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.     

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.     

Field studies of avian nocturnal migratory orientation I. interaction of sun,wind and stars as directional cues

Tracking radar and visual observation techniques were used to observe the orientation of free-flying passerine nocturnal migrants in situations in which potentially usable directional cues were absent or gave conflicting information. When migrants had seen the sun near the time of sunset and/or the stars, they oriented in appropriate migratory directions even when winds were opposed. Under solid overcast skies that prevented a view of both sun and stars, the birds headed downwind in opposing winds and thus moved in seasonally inappropriate directions. The data point to the primacy of visual cues over wind direction, with either sun or stars being sufficient to allow the birds to determine the appropriate migration direction.     

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.     

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.     

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.     

Reverse turning and angle compensation in a migratory passerine,passerculus sandwichensis

Reverse turning behaviour was revealed in the savannah sparrow (Passerculus sandwichensis), a migratory passerine, using a T-shaped runway system. Compensatory reverse turns were recorded for experimental birds which were forced to make 90° turns either to the left or right before proceeding to a choice point. Controls ran a straight runway from start to choice point and were as likely to turn left as right. A second experiment revealed an ability to compensate for angular deviations in course. Experimentals were forced to make turns of less than 90° before entering a semi-circular arena. They responded with a compensatory turn of the appropriate sign (left or right) and magnitude. An idiothetic mechanism is probably involved in the observed angle sense (Winkelsinn). The results are broadly relevant to animal orientation.     

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 cues used by migratory birds: A review of cue-conflict experiments

During the late 1960s and early 1970s the accumulating evidence of magnetic orientation forced the conclusion that the orientation of migratory birds and homing pigeons is based upon multiple stimuli. 'Cue-conflict experiments' have provided a powerful means of asking how these directional cues relate one to another. The weight of evidence suggests that in short-term orientation decision making, magnetic cues take precedence over stars, and visual information at sunset overrides both these stimuli. Recent experiments point to polarized skylight patterns as the relevant cue in dusk orientation. Although cue-conflict experiments have now been performed on a diversity of species, generalizations are weakened because of differences in experimental design, in the cues examined and in our ability to manipulate those cues. There remains a need for carefully designed comparative studies.     

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.     

The Orientation Behaviour of Chaffinches, Fringilla coelebs, Caught during Active Migratory Flight, in Relation to the Sun

The few orientation studies that have been carried out with day-migrating birds show that they are able to use solar and magnetic orientation cues for orientation. Previous orientation experiments in Emlen funnels have been carried out either with hand-raised birds or with birds caught during resting periods at stop-over sites. The aim of our study was to test whether birds caught during active flight show a higher concentration of migratory activity in the seasonally appropriate migratory direction in the funnels than birds that had not experienced migration just before the funnel experiments. The topography at the alpine pass Col de Bretolet at the border of Switzerland and France allowed us to capture birds during active migratory flight. These birds were in full migration disposition. Orientation experiments with chaffinches suggested an influence of the sun because chaffinches did not orient in the seasonally expected direction, but probably showed positive phototaxis towards the light of the sun at the opposite side of the funnel. Chaffinches tested under overcast conditions oriented to the north-west which probably was a 'nonsense' orientation and not a reverse migration or compensatory behaviour. We conclude that freshly caught birds are too stressed to show appropriate orientation when tested immediately after catching.     

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.     

Sunset,skylight polarization and the migratory orientation of yellow-rumped warblers,Dendroica coronata

Celestial light cues visible at sunset appear to play an important role in the nocturnal orientation of several species of night-migrating birds. The pattern of skylight polarization, an especially prominent geographical reference at sunrise and sunset, influences the orientation behaviour of migratory birds. Yellow-rumped warblers were capable of seasonally appropriate cage orientation at dusk and were sensitive to manipulation of the axis of skylight polarization (E-vector). A series of experimental treatments was designed to examine the relationship between sunset position and skylight polarization. The window panels of hexagonal enclosures were fitted with a depolarizer and a polaroid filter to rotate the E-vector, and mirrors to reflect the position of sunset. The results indicate that this migrant minimizes sunset position as an orientation relative to skylight polarization and may depend upon the latter to orient at dusk. The possibility that yellow-rumped warblers calibrate their sun compass in relation to polarized light remains a question for future research.     

On the evolution of brain size in relation to migratory behaviour in birds

Migratory birds appear to have relatively smaller brain size compared to sedentary species. It has been hypothesized that initial differences in brain size underlying behavioural flexibility drove the evolution of migratory behaviour; birds with relatively large brains evolved sedentary habits and those with relatively small brains evolved migratory behaviour (migratory precursor hypothesis). Alternative hypotheses suggest that changes in brain size might follow different behavioural strategies and that sedentary species might have evolved larger brains because of differences in selection pressures on brain size in migratory and nonmigratory species. Here we present the first evidence arguing against the migratory precursor hypothesis. We compared relative brain volume of three subspecies of the white-crowned sparrow: sedentary Zonotrichia leucophrys nuttalli and migratory Z. l. gambelii and Z. l. oriantha. Within the five subspecies of the white-crowned sparrow, only Z. l. nuttalli is strictly sedentary. The sedentary behaviour of Z. l. nuttalli is probably a derived trait, because Z. l. nuttalli appears to be the most recent subspecies and because all species ancestral to Zonotrichia as well as all older subspecies of Z. leucophrys are migratory. Compared to migratory Z. l. gambelii and Z. l. oriantha, we found that sedentary Z. l. nuttalli had a significantly larger relative brain volume, suggesting that the larger brain of Z. l. nuttalli evolved after a switch to sedentary behaviour. Thus, in this group, brain size does not appear to be a precursor to the evolution of migratory or sedentary behaviour but rather an evolutionary consequence of a change in migratory strategy.     

Reed warbler orientation: initiation of nocturnal migratory flights in relation to visibility of celestial cues at dusk

We used radiotelemetry to investigate the time of migratory flight initiation relative to available celestial orientation cues and departure direction of a nocturnal passerine migrant, the reed warbler, Acrocephalus scirpaceus, during autumn migration. The study was carried out at Falsterbo, a coastal site in southwest Sweden. The warblers initiated migration from times well after local sunset and well into the night, corresponding to sun elevations between -4 degrees and -35 degrees, coinciding with the occurrence of stars at night. They departed in the expected migratory direction towards south of southwest with a few initiating migration in reverse directions towards northeast to east. Flight directions under overcast conditions (7-8/8) were more scattered than under clear sky conditions (0-4/8). There were fewer clouds on departure nights than on nights when the birds did not initiate migration. For birds staying longer than one night at stopover the horizontal visibility was higher and precipitation was less likely on departure nights than on the previous night. The results show that the visibility of celestial cues, and stars in particular, are important for the decision to initiate migration in reed warblers. However, cloud cover, horizontal visibility and precipitation might be correlated with other weather variables (i.e. wind or air pressure) that are also likely to be important for the decision to migrate. Copyright 2001 The Association for the Study of Animal Behaviour.     

Manipulations of polarized skylight calibrate magnetic orientation in a migratory bird

1. Young migratory birds enter the world with two representations of the migratory direction, one coded with respect to the magnetic field, the other with respect to celestial rotation. The preferred magnetic direction of migratory orientation is malleable early in life: it may be calibrated by celestial rotation, observed either in daytime or at night.
2. Previous experiments showed that early experience with skylight polarization was necessary for calilbration to occur in daytime. In this study, we performed a direct manipulation of patterns of polarized skylight at dawn and dusk.
3. Hand-raised Savannah sparrows (Passerculus sandwichensis) were allowed to observe the clear sky for 1 h prior to local sunrise and for one h following local sunset. They never saw the Sun nor stars. The birds observed the sky through bands of polarizing material (HNP'B) aligned with the e-vector axis in one of three orientations with respect of the azimuth of sunrise and sunset: group 1) 90°; group 2) 45° CW; group 3) 45° CCW.
4. Tested indoors in covered cages in both shifted and unshifted magnetic fields, the autumn migratory orientation of the three groups differed significantly. Group 1 oriented magnetic N-S, group 2 oriented magnetic NW-SE, and group 3 oriented magnetic NNE-SSW. These observed orientation directions are very close to those predicted by the manipulations of polarized skylight.
5. These results indicated that a fairly simplified, static polarized light pattern viewed a limited number of times only in dawn and dusk snapshots is sufficient to produce calibration of the preferred magnetic migratory orientation direction.

     

昆虫迁飞行为的参数化Ⅱ.模式与检验

对通过昆虫迁飞行为分析得到的迁飞时间参数、高度参数、速度和方向参数等分别以一定的数学形式加以表达。其中,起飞时间以日出日没及晨昏朦影时刻为基准,用天文公式求出;边界层顶与飞行低温阈限所在高度及运行高度上的风速、风向由一维湍能（ＴＫＥ）模式以Ｅ－ε闭合做数值模拟：对飞行力较弱的小型或微小昆虫做随风运行处理,而对大型昆虫则根据其自身的飞行速度和定向方位与其飞行高度上的风向风速做矢量运算,求得位移方向和速度。通过我国小地老虎和草地螟标放回收试验结果的检验,表明本文提出的迁飞行为参数化方案是合理可行的。以此为基础组建数值模型进行昆虫迁飞轨迹分析,可望进一步提高迁飞性害虫异地预测的水平     

Interactions of the polarization and the sun compass in path integration of desert ants

Desert ants, Cataglyphis fortis, perform large-scale foraging trips in their featureless habitat using path integration as their main navigation tool. To determine their walking direction they use primarily celestial cues, the sky’s polarization pattern and the sun position. To examine the relative importance of these two celestial cues, we performed cue conflict experiments. We manipulated the polarization pattern experienced by the ants during their outbound foraging excursions, reducing it to a single electric field (e-)vector direction with a linear polarization filter. The simultaneous view of the sun created situations in which the directional information of the sun and the polarization compass disagreed. The heading directions of the homebound runs recorded on a test field with full view of the natural sky demonstrate that none of both compasses completely dominated over the other. Rather the ants seemed to compute an intermediate homing direction to which both compass systems contributed roughly equally. Direct sunlight and polarized light are detected in different regions of the ant’s compound eye, suggesting two separate pathways for obtaining directional information. In the experimental paradigm applied here, these two pathways seem to feed into the path integrator with similar weights.     

Orientation to shorelines by the supratidal amphipod Talorchestia longicornis: Wavelength specific behavior during sun compass orientation

If released in water or on sand the supratidal amphipod Talorchestia longicornis Say amphipods moves in the onshore direction. The present study was designed to determine whether this species uses the sun as a cue for orientation and if so, which visual pigment in the compound eyes is involved. When tested in an apparatus with a view of only the sun and sky amphipods were disoriented when the sun was obscured by clouds. However, when the sun was visible, they oriented in the onshore direction of their home beach in both water and air during both the morning and afternoon. Resetting the time of their circadian rhythm in activity with either an altered light:dark or diel temperature cycle also reset the chronometric mechanism associated with sun compass. orientation. T. longicornis has two visual pigments with absorption maxima near 420 nm and 520 nm. Only the 420 nm pigment is used for sun compass orientation, which may be an adaptation for increasing the contrast between the sun and background scattered skylight or for detecting the radiance distribution of skylight. Irradiating the 520 nm absorbing pigment alone induced positive phototaxis to the sun but not onshore orientation. Thus, T. longicornis shows wavelength specific behavior by using only one of its visual pigments for sun compass orientation.     

Visual cues used by ball-rolling dung beetles for orientation

Ball rolling by dung beetles is considered to be a derived behaviour that evolved under pressure for space, and from competitors at the dung pat. Straight-line orientation away from the pat using a celestial cue should be the most successful rolling strategy to move dung to an unknown burial site. We tested this hypothesis in the field and the laboratory by presenting five species of ball-rolling beetles with different orientation tasks, involving reaction to obstacles as well as to reflected sunlight and artificial light sources. Beetles were found to consistently orientate along a chosen route, usually in the direction of the sun. Beetles rolling dung balls successfully negotiated barriers and returned to the original path as did beetles falling from ramps, or rotated about a fixed point while rolling a ball. The sun was found to be the main orientation cue, which could be substituted by reflected or artificial light. However, beetles reoriented themselves less accurately in response to lights in the laboratory, than they did to the reflected sun in the field. It is probable that phototactic orientation using the sun, which is widespread amongst arthropods, has been incorporated in the straight-line foraging behaviour that has evolved in ball-rolling dung beetles.