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1.  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
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.  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
5.  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
6.  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
7.  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
8.  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
9.  Seasonality Directs Contrasting Food Collection Behavior and Nutrient Regulation Strategies in Ants 
PLoS ONE  2011;6(9):e25407.
Long-lived animals, including social insects, often display seasonal shifts in foraging behavior. Foraging is ultimately a nutrient consumption exercise, but the effect of seasonality per se on changes in foraging behavior, particularly as it relates to nutrient regulation, is poorly understood. Here, we show that field-collected fire ant colonies, returned to the laboratory and maintained under identical photoperiod, temperature, and humidity regimes, and presented with experimental foods that had different protein (p) to carbohydrate (c) ratios, practice summer- and fall-specific foraging behaviors with respect to protein-carbohydrate regulation. Summer colonies increased the amount of food collected as the p:c ratio of their food became increasingly imbalanced, but fall colonies collected similar amounts of food regardless of the p:c ratio of their food. Choice experiments revealed that feeding was non-random, and that both fall and summer ants preferred carbohydrate-biased food. However, ants rarely ate all the food they collected, and their cached or discarded food always contained little carbohydrate relative to protein. From a nutrient regulation strategy, ants consumed most of the carbohydrate they collected, but regulated protein consumption to a similar level, regardless of season. We suggest that varied seasonal food collection behaviors and nutrient regulation strategies may be an adaptation that allows long-lived animals to meet current and future nutrient demands when nutrient-rich foods are abundant (e.g. spring and summer), and to conserve energy and be metabolically more efficient when nutritionally balanced foods are less abundant.
doi:10.1371/journal.pone.0025407
PMCID: PMC3180453  PMID: 21966522
10.  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
11.  Coupled oscillators and activity waves in ant colonies 
We investigated the phenomenon of activity cycles in ants, taking into account the spatial structure of colonies. In our study species, Leptothorax acervorum, there are two spatially segregated groups in the nest. We developed a model that considers the two groups as coupled oscillators which can produce synchronized activity. By investigating the effects of noise on the model system we predicted how the return of foragers affects activity cycles in ant colonies. We tested these predictions empirically by comparing the activity of colonies under two conditions: when foragers are and are not allowed to return to the nest. The activity of the whole colony and of each group within the colony was studied using image analysis. This allowed us to reveal the spatial pattern of activity wave propagation in ant colonies for the first time.
doi:10.1098/rspb.1999.0647
PMCID: PMC1689693
12.  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
13.  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
14.  Optimality in a partitioned task performed by social insects 
Biology Letters  2008;4(6):627-629.
Biologists have long been aware that adaptations should not be analysed in isolation from the function of the whole organism. Here, we address the equivalent issue at the scale of a social insect colony: the optimality of component behaviours in a partitioned sequence of tasks. In colonies of Atta colombica, a leaf-cutting ant, harvested leaf tissue is passed from foragers to nest workers that distribute, clean, shred and implant the tissue in fungal gardens. In four laboratory colonies of A. colombica, we found that the highest colony-wide rate of leaf tissue processing in the nest was achieved when leaf fragment sizes were suboptimal for individual delivery rate by foragers. Leaf-cutting ant colonies appear to compromise the efficiency of collecting leaf tissue in order to increase their ability to handle the material when it arrives in the nest. Such compromise reinforces the idea that behavioural adaptations, like adaptations in general, must be considered within the context of the larger entity of which they are a part.
doi:10.1098/rsbl.2008.0398
PMCID: PMC2614165  PMID: 18782732
adaptation; Atta colombica; foraging; leaf-cutting ant; optimality; task partitioning
15.  The Old Ladies of the Seed Harvester ant Pogonomyrmex Rugosus: Foraging Performed by Two Groups of Workers 
Journal of Insect Behavior  2008;22(3):217-226.
We examined temporal polyethism in Pogonomyrmex rugosus, predicting a pattern of decreasing age from foragers to nest maintenance workers to individuals that were recruited to harvest a temporary food source. Nest maintenance workers were younger than foragers, as indicated by their heavier mass and lower mandibular wear. In contrast, recruited foragers were similar in mass to foragers but they displayed higher mandibular wear, suggesting that they were at least as old as foragers. Longevity estimates for marked individuals of these two latter task groups showed mixed results. Higher mandibular wear of recruited foragers suggests that they did not follow the normal sequence for temporal polyethism, but rather that they functioned as seed-millers, which should more quickly abrade their dentition. This would be the first demonstration of specialist milling individuals in a monomorphic seed-harvester ant.
doi:10.1007/s10905-008-9167-7
PMCID: PMC3085757  PMID: 21654914
Age polyethism; forager; Pogonomyrmex rugosus; nest maintenance workers; recruited foragers
16.  Rank orders and division of labour among unrelated cofounding ant queens. 
Young, unrelated queens may cooperate in colony founding (pleometrosis) in many species of ants. Whereas the founding queens of many 'advanced' species rely completely on body reserves in order to rear their first young, queens of the ponerine Pachycondyla 'inversa' forage for food. In founding associations, only one queen specializes in this risky task. Here we show that the division of labour is strongly affected by aggressive interactions between cofounding queens: the dominant remains in the nest and guards the brood, whereas the subordinate is forced to leave and forage. The frequency of queen antagonism increased with the duration since food was last added to the foraging arena. Egg-laying rates did not differ significantly between nest-mate queens, but dominant queens destroyed and ate some of the eggs laid by subordinates.
PMCID: PMC1690735  PMID: 12233769
17.  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
18.  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
19.  Record Dynamics in Ants 
PLoS ONE  2010;5(3):e9621.
The success of social animals (including ourselves) can be attributed to efficiencies that arise from a division of labour. Many animal societies have a communal nest which certain individuals must leave to perform external tasks, for example foraging or patrolling. Staying at home to care for young or leaving to find food is one of the most fundamental divisions of labour. It is also often a choice between safety and danger. Here we explore the regulation of departures from ant nests. We consider the extreme situation in which no one returns and show experimentally that exiting decisions seem to be governed by fluctuating record signals and ant-ant interactions. A record signal is a new ‘high water mark’ in the history of a system. An ant exiting the nest only when the record signal reaches a level it has never perceived before could be a very effective mechanism to postpone, until the last possible moment, a potentially fatal decision. We also show that record dynamics may be involved in first exits by individually tagged ants even when their nest mates are allowed to re-enter the nest. So record dynamics may play a role in allocating individuals to tasks, both in emergencies and in everyday life. The dynamics of several complex but purely physical systems are also based on record signals but this is the first time they have been experimentally shown in a biological system.
doi:10.1371/journal.pone.0009621
PMCID: PMC2836372  PMID: 20300174
20.  Surface structure helps desert ants return to known feeding sites 
Desert ants, Cataglyphis fortis, return to their nest when they are disturbed during their foraging trips. Training them to a landmark corridor enabled us to induce ants that were captured immediately after leaving the nest and transferred to an unknown area to start their foraging trips.1 However, most of the ants never traveled the entire foraging distance to the feeder, but aborted their runs after the landmark corridor was no longer visible. Therefore, apart from landmark information and path integrator, there are additional cues that determine the ants' foraging behavior. Considering the reduced straightness of the outbound runs, I argue that surface structure might have a remarkable impact on foraging desert ants.
PMCID: PMC2649295  PMID: 19704861
desert ants; foraging behavior; landmarks; surface structure; training; feeding site
21.  Soldiers Initiate Foraging Activities in the Subterranean Termite, Heterotermes tenuis  
Caste polyethism has been recorded in some termite species, however the foraging behavior of subterranean termites remains poorly known. Heterotermes tenuis Hagen (Isoptera: Rhinotermitidae) is a subterranean termite that is native to Brazil and is an agricultural and urban pest. The aim of this study was to investigate which caste acts as scouts when searching for food sources and determinate the percentages of each caste present in the foraging territories of field colonies of H. tenuis. Our results showed no significant differences among the caste proportions present in the foraging territories of the three colonies studied in the field. Laboratory experiments showed that minor soldiers were the most frequent initiators of foraging activities. This result suggests that the exploratory phase of the foraging behavior may be regulated by the number of soldiers present in the foraging territories of each colony.
doi:10.1673/031.008.0201
PMCID: PMC3061577  PMID: 20345313
termites; Heterotermes tenuis; soldier; foraging behavior; polyethism
22.  How Load-Carrying Ants Avoid Falling Over: Mechanical Stability during Foraging in Atta vollenweideri Grass-Cutting Ants 
PLoS ONE  2013;8(1):e52816.
Background
Foraging workers of grass-cutting ants (Atta vollenweideri) regularly carry grass fragments larger than their own body. Fragment length has been shown to influence the ants’ running speed and thereby the colony’s food intake rate. We investigated whether and how grass-cutting ants maintain stability when carrying fragments of two different lengths but identical mass.
Principal Findings
Ants carried all fragments in an upright, backwards-tilted position, but held long fragments more vertically than short ones. All carrying ants used an alternating tripod gait, where mechanical stability was increased by overlapping stance phases of consecutive steps. The overlap was greatest for ants carrying long fragments, resulting in more legs contacting the ground simultaneously. For all ants, the projection of the total centre of mass (ant and fragment) was often outside the supporting tripod, i.e. the three feet that would be in stance for a non-overlapping tripod gait. Stability was only achieved through additional legs in ground contact. Tripod stability (quantified as the minimum distance of the centre of mass to the edge of the supporting tripod) was significantly smaller for ants with long fragments. Here, tripod stability was lowest at the beginning of each step, when the center of mass was near the posterior margin of the supporting tripod. By contrast, tripod stability was lowest at the end of each step for ants carrying short fragments. Consistently, ants with long fragments mainly fell backwards, whereas ants carrying short fragments mainly fell forwards or to the side. Assuming that transporting ants adjust neither the fragment angle nor the gait, they would be less stable and more likely to fall over.
Conclusions
In grass-cutting ants, the need to maintain static stability when carrying long grass fragments has led to multiple kinematic adjustments at the expense of a reduced material transport rate.
doi:10.1371/journal.pone.0052816
PMCID: PMC3534694  PMID: 23300994
23.  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
24.  Dealing with water deficit in Atta ant colonies: large ants scout for water while small ants transport it 
Biology Open  2012;1(9):827-830.
Summary
Leafcutter ants (Atta sexdens rubropilosa) (Forel 1908) have an elaborate social organization, complete with caste divisions. Activities carried out by specialist groups contribute to the overall success and survival of the colony when it is confronted with environmental challenges such as dehydration. Ants detect variations in humidity inside the nest and react by activating several types of behavior that enhance water uptake and decrease water loss, but it is not clear whether or not a single caste collects water regardless of the cost of bringing this resource back to the colony. Accordingly, we investigated water collection activities in three colonies of Atta sexdens rubropilosa experimentally exposed to water stress. Specifically, we analyzed whether or not the same ant caste foraged for water, regardless of the absolute energetic cost (distance) of transporting this resource back to the colony. Our experimental design offered water sources at 0 m, 1 m and 10 m from the nest. We studied the body size of ants near the water sources from the initial offer of water (time  =  0) to 120 min, and tested for specialization. We observed a reduction in the average size and variance of ants that corroborated the specialization hypothesis. Although the temporal course of specialization changed with distance, the final outcome was similar among distances. Thus, we conclude that, for this species, a specialist (our use of the word “specialist” does not mean exclusive) task force is responsible for collecting water, regardless of the cost of transporting water back to the colony.
doi:10.1242/bio.2012703
PMCID: PMC3507235  PMID: 23213476
Atta sexdens rubropilosa; Water stress; Task division; Task specialization
25.  Allometric scaling of foraging rate with trail dimensions in leaf-cutting ants 
Leaf-cutting ants (Atta spp.) create physical pathways to support the transport of resources on which colony growth and reproduction depend. We determined the scaling relationship between the rate of resource acquisition and the size of the trail system and foraging workforce for 18 colonies of Atta colombica and Atta cephalotes. We examined conventional power-law scaling patterns, but did so in a multivariate analysis that reveals the simultaneous effects of forager number, trail length and trail width. Foraging rate (number of resource-laden ants returning to the nest per unit time) scaled at the 0.93 power of worker numbers, the –1.02 power of total trail length and the 0.65 power of trail width. These scaling exponents indicate that individual performance declines only slightly as more foragers are recruited to the workforce, but that trail length imposes a severe penalty on the foraging rate. A model of mass traffic flow predicts the allometric patterns for workforce and trail length, although the effect of trail width is unexpected and points to the importance of the little-known mechanisms that regulate a colony's investment in trail clearance. These results provide a point of comparison for the role that resource flows may play in allometric scaling patterns in other transport-dependent entities, such as human cities.
doi:10.1098/rspb.2011.2583
PMCID: PMC3350673  PMID: 22337696
allometry; Atta; foraging; leaf-cutting ants; scaling; traffic flow

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