Context-dependent navigation in a collectively foraging species of ant, Messor cephalotes

More than 100 years of scientific research has provided evidence for sophisticated navigational mechanisms in social insects. One key role for navigation in ants is the orientation of workers between food sources and the nest. The focus of recent work has been restricted to navigation in individually foraging ant species, yet many species do not forage entirely independently, instead relying on collectively maintained information such as persistent trail networks and/or pheromones. Harvester ants use such networks, but additionally, foragers often search individually for food either side of trails. In the absence of a trail, these ‘off-trail’ foragers must navigate independently to relocate the trail and return to the nest. To investigate the strategies used by ants on and off the main trails, we conducted field experiments with a harvester ant species, Messor cephalotes, by transferring on-trail and off-trail foragers to an experimental arena. We employed custom-built software to track and analyse ant trajectories in the arena and to quantitatively compare behaviour. Our results indicate that foragers navigate using different cues depending on whether they are travelling on or off the main trails. We argue that navigation in collectively foraging ants deserves more attention due to the potential for behavioural flexibility arising from the relative complexity of journeys between food and the nest.     

How patrollers set foraging direction in harvester ants

Recruitment to food or nest sites is well known in ants; the recruiting ants lay a chemical trail that other ants follow to the target site, or they walk with other ants to the target site. Here we report that a different process determines foraging direction in the harvester ant Pogonomyrmex barbatus. Each day, the colony chooses from among up to eight distinct foraging trails; colonies use different trails on different days. Here we show that the patrollers regulate the direction taken by foragers each day by depositing Dufour's secretions onto a sector of the nest mound about 20 cm long and leading to the beginning of a foraging trail. The patrollers do not recruit foragers all the way to food sources, which may be up to 20 m away. Fewer foragers traveled along a trail if patrollers had no access to the sector of the nest mound leading to that trail. Adding Dufour's gland extract to patroller-free sectors of the nest mound rescued foraging in that direction, while poison gland extract did not. We also found that in the absence of patrollers, most foragers used the direction they had used on the previous day. Thus, the colony's 30-50 patrollers act as gatekeepers for thousands of foragers and choose a foraging direction, but they do not recruit and lead foragers all the way to a food source.     

The allocation of foragers in red wood ants

Abstract. 1. We studied how colonies of the red wood ant, Formica polyctena , adjust the numbers of foragers allocated to different foraging trails. In a series of field experiments, foragers were marked and transferred from one nest to another, related nest, where they joined the foraging force. Transferred workers acted as a reserve of uncommitted, available foragers.
2. Previous work shows that each individual forager habitually uses one trail. We found that for an uncommitted forager, the influence of recruitment initially is stronger than that of directional fidelity. Transferred workers were likely to use trails leading to new food sources. When transferred to a new nest, foragers were not likely to use a trail in the same direction as their original trail in the donor nest.
3. After a week, transferred foragers tended to develop route fidelity. Even after bait was no longer present, they continued to use the trail that had formerly led to a bait source.
4. We examined how colonies adjust numbers on a trail by experimentally depleting some trails. Colonies usually did not compensate for depletion: foragers were not recruited to depleted trails.
5. In general, the dynamics of foraging in this species facilitate a consistent foraging effort rather than rapid adjustments of forager allocation.     

The Dynamics of Foraging Trails in the Tropical Arboreal Ant Cephalotes goniodontus

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.     

To be or not to be faithful: flexible fidelity to foraging trails in the leaf‐cutting ant Acromyrmex lobicornis

1. Ants using trails to forage have to select between two alternative routes at bifurcations, using two, potentially conflicting, sources of information to make their decision: individual experience to return to a previous successful foraging site (i.e. fidelity) and ant traffic. In the field, we investigated which of these two types of information individuals of the leaf‐cutting ant Acromyrmex lobicornis Emery use to decide which foraging route to take. 2. We measured the proportion of foraging ants returning to each trail of bifurcations the following day, and for 4–7 consecutive days. We then experimentally increased ant traffic on one trail of the bifurcation by adding additional food sources to examine the effect of increased ant traffic on the decision that ants make. 3. Binomial tests showed that for 62% of the trails, ant fidelity was relatively more important than ant traffic in deciding which bifurcation to follow, suggesting the importance of previous experience. 4. When information conflict was generated by experimentally increasing ant traffic along the trail with less foraging activity, most ants relied on ant traffic to decide. However, in 33% of these bifurcations, ants were still faithful to their trail. Thus, there is some degree of flexibility in the decisions that A. lobicornis make to access food resources. 5. This flexible fidelity results in individual variation in the response of workers to different levels of ant traffic, and allows the colony to simultaneously exploit both established and recently discovered food patches, aiding efficient food gathering.     

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

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

Flexibility of Individual Load-mass Selection in Relation to Foraging Trail Gradient in the Leaf-cutter Ant Acromyrmex octospinosus

The stochasticity in food quality and availability, and physical trail characteristics experienced by leaf-cutter ants, may favour individual flexibility in load-mass selection so as to forage effectively. The present study aimed to confirm previous evidence, from Atta cephaoltes foragers, of variable load-mass selection in response to steep inclines and declines in the leaf-cutter ant Acromyrmex octospinosus. The foraging trail gradient of a captive colony of Ac. octospinosus was manipulated by altering the position of a foraging platform relative to the nest box. The results indicate an effect of steep gradients on walking speed and variation in load mass in relation to gradient as a result of individual plasticity, not recruitment of different-sized individuals. Ants selected heavier loads when returning to the nest vertically downwards than when returning horizontally or vertically upwards. These results are discussed with reference to foraging performance. Walking speed was considerably reduced on upward returns to the nest, but was also slower when travelling vertically downwards compared with horizontal trails, suggesting vertical trails per se impact on the time costs of foraging. Differences in load-mass selection were evident from the onset of foraging and did not change significantly over the course of 24 h, suggesting this behaviour was based on individual experience, rather than colony-level information feedback. The present study has demonstrated that Ac. octospinosus foragers are capable of individual flexibility in load-mass selection in response to a physical trail characteristic that is pertinent to their natural habitat and is a factor seldom considered in theoretical foraging models.     

Foraging in highly dynamic environments: leaf‐cutting ants adjust foraging trail networks to pioneer plant availability

Major shifts in the availability of palatable plant resources are of key relevance to the ecology of leaf‐cutting ants in human‐modified landscapes. However, our knowledge is still limited regarding the ability of these ants to adjust their foraging strategy to dynamic environments. Here, we examine a set of forest stand attributes acting as modulating forces for the spatiotemporal architecture of foraging trail networks developed by Atta cephalotes L. (Hymenoptera: Formicidae: Attini). During a 12‐month period, we mapped the foraging systems of 12 colonies located in Atlantic forest patches with differing size, regeneration age, and abundance of pioneer plants, and examined the variation in five trail system attributes (number of trails, branching points, leaf sources, linear foraging distance, and trail complexity) in response to these patch‐related variables. Both the month‐to‐month differences (depicted in annual trail maps) and the steadily accumulating number of trails, trail‐branching points, leaf sources, and linear foraging distance illustrated the dynamic nature of spatial foraging and trail complexity. Most measures of trail architecture correlated positively with the number of pioneer trees across the secondary forest patches, but no effects from patch age and size were observed (except for number of leaf sources). Trail system complexity (measured as fractal dimension; Df index) varied from 1.114 to 1.277 along the 12 months through which ant foraging was monitored, with a marginal trend to increase with the abundance of pioneer stems. Our results suggest that some leaf‐cutting ant species are able to generate highly flexible trail networks (via fine‐tuned adjustment of foraging patterns), allowing them to profit from the continuous emergence/recruitment of palatable resources.     

Waste management in the leaf-cutting ant Atta colombica

Unlike most leaf-cutting ants, which have underground wastedumps, the leaf-cutting ant Atta colombica dumps waste in aheap outside the nest. Waste is hazardous, as it is contaminatedwith pathogens. We investigated the organization of the workforceinvolved in outside-nest tasks (foraging, waste disposal) andquantified task switching and heap location to test hypothesesthat these tasks are organized to minimize contact between the heap and foraging entrances and trails. Waste management isan important task: 11% of externally working ants were eithertransporting waste or manipulating waste on the heap, and theother 89% were foragers. There is strict division of laborbetween foragers and waste workers, with no task switching.Waste management also has division of labor and is undertakenby transporters that carry waste to the heap margins and heapworkers that manage the heap. Waste heaps are always locateddownhill from nest entrances. The distance to the waste heapis positively related to colony size and negatively relatedto slope. Foraging trails avoid the heap, with 92% of trailsgoing away from the heap. This avoidance behavior is costly,increasing foraging trail length by at least 6%. Waste managementin A. colombica is a sophisticated system that encompassesboth work and spatial organization. This organization is probablyadaptive in reducing disease transmission. Division of labor separates waste management from foraging, reducing the likelihoodof foragers becoming contaminated with waste. The downhilllocation of heaps reduces waste entering entrances during rain.The orientation of foraging trails reduces the possibilityof foragers becoming accidentally contaminated with waste.     

Better tired than lost: Turtle ant trail networks favor coherence over short edges

Creating a routing backbone is a fundamental problem in both biology and engineering. The routing backbone of the trail networks of arboreal turtle ants (Cephalotes goniodontus) connects many nests and food sources using trail pheromone deposited by ants as they walk. Unlike species that forage on the ground, the trail networks of arboreal ants are constrained by the vegetation. We examined what objectives the trail networks meet by comparing the observed ant trail networks with networks of random, hypothetical trail networks in the same surrounding vegetation and with trails optimized for four objectives: minimizing path length, minimizing average edge length, minimizing number of nodes, and minimizing opportunities to get lost. The ants’ trails minimized path length by minimizing the number of nodes traversed rather than choosing short edges. In addition, the ants’ trails reduced the opportunity for ants to get lost at each node, favoring nodes with 3D configurations most likely to be reinforced by pheromone. Thus, rather than finding the shortest edges, turtle ant trail networks take advantage of natural variation in the environment to favor coherence, keeping the ants together on the trails.     

A field assessment of optimal foraging in ants: trail patterns and seed retrieval by the European harvester ant Messor barbarus

Summary: The ant Messor barbarus is a major seed predator on annual grasslands of the Mediterranean area. This paper is an attempt to relate the foraging ecology of this species to resource availability and to address several predictions of optimal foraging theory under natural conditions of seed harvesting.¶Spatial patterns of foraging trails tended to maximise acquisition of food resources, as trails led the ants to areas where seeds were more abundant locally. Moreover, harvesting activity concentrated on highly frequented trails, on which seeds were brought into the nest in larger numbers and more efficiently, at a higher mean rate per worker.¶The predictions of optimal foraging theory that ants should be more selective in both more resource-rich and more distant patches were tested in the native seed background. We confirm that selectivity of ants is positively related to trail length and thus to distance from the nest of foraged seeds. Conversely, we fail to find a consistent relationship between selectivity and density or species diversity of seed patches. We discuss how selectivity assessed at the colony level may depend on factors other than hitherto reported behavioural changes in seed choice by individual foragers.     

The Regulation of Ant Colony Foraging Activity without Spatial Information

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

Synergy between social and private information increases foraging efficiency in ants

Insect societies integrate many information sources to organize collective activities such as foraging. Many ants use trail pheromones to guide foragers to food sources, but foragers can also use memories to find familiar locations of stable food sources. Route memories are often more accurate than trail pheromones in guiding ants, and are often followed in preference to trail pheromones when the two conflict. Why then does the system expend effort in producing and acquiring seemingly redundant and low-quality information, such as trail pheromones, when route memory is available? Here we show that, in the ant Lasius niger, trail pheromones and route memory act synergistically during foraging; increasing walking speed and straightness by 25 and 30 per cent, respectively, and maintaining trail pheromone deposition, but only when used together. Our results demonstrate a previously undescribed major role of trail pheromones: to complement memory by allowing higher confidence in route memory. This highlights the importance of multiple interacting information sources in the efficient running of complex adaptive systems.     

Regulation of ants' foraging to resource productivity

We investigate the behavioural rule used by ant societies to adjust their foraging response to the honeydew productivity of aphids. When a scout finds a single food source, the decision to lay a recruitment trail is an all-or-none response based on the opportunity for this scout to ingest a desired volume acting as a threshold. Here, we demonstrate, through experimental and theoretical approaches, the generic value of this recruitment rule that remains valid when ants have to forage on multiple small sugar feeders to reach their desired volume. Moreover, our experiments show that when ants decide to recruit nest-mates they lay trail marks of equal intensity, whatever the number of food sources visited. A model based on the 'desired volume' rule of recruitment as well as on experimentally validated parameter values was built to investigate how ant societies adjust their foraging response to the honeydew productivity profile of aphids. Simulations predict that, with such recruiting rules, the percentage of recruiting ants is directly related to the total production of honeydew. Moreover, an optimal number of foragers exists that maximizes the strength of recruitment, this number being linearly related to the total production of honeydew by the aphid colony. The 'desired volume' recruitment rule that should be generic for all ant species is enough to explain how ants optimize trail recruitment and select aphid colonies or other liquid food resources according to their productivity profile.     

华南地区桑园和荒地两种生境中红火蚁觅食工蚁的食物组成

【目的】红火蚁Solenopsis invicta Buren是世界最危险的有害入侵生物之一,2004年入侵我国华南地区,并给农林业安全、生态安全带来极大危害。调查并明确田间红火蚁觅食工蚁的食物种类及数量,不仅为评估红火蚁猎食对生态环境中节肢动物群落的影响,而且为红火蚁防治饵剂的改进提供科学依据。【方法】本研究采用蚁道剖析法,对华南地区桑园和荒地两种生境中红火蚁觅食工蚁搬运的固体残片取样和鉴定;依搬运工蚁及其固体残片尺寸进行测量分级并称重,以分析工蚁多态性与固体食物大小的关系;采用薄层色谱法和氨基酸分析法测定嗉囊液体样品的营养成分及含量。【结果】在华南地区桑园和荒地中,红火蚁觅食工蚁搬运回巢的固体食物包括固体的动物残片和植物种子,其中动物残片属于3门7纲21个类群(包括14个昆虫目),昆虫纲动物所占比例为总固体食物的45.53%~46.10%。工蚁偏好搬运长1.400±0.043 mm~2.306±0.063 mm和宽0.723±0.028 mm~1.261±0.051 mm的固体残片,其重量在0.203~0.413 mg之间。红火蚁觅食工蚁嗉囊液体由多种氨基酸、果糖和葡萄糖组成,在桑园和荒地采集到的红火蚁嗉囊液体样本中的氨基酸总含量分别为1 544.31 mg/L和861.48 mg/L,氨基酸种类分别为33种和32种,其中31种氨基酸为共有的。【结论】华南地区桑园和荒地中,红火蚁固体食物组成均以昆虫纲动物为主;参与固体残片搬运觅食蚁的80%属于中型工蚁,搬运较大型固体残片的大型工蚁仅占5%;红火蚁工蚁嗉囊液体含有丰富的氨基酸和单糖。     

Crowding increases foraging efficiency in the leaf-cutting ant <Emphasis Type="Italic">Atta colombica</Emphasis>

Many animals, including humans, organize their foraging activity along well-defined trails. Because trails are cleared of obstacles, they minimize energy expenditure and allow fast travel. In social insects such as ants, trails might also promote social contacts and allow the exchange of information between workers about the characteristics of the food. When the trail traffic is heavy, however, traffic congestion occurs and the benefits of increased social contacts for the colony can be offset by a decrease of the locomotory rate of individuals. Using a small laboratory colony of the leaf-cutting ant Atta colombica cutting a mix of leaves and Parafilm, we compared how foraging changed when the width of the bridge between the nest and their foraging area changed. We found that the rate of ants crossing a 5 cm wide bridge was more than twice as great as the rate crossing a 0.5 cm bridge, but the rate of foragers returning with loads was less than half as great. Thus, with the wide bridge, the ants had about six times lower efficiency (loads returned per forager crossing the bridge). We conclude that crowding actually increased foraging efficiency, possibly because of increased communication between laden foragers returning to the nest and out-going ants. Received 15 December 2006; revised 16 February 2007; accepted 19 February 2007.     

Maintenance of foraging trails by the giant tropical antParaponera clavata (Insecta: Formicidae: Ponerinae)

Summary Establishment and maintenance of foraging trails to an artificial nectar source by ten colonies ofParaponera davata (Fabr.) in Panama is reported. The first forager to locate the artificial nectar source was responsible for recruiting additional foragers and for marking trails to orient these foragers. More than half of the trail marking was performed by the first two ants to mark the path back to the colony, although up to 11 ants per colony per hour marked trails. The number of trail marks and the number of marking ants decreased through time, presumably as foragers learned the location of the artificial nectar source. Four categories of recruits were noted: markers, foragers, patrollers, and visitors.     

Chemical trail systems,orientation, and territorial interactions in the antLasius neoniger

Foraging and territoriality in the ant Lasius neonigerinvolves a series of trails which channel foragers away from adjacent colonies. Experimental studies suggest that the trails are composed of colony-specific, persistent orientation components of hindgut material that accumulate on trails during foraging. A less durable component of the hindgut trail pheromone regulates recruitment. Foraging directionality and the use of a trail could be modified by experimentally arranging confrontations with conspecifics. The orientation of foragers is mediated by visual as well as chemical cues. Components of the foraging and territorial system of L. neonigerappear to include (1) a network of subnests which change in position seasonally within each polydomous nest; (2) a series of trails emanating from each subnest that adjusts search toward resource patches and away from aggressive, neighboring conspecifics; and (3) trail communication involving an ephemeral component of the hindgut trail pheromone that regulates the organization of cooperative prey retrieval and a more persistent component that serves as an orientation guide.     

Effect of Trail Bifurcation Asymmetry and Pheromone Presence or Absence on Trail Choice by Lasius niger Ants

During foraging, ant workers are known to make use of multiple information sources, such as private information (personal memory) and social information (trail pheromones). Environmental effects on foraging, and how these interact with other information sources, have, however, been little studied. One environmental effect is trail bifurcation asymmetry. Ants forage on branching trail networks and must often decide which branch to take at a junction (bifurcation). This is an important decision, as finding food sources relies on making the correct choices at bifurcations. Bifurcation angle may provide important information when making this choice. We used a Y‐maze with a pivoting 90° bifurcation to study trail choice of Lasius niger foragers at varying branch asymmetries (0°, [both branches 45° from straight ahead], 30° [branches at 30° and 60° from straight ahead], 45°, 60° and 90° [one branch straight ahead, the other at 90°]). The experiment was carried out either with equal amounts of trail pheromone on both branches of the bifurcation or with pheromone present on only one branch. Our results show that with equal pheromone, trail asymmetry has a significant effect on trail choice. Ants preferentially follow the branch deviating least from straight, and this effect increases as asymmetry increases (47% at 0°, 54% at 30°, 57% at 45°, 66% at 60° and 73% at 90°). However, when pheromone is only present on one branch, the graded effect of asymmetry disappears. Overall, however, there is an effect of asymmetry as the preference of ants for the pheromone‐marked branch over the unmarked branch is reduced from 65%, when it is the less deviating branch, to 53%, when it is the more deviating branch. These results demonstrate that trail asymmetry influences ant decision‐making at bifurcations and that this information interacts with trail pheromone presence in a non‐hierarchical manner.     

The Behavior of <Emphasis Type="Italic">Acromyrmex crassispinus</Emphasis> (Hymenoptera: Formicidae) on Trail Bifurcations and the Influence of Ant Flow on Error Rates of Nestbound Laden Workers

Ants are ordinarily faced with a succession of bifurcations along their foraging networks. Given that there is no directionality in pheromone trails, each bifurcation is potentially an opportunity for error in the trajectory of laden workers to the nest, which could entail considerable inefficiencies in the transportation of food to the colony. Leaf-cutting ants (Atta and Acromyrmex) commonly show intense traffic and complex foraging trail systems, which make them ideal organisms to study worker behavior in trail bifurcations. The behavior of leaf-cutting ants of the genus Acromyrmex in trail bifurcations is still largely unexplored. Thus, this study aimed to assess the behavior of Acromyrmex crassispinus workers on trail bifurcations and to investigate whether differences in ant flow on foraging trails influence the error rate of nestbound laden workers at trail bifurcation. There was a negative relationship between ant flow and error rate of nestbound laden workers. Most workers walked in the central part of the foraging trails but occupied a broader area of the foraging trail when the ant flow was high. The results of this study provide valuable insight into the organization of traffic flow in A. crassispinus and its impacts on the foraging strategy of the species.