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.

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.

The Geomagnetic Field Is a Compass Cue in Cataglyphis Ant Navigation.

Desert ants (Cataglyphis) are famous insect navigators. During their foraging lives, the ants leave their underground colonies for long distances and return to their starting point with fair accuracy [1, 2]. Their incessantly running path integrator provides them with a continually updated home vector [3-5]. Directional input to their path integrator is provided by a visual compass based on celestial cues [6, 7]. However, as path integration is prone to cumulative errors, the ants additionally employ landmark guidance routines [8-11]. At the start of their foraging lives, they acquire the necessary landmark information by performing well-structured learning walks [12, 13], including turns about their vertical body axes [14]. When Cataglyphis noda performs these pirouettes, it always gazes at the nest entrance during the longest of several short stopping phases [14]. As the small nest entrance is not visible, the ants can adjust their gaze direction only by reading out their path integrator. However, recent experiments have shown that, for adjusting the goal-centered gaze directions during learning walks, skylight cues are not required [15]. A most promising remaining compass cue is the geomagnetic field, which is used for orientation in one way or the other by a variety of animal species [16-25]. Here, we show that the gaze directions during the look-back-to-the-nest behavior change in a predictable way to alterations of the horizontal component of the magnetic field. This is the first demonstration that, in insects, a geomagnetic compass cue is both necessary and sufficient for accomplishing a well-defined navigational task.

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.

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.

The Role of Celestial Compass Information in Cataglyphis Ants during Learning Walks and for Neuroplasticity in the Central Complex and Mushroom Bodies.

Central place foragers are faced with the challenge to learn the position of their nest entrance in its surroundings, in order to find their way back home every time they go out to search for food. To acquire navigational information at the beginning of their foraging career, Cataglyphis noda performs learning walks during the transition from interior worker to forager. These small loops around the nest entrance are repeatedly interrupted by strikingly accurate back turns during which the ants stop and precisely gaze back to the nest entrance-presumably to learn the landmark panorama of the nest surroundings. However, as at this point the complete navigational toolkit is not yet available, the ants are in need of a reference system for the compass component of the path integrator to align their nest entrance-directed gazes. In order to find this directional reference system, we systematically manipulated the skylight information received by ants during learning walks in their natural habitat, as it has been previously suggested that the celestial compass, as part of the path integrator, might provide such a reference system. High-speed video analyses of distinct learning walk elements revealed that even exclusion from the skylight polarization pattern, UV-light spectrum and the position of the sun did not alter the accuracy of the look back to the nest behavior. We therefore conclude that C. noda uses a different reference system to initially align their gaze directions. However, a comparison of neuroanatomical changes in the central complex and the mushroom bodies before and after learning walks revealed that exposure to UV light together with a naturally changing polarization pattern was essential to induce neuroplasticity in these high-order sensory integration centers of the ant brain. This suggests a crucial role of celestial information, in particular a changing polarization pattern, in initially calibrating the celestial compass system.

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.

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.

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.

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.

Experience-related reorganization of giant synapses in the lateral complex: Potential role in plasticity of the sky-compass pathway in the desert ant Cataglyphis fortis.

Cataglyphis desert ants undergo an age-related polyethism from interior workers to relatively short-lived foragers with remarkable visual navigation capabilities, predominantly achieved by path integration using a polarized skylight-based sun compass and a stride-integrating odometer. Behavioral and physiological experiments revealed that the polarization (POL) pattern is processed via specialized UV-photoreceptors in the dorsal rim area of the compound eye and POL sensitive optic lobe neurons. Further information about the neuronal substrate for processing of POL information in the ant brain has remained elusive. This work focuses on the lateral complex (LX), known as an important relay station in the insect sky-compass pathway. Neuroanatomical results in Cataglyphis fortis show that LX giant synapses (GS) connect large presynaptic terminals from anterior optic tubercle neurons with postsynaptic GABAergic profiles of tangential neurons innervating the ellipsoid body of the central complex. At the ultrastructural level, the cup-shaped presynaptic structures comprise many active zones contacting numerous small postsynaptic profiles. Three-dimensional quantification demonstrated a significantly higher number of GS (∼ 13%) in foragers compared with interior workers. Light exposure, as opposed to age, was necessary and sufficient to trigger a similar increase in GS numbers. Furthermore, the increase in GS numbers was sensitive to the exclusion of UV light. As previous experiments have demonstrated the importance of the UV spectrum for sky-compass navigation in Cataglyphis, we conclude that plasticity in LX GS may reflect processes involved in the initial calibration of sky-compass neuronal circuits during orientation walks preceding active foraging.

Thermal physiology. Keeping cool: Enhanced optical reflection and radiative heat dissipation in Saharan silver ants.

Saharan silver ants, Cataglyphis bombycina, forage under extreme temperature conditions in the African desert. We show that the ants' conspicuous silvery appearance is created by a dense array of triangular hairs with two thermoregulatory effects. They enhance not only the reflectivity of the ant's body surface in the visible and near-infrared range of the spectrum, where solar radiation culminates, but also the emissivity of the ant in the mid-infrared. The latter effect enables the animals to efficiently dissipate heat back to the surroundings via blackbody radiation under full daylight conditions. This biological solution for a thermoregulatory problem may lead to the development of biomimetic coatings for passive radiative cooling of objects.

Beginnings of a synthetic approach to desert ant navigation.

In a synthetic approach to studying navigational abilities in desert ants, we review recent work comparing ants living in different visual ecologies. Those living in a visually rich habitat strewn with tussocks, bushes, and trees are compared to those living in visually barren salt pans, as exemplified by the Central Australian Melophorus bagoti and the North African Cataglyphis fortis, respectively. In bare habitats the navigator must rely primarily on path integration, keeping track of the distance and direction in which it has travelled, while in visually rich habitats the navigator can rely more on guidance by the visual panorama. Consistent with these expectations, C. fortis performs better than M. bagoti on various measures of precision at path integration. In contrast, M. bagoti learned a visually based associative task better than C. fortis, the latter generally failing at the task. Both these ants, however, exhibit a similar pattern of systematic search as a 'back up' strategy when other navigational strategies fail. A newly investigated salt-pan species of Melophorus (as yet unnamed) resembles C. fortis more, and its congener M. bagoti less, in its path integration. The synthetic approach would benefit from comparing more species chosen to address evolutionary questions. This article is part of a Special Issue entitled: CO3 2013.

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.

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.

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.

Visual experience affects both behavioral and neuronal aspects in the individual life history of the desert ant Cataglyphis fortis.

The individual life history of the desert ant Cataglyphis fortis is characterized by a fast transition from interior tasks to mainly visually guided foraging. Previous studies revealed a remarkable structural synaptic plasticity in visual and olfactory input regions within the mushroom bodies of the ants' brain centers involved in learning and memory. Reorganization of synaptic complexes (microglomeruli) was shown to be triggered by sensory exposure rather than an internal program. Using video analyses at the natural nest site and activity recordings after artificial light treatments we investigated whether the ants get exposed to light before onset of foraging and whether this changes the ants' activity levels. We asked whether synaptic reorganization occurs in a similar time window by immunolabeling and quantification of pre- and postsynaptic compartments of visual and olfactory microglomeruli after periods of light-exposure. Ants reverted back to dark nest conditions were used to investigate whether synaptic reorganization is reversible. The behavior analyses revealed that late-interior ants (diggers) are exposed to light and perform exploration runs up to 2 days before they start foraging. This corresponds well with the result that artificial light treatment over more than 2-3 days significantly increased the ants' locomotor activities. At the neuronal level, visual exposure of more than 1 day was necessary to trigger reorganization of microglomeruli, and light-induced changes were only partly reversible in the dark. We conclude that visual preexposure is an important and flexible means to prepare the ants' visual pathway for orientation capabilities essential during foraging.

Leg allometry in ants: extreme long-leggedness in thermophilic species.

The thermophilic ant genera Cataglyphis and Ocymyrmex share a variety of specialisations that enable them to engage in high-speed foraging at considerably higher temperatures than less heat-tolerant species. In the present account we test the hypothesis that thermophilic ants have longer legs than closely related species from more mesic habitats. By comparing large-sized, medium-sized, and small-sized species of Cataglyphis and Ocymyrmex with size-matched species of the closely related non-thermophilic genera Formica (Formicinae) and Messor (Myrmicinae), respectively, we show that the thermophilic species are equipped with considerably longer legs than their less heat-tolerant relatives. Hence phylogenetically, extreme long-leggedness has evolved at least twice in desert ants: in the Formicinae and the Myrmicinae. Functionally, this morphological trait is adaptive for a number of reasons. The long legs raise the body into cooler layers of air and enable higher running speeds, which increase convective cooling and reduce foraging time. These are important adaptations all the more as due to the low food density prevailing in desert habitats foraging Cataglyphis and Ocymyrmex ants have to cover large distances within their physically demanding foraging grounds.

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.