The social transmission of spatial information in homing pigeons

We adapted a technique to explore the social transmission of spatial information in homing pigeons Columba livia. Five demonstrator pigeons were first trained to find a food goal within an indoor arena. This arena consisted of nine lidded cups laid out within a 12x12 grid on the floor. The task was to find the goal cup and flip the lid to obtain the food hidden within. Once the demonstrators had reached criterion the experiment proper began. During stage 1 of the experiment, 10 target birds, which had not previously been trained to find the goal, were introduced to the spatial task either in isolation or paired with a demonstrator. We measured how long they took to complete the task, the number of squares crossed on the grid, and the number of incorrect lids flipped. In stage 2, the target birds were introduced to the arena a second time, by themselves, and we compared the performance of the birds in the two treatments. The pigeons that had been introduced to the task with a demonstrator in stage 1 walked further and made more incorrect choices when searching for the food goal in stage 2 than the pigeons that were introduced to the task alone. This indicates that pigeons learn a spatial, food-finding task more effectively when performing the task alone than when accompanied by a knowledgeable conspecific. We discuss possible reasons for this in the light of previous experiments. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.

     

Learning multiple routes in homing pigeons

The aerial lifestyle of central-place foraging birds allows wide-ranging movements, raising fundamental questions about their remarkable navigation and memory systems. For example, we know that pigeons (Columba livia), long-standing models for avian navigation, rely on individually distinct routes when homing from familiar sites. But it remains unknown how they cope with the task of learning several routes in parallel. Here, we examined how learning multiple routes influences homing in pigeons. We subjected groups of pigeons to different training protocols, defined by the sequence in which they were repeatedly released from three different sites, either sequentially, in rotation or randomly. We observed that pigeons from all groups successfully developed and applied memories of the different release sites (RSs), irrespective of the training protocol, and that learning several routes in parallel did not impair their capacity to quickly improve their homing efficiency over multiple releases. Our data also indicated that they coped with increasing RS uncertainty by adjusting both their initial behaviour upon release and subsequent homing efficiency. The results of our study broaden our understanding of avian route following and open new possibilities for studying learning and memory in free-flying animals.     

Effects of flight on blood parameters in homing pigeons

The influence of flight and flight duration on 13 blood parameters was studied in homing pigeons which returned after 2–22 h of flight from release sites 113–620 km away. The haematocrit value decreased from 54.4% in controls to 51.0% in the flown birds. A lowered haematocrit overproportionately improves blood flow. The plasma concentrations of glucose and l(+)-lactate did not differ between experimental and control birds. This is compatible with the idea that carbohydrates are utilized as fuel mainly in the initial phase of flight. Plasma free fatty acid levels were significantly increased during flight and triglyceride concentrations gradually decreased with progressive flight duration. These findings support the view that lipids are the main energy source during flight. Plasma uric acid concentrations were increased two- to fourfold in flown birds. Urea levels gradually rose with flight duration to 400% of controls. Plasma protein concentration was lowered in flown pigeons. These results hint to an increased protein degradation during flight. Na⁺, K⁺, Ca²⁺, and Mg²⁺ levels in the plasma of the flown pigeons were not significantly different from control values. This finding together with the urea/uric acid ratio indicates that no severe dehydration occurred in our pigeons during free-range flight.Abbreviations FA fatty acids - FFA free fatty acids     

Two spatial memories for honeybee navigation

Insect navigation is thought to be based on an egocentric reference system which relates vector information derived from path integration to views of landmarks experienced en route and at the goal. Here we show that honeybees also possess an allocentric form of spatial memory which allows localization of multiple places relative to the intended goal, the hive. The egocentric route memory, which is called the specialized route memory (SRM) here, initially dominates navigation when an animal is first trained to a feeding site and then released at an unexpected site and this is why it is the only reference system detected so far in experiments with bees. However, the SRM can be replaced by an allocentric spatial memory called the general landscape memory (GLM). The GLM is directly accessible to the honeybee (and to the experimenter) if no SRM exists, for example, if bees were not trained along a route before testing. Under these conditions bees return to the hive from all directions around the hive at a speed comparable to that of an equally long flight along a trained route. The flexible use of the GLM indicates that bees may store relational information on places, connections between landmarks and the hive and/or views of landmarks from different directions and, thus, the GLM may have a graph structure, at least with respect to one goal, i.e. the hive.     

Small-scale spatial cognition in pigeons

Roberts and Van Veldhuizen's [Roberts, W.A., Van Veldhuizen, N., 1985. Spatial memory in pigeons on the radial maze. J. Exp. Psychol.: Anim. Behav. Proc. 11, 241-260] study on pigeons in the radial maze sparked research on landmark use by pigeons in lab-based tasks as well as variants of the radial-maze task. Pigeons perform well on open-field versions of the radial maze, with feeders scattered on the laboratory floor. Pigeons can also be trained to search precisely for buried food. The search can be based on multiple landmarks, but is sometimes controlled by just one or two landmarks, with the preferred landmarks varying across individuals. Findings are similar in landmark-based searching on a computer monitor and on a lab floor, despite many differences between the two kinds of tasks. A number of general learning principles are found in landmark-based searching, such as cue competition, generalization and peak shift, and selective attention. Pigeons also learn the geometry of the environment in which they are searching. Neurophysiological studies have implicated the hippocampal formation (HF) in avian spatial cognition, with the right hippocampus hypothesized to play a more important role in the spatial recognition of goal locations. Most recently, single-cell recording from the pigeon's hippocampal formation has revealed cells with different properties from the classic 'place' cells of rats, as well as differences in the two sides of the hippocampus.     

Polymorphism within theLDHA gene in the homing and non-homing pigeons

A total of 445 domestic pigeons were genotyped for the lactate dehydrogenase (LDHA) gene. Crude DNA was isolated from blood samples and feathers. Two polymorphic sites were identified in intron 6: one near the splice donor site GT is called site H and the other near the splice acceptor site is called site B. Interestingly, the nucleotide changes of both these sites associate perfectly with the A and B alleles of HaeIII polymorphism: the A allele with nucleotide A of site H and nucleotide T of site B; while the B allele with nucleotide G of site H and nucleotide G of site B. In this study, we have identified the molecular difference between alleles A and B of the pigeon LDHA gene. The difference at site H in intron 6 explains the HaeIII polymorphism. The frequencies of LDHAAB and LDHABB genotypes between the analysed groups differ significantly (P < 0.001); the LDHAA allele was more frequent in the groups of pigeons with elevated homing performance (P < 0.001). The functional difference may be due to the change at site B, the potential splice branch site. Since LDHA activity is associated with the homing ability, it is possible that during the process of selection for the homing ability, the LDHAA allele has been selected, and is more prevalent in the top-racing groups.     

Testing for the presence of magnetite in the upper-beak skin of homing pigeons

We carried out magnetic and nonmagnetic experiments on fresh, upper-beak skin tissue samples isolated from six pairs of homing pigeons to test whether the tissue contains magnetite particles. Results of (1) room-temperature isothermal remanent magnetization (IRM) acquisition and alternating field (AF) demagnetization, (2) low-temperature demagnetization of saturation IRM acquired at 5 K in a field of 5 tesla (T) (SIRM_{5 K}) after zero-field cooled (ZFC) and field cooled (FC) treatments, and (3) cycling of the saturation IRM acquired at 300 K in a field of 5 T (SIRM_{300 K}) between 5 and 300 K, indicate the presence of magnetite in the measured samples. A significant loss of SIRM_{5 K} below 20 K suggests the dominance of superparamagnetic (SPM) particles. The SIRM acquisition capacity of the female pigeon is stronger than that of the male pigeon in all four measured pairs, suggesting for the first time that the magnetite concentration is probably sex dependent. Light microscopic observation on the histological sections stained with Prussian Blue detected the presence of some tiny, dotted, dark-blue staining Fe³⁺ aggregates (size 1–4 μm) located directly beneath the subcutis within strands of connective tissue, nearby the rim of the regions full of red nuclei. The results of this study support the idea that homing pigeons may have a magnetite-based receptor, which potentially could be used for sensing the Earth’s magnetic field during navigation.     

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.     

Flight effects on certain blood parameters in homing pigeons Columba livia

• 1.1. Various blood parameters were monitored in resting and flown homing pigeons. A homing flight of 48 km lasting 60–80 min did not significantly alter plasma levels of total protein, electrolytes and plasma osmolality, which indicated maintenance of the homeostatic stability of the internal milieu during moderate exercise.
• 2.2. Plasma concentrations of marker enzymes such as alanine aminotransferase (ALAT), aspartate aminotransferase (ASAT), laetate dehydrogenase (LDH) and creatine phosphokinase (CPK) that tend to denote muscle damage and metabolic flux in prolonged exercise, were also not altered, thereby indicating the steady state of tissue structure and function during a flight of this magnitude.
• 3.3. Significant increases in plasma levels of uric acid and creatinine and decreases in plasma albumin were observed in the flown pigeons.
• 4.4. The flight-induced increase in blood uric acid could be attributed to increased purine catabolism and the increase in creatinine to increased nucleotide turnover.
• 5.5. It is suggested that the higher uric acid levels should not only enhance water conservation, but may also reduce flight-induced hyperthermia besides acting as an antioxidant defence against oxidative tissue injury.
• 6.6. The rise in creatinine is indicative of the breakdown of phosphocreatine for energy during the initial period of flight prior to the utilization of carbohydrate and lipid as fuels.
• 7.7. The decrease in plasma albumin should account for the albumin as lipid carrier lost in transport to the muscles during flight.

     

Hippocampal participation in the sun compass orientation of phase-shifted homing pigeons

The orientation of phase-shifted control and hippocampal lesioned homing pigeons with previous homing experience was examined to investigate the possible participation of the hippocampal formation in sun compass orientation. Hippocampal lesioned pigeons displayed appropriate shifts in orientation indicating that such birds possess a functional sun compass that is used for orientation. However, their shift in orientation was consistently larger than in control pigeons revealing a difference in orientation never observed in pigeons that have not undergone a phase shift. Although alternative interpretations exist, the data suggest the intriguing possibility that following a change in the light-dark cycle, the hippocampal formation participates in the re-entrainment of a circadian rhythm that regulates sun compass orientation.     

Olfactory deprivation in pigeons: examination of methods applied in homing experiments

1. Effectiveness of three methods of olfactory deprivation or impairment was tested by means of unconditioned cardiac acceleration in response to odorous stimuli. 2. Occlusion of nostrils reduced stimulus intensity to approx. 20-30% of the level in unimpeded state. Capability of stimulus quantification remained unimpaired. 3. Bilateral olfactory nerve section and backward bending of the nerve stumps irreversibly eliminated responses to weaker stimuli. With higher concentrations of the odorant, pigeons responded at a reduced level, most likely due to trigeminal reception. 4. Spraying the nasal cavities with an anaesthetic largely abolished sensitivity to odorous stimuli. However, its effect was quite variable depending on the kind of application (which cannot be fully standardized). The time course of effectiveness is shown. 5. The relevance of these findings to experiments on pigeon homing is discussed. Conclusions on involvement of unspecified non-olfactory stimuli can only be drawn if methods are applied that reliably isolate the birds from airborne environmental odours.     

The orientation of homing pigeons in relation to change in sun declination

Summary The sun navigation hypothesis ofMatthews is briefly reviewed with special reference to his sun occlusion experiment which supports this hypothesis. The results of a similar experiment are presented in which 13 young pigeons were kept from sight of the sun during a seven day period including the fall equinox while the sun height at noon decreased 3° 6.7. When the birds were released from a point 93 km. south of their loft they were exposed to a noon sun height equal to that of a point north of their home loft eight days earlier. Nevertheless they showed a northward orientation as did the 10 control birds with no difference in homing performance between the experimental and control groups. These results are not in agreement with those ofMatthews and do not support his sun navigation hypothesis.

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Zusammenfassung Die Sonnennavigations-Hypothese vonMatthews wird kurz besprochen, besonders im Hinblick auf den Warte-Versuch (Sun occlusion experiment), der unter anderem zur Prüfung der Hypothese angestellt wurde. Die Ergebnisse eines im Wilhelmshavener Gebiet angestellten Warteversuchs werden mitgeteilt: 13 Tauben wurden um die Herbst-Tagundnachtgleiche für 7 Tage ohne Sicht der Sonne gehalten, deren Mittagshöhe in dieser Zeit um 3° 6,7 abnahm. Als die Vögel 93 km südlich ihres Heimatorts aufgelassen wurden, befanden sie sich im Gebiet einer Mittags-Sonnenhöhe gleich der, welche vor der Warteperiode etwa 2° nördlich vom Heimatort herrschte. Trotzdem flogen sie gleich den Kontrollen nordwärts ab. Auch im Heimkehrerfolg bestand kein Unterschied zwischen Versuchs-und Kontrolltauben. Diese Ergebnisse stimmen mit den vonMatthews berichteten nicht überein und stützen seine Sonnen-Navigations-Hypothese nicht.

     

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.     

Degenerative and regenerative processes in the olfactory system of homing pigeons.

Experimental resection of the olfactory nerve in the homing pigeon induces a total degeneration of the nerve and olfactory epithelium. The orthograde degenerative process starts before the retrograde one. Ten days after resection, new neurons begin to differentiate from the basal cells. The axon forms earlier than the distal dendritic process, and the speed of growth increases slowly. The regenerated axons only reach the bulb in the 5th month. Two months after resection the olfactory epithelium is similar to that of the intact control side. The ultrastructural features of the mucosa and olfactory axons are similar to those of normal ones.     

Staying in plastic containers interferes with the orientation of clock-shifted homing pigeons

Staying in plastic containers ventilated with natural air during transport and while waiting at the release site was found to affect the initial orientation of pigeons, Columba livia f. domestica, that were exposed to a 6-h clock-shift. The deflection from the mean direction of controls was significantly smaller, and the mean vector length was significantly shorter, than that of clock-shifted pigeons transported in conventional wooden cages. This effect was most pronounced when the birds stayed in plastic containers for the first and second time. Nonshifted control birds seemed to be largely unaffected by plastic containers. There was no influence on homing performance, which suggests a transient nature of the effect. Since the clock-shifted birds had access to the same orientational cues as the controls, we suggest that their sun compass was impaired by stress. We discuss general implications of this container effect, particularly in relation to some cases of olfactory deprivation where containers have been used and stress-induced side-effects cannot be excluded. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

Calculating spatial statistics for velocity jump processes with experimentally observed reorientation parameters

Mathematical modelling of the directed movement of animals, microorganisms and cells is of great relevance in the fields of biology and medicine. Simple diffusive models of movement assume a random walk in the position, while more realistic models include the direction of movement by assuming a random walk in the velocity. These velocity jump processes, although more realistic, are much harder to analyse and an equation that describes the underlying spatial distribution only exists in one dimension. In this communication we set up a realistic reorientation model in two dimensions, where the mean turning angle is dependent on the previous direction of movement and bias is implicitly introduced in the probability distribution for the direction of movement. This model, and the associated reorientation parameters, is based on data from experiments on swimming microorganisms. Assuming a transport equation to describe the motion of a population of random walkers using a velocity jump process, together with this realistic reorientation model, we use a moment closure method to derive and solve a system of equations for the spatial statistics. These asymptotic equations are a very good match to simulated random walks for realistic parameter values.