S15.3: Behavioural ecology of migratory orientation

Department of Animal Ecology, Lund University, Ecology Building, S-223 62 Lund, Sweden, fax 46 46 2224716, e-mail Roland.Sandberg@zooekol.lu.se & Susanne.Akesson@zooekol.lu.se

Recent investigations concerning the behavioural basis of orientation systems of migratory birds have revealed a complicated web of interactions with physiological status and other ecological factors. Although migration allows individual birds to take advantage of different habitats as environments change seasonally (e.g. Alerstam and Enckell 1979; Alerstam and Högstedt 1982; Levey and Stiles 1992), it also involves several behavioural challenges that have to be met in a timely manner to ensure survival (Alerstam and Lindström 1990). Migrants must deal with potential costs including (a) high-level energetic demands of flight (Blem 1980; Pennycuick 1989; Norberg 1990), (b) foraging in unfamiliar habitats which may lead to increased exposure to predation (Lindström 1990; Moore 1994), (c) competition with other individuals at stopover sites which may result in impaired food acquisition (Hansson and Pettersson 1989; Moore and Yong 1991), (d) weather variations that influence energetic costs of flight, the maintenance of preferred headings and mortality en route (Richardson 1978, 1990; Alerstam 1981) and (e) the risk of orientation errors (Alerstam 1988, 1990).

In this paper, we consider the available experimental evidence concerning the influence of several ecological factors on the migratory orientation behaviour of birds. In doing so, we will attempt to answer the following questions: (1) How do the energetic stores of migrants influence the decision to embark on migration and the subsequent choice of a migratory direction? (2) How does the accessibility of different orientation cues affect directional choices (e.g. under clear skies and complete overcast)? (3) Do orientation behaviour and directional accuracy differ between experienced (old) and inexperienced (young) migrants? (4) How do migratory habits (i.e. long-distance vs. short-distance migrants) affect the orientation behaviour of migrants? (5) How is the integration of different directional information tied to the ecological context (i.e. migratory situation)?

One of the most important requirements during migration is to meet energetic demands, particularly in relation to the crossing of ecological barriers (Wood 1982; Bairlein 1985; Biebach 1985, 1990; Biebach et al. 1986; Moore and Kerlinger 1987; Safriel and Lavee 1988; Dolnik 1990; Kuenzi et al. 1991). Migratory birds, especially when facing a barrier crossing, are expected to show well-oriented activity in the seasonally appropriate direction only if they have deposited adequate fat stores for long-distance flights. Individuals carrying insufficient energy stores should either suppress migratory activity if stopover conditions are benign (i.e. stay on their current location, cf. Moore and Kerlinger 1991; Sandberg et al. 1991; Yong and Moore 1993; Sandberg and Moore 1996) or, if feeding opportunities are restricted, reorient in search of more profitable feeding areas (Alerstam 1978; Terrill and Ohmart 1984; Lindström and Alerstam 1986; Sandberg et al. 1988a, 1991; Sandberg 1994; Åkesson et al. 1996; Sandberg and Moore 1996).

Recently, clear-cut evidence was presented by Sandberg et al. (1991) who performed free-flight release experiments where Robins Erithacus rubecula were released singly 1-2 h after local sunset. The birds which were carrying a small chemiluminescent lightstick were tossed into the air much in the same way as homing pigeons. Released birds were then followed by using 10x40 binoculars until they vanished from sight (for further details on methods, see Sandberg et al. 1991). The results show that the amount of stored fat has a strong effect on the birds' decision to take off on migratory flights or not (Fig. 1). Robins with high fat levels were significantly more likely to embark on autumn migration flights than were individuals with low fuel stores. This result has been confirmed in similar release experiments with Red-Eyed Vireos Vireo olivaceus where 38% of the lean birds decided to stay on their current location whereas 100% of the fat birds took off on migratory flights in the seasonally appropriate direction (Sandberg & Moore 1996). Furthermore, in those few cases when lean birds actually flew away from the release site, they most often reoriented in directions roughly opposite to the seasonally appropriate (Sandberg et al. 1991, Sandberg and Moore 1996). Finally, in orientation cage tests with Red-eyed vireos, fat individuals were significantly more inclined to display migratory activity (81%) than were lean birds (61%; Sandberg & Moore 1996).

The influence of varying amounts of energetic stores on the migratory orientation of birds has received surprisingly little experimental attention. Able (1977) performed a study on a number of different North American warblers, using Emlen-funnels (cf. Emlen and Emlen 1966), and showed that the amount of visually estimated fat stores did not affect the quantity of migratory activity in orientation cages, but had a pronounced effect on the concentration of directional selections (i.e. fat birds were well oriented whereas lean individuals were not). Reoriented autumn migration, more or less in the opposite direction relative to the seasonally appropriate, is not uncommon when landbirds encounter an ecological barrier (e.g. Able 1977; Alerstam 1978; Richardson 1978; Bruderer and Jenni 1988; Sandberg et al. 1988a; Åkesson et al. 1996). Such a behaviour may constitute an adaptive response which permits migrants to search from profitable stopover sites away from densely populated coastal areas (avoidance of competitors and predators; cf. Alerstam 1978).

Recent experimental evidence for a clear connection between the amount of stored fat and directional selections stem from orientation cage studies using Robins (Sandberg et al. 1988a; cf. also Sandberg 1994), Chaffinches Fringilla coelebs (Bäckman et al. 1997), Red-eyed Vireos Vireo olivaceus (Sandberg and Moore 1996) and Snow Buntings Plectrophenax nivalis (Sandberg et al. 1998). For example, Snow Buntings tested in high arctic Canada (Resolute; Cornwallis Island) during the autumn migration period showed distinct differences in preferred mean orientation between fat and lean birds (Fig. 2; Sandberg et al. 1998). Similar clear-cut evidence has been obtained in free-flight release experiments with Pied Flycatchers Ficedula hypoleuca (Sandberg et al. 1991) and Red-eyed Vireos (Sandberg and Moore 1996).

Radar and ceilometer studies have demonstrated that fewer birds embark on migration under solid overcast as compared to clear skies (e.g. Richardson 1978). Furthermore, with access to sunset and/or stellar information, birds usually orient in the expected direction for the season, even into headwinds, whereas migrants often seem to have difficulties in selecting a seasonally appropriate direction under solid overcast, and instead opt for downwind headings (Able 1978, 1980, 1982a,b).

Several experimental studies, including free-flight release experiments and orientation cage studies, have confirmed the importance of access to visual celestial cues for seasonally appropriate and well-oriented behaviour (e.g. Emlen and Demong 1978; Able et al. 1982; Sandberg 1991; Sandberg et al. 1991; Åkesson 1993,1994). For example, Robins released under clear autumn skies in South Scandinavia managed to select a well-defined mean direction towards the expected SW direction, in good agreement with available ringing data (Fig. 3, left diagram; Sandberg et al. 1991). In contrast, autumn releases under complete overcast resulted in strikingly different headings (Fig. 3, right diagram) with a significant cluster of vanishing bearings in the downwind direction. Moreover, the Robins required significantly longer time to select their vanishing directions in the absence of visual cue information. Studies performed by using orientation cages covered with white diffusing Plexiglass to simulate complete overcast conditions commonly result in random orientation and/or high angular dispersion of directional choices (Åkesson 1993, 1994), but not consistently so (cf. Sandberg and Pettersson 1996). Interestingly, visual information low over the horizon during the twilight period seems to be important for seasonally correct orientation. Robins tested in orientation cages with access to either 90° or 160° field of vision, centered around zenith, displayed significantly different orientation behaviour. When tested with a restricted field of vision (90° ) the Robins chose headings almost directly towards the position of the setting sun whereas individuals with more unrestricted visual access to the lower parts of the twilight sky oriented in their expected autumn migration direction (Sandberg 1991).

Yearling migrants are presumed to fly along inherited directions for an endogenously controlled time period (the so-called 'clock and compass hypothesis') to reach their population-specific wintering grounds during the first autumn migration, whereas second-year birds and adults in all seasons may use some form of bi-coordinate navigation to reach their migratory destinations (reviewed by: Berthold 1988, 1991; but see Rabøl 1985). Innate programs, of course, do not preclude an importance of experience. Conditions encountered en route and experiences during previous migratory journeys may modify orientation behaviour and play a role in the regulation of bird migration (Ketterson and Nolan 1985, 1988; Gauthreaux 1982; Terrill 1988). Migratory experience may affect the integration of different orientation cues in the determination of a direction (Keeton 1980; Sandberg 1990; Wiltschko 1991) as well as the maintenance of a preferred heading (Moore 1984; Able and Bingman 1987; Alerstam 1990; Sandberg et al. 1991).

Reports on orientation errors in the literature almost exclusively refer to migratory naive (inexperienced) birds on their first autumn migration (Drury and Keith 1962; Able 1977; Ralph 1978; DeSante 1983). This is further stressed by the fact that 'vagrancy' is most often connected with young birds found in coastal areas, far off their normal migration route (Alerstam 1990). Orientation errors could result from either an inability to follow a consistent compass course within a migratory season (disorientation), or from a failure to select the correct species-specific migratory direction (misorientation) (DeSante 1983; Alerstam 1990). Observed variability in the compass orientation of a population is a composite function of variation within and between individuals (Moore 1985). Individuals that consistently select seasonally appropriate headings would be at a selective advantage, especially in the light of the possibly dire consequences associated with orientational errors (Ralph 1978, 1981; Alerstam 1988, 1990).

Yearling migrants are more likely to become misoriented than adult birds (DeSante 1983; Ralph 1978; Williams and Williams 1978), and directional selections of juveniles often show greater angular dispersion than those of adults (e.g. Rabøl 1978; Moore 1984; Fransson 1986; Hedenström and Pettersson 1987; Sandberg 1990). For example, Sandberg et al. (1988a) reported that juvenile autumn migrating Robins showed a significantly larger scatter of headings than adults when tested in orientation cages at twilight. Similarly, in both Robins and Pied Flycatchers, adults displayed more concentrated vanishing directions than yearling birds during free-flight release experiments in southern Scandinavia (Sandberg et al. 1991). In Fig. 4, we have compiled ringing recovery data for Pied Flycatchers and Reed Warblers Acrocephalus scirpaceus, two intercontinental migrants, both of which show significantly greater angular dispersion of migratory directions for first-year birds as compared to adults.

Are there any differences in the concentration of preferred headings between intercontinental (long-distance) and intracontinental (short-distance) migrants? This question has received little, if any, attention in the scientific literature. The ample availability of ringing data, especially on Palaearctic migrants, makes it possible to investigate whether there are any differences in the orientation behaviour between long-distance and short-distance migrants.

In Fig. 5, we have analysed ringing data for two intracontinental migrants, the Song Thrush Turdus philomelos and the Reed Bunting Emberiza schoeniclus. There were no significant differences in either directional choices or in the concentration of mean orientation between adults and first-year birds. However, if we compare the concentration of headings between adult Pied Flycatchers and Reed Warblers (intercontinental migrants; cf. Fig. 4) with adult Song Thrushes and Reed Buntings, we find that long-distance migrants show significantly more concentrated orientation behaviour (t₃>2.8, P<0.001 in all four comparisons according to the 'test for the homogeneity of contration parameters'; Mardia 1972) than do intracontinental migrants (compare Fig. 4 and Fig. 5). Is this an adaptation to compensate for the inevitably higher risks of accumulating orientation errors during long-distance, intercontinental migration flights?

Orientation cage experiments have demonstrated that both diurnal and nocturnal migrants are capable of using directional information from a variety of different environmental sources to select an appropriate compass course for their migratory movements (reviewed by: Moore 1987; Wiltschko and Wiltschko 1991). The orientation behaviour of migrating birds is characterised by complex interrelated mechanisms and flexibility in the use of directional information from the sun, the skylight polarisation patterns, mainly during twilight periods, the rotation of the starry sky and the geomagnetic field (e.g. Baker 1984; Moore 1987; Wiltschko and Wiltschko 1991; Able 1993). The priority and use of different available orientation cues may vary depending on the ecological context within which a migrant finds itself (Sandberg et al. 1988a, b; Sandberg 1991; Pettersson et al. 1991; Åkesson 1993; Sandberg and Moore 1996).

For example, Sandberg et al. (1988a) tested Robins which were captured at two nearby stopover sites in southern Sweden (Falsterbo: 55° 23'N, 12° 50'E and Ottenby: 56° 12'N, 16° 24'E) and showed that birds which arrived on the south-westernmost coast of Sweden (Falsterbo), by overland migration, were lean and temporarily reoriented northwards in unmanipulated orientation cage tests rather than in the expected seasonally appropriate southwesterly direction, which would have brought them across the Baltic Sea. In contrast, Robins that interrupted their flight across the Baltic Sea (presumably originating from Finland) to stopover at Ottenby, on an island in southeastern Sweden, had on average significantly larger fat stores than Falsterbo birds and oriented their migratory activity in the expected southwesterly direction (see also Moore and Kerlinger 1991). In addition to the distinct differences in behaviour under normal geomagnetic field conditions, Ottenby Robins responded to experimental deflections of the geomagnetic field, whereas Falsterbo birds failed to do so, thus indicating a context dependent use of different available orientation cues.

These results have been confirmed in a recent study on the orientation behaviour of Red-eyed Vireos which seemed to integrate geomagnetic information more readily if they were physiologically prepared to cross the Gulf of Mexico (adequate fat stores for a barrier crossing), most likely as a hedge against the possibility of encountering adverse weather like complete overcast and fog while en route (Sandberg and Moore 1996). Considering these results, we argue that migrants are especially sensitive to the availability of directional information when confronted with ecological barriers because of the dire consequences that may occur when landing possibilities are restricted by inhospitable terrain (se also Alerstam 1988, 1990).

We have attempted to, based on available experimental evidence, bring to the attention the importance of ecological factors in the orientation system of migratory birds. Although endogenous mechanisms are thought to control several aspects of a migrants' physiology and behaviour (e.g. Berthold 1990) such as: the circannual pattern of body mass change, including fat deposition, onset and cessation of migratory activity and seasonally appropriate orientation, it is by no means precluded that external factors may modify migratory behaviour in important ways.

In a number of recent studies, it has been shown that the amount of stored fat play an important role when migrants decide whether or not to embark on migratory flights (e.g. Sandberg et al. 1991; Sandberg and Moore 1996). Furthermore, fat stores can be used to predict whether an individual migrant will select a seasonally appropriate migratory direction or engage in reoriented movements (e.g. Sandberg 1994; Bäckman et al. 1997; Sandberg et al. 1998). Reoriented migration is especially conspicuous during autumn migration when landbirds encounter an ecological barrier for the first time and highlights the complicated web of interactions between energetic status and ecological context in the orientation system of intercontinental migrants.

Not only do birds have to be adequately prepared in terms of energy stores, but long-distance, nonstop flights across ecological barriers pose several challenges to their orientation capacity. We argue that migrants are especially sensitive to the availability of directional information when about to cross an ecological barrier. Several studies have indicated that landbird migrants integrate geomagnetic information more readily into their orientation system while in the process of negotiating a sea passage (Sandberg et al. 1988a, b; Sandberg and Moore 1996; Bäckman et al. 1997). Since orientation errors may have especially dire consequences during barrier crossings where landing possibilities are restricted or completely absent, geomagnetic information may assume greater importance, most likely as a hedge against the possibility of encountering adverse weather en route (e.g. complete overcast, fog), than during overland migration (see also Alerstam 1988, 1990). Clearly there is a need for comparative field studies at inland and coastal sites to disentangle the relative importance of ecophysiological factors and migratory situation in the migratory orientation system of birds (cf. Sandberg 1991; Ehnbom et al. 1993).

Experienced (old) migrants have repeatedly been shown to orient within significantly more narrow limits (less inter-individual scatter in directional choices) than inexperienced birds (Rabøl 1978; Moore 1984; Sandberg et al. 1991). This indicates that old birds are less likely to make orientation errors. The fact that first-year migrants show a higher variability in directional choices suggests either that stabilising selection operates to maintain the orientation within narrow limits (cf. Rabøl 1978), or that adults orient with higher precision due to experience. En route experience, including stopover and winter site attachment, may explain why the orientation performance of adult birds differs fundamentally from that of first-year migrants (see Alerstam 1990).

Given that orientational accuracy differs between experienced and inexperienced migrants, we found it worthwhile to investigate whether there might be a similar difference between long- and short-distance migrants. The rationale behind this being that the longer the migratory distance, the greater the need for orientational precision since even small orientation errors may accumulate in a way that threatens survival. We did indeed find that intracontinental migrants displayed significantly more scatter in their directional choices as compared to intercontinental migrants (but see Åkesson 1993). Admittedly, the number of samples are small, but we find this little used approach interesting and worthy of consideration in future analyses of bird orientation systems.

This study was supported by grants from the Swedish Natural Science Research Council (NFR) and the Swedish Foundation for International Cooperation in Research and Higher Education (STINT) to R. Sandberg, and from NFR to S. Åkesson.

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Fig. 1. Free-flight release experiments with Robins during the autumn migration period in South Scandinavia showing the relationship between the amount of fat stores carried by released birds (visual fat scoring according to Pettersson and Hasselquist (1985)) and the motivation to migrate. The proportion of successful (birds that took off on migratory flights) and unsuccessful (birds that landed) releases are shown for different fat class categories (fat classes with few data have been pooled). Fat Robins were significantly more likely to embark on migration than were birds with low fuel stores (c ²=17.9, df.=2, P<0.001). Modified after Sandberg et al. 1991.

Fig. 2. Autumn orientation of Snow Buntings under clear sunset skies at Resolute in the Canadian Arctic. Results of orientation cage experiments under unmanipulated clear sky control conditions, subdivided into lean (visually estimated fat classes 0-3; top diagram) and fat (fat classes 4-6; bottom diagram) birds. The mean sunset position is indicated outside each circular diagram. Similarly, the direction towards geographic north (gN=360° ) is shown. Each symbol on the periphery of the diagrams represents the mean heading of one individual. The mean vector (a ) of each sample is illustrated by an arrow surrounded by the 95% confidence interval (shaded). Arrow lengths are proportional to the mean vector length (r) and are drawn relative the radius of the circles (radius=1). Significance levels (P) are according to the Rayleigh test (Batschelet 1981). The mean orientation of lean and fat birds were significantly different according to the 'one-way classification test' (F_1,26=21.2, P<0.001; Mardia 1972). Based on Sandberg et al. (1998).

Fig. 3. Vanishing directions of Robins released under clear skies (left diagram) and under complete overcast (right diagram) during autumn migration in South Scandinavia. Wind directions (towards which the wind was blowing) and velocities during the release experiments are shown outside the diagrams, where relevant. The results reveal significantly different orientation behaviour under clear skies and solid overcast, respectively (P<0.001, one-way classification test, Mardia 1972). Other details as in Fig. 2. Modified after Sandberg et al. (1991).

Fig. 4. Circular distributions of ringing recoveries of autumn migrating Pied Flycatchers (top row) and Reed Warblers (bottom row), two intercontinental migrants. Left column shows recoveries of adult birds while the right column shows the corresponding data for first-year migrants. The shortest spoke in each diagram represents the recovery direction of one individual. P_c denotes significance values when the concentration of mean directions were compared between adults and first-year birds (test for the homogeneity of concentration parameters, Mardia 1972). The data is based on annual reports 1972-1986 from the Bird Ringing Centre, Swedish Museum of Natural History. For further details, see Figs 2 and 3.