The role of memory-based movements in the formation of animal home ranges.

Most animals live in spatially-constrained home ranges. The prevalence of this space-use pattern in nature suggests that general biological mechanisms are likely to be responsible for their occurrence. Individual-based models of animal movement in both theoretical and empirical settings have demonstrated that the revisitation of familiar areas through memory can lead to the formation of stable home ranges. Here, we formulate a deterministic, mechanistic home range model that includes the interplay between a bi-component memory and resource preference, and evaluate resulting patterns of space-use. We show that a bi-component memory process can lead to the formation of stable home ranges and control its size, with greater spatial memory capabilities being associated with larger home range size. The interplay between memory and resource preferences gives rise to a continuum of space-use patterns-from spatially-restricted movements into a home range that is influenced by local resource heterogeneity, to diffusive-like movements dependent on larger-scale resource distributions, such as in nomadism. Future work could take advantage of this model formulation to evaluate the role of memory in shaping individual performance in response to varying spatio-temporal resource patterns.

Importance of magnetic information for neuronal plasticity in desert ants.

Many animal species rely on the Earth's magnetic field during navigation, but where in the brain magnetic information is processed is still unknown. To unravel this, we manipulated the natural magnetic field at the nest entrance of Cataglyphis desert ants and investigated how this affects relevant brain regions during early compass calibration. We found that manipulating the Earth's magnetic field has profound effects on neuronal plasticity in two sensory integration centers. Magnetic field manipulations interfere with a typical look-back behavior during learning walks of naive ants. Most importantly, structural analyses in the ants' neuronal compass (central complex) and memory centers (mushroom bodies) demonstrate that magnetic information affects neuronal plasticity during early visual learning. This suggests that magnetic information does not only serve as a compass cue for navigation but also as a global reference system crucial for spatial memory formation. We propose a neural circuit for integration of magnetic information into visual guidance networks in the ant brain. Taken together, our results provide an insight into the neural substrate for magnetic navigation in insects.

Effect of repetition of vertical and horizontal routes on navigation performance in Australian bull ants.

Solitarily foraging ant species differ in their reliance on their two primary navigational systems- path integration and visual learning. Despite many species of Australian bull ants spending most of their foraging time on their foraging tree, little is known about the use of these systems while climbing. "Rewinding" displacements are commonly used to understand navigational system usage, and work by introducing a mismatch between these navigational systems, by displacing foragers after they have run-down their path integration vector. We used rewinding to test the role of path integration on the arboreal and terrestrial navigation of M. midas. We rewound foragers along either the vertical portion, the ground surface portion, or across both portions of their homing trip. Since rewinding involves repeatedly capturing and releasing foragers, we included a nondisplacement, capture-and-release control, in which the path integration vector is unchanged. We found that rewound foragers do not seem to accumulate path integration vector, although a limited effect of vertical rewinding was found, suggesting a potential higher sensitivity while descending the foraging tree. However, the decrease in navigational efficiency due to capture was larger than the vertical rewinding effect, which along with the negative impact of the vertical surface, and an interaction between capture and rewinding, may suggest aversion rather than path integration caused the vertical rewinding response. Together these results add to the evidence that M. midas makes minimal use of path integration while foraging, and the growing evidence that they are capable of quickly learning from aversive stimulus.

Hippocampal firing fields anchored to a moving object predict homing direction during path-integration-based behavior.

Homing based on path integration (H-PI) is a form of navigation in which an animal uses self-motion cues to keep track of its position and return to a starting point. Despite evidence for a role of the hippocampus in homing behavior, the hippocampal spatial representations associated with H-PI are largely unknown. Here we developed a homing task (AutoPI task) that required a mouse to find a randomly placed lever on an arena before returning to its home base. Recordings from the CA1 area in male mice showed that hippocampal neurons remap between random foraging and AutoPI task, between trials in light and dark conditions, and between search and homing behavior. During the AutoPI task, approximately 25% of the firing fields were anchored to the lever position. The activity of 24% of the cells with a lever-anchored field predicted the homing direction of the animal on each trial. Our results demonstrate that the activity of hippocampal neurons with object-anchored firing fields predicts homing behavior.

The potential underlying mechanisms during learning flights.

Hymenopterans, such as bees and wasps, have long fascinated researchers with their sinuous movements at novel locations. These movements, such as loops, arcs, or zigzags, serve to help insects learn their surroundings at important locations. They also allow the insects to explore and orient themselves in their environment. After they gained experience with their environment, the insects fly along optimized paths guided by several guidance strategies, such as path integration, local homing, and route-following, forming a navigational toolkit. Whereas the experienced insects combine these strategies efficiently, the naive insects need to learn about their surroundings and tune the navigational toolkit. We will see that the structure of the movements performed during the learning flights leverages the robustness of certain strategies within a given scale to tune other strategies which are more efficient at a larger scale. Thus, an insect can explore its environment incrementally without risking not finding back essential locations.

Scanning behaviour in ants: an interplay between random-rate processes and oscillators.

At the start of a journey home or to a foraging site, ants often stop, interrupting their forward movement, turn on the spot a number of times, and fixate in different directions. These scanning bouts are thought to provide visual information for choosing a path to travel. The temporal organization of such scanning bouts has implications about the neural organisation of navigational behaviour. We examined (1) the temporal distribution of the start of such scanning bouts and (2) the dynamics of saccadic body turns and fixations that compose a scanning bout in Australian desert ants, Melophorus bagoti, as they came out of a walled channel onto open field at the start of their homeward journey. Ants were caught when they neared their nest and displaced to different locations to start their journey home again. The observed parameters were mostly similar across familiar and unfamiliar locations. The turning angles of saccadic body turning to the right or left showed some stereotypy, with a peak just under 45°. The direction of such saccades appears to be determined by a slow oscillatory process as described in other insect species. In timing, however, both the distribution of inter-scanning-bout intervals and individual fixation durations showed exponential characteristics, the signature for a random-rate or Poisson process. Neurobiologically, therefore, there must be some process that switches behaviour (starting a scanning bout or ending a fixation) with equal probability at every moment in time. We discuss how chance events in the ant brain that occasionally reach a threshold for triggering such behaviours can generate the results.

Comparative biology of spatial navigation in three arachnid orders (Amblypygi, Araneae, and Scorpiones).

From both comparative biology and translational research perspectives, there is escalating interest in understanding how animals navigate their environments. Considerable work is being directed towards understanding the sensory transduction and neural processing of environmental stimuli that guide animals to, for example, food and shelter. While much has been learned about the spatial orientation behavior, sensory cues, and neurophysiology of champion navigators such as bees and ants, many other, often overlooked animal species possess extraordinary sensory and spatial capabilities that can broaden our understanding of the behavioral and neural mechanisms of animal navigation. For example, arachnids are predators that often return to retreats after hunting excursions. Many of these arachnid central-place foragers are large and highly conducive to scientific investigation. In this review we highlight research on three orders within the Class Arachnida: Amblypygi (whip spiders), Araneae (spiders), and Scorpiones (scorpions). For each, we describe (I) their natural history and spatial navigation, (II) how they sense the world, (III) what information they use to navigate, and (IV) how they process information for navigation. We discuss similarities and differences among the groups and highlight potential avenues for future research.

Impact of central complex lesions on innate and learnt visual navigation in ants.

Wood ants are excellent navigators, using a combination of innate and learnt navigational strategies to travel between their nest and feeding sites. Visual navigation in ants has been studied extensively, however, we have little direct evidence for the underlying neural mechanisms. Here, we perform lateralized mechanical lesions in the central complex (CX) of wood ants, a midline structure known to allow an insect to keep track of the direction of sensory cues relative to its own orientation and to control movement. We lesioned two groups of ants and observed their behaviour in an arena with a large visual landmark present. The first group of ants were naïve and when intact such ants show a clear innate attraction to the conspicuous landmark. The second group of ants were trained to aim to a food location to the side of the landmark. The general heading of naïve ants towards a visual cue was not altered by the lesions, but the heading of ants trained to a landmark adjacent food position was affected. Thus, CX lesions had a specific impact on learnt visual guidance. We also observed that lateralised lesions altered the fine details of turning with lesioned ants spending less time turning to the side ipsilateral of the lesion. The results confirm the role of the CX in turn control and highlight its important role in the implementation of learnt behaviours that rely on information from other brain regions.

Anthropogenic subsidies influence resource use during a mange epizootic in a desert coyote population.

Colonization of urban areas by synanthropic wildlife introduces novel and complex alterations to established ecological processes, including the emergence and spread of infectious diseases. Aggregation at urban resources can increase disease transfer, with wide-ranging species potentially infecting outlying populations. The garrison at the National Training Center, Fort Irwin, California, USA, was recently colonized by mange-infected coyotes (Canis latrans) that also use the surrounding Mojave Desert. This situation provided an ideal opportunity to examine the effects of urban resources on disease dynamics. We evaluated seasonal space use and determined the influence of anthropogenic subsidies, water sources, and prey density on urban resource selection. We found no difference in home range size between healthy and infected individuals, but infected residents had considerably more spatial overlap with one another than healthy residents. All coyotes selected for anthropogenic subsidies during all seasons, while infected coyotes seasonally selected for urban water sources, and healthy coyotes seasonally selected for urban areas with greater densities of natural prey. These results suggest that while all coyotes were selecting for anthropogenic subsidies, infected resident coyotes demonstrated a greater tolerance for other conspecifics, which could be facilitating the horizontal transfer of sarcoptic mange to non-resident coyotes. Conversely, healthy coyotes also selected for natural prey and healthy residents exhibited a lack of spatial overlap with other coyotes suggesting they were not reliant on anthropogenic subsidies and were maintaining territories. Understanding the association between urban wildlife, zoonotic diseases, and urban resources can be critical in determining effective responses for mitigating future epizootics.

Insect navigation: Where to face when moving through space.

Ants perform oscillating scans of the environment during homing. A new study has shown that this scanning behaviour in ants is controlled by an intrinsic neuronal oscillator, which is modulated by both innate, and learnt visual cues.

The role of learning-walk related multisensory experience in rewiring visual circuits in the desert ant brain.

Efficient spatial orientation in the natural environment is crucial for the survival of most animal species. Cataglyphis desert ants possess excellent navigational skills. After far-ranging foraging excursions, the ants return to their inconspicuous nest entrance using celestial and panoramic cues. This review focuses on the question about how naïve ants acquire the necessary spatial information and adjust their visual compass systems. Naïve ants perform structured learning walks during their transition from the dark nest interior to foraging under bright sunlight. During initial learning walks, the ants perform rotational movements with nest-directed views using the earth's magnetic field as an earthbound compass reference. Experimental manipulations demonstrate that specific sky compass cues trigger structural neuronal plasticity in visual circuits to integration centers in the central complex and mushroom bodies. During learning walks, rotation of the sky-polarization pattern is required for an increase in volume and synaptic complexes in both integration centers. In contrast, passive light exposure triggers light-spectrum (especially UV light) dependent changes in synaptic complexes upstream of the central complex. We discuss a multisensory circuit model in the ant brain for pathways mediating structural neuroplasticity at different levels following passive light exposure and multisensory experience during the performance of learning walks.

What view information is most important in the homeward navigation of an Australian bull ant, Myrmecia midas?

Many insects orient by comparing current panoramic views of their environment to memorised views. We tested the navigational abilities of night-active Myrmecia midas foragers while we blocked segments of their visual panorama. Foragers failed to orient homewards when the front view, lower elevations, entire terrestrial surround, or the full panorama was blocked. Initial scanning increased whenever the visual panorama was blocked but scanning only increased along the rest of the route when the front, back, higher, or lower elevations were blocked. Ants meandered more when the front, the back, or the higher elevations were obscured. When everything except the canopy was blocked, the ants were quick and direct, but moved in random directions, as if to escape. We conclude that a clear front view, or a clear lower panorama is necessary for initial homeward headings. Furthermore, the canopy is neither necessary nor sufficient for homeward initial heading, and the back and upper segments of views, while not necessary, do make finding home easier. Discrepancies between image analysis and ant behaviour when the upper and lower views were blocked suggests that ants are selective in what portions of the scene they attend to or learn.

Vector navigation in walking bumblebees.

Path integration is a computational strategy that allows an animal to maintain an internal estimate of its position relative to a point of origin. Many species use path integration to navigate back to specific locations, typically their homes, after lengthy and convoluted excursions. Hymenopteran insects are impressive path integrators, directly returning to their hives after hundreds of meters of outward travel. Recent neurobiological insights have established hypotheses for how path integration vectors could be encoded in the brains of bees, but clear ways to test these hypotheses in the laboratory are currently unavailable. Here, we report that the bumblebee, Bombus terrestris, uses path integration while walking over short distances in an indoor arena. They estimate accurate vector distances after displacement and orient by artificial celestial cues. Walking bumblebees also exhibited systematic search patterns when home vectors failed to lead them accurately back to the nest, closely resembling searches performed by other species under natural conditions. We thus provide a robust experimental system to test navigation behavior in the laboratory that reflects most aspects of natural path integration. Importantly, we established this assay in an animal that is both readily available and resilient to invasive manipulations, as we demonstrate with the retention of the homing behavior post-anesthesia and surgery. In the future, our behavioral assay can therefore be combined with current electrophysiological techniques, opening a path toward directly probing the neural basis of the sophisticated vector navigation abilities of bees.

Rotation of skylight polarization during learning walks is necessary to trigger neuronal plasticity in Cataglyphis ants.

Many animals use celestial cues for impressive navigational performances in challenging habitats. Since the position of the sun and associated skylight cues change throughout the day and season, it is crucial to correct for these changes. Cataglyphis desert ants possess a time-compensated skylight compass allowing them to navigate back to their nest using the shortest way possible. The ants have to learn the sun's daily course (solar ephemeris) during initial learning walks (LW) before foraging. This learning phase is associated with substantial structural changes in visual neuronal circuits of the ant's brain. Here, we test whether the rotation of skylight polarization during LWs is the necessary cue to induce learning-dependent rewiring in synaptic circuits in high-order integration centres of the ant brain. Our results show that structural neuronal changes in the central complex and mushroom bodies are triggered only when LWs were performed under a rotating skylight polarization pattern. By contrast, when naive ants did not perform LWs, but were exposed to skylight cues, plasticity was restricted to light spectrum-dependent changes in synaptic complexes of the lateral complex. The results identify sky-compass cues triggering learning-dependent versus -independent neuronal plasticity during the behavioural transition from interior workers to outdoor foragers.

Investigating the impact of weak geomagnetic fluctuations on pigeon races.

The existence of avian magnetic orientation has been proved by many experimental studies, however, evidence for the use of magnetic cues by homing pigeons remains controversial. To investigate magnetic orientation by homing pigeons, we analyzed the results of pigeon races relative to weak fluctuations in the geomagnetic field, assuming that such disturbances could impact navigational efficiency if based on magnetoreception. Whereas most of the previous studies recorded and analyzed vanishing bearing of individually released pigeons, we evaluated relative duration of the homeward flight (homing speed, as a proxy of navigational efficiency) and its dependence on specific geomagnetic indices in racing pigeons released collectively. Our analysis of orientation efficiency of about 289 pigeon races over 15 years suggested slight negative correlations between geomagnetic fluctuations and homing time. Although the interpretation of this finding is manifold and not clear, it suggests that natural magnetic variations or disturbances can affect the homing orientation performance of pigeons. We suggest that studying pigeon races may have a heuristic potential and since these races are regularly and frequently organized in many countries all over the globe, examining homing performance relative to a suite of environmental variables may be useful for exploring hypotheses about pigeon navigation.

Magnetosensation during re-learning walks in desert ants (Cataglyphis nodus).

At the beginning of their foraging careers, Cataglyphis desert ants calibrate their compass systems and learn the visual panorama surrounding the nest entrance. For that, they perform well-structured initial learning walks. During rotational body movements (pirouettes), naïve ants (novices) gaze back to the nest entrance to memorize their way back to the nest. To align their gaze directions, they rely on the geomagnetic field as a compass cue. In contrast, experienced ants (foragers) use celestial compass cues for path integration during food search. If the panorama at the nest entrance is changed, foragers perform re-learning walks prior to heading out on new foraging excursions. Here, we show that initial learning walks and re-learning walks are structurally different. During re-learning walks, foragers circle around the nest entrance before leaving the nest area to search for food. During pirouettes, they do not gaze back to the nest entrance. In addition, foragers do not use the magnetic field as a compass cue to align their gaze directions during re-learning walk pirouettes. Nevertheless, magnetic alterations during re-learning walks under manipulated panoramic conditions induce changes in nest-directed views indicating that foragers are still magnetosensitive in a cue conflict situation.

Variable intraspecific space use supports optimality in an apex predator.

Within optimality theory, an animal's home range can be considered a fitness-driven attempt to obtain resources for survival and reproduction while minimizing costs. We assessed whether brown bears (Ursus arctos) in two island populations maximized resource patches within home ranges (Resource Dispersion Hypothesis [RDH]) or occupied only areas necessary to meet their biological requirements (Temporal Resource Variability Hypothesis [TRVH]) at annual and seasonal scales. We further examined how intrinsic factors (age, reproductive status) affected optimal choices. We found dynamic patterns of space use between populations, with support for RDH and TRVH at both scales. The RDH was likely supported seasonally as a result of bears maximizing space use to obtain a mix of nutritional resources for weight gain. Annually, support for RDH likely reflected changing abundances and distributions of foods within different timber stand classes. TRVH was supported at both scales, with bears minimizing space use when food resources were temporally concentrated. Range sizes and optimal strategies varied among sex and reproductive classes, with males occupying larger ranges, supporting mate seeking behavior and increased metabolic demands of larger body sizes. This work emphasizes the importance of scale when examining animal movement ecology, as optimal behavioral decisions are scale dependent.

Exogenous corticosterone and melanin-based coloration explain variation in juvenile dispersal behaviour in the barn owl (Tyto alba).

Natal dispersal affects many processes such as population dynamics. So far, most studies have examined the intrinsic and extrinsic factors that determine the distance between the place of birth and of first breeding. In contrast, few researchers followed the first steps of dispersal soon after fledging. To study this gap, we radio-tracked 95 barn owl nestlings (Tyto alba) to locate their diurnal roost sites from the fledging stage until December. This was used to test whether the age of nest departure, post-fledging movements and dispersal distance were related to melanin-based coloration, which is correlated to fitness-related traits, as well as to corticosterone, a hormone that mediates a number of life history trade-offs and the physiological and behavioural responses to stressful situations. We found that the artificial administration of corticosterone delayed the age when juveniles left their parental home-range in females but not in males. During the first few months after fledging, longer dispersal distances were reached by females compared to males, by individuals marked with larger black feather spots compared to individuals with smaller spots, by larger individuals and by those experimentally treated with corticosterone. We conclude that the onset and magnitude of dispersal is sensitive to the stress hormone corticosterone, melanin-based coloration and body size.

Visual control of refuge recognition in the whip spider Phrynus marginemaculatus.

Amblypygids, or whip spiders, are nocturnally active arachnids which live in structurally complex environments. Whip spiders are excellent navigators that can re-locate a home refuge without relying on visual input. Therefore, an open question is whether visual input can control any aspect of whip spider spatial behavior. In the current study, Phrynus marginemaculatus were trained to locate an escape refuge by discriminating between differently oriented black and white stripes placed either on the walls of a testing arena (frontal discrimination) or on the ceiling of the same testing arena (overhead discrimination). Regardless of the placement of the visual stimuli, the whip spiders were successful in learning the location of the escape refuge. In a follow-up study of the overhead discrimination, occluding the median eyes was found to disrupt the ability of the whip spiders to locate the shelter. The data support the conclusion that whip spiders can rely on vision to learn and recognize an escape shelter. We suggest that visual inputs to the brain's mushroom bodies enable this ability.

Recent expansion of marine protected areas matches with home range of grey reef sharks.

Dramatic declines in reef shark populations have been documented worldwide in response to human activities. Marine Protected Areas (MPAs) offer a useful mechanism to protect these species and their roles in coral reef ecosystems. The effectiveness of MPAs notably relies on compliance together with sufficient size to encompass animal home range. Here, we measured home range of 147 grey reef sharks, Carcharhinus amblyrhynchos, using acoustic telemetry in New Caledonia. The distribution of home range was then compared to local MPA sizes. We report a home range of 12 km2 of reef for the species with strong differences between adult males (21 km2), adult females (4.4 km2) and juveniles (6.2 km2 for males, 2.7 km2 for females). Whereas local historic MPA size seemed adequate to protect reef shark home range in general, these were clearly too small when considering adult males only, which is consistent with the reported failure of MPAs to protect sharks in New Caledonia. Fortunately, the recent implementation of several orders of magnitude larger MPAs in New Caledonia and abroad show that recent Indo-Pacific MPAs are now sufficiently large to protect the home ranges of this species, including males, across its geographical range. However, protection efforts are concentrated in a few regions and cannot provide adequate protection at a global scale.