S40.1: Migratory orientation: Learning rules for a complex behaviour

1Department of Biological Sciences, University at Albany, State University of New York, Albany, New York 12222, USA, fax 518 442 4767, e-mail kpa@csc.albany.edu

Long-distance migration is one of the most complex and risk-prone tasks performed by birds. For most passerine birds, especially those that migrate at night, the first migration apparently takes place without the aid of other individuals. To be successful, the young bird must combine a variety of congenital information with experience during the first few months of life to obtain all of the skills necessary to reach an appropriate locale in which to spend the winter. The bird must migrate at the proper time of year, it must fly in an appropriate direction for an approximately correct distance, know where or when to cease migrating, and be able to find its way back to the breeding range of its population. In this paper we will focus on the orientation component of migration: how does the bird know which direction to migrate and what mechanisms does it employ to identify those directions? We will illustrate the points with data from our experiments performed with the North American Savannah Sparrow Passerculus sandwichensis (Able & Able 1996), a typical nocturnal migrant, and with the results of experiments performed on a variety of other species.

Orientation in nocturnal migrants is based upon three known compass mechanisms: a magnetic compass, star pattern compass and a compass based on patterns of polarised skylight. One can only speculate about the selection pressures that favoured the evolution of multiple compasses (Terrill 1991), but their existence provides birds with a potentially useful redundancy of orientation machinery and with the possibility of pooling information from the different sources (Wiltschko & Wiltschko 1994). The development of functional compasses in young migrants is based upon the interplay of apparently genetically-programmed information with a suite of innate learning rules. The congenital information becomes combined, via these learning rules, with relevant environmental stimuli to produce functional compasses that not only confer effective orientation ability, but also provide a degree of plasticity in orientation behaviour that enables the birds to respond to spatial and temporal variability in orientation information in ways that may provide a survival advantage.

A considerable volume of work has shown that hand-raised migrants held in captivity exhibit migratory behaviour characterised by orientation directions and timing characteristic of free-living conspecifics from the same populations (summarised by Berthold 1996). Hypothesising that migratory behaviour was based on endogenous time and directional programmes, Schmidt-Koenig (1973) termed the phenomenon vector-navigation. Experiments performed with Blackcaps Sylvia atricapilla showed that hand-raised birds from eastern Europe showed population-typical southeastward directions in orientation cages, whereas those from farther west showed the expected southwestward direction (Helbig 1991). Captive-bred hybrids between the two populations oriented in nearly intermediate directions. A similar degree of genetic control was demonstrated in the orientation directions selected by Blackcaps that migrate from central Europe to the British Isles for the winter (Helbig et al. 1994). Several European migrants also exhibit characteristic changes in direction during the course of migration (e.g. those that migrate to Africa around the western end of the Mediterranean Sea first fly southwestward and later turn to more southward or southeastward directions). These changes in direction also appear to be under genetic control (Gwinner & Wiltschko 1978; Helbig et al. 1989).

The information that comprises the directional programme of vector-navigation appears to be genetically coded in at least two ways in newborn migratory songbirds. The direction of the first migration is represented with respect to the magnetic field and with respect to the axis of celestial rotation (Wiltschko et al. 1987), but the information coded seems to be somewhat different for the two sets of cues. The development of functional compass capabilities is known to involve several complex interactions among these information systems and experience during the first three or so months of the bird’s life.

Young birds that grow up isolated from any exposure to visual orientation information (daytime or night sky) still develop a magnetic compass capability sufficient to enable them to orient in the appropriate migration direction with respect to the magnetic field (summary in Wiltschko & Wiltschko 1995). Population-specific migration directions are coded with respect to the magnetic field (Weindler et al. 1996). In several European and one Australian species in which migration routes include large changes in direction, the vector-navigation programme also contains the necessary information to enable the birds to execute those changes in orientation when raised and tested only in the presence of the magnetic field (Gwinner & Wiltschko 1978; Helbig et al. 1989; Munro et al. 1993). Studies of the Pied Flycatcher Ficedula hypoleuca, which shows a shift in the direction of autumn migration from southwestward early in the season to southeastward later, indicated that the expected change in direction occurred only if the birds experienced a change in the ambient magnetic field that would have been experienced as they migrated to lower latitudes (Beck 1984; Beck & Wiltschko 1988). These data suggest a complex interaction between the endogenous temporal programme and some parameter of the magnetic field: only when the 'expected' magnetic field condition is experienced at the proper time does appropriate orientation occur.

The data available indicate that a quite substantial amount of ecologically appropriate orientation behaviour can develop in birds whose experience is limited to growing up in a magnetic field with properties similar to that of the earth. Development of a functional magnetic compass capability might be restricted to a range of magnetic field intensities similar to those found on the earth (Wiltschko 1978), and the inclination or dip angle of the field may also affect the resultant magnetic orientation (Weindler et al. 1995, 1998).

The migratory compasses based on visual information also develop during the months prior to the first migration. Many species of nocturnally migrating songbirds possess compasses based on star patterns and patterns of polarised skylight at dawn and dusk. Classic experiments by Emlen (1970; Wiltschko et al. 1987) showed that configurational star patterns acquire learned directional meaning from the axis of stellar rotation. Once this learning process has been completed, rotational information is no longer required, and the static relationships between stars are sufficient for meaningful orientation: birds that have reached migratory age and been exposed to stellar rotation when young can orient under stationary planetarium skies. This process seems to be guided by some innate rules. Birds are apparently predisposed to pay attention to the movement of celestial objects and to identify the center of celestial rotation (true north). This information is then interpreted in light of a rule that translates the genetically coded migration direction into this frame of reference, e.g. fly away from the center of rotation.

Visual information at sunset provides important compass information for many species of nocturnal migrants (Moore 1987; Able 1993; Wiltschko et al. 1997). Polarised skylight patterns, rather than the sun itself, seem to provide the relevant directional information (Helbig 1990a, 1991). During daytime, these patterns of polarised skylight apparently provide the relevant stimulus from which celestial rotation is assessed, but it is not yet clear whether the birds directly observe the dynamics of rotation or locate the pole point by observing static patterns of polarised light, e.g. at dawn or dusk (Phillips & Waldvogel 1988; Able & Able 1990a, 1995a). Similar to the star pattern compass, once the pattern of celestial rotation has been learned, birds are able to determine orientation directions essentially instantaneously from static polarised skylight patterns just after sunset (Able 1989).

These visual compasses appear to develop to an extent at least sufficient to enable a bird to identify its general migration direction even if the birds never have experience with the visual orientation cues in the presence of magnetic information (but see Katz et al. 1988). Savannah Sparrows reared outdoors in a vertical magnetic field (no directional information) oriented southwestward when tested just after sunset (also in a vertical magnetic field) (Able & Able unpublished data), and Pied Flycatchers reared under similar conditions oriented in the same direction as controls under stars (Bingman 1984). Further evidence of the general independence of the development of visual compasses from magnetic influence comes from experiments in which birds have been raised with exposure to natural and artificial visual orientation cues only within shifted magnetic fields. In all such cases, stellar or sunset orientation was unaffected by rearing in the shifted field (Bingman 1984; Wiltschko 1982; Wiltschko et al 1987; Able & Able 1997). Whereas the evidence indicates that at a coarse level, the ontogeny of visual compasses is immune to magnetic influence, recent experiments have shown that more subtle interactions are occurring in at least one species (see below).

Two types of interactions of cue systems and innate information have been identified during the development of compass capabilities. The first involves the transfer of information about the population-specific details of migration direction from one cue system to another. As noted above, Weindler et al (1996) found that in hand-raised Garden Warblers Sylvia borin, the innate information indicating that southwest is the initial direction of autumn migration seems to be coded only with respect to the magnetic field. Birds exposed to rotating artificial stars in a vertical magnetic field hopped toward south; those exposed to the same sky in the presence of the magnetic field oriented in the expected southwestward direction typical of the population. This result suggests that the migration direction coded with respect to celestial rotation may be only a general one, e.g. away from the centre of rotation. The more specific directional information exists initially only with respect to the magnetic field, but under normal conditions is transferred to visual cues during the learning of stellar rotation. Additional experiments indicated that for this transfer of information to occur, the sense of stellar rotation must be that of the natural sky (Weindler et al. 1997). Whether similar complex and subtle processes are going on in other species is not known. In Savannah Sparrows, sunset orientation was identical in sparrows raised outdoors in a normal magnetic field and in those raised outdoors in a vertical magnetic field (Able & Able unpublished data). This suggests that in this species, no additional information not coded with respect to celestial rotation was available via the magnetic field.

The second interaction involves a transfer of information between celestial rotation (which reveals true compass directions) and the preferred magnetic direction of migration, a process referred to as calibration of magnetic orientation. In experiments with Savannah Sparrows and Pied Flycatchers, it has been found that if hand-raised birds experience celestial rotation only in a situation in which magnetic compass directions are different from true compass directions (magnetic declination), the magnetic orientation expressed during the first autumn will be altered (Bingman 1983; Bingman et al 1985; Prinz & Wiltschko 1992). The birds raised in a large magnetic declination will orient in the magnetic direction that corresponded to the appropriate true migration direction (e.g. if the expected migration direction is south and the bird’s experience was that magnetic east corresponded to true south, it will orient toward magnetic east when tested in the magnetic field without visual cues).

Experiments have shown that the visual information responsible for this calibration of magnetic orientation is celestial rotation. Stellar rotation at night (Able & Able 1990b) and polarised skylight in the daytime (Able & Able 1993, 1995a; Weindler et al. 1998) provide the necessary information about true compass directions employed in the calibration. Such primacy of true compass directions over magnetic ones provides birds that might grow up in a region of large magnetic declination with a means of bringing their various orientation mechanisms into conformity. This makes adaptive sense inasmuch as true compass directions are the ones most relevant to a migrant required to move from high to low latitudes on its first migration, and many Savannah Sparrows are born in areas with large magnetic declination wherein such developmental plasticity might be advantageous.

Varying degrees of openness and plasticity characterise migrant bird orientation mechanisms, both during early development and as functional components of an adult bird’s migratory compasses. During development, transfers of information take place, in both directions, between orientation based on visual cues and that based on the magnetic field. Based as they are upon celestial rotation, an invariant source of true compass directions, there might be no advantage in having the visual compasses remain susceptible to modification later in life. The only experimental evidence relevant to this question comes from an experiment on Indigo Buntings Passerina cyanea. An incorrect star pattern compass learned during the first summer of life was not subsequently modified when the birds were exposed to a different (and normal) stellar rotation during their second summer (Emlen 1972). More study of the time course of learning of these behaviours is needed, but this one experiments suggests the existence of a finite sensitive period for learning that may end prior to the first migration.

Of course, the potential advantages of possessing a somewhat flexible orientation system do not end with the onset of the first migration. During migration, birds may experience substantial spatial and temporal variability in the environmental information that forms the bases of their compasses (Table 1). We have tended to assume that most plasticity in orientation systems ended by the time the first migration began, but few experiments have tested this assumption. Adult as well as first-summer Savannah Sparrows, exposed to clear day and night skies within a shifted magnetic field for four days during the migration season, exhibited the same type of recalibration of magnetic orientation found in young birds during their first summer (Able & Able 1995b). By alternating the birds’ exposure between shifted and unshifted fields, we found that this calibration process may occur repeatedly over the course of a single migration season. For a species like the Savannah Sparrow that calibrates magnetic orientation in response to declination on the breeding ground, such an open-ended plasticity makes sense. Magnetic orientation calibrated to a particular value of declination in the natal area would result in orientation errors when the bird migrated into an area where declination was markedly different: the calibrated magnetic preference would no longer correspond to the correct true compass direction.

Other species do not seem to respond in the same way. For example, in the Australian Silvereye Zosterops lateralis and several European species, magnetic orientation remained unchanged following exposure to visual cues in a shifted magnetic field during the migration season. In fact, in some cases the orientation direction with respect to visual cues was altered, i.e. magnetic information appeared to calibrate orientation based on visual information (Wiltschko, et al. 1997). There may be many reasons for such differences in results and they confound our desire for generality of orientation mechanisms across species. Indeed, in terms of the basic mechanisms of compass orientation, there does seem to be broad similarity that spans a diversity of taxa and little compelling evidence for interspecies differences (Helbig 1990b). On the other hand, if birds have evolved flexible, interactive orientation behaviour as an adaptation enabling them to cope with various sorts of environmental variability, we should probably expect to discover species-specific differences as we explore ever finer details of the orientation mechanisms. All migratory birds may possess the same suite of compasses, but the details of their workings and relationships may differ in ways that reflect the evolutionary histories of the different lineages. In this particular case, Savannah Sparrows occupy a breeding range that encompasses a wide range of magnetic declination, inclination and total intensity. In contrast, across western Europe, Africa, and the small range of the Tasmanian population of the Australian Silvereye, magnetic variation is slight. The migration route of the silvereye encompasses only about 2^o of declination, and birds migrating between western Europe and Africa are unlikely to encounter magnetic declination values greater than about 10^o (versus Savannah Sparrows born at high latitudes, which might experience declination values of 50-60^o). It is perhaps not surprising that individuals of these species seem not to have evolved means of coping with conditions that neither they nor their recent ancestors has experienced.

The foregoing examples illustrate the sorts of complex interactions of innate information and programmed learning that characterise the development of compass orientation mechanisms in migratory birds. Experimental data reveal a substantial amount of apparently genetically programmed information (Table 2) and canalisation of development through a series of rules by which that information interacts with experience with stimuli to which the animals are to some degree predisposed to respond (Table 3). At the same time, the richness of the system, with its multiple compasses and susceptibility to open-ended calibration, imbues migratory orientation with a remarkable flexibility.

There are many obvious parallels between the development of migratory orientation and the ontogeny of passerine song. Although the history of experimental work in the two areas is of similar duration, the song system is much more thoroughly understood. There are a number of reasons for this. Song is a more robust and tractable behavioural assay than is migratory orientation and this facilitates behavioural studies. Secondly, major portions of the neural circuitry involved in the learning and control of bird song are known. In the case of migratory orientation, almost nothing beyond the level of the sensory receptors is known, and in the case of the magnetic field, even the receptor(s) are not fully characterised (e.g.Walker et al. 1997). In the brain itself, there is evidence that melatonin is necessary for the expression of magnetic migratory orientation, perhaps required for the transfer of the innate migratory direction into a direction with respect to the magnetic field (Schneider et al. 1994) and that the hippocampus may be somehow involved in sun compass orientation in homing pigeons (Bingman et al. 1996). There must exist dedicated brain regions in which the innate components of vector-navigation are integrated with sensory information acquired during early experience with the relevant orientation cues, analogous to the well-known centres associated with the song system. Identifying the neural substrates of migratory orientation is the route to the next major breakthrough in our understanding of this behaviour, but much work will be required to chart that path.

Our work on migratory orientation has been generously supported over the years by the National Science Foundation (grants BNS7923711, BNS 8217633, BNS 8608653, BNS 8909886, IBN 9119508, and IBN 9419644).

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