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.     

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.     

Learning about food: starlings, skinner boxes, and earthworms

Despite its importance as a tool for understanding a wide range of animal behavior, the study of reinforcement schedules in the laboratory has suffered from difficulties in the biological interpretation of its findings. This study is an operant-laboratory investigation of the ability of European starlings, Sturnus vulgaris, to learn to respond adaptively to the problem of foraging on patchily distributed prey that are uncertainly located in space. In order to maximize the biological relevance of the laboratory study, variation in the aggregation of earthworms, Lumbricus terrestris (a prey species), was rigorously quantified from the field, and the experimental birds were presented with reinforcement schedules designed to represent the extremes of the observed variation. The results demonstrate that, even for a single prey species, the degree to which individuals are aggregated can vary markedly over a range of spatial scales, and that starlings can rapidly learn to respond, in an adaptive manner, to these variations. These findings suggest that starlings are capable of adjusting their behavior to facilitate the efficient exploitation of prey that occurs in patches of an uncertain nature, and thus illustrate the heuristic value of an ecologically informed operant-laboratory approach to studying foraging behavior.     

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.     

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.     

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.     

Learning reward expectations in honeybees

The aim of this study was to test whether honeybees develop reward expectations. In our experiment, bees first learned to associate colors with a sugar reward in a setting closely resembling a natural foraging situation. We then evaluated whether and how the sequence of the animals’ experiences with different reward magnitudes changed their later behavior in the absence of reinforcement and within an otherwise similar context. We found that the bees that had experienced increasing reward magnitudes during training assigned more time to flower inspection 24 and 48 h after training. Our design and behavioral measurements allowed us to uncouple the signal learning and the nutritional aspects of foraging from the effects of subjective reward values. We thus found that the animals behaved differently neither because they had more strongly associated the related predicting signals nor because they were fed more or faster. Our results document for the first time that honeybees develop long-term expectations of reward; these expectations can guide their foraging behavior after a relatively long pause and in the absence of reinforcement, and further experiments will aim toward an elucidation of the neural mechanisms involved in this form of learning.     

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.     

Use of visual, acoustic, and olfactory information during embedded invertebrate foraging in brown capuchins (Cebus apella)

Experiments were conducted to investigate which sensory cues are used by brown capuchins (Cebus apella) in embedded invertebrate foraging. The importance of visual, olfactory, and acoustic cues in such foraging was determined by presenting subjects with a stimulus log modified to block out given sensory cues. Experiment 1 was designed to investigate whether subjects could locate an invertebrate embedded in wood when only visual, acoustic, or olfactory information was available. Experiments 2 and 3 were designed to investigate extractive foraging behavior when two sensory cues were provided. It was hypothesized that the combination of visual and acoustic information would be necessary for subjects to successfully locate embedded invertebrates. Results indicated that subjects' performance was most successful when both visual and acoustic information was available.     

The Effect of Stress on Spontaneous Nest Leaving Behavior in the Mouse: An Improved Model of Stress-Induced Behavioral Pathology

The present experiments were conducted to develop a more sensitive and reliable model of stress-induced behavioral pathology in the mouse. Male mice were housed singly in nest cages connected to either a circular tunnel, a recreational cage or a large box with food foraging apparatus. Spontaneous nocturnal out of nest activity or food foraging behavior in these environments was continuously monitored for a two week period during which time the effects of stress were examined. It was found that both repeated restraint and aggression stress markedly and persistently reduced out of nest nocturnal activity or food foraging behavior in all 3 environments but did not alter activity in a novel open field or plus maze or food or saccharin intake in the nest cage. In a preliminary experiment the reduction in out of nest activity by stress was attenuated by prior chronic treatment with the antidepressant, desmethylimipramine. Plasma corticosterone was elevated immediately after aggression stress but reduced 5 hr after chronic aggression stress. The reduction in activity did not appear the result of increased anxiety as measured by spontaneous risk assessment behavior in the nest. It is concluded that the decrease in out of nest activity after stress in the present studies models a withdrawn behavioral state and may be due to either or both a decrease in appetitive motivation to leave the nest or an increased aversion to the external environment which does not apparently involve anxiety.     

Animal foraging and the evolution of goal-directed cognition

Foraging- and feeding-related behaviors across eumetazoans share similar molecular mechanisms, suggesting the early evolution of an optimal foraging behavior called area-restricted search (ARS), involving mechanisms of dopamine and glutamate in the modulation of behavioral focus. Similar mechanisms in the vertebrate basal ganglia control motor behavior and cognition and reveal an evolutionary progression toward increasing internal connections between prefrontal cortex and striatum in moving from amphibian to primate. The basal ganglia in higher vertebrates show the ability to transfer dopaminergic activity from unconditioned stimuli to conditioned stimuli. The evolutionary role of dopamine in the modulation of goal-directed behavior and cognition is further supported by pathologies of human goal-directed cognition, which have motor and cognitive dysfunction and organize themselves, with respect to dopaminergic activity, along the gradient described by ARS, from perseverative to unfocused. The evidence strongly supports the evolution of goal-directed cognition out of mechanisms initially in control of spatial foraging but, through increasing cortical connections, eventually used to forage for information.     

A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila

The Drosophila giant fiber jump-and-flight escape response is a model for genetic analysis of both the physiology and the plasticity of a sensorimotor behavioral pathway. We previously established the electrically induced giant fiber response in intact tethered flies as a model for habituation, a form of nonassociative learning. Here, we show that the rate of stimulus-dependent response decrement of this neural pathway in a habituation protocol is correlated with PKG (cGMP-Dependent Protein Kinase) activity and foraging behavior. We assayed response decrement for natural and mutant rover and sitter alleles of the foraging (for) gene that encodes a Drosophila PKG. Rover larvae and adults, which have higher PKG activities, travel significantly farther while foraging than sitters with lower PKG activities. Response decrement was most rapid in genotypes previously shown to have low PKG activities and sitter-like foraging behavior. We also found differences in spontaneous recovery (the reversal of response decrement during a rest from stimulation) and a dishabituation-like phenomenon (the reversal of response decrement evoked by a novel stimulus). This electrophysiological study in an intact animal preparation provides one of the first direct demonstrations that PKG can affect plasticity in a simple learning paradigm. It increases our understanding of the complex interplay of factors that can modulate the sensitivity of the giant fiber escape response, and it defines a new adult-stage phenotype of the foraging locus. Finally, these results show that behaviorally relevant neural plasticity in an identified circuit can be influenced by a single-locus genetic polymorphism existing in a natural population of Drosophila.     

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 bare bones bacterial foraging optimization algorithm

Bacterial foraging optimization (BFO), based on the social foraging behaviors of bacteria, is a new intelligent optimizer. It has been widely accepted as an optimization algorithm of current interest for a variety of fields. However, compared with other optimizers, the BFO possesses a poor convergence performance over complex optimization problems. To improve the optimization capability of the BFO, in this paper a bare bones bacterial foraging optimization (BBBFO) algorithm is developed. First, a chemotactic strategy based on Gaussian distribution is incorporated into this method through making use of both the historical information of individual and the share information of group. Then the swarm diversity is introduced in the reproduction strategy to promote the exploration ability of the algorithm. The performance of BBBFO is verified on various benchmark functions, the comparative results reveal that the proposed approach is more superior to its counterparts.     

“To eat or not to be eaten?” Collective risk-monitoring in groups

The importance of risk-monitoring has been increasing in many key aspects of our modern lives. This paper examines how individuals monitor such risks collectively by extending a behavioral ecological model of animal foraging to human groups. Just as animals must forage for food under predatory risk, humans must divide valuable material and psychological resources between foraging activity and risk-monitoring activity. We predicted that game-theoretic aspects of the group situation complicate such a trade-off decision in resource allocation, eventually yielding a mixed equilibrium in a group. When the equilibrium is reached, only a subset of members engage in the risk-monitoring activity while others free-ride, concentrating mainly on their own foraging activity. Laboratory groups engaging in foraging under moderate risk provided a support to this prediction. When the risk-level was set higher, however, “herding behavior” (conforming to the dominant behavior) interfered with the emergence of equilibrium. Implications for risk management are discussed.     

Foraging in a simulated natural environment: There's a rat loose in the lab

Rats were required to earn their food in a large room having nine boxes placed in it, each of which contained food buried in sand. In different phases of the experiment the amount of time allowed for foraging, the amount of food available in each food patch, and the location of the different available amounts were varied. The rats exhaustively sampled all patches each session but seemed to have fairly strong preferences for certain locations over others. If position preferences were for patches containing small amounts of food, the sensitivity to amount available was increased so that when location was compensated for, a pattern of optimal foraging was evident. The importance of environmental constraints in producing optimal behavior and the relation of the observed behavior to laboratory findings are discussed.     

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.     

Imitative learning by captive western lowland gorillas (Gorilla gorilla gorilla) in a simulated food-processing task

Although field studies have suggested the existence of cultural transmission of foraging techniques in primates, identification of transmission mechanisms has remained elusive. To test experimentally for evidence of imitation in the current study, we exposed gorillas (Gorilla gorilla gorilla) to an artificial fruit foraging task designed by A. Whiten and D. M. Custance (1996). Gorillas (n=6) watched a human model remove a series of 3 defenses around a fruit. Each of the defenses was removed using 1 of 2 alternative techniques. Subsequent video analysis of gorillas' behavior showed a significant tendency to copy the observed technique on 1 of the individual defenses and the direction of removal on another defense. This is the first statistically reliable evidence of imitation in gorillas. Sequence of defense removal was not replicated. The gorillas' responses were most similar to those of chimpanzees.     

Meal patterns of cats encountering variable food procurement cost.

The meal patterns of 2 cats in a laboratory habitat with variable foraging costs were examined in a foraging paradigm in which subjects could initiate meals at any time by completing a predetermined number of bar presses (the procurement price) and then could eat any amount. From meal to meal, the procurement price either was fixed or varied among a geometric series of five prices. As the fixed price or the mean of the variable prices increased, meal frequency decreased and meal size increased; daily intake was unaffected. Within variable-price schedules, meal size was not related to the just-paid procurement price. These results suggest that cats respond to the global rather than to the local cost structure of their habitat. They appear to respond to an average of the prices encountered, initiating meals of a frequency and size appropriate to that average. This was true even when the average price was high, meals were infrequent, and thus price encounters were widely separated in time. Therefore, the time window over which the consequences of behavior can affect behavior is longer than often conceived, at least in economies in which the animal controls its intake and the frequency, size, and distribution of its meals.