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.     

The hidden spiral: systematic search and path integration in desert ants,Cataglyphis fortis

The main navigational mechanism used by foraging desert ants of the genus Cataglyphis is path integration (dead reckoning). Any such egocentric system of navigation is prone to cumulative navigational errors. Hence, while homing Cataglyphis might have reset its path integration system and yet not arrived at the start of its foraging excursion, the nest entrance. Then it resorts to piloting or performs a systematic search for the nest. The search pattern consists of a system of loops of ever increasing size centred about the origin, i.e. the start of the search. Here we show that underlying the system of loops is a spiral search programme that gets transformed into the observed pattern of loops by the ant's idiosyncratic path-integration algorithm. The ant starts to follow a spiral course, then breaks off this course and walks towards the centre, i.e. to what its path-integration system has computed to be the origin of the search. This reset episode is followed by another spiral course, which is terminated by the next reset, and so forth. After each reset, the spiral gets wider, so that the whole pattern expands. Futhermore, every now and then the spiral might change its sign. Computer simulations based on these simple rules lead to search patterns of the kind actually recorded in Cataglyphis ants. These patterns ensure that those parts of the area in which the target (nest entrance) is most likely to be located are searched most heavily; in other words: the search density profile is adapted to the probability density function of the target.     

Homing by path integration in the spider Agelena labyrinthica Clerck

Moving about the web the spider Agelena labyrinthica continuously adjusts the prospective return angle. The amount of path integration was indicated by two compromise angles, return angle e and goal angle (Fig. 2). The spider was primed to one of two perpendicular light azimuths, L1 or L2. Subsequently, the discrete effects of a 90° change in light azimuth on the return direction were recorded (Fig. 3). When primed to L1, and the spider was exposed to L2: (1) while homebound, the deviation from straight home was clockwise and largest, (2) both while outbound and returning, the deviation was smallest (Fig. 4), (3) while outbound, either during the first or second half of the outbound run, the deviations were between those obtained in (1) and (2). When the spider was primed to L1, but given L2 while outbound and L1 again while homebound, Agelena deviated counterclockwise, the most with L2 on during the entire outbound run, and less when L2 was available only during a portion of the outbound run. The degree of adjustment of the home path direction is not correlated with the actual path length but with the shortest distance (bee line) between the two points during which the spider was exposed to one of the two light azimuths.On fellowship leave from Hunter College of the City University of New York, Department of Psychology, New York, NY 10021, USA     

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.     

View-based navigation in Hymenoptera: multiple strategies of landmark guidance in the approach to a feeder

In order to analyse how landmarks guide the last stages of an insect's approach to a goal, we recorded many flights of individual wasps and honeybees as they flew to an inconspicuous feeder on the ground that was marked by one or by two nearby landmarks. An individual tends to approach the feeder from a constant direction, flying close to the ground. Its body is oriented in roughly the same horizontal direction during the approach so that the feeder and landmarks are viewed over a narrow range of directions. Consequently, when the insect arrives at the feeder, the landmarks take up a standard position on the retina. Three navigational strategies govern the final approach. The insect first aims at a landmark, treating it as a beacon. Secondly, bees learn the appearance of a landmark with frontal retina and they associate with this stored view a motor trajectory which brings them from the landmark sufficiently close to the goal that it can be reached by image matching. Insects then move so as to put the landmark in its standard retinal position. Image matching is shown to be accomplished by a control system which has as set points the standard retinal position of the landmark and some parameter related to its retinal size. Accepted: 1 March 1997     

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.     

Spatial memory, navigation and dance behaviour in Apis mellifera

Navigation and dance communication in Apis mellifera have been extensively studied on the level of sensory processing, but the structure and content of the spatial memory underlying such phenomena have yet to be addressed. Here we survey new findings indicating that the memory used by bees to navigate within the range of their orientation flights is much more complex than hitherto thought. It appears to allow them to decide between at least two goals in the field, and to steer towards them over considerable distances. Two models concerning the structure of bees’ spatial memory are developed from new empirical evidence. The first one relies on the integration of at least two flight vectors, while the second assumes the existence of a ‘functional’ map based on the information available on-site. These findings also raise questions about the process of encoding and decoding information in the context of the waggle dance. We review published data and recent evidence indicating that memories of topographical features might also be involved in dance communication, and point out what needs to be addressed to elucidate the corresponding memory demands. The flight paths of recruited bees can now be traced by means of radar techniques, and thus tools are available to tackle these questions.     

The night-time temporal window of locomotor activity in the Namib Desert long-distance wandering spider, Leucorchestris arenicola

Even though being active exclusively after sunset, the male Leucorchestris arenicola spiders are able to return to their point of departure by following bee-line routes of up to several hundreds of meters in length. While performing this kind of long-distance path integration they must rely on external cues to adjust for navigational errors. Many external cues which could be used by the spiders change dramatically or disappear altogether in the transition period from day to night. Hence, it is therefore imperative to know exactly when after sunset the spiders navigate in order to find out how they do it. To explore this question, we monitored their locomotor activity with data loggers equipped with infrared beam sensors. Our results show that the male spiders are most active in the period between the end and the beginning of the astronomical twilight period. Moreover, they prefer the moonless, i.e. darkest times at night. Hence, we conclude that the males are truly—and extremely—nocturnal. We further show that they are able to navigate under the very dim light conditions prevailing on moonless nights, and thus do not have to rely on the moon or on moon-related patterns of polarised light as potential compass cues.     

Behavioral ecology of odometric memories in desert ants: acquisition, retention, and integration

Assuming that the acquisition and retention of memories havecosts, properties of memories should fit the functional requirementsfor the system of memory. Based on a functional analysis ofwhat path integration is meant to do, we predicted that odometricmemories in desert ants should show (1) little improvement withrepeated training: performance should be as good after one trainingtrial as after six training trials, (2) decay of memory after24 h, and (3) performance based solely on the most recent outboundtrip, with no integration over multiple memories. Desert ants(Cataglyphis fortis) traveled in narrow straight plastic channelsto forage for cookie crumbs in a feeder at 6- or 12-m distance.Each ant was tested once by being taken from the feeder andreleased 2 m from the end of a 32-m channel to run home. Thedistance at which the ant first turned back (first turn) constitutedthe data. In acquisition, groups trained one or six times beforebeing tested had unsystematic scatter that did not differ significantly.In retention, ants tested after a 24-h delay showed larger unsystematicscatter than control animals tested after no delay. In integration,ants were trained five times at 6 or 12 m and then tested at12 or 6 m, respectively. No evidence of integration of multipleodometric memories was found. The results show that the propertiesof odometric memories are indeed tailored to what the memorysystem is used for.     

Optokinetic speed control and estimation of travel distance in walking honeybees

Honeybees returning from foraging trips were video-filmed while they walked through a narrow transparent gangway to reach the hive entrance. On their way they were presented with black-and-white gratings viewed underneath as well as to both sides of the gangway. Bees could exit the gangway through one of two or three side exits installed at different distances from the gangway entrance. In one set of experiments, the substrate on which the bees walked was moved either in the bee's direction or against it. In another set of experiments, the substrate was stationary, but the pattern was moved in one or the other direction. The bee's walking speed (WS) was evaluated from the video tapes. When the substrate moved against, or the pattern in the bee's direction, in either case decreasing the speed of pattern flow (PFS), the bees increased WS, and, at the same time, they preferred the more distant exit. When the substrate moved in, or the pattern against the bee's direction, thus increasing PFS, WS decreased and the bees preferred the nearer exit. These results suggest that the speed of optic flow controls the speed of locomotion and might therefore also serve for assessing the distance travelled.Abbreviations PFS pattern-flow speed - WS walking speed Dedicated to Hans-Jochen Autrum, editor emeritus, for help in giving birth to this and many other papers over very many years, often with criticism but nevertheless with encouragement and sympathy.     

Whole-field integration, not detailed analysis, is used by the crab optokinetic system to separate rotation and translation in optic flow

For optimal visual control of compensatory eye movements during locomotion it is necessary to distinguish the rotational and translational components of the optic flow field. Optokinetic eye movements can reduce the rotational component only, making the information contained in the translational flow readily available to the animal. We investigated optokinetic eye rotation in the marble rock crab, Pachygrapsus marmoratus, during translational movement, either by displacing the animal or its visual surroundings. Any eye movement in response to such stimuli is taken as an indication that the system is unable to separate the translational and the rotational components in the optic flow in a mathematically perfect way. When the crabs are translated within a pseudo-natural environment, eye movements are negligible, especially during sideways translation. When, however, crabs were placed in a gangway between two elongated rectangular sidewalls carrying dotted patterns which were translated back and forth, marked eye movements were elicited, depending on the translational velocity. To resolve this discrepancy, we tested several hypotheses about mechanisms using detailed analysis of the optic flow or whole-field integration. We found that the latter are sufficient to explain the efficient separation of translation and rotation of crabs in quasi-natural situations. Accepted: 6 May 1997     

Review: Depth, navigation and orientation in crabs: Angular acceleration, gravity and hydrostatic pressure sensing during path integration

This review shows how well the published work on the neural basis of balance and hydrostatic pressure reception in crabs agrees with the analyses and models of path integration. Fiddler crabs allow analyses at the level of behaviour. With considerable accuracy, they continuously show the direction to home with their body orientation and use idiothetic path integration to calculate a home vector from the internal measurements of their locomotion. All crabs have a well-developed vestibular system in the statocyst with horizontal and vertical canals which is used for angular acceleration sensing and depth reception. Large identified interneurones abstract the component of angular acceleration in one of the three orthogonal planes. These have properties consistent with a key role in path integration, combining vestibular and proprioceptor information with a central excitatory drive from the hemiellipsoid bodies. They have been monitored during walking, swimming and even in freefall for a 22 s period in parabolic flight.     

Desert ants: is active locomotion a prerequisite for path integration?

Desert ants Cataglyphis fortis have been shown to be able to employ two mechanisms of distance estimation: exploiting both optic flow and proprioceptive information. This study aims at understanding possible interactions between the two possibly redundant mechanisms of distance estimation. We ask whether in Cataglyphis the obviously minor contribution of optic flow would increase or even take over completely if the ants were deprived of reliable proprioceptive information. In various experimental paradigms ants were subjected to passive horizontal displacements during which they perceived optic flow, but were prohibited from active locomotion. The results show that in desert ants active locomotion is essential for providing the ants’ odometer and hence its path integrator with the necessary information.     

On the integration of subthreshold inputs from Perforant Path and Schaffer Collaterals in hippocampal CA1 pyramidal neurons

Using a realistic model of a CA1 hippocampal pyramidal neuron, we make experimentally testable predictions on the roles of the non-specific cation current, I _h , and the A-type Potassium current, I _A , in modulating the temporal window for the integration of the two main excitatory afferent pathways of a CA1 neuron, the Schaffer Collaterals and the Perforant Path. The model shows that the experimentally observed increase in the dendritic density of I _h and I _A could have a major role in constraining the temporal integration window for these inputs, in such a way that a somatic action potential (AP) is elicited only when they are activated with a relative latency consistent with the anatomical arrangement of the hippocampal circuitry.