Homing pigeons as a model for avian navigation?

The findings on the navigational mechanisms of homing pigeons and the available data on those of wild birds, in particular migrants, are compared. There are important parallels in the use of the magnetic field and the sun for directional orientation. Also the findings on the navigational ‘map’, its preferred use by experienced birds and the strategy of using route information to acquire the necessary knowledge to establish the ‘map’, obtained in pigeons studies, can probably be generalized to wild birds and migrants in their home region. It seems that birds share a common navigational system. Special development of migratory birds, however, is the innate migration program that enables young first‐time migrants to reach their still unknown wintering area.     

The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period

Homing pigeons can learn a navigational map by relying on the heterogeneous distribution of atmospheric odours in the environment. To test whether there might be a sensitive period for learning an olfactory-based navigational map, we maintained a group of young pigeons in an aviary screened from the winds until the age of three to four months post-fledging. Subsequently, the screens were removed and the pigeons were exposed to the winds and the environmental odours they carry for three months. One control group of pigeons was held in a similar aviary but exposed to the winds immediately upon Hedging, while another control group of pigeons was allowed free-flight. When the pigeons from the three groups were released from two distant release sites at about six months of age post-fledging, the two control groups were found to be equally good at orientating and returning home, while the experimental pigeons held in the shielded aviary for the first three months post-fledging were unable to orientate homeward and they were generally unsuccessful in returning home. This result supports the hypothesis that environmental experience during the first three months post-fledging is critical for some aspect of navigational map learning and that navigational map learning displays sensitive period-like properties.     

The Role of “Outward-Journey Information” in Homing Experiments with Pigeons: New Data on Ontogeny of Navigation and General Survey

Potentially, homing from distant areas can be based on two different principles of navigation: (1) A path-integration mechanism records and integrates an animal's motions during the outward trip; it is independent of location-specific stimuli. (2) Site localization, by contrast, is performed by deducing the animal's position in relation to home from such stimuli. Hence the first mechanism entirely depends on an uninterrupted flow of “outward-journey information”. The second mechanism may but need not be independent of stimuli recorded during the outward journey. Homing of pigeons is evidently based on site localization. Empirical findings do not support the idea that in experiments using passive displacement path integration is involved in addition or alternatively. Also, there is no reason to assume that very young pigeons transitionally, for only few weeks, apply such a method (as has been concluded by Wiltschko & Wiltschko 1982, 1985, etc.). It is shown that very young pigeons require local olfactory signals for initial homeward orientation as do older birds (Fig. 1). They are not generally better at homeward orientation than older inexperienced pigeons and show similar deviations from home and preferences for a particular compass direction (Table 1, Fig. 2). Olfactory signals appear to be gathered, as good as conditions allow, during any stage of a homing experiment. No fundamental difference can be recognized between olfactory “outward-journey information”, “release-site information”, etc. Signals received at different times and sites before release may contribute by varying proportions to the initial-orientation patterns observed under varying circumstances.     

The magnetite-based receptors in the beak of birds and their role in avian navigation

Iron-rich structures have been described in the beak of homing pigeons, chickens and several species of migratory birds and interpreted as magnetoreceptors. Here, we will briefly review findings associated with these receptors that throw light on their nature, their function and their role in avian navigation. Electrophysiological recordings from the ophthalmic nerve, behavioral studies and a ZENK-study indicate that the trigeminal system, the nerves innervating the beak, mediate information on magnetic changes, with the electrophysiological study suggesting that these are changes in intensity. Behavioral studies support the involvement of magnetite and the trigeminal system in magnetoreception, but clearly show that the inclination compass normally used by birds represents a separate system. However, if this compass is disrupted by certain light conditions, migrating birds show ‘fixed direction’ responses to the magnetic field, which originate in the receptors in the beak. Together, these findings point out that there are magnetite-based magnetoreceptors located in the upper beak close to the skin. Their natural function appears to be recording magnetic intensity and thus providing one component of the multi-factorial ‘navigational map’ of birds.     

Development of the navigational map in homing pigeons: effects of flight experience on orientation performance

Experiments have shown that pigeons, Columba livia, are able to develop navigational abilities even if reared and kept confined in an aviary, provided that they are exposed to the natural winds. In contrast, pigeons reared in a wind-screened aviary do not learn to navigate. Pigeons kept confined in a screened aviary when young do not learn to navigate even if, once they become adult, the screens are removed and the birds are exposed to natural winds for a period sufficiently long for map learning. In all of these experiments, pigeons were kept confined until the day of test release. In the present study we found that pigeons reared in a wind-screened aviary developed navigational abilities if, once adult, they were allowed to perform spontaneous flights around the loft. Nevertheless, their navigational performance never reached the level of controls.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Pigeon Homing: The Orientation of Young Birds that had been Prevented from Seeing the Sun

To test whether the sun is an essential factor for the development of a functioning orientation system in birds, a group of young pigeons was raised as ‘No-Sun’-birds. They were not allowed to see the sun, and they were released to fly around their loft only under total overcast. The control group had an equal number of opportunities to fly under overcast plus additional flights under sun. When released as untrained birds under solid cloud cover, the ‘No-Sun’-birds were significantly oriented, whereas the controls were not. Small magnets glued between the wings (north toward the head) reversed the ‘No-Sun’-birds' orientation, indicating they used a magnetic compass. These findings show that the orientation system can develop without information from the sun. Differences in the orientation behavior of the ‘No-Sun’-birds and normally raised young pigeons are discussed.     

Light-dependent information: influence of loft conditions on young pigeon’s navigational system

This study compares the initial orientation and homing performance of young inexperienced pigeons following their transportation to near and distant places in total darkness (treatment) and their subsequent release. The birds were housed in two lofts at the Lisbon Zoo. Each loft had its own specific features: the H-loft was exposed to prevailing winds and allowed an unhindered view of the surrounding landscape; the L-loft was protected from the wind and allowed only a partial view of the surroundings. Pigeons used in the release tests were between 6 and 7 weeks old. We found that, in general, the initial orientation of the pigeons was affected by the treatment: following release at near places, there was an increase in the scatter and a decrease the homeward component, suggesting that light-dependent information collected en route was used by young pigeons. The effect of the treatment was only temporary based on the observation that the homing performance was not affected. However, the distance of the release site strongly influenced the homing performances as pigeons appeared to be unable to home when released at locations distant from the loft. Based on the scatter or the homeward component, inter-loft differences were apparent with respect to different median vanishing intervals and the reactions of specific pigeons when subjected to the same treatment (transport in darkness) following release at near and distant places. These findings suggest that light-dependent information collected en route is a component of the young pigeon’s navigational system but that, at the young age of the birds tested here, it is preferentially used in familiar areas. In addition, the importance of the light-dependent information appears to depend upon prior experience obtained in the lofts.     

The Effects of Zinc Sulphate Anosmia on Homing Pigeons,Columba livia,in a Homing and a Non-homing Experiment

There is debate over whether homing pigeons, Columba livia, use olfactory information as part of their navigational map. Antagonists of the theory argue that homing deficits noted in anosmic pigeons may be due to a non-specific impairment in general information processing. In Experiment I, we present data from a modest investigation describing the typical navigational deficits that occur following zinc sulphate-mediated anosmia. Our results are consistent with previous experiments that noted impairments in homing performance from unfamiliar locations of anosmic pigeons. Experiment II is a critical experiment that involved a spatial working memory paradigm; this paradigm consisted of testing zinc sulphate-treated birds in a forced-choice alternation task in a T-maze. This experiment allowed us to determine whether anosmic pigeons were impaired in memory performance, a robust measure of general information processing. There were no differences between the last day of training and a subsequent-test day when pigeons received an intranasal injection of zinc sulphate. This experiment suggests that zinc sulphate anosmia does not impair general information processing, supporting the hypothesis that homing pigeons use olfactory cues when homing from unfamiliar locations.     

Pigeon Homing: The Navigational Map Developed in Adulthood is Based on Olfactory Information

Homing pigeons raised in a shielded aviary and kept confined until the day of the test releases are not able to navigate even if, once adult, the screens are removed and the birds are exposed to natural winds for a sufficiently long period for map learning. However, pigeons raised in the same condition but, once adult, allowed to perform spontaneous flights around the loft are able to develop navigational abilities which, however, never reach the level of controls. In the present study, we show that the navigational map learned by the adult birds, which had the possibility to perform spontaneous flights, is based on olfactory information.     

Does pigeon homing depend on stimuli perceived during displacement?

Summary In order to test whether stimuli perceived during passive displacement are important for the subsequent homing, pigeons were transported in an apparatus designed to prevent them from receiving relevant information: The experimental birds were continuously rotated quite rapidly (1.5 cps, radial acceleration about 4 g); in addition, they were exposed to an artificial magnetic field and supplied with bottled air. Control birds were transported in open-air cages on top of the van with free view to all sides.Five pairs of releases from equal distances in opposite directions were conducted. Experienced birds were released at distances of about 15, 90, and 300 km from the loft, inexperienced birds at distances of about 180km. In each pair of releases both groups of pigeons were significantly homeward oriented. Neither in initial orientation nor in homing performance nor in the distribution of recoveries were the experimental birds inferior to the controls or in any perceptable way different from them.It is concluded that homing of passively displaced pigeons is not primarily based on information gathered during the outward journey.Abbreviations EP experimental pigeon(s) - CP control pigeon(s) The possibility to maintain our pigeon loft in a building that belongs to the Zoological Institute (Prof. M. Lindauer) of the University of Würzburg is gratefully acknowledged.     

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.     

Pigeon Navigation: Different Routes Lead to Frankfurt

Background

Tracks of pigeons homing to the Frankfurt loft revealed an odd phenomenon: whereas birds returning from the North approach their loft more or less directly in a broad front, pigeons returning from the South choose, from 25 km from home onward, either of two corridors, a direct one and one with a considerable detour to the West. This implies differences in the navigational process.

Methodology/Principle Findings

Pigeons released at sites at the beginning of the westerly corridor and in this corridor behave just like pigeons returning from farther south, deviating to the west before turning towards their loft. Birds released at sites within the straight corridors, in contrast, take more or less straight routes. The analysis of the short-term correlation dimension, a quantity reflecting the complexity of the system and with it, the number of factors involved in the navigational process, reveals that it is significantly larger in pigeons choosing the westerly corridor than in the birds flying straight - 3.03 vs. 2.85. The difference is small, however, suggesting a different interpretation of the same factors, with some birds apparently preferring particular factors over others.

Conclusions

The specific regional distribution of the factors which pigeons use to determine their home course seems to provide ambiguous information in the area 25 km south of the loft, resulting in the two corridors. Pigeons appear to navigate by deriving their routes directly from the locally available navigational factors which they interpret in an individual way. The fractal nature of the correlation dimensions indicates that the navigation process of pigeons is chaotic-deterministic; published tracks of migratory birds suggest that this may apply to avian navigation in general.     

The Orientational Consequences of Flocking Behaviour in Homing Pigeons,Columba livia

Two experiments are described which investigate the orientational consequences of flocking in homing pigeons Columba livia. Previous experiments have shown that homing pigeons placed inside a clear-sided release box for 5 min before release from a familiar site have enhanced ground homing speed compared with those placed in an opaque-sided box. It is assumed that previewing the surrounding landscape allows for faster homing since a bird denied this information must accumulate the knowledge on release. In experiment 1, using the same technique developed in these experiments but releasing the birds in pairs we showed that within familiar areas, homing pigeons can exploit a partner that has acquired more information, allowing them to home more quickly. In experiment 2 we attempted to test three potential strategies which may occur during homing flights. The results do not conclusively distinguish between these three mechanisms but suggest that orientation of the pairs of birds is most likely to have resulted from a compromise of individual tendencies, or from following the best homer, but not from following a ‘governing leader’. The consequence of these mechanisms is discussed.     

Changes in the short-term deflector loft effect are linked to the sun compass of homing pigeons

Despite being the most studied of all avian orientation systems, important questions still remain about the sun compass of homing pigeons, Columba livia. White it is well-documented that the sun compass is usually learned by young pigeons during the first 10–12 weeks of life, the mechanism by which it is calibrated to adjust for seasonal changes in the sun's azimuth is not known with certainty. Previous experiments using short-term deflector loft pigeons indicated that the sun compass may be calibrated by referencing celestial polarization patterns. The present paper describes important measurable changes in the previously reported orientation behaviour of short-term deflector loft birds, and suggests a correlation between these changes and the presence of a massive upper-atmospheric dust cloud of volcanic origin which significantly altered natural skylight polarization patterns in 1982 and 1983. Moreover, it is shown that when the short-term effect was absent (at times when data from previous years suggested it should be present), the birds were also not using sun compass orientation, as demonstrated by their failure to show the standard ‘clockshift’ response to a 6-h fast shift of their internal clocks. These results support the hypothesis that reflected light cues, rather than odours, are the basis of the deflector loft effect in pigeon homing.     

Not just passengers: pigeons,Columba livia,can learn homing routes while flying with a more experienced conspecific

For animals that travel in groups, the directional choices of conspecifics are potentially a rich source of information for spatial learning. In this study, we investigate how the opportunity to follow a locally experienced demonstrator affects route learning by pigeons over repeated homing flights. This test of social influences on navigation takes advantage of the individually distinctive routes that pigeons establish when trained alone. We found that pigeons learn routes just as effectively while flying with a partner as control pigeons do while flying alone. However, rather than learning the exact route of the demonstrator, the paired routes shifted over repeated flights, which suggests that the birds with less local experience also took an active role in the navigational task. The efficiency of the original routes was a key factor in how far they shifted, with less efficient routes undergoing the greatest changes. In this context, inefficient routes are unlikely to be maintained through repeated rounds of social transmission, and instead more efficient routes are achieved because of the interaction between social learning and information pooling.     

Homing pigeons only navigate in air with intact environmental odours: a test of the olfactory activation hypothesis with GPS data loggers

A large body of evidence has shown that anosmic pigeons are impaired in their navigation. However, the role of odours in navigation is still subject to debate. While according to the olfactory navigation hypothesis homing pigeons possess a navigational map based on the distribution of environmental odours, the olfactory activation hypothesis proposes that odour perception is only needed to activate a navigational mechanism based on cues of another nature. Here we tested experimentally whether the perception of artificial odours is sufficient to allow pigeons to navigate, as expected from the olfactory activation hypothesis. We transported three groups of pigeons in air-tight containers to release sites 53 and 61 km from home in three different olfactory conditions. The Control group received natural environmental air; both the Pure Air and the Artificial Odour groups received pure air filtered through an active charcoal filter. Only the Artificial Odour group received additional puffs of artificial odours until release. We then released pigeons while recording their tracks with 1 Hz GPS data loggers. We also followed non-homing pigeons using an aerial data readout to a Cessna plane, allowing, for the first time, the tracking of non-homing homing pigeons. Within the first hour after release, the pigeons in both the Artificial Odour and the Pure Air group (receiving no environmental odours) showed impaired navigational performances at each release site. Our data provide evidence against an activation role of odours in navigation, and document that pigeons only navigate well when they perceive environmental odours.     

Homing pigeons develop local route stereotypy

The mechanisms used by homing pigeons (Columba livia) to navigate homeward from distant sites have been well studied, yet the mechanisms underlying navigation within, and mapping of, the local familiar area have been largely neglected. In the local area pigeons pote ntially have access to a powerful navigational aid--a memorized landscape map. Current opinion suggests that landmarks are used only to recognize a familiar start position and that the goalward route is then achieved solely using compass orientation. We used high-resolution global positioning system (GPS) loggers to track homing pigeons as they became progressively familiar with a local homing task. Here, we demonstrate that birds develop highly stereotyped yet individually distinctive routes over the landscape, which remain substantially inefficient. Precise aerial route recapitulation implies close control by localized geocentric cues. Magnetic cues are unlikely to have been used, since recapitulation remains despite magnetic disruption treatment, and olfactory cues would have been positionally unstable under the variable wind conditions, making visual landmarks the most likely cues used.     

Time‐of‐Day Discriminative Learning: Contrasting the Use of Spatial Compared to Feature Information in Homing Pigeons (Columba livia)

This study examined time‐of‐day associative learning to either spatial or feature information in homing pigeons in an open‐field, laboratory setting. Homing pigeons are well known for their navigational abilities and generally have been shown to rely more heavily on spatial than nonspatial cues in recognizing a goal. However, during goal localization, homing pigeons also successfully use nonspatial, feature information. Homing pigeons were divided into two groups and were trained to locate two time‐of‐day dependent, food reward sites using either discriminative spatial or feature information. Because of the importance of the hippocampus in controlling avian memory, we hypothesized that homing pigeons trained with spatial cues would be superior in learning the time‐of‐day discrimination compared to the pigeons trained with feature cues. Indeed, homing pigeons that were trained with spatial information outperformed the pigeons trained with feature information in learning the time‐of‐day discrimination task.     

Das Orientierungssystem der V?gel II. Heimfinden und Navigation

Zusammenfassung Die Analyse des Navigationssystems der Vögel bezieht sich meist auf Versuche mit Brieftauben. Kramers Karte-Kompaß-Prinzip geht davon aus, daß die Heimrichtung zunächst als Kompaßkurs bestimmt wird. Dies wurde durch zahlreiche Zeitumstimmungsversuche bestätigt. Damit erscheinen nur zwei Navigationsstrategien möglich: (1) Benutzen von Weginformation, die auf einem Richtungsreferenzsystem beruht, und (2) Benutzen von Ortsinformation, deren Richtungsbeziehung zum Ziel bekannt ist.Junge Tauben, denen während der Verfrachtung der Zugang zu magnetischer Information verwehrt worden war, flogen ungerichtet ab. Dies spricht für eine Navigationsstrategie, bei der die Richtung des Hinwegs mit dem Magnetkompaß gemessen wird. Diese Art von Wegintegration stellt aber nur eine erste Strategie sehr junger, unerfahrener Tauben dar; sobald wie möglich benutzen die Tauben Ortsinformation, denn diese erlaubt Nachbestimmung des Heimkurses und damit das Korrigieren von Fehlern.Navigation anhand von Ortsinformation bedeutet, daß Vögel den Heimkurs aufgrund von Faktoren am Auflaßort bestimmen. Die modernen Vorstellungen berücksichtigen die zentrale Rolle eines äußeren Referenzsystems und gehen von einer Navigationskarte aus, die einer kompaßmäßig ausgerichteten mentalen Repräsentation des Verlaufs der Navigationsfaktoren entspricht. Der Heimkurs wird aus den Unterschieden zwischen den Werten am Auflaßort und denen am Heimatort abgeleitet. Da es sich bei den Navigationsfaktoren um Gradienten handelt, können die Vögel deren Verlauf extrapolieren und ihren Heimkurs auch in unbekanntem Gelände bestimmen. Unregelmäßigkeiten im Gradientenverlauf führen zu Abweichungen von der Heimrichtung, sogenannten Ortsmißweisungen. In der Nähe des Heimatorts wird die Navigationskarte durch eine entsprechende Mosaik-Karte von Landmarken ergänzt.Beide Karten werden durch Lernvorgänge erstellt. Junge Tauben verschaffen sich die notwendige Information auf spontanen Flügen, indem sie Information über den zurückgelegten Weg mit Ortsinformation verknüpfen und gemeinsam in den Karten abspeichern. Bei Tauben wird die Navigationskarte etwa im dritten Lebensmonat funktionstüchtig, aber sie wird auch später noch ständig erweitert und verbessert. Ihre Größe hängt von der Erfahrung der Vögel ab. Die Karte enthält offenbar Entfernungsangaben und erlaubt freie Flüge zwischen beliebigen Zielen. In einigen Punkten entspricht sie der in der psychologischen Literatur diskutierten kognitiven Karte.Das Navigationssystem der Vögel ist dadurch gekennzeichnet, daß sie sich mit Hilfe eines einfachen angeborenen Mechanismus, des Magnetkompaß, viele andere Faktoren durch Lernvorgänge nutzbar machen und diese in komplexe Mechanismen wie die Karten integrieren.

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The orientation system of birds — II. Homing and navigation

Summary The analysis of the navigational system of birds is largely based on experiments with displaced homing pigeons. Kramer's map-and-compass model assumes that the home direction is first established as a compass course. This is confirmed by numerous clock-shift experiments. Consequently, only two types of navigational strategy appear possible: (1) the use of route-specific information based on an external reference or (2) the use of site-specific information whose directional relationship is familiar to the birds.The use of route-specific information is indicated by the finding that young birds deprived of magnetic information during displacement were disoriented, whereas birds receiving the same treatment at the release site were not. This suggests that birds navigate by recording the direction of the outward journey with their magnetic compass, determining the home course by reversing it. This strategy of path integration with the help of an external reference, however, is used only by very young, inexperienced pigeons during an early phase in the development of the navigational system. As soon as birds become more experienced and are able to use site-specific information, they give up route-specific information in favor of the former. The reasons for this change in strategy lie in the fact that using site-specific information enables birds to redetermine their home course as often as necessary, thus allowing the correction of initial mistakes.Site-specific information means that birds can derive their home course from factors perceived at the release site. The present models on navigation acknowledge the crucial role of an external reference system by proposing the navigational map to be a directionally oriented mental representation of the spatial distribution of at least two navigational factors, which are assumed to be environmental gradients. The birds determine their home course by comparing the local values of these factors with the remembered home values. Gradients can be extrapolated beyond the range of direct experience, which explains the birds' ability to home from distant, unfamiliar sites. Deviations from the true home direction, so-called release site biases, as frequently observed in pigeons and other bird species, may be attributed to unforeseen irregularities in the distribution of the navigational factors, which cause birds to misinterpret their position. Near home, the navigational or grid map is supplemented by the mosaic map, which is supposed to be a directionally oriented mental representation of the distribution of familiar landmarks.Both maps are based on experience. Young birds obtain the relevant information during spontaneous flights by combining information on the route travelled with information on the location of prominent landmarks and the direction of environmental gradients. In pigeons, the maps become functional during the third month of life. They are continuously enlarged and updated also in later years. The total size of the navigational map appears to depend on the spatial range of the birds' experience. The maps seem to include information on distance; they are not restricted to homing, but allow free movements between arbitrary goals. In several respects, the model of the avian navigational map is similar to the concept of the cognitive map discussed in psychological literature, the main differences being the larger distances involved, the representation of continuous environmental gradients instead of separate entities, and the essential role of an external reference.The navigational system of birds is thus characterized as utilizing a wide variety of environmental cues. Learning processes, which are based on a simple, innate mechanism, the magnetic compass, integrate these cues and form complex, experience-based mechanisms, such as the maps.

     

Accurate route demonstration by experienced homing pigeons does not improve subsequent homing performance in naive conspecifics.

We describe an experiment that uses the grouping tendencies and navigational abilities of the homing pigeon (Columba livia) to investigate the possibility of socially mediated information transfer in a field setting. By varying the composition of paired-release types, we allowed some naive birds to receive an accurate demonstration of the home route whilst others were paired with similarly naive conspecifics. After this 'paired phase', we predicted that if any learning of spatial information occurred then naive members of the former pairs would outperform their untutored conspecifics when re-released individually during the subsequent 'single phase' of the experiment. This prediction was not confirmed. Neither homing speed nor initial orientation was superior in individually released tutored versus untutored birds, despite the fact that both performance measures were better in the earlier 'paired phase' with experienced demonstrators. Our results suggest that although naive homing pigeons clearly interact with their experienced partners, they are unable to transfer any individually useful spatial information to subsequent homing flights.