Animal navigation: How animals use environmental factors to find their way
Migratory animals have innate programs to guide them to their still unknown goal. Highly mobile animals with large ranges develop a so-called navigational ‘map’, a mental representation of the spatial distribution of navigational factors within their home region and their migration route. Readers may recall that the first part was published in November issue. We present here the concluding part.
4 The course to the goal
The mechanisms of determining the course to the goal, that is, the direction that is to be pursued to reach the goal, are less well known than the compass mechanisms, although there has been considerable progress during the last decades. Again, birds, in particular homing pigeons, are the best studied group, but also marine turtles and the desert ant Cataglyphis have been studied in detail.
For most animals, a frequent task is to orient within their home range, i.e., to return to a resting place, their burrow, their nest, etc. In this case, for the first step of the navigational process, the animals have the option to use various informations collected during the outward journey. Animals that cover larger distances, e.g., birds, can also establish a learned system based on remembering the spatial distribution of several environmental factors, the so-called navigational ‘map’. Another task is to reach a yet unknown goal in migration—for this animals have to rely on innate programs.
4.1 The use of information obtained during the outward journey
When returning to a specific place, such as a burrow or a nest, animals can theoretically rely on landmarks, following the sequence of landmarks they observed during the outward journey in reverse order. Many animals have been shown to respond to landmarks, in particular in the vicinity of their nest (e.g., [125,126] a.o.). However, it is difficult to demonstrate that this strategy is used during natural movements, and clear evidence is not available. If the outward journey has not been on a straight route, following a sequence of landmarks backwards has the disadvantage that the return paths is not the most direct, but shows the same windings and detours.
Another strategy would be to record the direction of an outward journey with a compass and reverse this direction to head home. If the outward journey was not straight, but consisted of frequent changes in direction, the animal must consider the various compass directions and the respective distances of the parts of path and integrated them, to obtain the net direction of the outward journey. This strategy—path integration —has been observed in desert ants: Leaving their nest, they start to search around for food, with winding paths covering a certain area—after having found a food item, however, they carry it back to their nest on the direct route (Fig. 4). Experiments have shown that the ants use their skylight compass, integrating all the twists and turns of the outward journey (for details, see ). They also have a rather precise idea of the distance to home—after covering that distance, they start to systematically search around . Path integration may be combined with landmark memories to guide ants and bees back to their nest (see e.g., [130–132], which is a very effective, safe strategy. Little is known about other animals, but it may be assumed that many make use of this strategy.
Experiments with young, inexperienced homing pigeons indicate that for determining the heading home, they also rely on information obtained during the outward journey. The first spontaneous flights escape analysis, but young birds can apply path integration also when passively transported, using their magnetic compass to record the direction of the outward journey. Displacing them in a distorted magnetic field caused disorientation, while staying in the same distorted field after arrival at the release site had no effect —having access to magnetic compass information during displacement proved crucial. This effect could only be observed in young, inexperienced birds, however; experienced pigeons apparently change their navigational strategy and do not need this type of outward journey information any longer . Yet to what extent they may additionally use it when available is unclear.
Relying on route information and path integration is an efficient strategy over short distances, as it does not require any previous knowledge. Yet over longer distances, it has the disadvantage that small mistakes may accumulate, and there is no way to correct these mistakes relying on outward journey information alone.
4.2 Migration: reaching a still unknown goal by innate programs
Many animals start migrating immediately after they are born. With mammals like caribous or gnus and zebras, but also with whales, the young ones stay with their mothers and follow them to the regions where they have to go—here, parental guidance leads them along traditional routes. This may also apply to some bird species that migrate as families in flocks. Other young animals, however, have to start migrating alone, and they are endowed with innate programs that guide their movements.
In migratory birds, the innate program consists of directions and distances to the wintering area of their species/ population. The direction is genetically encoded with respect to the magnetic compass and celestial rotation: Birds handraised without ever seeing the sky, tested during autumn migration in cages in the geomagnetic field headed into their migratory direction ([e.g., [135,136] a.o.); they even change direction if their migration route is not straight (Fig. 5) ). Birds handraised under a rotating planetarium sky or an artificial “sky” with an arbitrary pattern of little light dots headed away from the center of rotation [122,124]. When migratory birds were caught during migration and displaced several 100 km perpendicularly to their migration route, young birds migrating for the first time continued in their migratory direction, ending up in a different region (Fig. 6)—not knowing their goal yet, they could not yet navigate toward it. Adult birds that had already stayed in the wintering area the year before, in contrast, compensated for the displacement (see below); they changed course and headed directly toward their winter quarters ([138,139] a.o.). Newly hatched marine turtle spontaneously move from the beach into the ocean, guided by visual cues, heading toward the brightest part of the sky. After having reached the water, they start swimming into the incoming waves, probably detecting their direction by their orbital movements, and later maintain this direction by their magnetic compass. Hatchling loggerheads, Caretta caretta (Cheloniidae) from Florida then enter the Atlantic gyre where the stay the next years (see  for details). Innate directional responses to certain combinations of magnetic intensity and inclination ensure that they stay inside favorable marine areas ( a.o.).
Fishes like Pacific salmons and eels migrate only twice during their life— from their birthplace to the region where they spend most of their life and later back to their birth place; they also follow innate programs for their migration. Sockeye Salmon, Oncorhynchus nerka (Salmonidae), leave their hatching site in little streams and creeks, responding to currents and heading in specific directions by magnetic and celestial cues, first to reach a nursery lake and later to migrate downstream toward the ocean (for details, see ).These innate programs are specifically adapted to the stream systems where they live . When in the ocean, specific magnetic conditions elicit swimming in particular directions to make them stay in their normal habitat . Eels, born in the ocean, migrate to spend most of their life in fresh water. European eels, Anguilla anguilla, born in the Sargasso Sea, follow the current of the Golf stream, but this passive transportation is supported by active swimming, presumably in directions indicated by their magnetic compass. When in brackish water, they enter an estuary and move upstream, swimming actively against the current for various distances into fresh water . Marine turtles as well as salmon and eels return to their birthplace to lay their own eggs. They imprint on their hatching site and store the respective conditions in their memory. Marine turtles probably rely on the local magnetic conditions , whereas salmons imprint on the odors of their natal creeks .
4.3 True navigation: use of local, site-specific information: the ‘Map’
Many animals return after passive displacement over various distances; they are capable of true navigation in the sense that they can head towards a specific goal from unfamiliar sites. The mechanisms they use are largely unknown; they have been analysis to some extend only in birds, in particular in homing pigeons.
In the middle of the last century, navigation by astronomical factors was suggested for birds: Matthews forwarded the Sun navigation hypothesis , and Sauer interpreted his planetarium results with migrants as indicating true navigation by stellar cues . The clockshift experiments (see above), however, clearly show that shifting the internal clock affects the compass only, while the bird determined their location and the home course correctly (e.g., , see above). The planetarium experiments by Emlen (, see above) identified the birds’ use of stars as compass orientation. This indicates that the factors birds use for true navigation are not astronomical, but geophysical in nature.
4.3.1 The concept of the navigational ‘map’ Pigeons return when displaced to unfamiliar distant sites from the area of their direct experience they usually leave these sites heading into directions not far from their home direction—this indicates that they can interpret the local factors more or less correctly, even if they have never been there before. It suggests that these factors have the nature of gradients—birds familiarize themselves with the course of these gradients in their home area and can extrapolate this knowledge when they are at an unfamiliar site. They compare the local values of the gradients with the remembered values from home. If a pigeon has experienced that, e.g., factor A increases toward north and at a given site it encounters values of A that are larger than within its home range, it knows that it is farther north and consequently has to head south to return. Wallraff  described this model in detail, assuming that the birds’ navigation is based on at least two, possibly more gradients that enable birds to determine their position relative to home, and from this derive the home course.
The birds’ headings often deviate somewhat from the true home direction, with these deviations being characteristic for a given site—the so-called release site biases (Fig. 7). These deviations are attributed to local irregularities in the distribution of the navigational factors ; they are normally not very large and do not prevent birds from returning—obviously, the initial error is later corrected.
The ‘map’ is a learned system, based on experience. Young birds acquire the respective knowledge during spontaneous flights in their home range. When homing pigeons are regularly released at the loft, in about their third months of life, they start to venture further away from their loft, often staying out of sight for more than an hour. It is to be assumed that during these flights they are aware of their flight directions by a compass and observe how the potential navigational factors change with distance in the various directions, thus establishing their navigational ‘map’, a directionally oriented mental representation of the spatial distribution of the navigational factors in their home region. This applies to migratory and sedentary birds alike. Young migrants roam around in their home region before their start migration—e.g., young bank swallows, Riparia riparia (Hirundinidae) from a colony at the southeastern English coast were found to move all over England, several as far north as Scotland, before they left for fall migration . A study with handraised migrants showed that only birds that had had the chance to fly around at the release site for some time could return to that region next spring; birds that had been released after the onset of migration and left right away did not come back .
While all birds probably establish a ‘map’ of their home region, migrating birds also experience the distribution of ‘map’ factors during their first migration, establishing a ‘map’ of their migration route. This is documented by the observation that from their second migration onward, migrants are able to compensate for displacements— they abandon their traditional migratory direction and head directly toward their goal—their breeding ground or wintering area (see Fig. 6)(e.g., [138,139]). Tracking displaced migrants showed that in species with long migration routes, some birds also headed to intermediate feeding areas and from there join the traditional migration route for the rest of the journey .
4.3.2 The nature of the factors included in the navigational ‘map’
The nature of the factors used for true navigation is still a largely open question. A number of factors have been suggested, among them some with global gradients like magnetic factors (see  a.o.) or gravity  , but also factors of more regional importance like infrasound  and odors (see e.g., [158,159]). Most of these con siderations involve the navigation of birds (see for review).
Magnetic factors: Magnetic factors are the ones that are best supported by experimental evidence so far. They involve total intensity and inclination, both forming global gradients running roughly north/south from pole to pole. In many parts of the Earth, the angle between the two gradient directions is sufficiently large to form a bicoordinate ‘map’ . Magnetic declination was also considered as a navigational factor , but later experiments did not support such a role [163,164].
The first indications for the use of magnetic factors came in the late 1970s from the observation that pigeons released in a strong magnetic anomaly seemed disoriented and departed in random directions ; similar findings were reported from magnetic anomalies in other regions [166–168]. The use of magnetic factors is also supported by the observation that pigeons treated with a brief, strong magnetic pulse to interfere with the receptor system for magnetic intensity (see below) showed significant deviations from untreated controls at some sites more than 80 km away . In caged migrants, the pulse caused a significant shift in direction that lasted about 3 days, followed by ca. 1 week of disorientation before the birds resumed their normal migratory headings . Treatment with such a pulse had a similar effect on freeflying migrants, but only on experienced birds; young migrants on their first migration (which is still controlled by the innate migration program) remained unaffected .
The best evidence for the use of a magnetic ‘map’, however, comes from magnetically simulated displacements. The first such experiment was performed with the spiny lobster, Panulirus argus (Decapoda), at the Florida Keys. When displaced, lobsters tested in arenas, showed directional tendencies to compensate for the displacement, heading toward the capture site. Tested at the capture site in a magnetic field as it occurs north of that site, they headed southward, whereas lobsters tested in a field as found south of that site headed northward (Fig. 8), i.e., in directions that would have brought them back from the respective sites to capture site . Similar results were obtained with green sea turtles, Chelonia mydas, at the Florida coast, tested in the magnetic fields found ca. 340 km north and south of the capture site (; see also : They, too, compensate for the simulated displacements.
Corresponding experiments with caged migrating birds likewise showed that displacements can be simulated by testing birds in a magnetic field of a distant site. Reed warblers, Acrocephalus scirpaceaus (Muscicapidae) caught during spring migration at the Kurish Spit near the Baltic Sea showed northwesterly headings toward their breeding area in Southern Finland; tested in the magnetic field of a site about 1000 km eastward, they changed this direction, now preferring northwesterly headings , just as they had had done when really displaced to that site . That is, birds, too, compensated for the virtual displacement simulated by magnetic intensity and inclination (see also ).
A magnetic ‘map’ or the involvement of magnetic components in the ‘map’ are also proposed for other animals, among them amphibians —the observations that animals as different as spiny lobsters, marine turtles and birds compensate for magnetically simulated displacements suggests that a magnetic ‘map’ may be widespread among animals.
Little is known about the sensory basis of magnetic ‘maps’. While the perception of magnetic directions in birds is based on radical pair processes and is associated with the visual system (see above), the effect of the magnetic pulse (see above) indicates that sensing the magnetic ‘map’ involves magnetite , with the duration of the pulse effect—about 10 days —suggesting superparamagnetic particles (see ). The respective information is transmitted to the brain by the trigeminal system (see [180,181] for details). Without intact trigeminal nerve, birds could not compensate for virtual displacements . How magnetic ‘map’ information is obtained by other animals remains largely unknown.
Gravity: It was considered as a possible navigational factor when the disorientation of displaced homing pigeons in magnetic anomalies was observed , because magnetic anomalies often coincide with gravity anomalies. Yet releasing pigeons in a gravity anomaly in America spoke against this possibility . Recently, however, an effect of raising pigeons in different gravities anomalies in Southeastern Europe was reported , and tracking the flight of pigeons across gravity anomalies showed increased scatter up to disorientation, together with greater losses, which was interpreted as indicating navigation by use of gravity . A possible role of gravity in avian navigation is still open.
Infrasound: Natural infrasound (frequencies below 20 Hz) arises from wind over mountains, waves on the shore, etc.; they are transported over long distances in the atmosphere and in the ground with little attenuation. Pigeons were shown to be able to hear them , hence they were considered as a potential navigational cue [186,187].
Hagstrum  analyzed large data sets of the late W.T. Keeton and found a correlation between predictions concerning atmospheric infrasound and the initial orientation of pigeons toward home. Another analysis comparing the orientation of pigeons deprived of hearing with that of untreated controls produced mixed results . Altogether, the validity of the acoustic navigation model proposed by Hagstum  is unclear, the more so since it is hardly compatible with the Map-andCompass model (see  for discussion).
Odors: The role of odors in avian navigation has been most controversially discussed so far. In the beginning of the 1970s, Papi and colleagues in Italy reported that pigeons deprived of olfaction were reluctant to take off, departed randomly, and many got lost . The authors concluded that odors are essential navigational cues and forwarded the olfactory navigation hypothesis. It assumes that birds associate airborne chemical substances with the respective wind direction, thus forming an olfactory ‘map’, which was believed to provide the most important, it not the only navigational information for birds. Numerous further experiments testing the role of olfaction in pigeon homing in various ways were conducted in the following years (for review, see [159,160,191].
Replicating the experiments with anosmic pigeons (i.e., pigeons deprived of smelling) in the USA and Germany produced different results; however (e.g., [192, 193]), further experiments indicated that the conditions of raising and training the birds were of crucial importance  for the pigeons’ response to olfactory deprivation. Experiments with migrating birds also showed that birds deprived of olfaction were unable to compensate for displacements and fell back on their innate migratory direction [195,196].
An odd aspect of the olfactory findings was that olfactory deprivation had an effect only at sites that were unfamiliar to the birds. The protagonists of the olfactory hypothesis claimed that at familiar sites, birds followed sequences of familiar landmarks (e.g., , see ). In critical tests at a familiar site, however, anosmic pigeons deprived of object vision by frosted lenses departed homeward oriented , indicating that they used non-olfactory, non-visual cues to determine their home direction. Anosmic pigeons released at familiar sites also responded to shifting their internal clock with departing in the expected, deflected direction with respect to untreated controls (see above) , showing that they did not follow sequences of landmarks, but they determined their home direction as a compass course.
In 2009, Jorge and colleagues replaced natural odors by artificial odors and got similar results as in the olfactory studies [200,201]. The authors suggested that instead of providing navigational information, odors had an activation effect, a hypothesis which was supported by electrophysiological data .This, together with the findings at familiar sites, suggests that odors may play a activating role when pigeons have to integrate new local data into their ‘map’ at an unfamiliar site (see  for a discussion). The controversy on the role of odors in bird orientation is still not finally resolved.
Salmons, however, orient by odors solved in the water when returning to their natal creeks. They have been imprinted on the chemical situation of the stream in which they were born . After spending a number of years in the ocean, they begin to return to their parental creek to spawn. When reaching the estuary of their natal river system, they swim upstream, following the imprinted odors until they reach their natal creek (see  for an overview). Here, however, odors are not used as part of a ‘map’, but as a direct cue which the fishes follow when heading upstream against the current.
4.3.3 Navigation near home: the ‘Mosaic Map’
In the vicinity of home, there is an area where birds are no longer able to distinguish the local values of the navigational factors from the home values. Here, they turn to landmarks. A study where the routes of pigeons deprived of object vision by frosted lenses were recorded showed that these birds managed to approach the loft in Upstate New York about 0.5–5 km , while in Germany many birds with frosted lenses ended up closer to the loft, within 100 m, some of them even managing to reach the loft itself . Landmarks thus appear to be important in the immediate vicinity and the final approach to the loft.
Yet even here near their loft, pigeons do not seem to follow sequences of landmarks, but still determine their home course as a compass course. This is indicated by clockshift experiments within 1.6 km from the loft, where the birds showed deviations from the untreated controls indicating sun compass use [207,208]. This led to the concept of the Mosaic Map, which assumes that birds memorize the directional relationship and distance of landmarks near their home, thus forming a ‘map’ analogue to the navigational ‘map’, but consisting of the representation of numerous individual marks instead of gradients (see [150,209]).
4.4 A flexible system based on innate and learned components
Young, inexperienced birds first rely on innate mechanisms like route reversal and path integration on the basis of compass orientation; inexperienced migrants are guided by innate migration programs. This gives them a chance to learn and memorize the spatial distribution of potential navigational factors, i.e., to establish a ‘map’ of their home region and their migration route. The ‘map’, in contrast to routebased information, allows birds to redetermine the course to the goal whenever they feel it necessary—this increases the certainty of reaching the goal.
We must assume that young birds include in their ‘map’ all suitable factors that can be used for navigation—the ‘map’ is multifactorial (see e.g., [209,210]) and probably includes more factors than just the ones mentioned above, e.g., the view of landscape feature as they change with distance  and others. The ‘map’ appears to be largely redundant: When released within a strong magnetic anomaly, pigeons deprived of magnetic ‘map’ information by local anesthesia of their upper beak left in an oriented way— not being able to sense the anomalous magnetic field they were not confused and obviously turned to non-magnetic cues for navigation right away .
Being based on experience, the ‘map’ is perfectly adapted to the situation within the home region and along the migration route and allows birds to directly head to familiar goals. However, the available navigational factors may differ in various regions, and so we cannot expect the ‘map’ to be identical everywhere. There may be differences in the preferred cues, and findings obtained in one region thus cannot simply be generalized to another without testing.
The above considerations are based on navigational experiments with birds—to what extent they also apply to other animals covering greater distances remains to be determined.
Funding Information Open Access funding enabled and organized by Projekt DEAL.
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