Visual navigation in ants has long been a focus of experimental study [1][2][3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MB) may be the substrate for visual memory in navigation tasks [5-8],
Desert ants feeding on dead arthropods forage for food items that are distributed unpredictably in space and time in the food-scarce terrain of the Saharan salt pans [1]. Scavengers of the genus Cataglyphis forage individually and do not lay pheromone trails [2]. They rely primarily on path integration [3] for navigation and, in addition, use visual [4] and olfactory cues [5-7]. While most studies have focused on the navigational mechanisms of ants targeting a familiar place like the nest or a learned feeding site, little is known about how ants locate food in their natural environment. Here we show that Cataglyphis fortis is highly sensitive to and attracted by food odors, especially the necromone linoleic acid, enabling them to locate tiny arthropods over several meters in distance. Furthermore, during the search for food, ants use extensive crosswind walks that increase the chances of localizing food plumes. By combining high sensitivity toward food odors with crosswind runs, the ants efficiently screen the desert for food and hence reduce the time spent foraging in their harsh desert environment.
The desert ant Cataglyphis fortis is equipped with sophisticated navigational skills for returning to its nest after foraging. The ant's primary means for long-distance navigation is path integration, which provides a continuous readout of the ant's approximate distance and direction from the nest. The nest is pinpointed with the aid of visual and olfactory landmarks. Similar landmark cues help ants locate familiar food sites. Ants on their outward trip will position themselves so that they can move upwind using odor cues to find food. Here we show that homing ants also move upwind along nest-derived odor plumes to approach their nest. The ants only respond to odor plumes if the state of their path integrator tells them that they are near the nest. This influence of path integration is important because we could experimentally provoke ants to follow odor plumes from a foreign, conspecific nest and enter that nest. We identified CO(2) as one nest-plume component that can by itself induce plume following in homing ants. Taken together, the results suggest that path-integration information enables ants to avoid entering the wrong nest, where they would inevitably be killed by resident ants.
Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species' sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities.Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can elicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimal cue integration.
The desert ants Cataglyphis navigate not only by path integration but also by using visual and olfactory landmarks to pinpoint the nest entrance. Here we show that Cataglyphis noda can additionally use magnetic and vibrational landmarks as nest-defining cues. The magnetic field may typically provide directional rather than positional information, and vibrational signals so far have been shown to be involved in social behavior. Thus it remains questionable if magnetic and vibration landmarks are usually provided by the ants' habitat as nest-defining cues. However, our results point to the flexibility of the ants' navigational system, which even makes use of cues that are probably most often sensed in a different context.
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