Individual and collective problem-solving in a foraging context in the leaf-cutting ant Atta colombica

In this paper we investigate the flexibility of foraging behavior in the leaf-cutting ant Atta colombica, both at the individual and collective levels, following a change in the physical properties of their environment. We studied in laboratory conditions the changes occurring in foraging behavior when a height constraint was placed 1 cm above part of the trail linking the nest to the foraging area. We found that the size and shape of the fragments of foraging material brought back to the nest were significantly modified when the constraint was placed on the trail: independent of their size, forager ants cut smaller and rounder fragments in the presence of a height constraint than in its absence. This size adjustment does not require any direct sensory feedback because it occurred when the ants cut fragments in the foraging area; no further cutting was done when they encountered the constraint. This points to the existence of a template that ants store and use as a reference to adjust their reach while cutting. Remarkably, despite the decrease in the foraging material brought to the nest per capita the colony was still able to improve its foraging performance by doubling the number of transporters. This study illustrates the flexibility of foraging behavior exhibited by an ant colony. It provides a rare example of insects finding an intelligent solution to a problem occurring in a foraging context, at both the individual and collective levels.     

Idiosyncratic route-based memories in desert ants, Melophorus bagoti: how do they interact with path-integration vectors?

Individually foraging desert ants of central Australia, Melophorus bagoti, exhibit amazingly precise mechanisms of visual landmark guidance when navigating through cluttered environments. If trained to shuttle back and forth between the nest and a feeder, they establish habitual outbound and inbound routes, which guide them idiosyncratically across the natural maze of extended arrays of grass tussocks covering their foraging areas. The route-based memories that usually differ between outbound and inbound runs are acquired already during the first runs to the nest and feeder. If the ants are displaced sideways of their habitual routes, they can enter their stereotyped routes at any place and then follow these routes with the same accuracy as if they had started at the usual point of departure. Furthermore, the accuracy of maintaining a route does not depend on whether homebound ants have been captured at the feeder shortly before starting their home run and, hence, with their home vector still fully available (full-vector ants), or whether they have been captured at the nest after they had already completed their home run (zero-vector ants). Hence, individual landmark memories can be retrieved independently of the state of the path-integration vector with which they have been associated during the acquisition phase of learning. However, the ants display their path-integration vector when displaced from the feeder to unfamiliar territory.     

Visual discrimination,sequential learning and memory retrieval in the Australian desert ant <Emphasis Type="Italic">Melophorus bagoti</Emphasis>

Bees, wasps and ants—so-called central-place foragers—need potent homing strategies to return to their nest. Path integration and view-based landmark guidance are the key strategies for the ants’ navigation. For instance, they memorise different views in a sequence (sequential memory) but also have a step counter that informs them about the covered distance during each foraging trip (odometer). The sequential memory and the odometer information can act as contextual cues during travel for retrieving the appropriate stored view. When and which cue is used at different stages and lengths of the foraging trips is still unknown. In this study, we examined how the Australian desert ant Melophorus bagoti uses sequential memory and odometric information to retrieve visual memories. Using a set-up made out of channels and two-choice boxes (Y-mazes), we demonstrate first that M. bagoti foragers are able to learn and discriminate a variety of visual stimuli in a sequence of views along the inbound trip back to the nest. We then forced the homing ants to encounter a fixed sequence of two visual patterns during their inbound trips. By manipulating the position and distance of the visual stimuli and decision boxes, we could set the two contextual cues (sequential memory and odometer) into conflict. After the short 4-m outbound distance, a preference for odometric information as a contextual cue was found, but after the long 8-m outbound distance, ants relied primarily on their sequential memory retrieval. Odometer precision deteriorates with increasing travel distance, and accordingly, our findings imply that desert ants may be relying on the most reliable contextual cue for retrieving visual memories.     

Rapid spatial learning in a velvet ant (<Emphasis Type="Italic">Dasymutilla coccineohirta</Emphasis>)

Spatial learning has been examined in a variety of animals to determine what cues are used to navigate through a complex environment. A common feature of previously studied vertebrates and invertebrates is their need to return to a previously visited site for mating, nesting, foraging or predator avoidance. Velvet ants (Hymenoptera: Mutillidae) are cursorial parasitoids with flightless females that must walk through complex terrain to find ground dwelling host larvae burrows. Velvet ants are not central-place foragers (they do not return to an established nest site) so much of the previous work on spatial learning does not directly apply in this context. It was assumed that females primarily use chemosensory cues for navigation and burrow location instead of visual learning. This study, however, demonstrates that velvet ant females are able to use visual landmarks to find an inconspicuous exit in an aversion-motivation spatial learning task. A significant number of velvet ants learned to locate the exit after seven training trials and went to the previous location of the exit even after the maze had been rotated, showing that landmarks external to the maze were used to learn the escape location.     

Win-shift and win-stay learning in the short-beaked echidna (<Emphasis Type="Italic">Tachyglossus aculeatus</Emphasis>)

Numerous previous investigators have explained species differences in spatial memory performance in terms of differences in foraging ecology. In three experiments we attempted to extend these findings by examining the extent to which the spatial memory performance of echidnas (or "spiny anteaters") can be understood in terms of the spatio-temporal distribution of their prey (ants and termites). This is a species and a foraging situation that have not been examined in this way before. Echidnas were better able to learn to avoid a previously rewarding location (to "win-shift") than to learn to return to a previously rewarding location (to "win-stay"), at short retention intervals, but were unable to learn either of these strategies at retention intervals of 90 min. The short retention interval results support the ecological hypothesis, but the long retention interval results do not. Electronic Publication     

Are ants sensitive to the geometry of tunnel bifurcation?

The ability to orient and navigate in space is essential for all animals whose home range is organized around a central point. Because of their small home range compared to vertebrates, central place foraging insects such as ants have for a long time provided a choice model for the study of orientation mechanisms. In many ant species, the movement of individuals on their colony home range is achieved essentially collectively, on the chemical trails laid down by their nest mates. In the initial stage of food recruitment, these trails can cross each other and thus form a network of interconnected paths in which ants have to orient. Previous simulation studies have shown that ants can find the shortest path between their nest and a food source in such a network only if there is a bias in the branch they choose when they reach an asymmetrical bifurcation. In this paper, we studied the choice of ants when facing either a symmetrical or an asymmetrical bifurcation between two tunnels. Ants were tested either on their way to a food source or when coming back to their nest, and either in the presence or in the absence of a chemical trail. Overall, our results show that the choice of an ant at a tunnel bifurcation depends more on the presence/absence of a trail pheromone than on the geometry of the bifurcation itself.     

Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae)

Adult workers of some social insect species show dramatic behavioral changes as they pass through a sequence of task specializations. In the paper wasp, Polybia aequatorialis, female workers begin adult life within the nest tending brood, progress to maintaining and defending the nest exterior, and ultimately leave the nest to forage. The mushroom body (MB) calyx neuropil increases in volume as workers progress from in-nest to foraging tasks. In other social Hymenoptera (bees and ants), MB Kenyon cell dendrites, axons and synapses change with the transition to foraging, but these neuronal effects had not been studied in wasps. Furthermore, the on-nest worker of Polybia wasps, an intermediate task specialization not identified in bees or ants, provides the opportunity to study pre-foraging worker class transitions. We asked whether Kenyon cell dendritic arborization varies with the task specialization of Polybia workers observed in the field near Monteverde, Costa Rica. Golgi-impregnated arbors in the lip and collar calyces, which receive a predominance of olfactory and visual input, respectively, were quantified using Sholl’s concentric circles and a novel application of virtual spherical probes. Arbors of the lip varied in a manner reminiscent of honeybees, with foragers having the largest and in-nest workers having the smallest arbors. In contrast, arbors of the collar were largest in foragers but smallest in on-nest workers. Thus, progression through task specializations in P. aequatorialis involves subregion specific dendritic growth and regression in the MB neuropil. These results may reflect the sensitivity of Kenyon cell dendritic structure to specialization dependent social and sensory experience.     

Aggression in wood ants (Formica polyctena Foerst., Hymenoptera,Formicidae)

The relationship between aggression and predation was surveyed in Red wood ants, in the field as well as under laboratory conditions. Aggression between wood ant nests is highest in early spring, and many wood ant wars break out then. The end of these wars coincides with a strong increase in prey density. Since the casualties are taken as food to the warring nests, a hypothesis is formulated that warfare between wood ant nests only occurs in periods when prey demand exceeds the supply. Protein-rich food in early spring is mainly for the benefit of the queens and the sexual larvae. Although the most obvious function of warfare is the defence of a foraging area, the main function may be the advancement of the mating flight dates of the queens in order to make the chance of propagating their genes greatest.     

Not using the obvious: desert ants, Melophorus bagoti, learn local vectors but not beacons in an arena

Many ant species travel large distances to find food, sometimes covering distances that are up to one million times their body length. Even when these foraging trips follow convoluted paths, the ants usually find their way back to their nest with precision (Wehner et al. in J Exp Biol 199:129–140, 1996). Ants have been shown to use both compass cues in the sky (pattern of polarised light) and landmarks on Earth to return to their nest. We present two experiments conducted on a solitary foraging ant: Melophorus bagoti in their natural habitat in the central Australian desert. Ants were trained and tested in situ. We tested foragers’ ability to exit a circular arena which provided an undifferentiated panorama. Artificial visual landmarks were located near a small exit. On tests in which path integration information was not available, foragers did not use artificial landmarks as beacons. Instead, they oriented in the learned exit direction, whether or not it pointed to the nest. We suggest that M. bagoti foragers learned a context-specific local vector when cued by the context of the circular arena. Our findings present the first evidence that M. bagoti foragers learn context-specific compass directions to chart their initial path home.     

Female degus (Octodon degus) monitor their environment while foraging socially

Vigilance or scanning involves interruptions in foraging behavior when individuals lift their heads and conduct visual monitoring of the environment. Theoretical considerations assume that foraging with the "head down", and scanning ("head up") are mutually exclusive activities, such that foraging precludes vigilance. We tested this generalization in a socially foraging, small mammal model, the diurnal Chilean degu (Octodon degus). We studied spontaneous bouts of scanning of captive degus when foraging in pairs of female sibs and non-sibs. We examined the extent to which foraging (head down postures) and scanning (head up postures) were mutually exclusive in subjects exposed to none, partial, and complete lateral visual obstruction of their partners. In addition, we monitored the orientation of their bodies to examine the target of attention while foraging and scanning. Lastly, we examined the temporal occurrence of scanning events to assess the extent of scanning coordination, and whether this coordination is kin-biased. Visual obstruction had a significant influence on degu vigilance. Focal degus increased their quadrupedal and semi-erect scanning when foraging under a partially obstructed view of their partners. Degus oriented their bodies toward partners when foraging and scanning. Despite this, degus did not coordinate scanning bouts; instead, they scanned independently from one another. Relatedness among cage mates did not influence any aspect of degu behavior. Contrary to theoretical expectations, these results indicate that foraging and vigilance are not mutually exclusive, and that kinship per se does not influence scanning behavior and coordination.     

Risk-sensitive foraging theory and operant psychology.

Hastjarjo, Silberberg, and Hursh (1990) have presented data on the foraging behavior of rats and discussed it in terms of risk-sensitive foraging theory. Because risk-sensitive foraging theory is comprised of several different models, it does not lead to general predictions about when an organism should prefer a foraging option with high variance to a foraging option with low variance. Any comparison of data with the predictions of the theory must be based on an appropriate model. I draw attention to various experiments that are potentially relevant to the results reported by Hastjarjo et al. and show how the time period over which the organism must survive can influence a model's predictions about risk sensitivity.     

Decision ecology: Foraging and the ecology of animal decision making

In this article, I review the approach taken by behavioral ecologists to the study of animal foraging behavior and explore connections with general analyses of decision making. I use the example of patch exploitation decisions in this article in order to develop several key points about the properties of naturally occurring foraging decisions. First, I argue that experimental preparations based on binary, mutually exclusive choice are not good models of foraging decisions. Instead, foraging choices have a sequential foreground-background structure, in which one option is in the background of all other options. Second, behavioral ecologists view foraging as a hierarchy of decisions that range from habitat selection to food choice. Finally, data suggest that foraging animals are sensitive to several important trade-offs. These trade-offs include the effects of competitors and group mates, as well as the problem of predator avoidance.     

Re-evaluating the extractive foraging hypothesis

In his seminal 1992 paper, Dunbar examined three hypotheses advanced to explain primate intelligence, arguing that whereas his social group size hypothesis was supported, neither of two ecological hypotheses, the extractive foraging and frugivory hypotheses, were supported. Following this, and Dunbar's subsequently elaborated argument, many investigators concluded that primate intelligence arose as social rather than ecological adaptations. This paper questions Dunbar's characterization of extractive foraging and social intelligence as alternative hypotheses, raises sampling issues about Dunbar's brain data, species choice, and measurement of extractive foraging. It summarizes the extractive foraging hypothesis, and counters its critics. It reexamines the hypothesis in light of recent behavioral and brain data, new methodology for quantifying extractive foraging, and a new phylogeny of primate intelligence. It concludes that the extractive foraging hypothesis is now supported by several converging lines of evidence.     

Honeybee methodology, cognition, and theory: recording local directional decisions in interpatch foraging and interpreting their theoretical relevance

Investigations made into the cognitive decision making of honeybees (Apis mellifera) traveling from one flower patch to another flower patch (interpatch foraging) are few. To facilitate such research, we present methods to artificially emulate interpatch foraging and quantify the immediate decision making of honeybees (within 50 cm) choosing to fly an interpatch path. These “Interpatch Methods” are validated, applied, and shown to produce novel information for the field of honeybee spatial cognition. Generally, we demonstrate that a single foraging cohort of honeybees is shown to be capable of making decisions based upon different sets of learned cues, in the exact same context. Specifically, both terminal beacon orientation cues and compass navigation cues can guide the cognitive decision making of interpatch foraging honeybees; our bees chose both cues equally. Finally, the theoretical importance of decision making for interpatch paths is compared with the other foraging paths (outward and homing) with respect to the information available to recruited foragers and scout foragers. We conclude that the ability to analyze interpatch foraging is critical for a more complete understanding of honeybee foraging cognition and that our methods are capable of providing that understanding.     

Honeybee Memory: Navigation by Associative Grouping and Recall of Visual Stimuli

Studies of navigation in bees and ants are beginning to reveal that foraging insects traveling repeatedly to a food source navigate by using a series of visual images of the environment acquired en route (Collett, 1996; Collett et al., 1993; Judd & Collett, 1998; Wehner et al., 1990, 1996). By comparing the currently viewed scene with the appropriate stored image, the insect is able to ascertain whether or not it is on the correct path and make any necessary corrections. If a bee happens to forage at more than one site, then she needs not only to memorize a separate set of images for each route that she has learned but also to retrieve the set of images that is appropriate to each route. Here we examine the bee's capacity to learn and later retrieve from memory two different sets of visual stimuli. Bees were trained to fly through a compound Y-maze where they were presented alternately with two different sequences of visual stimuli on their route to a food reward. We find that bees can indeed store two different sequences of images simultaneously. Furthermore, the trained bees are able to classify the memorized images into two groups, one pertaining to each three-stimulus set. Exposure to any of the images pertaining to one set triggers recall of all of the other images associated with that set. Associative grouping and recall of visual stimuli, demonstrated here for the first time in honeybees, provide an effective means of retrieving the appropriate navigational information from memory.     

Common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>) do not utilize social information in three simultaneous social foraging tasks

Social foraging is suggested to increase foraging efficiency, as individuals might benefit from public information acquired by monitoring the foraging activities of other group members. We conducted a series experiments with captive common marmosets (Callithrix jacchus) to investigate to what extent marmosets utilize social information about food location when foraging simultaneously with conspecifics. Subjects were confronted with dominant and subordinate demonstrators in three experiments which differed in the amount of information about food location available to the demonstrators. In all three experiments, the focal subjects’ performance in the social condition was not enhanced in comparison to a non-social control condition. Because we could rule out kleptoparasitism and aggressive displacements as explanations, we argue that the subjects’ tendency for scramble competition by avoiding others and dispersing over the foraging area seems to inhibit or mask the acquisition of social information about the location of rewarded patches.     

Spatial working memory for clustered and linear configurations of sites in a virtual reality foraging task

Two experiments using an immersive virtual reality foraging environment determined the spatial strategies spontaneously deployed by people in a foraging task and the effects on immediate serial recall of trajectories though the foraging space, which could conform or violate specific organisational constraints. People benefitted from the use of organised search patterns when attempting to monitor their travel though either a clustered "patchy" space or a matrix of locations. The results are discussed within a comparative framework.     

Dorsal anterior cingulate and ventromedial prefrontal cortex have inverse roles in both foraging and economic choice

Recent research has highlighted a distinction between sequential foraging choices and traditional economic choices between simultaneously presented options. This was partly motivated by observations in Kolling, Behrens, Mars, and Rushworth, Science, 336(6077), 95–98 (2012) (hereafter, KBMR) that these choice types are subserved by different circuits, with dorsal anterior cingulate (dACC) preferentially involved in foraging and ventromedial prefrontal cortex (vmPFC) preferentially involved in economic choice. To support this account, KBMR used fMRI to scan human subjects making either a foraging choice (between exploiting a current offer or swapping for potentially better rewards) or an economic choice (between two reward-probability pairs). This study found that dACC better tracked values pertaining to foraging, whereas vmPFC better tracked values pertaining to economic choice. We recently showed that dACC’s role in these foraging choices is better described by the difficulty of choosing than by foraging value, when correcting for choice biases and testing a sufficiently broad set of foraging values (Shenhav, Straccia, Cohen, & Botvinick Nature Neuroscience, 17(9), 1249–1254, 2014). Here, we extend these findings in 3 ways. First, we replicate our original finding with a larger sample and a task modified to address remaining methodological gaps between our previous experiments and that of KBMR. Second, we show that dACC activity is best accounted for by choice difficulty alone (rather than in combination with foraging value) during both foraging and economic choices. Third, we show that patterns of vmPFC activity, inverted relative to dACC, also suggest a common function across both choice types. Overall, we conclude that both regions are similarly engaged by foraging-like and economic choice.     

Foraging for brain stimulation: toward a neurobiology of computation

The self-stimulating rat performs foraging tasks mediated by simple computations that use interreward intervals and subjective reward magnitudes to determine stay durations. This is a simplified preparation in which to study the neurobiology of the elementary computational operations that make cognition possible, because the neural signal specifying the value of a computationally relevant variable is produced by direct electrical stimulation of a neural pathway. Newly developed measurement methods yield functions relating the subjective reward magnitude to the parameters of the neural signal. These measurements also show that the decision process that governs foraging behavior divides the subjective reward magnitude by the most recent interreward interval to determine the preferability of an option (a foraging patch). The decision process sets the parameters that determine stay durations (durations of visits to foraging patches) so that the ratios of the stay durations match the ratios of the preferabilities.     

Evidence of teaching in atlantic spotted dolphins (Stenella frontalis) by mother dolphins foraging in the presence of their calves

Teaching is a powerful form of social learning, but there is little systematic evidence that it occurs in species other than humans. Using long-term video archives the foraging behaviors by mother Atlantic spotted dolphins (Stenella frontalis) were observed when their calves were present and when their calves were not present, including in the presence of non-calf conspecifics. The nine mothers we observed chased prey significantly longer and made significantly more referential body-orienting movements in the direction of the prey during foraging events when their calves were present than when their calves were not present, regardless of whether they were foraging alone or with another non-calf dolphin. Although further research into the potential consequences for the naïve calves is still warranted, these data based on the maternal foraging behavior are suggestive of teaching as a social-learning mechanism in nonhuman animals.