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)     

Das Richtungsverhalten verfrachteter Brieftauben (Columba livia) im Orientierungsk?fig

The orientation of displaced homing pigeons at the moment of their release was tested using an octagonal orientation cage. Under certain conditions, the cage bearings of old, experienced pigeons show rather good homeward orientation, while the directional choices of young birds are not related to the home direction.     

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.     

Olfaction and homing in pigeons: Nerve-section experiments,critique, hypotheses

Summary At four sites in the cardinal directions from the home loft in about 180 km distance, 135 experimental pigeons (EPs) and 171 control pigeons (CPs) were released. The EPs had been made anosmic by bilateral olfactory nerve section. All birds were completely inexperienced in homing.Homeward orientation was clearly established in the CPs of which 19% returned to the loft. The performances of the EPs were significantly worse in (a) initial orientation, (b) vanishing intervals, (c) distribution of recoveries, and (d) homing success (none of them homed).The EPs still showed the loft-specific preferred compass direction (PCD).The recoveries of the EPs are much more widely scattered in direction than those of the rather well homeward oriented CPs, even if the distances from the release site are the same in both groups. It is concluded that the navigational capability rather than the motivation to fly or to return home is affected by olfactory deprivation. It is further concluded that homing of pigeons depends on olfactory stimuli perceived at the remote sites even at distances as large as 180km.In the data of the anosmic pigeons a non-olfactory component of homeward orientation persists which is much more pronounced on the W-E axis than on the N-S axis. This component alone appears to be insufficient for a return to the loft.Earlier results and conclusions that gave rise to some controversy are critically examined.The present as well as earlier findings are discussed with respect to two alternative hypotheses of olfactory navigation, the mosaic hypothesis (favoured by Papi) and the gradient hypothesis (favoured by the author).Abbreviations EP experimental pigeon(s) - CP control pigeon(s) - CLCP cueless transported control pigeon(s) (see p. 210) - PCD preferred compass direction I gratefully acknowledge the possibility to maintain our pigeon loft in a building that belongs to the Zoological Institute (Prof. M. Lindauer) of the University of Würzburg. I thank B. and K. Brendle, E. Thiele, and K. Wielander for the releasing of pigeons and for other technical assistance.     

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.     

Orientation of anosmatic pigeons

Summary Test releases performed at five symmetrically arranged sites around the loft, at a distance of 78–99 km from it, showed that 1) anosmatic birds transported without alteration of the earth's magnetic field were completely random-oriented, 2) anosmatic birds transported in a container inside which the intensity of the magnetic field was strongly reduced were unable to orientate homewards and mostly departed according to a preferred compass direction, 3) control birds, which could smell, and were transported without alteration of the magnetic field, were homeward oriented and performed better in homing than both experimental groups. The conclusion is that anosmatic birds are unable to detect home direction at unfamiliar sites and that magnetic stimuli perceived during the outward journey are unable to substitute olfactory cues.Abbreviation PCD preferred compass direction Supported by a grant from the Consiglio Nazionale delle Ricerche     

Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena

Whether pigeons use visual landmarks for orientation from familiar locations has been a subject of debate. By recording the directional choices of both anosmic and control pigeons while exiting from a circular arena we were able to assess the relevance of olfactory and visual cues for orientation from familiar sites. When the birds could see the surroundings, both anosmic and control pigeons were homeward oriented. When the view of the landscape was prevented by screens that surrounded the arena, the control pigeons exited from the arena approximately in the home direction, while the anosmic pigeons' distribution was not different from random. Our data suggest that olfactory and visual cues play a critical, but interchangeable, role for orientation at familiar sites.     

Attempts to Determine the Roles of Visual and Olfactory Inputs in Initial Orientation and Homing of Pigeons over Familiar Terrain

The role of familiar visual landmarks in pigeon homing is still unsettled. If they are involved, they must be thought to be utilized in parallel with olfactory signals. In order to recognize the effectiveness of either one of the input channels separately, vision and olfaction, it is therefore necessary to interfere with both of them. Pigeons were temporarily deprived of image vision by spectacles made of translucent white paper, producing a condition called V^- as compared with the largely unimpaired condition V⁺. Access to olfactory signals was temporarily prohibited by charcoal filters before release and nasal anaesthesia upon release, resulting in condition O^- versus unimpaired smelling of natural air in O⁺. Prior to the test releases, all the participating pigeons had been made familiar with the two or four test sites (and with other sites in the area) by training flights. According to decreasing levels of initial homeward orientation and homing performance, the four combinations of treatments are to be arranged in the following order: V⁺O⁺, V⁺O^-, V^-O⁺, V^-O^-. In the last type, no trace of initial homeward orientation remained, indicating that at least one of the two input channels need be functional to enable home-related orientation. Over well known terrain, either alone seems to be more or less sufficient. The results are indicative but not definitely conclusive. Effects of visual impairment on behavioural activities in general cannot clearly be separated from orientation-specific effects. Therefore, and because many pigeons refuse to fly in V^- condition or fail to provide useful data, we stopped applying this method.     

Directional components derived from initial-orientation data of inexperienced homing pigeons

Summary 1,324 vanishing bearings of individual pigeons, completely inexperienced in homing, were recorded during 100 releases at 36 sites symmetrically distributed around their home loft near Würzburg at distances ranging from 7 to 180 km. Two directional components could be derived from the data: (a) a weak but significant homeward component pointing to the loft site and (b) a more pronounced compass component pointing to the northwest (Fig. 1). With the latter kind of tendency the pigeons clearly demonstrated what earlier had been described as preferred compass direction (PCD).Homeward directedness at the 36 differently situated release sites is negatively correlated with angular divergence between PCD and homeward direction (Fig. 2). Compass preferences derived from different quartets of symmetrically arranged sites were similar. Over a period of 11 years the PCD varied significantly in time but did not change fundamentally (Figs. 3, 4). Interrelations between various parameters of initial-orientation data were investigated by correlation analyses (Table 3).PCDs have not only been found in the Würzburg area but around many other loft sites as well. They are, however, differently pronounced, and in experienced pigeons they are generally weaker than in first-flight birds. Various reasons (partly evident, partly thought possible) for variability of PCDs, and for their absence in some series of experiments, are discussed.As a PCD persists, and even tends to become clearer, after elimination of homeward orientation by olfactory deprivation, it is concluded that it reflects directional tendencies which are independent of the process of site localization. A great deal of what is called release-site biases, i.e., site-specific deviations from the beeline course towards home, can be understood on a PCD basis. The functional background of the PCD is unknown. Hypothetical advantages for the pigeons homing strategy are considered.Abbreviations RSB release-site bias - PCD preferred compass direction     

Besprechungen / Reviews

Book Reviewed in this article: Wallraff , H. G. (1970): Weitere Volierenversuche mit Brieftauben: Wahrscheinlicher Einfluß dynamischer Faktoren der Atmosphäre auf die Orientierung. Wallraff , H. G. (1974): Das Navigationssystem der Vögel. R. Oldenbourg Verlag, München — Wien. (Schriftenreihe Kybernetik, H. Marko und H. Mittelstaedt eds.) Papi , F., V. Fiaschi , S. Benvenuti und N. E. Baldaccini (1973): Pigeon homing: outward journey detours influence the initial orientation (Zum Heimfinden der Tauben: Umwege zum Auflaßplatz beeinflussen die Anfangsorientierung). Benvenuti , S., V. Fiaschi , L. Fiore und F. Papi (1973): Disturbances of homing behaviour in pigeons experimentally induced by olfactory stimuli (Durch Geruchsreize künstlich gestörtes Heimfinden von Tauben). Benvenuti , S., V. Fiaschi , L. Fiore und F. Papi (1973): Homing performances of inexperienced and directionally trained pigeons subjected to olfactory nerve section (Heimfinden richtungsdressierter und unerfahrener Tauben nach Durchtrennung des Riechnervs). Papi , F., L. Fiore , V. Fiaschi und S. Benvenuti (1973): An experiment for testing the hypothesis of olfactory navigation of homing pigeons (Experimentelle Prüfung der Annahme, daß Tauben nach dem Geruch heimfinden). Baldaccini , N. E., S. Benvenuti , V. Fiaschi , P. Ioalé und F. Papi (1974): Pigeon homing: Effects of manipulation of sensory experience at home site (Zum Heimfinden der Tauben: Wirkungen aufgezwungener Geruchserfahrung am Heimatort). Papi , F., P. Ioalé , V. Fiaschi , S. Benvenuti und N. E. Baldaccini (1974): Olfactory navigation of pigeons: the effect of treatment with odorous air currents (Geruchsorientierung von Tauben nach Gewöhnung an duftende Luftströme). Scherzinger , W. (1974): Zur Ethologie und Jugendentwicklung der Schnee-Eule (Nyctea scandiaca) nach Beobachtungen in Gefangenschaft. Jilka , A., und B. Leisler (1974): Die Einpassung dreier Rohrsängerarten (Acrocephalus schoenobaenus, A. scirpaceus, A. arundinaceus) in ihre Lebensräume in bezug auf das Frequenzspektrum ihrer Reviergesänge. J. Orn. Thielcke , G. (1974): Stabilität erlernter Singvogel-Gesänge trotz vollständiger geographischer Isolation. Frisch , K. von (1974): Tiere als Baumeister (unter Mitarbeit von O. von Frisch).     

Olfaction and the homing ability of pigeons raised in a tropical area in Brazil

Several workers have investigated the effect of anosmia on pigeon navigation in different geographical locations because it has been suggested that homing behavior is based on different cues, such as olfactory cues, the Earth's magnetic field or infrasound, and that in the absence of one cue another would be used. In this situation, no cue is universally indispensable, including olfactory ones. In order to extend such observations to a novel biome, we observed the behaviour of 192 young inexperienced birds raised in southeastern Brazil, a tropical area where olfactory tests had never been run before. The birds were released from eight symmetrically distributed sites 17 to 44 km from the loft. Half of these birds (experimentals) had been made temporarily anosmic by washing their olfactory mucosae with 4% solution of ZnSO4 the day before release, while controls were treated with Ringer solution. The results of release tests showed that anosmia totally impaired the navigational performance of experimental birds, which were unable to home from sites at relatively short distances from home (34-44 km) and whose pooled initial bearings produced a (negative) homeward component not significantly different from 0. Homing performance of controls was significantly better, and their pooled vanishing bearings had a significant homeward component, in spite of much scatter in individual releases. We conclude that pigeon homing in the study area depends on olfactory information, even though local environmental conditions in the interior of the State of Sao Paulo, as in several other parts of the world, do not appear to be as favorable as Italy for the development of efficient olfactory navigation.     

Pineal Body and Magnetic Sensitivity: Homing in Pinealectomized Pigeons under Overcast Skies

Since birds use the earth's magnetic field for compass orientation when astronomical cues are lacking and it has recently been suggested that the pineal body is part of their magnetic compass, test releases have been performed in overcast conditions with pigeons deprived of the pineal body. On the whole, both experimental and control birds were capable of homeward orientation, though the bearings of experimental were rather more scattered. No differences in homing speed or success were recorded. Thus, the pineal body does not appear to play an important role in the homing of pigeons.     

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.     

A geometric model for initial orientation errors in pigeon navigation

All mobile animals respond to gradients in signals in their environment, such as light, sound, odours and magnetic and electric fields, but it remains controversial how they might use these signals to navigate over long distances. The Earth's surface is essentially two-dimensional, so two stimuli are needed to act as coordinates for navigation. However, no environmental fields are known to be simple enough to act as perpendicular coordinates on a two-dimensional grid. Here, we propose a model for navigation in which we assume that an animal has a simplified ‘cognitive map’ in which environmental stimuli act as perpendicular coordinates. We then investigate how systematic deviation of the contour lines of the environmental signals from a simple orthogonal arrangement can cause errors in position determination and lead to systematic patterns of directional errors in initial homing directions taken by pigeons. The model reproduces patterns of initial orientation errors seen in previously collected data from homing pigeons, predicts that errors should increase with distance from the loft, and provides a basis for efforts to identify further sources of orientation errors made by homing pigeons.     

Evidence that pigeons orient to geomagnetic intensity during homing

The influence of the Earth's magnetic field on locomotory orientation has been studied in many taxa but is best understood for homing pigeons (Columba livia). Effects of experimentally induced and naturally occurring perturbations in the geomagnetic field suggest that pigeons are sensitive to changes in geomagnetic parameters. However, whether pigeons use the Earth's magnetic field for position determination remains unknown. Here we report an apparent orientation to the intensity gradient of the geomagnetic field observed in pigeons homing from sites in and around a magnetic anomaly. From flight trajectories recorded by GPS-based tracking devices, we noted that many pigeons released at unfamiliar sites initially flew, in some cases up to several kilometres, in directions parallel and/or perpendicular to the bearing of the local intensity field. This behaviour occurred irrespective of the homeward direction and significantly more often than what was expected by random chance. Our study describes a novel behaviour which provides strong evidence that pigeons when homing detect and respond to spatial variation in the Earth's magnetic field--information of potential use for navigation.     

Pigeon homing: change in navigational strategy during ontogeny

Pigeons of various ages and experience were prevented from collecting meaningful information during the outward journey by being transported in either a distorted magnetic field or in total darkness. In very young, inexperienced birds, these manipulations caused disorientation, the effect decreasing as the birds grew older. Experienced, trained pigeons did not seem to be affected. These results suggest a switch in strategy during the development of the pigeons' navigational system: young pigeons first determine their home direction using information collected en route during the outward journey, but with increasing age and experience, they switch to using local ‘map’ information obtained at the release site. The advantages of using a navigational ‘map’ are discussed.     

Homing after Displacement in Open or Closed Containers by the Digger Wasp Argogorytes carbonarius (Hymenoptera,Sphecidae)

Initial orientation and homing time were recorded in Argogorytes carbonarius after displacement in “open” and “closed” containers during two periods: “first” release dates and “later” release dates. At the later releases “closed” wasps homed much better than at first releases and better than “open” wasps. At the first releases, on the other hand, the “open” wasps homed (slightly) better than the “closed” wasps. An interpretation relates the better homing of “closed” wasps at the later trials to route learning at the first trials and discusses the differences and peculiarities of homing from familiar terrain and of home orientation by path integration.     

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.     

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.