On the 'cognitive map debate' in insect navigation.

In a historical account recently published in this journal Dhein argues that the current debate whether insects like bees and ants use cognitive maps (centralized map hypothesis) or other means of navigation (decentralized network hypothesis) largely reflects the classical debate between American experimental psychologists à la Tolman and German ethologists à la Lorenz, respectively. In this dichotomy we, i.e., the proponents of the network hypothesis, are inappropriately placed on the Lorenzian line. In particular, we argue that in contrast to Dhein's claim our concepts are not based on merely instinctive or peripheral modes of information processing. In general, on the one side our approaches have largely been motivated by the early biocybernetics way of thinking. On the other side they are deeply rooted in studies on the insect's behavioral ecology, i.e., in the ecological setting within which the navigational strategies have evolved and within which the animal now operates. Following such a bottom-up approach we are not "anti-cognitive map researchers" but argue that the results we have obtained in ants, and also the results of some decisive experiments in bees, can be explained and simulated without the need of invoking metric maps.

Optimal multiguidance integration in insect navigation.

In the last decades, desert ants have become model organisms for the study of insect navigation. In finding their way, they use two major navigational routines: path integration using a celestial compass and landmark guidance based on sets of panoramic views of the terrestrial environment. It has been claimed that this information would enable the insect to acquire and use a centralized cognitive map of its foraging terrain. Here, we present a decentralized architecture, in which the concurrently operating path integration and landmark guidance routines contribute optimally to the directions to be steered, with "optimal" meaning maximizing the certainty (reliability) of the combined information. At any one time during its journey, the animal computes a path integration (global) vector and landmark guidance (local) vector, in which the length of each vector is proportional to the certainty of the individual estimates. Hence, these vectors represent the limited knowledge that the navigator has at any one place about the direction of the goal. The sum of the global and local vectors indicates the navigator's optimal directional estimate. Wherever applied, this decentralized model architecture is sufficient to simulate the results of quite a number of diverse cue-conflict experiments, which have recently been performed in various behavioral contexts by different authors in both desert ants and honeybees. They include even those experiments that have deliberately been designed by former authors to strengthen the evidence for a metric cognitive map in bees.

Cataglyphis meets Drosophila.

In Cataglyphis and Drosophila - in desert ants and fruit flies - research on visually guided behavior took different paths. While work in Cataglyphis started in the field and covered the animal's wide navigational repertoire, in Drosophila the initial focus was on a particular kind of visual control behavior scrutinized within the confines of the laboratory arena, before research concentrated on more advanced behaviors. In recent times, these multi-pronged approaches in flies and ants increasingly converge, both conceptually and methodologically, and thus lay the ground for combined neuroethological efforts. In spite of the obvious differences in the behavioral repertoire of these two groups of insects, likely commonalities in the navigational processes and underlying neuronal circuitries are increasingly coming to the fore.

The Cataglyphis Mahrèsienne: 50 years of Cataglyphis research at Mahrès.

Every year since 1969, research groups from Zürich have spent the summer months in the barren sandy areas around the Tunisian village Mahrès to study the navigational behaviour of Cataglyphis desert ants, its sensory underpinnings, and ecophysiological settings. From the 1990s onwards, researchers from other countries were invited to join the Zürich group, so that Cataglyphis increasingly advanced to become a model organism for the study of animal navigation. Its cockpit became the focus of a dynamic research system, an 'epistemic thing', as modern parlance in the philosophy of science has it. Investigations aimed at the ants' compasses and odometers, at path integration, view-based landmark guidance, and how information from these various navigational routines is combined in computing the courses to steer. In this multifaceted work, the researchers' familiarity with the site, with Mahrès, and its local geographical and historical conditions, has been essential. The essay briefly retraces the historical development of this research system. After the system had been firmly established at the North African Mahrès site, it was extended to the ecological equivalents of Cataglyphis in other true deserts of the world, to Ocymyrmex in the Namib Desert of southern Africa, and to Melophorus in central Australia.

Early foraging life: spatial and temporal aspects of landmark learning in the ant Cataglyphis noda.

Within the powerful navigational toolkit implemented in desert ants, path integration and landmark guidance are the key routines. Here, we use cue-conflict experiments to investigate the interplay between these two routines in ants, Cataglyphis noda, which start their foraging careers (novices) with learning walks and are then tested at different stages of experience. During their learning walks, the novices take nest-centered views from various directions around the nest. In the present experiments, these learning walks are spatially restricted by arranging differently sized water moats around the nest entrance and thus, limiting the space available around the nest and the nest-feeder route. First, we show that the ants are able to return to the nest by landmark guidance only when the novices have had enough space around the nest entrance for properly performing their learning walks. Second, in 180° cue-conflict situations between path integration and landmark guidance, path integration dominates in the beginning of foraging life (after completion of the learning walks), but with increasing numbers of visits to a familiar feeder landmark guidance comes increasingly into play.

Species-specific differences in the fine structure of learning walk elements in Cataglyphis ants.

Cataglyphis desert ants are famous navigators. Like all central place foragers, they are confronted with the challenge to return home, i.e. relocate an inconspicuous nest entrance in the ground, after their extensive foraging trips. When leaving the underground nest for the first time, desert ants perform a striking behavior, so-called learning walks that are well structured. However, it is still unclear how the ants initially acquire the information needed for sky- and landmark-based navigation, in particular how they calibrate their compass system at the beginning of their foraging careers. Using high-speed video analyses, we show that different Cataglyphis species include different types of characteristic turns in their learning walks. Pirouettes are full or partial rotations (tight turns about the vertical body axis) during which the ants frequently stop and gaze back in the direction of the nest entrance during the longest stopping phases. In contrast, voltes are small walked circles without directed stopping phases. Interestingly, only Cataglyphis ant species living in a cluttered, and therefore visually rich, environment (i.e. C. noda and C. aenescens in southern Greece) perform both voltes and pirouettes. They look back to the nest entrance during pirouettes, most probably to take snapshots of the surroundings. In contrast, C. fortis inhabiting featureless saltpans in Tunisia perform only voltes and do not stop during these turns to gaze back at the nest - even if a set of artificial landmarks surrounds the nest entrance.

Early ant trajectories: spatial behaviour before behaviourism.

In the beginning of the twentieth century, when Jacques Loeb's and John Watson's mechanistic view of life started to dominate animal physiology and behavioural biology, several scientists with different academic backgrounds got engaged in studying the wayfinding behaviour of ants. Largely unaffected by the scientific spirit of the time, they worked independently of each other in different countries: in Algeria, Tunisia, Spain, Switzerland and the United States of America. In the current literature on spatial cognition these early ant researchers--Victor Cornetz, Felix Santschi, Charles Turner and Rudolf Brun--are barely mentioned. Moreover, it is virtually unknown that the great neuroanatomist Santiago Ramón y Cajal had also worked on spatial orientation in ants. This general neglect is certainly due to the fact that nearly all these ant researchers were scientific loners, who did their idiosyncratic investigations outside the realm of comparative physiology, neurobiology and the behavioural sciences of the time, and published their results in French, German, and Spanish at rather inaccessible places. Even though one might argue that much of their work resulted in mainly anecdotal evidence, the conceptual approaches of these early ant researchers preempt much of the present-day discussions on spatial representation in animals.

Steering intermediate courses: desert ants combine information from various navigational routines.

A number of systems of navigation have been studied in some detail in insects. These include path integration, a system that keeps track of the straight-line distance and direction travelled on the current trip, the use of panoramic landmarks and scenery for orientation, and systematic searching. A traditional view is that only one navigational system is in operation at any one time, with different systems running in sequence depending on the context and conditions. We review selected data suggesting that often, different navigational cues (e.g., compass cues) and different systems of navigation are in operation simultaneously in desert ant navigation. The evidence suggests that all systems operate in parallel forming a heterarchical network. External and internal conditions determine the weights to be accorded to each cue and system. We also show that a model of independent modules feeding into a central summating device, the Navinet model, can in principle account for such data. No central executive processor is necessary aside from a weighted summation of the different cues and systems. Such a heterarchy of parallel systems all in operation represents a new view of insect navigation that has already been expressed informally by some authors.

Ontogeny of learning walks and the acquisition of landmark information in desert ants, Cataglyphis fortis.

At the beginning of their foraging lives, desert ants (Cataglyphis fortis) are for the first time exposed to the visual world within which they henceforth must accomplish their navigational tasks. Their habitat, North African salt pans, is barren, and the nest entrance, a tiny hole in the ground, is almost invisible. Although natural landmarks are scarce and the ants mainly depend on path integration for returning to the starting point, they can also learn and use landmarks successfully to navigate through their largely featureless habitat. Here, we studied how the ants acquire this information at the beginning of their outdoor lives within a nest-surrounding array of three artificial black cylinders. Individually marked 'newcomers' exhibit a characteristic sequence of learning walks. The meandering learning walks covering all directions of the compass first occur only within a few centimeters of the nest entrance, but then increasingly widen, until after three to seven learning walks, foraging starts. When displaced to a distant test field in which an identical array of landmarks has been installed, the ants shift their search density peaks more closely to the fictive goal position, the more learning walks they have performed. These results suggest that learning of a visual landmark panorama around a goal is a gradual rather than an instantaneous process.

Life as a cataglyphologist--and beyond.

Rüdiger Wehner's lifelong research activities centered on Cataglyphis have rendered these thermophilic desert ants model organisms in the study of animal navigation. The present account describes how the author encountered Cataglyphis and established a study site at Maharès, Tunisia; how he increasingly focused his research on the neuroethological analysis of the ant's navigational toolkit; and finally, how he extended these studies to thermophilic desert ants in other deserts of the world, to Ocymyrmex in southern Africa and Melophorus in central Australia. By including aspects of functional morphology, physiology, and ecology in his research projects, he has favored-and advocated-an organism-centered approach. Beyond "cataglyphology," he was engaged in substantial teaching both at his home university in Zürich and overseas, writing a textbook, running a department, and working as a Permanent Fellow at the Institute for Advanced Study in Berlin.

Group recruitment in a thermophilic desert ant, Ocymyrmex robustior.

Thermophilic desert ants-Cataglyphis, Ocymyrmex, and Melophorus species inhabiting the arid zones of the Palaearctic region, southern Africa and central Australia, respectively-are solitary foragers, which have been considered to lack any kind of chemical recruitment. Here we show that besides mainly employing the solitary mode of food retrieval Ocymyrmex robustior regularly exhibits group recruitment to food patches that cannot be exploited individually. Running at high speed to recruitment sites that may be more than 60 m apart from the nest a leading ant, the recruiter, is followed by a loose and often quite dispersed group of usually 2-7 recruits, which often overtake the leader, or may lose contact, fall back and return to the nest. As video recordings show the leader, while continually keeping her gaster in a downward position, intermittently touches the surface of the ground with the tip of the gaster most likely depositing a volatile pheromone signal. These recruitment events occur during the entire diurnal activity period of the Ocymyrmex foragers, that is, even at surface temperatures of more than 60 °C. They may provide promising experimental paradigms for studying the interplay of orientation by chemical signals and path integration as well as other visual guidance routines.

Vector-based and landmark-guided navigation in desert ants of the same species inhabiting landmark-free and landmark-rich environments.

The central Australian desert ant Melophorus bagoti lives in a visually cluttered semi-arid habitat dotted with grass tussocks, bushes and trees. Previously, it was shown that this species has a higher propensity to switch from vector-based navigation to landmark-guided navigation compared with the North African desert ant Cataglyphis fortis, which usually inhabits a visually bare habitat. Here, we asked whether different colonies of M. bagoti, inhabiting more and less cluttered habitats, show a similar difference. We compared ants from typically cluttered habitats with ants from an exceptional nest located in an open field largely devoid of vegetation. Ants from both kinds of nests were trained to forage from a feeder and were then displaced to a distant test site on the open field. Under these conditions, ants from cluttered habitats switched more readily from vector-based navigation to landmark-guided navigation than ants from the open field. Thus, intraspecific differences caused by the experience of particular landmarks encountered en route, or of particular habitats, influence navigational strategies in addition to previously found interspecific, inherited differences due to the evolutionary history of living in particular habitats.

Cataglyphis desert ants improve their mobility by raising the gaster.

We analyze theoretically the moment of inertia of the desert ant Cataglyphis (C. bicolor and C. fortis) around a vertical axis through its own center of mass when the animal raises its gaster to a vertical position. Compared to the value when the gaster is horizontal, the moment of inertia is reduced to one half; this implies that when increasing its angular acceleration the ant need apply only half the level of torque when the gaster is raised, compared to when the gaster is lowered. As an example, we analyze the cases of an ant running on circular and sinusoidal paths. In both cases, the ant must apply a sideways thrust, anti-roll and anti-pitch torques to avoid toppling, and, on the circular path when accelerating and throughout the sinusoidal trajectory, a torque to enable turning as the path curves. When the ant is accelerating in a very tight circle or running on a very narrow sinusoidal path, in which the amplitude of the sinusoid is less than the length of the ant's body, the forces required for the turning torque can equal and exceed those required for the sideways thrust, and can be reduced significantly by the ant raising the gaster, whereas the foot-thrust for the anti-roll and anti-pitch torques rises only modestly when the gaster is up. This suggests that there may be an evolutionary advantage for employing the gaster-raising mode of locomotion, since this habit will allow desert ants to use lower forces and less energy, and perhaps run faster on more tortuous paths.

No need for a cognitive map: decentralized memory for insect navigation.

In many animals the ability to navigate over long distances is an important prerequisite for foraging. For example, it is widely accepted that desert ants and honey bees, but also mammals, use path integration for finding the way back to their home site. It is however a matter of a long standing debate whether animals in addition are able to acquire and use so called cognitive maps. Such a 'map', a global spatial representation of the foraging area, is generally assumed to allow the animal to find shortcuts between two sites although the direct connection has never been travelled before. Using the artificial neural network approach, here we develop an artificial memory system which is based on path integration and various landmark guidance mechanisms (a bank of individual and independent landmark-defined memory elements). Activation of the individual memory elements depends on a separate motivation network and an, in part, asymmetrical lateral inhibition network. The information concerning the absolute position of the agent is present, but resides in a separate memory that can only be used by the path integration subsystem to control the behaviour, but cannot be used for computational purposes with other memory elements of the system. Thus, in this simulation there is no neural basis of a cognitive map. Nevertheless, an agent controlled by this network is able to accomplish various navigational tasks known from ants and bees and often discussed as being dependent on a cognitive map. For example, map-like behaviour as observed in honey bees arises as an emergent property from a decentralized system. This behaviour thus can be explained without referring to the assumption that a cognitive map, a coherent representation of foraging space, must exist. We hypothesize that the proposed network essentially resides in the mushroom bodies of the insect brain.

Vector-based and landmark-guided navigation in desert ants inhabiting landmark-free and landmark-rich environments.

Two species of desert ants - the North African Cataglyphis fortis and the central Australian Melophorus bagoti - differ markedly in the visual complexity of their natural habitats: featureless salt pans and cluttered, steppe-like terrain, respectively. Here we ask whether the two species differ in their navigational repertoires, in particular, whether in homing they place different emphasis on their vector-based and landmark-based routines. In trying to answer this question, we applied the same experimental paradigms to individual foragers of either species on either continent: training and/or testing with and/or without artificial landmark arrays. We found that the open-terrain species C. fortis runs off its (path integration) home vector much more readily even in unfamiliar landmark settings than the cluttered-terrain species M. bagoti. These data support the hypothesis that C. fortis has a higher propensity to rely on vector-mediated navigation, whereas in the same experimental situations M. bagoti more easily switches to landmark-guided behaviour. In the actual navigational performances, such species-specific propensities are most likely shaped by environment-dependent individual experiences.

Antennal-lobe organization in desert ants of the genus Cataglyphis.

Desert ants of the genus Cataglyphis possess remarkable visual navigation capabilities. Although Cataglyphis species lack a trail pheromone system, Cataglyphis fortis employs olfactory cues for detecting nest and food sites. To investigate potential adaptations in primary olfactory centers of the brain of C. fortis, we analyzed olfactory glomeruli (odor processing units) in their antennal lobes and compared them to glomeruli in different Cataglyphis species. Using confocal imaging and 3D reconstruction, we analyzed the number, size and spatial arrangement of olfactory glomeruli in C. fortis, C.albicans, C.bicolor, C.rubra, and C.noda. Workers of all Cataglyphis species have smaller numbers of glomeruli (198-249) compared to those previously found in olfactory-guided ants. Analyses in 2 species of Formica - a genus closely related to Cataglyphis - revealed substantially higher numbers of olfactory glomeruli (c. 370), which is likely to reflect the importance of olfaction in these wood ant species. Comparisons between Cataglyphis species revealed 2 special features in C. fortis. First, with c. 198 C. fortis has the lowest number of glomeruli compared to all other species. Second, a conspicuously enlarged glomerulus is located close to the antennal nerve entrance. Males of C. fortis possess a significantly smaller number of glomeruli (c. 150) compared to female workers and queens. A prominent male-specific macroglomerulus likely to be involved in sex pheromone communication occupies a position different from that of the enlarged glomerulus in females. The behavioral significance of the enlarged glomerulus in female workers remains elusive. The fact that C. fortis inhabits microhabitats (salt pans) that are avoided by all other Cataglyphis species suggests that extreme ecological conditions may not only have resulted in adaptations of visual capabilities, but also in specializations of the olfactory system.

Multiroute memories in desert ants.

When offered a permanent food source, central Australian desert ants, Melophorus bagoti, develop individually distinct, view-based foraging routes, which they retrace with amazing accuracy during each foraging trip. Using a particular channel setup connected to an artificial feeder, we trained M. bagoti ants to either two or three inward routes that led through different parts of their maze-like foraging grounds. Here, we show that ants are able to adopt multiple habitual paths in succession and that they preserve initially acquired route memories even after they have been trained to new routes. Individual ants differ in the consistency with which they run along habitual pathways. However, those ants that follow constant paths retain their route-specific memories for at least 5 days of suspended foraging, which suggests that even multiple route memories, once acquired, are preserved over the entire lifetime of a forager.

Piloting in desert ants: pinpointing the goal by discrete landmarks.

The inconspicuous nest entrances of the Namibian desert ant Ocymyrmex robustior are located on barren sandflats often devoid of any goal-defining landmark. Foragers that have returned by path integration to the rough area of the goal need a considerable amount of time to finally pinpoint the goal. Even a single landmark decreases the search time dramatically. By using artificial landmarks placed in the neighbourhood of the goal, we show that the larger the image transformations (caused by the landmarks) in the ant's visual field, the faster the homing ants localize the goal. While approaching the goal the ants do not try to fixate the landmarks frontally. Hence, even if provided with discrete landmarks rather than extended visual scenes, Ocymyrmex relies on image changes occurring in wide areas of its panoramic field of view rather than those occurring in a frontal fixation area alone.

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.

Walking on inclines: how do desert ants monitor slope and step length.

BACKGROUND: During long-distance foraging in almost featureless habitats desert ants of the genus Cataglyphis employ path-integrating mechanisms (vector navigation). This navigational strategy requires an egocentric monitoring of the foraging path by incrementally integrating direction, distance, and inclination of the path. Monitoring the latter two parameters involves idiothetic cues and hence is tightly coupled to the ant's locomotor behavior. RESULTS: In a kinematic study of desert ant locomotion performed on differently inclined surfaces we aimed at pinpointing the relevant mechanisms of estimating step length and inclination. In a behavioral experiment with ants foraging on slippery surfaces we broke the otherwise tightly coupled relationship between stepping frequency and step length and examined the animals' ability to monitor distances covered even under those adverse conditions. We show that the ants' locomotor system is not influenced by inclined paths. After removing the effect of speed, slope had only marginal influence on kinematic parameters. CONCLUSION: From the obtained data we infer that the previously proposed monitoring of angles of the thorax-coxa joint is not involved in inclinometry. Due to the tiny variations in cycle period, we also argue that an efference copy of the central pattern generator coding the step length in its output frequency will most likely not suffice for estimating step length and complementing the pedometer. Finally we propose that sensing forces acting on the ant's legs could provide the desired neuronal correlate employed in monitoring inclination and step length.