Nocturnal Homing: Learning Walks in a Wandering Spider?

Homing by the nocturnal Namib Desert spider Leucorchestris arenicola (Araneae: Sparassidae) is comparable to homing in diurnal bees, wasps and ants in terms of path length and layout. The spiders'' homing is based on vision but their basic navigational strategy is unclear. Diurnal homing insects use memorised views of their home in snapshot matching strategies. The insects learn the visual scenery identifying their nest location during learning flights (e.g. bees and wasps) or walks (ants). These learning flights and walks are stereotyped movement patterns clearly different from other movement behaviours. If the visual homing of L. arenicola is also based on an image matching strategy they are likely to exhibit learning walks similar to diurnal insects. To explore this possibility we recorded departures of spiders from a new burrow in an unfamiliar area with infrared cameras and analysed their paths using computer tracking techniques. We found that L. arenicola performs distinct stereotyped movement patterns during the first part of their departures in an unfamiliar area and that they seem to learn the appearance of their home during these movement patterns. We conclude that the spiders perform learning walks and this strongly suggests that L. arenicola uses a visual memory of the burrow location when homing.     

Long-distance Homing Ability in Dasypoda altercator (Hymenoptera,Melittidae)

Homing rates and initial orientations after release from different directions were investigated in the solitary bee Dasypoda altercator. Homing rates and the proportion of individuals returning on the day of release declined with distance, implying that homing from greater distances is not based solely on the use of landmarks. A long duration of return (often not on the same day) and high efficiency of homing (four bees out of 10 returned from a 4 km distance over the lake), as well as an increase in average return speed ? 10 m/min) with distance of bees homing on the same day suggest that homing is also not based upon radial scatter as the sole tactic. This is supported by the observation that the initial orientations of the bees were not equally probable. Departures towards the sun greatly exceeded those away from the sun and the bees also tended to depart in cardinal geographical (or geomagnetic) directions, preferring meridional directions (especially southward) to parallel ones (of which east was preferred). Departure directions did not depend on wind direction but did depend, to some extent, on the landscape features of release sites. However, bees neither tended to depart in the direction of the nest, nor did homing success correlate with the direction of departure in relation to that of the nest.     

Altered Orientation and Flight Paths of Pigeons Reared on Gravity Anomalies: A GPS Tracking Study

The mechanisms of pigeon homing are still not understood, in particular how they determine their position at unfamiliar locations. The “gravity vector” theory holds that pigeons memorize the gravity vector at their home loft and deduct home direction and distance from the angular difference between memorized and actual gravity vector. However, the gravity vector is tilted by different densities in the earth crust leading to gravity anomalies. We predicted that pigeons reared on different gravity anomalies would show different initial orientation and also show changes in their flight path when crossing a gravity anomaly. We reared one group of pigeons in a strong gravity anomaly with a north-to-south gravity gradient, and the other group of pigeons in a normal area but on a spot with a strong local anomaly with a west-to-east gravity gradient. After training over shorter distances, pigeons were released from a gravitationally and geomagnetically normal site 50 km north in the same direction for both home lofts. As expected by the theory, the two groups of pigeons showed divergent initial orientation. In addition, some of the GPS-tracked pigeons also showed changes in their flight paths when crossing gravity anomalies. We conclude that even small local gravity anomalies at the birth place of pigeons may have the potential to bias the map sense of pigeons, while reactivity to gravity gradients during flight was variable and appeared to depend on individual navigational strategies and frequency of position updates.     

Homing by path integration in a new environment

Path integration was tested in golden hamsters, Mesocricetus auratus, within a new environment and in darkness. From the exit of its home cage, the subject was lured over a certain distance into the experimental arena, and then startled by a sudden noise to induce instantaneous homing. The subjects in experiment 1 had previously been tested within an identical arena in another building; they started the outward journey from a peripheral nest. Upon hearing the sound, all subjects returned in the correct direction to the arena border. In experiments 2 and 3, experimentally na?ve subjects started the outward trip from a central nest exit. Both groups initially oriented correctly, but only a few of subjects returned to the nest. According to computational considerations, experiment 1 required mainly the calculation of the homing direction, while experiments 2 and 3 required a homing vector. Furthermore, the experienced subjects may have been helped by their homing experience in the same type of arena, while the na?ve subjects may not have ‘trusted’ self-generated vector information sufficiently to follow it to the goal in an uncharted environment. Thus, the performance, but not the computation of self-generated vector information, may depend on the animal's experience. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Avian navigation: from historical to modern concepts

Studies on avian navigation began at the end of the 19th century with testing various hypotheses, followed by large-scale displacement experiments to assess the capacity of the birds' navigational abilities. In the 1950s, the first theoretical concepts were published. Kramer proposed his ‘Map-and-Compass’ model, assuming that birds establish the direction to a distant goal with the help of an external reference, a compass. The model describes homing as a two-step process, with the first step determining the direction to the goal as a compass course and the second step locating this course with the help of a compass. This model was widely accepted when numerous experiments with clock-shifted pigeons demonstrated the use of the sun compass, and thus a general involvement of compass orientation, in homing. The ‘map’ step is assumed to use local site-specific information, which led to the idea of a ‘grid map’ based on environmental gradients. Kramer's model still forms the basis of our present concept on avian homing, yet route integration with the help of an external reference provides an alternative strategy to determine the home course, and the magnetic compass is a second compass mechanism available to birds. These mechanisms are interrelated by ontogenetic learning processes. A two-step process, with the first step providing the compass course and the second step locating this course with the help of a compass, appears to be a common feature of avian navigation tasks, yet the origin of the compass courses differs between tasks according to their nature, with courses acquired by experience for flights within the home range, courses based on navigational processes for returning home, and courses derived from genetically coded information in first-time migrants. Compass orientation thus forms the backbone of the avian navigational system. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

A sedentary fish on the move: effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use

To understand how a sedentary fish responds to displacement and identify key habitat characteristics for that fish, we translocated long-snouted seahorses (Hippocampus guttulatus) within their natural habitat but far beyond their home range. After displacement, we located these small fish using acoustic technology and collected environmental data where we captured, released, and relocated them. Displaced fish (n?=?9) moved much greater distances (max: 150?m; mean daily: 6.4?C48.2?m) than expected from known home range movements and there was no evidence of homing. Seahorses varied in the specific environments they moved towards but tended to move towards environments more similar in both depth and water current speed to their original capture locations than their release locations.     

Overexpression of the Mesenchymal Stem Cell Cxcr4 Gene in Irradiated Mice Increases the Homing Capacity of These Cells

The efficiency of the intravascular delivery of mesenchymal stem cells (MSCs) homing to bone marrow has been largely limited. This study aimed to evaluate the homing efficacy in irradiated mice of MSCs that have been engineered to overexpress the murine Cxcr4 gene. Mouse MSCs were infected by a lentivirus vector carrying Cxcr4. MSC migration was detected by an in vitro transwell migration assay. EGFP-positive MSCs were systemically injected into BALB/c mice and detected in bone marrow samples by flow cytometry. The concentration of mouse stromal-derived factor 1 was detected by ELISA. The plasma concentration of the inflammatory cytokines, interleukin (IL)-6, IL-10, MCP-1, IFN-γ, TNF-α, and IL-12p70, were determined by cytometric bead array. MSCs that overexpressed Cxcr4 displayed enhanced migration toward a stromal-derived factor 1 gradient. The transplantation of Cxcr4-overexpressing MSCs into irradiated mice leads to increased homing to the bone marrow. Moreover, the frequency of the EGFP-positive cells in a bone marrow infusion 24 h after total body irradiation was 2.2-fold more than at 4 h after irradiation. The concentration of both plasma and bone marrow stromal-derived factor 1 increased after irradiation, and this was positively correlated with the number of Cxcr4-overexpressing MSCs homing to the bone marrow. Moreover, compared with the control groups, the plasma levels of IL-6, IFN-γ, TNF-α, and MCP-1 and IL-12p70 in recipients infused with Cxcr4-overexpressing MSCs was significantly decreased. The level of IL-10 was increased, which correlated with changes in the Th1 and Th2 subset balance. MSCs that overexpressed Cxcr4 and were injected into irradiated mice had an enhanced homing capacity which was related to the bone marrow level of stromal-derived factor 1.     

Role of olfaction and vision in homing behaviour of black rockfish Sebastes inermis

How fish find their original habitat and natal home remains an unsolved riddle of animal behaviour. Despite extensive efforts to study the homing behaviour of diadromous fish, relatively little attention has been paid to that of non-diadromous marine fish. Among these, most rockfish of the genus Sebastes exhibit homing ability and/or a strong fidelity to their habitats. However, how these rockfish detect the homeward direction has not been clarified. The goal of the present research was to investigate the sensory mechanisms involved in the homing behaviour of the black rockfish Sebastes inermis, using acoustic telemetry. Vision-blocked or olfactory-ablated rockfish were released in natural waters and their homing behaviours compared with those of intact or control individuals. Blind rockfish showed homing from both inside and outside their habitat. The time taken by blind fish to reach their home habitat was not significantly different from that of the control fish. In contrast, most olfactory-ablated fish did not successfully reach their original habitat. Our results indicate that black rockfish predominantly use the olfactory sense in their homing behaviour.     

Visual marks learned by the solitary bee Megachile rotundata for localizing its nest

We studied homing behaviour of leaf-cutter bees, Megachile rotundata, by using artificial landmarks. We evaluated their nest-searching behaviour in different test situations to elucidate the nature of the visual marks they used in this task. When we modified or removed geometrical figures surrounding the nest, the bees searched for longer, showing that they noticed the introduced changes. However, these manipulations never prevented bees from finding their nest, suggesting that other visual cues were crucial in the task. Manipulations of the edges provided by the boundaries of the device (nest block, metal sheet on which the block was mounted) strongly impaired the homing performance. The further away the edges that were left intact, the stronger was the impairment of the homing behaviour. These results suggest that bees learn the distances of the various edges from the goal and that edges have a hierarchical significance according to their distance from the nest. The most distant edges provide vague information, which suffices to guide the insect towards the next edge in the sequence, until it recognizes the final, precise location of the nest. The results support the conclusion that information on distances is acquired using cues derived from motion parallax generated by the insect's self-motion. Recognition of edge parameters such as position and orientation might be achieved by an image-matching mechanism based on dynamic processes. Thus, in the homing task, there is no clear discrepancy between the eidetic and the parametric hypotheses of spatial representation.     

Landmark cues can change the motivational state of desert ant foragers

Desert ants of the genus Cataglyphis rely on path integration vectors to return to the nest (inbound runs) and back to frequently visited feeding sites (outbound runs). If disturbed, e.g., experimentally displaced on their inbound runs, they continue to run off their home-bound vector, but if disturbed in the same way on their outbound runs, they do not continue their feeder-based vector, but immediately switch on the home-bound state of their path integration vector and return to the nest. Here we show that familiar landmarks encountered by the ants during their run towards the feeder can change the ants’ motivational state insofar that the ants even if disturbed continue to run in the nest-to-feeder direction rather than reverse their courses, as they do in landmark-free situations. Hence, landmark cues can cause the ants to change their motivational state from homing to foraging.     

Dispersal behaviour of individuals in metapopulations of two British butterflies

Dispersal patterns are important in metapopulation ecology because they affect the dynamics and survival of populations. However, because little empirical information exists on dispersal behaviour of individuals, theoretical models usually assume random dispersal. Recent empirical evidence, by contrast, suggests that the butterfly Maniola jurtina uses a non‐random, systematic dispersal strategy, can detect and orient towards habitat from distances of 100–150 m, and prefers a familiar habitat patch over a non‐familiar one (‘homing behaviour’). The present study (1) investigated whether these results generalise to another butterfly species, Pyronia tithonus; and (2) examined the cause of the observed ‘homing behaviour’ in M. jurtina. P. tithonus used a similar non‐random, systematic dispersal strategy to M. jurtina, had a similar perceptual range for habitat detection and preferred a familiar habitat patch over a non‐familiar one. The ‘homing behaviour’ of M. jurtina was found to be context‐dependent: individual M. jurtina translocated within habitat did not return towards their capture point, whereas individuals translocated similar distances out of habitat did return to their ‘home’ patch. We conclude that butterfly ‘homing behaviour’ is not based on an inherent preference for a familiar location, but that familiarity with an area facilitates the recognition of suitable habitat, towards which individuals orient if they find themselves in unsuitable habitat. Contrary to conventional wisdom, we suggest that frequent, short ‘excursions’ over habitat patch boundaries are evolutionarily advantageous to individuals, because increased familiarity with the surrounding environment is likely to increase the ability of a straying animal to return to its natural habitat, and to reduce the rate of mortality experienced by individuals attempting to disperse between habitat patches. We discuss the implications of the non‐random dispersal for existing metapopulation models, including models of the evolution of dispersal rates.     

Interactions of the polarization and the sun compass in path integration of desert ants

Desert ants, Cataglyphis fortis, perform large-scale foraging trips in their featureless habitat using path integration as their main navigation tool. To determine their walking direction they use primarily celestial cues, the sky’s polarization pattern and the sun position. To examine the relative importance of these two celestial cues, we performed cue conflict experiments. We manipulated the polarization pattern experienced by the ants during their outbound foraging excursions, reducing it to a single electric field (e-)vector direction with a linear polarization filter. The simultaneous view of the sun created situations in which the directional information of the sun and the polarization compass disagreed. The heading directions of the homebound runs recorded on a test field with full view of the natural sky demonstrate that none of both compasses completely dominated over the other. Rather the ants seemed to compute an intermediate homing direction to which both compass systems contributed roughly equally. Direct sunlight and polarized light are detected in different regions of the ant’s compound eye, suggesting two separate pathways for obtaining directional information. In the experimental paradigm applied here, these two pathways seem to feed into the path integrator with similar weights.     

Multistep Navigation and the Combinatorial Control of Leukocyte Chemotaxis

Cells migrating within tissues may encounter multiple chemoattractant signals in complex spatial and temporal patterns. To understand leukocyte navigation in such settings, we have explored the migratory behavior of neutrophils in model scenarios where they are presented with two chemoattractant sources in various configurations. We show that, over a wide range of conditions, neutrophils can migrate “down” a local chemoattractant gradient in response to a distant gradient of a different chemoattractant. Furthermore, cells can chemotax effectively to a secondary distant agonist after migrating up a primary gradient into a saturating, nonorienting concentration of an initial attractant. Together, these observations suggest the potential for cells' step-by-step navigation from one gradient to another in complex chemoattractant fields. The importance of such sequential navigation is confirmed here in a model system in which neutrophil homing to a defined domain (a) requires serial responses to agonists presented in a defined spatial array, and (b) is a function of both the agonist combination and the sequence in which gradients are encountered. We propose a multistep model of chemoattractant-directed migration, which requires that leukocytes display multiple chemoattractant receptors for successful homing and provides for combinatorial determination of microenvironmental localization.     

Collective Decision-Making in Homing Pigeons: Larger Flocks Take Longer to Decide but Do Not Make Better Decisions

Social animals routinely are challenged to make consensus decisions about movement directions and routes. However, the underlying mechanisms facilitating such decision-making processes are still poorly known. A prominent question is how group members participate in group decisions. We addressed this question by examining how flocks of homing pigeons (Columba livia) decide their homing direction. We released newly formed flocks varying in size and determined the time taken to choose a homing direction (decision-making period) and the accuracy of that choice. We found that the decision-making period increases exponentially with flock size, which is consistent with a participatory decision-making process. We additionally found that there is no effect of flock size on the accuracy of the decisions made, which does not match with current theory for democratic choices of flight directions. Our combined results are better explained by a participatory choice of leaders that subsequently undertake the flock directional decisions. However, this decision-making model would only entirely fit with our results if leaders were chosen based on traits other than their navigational experience. Our study provides rare empirical evidence elucidating decision-making processes in freely moving groups of animals.     

Conditions for landmark-based navigation in the house mouse, Mus musculus

I investigated whether mice, after learning to home by relying on visual extra-arena landmarks, still required instantaneous access to such cues for successful navigation. Two groups of lactating mice were trained to retrieve their pups from the centre of a circular arena back to their peripheral nest. On test trials, mice from one group were allowed to view distal visual cues while moving from the nest towards the centre, and mice from the other group were allowed to view distal visual cues when homing from the centre towards the nest. The results indicate that viewing the visual cues when homing is necessary for landmark-based navigation.     

Polarized skylight does not calibrate the compass system of a migratory bat

In a recent study, Greif et al. (Greif et al. Nat Commun 5, 4488. (doi:10.1038/ncomms5488)) demonstrated a functional role of polarized light for a bat species confronted with a homing task. These non-migratory bats appeared to calibrate their magnetic compass by using polarized skylight at dusk, yet it is unknown if migratory bats also use these cues for calibration. During autumn migration, we equipped Nathusius'' bats, Pipistrellus nathusii, with radio transmitters and tested if experimental animals exposed during dusk to a 90° rotated band of polarized light would head in a different direction compared with control animals. After release, bats of both groups continued their journey in the same direction. This observation argues against the use of a polarization-calibrated magnetic compass by this migratory bat and questions that the ability of using polarized light for navigation is a consistent feature in bats. This finding matches with observations in some passerine birds that used polarized light for calibration of their magnetic compass before but not during migration.     

Do release-site biases reflect response to the Earth's magnetic field during position determination by homing pigeons?

How homing pigeons (Columba livia) return to their loft from distant, unfamiliar sites has long been a mystery. At many release sites, untreated birds consistently vanish from view in a direction different from the home direction, a phenomenon called the release-site bias. These deviations in flight direction have been implicated in the position determination (or map) step of navigation because they may reflect local distortions in information about location that the birds obtain from the geophysical environment at the release site. Here, we performed a post hoc analysis of the relationship between vanishing bearings and local variations in magnetic intensity using previously published datasets for pigeons homing to lofts in Germany. Vanishing bearings of both experienced and naïve birds were strongly associated with magnetic intensity variations at release sites, with 90 per cent of bearings lying within ±29° of the magnetic intensity slope or contour direction. Our results (i) demonstrate that pigeons respond in an orderly manner to the local structure of the magnetic field at release sites, (ii) provide a mechanism for the occurrence of release-site biases and (iii) suggest that pigeons may derive spatial information from the magnetic field at the release site that could be used to estimate their current position relative to their loft.     

Pigeon homing and magnetic fields: a response to Luschi et al. (1996)

This paper comments on an article ''Pigeon homing: evidence against reliance on magnetic information picked up en route at release sites'' by P. Luschi, C. del Seppia, E. Crosio and F. Papi, which appeared in this journal. It is pointed out that the particular effects which these authors show to be stress-induced artefacts are restricted to their specific strain of homing pigeons. The same effects could not be observed in pigeons from two other lofts: a difference in response that was shown to have a genetic base. In view of this, conclusions drawn from the results of Luschi et al. must be restricted to their own findings; they cannot be generalized to the other findings which indicate the use of magnetic outward journey information in young homing pigeons.     

Cells responding to chemoattractant on a structured substrate

Cell migration on an adhesive substrate surface comprises actin-based protrusion at the front and retraction of the tail in combination with coordinated adhesion to, and detachment from, the substrate. To study the effect of cell-to-substrate adhesion on the chemotactic response of Dictyostelium discoideum cells, we exposed the cells to patterned substrate surfaces consisting of adhesive and inert areas, and forced them by a gradient of chemoattractant to enter the border between the two areas. Wild-type as well as myosin II-deficient cells stop at the border of an adhesive area. They do not detach with their rear part, while on the nonadhesive area they protrude pseudopods at their front toward the source of chemoattractant. Avoidance of the nonadhesive area may cause a cell to move in tangential direction relative to the attractant gradient, keeping its tail at the border of the adhesive surface.     

Avian olfactory navigation: its empirical foundation and conceptual state

Over the last three decades, empirical evidence has been accumulated indicating that displaced homing pigeons, and most likely other birds as well, are able to navigate home by deducing positional information from atmospheric trace gases perceived by olfaction. I briefly describe the most important results leading to this unexpected conclusion and experiments revealing the decisive role of winds at the home site. A hypothesis trying to explain the results proposes that proportional relationships among a number of atmospheric trace compounds (which determine the quality of a resulting odour) show fairly regular spatial distributions with gradient character. Gas-chromatographic analyses of air samples in an area covering 400 km in diameter revealed that differently oriented ratio gradients of volatile hydrocarbons do in fact exist. They are fairly resistant against, but not independent of, changes of wind direction. Using the measured atmospheric data as inputs, a model system is able to simulate homing navigation on a performance level similar to that observed in pigeons. Results of both pigeon experiments and air analyses are incorporated into an earlier (‘preolfactory’) concept of a hypothetical gradient map linked with a sun compass, which is now modified and furnished with more concrete physical substrates. Winds are identified as the crosslink embedding atmospheric ratio gradients into a directional reference scale provided by the periodically moving sun and the geomagnetic field. Kramer's ‘map-and-compass concept’ is reconsidered. As crucial questions are still unsolved, olfactory navigation remains a challenge for future research.