Ants use directionless odour cues to recall odour-associated locations

Ants are key model organisms in the study of navigation and memory formation. Many ants learn food locations very quickly and with high accuracy. But can individual ants learn multiple separate food locations, associate them with a cue, and then correctly recall the food location and navigate towards it when later presented with that cue? In this experiment, we sequentially trained Lasius niger foragers to two scented feeders at either end of a T-maze. The next day, an odour cue corresponding to one of the food sources was presented to the ants in the air, on the substrate and via trophallaxis with nest mates. Trained foragers accurately navigated to the correct side of the T-maze (89 % correct decisions), but only after the first 10 min of testing. This demonstrates the ability of ants to perform associative recall, forming clear associates between odour cues and food locations and using these associations to navigate to food sources. We also found that trained ants in the first 10 min of testing showed no preference for the correct side (57 % correct decisions), which may be related to the motivational state of the ants tested. Ants with different motivational states (whether they are ‘scouting’ or ‘recruited’) made use of route memories in a completely different manner. This highlights the importance of taking account of motivational states when performing behavioural experiments.     

Learning,retention and coding of nest-associated visual cues by the Australian desert ant, <Emphasis Type="Italic">Melophorus bagoti</Emphasis>

A variety of social insects use visual cues for homing. In this study, we examine the possible factors affecting the learning and retention of nest-associated visual cues by the Australian desert ant Melophorus bagoti and the manner in which such cues are encoded by foraging ants. We placed four prominent cylindrical landmarks around a nest and trained foragers from that nest to a food source. Ants were tested with the landmark array in a distant testing field after (1) a known number of exposures to the landmarks (1, 3, 7 or 15 trials, spread over a period of 1 day, 2 days or ≥3 days) and (2) after a known period of delay (0, 24, 48, 96 or 192 h). The results show that a combination of an increase in training trials and an increase in number of training days affected the acquisition of landmark memory. Moreover, once the landmarks were learnt, they became a part of long-term memory and lasted throughout the ants’ foraging lifetime. To examine visual cue encoding behaviour, ants trained under similar conditions for 4 days were tested with (1) an identical landmark array, (2) landmarks of the same size used in training, but placed at twice the distance from each other, and (3) landmarks whose dimensions were doubled and placed at twice the distance from each other. In conditions (1) and (3), the ants searched extensively at the centre of the four landmarks, suggesting that, similar to the Saharan ant (genus Cataglyphis) and the honeybee, M. bagoti too uses a snapshot to match the view of the landmarks around the nest. But contrary to the snapshot model, in condition (2), the ants did not search extensively at the centre of the landmarks, but searched primarily 0.5 m from the landmark, the distance from each landmark to the nest during training. We discuss how various search models fare in accounting for these findings.     

Sympatric species of threespine stickleback differ in their performance in a spatial learning task

Increasing evidence suggests that cognitive function is under selection in diverse taxa and that this results in different cognitive abilities in taxa experiencing different selective environments. For example, species inhabiting spatially complex environments might be expected to have good spatial learning ability. We investigated whether local habitat conditions influence learning by comparing the performance of two recently diverged species of threespine stickleback (Gasterosteus aculeatus complex) in a spatial learning task. The two species reside sympatrically in several lakes. Benthics occupy the spatially structured vegetated littoral zone, whereas limnetics occupy the spatially homogenous open-water pelagic zone. We trained fish to locate a hidden reward in a T-maze and asked whether they did so by learning a body-centred pattern of movement (turn left or right) or by using plant landmarks. Both benthics and limnetics used turn and landmark cues, but benthics learnt the task almost twice as quickly as limnetics. This difference is consistent with the hypothesis that benthic and limnetic sticklebacks are equipped with spatial learning abilities well suited to the spatial complexity of their littoral and pelagic habitats. Our findings add to the understanding of the evolution of learning.     

Honeybees use a Lévy flight search strategy and odour-mediated anemotaxis to relocate food sources

The availability of food resources changes over time and space, and foraging animals are constantly faced with choices about how to respond when a resource becomes depleted. We hypothesise that flying insects like bees discover new food sources using an optimal Lévy flight searching strategy and odour-mediated anemotaxis, as well as visual cues. To study these searching patterns, foraging honeybees were trained to a scented feeder which was then removed. Two new unrewarding feeders, or ‘targets’, were then positioned up- and downwind of the original location of the training feeder. The subsequent flight patterns of the bees were recorded over several hundred metres using harmonic radar. We show that the flight patterns constitute an optimal Lévy flight searching strategy for the location of the training feeder, a strategy that is also optimal for the location of alternative food sources when patchily distributed. Scented targets that were positioned upwind of the original training feeder were investigated most with the numbers of investigations declining with increasing distance from the original feeder. Scented targets in downwind locations were rarely investigated and unscented targets were largely ignored, despite having the same visual appearance as the rewarding training feeder.     

Research Training for Releasable Animals

Abstract:  Restrictions on training potentially releasable animals such as those undergoing rehabilitation care or wild-caught captives have limited our understanding of sensory processes, cognition, and physiology important for conservation of species. It is common practice among several U.S. federal agencies to limit training of animals available for release. The behavioral argument justifying this practice is that training habituates subjects to people and conditions them to associate people with rewards such as food; habituation to and positive associations with people will lead animals into dangerous situations after their release. If under special circumstances research training is permitted, all trained behaviors must be extinguished before release because behaviors will transfer to the natural setting. Research on animal learning and memory indicates that these may not be accurate scenarios. A review of the literature on habituation, classical and instrumental conditioning, and compound conditioning suggests that learning within a research setting does not add to learning that already occurs in procedures associated with basic feeding and care. In fact, animals probably learn less about people in a training setting. Furthermore, context-specific effects on memory limit behavior transfer from captive to natural settings. Extinction is strongly susceptible to context effects, which suggests that extinction does not effectively transfer to the postrelease setting. Counterintuitively, extinction of responses to experimental stimuli under some circumstances may enhance undesirable learning about humans. Under those circumstances in which isolation from human contact is difficult or undesirable, behavioral research can present an ideal format for minimizing learning about humans and provide biological information important for conservation.     

Recruitment to food by the German yellowjacket, Vespula germanica

The hypothesis that Vespula germanica foragers can recruit nestmates to food resources was tested using a protocol that controlled for the biasing effects of social factors at the resource, including local enhancement and food-site marking substances. Foragers from an observation colony in the field were trained to visit a dish of scented corn syrup solution 15?m east of the nest. A second feeding station, 22?m northeast of the nest, offered incoming foragers a choice between food with the training scent and food with a control scent. Significantly more naive foragers arriving at that station chose the food with the training scent. We conclude that the German yellowjacket is able to recruit nestmates to carbohydrate food sources, and that recruits use food odor to locate the source of food being brought into the nest.     

Visual associative learning in two desert ant species

Visual cues are important navigational tools for many solitary foraging insects. In addition to information provided by path integration, desert ants learn and use visual cues for homing back to their nest. In this study, we compared the visually based learning of two desert ant species: the North African Cataglyphis fortis and the Australian Melophorus bagoti, each of which lives in ecologically similar but visually different environments. In our experiment, ants’ choice performance was measured by training foragers in a channel system. We used a decision box with two visual stimuli during their homebound trips, with one of the stimuli always being the correct one that provided thoroughfare. To determine any habitat effects on learning, we examined intraspecific comparisons in C. fortis with different nest surroundings. The intraspecific comparison in C. fortis revealed no differences in learning the task. In general, C. fortis showed little learning in our task and the results were similar for ants from barren and cluttered environments. Overall, M. bagoti learned the task faster and had a higher level of accuracy than C. fortis. One explanation for this species-specific difference could be that the cluttered habitat of M. bagoti favours the evolution of visual associative learning more so than the plain habitat of C. fortis.     

Responses to sugars and their behavioural mechanisms in the starling (Sturnus vulgaris L.)

Summary The response of the starling to sugar solutions was investigated as this species, which eats sweet fruits, does not prefer sugar solutions according to the literature.In choice tests using two identical fountains, moderate preference for higher concentrations (0.5 M and 1 M) of glucose and fructose to water was demonstrated. The same concentrations of sucrose were rejected. Lower concentrations (0.25 M and less) of all three sugars were neither preferred nor rejected. In choice tests using two differently coloured fountains the subjects did not generally respond more sensitively to sugar solutions. In learning experiments with differently coloured fountains the starlings developed very marked preferences for 0.5 M glucose and 0.5 M fructose and a corresponding rejection of 0.5 M sucrose in the course of 1–2 days. In a learning experiment with dentical fountains they also developed a pronounced preference; the preference values obtained, however, are higher if secondary cues such as the colour of the fountain or its position are available. In short time tests immediate responses to sugar solutions could not be demonstrated.The rejection of sucrose is attributed to illness-induced aversion learning, the learned preference for glucose and fructose to the preference according to gain in energy per unit of time as postulated by the optimal foraging theory. Taste sensations play, if any, only a minor role. The learning mechanisms operating in the experiments could be employed by the starling for the selection of fruits.     

Rick-sensitive foraging in common shrews: an interruption model and the effects of mean and variance in reward rate

Summary A model of risk-sensitive foraging based on a continuously foraging but interruptable predator is developed and tested in a simple choice experiment using common shrews.Given a choice of two feeding stations, shrews behaved in accordance with the broad predictions of the model. Having been trained below their estimated food requirement, shrewss preferred the station y elding the higher mean reward rate, but prefereence for a constant (constant reward rate) or risky variable reward rate) station was influenced by experience of variance in reward rate at the risky station.Preference was influenced most clearly by experience of reward rate variance during tests rather than training.     

Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning

It is usually assumed that the choice behavior of bees for floral colors is influenced by innate preferences only for the first flower visits prior to any experience. After visits to rewarding flowers bees learn to associate their colors with a reward. This learning process leads to an acquired preference for the trained colors that has been believed to dominate over previous experiences and over innate preferences. This work investigates how bumble bees (Bombus terrestris) chose among artificial flowers of different colors after they had been extensively trained to other colors. The bees chose novel colors according to their similarity to the trained color if the trained color was similar to some of the test colors. This was true also if trained colors and test colors were well distinguished, so their color choice reflected generalization between colors. If the test colors were so different from the trained color that no generalization took place, choice behavior was not affected by the trained color and reflected innate preferences. The differences in choice frequencies could not be explained by physical properties of the test colors other than the dominant wavelength, a parameter taken to reflect hue perception. Preferred dominant wavelengths correspond to those observed in naive bumble bees and honeybees. Thus bumble bees show innate preferences for certain colors not only prior to color learning but also after intensive learning when choosing among very different novel colors. Color choice among similar colors, however, is controlled by generalization from the learned color. Received: 9 November 1999 / Received in revised form: 19 March 2000 / Accepted: 31 March 2000     

Environmental chemical cues associated with prey and subsequent prey preference in the wolf spider Hogna carolinensis Hentz (Araneae,Lycosidae)

The purpose of this study was to determine if environmental chemical cues associated with prey can affect subsequent prey choice in wolf spiderlings (Hogna carolinensis). After emergence from the egg sac, three groups of 10 spiderlings were each fed for one-week on one of three naturally-occurring prey species: group 1 fed on nymphs of the field cricket Gryllus pennsylvanicus; group 2 (house cricket, Acheta domesticus); group 3 (mole cricket, Gryllotalpa hexadactyla). They were then tested for subsequent prey preference in choice tests conducted in a plastic arena. Each spiderlings was presented simultaneously with one individual of each prey species in a randomized design. Spiderlings exhibited a significant first preference for the original diet. Thus, experience with certain foods (environmental chemical cues) encountered by newly hatched spiderlings can affect subsequent prey preference in this species.     

Does colour matter? The importance of colour in avoidance learning, memorability and generalisation

Aposematic species exploit the ability of predators to associate, for example, conspicuous colouration with the unprofitability of prey. We tested the importance of colour for avoidance learning, memory and generalisation in wild-caught great tits (Parus major). First, we determined the birds’ initial colour preferences for red, yellow, orange and grey artificial prey items. The birds showed some preferences, as they were more willing to eat grey prey as their first choice, but these were not strong preferences. We then trained birds to discriminate red, yellow or variable (red and yellow) signals from grey where colours signalled palatable and unpalatable food. In general, the birds learned the discrimination task equally well, irrespective of which colours signalled unpalatability, and subsequently remembered the distinction between previously palatable and previously unpalatable colours in the memorability test. We did not find strong evidence that variability in the signal affected learning or memory. Our results suggest that, in a task where birds must discriminate between palatable and unpalatable prey, it does not matter which specific colour signals unpalatability, although this might be context-dependent. To study whether training also affects responses to unconditioned stimuli, we included orange prey items in the memorability test. Although orange had been palatable in the initial preference test, the birds ate fewer orange prey items after they had been trained to avoid red, yellow or both colours (variable signal) as unpalatable prey, but did not change their preference when trained that these colourful signals were palatable. This indicates that generalisation occurred more readily after a negative experience than a positive experience, a situation that would potentially allow imperfect mimicry to occur.     

The peculiar case of an insectivorous iguanid lizard that detects chemical cues from prey

Summary. Ecological and phylogenetic factors determine which sensory modalities organisms use in their day-to-day activities. Among lizards, empirical studies indicate a tight association between foraging strategies and the ability to detect chemical cues from prey. Consequently, ambush insectivores do not detect food chemicals and these differences have a phylogenetic basis, as ambush lizards mainly belong to the Iguania clade. These data contrast, however, with the widespread uses of chemoreception in the Iguania genus Liolaemus, which are mostly insectivorous ambush predators. Moreover, observations from different Liolaemus species suggest a capability to find prey through chemoreception. In order to clarify the abilities of Liolaemus to detect chemical cues from prey, the chemoreceptive behavior of the insectivorous ambush predator, L. lemniscatus, was studied. Lizards were given the choice between areas with and without chemical cues from a food item (mealworms). Results show that test animals stayed for longer, moved more, and did more chemical exploration (tongue flicks) in the area where chemical cues from mealworms were present. Furthermore, in this area, more individuals displayed behaviors that suggest maintenance and defense of the prey patch. Thus, L. lemniscatus is the first insectivorous Iguania reported to be able to detect chemical cues from prey. Although I propose a mechanism for acquiring chemical detection of prey cues in Liolaemus, I also remark that it is necessary to reanalyze both the abilities to detect and use chemical foraging cues in Iguania at large, and the methodologies traditionally used to study these issues.     

Risk vs. reward: how predators and prey respond to aging olfactory cues

Many animals use olfaction to find food and avoid predators, and must negotiate environments containing odors of varying compositions, strengths, and ages to distinguish useful cues from background noise. Temporal variation in odor cues (i.e., “freshness”) seems an obvious way that animals could distinguish cues, yet there is little experimental evidence for this phenomenon. Fresh cues provide a more reliable indicator of donor presence than aged cues, but we hypothesize that the benefits of responding to aged cues depend on whether the cue indicates the proximity of a predator or a potential meal. As prey cannot remain eternally risk averse in response to predator odor, we predict that antipredator responses should diminish as predator cues age. In contrast, animals searching for food should investigate aged prey cues if investigation costs are sufficiently low and the potential benefit (a meal) sufficiently high; thus, we predict that predators will maintain interest in aged prey cues. We tested these ideas using free-ranging rats (Rattus spp.) in two separate experiments; firstly assessing giving-up densities in the presence of predator odor, and secondly examining investigation rates of prey odors. As predicted, giving-up densities dropped once predator odor had aged, but investigation rates remained similar for aged and fresh prey odor. Thus, rats used temporal variation in odor cues to evaluate the cost–benefit relationship of responding to predator and prey odors. We suggest that the ecological significance of variable cue age needs more research and should be considered when interpreting behavioral responses to olfactory information.     

Spatial orientation of the golden hamster in conditions of conflicting location-based and route-based information

Summary The orientation of golden hamsters during their return from a food source at the centre of an experimental arena to their nest at the arena's periphery was examined. The experiments took place under different visual conditions and involved conflicting spatial information, which the animal could collect either en route, during the outward journey to the food source, or on site, at the point of departure of the return trip. When the arena and nest box were rotated before the start of the trial (so that the hamsters started the outward journey from different points in absolute space), the animals returned directly to the point of departure of each particular hoarding trip when tested under infra-red light. Deprived of visual cues, they resorted to route-based information, i.e. they depended on the registration and computation of cues which had been generated during the outward journey. If tested under the ordinary room lights, the animals returned in a constant direction towards the usual location of the nest box, but with slight deviations towards the changing point in space where they had initiated each hoarding trip. They therefore relied mainly on stable location-based features from the distant visual background which they had associated with the standard location of the nest entrance; at the same time, however, they were also influenced by information derived from the outward journey. If exposed to a weak light source from outside the arena, the animals' homing behaviour reflected the simultaneous influence of three categories of information: (a) The light as a stable, location-based cue which the subjects had associated with the usual location of the nest; (b) the registration of the previous outward journey by means of internal (idiothetic) path-dependent variables; and (c) the registration of the previous outward journey using the light as visual reference. These results illustrate the interplay and functional hierarchy of various categories of spatial information which the hamster, active at dusk and at night, can use in laboratory conditions as well as in its natural habitat.     

Collective foraging decision in a gregarious insect

Group foraging by eusocial insects implies sophisticated recruitment processes that often result in collective decisions to exploit the most profitable sources. These advanced levels of cooperation, however, remain limited to a small range of species, and we still know little about the mechanisms underlying group foraging behaviours in the great mass of animals exhibiting lower levels of social complexity. In this paper, we report, for the first time in a gregarious insect, the cockroach Blattella germanica (L.), a collective foraging decision whereby the selection of food sources is reached without requiring active recruitment. Groups of cockroaches given a binary choice between identical food sources exhibited exploitation asymmetries whose amplitude increases with group size. By coupling behavioural observations to computer simulations, we demonstrate that selection of food sources relies uniquely on a retention effect of feeding individuals on newcomers without comparison between available opportunities. This self-organised pattern presents similarities with the foraging dynamics of eusocial species, thus stressing the generic dimension of collective decision-making mechanisms based on social amplification rules despite fundamental differences in recruitment processes. We hypothesise that such parsimony could apply to a wide range of species and help understand the emergence of collective behaviours in simple social systems.     

Within-group spatial position in ring-tailed coatis: balancing predation, feeding competition, and social competition

A variety of factors can influence an individual’s choice of within-group spatial position. For terrestrial social animals, predation, feeding success, and social competition are thought to be three of the most important variables. The relative importance of these three factors was investigated in groups of ring-tailed coatis (Nasua nasua) in Iguazú, Argentina. Different age/sex classes responded differently to these three variables. Coatis were found in close proximity to their own age/sex class more often than random, and three out of four age/sex classes were found to exhibit within-group spatial position preferences which differed from random. Juveniles were located more often at the front edge and were rarely found at the back of the group. Juveniles appeared to choose spatial locations based on feeding success and not predation avoidance. Since juveniles are the most susceptible to predation and presumably have less prior knowledge of food source location, these results have important implications in relation to predator-sensitive foraging and models of democratic group leadership. Subadults were subordinate to adult females, and their relationships were characterized by high levels of aggression. This aggression was especially common during the first half of the coati year (Nov–April), and subadults were more peripheralized during this time period. Subadults likely chose spatial positions to avoid aggression and were actively excluded from the center of the group by adult females. In the Iguazú coati groups, it appeared that food acquisition and social agonism were the major determinants driving spatial choice, while predation played little or no role. This paper demonstrates that within-group spatial structure can be a complex process shaped by differences in body size and nutritional requirements, food patch size and depletion rate, and social dominance status. How and why these factors interact is important to understanding the costs and benefits of sociality and emergent properties of animal group formation.     

Honeybee recruitment to scented food sources: correlations between in-hive social interactions and foraging decisions

Information exchange of environmental cues facilitates decision-making processes among members of insect societies. In honeybee foraging, it is unknown how the odor cues of a resource are relayed to inactive nest mates to enable resource exploitation at specific scented sources. It is presumed that bees need to follow the dance or to be involved in trophallaxis with a successful forager to obtain the discovered floral scent. With this in mind, we evaluated the influence of food scent relayed through in-hive interactions and the subsequent food choices. Results obtained from five colonies demonstrated that bees arriving at a feeding area preferred to land at a feeder carrying the odor currently exploited by the trained forager. The bees that landed at this feeder also showed more in-hive encounters with the trained forager than the individuals that landed at the alternative scented feeder. The most frequent interactions before landing at the correct feeder were body contacts with the active forager, a behavior that involves neither dance following nor trophallaxis. In addition, a reasonable proportion of successful newcomers showed no conspicuous interactions with the active forager. Results suggest that different sources of information can be integrated inside the hive to establish an odor-rewarded association useful to direct honeybees to a feeding site. For example, simple contacts with foragers or food exchanges with non-active foragers seem to be enough to choose a feeding site that carries the same scent collected by the focal forager.     

Position preferences within groups: do whirligigs select positions which balance feeding opportunities with predator avoidance?

The benefits and costs of group living are likely to be asymmetric within a group. Animals at the edge of a group are more at risk from predators, according to the selfish herd hypothesis, but are also more likely to obtain scattered food resources. Does an animal's choice between these two conflicting positions depend on its body reserves? The hunger level of marked whirligig beetles (Coleoptera: Gyrinidae) was manipulated and the positions of individuals relative to the rest of the group on the surface of the water were determined with image analysis software. In 12 out of 13 groups, of approximately 18 beetles each, hungry beetles were closer to the edge of a group and had a higher distance to their nearest neighbor than well-fed beetles. Hungry beetles at the edge obtained nearly all of the food particles dropped onto the surface of the water. These results show that position preferences within groups may involve a dynamic feedback between foraging, predator avoidance, and shortterm hunger levels.     

A simulation model for Japanese sardine (Sardinops melanostictus) migrations in the western North Pacific

A two-dimensional individual-based model coupled with fish bioenergetics was developed to simulate migration and growth of Japanese sardine (Sardinops melanostictus) in the western North Pacific. In the model, fish movement is controlled by feeding and spawning migrations with passive transport by simulated ocean current. Feeding migration was assumed to be governed by search for local optimal habitats, which is estimated by the spatial distribution of net growth rate of a sardine bioenergetics model. The forage density is one of the most important factors which determines the geographical distributions of Japanese sardine during their feeding migrations. Spawning migration was modeled by an artificial neural network (ANN) with an input layer composed of five neurons that receive environmental information (surface temperature, temperature change experienced, current speed, day length and distance from land). Once the weight of the ANN was determined, the fish movement was solved by combining with the feeding migration model. To obtain the weights of the ANN, three experiments were conducted in which (1) the ANN was trained with back propagation (BP) method with optimum training data, (2) genetic algorithm (GA) was used to adjust the weights and (3) the weights of the ANN were decided by the GA with BP, respectively. BP is a supervised learning technique for training ANNs. GA is a search technique used in computing to find approximate solutions, such as optimization of parameters. Condition factor of sardine in the model is used as a factor of optimization in the GA works. The methods using only BP or GA did not work to search the appropriate weights in the ANN for spawning migration. In the third method, which is a combined approach of GA with BP, the model reproduced the most realistic spawning migration of Japanese sardine. The changes in temperature and day length are important factors for the orientation cues of Japanese sardine according to the sensitivity analysis of the weights of the ANN.