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.     

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.     

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.     

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.     

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.     

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     

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.     

Metabolic responses of homing pigeons to flight and subsequent recovery

This study examines metabolic changes occurring during short to endurance flights and during subsequent recovery in free-flying pigeons, in particular the change towards lipid utilization with increasing flight duration, lipid supply to the flight muscles, protein utilization and the time needed to metabolically recover. Eight plasma metabolite concentrations were measured in homing pigeons released from sites 20–200 km from the loft (0.3–4.8 h flight duration) just after landing and after keeping birds fasting at rest for 30 and 60 min, respectively, after their return. Birds kept in the loft fasting at rest were used as controls. Plasma free fatty acid and glycerol concentrations increased rapidly with flight duration and leveled off after about 1.5 h. This indicates a marked change towards a high and stable lipid utilization from adipose tissues within 1–2 h of flight. Plasma triglyceride levels and very-low-density lipoproteins were decreased after short flights, but subsequently regained or surpassed fasting levels at rest. This indicates that re-esterification of free fatty acids and delivery as very-low-density lipoproteins to the flight muscles to circumvent constraints of fatty acid supply, as described previously for small passerines, is not as significant in the pigeon which has a much lower mass-specific energy rate. An initial increase in plasma glucose levels and a transient decrease to fasting levels at rest was observed and may reflect the initial use and subsequent exhaustion of glycogen stores. Contrary to other birds and mammals, -hydroxy-butyrate levels increased markedly with flight duration. This may suggest a more important sparing of carbohydrates and protein as gluconeogenic precursors in the pigeon than in other species. Plasma uric acid levels increased linearly up to about 4 h flight duration. This indicates an accelerated protein breakdown during flight which may primarily serve to deliver amino acids as glucogenic precursors and citrate cycle intermediates. With increasing flight duration, the energy sources change from an initial phase based primarily on carbohydrates to a lipid-based endurance phase. It is discussed whether this metabolic change depends on the level of power output or the performed work (energy spent) since the start of flight. During the first hour of recovery, most metabolites reached or approached fasting levels at rest, indicating a marked reduction in lipolysis and protein breakdown. -hydroxy-butyrate levels remained at flight levels and glucose levels increased slightly, indicating a restoration of glycogen stores.Abbreviations VLDL very-low-density lipoproteins - FFA free fatty acids     

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.     

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.     

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.     

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.     

The effects of hippocampal lesions in homing pigeons on a one-trial food association task

The role of the avian hippocampal formation in a one-trial food association task was investigated across various retention intervals. Control pigeons, lesioned controls, and pigeons with hippocampal formation lesions were allowed to find food hidden in one of four uniquely decorated bowls in a specific location in a room. After retention intervals of 10 min, 1 h, 7 h, and 24 h, pigeons were placed back in the room with the same bowl in the same location (unmanipulated trials) or with the previously rewarding bowl in a new location and a different bowl in the previously rewarding location (test trials). Although all groups chose the correct bowl during unmanipulated trials, hippocampal formation lesioned birds' choices to the bowl in the correct location decreased compared to the combined controls during the test trials. The results suggest that hippocampal formation lesions do not impair long-term memory of a goal after one experience but significantly decrease the use of spatial information to return to that goal. Accepted: 18 September 1999     

Effects of exogenous melatonin on sun-compass orientation of homing pigeons

Experiments were performed to test whether melatonin plays a role in sun-compass orientation of homing pigeons. Birds were kept for a period of time in dim continuous light (LL) or in artificial light-dark (LD) cycles and then released under the sun from unfamiliar sites. Control birds in dim LL were oriented homeward in all cases. Birds with melatonin implants in LD were capable of a correct use of the sun compass at release. Birds with melatonin implants in dim LL, on the contrary, performed very poorly in orientation. The present results demonstrate for the first time that melatonin is involved in the control of the circadian rhythms underlying sun-compass orientation in birds.     

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

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