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.     

Local vectors in desert ants: context-dependent landmark learning during outbound and homebound runs

Desert ants, Cataglyphis fortis, associate nestward-directed vector memories (local vectors) with the sight of landmarks along a familiar route. This view-based navigational strategy works in parallel to the self-centred path integration system. In the present study we ask at what temporal stage during a foraging journey does the ant acquire nestward-directed local vector information from feeder-associated landmarks: during its outbound run to a feeding site or during its homebound run to the nest. Tests performed after two reversed-image training paradigms revealed that the ants associated such vectors exclusively with landmarks present during their homebound runs.     

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: one-way routes rather than maps

In recent years, there has been an upsurge of interest and debate about whether social insects-central-place foragers such as bees and ants-acquire and use cognitive maps, which enable the animal to steer novel courses between familiar sites . Especially in honey bees, it has been claimed that these insects indeed possess such "general landscape memories" and use them in a "map-like" way . Here, we address this question in Australian desert ants, Melophorus bagoti, which forage within cluttered environments full of nearby and more distant landmarks. Within these environments, the ants establish landmark-based idiosyncratic routes from the nest to their feeding sites and select different one-way routes for their outbound and inbound journeys. Various types of displacement experiments show that inbound ants when hitting their inbound routes at any particular place immediately channel in and follow these routes until they reach the nest, but that they behave as though lost when hitting their habitual outbound routes. Hence, familiar landmarks are not decoupled from the context within which they have been acquired and are not knitted together in a more general and potentially map-like way. They instruct the ants when to do what rather than provide them with map-like information about their position in space.     

Memory use in insect visual navigation

The navigational strategies that are used by foraging ants and bees to reach a goal are similar to those of birds and mammals. Species from all these groups use path integration and memories of visual landmarks to navigate through familiar terrain. Insects have far fewer neural resources than vertebrates, so data from insects might be useful in revealing the essential components of efficient navigation. Recent work on ants and bees has uncovered a major role for associative links between long-term memories. We emphasize the roles of these associations in the reliable recognition of visual landmarks and the reliable performance of learnt routes. It is unknown whether such associations also provide insects with a map-like representation of familiar terrain. We suggest, however, that landmarks act primarily as signposts that tell insects what particular action they need to perform, rather than telling them where they are.     

A new navigational mechanism mediated by ant ocelli

Many animals rely on path integration for navigation and desert ants are the champions. On leaving the nest, ants continuously integrate their distance and direction of travel so that they always know their current distance and direction from the nest and can take a direct path to home. Distance information originates from a step-counter and directional information is based on a celestial compass. So far, it has been assumed that the directional information obtained from ocelli contribute to a single global path integrator, together with directional information from the dorsal rim area (DRA) of the compound eyes and distance information from the step-counter. Here, we show that ocelli mediate a distinct compass from that mediated by the compound eyes. After travelling a two-leg outbound route, untreated foragers headed towards the nest direction, showing that both legs of the route had been integrated. In contrast, foragers with covered compound eyes but uncovered ocelli steered in the direction opposite to the last leg of the outbound route. Our findings suggest that, unlike the DRA, ocelli cannot by themselves mediate path integration. Instead, ocelli mediate a distinct directional system, which buffers the most recent leg of a journey.     

Learning and time‐dependent cue choice in the desert ant,Melophorus bagoti

Foraging ants are known to use multiple sources of information to return to the nest. These cue sets are employed by independent navigational systems including path integration in the case of celestial cues and vision‐based learning in the case of terrestrial landmarks and the panorama. When cue sets are presented in conflict, the Australian desert ant species, Melophorus bagoti, will choose a compromise heading between the directions dictated by the cues or, when navigating on well‐known routes, foragers choose the direction indicated by the terrestrial cues of the panorama against the dictates of celestial cues. Here, we explore the roles of learning terrestrial cues and delays since cue exposure in these navigational decisions by testing restricted foragers with differing levels of terrestrial cue experience with the maximum (180°) cue conflict. Restricted foragers appear unable to extrapolate landmark information from the nest to a displacement site 8 m away. Given only one homeward experience, foragers can successfully orient using terrestrial cues, but this experience is not sufficient to override a conflicting vector. Terrestrial cue strength increases with multiple experiences and eventually overrides the celestial cues. This appears to be a dynamic choice as foragers discount the reliability of the terrestrial cues over time, reverting back to preferring the celestial vector when the forager has an immediate vector, but the forager's last exposure to the terrestrial cues was 24 hr in the past. Foragers may be employing navigational decision making that can be predicted by the temporal weighting rule.     

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.     

Route learning by insects

Ants and other insects often follow fixed routes from their nest to a foraging site. The shape of an ant's route is set, initially, by navigational strategies, such as path integration and the ant's innate responses to landmarks, which depend minimally on memory. With increasing experience, these early routes are stabilised through the learning of views of landmarks and of associated actions. The substitution of memory-based strategies makes an insect's route more robust and precise. The ability to select between different learnt routes might incur additional memory requirements to those needed for performing a route, and lead to the associative grouping of those memories that relate to a particular route.     

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.     

Use of Long-Term Stored Vector Information in the Neotropical Ant <Emphasis Type="BoldItalic">Gigantiops destructor</Emphasis>

We investigated how the formicine ant Gigantiops destructor can use vector information to navigate within the cluttered environment of the rain forest. Displaced foragers use skylight information to move in the theoretical feeder-to-nest direction, whether they are prevented from updating their path-integrator during foraging or captured at the departure from their nest, i.e. with a current accumulator state very close to zero. Only ants that have collected food are able to download a long-term stored reference vector pointing in the nest direction, irrespective of the current accumulator state of their path-integrator stored in a working memory and independent of familiar landmarks. Depending on the release sites, ants that became lost at a maximum distance of 50 cm could still hit and recognize their familiar route, or they engaged in a systematic search for it centered on the release sites. In contrast to Cataglyphis desert ants, Gigantiops ants do not rely primarily on the current accumulator state of their egocentric path integrator. Such a long-term vector-based navigation primed by food capture is well adapted for a tropical ant foraging during periods spanning several hours. This could prevent the numerous cumulative errors in the evaluation of the angles steered that might result from a continuously running path-integrator operating during complex foraging patterns performed at ground or arboreal levels and during passive displacement in response to heavy rain.     

Landmark cues can change the motivational state of desert ant foragers

Desert ants of the genus Cataglyphis rely on path integration vectors to return to the nest (inbound runs) and back to frequently visited feeding sites (outbound runs). If disturbed, e.g., experimentally displaced on their inbound runs, they continue to run off their home-bound vector, but if disturbed in the same way on their outbound runs, they do not continue their feeder-based vector, but immediately switch on the home-bound state of their path integration vector and return to the nest. Here we show that familiar landmarks encountered by the ants during their run towards the feeder can change the ants’ motivational state insofar that the ants even if disturbed continue to run in the nest-to-feeder direction rather than reverse their courses, as they do in landmark-free situations. Hence, landmark cues can cause the ants to change their motivational state from homing to foraging.     

Views,landmarks, and routes: how do desert ants negotiate an obstacle course?

The Australian desert ant Melophorus bagoti often follows stereotypical routes through a cluttered landscape containing both distant panoramic views and obstacles (plants) to navigate around. We created an artificial obstacle course for the ants between a feeder and their nest. Landmarks comprised natural objects in the landscape such as logs, branches, and tussocks. Many ants travelled stereotypical routes home through the obstacle course in training, threading repeatedly the same gaps in the landmarks. Manipulations altering the relations between the landmarks and the surrounding panorama, however, affected the routes in two major ways. Both interchanging the positions of landmarks (transpositions) and displacing the entire landmark set along with the starting position of the ants (translations) (1) reduced the stereotypicality of the route, and (2) increased turns and meanders during travel. The ants might have used the entire panorama in view-based travel, or the distal panorama might prime the identification and use of landmarks en route. Despite the large data set, both options (not mutually exclusive) remain viable.     

Traveling in clutter: Navigation in the Central Australian desert ant Melophorus bagoti

The Central Australian desert ant Melophorus bagoti is the most thermophilic ant on the continent. It comes out to forage during the hottest part of the day in the summer months. The ant shares a cluttered, plant-filled habitat with other arthropods and uses a range of navigational strategies. We review recent studies on this species concerning its use of habitual routes, distant landmarks, landmarks around the nest, and path integration, which is keeping track of the distance and direction traveled from one's starting point. Functional predictions concerning the acquisition, retention, and integration of memories of distances and of landmarks are also reviewed, illuminating the behavioral ecology of spatial cognition.     

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.     

Looking and homing: how displaced ants decide where to go

We caught solitary foragers of the Australian Jack Jumper ant, Myrmecia croslandi, and released them in three compass directions at distances of 10 and 15 m from the nest at locations they have never been before. We recorded the head orientation and the movements of ants within a radius of 20 cm from the release point and, in some cases, tracked their subsequent paths with a differential GPS. We find that upon surfacing from their transport vials onto a release platform, most ants move into the home direction after looking around briefly. The ants use a systematic scanning procedure, consisting of saccadic head and body rotations that sweep gaze across the scene with an average angular velocity of 90° s⁻¹ and intermittent changes in turning direction. By mapping the ants’ gaze directions onto the local panorama, we find that neither the ants’ gaze nor their decisions to change turning direction are clearly associated with salient or significant features in the scene. Instead, the ants look most frequently in the home direction and start walking fast when doing so. Displaced ants can thus identify home direction with little translation, but exclusively through rotational scanning. We discuss the navigational information content of the ants’ habitat and how the insects’ behaviour informs us about how they may acquire and retrieve that information.     

Visual cue learning and odometry in guiding the search behavior of desert ants, Melophorus bagoti, in artificial channels

Terrestrial panoramic cues, path integration and search behavior are the main navigational strategies used by ants to locate food and find their way back to the nest. Searching becomes important when the other navigational cues are either not available or cannot provide sufficient information to pinpoint the goal. When searching in one-dimensional channels Melophorus bagoti ants exhibit a systematic drift in the starting-point-to-goal direction as they turn back and forth, sometimes past the goal location ( Narendra et al., 2008). Here we show that this drift in channels is not a stereotypical part of the search behavior in these ants. It rather depends on the conditions of training. In experiments in which the nest entrance is located not at the end but at the side of the channel, forward drift is not always part of the nest search. Experiments on food searches showed that with the food source at the end of the channel, ants performed a linear drift in the starting-point-to-food direction. With food at the side of the channel, they showed a less pronounced drift toward the food source. In this constrained environment, especially with the goal at the end of the channel, ants seem to learn a routine such as ‘run along the channel’, and mix this routine with their usual strategy of turning back and forth in search.     

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.     

Wüstennavigatoren en miniature

Desert navigators en miniature Cataglyphis, a strictly diurnal, heat‐tolerant, high‐speed desert ant, employs a path integrator as its main navigational means. By continually measuring directions steered and distances covered the path integrator computes a navigation vector, which can lead the ant directly back to its central place, the nest, and to any point which it has visited before. The path integration vector receives compass information from the pattern of polarized light in the sky (via a set of specialized photoreceptors at the dorsal rim of the eye), and derives information about travel distance from a stride integrator (pedometer) and an optic‐flow meter exploiting self‐induced image motion across the ventral retina. The path integrator is fully functional already at the beginning of the ant's foraging life. Later it keeps running whenever the ant is on a foraging excursion irrespective of whether other navigational tools are at work as well. Finally it provides a scaffold for landmark learning. View‐based landmark information is acquired by taking panoramic “snapshots” at certain places and routes. By comparing this memorized visual information with the actual one received during later journeys the ants are able to return to familiar places and to follow familiar routes even without the aid of the path integrator. The ant's navigational performances known to date can be simulated by designing a decentralized network, in which the individual tools are interconnected in flexible and context dependent ways.     

How do insects use path integration for their navigation?

 We combine experimental findings on ants and bees, and build on earlier models, to give an account of how these insects navigate using path integration, and how path integration interacts with other modes of navigation. At the core of path integration is an accumulator. This is set to an initial state at the nest and is updated as the insect moves so that it always reports the insect's current position relative to the nest. Navigation that uses path integration requires, in addition, a way of storing states of the accumulator at significant places for subsequent recall as goals, and a means of computing the direction to such goals. We discuss three models of how path integration might be used for this process, which we call vector navigation. Vector navigation is the principal means of navigating over unfamiliar terrain, or when landmarks are unavailable. Under other conditions, insects often navigate by landmarks, and ignore the output of the vector navigation system. Landmark navigation does not interfere with the updating of the accumulator. There is an interesting symmetry in the use of landmarks and path integration. In the short term, vector navigation can be independent of landmarks, and landmark navigation needs no assistance from path integration. In the longer term, visual landmarks help keep path vector navigation calibrated, and the learning of visual landmarks is guided by path integration. Received: 6 June 1999 / Accepted in revised form: 20 March 2000