Visual cues for the retrieval of landmark memories by navigating wood ants

BACKGROUND: Even on short routes, ants can be guided by multiple visual memories. We investigate here the cues controlling memory retrieval as wood ants approach a one- or two-edged landmark to collect sucrose at a point along its base. In such tasks, ants store the desired retinal position of landmark edges at several points along their route. They guide subsequent trips by retrieving the appropriate memory and moving to bring the edges in the scene toward the stored positions. RESULTS: The apparent width of the landmark turns out to be a powerful cue for retrieving the desired retinal position of a landmark edge. Two other potential cues, the landmark's apparent height and the distance that the ant walks, have little effect on memory retrieval. A simple model encapsulates these conclusions and reproduces the ants' routes in several conditions. According to this model, the ant stores a look-up table. Each entry contains the apparent width of the landmark and the desired retinal position of vertical edges. The currently perceived width provides an index for retrieving the associated stored edge positions. The model accounts for the population behavior of ants and the idiosyncratic training routes of individual ants. DISCUSSION: Our results imply binding between the edge of a shape and its width and, further, imply that assessing the width of a shape does not depend on the presence of any particular local feature, such as a landmark edge. This property makes the ant's retrieval and guidance system relatively robust to edge occlusions.     

Invertebrate memory: wide-eyed ants retrieve visual snapshots

Ants retrieve visual memories to guide them en route to their goal. A new study shows that wood ants use object width to retrieve the correct visual memory at the appropriate position along their route. A computational model that accurately reproduces the ants' behaviour raises questions about the underlying mechanisms.     

How navigational guidance systems are combined in a desert ant

Animals use information from multiple sources in order to navigate between goals. Ants such as Cataglyphis fortis use an odometer and a sun-based compass to provide input for path integration (PI). They also use configurations of visual features to learn both goal locations and habitual routes to the goals. Information is not combined into a unified representation but appears to be exploited by separate expert guidance systems. Visual and PI goal memories are acquired rapidly and provide the consistency for route memories to be formed. Do established route memories then suppress the guidance from PI? A series of manipulations putting PI and route memories into varying levels of conflict found that ants follow compromise trajectories. The guidance systems are therefore active together and share the control of behavior. Route memories do not suppress the other guidance systems. A simple model shows that observed patterns of control could arise from a superposition of the output commands from the guidance systems, potentially approximating Bayesian inference. These results help show how an insect's relatively simple decision-making can produce navigation that is reliable and efficient and that also adapts to changing demands.     

Three-dimensional orientation in desert ants: context-independent memorisation and recall of sloped path segments

Desert ants (Cataglyphis fortis) navigate by a combination of path integration and landmark-based route memories. Their ability to correct sloped path segments to their ground distances enables them to orientate accurately even in undulating terrain. In this study, we tested whether or not ants incorporate vertical components of an itinerary into their route memory in similar ways as they do with visual landmarks and horizontal changes of direction. In two separate experiments, we trained desert ants to walk over artificial hills and later tested their acceptance of slopes within novel contexts. In the first paradigm, ants had to traverse a hill only on their outbound run, but not on their homebound trip. In a follow-up experiment, we confronted ramp-trained animals with descents in a completely new temporal and spatial context. The animals transferred their newly acquired acceptance of slopes from the outbound to the homebound run as well as to novel foraging trips. Cataglyphis obviously dissociates the experience of sloped path segments from the original context in which they appeared, thus reducing their significance as a navigational aid.     

Sex-inducing effect of a hydrophilic fraction on reproductive switching in the planarian Dugesia ryukyuensis (Seriata, Tricladida)

Background

Insects are known to rely on terrestrial landmarks for navigation. Landmarks are used to chart a route or pinpoint a goal. The distant panorama, however, is often thought not to guide navigation directly during a familiar journey, but to act as a contextual cue that primes the correct memory of the landmarks.

Results

We provided Melophorus bagoti ants with a huge artificial landmark located right near the nest entrance to find out whether navigating ants focus on such a prominent visual landmark for homing guidance. When the landmark was displaced by small or large distances, ant routes were affected differently. Certain behaviours appeared inconsistent with the hypothesis that guidance was based on the landmark only. Instead, comparisons of panoramic images recorded on the field, encompassing both landmark and distal panorama, could explain most aspects of the ant behaviours.

Conclusion

Ants navigating along a familiar route do not focus on obvious landmarks or filter out distal panoramic cues, but appear to be guided by cues covering a large area of their panoramic visual field, including both landmarks and distal panorama. Using panoramic views seems an appropriate strategy to cope with the complexity of natural scenes and the poor resolution of insects' eyes. The ability to isolate landmarks from the rest of a scene may be beyond the capacity of animals that do not possess a dedicated object-perception visual stream like primates.     

Optimal cue integration in ants

In situations with redundant or competing sensory information, humans have been shown to perform cue integration, weighting different cues according to their certainty in a quantifiably optimal manner. Ants have been shown to merge the directional information available from their path integration (PI) and visual memory, but as yet it is not clear that they do so in a way that reflects the relative certainty of the cues. In this study, we manipulate the variance of the PI home vector by allowing ants (Cataglyphis velox) to run different distances and testing their directional choice when the PI vector direction is put in competition with visual memory. Ants show progressively stronger weighting of their PI direction as PI length increases. The weighting is quantitatively predicted by modelling the expected directional variance of home vectors of different lengths and assuming optimal cue integration. However, a subsequent experiment suggests ants may not actually compute an internal estimate of the PI certainty, but are using the PI home vector length as a proxy.     

Synergy between social and private information increases foraging efficiency in ants

Insect societies integrate many information sources to organize collective activities such as foraging. Many ants use trail pheromones to guide foragers to food sources, but foragers can also use memories to find familiar locations of stable food sources. Route memories are often more accurate than trail pheromones in guiding ants, and are often followed in preference to trail pheromones when the two conflict. Why then does the system expend effort in producing and acquiring seemingly redundant and low-quality information, such as trail pheromones, when route memory is available? Here we show that, in the ant Lasius niger, trail pheromones and route memory act synergistically during foraging; increasing walking speed and straightness by 25 and 30 per cent, respectively, and maintaining trail pheromone deposition, but only when used together. Our results demonstrate a previously undescribed major role of trail pheromones: to complement memory by allowing higher confidence in route memory. This highlights the importance of multiple interacting information sources in the efficient running of complex adaptive systems.     

GSM 900 MHz radiation inhibits ants' association between food sites and encountered cues

The kinetics of the acquisition and loss of the use of olfactory and visual cues were previously obtained in six experimental colonies of the ant Myrmica sabuleti meinert 1861, under normal conditions. In the present work, the same experiments were conducted on six other naive identical colonies of M. sabuleti, under electromagnetic radiation similar to those surrounding GSM and communication masts. In this situation, no association between food and either olfactory or visual cues occurred. After a recovery period, the ants were able to make such an association but never reached the expected score. Such ants having acquired a weaker olfactory or visual score and still undergoing olfactory or visual training were again submitted to electromagnetic waves. Not only did they lose all that they had memorized, but also they lost it in a few hours instead of in a few days (as under normal conditions when no longer trained). They kept no visual memory at all (instead of keeping 10% of it as they normally do). The impact of GSM 900?MHz radiation was greater on the visual memory than on the olfactory one. These communication waves may have such a disastrous impact on a wide range of insects using olfactory and/or visual memory, i.e., on bees.     

GSM 900 MHz radiation inhibits ants' association between food sites and encountered cues

The kinetics of the acquisition and loss of the use of olfactory and visual cues were previously obtained in six experimental colonies of the ant Myrmica sabuleti meinert 1861, under normal conditions. In the present work, the same experiments were conducted on six other naive identical colonies of M. sabuleti, under electromagnetic radiation similar to those surrounding GSM and communication masts. In this situation, no association between food and either olfactory or visual cues occurred. After a recovery period, the ants were able to make such an association but never reached the expected score. Such ants having acquired a weaker olfactory or visual score and still undergoing olfactory or visual training were again submitted to electromagnetic waves. Not only did they lose all that they had memorized, but also they lost it in a few hours instead of in a few days (as under normal conditions when no longer trained). They kept no visual memory at all (instead of keeping 10% of it as they normally do). The impact of GSM 900 MHz radiation was greater on the visual memory than on the olfactory one. These communication waves may have such a disastrous impact on a wide range of insects using olfactory and/or visual memory, i.e., on bees.     

An experimental study of the foraging strategy of the wood ant Formica aquilonia

Individual foragers return to a site at which food has been discovered. This site allegiance is maintained provided that the food source is maintained. If it is not, a random search precedes discovery of an alternative source to which allegiance is transferred. Particular sites are located initially by the use of visual cues. However, such cues have a diminishing importance for orientation since, as the route becomes familiar, a spatial map is constructed from bearings of, and distances between, the major topographical features. Since ants individually learn the most economical route, this ability, together with site allegiance, results in the observed route fidelity. The foraging population established is variable and is related to the previous availability of food and consequent need of the colony. Environmental factors affect the amount of food collected and influence the size of the foraging population through the hunger of the colony. A variable colonial foraging response is dependent upon the tendency of individual nest-bound ants to forage when stimulated by an aroused replete ant returning from a successful foray. The availability of food, but apparently not its position, is communicated: recruited ants forage to remembered sites at which they have been rewarded.     

Visual Navigation during Colony Emigration by the Ant Temnothorax rugatulus

Many ants rely on both visual cues and self-generated chemical signals for navigation, but their relative importance varies across species and context. We evaluated the roles of both modalities during colony emigration by Temnothorax rugatulus. Colonies were induced to move from an old nest in the center of an arena to a new nest at the arena edge. In the midst of the emigration the arena floor was rotated 60°around the old nest entrance, thus displacing any substrate-bound odor cues while leaving visual cues unchanged. This manipulation had no effect on orientation, suggesting little influence of substrate cues on navigation. When this rotation was accompanied by the blocking of most visual cues, the ants became highly disoriented, suggesting that they did not fall back on substrate cues even when deprived of visual information. Finally, when the substrate was left in place but the visual surround was rotated, the ants'' subsequent headings were strongly rotated in the same direction, showing a clear role for visual navigation. Combined with earlier studies, these results suggest that chemical signals deposited by Temnothorax ants serve more for marking of familiar territory than for orientation. The ants instead navigate visually, showing the importance of this modality even for species with small eyes and coarse visual acuity.     

Route and landmark learning by rats searching for food

Many foraging animals rely on visual landmarks and/or habitual paths to locate important resources. We examined the degree to which rats rely on these cues when they predicted conflicting food locations. In this foraging task, rats were required to find food which could be located using either a fixed route or a nearby visual landmark. In tests, we found that their subsequent search-based estimates of the food location were the same when animals had acquired a long-term memory of the route, the landmark, or both. We show that the degree to which animals rely on the cues depends not only on the discrepancy between the two cues, but also on whether animals can match the testing “view” with a learned “view” that has been acquired during training.     

Garden ant homing behavior in a maze task based on local visual cues

Although it has been shown that visual cues play an essential role in navigation by the garden ant Lasius niger, no previous studies have addressed the way in which information from local visual cues is acquired and utilized in navigation. We found that in the absence of pheromone trails, ants whose homing motivation was triggered by feeding returned to the nest following local visual cues. In our experiments, the ants travelled through a maze to reach a feeder. They explored the maze and sometimes became trapped in its dead ends. We found that the ants more effectively used visual cues during their homeward journey if they experienced a dead end during their outward journey. This result suggested that the ants used the information acquired from visual cues during the outward journey to avoid a dead end on their return journey.     

Recognition of a familiar place by the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Recent work shows that at any one place bees detect a limited variety of simple cues in parallel. At each choice point, they recognize a few cues in the range of positions where the cues occurred during the learning process. There is no need to postulate that they re-assemble the surrounding panorama in memory; only that they retain memories of the coincidences of cues in the expected retinotopic directions. The cues could be stimuli that excite groups of peripheral visual neurons. All the experimentally known cues are described, including modulation of the receptors, the locations of areas of black or colour, the nearness, size, averaged edge orientation, and radial and tangential edges. Cues of each type are separately summed within large fields, the size of which varies with the cue. Local orientation cues from edges at right angles cancel each other within each field, which also suggests that the discrimination of shape and texture is limited. Resolution depends on lateral interactions and the number of ommatidia required for each cue. To identify a new place, a few sparse cues, together with their directions, are learned in orientation flights. When the bee returns, the cues in the panorama are progressively matched as they coincide with the cues in memory. The limited number of cues, though economical for memory, may restrict the foraging behaviour and lead to flower constancy. This kind of a visual system is a candidate model for other animals or machines with economical processing systems.     

How do insects represent familiar terrain?

We argue here that ants and bees have a piecemeal representation of familiar terrain. These insects remember no more than what is needed to sustain the separate and parallel strategies that they employ when travelling between their nest and foraging sites. One major strategy is path integration. The insect keeps a running tally of its distance and direction from the nest and so can always return home. This global path integration is enhanced by long-term memories of significant sites that insects store in terms of the coordinates (direction and distance) of these sites relative to the nest. With these memories insects can plan routes that are steered by path integration to such sites. Quite distinct from global path integration are memories associated with familiar routes. Route memories include stored views of landmarks along the route with, in some cases, local vectors linked to them. Local vectors by encoding the direction and/or distance from one landmark to the next, or from one landmark to a goal, help an insect keep to a defined route. We review experiments showing that although local vectors can be recalled by recognising landmarks, the global path integration system is independent of landmark information and that landmarks do not have positional coordinates associated with them. The major function of route landmarks is thus procedural, telling an insect what action to perform next, rather than its location relative to the nest.     

Visual scanning behaviours and their role in the navigation of the Australian desert ant Melophorus bagoti

Ants are excellent navigators, using a combination of innate strategies and learnt information to guide habitual routes. The mechanisms underlying this behaviour are little understood though one avenue of investigation is to explore how innate sensori-motor routines are used to accomplish route navigation. For instance, Australian desert ant foragers are occasionally observed to cease translation and rotate on the spot. Here, we investigate this behaviour using high-speed videography and computational analysis. We find that scanning behaviour is saccadic with pauses separated by fast rotations. Further, we have identified four situations where scanning is typically displayed: (1) by naïve ants on their first departure from the nest; (2) by experienced ants departing from the nest for their first foraging trip of the day; (3) by experienced ants when the familiar visual surround was experimentally modified, in which case frequency and duration of scans were proportional to the degree of modification; (4) when the information from visual cues is at odds with the direction indicated by the ant’s path integration system. Taken together, we see a general relationship between scanning behaviours and periods of uncertainty.     

Visual and Chemical Cues Used in Host Location and Acceptance by a Dipteran Parasitoid

Locating potential hosts for egg laying is a critical challenge in the life history of many insects. Female insects in several orders have evolved mechanisms to find hosts by using olfactory and visual signals derived from their hosts. We describe visual and chemical cues used by the dipteran parasitoid Apocephalus paraponerae (Diptera: Phoridae) in the location and acceptance of its host ant Paraponera clavata (Hymenoptera: Formicidae: Ponerinae). Our results show that A. paraponerae uses the visual cue of ant body size when locating hosts at short range and that these flies lay more eggs in ants that retain their surface chemicals than in ants with these chemicals removed. We compare the cues used by A. paraponerae with cues used by tephritid fruit flies in location and acceptance of their hosts, and we suggest further avenues for the study of host location, acceptance, and host discrimination of A. paraponerae and other parasitoids of ants.     

The Use of Edges in Visual Navigation by the Ant Leptothorax albipennis

Certain navigating insects home in on their goal by moving so that currently viewed images of landmarks fall on the same retinal locations memorized during previous visits. Here we show that ants can use similar retinotopic learning to guide lengthy routes, by memorizing and walking parallel to a distinct visual edge. We induced workers of the ant Leptothorax albipennis to travel parallel to a prominent wall. When the wall's height was changed, the ants' paths consistently shifted toward a lowered wall and away from a raised wall, as would be expected if they attempt to keep the wall's image at a constant retinal position. These path shifts were smaller than would be expected if the wall was the only guide to navigation, suggesting that other cues are also important. Significantly larger shifts were seen when edge guidance was enhanced by using two walls, one on each side of the path.     

Path integration controls nest-plume following in desert ants

The desert ant Cataglyphis fortis is equipped with sophisticated navigational skills for returning to its nest after foraging. The ant's primary means for long-distance navigation is path integration, which provides a continuous readout of the ant's approximate distance and direction from the nest. The nest is pinpointed with the aid of visual and olfactory landmarks. Similar landmark cues help ants locate familiar food sites. Ants on their outward trip will position themselves so that they can move upwind using odor cues to find food. Here we show that homing ants also move upwind along nest-derived odor plumes to approach their nest. The ants only respond to odor plumes if the state of their path integrator tells them that they are near the nest. This influence of path integration is important because we could experimentally provoke ants to follow odor plumes from a foreign, conspecific nest and enter that nest. We identified CO(2) as one nest-plume component that can by itself induce plume following in homing ants. Taken together, the results suggest that path-integration information enables ants to avoid entering the wrong nest, where they would inevitably be killed by resident ants.     

Ant navigation en route to the goal: signature routes facilitate way-finding of Gigantiops destructor

We investigated in laboratory conditions how foragers of the tropical ant Gigantiops destructor develop individually distinctive landmark routes. Way-finding along a familiar route involved the recognition of at least two locations, nest and feeding site, and the representation of spatial relations between these places. Familiar visual landmarks were important both at the beginning and at the end of the foraging journey. A motor routine guided the ants at the start of their foraging path towards the first landmarks, which they learnt to pass consistently on the same side, before taking the next direction. At the last stage of the route, landmark recognition allowed them to pinpoint their preferred feeding site without using distant cues or odometric information. By contrast, ants en route to the goal were not systematically guided by a stereotyped sequence of snapshots recalled at each corresponding stage of the route. Each ant slalomed in an idiosyncratic distinctive way around different midway landmarks from a foraging excursion to the next, which induced a variability of the path shapes in their intermediate parts. By reducing the number of landmark recognition-triggered responses, this economical visuomotor strategy may be helpful in the Amazonian forest where many prominent landmarks are alike.