Making learning easy: the acquisition of visual information during the orientation flights of social wasps

The flights of individual wasps (Vespula) were recorded as they approached a small feeder on the ground that was marked by a black cylinder ca 15 cm away. Two navigational strategies are used in these approaches. Initially, the wasp aims at the cylinder, treating it as a beacon and fixating it with frontal retina. In the last stage of the flight, the wasp assumes a preferred orientation so that the cylinder takes up a constant, more peripheral retinal position as the wasp nears the feeder. Path guidance by image-matching is likely to be limited to this final segment of the return. Wasps could gain the information needed for these distinct navigational strategies during the learning flights that they perform on their initial departures from the feeder. They fly away from the feeder in a series of arcs while turning at a mean angular velocity of 226°/s. The cylinder tends to be viewed with frontal retina during the arcs suggesting that the information required for aiming at the cylinder is acquired then. For image matching, the appearance of the cylinder needs to be learnt when the wasp is in the orientation that it adopts close to the feeder on its return flight. Wasps tend to assume this orientation during learning flights while they face the feeder. Such inspections of the feeder occur at the ends of arcs when a wasp's turning velocity is low.     

Landmark learning and visuo-spatial memories in gerbils

The aim of this study is to understand what a rodent (Meriones unguiculatus) learns about the geometrical relations between a goal and nearby visual landmarks and how it uses this information to reach a goal. Gerbils were trained to find sunflower seeds on the floor of a light-tight, black painted room illuminated by a single light bulb hung from the ceiling. The position of the seed on the floor was specified by an array of one or more landmarks. Once training was complete, we recorded where the gerbils searched when landmarks were present but the seed was absent. In such tests, gerbils were confronted either with the array of landmarks to which they were accustomed or with a transformation of this array. Animals searched in the appropriate spot when trained to find seeds placed in a constant direction and at a constant distance from a single cylindrical landmark. Since gerbils look in one spot and not in a circle centred on the landmark, the direction between landmark and goal must be supplied by cues external to the landmark array. Distance, on the other hand, must be measured with respect to the landmark. Tests in which the size of the landmark was altered from that used in training suggest that distance is not learned solely in terms of the apparent size of the landmark as seen from the goal. Gerbils can still reach a goal defined by an array of landmarks when the room light is extinguished during their approach. This ability implies that they have already planned a trajectory to the goal before the room is darkened. In order to compute such a trajectory, their internal representation of landmarks and goal needs to contain information about the distances and bearings between landmarks and goal. For planning trajectories, each landmark of an array can be used separately from the others. Gerbils trained to a goal specified by an array of several landmarks were tested with one or more of the landmarks removed or with the array expanded. They then searched as though they had computed an independent trajectory for each landmark. For instance, gerbils trained with an array of two landmarks were tested with the distance between two landmarks doubled. The animals then searched for seeds in two positions, which were at the correct distance and in the right direction from each landmark.(ABSTRACT TRUNCATED AT 400 WORDS)     

Approaching and departing bees learn different cues to the distance of a landmark

Bees learn both the absolute distance and the apparent size of landmarks in the vicinity of a foraging site. They learn about landmarks both when approaching and when leaving the site. Whereas learning on arrival can take place on every visit to the food source, learning on departure is limited to the first few visits, when the bee Turns Back and Looks (TBL) at the feeder in a stereotyped manoeuvre before flying off. We investigated whether one specific function of TBLs is to acquire information about the absolute distance of landmarks from the feeding site. Bees were trained to forage from a feeder which lay at a fixed distance from a cylinder. During training, bees were exposed to the cylinder either only while they approached and landed on the feeder, or only on their departure from it, or at both of these times. Tests on trained bees immediately after the TBL phase revealed that those bees which had viewed the cylinder only on arrival had learnt the apparent size of the cylinder, but not its distance from the feeder. In contrast, bees which saw the cylinder on departure had learnt its absolute distance. They also learnt the cylinder's apparent size, provided that the cylinder was close to the feeder. Bees which had viewed the cylinder on arrival as well as on departure learnt both absolute distance and apparent size. Distance dominated the bees' behaviour in the initial phase of learning, apparent size was more important later on. We suggest that early during learning bees need information about the 3-D structure of the environment so that they can identify those landmarks close to a foraging site which will specify accurately the site's position. This information is acquired during TBLs. Later, landmark guidance can be achieved by 2-D image matching.     

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.     

Target-directed Orientation in Displaced Honeybees

Under sunny weather conditions, displaced honeybees (Apis mellifera) usually fly into the celestial compass direction and thus may be misled from their goal, or they are disorientated. Under cloudy conditions, they may determine the celestial compass direction from prominent landmarks. They may also fly directly toward their goal from a release site. In two experiments, we investigated the orientation of displaced bees when a landmark (target) was close to the goal under different weather conditions. It is shown that in sunny conditions, the celestial compass will override target orientation under most conditions. Under 100% cloud cover, the celestial compass direction retrieved from landmarks modulates target-orientated behaviour but is not by itself a primary orientation factor. The bees will fly toward a previously encountered landmark that signals the target, and in case of several similar landmarks which are visible to the bees, they will choose the one in the direction nearest the celestial compass direction. The results indicate that honeybee orientation is the result of a set of context-specific interdependent orientation mechanisms.     

Landmark maps for honeybees

Experiments by Fabre (1915), Thorpe (1950), Chmurzynski (1964), and most recently Gould (1986) suggest that insects have maps of their terrain which enable them to find their way directly to a goal when they are displaced several hundred metres from it. This paper discusses what might constitute an insect's map in terms of a two-part computational model. The first part describes how an insect reaches a goal when the insect is sufficiently close that it can see some of the landmarks which are visible from the goal. The second part considers the problem of navigating when there is no similarity between the view from the release-site and the view from the goal.We start from a model designed to explain how a bee might return to a goal using a two-dimensional snapshot of the landscape seen from the goal (Collett and Cartwright 1983). To guide its return, the model bee continuously compares its snapshot with its current retinal image and moves so as to reduce the discrepancy between the two. Bees can only be guided in the right direction by the difference between current retinal image and snapshot when there is some resemblance between the two. In a realistically cluttered world, snapshot and retinal image become very dis-similar only a short distance from the goal.To increase the distance from which a model bee can return, the bee takes two snapshots at the goal. The first snapshot excludes landmarks near to the goal and the second snapshot includes them. With close landmarks filtered from both snapshot and retinal image, the match between the two deteriorates gradually as the bee moves away from the goal. A model bee using a filtered snapshot and image finds its way back to the neighbourhood of the goal from a relatively long distance (Fig. 2). The bee then switches to the second snapshot and is guided to the precise spot by its memory of the close landmarks.For longer range guidance, the model bee is equipped with an album of snapshots, each taken at a different location within the terrain. Linked to each snapshot is a vector encoding the distance and direction from the place where the snapshot was taken to the hive. When the bee is displaced to a new position, it selects the snapshot which best matches its current image and follows the associated home-vector back to the hive (Fig. 3). Such a hive-centred map can also be used to devise novel routes to places other than the hive. For instance, a bee can reach a foraging site from anywhere in its terrain by adding the home-vector recalled at the starting position to a vector specifying the distance and direction of the foraging site from the hive. The sum of these two vectors defines a direct trajectory to the foraging site.     

Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera)

Bees and wasps are known to use a visual representation of the nest environment to guide the final approach to their nest. It is also known that they acquire this representation during an orientation flight performed on departure.A detailed film analysis shows that orientation flights in solitary wasps of the genus Cerceris consist of a systematic behavioural sequence: after lift-off from the nest entrance, wasps fly in ever increasing arcs around the nest. They fly along these arcs obliquely to their long axis and turn so that the nest entrance is held in the left or right visual field at retinal positions between 30° and 70° from the midline. Horizontal distance from the nest and height above ground increase throughout an orientation flight so that the nest is kept at retinal elevations between 45° and 60° below the horizon. The wasps' rate of turning is constant at between 100°/s and 200°/s independent of their distance from the nest and their ground velocity increases with distance. The consequence of this is that throughout the flight wasps circle at a constant angular velocity around the nest.Orientation flights are strongly influenced by landmark lay-out. Wasps adjust their flight-path and their orientation in a way that allows them to fixate the nest entrance and to hold the closest landmark in their frontal visual field.The orientation flight generates a specific topography of motion parallax across the visual field. This could be used by wasps to acquire a series of snapshots that all contain the nest position, to acquire snapshots of close landmarks only (distance filtering), to exclude shadow contours from their visual representation (figure-ground discrimination) or to gain information on the distance of landmarks relative to the nest.     

Landmark orientation during the approach to the nest in the stingless beeTrigona (Tetragonisca) angustula (Apidae,Meliponinae)

Summary We displaced a small nest box containing stingless bees (Trigona (Tetragonisca)angustula) over distances of up to 1.6 meters in different directions and counted the numbers of returning foragers to measure the effects of this manipulation on the homing ability of bees. Bees find it hard to locate the nest box when it was displaced more than about 1 m backwards, forwards or sideways relative to the direction into which the nest entrance pointed. They do not find the nest when its height above ground is changed. The bees use landmarks in the vicinity of the nest to locate it: When the nest box is displaced and landmark positions are changed so that their angular position at the new nest site is the same as at the normal nest position their homing ability is less impaired than it is without changes in landmark positions. Our results show that the bees do not use the nest box itself as a landmark until they have approached the nest position to within about 1 meter with the aid of surrounding landmarks.     

Spatial memory in a food storing corvid

This work suggests how food storing corvids use spatial memory to relocate caches, and how they can do this after some landmarks surrounding caches have become hidden due to leaf fall, snow fall or plant growth. Experiments involved training European jays (Garrulus glandarius) to find buried food, the location of which was specified by an array of 12 landmarks. Tests were then performed with the array rotated, or with certain landmarks removed from the array. The main findings were: (1) birds primarily remembered the position of the goal using the near tall landmarks (15–30 cm from the goal and 20 cm high); (2) birds obtained a sense of direction both from the landmark array and something external to the array; (3) birds did not use smell or marks in the surface of the ground to find the goal. Memory of near tall landmarks is likely to be functional for these birds since (a) nearer landmarks provide a more accurate fix, and (b) taller landmarks are less likely to be completely obscured by snow fall, leaf fall or intervening vegetation. The work also demonstrates the use of G.I.S. software for the analysis and representation of animal search patterns.     

Foraging navigation of hornets studied in natural habitats and laboratory experiments

Foraging flights have been studied in three species of hornets (Vespa mandarinia, V. simillima and V. analis) in the field and the laboratory. Hornets seem to use multiple navigational cues for visiting a familiar feeding place. They could orient towards the feeding place immediately after they rose in air from the nest without directly viewing the feeder. They could visit the feeding place after dark at a luminosity 8 lux. These data suggest that they can navigate for some distance with few external cues. Hornets also seem to rely on visual cues for their mid-range navigation. They used some structures on their way as navigational landmarks to negotiate. Individual hornets are supposed to have their own landmarks. Olfactory cues seem to be used to find a new feeding place or to recruit other member. In the approach flight hornets seemed to use multiple visual cues such as the visual characteristics of the feeder and the wider scenery around the feeder. Even if the feeder in training was removed during the test, they flew with a smooth course as if they were pin-pointing the missing feeder, but without sitting on the ground. Hornets learnt how to fly to reach the feeder without external cues after passing by the last visual landmark under conditions with extremely poor visual cues. The present work suggests that hornets retain multiple navigational cues during repeated foraging behavior, and which cues they use seems to depend upon environmental conditions.     

Some psychophysics of the pigeon's use of landmarks

1. Three pigeons (Columba livia) were trained to find hidden food in a sunken well (3.3 cm in diameter) at a constant place within an (160 cm x 160 cm) experimental box (Fig. 1). After learning the location, the animals were tested occasionally with the well and food absent. Landmarks in the experimental box might be transformed on such tests. 2. Changing the height or width of a nearby landmark had no systematic influence on the position of peak search. Translating a nearby landmark, however, led to a shift in peak search position. All three birds then searched most somewhere between the original goal location, as defined by the unmoved landmarks, and the goal location as defined by the shifted landmark. Within a limited range of landmark shift, the peak shift as a function of landmark shift is linear (Fig. 3). 3. To explain the data (Fig. 7), the pigeon records at the location of the goal the algebraic vectors from a number of landmarks to the goal. These vectors have both a direction and a distance component. When searching for the goal again in the experimental box, it computes independently for each landmark a navigation vector. This is arrived at by vector-adding the algebraic vector from the bird's current position to the landmark in question, supplied by perception, to the corresponding landmark-goal vector in its record. The pigeon moves in the direction and distance specified by a weighted average of the independently calculated navigation vectors. For positive vector weights, vector geometry guarantees that the bird would search somewhere between the original goal and the goal according to the shifted landmark. The extent to which it shifts toward the shifted goal reflects the vector weight given to the shifted landmark.     

Neural systems for landmark-based wayfinding in humans

Humans and animals use landmarks during wayfinding to determine where they are in the world and to guide their way to their destination. To implement this strategy, known as landmark-based piloting, a navigator must be able to: (i) identify individual landmarks, (ii) use these landmarks to determine their current position and heading, (iii) access long-term knowledge about the spatial relationships between locations and (iv) use this knowledge to plan a route to their navigational goal. Here, we review neuroimaging, neuropsychological and neurophysiological data that link the first three of these abilities to specific neural systems in the human brain. This evidence suggests that the parahippocampal place area is critical for landmark recognition, the retrosplenial/medial parietal region is centrally involved in localization and orientation, and both medial temporal lobe and retrosplenial/medial parietal lobe regions support long-term spatial knowledge.     

Visual landmarks and route following in desert ants

Summary Little is known about the way in which animals far from home use familiar landmarks to guide their homeward path. Desert ants, Cataglyphis spp., which forage individually over long distances are beginning to provide some answers. We find that ants running 30 m from a feeding place to their nest memorise the visual characteristics of prominent landmarks which lie close to their path. Although remembered visual features are used for identifying a landmark and for deciding whether to go to its left or right, they are not responsible for the detailed steering of an ant's path. The form of the trajectory as an ant approaches and detours around a landmark seems to be controlled by the latter's immediate retinal size; the larger it is, the greater the ant's turning velocity away from the landmark.     

The use of visual landmarks by gerbils: Reaching a goal when landmarks are displaced

Summary Gerbils (Meriones unguiculatus) can specify the location of a goal by means of visual landmarks and will return to such a goal from different starting positions in the vicinity of the landmarks. To discover whether landmark-cues are used continuously during an approach to the goal, gerbils were trained to forage for sunflower seeds close to a single illuminated light-bulb on the floor of an arena. As they approached the bulb, it was switched off and another bulb in a variable position with respect to the first turned on. On 52 out of 71 trials the gerbils changed their trajectory (latency ca. 240 ms) to aim for the newly lit bulb (Fig. 1 A, B). On the remaining trials, gerbils maintained their original course towards the first bulb as though it were still lit and then paused after a longer delay before eventually changing direction (Fig. 1C). Thus, an approach to a beacon is usually under continuous visual control. This ensures that the gerbil will reach its goal correctly despite any inaccuracies in its initial computation of its approach.When switches were made between more complex arrays of landmarks, the gerbils' behaviour was less clear-cut. Possible reasons for this difference are suggested.     

A lightweight keypoint matching framework for insect wing morphometric landmark detection

Geometric morphometrics has become an important approach in insect morphology studies because it capitalizes on advanced quantitative methods to analyze shape. Shape could be digitized as a set of landmarks from specimen images. However, the existing tools mostly require manual landmark digitization, and previous works on automatic landmark detection methods do not focus on implementation for end-users. Motivated by that, we propose a novel approach for automatic landmark detection, based on visual features of landmarks and keypoint matching techniques. While still archiving comparable accuracy to that of the state-of-the-art method, our framework requires less initial annotated data to build prediction model and runs faster. It is lightweight also in terms of implementation, in which a four-step workflow is provided with user-friendly graphical interfaces to produce correct landmark coordinates both by model prediction and manual correction. The utility iMorph is freely available at https://github.com/ha-usth/InsectWingLandmark, currently supporting Windows, MacOS, and Linux.     

The problem of assessing landmark error in geometric morphometrics: theory, methods, and modifications

Geometric morphometric methods rely on the accurate identification and quantification of landmarks on biological specimens. As in any empirical analysis, the assessment of inter- and intra-observer error is desirable. A review of methods currently being employed to assess measurement error in geometric morphometrics was conducted and three general approaches to the problem were identified. One such approach employs Generalized Procrustes Analysis to superimpose repeatedly digitized landmark configurations, thereby establishing whether repeat measures fall within an acceptable range of variation. The potential problem of this error assessment method (the "Pinocchio effect") is demonstrated and its effect on error studies discussed. An alternative approach involves employing Euclidean distances between the configuration centroid and repeat measures of a landmark to assess the relative repeatability of individual landmarks. This method is also potentially problematic as the inherent geometric properties of the specimen can result in misleading estimates of measurement error. A third approach involved the repeated digitization of landmarks with the specimen held in a constant orientation to assess individual landmark precision. This latter approach is an ideal method for assessing individual landmark precision, but is restrictive in that it does not allow for the incorporation of instrumentally defined or Type III landmarks. Hence, a revised method for assessing landmark error is proposed and described with the aid of worked empirical examples.     

Using artificial evolution and selection to model insect navigation.

BACKGROUND: An animal's behavioral strategies are often constrained by its evolutionary history and the resources available to it. Artificial evolution allows one to manipulate such constraints and explore how they influence evolved strategies. Here we compare the navigational strategies of flying insects with those of artificially evolved "animats" endowed with various motor architectures. Using evolutionary algorithms, we generated artificial neural networks that controlled a virtual animat's navigation within a 2D, simulated world. Like a flying insect, the animat possessed motors that generated thrust and torque, a compass, and visual sensors. Some animats were limited to forward motion, while others could also move sideways. Animats were selected for the precision with which they reached a target specified by a visual landmark. RESULTS: Animats given sideways motors could alter flight direction without changing body orientation and evolved strategies similar to those of flying bees or wasps performing the same task. Both animats and insects first aimed at the landmark. In the last phase, both adopted a fixed body orientation and adjusted their position to keep the landmark at a fixed retinal location. Animats unable to uncouple flight direction and body orientation evolved subtly different strategies and performed less robustly. CONCLUSIONS: This convergence between the navigational strategies of animals and animats suggests that the insect's strategies are primarily an adaptation to the demands of using visual information and compass direction to reach a position in space and that they are not significantly compromised by the insect's evolutionary history.     

Landmark Use by Cebus apella

We investigated the use of landmarks by capuchins to solve spatial search tasks. In Experiment 1 one subject learned to find a hidden reward in the middle of a 4-landmark configuration. During probe trials, with the landmark configuration expanded and no reward, the capuchin mainly searched near 2 of the 4 landmarks, thus showing it used the landmarks as beacons. In Experiment 2 two subjects learned to find a reward halfway between 2 landmarks, with the inter-landmark line variously oriented with respect to the room. During probe trials, with the landmark configuration expanded and no reward, the capuchins no longer searched in the middle of the landmark configuration. The capuchins searched between the landmarks, but at the training distance from each landmark separately. To do so, the capuchins may have memorized a certain distance to cover, beginning from a landmark, or exploited different types of perceptual information. Therefore, the capuchins use nearby landmarks to locate a goal, but not configurationally. We compare the results with those of previous studies with other animal species and discuss them in relation to issues of spatial cognition.     

Influence of visual targets and landmarks on honey bee foraging and waggle dancing

Animals use diverse sensory stimuli to navigate their environment and to recognize rewarding food sources.Honey bees use visual atributes of the targeted food source,such as its color,shape,size,direction and distance from the hive,and the landmarks around it to navigate during foraging.They transmit the location information of the food source to other bees if it is highly rewarding.To investigate the relative importance of these attributes,we trained bees to feeders in two different experiments.In the first experiment,we asked whether bees prefer to land on(a)a similar feeder at a different distance on the same heading or on(b)a visually distinct feeder located at the exact same location.We found that,within a short foraging range,bees relied heavily on the color and the shape of the food source and to a lesser extent on its distance from the hive.In the second experiment,we asked if moving the main landmark or the feeder(visual target)influenced recruitment dancing for the feeder.We found that foragers took longer to land and danced fewer circuits when the location of the food source,or a major landmark associated with it,changed.These results demonstrate that prominent visual atributes of food sources and landmarks are evidently more reliable than distance information and that foraging bees heavily utilize these visual cues at the later stages of their journey.     

Snapshot memories and landmark guidance in wood ants

Insects are thought to pinpoint a place by using memorized "snapshots," i.e., two-dimensional retinotopic views of the surrounding landmarks recorded when at the place (reviewed in ). Insects then reach the place by moving until their current view matches their snapshot. To determine when snapshots are recalled, and how differences between view and snapshot are translated into appropriate movements, we analyzed the approaches of wood ants to a feeding site that was located in the center of an array of two or three cylinders. In ants, contrary to flying hymenopterans, body orientation and direction of travel are collinear, so that an ant approaching an object always looks at it with frontal visual field. On their way to a food site, ants fixated and approached a cylinder predominantly when its angular size was smaller than when viewed from the food site. This finding implies that ants store snapshots at this place while fixating landmarks with frontal retina, so simplifying the later alignment of snapshots with their current view. It also means that ants recall snapshots well in advance of reaching the place. Although snapshots are centered on a landmark, we show that they extend at least 120 degrees into the periphery.