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.     

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.     

Object-goal positioning influences spatial representation in rats

Three tests investigated how the geometric relation between object/landmarks and goals influenced spatial choice behavior in rats. Two groups searched for hidden food in an object-filled circular arena containing 24 small poles. For the “Proximal” group, four distinct objects in a square configuration were placed close to four baited poles. For the “Distal” group, the identical configuration of objects was rotated 45° relative to the poles containing the hidden food. The Proximal group learned to locate the baited poles more quickly than the Distal group. Tests with removed and rearranged landmarks indicated that the two groups learned to use the objects differently. The results suggested that close proximity of objects to goals encouraged their use as beacons, while greater distance of objects from goals resulted in the global encoding of the geometric properties of the arena and the use of the objects as landmarks. Received: 22 June 1998 / Accepted after revision: 23 January 1999     

Sampling and decision rules used by honey bees in a foraging arena

Animals must continuously choose among various available options to exploit the most profitable resource. They also need to keep themselves updated about the values of all available options, since their relative values can change quickly due to depletion or exploitation by competitors. While the sampling and decision rules by which foragers profitably exploit a flower patch have attracted a great deal of attention in theory and experiments with bumble bees, similar rules for honey bee foragers, which face similar foraging challenges, are not as well studied. By presenting foragers of the honey bee Apis cerana with choice tests in a foraging arena and recording their behavior, we investigate possible sampling and decision rules that the foragers use to choose one option over another and to track other options. We show that a large part of the sampling and decision-making process of a foraging honey bee can be explained by decomposing the choice behavior into dichotomous decision points and incorporating the cost of sampling. The results suggest that a honey bee forager, by using a few simple rules as part of a Bayesian inference process, is able to effectively deal with the complex task of successfully exploiting foraging patches that consist of dynamic and multiple options.     

Humans do not switch between path knowledge and landmarks when learning a new environment

Using a metric shortcut paradigm, we have found that like honeybees (Dyer in Animal Behaviour 41:239–246, 1991), humans do not seem to build a metric “cognitive map” from path integration. Instead, observers take novel shortcuts based on visual landmarks whenever they are available and reliable (Foo, Warren, Duchon, & Tarr in Journal of Experimental Psychology-Learning Memory and Cognition 31(2):195–215, 2005). In the present experiment we examine whether humans, like ants (Wolf & Wehner in Journal of Experimental Biology 203:857–868, 2000), first use survey-type path knowledge, built up from path integration, and then subsequently shift to reliance on landmarks. In our study participants walked in an immersive virtual environment while head position and orientation were recorded. During training, participants learned two legs of a triangle with feedback: paths from Home to Red and Home to Blue. A configuration of colored posts surrounded the Red location. To test reliance on landmarks, these posts were covertly translated, rotated, or left unchanged during six probe trials. These probe trials were interspersed during the training procedure to measure changes over learning. Dependence on visual landmarks was immediate and sustained during training, and no significant learning effects were observed other than a decrease in hesitation time. Our results suggest that while humans have at least two distinct navigational strategies available to them, unlike ants, a computationally-simpler landmark strategy dominates during novel shortcut navigation.     

Mental maps in chacma baboons (<Emphasis Type="Italic">Papio ursinus</Emphasis>): using inter-group encounters as a natural experiment

Encounters between groups of wild chacma baboons (Papio ursinus) can be viewed as a natural experiment to investigate the nature of these primates’ mental representations of large-scale space. During a 16-month field study in a high population density habitat we recorded the foraging routes and the most important resources of a group of 25 individuals. Also, we estimated the locations of additional baboon groups relative to the study group. Routes were less linear, travel speed was higher, and inter-resource distances were larger when other groups were present within 500 m of the focal group; thus, the study group avoided others by taking detours. We predicted that evasive manoeuvres would be characteristic of different possible orientation mechanisms, and compared them with our observations. We analysed 34 evasive manoeuvres in detail. In an area that lacked prominent landmarks, detours were small; larger detours occurred when resources were directly visible, or in the vicinity of a hill offering conspicuous landmarks. In areas without prominent landmarks, detours were along familiar routes and waiting bouts of up to 60 min occurred; on one occasion the study group aborted their entire day’s journey. We discuss these findings in the light of time and energy costs and suggest that the baboons lack the ability to compute Euclidean relations among locations, but use network maps to find their way to out-of-sight locations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007a).     

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.     

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.     

Evidence against integration of spatial maps in humans: generality across real and virtual environments

A real-world open-field search task was implemented with humans as an analogue of Blaisdell and Cook’s (Anim Cogn 8:7–16, 2005) pigeon foraging task and Sturz, Bodily, and Katz’s (Anim Cogn 9:207–217, 2006) human virtual foraging task to 1) determine whether humans were capable of integrating independently learned spatial maps and 2) make explicit comparisons of mechanisms used by humans to navigate real and virtual environments. Participants searched for a hidden goal located in one of 16 bins arranged in a 4 × 4 grid. In Phase 1, the goal was hidden between two landmarks (blue T and red L). In Phase 2, the goal was hidden to the left and in front of a single landmark (blue T). Following training, goal-absent trials were conducted in which the red L from Phase 1 was presented alone. Bin choices during goal-absent trials assessed participants’ strategies: association (from Phase 1), generalization (from Phase 2), or integration (combination of Phase 1 and 2). Results were inconsistent with those obtained with pigeons but were consistent with those obtained with humans in a virtual environment. Specifically, during testing, participants did not integrate independently learned spatial maps but used a generalization strategy followed by a shift in search behavior away from the test landmark. These results were confirmed by a control condition in which a novel landmark was presented during testing. Results are consistent with the bulk of recent findings suggesting the use of alternative navigational strategies to cognitive mapping. Results also add to a growing body of literature suggesting that virtual environment approaches to the study of spatial learning and memory have external validity and that spatial mechanisms used by human participants in navigating virtual environments are similar to those used in navigating real-world environments.     

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.     

Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications

Many wild primates occupy large home ranges and travel long distances each day. Navigating these ranges to find sufficient food presents a substantial cognitive challenge, but we are still far from understanding either how primates represent spatial information mentally or how they use this information to navigate under natural conditions. In the course of a long-term socioecological study, we investigated and compared the travel paths of sympatric spider monkeys (Ateles belzebuth) and woolly monkeys (Lagothrix poeppigii) in Amazonian Ecuador. During several field seasons spanning an 8-year period, we followed focal individuals or groups of both species continuously for periods of multiple days and mapped their travel paths in detail. We found that both primates typically traveled through their home ranges following repeatedly used paths, or “routes”. Many of these routes were common to both species and were stable across study years. Several important routes appeared to be associated with distinct topographic features (e.g., ridgetops), which may constitute easily recognized landmarks useful for spatial navigation. The majority of all location records for both species fell along or near identified routes, as did most of the trees used for fruit feeding. Our results provide strong support for the idea that both woolly and spider monkey use route-based mental maps similar to those proposed by Poucet (Psychol Rev 100:163–182, 1993). We suggest that rather than remembering the specific locations of thousands of individual feeding trees and their phenological schedules, spider and woolly monkeys could nonetheless forage efficiently by committing to memory a series of route segments that, when followed, bring them into contact with many potential feeding sources for monitoring or visitation. Furthermore, because swallowed and defecated seeds are deposited in greater frequency along routes, the repeated use of particular travel paths over generations could profoundly influence the structure and composition of tropical forests, raising the intriguing possibility that these and other primate frugivores are active participants in constructing their own ecological niches. Building upon the insights of Byrne (Q J Exp Psychol 31:147–154, 1979, Normality and pathology in cognitive functions. Academic, London, pp 239–264, 1982) and Milton (The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York, 1980, On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 375–417, 2000), our results highlight the likely general importance of route-based travel in the memory and foraging strategies of nonhuman primates.

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This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Multiple landmarks, the encoding of environmental geometry and the spatial logics of a dual brain

A series of place learning experiments was carried out in young chicks (Gallus gallus) in order to investigate how the geometry of a landmark array and that of a walled enclosure compete when disoriented animals could rely on both of them to re-orient towards the centre of the enclosure. A square-shaped array (four wooden sticks) was placed in the middle of a square-shaped enclosure, the two structures being concentric. Chicks were trained to ground-scratch to search for food hidden in the centre of the enclosure (and the array). To check for effects of array degradation, one, two, three or all landmarks were removed during test trials. Chicks concentrated their searching activity in the central area of the enclosure, but their accuracy was inversely contingent on the number of landmarks removed; moreover, the landmarks still present within the enclosure appeared to influence the shape of the searching patterns. The reduction in the number of landmarks affected the searching strategy of chicks, suggesting that they had focussed mainly on local cues when landmarks were present within the enclosure. When all the landmarks were removed, chicks searched over a larger area, suggesting an absolute encoding of distances from the local cues and less reliance on the relationships provided by the geometry of the enclosure. Under conditions of monocular vision, chicks tended to rely on different strategies to localize the centre on the basis of the eye (and thus the hemisphere) in use, the left hemisphere attending to details of the environment and the right hemisphere attending to the global shape.This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).     

Place navigation in mammals: a configuration-based model

Recent water maze experiments suggest that rats performing place navigation primarily use the geometric information provided by a set of landmarks, and neglect the featural information provided by the identities of the landmarks. Here, I develop a model that explains how an animal may perform place navigation by relying only on geometric information. The core of the model is the representation of places as panoramas defined by circular bar-codes embodying the relative bearings and apparent sizes of the landmarks, irrespective of their identities. There are two stages in the model. During the first stage, the animal freely explores its environment in order to acquire spatial information at the local level. During the second stage, the animal uses the information previously memorized to perform place navigation towards the goal it intends to reach. The possible role of two brain areas in place navigation is discussed within this framework. Beyond their primary role in landmark-based representations of places, hippocampal place cells may be involved in computing the current distances to the landmarks. Beyond their primary role in landmark-based representations of headings, post-subicular head-direction cells may be involved in computing the “compass bearings” of the landmarks. Received: 17 January 1998 / Accepted after revision: 19 April 1998     

Harbour seals (<Emphasis Type="Italic">Phoca vitulina</Emphasis>) can steer by the stars

Offshore orientation in marine mammals is still a mystery. For visual orientation during night-time foraging and travelling in the open seas, seals cannot rely on distant terrestrial landmarks, and thus might use celestial cues as repeatedly shown for nocturnally migrating birds. Although seals detect enough stars to probably allow for astronavigation, it was unclear whether they can orient by the night sky. The widely accepted cognitive mechanism for bird night-time orientation by celestial cues is a time-independent star compass with learned geometrical star configurations used to pinpoint north as the rotational centre of the starry sky while there is no conclusive evidence for a time-compensated star compass or true star navigation. Here, we present results for two harbour seals orienting in a custom made swimming planetarium. Both seals learned to highly accurately identify a lodestar out of a pseudo-randomly oriented, realistic projection of the northern hemisphere night sky. Providing the first evidence for star orientation capability in a marine mammal, our seals’ outstanding directional precision would allow them to steer by following lodestars of learned star courses, a celestial orientation mechanism that has been known to be used by Polynesian navigators but has not been considered for animals yet.     

Exploration Is Sufficient but Not Necessary for Navigation with Landmarks in the House Mouse (Mus musculus)

Exploration is a locomotor and scanning behavior accompanied by the acquisition of information that can be used for topographic orientation and homing. Our experiments demonstrate that the exploring house mouse (Mus musculus) learns the use of distal landmarks for short-range homing. However, mice that had no exploratory experience at all also learned how to use distal landmarks for homing while shuttling between two goals. In addition, exploration-based knowledge in itself appears to be weak or provisional. Whereas one straight line path integration is strong enough to override orientation by distal landmarks based on 1 day of exploration, prolonged straight line shuttling results in navigation by distal landmarks that is strong enough to override path integration based on prolonged straight line shuttling. We conclude that exploratory behavior by itself is sufficient, but not necessary, for learning the use of distal landmarks for navigation within the home range.     

Strategies in landmark use by children, adults, and marmoset monkeys

Common marmosets (Callithrix jacchus jacchus), human children, and human adults learned to find a goal that was located in the center of a square array of four identical landmarks. The location of the landmark array and corresponding goal varied across trials, so the task could not be solved without using the landmark array. In Experiment 1, a matrix of discrete goal locations was presented and the landmarks surrounded and were adjacent to the correct location during training. After training, an expansion test was given in which the distance between landmarks was increased. Marmosets, children (ages 5–9), and adults all readily learned to use the landmarks to search accurately during training. On the expansion test, adults uniformly searched in the center of the array. Monkeys and children concentrated their searching near the landmarks rather than in the center. The monkeys, but not the children, searched more often on the directionally appropriate side of the landmarks than on other sides of the landmarks. In Experiment 2, children (ages 3–5) were trained with a continuous search space and with the goal farther from the landmarks so that a beaconing strategy rule could not be used. Several of the children failed to acquire the training task. Of those who learned to find the goal, three searched in the middle on expansion tests but most searched nearer to the landmarks. The “middle rule” strategy that is uniformly used by adult humans does not appear to be a preferred strategy for children or non-human primates.     

Integrating information about location and value of resources by white-faced saki monkeys (<Emphasis Type="Italic">Pithecia pithecia</Emphasis>)

Most studies of spatial memory in primates focus on species that inhabit large home ranges and have dispersed, patchy resources. Researchers assume that primates use memory to minimize distances traveled between resources. We investigated the use of spatial memory in a group of six white-faced sakis (Pithecia pithecia) on 12.8-ha Round Island, Guri Lake, Venezuela during a period of fruit abundance. The sakis’ movements were analyzed with logistic regressions, a predictive computer model and a computer model that simulates movements. We considered all the resources available to the sakis and compared observed distances to predicted distances from a computer model for foragers who know nothing about the location of resources. Surprisingly, the observed distances were four times greater than the predicted distances, suggesting that the sakis passed by a majority of the available fruit trees without feeding. The odds of visiting a food tree, however, were significantly increased if the tree had been visited in the previous 3 days and had more than 100 fruit. The sakis’ preferred resources were highly productive fruit trees, Capparis trees, and trees with water holes. They traveled efficiently to these sites. The sakis choice of feeding sites indicate that they combined knowledge acquired by repeatedly traveling through their home range with ‘what’ and ‘where’ information gained from individual visits to resources. Although the sakis’ foraging choices increased the distance they traveled overall, choosing more valued sites allowed the group to minimize intragroup feeding competition, maintain intergroup dominance over important resources, and monitor the state of resources throughout their home range. The sakis’ foraging decisions appear to have used spatial memory, elements of episodic-like memory and social and nutritional considerations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Carbon dioxide narcosis modifies the patch leaving decision of foraging parasitoids

Gleaning information is a way for foragers to adjust their behavior in order to maximize their fitness. Information decreases the uncertainty about the environment and could help foragers to accurately estimate environmental characteristics. In a patchy resource, information sampled during previous patch visits is efficient only if it is retained in the memory and retrieved upon arrival in a new patch. In this study, we tested whether the braconid Asobara tabida, a parasitoid of Drosophila larvae, retains information gleaned on patch quality in the memory and adjusts its foraging behavior accordingly. Females were anesthetized with CO₂ after leaving a first patch containing a different number of hosts and were allowed to visit a second patch containing only kairomones. CO₂ is known to erase unconsolidated information from the memory. We show that in the absence of a short CO₂ narcosis, females responded according to their previous experience, whereas anesthetized females did not. The anesthetized females stayed a given time in the second patch irrespective of what they encountered before. CO₂ narcosis had no effect on the residence time of the non-experienced females in a patch containing hosts or only kairomones in comparison with the non-anesthetized females that had a previous foraging experience. We conclude that CO₂ narcosis erases the effect of the previous patch quality, perhaps due to a memory disruption. Direct information processing is likely to be involved in parasitoid decision making through retention of the information on the previous patch quality into a CO₂ sensitive memory.     

Evidence against integration of spatial maps in humans

A dynamic 3-D virtual environment was constructed for humans as an open-field analogue of Blaisdell and Cook's (2005) pigeon foraging task to determine if humans, like pigeons, were capable of integrating separate spatial maps. Participants used keyboard keys and a mouse to search for a hidden goal in a 4×4 grid of raised cups. During Phase 1 training, a goal was consistently located between two landmarks (Map 1: blue T and red L). During Phase 2 training, a goal was consistently located down and left of a single landmark (Map 2: blue T). Transfer trials were then conducted in which participants were required to make choices in the presence of the red L alone. Cup choices during transfer assessed participants’ strategies: association (from Map 1), generalization (from Map 2), or integration (combining Map 1 and 2). During transfer, cup choices increased to a location which suggested an integration strategy and was consistent with results obtained with pigeons. However, additional analyses of the human data suggested participants initially used a generalization strategy followed by a progressive shift in search behavior away from the red L. This shift in search behavior during transfer was responsible for the changes in cup choices across transfer trials and was confirmed by a control condition. These new analyses offer an alternative explanation to the spatial integration account proposed for pigeons.Electronic Supplementary Material Supplementary material is available for this article at