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.     

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.     

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.     

The effect of digging on development of adult characters in blowflies Calliphora erythrocephala

Digging delays expansion after emergence of adult Calliphora. If flies are kept digging for 12 to 14 hr they lose the capacity to expand and, if they are then reared for 10 days, do not develop the normal adult corpus allatum, ovaries, and cuticle. In particular, ultrastructural examination of the resilin tendon of the pleurotergal muscle shows that development is arrested at a stage similar to that in the late pharate adult but the resilin is not cross-linked. It is suggested that bursicon release is irreversibly inhibited in flies that fail to expand normally.     

Rearing in a distorted magnetic field disrupts the ‘map sense’ of juvenile steelhead trout

We used simulated magnetic displacements to test orientation preferences of juvenile steelhead trout (Oncorhynchus mykiss) exposed to magnetic fields existing at the northernmost and southernmost boundaries of their oceanic range. Fish reared in natural magnetic conditions distinguished between these two fields by orienting in opposite directions, with headings that would lead fish towards marine foraging grounds. However, fish reared in a spatially distorted magnetic field failed to distinguish between the experimental fields and were randomly oriented. The non-uniform field in which fish were reared is probably typical of fields that many hatchery fish encounter due to magnetic distortions associated with the infrastructure of aquaculture. Given that the reduced navigational abilities we observed could negatively influence marine survival, homing ability and hatchery efficiency, we recommend further study on the implications of rearing salmonids in unnatural magnetic fields.     

Statistical and Prosodic Cues for Song Segmentation Learning by Bengalese Finches (Lonchura striata var. domestica)

Juvenile songbirds learn their songs from adults. Birds do not simply learn songs verbatim but they sometimes learn parts of songs from multiple tutors and recombine these into one song sequence. How they segment a particular part and select that as a chunk and how these chunks are recombined are interesting questions to ask, because such segmentation and chunking is also considered to be a basic mechanism in human language acquisition. The song of the Bengalese finch has a complex syntax with variable note‐to‐note transition probabilities and could thus be suitable for the study of segmentation and chunking in birdsong. Thirty‐two male Bengalese finch chicks were reared in a large aviary where 11 adult tutors and 10 adult females were breeding freely. In this environment most male chicks learned songs from several tutors. The song note‐chunks that juveniles copied had higher transition probabilities and shorter silent intervals than did the boundaries of the chunks, suggesting that Bengalese finches segment songs using both statistical and prosodic cues. Thus, the Bengalese finch could prove to be an excellent model in which to study neural and behavioral mechanism for sound segmentation.     

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.     

Multi-modal Orientation Cues in Homing Pigeons

How homing pigeons displaced into unfamiliar territory findtheir way home has been the subject of extensive experimentationand debate. One reason for the controversy is that pigeons seemto use multiple cues. Clock-shifting experiments show that experiencedpigeons use the sun as a preferred compass; when it is not availablethey rely on magnetic cues. That pigeons can home successfullywhile wearing frosted lenses suggests that landmarks, whilenot an essential navigational cue, are important in the finalstages. The sensory basis of the "map" or position finding systemis probably equally or even more complicated. When conditionsaround the loft are suitable, pigeons may use olfactory cuesto find their way or might use some feature of the earth's magneticfield for their navigation. The Wiltschkos (1989) showed thatpigeons raised without free access to ambient odors are notdisoriented when anosmic while their siblings raised with freeaccess to the prevailing wind were disoriented. Similarly, siblingpigeons from two lofts in Lincoln, Massachusetts. were welloriented or totally disoriented when released at magnetic anomaliesunder sunny skies depending upon which of the two lofts theyhad been reared in. All of these experiments and many more suggestthat pigeons use multiple and redundant cues to find their wayhome. Further, there is the suggestion that which cues theyadopt may well be influenced by the characteristics of the areaaround the home loft in which they were reared.     

Kompass im Kopf

Ant compass – how desert ants learn to navigate Successful spatial orientation is a daily challenge for many animals. Cataglyphis desert ants are famous for their navigational performances. They return to the nest after extensive foraging trips without any problems. How do ants take their navigational systems into operation? After conducting different tasks in the dark nest for several weeks, they become foragers under bright sun light. This transition requires both a drastic switch in behavior and neuronal changes in the brain. Experienced foragers mainly rely on visual cues. They use a celestial compass and landmark panoramas. For that reason, naïve ants perform stereotype learning walks to calibrate their compass systems and acquire information about the nest's surroundings. During their learning walks, the ants frequently look back to the nest entrance to learn the homing direction. For aligning their gazes, they use the earth's magnetic field as a compass reference. This magnetic compass in Cataglyphis ants was previously unknown.     

Does Rearing Laying Hens in Aviaries Adversely Affect Long-Term Welfare following Transfer to Furnished Cages?

This study tests the hypothesis that hens that are reared in aviaries but produce in furnished cages experience poorer welfare in production than hens reared in caged systems. This hypothesis is based on the suggestion that the spatial restriction associated with the transfer from aviaries to cages results in frustration or stress for the aviary reared birds. To assess the difference in welfare between aviary and cage reared hens in production, non-beak trimmed white leghorn birds from both rearing backgrounds were filmed at a commercial farm that used furnished cage housing. The videos were taken at 19 and 21 weeks of age, following the birds'' transition to the production environment at 16 weeks. Videos were analysed in terms of the performance of aversion-related behaviour in undisturbed birds, comfort behaviour in undisturbed birds, and alert behaviour directed to a novel object in the home cage. A decrease in the performance of the former behaviour and increase in the performance of the latter two behaviours indicates improved welfare. The results showed that aviary reared birds performed more alert behaviour near to the object than did cage reared birds at 19 but not at 21 weeks of age (P = 0.03). Blood glucose concentrations did not differ between the treatments (P>0.10). There was a significant difference in mortality between treatments (P = 0.000), with more death in aviary reared birds (5.52%) compared to cage birds (2.48%). The higher mortality of aviary-reared birds indicates a negative effect of aviary rearing on bird welfare, whereas the higher duration of alert behavior suggests a positive effect of aviary rearing.     

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.     

Age‐dependent and task‐related volume changes in the mushroom bodies of visually guided desert ants,Cataglyphis bicolor

Desert ants of the genus Cataglyphis are skillful long‐distance navigators employing a variety of visual navigational tools such as skylight compasses and landmark guidance mechanisms. However, the time during which this navigational toolkit comes into play is extremely short, as the average lifetime of a Cataglyphis forager lasts for only about 6 days. Here we show, by using immunohistochemistry, confocal microscopy, and three‐dimensional reconstruction software, that even during this short period of adult life, Cataglyphis exhibits a remarkable increase in the size of its mushroom bodies, especially of the visual input region, the collar, if compared to age‐matched dark‐reared animals. This task‐related increase rides on a much smaller age‐dependent increase of the size of the mushroom bodies. Due to the variation in body size exhibited by Cataglyphis workers we use allometric analyses throughout and show that small animals exhibit considerably larger task‐related increases in the sizes of their mushroom bodies than larger animals do. It is as if there were an upper limit of mushroom body size required for accomplishing the ant's navigational tasks. © 2006 Wiley Periodicals, Inc. J Neurobiol, 2006     

Pigeon navigation: Time course of olfactory signal processing and dependence on access to fresh environmental air

Summary 16 releases, centrally symmetrical by pairs and involving distances of displacement from 25 to 172 km, were conducted with homing pigeons pre-treated in different ways: FIL birds were, until few minutes before release, confined to containers ventilated with ambient air that had passed through filters consisting of activated charcoal. NOFIL birds were confined to containers ventilated with unfiltered air, either from departure at the loft onwards (4 experiments) or for at least 4 h at the release site (after transport under FIL conditions; 12 experiments). The olfactory epithelia of XYL birds were locally anaesthetized a few minutes before release, while NOXYL birds were not treated with xylocain. FIL/NOFIL conditions were combined with XYL/NOXYL conditions, resulting in 4 types of experimental treatment.On average, the untreated pigeons (NOFILNOXYL) were best homeward oriented and the double-treated pigeons (FIL-XYL) poorest. More importantly, the effect of olfactory deprivation during initial flight alone (NOFIL-XYL) was small, whereas long-term filtration of environmental air was quite effective even if the pigeons could smell during release time (FIL-NOXYL) (Fig. 5).These findings indicate that pigeons usually need to be exposed to local odorous air for more than only few minutes in order to utilize information extricated from this air for site localization.Additional experiments showed that homeward orientation is also prevented, if the pigeons, although breathing natural air, are ventilated with restricted volumes of fresh air.Our results are discussed with regard to the homing mechanism of pigeons as well as to their methodological consequences.Abbreviations FIL breathing air filtered by charcoal - NOFIL breathing air unfiltered - XYL xylocain applied to pigeons' nostrils - NOXYL no xylocain applied (see p. 140)     

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.     

Pigeon navigation: Effects upon homing behaviour by reversing wind direction at the loft

Summary In order to test the nature of the information acquired by pigeons at home and utilized as map component in their navigational mechanism, groups of birds were kept since fledging time in glass corridors, which had their main axis oriented E-W (or ESE-WNW). Referring to the quadrants centered by these directions as experimental quadrants, the treatment of the birds was as follows. Whenever a wind was blowing from one of the experimental quadrants, C1-and C-birds were subjected to an artificial air current blowing from the center of the same quadrant, and E-birds to air currents from the center of the opposite quadrant. C2-birds, reared in a corridor which was unscreened at both ends, were not treated with artificial winds and could perceive the natural winds from the experimental quadrants. Finally, S-birds were never exposed to either natural or artificial winds.When released from directions comprised in the xperimental quadrants, C-, C1-, and C2-birds were homeward oriented, while E-birds oriented themselves toward the opposite direction (Fig. 7), and S-birds' bearings were random. The homing performances of E-birds were poorer than those of the other birds, and on some releases, disastrous.It is concluded that the information that pigeons acquire at home and then use for navigational purposes is wind borne and can be conveyed by an artificial air current. This confirms previous results which indicated the olfactory nature of the information.Dedicated to Prof. Dr. H. Autrum, on occasion of his seventieth birthdayThis study was supported by the Cosiglio Nazionale delle Ricerche. We thank the Command of the Brigata Paracadutisti Folgore, Italian Army, which kindly allowed us to use a power boat for the releases from over the sea. We also wish to thank Dr. R.F. Hartwick for valuable help with some experiments and for stimulating discussions, Mr G. Mela and Mr D. Moretti for constructing the control drices for the fans.     

Larval memory affects adult nest-mate recognition in the ant Aphaenogaster senilis

Prenatal olfactory learning has been demonstrated in a wide variety of animals, where it affects development and behaviour. Young ants learn the chemical signature of their colony. This cue-learning process allows the formation of a template used for nest-mate recognition in order to distinguish alien individuals from nest-mates, thus ensuring that cooperation is directed towards group members and aliens are kept outside the colony. To date, no study has investigated the possible effect of cue learning during early developmental stages on adult nest-mate recognition. Here, we show that odour familiarization during preimaginal life affects recognition abilities of adult Aphaenogaster senilis ants, particularly when the familiarization process occurs during the first larval stages. Ants eclosed from larvae exposed to the odour of an adoptive colony showed reduced aggression towards familiar, adoptive individuals belonging to this colony compared with alien individuals (true unfamiliar), but they remained non-aggressive towards adult individuals of their natal colony. Moreover, we found that the chemical similarity between the colony of origin and the adoptive colony does not influence the degree of aggression, meaning that the observed effect is likely to be due only to preimaginal learning experience. These results help understanding the developmental processes underlying efficient recognition systems.     

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.     

Pigeons do not perceptually complete partly occluded photos of food: an ecological approach to the "pigeon problem"

Humans routinely complete partly occluded objects to recognize the whole objects. However, a number of studies using geometrical figures and even conspecific images have shown that pigeons fail to do so. In the present study, we tested whether pigeons complete partially occluded objects in a situation simulating a natural feeding context. In Experiment 1, we trained pigeons to peck at any photograph of food and not to peck at any containing a non-food object. At test, we presented both photos of food partly occluded by pigeon's feather and photos simply truncated at the same part. We predicted that if the pigeons perceptually completed the occluded portion, then they would discriminate the photos of occluded food better than the truncated photos. The result was that the pigeons pecked at the truncated photos earlier than the occluded photos. Placing the occluder next to all of the stimuli in Experiment 2 or substituting indented lozenge for the feather in Experiment 3 did not affect the results. Thus, even in a simulated ecologically significant situation, pigeons continued to not show evidence of perceptual completion.     

Spatial Memory of Homing Pigeons,Columba livia,Tested in an Outdoor Aviary

Five homing pigeons were trained to dig up hidden seeds buried in one of eight sand-filled cups in an octagonal aviary. All birds located the correct cup with an accuracy well above chance, irrespective of whether the retention time was between 15 min and 2 1/2 h, or whether it was between 1 d and 4 d. Even after 10 mo, the birds remembered the correct cup with great accuracy. This indicates well-developed spatial memory capacities of long duration. The method used in this study, based on training pigeons to dig for hidden seeds in combination with an arbitrary standard task, seems highly suitable to test pigeons for their spatial abilities.     

Song learning in domesticated canaries in a restricted acoustic environment

Many songbirds learn their songs early in life from a song model. In the absence of such a model, they develop an improvised song that often lacks the species-typical song structure. Open-ended learners, such as the domesticated canary, are able to modify their songs in adulthood, although the mechanisms that guide and time the song-learning process are still not fully understood. In a previous study, we showed that male domesticated canaries lacking an adult song model in their first year substantially change their song repertoire and composition when exposed to normally reared conspecifics in their second year. Here, we investigate song development in descendants of canaries that were raised and kept as a peer group without a song model. Such males represent tutors with abnormal song characteristics. Interestingly, the F₁ generation developed quite normal song structure, and when brought into an environment with normally raised canaries in their second year, they did not modify their songs substantially. These results suggest that contact with an adult song model early in life is crucial for song crystallization, but also that song development is at least partly guided by innate rules. They also question the existing classification of canaries as open-ended learners.