The discovery of the use of magnetic navigational information.

The magnetic field of the Earth provides animals with various kinds of information. Its use as a compass was discovered in the mid-1960s in birds, when it was first met with considerable skepticism, because it initially proved difficult to obtain evidence for magnetic sensitivity by conditioning experiments. Meanwhile, a magnetic compass was found to be widespread.

The Magnetic Compass of Birds: The Role of Cryptochrome.

The geomagnetic field provides directional information for birds. The avian magnetic compass is an inclination compass that uses not the polarity of the magnetic field but the axial course of the field lines and their inclination in space. It works in a flexible functional window, and it requires short-wavelength light.

Magnetoreception in birds.

Birds can use two kinds of information from the geomagnetic field for navigation: the direction of the field lines as a compass and probably magnetic intensity as a component of the navigational 'map'. The direction of the magnetic field appears to be sensed via radical pair processes in the eyes, with the crucial radical pairs formed by cryptochrome. It is transmitted by the optic nerve to the brain, where parts of the visual system seem to process the respective information.

Magnetoreception: activation of avian cryptochrome 1a in various light conditions.

The avian magnetic inclination compass is based on radical pair processes, with cryptochrome (Cry) assumed to form the crucial radical pairs; it requires short-wavelength light from UV to green. Under high-intensity narrow-band lights and when yellow light is added, the magnetic compass is disrupted: migratory birds no longer prefer their migratory direction, but show other orientation responses. The candidate receptor molecule Cry1a is located in the shortwavelength-sensitive SWS1 cone photoreceptors in the retina.

Behavioural traits of individual homing pigeons, Columba livia f. domestica, in their homing flights.

Homing tracks of two groups of pigeons, Columba livia f. domestica, were analyzed in view of difference between individual birds and correlations between characteristic variables, looking at the initial phase while the pigeons were still at the release site, and the homing phase separately. Individual birds differed significantly in their flying speed during the initial phase, and one pigeon tended to stay longer at the release site than the others.

Olfactory navigation versus olfactory activation: a controversy revisited.

In the early 1970s, Floriano Papi and colleagues proposed the olfactory-navigation hypothesis, which explains the homing ability of pigeons by the existence of an odor-based map acquired through learning. This notion, although supported by some observations, has also generated considerable controversy since its inception. As an alternative, Paulo Jorge and colleagues formulated in 2009 the olfactory-activation hypothesis, which states that atmospheric odorants do not provide navigational information but, instead, activate a non-olfactory path integration system.

Considerations on the role of olfactory input in avian navigation.

A large amount of data documents an important role of olfactory input in pigeon navigation, but the nature of this role is not entirely clear. The olfactory navigation hypothesis assumes that odors are carrying essential navigational information, yet some recent experiments support an activating role of odors. This led to an ongoing controversy.

Navigation.

Experiments with migrating birds displaced during autumn migration outside their normal migration corridor reveal two different navigational strategies: adult migrants compensate for the displacement, and head towards their traditional wintering areas, whereas young first-time migrants continue in their migratory direction. Young birds are guided to their still unknown goal by a genetically coded migration program that indicates duration and direction(s) of the migratory flight by controlling the amount of migratory restlessness and the compass course(s) with respect to the geomagnetic field and celestial rotation. Adult migrants that have already wintered and are familiar with the goal area approach the goal by true navigation, specifically heading towards it and changing their course correspondingly after displacement.

Mathematical analysis of the homing flights of pigeons based on GPS tracks.

To analyse the effect of magnetic and olfactory deprivation on the homing flight of pigeons, we released birds from a familiar site with either their upper beak or their nostrils anaesthetized. The tracks were analysed by time lag embedding to calculate the short-term correlation dimension, a variable that reflects the degrees of freedom and thus the number of factors involved in a system. We found that higher natural fluctuations in the earth's magnetic field characterized by A -indices of 8 and above caused a reduction of the correlation dimension of the control birds.

Light-dependent magnetoreception in birds: the crucial step occurs in the dark.

The Radical Pair Model proposes that the avian magnetic compass is based on spin-chemical processes: since the ratio between the two spin states singlet and triplet of radical pairs depends on their alignment in the magnetic field, it can provide information on magnetic directions. Cryptochromes, blue light-absorbing flavoproteins, with flavin adenine dinucleotide as chromophore, are suggested as molecules forming the radical pairs underlying magnetoreception. When activated by light, cryptochromes undergo a redox cycle, in the course of which radical pairs are generated during photo-reduction as well as during light-independent re-oxidation.

Seasonally Changing Cryptochrome 1b Expression in the Retinal Ganglion Cells of a Migrating Passerine Bird.

Cryptochromes, blue-light absorbing proteins involved in the circadian clock, have been proposed to be the receptor molecules of the avian magnetic compass. In birds, several cryptochromes occur: Cryptochrome 2, Cryptochrome 4 and two splice products of Cryptochrome 1, Cry1a and Cry1b. With an antibody not distinguishing between the two splice products, Cryptochrome 1 had been detected in the retinal ganglion cells of garden warblers during migration.

Sensing magnetic directions in birds: radical pair processes involving cryptochrome.

Birds can use the geomagnetic field for compass orientation. Behavioral experiments, mostly with migrating passerines, revealed three characteristics of the avian magnetic compass: (1) it works spontaneously only in a narrow functional window around the intensity of the ambient magnetic field, but can adapt to other intensities, (2) it is an "inclination compass", not based on the polarity of the magnetic field, but the axial course of the field lines, and (3) it requires short-wavelength light from UV to 565 nm Green. The Radical Pair-Model of magnetoreception can explain these properties by proposing spin-chemical processes in photopigments as underlying mechanism.

Magnetoreception in birds: the effect of radio-frequency fields.

The avian magnetic compass, probably based on radical pair processes, works only in a narrow functional window around the local field strength, with cryptochrome 1a as most likely receptor molecule. Radio-frequency fields in the MHz range have been shown to disrupt the birds' orientation, yet the nature of this interference is still unclear. In an immuno-histological study, we tested whether the radio-frequency fields interfere with the photoreduction of cryptochrome, but this does not seem to be the case.

Magnetoreception in birds: II. Behavioural experiments concerning the cryptochrome cycle.

Behavioural tests of the magnetic compass of birds and corresponding immunohistological studies on the activation of retinal cryptochrome 1a, the putative receptor molecule, showed oriented behaviour and activated Cry1a under 373 nm UV, 424 nm blue, 502 nm turquoise and 565 nm green light, although the last wavelength does not allow the first step of photoreduction of cryptochrome to the semiquinone form. The tested birds had been kept under 'white' light before, hence we suggested that there was a supply of semiquinone present at the beginning of the exposure to green light that could be further reduced and then re-oxidized. To test the hypothesis in behavioural experiments, we tested robins, Erithacus rubecula, under various wavelengths (1) after 1 h pre-exposure to total darkness and (2) after 1 h pre-exposure to the same light as used in the test.

Magnetoreception in birds: I. Immunohistochemical studies concerning the cryptochrome cycle.

Cryptochrome 1a, located in the UV/violet-sensitive cones in the avian retina, is discussed as receptor molecule for the magnetic compass of birds. Our previous immunohistochemical studies of chicken retinae with an antiserum that labelled only activated cryptochrome 1a had shown activation of cryptochrome 1a under 373 nm UV, 424 nm blue, 502 nm turquoise and 565 nm green light. Green light, however, does not allow the first step of photoreduction of oxidized cryptochromes to the semiquinone.

Pigeon navigation: different routes lead to Frankfurt.

Background: Tracks of pigeons homing to the Frankfurt loft revealed an odd phenomenon: whereas birds returning from the North approach their loft more or less directly in a broad front, pigeons returning from the South choose, from 25 km from home onward, either of two corridors, a direct one and one with a considerable detour to the West. This implies differences in the navigational process.

Methodology/principle Findings: Pigeons released at sites at the beginning of the westerly corridor and in this corridor behave just like pigeons returning from farther south, deviating to the west before turning towards their loft.

Following the sun: a mathematical analysis of the tracks of clock-shifted homing pigeons.

We analysed the tracks of clock-shifted pigeons from six releases to determine how they cope with the conflict between their sun compass and other navigational cues. Time-lag embedding was used to calculate the short-term correlation dimension, a parameter that reflects the complexity of the navigational system, and with it, the number of factors involved. Initially, while pigeons were still at the release site, the short-term correlation dimension was low; it increased as the birds left the site, indicating that the birds were now actively navigating.

Orientation of migratory birds under ultraviolet light.

In view of the finding that cryptochrome 1a, the putative receptor molecule for the avian magnetic compass, is restricted to the ultraviolet single cones in European Robins, we studied the orientation behaviour of robins and Australian Silvereyes under monochromatic ultraviolet (UV) light. At low intensity UV light of 0.3 mW/m(2), birds showed normal migratory orientation by their inclination compass, with the directional information originating in radical pair processes in the eye.

Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds.

The radical pair model proposes that the avian magnetic compass is based on radical pair processes in the eye, with cryptochrome, a flavoprotein, suggested as receptor molecule. Cryptochrome 1a (Cry1a) is localized at the discs of the outer segments of the UV/violet cones of European robins and chickens. Here, we show the activation characteristics of a bird cryptochrome in vivo under natural conditions.

Avian magnetic compass can be tuned to anomalously low magnetic intensities.

The avian magnetic compass works in a fairly narrow functional window around the intensity of the local geomagnetic field, but adjusts to intensities outside this range when birds experience these new intensities for a certain time. In the past, the geomagnetic field has often been much weaker than at present. To find out whether birds can obtain directional information from a weak magnetic field, we studied spontaneous orientation preferences of migratory robins in a 4 µT field (i.

Development of the navigational system in homing pigeons: increase in complexity of the navigational map.

In the present study we analysed GPS-recorded tracks from pigeons of different ages from 11 sites between 3.6 and 22.1 km from the home loft, which revealed changes in the navigational system as the birds grew older and became more experienced.

Different responses of two strains of chickens to different training procedures for magnetic directions.

In previous conditioning experiments training domestic chickens to magnetic directions, a brown strain solved the task, whereas a white strain seemed unable to do so (Freire et al. Anim Cogn 11:547-552, 2008). To test whether this was possibly caused by loss of magnetic compass orientation in the white chickens, we analyzed the distribution of cryptochrome 1a, the candidate receptor molecule mediating magnetic compass information, in the retinae of Lohmann Browns and White Leghorns and found no difference between the two strains.

Development of lateralization of the magnetic compass in a migratory bird.

The magnetic compass of a migratory bird, the European robin (Erithacus rubecula), was shown to be lateralized in favour of the right eye/left brain hemisphere. However, this seems to be a property of the avian magnetic compass that is not present from the beginning, but develops only as the birds grow older. During first migration in autumn, juvenile robins can orient by their magnetic compass with their right as well as with their left eye.

Interactions between the visual and the magnetoreception system: different effects of bichromatic light regimes on the directional behavior of migratory birds.

When magnetic compass orientation of migratory robins was tested, the birds proved well oriented under low intensity monochromatic light of shorter wavelengths up to 565 nm green; from 583 nm yellow onward, they were disoriented. In the present study, we tested robins under bichromatic lights composed (1) of 424 nm blue and 565 nm green and (2) of 565 nm green and 583 nm yellow at two intensities. Under dim blue-green light with a total quantal flux of ca.

Avian ultraviolet/violet cones as magnetoreceptors: The problem of separating visual and magnetic information.

In a recent paper, we described the localization of cryptochrome 1a in the retina of domestic chickens, Gallus gallus, and European robins, Erithacus rubecula: Cryptochrome 1a was found exclusively along the membranes of the disks in the outer segments of the ultraviolet/violet single cones. Cryptochrome has been suggested to act as receptor molecule for the avian magnetic compass, which would mean that the UV/V cones have a double function: they mediate vision in the short-wavelength range and, at the same time, magnetic directional information. This has important implications and raises a number of questions, in particular, how the two types of input are separated.