Orientation and Navigation
Sun compass
A crucial observation for the study of bird orientation was the directional preferences of migratory activity behavior (Zugunruhe) by Kramer (1949). Using orientation cages the amount of activity and the preferred direction can be measured. This also allows experimenting with different cues that may affect bird orientation.
That birds use the sun for orientation has first been shown by Karl Schmidt-Koenig (Schmidt-Koenig 1958, 1961). He shifted the internal clock of homing pigeons. This resulted in an expected directional error when homing to the loft. The sun is used as a compass. The brightest part of the sky, if visible, is interpreted as the sun and only the azimuth is important. Directions can be distinguished even when the sun is at elevations close to the zenit, e.g. at 87° (R. Wiltschko and Wiltschko 1999a).
At dusk and dawn, birds may use the polarization pattern of the light to determine the direction. But this is still a matter of open research (Muheim 2011).
Star compass
Sauer (1957) showed with experiments in the planetarium that birds use the stars for orientation. Indigo Buntings Passerina cyanea reversed their preferred direction in orientation experiments in a planetarium when the northern stars were reflected to the south (Emlen 1967). Birds use the stars, like the sun, as a compass. That is, they can determine a direction from the stars but they are not able to read a position from them (true navigation). In contrast to the sun compass, the star compass is independent of the internal clock. Birds need to have the ability to observe the sky before they can use the star compass. Emlen (1970) raised birds in a planetarium that rotated around an arbitrary star. These birds, when tested during migration, moved away from this star which they mistook for the rotation center. Further experiments showed that only the learned rotation center matters. There is no innate map of stars (R. Wiltschko and Wiltschko 1999a). Also, migratory birds recalibrate their star compass along their migratory route based on the magnetic compass. This is important because the star pattern change when migrating along the north-south axis.
Magnetic compass
The magnetic field seems to play a key role in the orientation of migratory birds. It looks like the birds’ innate migration direction is based on the magnetic field (R. Wiltschko and Wiltschko 1999b). That birds use the magnetic field to determine their migration direction has first been shown by Merkel and Wiltschko (1965). They tested European Robins Erithacus rubicula during spring migration in the natural magnetic field as well as in magnetic fields of which the horizontal and the vertical component respectively was reflected. Under both artificial magnetic fields the Robins preferred southern instead of northern directions. This and subsequent experiments revealed that birds can perceive the inclination angle of the magnetic field and that they are not sensitive to the direction of the field (W. Wiltschko and Wiltschko 1972). They use an inclination compass. The inclination compass is very precise: deviations of 2° from vertical can be perceived by birds in high Arctic zones (Muheim, Åkesson, and Alerstam 2003).
The ability to perceive the magnetic field is present in many organisms. Behavioral and physiological studies on taxonomically diverse animals suggest the presence of two fundamentally different, independent magnetoreception mechanisms that detect different parameters of the Earth’s magnetic field (R. Wiltschko and Wiltschko 1995). A light-dependent magnetic compass detects the axial alignment of the magnetic field, and a ferromineral-based mechanism provides positional magnetic map information (Phillips, Jorge, and Muheim 2010). However, the receptors still remain to be identified. In birds, the magnetite based mechanism is localised in the nostrils, whereas the light-dependent mechanism is localised in the retina. The function of the light-dependent orientation mechanism depends on the wavelengths of the light the bird experiences (Muheim, Bäckman, and Åkesson 2002). Birds are better oriented in short wavelength environments. Further, the neural visual system is active when nocturnally migrating passerines perform magnetic orientation (Heyers et al. 2007). However under long wavelengths, Robins were oriented well with intact nostrils but they were disoriented if the nostrils were anesthetized (R. Wiltschko et al. 2011). This indicates that they may also be able to use their nostrils for magnetic orientation when the visual system is not able to do so.
The light-dependent magnetoreception mechanism is based on radical pairs (Ritz, Adem, and Schulten 2000). Under some wavelengths, the retina produces pairs of radicals that either can spin parallel or in opposite directions. The ratio between the two spinning states depends on their orientation in the magnetic field. Therefore, birds seem to be able to “see” the magnetic field (Muheim et al. 2014).
Landmarks
That birds use landmarks to find their nest or cache where they previously stored food has been shown at a local scale for several species (e.g. Duff et al. (1998)). It is very likely that also migratory birds use landmarks, particularly for navigation (see below).
Olfactory cues
It has long been known that homing pigeons also use olfactory cues for finding the way home. There is recent evidence that also other bird species including migratory birds use smell for their orientation. Anosmic shearwaters have difficulties to find back to their colony after a foraging trip (Padget et al. 2017). Tracking Catbirds Dumetella carolinensis on their autumn migration showed that adult birds treated with zinc sulphate to produce anosmia were unable to show the same orientation as control adults, and instead reverted to a direction similar to that shown by juveniles making their first migration. Experimentally offsetting the magneto-receptors had no effect on the orientation of either adults or juveniles. These results suggest that olfactory sense may play a role in experience based migration in adult catbirds (Holland et al. 2009). The role of olfactory cues for the orientation on migration is subject to ongoing research.
Compass orientation vs. navigation
Compass orientation is the ability to move in the correct direction. Clock-and-compass orientation is the ability to move in the correct direction for a specific time (distance) so that a specific goal is reached. Compass or clock-and-compass is also called “vector navigation”. True navigation is the ability to find a specific location of the world from any actual location, i.e. it involves the ability to identify the actual location and its relative position to the destination location. The difference between compass orientation and navigation has been shown in a famous displacement experiment by Perdeck (1958). He translo-ated more than 10000 Starlings Sturnus vulgaris that were on their autumn migration from the Netherlands to Switzerland. Subsequent ring recovery locations of these translocated birds differed between adults and juveniles. Adults were found back in the normal wintering area, whereas juveniles were found further south outside of their normal winter range but in the correct migration direction from the release location. Thus adults were able to compensate for the displacement and navigate to their correct winter range, whereas juveniles proceeded migration in the correct direction without compensating for the displacement.
Migratory birds use different compass systems depending on the circumstances (Muheim, Åkesson, and Alerstam 2003). The different orientation systems can be used in parallel, hierarchically or to calibrate each other. The interplay of the different systems is very complex and yet not fully understood.
Further reading on orientation: The state of the knowledge on orientation at that time is nicely summarized and reviewed by R. Wiltschko and Wiltschko (1999a)]. A more recent review with focus on the interplay between the different compass systems and the ontogeny of orientation is given in the book by Hansson and Åkesson (2014).
Duff, S. J., L. A. Brownlie, D. F. Sherry, and M. Sangster. 1998. “Sun Compass and Landmark Orientation by Black-Capped Chickadees (Parus Atricapillus).” Journal of Experimental Psychology: Animal Behavior Processes 24: 243–53.
Emlen, S. T. 1967. “Migratory Orientation in the Indigo Bunting, Passerina Cyanea. Part II: Mechanisms of Celestial Orientation.” Auk 84: 463–89.
———. 1970. “Celestial Rotation: Its Importance in the Development of Migratory Orientation.” Science 170: 1198–1201.
Hansson, Lars-Anders, and Susanne Åkesson, eds. 2014. Animal Movement Across Scales. First edition. Oxford: Oxford University Press.
Heyers, D., M. Manns, H. Luksch, O. Güntürkün, and H. Mouritsen. 2007. “A Visual Pathway Links Brain Structures Active During Magnetic Compass Orientation in Migratory Birds.” PLoS ONE 2 (9): e937. doi:10.1371/journal.pone.0000937.
Holland, R. A., K. Thorup, A. Gagliardo, I. A. Bisson, E. Knecht, D. Mizrahi, and M. Wikelski. 2009.
“Testing the Role of Sensory Systems in the Migratory Heading of a Songbird.” The Journal of Experimental Biology 212 (Pt 24): 4065–71.
https://doi.org/10.1242/jeb.034504.
Kramer, G. 1949. “Über Richtungstendenzen Bei Der nächtlichen Zugunruhe Gekäfigter vögel.” In Ornithologie Als Biologische Wissenschaft, edited by E. Mayr and E. Schütz, 269–83. Heidelberg: Heidelberg.
Merkel, F. W., and W. Wiltschko. 1965. “Magnetismus Und Richtungsfinden Zugunruhiger Rotkehlchen Erithacus Rubecula.” Die Vogelwarte 23 (1): 71–77.
Muheim, Rachel. 2011. “Behavioural and Physiological Mechanisms of Polarized Light Sensitivity in Birds.” Phil. Trans. R. Soc. B 366: 763–71.
Muheim, Rachel, Susanne Åkesson, and Thomas Alerstam. 2003. “Compass Orientation and Possible Migration Routes of Passerine Birds at High Arctic Latitudes.” Oikos 103: 341–49.
Muheim, Rachel, J. Bäckman, and Susanne Åkesson. 2002. “Magnetic Compass Orientation in European Robins Is Dependent on Both Wavelenght and Intensity of Light.” Journal of Experimental Biology 205: 3845–56.
Muheim, Rachel, Jannika Boström, Susanne Åkesson, and Miriam Liedvogel. 2014. “Sensory Mechanisms of Animal Orientation and Navigation.” In Animal Movement Across Scales, edited by Lars-Anders Hansson and Susanne Åkesson, 179–94. Oxford: Oxford University Press.
Padget, O., G. Dell’Ariccia, A. Gagliardo, J. González-Solís, and T. Guilford. 2017.
“Anosmia Impairs Homing Orientation but Not Foraging Behaviour in Free-Ranging Shearwaters.” Scientific Reports 7 (1): 9668.
https://doi.org/10.1038/s41598-017-09738-5.
Perdeck, A. C. 1958. “Two Types of Orientation in Migrating Starlings, Sturnus Vulgaris l., and Chaffinches, Fringilla Coelebs l., as Revealed by Displacement Experiments.” Ardea 46: 1–37.
Phillips, John B., Paulo Esteves Jorge, and Rachel Muheim. 2010.
“Light-Dependent Magnetic Compass Orientation in Amphibians and Insects: Candidate Receptors and Candidate Molecular Mechanisms.” Journal of the Royal Society Interface 7: S241–56.
https://doi.org/10.1098/rsif.2009.0459.focus.
Ritz, T., S. Adem, and K. Schulten. 2000. “A Model for Photoreceptor-Based Magnetoreception in Birds.” Biophysical Journal 78: 707–18.
Sauer, F. 1957. “Die Sternorientierung nächtlich Ziehender Grasmücken Sylvia Atricapilla, Borin Und Curruca.” Zeitschrift für Tierpsychologie 14 (1): 29–70.
Schmidt-Koenig, K. 1958. “Der Einfluss Experimentell Veränderter Zeitschätzung Auf Das Heimfindevermögen von Brieftauben.” Naturwissenschaften 45: 47.
———. 1961. “Die Sonne Als Kompass Im Heim-Orientierungssystem Der Brieftauben.” Zeitschrift für Tierpsychologie 18: 221–44.
Wiltschko, R., S. Denznau, D. Gehrung, P. Thalau, and W. Wiltschko. 2011. “Magnetic Orientation of Migratory Robins, Erithacus Rubecula, Under Long-Wavelength Light.” Journal of Experimental Biology 214: 3096–3101.
Wiltschko, R., and W. Wiltschko. 1995. Magnetic Orientation in Animals. Berlin: Springer.
———. 1999a. “Das Orientierungssystem Der Voegel 1) Kompassmechanismen.” Journal of Ornithology 140: 1–40.
———. 1999b. “Das Orientierungssystem Der Voegel 2) Heimfinden Und Navigation.” Journal of Ornithology 140: 129–64.
Wiltschko, W., and R. Wiltschko. 1972. “Magnetic Compass of European Robins.” Science 176: 62–64.