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.     

The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals

Homing pigeons and migratory birds are well known examples for animals that use the geomagnetic field for their orientation. Yet, neither the underlying receptor mechanism nor the magnetoreceptor itself is known. Recently, an innervated structure containing clusters of magnetite nanocrystals was identified in the upper beak skin of the homing pigeon. Here we show theoretically that such a cluster has a magnetic-field-dependent shape, even in fields as weak as the Earth's magnetic field; by converting magnetic stimuli into mechanical strain, the clusters can be assumed as primary units of magnetoperception in homing pigeons. Since the orientation of the strain ellipsoid indicates the direction of the external magnetic field, a cluster of magnetite nanocrystals also has the potential to serve as the basis of the so-called inclination compass of migratory birds. It is quantitatively demonstrated that the magnetic-field-induced shape change of a cluster can be amplified as well as counterbalanced by means of osmotic pressure regulation, which offers an elegant possibility to determine the magnetic field strength just by measuring changes in concentration. Received: 18 May 1998 / Revised version: 11 February 1999 / Accepted: 11 February 1999     

Causes of homing behaviour in a group living reef fish

Homing is a common feature in fish, where for instance many freshwater species return to their place of birth to reproduce. Homing in marine species is, however, less understood. Such homing behaviour may be explained by fitness advantages from staying in a known physical environment as well as a known social environment. Cardinalfish of the family of Apogonidae are small, schooling fish, common in shallow waters in temperate and tropical seas. They form apparently stable group structures both in space and time and it has been shown that they may return to their home site after being experimentally removed up to several kilometres. In order to disentangle whether this homing behaviour in one such cardinalfish species, the Banggai cardinalfish, is driven by preference for the home locality or their original social group, I performed a two part field experiment. Firstly, individuals were allowed to choose between known individuals from their original group and unknown individuals from another group. Secondly, individuals were allowed to choose between their original location inhabited by unknown individuals from another group, and a new location inhabited by individuals from their original group. I discuss the evolution of homing behaviours in fish in light of these experiments.     

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。     

Frequency shift discrimination: Can homing pigeons locate infrasounds by Doppler shifts?

Summary Homing pigeons can detect small shifts in sound frequency at 1, 2, 5, 10, and 20 Hz. Their thresholds range from a 1% shift at 20 Hz to a 7% shift at 1 Hz. The frequency shifts used were designed to simulate the natural Doppler shifts resulting from changes in flight path. Their ability was sufficiently sensitive to make it feasible that natural Doppler shifts can be detected. Further tests indicated that the birds can perform true frequency discrimination when all subjective amplitude cues are removed. These laboratory tests are further steps in a series designed to find out if homing pigeons use infrasounds as cues for orientation and navigation.We thank our colleague, Prof. Wm. T. Keeton for his encouragement and support and John Willis for technical assistance. This research was supported by Grants No. BNS 77-24903 and BNS 78-13016 from the National Science Foundation, and by Hatch funds.Present address: Department of Biology, University of Pittsburgh, and Section of Birds, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania 15260, USA     

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.     

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.     

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.     

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 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.     

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.     

Perceptual Strategies of Pigeons to Detect a Rotational Centre—A Hint for Star Compass Learning?

Birds can rely on a variety of cues for orientation during migration and homing. Celestial rotation provides the key information for the development of a functioning star and/or sun compass. This celestial compass seems to be the primary reference for calibrating the other orientation systems including the magnetic compass. Thus, detection of the celestial rotational axis is crucial for bird orientation. Here, we use operant conditioning to demonstrate that homing pigeons can principally learn to detect a rotational centre in a rotating dot pattern and we examine their behavioural response strategies in a series of experiments. Initially, most pigeons applied a strategy based on local stimulus information such as movement characteristics of single dots. One pigeon seemed to immediately ignore eccentric stationary dots. After special training, all pigeons could shift their attention to more global cues, which implies that pigeons can learn the concept of a rotational axis. In our experiments, the ability to precisely locate the rotational centre was strongly dependent on the rotational velocity of the dot pattern and it crashed at velocities that were still much faster than natural celestial rotation. We therefore suggest that the axis of the very slow, natural, celestial rotation could be perceived by birds through the movement itself, but that a time-delayed pattern comparison should also be considered as a very likely alternative strategy.     

Hippocampal ablated homing pigeons show a persistent impairment in the time taken to return home

Summary Homing pigeons were subjected to either hippocampal or control anterior forebrain ablations to examine what role the hippocampus and related structures may play in homing behavior. One year after surgery, the test birds were released from five locations where they had never been before. Both groups were successful in orienting homeward from the release sites, indicating that the hippocampus is not necessary for the neural regulation of a pigeon's map and compass system. Nonetheless, hippocampal ablated pigeons were significantly poorer with respect to the time required to return home, indicating a homing performance impairment. Alternative hypotheses are discussed to explain this result, the most parsimonious being impaired ability on the part of the hippocampal ablated birds to direct a course homeward.     

Simulated navigation based on observed gradients of atmospheric trace gases (Models on pigeon homing, part 3)

An earlier developed model, simulating pigeon homing based on fictitious gradients of atmospheric odours, was applied to actually observed spatial distributions of volatile hydrocarbons. The model calculations demonstrate that sufficient information on a bird's current position with respect to home can be derived from the ratios among three or more chemical compounds which gradually vary over distances of several hundreds of kilometres, differently in different directions. Flight directions computed by model birds from such observed ratios are roughly but not perfectly homeward-oriented from most positions within the investigated radius of 200 km around home. Performances of model birds are at least as good as those of real pigeons in the field. According to calculations using atmospheric data collected under different wind directions, the birds might, but possibly need not, take the current weather conditions into account when evaluating olfactory signals. It is necessary, however, that the birds acquire, during their long-term stay at the home site, some knowledge of the directions of relevant gradients. Homing experiments with pigeons as well as measurements of atmospheric trace substances are consistent with the hypothesis that this knowledge is gained by correlating wind directions with specific changes of ratios among a number of compounds. This assumed process requires further elucidation.     

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.     

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.

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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.

     

Superparamagnetic Magnetite in the Upper Beak Tissue of Homing Pigeons

Homing pigeons have been subject of various studies trying to detect magnetic material which might be involved in magnetic field perception. Here we focus on the upper-beak skin of homing pigeons, a region that has previously been shown to contain nerves sensitive to changes of the ambient magnetic field. We localized Fe³⁺ concentrations in the subcutis and identified the material by transmission electronmicroscopy (TEM) as aggregates of magnetite nanocrystals (with grain sizes between 1 and 5 nm). The particles form clusters of 1–3 m diameter, which are arranged in distinct coherent elongated structures, associated with nervous tissue and located between fat cells. Complementary low-temperature magnetic measurements confirm the microscopic observations of fine-grained superparamagnetic particles in the tissue. Neither electron-microscopic nor magnetic measurements revealed any single-domain magnetite in the upper-beak skin tissue.     

Homing endonuclease structure and function

Homing endonucleases are encoded by open reading frames that are embedded within group I, group II and archael introns, as well as inteins (intervening sequences that are spliced and excised post-translationally). These enzymes initiate transfer of those elements (and themselves) by generating strand breaks in cognate alleles that lack the intervening sequence, as well as in additional ectopic sites that broaden the range of intron and intein mobility. Homing endonucleases can be divided into several unique families that are remarkable in several respects: they display extremely high DNA-binding specificities which arise from long DNA target sites (14-40 bp), they are tolerant of a variety of sequence variations in these sites, and they display disparate DNA cleavage mechanisms. A significant number of homing endonucleases also act as maturases (highly specific cofactors for the RNA splicing reactions of their cognate introns). Of the known homing group I endonuclease families, two (HNH and His-Cys box enzymes) appear to be diverged from a common ancestral nuclease. While crystal structures of several representatives of the LAGLIDADG endonuclease family have been determined, only structures of single members of the HNH (I-HmuI), His-Cys box (I-PpoI) and GIY-YIG (I-TevI) families have been elucidated. These studies provide an important source of information for structure-function relationships in those families, and are the centerpiece of this review. Finally, homing endonucleases are significant targets for redesign and selection experiments, in hopes of generating novel DNA binding and cutting reagents for a variety of genomic applications.     

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.     

Experience Based Use of Landmark and Vector Based Orientation During Homing by the Ant Formica cunicularia (Hymenoptera: Formicidae)

Homing paths of Formica cunicularia foragers from an artificial food reward were analyzed on a familiar terrain and in displacement experiments on a familiar and an unfamiliar terrain. Foragers were tested either when relatively new to a foraging route (untrained group) or after a day’s experience with it (trained group). Untrained foragers followed direct homing paths to the nest site when tested in the familiar terrain but followed tortuous paths when displaced to the unfamiliar terrain. Trained foragers behaved similarly to untrained ones when tested from the food reward to the nest site in the familiar terrain but their behavior changed in displacements. Irrespective of the familiarity of the displacement site, these foragers followed paths taking them to the expected nest sites. The results showed that foragers did not rely on chemical cues for homing and revealed that untrained foragers disregarded path integration and were directed to the nest site when it is in their visual panorama. On the contrary, trained foragers may have relied on path integration on familiar and unfamiliar terrain. The results also demonstrated that experience greatly affected the preferential use of visual and vector based cues by foragers during homing.