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.     

A neural network model of foraging decisions made under predation risk

This article develops the cognitive—emotional forager (CEF) model, a novel application of a neural network to dynamical processes in foraging behavior. The CEF is based on a neural network known as the gated dipole, introduced by Grossberg, which is capable of representing short-term affective reactions in a manner similar to Solomon and Corbit’s (1974) opponent process theory. The model incorporates a trade-off between approach toward food and avoidance of predation under varying levels of motivation induced by hunger. The results of simulations in a simple patch selection paradigm, using a lifetime fitness criterion for comparison, indicate that the CEF model is capable of nearly optimal foraging and outperforms a run-of-luck rule-of-thumb model. Models such as the one presented here can illuminate the underlying cognitive and motivational components of animal decision making.     

Interpatch foraging in honeybees—rational decision making at secondary hubs based upon time and motivation

For honeybees, Apis mellifera, the hive has been well known to function as a primary decision-making hub, a place from which foragers decide among various directions, distances, and times of day to forage efficiently. Whether foraging honeybees can make similarly complex navigational decisions from locations away from the hive is unknown. To examine whether or not such secondary decision-making hubs exist, we trained bees to forage at four different locations. Specifically, we trained honeybees to first forage to a distal site “CT” 100?m away from the hive; if food was present, they fed and then chose to go home. If food was not present, the honeybees were trained to forage to three auxiliary sites, each at a different time of the day: A in the morning, B at noon, and C in the afternoon. The foragers learned to check site CT for food first and then efficiently depart to the correct location based upon the time of day if there was no food at site CT. Thus, the honeybees were able to cognitively map motivation, time, and five different locations (Hive, CT, A, B, and C) in two spatial dimensions; these are the contents of the cognitive map used by the honeybees here. While at site CT, we verified that the honeybees could choose between 4 different directions (to A, B, C, and the Hive) and thus label it as a secondary decision-making hub. The observed decision making uncovered here is inferred to constitute genuine logical operations, involving a branched structure, based upon the premises of motivational state, and spatiotemporal knowledge.     

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.     

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.     

Fishing for the right words: decision rules for human foraging behavior in internal search tasks

Animals depleting one patch of resources must decide when to leave and switch to a fresh patch. Foraging theory has predicted various decision mechanisms; which is best depends on environmental variation in patch quality. Previously we tested whether these mechanisms underlie human decision making when foraging for external resources; here we test whether humans behave similarly in a cognitive task seeking internally generated solutions. Subjects searched for meaningful words made from random letter sequences, and as their success rate declined, they could opt to switch to a fresh sequence. As in the external foraging context, time since the previous success and the interval preceding it had a major influence on when subjects switched. Subjects also used the commonness of sequence letters as a proximal cue to patch quality that influenced when to switch. Contrary to optimality predictions, switching decisions were independent of whether sequences differed little or widely in quality.     

How to measure patch encounter rate: decision-making mechanisms in the parasitic wasp <Emphasis Type="Italic">Asobara tabida</Emphasis>

Parasitic wasps are faced with the decision of where and for how long to search for hosts. Their leaving decisions depend on the rate at which new host-containing patches are encountered: parasitoids increase foraging efficiency by leaving earlier when patch encounter rates become higher. The mechanisms by which these often tiny insects can assess patch encounter rates have not been thoroughly investigated so far. The aim of the present study, where females of the braconid wasp Asobara tabida encountered patches after varying time intervals, was to measure the shape of the travel–time response curve and to analyse how information on inter-patch distances is translated into foraging behaviour. I examined several proxies for travel-time duration, like those of physiological nature as egg content, cues of senescence, amount of energy spent, or muscle fatigue, as well as true cognitive mechanisms, like measurement of distance or interval timing. Constraints in the wasp’s ability to detect patch borders accurately after travelling, e.g. habituation to the patch odour or receptor blocking, are also discussed. From the data presented, most of the above-mentioned mechanisms and constraints can be rejected to work for A. tabida. The effects of inter-patch travel time are strongest when they are short, and even though it cannot be excluded that time measures are processed using an internal clock, I suggest that a Bayesian-like mechanism of timing, the biological basis of which might involve the build-up of neurosecretory material, is the most likely candidate influencing leaving decisions in A. tabida.     

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.     

GROUP FORAGING SENSITIVITY TO PREDICTABLE AND UNPREDICTABLE CHANGES IN FOOD DISTRIBUTION: PAST EXPERIENCE OR PRESENT CIRCUMSTANCES?

The ideal free distribution theory (Fretwell & Lucas, 1970) predicts that the ratio of foragers at two patches will equal the ratio of food resources obtained at the two patches. The theory assumes that foragers have "perfect knowledge" of patch profitability and that patch choice maximizes fitness. How foragers assess patch profitability has been debated extensively. One assessment strategy may be the use of past experience with a patch. Under stable environmental conditions, this strategy enhances fitness. However, in a highly unpredictable environment, past experience may provide inaccurate information about current conditions. Thus, in a nonstable environment, a strategy that allows rapid adjustment to present circumstances may be more beneficial. Evidence for this type of strategy has been found in individual choice. In the present experiments, a flock of pigeons foraged at two patches for food items and demonstrated results similar to those found in individual choice. Experiment 1 utilized predictable and unpredictable sequences of resource ratios presented across days or within a single session. Current foraging decisions depended on past experience, but that dependence diminished when the current foraging environment became more unpredictable. Experiment 2 repeated Experiment I with a different flock of pigeons under more controlled circumstances in an indoor coop and produced similar results.     

A socioecological perspective on primate cognition,past and present

The papers in this special issue examine the relationship between social and ecological cognition in primates. We refer to the intersection of these two domains as socioecological cognition. Examples of socioecological cognition include socially learned predator alarm calls and socially sensitive foraging decisions. In this review we consider how primate cognition may have been shaped by the interaction of social and ecological influences in their evolutionary history. The ability to remember distant, out-of-sight locations is an ancient one, shared by many mammals and widespread among primates. It seems some monkeys and apes have evolved the ability to form more complex representations of resources, integrating “what-where-how much” information. This ability allowed anthropoids to live in larger, more cohesive groups by minimizing competition for limited resources between group members. As group size increased, however, competition for resources also increased, selecting for enhanced social skills. Enhanced social skills in turn made a more sophisticated relationship to the environment possible. The interaction of social and ecological influences created a spiraling effect in the evolution of primate intelligence. In contrast, lemurs may not have evolved the ability to form complex representations which would allow them to consider the size and location of resources. This lack in lemur ecological cognition may restrict the size of frugivorous lemur social groups, thereby limiting the complexity of lemur social life. In this special issue, we have brought together two review papers, five field studies, and one laboratory study to investigate the interaction of social and ecological factors in relation to foraging. Our goal is to stimulate research that considers social and ecological factors acting together on cognitive evolution, rather than in isolation. Cross fertilization of experimental and observational studies from captivity and the field is important for increasing our understanding of this relationship. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition”.     

Time horizons in rats foraging for food in temporally separated patches

An important tenet of optimal foraging theory is that foragers compare prey densities in alternative patches to determine an optimal distribution of foraging behavior over time. A critical question is over what time period (time horizon) this integration of information and behavior occurs. Recent research has indicated that rats do not compare food density in a depleting patch with that in a rich patch delayed by an hour or more (Timberlake, 1984). In the present research we attempted to specify over what time period a future rich patch would affect current foraging. The effect of future food was measured by early entry into the rich patch (anticipation) and by a decrease in food obtained in the depleting patch (suppression). The rats showed anticipation of a rich patch up to an hour distant, but suppressed current feeding only if the rich patch was 16 min distant or less. The suppression effect appeared mediated by competition for expression between anticipatory entries into the rich patch and continued foraging in the depleting patch. These results suggest that optimal foraging is based on a variety of specific mechanisms rather than a general optimizing algorithm with a single time horizon.     

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.     

Observation system for the control of the hive environment by the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

The honeybee can control its hive environment to survive drastic changes in the field environment. To study the control of multiple environmental factors by honeybees, in this experiment, we developed a continual and simultaneous monitoring system for the temperature, moisture, and carbon dioxide (CO₂) concentration in a honeybee hive. Changes in hive weight, CO₂ production rate, and honeybee behavior were also monitored to estimate energy costs and behavioral activity for the environmental regulation. Measurements were conducted in August 2008. We found that the honeybee hive has a microclimate different from the ambient climate, and that the difference was partly accompanied by changes in honeybee activity. Our results also suggest that hive temperature, humidity, and CO₂ concentrations are controlled by different mechanisms. Additional monitoring of the hive environment and honeybee behavior for longer periods would enable us to understand the mechanisms of environmental control by honeybees, which is one of the behaviors that define honeybees as social insects.     

Categorization of visual stimuli in the honeybee Apis mellifera

Categorization refers to the classification of perceptual input into defined functional groups. We present and discuss evidence suggesting that stimulus categorization can also be found in an invertebrate, the honeybee Apis mellifera, thus underlining the generality across species of this cognitive process. Honeybees show positive transfer of appropriate responding from a trained to a novel set of visual stimuli. Such a transfer was demonstrated for specific isolated features such as symmetry or orientation, but also for assemblies (layouts) of features. Although transfer from training to novel stimuli can be achieved by stimulus generalization of the training stimuli, most of these transfer tests involved clearly distinguishable stimuli for which generalization would be reduced. Though in most cases specific experimental controls such as stimulus balance and discriminability are still required, it seems appropriate to characterize the performance of honeybees as reflecting categorization. Further experiments should address the issue of which categorization theory accounts better for the visual performances of honeybees.This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).     

Cognitive architecture of a mini-brain: the honeybee

Honeybees have small brains, but their behavioural repertoire is impressive. In this article we focus on the extent to which adaptive behaviour in honeybees exceeds elementary forms of learning. We use the concept of modularity of cognitive functions to characterize levels of complexity in the honeybee brain. We show that behavioural complexity in the honeybee cannot be explained by independent functions of vertically arranged, domain-specific processing modules, but requires horizontal integration in a central state, and we identify neural mechanisms that may underlie domain-specific processing and central integration. The honeybee may serve as a useful model for the study of intermediate levels of complexity in cognitive functions and the search for their neural substrates.     

Benefits of team participative decision making and its potential to affect individual creativity

How does team participative decision‐making affect individual creative performance? Building on team climate theory (Anderson & West, 1998; West 1990, 2002; West & Sacramento, 2012), this study investigates the indirect effect of team participative decision making on employee creativity through individual perception of cognition team diversity and psychological safety. Results from 256 supervisor–subordinate dyads in 45 teams show that team participative decision making is positively associated with cognitive team diversity and psychological safety. For the mediating effects, team participative decision‐making climate is positively indirectly related to creative performance via psychological safety but not via cognitive team diversity. Theoretical and practical implications are discussed.     

A biologically plausible robot attention model,based on space and time

After half a century of cognitive revolution we remain far from agreement about what cognition is and what cognition does. It was once thought that these questions could wait until the data were in. Today there is a mountain of data, but no way of making sense of it. The time for tackling the fundamental issues has arrived. The biogenic approach to cognition is introduced not as a solution but as a means of approaching the issues. The traditional, and still predominant, methodological stance in cognitive inquiry is what I call the anthropogenic approach: assume human cognition as the paradigm and work ‘down’ to a more general explanatory concept. The biogenic approach, on the other hand, starts with the facts of biology as the basis for theorizing and works ‘up’ to the human case by asking psychological questions as if they were biological questions. Biogenic explanations of cognition are currently clustered around two main frameworks for understanding biology: self-organizing complex systems and autopoiesis. The paper describes the frameworks and infers from them ten empirical principles—the biogenic ‘family traits’—that constitute constraints on biogenic theorizing. Because the anthropogenic approach to cognition is not constrained empirically to the same degree, I argue that the biogenic approach is superior for approaching a general theory of cognition as a natural phenomenon.

The psychology of memory,extended cognition,and socially distributed remembering

This paper introduces a new, expanded range of relevant cognitive psychological research on collaborative recall and social memory to the philosophical debate on extended and distributed cognition. We start by examining the case for extended cognition based on the complementarity of inner and outer resources, by which neural, bodily, social, and environmental resources with disparate but complementary properties are integrated into hybrid cognitive systems, transforming or augmenting the nature of remembering or decision-making. Adams and Aizawa, noting this distinctive complementarity argument, say that they agree with it completely: but they describe it as “a non-revolutionary approach” which leaves “the cognitive psychology of memory as the study of processes that take place, essentially without exception, within nervous systems.” In response, we carve out, on distinct conceptual and empirical grounds, a rich middle ground between internalist forms of cognitivism and radical anti-cognitivism. Drawing both on extended cognition literature and on Sterelny’s account of the “scaffolded mind” (this issue), we develop a multidimensional framework for understanding varying relations between agents and external resources, both technological and social. On this basis we argue that, independent of any more “revolutionary” metaphysical claims about the partial constitution of cognitive processes by external resources, a thesis of scaffolded or distributed cognition can substantially influence or transform explanatory practice in cognitive science. Critics also cite various empirical results as evidence against the idea that remembering can extend beyond skull and skin. We respond with a more principled, representative survey of the scientific psychology of memory, focussing in particular on robust recent empirical traditions for the study of collaborative recall and transactive social memory. We describe our own empirical research on socially distributed remembering, aimed at identifying conditions for mnemonic emergence in collaborative groups. Philosophical debates about extended, embedded, and distributed cognition can thus make richer, mutually beneficial contact with independently motivated research programs in the cognitive psychology of memory.     

Spontaneous performance of wild baboons on three novel food-access puzzles

Although the technical problem-solving expertise of nonhuman primates has been investigated extensively in captivity, few species have been tested in their natural habitats. Here I examine the physical cognition of wild savanna baboons (Papio anubis), a species that occupies an omnivorous foraging niche in which a variety of embedded food items are extracted and processed. Baboons were tested on three puzzles, each involving high-quality food that required removal from a novel obstruction: (1) a string-pulling puzzle in which food was hung from tree branches, (2) a twig-dipping puzzle in which food was embedded in a vertical tube, and (3) a stick-pushing puzzle in which food was contained in a horizontal conduit. The baboons failed to solve the second and third puzzles even when tools had been appropriately positioned in advance. And although they solved the first puzzle, their actions (running while holding food that was still attached to the string), suggested they did not fully comprehend the string’s connective property. The baboons’ performance might reflect the time constraints of life in the wild, which relative to captivity may provide fewer opportunities for the development of understanding about the physical properties of objects and their potential uses as tools. Further experiments on the physical cognition of baboons and many other primate species in their natural habitats would help test this ontogenetic hypothesis. Such field experiments would be especially fruitful if they continued to target extractive foragers like baboons: these experiments could simultaneously provide a test of phylogenetic hypotheses that invoke extractive foraging as the key stimulus for brain expansion in savanna-dwelling hominids. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Limitations to the deficit attenuation hypothesis: Aging and decision making

The deficit attenuation hypothesis is the proposal that age related declines in basic cognitive functions often result in compensatory changes in decision making strategies. However, the patterns of cognitive changes across the adult life span are complex: Many cognitive abilities change across the adult life span while others do not. Some of the cognitive changes will be detrimental to decision making, others will have no impact and still others may actually improve decision making. We illustrate the complexity of the impact of cognition on aging and decision making with examples from working and long-term memory and use these to suggest boundary conditions for the deficit attenuation hypothesis.