Development of the navigational map in homing pigeons: effects of flight experience on orientation performance

Experiments have shown that pigeons, Columba livia, are able to develop navigational abilities even if reared and kept confined in an aviary, provided that they are exposed to the natural winds. In contrast, pigeons reared in a wind-screened aviary do not learn to navigate. Pigeons kept confined in a screened aviary when young do not learn to navigate even if, once they become adult, the screens are removed and the birds are exposed to natural winds for a period sufficiently long for map learning. In all of these experiments, pigeons were kept confined until the day of test release. In the present study we found that pigeons reared in a wind-screened aviary developed navigational abilities if, once adult, they were allowed to perform spontaneous flights around the loft. Nevertheless, their navigational performance never reached the level of controls.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Pigeon Homing: The Orientation of Young Birds that had been Prevented from Seeing the Sun

To test whether the sun is an essential factor for the development of a functioning orientation system in birds, a group of young pigeons was raised as ‘No-Sun’-birds. They were not allowed to see the sun, and they were released to fly around their loft only under total overcast. The control group had an equal number of opportunities to fly under overcast plus additional flights under sun. When released as untrained birds under solid cloud cover, the ‘No-Sun’-birds were significantly oriented, whereas the controls were not. Small magnets glued between the wings (north toward the head) reversed the ‘No-Sun’-birds' orientation, indicating they used a magnetic compass. These findings show that the orientation system can develop without information from the sun. Differences in the orientation behavior of the ‘No-Sun’-birds and normally raised young pigeons are discussed.     

Energy Expenditure and Metabolic Changes of Free-Flying Migrating Northern Bald Ibis

Many migrating birds undertake extraordinary long flights. How birds are able to perform such endurance flights of over 100-hour durations is still poorly understood. We examined energy expenditure and physiological changes in Northern Bald Ibis Geronticus eremite during natural flights using birds trained to follow an ultra-light aircraft. Because these birds were tame, with foster parents, we were able to bleed them immediately prior to and after each flight. Flight duration was experimentally designed ranging between one and almost four hours continuous flights. Energy expenditure during flight was estimated using doubly-labelled-water while physiological properties were assessed through blood chemistry including plasma metabolites, enzymes, electrolytes, blood gases, and reactive oxygen compounds. Instantaneous energy expenditure decreased with flight duration, and the birds appeared to balance aerobic and anaerobic metabolism, using fat, carbohydrate and protein as fuel. This made flight both economic and tolerable. The observed effects resemble classical exercise adaptations that can limit duration of exercise while reducing energetic output. There were also in-flight benefits that enable power output variation from cruising to manoeuvring. These adaptations share characteristics with physiological processes that have facilitated other athletic feats in nature and might enable the extraordinary long flights of migratory birds as well.     

Not just passengers: pigeons,Columba livia,can learn homing routes while flying with a more experienced conspecific

For animals that travel in groups, the directional choices of conspecifics are potentially a rich source of information for spatial learning. In this study, we investigate how the opportunity to follow a locally experienced demonstrator affects route learning by pigeons over repeated homing flights. This test of social influences on navigation takes advantage of the individually distinctive routes that pigeons establish when trained alone. We found that pigeons learn routes just as effectively while flying with a partner as control pigeons do while flying alone. However, rather than learning the exact route of the demonstrator, the paired routes shifted over repeated flights, which suggests that the birds with less local experience also took an active role in the navigational task. The efficiency of the original routes was a key factor in how far they shifted, with less efficient routes undergoing the greatest changes. In this context, inefficient routes are unlikely to be maintained through repeated rounds of social transmission, and instead more efficient routes are achieved because of the interaction between social learning and information pooling.     

Anfangsorientierung und Heimkehrverhalten von Brieftauben unter dem Einflu? von Kurzwellen

Zusammenfassung Um den potentiellen Einfluß von Kurzwellen auf die Orientierung und das Heimkehrverhalten von Brieftauben zu testen, wurden zwei Schläge in der Nähe eines Kurzwellensenders eingerichtet, der eine der Strahlung voll ausgesetzt, der anderer in einem tagsüber nicht für Sendungen benutzten Sektor und zudem topographisch gegen den Sender geschützt. In beiden Schlägen wurden Jungtauben aufgezogen und im Alter von drei Monaten für Testflüge genutzt. Die mit bzw. ohne Kurzwellen am neuen Standort angewöhnten Alttauben sowie die mit bzw. ohne Kurzwellen an diesem Standort aufgewachsenen Jungtauben wurden von einem etwa 11 km entfernten Auflaßort für Heimflüge gegen den Sender mit und ohne Kurzwellen-Einfluß im relevanten Sektor eingesetzt.Es ergaben sich keine Unterschiede in der Anfangsorientierung zwischen den Versuchsgruppen. Dagegen flogen alle ohne Kurzwellen-Einfluß aufgewachsenen Gruppen tendenziell rascher heim, wenn kein aktueller Kurzwellen-Einfluß vorhanden war. Faßte man alle drei Gruppen zusammen, so wurde dieser Unterschied signifikant. Demgegenüber zeigten die beiden mit Strahlung aufgewachsenen Gruppen unter den beiden Strahlungsbedingungen keine unterschiedlichen Heimkehrgeschwindigkeiten. Die fünf Testgruppen zusammengefaßt zeigten geringere Flughöhen unter Kurzwellen-Einfluß. Diese Ergebnisse lassen darauf schließen, daß die Brieftauben die Kurzwellen fühlen können, daß aber ihre Anfangsorientierung dadurch nicht beeinträchtigt wird. Reduzierte Heimkehrgeschwindigkeiten und geringe Flughöhen unter Kurzwellen-Einfluß, deuten auf einen störenden Effekt der elektromagnetischen Felder hin. Das Verhalten der unter Kurzwellen aufgewachsenen juvenilen Gruppen erlaubt den Schluß, daß sich Tauben an gewisse Kurzwellenbedingungen gewöhnen können.

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Initial orientation and homing behaviour of pigeons under the influence of short wave transmissions

Summary In order to test the potential influence of short wave radiation on the homing behaviour of pigeons we positioned two lofts with adult homing pigeons in the vicinity of a short wave transmitter. One loft was next to the transmitter and fully exposed to the radiation, the second protected against the radiation (a) by topographical features and (b) by its position in a sector that was not used for transmission during daytime. In both lofts young pigeons were raised and used for experimental flights at the age of three months. Adults accustomed to the new sites as well as young birds from the exposed and non-exposed lofts, respectively, were released some 11 km from the loft for homeward flights towards the transmitter, with and without transmission towards the relevant sector.Vanishing direction and vanishing time were not affected by the short wave radiation in any of the groups, thus corroborating earlier experiments with pigeons flying homewards from the transmitter towards distant lofts. However, all three groups raised in the absence of short wave radiation (A–, A+, J–) homed tendentially faster in situations where radiation was absent compared to situations with radiation. Pooled in one data set the three groups were significantly faster without radiation. On the other hand, the two juvenile groups raised under radiation (J1+ and J2+) homed at the same speed under both short wave situations. Furthermore, all five groups tended to choose lower flight altitudes when released under the influence of short wave radiation (significantly when groups were pooled). Besides the experiments, observations near the loft gave the impression that the pigeons kept in the exposed loft were reluctant to fly in the neighbourhood of the loft, particularly the adults.We conclude that short wave radiation can be felt by the pigeons, but does not interfere with their initial orientation. Reduced homing speeds of birds grown up without experiencing radiation, low flight levels in flights under radiation in all groups, and a general reluctance to fly of the pigeons next to the exposed loft, suggest that the radiation has an undefined negative effect on the birds. Unimpaired homing speeds in juveniles having grown up under varying field strengths suggest that homing pigeons can become accustomed to short wave radiation to a certain extent.

     

Homing pigeons as a model for avian navigation?

The findings on the navigational mechanisms of homing pigeons and the available data on those of wild birds, in particular migrants, are compared. There are important parallels in the use of the magnetic field and the sun for directional orientation. Also the findings on the navigational ‘map’, its preferred use by experienced birds and the strategy of using route information to acquire the necessary knowledge to establish the ‘map’, obtained in pigeons studies, can probably be generalized to wild birds and migrants in their home region. It seems that birds share a common navigational system. Special development of migratory birds, however, is the innate migration program that enables young first‐time migrants to reach their still unknown wintering area.     

The Orientational Consequences of Flocking Behaviour in Homing Pigeons,Columba livia

Two experiments are described which investigate the orientational consequences of flocking in homing pigeons Columba livia. Previous experiments have shown that homing pigeons placed inside a clear-sided release box for 5 min before release from a familiar site have enhanced ground homing speed compared with those placed in an opaque-sided box. It is assumed that previewing the surrounding landscape allows for faster homing since a bird denied this information must accumulate the knowledge on release. In experiment 1, using the same technique developed in these experiments but releasing the birds in pairs we showed that within familiar areas, homing pigeons can exploit a partner that has acquired more information, allowing them to home more quickly. In experiment 2 we attempted to test three potential strategies which may occur during homing flights. The results do not conclusively distinguish between these three mechanisms but suggest that orientation of the pairs of birds is most likely to have resulted from a compromise of individual tendencies, or from following the best homer, but not from following a ‘governing leader’. The consequence of these mechanisms is discussed.     

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.     

Great flights by great snipes: long and fast non-stop migration over benign habitats

Migratory land birds perform extreme endurance flights when crossing ecological barriers, such as deserts, oceans and ice-caps. When travelling over benign areas, birds are expected to migrate by shorter flight steps, since carrying the heavy fuel loads needed for long non-stop flights comes at considerable cost. Here, we show that great snipes Gallinago media made long and fast non-stop flights (4300-6800 km in 48-96 h), not only over deserts and seas but also over wide areas of suitable habitats, which represents a previously unknown migration strategy among land birds. Furthermore, the great snipes achieved very high ground speeds (15-27 m s(-1)), which was not an effect of strong tailwind support, and we know of no other animal that travels this rapidly over such a long distance. Our results demonstrate that some migratory birds are prepared to accept extreme costs of strenuous exercise and large fuel loads, even when stopover sites are available along the route and there is little tailwind assistance. A strategy of storing a lot of energy before departure, even if migration is over benign habitats, may be advantageous owing to differential conditions of fuel deposition, predation or infection risk along the migration route.     

Pigeon homing: change in navigational strategy during ontogeny

Pigeons of various ages and experience were prevented from collecting meaningful information during the outward journey by being transported in either a distorted magnetic field or in total darkness. In very young, inexperienced birds, these manipulations caused disorientation, the effect decreasing as the birds grew older. Experienced, trained pigeons did not seem to be affected. These results suggest a switch in strategy during the development of the pigeons' navigational system: young pigeons first determine their home direction using information collected en route during the outward journey, but with increasing age and experience, they switch to using local ‘map’ information obtained at the release site. The advantages of using a navigational ‘map’ are discussed.     

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.     

Nocturnal life of young songbirds well before migration

In songbirds, nocturnal activity is believed to be a characteristic feature of migration. However, unlike experimental conditions where the onset of nocturnal restlessness is defined as a shift of activity leading up to the dark period, this behaviour has, until now, not been observed in natural conditions. Here we studied the nocturnal behaviour of radio-tagged juvenile Eurasian reed warblers (Acrocephalus scirpaceus) during the pre-migratory period. The birds started nocturnal flights at the age of 38 days, whereas migration did not commence until they were at least 50 days old. The birds left their natal site by nocturnal flights and repeatedly returned to it. Such shuttle movements suggest the existence of a previously unknown period of nocturnal activity. Motivation to perform such night flights gradually increases with age. We relate the function of these nocturnal pre-migratory flights to the development of a stellar compass, necessary for detecting the compass direction towards winter quarters and for the formation of a navigational target, which will be used during return (spring) migration.     

Multi-modal Orientation Cues in Homing Pigeons

How homing pigeons displaced into unfamiliar territory findtheir way home has been the subject of extensive experimentationand debate. One reason for the controversy is that pigeons seemto use multiple cues. Clock-shifting experiments show that experiencedpigeons use the sun as a preferred compass; when it is not availablethey rely on magnetic cues. That pigeons can home successfullywhile wearing frosted lenses suggests that landmarks, whilenot an essential navigational cue, are important in the finalstages. The sensory basis of the "map" or position finding systemis probably equally or even more complicated. When conditionsaround the loft are suitable, pigeons may use olfactory cuesto find their way or might use some feature of the earth's magneticfield for their navigation. The Wiltschkos (1989) showed thatpigeons raised without free access to ambient odors are notdisoriented when anosmic while their siblings raised with freeaccess to the prevailing wind were disoriented. Similarly, siblingpigeons from two lofts in Lincoln, Massachusetts. were welloriented or totally disoriented when released at magnetic anomaliesunder sunny skies depending upon which of the two lofts theyhad been reared in. All of these experiments and many more suggestthat pigeons use multiple and redundant cues to find their wayhome. Further, there is the suggestion that which cues theyadopt may well be influenced by the characteristics of the areaaround the home loft in which they were reared.     

The ontogeny of orientation in young pigeons

When young pigeons begin to fly, their only means of orientation appears to be a magnetic compass provided by their innate ability to perceive the geomagnetic field. This magnetic compass enables the birds to calibrate other potential orientation stimuli found in their environment thus establishing complex learned mechanisms of orientation preferentially used by experienced birds, like the sun compass and the navigational “map”. The learning processes are described and discussed.     

Introductory remarks on this issue. On the role of the ampulla in disturbances of vestibular function.

The article reports on the use of pigeons as models in the study of vestibular dysfunction. In the experiment reported, the cupula was loosened by raising the endolymph pressure on one side of the ampulla. The pigeon eyes showed a nystagmus. One day later, the pigeons were able to stand upright, but with head tilted toward the side of operation. The pigeons were able to fly within 15 days. Vestibular defects added in some experimental birds resulted in an inability to regain flying capacity.     

Avian olfactory navigation: its empirical foundation and conceptual state

Over the last three decades, empirical evidence has been accumulated indicating that displaced homing pigeons, and most likely other birds as well, are able to navigate home by deducing positional information from atmospheric trace gases perceived by olfaction. I briefly describe the most important results leading to this unexpected conclusion and experiments revealing the decisive role of winds at the home site. A hypothesis trying to explain the results proposes that proportional relationships among a number of atmospheric trace compounds (which determine the quality of a resulting odour) show fairly regular spatial distributions with gradient character. Gas-chromatographic analyses of air samples in an area covering 400 km in diameter revealed that differently oriented ratio gradients of volatile hydrocarbons do in fact exist. They are fairly resistant against, but not independent of, changes of wind direction. Using the measured atmospheric data as inputs, a model system is able to simulate homing navigation on a performance level similar to that observed in pigeons. Results of both pigeon experiments and air analyses are incorporated into an earlier (‘preolfactory’) concept of a hypothetical gradient map linked with a sun compass, which is now modified and furnished with more concrete physical substrates. Winds are identified as the crosslink embedding atmospheric ratio gradients into a directional reference scale provided by the periodically moving sun and the geomagnetic field. Kramer's ‘map-and-compass concept’ is reconsidered. As crucial questions are still unsolved, olfactory navigation remains a challenge for future research.     

Organizing effects of adverse early‐life condition on body mass,compensatory growth and reproduction: experimental studies in rock pigeons

Early‐life food conditions can have profound impact on adult behavioural performance. In song birds, early‐life food conditions affect adult physiology and cognitive performance such as song learning and spatial learning. However, effects on reproductive behaviour other than song, such as visual courtship display, pair formation, and egg laying, which are all important determinants of fitness, received hardly any attention. In this study, rock pigeons Columba livia were raised either in a food ad‐libitum or at impoverished (quality) and restricted (quantity) food conditions, in which the latter was applied for either 26 or 8 d after hatching and in slightly different severity. Their growth and reproductive behaviour in adulthood was analysed under semi‐natural conditions. Impoverished and restricted food (IRF) negatively affected adult body mass, pair‐bonding behaviour, courtship (males) and being courted (females), and induced incomplete compensatory growth. Further analyses suggest that the effects of IRF on behaviour could result from the strong effects on body mass, and perhaps also from detrimental effects of compensatory growth. These results provide evidence that adverse early‐life condition can negatively impact on reproductive success, as suggested by the significant effect on egg production, which will very likely lead to a lower life‐time fitness. The detrimental effects on male courtship indicate that IRF can affect sexual displays via other pathways than by impaired cognition as has been suggested for bird song, since courtship in the pigeons is not learned.     

Flight Energetics in Birds

SYNOPSIS. Some birds can fly for more than 1000 kilometers withoutfeeding. Are these distances compatible with the fuel reservesand the power requirements that flying birds are thought tohave? The fuel for flight is primarily fat, which can make up50% of the total body mass of a bird prior to a long distanceflight. As the bird uses up fuel during the flight and becomeslighter, the power requirements of flight probably decrease.However, a constant power requirement can be assumed throughoutthe flight without introducing serious errors into the estimateof maximum flight distance at a given flight speed. Variousmethods that have been used to estimate the power requirementsof flight are reviewed. Estimates based on indirect calorimetryindicate that the maximum flight distances of birds, when agiven proportion of body mass is used as fuel, are directlyproportional to body mass raised to the 0.227 power. Calculatedvalues of range suggest that birds have small margins of safelyin long, over-water flights unless they are aided by winds orvertical air currents.     

Bird maneuvering flight: blurred bodies, clear heads

While useful in describing the efficiency of maneuvering flight,steady-state (i.e., fixed wing) models of maneuvering performancecannot provide insight to the efficacy of maneuvering, particularlyduring low-speed flapping flight. Contrasted with airplane-analogousgliding/high speed maneuvering, the aerodynamic and biomechanicalmechanisms employed by birds at low flight speeds are violent,with rapidly alternating forces routinely being developed. Thesaltatory nature of this type of flight results in extreme linearand angular displacements of the bird's body; however, birdsisolate their heads from these accelerations with cervical reflexes.Experiments with pigeons suggest this ability to isolate thevisual and vestibular systems is critical to controlled flappingflight: birds wearing collars that prohibited the neck fromisolating the head from the angular accelerations of inducedrolls frequently exhibited (50% of flights) a loss of vestibularand/or visual horizon and were unable to maintain controlledflight.     

Flight energetics in relation to sexual differences in the mating behaviour of a mayfly,Siphlonurus aestivalis

Summary Mayflies (Ephemeroptera) are known to have short adult life-spans. Adults are unable to feed, and they utilize reserves stored during their aquatic larval stage. Energy reserves (fat, glycogen, and free sugars) of mature larvae, subimagoes and imagoes of both sexes of Siphlonurus aestivalis Eaton were compared. All the stages of both sexes had low glycogen and free sugar contents, and the only significant change occurred during the transformation of the mature larva to subimago when almost all the reserves of free sugars were used up. Glycogen and free sugars may serve as energy sources permitting individuals to swim and fly out of the water during emergence. Fat made up most of the energy reserves of mature larvae and was the main source of energy used during the final development of both sexes. Young adult males had high fat reserves which they used as a source of energy for their swarming flights. In contrast, females did not seem to use a significant amount of fat for flight. This difference is probably related to the different mating strategies of the sexes in this species. Males perform long flights waiting for females, whereas females perform only brief flights to mate and reproduce.