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 .     

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.     

Orientation in pied flycatchers: the relative importance of magnetic and visual information at dusk

We investigated the orientation of juvenile pied flycatchers, Ficedula hypoleuca, during autumn migration in south Sweden using orientation cage experiments, to study the relative importance of visual and magnetic information at sunset. We performed cage tests under 12 experimental conditions that manipulated the geomagnetic and visual sunset cues available for orientation: natural clear skies in the local or a vertical magnetic field; simulated total overcast in the local or a vertical magnetic field; natural pattern of skylight polarization and directional information from stars screened off, with the sun's position as normal or shifted 120 degrees anticlockwise with mirrors; reduced polarization in the local or a vertical magnetic field; directions of polarization (e-vector) NE/SW and NW/SE, respectively, in the local or a vertical magnetic field. The pied flycatchers were significantly oriented towards slightly south of west when they could use a combination of skylight and geomagnetic cues. The mean orientation was significantly shifted along with the deflection of the sunset position by mirrors. Reduced polarization had no significant effect on orientation either in the local, or in a vertical, magnetic field. The birds tended to orient parallel with the axis of polarization, but only when the artificial e-vector was aligned NW/SE. The mean orientation under simulated total overcast in a vertical, and in the local, magnetic field was not significantly different from random. It is difficult to rank either cue as dominant over the other and we conclude that both visual and magnetic cues seem to be important for the birds' orientation when caught and tested during active migration. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

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.     

Sunset and the orientation of European robins (Erithacus rubecula)

The migratory orientation of European robins (Erithacus rubecula) in autumn was tested immediately after sunset and also after the beginning of astronomical darkness. In twilight tests under clear skies, the birds selected an appropriate migratory direction. During the course of autumn, along with the shift of sunset azimuth, the orientation of birds also shifted, always in a counter-clockwise direction. Although this shift of orientation was not statistically significant, the difference between the mean direction and the sunset was the same for each autumn period. This suggests that the migratory direction was selected on the basis of menotactic orientation re the setting sun. Random directions were observed under solid overcast skies as well as during tests under starry skies, begun after all trace of the sunset position had disappeared.     

Magnetic versus celestial cues: cue-conflict experiments with migrating silvereyes at dusk

To assess the relative importance of celestial and magnetic cues for orientation at dusk, Australian silvereyes, Zosterops l. lateralis, were subjected to artificial magnetic fields under the natural evening sky, beginning 30 min before sunset. Control birds tested in the local geomagnetic field preferred their normal south-southwesterly migratory direction. Birds tested in a magnetic field with north deflected counterclockwise to 240°WSW showed northeasterly tendencies from the first test onward. Birds subjected to a corresponding clockwise deflection to 120°ESE, in contrast, first showed southerly directions, but from the 7th test onward shifted towards the northwest. Hence, both experimental groups followed the shift in magnetic north, one immediately, the other after a delay. When the birds were later tested in a vertical magnetic field without directional information, the two experimental groups continued in the direction they had preferred in the artificial magnetic fields, presumably by celestial cues alone. This indicates that they had not simply ignored celestial cues, but had recalibrated them according to the altered magnetic fields. The reasons for the initial difference between the two experimental groups remain unclear. Delayed responses to deflections of magnetic north have also been observed in previous studies. They appear to be the main reason why studies that expose birds only once to a cue-conflict situation often seem to indicate a dominance of celestial cues, whereas studies exposing the birds repeatedly usually indicate a dominance of magnetic cues. Accepted: 17 September 1997     

Why do migrating robins,Erithacus rubecula,captured at two nearby stop-over sites orient differently?

The orientation of robins captured during autumn and spring migration at two different sites, Falsterbo and Ottenby, in southern Sweden was investigated by cage experiments during the twilight period after sunset. The robins were tested under clear skies with skylight from sunset visible, and under simulated total overcast. The robins from the two sites differed in orientation, especially during autumn migration. While robins from Ottenby generally oriented in their expected migratory direction, the birds from Falsterbo under clear skies oriented towards the sunset direction with a narrow scatter in individual mean headings. Under simulated total overcast the robins from Falsterbo perferred northerly directions in autumn. Short-distance recoveries, one or only a few days after ringing, show that robins in autumn regularly fly 20–80 km from Falsterbo on northerly courses, indicating that they have temporarily reoriented from their normal migratory direction when confronted with the Baltic Sea. In contrast, most robins arrive at Ottenby by extensive flights across the Baltic Sea, and rapidly continue their sea crossing in the normal migratory directions. Mean fat deposits in autumn robins were significantly larger at Ottenby than at Falsterbo. These results indicate that migrating birds may show markedly different orientational dispositions depending on body condition and on their situation with respect to preceding and impending migration over land and sea, respectively.     

Orientation by magnetic field in leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae)

Leaf‐cutter ants (Atta colombica) use trail following to travel between foraging sites and the home nest. However, this combination of pheromone and visual cues is likely to be complemented by a directional reference system such as a compass, used not only when foraging but also during colony formation, where foraging trails degrade or where ants become displaced. One candidate system is the magnetic polarity compass. We tested the orientation of leaf‐cutter ants under a magnetic field of reversed‐polarity, with the prediction that the ants would show 180° deflection compared with control ants in an unchanged geomagnetic field. When the sun's disc was unobstructed by clouds, orientation was the same as that of control ants, implying that magnetic cues were not used to orient. However, when the sky was overcast, ants in the experimental treatment significantly shifted their mean orientation both in comparison with controls and reversed‐polarity ants under the sun. Although a total reversal in orientation was not induced, the results demonstrate that Atta respond to magnetic reversal in the absence of sunlight cues, and suggest a role for magnetic cues in determining direction during orientation.     

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.     

Solar cues in the migratory orientation of the Savannah sparrow, Passerculus sandwichensis

Results clearly implicate the setting sun as a critical source of directional information in the migratory orientation of the savannah sparrow, Passerculus sandwichensis. Savannah sparrows allowed a view of both sunset and stars displayed oriented behaviour in biologically meaningful directions during spring and fall seasons. When the same individuals were denied a view of sunset, and tested under the stars alone, disorientation characterized their behaviour. Furthermore, birds allowed a view of sunset, but tested under ‘overcast’ night skies (no stars visible), displayed well-oriented behaviour indicating the sufficiency of sunset. Experiments in which the migrant's internal chronometer was shifted suggested a fixed-angle (menotactic) response to the sunset cue rather than a time-compensating compass mechanism. I believe stars are valuable to this migrant as celestial reference points. Orientational information gained at the time of sunset is transferred to stars on a nightly basis. The relationship between solar and stellar cues is apparently hierarchical in the savannah sparrow. Information necessary to select the appropriate migratory direction is gained from the primary cue, the setting sun, while maintenance of that heading is dependent on a secondary cue, probably the stars.     

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.     

Magnetic Orientation in Solenopsis sp. Ants

It is known that magnetic fields affect ants behavior. It has been shown that Solenopsis ants are sensitive to magnetic fields but there is no experimental evidence for magnetic orientation. In this paper experiments were done to verify the magnetic orientation of Solenopsis sp. ants. The spontaneous orientation of ants in a circular arena was studied in two different magnetic conditions: in the natural geomagnetic field and under an altered magnetic field, with the horizontal geomagnetic axis shifted in 90?o. Our results show that ants consistently change their orientation direction when the magnetic field was altered. Axial circular statistics analysis showed that, in the absence of other cues, ants orient spontaneously to the horizontal geomagnetic field axis. The present paper shows for the first time magnetic orientation in Solenopsis sp. ants.     

Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect

Recent evaluations of both temporal and spatial precision in bird migration have called for external cues in addition to the inherited programme defining the migratory journey in terms of direction, distance and fuelling behaviour along the route. We used juvenile European robins (Erithacus rubecula) to study whether geomagnetic cues affect fuel deposition in a medium-distance migrant by simulating a migratory journey from southeast Sweden to the wintering area in southern Spain. In the late phase of the onset of autumn migration, robins exposed to the magnetic treatment attained a lower fuel load than control birds exposed to the ambient magnetic field of southeast Sweden. In contrast, robins captured in the early phase of the onset of autumn migration all showed low fuel deposition irrespective of experimental treatment. These results are, as expected, the inverse of what we have found in similar studies in a long-distance migrant, the thrush nightingale (Luscinia luscinia), indicating that the reaction in terms of fuelling behaviour to a simulated southward migration varies depending on the relevance for the species. Furthermore, we suggest that information from the geomagnetic field act as an important external cue overriding the seasonal effect on fuelling behaviour in migratory birds.     

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.     

An experimental analysis on the magnetic field sensitivity of the black-meadow ant Formica pratensis Retzius (Hymenoptera: Formicidae)

Ant responses were tested under both the natural geomagnetic and artificially induced Earth-strength electromagnetic field. Foragers were trained for a month to visit a food source at the north arm accessed through an orientation platform assembly. Under the natural geomagnetic field, when all other orientational cues were eliminated, results indicated significant heterogeneity of ant distribution with the majority seeking geomagnetic north in darkness. However, in light, foragers failed to discriminate geomagnetic north. Under shifted artificial electromagnetic field, orientation was predominantly on the artificial magnetic N/S axis with a significant preference for the artificial north in both light and dark conditions.     

Magnetic information calibrates celestial cues during migration

Migratory birds use celestial and geomagnetic directional information to orient on their way between breeding and wintering areas. Cue-conflict experiments involving these two orientation cue systems have shown that directional information can be transferred from one system to the other by calibration. We designed experiments with four species of North American songbirds to: (1) examine whether these species calibrate orientation information from one system to the other; and (2) determine whether there are species-specific differences in calibration. Migratory orientation was recorded with two different techniques, cage tests and free-flight release tests, during autumn migration. Cage tests at dusk in the local geomagnetic field revealed species-specific differences: red-eyed vireo, Vireo olivaceus, and northern waterthrush, Seiurus noveboracensis, selected seasonally appropriate southerly directions whereas indigo bunting, Passerina cyanea, and grey catbird, Dumetella carolinensis, oriented towards the sunset direction. When tested in deflected magnetic fields, vireos and waterthrushes responded by shifting their orientation according to the deflection of the magnetic field, but buntings and catbirds failed to show any response to the treatment. In release tests, all four species showed that they had recalibrated their star compass on the basis of the magnetic field they had just experienced in the cage tests. Since release tests were done in the local geomagnetic field it seems clear that once the migratory direction is determined, most likely during the twilight period, the birds use their recalibrated star compass for orientation at departure. Copyright 2000 The Association for the Study of Animal Behaviour.     

Mechanisms of dusk orientation in white-throated sparrows (Zonotrichia albicollis): Clock-shift experiments

Summary Several species of night migrating birds, especially North American emberizines, exhibit markedly different orientation behaviour when tested in circular cages under clear skies at dusk as compared with tests performed after complete darkness. During the period between sunset and the first appearance of stars, birds tend to show high levels of well-oriented hopping; birds deprived of exposure to clear skies at dusk hop less and their activity is usually not oriented. There is evidence that visual cues available during the dusk period, but not later, are responsible for this difference, but details of the orientation mechanisms involved are unclear. We performed 3-h fast and slow clock shifts on white-throated sparrows (Zonotrichia albicollis) to address two questions concerning migratory orientation at dusk: (1) Is the better orientation of sparrows tested at dusk a function of the visual cues available at that time, or does it result from circadian changes in motivation?; and (2) Is the dusk orientation based on a time-compensated sun compass?Sparrows subjected to a 3-h slow clock shift were tested with controls on clear, moonless nights beginning immediately after lights-off in the clock shift room and thus about 3.5 h after local sunset. Individuals of both groups performed poorly oriented hopping typical of tests performed after complete darkness. The pooled data from each group were not significantly oriented. These results show that the visual cues available shortly after sunset, not temporal changes in the motivation of the birds, are responsible for the qualitative differences in orientation.Birds exposed to a 3-h fast clock shift were tested with controls on clear evenings between sunset and the first appearance of stars. Both groups showed well-oriented hopping. The mean direction of the pooled tests of controls was 325°, a typical spring orientation direction for this species. The mean direction of the pooled tests of the clock shifted birds (274°) was significantly different from that of controls and the 51° counterclockwise shift is consistent with that predicted by a time-compensated sun compass model.     

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.     

SUNSET AND THE ORIENTATION BEHAVIOUR OF MIGRATING BIRDS

1. Migratory birds integrate information from a wide array of environmental sources. As our knowledge of migratory orientation depends heavily upon the results of cage-experiments with nocturnal migrants, it is essential that the results of these cage studies be interpreted in the light of field observations of migratory behaviour and experiments with free-flying migrants. When this is done, the impression emerges that night-migrating birds integrate directional information prior to departure, probably during the transition between daylight and darkness. At this time, information gained from the sun, in conjunction with other references, becomes especially valuable. 2. Despite intensive work with a few species, how migrants integrate information in the selection and maintenance of a direction is not well understood. The relationship between magnetic stimuli and solar cues at sunset in the selection process, for example, remains to be resolved, as does the contribution of skylight polarization patterns at sunset. Once a migratory heading is selected, birds probably use the stars or winds aloft to maintain that direction. How migrants integrate information is largely a matter of unravelling the complex causal relations among the different environmental stimuli that serve as orientation cues. Imagine a hypothetical migrant that departs on a migratory flight around the time of sunset. Given the uncertain relationship among variables (orientation cues) that might influence her migratory orientation, a path diagram is a useful device for displaying graphically the pattern of causal relations among the set of variables (see Fig. 1). This technique is adopted from path analysis, which is a statistical method developed by Sewall Wright for studying the direct and indirect causal relations among variables (see Kerlinger & Pedhazur, 1973). The pattern depicted in the figure is less a specific model of causal relations than it is a summary of possible relationships among the several cues based on current understanding. Causal flow in this ‘model’ is unidirectional, i.e. at any given point in time a variable cannot be both a cause and an effect of another variable. For example, variable 3 is dependent on variables 1 and/or 2, and is one of the independent variables in relation to variable 5 (orientation of migratory activity). Although the value of path analysis to the study of migratory orientation may be largely heuristic at this point, ‘one virtue of the method is that in order to apply it the researcher is required to make explicit the theoretical framework within which he operates’ (Kerlinger & Pedhazur, 1973). For instance, path diagrams (and path analysis, to the degree that correlations between variables can be specified) would help researchers study (i) the apparent redundancy built into the orientation process (see Fig. 1), (ii) alternative or competing causal models of orientation and navigation, or (iii) the ontogenetic changes that affect the relationship among orientation variables. Imagine, for example, how path coefficients might change in value with migratory experience. 3. Migrants probably redetermine preferred directions soon after landing or shortly before their next departure rather than while aloft. Cage-orientation results as well as observations of free-flying migrants suggest that solar-related information is involved in the morning orientation of ongoing migratory flight and possibly the re-determination of direction following night-time displacement. 4. Evidence is not clear on whether migrants respond to sunset by constant-angle orientation (menotaxis) or constant-azimuth orientation. 5. How migrants correctly identify sunset as a reference stimulus is an unresolved question. Identification might be based upon the characteristic spectral distribution of sunset, its pattern of illumination, or some other feature, such as the characteristic pattern of skylight polarization at sunset. 6. Several lines of evidence suggest that migrants learn to use the setting sun and associated skylight features as orientation cues. 7. The setting sun functions not only as a source of directional information but also as an environmental stimulus that influences the likelihood of migratory activity.