Orientation by pigeons deprived of olfaction by nasal tubes

Summary In an effort to avoid the trauma and other nonolfactory effects produced by surgical sectioning of pigeons' olfactory nerves, and to avoid the interference with breathing produced by nostril plugs, a way of making pigeons anosmic by inserting plastic tubes in their nostrils was developed. A total of 16 experimental releases were conducted from unfamiliar sites to compare the homing behavior of birds wearing a tube in each nostril with controls wearing a tube in only one nostril. In five short-distance releases (less than 25 km), no convincing differences in initial orientation, vanishing intervals, or homing success were observed. In eleven releases from longer distances (more than 76 km), the experimental birds were random in three cases and the controls were random in two. In no case were the differences in the distributions of the bearings of experimental and control birds statistically significant, nor were there ever significant differences in vanishing intervals. However, experimental birds had much poorer homing success from these long-distance releases. It is concluded, in view of the anosmic pigeons' good orientation at distant unfamiliar sites, that olfaction is not necessary for homeward orientation and hence that it cannot be the basis of the birds' navigational map. Poor homing success from long distances is probably a consequence of the physical irritation and interference with breathing unfortunately produced by the nasal tubes.We thank our colleagues, Irene Brown, Timothy Larkin, and André Gobert for their help in conducting the releases. This research was supported by Grant BMS 75 18905 AO2 from the National Science Foundation.     

Visual marks learned by the solitary bee Megachile rotundata for localizing its nest

We studied homing behaviour of leaf-cutter bees, Megachile rotundata, by using artificial landmarks. We evaluated their nest-searching behaviour in different test situations to elucidate the nature of the visual marks they used in this task. When we modified or removed geometrical figures surrounding the nest, the bees searched for longer, showing that they noticed the introduced changes. However, these manipulations never prevented bees from finding their nest, suggesting that other visual cues were crucial in the task. Manipulations of the edges provided by the boundaries of the device (nest block, metal sheet on which the block was mounted) strongly impaired the homing performance. The further away the edges that were left intact, the stronger was the impairment of the homing behaviour. These results suggest that bees learn the distances of the various edges from the goal and that edges have a hierarchical significance according to their distance from the nest. The most distant edges provide vague information, which suffices to guide the insect towards the next edge in the sequence, until it recognizes the final, precise location of the nest. The results support the conclusion that information on distances is acquired using cues derived from motion parallax generated by the insect's self-motion. Recognition of edge parameters such as position and orientation might be achieved by an image-matching mechanism based on dynamic processes. Thus, in the homing task, there is no clear discrepancy between the eidetic and the parametric hypotheses of spatial representation.     

The directional homing behaviour of the subsocial shield bug,Parastrachia japonensis (Heteroptera: Cydnidae), under different photic conditions

The female subsocial shield bug, Parastrachia japonensis, provisions its nymphs by foraging on the ground in the forest during the Japanese rainy season, and the bug uses homing navigation to drag a drupe back to its burrow by the shortest route during the day. To study whether or not this bug performs this provisioning behaviour under different photic conditions, we observed the homing behaviour and homing direction of bugs in the field around the clock and/or under various weather conditions. The bugs foraged the whole day during the busiest provisioning period, and the number of walking bugs was not affected by the different weather conditions. Such navigational behaviour, regardless of the time of the day and the weather conditions, is rare in insect navigation. To test whether the bug uses visual cues, we covered the compound eyes and ocelli with opaque or clear paint just before homing began. During the day and at night, and in all weather conditions, the homing direction of blind bugs, but not those with clear-painted eyes was disoriented, indicating that this species uses visual cues dominantly under all photic conditions.     

So Near and Yet So Far: Harmonic Radar Reveals Reduced Homing Ability of Nosema Infected Honeybees

Pathogens may gain a fitness advantage through manipulation of the behaviour of their hosts. Likewise, host behavioural changes can be a defence mechanism, counteracting the impact of pathogens on host fitness. We apply harmonic radar technology to characterize the impact of an emerging pathogen - Nosema ceranae (Microsporidia) - on honeybee (Apis mellifera) flight and orientation performance in the field. Honeybees are the most important commercial pollinators. Emerging diseases have been proposed to play a prominent role in colony decline, partly through sub-lethal behavioural manipulation of their hosts. We found that homing success was significantly reduced in diseased (65.8%) versus healthy foragers (92.5%). Although lost bees had significantly reduced continuous flight times and prolonged resting times, other flight characteristics and navigational abilities showed no significant difference between infected and non-infected bees. Our results suggest that infected bees express normal flight characteristics but are constrained in their homing ability, potentially compromising the colony by reducing its resource inputs, but also counteracting the intra-colony spread of infection. We provide the first high-resolution analysis of sub-lethal effects of an emerging disease on insect flight behaviour. The potential causes and the implications for both host and parasite are discussed.     

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.     

Magnetic Navigation

Recent evidence suggests that some amphibians, reptiles and birds may be capable of homing using information about geographic position (“map” information) derived from subtle geographic gradients in the earth's magnetic field. The “magnetic map” hypothesis faces numerous theoretical difficulties, however, due to the extremely high level of sensitivity that would be necessary to detect natural magnetic gradients, and to the presence of spatial irregularities and temporal variation in the geomagnetic field that might make map coordinates derived from magnetic gradients unreliable. To date, the majority of studies carried out to test the magnetic map hypothesis have involved field observations of the effects on homing orientation of naturally occurring spatial or temporal variation in the geomagnetic field. While providing an important first step, these studies are subject to the criticism that the observed changes in homing orientation could result from effects on a magnetic compass, or some other unidentified component of the navigational system, rather than from effects on a magnetic map. The recent development of experimental systems in which navigational ability can be studied under controlled or semi-controlled laboratory conditions has opened up the possibility of using new experimental approaches to more rigorously test the magnetic map hypothesis. After briefly reviewing the available evidence of the geomagnetic field's involvement in the map component of homing, a simple graphical model is presented which describes how the home direction derived from a bicoordinate map varies as a function of the value of one of the map coordinates when the value of the second map coordinate is held constant. In studies of homing orientation in which the value of a specific magnetic field parameter (e.g., total intensity, inclination, etc.) can be varied independently of other putative map parameters, the graphical model can be used to generate qualitative predictions about the changes in the direction of homing orientation that should be observed if the magnetic field parameter being manipulated serves as one coordinate of a bicoordinate map. The relationship between the direction of homing orientation and the value of a putative magnetic map parameter can also be used to generate quantitative predictions about characteristics of the local gradient of that magnetic field parameter in the vicinity of the home site (i.e., the alignment and “home value” of the local gradient) which can then be compared with actual measured values. Together, the qualitative and quantitative predictions of the graphical model permit rigorous tests of whether one or both coordinates of a bicoordinate navigational map are derived from the geomagnetic field.     

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.     

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

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

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.     

Concepts in vertebrate neuroethology

Neuroethology is concerned with the analysis of the neural substrates and mechanisms that underlie behaviour. In 1951, Tinbergen implied the following goals of Ethophysiology, today known as Neuroethology: (1) recognition and localization of behaviourally meaningful stimuli, e.g. key stimuli; (2) sensorimotor interfacing and feedback interactions; (3) modulations according to internal states and acquired information; (4) motor pattern generation; and (5) ontogenetic and phylogenetic aspects. Using the toad's (Bufo bufo) visually-guided prey-catching behaviour as an example, experimental strategies and concepts of vertebrate Neuroethology can be demonstrated: (i) visual space is mapped in the brain in a multiple manner; (ii) specification of neurons results from inhibitory and/or excitatory interactions among and within space-mapped neuronal networks; (iii) specialized neurons, e.g. those with stimulus recognition and localization properties, show information processing that takes place in functional units of cell assemblies (so-called ‘neuronal machines’ or ‘brain chips’); (iv) activation of motor pattern generators for different behavioural actions may require coincidence of inputs from different combinations of specialized neurons that serve as command elements and together form a command system; (v) a command system can be regarded as a sensorimotor interface fulfilling tasks with respect to (a) visual pattern recognition and localization, (b) command functions, by initiating the activation of the motor pattern generation system, (c) motor pattern generation through participation in the temporal sequence of the positive feedback from the motor system, and (d) integration of modulatory inputs according to internal states; (vi) the motor pattern generation circuitry consists of a neuronal network capable of producing a consistent distribution of excitation and inhibition and whose output has privileged access to the required motoneuronal pools; (vii) the basic principles of prey selection and motor pattern generation of prey capture emerge in the post-metamorphic juvenile toad with the transition to land and without previous prey experience. During early ontogeny the acuity of sensory discrimination and the performance of motor patterns are subject to maturation paralleled by neural differentiations in the bbrain. performance of motor patterns are subject to maturation paralleled by neural differentiations in the brain. those are programmed and, in amphibians, presumably less dependent on the interaction with the environment than in mammals. This of course does not exclude the possibility of modulating, modifying, specifying and/or extending the visual pattern recognition system of toads due to internal states and individual experience.     

Global navigation in migratory birds: tracks, strategies, and interactions between mechanisms

The advancing development of tracking techniques has led to fascinating new insights into avian migration, documenting the immense diversity, complexity, and flexibility of this phenomenon. Tracking studies so far have confirmed many findings from ringing recoveries and cage studies, for example, the change from flying innate compass courses in the first migration to true navigation, as experienced migrants head toward familiar goals. First attempts to analyze the navigational mechanisms by tracking manipulated migrants indicate strong parallels to those of homing pigeons. Findings suggesting that the magnetic compass of migrants is regularly calibrated by the pattern of polarized light could not be replicated with a number of other birds, pointing out differences between species and possibly region and phases of migration. Tracking has become a valuable tool, complimenting traditional methods by documenting migration behavior in the wild; whether it can be used to further unveil the navigational mechanisms of migrants and the factor used remains an open question.     

Sea turtles: navigating with magnetism

Young sea turtles use the Earth's magnetic field as a source of navigational information during their epic transoceanic migrations and while homing. A new study using satellite telemetry has now demonstrated for the first time that adult turtles also navigate using the Earth's magnetic field.     

Economic context and pigeons' risk-taking: an integrative approach

The present work tested pigeons' (Columba livia) risk sensitivity to changes in resource availability in the concurrent-chains choice procedure. Subjects were provided choices, generally between variable-ratio (VR) and fixed-ratio (FR) outcome schedules with equal or different mean values. Predictions from ecology's risk sensitivity, behavioral economic's rate maximization, and psychology's delay-reduction theory were contrasted under settings where budget was adversely affected by one of three manipulations in seven experiments: (1) session length was dramatically reduced; (2) choice-phase duration was substantially increased by increasing the response requirements in the choice phase, or (3) outcome duration was significantly increased by increasing the response requirements in the outcome phase while holding session length constant. Although preference measures were sensitive to every budget manipulation, the nature of the changes observed were dependent upon the manner in which resource availability was manipulated and the choice alternatives offered. For example, choice was affected in an opposite manner when budget was adversely altered by lengthening choice duration ("search time") as opposed to lengthening outcome duration ("handling time"). Findings revealed partial support for pigeons' sensitivity both to changes in budget and to changes in conditioned reinforcer value. The overall pattern of results thus favors an integrative approach to describing the effect of economic context on general risk sensitivity.     

Positional entropy during pigeon homing I: application of Bayesian latent state modelling

In these two companion papers, we introduce a new approach to the analysis of bird navigation which brings together several novel mathematical and technical applications. Miniaturized GPS logging devices provide track data of sufficiently high spatial and temporal resolution that considerable variation in flight behaviour can be observed remotely from the form of the track alone. We analyse a fundamental measure of bird flight track complexity, spatio-temporal entropy, and explore its state-like structure using a probabilistic hidden Markov model. The emergence of a robust three-state structure proves that the technique has analytical power, since this structure was not obvious in the tracks alone. We propose the hypothesis that positional entropy is indicative of underlying navigational uncertainty, and that familiar area navigation may break down into three states of navigational confidence. By interpreting the relationship between these putative states and features on the map, we are able to propose a number of hypothetical navigational strategies feeding into these states. The first of these two papers details the novel technical developments associated with this work and the second paper contains a navigational interpretation of the results particularly with respect to visual features of the landscape.     

Positional entropy during pigeon homing II: navigational interpretation of Bayesian latent state models

In these two companion papers we introduce a new approach to the analysis of bird navigation which brings together several novel mathematical and technical applications. Miniaturized GPS logging devices provide track data of sufficiently high spatial and temporal resolution that considerable variation in flight behaviour can be observed remotely from the form of the track alone. We analyse a fundamental measure of bird flight track complexity, spatio-temporal entropy, and explore its state-like structure using a probabilistic hidden Markov model. The emergence of a robust three-state structure proves that the technique has analytical power, since this structure was not obvious in the tracks alone. We propose the hypothesis that positional entropy is indicative of underlying navigational uncertainty, and that familiar area navigation may break down into three states of navigational confidence. By interpreting the relationship between these putative states and features on the map, we are able to propose a number of hypothetical navigational strategies feeding into these states. The first of these two papers details the novel technical developments associated with this work and the second paper contains a navigational interpretation of the results particularly with respect to visual features of the landscape.     

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.     

Nocturnal homing in pigeons

• 1.1. A total of 541 pigeons from 3 populations was tested for the ability of nocturnal homing over increasing distances from 1 to 33 km.
• 2.2. Nocturnal homing over 20 km was an individual characteristic found only in a fraction of pigeons in a loft (30–35%). Its expression was not affected by variables influencing diurnal homing performance such as age, experience and breeding status.
• 3.3. This particular ability is likely to reflect superior navigational abilities related to non-visual orientation mechanisms.
• 4.4. The ability for nocturnal homing is probably genetically dependent: offspring from good nocturnal homers performed significantly better than offspring from poor homers.

     

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.     

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.     

Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI

Homing endonucleases are highly specific catalysts of DNA strand breaks that induce the transposition of mobile intervening sequences containing the endonuclease open reading frame. These enzymes recognize long DNA targets while tolerating individual sequence polymorphisms within those sites. Sequences of the homing endonucleases themselves diversify to a great extent after founding intron invasion events, generating highly divergent enzymes that recognize similar target sequences. Here, we visualize the mechanism of flexible DNA recognition and the pattern of structural divergence displayed by two homing endonuclease isoschizomers. We determined structures of I-CreI bound to two DNA target sites that differ at eight of 22 base-pairs, and the structure of an isoschizomer, I-MsoI, bound to a nearly identical DNA target site. This study illustrates several principles governing promiscuous base-pair recognition by DNA-binding proteins, and demonstrates that the isoschizomers display strikingly different protein/DNA contacts. The structures allow us to determine the information content at individual positions in the binding site as a function of the distribution of direct and water-mediated contacts to nucleotide bases, and provide an evolutionary snapshot of endonucleases at an early stage of divergence in their target specificity.