Integration of environmental stimuli in the migratory orientation of the savannah sparrow (Passerculus sandwichensis)

Two ‘cue-conflict’ experiments were designed to evaluate the role of (1) solar cues at sunset and stars, and (2) solar cues at sunset and geomagnetic stimuli, in the migratory orientation of the savannah sparrow (Passerculus sandwichensis). A sunset and stars experiment exposed birds in the experimental group to a mirror-reflected sunset followed by an unmanipulated view of stars. Experimental birds shifted their migratory activity in accordance with the setting sun despite exposure to a normal night sky. The sunset and geomagnetism experiment exposed birds in the experimental group to a simultaneous shift in both the position of sunset and the earth's magnetic field. Again experimentals shifted their activity in accordance with the setting sun rather than the artificially shifted magnetic field. Savannah sparrows probaly use stars as celestial landmarks to maintain a preferred direction and do not reorient their activity when exposed to an alternative cue once a direction is established. Moreover, savannah sparrows with experience of migration do not require geomagnetic information in order to use the solar cues available at sunset to select a migratory direction.     

Dramatic orientation shift of white-crowned sparrows displaced across longitudes in the high Arctic

Advanced spatial-learning adaptations have been shown for migratory songbirds, but it is not well known how the simple genetic program encoding migratory distance and direction in young birds translates to a navigation mechanism used by adults. A number of convenient cues are available to define latitude on the basis of geomagnetic and celestial information, but very few are useful to defining longitude. To investigate the effects of displacements across longitudes on orientation, we recorded orientation of adult and juvenile migratory white-crowned sparrows, Zonotrichia leucophrys gambelii, after passive longitudinal displacements, by ship, of 266-2862 km across high-arctic North America. After eastward displacement to the magnetic North Pole and then across the 0 degrees declination line, adults and juveniles abruptly shifted their orientation from the migratory direction to a direction that would lead back to the breeding area or to the normal migratory route, suggesting that the birds began compensating for the displacement by using geomagnetic cues alone or together with solar cues. In contrast to predictions by a simple genetic migration program, our experiments suggest that both adults and juveniles possess a navigation system based on a combination of celestial and geomagnetic information, possibly declination, to correct for eastward longitudinal displacements.     

Avian orientation: effects of cue-conflict experiments with young migratory songbirds in the high Arctic

The migratory orientation of juvenile white-crowned sparrows, Zonotrichia leucophrys gambelli, was investigated by orientation cage experiments in manipulated magnetic fields performed during the evening twilight period in northwestern Canada in autumn. We did the experiments under natural clear skies in three magnetic treatments: (1) in the local geomagnetic field; (2) in a deflected magnetic field (mN shifted −90°); and (3) after exposure to a deflected magnetic field (mN −90°) for 1 h before the cage experiment performed in the local geomagnetic field at dusk. Subjects showed a mean orientation towards geographical east in the local geomagnetic field, north of the expected migratory direction towards southeast. The sparrows responded consistently to the shifted magnetic field, demonstrating the use of a magnetic compass during their first autumn migration. Birds exposed to a cue conflict for 1 h on the same day before the experiment, and tested in the local geomagnetic field at sunset, showed the same northerly orientation as birds exposed to a shifted magnetic field during the experiment. This result indicates that information transfer occurred between magnetic and celestial cues. Thus, the birds' orientation shifted relative to available sunset and geomagnetic cues during the experimental hour. The mean orientation of birds exposed to deflected magnetic fields prior to and during testing was recorded up to two more times in the local geomagnetic field under natural clear and overcast skies before release, resulting in scattered mean orientations.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.)

It has been hypothesized that individuals who have higher demands for spatially based behaviours should show increases in hippocampal attributes. Some avian species have been shown to use a spatially based representation of their environment during migration. Further, differences in hippocampal attributes have been shown between migratory and non-migratory subspecies as well as between individuals with and without migratory experience (juveniles versus adults). We tested whether migratory behaviour might also be associated with increased hippocampal neurogenesis, and whether potential differences track previously reported differences in hippocampal attributes between a migratory (Zonotrichia leucophrys gambelii) and non-migratory subspecies (Z. l. nuttalli) of white-crowned sparrows. We found that non-migratory adults had relatively fewer numbers of immature hippocampal neurons than adult migratory birds, while adult non-migrants had a lower density of new hippocampal neurons than adult and juvenile migratory birds and juvenile non-migratory birds. Our results suggest that neurogenesis decreases with age, as juveniles, regardless of migratory status, exhibit similar and higher levels of neurogenesis than non-migratory adults. However, our results also suggest that adult migrants may either seasonally increase or maintain neurogenesis levels comparable to those found in juveniles. Our results thus suggest that migratory behaviour in adults is associated with maintained or increased neurogenesis and the differential production of new neurons may be the mechanism underpinning changes in the hippocampal architecture between adult migratory and non-migratory birds.     

A visual pathway links brain structures active during magnetic compass orientation in migratory birds

The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, "Cluster N", show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds "see" the reference compass direction provided by the geomagnetic field.     

Field studies of avian nocturnal migratory orientation II. Experimental manipulation of orientation in white-throated sparrows (Zonotrichia albicollis) released aloft

Migrant white-throated sparrows (Zonotrichia albicollis) were released from boxes carried aloft by balloon and tracked with radar. All birds were released on clear nights when winds were light and opposed to the normal migration direction for the season. Birds were treated in one of two ways: Lens birds were fitted with frosted lenses prior to release; No Lens birds were released without lenses. No Lens birds that engaged in straight and level flight generally headed in the predicted migratory direction and as a group were not oriented with respect to wind direction. Lens birds did not head in the predicted migratory direction, but instead oriented downwind. This orientation behaviour is consistent with the relationship of orientation cues inferred from the field observations described in part I of this paper. The data show that flying birds deprived of all detailed form vision can determine wind direction.     

Magnetic Orientation in the Savannah Sparrow

Although magnetic compass orientation has been reported in a number of invertebrate and vertebrate taxa, including about a dozen migratory bird species, magnetic orientation capabilities in animals remain somewhat controversial. We have hand-raised a large number of Savannah sparrows (Passerculus sandwichensis) to study the ontogeny of orientation behavior. Young birds with a variety of early experience with visual and magnetic orientation cues have been tested for magnetic orientation during their first autumn migration. Here we present data from 80 hand-raised sparrows, each tested several times in both normal and shifted magnetic fields. Birds reared indoors with no experience with visual orientation cues showed axial north-south orientation that shifted by almost exactly the magnitude of 90° clockwise and counterclockwise shifts in the direction of magnetic north. Other groups of birds with varying early experience with visual orientation cues showed different preferred orientation directions, but all groups shifted orientation direction in response to shifts in the magnetic field. The data thus demonstrate a robust magnetic orientation ability in this species.     

The role of skylight polarization in the orientation of a day-migrating bird species

To assess the role of skylight polarization in the orientation system of a day-migrating bird, Yellow-faced Honeyeaters (Lichenostomus chrysops, Meliphagidae) were tested in funnel cages for their directional preferences. In control tests in the natural local geomagnetic field under the clear natural sky, they preferred their normal migratory course. Manipulations of the e-vector by depolarizing the skylight or rotating the axis of polarization failed to affect the orientation as long as the natural geomagnetic field was present. When deprived of magnetic information, the birds continued in their normal migratory direction as long as they had access to information from the natural sky, or when either the sun or polarized light was available. However, when sun was hidden by clouds, depolarizers caused disorientation. — These findings indicate that polarized skylight can be used for orientation when no other known cues are available. However in the hierarchy of cues of this species, the polarization pattern clearly ranks lower than information from the geomagnetic field.     

Fuel reserves affect migratory orientation of thrushes and sparrows both before and after crossing an ecological barrier near their breeding grounds

Fat reserves influence the orientation of migrating songbirds at ecological barriers, such as expansive water crossings. Upon encountering a body of water, fat migrants usually cross the barrier exhibiting 'forward' migration in a seasonally appropriate direction. In contrast, lean birds often exhibit temporary 'reverse' orientation away from the water, possibly to lead them to suitable habitats for refueling. Most examples of reverse orientation are restricted to autumn migration and, in North America, are largely limited to transcontinental migrants prior to crossing the Gulf of Mexico. Little is known about the orientation of lean birds after crossing an ecological barrier or on the way to their breeding grounds. We examined the effect of fat stores on migratory orientation of both long- and short-distance migrants before and after a water crossing near their breeding grounds; Catharus thrushes (Swainson's and gray-cheeked thrushes, C. ustulatus and C. minimus ) and white-throated sparrows Zonotrichia albicollis were tested for orientation at the south shore of Lake Ontario during spring and autumn. During both spring and autumn, fat birds oriented in a seasonally appropriate, forward direction. Lean thrushes showed a tendency for reverse orientation upon encountering water in the spring and axial, shoreline orientation after crossing water in the autumn. Lean sparrows were not consistently oriented in any direction during either season. The responses of lean birds may be attributable to their stopover ecology and seasonally-dependent habitat quality.     

Moonlight and the Migratory Orientation of Savannah Sparrows (Passerculus sandwichensis)

Migratory birds might respond to moonlight in at least four ways: (1) a geographical reference for selecting a compass direction, (2) a celestial ‘landmark’ to facilitate maintenance of a preferred heading, (3) a stimulus that distracts migrants and introduces error in compass orientation, or (4) a source of illumination that facilitates nocturnal flight. This study examines the response of migratory savannah sparrows (Passerculus sandwichensis) to moonlight during controlled tests in orientation cages. I found no evidence that savannah sparrows use a lunar compass to select a direction. If savannah sparrows do use the moon as a ‘landmark’ to maintain a direction selected with reference to a different cue, I expected birds to be better oriented on overcast nights when the moon is present than they are when the moon is absent. The results suggest otherwise. Usually, savannah sparrows respond phototactically to the moon by directing their cage activity toward or at a constant angle with respect to the moon's azimuth. Interestingly, the migrant's response to moonlight depended on whether the bird viewed the setting sun earlier that evening.     

Orientation of Dunnocks (Prunella modularis) at Sunset

To find out the relative importance of the geomagnetic and solar cues for the orientation at the time of sunset, dunnocks were tested outdoors during the spring migration periods of 1982 and 1983. Experimental magnetic fields were produced by Helmholtz coils. In the various magnetic conditions, the following results were obtained:

• 1 In the local geomagnetic field, the dunnocks oriented in a seasonally appropriate northerly direction.
• 2 In a magnetic field the north of which was shifted 120° clock-wise to ESE, the birds showed a corresponding shift in their orientation.
• 3 In a vertical magnetic field without meaningful directional information, birds previously tested in either the local geomagnetic field or the shifted magnetic field now displayed axially bimodal orientation, with the axes of the two groups differing.

These findings indicate that for migratory dunnocks, the magnetic field plays a dominant role in determining their orientation at the time of sunset, and that magnetic information may affect the dunnocks' response to other directional, presumably solar cues as well.     

Compass orientation and possible migration routes of passerine birds at high arctic latitudes

The use of celestial or geomagnetic orientation cues can lead migratory birds along different migration routes during the migratory journeys, e.g. great circle routes (approximate), geographic or magnetic loxodromes. Orientation cage experiments have indicated that migrating birds are capable of detecting magnetic compass information at high northern latitudes even at very steep angles of inclination. However, starting a migratory journey at high latitudes and following a constant magnetic course often leads towards the North Magnetic Pole, which means that the usefulness of magnetic compass orientation at high latitudes may be questioned. Here, we compare possible long‐distance migration routes of three species of passerine migrants breeding at high northern latitudes. The initial directions were based on orientation cage experiments performed under clear skies and simulated overcast and from release experiments under natural overcast skies. For each species we simulated possible migration routes (geographic loxodrome, magnetic loxodrome and sun compass route) by extrapolating from the initial directions and assessing a fixed orientation according to different compass mechanisms in order to investigate what orientation cues the birds most likely use when migrating southward in autumn. Our calculations show that none of the compass mechanisms (assuming fixed orientation) can explain the migration routes followed by night‐migrating birds from their high Nearctic breeding areas to the wintering sites further south. This demonstrates that orientation along the migratory routes of arctic birds (and possibly other birds as well) must be a complex process, involving different orientation mechanisms as well as changing compass courses. We propose that birds use a combination of several compass mechanisms during a migratory journey with each of them being of a greater or smaller importance in different parts of the journey, depending on environmental conditions. We discuss reasons why birds developed the capability to use magnetic compass information at high northern latitudes even though following these magnetic courses for any longer distance will lead them along totally wrong routes. Frequent changes and recalibrations of the magnetic compass direction during the migratory journey are suggested as a possible solution.     

The Magnetic Field as a Reference System for Genetically Encoded Migratory Direction in Pied Flycatchers (Ficedula hypoleuca Pallas)

To see whether the migratory orientation of pied flycatchers (Ficedula hypoleuca Pallas) is genetically encoded with respect to the earth magnetic field a group of young birds was hand-raised. They were thus prevented from ever experiencing the sky. The birds were tested in autumn 1980 and 1981 in the local geomagnetic field (Fig. 1) and in three artificial fields (Fig. 2a-c). The results show that their magnetic compass matures independent of any experience with the sky and contains sufficient information for the birds to orient toward their migratory direction.     

The Direction of Celestial Rotation Affects the Development of Migratory Orientation in Pied Flycatchers,Ficedula hypoleuca

The migratory direction in young passerine migrants is based on innate information, with the geomagnetic field and celestial rotation as references. To test whether the direction of celestial rotation is of importance, hand-raised pied flycatchers in Latvia were exposed during the premigratory period to a planetarium rotating in different directions. During autumn migration, when their orientation behavior was recorded in the local geomagnetic field in the absence of celestial cues, birds that had been exposed to a sky rotating in the natural direction showed a unimodal preference of their south-westerly migratory direction. Birds that had been exposed to a sky rotating in the reversed direction, in contrast, showed a bimodal preference of an axis south-west-north-east. Their behavior was similar to that of pied flycatchers that had been raised without access to celestial cues. In Latvia, the magnetic field alone allows only orientation along the migratory axis, and celestial rotation enables birds to select the correct end of this axis. Our findings show that the direction of rotation is of crucial importance: celestial rotation is effective only if the stars move in the natural direction.     

Orientation Cage and Release Experiments with Migratory Wheatears (Oenanthe oenanthe) in Scandinavia and Greenland: The Importance of Visual Cues

Migratory orientation of Scandinavian and Greenland wheatears was recorded during the autumn migration periods of 1988 and 1989. Orientation cage tests were conducted under clear sunset skies, to investigate the importance of different visible sky sections on orientation performance. In addition, wheatears were released under clear starry skies and under total overcast to examine the orientation of free-flying birds. The following results were obtained:

• 1 Wheatears tested with a restricted visible sky section (90° centered around zenith) in orientation cages, showed a mean orientation towards geographic W/geomagnetic NW (Greenland) and towards geographic and magnetic WNW-NW (Sweden). These mean directions are clearly inconsistent with the expected autumn migration directions, SW-SSW in Scandinavia and SE in Greenland, as revealed by ringing recoveries for the two populations.
• 2 When the birds were allowed a much more extensive view of the sky, almost down to the horizon (above 10° elevation), Scandinavian wheatears chose headings in agreement with ringing data. Greenland birds were not significantly oriented.
• 3 Release experiments under clear starry skies resulted in mean vanishing directions in good agreement with ringing data from both sites. Greenland wheatears released under total overcast showed a similar orientation as under clear skies, indicating that a view of the stars may not be of crucial importance for selecting a seasonally accurate migratory direction.

The results suggest that an unobstructed view of the sky, including visual cues low over the horizon, is important, possibly in combination with geomagnetic cues, for the orientation of migratory naive wheatears. Furthermore, the birds showed remarkably similar orientation responses in Greenland and Scandinavia, respectively, indicating that they use basically the same orientation system, despite considerable differences in visual and geomagnetic orientation premises at the two different geographic and magnetic latitudes.     

Avian orientation at steep angles of inclination: experiments with migratory white-crowned sparrows at the magnetic North Pole

The Earth's magnetic field and celestial cues provide animals with compass information during migration. Inherited magnetic compass courses are selected based on the angle of inclination, making it difficult to orient in the near vertical fields found at high geomagnetic latitudes. Orientation cage experiments were performed at different sites in high Arctic Canada with adult and young white-crowned sparrows (Zonotrichia leucophrys gambelii) in order to investigate birds' ability to use the Earth's magnetic field and celestial cues for orientation in naturally very steep magnetic fields at and close to the magnetic North Pole. Experiments were performed during the natural period of migration at night in the local geomagnetic field under natural clear skies and under simulated total overcast conditions. The experimental birds failed to select a meaningful magnetic compass course under overcast conditions at the magnetic North Pole, but could do so in geomagnetic fields deviating less than 3 degrees from the vertical. Migratory orientation was successful at all sites when celestial cues were available.     

Avian navigation and geographic positioning

Site fidelity to breeding and wintering grounds, and even stopover sites, suggests that passerines are capable of accurate navigation during their annual migrations. Geolocator‐based studies are beginning to demonstrate precise population‐specific migratory routes and even some interannual consistency in individual routes. Displacement studies of birds have shown that at least adult birds are capable of goal‐oriented movements, likely involving some type of map or geographic position system. In contrast, juveniles on their first migration use a clock‐and‐compass orientation strategy, with limited knowledge about locations along their migratory routes. Positioning information could come from a variety of cues including visual, olfactory, acoustic, and geomagnetic sources. How information from these systems is integrated and used for avian navigation has yet to be fully articulated. In this review, we (1) define geographic positioning and distinguish the types of navigational strategies that birds could use for orientation, (2) describe sensory cues available to birds for geographic positioning, (3) review the evidence for geographic positioning in birds and methods used to collect that evidence, and (4) discuss ways ornithologists, particularly field ornithologists, can contribute to and advance our knowledge of the navigational abilities of birds. Few studies of avian orientation and navigation mechanisms have been conducted in the Western Hemisphere. To fully understand migratory systems in the Western Hemisphere and develop better conservation policies, information about the orientation and navigation mechanisms used by specific species needs to be integrated with other aspects of their migration ecology and biology.     

Shifted magnetic fields lead to deflected and axial orientation of migrating robins,Erithacus rubecula,at sunset

The migratory orientation of the robin was tested in shifted magnetic fields during the twilight period after sunset, under clear skies and under simulated total overcast. The horizontal direction of the geomagnetic field was shifted 90° to the right or left in relation to the local magnetic field, without changing either the intensity of the field or its angle of inclination. Experiments were conducted during both spring and autumn, with robins captured as passage migrants at the Falsterbo and Ottenby bird observatories in southern Sweden as test subjects. Generally, the orientation of robins was affected by magnetic shifts compared to controls tested in the natural geomagnetic field. Autumn birds from the two capture sites differed in their responses, probably because of different migratory dispositions and body conditions. The robins most often changed their orientation to maintain their typical axis of migration relative to the shifted magnetic fields. However, preferred directions in relation to the shifted magnetic fields were frequently reverse from normal, or axial rather than unimodal. These results disagree with suggested mechanisms for orientation by visual sunset cues and with the proposed basis of magnetic orientation. They do, however, demonstrate that the geomagnetic field is involved in the sunset orientation of robins, probably in combination with additional visual or non-visual cues that contribute to establish magnetic polarity.     

Bird navigation: what type of information does the magnetite-based receptor provide?

Previous experiments have shown that a short, strong magnetic pulse caused migratory birds to change their headings from their normal migratory direction to an easterly direction in both spring and autumn. In order to analyse the nature of this pulse effect, we subjected migratory Australian silvereyes, Zosterops lateralis, to a magnetic pulse and tested their subsequent response under different magnetic conditions. In the local geomagnetic field, the birds preferred easterly headings as before, and when the horizontal component of the magnetic field was shifted 90 degrees anticlockwise, they altered their headings accordingly northwards. In a field with the vertical component inverted, the birds reversed their headings to westwards, indicating that their directional orientation was controlled by the normal inclination compass. These findings show that although the pulse strongly affects the magnetite particles, it leaves the functional mechanism of the magnetic compass intact. Thus, magnetite-based receptors seem to mediate magnetic 'map'-information used to determine position, and when affected by a pulse, they provide birds with false positional information that causes them to change their course.     

Migratory Sleeplessness in the White-Crowned Sparrow (Zonotrichia leucophrys gambelii)

Twice a year, normally diurnal songbirds engage in long-distance nocturnal migrations between their wintering and breeding grounds. If and how songbirds sleep during these periods of increased activity has remained a mystery. We used a combination of electrophysiological recording and neurobehavioral testing to characterize seasonal changes in sleep and cognition in captive white-crowned sparrows (Zonotrichia leucophrys gambelii) across nonmigratory and migratory seasons. Compared to sparrows in a nonmigratory state, migratory sparrows spent approximately two-thirds less time sleeping. Despite reducing sleep during migration, accuracy and responding on a repeated-acquisition task remained at a high level in sparrows in a migratory state. This resistance to sleep loss during the prolonged migratory season is in direct contrast to the decline in accuracy and responding observed following as little as one night of experimenter-induced sleep restriction in the same birds during the nonmigratory season. Our results suggest that despite being adversely affected by sleep loss during the nonmigratory season, songbirds exhibit an unprecedented capacity to reduce sleep during migration for long periods of time without associated deficits in cognitive function. Understanding the mechanisms that mediate migratory sleeplessness may provide insights into the etiology of changes in sleep and behavior in seasonal mood disorders, as well as into the functions of sleep itself.