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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.

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.

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.

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. Expected final online publication date for the Annual Review of Psychology, Volume 73 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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.

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 brush, triggering an increase in hesitation behavior. These memories were based on the accumulation of experiences over multiple trips with each new experience regulating forager’s 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 significantly less hesitation to the risky outcome compared to the fixed, 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 conclude by characterizing how these behaviors can be executed within the mushroom bodies’ neural circuitry.

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.

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.

When deciding between different courses of action, both the potential outcomes and the costs of making a choice should be considered. To date, most studies of risk-sensitive choice have focused on the probability of different reward amounts. Here we studied choice between options that varied in the riskiness of the effort (number of responses) required. People made repeated choices between pairs of options that required them to click different numbers of sequentially presented response circles. Easy (low effort) options led to small numbers of response circles, whereas hard (high effort) options led to larger numbers of response circles. For both easy and hard options, safe options led to a fixed effort, whereas risky options led to variable effort that, with a 50/50 chance, required more or less effort. Participants who showed a preference for easier over harder options (63% in Experiment 1 and 93% in Experiment 2) were risk averse overall. Participants were more risk averse for decisions involving hard options than for decisions involving easy options. On subsequent memory tests, people most readily recalled the hardest outcome, and they overestimated its frequency of occurrence. Strikingly, memory for the effort associated with each risky option strongly correlated with risky choices for both easy-effort and hard-effort choices, suggesting that the memory may determine choices based on risky effort.

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 3-40m 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 as well as 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 cue acts as a contextual cue triggering both the retrieval of the column vector memory and its integration with the forager’s current fan vector.

Role of the pheromone for orientation 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. An additional navigational challenge is coping with forces such as wind and water currents that push navigators off-course. Here, we explore the cue interactions that dictate orientation and foragers’ ability to counter course altering rotational changes in the desert ant, Veromessor pergandei. We found 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 behavioral responses (vector orientation, search and backtracking). A particularly interesting interaction occurs between the pheromone and the forager’s vector state. While exposed to the pheromone, foragers orient to the vector direction regardless of vector state, while in the pheromone’s absence the current vector triggers the switch between behaviors. Such interactions maximize the foragers’ return to the nest and inhibit movement off the trail. Finally, our manipulations continuously pushed foragers away from their desired heading, yet foragers were highly proficient at counteracting these changes, steering to maintain a correct heading even at rotational speeds of ~40°/s.

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.

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.

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).

Desert ants that forage solitarily continually update their position relative to the nest through path integration. This is accomplished by combining information from their celestial compass and pedometer. The path integration system can adapt when memories of previous inbound routes do not coincide with the outbound route, through vector calibration. Here, we test the speed and limit of vector calibration in the desert ant Melophorus bagoti by creating directional conflicts between the inbound and outbound routes (45°, 90°, 135°, 180°). The homeward vector appears to calibrate rapidly after training with shifts occurring after three foraging trips, yet the limit of the vector’s plasticity appears to be a maximum of 45°. At 45° conflicts, the vector calibrates the full 45°, suggesting dominance of the previous inbound memories over the outbound cues of the current trip. Yet at larger directional conflicts, vector shifts after training diminish, with foragers in the 90° and 135° conditions showing smaller intermediate shifts between the inbound memories and the current outbound vector. When the conflict is at its maximum (180°), foragers show no calibration, suggesting the outbound vector is dominant. Panorama exposure during training appears to aid foragers orienting to the true nest, but this also appears limited to about a 45° shift and does not improve with training.

Foraging ants are known to use multiple sources of information to return to the nest. These cue sets are employed by independent navigational systems including path integration in the case of celestial cues and vision-based learning in the case of terrestrial landmarks and the panorama. When cue sets are presented in conflict, the Australian desert ant species, Melophorus bagoti, will choose a compromise heading between the directions dictated by the cues or, when navigating on well-known routes, foragers choose the direction indicated by the terrestrial cues of the panorama against the dictates of celestial cues. Here, we explore the roles of learning terrestrial cues and delays since cue exposure in these navigational decisions by testing restricted foragers with differing levels of terrestrial cue experience with the maximum (180°) cue conflict. Restricted foragers appear unable to extrapolate landmark information from the nest to a displacement site 8 m away. Given only one homeward experience, foragers can successfully orient using terrestrial cues, but this experience is not sufficient to override a conflicting vector. Terrestrial cue strength increases with multiple experiences and eventually overrides the celestial cues. This appears to be a dynamic choice as foragers discount the reliability of the terrestrial cues over time, reverting back to preferring the celestial vector when the forager has an immediate vector, but the forager's last exposure to the terrestrial cues was 24 hr in the past. Foragers may be employing navigational decision making that can be predicted by the temporal weighting rule.

Visual cues commonly aid solitary foraging ants. Specifically, foragers can use the skyline where terrestrial landmarks meet the sky. Foraging ants show a remarkable affinity to retain these terrestrial cues, developing lifelong memories of the nest site panorama. Here we explore foragers' ability to retain skyline cues of resource locations at some distance from the nest through experiments with artificial skylines erected around a resource location. We also tested the foragers' memories of one skyline at several time points after the skyline was replaced by a different one. During retention testing, foragers appear able to retain robust memories of these skylines over periods (5 days) that surpass their average life span. Exposure to the nest panorama during these periods did not interfere with navigational performance at the distant skyline. Foragers in the replacement experiment initially oriented correctly to both skylines. Thereafter, the foragers' headings in tests with the first skyline gradually shifted away from the correct homeward direction. We argue that new skyline memories cause retroactive interference in the retention of previously learned skylines. Skyline memories may compete during memory retrieval, or may be retrieved in association with context cues present in the current testing paradigm such as vector length.

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.

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.

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.

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, be it 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 nest-ward 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 up the foraging tree or to close trees around the nest show reduced navigational success in orienting and returning from displacements compared to 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 only useful over a small area and memories acquired along foraging routes become critical.

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.

Synopsis Harsh environments and severe winters have been hypothesized to favor improvement of the cognitive abilities necessary for successful foraging. Geographic variation in winter climate, then, is likely associated with differences in selection pressures on cognitive ability, which could lead to evolutionary changes in cognition and its neural mechanisms, assuming that variation in these traits is heritable. Here, we focus on two species of food-caching chickadees (genus Poecile), which rely on stored food for survival over winter and require the use of spatial memory to recover their stores. These species also exhibit extensive climate-related population level variation in spatial memory and the hippocampus, including volume, the total number and size of neurons, and adults’ rates of neurogenesis. Such variation could be driven by several mechanisms within the context of natural selection, including independent, population-specific selection (local adaptation), environment experience-based plasticity, developmental differences, and/or epigenetic differences. Extensive data on cognition, brain morphology, and behavior in multiple populations of these two species of chickadees along longitudinal, latitudinal, and elevational gradients in winter climate are most consistent with the hypothesis that natural selection drives the evolution of local adaptations associated with spatial memory differences among populations. Conversely, there is little support for the hypotheses that environment-induced plasticity or developmental differences are the main causes of population differences across climatic gradients. Available data on epigenetic modifications of memory ability are also inconsistent with the observed patterns of population variation, with birds living in more stressful and harsher environments having better spatial memory associated with a larger hippocampus and a larger number of hippocampal neurons. Overall, the existing data are most consistent with the hypothesis that highly predictable differences in winter climate drive the evolution and maintenance of differences among populations both in cognition and in the brain via local adaptations, at least in food-caching parids.

Rüdiger Wehner's work on insect orientation and navigation has influenced many scientists studying navigation, not only in ants and bees, but in other animals as well. We review the scientific legacy of six topics arising from Wehner's work on navigation. The polarisation compass is a chapter with a lot of behavioural and neurobiological detail. It has influenced the study of polarisation vision in other systems, and led Wehner to formulate the concept of a matched filter. The matched filter has probably had earlier formulations, but Wehner's paper on it has been much cited in studies on navigation and in other fields. The polarisation compass serves the task of path integration in insects. Work on path integration took off in the 1980s with work on desert ants and rodents. The use of terrestrial visual cues, landmarks or the panorama in view-based matching is another major theme of navigational research today. Search strategies were also well described in desert ants, and this line of research helped to launch theoretical and empirical developments in searching behaviour, now a lively area of research. Finally, robotic work has often drawn inspiration from work on insect navigation. We end with some discussion of current research directions.

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.

Summary 1. Differential demands on cognitive ability may be expected to result in the evolution of cognition and associated changes in underlying neural mechanisms. While most comparative studies of cognition have focused on volumetric brain measurements, it remains unclear whether neuron morphology, which appears to be directly linked to cognitive functions, may be responsive to differential selection on cognitive ability. 2. Food-caching birds rely on caches to survive winter and use spatial memory to recover previously stored food. Birds in more harsh winter climates have been hypothesized to be more dependent on cached food, and therefore, their winter survival may be expected to be more memory-dependent relative to their conspecifics from the milder winter climates. Here, we show that neuron soma size in the hippocampus, a brain region involved in memory function, exhibits significant population variation associated with different environmental pressures on spatial memory related to differences in winter climate harshness in two species of foodcaching chickadees. Comparing ten populations of black-capped chickadees and three populations of mountain chickadees along a gradient of winter climate harshness, we found that birds from harsher environments had significantly larger hippocampal neuron soma sizes. 3. Using chickadees from the two most divergent populations reared in a laboratory environment, we showed that these differences appear to be at least partly heritable as significant differences between these populations remained in birds sharing the same laboratory environment. At the same time, laboratory-reared birds had significantly smaller neuron soma size compared with the wild-sampled birds, suggesting that at least some variation in neuron soma size may be due to environment-related plasticity. 4. Our data suggest that environment-related selection on memory may generate differences in neuron morphology, which appear to be controlled by some heritable mechanisms and likely underlie population differences in spatial memory.

Ants use both terrestrial landmarks and cues derived from path integration to navigate to and from their nest location. These cues persist even as light levels drop during the twilight/night. Here we determined the compass cues used by a nocturnal bull ant, Myrmecia midas, in which the majority of the individuals begin foraging during the evening twilight period. Foragers of M. midas with vectors of≤5 m when displaced to unfamiliar locations did not follow the home vector, but instead showed random heading directions. Foragers with larger home vectors (≥ 10 m) oriented toward the fictive nest, indicating a possible increase in cue strength with vector length. When the ants were displaced locally to create a conflict between the home direction indicated by path integration and terrestrial landmarks, foragers oriented using landmark information exclusively and ignored any accumulated home vector regardless of vector length. When the visual landmarks at the local displacement site were blocked, foragers were unable to orient to the nest direction and their heading directions were randomly distributed. Ants of M. midas typically nest at the base of the tree and some individuals forage on the same tree. Foragers collected on the nest tree during evening twilight were unable to orient toward the nest after small lateral displacements away from the nest, suggesting the possibility of high tree fidelity and an inability to extrapolate landmark compass cues from information collected on the tree and at the nest site to close displacement sites.

Ants use both terrestrial landmarks and celestial cues to navigate to and from their nest location. These cues persist even as light levels drop during the twilight/night. Here, we determined the compass cues used by a nocturnal bull ant

Ants use the panoramic skyline in part to determine a direction of travel. A theoretically elegant way to define where terrestrial objects meet the sky is to use an opponent-process channel contrasting green wavelengths of light with ultraviolet (UV) wavelengths. Compared with the sky, terrestrial objects reflect relatively more green wavelengths. Using such an opponent-process channel gains constancy in the face of changes in overall illumination level. We tested the use of UV wavelengths in desert ants by using a plastic that filtered out most of the energy below 400 nm. Ants, Melophorus bagoti, were trained to home with an artificial skyline provided by an arena (experiment 1) or with the natural panorama (experiment 2). On a test, a homing ant was captured just before she entered her nest, and then brought back to a replicate arena (experiment 1) or the starting point (the feeder, experiment 2) and released. Blocking UV light led to deteriorations in orientation in both experiments. When the artificial skyline was changed from opaque to transparent UV-blocking plastic (experiment 3) on the other hand, the ants were still oriented. We conclude that UV wavelengths play a crucial role in determining direction based on the terrestrial surround.

Harsh environments may lead to increased demands on memory in animals that rely on memory for survival. We previously showed that winter severity is associated with non-experience-based differences in memory and the hippocampus over a large continental scale in food-caching black-capped chickadees, Poecile atricapillus. However, large climatic differences also occur along steep elevational gradients in montane environments over a small geographical scale. Here, we demonstrate for the first time that large differences in memory and the hippocampus exist over extremely short distances (10 km) along the elevation gradient. We found that food-caching mountain chickadees (P. gambeli) from the highest elevations in the Sierra Nevada Mountains had significantly better spatial memory associated with larger hippocampi, with almost twice the number of hippocampal neurons, than individuals only 600 m lower in elevation. We found similarly large differences in hippocampal neurogenesis rates as indicated by the total number of immature neurons. Our study therefore suggests that climate-related environmental differences can produce dramatic differences in memory and the hippocampus in animals within close proximity on small spatial scales and that currently observed trends in global climate may have significant effects on cognition and the brain.

Selection for enhanced cognitive traits is hypothesized to produce enhancements to brain structures that support those traits. Although numerous studies suggest that this pattern is robust, there are several mechanisms that may produce this association. First, cognitive traits and their neural underpinnings may be fixed as a result of differential selection on cognitive function within specific environments. Second, these relationships may be the product of the selection for plasticity, where differences are produced owing to an individual's experiences in the environment. Alternatively, the relationship may be a complex function of experience, genetics and/or epigenetic effects. Using a well-studied model species (black-capped chickadee, Poecile atricapillus ), we have for the first time, to our knowledge, addressed these hypotheses. We found that differences in hippocampal (Hp) neuron number, neurogenesis and spatial memory previously observed in wild chickadees persisted in hand-raised birds from the same populations, even when birds were raised in an identical environment. These findings reject the hypothesis that variation in these traits is owing solely to differences in memory-based experiences in different environments. Moreover, neuron number and neurogenesis were strikingly similar between captive-raised and wild birds from the same populations, further supporting the genetic hypothesis. Hp volume, however, did not differ between the captive-raised populations, yet was very different in their wild counterparts, supporting the experience hypothesis. Our results indicate that the production of some Hp factors may be inherited and largely independent of environmental experiences in adult life, regardless of their magnitude, in animals under high selection pressure for memory, while traits such as volume may be more plastic and modified by the environment.

Variation in environmental conditions associated with differential selection on spatial memory has been hypothesized to result in evolutionary changes in the morphology of the hippocampus, a brain region involved in spatial memory. At the same time, it is well known that the morphology of the hippocampus might also be directly affected by environmental conditions. Understanding the role of environment-based plasticity is therefore critical when investigating potential adaptive evolutionary changes in the hippocampus associated with environmental variation. We previously demonstrated large elevation-related variation in hippocampus morphology in mountain chickadees over an extremely small spatial scale. We hypothesized that this variation is related to differential selection pressures associated with differences in winter climate severity along an elevation gradient, which make different demands on spatial memory used for food cache retrieval. Here, we tested whether such variation is experience based, generated by potential differences in the environment, by comparing the hippocampus morphology of chickadees from different elevations maintained in a uniform captive environment in a laboratory with those sampled directly from the wild. In addition, we compared hippocampal neuron soma size in chickadees sampled directly from the wild with those maintained in laboratory conditions with restricted and unrestricted spatial memory use via manipulation of food-caching experiences to test whether memory use can affect neuron soma size. There were significant elevation-related differences in hippocampus volume and the total number of hippocampal neurons, but not in neuron soma size, in captive birds. Captive environmental conditions were associated with a large reduction in hippocampus volume and neuron soma size, but not in the total number of neurons or in neuron soma size in other telencephalic regions. Restriction of memory use while in laboratory conditions produced no significant effects on hippocampal neuron soma size. Overall our results showed that captivity has a strong effect on hippocampus volume, which could be due, at least partly, to a reduction in neuron soma size specifically in the hippocampus, but it did not override elevation-related differences in hippocampus volume or in the total number of hippocampal neurons. These data are consistent with the idea of the adaptive nature of the elevation-related differences associated with selection on spatial memory, while at the same time demonstrating additional environment-based plasticity in hippocampus volume, but not in neuron numbers. Our results, however, cannot rule out that the differences between elevations might still be driven by some developmental or early posthatching conditions/experiences.