MIGRATION, NAVIGATION, AND HOMING

The prevailing view among behavioral biologists and ethologists of the 1950s was that the remarkable ability of migratory animals, especially birds, to return to the same breeding and wintering area year after year was based on innate mechanisms of orientation and navigation. Later this emphasis on hereditary control yielded to more dynamic conceptualizations of spatial-behavior mechanisms. The revised theory assigns a larger role to environmental influences and learning—experience-dependent change in behavior—in animal orientation and navigation.

Orientation

Orientation refers to a heading or directed movement that bears a specific spatial relationship to some environmental or proprioceptive reference. It is typically discussed metaphorically in terms of compass directions when the sun, stars, or the earth's magnetic field are used as orientation stimuli. Birds that migrate at night use all three of these environmental stimuli to orient their seasonal movements. Nocturnal migrants show an impressive ability to vary their response in accordance with changes of information from one orientation stimulus to another. For example, several species of birds have been shown to change their response based on experience with different ambient magnetic fields. Wiltschko and Wiltschko found that shifting the orientation of an ambient magnetic field resulted in birds' correspondingly shifting their migratory orientation. The birds likewise shifted their orientation with respect to the stars, which were not subjected to experimental shifting. This behavior suggests that birds could learn a new orientation response to the stars by using the magnetic field as a calibrating reference. Bingman and Wiltschko described similar results in birds of another species that learned a new orientation response to the setting sun based on their magnetic field experience.

But the earth's magnetic field is not always the primary calibrating orientation stimulus. Able and Able found that in one species orientation to the earth's magnetic field varied with information gleaned from celestial cues. These findings demonstrate that the migratory orientation of birds is modifiable by experience and hence, to that extent, learned.

The results described above were taken from experiments with birds that had already experienced at least one migration. Work with birds prior to their first migration has revealed that experience during their first summer may have an even larger effect on subsequent migratory behavior. Evidence suggests that migrant birds are born with an inherited disposition to orient in a particular direction with respect to the axis of celestial rotation and the earth's magnetic field. Emlen has shown that to learn a migratory-orientation response to specific star patterns, birds rely on the rotation of the night sky about its axis as a directional reference. Once directional information from celestial rotation is transferred to the star patterns during the birds' first summer, they can use the patterns as an independent source of directional information.

Surprisingly, the inherited migratory-orientation response to the earth's magnetic field can vary with a bird's first summer experience. Bingman (1983) found that varying magnetic-field experiences during the summer resulted in birds' learning different autumn migratory-orientation responses to the earth's magnetic field. The advantage of being able to change the innate orientation preference to the earth's magnetic field is that birds raised in areas of different magnetic field declination (the angular difference between magnetic north and geographic north) are still able to maintain both seasonally and geographically appropriate migratory orientation. Able and Able found that celestial rotation is the reference used by young birds to override their innate orientation response to the earth's magnetic field and learn a new response better suited to reaching their winter homes. Like experienced birds, young birds who have yet to engage in their first migration manifest learned changes in orientation behavior based on interpreting the directional relationships among a variety of environmental stimuli.

Birds are unique neither in their highly directed movements nor in their ability to learn new orientation responses. From its birth, the beachhopper (Talitrus saltator), a small crustacean that inhabits the shoreline of the Mediterranean, displays an orientation response to the sun that enables it to quickly move perpendicular to the shoreline axis in order to avoid danger. Ugolini and Macchi have shown that exposing young animals to a different environment can modify this innate orientation response. This is another example of altered orientation based on learning the spatial relationship among salient environmental stimuli, in this case sun and shoreline.

Navigation

Homing is the ability of an animal to return to some goal location or "home." Navigation is the range of spatial behavior mechanisms that facilitate homing. Traditionally, true navigation has encompassed both the ability to specify one's location in space relative to an undetectable goal location and the subsequent ability to determine a goal-oriented directional bearing.

The spatial orientation evinced by migratory birds does not necessarily involve true navigation, as was shown in Perdeck's experiments. Perdeck captured and marked thousands of starlings (Sturnus vulgaris) that were migrating through the Netherlands in autumn. The birds were then transported to Switzerland and released. An examination of the locations where the birds were subsequently recaptured revealed an important difference between adults that had already experienced one migration cycle and young birds that were migrating for the first time. Adult starlings were recovered primarily northwest of the release point. The northwesterly orientation corresponded to the direction needed to reach the birds' normal wintering homes near the northern coast of France. Therefore, the adults displayed true navigational behavior—they succeeded in determining a course from an unfamiliar location that brought them close to their traditional wintering quarters. Young birds, in contrast, were recovered primarily southwest of the release point. The southwesterly orientation corresponded to the direction required to reach the birds' winter homes from the area from which they were captured but not from the release location. Although displaying good orientation, the young birds failed to orient in a manner consistent with goal-directed, true navigation.

In addition to emphasizing the difference between orientation and navigation, Perdeck's results demonstrate the importance of experiential learning in at least some aspects of avian navigation toward a goal location. Young birds that had never been to the wintering area could not navigate a course to it. Young birds on their first migration appear to employ vector navigation, an innate disposition to fly in a certain direction for a fixed period of time in order to arrive in the general vicinity of their population's wintering range. However, it is only after experiencing their winter home that they develop the ability to navigate to it from unfamiliar locations. It appears that a similar learning process supports the ability of birds to navigate to and recognize the same breeding site year after year.

Salmon evince a similar aptitude for learning in returning to breed in their natal stream, as has been well documented by Cooper et al., who placed young coho salmon (Oncorhynchus kisutch) in a tank of water containing a specific odorant. They marked the fish and later released them into Lake Michigan. They then placed the odorant at the mouth of one stream that feeds into the lake. Sometime later, as the fish began to enter streams for breeding, the fish that had been exposed to the odorant in the tank were much more likely to enter the specially odorized stream. The fish apparently learned the characteristic odor of their stream during early development and used that information to guide their return home.

Perhaps the best-studied navigational system in animals is that of the homing pigeon. A number of distinct spatial-behavior mechanisms, nearly all of them influenced by environmental experience, govern pigeon homing. To orient in space, homing pigeons prefer to rely on the sun, but they can also have recourse to the earth's magnetic field. Wiltschko and Wiltschko have shown that sun orientation is not innate but depends on a young bird's learning the sun's path across the sky. Although they further reported that pigeons could learn to use the sun for orientation only during intervals of direct exposure to the sun, Budzynski et al. have shown that when young pigeons, like bees and other animal groups, are allowed to experience the sun for only one part of the day, that experience is sufficient for them to use the sun for orientation at any time of day.

Pigeons rely on at least two navigational mechanisms: a navigational map that they can use from distant locations where they have never been before, and landmark navigation, which they can use when they are in sensory contact with familiar environmental stimuli. In some young pigeons the ability to learn a navigational map depends on the opportunity to associate atmospheric odors with wind directions. Using fans to alter the relationship between wind direction and atmospheric odors experienced by different groups of young pigeons, Ioalé et al. raised pigeons that learned navigational maps that varied with the birds' experience of odors and wind direction.

Landmark navigation is similarly dependent on experience. Wallraff has shown that young birds confined to an outdoor aviary are able to learn a navigational map, as evidenced by their ability to orient toward home when released from a distant, unfamiliar location. Such birds are nonetheless impaired in returning home because of an inability to navigate in the vicinity of their home aviary. The lack of opportunity to fly outside their aviary rendered them unable to learn to navigate by familiar landmarks, which is important for navigation near home. Gagliardo et al. have shown that landmark navigation is at least partially based on visual information. Although the two navigational systems seem to be parts of a single learning mechanism, Ioalé et al. (for the navigational map) and Gagliardo et al. (for landmark navigation) have shown that brain lesions to the hippocampus can impair navigational map and landmark navigation under some training conditions but not others. The implications of the hippocampus research is that there is more than one kind of navigational map and more than one type of landmark navigation differing at least in the neural mechanisms that support their acquisition.

Like orientation, learning in navigation is not unique to vertebrates. Gould has shown that honey bees (Apis mellifera) can learn a familiar landmark map in a manner similar to that of homing pigeons and that they are able to use this map from locations where they have never been before as long as they can maintain sensory contact with familiar landmarks.

What is remarkable about naturally occurring spatial learning is that it often occurs in the absence of any tangible external reward. For example, what is rewarding about associating atmospheric odors with wind direction to a young pigeon enclosed in an outdoor aviary? What is rewarding about learning the sun's path? It is difficult to explain such phenomena without assuming that animals are biologically predisposed to learn spatial relationships among environmental stimuli in a rapid and efficient way without dependence on environmental reinforcement. Natural selection has seemingly endowed animals with nervous systems that predispose intrinsic reinforcement of exploration. A spontaneous proclivity to explore, therefore, is a crucial element in most learned spatial behavior.

See also:SPATIAL LEARNING: ANIMALS

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Verner P.Bingman