Nocturnal orientation of robins, Erithacus rubecula: birds caught during migratory flight are disoriented

For conventional experiments on the orientation behavior of migrant birds in funnels, either hand-raised birds or birds caught during resting periods at stopover sites are generally used. Topographic circumstances at the Alpine pass Col de Bretolet at the Switzerland/France border allow the capture of birds during active migratory flight during the whole night. These birds are in full migratory disposition. We expected them to orient in the seasonally appropriate direction more accurately than birds that had not experienced migration just before the funnel experiment. Experiments with robins, however, revealed a strong influence of the moon on the orientation behavior. The birds did not orient in the seasonally expected migratory direction but showed positive phototaxis, usually toward the lightest part of the funnel in the direction opposite to the moon. When the moon was absent the robins were disoriented. Sunset experiments with robins caught during the night before the experiment revealed a strong phototactic reaction toward the setting sun. As reasons for this poor orientation in the absence of light stimuli, the influence of the topography of the mountainous region and magnetic anomalies can be excluded. It is concluded that freshly caught birds are too stressed when tested immediately after capture or that the migration direction cannot be maintained. Testing of night migrants in complete darkness is also of disadvantage. Received: 23 December 1998 / Received in revised form: 16 July 1999 / Accepted: 30 July 1999     

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.     

BirdOriTrack: a new video‐tracking program for orientation research with migratory birds

Experimental research on the orientation of migratory songbirds is traditionally conducted using orientation funnels or automatic registration cages that record the directional activity of individual birds on paper or a computer. Most traditionally used funnel and cage designs do not permit investigators to observe detailed behavior of the birds and, therefore, we have gained little insight into the actual behavior of birds while they are exhibiting migratory restlessness and making directional choices. Such behavior can only be studied by direct observation or by video filming. Here, we present BirdOriTrack, a video‐tracking program for extracting time‐resolved, positional data of birds (and potentially other animal species) to determine their orientation relative to the center of a circular cage/funnel. With relatively inexpensive cameras, recording equipment, and cages, orientation experiments can easily be conducted and analyzed using BirdOriTrack. The program is designed to be flexible, allowing analysis of orientation behavior of birds of any size in different cage designs and in both controlled laboratory settings and field‐based studies. To demonstrate the program's utility, we show the results of preliminary field experiments on several species of migratory birds captured at a migration monitoring station. BirdOriTrack is freely available at http://canmove.lu.se/birdoritrack .     

The Influence of Fat Stores on Magnetic Orientation in Day-migrating Chaffinch,Fringilla coelebs

Earlier experimental studies have demonstrated the ability of day-migrating birds to perform migration under overcast skies, thereby indicating use of cues other than solar. The orientation behaviour of the chaffinch, a diurnal migrant, was investigated in orientation cage experiments during the autumn migration period. The aim of our experiments was to examine the relationship between different orientation cues and the influence of body condition on directional choices. We obtained the following results: 1. Chaffinches displayed a bimodal distribution of headings along a SW-NE axis when tested in the local geomagnetic field (controls); 2. When the geomagnetic field was experimentally deflected 90° counterclockwise, the chaffinches responded by changing their preferred axial orientation to SE-NW; and 3. The predictive power of stored fat reserves became evident when both the control and experimental samples were subdivided into fat and lean individuals. The majority of fat controls orientated towards a seasonally appropriate SW direction, whereas lean controls chose mean directions towards the NE. Experimentals followed the same pattern, but with the expected deflection, i.e. fat birds selected SE headings and lean individuals chose a NW mean direction.     

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.     

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.     

Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds

Vast numbers of insects and passerines achieve long-distance migrations between summer and winter locations by undertaking high-altitude nocturnal flights. Insects such as noctuid moths fly relatively slowly in relation to the surrounding air, with airspeeds approximately one-third of that of passerines. Thus, it has been widely assumed that windborne insect migrants will have comparatively little control over their migration speed and direction compared with migrant birds. We used radar to carry out the first comparative analyses of the flight behaviour and migratory strategies of insects and birds under nearly equivalent natural conditions. Contrary to expectations, noctuid moths attained almost identical ground speeds and travel directions compared with passerines, despite their very different flight powers and sensory capacities. Moths achieved fast travel speeds in seasonally appropriate migration directions by exploiting favourably directed winds and selecting flight altitudes that coincided with the fastest air streams. By contrast, passerines were less selective of wind conditions, relying on self-powered flight in their seasonally preferred direction, often with little or no tailwind assistance. Our results demonstrate that noctuid moths and passerines show contrasting risk-prone and risk-averse migratory strategies in relation to wind. Comparative studies of the flight behaviours of distantly related taxa are critically important for understanding the evolution of animal migration strategies.     

Migratory Orientation of Blackcaps (Sylvia atricapilla): Population-specific Shifts of Direction during the Autumn

The population-specific orientation of two groups of blackcaps (Sylvia atricapilla), one from southwest Germany, the other from easternmost Austria, was studied outdoors in Emlen funnels. We investigated whether a seasonal shift in the migratory direction — as expected for the Austrian birds from ringing recoveries — occurs under experimental conditions and in a seasonally constant magnetic field. The West German birds, for which no shift was expected, oriented southwest during the entire season. The Austrian birds oriented southeast in October and southsouthwest in November. The clockwise shift by about 60° occurred within a 10-day period. The results indicate that in this species seasonal changes of migratory direction are probably based on an endogenous program, occur without the birds actually migrating and are independent of changes in the magnetic field. Our results provide further evidence that directional shifts in Sylvia warblers may be controlled by a different mechanism than in pied flycatchers (Ficedula hypoleuca).     

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 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.     

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.     

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.     

Characteristics of the distribution of birds infected with hemosporidians (Sporozoa, Haemosporidia) during the fall migration in flight waves

Chaffinches, infected with hemoproteids (Haemoproteidae) and leucocytozoids (Leucocytozoidae), are uniformly distributed in the ranges of each nonequivalent from the point of view of bioenergetics migratory wave. Extensiveness of infection of birds with leucocytozoids in autumn increases reliably at the time of late migratory waves as compared to early ones. The last flight wave, which is observed in the Kurskaya Kosa in the second half of October, consists, in general, of chaffinches which have already gone through the leucocytozoonosis. Concentration of infected birds at the end of the species migration flow can be regarded as a peculiar parasitic filter delaying the birds, which have been seriously ill, from flying away to wintering places at the most favourable periods. The thesis on different influence of hemosporidians on energetic balance of birds during spring and autumn migrations is substantiated. Hypothesis has been advanced on the causal relationship between high bird mortality during spring migration and the most high extensiveness and intensity of their infection with hemosporidians.     

Breeding biology of the Madagascar Paradise Flycatcher,Terpsiphone mutata,with special reference to plumage variation in males

This study was undertaken to understand the migratory strategies of the Dunlins (Calidris alpina) caught in Eilat, Israel, before and after they accomplish the crossing of the combined ecological barrier of the Sinai, Sahara and Sahel deserts. Between 1999–2001, a total of 410 adults and 342 juveniles were banded. The significant difference in mean wing length between birds caught in autumn and spring reflects the degree of abrasion of the outer primaries during over-wintering in Africa. Dunlins caught in Eilat in autumn and early winter had a mean wing length 1.4–1.9mm longer than in the spring. The rate of body mass increase was comparatively high and the mean body mass of the heaviest 10% of Dunlin at Eilat was 56.2g (SE ± 0.6, N = 80). The heaviest birds from Eilat carried on average about 10g of fat with a lipid index (fat mass as a percentage of total body mass) of 18%. These reserves allow a flight of approximately 1 000km, which is probably sufficient for continued migration to more southerly wintering grounds.     

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.     

昆虫定向机制研究进展

许多昆虫具有定向运动的行为。对部分社会性昆虫和迁飞性昆虫定向行为的大量研究已经初步阐明太阳、地磁场、天体、风及地面标志物等都可能成为昆虫返巢和迁飞定向的线索。社会性昆虫具有对不同定向线索进行整合而实现精确导航的能力。日间迁飞性昆虫利用时间补偿太阳罗盘进行定向的机制亦已明确,但夜间迁飞昆虫的定向机制尚需深入研究。迁飞性害虫定向机制的明确将有助于判断害虫迁飞路径及降落区域,为迁飞害虫的准确预测提供科学依据。本文对昆虫的定向机制研究进展进行了综述。     

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.     

Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia)

Bird migration requires high energy expenditure, and long-distance migrants accumulate fat for use as fuel during stopovers throughout their journey. Recent studies have shown that long-distance migratory birds, besides accumulating fat for use as fuel, also show adaptive phenotypic flexibility in several organs during migration. The migratory routes of many songbirds include stretches of sea and desert where fuelling is not possible. Large fuel loads increase flight costs and predation risk, therefore extensive fuelling should occur only immediately prior to crossing inhospitable zones. However, despite their crucial importance for the survival of migratory birds, both strategic refuelling decisions and variation in phenotypic flexibility during migration are not well understood. First-year thrush nightingales (Luscinia luscinia) caught in the early phase of the onset of autumn migration in southeast Sweden and exposed to a magnetic treatment simulating a migratory flight to northern Egypt increased more in fuel load than control birds. By contrast, birds trapped during the late phase of the onset of autumn migration accumulated a high fuel load irrespective of magnetic treatment. Furthermore, early birds increased less in flight-muscle size than birds trapped later in autumn. We suggest that the relative importance of endogenous and environmental factors in individual birds is affected by the time of season and by geographical area. When approaching a barrier, environmental cues may act irrespective of the endogenous time programme.     

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.     

Circadian flight schedules in night-migrating birds caught on migration

Many species of migratory birds migrate in a series of solitary nocturnal flights. Between flights, they stop to rest and refuel for the next segment of their journey. The mechanism controlling this behaviour has long remained elusive. Here, we show that wild-caught migratory redstarts (Phoenicurus phoenicurus) are consistent in their flight scheduling. An advanced videographic system enabled us to determine the precise timing of flight activity in redstarts caught at a northern European stopover site during their return trip from Africa. Birds were held captive for three days in the absence of photoperiodic cues (constant dim light) and under permanent food availability. Despite the absence of external temporal cues, birds showed clear bimodal activity patterns: intense nocturnal activity alternating with diurnal foraging and resting periods. The onset of their migratory activity coincided with the time of local sunset and was individually consistent on consecutive nights. The data demonstrate that night-migrating birds are driven by autonomous circadian clocks entrained by sunset cues. This timekeeping system is probably the key factor in the overall control of nocturnal songbird migration.