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: Does Early Experience Determine what Cues are Used to Navigate?

To test the hypothesis that early experience might determine the nature of the cues used to navigate, homing pigeons were made anosmic by nerve section before they could experience the natural odours in the region of the loft. They were allowed to make free flights and trained by flock releases with intact controls. Next they were tested and compared with intact controls as well as birds made temporarily anosmic just before the experiment. Initial orientation and homing performance of the experimental birds were very poor and showed that the pigeons were unable to acquire an alternative mechanism of navigation.     

Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration

The dorsolateral area of the hippocampal formation of birds is commonly assumed to play a central role in processing information needed for geographical positioning and homing. Previous work has interpreted odour-induced activity in this region as evidence for an ‘olfactory map’. Here, we show, using c-Fos expression as a marker, that neuronal activation in the dorsolateral area of the hippocampal formation of pigeons is primarily a response to odour novelty, not to the spatial distribution of odour sources that would be necessary for an olfactory map. Pigeons exposed to odours had significantly more neurons activated in this area of the brain than pigeons exposed to filtered air with odours removed. This increased activity was observed only in response to unfamiliar odours. No change in activity was observed when pigeons were exposed to home odours. These findings are consistent with non-home odours activating non-olfactory components of the pigeon''s navigation system. The pattern of neuronal activation in the triangular and dorsomedial areas of the hippocampal formation was, by contrast, consistent with the possibility that odours play a role in providing spatial 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.     

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.     

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.     

HOMING AND OLFACTION IN SALMONIDS: A CRITICAL REVIEW WITH SPECIAL REFERENCE TO THE ATLANTIC SALMON

(1) Based on data from the literature, the phenomenon of homing in salmonids is examined with special reference to the Atlantic salmon. Wild, native fish demonstrate an excellent homing ability, judged from percent return to the home river (1–3 %) and straying to non-native watersheds (less than 3 % of returning fish). (2) The homing ability in wild fish is shown to be closely related to the existence of reproductively isolated populations between and within watersheds, as demonstrated by data from salmonid ecology and biochemical genetics. (3) Two main hypotheses have dominated the literature on salmonid homing during recent years: (a) An ‘imprinting’ hypothesis based on a process of learning of stream odours during seaward migration, coupled with sun-orientation for open sea navigation, (b) A ‘pheromone’ hypothesis related to odours from fish and based on inheritance and the seasonal migrating schedules of discrete populations. (4) The olfactory sense has been demonstrated as mandatory for salmonids, both in near range and open sea navigation. According to genetic, sensory and ecological aspects of homing, the pheromone hypothesis is therefore concluded to be the most appropriate. (5) Fish produced from artificially fertilized eggs, released within native systems or transplanted, demonstrate a reduced homing ability. Since hatchery-raised fish demonstrate a survival in sea equivalent to that of wild fish, a genetic disturbance of navigational ability has been suggested, resulting from the production of population hybrids by man. (6) Studies made in the fields of behaviour, electrophysiology and chemistry strongly suggest that population-specific fish odours are involved in home-stream recognition by salmonids. (7) An evaluation of ‘imprinting’ experiments related to artificial organic compounds reveals that: (a) the odorant properties of the applied chemicals must be questioned, (b) imprinting related to olfaction may be based on a weak theoretical foundation, (c) returns obtained in census experiments may be adequately explained through ecological interpretations, and (d) behavioural preferences obtained from exposure to non-natural compounds may be founded on mechanisms not associated with homing. (8) A logical link between the use of olfaction and the role of genetics in salmonid homing is emphasized, together with its practical implications for salmonid management.     

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.     

空气污染对信鸽比赛个体归巢速度的影响

空气污染作为一种有害的环境因素,对人类及动物的生理、心理均有影响。在鸟类中,信鸽(Columba livia)是研究空气污染影响的理想模型。为探究空气污染的行为学效应,通过收集并筛选2018和2019年成都市信鸽协会春秋两个季节举办的64场赛事共285羽参赛5场及以上的信鸽不同空距等级下的归巢速度,利用混合线性模型分析了6种大气污染物(CO、NO₂、O₃、PM_2.5、PM₁₀、SO₂)及气温、季节、天气等环境因子对信鸽归巢速度的影响。结果表明,PM₁₀、SO₂、NO₂、O₃浓度与归巢速度间有显著正相关关系,即这些空气污染物浓度越高,信鸽归巢速度越快;而CO浓度与归巢速度显著负相关,即CO浓度越高,信鸽归巢速度越慢。通过模型评估及比较,发现O3模型是归巢速度的最佳拟合模型,其次是NO2模型。本研究表明,信鸽的归巢速度的确受到空气污染的影响,但潜在的影响机制如归巢动机假说和嗅觉强化假说仍需进一步研究。     

Just follow your nose: homing by olfactory cues in ants

How is an ant-equipped with a brain that barely exceeds the size of a pinhead-capable of achieving navigational marvels? Even though evidences suggest that navigation is a multimodal process, ants heavily depend on olfactory cues-of pheromonal and non-pheromonal nature-for foraging and orientation. Recent studies have directed their attention to the efficiency of pheromone trail networks. Advances in neurophysiological techniques make it possible to investigate trail pheromone processing in the ant's brain. In addition to relying on pheromone odours, ants also make use of volatiles emanating from the nest surroundings. Deposited in the vicinity of the nest, these home-range markings help the ants to home after a foraging run. Furthermore, olfactory landmarks associated with the nest enhance ants' homing abilities.     

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.     

A new PCR-RFLP within the domestic pigeon (Columba livia var. domestica) cytochrome b (MTCYB) gene

A total of 244 domestic pigeons (Columba livia var. domestica) were genotyped using the PCR-RFLP method. A 999 bp fragment of the MTCYB gene was amplified. The amplification products were digested with restriction enzymes. PCR-RFLP for MvaI restriction enzyme was observed. Frequencies of alleles were as follows: MTCYB(C)--0.926, MTCYB(G)-- 0.074. The frequencies of MTCYB/MvaI alleles found in this study for non-homing pigeons considerably deviate from the values found for homing/racing pigeons (allele MTCYB(G) occurred only in the non-homing breeds).     

Konditionierung verfrachteter Brieftauben: eine ?neue“ Methode zur Analyse der Karte von Brieftauben

Zusammenfassung Es wird vorgeschlagen, mit Hilfe klassischer Konditionierung sowohl die physikalischen Charakteristika als auch die Verteilung der bei der Navigation von Tauben relevanten Faktoren zu überprüfen. Dabei wird ein neutraler, physikalisch eindeutig definierbarer Reiz mit der Heimkehrreaktion verfrachteter Brieftauben verknüpft. In standardisierten Versuchsreihen kann die Schnelligkeit, mit der Tauben die neue Reizmodalität mit der Aufgabe assoziieren, nach Hause zu fliegen, als Maß für die biologische Relevanz des Reizes dienen. Weiterhin kann mit dieser Methode im Freiland überprüft werden, ob die Taube mit einer vorgegebenen Reizmodalität einen Ort, eine Region oder eine Verfrachtungsrichtung assoziiert. Vorläufige Resultate einer laufenden Arbeit zeigen, daß Tauben in Heimkehrexperimenten auf künstliche Reize (im vorliegenden Fall Geruchsreize) konditioniert werden können. Die hiermit erhaltenen Ergebnisse sollten spezifischere Vorhersagen über mögliche Karteninformation erlauben als bisher, die dann experimentell getestet werden können.

---

Conditioning of homing pigeons en route and at the release site: a new method to assess the map component

Summary The present study suggests classical conditioning as a possibility to assess the elusive map of the homing pigeon. In classical conditioning a previously neutral stimulus is associated with an already existing response. In case of the study of pigeon homing well defined physical cues (such as odours, magnetic fields or infrasound) can be presented to the pigeons prior to release. After a series of training sessions the pigeon learns to associate a given stimulus with a certain home direction.According to the preliminary results of this ongoing study, pigeons can learn in homing experiments to associate artificial odours with different home directions. Pigeons have been trained to associated amylacetate with releases from different sites located north of home and benzaldehyde with releases from the south. Exchange of the two odours for the experimental pigeons after ten training sessions results in impaired initial orientation and reduced homing speed of experimentals compared to controls when released at new sites.In comparative studies the time needed to achieve a preset level of performance could be used to rate the biological significance of different stimuli for homing. By releasing conditioned pigeons at different sites it can also be tested whether or not the simulus is being associated with a site, a region or a direction with respect to home. With this approach the distribution as well as the physical characteristics of different cues can be evaluated for their potential as information relevant for pigeon homing.

     

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.      

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.     

Orientation and navigation in Amphibia

Aquatic and terrestrial amphibians integrate acoustic, magnetic, mechanical, olfactory and visual directional information into a redundant-multisensory orientation system. The sensory information is processed to accomplish homing following active or passive displacement by either path integration, beaconing, pilotage, compass orientation or true navigation. There is evidence for two independent compass systems, a time-compensated compass based on celestial cues and a light-dependent magnetic inclination compass. Beaconing along acoustic or olfactory gradients emanating from the home site, as well as pilotage along fixed visual landmarks also form an important part in the behaviour of many species. True navigation has been shown in only one species, the aquatic salamander Notophthalmus viridescens. Evidence on the nature of the navigational map obtained so far is compatible with the magnetic map hypothesis.     

Patterns in air pollution as model for the physical basis for olfactory navigation in pigeon homing

Spatial distribution and temporal variability of air pollution were used as a model to describe the stability and predictability of the distribution of airborne substances, postulated by some to be used by homing pigeons to navigate. If the man-made substances reflect the distributional characteristics of natural airborne substances, navigation based on airborne substances is unlikely to be possible.     

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.     

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.     

The avian hippocampus, homing in pigeons and the memory representation of large-scale space

The extraordinary navigational ability of homing pigeons providesa unique spatial cognitive system to investigate how the brainis able to represent past experiences as memory. In this paper,we first summarize a large body of lesion data in an attemptto characterize the role of the avian hippocampal formation(HF) in homing. What emerges from this analysis is the criticalimportance of HF for the learning of map-like, spatial representationsof environmental stimuli used for navigation. We then exploresome interesting properties of the homing pigeon HF, using fordiscussion the notion that the homing pigeon HF likely displayssome anatomical or physiological specialization(s), comparedto the laboratory rat, that account for its participation inhoming and the representation of large-scale, environmentalspace. Discussed are the internal connectivity among HF subdivisions,the occurrence of neurogenesis, the presence of rhythmic thetaactivity and the electrophysiological profile of HF neurons.Comparing the characteristics of the homing pigeon HF with thehippocampus of the laboratory rat, two opposing perspectivescan be supported. On the one hand, one could emphasize the subtledifferences in the properties of the homing pigeon HF as possibledeparture points for exploring how the homing pigeon HF maybe adapted for homing and the representation of large-scalespace. Alternatively, one could emphasize the similarities withthe rat hippocampus and suggest that, if homing pigeons representspace in a way different from rats, then the neural specializationsthat would account for the difference must lie outside HF. Onlyfuture research will determine which of these two perspectivesoffers a better approximation of the truth.