Influence of habitat complexity on route learning among different populations of climbing perch (Anabas testudineus Bloch, 1792)

Animals use different behavioral strategies to maximize their fitness in the natural environment. Learning and memory are critical in this context, allowing organisms to flexibly and rapidly respond to environmental changes. We studied how the physical characteristics of the native habitat influence the spatial learning capacity of Anabas testudineus belonging to four different populations collected from two streams and two ponds, in a linear maze. Stream fish were able to learn the route faster than pond fish irrespective of the presence or absence of landmarks in the maze. However, climbing perch collected from ponds learned the route faster in the maze provided with landmarks than in Plain maze. The results indicate that fish inhabiting a lotic ecosystem use egocentric cues in route learning rather than visual cues like landmarks. A local landmark may be a more reliable cue in route learning in a relatively stable habitat like a pond. In flowing aquatic systems, water flow may continually disrupt the visual landscape and thus landmarks as visual cues become unreliable. Spatial learning is thus a fine-tuned response to the complexity of the habitat and early rearing conditions may influence the spatial learning ability in fish.     

Homing pigeons develop local route stereotypy

The mechanisms used by homing pigeons (Columba livia) to navigate homeward from distant sites have been well studied, yet the mechanisms underlying navigation within, and mapping of, the local familiar area have been largely neglected. In the local area pigeons pote ntially have access to a powerful navigational aid--a memorized landscape map. Current opinion suggests that landmarks are used only to recognize a familiar start position and that the goalward route is then achieved solely using compass orientation. We used high-resolution global positioning system (GPS) loggers to track homing pigeons as they became progressively familiar with a local homing task. Here, we demonstrate that birds develop highly stereotyped yet individually distinctive routes over the landscape, which remain substantially inefficient. Precise aerial route recapitulation implies close control by localized geocentric cues. Magnetic cues are unlikely to have been used, since recapitulation remains despite magnetic disruption treatment, and olfactory cues would have been positionally unstable under the variable wind conditions, making visual landmarks the most likely cues used.     

Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena

Whether pigeons use visual landmarks for orientation from familiar locations has been a subject of debate. By recording the directional choices of both anosmic and control pigeons while exiting from a circular arena we were able to assess the relevance of olfactory and visual cues for orientation from familiar sites. When the birds could see the surroundings, both anosmic and control pigeons were homeward oriented. When the view of the landscape was prevented by screens that surrounded the arena, the control pigeons exited from the arena approximately in the home direction, while the anosmic pigeons' distribution was not different from random. Our data suggest that olfactory and visual cues play a critical, but interchangeable, role for orientation at familiar sites.     

When Does Previewing the Landscape Affect Pigeon Homing?

The importance of visual landmarks during homing in pigeons (Columba livia) remains a contentious issue. Three experiments which explore the role of visual landmarks at release sites are reported here. The effects of releasing homing pigeons after a 5-minute period in either a clear or an opaque sided release box were investigated. In the clear sided box pigeons were able to observe local surroundings at a release site, but this view was obstructed in the opaque sided box. In experiment 1 pigeons were released from familiar locations close to home (between 2 and 5.6 km): being unable to view landmarks prior to release significantly slowed homing speeds. In experiment 2 pigeons were released at familiar locations further from home (between 8.4 and 10 km): being unable to view landmarks prior to release did not significantly affect homing speeds. In experiment 3 pigeons were trained to home from distant release sites but were tested at closer, unfamiliar sites located on the likely homing routes used by the pigeons in training. No significant difference in homing speeds were observed when pigeons were released from either the clear or opaque sided box. The significance of these results for understanding the role of visual landmarks within a pigeon's familiar area is discussed.     

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.     

Group decisions and individual differences: route fidelity predicts flight leadership in homing pigeons (Columba livia)

How social-living animals make collective decisions is currently the subject of intense scientific interest, with increasing focus on the role of individual variation within the group. Previously, we demonstrated that during paired flight in homing pigeons, a fully transitive leadership hierarchy emerges as birds are forced to choose between their own and their partner''s habitual routes. This stable hierarchy suggests a role for individual differences mediating leadership decisions within homing pigeon pairs. What these differences are, however, has remained elusive. Using novel quantitative techniques to analyse habitual route structure, we show here that leadership can be predicted from prior route-following fidelity. Birds that are more faithful to their own route when homing alone are more likely to emerge as leaders when homing socially. We discuss how this fidelity may relate to the leadership phenomenon, and propose that leadership may emerge from the interplay between individual route confidence and the dynamics of paired flight.     

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.     

Not just passengers: pigeons,Columba livia,can learn homing routes while flying with a more experienced conspecific

For animals that travel in groups, the directional choices of conspecifics are potentially a rich source of information for spatial learning. In this study, we investigate how the opportunity to follow a locally experienced demonstrator affects route learning by pigeons over repeated homing flights. This test of social influences on navigation takes advantage of the individually distinctive routes that pigeons establish when trained alone. We found that pigeons learn routes just as effectively while flying with a partner as control pigeons do while flying alone. However, rather than learning the exact route of the demonstrator, the paired routes shifted over repeated flights, which suggests that the birds with less local experience also took an active role in the navigational task. The efficiency of the original routes was a key factor in how far they shifted, with less efficient routes undergoing the greatest changes. In this context, inefficient routes are unlikely to be maintained through repeated rounds of social transmission, and instead more efficient routes are achieved because of the interaction between social learning and information pooling.     

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.     

Learning multiple routes in homing pigeons

The aerial lifestyle of central-place foraging birds allows wide-ranging movements, raising fundamental questions about their remarkable navigation and memory systems. For example, we know that pigeons (Columba livia), long-standing models for avian navigation, rely on individually distinct routes when homing from familiar sites. But it remains unknown how they cope with the task of learning several routes in parallel. Here, we examined how learning multiple routes influences homing in pigeons. We subjected groups of pigeons to different training protocols, defined by the sequence in which they were repeatedly released from three different sites, either sequentially, in rotation or randomly. We observed that pigeons from all groups successfully developed and applied memories of the different release sites (RSs), irrespective of the training protocol, and that learning several routes in parallel did not impair their capacity to quickly improve their homing efficiency over multiple releases. Our data also indicated that they coped with increasing RS uncertainty by adjusting both their initial behaviour upon release and subsequent homing efficiency. The results of our study broaden our understanding of avian route following and open new possibilities for studying learning and memory in free-flying animals.     

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.     

Differential Recruitment of Brain Networks following Route and Cartographic Map Learning of Spatial Environments

An extensive neuroimaging literature has helped characterize the brain regions involved in navigating a spatial environment. Far less is known, however, about the brain networks involved when learning a spatial layout from a cartographic map. To compare the two means of acquiring a spatial representation, participants learned spatial environments either by directly navigating them or learning them from an aerial-view map. While undergoing functional magnetic resonance imaging (fMRI), participants then performed two different tasks to assess knowledge of the spatial environment: a scene and orientation dependent perceptual (SOP) pointing task and a judgment of relative direction (JRD) of landmarks pointing task. We found three brain regions showing significant effects of route vs. map learning during the two tasks. Parahippocampal and retrosplenial cortex showed greater activation following route compared to map learning during the JRD but not SOP task while inferior frontal gyrus showed greater activation following map compared to route learning during the SOP but not JRD task. We interpret our results to suggest that parahippocampal and retrosplenial cortex were involved in translating scene and orientation dependent coordinate information acquired during route learning to a landmark-referenced representation while inferior frontal gyrus played a role in converting primarily landmark-referenced coordinates acquired during map learning to a scene and orientation dependent coordinate system. Together, our results provide novel insight into the different brain networks underlying spatial representations formed during navigation vs. cartographic map learning and provide additional constraints on theoretical models of the neural basis of human spatial representation.     

The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback

The capacity to learn enables animals to match their phenotypic response to a changing environment on the basis of experience but learning is likely to incur costs such as the cost of making mistakes or the energetic cost of processing information. Little is known about how animals optimize the use of learned behaviour within their natural environments such that potential costs are minimized. We investigated whether the use of local landmarks in learning orientation routes by the three-spined stickleback, Gasterosteus aculeatus, varied in response to the visual stability of their natural habitats. Sticklebacks collected from five fast-flowing rivers and five ponds were trained to locate a hidden reward in a T-maze. Locating the reward required the fish to learn a body-centred algorithmic behaviour (turn left or right) or to follow plant landmarks. Probe trials, in which these cues conflicted, revealed which spatial cue the fish was using. Pond fish appeared to rely more than river fish on visual landmarks, which is consistent with the suggestion that even within a species, learned behaviour is fine-tuned in response to local environmental conditions. Landmarks may be reliable indicators of location only in stable pond habitats. In rivers, turbulence and flow may continually disrupt the visual landscape such that river fish may benefit from learning orientation routes only if learning is constrained so that unreliable visual cues are ignored. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Deciding to learn: modulation of learning flights in honeybees, <Emphasis Type="Italic">Apis mellifera</Emphasis>

Upon discovering new sources of food, honeybees and other insects perform learning flights to memorize visual landmarks that can guide their return. Learning flights are longest following initial visits to the food and subsequently decline in duration, which suggests that the investment in learning results from an active decision modulated by a bee's accumulating experience. We document various factors that influence this decision: (1). learning flights reappear when experienced bees encounter a delay in finding food at a familiar place and the durations of such "reorientation flights" increase with the length of the delay; (2). the decay in learning flight duration over visits following such reorientation flights is more rapid than following initial discovery of the food; (3). learning flight duration increases with the visual complexity of the scene surrounding the food, and when spatial relationships among landmarks are unstable; and (4). durations of learning flights at a new feeding place are influenced by the sucrose concentration in the food. Taken together, these experiments suggest that bees can adjust their learning efforts in response to changing needs for visual information and that both sources of spatial uncertainty and the quality of the food influence the value of such information.     

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.     

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.     

Two spatial memories for honeybee navigation

Insect navigation is thought to be based on an egocentric reference system which relates vector information derived from path integration to views of landmarks experienced en route and at the goal. Here we show that honeybees also possess an allocentric form of spatial memory which allows localization of multiple places relative to the intended goal, the hive. The egocentric route memory, which is called the specialized route memory (SRM) here, initially dominates navigation when an animal is first trained to a feeding site and then released at an unexpected site and this is why it is the only reference system detected so far in experiments with bees. However, the SRM can be replaced by an allocentric spatial memory called the general landscape memory (GLM). The GLM is directly accessible to the honeybee (and to the experimenter) if no SRM exists, for example, if bees were not trained along a route before testing. Under these conditions bees return to the hive from all directions around the hive at a speed comparable to that of an equally long flight along a trained route. The flexible use of the GLM indicates that bees may store relational information on places, connections between landmarks and the hive and/or views of landmarks from different directions and, thus, the GLM may have a graph structure, at least with respect to one goal, i.e. the hive.     

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.     

Extremely detoured migration in an inexperienced bird: interplay of transport costs and social interactions

We tagged two juvenile short‐toed eagles in southern Italian peninsula with GPS satellite transmitters. According to previous visual observations, two different migratory routes for Italian short‐toed eagles to reach Africa in autumn have been proposed: via Sicily and via Gibraltar. These routes include different over‐water distances to cross the Mediterranean Sea, and thus different proportions of flight modes (soaring–gliding vs flapping–gliding) with resulting different transport costs. Considering different scenarios of energy cost of transport, with flapping–gliding flight over water being more costly than flying over land using soaring–gliding flight, we predicted a maximum optimal detour of 1218 km. Both individuals reached Africa using the longest, detoured, route, avoiding the longest water crossing. To achieve this they began migrating northwards, keeping for ca 700 km a direction opposite to that followed by any other migrating bird from the Northern hemisphere in autumn. The comparison of optimal detour predictions with observed migratory tracks suggests that this migratory strategy prioritizes not only energy minimization, but also safety, given the mortality risk associated with the sea crossing. Finally, it is unlike that these inexperienced individuals followed such a complex route relying only on endogenous information and we therefore suggest, also on the basis of field observations, that social interactions (adult guidance) allow these individuals to learn the detoured route.     

Which portion of the natural panorama is used for view-based navigation in the Australian desert ant?

Ants that forage in visually rich environments often develop idiosyncratic routes between their nest and a profitable foraging ground. Such route knowledge is underpinned by an ability to use visual landmarks for guidance and place recognition. Here we ask which portions of natural visual scenes are essential for visually guided navigation in the Australian desert ant Melophorus bagoti whose foragers navigate through a habitat containing grass tussocks, shrubs and trees. We captured M. bagoti foragers after they had returned to their nest from a feeder, but before they had entered their nest, and tested their ability to home accurately from a series of release locations. We used this simple release paradigm to investigate visually guided navigation by monitoring the accuracy of nestwards orientation when parts of the ants’ visual field were obscured. Results show that the lower portion of the visual panorama is more important for visually guided homing than upper portions. Analysis of panoramic images captured from the release and nest locations support the hypothesis that the important visual information is provided by the panoramic contour, where terrestrial objects contrast against sky, rather than by a limited number of salient landmarks such as tall trees.