Avian Migration and Navigation

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Avian migration and navigation

What is migration?

Ornithologists typically think of migration in terms of the dramatic round-trip journeys undertaken by species that move between high and low latitudes. Even in birds, however, migrations of many types occur that vary in regularity of occurrence, duration, and distance covered. The theme that ties the various types of migration together is that they are all evolved adaptations to fluctuating environmental conditions that render some areas uninhabitable during some portion of the year.

The adaptations to fluctuating environmental conditions that render some areas uninhabitable range from irruptive movements to true migration. Irruptive movements involve irregular dispersal from an unfavorable area to a more favorable area. In contrast, true migration characteristically involves return to the place of origin when conditions improve.

Bird migration includes a broad spectrum of movements by individuals that range from irregular eruptions of individuals to the long-distance round-trip flights that we typically think of when migration is mentioned. There are between 9,000 and 10,000 species of birds and more than half of these migrate regularly. Billions of individual birds are involved in these migrations. Depending upon species, the migration might comprise a journey on foot up and down a mountain (as in some grouse), or it might involve a flight that literally spans the globe. Some species fly by day, others almost exclusively at night; some migrate alone, others in flocks that may reach immense size; many migrations involve a return, often with uncanny precision, to localities previously occupied.

In terms of sheer magnitude, the migrations of many seabirds are the most impressive. The famous Arctic tern (Sterna paradisea) nests as far north as open ground exists and migrates the length of the oceans to spend the winter in Antarctic waters, a round-trip of some 25,000 mi (40,000 km) performed every year of the bird's life. Some of the great albatrosses, such as the wandering albatross (Diomedia exulans), circumnavigate the globe by moving west to east over the turbulent oceans within the "roaring forties" latitudes south of the tips of the southern continents. Sooty shearwaters (Puffinus griseus) are extremely abundant seabirds that breed on islands deep in the Southern Hemisphere, mostly around New Zealand and the southern tip of South America. In late spring and throughout the northern summer, sooty shearwaters migrate northward and circle the basins of the northern Pacific and northern Atlantic Oceans. Flocks of many thousands of individuals may be seen along the Pacific coast of North America. By late summer they are headed back across the ocean to their distant nesting islands, having circled the ocean in the process.

Many shorebirds nest at high latitudes in the Arctic and spend the winter far into the Southern Hemisphere. Their chicks are precocial and thus require relatively little parental care. Adult birds often depart on autumn migration before juveniles, leaving the inexperienced youngsters to make their way to the wintering grounds on their own. Typically, shore-birds migrate in flocks, often at night, but also during the day when crossing large ecological barriers such as oceans, gulfs, or deserts requires extremely long flights. American golden-plovers (Pluvialis dominica) make a non-stop flight from the Maritime Provinces of Canada across the western Atlantic Ocean to South America, often flying at altitudes that exceed 20,000 ft (6,000 m). In spring, the species follows a different route northward, crossing the Caribbean and Gulf of Mexico and then heading north through the interior of North America. Its western cousin, the Pacific golden-plover (P. fulva), departs its Alaskan nesting areas and flies over the Pacific to Hawaii and beyond, performing single flights of 25,000 mi (7,500 km) or more.

Most waterfowl (swans, geese, and ducks) are shorterdistance migrants, typically nesting and overwintering on the same continent. They tend to migrate in cohesive flocks that often contain family groups and repeatedly use traditional stop-over locations to rest and refuel. Often flying both day and night, migrating waterfowl are strongly influenced by weather conditions. When the conditions are right, they can cover many hundreds of miles in a single, high-altitude flight.

Soaring birds can take advantage of a free energy-subsidy from the atmosphere. Warming of the earth's surface induces columns of rising warmer air (thermals). Hawks, eagles, vultures, storks, and cranes use this atmospheric structure by finding a thermal and then circling within the column of rising air, gaining altitude with almost no expenditure of energy. Once a substantial altitude has been reached, the birds glide

off, covering ground as their path slowly descends. After covering a considerable distance, often without the need to flap their wings, the birds need to locate another thermal and repeat the process. Under the right weather conditions, large distances over the ground can be covered with very little energetic cost. Because thermals are present only during the warmer portions of the day, soaring migrants are almost exclusively diurnal and selective in terms of the weather conditions under which they migrate.

Some common landbirds (including the passerines) migrate during daylight hours. These include swifts, some woodpeckers, swallows, some New World flycatchers, jays, crows, bluebirds, American robin (Turdus migratorius), New World blackbirds, European starling (Sturnus vulgaris), larks, pipits, some buntings, cardueline finches, and others. Most songbirds, however, migrate almost exclusively at night. Nocturnal migrants include many thrushes, flycatchers, sylviid and parulid warblers, vireos, orioles, tanagers, and many buntings and New World sparrows. Night migrants typically fly alone or in only very loosely organized flocks and because of their lesser powers of flight, most make shorter individual flights and overall migrations than larger, stronger fliers. A typical night migration under good flying conditions might encompass 200 mi (320 km) and be followed by two or three days on the ground during which the birds rest, feed, and deposit fat supplies that will fuel the next leg of the migration. Some small songbirds regularly cross the Gulf of Mexico and the Mediterranean Sea-Sahara Desert. Such flights, initiated at dusk, often require more than the night to complete, thus the birds continue to fly into the following day until a suitable landing place is reached. If bad weather is encountered, especially over water, many birds may become exhausted and perish.

The blackpoll warbler (Dendroica striata) of North America is exceptional. Weighing about 0.4 oz (11 g) at the end of its breeding season, blackpolls may accumulate enough sub-cutaneous fat in autumn to increase its body weight to approximately 0.7 oz (21 g) before departing from northeastern North America on a non-stop flight over the western Atlantic Ocean. The trip takes from three to four days to complete, and with an in-flight fat consumption rate of 0.6% of its body weight per hour, the blackpoll has enough added fuel for approximately 90 hours of flight. There is essentially no place to stop enroute and most individuals overfly the Antilles and make first landfall on the continent of South America. Their autumn journey is surely among the greatest feats of endurance in the bird world.

Why migrate?

Despite the obvious diversity in migration strategies among birds, they all represent adaptations to variability in resources and the predictability of that variability. These two variables determine to a large extent what kind of migratory behavior will evolve. Resources are the necessities of life: food, water, shelter, etc. Many animals respond to the seasonal dis-appearance of some essential resource by entering an inactive or dormant state (e.g., hibernation). Most birds, however, preadapted by the ability to fly long distances, have responded to variable resources by moving to more hospitable areas.

The more variable the resources on which a bird depends, the stronger will be the selection pressure favoring the evolution of migration. Another important consideration is the predictability with which the resources fluctuate. There is no option for an insectivorous bird such as the blackpoll warbler to spend the winter in its breeding range. Selection favoring obligatory migratory behavior will be strong because any individual that fails to migrate will not survive the winter. In more temperate areas, differences in the severity of winter from year to year might make it possible for a bird to over-winter in some years, but not in others. Selection in these less predictable environments should favor the evolution of more flexible strategies such as partial migration in which some individuals of a population migrate whereas others remain year round in the breeding area. Some fluctuations in resources do not always follow regular seasonal changes in climate. The coniferous seeds and buds eaten by various cardueline finches, such as crossbills, fluctuate not only seasonally, but also from year to year and region to region. These fluctuations may be

quite unpredictable, so migration in these species must be facultative, responding directly to local conditions. These movements are termed irruptive because large numbers of birds emigrate from the boreal forests in some years, but remain there in others. Nomadism implies that individuals are perpetually on the move. It is not clear that any bird species are truly nomadic, although birds of the desert interior of Australia are often cited as examples.

Origin and evolution of migration

Seasonal migration is found on all the continents and among species as diverse as penguins, owls, parrots, and hummingbirds. Evidence of the first origins of migration are probably lost forever, but recent phylogenetic reconstructions suggest that migratory behavior has appeared and disappeared repeatedly in avian lineages. Its first appearance may well have coincided with the acquisition of efficient long-distance flight capability. Although present patterns of migration may have been influenced by global climatic events such as glaciation, migration on a large scale probably predated these events.

There is considerable evidence that migratory behavior can appear and disappear quite rapidly in populations. House finches (Carpodacus mexicanus) introduced into the more seasonal climate of the northeastern United States from a sedentary population in southern California have evolved full-scale partial migration in fewer than 50 years. Experiments with a sylviid warbler, the blackcap (Sylvia atricapilla), have demonstrated strong genetic control over several aspects of migratory behavior. The blackcap is widespread in western Europe from Scandinavia south to areas around the Mediterranean, and island populations live on the Canary and Cape Verde Islands. This single species exhibits a wide range of migratory behavior from obligate long distance migrants in the north to non-migratory populations on the Cape Verdes. Cross-breeding of Canary Island birds with northern obligate migrants produced individuals that showed almost exactly intermediate levels of migratory activity in captivity. This activity, known as Zugunruhe or migratory restlessness, is exhibited twice a year in captive migratory birds. It is characterized by a daily rhythm in which these birds rest for a short

period in the evening and then awaken and flutter vigorously on their perches throughout much of the night.

Control of the annual cycle

Migratory behavior is an integral part of the annual cycle of those species that are obligate migrants. Like other events that occur during each year of a bird's life (e.g., molt, breeding), migration is under the control of an endogenous clock called a circannual rhythm, a clock that runs with a periodicity of approximately one year. In birds held under constant environmental conditions (constant temperature, constant dim light), the events of the annual cycle, including migratory behavior, continue to recur in the proper sequence for years. Thus, although migration in the real world is certainly influenced by ambient environmental conditions (climate, weather, food supply, changes in photoperiod), the underlying stimulus comes from within. In nature, circannual rhythms are synchronized with the real world changes in seasons through the associated systematic changes in day-length (photoperiod).

Energetics of migration

Birds are remarkably adapted to flight by virtue of a lung and air-sac system that permits maximal oxygen uptake, hollow bones and other weight-reduction adaptations, and extraordinarily efficient hemoglobin. Nonetheless, long migratory flights are extremely strenuous and energy-demanding. Gram for gram, fat is the most calorie-rich sub-stance that animals can sequester in their bodies. It provides about twice the calories per gram as a carbohydrate or protein, and oxidation of fat is a more efficient metabolic process. Fat deposition prior to migration results from changes in diet, increases in food intake, and changes in metabolism. Migratory fat is deposited throughout a bird's body, including within internal organs such as the heart and liver, but most is laid down in subcutaneous "fat bodies." The amount of fat deposited varies greatly among migratory species. Long-distance migrants and those that must cross large ecological barriers (e.g., the blackpoll warbler) deposit larger amounts of fat prior to initiating flight. Typical nonmigratory birds carry 3–5% of fat-free mass as fat; in passerine migrants this figure may reach 60–100% at the beginning of a long flight.

Once in flight, the migrant's fat deposits are depleted. Fuel stores must be replenished during a migratory stop-over before the bird will be able to execute another flight segment. The rate of fuel recovery will depend upon the quality of the habitat in which the bird lands and lays over. Typically, song-birds are able to deposit fat at rates of 2–3% per day and under optimal conditions the rate may reach 10% of fat-free body mass. Given the obvious importance of stored fat to the success of a continuing migration, finding stop-over habitat in which fuel supplies can be quickly replenished is critical to a migrant's success.

Altitude of migration and flight speed

Most bird migration proceeds at rather low altitudes, as has been revealed by radar studies. Larger, faster-flying species such as shorebirds and waterfowl tend to fly at the highest altitudes. It is usual to find them up to 15,000 ft (4,500m) or higher when migrating over land. Shorebirds on a transoceanic flight have been detected passing over Puerto Rico at 23,000 ft (7,000 m). Bar-headed geese (Anser indicus), regularly migrate over the tops of the highest Himalayas. Song-birds migrate at substantially lower altitudes. At night, most typically fly below 2,000 ft (600 m) and nearly all will be below 6,500 ft (2,000 m).

The speed at which a migrating bird makes progress over the ground depends upon how fast it flies (its air speed) and the wind direction and speed where it is flying. Most passerine migrants fly at relatively slow air speeds of 20–30 mph (32–48 km/hr). Flying in a tail wind could easily double their speed over the ground; likewise a head wind could substantially retard progress and a cross-wind could cause the bird to drift from its preferred heading direction. Waterfowl and shorebirds fly faster, with air speeds in the 30–50 mph (48–80 km/hr) range. Given the potential influence of winds on the progress and success of migration, it is not surprising that migrating birds show quite refined selectivity in terms of the weather conditions under which they initiate flight.

Orientation and navigation

One of the most remarkable things about birds, and migrating birds in particular, is their ability to return to specific spots on the earth with amazing precision. This phenomenon is termed homing. Many different kinds of animals exhibit homing ability, but the behavior reaches its pinnacle in birds where the scale of homing flights may reach thousands of miles in a long-distance migrant. Not all migratory species show strong fidelity to previously occupied places, but many do, returning year after year to exactly the same place to nest and to exactly the same place to spend the winter. How they are able to navigate with such precision over great distances is a question that we still cannot answer completely.

Many young birds on their first migration travel alone, without the potential aid of more experienced parents or other older birds. Having never been to the winter range of their population before, they are not navigating toward a precise locality, but rather toward the general region in which their relatives spend the winter. But, how do they know in which direction the wintering place lies and how far it is from their birthplace? At least some of this information is genetically coded and controlled by the endogenous circannual rhythms discussed above. This migratory program provides the young bird with information about the direction it should fly on its first migration. This can be demonstrated readily by captive nocturnal migrants during the seasons of migration when the birds become restless and active at night. Displaying a behavior known as Zugunruhe, birds placed in a circular orientation cage will exhibit hopping that indicates the direction in which they would migrate if free-flying. Cross-breeding experiments with European blackcaps from populations with quite different migration directions have shown that the bearing taken up by inexperienced first-time migrants is strongly heritable and controlled by a small number of genes. Some species have complicated migration routes involving large changes in direction. The garden warbler (Sylvia borin) and blackcap are examples that have been studied. Western European populations initially migrate southwestward toward the Iberian Peninsula and then change direction to a more southward heading that takes them into Africa. Hand-raised warblers kept in Germany for the entire season and tested repeatedly in orientation cages showed this change in direction at approximately the right time during the migration season.

It is less clear how the distance of the first migration might be coded. It is known that the amount and duration of migratory restlessness exhibited by different species and populations is correlated with the distances that they migrate and the lengths of their migration seasons, suggesting that some component of the endogenous time-based program also controls the distance migrated. However, migrants are often stopped and held up by bad weather and it is not clear how the endogenous program might adjust for these changes.

Once having bred or spent the winter in a specific place, many birds will show strong site fidelity to those places. To home to a specific site requires more than a simple direction and distance program. The animal must be able to navigate to a particular goal, compensating for errors made along the way or for departures from course caused by wind. This has been demonstrated with individuals of many species that have homed after being artificially transported to places where they have never been before. In the case of various seabirds, homing distances were thousands of miles. Animals employ a variety of different mechanisms in order to home. For short distances, a number of relatively simple strategies will work: laying down a trail that is retraced; maintaining sensory contact with the goal by sight, sound, or smell; inertial navigation; referring to learned landmarks; or even random or systematic search. But for the very large distances involved in some cases of goal navigation in birds, including long-distance homing by pigeons, some other explanation is required. The best evidence suggests that birds employ a navigational mechanism based on possessing an extensive map that provides the individual with information about its spatial location relative to its goal (home), and a compass that is used to identify the course direction indicated by the map. Obviously, neither

component will work by itself. A compass will be useless without information about the direction toward home from the map. Likewise, the map, telling the bird that home lies to the north of its present location, will also be ineffective in the absence of a compass to indicate the direction "north."

Homing pigeons, and probably other birds as well, employ a number of strategies when attempting to return to a specific goal. There is good evidence that they use information perceived during the displacement journey to the release site to determine the direction of displacement (route-based navigation). They probably also use familiar landmarks when navigating close to home. These means will be of limited effectiveness at great distances, yet even when released at unfamiliar sites hundreds of miles from their home loft, pigeons with some homing experience return directly and rapidly. Therefore, whereas pigeons may make use of various strategies when homing, it appears that a map based solely on stimuli perceived at a distant and unfamiliar location are sufficient to provide the requisite homing information.

During the last half of the twentieth century, a great deal of experimental effort was devoted to discovering the physical basis of the compass and map employed in homing navigation by birds. Interestingly, compasses have been studied primarily in migratory birds, especially those species that migrate at night, whereas the map component of navigation has been studied almost exclusively in nonmigratory homing pigeons.

Bird compasses

A compass is involved not only in map and compass navigation such as occurs when a homing pigeon is taken away from its loft; it is also a fundamental component of orientation by migrating birds. Two main experimental approaches have been used to study bird compasses. First, various manipulations have been performed on homing pigeons and their effects monitored by observing the initial flight direction taken by pigeons when they were released at distant sites. Second, orientation in migratory birds has been studied by observing captive birds in a migratory condition. These birds will hop and flutter in the intended migratory direction when placed in a circular orientation cage (a behavior known as Zugunruhe). The studies on pigeons and captive migrants revealed that birds possess several different compass capabilities.

Magnetic compass

The ability to detect the earth's magnetic field is widespread among animals and microbes. The magnetic compass in birds has been demonstrated by predictably altering the migratory orientation of birds through manipulating the magnetic field within their cages, and by altering the initial homing bearings of pigeons by changing the magnetic field around a bird's head with miniature magnetic coils. By independently manipulating the horizontal and vertical components of an earth-strength magnetic field, it has been shown that the magnetic compass of birds is not based on the polarity of the field as is our technical compass. Rather, the bird compass relies on the inclination or dip angle of magnetic field lines to determine the direction toward the pole or toward the equator. Within both the Northern and Southern Hemispheres, magnetic lines of force dip downward toward the poles, so the same magnetic compass mechanism is effective for species living within either hemisphere. Birds that cross the magnetic equator will face a problem and in two species of trans-equatorial migrants it has been shown that the birds' directional response, with respect to magnetic inclination, reverses after they experience a period in a magnetic field without inclination, simulating an equatorial field.

A magnetic orientation capability develops spontaneously in young birds. The mechanism by which birds perceive the magnetic field remains uncertain. There is experimental evidence to support a receptor based on tiny particles of magnetite located in the anterior region of the head and evidence suggesting that photoreceptive pigments in the eye provide the sensor.

Sun compass

The sun compass is found in many animals. To use the sun as a compass, of course, one must take time of day into account. Animals accomplish this because the sun compass is linked to the internal circadian clock possessed by all animals. With this time-compensation mechanism in place, a bird can orient in a given compass direction at any time of day. The link between the circadian clock and sun-compass orientation can be demonstrated by changing the bird's internal clock by confining it in a room with a light:dark cycle that differs by several hours from that outside. If this is done with a homing pigeon that is then released on a sunny day, it will make a predictable error in identifying the direction in which to fly. It will take the time indicated by its internal clock to be correct and thus misinterpret the direction of the sun. With this sort of experiment it can be shown, for example, that a pigeon will mistake a midday sun, high in the sky, for a rising or setting sun that would be near the horizon. This is because only the azimuth direction of the sun is used in sun compass orientation; the sun's elevation is ignored. Birds apparently have to learn the sun's path across the sky and that path varies considerably with latitude and with season. Once the path is learned, compass directions must be assigned to it, i.e., the pigeon must learn that the sun rises in the east, etc. There is evidence that the magnetic compass provides the compass directions that are then associated with the azimuths of the sun's path. The sun compass is the primary compass employed by homing pigeons to identify the direction that its map indicates is homeward. Its role in migratory birds is less clear, but it may be important for species that migrate at very high latitudes in the Arctic where daylight is nearly continuous and magnetic directions often unreliable.

Star-pattern compass

Night-migrating birds are the only animals known to use the stars as a compass. Once learned, orientation is based on the fixed spatial relationships among stars and groups of stars: birds can orient even under the fixed sky of a planetarium. Young birds learn the relationships among star patterns by observing the rotation of the night sky that results from the earth's rotation on its axis. In this way they are able to localize the center of rotation (Polaris) and thus true north. The innate migratory direction is coded with respect to stellar rotation in young birds.

Polarized-light compass

Most nocturnal migrants initiate flights shortly after sunset and diurnal migrants often take flight around sunrise. At these times of day, patterns of polarized skylight, resulting from the sun's light passing through the earth's atmosphere are very conspicuous across the vault of the sky. Because it is sunlight that is being polarized, the patterns of polarized light in the sky change in parallel with the movement of the sun and rotate around the celestial pole similar to stars at night. Thus observation of celestial rotation via polarized light in the sky can also reveal true north. Experiments with migrants in orientation cages in which polarized light has been manipulated and skylight polarization patterns have been eliminated show that the birds employ a polarized light compass.

Multiple compasses and interactions

It is impossible to know why evolution has endowed birds with so many compasses, but presumably it is advantageous to have back-up systems available when navigational problems such as overcast skies or magnetic anomalies are encountered enroute. The compasses appear to be related to one another hierarchically. In homing pigeons, for example, the sun compass is used preferentially whenever the sun is visible; the magnetic compass seems to provide an overcast sky back-up. In adult migrants, the relationship among compasses is somewhat less clear and there may be differences among species. Based on the information available as of 2001, the magnetic compass appears to be central to migratory orientation, providing the primary directional information. When an immediate choice of direction needs to be made, visual compasses may be used, but ultimately the birds seem to rely on their magnetic compass.

In many areas, especially at high latitudes, magnetic and geographic compass directions may differ substantially (magnetic declination). In these situations, the true or geographic compass directions will be the more reliable indicators of the directions that birds need to travel. During the development of compass capabilities in young songbirds, true compass directions identified by observing celestial rotation of stars at night and skylight polarization patterns during the day are used to calibrate the preferred magnetic migratory direction. In this way, the visual and non-visual compasses are brought into conformity.

Navigational maps

The search for the physical basis of the navigational map sense has been one of the more controversial issues in the study of animal behavior. There are currently two hypotheses to explain the map sense of birds. They may not be mutually exclusive and as is the case with the compass, birds may have more than one map to consult when faced with a navigational problem. Experimental studies of the navigational map have been confined almost exclusively to homing pigeons.

The olfactory map hypothesis is based almost entirely on work done with homing pigeons. It states that pigeons learn an odor map of the region by associating different odors with the different directions from which winds carry them past the loft. A large body of experimental evidence involving both manipulations of the pigeon's olfactory system and manipulations of the odor environment supports the odor map. Experienced pigeons seem to be able to use an odor-based map over surprisingly large distances (up to 250 mi [400 km]). How odorous substances could provide reliable spatial information while being transported in an often turbulent atmosphere has been a contentious issue. Very recently, analysis of trace gases in the atmosphere has shown that spatially stable patterns of odorants sufficient to account for the known levels of precision exhibited by homing pigeons do exist, although the odors actually used by the pigeons remain unknown.

The other hypothesis is that birds might use the earth's magnetic field as a map. Components of the magnetic field vary systematically over the earth, particularly as a function of latitude. There is good evidence that homing pigeons can detect very small differences in magnetic fields that would be required to use the information as a map (a much more challenging task than using the magnetic field as a compass). The best evidence supporting the idea of a magnetic map is indirect. Homing pigeons are often disoriented when released at magnetic anomalies—places where the earth's field is disturbed, usually as a result of large iron deposits underground. The effect occurs only when the pigeons are forced to make their navigational decisions right at the anomaly: if released outside the anomaly, they are not disturbed by flying across it on the way home. That the pigeons are disturbed even under sunny skies when their sun compass is readily available further suggests that the magnetic anomalies are somehow affecting the map step of navigation rather than the compass.

We know that migratory birds exhibit striking site accuracy and therefore must possess sophisticated homing abilities. However, very little is known about navigational maps in these species. Although many migrants return with precision to previously occupied places, we do not know whether they are really goal-orienting throughout the migratory journey or only when they get closer to the destination.

Resources

Books

Able, Kenneth P., and Mary A. Able. "Migratory Orientation: Learning Rules for a Complex Behaviour." In Proceedings of the 22nd International Ornithological Congress, Durban, edited by Nigel J. Adams and Robert H. Slotow. Johannesburg: Birdlife South Africa, 1999.

Berthold, Peter. Bird Migration. 2nd ed. New York: Oxford University Press, 2001.

Berthold, Peter. Control of Bird Migration. New York: Chapman and Hall, 1996.

Wiltschko, Roswitha, and Wolfgang Wiltschko. "Compass Orientation as a Basic Element in Avian Orientation and Navigation." In Wayfinding Behavior: Cognitive Mapping and Other Spatial Processes, ed. R. G. Golledge. Baltimore: Johns Hopkins University Press, 1999.

Wiltschko, Roswitha, and Wolfgang Wiltschko. Magnetic Orientation in Animals. Berlin: Springer-Verlag, 1995.

Periodicals

Able, Kenneth P. "The Concepts and Terminology of Bird Navigation." Journal of Avian Biology 32 (2000): 174–183.

Able, Kenneth P. "The Debate Over Olfactory Navigation by Homing Pigeons." Journal of Experimental Biology 199(1999): 121–124.

Phillips, John B. "Magnetic Navigation." Journal of Theoretical Biology 180 (1996): 309–319.

Wallraff, Hans G. "Navigation by Homing Pigeons: Updated Perspective." Ethology, Ecology and Evolution 13 (2001): 1–48.

Wallraff, Hans G., and M. O. Andreae. "Spatial Gradients in Ratios of Atmospheric Trace Gases: A Study Stimulated by Experiments on Bird Navigation." Tellus 52B (2000): 1138–1157.

Wiltschko, Wolfgang, et al. "Interaction of Magnetic and Celestial Cues in the Migratory Orientation of Passerines." Journal of Avian Biology 29 (1998): 606–617.