Directed retreat and navigational mechanisms in trail following Formica obscuripes.

Ant species exhibit behavioural commonalities when solving navigational challenges for successful orientation and to reach goal locations. These behaviours rely on a shared toolbox of navigational strategies that guide individuals under an array of motivational contexts. The mechanisms that support these behaviours, however, are tuned to each species' habitat and ecology with some exhibiting unique navigational behaviours. This leads to clear differences in how ant navigators rely on this shared toolbox to reach goals. Species with hybrid foraging structures, which navigate partially upon a pheromone-marked column, express distinct differences in their toolbox, compared to solitary foragers. Here, we explore the navigational abilities of the Western Thatching ant (Formica obscuripes), a hybrid foraging species whose navigational mechanisms have not been studied. We characterise their reliance on both the visual panorama and a path integrator for orientation, with the pheromone's presence acting as a non-directional reassurance cue, promoting continued orientation based on other strategies. This species also displays backtracking behaviour, which occurs with a combination of unfamiliar terrestrial cues and the absence of the pheromone, thus operating based upon a combination of the individual mechanisms observed in solitarily and socially foraging species. We also characterise a new form of goalless orientation in these ants, an initial retreating behaviour that is modulated by the forager's path integration system. The behaviour directs disturbed inbound foragers back along their outbound path for a short distance before recovering and reorienting back to the nest.

Route retracing: way pointing and multiple vector memories in trail-following ants.

Maintaining positional estimates of goal locations is a fundamental task for navigating animals. Diverse animal groups, including both vertebrates and invertebrates, can accomplish this through path integration. During path integration, navigators integrate movement changes, tracking both distance and direction, to generate a spatial estimate of their start location, or global vector, allowing efficient direct return travel without retracing the outbound route. In ants, path integration is accomplished through the coupling of pedometer and celestial compass estimates. Within path integration, it has been theorized navigators may use multiple vector memories for way pointing. However, in many instances, these navigators may instead be homing via view alignment. Here, we present evidence that trail-following ants can attend to segments of their global vector to retrace their non-straight pheromone trails, without the confound of familiar views. Veromessor pergandei foragers navigate to directionally distinct intermediate sites via path integration by orienting along separate legs of their inbound route at unfamiliar locations, indicating these changes are not triggered by familiar external cues, but by vector state. These findings contrast with path integration as a singular memory estimate in ants and underscore the system's ability to way point to intermediate goals along the inbound route via multiple vector memories, akin to trapline foraging in bees visiting multiple flower patches. We discuss how reliance on non-straight pheromone-marked trails may support attending to separate vectors to remain on the pheromone rather than attempting straight-line shortcuts back to the nest.

Varieties of visual navigation in insects.

The behaviours and cognitive mechanisms animals use to orient, navigate, and remember spatial locations exemplify how cognitive abilities have evolved to suit a number of different mobile lifestyles and habitats. While spatial cognition observed in vertebrates has been well characterised in recent decades, of no less interest are the great strides that have also been made in characterizing and understanding the behavioural and cognitive basis of orientation and navigation in invertebrate models and in particular insects. Insects are known to exhibit remarkable spatial cognitive abilities and are able to successfully migrate over long distances or pinpoint known locations relying on multiple navigational strategies similar to those found in vertebrate models-all while operating under the constraint of relatively limited neural architectures. Insect orientation and navigation systems are often tailored to each species' ecology, yet common mechanistic principles can be observed repeatedly. Of these, reliance on visual cues is observed across a wide number of insect groups. In this review, we characterise some of the behavioural strategies used by insects to solve navigational problems, including orientation over short-distances, migratory heading maintenance over long distances, and homing behaviours to known locations. We describe behavioural research using examples from a few well-studied insect species to illustrate how visual cues are used in navigation and how they interact with non-visual cues and strategies.

Aversive view memories and risk perception in navigating ants.

Many ants establish foraging routes through learning views of the visual panorama. Route models have focused primarily on attractive view use, which experienced foragers orient towards to return to known sites. However, aversive views have recently been uncovered as a key component of route learning. Here, Cataglyphis velox rapidly learned aversive views, when associated with a negative outcome, a period of captivity in vegetation, triggering increases in hesitation behavior. These memories were based on the accumulation of experiences over multiple trips with each new experience regulating forager hesitancy. Foragers were also sensitive to captivity time differences, suggesting they possess some mechanism to quantify duration. Finally, we analyzed foragers' perception of risky (i.e. variable) versus stable aversive outcomes by associating two sites along the route with distinct captivity schedules, a fixed or variable duration, with the same mean across training. Foragers exhibited fewer hesitations in response to risky outcomes compared to fixed ones, indicating they perceived risky outcomes as less severe. Results align with a logarithmic relationship between captivity duration and hesitations, suggesting that aversive stimulus perception is a logarithm of its actual value. We discuss how aversive view learning could be executed within the mushroom bodies circuitry following a prediction error rule.

The Basis of Navigation Across Species.

Animals navigate a wide range of distances, from a few millimeters to globe-spanning journeys of thousands of kilometers. Despite this array of navigational challenges, similar principles underlie these behaviors across species. Here, we focus on the navigational strategies and supporting mechanisms in four well-known systems: the large-scale migratory behaviors of sea turtles and lepidopterans as well as navigation on a smaller scale by rats and solitarily foraging ants. In lepidopterans, rats, and ants we also discuss the current understanding of the neural architecture which supports navigation. The orientation and navigational behaviors of these animals are defined in terms of behavioral error-reduction strategies reliant on multiple goal-directed servomechanisms. We conclude by proposing to incorporate an additional component into this system: the observation that servomechanisms operate on oscillatory systems of cycling behavior. These oscillators and servomechanisms comprise the basis for directed orientation and navigational behaviors.

Neuroecology beyond the brain: learning in Echinodermata.

We propose an expansion of neuroecological comparisons to include the capabilities of brainless and non-neural organisms. We begin this enterprise by conducting a systematic search for studies on learning in echinoderms. Echinodermata are marine invertebrates comprising starfish, brittle stars, sea cucumbers, sea urchins, and sea lilies. Animals in this phylum lack any centralized brain and instead possess diffuse neural networks known as nerve nets. The learning abilities of these animals are of particular interest as, within the bilaterian clade, they are close evolutionary neighbors to chordates, a phylum whose members exhibit complex feats in learning and contain highly specialized brains. The learning capacities and limitations of echinoderms can inform the evolution of nervous systems and learning in Bilateria. We find evidence of both non-associative and associative learning (in the form of classical conditioning) in echinoderms, which was primarily focused on starfish. Additional evidence of learning is documented in brittle stars, sand dollars, and sea urchins. We then discuss the evolutionary significance of learning capabilities without a brain, the presence of embodied cognition across multiple groups, and compare the learning present in echinoderms with the impressive cognitive abilities documented in the oldest linage group within vertebrates (the major group within the phylum of chordates), fish.

Role of the pheromone for navigation in the group foraging ant, Veromessor pergandei.

Navigation is comprised of a variety of strategies which rely on multiple external cues to shape a navigator's behavioral output. Here, we explored in the ant Veromessor pergandei, the interactions between the information provided by the pheromone trail and the home vector guided by the celestial compass. We found that a cross sensory interaction between the pheromone cue and the path integrator underlies correct orientation during the inbound journey. The celestial compass provides directional information, while the presence of the trail pheromone acts as a critical context cue, triggering distinct behaviors (vector orientation, search, and backtracking). While exposed to the pheromone, foragers orient to the vector direction regardless of vector state, while in the pheromone's absence, the current remaining vector determines the forager's navigational behavior. This interaction also occurs in foragers with no remaining path integrator, relying on the activation of a celestial compass-based memory of the previous trip. Such cue interactions maximize the foragers' return to the nest and inhibit movement off the pheromone trail. Finally, our manipulations continuously rotated foragers away from their desired heading, yet foragers were proficient at counteracting these changes, steering to maintain a correct compass heading even at rotational speeds of ~ 40°/s.

Traveling through light clutter: Path integration and panorama guided navigation in the Sonoran Desert ant, Novomessor cockerelli.

Foraging ants use multiple navigational strategies, including path integration and visual panorama cues, which are used simultaneously and weighted based upon context, the environment and the species' sensory ecology. In particular, the amount of visual clutter in the habitat predicts the weighting given to the forager's path integrator and surrounding panorama cues. Here, we characterize the individual cue use and cue weighting of the Sonoran Desert ant, Novomessor cockerelli, by testing foragers after local and distant displacement. Foragers attend to both a path-integration-based vector and the surrounding panorama to navigate, on and off foraging routes. When both cues were present, foragers initially oriented to their path integrator alone, yet weighting was dynamic, with foragers abandoning the vector and switching to panorama-based navigation after a few meters. If displaced to unfamiliar locations, experienced foragers travelled almost their full homeward vector (∼85 %) before the onset of search. Through panorama analysis, we show views acquired on-route provide sufficient information for orientation over only short distances, with rapid parallel decreases in panorama similarity and navigational performance after even small local displacements. These findings are consistent with heavy path integrator weighting over the panorama when the local habitat contains few prominent terrestrial cues.

Effect of large visual changes on the navigation of the nocturnal bull ant, Myrmecia midas.

Nocturnal insects have remarkable visual capacities in dim light. They can navigate using both the surrounding panorama and celestial cues. Individual foraging ants are efficient navigators, able to accurately reach a variety of goal locations. During navigation, foragers compare the current panoramic view to previously learnt views. In this natural experiment, we observed the effects of large panorama changes, the addition of a fence and the removal of several trees near the nest site, on the navigation of the nocturnal bull ant Myrmecia midas. We examined how the ants' navigational efficiency and behaviour changed in response to changes in ~ 30% of the surrounding skyline, following them over multiple nights. Foragers were displaced locally off-route where we collected initial orientations and homing paths both before and after large panorama changes. We found that immediately after these changes, foragers were unable to initially orient correctly to the nest direction and foragers' return paths were less straight, suggesting increased navigational uncertainty. Continued testing showed rapid recovery in both initial orientation and path straightness.

Pheromone cue triggers switch between vectors in the desert harvest ant, Veromessor pergandei.

The desert harvester ant (Veromessor pergandei) employs a mixture of social and individual navigational strategies at separate stages of their foraging trip. Individuals leave the nest along a pheromone-based column, travelling 3-40 m before spreading out to forage individually in a fan. Foragers use path integration while in this fan, accumulating a direction and distance estimate (vector) to return to the end of the column (column head), yet foragers' potential use of path integration in the pheromone-based column is less understood. Here we show foragers rely on path integration both in the foraging fan and while in the column to return to the nest, using separate vectors depending on their current foraging stage in the fan or column. Returning foragers displaced while in the fan oriented and travelled to the column head location while those displaced after reaching the column travel in the nest direction, signifying the maintenance of a two-vector system with separate fan and column vectors directing a forager to two separate spatial locations. Interestingly, the trail pheromone and not the surrounding terrestrial cues mediate use of these distinct vectors, as fan foragers briefly exposed to the pheromone cues of the column in isolation altered their paths to a combination of the fan and column vectors. The pheromone acts as a contextual cue triggering both the retrieval of the column-vector memory and its integration with the forager's current fan-vector.

Same but different: Socially foraging ants backtrack like individually foraging ants but use different mechanisms.

Diverse species may adopt behaviourally identical solutions to similar environmental challenges. However, the underlying mechanisms dictating these responses may be quite different and are often associated with the specific ecology or habitat of these species. Foraging desert ants use multiple strategies in order to successfully navigate. In individually foraging ants, these strategies are largely visually-based; this includes path integration and learned panorama cues, with systematic search and backtracking acting as backup mechanisms. Backtracking is believed to be controlled, at least in solitary foraging species, by three criteria: 1) foragers must have recent exposure to the nest panorama, 2) the path integrator must be near zero, and 3) the ant must be displaced to an unfamiliar location. Instead of searching for the nest, under these conditions, foragers head in the opposite compass direction of the one in which they were recently travelling. Here, we explore backtracking in the socially foraging desert harvester ant (Veromessor pergandei), which exhibits a foraging ecology consisting of a combination of social and individual cues in a column and fan structure. We find that backtracking in V. pergandei, similar to solitary foraging species, is dependent on celestial cues, and in particular on the sun's position. However, unlike solitary foraging species, backtracking in V. pergandei is not mediated by the same criteria. Instead the expression of this behaviour is dependent on the presence of the social cues of the column and the proportion of the column that foragers have completed prior to displacement.

Not just going with the flow: foraging ants attend to polarised light even while on the pheromone trail.

The polarisation pattern of skylight serves as an orientation cue for many invertebrates. Solitary foraging ants, in particular, rely on polarised light to orient along with a number of other visual cues. Yet it is unknown, if this cue is actively used in socially foraging species that use pheromone trails to navigate. Here, we explore the use of polarised light in the presence of the pheromone cues of the foraging trail. The desert harvester ant, Veromessor pergandei, relies on pheromone cues and path integration in separate stages of their foraging ecology (column and fan, respectively). Here, we show that foragers actively orient to an altered overhead polarisation pattern, both while navigating individually in the fan and while on the pheromone-based column. These heading changes occurred during twilight, as well as in the early morning and late afternoon before sunset. Differences in shift size indicate that foragers attend to both the polarisation pattern and the sun's position when available, yet during twilight, headings are dominated by the polarisation pattern. Finally, when the sun's position was experimentally blocked before sunset, shift sizes increased similar to twilight testing. These findings show that celestial cues provide directional information on the pheromone trail.

Panorama similarity and navigational knowledge in the nocturnal bull ant Myrmecia midas.

Nocturnal ants forage and navigate during periods of reduced light, making detection of visual cues difficult, yet they are skilled visual navigators. These foragers retain visual panoramic memories both around the nest and along known routes for later use, to return to previously visited food sites or to the nest. Here, we explore the navigational knowledge of the nocturnal bull ant Myrmecia midas by investigating differences in nestward homing after displacement of three forager groups based on similarities in the panoramas between the release site and previously visited locations. Foragers that travel straight to the foraging tree or to trees close to the nest show reduced navigational success in orienting and returning from displacements compared with individuals that forage further from the nest site. By analysing the cues present in the panorama, we show that multiple metrics of forager navigational performance correspond with the degree of similarity between the release site panorama and panoramas of previously visited sites. In highly cluttered environments, where panoramas change rapidly over short distances, the views acquired near the nest are useful only over a small area and memories acquired along foraging routes become critical.

Terrestrial cue learning and retention during the outbound and inbound foraging trip in the desert ant, Cataglyphis velox.

Foraging ants are able to acquire and retain long-term memories of panorama cues around the nest and along known routes. Here we explore foragers' ability to learn and retain skyline cues experienced on only the outbound or inbound portion of the foraging trip. Foragers exposed to the skyline on the outbound portion showed single trial learning of these cues. Furthermore, the navigational performance of these "Outbound-Only" foragers was on par with foragers that experienced the full route. In contrast, foragers experiencing the skyline only on the inbound portion, "Inbound-Only" foragers, took 5 trips to successfully learn these cues. These performance differences persisted for long-term memory retention. Outbound-Only foragers successfully oriented after a 3-day delay and showed similar performance to the full route control, whereas Inbound-Only foragers were no longer able to orient successfully to these cues after 3 days. Additionally, long-term memory formation of skyline cues appears to require multiple presentations, as foragers with only one outbound experience of the skyline could not successfully orient after the delay. Our results suggest that terrestrial cue learning and retention is more robust when cues are experienced on the outbound segment of the foraging trip.

Experimental ethology of learning in desert ants: Becoming expert navigators.

Foraging desert ants are repeatedly presented with the challenge of leaving the nest, searching the scorching desert landscape to find food, and then transporting it back home. To accomplish this task, foragers have a navigational toolbox, which relies on olfactory, idiothetic, visual and magnetic cues. Desert ants have been widely studied with regards to these abilities, including a heavy focus on learned visual cues, the most prominent being the terrestrial panorama. Nest cues are first acquired during pre-foraging learning walks. Once foragers leave the nest area, they also learn a number of cues to aid them when returning both back to the nest and to known food sites, using experience of previous trips to navigate on future trips. In this review, we describe the learning processes involved in accurate navigation in desert ants. We first focus on recent research on nest-site panorama learning during pre-foraging learning walks as well as panorama learning away from the nest during foraging. We also review learning cues beyond the terrestrial panorama, including tactile, magnetic, olfactory and vibrational cues. These studies provide a basis for future work to further explore how these navigators, despite their small brains, acquire, retain and use many cue sets present in their environments. We call for more experimental ethology focussed on learning processes, both by exploring run-by-run and step-by-step acquisition of information for navigation, as well as for other natural tasks in an animal's life.

Landmark learning, cue conflict, and outbound view sequence in navigating desert ants.

Mobile animals need to reliably find goal locations and animal navigators acquire and use multiple cue sets within their environment designating direction and distance estimates of these locations. Foraging ants use multiple navigational tools including path integration and the learning of the landmark panorama. During landmark-based navigation, foragers first acquire the landmark cues around the nest through preforaging learning walks, and then learn non-nest site cues along their foraging routes. Here, we explore both foragers' ability to extrapolate views from around the nest to local displacement sites and landmark learning during the first foraging trips away from the nest area. During Experiment 1, foragers were given variable amounts of exposure to the nest area before being displaced 8 m away where their return trips were recorded. In Experiment 2, foragers' return trips from a site 8 m from the nest were recorded with the surrounding landmarks during either the outbound or inbound trip obstructed from view and with/without the aid of a homeward vector. Foragers were unable to correctly orient or return home efficiently regardless of the exposure level to the nest panorama, suggesting an inability to extrapolate views from learning walks and supporting recognition-based navigation. Foragers were able to use experience of either the outbound- or inbound-view sequence to initially orient home, yet were unable to quickly return to the nest when only exposed to the inbound route. Our results suggest that exposure to the outbound foraging path is critical for efficient homeward route formation. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

How to Navigate in Different Environments and Situations: Lessons From Ants.

Ants are a globally distributed insect family whose members have adapted to live in a wide range of different environments and ecological niches. Foraging ants everywhere face the recurring challenge of navigating to find food and to bring it back to the nest. More than a century of research has led to the identification of some key navigational strategies, such as compass navigation, path integration, and route following. Ants have been shown to rely on visual, olfactory, and idiothetic cues for navigational guidance. Here, we summarize recent behavioral work, focusing on how these cues are learned and stored as well as how different navigational cues are integrated, often between strategies and even across sensory modalities. Information can also be communicated between different navigational routines. In this way, a shared toolkit of fundamental navigational strategies can lead to substantial flexibility in behavioral outcomes. This allows individual ants to tune their behavioral repertoire to different tasks (e.g., foraging and homing), lifestyles (e.g., diurnal and nocturnal), or environments, depending on the availability and reliability of different guidance cues. We also review recent anatomical and physiological studies in ants and other insects that have started to reveal neural correlates for specific navigational strategies, and which may provide the beginnings of a truly mechanistic understanding of navigation behavior.

The View from the Trees: Nocturnal Bull Ants, Myrmecia midas, Use the Surrounding Panorama While Descending from Trees.

Solitary foraging ants commonly use visual cues from their environment for navigation. Foragers are known to store visual scenes from the surrounding panorama for later guidance to known resources and to return successfully back to the nest. Several ant species travel not only on the ground, but also climb trees to locate resources. The navigational information that guides animals back home during their descent, while their body is perpendicular to the ground, is largely unknown. Here, we investigate in a nocturnal ant, Myrmecia midas, whether foragers travelling down a tree use visual information to return home. These ants establish nests at the base of a tree on which they forage and in addition, they also forage on nearby trees. We collected foragers and placed them on the trunk of the nest tree or a foraging tree in multiple compass directions. Regardless of the displacement location, upon release ants immediately moved to the side of the trunk facing the nest during their descent. When ants were released on non-foraging trees near the nest, displaced foragers again travelled around the tree to the side facing the nest. All the displaced foragers reached the correct side of the tree well before reaching the ground. However, when the terrestrial cues around the tree were blocked, foragers were unable to orient correctly, suggesting that the surrounding panorama is critical to successful orientation on the tree. Through analysis of panoramic pictures, we show that views acquired at the base of the foraging tree nest can provide reliable nest-ward orientation up to 1.75 m above the ground. We discuss, how animals descending from trees compare their current scene to a memorised scene and report on the similarities in visually guided behaviour while navigating on the ground and descending from trees.