by how specialized workers were on the respective task. Worker efficiency is also not consistently predicted by that worker's overall activity or delay to begin the task. Even when only the worker's rank relative to nestmates in the same colony was used, specialization did not predict efficiency in three out of the four tasks, and more specialized workers actually performed worse than others in the fourth task (collection of sand grains). I also show that the above relationships, as well as median individual efficiency, do not change with colony size. My results demonstrate that in an ant species without morphologically differentiated worker castes, workers may nevertheless differ in their ability to perform different tasks. Surprisingly, this variation is not utilized by the colony—worker allocation to tasks is unrelated to their ability to perform them. What, then, are the adaptive benefits of behavioral specialization, and why do workers choose tasks without regard for whether they can perform them well? We are still far from an understanding of the adaptive benefits of division of labor in social insects.
Author Summary
Social insects, including ants, bees, and termites, may make up 75% of the world's insect biomass. This success is often attributed to their complex colony organization. Each individual is thought to specialize in a particular task and thus become an “expert” for this task. Researchers have long assumed that the ecological success of social insects derives from division of labor, just as the increase in productivity achieved in human societies; however, this assumption has not been thoroughly tested. Here, I have measured task performance of specialized and unspecialized ants. In the ant species studied here, it turns out that specialists are no better at their jobs than generalists, and sometimes even perform worse. In addition, most of the work in the colony is not performed by the most efficient workers. So the old adage “The Jack of all trades is a master of none” does not seem to apply to these ants, suggesting that we may have to revise our understanding of the benefits of colony organization
The assumption that the success of social insects rests on the increased efficiency of dividing tasks within the colony is challenged by evidence that specialists are not always better at their jobs.
doi:10.1371/journal.pbio.0060285
PMCID: PMC2586388  PMID: 19018663
19.  Leaf endophyte load influences fungal garden development in leaf-cutting ants 
BMC Ecology  2012;12:23.
Background
Previous work has shown that leaf-cutting ants prefer to cut leaf material with relatively low fungal endophyte content. This preference suggests that fungal endophytes exact a cost on the ants or on the development of their colonies. We hypothesized that endophytes may play a role in their host plants’ defense against leaf-cutting ants. To measure the long-term cost to the ant colony of fungal endophytes in their forage material, we conducted a 20-week laboratory experiment to measure fungal garden development for colonies that foraged on leaves with low or high endophyte content.
Results
Colony mass and the fungal garden dry mass did not differ significantly between the low and high endophyte feeding treatments. There was, however, a marginally significant trend toward greater mass of fungal garden per ant worker in the low relative to the high endophyte treatment. This trend was driven by differences in the fungal garden mass per worker from the earliest samples, when leaf-cutting ants had been foraging on low or high endophyte leaf material for only 2 weeks. At two weeks of foraging, the mean fungal garden mass per worker was 77% greater for colonies foraging on leaves with low relative to high endophyte loads.
Conclusions
Our data suggest that the cost of endophyte presence in ant forage material may be greatest to fungal colony development in its earliest stages, when there are few workers available to forage and to clean leaf material. This coincides with a period of high mortality for incipient colonies in the field. We discuss how the endophyte-leaf-cutter ant interaction may parallel constitutive defenses in plants, whereby endophytes reduce the rate of colony development when its risk of mortality is greatest.
doi:10.1186/1472-6785-12-23
PMCID: PMC3537522  PMID: 23140096
Atta colombica; Attini; Leaf-cutting ants; Lepiotaceae; Mutualism; Symbioses
20.  Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias 
Animal behaviour  2010;79(5):1001-1006.
In honeybee colonies, food collection is performed by a group of mostly sterile females called workers. After an initial nest phase, workers begin foraging for nectar and pollen, but tend to bias their collection towards one or the other. The foraging choice of honeybees is influenced by vitellogenin (vg), an egg-yolk precursor protein that is expressed although workers typically do not lay eggs. The forager reproductive ground plan hypothesis (RGPH) proposes an evolutionary path in which the behavioural bias toward collecting nectar or pollen on foraging trips is influenced by variation in reproductive physiology, such as hormone levels and vg gene expression. Recently, the connections between vg and foraging behaviour were challenged by Oldroyd and Beekman (2008), who concluded from their study that the ovary, and especially vg, played no role in foraging behaviour of bees. We address their challenge directly by manipulating vg expression by RNA interference- (RNAi) mediated gene knockdown in two honeybee genotypes with different foraging behaviour and reproductive physiology. We show that the effect of vg on the food-loading decisions of the workers occurs only in the genotype where timing of foraging onset (by age) is also sensitive to vg levels. In the second genotype, changing vg levels do not affect foraging onset or bias. The effect of vg on workers' age at foraging onset is explained by the well-supported double repressor hypothesis (DHR), which describes a mutually inhibitory relationship between vg and juvenile hormone (JH) — an endocrine factor that influences development, reproduction, and behaviour in many insects. These results support the RGPH and demonstrate how it intersects with an established mechanism of honeybee behavioural control.
doi:10.1016/j.anbehav.2010.02.009
PMCID: PMC2863014  PMID: 20454635
Apis mellifera; juvenile hormone; reproductive ground plan hypothesis; RNA interference; social foraging; vitellogenin yolk protein
21.  Do Ants Need to Estimate the Geometrical Properties of Trail Bifurcations to Find an Efficient Route? A Swarm Robotics Test Bed 
PLoS Computational Biology  2013;9(3):e1002903.
Interactions between individuals and the structure of their environment play a crucial role in shaping self-organized collective behaviors. Recent studies have shown that ants crossing asymmetrical bifurcations in a network of galleries tend to follow the branch that deviates the least from their incoming direction. At the collective level, the combination of this tendency and the pheromone-based recruitment results in a greater likelihood of selecting the shortest path between the colony's nest and a food source in a network containing asymmetrical bifurcations. It was not clear however what the origin of this behavioral bias is. Here we propose that it results from a simple interaction between the behavior of the ants and the geometry of the network, and that it does not require the ability to measure the angle of the bifurcation. We tested this hypothesis using groups of ant-like robots whose perceptual and cognitive abilities can be fully specified. We programmed them only to lay down and follow light trails, avoid obstacles and move according to a correlated random walk, but not to use more sophisticated orientation methods. We recorded the behavior of the robots in networks of galleries presenting either only symmetrical bifurcations or a combination of symmetrical and asymmetrical bifurcations. Individual robots displayed the same pattern of branch choice as individual ants when crossing a bifurcation, suggesting that ants do not actually measure the geometry of the bifurcations when travelling along a pheromone trail. Finally at the collective level, the group of robots was more likely to select one of the possible shorter paths between two designated areas when moving in an asymmetrical network, as observed in ants. This study reveals the importance of the shape of trail networks for foraging in ants and emphasizes the underestimated role of the geometrical properties of transportation networks in general.
Author Summary
Most ant species form transportation networks, be they foraging trails linking food sources to the main colony or underground galleries connecting the different parts of the nest. As for human transportation networks (roads, airlines, etc.), the design and the placement of the connecting points (or nodes) dramatically affects the movement of individuals and hence the exchanges of material and information. In a previous study, we have shown that the geometrical configuration of these nodes (i.e., the angles between the different exiting branches) can affect the route followed by an ant in a network of galleries and, as a consequence, the efficiency of the pheromone-based recruitment toward a food source. Here we show that we can reproduce these results using ant-like robots with minimal perceptual and cognitive capabilities. We demonstrate that the simple interaction between the displacement of an ant and the geometrical configuration of the gallery network can greatly affect the foraging performances of the colony. This result increases our understanding of how workers move through structures built by ant colonies and more generally points toward possible improvements for the design of man-made transportation networks.
doi:10.1371/journal.pcbi.1002903
PMCID: PMC3610605  PMID: 23555202
22.  Division of Labor Associated with Brood Rearing in the Honey Bee: How Does It Translate to Colony Fitness? 
PLoS ONE  2011;6(2):e16785.
Division of labor is a striking feature observed in honey bees and many other social insects. Division of labor has been claimed to benefit fitness. In honey bees, the adult work force may be viewed as divided between non-foraging hive bees that rear brood and maintain the nest, and foragers that collect food outside the nest. Honey bee brood pheromone is a larval pheromone that serves as an excellent empirical tool to manipulate foraging behaviors and thus division of labor in the honey bee. Here we use two different doses of brood pheromone to alter the foraging stimulus environment, thus changing demographics of colony division of labor, to demonstrate how division of labor associated with brood rearing affects colony growth rate. We examine the effects of these different doses of brood pheromone on individual foraging ontogeny and specialization, colony level foraging behavior, and individual glandular protein synthesis. Low brood pheromone treatment colonies exhibited significantly higher foraging population, decreased age of first foraging and greater foraging effort, resulting in greater colony growth compared to other treatments. This study demonstrates how division of labor associated with brood rearing affects honey bee colony growth rate, a token of fitness.
doi:10.1371/journal.pone.0016785
PMCID: PMC3035648  PMID: 21347428
23.  Effects of Selection for Honey Bee Worker Reproduction on Foraging Traits 
PLoS Biology  2008;6(3):e56.
The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked.
Author Summary
In social insects, the evolution of the worker caste and the regulation of reproductive behaviour by workers are poorly understood. Evolution is conservative and often proceeds by adapting an existing gene network to a new function. The “reproductive ground plan” hypothesis (RGPH) suggests that social insects evolved their queen and worker castes by modifying a gene network that once regulated the foraging and reproductive phases of solitary ancestors. In this model, queens retain characteristics of insects in their reproductive phase, whereas workers retain characteristics of the foraging phase. Moreover, the foraging behaviour of workers may also be regulated by the same genes that once controlled the switch between foraging and feeding young in the nest. We evaluated the RGPH by studying a line of honey bees selected for high rates of worker reproduction. We show that in this line workers forage late in life and some may never forage, supporting the idea that genes related to reproduction are also related to foraging. However, we found no support for recent suggestions that genes related to reproduction also regulate the foraging behaviour of individual workers: once they start foraging, our highly reproductive workers forage in the same way that unselected workers do.
A new study lends support to the model of social insect evolution, in which a gene regulatory network linked to the reproductive and foraging phases of ancestral solitary insects gave rise to queen and worker castes. But the study challenges the notion that genes related to reproduction also regulate the foraging behavior of workers.
doi:10.1371/journal.pbio.0060056
PMCID: PMC2270312  PMID: 18318602
24.  The Trail Less Traveled: Individual Decision-Making and Its Effect on Group Behavior 
PLoS ONE  2012;7(10):e47976.
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.
doi:10.1371/journal.pone.0047976
PMCID: PMC3480453  PMID: 23112880
25.  Bringing Home the Trash: Do Colony-Based Differences in Foraging Distribution Lead to Increased Plastic Ingestion in Laysan Albatrosses? 
PLoS ONE  2009;4(10):e7623.
When searching for prey, animals should maximize energetic gain, while minimizing energy expenditure by altering their movements relative to prey availability. However, with increasing amounts of marine debris, what once may have been ‘optimal’ foraging strategies for top marine predators, are leading to sub-optimal diets comprised in large part of plastic. Indeed, the highly vagile Laysan albatross (Phoebastria immutabilis) which forages throughout the North Pacific, are well known for their tendency to ingest plastic. Here we examine whether Laysan albatrosses nesting on Kure Atoll and Oahu Island, 2,150 km apart, experience different levels of plastic ingestion. Twenty two geolocators were deployed on breeding adults for up to two years. Regurgitated boluses of undigestable material were also collected from chicks at each site to compare the amount of plastic vs. natural foods. Chicks from Kure Atoll were fed almost ten times the amount of plastic compared to chicks from Oahu despite boluses from both colonies having similar amounts of natural food. Tracking data indicated that adults from either colony did not have core overlapping distributions during the early half of the breeding period and that adults from Kure had a greater overlap with the putative range of the Western Garbage Patch corroborating our observation of higher plastic loads at this colony. At-sea distributions also varied throughout the year suggesting that Laysan albatrosses either adjusted their foraging behavior according to constraints on time away from the nest or to variation in resources. However, in the non-breeding season, distributional overlap was greater indicating that the energy required to reach the foraging grounds was less important than the total energy available. These results demonstrate how a marine predator that is not dispersal limited alters its foraging strategy throughout the reproductive cycle to maximize energetic gain and how this has led to differences in plastic ingestion.
doi:10.1371/journal.pone.0007623
PMCID: PMC2762601  PMID: 19862322

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