The magnetite-based receptors in the beak of birds and their role in avian navigation.

Iron-rich structures have been described in the beak of homing pigeons, chickens and several species of migratory birds and interpreted as magnetoreceptors. Here, we will briefly review findings associated with these receptors that throw light on their nature, their function and their role in avian navigation. Electrophysiological recordings from the ophthalmic nerve, behavioral studies and a ZENK-study indicate that the trigeminal system, the nerves innervating the beak, mediate information on magnetic changes, with the electrophysiological study suggesting that these are changes in intensity. Behavioral studies support the involvement of magnetite and the trigeminal system in magnetoreception, but clearly show that the inclination compass normally used by birds represents a separate system. However, if this compass is disrupted by certain light conditions, migrating birds show 'fixed direction' responses to the magnetic field, which originate in the receptors in the beak. Together, these findings point out that there are magnetite-based magnetoreceptors located in the upper beak close to the skin. Their natural function appears to be recording magnetic intensity and thus providing one component of the multi-factorial 'navigational map' of birds.

Magnetic compass orientation of European robins under 565 nm green light.

European robins tested under monochromatic green light with a peak wavelength of 565 nm at an intensity of 2.1 mW m-2 in the local geomagnetic field preferred their migratory direction, heading southward in autumn and northward in spring. Inverting of the vertical component of the magnetic field caused the robins to reverse their headings, indicating that the birds used a magnetic inclination compass to locate their migratory direction. The behavior recorded under green light at an intensity of 2.1 mW m-2 is thus not different from that previously recorded under "white" light; it represents normal migratory orientation.

Light-dependent magnetoreception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities.

To investigate how magnetoreception is affected by the wavelength and intensity of light, we tested European robins, Erithacus rubecula, under monochromatic lights of various wavelengths at two intensities using oriented behaviour as an indicator of whether the birds could derive directional information from the geomagnetic field. At a quantal flux of 7 x 10(15) quanta s(-1) m(-2), the birds were well oriented in their migratory direction east of North under 424 nm blue, 510 nm turquoise and 565 nm green light, whereas they were disoriented under 590 nm yellow light. Increasing the intensity of light at the same wavelengths more than sixfold to 43 x 10(15) quanta s(-1) m(-2) resulted in a change in behaviour: under bright blue and green light, the birds now showed a preference for the East-West axis, with the majority of headings at the western end; under bright turquoise light, they oriented unimodally towards a direction slightly west of North. Under bright yellow light, the birds continued to be disoriented. These findings suggest a rather complex relationship between the receptors involved in magnetoreception. Magnetoreception appears to follow rules that are different from those of vision, suggesting that light-dependent magnetoreception may involve receptors and neuronal pathways of its own.

Light-dependent magnetoreception in birds: the effect of intensity of 565-nm green light.

In a previous study, Australian silvereyes tested in autumn under monochromatic 565-nm green light at intensities of 2.1 and 7.5 mW m-2 preferred their normal northerly migratory direction, whereas they showed a significantly different tendency towards northwest at 15.0 mW m-2. Repeating these experiments in spring with silvereyes migrating southward, we again observed well-oriented tendencies in the migratory direction at 2.1 and 7.5 mW m-2. At 15.0 mW m-2, however, the birds once more preferred northwesterly directions, i.e. their response under this condition proved to be independent of the migratory direction. This contradicts the interpretation that monochromatic green light of this high intensity leads to a rotation of compass information; instead, it appears to produce sensory input that causes birds to give up their migratory direction in favor of a fixed direction of as yet unknown origin.

Sun-compass orientation in homing pigeons: compensation for different rates of change in azimuth?

Birds using their sun compass must compensate for the apparent movement of the sun with the help of their internal clock. The movement of the sun is not uniform, being much faster around noon than near sunrise and sunset. If the sun-compass mechanisms are not adjusted to these variations, considerable errors might arise. To learn whether birds are able to take the different rates of sun azimuth change into account, we subjected homing pigeons to a 4 h fast clock-shift. The experiments were performed near Auckland, New Zealand, at a latitude of 37 degrees S, where the expected deflections for a 4 h shift in summer vary from less than 40 degrees to more than 120 degrees, depending on time of day. One group of birds was released just after sunrise or during the corresponding period in the afternoon when the expected deflections were minimal, the other group during late morning when they were maximal. The different sizes of the observed deflections - between 26 degrees and 51 degrees in the first group, and between 107 degrees and 153 degrees in the second group - clearly show that the birds' compensation mechanisms are closely tuned to the varying rates of change in sun azimuth. The results suggest that pigeons have a rather precise internal representation of the sun curve, which makes the avian sun compass a highly accurate mechanism of direction finding.

Light-dependent magnetoreception in birds: does directional information change with light intensity?

Magnetic compass orientation in birds is based on light-dependent processes, with magnetoreception being possible only under light containing blue and green wavelengths. To look for possible intensity-dependent effects we tested Australian silvereyes during autumn migration under monochromatic green light (565 nm) produced by light-emitting diodes at various light levels. At intensities of 0.0021 and 0.0075 W/m(2), the birds showed normal activity and were oriented in their seasonally appropriate migratory direction. Under low light of 0.0002 W/m(2) the birds were less active; scatter increased, but they still oriented in their migratory direction. Under a high light level of 0.0150 W/m(2), however, the test birds showed a counterclockwise shift in direction, preferring west-northwest instead of north. This change in behavior may reflect a change in the output of the magnetoreception system, resulting from a disruption of the natural balance between the wavelengths of light.

Staying in plastic containers interferes with the orientation of clock-shifted homing pigeons.

Staying in plastic containers ventilated with natural air during transport and while waiting at the release site was found to affect the initial orientation of pigeons, Columba livia f. domestica, that were exposed to a 6-h clock-shift. The deflection from the mean direction of controls was significantly smaller, and the mean vector length was significantly shorter, than that of clock-shifted pigeons transported in conventional wooden cages. This effect was most pronounced when the birds stayed in plastic containers for the first and second time. Nonshifted control birds seemed to be largely unaffected by plastic containers. There was no influence on homing performance, which suggests a transient nature of the effect. Since the clock-shifted birds had access to the same orientational cues as the controls, we suggest that their sun compass was impaired by stress. We discuss general implications of this container effect, particularly in relation to some cases of olfactory deprivation where containers have been used and stress-induced side-effects cannot be excluded. Copyright 1999 The Association for the Study of Animal Behaviour.

Effect of a magnetic pulse on the orientation of silvereyes, zosterops l. lateralis, during spring migration

The orientation behaviour of Australian silvereyes, Zosterops l. lateralis, was tested during their spring migration, when they head southward to their Tasmanian breeding grounds. With only the local geomagnetic field as a cue, the birds significantly preferred their normal southerly migratory direction. Treatment with a short, strong magnetic pulse designed to alter the magnetization of single-domain magnetite led to a significant deflection towards the east for the next 4 days. This was followed by a period of non-oriented behaviour. From day 10 onwards, the birds returned to their original southerly headings. Together with previous findings, these data suggest that the navigational 'map' of these birds includes magnetic parameters and that a magnetite-based receptor provides them with information about their position. The transient nature of the effect is not easily explained on the basis of single-domain magnetite.

Magnetoreception: why is conditioning so seldom successful?

Conditioning is a highly successful method for analyzing the sensory capacities of animals. With magnetic stimuli, however, it does not seem to work: negative results by far outnumber the positive ones. This is true for cardiac and operant conditioning as well as for directional training. The reasons for these failures are largely unclear. They may stem from the function of the magnetic field as orientation cue and from the fact that the magnetic field never undergoes a rapid change in nature, which means that animals might not be adapted to respond to such changes. Moreover, since the magnetic field contains directional information, animals might evade the problems arising from self-produced movements by calling on magnetic information only when needed for orientation. In view of this, conditioning does not appear to be a suitable technique for testing magnetic sensitivity.

Magnetic orientation in birds

The magnetic field of the earth is an omnipresent, reliable source of orientational information. A magnetic compass has been demonstrated in 18 species of migrating birds. In all species studied with regard to its functional properties, it was found to be an 'inclination compass', i.e. the birds derive directional information from the inclination of the field lines, and thus distinguish between 'poleward' and 'equatorward' rather than 'north' and 'south'. Such a mechanism means that birds from the northern and southern hemisphere may rely on the same migratory programme. Long-distance migrants, however, face the problem that their magnetic compass gives bimodal information at the magnetic equator. Transfers of information between the magnetic field and celestial sources of directional information have been demonstrated; the two systems interact in a complex way. The data on the use of magnetic parameters for position finding are less clear. The experiments involve releases of homing pigeons; correlations of their orientation with natural variations in the magnetic field and the effects of magnetic manipulation reveal an enormous variability. The role of magnetic parameters in the multifactorial navigational system is poorly understood.

The function of olfactory input in pigeon orientation: does it provide navigational information or play another role?

In 1972, Papi and his colleagues reported that anosmic pigeons were severely impaired in orientation and homing performance. This observation was followed up in a series of experiments involving numerous elaborate experimental manipulations. On the basis of their results, the hypothesis of olfactory navigation was proposed. Attempts to replicate these findings at other lofts produced widely differing effects, which suggested a highly variable role of olfaction. However, meteorological data, as well as certain other aspects of the findings, throw doubt on the role of odours as navigational cues. (1) Odours of the required characteristics and distribution do not seem to exist. (2) Some effects of 'olfactory' manipulations do not seem to depend on the availability of odours. (3) Olfactory treatments proved mostly effective, but often the effect was not as predicted. In view of these findings, explanations other than olfactory orientation cannot be excluded; accepting olfactory input as navigational information seems premature. Some of the findings are in agreement with the assumption that olfactory manipulations impair the birds' general processing and integration of information in some unknown way.

Orientation in birds. Magnetic orientation and celestial cues in migratory orientation.

Young birds on their first migration possess innate information on the direction of their migration route. It is represented twice, using both celestial rotation and the geomagnetic field as references. These two systems, together with information provided by factors associated with sunset, interact in a complex way to establish the migratory direction. During ontogeny, celestial rotation appears to be dominant; during migration, however, celestial cues appear to be controlled by the magnetic field.--The factors associated with sunset--the view of the setting sun and the characteristic pattern of polarized light--are important secondary cues which seem to derive their directional significance from the magnetic field. Their role appears to be more variable, with possible species-specific differences. During spring migration and later autumn migrations, flying in the migratory direction is complemented by navigational processes which enable the birds to return to a specific home site known from previous stays.

Magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae).

To test whether mole-rats Cryptomys hottentotus were able to use the magnetic field for orientation, laboratory experiments were conducted which were based on the animals' spontaneous tendency to build their nests at the same position in a circular arena. In the local geomagnetic field, the animals preferred the SE-sector. When magnetic north was turned by 120 degrees or by 180 degrees, the mole-rats changed their nest position accordingly. This clearly shows that they can use the magnetic field for direction finding.

Magnetic versus celestial orientation in migrating birds.

When experimental orientation research began more than 35 years ago, the sun, the stars and later the magnetic field were shown to be involved in the orientation of migrating birds, together with wind, weather and certain landscape features. The interaction of these cues, however, was little understood and became a subject of intensive research. Just recently we have begun to understand how these different mechanisms might work together to enable birds to cope with the navigational tasks of migration over distances of up to 5000 km and more.

Pigeon homing: does initial orientation include a 'preferred compass direction'?

To find out whether the initial orientation of pigeons is affected by a spontaneous directional tendency, as postulated by Wallraff's (1974, 1978, 1982) hypothesis, experienced birds were released at test sites distributed symmetrically around their loft. The length of the mean vectors of the single releases, the deviations from the home direction, the homeward components as well as the homing speed did not show a correlation with the geographic position of the home direction. Summarizing four sites each on 21 experimental circles, we frequently obtained significant compass vectors, but they varied in direction between 115 degrees ESE and 351 degrees N, depending on what sites had been used, and did not indicate a uniform trend. A 'preferred compass direction' as an integrated part of pigeon navigation, being the reason for the frequently observed deviations from the home direction, could not be confirmed. The problematic nature of simply pooling the data of several symmetrically distributed test sites and calling any resulting significant vector a 'preferred compass direction' is discussed, together with other possible reasons for asymmetrical distributions of release site biases.

Pigeons with a deficient sun compass use the magnetic compass.

Homing pigeons that had never seen the sun before noon could not use the sun compass in the morning; nevertheless they were homeward oriented. When such birds carried magnets, however, they were disoriented, suggesting they were using a magnetic compass. These findings indicate that the magnetic compass is available to pigeons whether or not the sun compass has been established and that the magnetic compass is apparently the first source of compass information.