J Ornithol (2007) 148 (Suppl 1):S61–S76
DOI 10.1007/s10336-007-0233-2
REVIEW
Magnetoreception in birds: two receptors for two different tasks
Wolfgang Wiltschko Æ Roswitha Wiltschko
Received: 21 February 2007 / Revised: 7 September 2007 / Accepted: 18 September 2007 / Published online: 24 October 2007

Dt. Ornithologen-Gesellschaft e.V. 2007
Abstract Birds can use the geomagnetic field as a source
of navigational information in different ways: the magnetic
vector provides a compass; magnetic intensity and/or
inclination play a role as a component of the navigational
‘map’, and magnetic conditions of certain regions act as
‘sign posts’ or triggers, eliciting specific responses. Two
hypotheses on magnetoreception are currently under dis-
cussion. One proposes a chemical compass based on a
radical pair mechanism involving direction-dependent
reactions in specialized photopigments; the other postulates
processes involving iron-rich particles, such as magnetite.
Behavioral evidence suggests that birds use both mecha-
nisms, with radical pair processes in the right eye providing
directional information and an iron-based mechanism in
the upper beak providing information on position as a
component of the navigational ‘map’. Electrophysiological
data support this view. The interactions of the two mech-
anisms, however, are still poorly understood.
Keywords Avian navigation
Magnetic compass

Magnetite
Magnetoreception
Radical pair model
Introduction
Many animals are able to perceive the magnetic field of the
earth, among which are mollusks, arthropods and all major
groups of vertebrates, including birds, and they seem to use
Communicated by H. Mouritsen.
W. Wiltschko (&)
R. Wiltschko
FB Biowissenschaften, J.W.Goethe-Universität Frankfurt,
Siesmayerstr. 70, 60054 Frankfurt am Main, Germany
e-mail: wiltschko@bio.uni-frankfurt.de
the information from the magnetic field in several ways. As
humans cannot consciously sense the geomagnetic field
(but see Baker 1989), this initially appears to be an alien
concept. Consequently, in order to obtain a more complete
understanding of this phenomenon, we must first consider
what type of information the geomagnetic field can provide
and—even more importantly—what type of information do
birds actually use.
The earth itself is a huge magnet, with its magnetic poles
situated close to the rotational poles. The magnetic field
lines leave the surface of the earth at the southern magnetic
pole, run around the globe and reenter at the northern
magnetic pole. Consequently, the magnetic field lines point
upward in the southern hemisphere, run parallel to the
earth’s surface at the magnetic equator and point down-
ward in the northern hemisphere (Fig. 1). Magnetic
inclination, or dip, which is the angle between the local
magnetic vector and the horizontal, changes continuously,
showing a fairly regular gradient that varies from –90 at
the southern magnetic pole to +90 at the northern mag-
netic pole, being 0 at the magnetic equator. The intensity
of the geomagnetic field, indicated by the length of the
arrows in Fig. 1, is highest at the two poles and lowest near
the magnetic equator; as such it forms gradients running
from the poles to the equator in each hemisphere (see
Skiles 1985 for details). This regular field can be locally
distorted by material in the upper crust, resulting in mag-
netic anomalies with slight increases or decreases in
intensity; it can also be temporally modulated by electro-
magnetic radiation originating in the sun. In the temperate
latitudes, these daily variations lead to a slight decrease in
magnetic intensity around noon. In addition, occasional
magnetic storms may disrupt the regular pattern. These
changes, however, are mostly very small compared to the
regular field.
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Fig. 1 Magnetic field of the earth. The arrows indicate the local
magnetic vectors with their lengths proportional to the intensity of the
local field (after Wiltschko and Wiltschko 1995)
The geomagnetic field therefore represents a reliable,
omnipresent source of navigational information. This
information can be of two kinds: directional informa-
tion—the magnetic vector can be used by animals as a
compass; positional information—total intensity and/or
inclination may provide information that may be used as
a component of the navigational ‘map’ indicating
position.
Magnetic orientation
Birds have been shown to use both types of magnetic
information. As far as responses to the magnetic field are
concerned, they are by far the best studied group among
animals. In particular, a great deal of research has focused
on the avian magnetic compass.
Magnetic compass orientation
A magnetic compass means that directions can be deter-
mined with the help of the magnetic field. In orientation
experiments, the observation that a bird responds to a shift
in magnetic North with a corresponding change in its
heading is diagnostic of its use of a magnetic compass.
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Demonstration of magnetic compass orientation
A magnetic compass appears to be rather widespread
among birds. It was first demonstrated in passerine
migrants as these birds show a spontaneous directional
behavior: during the migration season, their urge to move
into the migratory direction is so strong that even captive
birds in cages turn into the respective direction.
Researchers took advantage of this urge to migrate and,
during the migration season, tested birds in suitable cages
to record their directional preferences. The most commonly
used type of cage for this research is a funnel-shaped cage
(see Emlen and Emlen 1966) in which the inclined walls
are covered with coated paper where the bird leaves scratch
marks as it moves (Fig. 2). These marks are then counted
to assess the bird’s heading.
When tested in the local geomagnetic field, the Euro-
pean Robin, Erithacus rubecula, but also other species of
migrants, showed a strong preference to orient towards
their seasonally appropriate migratory direction. Tested in
an experimental field of equal intensity, but with magnetic
North turned by a certain angle with the help of Helmholtz
coils, the same birds altered their headings accordingly and
preferred the direction that now corresponded to the same
magnetic course (Fig. 3). This clearly shows that the birds
used the geomagnetic field to orient their movements (see
Wiltschko and Wiltschko 1995 for details).
A magnetic compass has since been demonstrated in
more than 20 avian species (see Table 1). The vast
majority of these are passerine migrants because their
orientation in the migratory direction is a very reliable
behavior that provides an excellent tool for analyzing the
underlying compass mechanisms. A magnetic compass has
been found in birds living on different continents and with
different distances of migration and of time of the day
when they migrate. It seems that a magnetic compass is a
Fig. 2 Test apparatus for recording the directional preference of an
individual bird
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Fig. 3 Demonstrating magnetic compass orientation in the migrating
European Robin. Left Orientation in the local geomagnetic field, right
orientation in a field with magnetic North turned by 120 to ESE. mN
Magnetic North. The triangles at the periphery of the circle mark
mean headings of individual birds, the arrows represent the grand
mean vectors with their lengths proportional to the radius of the
circle. The two inner circles are the 5% (dashed) and the 1%
significance border of the Rayleigh test (data from Wiltschko and
Wiltschko 1999)

general mechanism in migrants, but it is not restricted to displacement produced reliable directional tendencies for
them. The non-migrating carrier pigeon, Columba livia analysis. Magnetic compass orientation has also been
domestica, has also been shown to use the geomagnetic demonstrated recently by directional training in young
field as a compass (Keeton 1971); here, homing after domestic chickens, Gallus gallus (Fig. 4; Freire et al. 2005;
Table 1 Avian species that
Species (family) Distribution Distance Time of day
have been shown to use a
magnetic compass Fowl (Galliformes)
Gallus gallus (Phasanidae)a Eurasia + (Very short)b Day
Pigeons and doves (Columbiformes)
Columba livia f. domestica (Columbidae)a Europe + (Short) Day
Shorebirds (Charadriiformes)
Calidris alba (Scolopacidae) Arctic Medium-long Day + night
Passerines (Passeriformes)
Hirundo rustica (Hirundinidae) Holarctic Long Day
Erithacus rubecula (Turdidae)a Eurasia Short Night
Oenanthe oenanthe (Turdidae) Holarctic Long Night
Ficedula hypoleuca (Muscicapidae)a Eurasia Long Night
Sylvia communis (Sylviidae) Eurasia Long Night
a
Sylvia borin (Sylviidae) Eurasia Long Night
Sylvia atricapilla (Sylviidae)a Europe Medium-long Night
Syilvia cantillans (Sylviidae) Europe Medium Night
Regulus regulus (Sylviidae)a Europe Short Day + night
Prunella modularis (Prunellidae) Europe Short Twilight
Fringilla coelebs (Fringillidae) Europe Short Day
Carpodactus erythinus (Fringillidae) Eurasia Medium Night
Plectrophenax nivalis (Emberizidae) Arctis Short Day + night
Vireo olivaceus (Vireonidae) North America Long Night
Seiurus noveboracensis (Parulidae) North America Medium-long Night
Passerina cyanea (Emberizidae) North America Long Night
Passerculus sandwichensis (Emberizidae) North America Medium-short Night
a
Species for which an Dolichonyx oryzivorus (Icteridae)a North America Long Night
inclination compass has been Zosterops lateralis (Zosteropidae)a Australia Medium Twilight
demonstrated Lichenostomus chrysops (Meliphagidae)a Australia Medium Day
b
Parentheses around the Taeniopygia guttata (Estrildidae) Australia (Short) Day
distance indicate non-migrants

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Fig. 4 Conditioning experiments with young domestic chickens. The
chicks had been imprinted on a red ball and then trained to locate this
ball when it was hidden behind one of four screens in the north, east
south or west. Their choices were axial, as they preferred the correct
screen (CS) and the one opposite. Left Experiments in the local
Wiltschko et al. 2007c) and in Zebrafinches, Taeniopygia
guttata (Voss et al. 2007), both non-migrant species.
The magnetic compass is also used by domestic chick-
ens, making this phenomenon even more remarkable in an
evolutionary context. Chickens belong to an ancient line-
age that separated from the other, more modern lines of
birds as early as in the Cretaceous period (Cooper and
Penny 1997). Consequently, the presence of a magnetic
compass in chickens suggests that the avian magnetic
compass is of great age and may already have been
developed in the common ancestors of all modern birds. At
the same time, the observation that a sedentary species like
the chicken and birds like Zebrafinches can both locate
directions with the help of the geomagnetic field throws
light on the ecophysiological origin and the significance of
the magnetic compass in avian orientation, suggesting that
this mechanism was primarily developed for facilitating
everyday orientation within the home range, where it
would be important for optimizing routes between various
goals like nest, feeding place, drinking place, etc. When
some species of birds began to migrate, it was also used to
orient their extended overland flights.
Functional mode of the avian magnetic compass
The functional mode of the avian magnetic compass was
first also analyzed in studies of migratory orientation. Two
unexpected properties of this mechanism became evident:
In contrast to our technical compass, the avian magnetic
compass was found to be an ‘inclination compass’, based
on the inclination of the field lines instead of their polarity.
Birds can apparently only perceive the axial course of the
field lines; to derive non-ambiguous directional informa-
tion, they must interpret the inclination of the field lines
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geomagnetic field, right experiments in a field with magnetic North
shifted by 90 to the east. mN Magnetic North. The numbers
summarize the choices of each screen by the eight chicks tested five
times each (after Freire et al. 2005)
with respect to up and down. This was demonstrated by
testing robins in a magnetic field with the vertical com-
ponent inverted: inversion of the vertical component of the
field caused the birds to reverse their heading, preferring
magnetic south instead of north. Reversal of the horizontal
component and inversion of the vertical component alter
the axial course of the field lines in the same way; conse-
quently, an animal not perceiving the polarity of the
magnetic field will not realize the difference. Birds reverse
their headings in both situations alike (Wiltschko and
Wiltschko 1972), indicating that the avian magnetic com-
pass does not distinguish between magnetic ‘north’ and
‘south’ as indicated by polarity but, instead, they perceive
the difference between ‘poleward’, where the field lines
point to the ground, and ‘equatorward’, where they point
upward (Fig. 5).
The other surprising finding was that the avian magnetic
compass is closely tuned to the total intensity of the
ambient field. When the intensity of an experimental field
was reduced or increased by 30%, the birds were no longer
oriented, suggesting a rather narrow functional window.
This window is not fixed, however, as it was shown to be
adjustable to lower or to higher intensities when the birds
were exposed to these intensities for a certain length of
time. At the same time, these birds did not lose their ability
to orient in the local geomagnetic field, yet they proved
unable to orient in an intermediate field (Wiltschko 1978).
This indicates that the newly gained ability to orient in
higher or lower fields represents neither a shift nor an
amplification of the functional range. Birds can apparently
orient only in field intensities they have experienced ear-
lier, with this experience possibly forming a new functional
range.
These two properties of the avian magnetic compass
were first described for European robins. An inclination
J Ornithol (2007) 148 (Suppl 1):S61–S76
Fig. 5 Vertical section through the geomagnetic field to illustrate the
inclination compass. Left The local geomagnetic field in Frankfurt,
right a field with the vertical component inverted. N, S North and
South, H magnetic vector, He the vector of the geomagnetic field, Hh,
Hv horizontal and vertical component, respectively, g gravity vector.
Red arrowheads give the polarity, with mN’ and mS’ in red indicating
magnetic north and south, respectively; blue lines indicate the course
of the field lines, the crucial factor for the inclination compass, with p’
and e’ in blue giving the readings of the avian compass ‘poleward’
and ‘equatorward’, respectively. The birds are flying ‘poleward’
compass has since been found in all avian species in which
the functional mode of the compass has been analyzed (see
Table 1), among them homing pigeons (Walcott and Green
1974; Visalberghi and Alleva 1979). For migrants, this has
an interesting consequence, as birds living in the northern
and southern hemisphere of the Earth may have the same
migration program: when the days get shorter in autumn,
they head ‘equatorward’, which is south in the northern and
north in the southern hemisphere (Wiltschko et al. 1993a).
Chickens could not be tested for an inclination compass
because their directional choices were bimodal: they pre-
ferred the correct and the opposite direction (see Fig. 4).
However, the second characteristic, the functional window,
was also observed in chickens: they, too, became disori-
ented when the intensity of the ambient magnetic field was
markedly decreased or increased (Wiltschko et al. 2007c).
To date, only a small number of bird species have been
tested for the functional properties of their magnetic
compass, but the evidence currently available suggests the
same type of mechanism, which may be common to all
present-day birds.
Non-compass use of the magnetic field
Due to their intrinsic nature as gradients running from
north to south, magnetic intensity and inclination can
provide information on position. Evidence for this use of
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Fig. 6 Schema of a navigational ‘map’, with magnetic intensity,
given in relative units, showing a north–south gradient that can be
used as component indicating position. Home is marked by a star, P1
to P3 give the starting sites and the respective starting directions, with
the irregularity in the north leading to deviations from true home
direction at P3
magnetic information is much rarer than that supporting
compass use, and the number of species involved is much
smaller.
Magnetic navigation
Magnetic intensity has been discussed as a component of
the navigational ‘map’ ever since the late 19th century
(Viguier 1882). It could be used in the following way: in
the northern hemisphere, birds know by experience that
magnetic intensity increases towards the north; when
finding themselves at a location with intensity higher than
at home, they would conclude that they are north of home
and hence must head south to return (Fig. 6). First indi-
cations that birds use magnetic parameters in their
navigational ‘map’ came from correlations of the vanishing
bearings of homing pigeons with temporal changes of the
magnetic field (e.g. Keeton et al. 1974). In subsequent
experiments, pigeons released in a magnetic anomaly
showed an increase in scatter that extended up to disori-
entation, with the severity of the scatter being strongly
correlated with the steepness of the local intensity gradient
(Fig. 7; Walcott 1978). The effects of various magnetic
treatments on pigeons’ initial orientation that cannot be
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Fig. 7 Orientation of homing
pigeons at various sites in and
near a strong magnetic anomaly.
The vector lengths (ordinate,
logarithmic scale) are correlated
with the maximum difference in
intensity (abscissa, logarithmic
scale). The coefficient of
correlation is 0.96. The data of
three releases are given as
examples, with the home
direction upward (data from
Walcott 1978)
attributed to interference with the magnetic compass also
suggest an involvement of magnetic factors in the navi-
gational process (for summary, see Wiltschko and
Wiltschko 1995).
Conditioning experiments also demonstrate the pigeons’
ability to detect differences in magnetic intensity. Book-
man (1977) successfully conditioned pigeons in a flight
tunnel to distinguish between an inhomogeneous magnetic
field of about 50 lT and a weak field of 2 lT. Mora et al.
(2004) trained homing pigeons to detect the presence or
absence of a local magnetic ‘anomaly’ of about 190 lT. In
both cases, the magnetic stimulus indicated the correct
alternative of a conditioned two-way choice to obtain a
food reward. A recent study indicates that pigeons trained
to associate food with a magnetic ‘anomaly’ were able to
use this cues as a magnetic landmark to indicate the
location of hidden food (Thalau et al. 2007).
Magnetic conditions as triggers
Total intensity and/or inclination may also serve as ‘sign-
posts’ or triggers, marking specific regions where birds
must act in a particular way. The respective responses are
innate and are elicited when the birds encounter the specific
magnetic conditions.
A first example involved passerine birds that change
their migration course in order to avoid ecological barriers.
The central European population of Pied Flycatchers,
Ficedula hypoleuca, heads first southwest to Iberia, then
changes to a southeasterly course, this way traveling
around the Alps, the Mediterranean Sea and the central
Sahara. Hand-raised birds of this population tested in cages
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in the local geomagnetic field of Central Europe started the
autumn migration with southwesterly preferences, yet they
showed the change in direction only when the magnetic
field of their migration route was simulated and they
experienced the field of northern Africa at about the
appropriate time (Beck and Wiltschko 1988). Apparently,
these magnetic conditions served as a ‘sign post’ and ini-
tiated the second leg of migration. Likewise, in Garden
Warblers, Sylvia borin, that are transequatorial migrants
and have to cross the magnetic equator twice a year, a
horizontal field caused a reversal in headings: here, the
field of the equator serves as a trigger, eliciting the change
in magnetic heading from ‘equatorward’ to ‘poleward’ that
enables these birds to go on into the southern hemisphere
(Wiltschko and Wiltschko 1992).
The function of ‘sign post’ is not restricted to orientation
responses, however; it also includes physiological respon-
ses. Thrush nightingales, Luscinia luscinia, caught and held
in Sweden showed a slow weight gain during the autumn
migration, while simulation of the specific magnetic con-
ditions of northern Egypt induced a much more rapid gain
in weight. During a real migration, this extra fat load
enables these birds to cross the vast ecological barrier of
the Sahara (Fransson et al. 2001). In a subsequent study,
magnetic conditions of the migration route presented in fast
succession were found to elicit this fast weight gain also
early in the migration season, weeks before it was normally
initiated by the endogenous migration program (Kullberg
et al. 2003). In a median distance migrant like the robin, in
contrast, simulation of the magnetic conditions of the route
had hardly any effect during early migration. However,
later, birds kept in the fields simulating the migration route
gained significantly less weight than the control birds kept
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in the local geomagnetic field of Sweden (Kullberg et al.
2007)—the magnetic field conditions presumably signaled
the approach to the wintering area. These findings suggest
that the magnetic conditions encountered en route together
with the endogenous program control migration, with this
control closely adapted to the population-specific needs.
Magnetoreception
For a complete understanding of a ‘magnetic sense’, one
needs to know (1) details on the primary processes media-
ting magnetic input, (2) the location of the sensory organ,
its structure, and its connections to the central nervous
system, and (3) what parts of the brain are involved in
processing magnetic information. Unfortunately, our
knowledge of the physiological and neurobiological pro-
cesses associated with magnetoreception is still rather
limited, as the analysis has just begun.
An additional problem results from the fact that mag-
netoreception is not a uniform phenomenon. Since the
behavioral evidence summarized above clearly shows that
birds can use different parameters of the geomagnetic field
in different tasks, we must expect to find specialized
receptors for mediating magnetic intensity and others for
mediating information on direction.
Models for magnetoreception
A number of models for magnetoreception based on dif-
ferent physical principles have been proposed, the most
prominent ones being (1) interactions of chemical pro-
cesses with the ambient magnetic field and (2) processes
involving iron-rich magnetic material, in particular
magnetite.
The ‘Radical Pair’ model
The Radical Pair model, first proposed by Schulten (1982)
and later expanded upon by Ritz et al. (2000), postulates a
‘chemical compass’ based on direction-specific interactions
of macromolecules with the ambient magnetic field. In the
initial step, the model assumes that specialized photopig-
ments absorb a photon and are elevated to the singlet
excited state. They form singlet radical pairs with anti-
parallel spin, which, by singlet-triplet interconversion, may
turn into triplet pairs with parallel spin (Fig. 8). The
magnetic field alters the dynamics of the transition between
spin states; as a consequence, the triplet yield depends on
the alignment of the macromolecule in the ambient mag-
netic field (for details, see Ritz et al. 2000). As such, it can
S67
convey information on magnetic directions. As receptor
molecule, Ritz and colleagues suggested cryptochromes, a
class of photopigments that possess chemical properties
crucial for the model, including the ability to form radical
pairs (Giovani et al. 2003).
To obtain magnetic compass information by a radical
pair mechanism, birds must take advantage of the fact that
triplet products are chemically different from singlet
products and compare the triplet yields in different spatial
directions. This requires an orderly array of photopigments
oriented in the various directions. The required conditions
could be met by the more or less spherical arrangement of
receptors in the eyes—radical pair processes would gen-
erate characteristic patterns of activation across the retina
(Ritz et al. 2000). These patterns would be centrally sym-
metric around the axis of the field lines—that is, axial
rather than polar—and would enable birds to detect the
field lines of the ambient field. At the same time, the initial
photon absorption would make magnetoreception by a
radical pair mechanism light-dependent.
Because of the axial pattern of activation, a radical pair
mechanism would not be sensitive to the polarity of the
magnetic field and would therefore provide an inclination
compass as it is found in birds. The model also provides an
explanation for the narrow functional window of the
magnetic compass and its flexibility. The activation pattern
on the retina would also depend on magnetic intensity, and
when tested under intensities that differ markedly from that
of the local geomagnetic field, birds would be faced with a
novel pattern (for examples of what such patterns might
look like, see Ritz et al. 2000). This may confuse them at
first, yet the pattern retains its central symmetry around the
axis of the field lines. Given sufficient time, birds may
Fig. 8 Schema of a radical pair mechanism. A donor (D) absorbs a
photon and, by electron transfer, a singlet radical pair is formed.
Singlet-triplet interconversion leads to triplet pairs, with the triplet
yield depending on the alignment of the molecules in the ambient
magnetic field. Triplet products are chemically different from the
singlet products and, consequently, may play a role in magnetore-
ception (after Ritz et al. 2000)
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become familiar with the novel pattern and learn to inter-
pret it, thus regaining their ability to orient.
The magnetite hypothesis
Magnetite is a specific form of iron oxide Fe3O4 whose
general properties depend on the size and shape of the
particles. Spin interactions cause the spins of adjacent
atoms to align, thus forming domains with all spins parallel.
Large particles include multiple domains with their mag-
netic moments largely canceling each other; particles in the
range between about 1.2 and 0.05 lm consist of a single
domain and have a stable magnetic moment, acting as tiny
permanent magnets. Even smaller particles are superpara-
magnetic: their magnetic moment fluctuates as a result of
thermal agitation, but it can easily be aligned by an external
magnetic field (see Kirschvink et al. 1985 for details).
In the 1970s, bacteria were discovered that contained
chains of single-domain magnetite crystals that acted as
magnets and aligned these bacteria along the field lines
(Blakemore 1975). Magnetic information mediated by tiny
magnets was an attractive idea, and the existence of mag-
netic material of biogenic origin caused authors to
speculate about a potential role of magnetite in the orien-
tation of higher animals. Based on theoretical
considerations, a variety of models on how magnetite
particles could mediate magnetic information were pro-
posed, some of them involving single domains (e.g. Yorke
1979; Kirschvink and Gould 1981; Kirschvink and Walker
1985; Edmonds 1996), others superparamagnetic particles
(e.g. Kirschvink and Gould 1981; Shcherbakov and
Winklhofer 1999; Davila et al. 2003). A uniform, generally
accepted concept on how magnetite-based magnetorecep-
tors would work does not yet exist. Interestingly, some of
the models predict polar responses, others predict axial
responses. Model calculations showed that magnetite-
based receptors could convey directional information or
information on magnetic intensity, depending on their
specific structure and on the amount of magnetite included.
In birds, histological and electron-optic studies revealed
iron-rich particles in the orbital and nasal cavities, where
single domains had been reported (Beason and Nichols
1984; Beason and Brennon 1986; Williams and Wild
2001), and at specific locations in the skin of the upper
beak, where clusters of very small crystals had been
described (Fleissner et al. 2003, 2007), with the particles
identified by crystallographic tools as superparamagnetic
magnetite (Hanzlik et al. 2000). These clusters were loca-
ted within nervous tissue and associated with a remarkable
framework of platelets consisting of maghemite (Fig. 9);
the authors speculate about possible functions in a
magnetoreceptor (Fleissner et al. 2003, 2007).
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Evidence associated with the Radical Pair model
The Radical Pair model predicts that magnetoreception is
light-dependent. It is accepted that light is indeed required
for magnetic compass orientation in birds. The first evi-
dence of this came from behavioral experiments with
young homing pigeons: displaced in total darkness, they
were disoriented (Wiltschko and Wiltschko 1981), just as
young pigeons displaced in a distorted magnetic field had
been (Wiltschko and Wiltschko 1978).
Wavelength-dependence
If photopigments are involved, these pigments can hardly
be expected to absorb light over the entire range of the
visual spectrum. Hence, magnetoreception should depend
on the wavelength of the light, reflecting the absorption
ranges of the magnetosensitive pigments. A series of
experiments was conducted in which migratory birds were
tested under monochromatic light of various wavelengths,
with different birds used for each wavelength, again using
migratory orientation as a criterion of whether or not nor-
mal directional information from the magnetic field could
be obtained in a given situation.
Tests with the European Robin revealed the following
pattern: magnetic orientation was possible under 373 (UV),
424 (blue), 510 (turquoise), and 565 nm (green), whereas
under 590 (yellow) and 635 nm (red), the birds were dis-
oriented (Fig. 10; see Wiltschko and Wiltschko 2002;
Wiltschko et al. 2007a). Experiments with interference
filters narrowed down the onset of disorientation in robins
Fig. 9 Schematic reconstructions of structures in the skin of upper
beak of pigeons, based on ultra-thin section series. Above the terminal
region of a nerve containing a scaffold of maghemite platelets and
numerous spherules of superparamagnetic magnetite particles, below
a spherule of superparamagnetic particles and the maghemite
structures surrounding it (from Fleissner et al. 2003)
J Ornithol (2007) 148 (Suppl 1):S61–S76
Fig. 10 Orientation behavior of
the European Robin in the
spring under monochromatic
light of different wavelengths
(indicated in the diagrams);
symbols are as in Fig. 3 (after
Wiltschko and Wiltschko 2002)
even further to between 561 and 568 nm (Muheim et al.
2002). That is, the spectral range where birds obtain normal
magnetic compass information includes the entire short-
wavelength part of the visual spectrum. A similar pattern
emerged in corresponding tests with Australian Silvereyes,
Zosterops l. lateralis (Wiltschko et al. 1993b) and Euro-
pean Garden Warblers, Sylvia borin (Rappl et al. 2000) and
has also been indicated in tests with young homing pigeons
(Wiltschko and Wiltschko 1998). On the first glance, the
birds’ response to the different wavelengths appears to be
an ‘all-or-nothing’-response, reflecting the absorption of
one receptor only, yet the rather abrupt transition to dis-
orientation suggests an antagonistic interaction with a
second receptor (Wiltschko and Wiltschko 1999, 2001).
A second receptor is also indicated by another finding.
Although normally disoriented under long wavelengths,
birds could orient under 645 nm (red light) after they had
been exposed to this wavelength for 1 h prior to the critical
tests. The orientation induced this way was directed in the
normal migratory direction (Möller et al. 2001; Wiltschko
et al. 2004a).
Identifying the underlying physical mechanism
A diagnostic test based on magnetic resonance aimed at
obtaining direct evidence for a radical pair mechanism
underlying the avian magnetic compass was carried out. If
the triplet yield is crucial for magnetoreception, interfering
with the singlet-triplet interconversion should alter the
output of the receptor markedly and thus disrupt mag-
netoreception. The singlet–triplet interconversion rate can
be significantly affected by high-frequency fields in the
megaHertz range (Ritz et al. 2000), with the effect of these
fields depending on their orientation with respect to the
static background field (Cranfield et al. 1994).
S69
Robins exposed to weak high-frequency fields—a
broadband noise field of frequencies from 0.1 to 10 MHz, a
1.315-MHz and a 7.0-MHz field—were found to be dis-
oriented when these fields were presented at an 24 or 48
angle to the geomagnetic field, but the birds were well
oriented when the same fields were presented parallel to the
geomagnetic vector (Fig. 11; Ritz et al. 2004; Thalau et al.
2005; Wiltschko et al. 2005). This clearly shows that the
observed effect of a high-frequency field is a specific one.
As the intensity of the applied high-frequency fields was
much too low to affect, for example, particles of magnetite,
this result suggests an interference with resonance pro-
cesses and, thereby, identifies a radical pair mechanism as
acting as the primary process by which birds detect mag-
netic directions.
In a more recent study, robins whose upper beak had
been locally anesthetized to temporarily disable the iron-
based receptors described by Fleissner et al. (2003) con-
tinued, as did the untreated controls, to orient in their
migratory direction (Wiltschko et al. 2007b). This lack of
effect when these receptors were deactivated indicates that
they are not involved in the avian magnetic compass.
Site of magnetoreception and the magnetosensitive
photopigment
Theoretical considerations had favored the eyes as site of
magnetoreception because their almost spherical shape
which would allow receptors to be orientated in the various
directions and thus enable birds to compare activation in
different directions (Ritz et al. 2000). This prediction has
been confirmed in birds, with the surprising finding that
magnetoreception seems to be restricted to the right eye.
Passerine migrants tested with their left eye covered were
just as well oriented as binocular birds, whereas the same
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S70 J Ornithol (2007) 148 (Suppl 1):S61–S76

Fig. 11 The effect of a high-

frequency field added to the
static geomagnetic field in two
different orientations on the
migratory orientation of the
European Robin. Left Control in
the geomagnetic field, center a
1.315-MHz field parallel to the
magnetic vector, right the same
1.315-MHz field added to the
geomagnetic field at an angle of
14. The upper part of the
diagram illustrates the
orientation of the geomagnetic
field and the high-frequency
field in the three test conditions,
the lower part illustrates the
results. Symbols in the circular
diagrams are as in Fig. 3 (from
Thalau et al. 2005)

birds failed to show oriented behavior when their right eye
was covered (Fig. 12; Wiltschko et al. 2002a). The same
has been found to be true for Australian Silvereyes (Wilt-
schko et al. 2003a) and domestic chickens (Rogers et al.
2007) and is also indicated in homing pigeons (Prior et al.
2004). It may be a wide-spread phenomenon among birds.
Another question concerns the magnetosensitive mole-
cules that form the radical pairs leading to magneto-
reception. Most of the well-known photopigments, such as
the opsins that mediate vision, can be excluded because of
their inability to form radical pairs. Attention has therefore
focused on cryptochromes, a class of photopigments
known from plants but also found in animals (see Sancar
2003 for review). These photopigments seem to be prom-
ising candidates because they have the properties required
by the Radical Pair model (Ritz et al. 2000), in particular
the ability to undergo light-dependent electron transfer
reactions that lead to the formation of long-lived radical
pairs (Giovani et al. 2003), which is a prerequisite for
sensitivity to weak magnetic fields.
Cryptochromes have been found in the retina of birds,
originally in chicken (Bailey et al. 2002; Haque et al. 2002)
and then also in passerine migrants (Möller et al 2004;
Mouritsen et al. 2004). In the European Robin, Möller et al.
(2004) identified a novel form of cryptochrome 1, eCry1b,
which is a splice product of the known cryptochrome 1 with a
different C terminus, thereby suggesting a different function.
The sensitivity of cryptochrome to changes in the ambient
magnetic field has recently been demonstrated in plants,
where a more than twelvefold increase in magnetic intensity
led to an enhancement of inhibition of hypocotyl growth,
while no effect was observed in a cry-cry double mutant that
was devoid of cryptochrome (Ahmad et al. 2007).
In short, cryptochromes respond to the magnetic field
and are present in birds in the eyes where one would expect
them to be if they played a crucial role in magnetorecep-
tion. However, there is as yet no direct evidence
demonstrating their involvement.
Neuronal pathways associated with the avian magnetic
compass
Electrophysiological recordings in pigeons suggest that
directional input from the magnetic field is processed in
parts of the visual system. Recordings from the nucleus of
the basal optic root (nBOR) and from the tectum opticum
revealed the presence of units that responded to changes in
magnetic direction (Semm et al. 1984; Semm and Demain
1986). These responses are in accordance with the

Fig. 12 The effect of covering

one eye on the orientation of
robins. Left Binocular (Bi)
control birds with both eyes
open, center monocular birds
that had to rely on their right
eye (R), right monocular birds
that had to rely on their left eye
(L). Symbols as in Fig. 3 (from
Wiltschko et al. 2002a)

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J Ornithol (2007) 148 (Suppl 1):S61–S76
predictions of the Radical Pair model, as they were
observed only in the presence of light; they also seem to
originate in the retina, as they depended on an intact retina
and optic nerve. When the eyes were illuminated with
monochromatic light of various wavelengths, units with a
peak of responsiveness around 503 nm and others with a
peak beyond 580 nm were identified.
Individual neurons in the nBOR as well as the tectum
showed distinct peaks of responsiveness at particular
alignments of the magnetic field. These varied between
cells so that the input of a number of units would represent
all directions in space (Fig. 13). Processed collectively and
integrated, it would thus provide a suitable basis for a
compass, as predicted by the Radical Pair model (Semm
et al. 1984; Semm and Demaine 1986).
The finding that magnetic input is mediated exclusively
by the right eye (Wiltschko et al. 2002a, 2003a) indicates a
strong lateralization of the magnetic compass. Because of
the very few connections between the two hemispheres, it
means that magnetic information is processed almost
exclusively by the left hemisphere of the brain. This is
intriguing, as a number of morphological asymmetries have
been described in the tectofugal system, a part of the visual
system (Güntürkün 1997) which, aside from the tectum
opticum, comprises the nucleus rotundus, where activation
by magnetic stimuli by the glucose method had been
reported (Mai and Semm 1990). Mouritsen et al. (2005)
recently suggested that active cells in a night-vision area in a
part of the wulst, identified based on the expression of
ZENK and c-Fos in migratory active Garden Warblers, may
Fig. 13 Electrophysiological responses recorded from the nucleus of
the basal optic root (nBOR) of pigeons to a gradual change of
magnetic inclination from 62 downward to 62 upward (= vertical
component inverted); two individual units show their maximum
response at different magnetic directions (data from Semm et al.
1984)
S71
possibly related to the processing of magnetic compass
information; a recent study (Liedvogel et al. 2007) does not
support this view, however. Together, the few findings
available suggest that magnetic input originating in the right
eye shares neuronal pathways with the visual system, being
processed in the left hemisphere of the brain. The specific
parts of the brain involved remain to be determined in detail.
Findings associated with the magnetite hypothesis
The first behavioral tests designed to generally demonstrate
an involvement of magnetite in magnetoreception aimed at
interfering with the potential receptors by altering the
magnetization of the magnetite crystals. The underlying
premise was that even if it were not possible to specify in
detail what effect was to be expected, the output of mag-
netite-based receptors should change dramatically and thus
cause a significant after-effect on orientation behavior.
Treatment with a brief, strong magnetic pulse
One popular approach was to apply a brief, strong magnetic
pulse to the head of the test birds—the pulse had to be
strong enough to remagnetize the magnetite particles but,
at the same time, short enough to prevent these particles
from rotating into the pulse direction and thus escape
remagnetization. In most studies, a 0.5-Tesla pulse with a
duration of 3–5 ms was used.
Tests with passerine birds again used migratory orien-
tation to determine whether or not the pulse treatment
affected behavior. A pulse prior to the critical tests caused
a marked 90 change in direction, with Australian Silver-
eyes preferring easterly headings, regardless of whether
they had been heading northward in the autumn or south-
ward in the spring. This effect of the pulse lasted for about
3 days, after which time the birds became disoriented until
about 10 days after pulse treatment, when they resumed
their orientation in the migratory direction (Wiltschko et al.
1994, 1998). Interestingly, this effect of pulsing was
restricted to experienced migrants that had completed at
least one migratory trip (Fig. 14); young birds that had
been captured immediately after fledging did not respond
to the pulse and continued in their normal migratory
direction (Munro et al. 1997). These results suggest that the
pulse affected a mechanism that is based on experience and
points to the position-finding system of the ‘navigational
map’. The same pulse also caused experienced pigeons to
deviate from the mean of untreated control birds at unfa-
miliar sites (Beason et al. 1997).
The observation that the young migrants continued in
their migratory direction indicates that the pulse left the
123
S72
Fig. 14 Effect of a short, strong magnetic pulse on the orientation
behavior of Australian Silvereyes during the Australian autumn. Left
Old, experienced birds, right young, inexperienced birds. Open
symbols indicate control data recorded before the pulse, filled symbols
indicate data recorded after the pulse treatment. Symbols are as in Fig.
3 (data from Wiltschko et al. 1994; Munro et al. 1997)
magnetic compass intact (Munro et al. 1997). The direc-
tional orientation after pulse treatment was found to be
controlled by the normal inclination compass (Wiltschko
et al. 2006). Together, these findings suggest that the pulse
affected a mechanism that was involved in determining the
compass course rather than the compass itself—the com-
pass continues to function in the normal way.
In further tests, the protocol of the pulse treatments was
modified to reveal some properties of the receptor. An
identical pulse applied in two different orientations—for
example, ‘south anterior’, the induced south pole towards
the beak, and ‘south left’, the induced south pole towards
the left side of the head—lead to deflections to different
sides of the control birds. This was true for passerine
migrants, such as bobolinks, Dolichonyx orycivorus, as
well as homing pigeons (Beason et al. 1995, 1997) and
implies that the pulse did not deactivate the receptors
altogether, but instead caused them to provide altered
information so that the birds headed in a different direction.
In other tests, the same pulse was applied together with a
strong, 100-lT biasing field. It had been argued the pulse
alone would remagnetize only an unknown portion of the
particles of the receptor; therefore, the biasing field was
applied to align movable particles in one direction so that a
pulse affected them all. A pulse applied parallel would not
change their magnetization, whereas the pulse applied in
antiparallel direction should have a maximum effect. In
critical tests, however, both groups of birds showed the
same deflections (Wiltschko et al. 2002b). This result lar-
gely excludes single-domain particles free to move as part
of a magnetic sensor.
Single domains or superparamagnetic particles?
Since none of the other reception mechanisms would be
able to show an after-effect following treatment with a
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J Ornithol (2007) 148 (Suppl 1):S61–S76
magnetic pulse, the observation that the pulse had an effect
clearly indicates that magnetite particles are involved in the
receptor controlling the observed behavior. However, in
birds, single-domain particles as well as superparamagnetic
crystals have been described, and this raises the question of
which type of magnetite particles is involved in
magnetoreception.
The data available to date are not easy to explain,
assuming a mechanism based on single domains. In par-
ticular, the short duration of the pulse effect is not easily
reconciled with single domains. Remagnetization of single-
domain particles should be just as stable and lasting as the
original state, yet a clear pulse effect was observed only on
the day of pulsing and the following two days; 10 days
after pulse treatment, the birds oriented in their normal
migratory direction again (Wiltschko et al. 1994, 1998;
Beason et al. 1997). This cannot be explained on the basis
of a mechanism involving only single domains; conse-
quently, auxiliary mechanisms must be assumed. A second
pulse identical with the first, applied after the effect of the
first pulse had worn off, had a different effect. Instead of a
change in direction, it caused initial disorientation; yet the
birds recovered quickly and resumed their normal orien-
tation in migratory direction after only 4 days (Wiltschko
et al. 2007c). The different effect of the second pulse shows
that the initial state of the receptors had not been com-
pletely restored, but at the same time it indicates that the
input from these receptors was not ignored. A rearrange-
ment of superparamagnetic particles would seem to be a
possibility, but in what specific way they might mediate
magnetic information remains to be determined.
Neuronal pathways associated with magnetite-based
receptors
The region of the head where magnetite particles are found
is innervated by the ramus ophthalmicus, a branch of the
nervus trigeminus. Electrophysiological recordings from
the ophthalmic nerve in passerine birds revealed the pres-
ence of units responding to magnetic stimuli, with the
spontaneous activity of these neurons modified by changes
in magnetic intensity. The unit showed a logarithmic
characteristic; the minimum intensity difference tested was
200 nT, where the birds still showed a clear response
(Fig. 15). Similar recordings were reported from the tri-
geminal ganglion (Semm and Beason 1990).
Two other findings provide more direct evidence that the
input from magnetite-based receptors in birds is mediated
by the ophthalmic branch of the trigeminal nerve: behav-
ioral experiments showed that deactivating the ophthalmic
nerve with a local anesthetic suppressed the pulse effect
(Beason and Semm 1996). The bobolinks treated this way
J Ornithol (2007) 148 (Suppl 1):S61–S76
Fig. 15 Electrophysiological recordings from a trigeminal ganglion
cell of a Bobolink indicate responses to different changes in the
intensity of the geomagnetic field (Semm and Beason 1990)
continued in their migratory direction, which, like the
findings of Munro et al. (1997) and Wiltschko et al. (2006),
clearly shows that the pulse did not affect the compass
mechanism. In conditioning experiments, pigeons trained
to respond to the presence or absence of a magnetic
‘anomaly’ with large changes in intensity failed to respond
correctly after deactivation of the ophthalmic nerve (Mora
et al. 2004). These findings, together with those from other
behavioral studies, suggest that in birds, iron-based
receptors mediate information on intensity through the
ophthalmic and trigeminal nerve to the trigeminal ganglion
and further.
‘Fixed’ direction responses
We briefly mention here a recently described, rather odd
phenomenon that is associated with specific light regimes.
The response patterns of robins to monochromatic light
described in the section on ‘Wavelength dependence’
above were obtained under rather low light levels of 6–
7 · 10–15 quanta s–1m–2, an intensity found in nature more
than half an hour after sunset or before sunrise. When the
intensity of monochromatic light was increased sixfold or
more, a marked change in behavior was observed: under
light from the blue to green part of the spectrum, passerine
migrants no longer preferred their natural migratory
direction, but instead showed axial preferences or showed
odd unimodal tendencies that did not change between the
spring and autumn (Wiltschko et al. 2000, 2003b; Wilt-
schko and Wiltschko 2001; Wiltschko et al. 2007a,b). Such
‘fixed direction’ responses were also observed when robins
were tested under a combination of light from the short
wavelength part of the spectrum with 590 nm yellow light.
The specific manifestation of the ‘fixed direction’ respon-
ses depended on the light regime, with northerly, easterly,
S73
southerly or westerly directions observed under bichro-
matic and bright monochromatic lights (Wiltschko et al.
2000, 2003b, 2004b; Wiltschko et al. 2005, 2007a,b).
The analysis of the fixed direction’ responses revealed
that the latter did not depend on the inclination compass
normally used by birds (Wiltschko et al. 2003b) and did not
involve radical pair processes (Wiltschko et al. 2005,
2007b). Instead, they seem to originate in the iron-based
receptors in the upper beak as birds whose beak has been
locally anesthetized no longer show the ‘fixed direction’
responses, but are disoriented (Wiltschko et al. 2007b).
The ‘fixed direction’ responses are thus fundamentally
different from the compass used for migratory orientation.
Their biological significance is unclear. They are observed
only under light regimes that never occur in nature, so that
an imbalance of the activation of receptors of the visual
system might interfere with the magnetic information
provided by the radical pair processes. Hence, they may
simply reflect the response of a reception system driven
beyond its limits. On the other hand, these responses do
suggest a complex interaction between the light regime and
the iron-based receptors which, in this case, also seem to
provide directional input. This input, however, cannot be
used to locate the migratory direction; instead, it leads to
directional preferences that do not seem to be meaningful.
It controls behavior only in some situations where the
normal inclination compass no longer works; yet in others,
it does not do so, such as when birds are treated with weak
oscillating fields, where disorientation (see Fig. 11) rather
than a ‘fixed direction’ response is observed. The interac-
tions between the two systems require further analysis.
Two types of receptors for different tasks
In birds, the available data indicate the existence of two
magnetoreceptor systems that normally mediate different
types of information, as pointed out in Table 2: a radical
pair mechanism in the right eye mediates directional
information, and magnetite-based receptors in the upper
beak record differences in magnetic intensity. One might
say that birds have a compass in their right eye and a
magnetometer in their beak. Together, the two mechanisms
provide different components of the navigational system
that supplement each other (Fig. 16) when birds navigate
across long distances (for review, see Wiltschko and
Wiltschko 2003).
Where the two components finally converge is still
unknown. The directional input from the iron-based
receptors in the upper beak also represents a still unex-
plained phenomenon. In view of these and other open
questions, we can only hope that the ‘magnetic sense’ of
birds continues to receive great interest and that research in
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S74 J Ornithol (2007) 148 (Suppl 1):S61–S76

Table 2 The two types of magnetoreception in birds

Parameter of the geomagnetic field
Magnetic vector Intensity gradient

Function in the avian navigation system
Physical mechanism underlying the
reception process
Location of the receptors
Nerve structures and brain areas involved
as identified by electro-physiological studies
Directional orientation: magnetic compass
Radical pair processes in photopigments
Retina of the right eye
Visual system: optic nerve, nBOR,
tectum opticum
Determining position: ‘map’ and
serving as ‘trigger’
Processes involving iron-oxide particles
Upper beak and/or ethmoid region
Trigeminal system: ophthalmic
nerve, trigeminal ganglion

Beason RC, Dussourd N, Deutschlander M (1995) Behavioural

Fig. 16 Schematic diagram illustrating the use of the different types
of magnetic information in the navigational system (after Wiltschko
et al. 2006)
the years to come will lead to a better understanding of how
birds perceive and process magnetic information.
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