ArticlePDF Available

Magnetic Orientation in Animals

Authors:

Abstract and Figures

Animals use the geomagnetic field in many 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. A magnetic compass is widespread among animals, magnetic navigation is indicated e.g. in birds, marine turtles and spiny lobsters and the use of magnetic 'sign posts' has been described for birds and marine turtles. For magnetoreception, two hypotheses are currently discussed, one proposing a chemical compass based on a radical pair mechanism, the other postulating processes involving magnetite particles. The available evidence suggests that birds use both mechanisms , with the radical pair mechanism in the right eye providing directional information and a magnetite-based mechanism in the upper beak providing information on position as component of the 'map'. Behavioral data from other animals indicate a light-dependent compass probably based on a radical pair mechanism in amphibians and a possibly magnetite-based mechanism in mammals. Histological and elec-trophysiological data suggest a magnetite-based mechanism in the nasal cavities of salmonid fish. Little is known about the parts of the brain where the respective information is processed.
Content may be subject to copyright.
REVIEW
Wolfgang Wiltschko Æ Roswitha Wiltschko
Magnetic orientation and magnetoreception in birds and other animals
Received: 27 October 2004 / Revised: 4 March 2005 / Accepted: 5 March 2005 / Published online: 11 May 2005
Springer-Verlag 2005
Abstract Animals use the geomagnetic field in many
ways: the magnetic vector provides a compass; magnetic
intensity and/or inclination play a role as a component
of the navigational ‘map’, and magneti c conditions of
certain regions act as ‘sign posts’ or triggers, eliciting
specific responses. A magnetic compass is widespread
among animals, magnetic navigation is indicated e.g. in
birds, marine turtles and spiny lobsters and the use of
magnetic ‘sign posts’ has been described for birds and
marine turtles. For magnetoreception, two hypotheses
are currently discussed, one proposing a chemical
compass based on a radical pair mechanism, the other
postulating processes involving magnetite particles. The
available evidence suggests that birds use both mecha-
nisms, with the radical pair mechanism in the right eye
providing directional information and a magnetite-
based mechanism in the upper beak providing infor-
mation on position as component of the ‘map’.
Behavioral data from other animals indicate a light-
dependent compass probably based on a radical pair
mechanism in amp hibians and a possibly magnetite-
based mechanism in mammals. Histological and elec-
trophysiological data suggest a magnetite-based mech-
anism in the nasal cavities of salmonid fish. Little is
known about the parts of the brain where the respective
information is processed.
The geomagnetic field
Many anima ls are able to perceive the magnetic field of
the earth; among them are mollusks, arthropods and
members of all major groups of vertebrates. This seems
alien to us, as man cannot consciously sense the geo-
magnetic field (but see Baker 1989). To fully understand
this phenomenon, we must first consider the type of
information the geomagnetic field can provide and—e-
ven more important—the type of information animals
do actually use.
The earth itself is a huge magnet, with its poles sit-
uated 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 re-enter at the
northern magnetic pole. As a consequence, the magnetic
field lines point upward on the southern hemisphere, run
parallel to the earth’s surface at the magnetic equator
and point downward in the northern hemisphere .
Magnetic inclination or dip, the angle between the local
magnetic vector and the horizontal, changes continu-
ously, showing a fairly regular gradient, from 90 at
the southern magnetic pole to +90 at the northern
magnetic pole, being 0 at the magnetic equator (Fig. 1).
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. It thus forms
gradients running from the poles to the equator on each
hemisphere (see Skiles 1985 for details). This regular
field can be locally distorted by material in the upper
crust resulting in magnetic anomalies with slight in-
creases or decreases in intensity. It is temporally altered
by electromagnetic radiation originating in the sun
causing daily variations, which, in the temperate lati-
tudes, lead to slight decrease in magnetic intensity
around noon; occasional magnetic storms may cause
more pronounced changes in all magnetic parameters.
These changes, however, are mostly small compared to
the regular field.
The geomagnetic field thus represents a reliable,
omnipresent source of navigational information. This
information can be of two kinds: the magnetic vector
provides directional information that animals could use
as a compass, whereas total intensity and/or inclination
may provide information that might be used as a com-
ponent of the navigational ‘map’ indicating position.
W. Wiltschko (&) Æ R. Wiltschko
Zoologisches Institut der J.W.Goethe-Universita
¨
t Frankfurt,
Siesmayerstr. 70, 60054 Frankfurt am Main, Germany
E-mail: wiltschko@zoology.uni-frankfurt.de
J Comp Physiol A (2005) 191: 675–693
DOI 10.1007/s00359-005-0627-7
Magnetic orientation
Animals have been shown to use both types of
information for vari ous tasks. However, our knowl-
edge on magnetic orientation differs greatly between
the various animals. Birds are by far the best studied
group, followed by marine turtl es, while little is
known about other vertebrates and arthropods. Here,
we summarize the findings that are most important in
demonstrating how widespread the use of magnetic
information is and what types of information the
animals utilize.
Magnetic compass orientation
A magnetic compass means that directions can be
determined with the help of the magnetic field. In ori-
entation experiments, the observation that an animal
responds to shift in magnetic North with a corre-
sponding change in its heading is diagnostic of magnetic
compass use.
Demonstrating magnetic compass orientation
A magnetic compass appears to be rather widespread
among animals. It was first demonstrated in migratory
birds, taking advantage of a spontaneous behavior:
during migration season, the urge of migrants to move
into migratory direction is so strong that even captive
birds head into the respective direction in their cages.
When tested in the local geomagnetic field, European
robins, Erithacus rubecula, but also other species of
migrants, showed a strong preference of their seasonally
appropriate migratory direction. Tested in an experi-
mental 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 accordin gly
and preferred the direction that now corresponded to the
same magnetic course (Fig. 2, left, center). This clearly
shows that robins used the geomagnetic field to orient
their movements (see Wiltschko and Wiltschko 1995 for
details).
Meanwhile, magnetic compass orientation has been
described for a number of other birds, such as several
passerine migrants, homing pigeons (Walcott and Gr een
1974) and a shorebird species (Gudmundsson and
Sandberg 2000 ). A magnetic compass has also been
demonstrated in numerous other animals, including
members of the other major groups of vertebrates,
crustaceans, insects and a mollusk species (see Table 1).
The behaviors involved range from spontaneous
behavior, like e.g. the headings of sockeye salmon fry,
Oncorhynchus nerka (Quinn 1980) or building a nest in
Zambian mole rats, Cryptomy s sp. (Marhold et al.
1997a), over directions set by other environmental fac-
tors, like in hatchling marine loggerhead turtles Caretta
caretta heading away from the shore (e.g. Lohmann
1991), y-axis orientation of various arthropods (e.g.
Pardi et al. 1988) and the salamander Notophthalmus
viridescens (e.g. Phillips 1986) at the border land/water,
building activities in honeybees, Apis mellifera (e.g.
DeJong 1982) and compass termites, Amitermes merid-
ionalis (Duelli and Duelli-Klein 1978; Jacklyn and
Munro 2002) to directional training and other acquired
directions (for summary, see R. Wiltschko and Wilt-
schko 1995).
Functional mode of magnetic compass mechanisms
The functional mode of the magnetic compass was first
analyzed in birds, again with the help of migratory ori-
entation. Two unexpected properties became evident.
In contrast to our technical compass, the avian
magnetic com pass was found to be an inclination com-
pass’, based on the inclination of the field lines instead of
their polarity. Apparently, birds can only perceive the
axial course of the field lines; to derive non-ambiguous
directional information, they must interpret the incli-
nation of the field lines with respect to up and down.
This was demonstrated in a magnetic field where the
vertical component was inverted: birds heading north in
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. The magnetic poles and the magnetic equator are
marked in red (after Wiltschko and Wiltschko 1995)
676
the geomagnetic field reversed their heading, now pre-
ferring magnetic South (Fig. 2, right diagram). Revers-
ing the horizontal component and inverting the vertical
component alter the axial course of the field lines in the
same way (Fig. 3); an animal not perceiving the polarity
of the magnetic field will not realize any difference.
Hence birds reverse their headings in both situations
alike (Wiltschko and Wiltschko 1972). This means that
the avian magnetic compass does not distinguish be-
tween mag netic ‘north’ and ‘south’ as indicated by
polarity, but between ‘poleward’ where the field lines
point to the ground, and ‘equatorward’, where they
point upward (Fig. 3).
All bird species studied so far use an ‘inclination
compass’. Yet this is not the only type of magnetic
compass found in animals. Sea turtles possess an
inclination compass like birds (Light et al. 1993;
Lohmann and Lohmann 1992), whereas salmon
(Quinn and Brannon 1982) and rodents (Marhold
et al. 1997a) have a polarity compass based on the
polarity of the field lines (see Table 1, last column):
they do not reverse their headings when the vertical
component is inverted (Fig. 4). The latter seems to
apply also for the few invertebrate species analyzed so
far (e.g. Lohmann et al. 1995). Salamanders were first
reported to use both types of mechanisms, an inclina-
tion compass for shoreward orientation and a polarity
Fig. 2 Orientation behavior of migrating European Robins in
spring, tested in the local geomagnetic field and in two experimental
fields. 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; Wiltschko et al. 2001)
Table 1 Animals demonstrated
to use a magnetic compass
(numbers in parentheses give
the number of species where the
respective type of compass is
indicated; ??? means that the
type of compass has not yet
been analyzed)
Systematics No. of
orders
No. of
families
No. of
species
Type of
compass?
Mollusks
Snails 1 1 1 ???
Arthropods
Crustacean 3 3 5 Polarity compass (1)
Insects 6 7 9 Polarity compass? (1)
Vertebrates
Cartilageous fish 1 1 1 ???
Bony fish 2 2 4 Polarity compass? (1)
Amphibians 1 2 2 Inclination compass (1)
Reptilians 1 2 2 Inclination compass (2)
Birds 3 11 20 Inclination compass (8)
Mammals 2 2 3 Polarity compass (1)
Fig. 3 Vertical section through the geomagnetic field to illustrate
the functional mode of the inclination compass. N, S, magnetic
North and South.H, magnetic vector, with H
e
, the vector of the
geomagnetic field; H
h
, H
v
, horizontal and vertical component,
respectively; g, gravity vector. » p «, » e « , ‘poleward’ and
‘equatorward’, the readings of the inclination compass. The bird
flies ‘poleward’
677
compass for homing (Phillips 1986); however, as
magnetic parameters are also involved in determini ng
the home course, the data were interpreted to suggest a
polarity compass for homing may also reflect an effect
on the mechanisms determining this course (Phillips
and Borland 1994), leaving the inclination compass as
the only compass mechanism demonstrated in sala-
manders.
Another surprising finding in birds was that their
magnetic compass is closely tuned to the total intensity
of the ambient field. When the intensity of an experi-
mental field was reduced or increased by 20–30%, birds
were no longer oriented, suggesting a rather narrow
functional window (Fig. 5). This window is not fixed,
however, but adjusts to lower or to higher intensities
when birds are exposed to these intensities for three
days, but possibly also after a much shorter period 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. (see
Fig. 5; Wiltschko 1978). This indicates that the newly-
gained ability to orient in higher or lower fields rep-
resents neither a shift nor an amplification of the
functional range. Apparently, birds can orient only in
field intensities they experienced before, with this
experience possibly forming a new functional range.
The magnetic compass of other animals has not yet
been analyzed in view of a functional window of lim-
ited range.
Non-compass use of the magnetic field
Because of their nature as gradients runnin g from north
to south, magnetic intensity and inclination can give
information on position. Evidence for this use of mag-
netic 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’ of pigeons ever since the late
nineteenth century (Viguier 1882). It could be used in
the following way: in the northern hemisphere, birds
know by experience that magnetic intensity increases
towards north; when finding themselves at a location
with intensity higher than at home, they would con-
clude that they are north of home and hence must head
south to return. The intensity differenc e to be detected
for magnetic navigat ion within the home range would
be in the order of magnitude of 20 to 100 nT, the
Fig. 5 Orientation responses of robins in magnetic fields of
different total intensities indicating the functional window of the
avian magnetic compass (shaded in blue ). It is narrowly tuned to the
intensity in which the bird is living; keeping birds at other
intensities gives rise to a new functional window at the respective
intensity. The intensity of the local geomagnetic field, 46,000 nT, is
marked by a dashed line (data from Wiltschko 1978)
Fig. 4 Orientation of mole rats
Cryptomys sp.(Rodentia) in the
geomagnetic field and in two
experimental fields. The
triangles at the periphery of the
circle mark the direction of the
nest position from the center of
the arena; the arrow represents
the mean vector proportional to
the radius of the circle (data
from Marhold et al. 1997a)
678
differences in inclination in fractions of a degree,
depending on the regional gradients and the distances
involved.
First indications that animals use magnetic parame-
ters in their navigational ‘map’ came from correlations
of the vanishing bearings of homing pigeons, Columba
livia f. domestica, with temporal changes of the magnetic
field (e.g. Keeton et al. 1974). Pigeons released in a
magnetic anomaly showed an increase in scatter up to
disorientation that was strongly correlated with steep-
ness of the local intensity gradient (Walcott 1978). The
effects of various magnetic treatments on pigeons’ init ial
Fig. 6 True navigation by
magnetic parameters indicated
in spiny lobsters. The lobsters
were tested near their capture
site in magnetic fields
replicating the ones of two
distant geographic locations
(marked with asterisks). In the
circular diagrams, the small
arrows outside the circle
indicate the home directions
from the simulated sites. Dots at
the periphery of the circle mark
the headings of single lobsters;
the arrow represents the mean
vector proportional to the
radius of the circle, with the
dashed radii indicating the 95%
confidence interval of the mean
direction (after Boles and
Lohmann 2003)
Fig. 7 Specific magnetic
conditions acting as ‘sign posts’
in Pied Flycatchers: orientation
of hand-raised birds tested in
cages during their first autumn
migration. Left diagrams: birds
tested in the local magnetic field
of Frankfurt a.M. (46,000 nT,
66 inclination) during the
entire migration season; right
diagrams: birds tested in
magnetic fields simulating in
four steps the decrease in
intensity and inclination to
34,000 nT, 10 inclination Pied
Flycatchers would normally
experience during autumn
migration. Symbols as in Fig. 2
(data from Beck and Wiltschko
1988)
679
orientation that cannot be attributed to interfering with
the magnetic compass also suggested an involvement of
magnetic factors in the navigational process (for sum-
mary, see Wiltschko and Wiltschko 1995). Migratory
Australian Silvereyes, Zosterops lateralis, also responded
to slight changes in magnetic intensity and inclination
(Fisher et al. 2003).
Recently, however, more direct evidence for the use
of magnetic factors as navigational parameter s became
available: When spiny lobsters Panulirus argus were
captured and exposed at their capture site to magnetic
conditions found at a distant site, they headed into the
direction that would have brought them home from that
distant site (Fig. 6; Boles and Lohmann 2003 ). Similar
results also indicating true navigation by magnetic
parameters have now also been reported for subadult
green sea turtles, Chelonia mydas (Lohmann et al. 2004).
In salamanders Notophthalmus viridescens, a response to
changes in the angle of inclination alone has been de-
scribed (Phillips et al. 2002a).
Magnetic conditions as ‘sign posts’ or triggers
Total intensity and/or inclination may also serve as
‘sign-posts’, marking specific regions where animals
must act in a specific way. The respective responses are
innate and are elicited when the animals encounter the
crucial 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, in this way travelling around the
Alps, the Mediterranean Sea and the central Sahara.
Hand-raised birds of this population started autumn
migration with southwesterly preferences when tested in
cages in the local geomagnetic field of central Europe;
however, they showed the change in direction only when
they experienced the magnetic field of northern Africa
(Fig. 7; Beck and Wiltschko 1988). Apparently, these
magnetic conditions serve as a ‘sign post’ and initiate the
second leg of migration. Likewise, in Garden Warblers,
Sylvia borin, transequatorial migrants, a horizontal field
caused a reversal in headings here, the field of the
equator serves as trigger, eliciting the change in magnetic
heading from ‘equatorward’ to ‘poleward’ that enables
these birds to go on into the southern hemisphere
(Wiltschko and Wilts chko 1992). The function of mag-
netic parameters as ‘sign post’ is not restricted to ori-
entation responses, however; it also includes
physiological responses. Thrush nighting ales, L. lusc inia,
caught and held in Sweden, showed a slow weight gain
during autumn migra tion; simulation of the specific
magnetic condition of northern Egypt induced a much
more rapid gain in weight; during real migration, this
extra fat load enables these birds to cross the vast eco-
logical barrier of the Sahara (Fransson et al. 2001).
Other well-documented cases of magnetic conditions
of certain regions eliciting specific responses have been
reported from young loggerhead turtles. Juvenile turtles
from Florida spend the first years of their life in the
Atlantic gyre; conditions found at the edge of the
Atlantic gyre caused them to prefer headings that would
lead them back into the gyre and thus prevent them from
leaving the normal range of their population. Here,
intensity, incl ination and a combination of both proved
effective (Fig. 8; Lohmann and Lohmann 1994, 1996;
Lohmann et al. 2001).
Implications for magnetoreception
The behavioral evidence summarized above clearly
shows that magnetoreception is not a uniform phenom-
enon: animals use different parameters of the geoma g-
netic field in different tasks. The nature of these
parameters makes it rather unlikely that they are de-
tected by the same mechanism. The magnetic compass
does not respond to the small differenc es in intensity
whose detection is crucial for usi ng magnetic intensity as
component of the navigational ‘map’; these small chan-
ges are well within the functional window of the compass
mechanism and are thus filtered off. Likewise, a mecha-
nism designed to record tiny changes in intensity can, at
the same time, hardly measure the direction of the
magnetic field with great precision. Hence we must ex-
pect animals to have specialized receptors for mediating
magnetic intensity and others for mediating information
on magnetic direction, just as we use different technical
devices a compass and a magnetometer to measure
Fig. 8 Orientation of hatchling loggerhead turtles tested in
magnetic field characteristic for three locations (marked by dots)
at the edge of the Atlantic gyre (indicated by small arrows).
Symbols in the circular diagrams as in Fig. 6 (from Lohmann et al.
2001)
680
the direction and the intensity of the magnetic field.
Additionally, the two types of magnetic compass
inclination compass and polarity compass imply that
here, too, different mechanisms may be involved.
Magnetoreception
For a complete understanding of a ‘magnetic sense’, one
needs to know (1) details on the primary processes
mediating 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 in-
volved in processing magnetic information. Unfortu-
nately, our knowledge on the physiological and
neurobiological processes associated with magnetore-
ception is still rather limited. The various animal groups
are not equally represented: birds are by far the best
studied group; fish are the only other group where some
neuroanatomical and electrophysiological evidence is
available.
A number of models for mag netoreception based on
fundamentally different principles have been prop osed,
the three most prominent ones being (1) induction, (2)
interactions of chemical processes with the ambient
magnetic field and (3) processes involving permanently
magnetic material.
Induction would be restricted to marine animals be-
cause it requires sea water as a surrounding medium
with high conductivity. When skates and rays swim into
different directions, they cross the field lines of the
geomagnetic field at different angles, thus inducing dif-
ferent voltages at their electric organs (Murray 1962).
The ampullary organs of skates and rays are known to
be sensitive enough to detect the differences in voltage
induced when the fish are heading in different directions
(e.g. Kalmijn 1978), but evidence that this information is
indeed used to derive compass orientation is still lacking.
The other two models the ‘radical pair’-model and
the magnetite-hypothesis are more general and would
also ser ve terrestrial animals and those living in fresh
water.
Magnetoreception based on ‘radical pair’-mechanisms,
and associated findings
The radical pair model, first proposed by Schulten and
Windemuth (1986) and later detailed by Ritz et al.
(2000), postulates a ‘chemical compass’ based on direc-
tion-specific interactions of radical pairs with the
ambient magnetic field. It is supported by experimental
evidence in birds and amphibians.
The model
In the initial step, the radica l pair model assumes that
specialized photopigments absorb a photon and are
elevated to the singlet excited state. They form singlet
radical pairs with antiparallel spin, which, by singlet–
triplet interconversi on, may turn into triplet pairs with
parallel spin (Fig. 9). The magne tic 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 magnetic field (for
details, see Ritz et al. 2000) it can thus convey infor-
mation on magnetic directions. As receptor molecule,
Ritz and colleagues (2000) suggested cryptochromes, a
class of photopigments known from plants and related
to photolyases (Sancar 2003); they possess chemical
properties crucial for the model, including the ability to
form radical pairs (Giovani et al. 2003).
To obtain magnetic compa ss informa tion by a radical
pair mechanism, animals must take advantage of the
fact that triplet products are chemically different from
singlet products and compare the triplet yields in dif-
ferent directions. This requires an orderly array of
photopigments oriented in the various spatial directions.
These conditions could be met by the more or less
spherical arrangement of receptors in the eyes radical
pair processes would generate characteristic patterns of
activation across the retina (Ritz et al. 2000). These
patterns whose specific manifestations depend on mag-
netic intensity, would be centrally symmet ric around the
axis of the field lines, that is, axial rather than polar, and
would enable animals to detect the direction of the
ambient field. At the same time, the initial photon
absorption would make magnetoreception a light-
dependent process.
Evidence supporting the radical pair model
Because of the axial pattern of activation, a radical pair
mechanism would provide an inclination compass.
Fig. 9 Schema of a radical pair mechanism: a donor 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 thus may play a role in magnetoreception
(modified from Ritz et al. 2000)
681
Hence the radical pair model can only apply to the
magnetic compass of birds, amphibians and marine
turtles (see Table 1). In birds, this model also provides
an explanation for the narrow functional window of the
magnetic compass that can be altered by exposing them
to magnetic intensiti es outside the normal functional
range (see Fig. 5): when tested under intensities that
differ markedly from that of the local geomagnetic field,
the birds would be faced with a nove l activation pattern
(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, the birds may be-
come familiar with the novel pattern and learn to
interpret it, thus regaining their ability to orient.
The radical pair model predicts that magnetorecep-
tion is light-dependent. Light is indeed required for
magnetic compass orientation in birds and salamanders.
First evidence came from beha vioral experiments with
young homing pigeons that use their magnetic compass
to record the direction of displacement: 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 Wilt-
schko 1978). Disorientation in the absence of visible
light was also observed in the salamander Notophthal-
mus viridescens (Phillips and Borland 1992a ). Later tests
revealed a wavelength-dependency of the magnetic
compass in amphibians (Phillips and Borland 1992b),
migratory birds and pigeons (see Wiltschko and Wilt-
schko 2002). Marine turtles, on the other hand, proved
well orien ted in total darkness (Lohmann 1991;Loh-
mann and Lohmann 1993). Although an inclination
compass is involved here, magnetoreception as proposed
by the radical pair model appears unlikely, unless there
is a yet unknown way that radical pairs could be gen-
erated in total darkness.
Demonstrating a radical pair mechanism
A diagnostic test based on magnetic resonance aimed at
obtaining dir ect evidence for a radical pair mechanism
underlying the avian magnetic compass. If the triplet yield
is crucial for magnetoreception, interfering with the sin-
glet-triplet interconversion should alter the output of the
receptors markedly and thus disrupt magnetoreception.
The singlet–triplet interconversion rate can be signifi-
cantly affected by oscillating fields of specific frequencies
in the MegaH ertz range (Ritz et al. 2000). The intensities
required for these resonance effects are so low that they
would not affect any of the magnetite-based mechanisms
currently considered (as explained below), so that a dis-
ruption of magnetic orientation would be diagnostic for
the involvement of a radical pair mechanism.
At present, it is not easy to predict exactly which
specific frequencies will interfere with the radical pair
mechanisms underlying magnetoreception, because the
chemical compos ition and the geometric structures of
molecules involved are not yet known; theoretical
considerations and in vitro studies indicate that they are
to be expected in the 0.1–10-MHz range. The effect of
the oscillating fields should depend on their orientation
with respect to the static background field (Cran field
et al. 1994). These resonances are generally very broad
and might therefore lead to disturbing effects at virtually
all frequencies within this range, provided the intensity
of the oscillating field is sufficiently strong (Henbest
et al. 2004). However, a special resonance occurs when
the frequency of the oscillating field matches the ener-
getic splitting induced by the static geomagnetic field;
here, one expects a marked effect regardless of the
structure of the molecules forming the radical pairs. For
the 46,000 nT geomagnetic field of Frankfurt, this fre-
quency is 1.315 MHz (see Thalau et al. 2005).
First tests with a weak broad band noise field of
frequencies from 0.1 MHz to 10 MHz added to the
geomagnetic field indeed showed that this disrupted the
orientation of migratory birds (Ritz et al. 2004). Further
tests used the single frequencies of 1.315 and 7.0 MHz
with an intensity of about 480 nT. When these fields
were presented parallel to the geomagnetic vector, the
birds were oriented in their migratory direction, whereas
they were disoriented when the same fields were pre-
sented at an angle of 24 or 48 to the geomagnetic field
(Fig. 10; Ritz et al. 2004; Thalau et al. 2005). This is in
agreement with the radical pair model and clearly shows
that the observed effect of high-frequency field is a
specific one. Together, these findings indicate that the
primary process of magnetoreception in birds involves a
radical pair mechanism.
Interactions of at least two receptors
If photopigments were involved, these pigments can
hardly be expected to absorb light over the entire range
of the visual spectrum hence magnetoreception should
Fig. 10 Orientation of European Robins in the geomagnetic field
(Control, C) and in high-frequency fields added to the geomagnetic
field in two different orientation. The upper part of the diagram
illustrated the orientation of the geomagnetic field and the high-
frequency field in the three test conditions; symbols in the circular
diagrams as in Fig. 2 (data from Thalau et al. 2005)
682
depend on the wavelength of light. A wavelength-
dependency of magnetic compass orientation was re-
ported for salamanders, passerine birds, and homing
pigeons. In the respective experiments, salamanders and
birds were tested under monochromatic lights of various
wavelength and intensities. By reflecting the absorption
ranges of the crucial pigments, these studies may indi-
cate the number of receptors involved and how they
interact.
Salamanders Salamanders show a wavelength depen-
dency that is characterized by normal orientation only in
a rather narrow wavelength band at the short-wave-
length end of the spectrum and a variety of responses
induced by long-wavelength light, with the specific
manifestations of these responses attributed to different
motivational stages. Salamanders manipulated to head
shoreward showed normal orienta tion only up to
450 nm; at 475 nm, they were disoriented; and under
wavelength of 500 nm an d beyond, their headings were
shifted by approximately 90 counterclockwise. When
the animals were kept under long wavelength light with
k>500 nm, they showed a mirror-image clockwise shift
under ‘white’ light, but headed shoreward under long-
wavelength light (Phillips and Borland 1992b). To ex-
plain these findings, the authors suggested two antago-
nistic spectral mechanisms indicating directions
perpendicular to each other. Only the short wavelength
receptor was to indicate the correct magnetic directions,
while the long-wavelength receptor activated by most of
the visual spectrum indicated shifted ones. To reconcile
these findings with the normal orientation observed
under ‘white’ light, where both receptors are stimulated,
the authors postulate that the signal of the short-wave-
length dominates over the contradicting input (Phillips
and Borland 1992b; Phillips et al. 2001). Since a spectral
mechanism providing animals with false information is
difficult to accept, Phillips and Deutschlander (1997)
speculated about the two spectral mechanisms being
connected, possibly being essential components of the
same biochemical process.
When the salamanders were manipulated to head
homeward, however, they were normally oriented only
under 400 nm light and disoriented under wavelength of
450 nm and beyond (Phillips and Borland 1994). The
authors attributed this disorientation to the false com-
pass readings under long-wavelength light, which no
longer allow the ‘map’-rec eptors to work properly and
determine the home course. Held under long-wavelength
light, the salamanders now preferred an axis that
roughly corresponded with the magnetic north-south
axis under both, ‘white’ and long-wavelen gth light
(Phillips et al. 2002b). This response was discussed as
being related to alignments and possibly controlled by
tiny magnetite particles in the heads of the salamanders.
Birds Most tests with birds used migratory orientation
as a criterion whether or not normal directional infor-
mation from the magnetic field could be obtained in a
given situation. Migratory birds have not only been
tested under different wavelengths, but also under dif-
ferent intensities and under combinations of two
monochromatic lights. Their responses under the vari-
ous light regimes indicate highly complex interactions
between at least two, possibly more, receptors.
Wavelength-dependency: European Robins were tes-
ted under monochromatic light produced by light-
emitting diodes (LEDs) with a half band-width of 30–
50 nm. Their behavior at various wavelengths revealed
the following pattern: magnetic orientation was possible
under 424 nm blue, 510 nm turquoise and 565 nm green
light, whereas under 590 nm yello w and 635 nm red, the
birds were disoriented (Fig. 11; Wiltschko and Wilt-
Fig. 11 Orientation behavior of
European robins in spring
under monochromatic lights of
different wavelength (indicated
in the circles); symbols as in
Fig. 2. (after W. Wiltschko and
Wiltschko 2002)
683
schko 1999). Experiments using interference filters with
a half-band width of only 10 nm could narrow down the
onset of disorientation in robins even further to between
561 nm and 568 nm (Muheim et al. 2002). This pattern
seems to be common to passerine species and homing
pigeons (Fig. 12; see Wiltschko and Wiltschko 2002).
That is, in contrast to salamanders, the spectral range
where birds obtain normal magnetic compass
information includes the larger part of the visual spec-
trum. At the same time, this wavelength dependency of
magnetoreception shows no relationship to the peaks of
the four color cones of the birds’ visual system (see
Maier 1992) and thus speaks against their involvement
in mediating magnetic directions, suggesting the exis-
tence of another type of receptor. The birds’ respon se
looked like an ‘all-or-none’-response that could be
attributed to one receptor, yet the rather abrupt transi-
tion to disorientation, which persisted under increased
intensity of the yellow or red light (Wiltschko and
Wiltschko 2001; Wiltschko et al. 2004a), seems to sug-
gest an antagonistic interaction with a second receptor.
A second receptor with peak absorption at long
wavelengths is also indicated by another finding. Al-
though 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 test (Mo
¨
ller et al. 2001; Wiltschko et al. 2004a).
The orientation induced this way proved to be normal
migratory orientation. This ability to orient after having
been pre-exposed to the test condition shows an inter-
esting parallel to the ability to adjust the functional
window to magnetic intensities outside the normal
functional range (Wiltschko 1978) and may be based on
similar mechanisms, namely learning to interpret a novel
pattern of activation. The disorientation normally ob-
served under red light suggests that under ‘white’ light,
the long-wavelength receptor forms the minor compo-
nent of a complex respon se pattern. Presented by itself ,
it would seem novel, but it would also be centrally
symmetric to the axis of the field line s. Birds suddenly
faced with this pattern alone might need a certain time
until they are able to recognize its general characteristic
and interpret it to derive magnetic directions (for a more
detailed discussion, see Wiltschko et al. 2004b).
Fig. 12 Oriented behavior of
four birds species tested under
monochromatic light produced
by light-emitting diodes
(LEDs). Upper part of the
diagram: spectra of the test
lights; lower part: (+) oriented
behavior or () disoriented
behavior observed at the
respective wavelengths (after
W. Wiltschko and Wiltschko
2002)
Fig. 13 Orientation behavior of European robins under the same
565 nm green light at different intensities; the respective quantal
flux (in quanta m
2
s
1
) is indicated in the circular diagrams.
Symbols as in Fig. 2
684
Effect of higher intensities: The findings mentioned so
far were obtained under rather low light levels of 6–
9·10
15
quanta s
1
m
2
, an intensity found in nature
more than half an hour after sunset or before sunrise.
This seemed to be appropriate, because the passerine
species tested were either nocturnal migrants or migrat-
ing during the twilight hours. When the light intensity
was increased six times, birds were still disoriented under
yellow and red light (see above), but under light from the
blue-to-green part of the spectrum, a marked change in
behavior was observed: passerine migrants no longer
preferred their natural migratory direction, but instead
showed axial preferences or odd unimodal tendencies
(Wiltschko et al. 2000, 2003b ; Wiltschko and Wiltschko
2001). Tests at the same wavelength of light showed that
changes in intensity led to different responses: e.g. under
565 nm green light, robins first showed normal migra-
tory orientation, then disorientation, followed by pref-
erence of the east–west-axis and finally a preference of
the north–south-axis, depend ing on intensity (Fig. 13;R.
Wiltschko and R. Wiltschko, unpublished data). The
unimodal preferences observed at higher intensities were
‘fixed directions’ in the sense that they did not show the
normal seasonal change between spring and autumn
(Wiltschko et al. 2000). They were found to be funda-
mentally different from migratory orientation, as they
also did not depend on the inclination compass normally
used by birds (Wiltschko et al. 2003b).
The nature of these odd responses is not yet clear.
The axial preferences show some similarities to align-
ments, but unimodal tendencies in directions other than
the migratory direction (e.g. Wiltschko et al. 2000,
2004b) are hard to explain. As motivational differences
can largely be excluded, they imply that the magnetic
receptors no longer provide information that can be
used to locate the migratory course. Yet the light with
identical spectral compositions, but lower intensity, al-
lows excellent migra tory orientation. The light levels of
these brighter lights were still fairly low on a sunny
day, the natural light is brighter by powers of ten. Hence
saturation of the receptors appears highly unlikely. Be-
cause ‘white’ light of high intensity allows normal ori-
entation, the reason for the odd responses seem to lie in
the near monochromatic nature of the light consisting of
a narrow band of wavelengths only. Speculating on why
this should matter leads to considerations about the
interaction of the input of various receptors at higher
centers. The number of receptors involved in magneto-
reception is still unclear, but if they were more than one
or two, monochromatic light would stimulate one
receptor strongly, while others are not stimulated at all.
This could result in an imbal ance of input at higher units
where the input of these receptors converge. The other
receptors may also be specialized on magnetic input, or
they may involve the cones of color vision which might
provide background information of the general light
level. Possibly, as long as the quantal flux is so low that
the cones are not activated, monochromatic light from
the blue-to-green part of the spectrum allows normal
orientation; if the monochromatic lights are strong en-
ough to activate the cones, however, the resulting
imbalance might affect the processing of magnetic input
in a way that the information content of magnetic input
changes its general characteristics.
Bichromatic test lights: A combination of light from
the blue-to-green part of the spectrum with 590 nm
yellow light also leads to unimodal responses that no
longer coincided with the natural migratory direction.
These responses were likewise ‘fixed directions’, as they
failed to show the normal seasonal change (Wiltschko
et al. 2004b). The responses to bichromatic light com-
bined from wavelengths where birds normally show
excellent orientation, and yellow light, where they are
disoriented when it is presented alone, clearly show that
yellow light is not neutral, also pointing out interactions
between at least two receptors that have not yet been
fully understood. Interestingly, the specific response
depended on the wavelength from the blu e-to-green part
of the spectrum: robins preferred northerly headings
under green- and-yellow, southeasterly headings under
turquoise-and-yellow and southerly headings under
blue-and-yellow (Wiltschko et al. 2004b; Stapput et al.
2005). Apparently, the receptor(s) activated by light
from the blue-to green part of the spectrum, although no
longer providing magnetic compass information for
locating the migratory direction, are active and deter-
mine the specific directions of the ‘fixed’ headings.
Similar patterns in bird s and amphibians? The findings
described above indicate that certain light regimes drive
the reception mechanisms for compass information to-
wards their limits, leading to odd responses that cannot
yet be explained. In birds, specific combinations of
wavelengths as well as monochromatic light above a
certain quantal flux result in such responses. To what
extend this is also true for salamanders is unclear, be-
cause salamanders have not yet been tested under the
same wavelengths at different intensities. It is interesting
to note that the odd shifts in directions of salamanders
heading shoreward and the disoriented behavior of sal-
amanders heading homeward observed from 500 nm
onward (Phillips and Borland 1992b, 1994; Phillips et al.
2002b) were recorded at light intensities where birds no
longer prefer their migratory direction; at 400 nm, where
salamander always showed normal orientation, the light
intensity was markedly lower. Unfortunately, it is still
unknown how salamanders would respond to long
wavelengths at this lower light intensity. The manifesta-
tions of the responses under higher intensity unimodal
preference of unexplained directions, axial preferences
and disorientation are very similar in salaman ders and
birds. Hence it appears possible that the odd responses in
these two animal groups represent related phenomena,
which in salamanders depend not only on wavelength, as
described by Phillips et al. and colleagues (e.g. 2001), but
also on the intensity of light, reflecting a magnetorecep-
tion system functioning under borderline conditions.
Future studies will have to clarify this question.
685
The site of the light-dependent magnetoreceptors
Another question concerns the location of the magne-
toreceptors. Theoretical considerations favored the eyes
as site of magnetoreception because of their almost
spherical shape (Ritz et al. 2000 ) this prediction has
also been confirmed in birds, with the surprising findin g
that magnetore ception 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 birds failed to show oriented behavior when their
right eye was covered (Wiltschko et al. 2002a, 2003a). In
salamanders, however, the receptors were found to be
located in the pineal, the ancient third eye of vertebrates,
which in amphibians is directly sensitive to light. Critical
tests in which the skull above the pineal was covered
with a color filter, but the eyes were open to the natural
light, clearly showed that the magnetic compass in sal-
amanders depended solely on the spectral properties of
the light reaching the pineal (Deutschlander et al. 1999;
Phillips et al. 2001).
Cryptochromes, first known from plants, but recentl y
also discovered in animals (see Sancar 2003 for review)
have been suggested to form the radical pairs invo lved in
magnetoreception (Ritz et al. 2000). These photopig-
ments have been found in the retina of vertebrates, first
in mammals (Miyamoto and Sancar 1998), but also in
chicken (Haque et al. 2002) and recently in migrating
passerine birds. In Garden Warblers, Sylvia borin,
cryptochromes are located in the large displaced
ganglion cells (Mouritsen et al. 2004). In European
robins, two forms of cryptochrome 1, splice product of
the same gene, were identified, with the novel C-terminal
of the second form implying a novel function (Mo
¨
ller
et al. 2004). These findings support the idea that cryp-
tochromes may be involved in the radical pair processes
underlying the avian magnetic compass, yet direct evi-
dence for their crucial role is still lacki ng.
Neuronal pathways associated with the avian magnetic
compass
Our knowledge on the neural pathways and the parts of
the brain processing magnetic compass information is
rather limited; the available evidence comes entirely
from studies with birds. Electrophysiological recordings
in pigeons suggest that magnetic input is processed in
parts of the visual system. Recordings from the nucleus
of the basal optic root (nBOR) and from the tectum
opticum revealed units that responded to changes in
magnetic direction (Semm et al. 1984; Semm and De-
main 1986 ). These responses are in accordance with the
predictions of the radical pair model, as they were ob-
served only in the presence of light; they seem to origi-
nate 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, thus suggesting
the two types of receptors with different absorption
maxima, a finding that is in agreement with the behav-
ioral stud ies likewise indicating two types of receptors
with absorption peaks in the blue-to-green and in the
long-wavelength range (e.g. Mo
¨
ller et al. 2001; Wilt-
schko et al. 2004b).
Individual neurons in the nBOR as wel l as the tectum
opticum showed distinct peaks of response at particular
alignments of the magnetic field (Fig. 14). These varied
between cells so that the input of a number of units
Fig. 14 Electrophysiological responses recorded from direction-
selective cells in the nucleus of the basal optic root (nBOR) of
pigeons; the stimulus was a gradual change of magnetic inclination
from 62 downward to 62 upward (= vertical component
inverted). Left: responses of to individual units; right: different
neurons responding to different spatial directions of the magnetic
vector, with the horizontal bars indicating the range of augmen-
tation of electrical activity of representative neurons (data from
Semm et al. 1984)
686
would represent the various directions in spa ce model
(Semm et al. 1984; Semm and Demaine 1986). Processed
collectively and integrated, it would thus provide a
suitable basis for a compass as predicted by the radical
pair model.
The finding that magnetic input is mediated exclu-
sively by the right eye (Wiltschko et al. 2002a) indicates
a stong lateralization of the magnetic compass that ap-
pears to be rather widespread among birds (see Wilt-
schko et al. 2003a; Prior et al. 2004). Because of the very
few connections between the two hemispheres, it means
that magnetic information is processed almost exclu-
sively 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 (Gu
¨
ntu
¨
rku
¨
n 1997) which, aside from
the tectum opticum, comprises the nucleus rotundus,
where activation by magnetic stimuli was indicated by
the glucose method (Mai and Semm 1990). Together, the
few findings available suggest that magnetic input orig-
inating in the right eye shares neuronal pathways with
the visual system , being processed in the tectofugal
system of the left hemisphere of the brain. Other parts of
the brain involved in processing magnetic compass
information are yet to be determined.
Magnetoreception based on magnetite, and associated
findings
Magnetite is a specific form of iron oxide Fe
3
O
4
whose
general properties depend on the size and shape of the
particles (Fig. 15). Spin interactions cause the spins of
adjacent atoms to align, thus forming domains with all
spins parallel. Large particles include multiple domains
with their magnetic moments largely canceling each
other; particles in the range between about 1.2 lm and
0.05 lm consist of a single domain and have a stable
magnetic moment, acting as tiny permanent magnets.
Even smaller particles are superparamagnetic: at room
temperature, their magnetic moment fluctuates as a re-
sults of thermal agitation, but it can easily be aligned by
an external magnetic field (see Kirschvink et al. 1985 for
details).
The model
In the 197 0s, certain bacte ria were discovered to contain
chains of single domain magnetite (Blakemore 1975)
that act as magnets and align these bacteria along the
field lines of the geomagnetic field. Magnetic informa-
tion mediated by tiny magnets was an attractive idea,
and the existence of magnetic material of biogenic origin
caused authors to speculate about its potential role in
the orientation of higher animals.
Based on theoretical considerations, the magnetite
hypotheses propose a variety of models on how mag-
netite particles might mediate magnetic information,
some of them involving single domains (e.g. York e 1979;
Kirschvink and Gould 1981; Kirschvink and Walker
1985; Edmonds 1996), others superparamagnetic parti-
cles (e.g. Kirschvink and Gould 1981; Shcherbakov and
Winklhofer 1999). A uniform concept on how magne-
tite-based magnetoreceptors might work does not yet
exist. Interestingly, some of the models predict polar,
others 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
Fig. 16 Schematic reconstruction of structures found in the skin of
upper beak of pigeons, based on ultrathin section series. Above: the
terminal region of a nerve containing a scaffold of iron platelets
and numerous spherules of superparamagnetic magnetite particles;
below: a spherule of superparamagnetic particles and the structures
surrounding it (from Fleissner et al. 2003)
Fig. 15 Magnetic properties of magnetite particles: domain stabil-
ity field diagram indicating how the magnetic moments of particles
of a given shape differ with size; size of particles found in various
living beings is indicated (after Kirschvink and Gould 1981, with
the superparamagnetic particles identified by Fleißner et al. 2003
added)
687
of magnetite included; they could account for the sen-
sitivities indicated by behavioral evidence.
Histological findings
Magnetite has been discovered in a large number of
species belonging to all major phyla, mostly by mea-
suring the natural and induced remanence with highly
sensitive SQUID-magnetometers. In honey bees, Apis
mellifera, magnetic material was described in the front
part of the abdomen (Gould et al. 1978); in vertebrates,
it appears to be located mostly in the ethmoid region in
the front of the head (see Kirschvink et al. 1985).
In salmonid fish, chains of single domain magnetite
have been isolated from ethmoid tissue (Mann et al.
1988). A histological study showed magnetite particles
embedded in specific cells in the basal lamina within the
olfactory lamellae of rainbow trout, Oncorhynchus my-
kiss (Walker et al. 1997). These particles were identified
as single domains; applying a strong external magnetic
field could change the direction of thei r magnetization
(Diebel et al. 2000). In birds, histological and electron-
optic studies revealed magnetite particles in the orbital
and in the nasal cavity, where single domains were re-
ported (Beason and Nichols 1984; Beason and Brennon
1986; William and Wild 2001), and at specific locations
in the skin of the upper beak of pigeons, where clusters
of very small crystals were described, with the particles
identified by crystallographic means as superparamag-
netic magnetite (Hanzlik et al. 2000). These clusters were
located within nervous tissue and associated with a
remarkable framework of platelets consisting of ele-
mentary iron (Fig. 16); the authors speculate about
possible functions in a magnetoreceptor (Fleissner et al.
2003). Altogether, the magnetite-containing structures
found in birds and fish do not seem to be identical,
implying that the respective magnetite-based receptors
might differ in their general characteristics.
Effects of a strong, short magnetic pulse
The first behavioral tests were designed to generally
demonstrate an involvement of magnetite in magneto-
reception. They aimed at interfering with the potential
receptors by altering the magnetization of the magnetite
crystals. This was expected to change the output of
receptors in a dramatic way and thus cause a lasting
after-effect on orientation behavior. A popular method
was to apply a brief, strong magnetic pulse to the head
of the test animal 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 to escape re-
magnetization. In most studies, a 0.5 T pulse with 3–
5 ms duration was used.
Behavioral tests Tests with migratory birds again use
the preference of the migratory direction as a criterion
whether pulse treatment affected behavior. A pulse prior
to the critica l tests caused a marked 90 change in
direction: Australian Silvereyes, Zosterops lateralis,
preferred easterly headings, and that when they had
been heading northward in autumn as well as southward
in spring (Fig. 17, left). This effect of the pulse lasted for
about 3 days; after that, the birds became disoriented
and, about 10 days after pulse treatment, resumed their
original orientation in 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; young birds that had been
captured immediately after fledging proved to be unaf-
fected and continued in their normal migratory direction
(Fig. 17, right; Munro et al. 1997). This suggests that the
pulse affected a mechanism that is based on experience,
and points to the position-finding system of the ‘navi-
gational map’. The same pulse also caused experienced
pigeons to deviate from the mean of untreated control
birds (Beason et al. 1997 ).
In further tests, the protocol of the pulse treatments
was modified to identify specific properties of the
receptor. An identical pulse applied in two different
orientations e.g. ‘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
(Fig. 18). This was true for passerine migrants like
bobolinks, Dolichonyx orycivorus, as well as for homing
pigeons (Beason et al. 1995, 1997). It implies that the
pulse does not simply de activate the receptors alto-
gether, but instead causes them to provide altered
information, which causes birds to head in different
directions. 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 un-
known portion of the particles of the receptor; the
biasing field was to align movable particles in one
direction so that a pulse affected them all. A pulse ap-
plied parallel would not change their magnetization,
Fig. 17 Effect of a short, strong magnetic pulse on the orientation
behavior of Australian Silvereyes in Australian autumn. ad., old,
experienced birds tested; juv.: young, inexperienced birds tested.
Open symbols indicate control data recorded before, solid symbols
data recorded after pulse treatment. Symbols as in Fig. 2 (data
from W. Wiltschko et al. 1994, Munro et al. 1997).
688
whereas the pulse applied in an antiparallel direction
should have a maximum effect. In critical tests, however,
both groups of birds showed the same deflections
(Wiltschko et al. 2002b). These results largely exclude
single-domain particles free to move as part of a polar-
ity-sensitive receptor.
Treating mammals with the same pulse also induced
noticable deflections. Zambian molerat s shifted the po-
sition of their nest by about 75 from the south-south-
east to east. Retesting the same animals showed that this
altered preference, in contrast to the one observed in
birds, was stable for three months until the end of the
experiments (Marhold et al. 1997b).
Single domains or superparamagnetic particles? Since
none of the other recep tion mechanisms would show an
after-effect following trea tment with a magnetic pulse,
the observation that the pulse had an effect is diagnostic
for magnetite particles involved in the receptor
controlling the observed behavior. The response to pulse
treatment can also be interpreted in view of the type of
magnetite particles involved single domains or super-
paramagnetic particles.
In birds, where both types have been described, the
short duration of the pulse effect seems to speak against
single domains. Remagnetization of single domain par-
ticles should be just as stable and lasting as the original
one. Yet in birds, a clear pulse effect was observed only
on the day of pulsing and the foll owing two days
(Wiltschko et al. 1994, 1998; Beason et al. 1997). The
behavior of birds after pulse treatment thus indicates
magnetite-based receptors, but these receptors do not
seem to be based on single domains. This leaves super-
paramagnetic particles. Single superparamagnetic par-
ticles are not affected by a magnetic pulse as used in the
experiments described above, but clusters and chains of
clusters are. A strong pulse might break up the clusters
and disrupt the chains, but they rearrange themselves,
with a time rate in the order of several days, depending
on the specific structure of the clusters, the angle with
which they are hit by the pulse etc. (Davila et al., in
press).
In rodents, the situation is different insofar as ana-
tomical an d histological data are entirely lacking. The
pulse effect indicates a receptor based on magnetite, and
the long duration of the pulse effect would be in accor-
dance with single domains.
Neuronal pathways associated with magnetite-based
receptors
The region of the head where magnetite particles were
found in birds and fish is innervated by the ramus oph-
thalmicus, a branch of the nervus trigeminus. Electro-
physiological recordings from the ophthalmic nerve in
passerine birds used stimuli produced by a coil system
that in some experiments was set up in a way that the
axis of the coils was aligned with the magnetic vector so
Fig. 19 Electrophysiological
recordings from a trigeminal
ganglion cell of a bobolink,
responding to different changes
in the intensity of the
geomagnetic field (after Beason
and Semm 1991)
Fig. 18 The effect of a magnetic pulse on the orientation of homing
pigeons released at sites 129 km and 108 km from the loft; the
home directions 229 and 353 are indicated by a dashed radius. The
symbols at the periphery of the circle mark the vanishing bearings
of individual pigeons: open symbols, untreated control birds; blue
symbols, birds treated with a pulse oriented ‘south anterior’; red
symbols: birds treated with a pulse oriented ‘south left’; the arrows
represent the respective mean vectors (data from Beason et al.
1997)
689
that intensity alone could be modified. Units responding
to magnetic stimuli modified their spontaneous activity
by changes in magnetic intensity, showing a logarithmic
characteristic. The minimum intensity difference tested
was 200 nT (Fig. 19), where the birds still showed a clear
response. Similar recordings are reported from the tri-
geminal ganglion (Semm and Beason 1990). Electro-
physiological recordings from the corresponding nerve
in rainbow trouts produced likewise responses to chan-
ges in intensity (Walker et al. 1997).
Two other findings provide more direct evidence that
the input from magnetite-based receptors in birds is
mediated by the ophthalmic nerve: behavioral experi-
ments showed that deactivating the ophthalmic nerve
with a local anesthetic supp ressed the pulse effect (Bea-
son and Semm 1996); the bobolinks treated this way
continued in their migratory direction, which clearly
shows that the pulse does not affect the compass
mechanism. In conditioning experiments, pigeons
trained to respond to changes in intensity failed to re-
spond correctly after deactivation of the ophthalmic
nerve (Mora et al. 2004). Together, these findings sug-
gest that in birds and probably also in fish, magnetite-
based receptors mediate information on intensity rather
than compass information.
In rodents, a study using c-Fos identified the superior
colliculus as a site of neural activity caused by magnetic
stimulation (Ne
ˇ
mec et al. 2001). The origin of this
activity is unclear; an involvement of the magnetite-
based receptor indicated by the pulse effect seems pos-
sible.
Two types of receptors for different tasks
In recent years, the number of publications on the as-
pects of reception and processing magnetic information
has greatly increased, but it is only in case of birds, that
the various pieces of the puzzle begin to form a consis-
tent picture, although many questions still remain
unanswered. The available data indicate the existence of
two magnetoreceptor systems in birds for different types
of information (see Beason and Semm 1991): a radical-
pair mechanism in the right eye provides directional
information, and magnetite-based receptors in the upper
beak records differences in magnetic intensity one
might say: birds have a compass in their eye and a
magnetometer in their beak. The input of the former
appears to be mediated and processed by pa rts of the
visual system, involving the nBOR, the tectum opticum
and the nucleaus rotundus; the input of the latter by the
ophthalmic nerve and the trigeminal ganglion. It is still
unknown as to where these two types of information
finally converge to form crucial components of the ‘map
and compass’ system used for navigation (for review, see
Wiltschko and Wiltschko 2003).
In other vertebrates, our knowledge is limited to
certain aspects of magnetoreception. In marine turtles,
the various uses of magnetic information are well doc-
umented, yet magnetorecepti on has not yet bee n ana-
lyzed. The nature of the primary processes of
magnetoreception are indicated by behavioral data in
salamanders, where the light-dependency of an inclina-
tion compass suggests magnetoreception based on a
radical pair mechanism, and in mammals, where the
pulse effect points to magnetite-based receptors. The
position of the receptors and anatomical details about
their structure are known in fish, where they are found in
the olfactory lamellae; in salamanders, behavioral
studies identified the pineal as site of the receptors. Some
of the neuronal pathways are known in fish, where
electrophysiological recordings indicate that informa-
tion on magnetic intensity is mediated by the trigeminal
system; in mammals, an involvement of the superior
corniculus is suggested, but neither the origin nor the
type of the respective magnetic information is entirely
clear.
At the same time, the mechanisms employed by fish,
mammals and several arthropods in their polarity
compass are entirely unknown. Magnetite-based recep-
tors are an option, as they could theoretically provide
information on direction as well as on intensity. Here,
the lasting pulse effect on nest building in mole rats is
interesting: since the direction of the nest would involve
only a com pass, we may speculate that this compass
might be based on single domain magnetite, but direct
evidence is still lacking.
In view of the many open questions, we can only
hope that the ‘magnetic sense’ continues to meet with
great interest and that further research in the coming
years will lead to a better understanding of reception
and processing of magnetic information.
References
Baker RR (1989) Human navigation and magnetoreception.
Manchester University Press, Manchester and New York
Beason RC, Brennon WJ (1986) Natural and induced magnetiza-
tion in the bobolink (Dolichonyx orycivorus). Ethology 91:75–80
Beason RC, Nichols JE (1984) Magnetic orientation and magnet-
ically sensitive material in a transequatorial migratory bird.
Nature 309:151–153
Beason RC, Semm P (1991) Two different magnetic systems in
avian orientation. In: Bell BD, Cossee RO, Flux JEC, Heather
BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta
XX Congr Intern Ornithol, New Zealand Ornithological Con-
gress Trust Board, Wellington, pp 1813–1819
Beason RC, Semm P (1996) Does the avian ophthalmic nerve carry
magnetic navigational information? J Exp Biol 199:1241–1244
Beason RC, Dussourd N, Deutschlander M (1995) Behavioural
evidence for the use of magnetic material in magnetoreception
by a migratory bird. J Exp Biol 198:141–146
Beason RC, Wiltschko R, Wiltschko W (1997) Pigeon homing:
effects of magnetic pulses on initial orientation. Auk 114:405–
415
Beck W, Wiltschko W (1988) Magnetic factors control the migra-
tory direction of Pied Flycatchers (Ficedula hypoleuca Pallas).
In: Ouellet H (ed) Acta XIX Congr Int Ornithol Vol II. Uni-
versity of Ottawa Press, Ottawa, pp 1955–1962
Blakemore RP (1975) Magnetotactic bacteria. Science 190:377–379
690
Boles LC, Lohmann KJ (2003) True navigation and magnetic map
in spiny lobsters. Nature 421:60–63
Cranfield J, Belford R, Debrunner P, Schulten K (1994) A per-
turbation treatment of oscillating magnetic fields in the radical
pair mechanism. Chem Phys 182:1–18
Davila AF, Winklhofer M, Sheherbakov V, Petersen N Magnetic
pulse affects a putative magnetoreceptor mechanism. Biophys
J in press
DeJong D (1982) Orientation of comb building by honeybees.
J Comp Physiol 147:495–501
Deutschlander ME, Phillips JB, Borland SC (1999) The case for
light-dependent magnetic orientation in animals. J Exp Biol
202:891–908
Diebel CE, Proksch R, Green CR, Neilson P, Walker MM (2000)
Magnetite defines a vertebrate magnetoreceptor. Nature
406:299–302
Duelli P, Duelli-Klein R (1978) Die magnetische Nestausrichtung
der australischen Kompaßtermite Amitermes meridionalis. Mitt
Schweiz Entomol Ges 51:337–342
Edmonds DT (1996) A sensitive optically detected magnetic com-
pass for animals. Proc R Soc Lond B 263:295–298
Fisher JH, Munro U, Phillips JB (2003) Magnetic navigation in an
avian migrant? In: Berthold P, Gwinner E, Sonnenschein E (ed)
Avian migration. Springer, Berlin Heidelberg New York, pp
423–432
Fleissner G, Holtkamp-Ro
¨
tzler E, Hanzlik M, Winklhofer M,
Fleissner G, Petersen N, Wiltschko W (2003) Ultrastructural
analysis of a putative magnetoreceptor in the beak of homing
pigeons. J Comp Neurol 458:350–360
Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, Vallin
A (2001) Magnetic cues trigger extensive refuelling. Nature
414:35–36
Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced
electron transfer in a cryptochrome blue-light photoreceptor.
Nature Struct Biol 6:489–490
Gould JL, Kirschvink JL, Deffeyes KS (1978) Bees have magnetic
remanence. Science 201:1026–1028
Gundmundsson GA, Sandberg R (2000) Sanderlings (Calidris alba)
have a magnetic compass: orienation experiments during spring
migration in Iceland. J Exp Biol 203:3137–3144
Gu
¨
ntu
¨
rku
¨
n O (1997) Morphological asymmetries of the tectum
opticum in the pigeon. Exp Brain Res 116:561–566
Hanzlik M, Heunemann C, Holzkamp-Ro
¨
tzler E, Winklhofer M,
Petersen N, Fleissner G (2000) Superparamagnetic magnetite in
the upper beak tissue of homing pigeons. BioMetals 13:325–331
Haque R, Charausia SS, Wessel JH, Iuvone PM (2002) Dual reg-
ulation of cryptochrome I mRNA expression in chicken retina
by light and circadian oscillators. Neuroreport 13:2247–2251
Henbest KB, Kukura P, Rodgers CT, Hore PJ, Timmel CR (2004)
Radio frequency magnetic field effects on a radical recombi-
nation reaction: a diagnostic test for the radical pair mecha-
nism. J Am Chem Soc 126:8102–8103
Jacklyn PM, Munro U (2002) Evidence for the use of magnetic cues
in mound construction by the termite Amitermes meridionalis
(Isoptera, Termitinae). Austr J Zool 50:357–368
Kalmijn AJ (1978) Electric and magnetic sensory world of sharks,
skates, and rays. In: Hodgson FS, Mathewson RF (eds) Sensory
biology of sharks, skates and rays. Office Naval Res, Arlington,
VA, pp 507–528
Keeton WT, Larkin TS, Windsor DM (1974) Normal fluctuation in
the earth’s magnetic field influence pigeon orientation. J Comp
Physiol 95:95–103
Kirschvink JL, Gould JL (1981) Biogenetic magnetite as a basis for
magnetic field detection in animals. BioSystems 13:181–201
Kirschvink JL, Walker MM (1985) Particle-size considerations for
magnetite-based magnetoreceptors. In: Kirschvink JL, Jones
DS, MacFadden BJ (eds) Magnetite biomineralization and
magnetoreception in organisms. Plenum, New York, London,
pp 243–256
Kirschvink JL, Jones DS, MacFadden BJ (eds) (1985) Magnetite
biomineralization and magnetoreception in organisms. Plenum,
New York
Light P, Salmon M, Lohmann KJ (1993) Geomagnetic orientation
of loggerhead sea turtles: evidence for an inclination compass. J
Exp Biol 182:1–10
Lohmann KJ (1991) Magnetic orientation by hatchling loggerhead
sea turtles (Caretta caretta). J Exp Biol 155:37–49
Lohmann KJ, Lohmann CMF (1992) Orientation to oceanic waves
by green turtle hatchlings. J Exp Biol 171:1–13
Lohmann KJ, Lohmann CMF (1993) A light-independent mag-
netic compass in the leatherback sea turtle. Biol Bull 185:149–
151
Lohmann KJ, Lohmann CMF (1994) Detection of magnetic
inclination angle by sea turtles: a possible mechanism for
determining latitudes. J Exp Biol 194:23–32
Lohmann KJ, Lohmann CMF (1996) Detection of magnetic field
intensity by sea turtles. Nature 380:59–61
Lohmann KJ, Pentcheff ND, Nevitt GA, Stetten GD, Zimmer-
Faust RK, Jarrard HE, Boles LC (1995) Magnetic orientation
of spiny lobsters in the ocean: experiments with underseas coil
systems. J Exp Biol 198:2041–2048
Lohmann KJ, Cain SD, Dodge SA, Lohmann CMF (2001) Re-
gional magnetic fields as navigational markers for sea turtles.
Science 294:364–366
Lohmann KJ, Lohmann CMF, Erhart LM, Bagley DA, Swing T
(2004) Geomagnetic map used in sea-turtle navigation. Nature
428:909–910
Mai JK, Semm P (1990) Patterns of glucose utilization following
magnetic stimulation. J Hirnforsch 31:331–336
Maier EJ (1992) Spectral sensitivities including the ultraviolet of
the passeriform bird Leiothrix lutea. J Comp Physiol A
170:709–714
Mann S, Sparks NHC, Walker MM, Kirschvink JL (1988) Ultra-
structure, morphology and organization of biogenic magnetite
from Sockeyes salmon, Oncorhynchus nerka: implications for
magnetoreception. J Exp Biol 140:35–49
Marhold S, Burda H, Wiltschko W (1997a) A magnetic polarity
compass for direction finding in a subterranean mammal. Na-
turwissenschaften 84:421–423
Marhold S, Burda H, Kreilos I, Wiltschko W (1997b) Magnetic
orientation in the common mole-rat from Zambia. In: Orien-
tation and navigation—birds, humans and other animals.
Royal Instit of Navig, Oxford, 5-1–5-9
Miyamoto Y, Sancar A (1998) Vitamin B
2
-based blue-light pho-
toreceptors in the retinohypothalamic tract as the photoactive
pigments for setting the circadian clock in mammals. Proc Natl
Acad Sci USA 95:6097–6102
Mo
¨
ller A, Gesson M, Noll C, Phillips J, Wiltschko R, Wiltschko
W (2001) Light-dependent magnetoreception in migratory
birds previous exposure to red light alters the response to red
light. In: Orientation and navigation—birds, humans
and other animals. Royal Institute of Navigation, Oxford, 6-
1–6-6
Mo
¨
ller A, Sagasser S, Wiltschko W, Schierwater B (2004) Retinal
cryptochrome in a migratory passerine bird: a possible trans-
ducer for the avian magnetic compass. Naturwissenschaften
91:585–588
Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetore-
ception and its trigeminal mediation in the homing pigeon.
Nature 432:508–511
Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G,
Stalleicken J, Dirks P, Weiler R (2004) Cryptochromes and
neuronal-activity markers colocalize in the retina of migratory
birds during magnetic orientation. Proc Nat Acad Sci USA
101:14294–14299
Muheim R, Ba
¨
ckman J, A
˚
kesson S (2002) Magnetic compass ori-
entation in European robins is dependent on both wavelength
and intensity of light. J Exp Biol 205:3845–3856
Munro U, Munro JA, Phillips JB, Wiltschko R, Wiltschko W
(1997) Evidence for a magnetite-based navigational ‘map’ in
birds. Naturwissenschaften 84:26–28
Murray RW (1962) The response of the ampullae of Lorenzini of
elasmobranchs to electrical stimulation. J Exp Biol 39:119–
128
691
Ne
ˇ
mec P, Altmann J, Marhold S, Burds H, Oelschla
¨
ger HHA
(2001) Neuroanatomy of magnetoreception: the superior colli-
culus involved in magnetic orientation in a mammal. Science
294:366–368
Pardi L, Ugolini A, Faqi AS, Scapini F, Ercolini A (1988) Zonal
recovering in equatorial sandhoppers: Interaction between
magnetic and solar orientation. In: Chelazzi G, Vannini M (eds)
Behavioral adaptation to intertidal life. Proc of the NATO Sci,
Plenum, New York, London, pp 79–92
Phillips JB (1986) Two magnetoreception pathways in a migratory
salamander. Science 233:765–767
Phillips JB, Borland SC (1992a) Magnetic compass orientation is
eliminated under near-infrared light in the eastern red-spotted
newt Notophthalmus viridescens. Anim Behav 44:796–797
Phillips JB, Borland SC (1992b) Behavioral evidence for use of a
light-dependent magnetoreception mechanism by a vertebrate.
Nature 359:142–144
Phillips JB, Borland SC (1994) Use of a specialized magnetore-
ception system for homing by the eastern red-spotted newt
Notophthalmus viridescens. J Exp Biol 188:275–291
Phillips JB, Deutschlander ME (1997) Magnetoreception in ter-
restrial vertebrates: implications for possible mechanisms of
EMF interaction with biological systems. In: Stevens RG,
Wilson BW, Andrews LE (eds) The melatonin hypothesis:
electric power and the risk of breast cancer. Battelle Press,
Columbus Ohio, pp 111–172
Phillips JB, Deutschlander ME, Freake MJ, Borland SC (2001) The
role of extraocular photoreceptors in newt magnetic compass
orientation: parallels between light-dependent magnetorecep-
tion and polarized light detection in vertebrates. J Exp Biol
204:2543–2552
Phillips JB, Freake MJ, Borland SC (2002a) Behavioral titra-
tion of magnetic map coordinates. J Comp Physiol A
188:157–160
Phillips JB, Borland SC, Freake M, Brassart J, Kirschvink JL
(2002b) ‘Fixed-axis’ magnetic orientation by an amphibian:
non-shoreward-directed compass orientation, misdirected
homing or positioning a magnetite-based map detector in a
consistent alignment relative to the magnetic field? J Exp Biol
205:3903–3914
Prior H, Wiltschko R, Stapput K, Gu
¨
ntu
¨
rku
¨
n O, Wiltschko W
(2004) Visual lateralization and homing in pigeons. Behav Brain
Res 154:301–310
Quinn TP (1980) Evidence for celestial and magnetic compass
orientation in lake migrating sockeye salmon fry. J Comp
Physiol 137:243–248
Quinn TP, Brannon EL (1982) The use of celestial and magnetic
cues by orienting sockeye salmon smolts. J Comp Physiol
147:547–552
Ritz T, Adem S, Schulten K (2000) A model for vision-based
magnetoreception in birds. Biophys J 78:707–718
Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004)
Resonance effects indicate a radical-pair mechanism for avian
magnetic compass. Nature 429:177–180
Sancar A (2003) Structure and function of DNA photolyase and
cryptochrome blue-light photorceptors. Chem Rev 103:2203–
2237
Schulten K, Windemuth A (1986) Model for a physiological
magnetic compass. In: Maret G, Boccara N, Kiepenheuer
J (eds). Biophysical effects of steady magnetic fields. Springer,
Berlin Heidelberg New York, pp 99–106
Semm P, Beason RC (1990) Responses to small magnetic variations
by the trigeminal system of the Bobolink. Brain Res Bull
25:735–740
Semm P, Demaine C (1986) Neurophysiological properties of
magnetic cells in the pigeon’s visual system. J Comp Physiol A
159:619–625
Semm P, Nohr D, Demaine C, Wiltschko W (1984) Neural basis of
the magnetic compass: interaction of visual, magnetic and
vestibular inputs in the pigeons’s brain. J Comp Physiol
155:283–288
Shcherbakov VP, Winklhofer M (1999) The osmotic magnetome-
ter: a new model for magnetite-based magnetoreceptors in
animals. Eur Biophys J 28:380–392
Skiles DD (1985) The geomagnetic field: its nature, history and
biological relevance. In: Kirschvink JL, Jones DS MacFadden
BJ (eds) Magnetite biomineralization and magnetoreception in
organisms. Plenum, New York, London, pp 43–102
Stapput K, Gesson M, Wiltschko R, Wiltschko W (2005) Light-
dependent magnetoreception: behavior of migratory birds un-
der monochromatic and bichromatic lights. In: Orientation and
Navigation. Proc RIN 05 Conf, Royal Institute of Navigation,
Reading (in press)
Thalau P, Ritz T, Stapput K, Wiltschko R, Wiltschko W (2005)
Magnetic compass orientation of migratory birds in the pres-
ence of a 1.315 MHz oscillating field. Naturwissenschaften
92:86–90
Viguier C (1882) Le sens de l’orientation et ses organes chez les
animaux et chez l’homme. Revue Philosophique de la France et
de l’E
´
tranger 14:1–36
Walcott C (1978) Anomalies in the earth’s magnetic field increase
the scatter of pigeons’ vanishing bearings. In: Schmidt-Koenig
K, Keeton WT (eds) Animal migration, navigation and homing.
Springer, Berlin Heidelberg New York, pp 143–151
Walcott C, Green RP (1974) Orientation of homing pigeons alterd
by a change in the direction of an applied magnet field. Science
184:180–182
Walker MM, Diebel CE, Haugh CV, Pankhurst PM, Montgomery
JC Green CR (1997) Structure and function of the vertebrate
magnetic sense. Nature 390:371–376
Williams MN, Wild JM (2001) Trigeminally innervated iron-con-
taining structures in the beak of homing pigeons and other
birds. Brain Res 889:243–246
Wiltschko W (1978) Further analysis of the magnetic compass of
migratory birds. In: Schmidt-Ko
¨
nig K, Keeton WT (eds) Ani-
mal migration, navigation and homing. Springer, Berlin Hei-
delberg New York, pp 302–310
Wiltschko W, Wiltschko R (1972) Magnetic compass of European
Robins. Science 176:62–64
Wiltschko R, Wiltschko W (1978) Evidence for the use of magnetic
outward-journey information in homing pigeons. Naturwis-
senschaften 65:112
Wiltschko W, Wiltschko R (1981) Disorientation of inexperienced
young pigeons after transportation in total darkness. Nature
291:433–434
Wiltschko W, Wiltschko R (1992) Migratory orientation: mag-
netic compass orientation of Garden Warblers (Sylvia borin)
after a simulated crossing of the magnetic equator. Ethology
91:70–79
Wiltschko R, Wiltschko W (1995) Magnetic Orientation in Ani-
mals. Springer, Berlin Heidelberg New York
Wiltschko W, Wiltschko R (1999) The effect of yellow and blue
light on magnetic compass orientation in European Robins,
Erithacus rubecula. J Comp Physiol A 184:295–299
Wiltschko W, Wiltschko R (2001) Light-dependent magnetore-
ception in birds: the behavior of European Robins, Erithacus
rubecula, under monochromatic light of various wavelengths.
J Exp Biol 204:3295–3302
Wiltschko W, Wiltschko R (2002) Magnetic compass orientation in
birds and its physiological basis. Naturwissenschaften 89:445–
452
Wiltschko R, Wiltschko W (2003) Avian navigation: from histor-
ical to modern concepts. Anim Behav 65:257–272
Wiltschko W, Munro U, Ford H, Wiltschko R (1993) Red light
disrupts magnetic orientation of migratory birds. Nature
364:525–527
Wiltschko W, Munro U, Beason RC, Ford H, Wiltschko R (1994)
A magnetic pulse leads to a temporary deflection in the orien-
tation of migratory birds. Experientia 50:697–700
Wiltschko W, Munro U, Ford H, Wiltschko R (1998) Effect of a
magnetic pulse on the orientation of Silvereyes, Zosterops l.
lateralis, during spring migration. J Exp Biol 201:3257–3261
692
Wiltschko W, Wiltschko R, Munro U (2000) Light-dependent
magnetoreception in birds: the effect of intensity of 565-nm
green light. Naturwissenschaften 87:366–369
Wiltschko W, Gesson M, Wiltschko R (2001) Magnetic compass
orientatiom of European robins under 565 nm green light.
Naturwissenschaften 88:387–390
Wiltschko W, Traudt J, Gu
¨
ntu
¨
rku
¨
n O, Prior H, Wiltschko R
(2002a) Lateralization of magnetic compass orientation in a
migratory bird. Nature 419:467–470
Wiltschko W, Munro U, Wiltschko W, Kirschvink JL (2002b)
Magnetite-based magnetoreception in birds: the effect of a
biasing field and a pulse on migratory behavior. J Exp Biol
205:3031–3037
Wiltschko W, Munro U, Ford H, Wiltschko R (2003a) Laterali-
sation of magnetic compass orientation in silvereyes, Zosterops
lateralis. Austr J Zool 51:1–6
Wiltschko W, Munro U, Ford H, Wiltschko R (2003b) Magnetic
orientation in birds: non-compass responses under monochro-
matic light of increased intensity. Proc R Soc Lond B 270:2133–
2140
Wiltschko W, Mo
¨
ller A, Gesson M, Noll C, Wiltschko R (2004a)
Light-dependent magnetoreception in birds analysis of the
behaviour under red light after pre-exposure to red light. J Exp
Biol 207:1193–1202
Wiltschko W, Gesson M, Stapput K, Wiltschko R (2004b) Light-
dependent magnetoreception in birds: interaction of at least two
different receptors. Naturwissenschaften 91:130–134
Yorke ED (1979) A possible magnetic transducer in birds. J Theor
Biol 77:101–105
693
... This process reduces the photo-excited singlet state of the FAD to the anion radical, FAD •− , and oxidises the terminal, surface-exposed, tryptophan (Trp C H) to give the cation radical, Trp C H •+ . Formed with conservation of spin angular momentum, the radical pair is initially in an electronic singlet state, 1 [FAD •− Trp C H •+ ] 22,23,27 . This form of the protein is a coherent superposition of the eigenstates of the spin Hamiltonian which comprises the Zeeman, hyperfine, exchange and dipolar interactions of the electron spins. ...
... In the cryptochrome from the fruit fly, Drosophila melanogaster (DmCry), however, there is an additional electron donor, Trp D H, beyond Trp C H ( Fig. 1) 38 . The edge-to-edge distance between FAD and Trp D H in DmCry is 1.70 nm 35,36 which is large enough that direct charge recombination in 1 [FAD •− Trp D H •+ ] cannot compete effectively with electron spin relaxation, at least for the purified protein in vitro, explaining the weak magnetic field effects observed for DmCry 39 . Sequence alignments suggest that avian cryptochromes also have a fourth tryptophan which could be involved in radical pair formation; we return to this point below. ...
Preprint
Birds have a remarkable ability to obtain navigational information from the Earth's magnetic field. The primary detection mechanism of this compass sense is uncertain but appears to involve the quantum spin dynamics of radical pairs formed transiently in cryptochrome proteins. We propose here a new version of the current model in which spin-selective recombination of the radical pair is not essential. One of the two radicals is imagined to react with a paramagnetic scavenger via spin-selective electron transfer. By means of simulations of the spin dynamics of cryptochrome-inspired radical pairs, we show that the new scheme offers two clear and important benefits. The sensitivity to a 50 {\mu}T magnetic field is greatly enhanced and, unlike the current model, the radicals can be more than 2 nm apart in the magnetoreceptor protein. The latter means that animal cryptochromes that have a tetrad (rather than a triad) of tryptophan electron donors can still be expected to be viable as magnetic compass sensors. Lifting the restriction on the rate of the spin-selective recombination reaction also means that the detrimental effects of inter-radical exchange and dipolar interactions can be minimised by placing the radicals much further apart than in the current model.
... 6,9,[20][21][22][23] While the exact physico-chemical mechanisms of magnetoreception are not fully understood, its use is demonstrated by ample behavioural evidence. 3,9,24 The leading hypothesis assumes the photo-activation of lightsensitive cryptochrome 4 proteins in the avian retina and the consequent formation of radical pairs that are sensitive to the Earth's magnetic field. 23,[25][26][27][28][29] The magnetic field sensitivity of the radical pairs is expected to be transmitted to the brain via the thalamofugal visual pathway. ...
Preprint
Full-text available
Emlen funnels can be used to study the birds' ability to orient during the migratory seasons. Birds are so eager to migrate that they will jump in the direction in which they want to fly, even if they are placed in small cages during the night. Emlen funnels have therefore been used for decades to study the sensory capabilities and mechanisms that migratory birds use to find their way. A significant part of this research has focused on how night-migratory songbirds perceive the Earth's magnetic field. Even though Emlen funnels have been proven quite successful in capturing the birds' behavioural responses to different experimental conditions, the orientation behaviour of night-migratory songbirds in Emlen funnels is very noisy, i.e. tends to have a low signal to noise ratio. This noise makes Emlen funnel experiments very time consuming and limits the types of questions that can be studied to those which require very few different experimental conditions (permutations). Furthermore, the experimental design choices can be crucial, e.g. degree of blinding of the experimenters and data evaluators to the conditions tested, pre-testing of birds to make sure they are in a migratory state, and planning of the effective sample sizes. Hence, different traditions in experimental design choices can reduce reproducibility and comparability and render the interpretation of the results non-trivial. To better understand Emlen funnel data and the minimal requirements for good experimental design, we constructed and analyzed a large data set that we compiled by combining behavioural data from many previous Emlen funnel studies performed in Oldenburg. Our results provide realistic ranges for the expected orientation of the birds in Emlen funnels, which can be useful (and in some research crucial) for predicting the optimal sample sizes for future experiments. Our results thus offer concrete information for the design and analysis of statistically powerful future magnetic orientation experiments.
... , (1) in which and are the per pass absorbance (strictly extinction) and ring-down time recorded without the pump pulse. . (2) [ ] ...
Preprint
Full-text available
Cryptochromes are flavoproteins with a number of established and proposed biological functions based on their sensitivity to light. Amongst the latter is the possibility that cryptochromes mediate the geomagnetic compass sense used by migratory birds as a navigational cue. This hypothesis rests on a magnetically sensitive photochemical reaction of the flavin chromophore in which a series of electron transfers within the protein scaffold ultimately generates a signal propagated within the central nervous system of the animal. Although there is a good understanding of the photochemistry and the electron transfer pathway, the protein-mediated mechanisms of signal transduction are still unclear. Here we have examined the response of Drosophila melanogaster cryptochrome - DmCRY, an archetypal cryptochrome - to photochemical activation by means of molecular dynamics simulations, hydrogen-deuterium exchange mass spectrometry, and cavity ring-down spectroscopy. We were able to measure the dynamics of DmCRY at near-residue level resolution, revealing a reversible, long-lived, blue-light induced conformational change in the C-terminal tail of the protein. This putative signalling state was validated using different illumination conditions, and by examining DmCRY variants in which the electron transfer chain was disrupted by point mutation. Our results show how the photochemical behaviour of the flavin chromophore generates a state of DmCRY that may act as a key primer for modulating downstream interactions.
... It is well established that various animals are able to derive direction information from the geomagnetic field (Wiltschko and Wiltschko, 1995;Ritz et al., 2000;Johnsen and Lohmann, 2008). Some mammals perceive the Earth's field as a polarity compass, distinguishing north and south, while birds and reptiles rely on an inclination compass that discriminates between polewards and equatorwards and which exploits both the intensity and the gradient of the field. ...
Preprint
Quantum physics and biology have long been regarded as unrelated disciplines, describing nature at the inanimate microlevel on the one hand and living species on the other hand. Over the last decades the life sciences have succeeded in providing ever more and refined explanations of macroscopic phenomena that were based on an improved understanding of molecular structures and mechanisms. Simultaneously, quantum physics, originally rooted in a world view of quantum coherences, entanglement and other non-classical effects, has been heading towards systems of increasing complexity. The present perspective article shall serve as a pedestrian guide to the growing interconnections between the two fields. We recapitulate the generic and sometimes unintuitive characteristics of quantum physics and point to a number of applications in the life sciences. We discuss our criteria for a future quantum biology, its current status, recent experimental progress and also the restrictions that nature imposes on bold extrapolations of quantum theory to macroscopic phenomena.
... Установлено, что различные организмы, как и организм человека, могут реагировать на мельчайшие изменения МП, составляющие приблизительно одну тысячную часть геоМП. К этим явлениям относятся магнитная навигация животных [12] и кардиоваскулярные реакции на магнитные бури [13]. Правда, не всегда удается наблюдать такие эффекты в лабораторных условиях, поскольку они в целом имеют случайный характер уже на молекулярном уровне. ...
Article
Full-text available
The number of biomedical studies where the observed effects are determined by the laws of quantum physics is constantly growing. These include respiration, vision, smell, photosynthesis, mutations, etc., united by name "quantum biology". The effect on organisms of magnetic fields, including those weakened in comparison with the geomagnetic field, is one of such studies. The magnetic field can act only on magnetic moments, the most important representative of which is the electron. The magnetic field changes the quantum dynamics of electrons in the body, which ultimately leads to the observed reactions at the biochemical and behavioral levels. Organisms on Earth have evolved in a geomagnetic field, which means that its absence can cause disturbances in the normal functioning of organisms. Indeed, there are more than two hundred scientific publications on this topic. Today, it has been reliably established that the hypomagnetic field can change the functioning of organisms from bacteria and fungi to mammals and humans. In deep space flight and in future missions to the Moon and Mars, astronauts will be in a hypomagnetic field, which is less than a natural geomagnetic field by more than a hundred times. Such a weakening of the magnetic field is associated with an additional risk. This mini review provides initial information about the levels of the magnetic field on Earth, in near and distant outer space, and on the surfaces of the Moon and Mars. Information is provided on the hypomagnetic field effects on the human body and about the mechanisms of such effects. It is reported about the features of research in magnetobiology that require special statistical methods for processing the results. The complexity of creating a hypomagnetic field in volumes sufficient to accommodate the human body is discussed. The primary tasks in this relatively new research field are formulated.
Preprint
Full-text available
Animals navigating in fluid environments often face lateral forces from wind or water currents that challenge travel efficiency and route accuracy. We investigated how 27 Magellanic penguins ( Spheniscus magellanicus ) adapt their navigation strategies to return to their colony amid regional tidal ocean currents. Using GPS-enhanced dead-reckoning loggers and high-resolution ocean current data, we reconstructed penguin travel vectors during foraging trips to assess their responses to variable currents during their colony-bound movements. By integrating estimates of energy costs and prey pursuits, we found that birds balanced direct navigation with current-driven drift: in calm currents, they maintained precise line-of-sight headings to their colony. In stronger currents, they aligned their return with lateral flows, which increased travel distance, but at minimal energy costs, and provided them with increased foraging opportunities. Since the lateral tidal currents always reversed direction over the course of return paths, the penguins’ return paths were consistently S-shaped but still resulted in the birds returning efficiently to their colonies. These findings suggest that Magellanic penguins can sense current drift and use it to optimize energy expenditure by maintaining overall directional accuracy while capitalizing on foraging opportunities.
Preprint
Experiments on the effect of radio-frequency (RF) magnetic fields on the magnetic compass orientation of migratory birds are analyzed using the theory of magnetic resonance. The results of these experiments were earlier interpreted within the radical-pair model of magnetoreception. However, the consistent analysis shows that the amplitudes of the RF fields used are far too small to noticeably influence electron spins in organic radicals. Other possible agents that could mediate the birds' response to the RF fields are discussed, but apparently no known physical system can be responsible for this effect.
Article
Full-text available
(1) Background: Chitons (Mollusca, Polyplacophora) are relatively primitive species in Mollusca that allow the study of biomineralization. Although mitochondrial genomes have been isolated from Polyplacophora, there is no genomic information at the chromosomal level; (2) Methods: Here we report a chromosome-level genome assembly for Acanthochiton rubrolineatus using PacBio (Pacific Biosciences, United States) reads and high-throughput chromosome conformation capture (Hi-C) data; (3) Results: The assembly spans 1.08 Gb with a contig N50 of 3.63 Mb and 99.97% of the genome assigned to eight chromosomes. Among the 32,291 predicted genes, 76.32% had functional predictions. The divergence time of Brachiopoda and Mollusca was ~550.8 Mya (million years ago), and that of A. rubrolineatus and other mollusks was ~548.5 Mya; (4) Conclusions: This study not only offers high-quality reference sequences for the Acanthochiton rubrolineatus genome, but also establishes groundwork for investigating the mechanisms of Polyplacophora biomineralization and its evolutionary history. This research will aid in uncovering the genetic foundations of molluscan adaptations across diverse environments.
Chapter
Somewhat questionable evidence in support of reptilian polarization sensitivity (PS) has come from field and laboratory observations on the behaviour of a few species of marine and freshwater turtles. More convincing are conclusions based on PS-aided orientation primarily in the lizards Uma notata, Tiliqua rugosa and species of the genus Podarcis. It is suggested that submersed hunters like, for instance, sea snakes ought to be included in examinations for PS since contrast enhancement by PS underwater could bestow some benefits to them during food procurement. Moreover, certain terrestrial snakes such as rainbow boas, sunbeam and indigo snakes are highly iridescent, and courtship displays in certain species of lizards could also contain signals for which the presence of PS would be advantageous. However, unambiguous polarization signals have not yet been demonstrated in any species. Results based on electrophysiological recordings to demonstrate PS in photoreceptors of the lateral eyes or the pineal organs’ parietal eye are also scant, but a connection between PS and magnetoreception, as in amphibians and birds, is increasingly regarded as a feature present in numerous reptilians. The earlier literature on reptilian PS has been covered by Horváth and Varjú (Polarized Light in Animal Vision—Polarization Patterns in Nature. Springer, Heidelberg, Berlin, New York, 2004) and Meyer-Rochow (Polarized Light and Polarization Vision in Animal Sciences. Springer:, Heidelberg, Berlin, New York, 2014).
Chapter
Polarization sensitivity (PS) in amphibians has been examined in some species of anurans and urodelans. Gymnophiones, on account of their tiny eyes and fossorial or aquatic lifestyles are considered unlikely candidates for PS. Some anura and urodela have been shown to detect the direction of polarization with photoreceptors of the pineal organ rather than their lateral eyes. An ordered array of light-absorbing visual molecules is paramount for PS, but an ordered array of radical pairs generated through photo-induced electron transfer is also essential for magnetoreception, which suggests that there is some interaction between the two senses. An anatomical requirement for PS is a constant and characteristic orientation of the photoreceptor’s disc membranes. A closer look at ultrastructural modifications in different retinal regions of species that are expected to be polarization sensitive, seems warranted. Polarization sensitivity may help to relocate breeding sites in philotropic species and to improve visibility of prey in predatory larval and adult urodeles plus those few anurans that hunt underwater. Furthermore, it could possibly be of assistance in separating overlapping shadows and play a role during courtship in species with distinct sexually dimorphic colouration.
Article
Full-text available
Minutes after emerging from underground nests, hatchling green turtles (Chelonia mydas L.) enter the sea and begin a migration towards the open ocean. To test the hypothesis that migrating hatchlings use wave cues to maintain their seaward headings, we released turtles offshore during unusual weather conditions when waves moved in atypical directions. Hatchlings swam into approaching waves in all experiments, even when doing so resulted in orientation back towards land. These data suggest that green turtle hatchlings normally maintain seaward headings early in the offshore migration by using wave propagation direction as an orientation cue. Because waves and swells reliably move towards shore in shallow coastal areas, swimming into waves usually results in movement towards the open sea. The physiological mechanisms that underlie wave detection by sea turtle hatchlings are not known. Calculations indicate that, at the depth at which hatchlings swim, accelerations produced beneath typical waves and swells along the Florida coast are sufficient to be detected by the vertebrate inner ear. We therefore hypothesize that hatchlings determine wave direction while under water by monitoring the sequence of horizontal and vertical accelerations that occur as waves pass above.
Article
Full-text available
WHETHER migratory animals can determine their global position by detecting features of the Earth's magnetic field has long been debated1-4. To do this an animal must perceive (at least) two distinct magnetic parameters, each of which must vary in a different direction across the Earth's surface3,5. There has been no evidence that any animal can perceive two such magnetic features, and whether 'magnetic maps' exist at all has remained controversial2-6. Several populations of sea turtles7-9 undergo transoceanic migrations before returning to nest on or near the same beaches where they themselves hatched. Along the migratory routes, all or most locations have unique combinations of magnetic field intensity and field line inclination. It has been demonstrated that hatchling loggerhead turtles can distinguish between different magnetic inclination angles10. Here we report that turtles can also distinguish between different field intensities found along their migratory route. Thus sea turtles possess the minimal sensory abilities necessary to approximate global position using a bicoordinate magnetic map.
Chapter
An orienting mechanism based exclusively on a sun compass runs into considerable difficulties in the Tropics (see Braemer, 1960; Lindauer 1960; Ercolini, 1964) on account of the annual change in the sun’s declination.
Chapter
The orientation behavior of migratory European Robins (Erithacus rubecula) during Zugunruhe was used for a further analysis of the characteristics of the birds’ magnetic compass. Tests with Robins adapted to field intensities outside the normal functional range of the magnetic compass show that the process of adaptation to fields outside this range is neither a shifting nor a simple enlargement of the functional range. Tests in several 1-Hz alternating magnetic fields with rectangular and sine-shaped impulses indicate that a certain constant portion of the impulse is necessary to enable the birds to use it for orientation.
Chapter
In the past decade, it has become apparent that the importance of magnetic interactions is not confined to the world of physics but extends into the realm of physiology and whole organism biology. That this should be so follows from two elementary observations: (1) by virtue of their magnetic moments and electrical charges, the atoms and ions which make up an organism can magnetically interact with the organism’s environment, and (2) the environment of practically every organism includes a highly ordered and stable (relative to the lifetime of the organism) geomagnetic field which contains both spatial and temporal information of potential value to the organism.
Article
The Earth's magnetic field provides an important source of directional information for terrestrial organisms, but the sensory receptor or receptors responsible for magnetic field detection have yet to be identified. Theoretical models of the mechanism of magnetoreception have implicated specialized photoreceptors. the proposed mechanism would amplify the weak interaction of the geomagnetic field with a single electron spin to the level of photo detection, resulting in a modulation of the photoreceptor response to light. Although behavioural, and neurophysiological studies have established a link between magnetic field sensitivity and the visual system, definitive evidence for the use of a light-dependent mechanism has been lacking. Here we show that magnetic compass orientation in a semiaquatic salamander is affected by the wavelength of light, and that this wavelength-dependence is due to a direct effect of light on the underlying magnetoreception mechanism.